Abstract
Angiogenesis, one of the hallmarks of cancers, has become an attractive target for cancer therapy since decades ago. It is broadly thought that upregulation of angiogenesis is involved in tumor progression and metastasis. Though tumor vessels are tortuous, disorganized, and leaky, they deliver oxygen and nutrients for tumor development. Based on this knowledge, many kinds of drugs targeting angiogenesis pathways have been developed, such as bevacizumab. However, the clinical outcomes of anti-angiogenesis therapies are moderate in metastatic breast cancer as well as in metastatic colorectal cancer and non-small cell lung cancer, even combined with traditional chemotherapy. In this chapter, the morphologic angiogenesis patterns and the key molecular pathways regulating angiogenesis are elaborated. The FDA-approved anti-angiogenesis drugs and current challenges of anti-angiogenesis therapy are described. The strategies to overcome the barriers will also be elucidated.
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References
Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144(5):646–674. doi:10.1016/j.cell.2011.02.013
Folkman J (1971) Tumor angiogenesis: therapeutic implications. N Engl J Med 285(21):1182–1186. doi:10.1056/NEJM197111182852108
Sundberg C, Nagy JA, Brown LF, Feng D, Eckelhoefer IA, Manseau EJ, Dvorak AM, Dvorak HF (2001) Glomeruloid microvascular proliferation follows adenoviral vascular permeability factor/vascular endothelial growth factor-164 gene delivery. Am J Pathol 158(3):1145–1160. doi:10.1016/S0002-9440(10)64062-X
Birbrair A, Zhang T, Wang ZM, Messi ML, Mintz A, Delbono O (2015) Pericytes at the intersection between tissue regeneration and pathology. Clin Sci (Lond) 128(2):81–93. doi:10.1042/CS20140278
Senger DR, Davis GE Angiogenesis. (1943–0264 (Electronic)). doi:D - NLM: PMC3140681 EDAT- 2011/08/03 06:00 MHDA- 2011/12/13 00:00 CRDT- 2011/08/03 06:00 AID - cshperspect.a005090 [pii] AID - 10.1101/cshperspect.a005090 [doi] PST - epublish
Ribatti D, Crivellato E “Sprouting angiogenesis”, a reappraisal. (1095-564X (Electronic))
Guidolin D Fau - Nico B, Nico B Fau - Belloni AS, Belloni As Fau - Nussdorfer GG, Nussdorfer Gg Fau - Vacca A, Vacca A Fau - Ribatti D, Ribatti D Morphometry and mathematical modelling of the capillary-like patterns formed in vitro by bone marrow macrophages of patients with multiple myeloma. (0887–6924 (Print))
Maniotis AJ, Folberg R Fau - Hess A, Hess A Fau - Seftor EA, Seftor Ea Fau - Gardner LM, Gardner Lm Fau – Pe’er J, Pe’er J Fau - Trent JM, Trent Jm Fau - Meltzer PS, Meltzer Ps Fau - Hendrix MJ, Hendrix MJ Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. (0002–9440 (Print)). doi:D - NLM: PMC1866899 EDAT- 1999/09/17 09:00 MHDA- 2000/06/10 09:00 CRDT- 1999/09/17 09:00 AID - S0002–9440(10)65173–5 [pii] AID - 10.1016/S0002-9440(10)65173-5 [doi] PST - ppublish
Holash J, Maisonpierre Pc Fau - Compton D, Compton D Fau - Boland P, Boland P Fau - Alexander CR, Alexander Cr Fau - Zagzag D, Zagzag D Fau - Yancopoulos GD, Yancopoulos Gd Fau - Wiegand SJ, Wiegand SJ Vessel cooption, regression, and growth in tumors mediated by angiopoietins and VEGF. (0036–8075 (Print))
Ribatti D, Djonov V Intussusceptive microvascular growth in tumors. (1872–7980 (Electronic))
Hristov M, Weber C Endothelial progenitor cells: characterization, pathophysiology, and possible clinical relevance. (1582–1838 (Print))
Shirakawa K, Furuhata S Fau - Watanabe I, Watanabe I Fau - Hayase H, Hayase H Fau - Shimizu A, Shimizu A Fau - Ikarashi Y, Ikarashi Y Fau - Yoshida T, Yoshida T Fau - Terada M, Terada M Fau - Hashimoto D, Hashimoto D Fau - Wakasugi H, Wakasugi H Induction of vasculogenesis in breast cancer models. (0007–0920 (Print)). doi:D - NLM: PMC2376301 EDAT- 2002/11/28 04:00 MHDA- 2003/01/08 04:00 CRDT- 2002/11/28 04:00 PHST- 2002/04/04 [received] PHST- 2002/08/22 [revised] PHST- 2002/08/29 [accepted] AID - 10.1038/sj.bjc.6600610 [doi] AID - 6600610 [pii] PST - ppublish
Shaked Y, Bertolini F Fau - Man S, Man S Fau - Rogers MS, Rogers Ms Fau - Cervi D, Cervi D Fau - Foutz T, Foutz T Fau - Rawn K, Rawn K Fau - Voskas D, Voskas D Fau - Dumont DJ, Dumont Dj Fau - Ben-David Y, Ben-David Y Fau - Lawler J, Lawler J Fau - Henkin J, Henkin J Fau - Huber J, Huber J Fau - Hicklin DJ, Hicklin Dj Fau – D’Amato RJ, D’Amato Rj Fau - Kerbel RS, Kerbel RS Genetic heterogeneity of the vasculogenic phenotype parallels angiogenesis; Implications for cellular surrogate marker analysis of antiangiogenesis. (1535–6108 (Print))
Mancuso P, Antoniotti P Fau - Quarna J, Quarna J Fau - Calleri A, Calleri A Fau - Rabascio C, Rabascio C Fau - Tacchetti C, Tacchetti C Fau - Braidotti P, Braidotti P Fau - Wu H-K, Wu Hk Fau - Zurita AJ, Zurita Aj Fau - Saronni L, Saronni L Fau - Cheng JB, Cheng Jb Fau - Shalinsky DR, Shalinsky Dr Fau - Heymach JV, Heymach Jv Fau - Bertolini F, Bertolini F Validation of a standardized method for enumerating circulating endothelial cells and progenitors: flow cytometry and molecular and ultrastructural analyses. (1078–0432 (Print))
Kim HK, Song Ks Fau - Kim HO, Kim Ho Fau - Chung J-H, Chung Jh Fau - Lee KR, Lee Kr Fau - Lee Y-J, Lee Yj Fau - Lee DH, Lee Dh Fau - Lee ES, Lee Es Fau - Kim HK, Kim Hk Fau - Ryu KW, Ryu Kw Fau - Bae J-M, Bae JM Circulating numbers of endothelial progenitor cells in patients with gastric and breast cancer. (0304–3835 (Print))
Naik RP, Jin D Fau - Chuang E, Chuang E Fau - Gold EG, Gold Eg Fau - Tousimis EA, Tousimis Ea Fau - Moore AL, Moore Al Fau - Christos PJ, Christos Pj Fau - de Dalmas T, de Dalmas T Fau - Donovan D, Donovan D Fau - Rafii S, Rafii S Fau - Vahdat LT, Vahdat LT Circulating endothelial progenitor cells correlate to stage in patients with invasive breast cancer. (1573–7217 (Electronic))
Kuo YH, Lin Ch Fau - Shau W-Y, Shau Wy Fau - Chen T-J, Chen Tj Fau - Yang S-H, Yang Sh Fau - Huang S-M, Huang Sm Fau - Hsu C, Hsu C Fau - Lu Y-S, Lu Ys Fau - Cheng A-L, Cheng AL Dynamics of circulating endothelial cells and endothelial progenitor cells in breast cancer patients receiving cytotoxic chemotherapy. (1471–2407 (Electronic)). doi:D - NLM: PMC3561193 EDAT- 2012/12/28 06:00 MHDA- 2013/07/03 06:00 CRDT- 2012/12/28 06:00 PHST- 2012/03/20 [received] PHST- 2012/12/18 [accepted] AID - 1471-2407-12-620 [pii] AID - 10.1186/1471–2407–12-620 [doi] PST - epublish
Dome B, Timar J Fau - Dobos J, Dobos J Fau - Meszaros L, Meszaros L Fau - Raso E, Raso E Fau - Paku S, Paku S Fau - Kenessey I, Kenessey I Fau - Ostoros G, Ostoros G Fau - Magyar M, Magyar M Fau - Ladanyi A, Ladanyi A Fau - Bogos K, Bogos K Fau - Tovari J, Tovari J Identification and clinical significance of circulating endothelial progenitor cells in human non-small cell lung cancer. (0008–5472 (Print))
Shaked Y, Emmenegger U Fau - Man S, Man S Fau - Cervi D, Cervi D Fau - Bertolini F, Bertolini F Fau - Ben-David Y, Ben-David Y Fau - Kerbel RS, Kerbel RS Optimal biologic dose of metronomic chemotherapy regimens is associated with maximum antiangiogenic activity. (0006–4971 (Print)). doi:D - NLM: PMC1895327 EDAT- 2005/07/07 09:00 MHDA- 2005/12/13 09:00 CRDT- 2005/07/07 09:00 AID - 2005-04-1422 [pii] AID - 10.1182/blood-2005-04-1422 [doi] PST - ppublish
Shaked Y, Emmenegger U Fau - Francia G, Francia G Fau - Chen L, Chen L Fau - Lee CR, Lee Cr Fau - Man S, Man S Fau - Paraghamian A, Paraghamian A Fau - Ben-David Y, Ben-David Y Fau - Kerbel RS, Kerbel RS Low-dose metronomic combined with intermittent bolus-dose cyclophosphamide is an effective long-term chemotherapy treatment strategy. (0008–5472 (Print))
Munoz R, Man S Fau - Shaked Y, Shaked Y Fau - Lee CR, Lee Cr Fau - Wong J, Wong J Fau - Francia G, Francia G Fau - Kerbel RS, Kerbel RS Highly efficacious nontoxic preclinical treatment for advanced metastatic breast cancer using combination oral UFT-cyclophosphamide metronomic chemotherapy. (0008–5472 (Print))
Ng SSW, Sparreboom A, Shaked Y, Lee C, Man S, Desai N, Soon-Shiong P, Figg WD, Kerbel RS (2006) Influence of formulation vehicle on metronomic Taxane chemotherapy: albumin-bound versus Cremophor EL–based paclitaxel. Clin Cancer Res 12(14):4331
Le Bourhis X, Romon R, Hondermarck H (2010) Role of endothelial progenitor cells in breast cancer angiogenesis: from fundamental research to clinical ramifications. Breast Cancer Res Treat 120(1):17–24. doi:10.1007/s10549-009-0686-5
Shaked Y, Henke E, Roodhart JM, Mancuso P, Langenberg MH, Colleoni M, Daenen LG, Man S, Xu P, Emmenegger U, Tang T, Zhu Z, Witte L, Strieter RM, Bertolini F, Voest EE, Benezra R, Kerbel RS (2008) Rapid chemotherapy-induced acute endothelial progenitor cell mobilization: implications for antiangiogenic drugs as chemosensitizing agents. Cancer Cell 14(3):263–273. doi:10.1016/j.ccr.2008.08.001
Furstenberger G, von Moos R, Lucas R, Thurlimann B, Senn HJ, Hamacher J, Boneberg EM (2006) Circulating endothelial cells and angiogenic serum factors during neoadjuvant chemotherapy of primary breast cancer. Br J Cancer 94(4):524–531. doi:10.1038/sj.bjc.6602952
Paliege A, Rosenberger C Fau - Bondke A, Bondke A Fau - Sciesielski L, Sciesielski L Fau - Shina A, Shina A Fau - Heyman SN, Heyman Sn Fau - Flippin LA, Flippin La Fau - Arend M, Arend M Fau - Klaus SJ, Klaus Sj Fau - Bachmann S, Bachmann S Hypoxia-inducible factor-2alpha-expressing interstitial fibroblasts are the only renal cells that express erythropoietin under hypoxia-inducible factor stabilization. (1523–1755 (Electronic))
Schioppa T, Uranchimeg B, Saccani A, Biswas SK, Doni A, Rapisarda A, Bernasconi S, Saccani S, Nebuloni M, Vago L, Mantovani A, Melillo G, Sica A (2003) Regulation of the chemokine receptor CXCR4 by hypoxia. J Exp Med 198(9):1391–1402. doi:10.1084/jem.20030267
Ahn GO, Brown JM (2009) Role of endothelial progenitors and other bone marrow-derived cells in the development of the tumor vasculature. Angiogenesis 12(2):159–164. doi:10.1007/s10456-009-9135-7
Chen TG, Zhong ZY, Sun GF, Zhou YX, Zhao Y (2011) Effects of tumour necrosis factor-alpha on activity and nitric oxide synthase of endothelial progenitor cells from peripheral blood. Cell Prolif 44(4):352–359. doi:10.1111/j.1365-2184.2011.00764.x
Hattori K, Dias S, Heissig B, Hackett NR, Lyden D, Tateno M, Hicklin DJ, Zhu Z, Witte L, Crystal RG, Moore MA, Rafii S (2001) Vascular endothelial growth factor and angiopoietin-1 stimulate postnatal hematopoiesis by recruitment of vasculogenic and hematopoietic stem cells. J Exp Med 193(9):1005–1014
Lewis JS, Lee Ja Fau - Underwood JC, Underwood Jc Fau - Harris AL, Harris Al Fau - Lewis CE, Lewis CE Macrophage responses to hypoxia: relevance to disease mechanisms. (0741–5400 (Print))
Bingle L, Brown Nj Fau - Lewis CE, Lewis CE The role of tumour-associated macrophages in tumour progression: implications for new anticancer therapies. (0022–3417 (Print))
Imamura H, Ohta T, Tsunetoshi K, Doi K, Nozaki K, Takagi Y, Kikuta K (2010) Transdifferentiation of bone marrow-derived endothelial progenitor cells into the smooth muscle cell lineage mediated by tansforming growth factor-beta1. Atherosclerosis 211(1):114–121. doi:10.1016/j.atherosclerosis.2010.02.040
Sales VL, Engelmayr GC Jr, Mettler BA, Johnson JA Jr, Sacks MS, Mayer JE Jr (2006) Transforming growth factor-beta1 modulates extracellular matrix production, proliferation, and apoptosis of endothelial progenitor cells in tissue-engineering scaffolds. Circulation 114(1 Suppl):I193–I199. doi:10.1161/circulationaha.105.001628
Sasi SP, Yan X, Enderling H, Park D, Gilbert HY, Curry C, Coleman C, Hlatky L, Qin G, Kishore R, Goukassian DA (2012) Breaking the ‘harmony’ of TNF-alpha signaling for cancer treatment. Oncogene 31(37):4117–4127. doi:10.1038/onc.2011.567
Zeoli A, Dentelli P, Rosso A, Togliatto G, Trombetta A, Damiano L, di Celle PF, Pegoraro L, Altruda F, Brizzi MF (2008) Interleukin-3 promotes expansion of hemopoietic-derived CD45+ angiogenic cells and their arterial commitment via STAT5 activation. Blood 112(2):350–361. doi:10.1182/blood-2007-12-128215
Fan Y, Ye J, Shen F, Zhu Y, Yeghiazarians Y, Zhu W, Chen Y, Lawton MT, Young WL, Yang GY (2008) Interleukin-6 stimulates circulating blood-derived endothelial progenitor cell angiogenesis in vitro. J Cereb Blood Flow Metab 28(1):90–98. doi:10.1038/sj.jcbfm.9600509
Varnum-Finney B, Brashem-Stein C, Bernstein ID (2003) Combined effects of notch signaling and cytokines induce a multiple log increase in precursors with lymphoid and myeloid reconstituting ability. Blood 101(5):1784–1789. doi:10.1182/blood-2002-06-1862
Fernandez L, Rodriguez S, Huang H, Chora A, Fernandes J, Mumaw C, Cruz E, Pollok K, Cristina F, Price JE, Ferkowicz MJ, Scadden DT, Clauss M, Cardoso AA, Carlesso N (2008) Tumor necrosis factor-alpha and endothelial cells modulate notch signaling in the bone marrow microenvironment during inflammation. Exp Hematol 36(5):545–558. doi:10.1016/j.exphem.2007.12.012
Kwon SM, Eguchi M, Wada M, Iwami Y, Hozumi K, Iwaguro H, Masuda H, Kawamoto A, Asahara T (2008) Specific jagged-1 signal from bone marrow microenvironment is required for endothelial progenitor cell development for neovascularization. Circulation 118(2):157–165. doi:10.1161/circulationaha.107.754978
Yang DG, Liu L, Zheng XY (2008) Cyclin-dependent kinase inhibitor p16(INK4a) and telomerase may co-modulate endothelial progenitor cells senescence. Ageing Res Rev 7(2):137–146. doi:10.1016/j.arr.2008.02.001
Kaplan RN, Riba Rd Fau - Zacharoulis S, Zacharoulis S Fau - Bramley AH, Bramley Ah Fau - Vincent L, Vincent L Fau - Costa C, Costa C Fau - MacDonald DD, MacDonald Dd Fau - Jin DK, Jin Dk Fau - Shido K, Shido K Fau - Kerns SA, Kerns Sa Fau - Zhu Z, Zhu Z Fau - Hicklin D, Hicklin D Fau - Wu Y, Wu Y Fau - Port JL, Port Jl Fau - Altorki N, Altorki N Fau - Port ER, Port Er Fau - Ruggero D, Ruggero D Fau - Shmelkov SV, Shmelkov Sv Fau - Jensen KK, Jensen Kk Fau - Rafii S, Rafii S Fau - Lyden D, Lyden D VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. (1476–4687 (Electronic)). doi: D - NLM: NIHMS236203 D - NLM: PMC2945882 EDAT- 2005/12/13 09:00 MHDA- 2005/12/31 09:00 CRDT- 2005/12/13 09:00 PHST- 2005/05/13 [received] PHST- 2005/08/19 [accepted] AID - nature04186 [pii] AID - 10.1038/nature04186 [doi] PST - ppublish
Jin F, Brockmeier U, Otterbach F, Metzen E (2012) New insight into the SDF-1/CXCR4 axis in a breast carcinoma model: hypoxia-induced endothelial SDF-1 and tumor cell CXCR4 are required for tumor cell intravasation. Mol Cancer Res 10(8):1021–1031. doi:10.1158/1541-7786.mcr-11-0498
Kim HK, Song KS, Kim HO, Chung JH, Lee KR, Lee YJ, Lee DH, Lee ES, Kim HK, Ryu KW, Bae JM (2003) Circulating numbers of endothelial progenitor cells in patients with gastric and breast cancer. Cancer Lett 198(1):83–88
De Palma M, Venneri MA, Roca C, Naldini L (2003) Targeting exogenous genes to tumor angiogenesis by transplantation of genetically modified hematopoietic stem cells. Nat Med 9(6):789–795. doi:10.1038/nm871
Kim JA, Lee HJ, Kang HJ, Park TH (2009) The targeting of endothelial progenitor cells to a specific location within a microfluidic channel using magnetic nanoparticles. Biomed Microdevices 11(1):287–296. doi:10.1007/s10544-008-9235-y
van Noort D, Ong SM, Zhang C, Zhang S, Arooz T, Yu H (2009) Stem cells in microfluidics. Biotechnol Prog 25(1):52–60. doi:10.1002/btpr.171
di Tomaso E, Capen D, Haskell A, Hart J, Logie JJ, Jain RK, McDonald DM, Jones R, Munn LL (2005) Mosaic tumor vessels: cellular basis and ultrastructure of focal regions lacking endothelial cell markers. Cancer Res 65(13):5740–5749. doi:10.1158/0008-5472.CAN-04-4552
Chang YS, di Tomaso E, McDonald DM, Jones R, Jain RK, Munn LL (2000) Mosaic blood vessels in tumors: frequency of cancer cells in contact with flowing blood. Proc Natl Acad Sci U S A 97(26):14608–14613. doi:10.1073/pnas.97.26.14608
Jain RK (2001) Normalizing tumor vasculature with anti-angiogenic therapy: a new paradigm for combination therapy. Nat Med 7(9):987–989. doi:10.1038/nm0901-987
Jain RK (2005) Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science (New York, NY) 307(5706):58–62. doi:10.1126/science.1104819
Folkman J (2001) Can mosaic tumor vessels facilitate molecular diagnosis of cancer? Proc Natl Acad Sci U S A 98(2):398–400. doi:10.1073/pnas.98.2.398
Stephenson J (2001) Mosaic vessels shed cancer clues by the million. Lancet Oncol 2(3):130. doi:10.1016/s1470-2045(00)00249-7
Bertolini F, Lanza A, Peccatori F, Zibera C, Gibelli N, Perotti C, Da Prada GA, Torretta L, Cocorocchio E, Martinelli G, Robustelli della Cuna G (1998) Hematopoietic progenitor cell collection and neoplastic cell contamination in breast cancer patients receiving chemotherapy plus granulocyte-colony stimulating factor (G-CSF) or G-CSF alone for mobilization. Ann Oncology 9 (8):913–916
Kleinman MB, Wiley El Fau - Guo M, Guo M Fau - Rademaker AW, Rademaker Aw Fau - Villa M, Villa M Fau - Tallman MS, Tallman Ms Fau - Newman SB, Newman Sb Fau - Gordon LI, Gordon Li Fau - Winter JN, Winter JN Immunohistochemical detection of breast cancer cells in paired peripheral blood progenitor cell specimens collected after cytokine or cytokine and myelosuppressive chemotherapy. (0268–3369 (Print))
Bertolini F, Martinelli G, Goldhirsch A (2001) Mosaic tumour blood vessels and high-dose chemotherapy for breast cancer. Lancet Oncol 2(10):595. doi:10.1016/s1470-2045(01)00514-9
Folberg R, Hendrix MJ, Maniotis AJ (2000) Vasculogenic mimicry and tumor angiogenesis. Am J Pathol 156(2):361–381. doi:10.1016/s0002-9440(10)64739-6
Folberg R, Maniotis AJ (2004) Vasculogenic mimicry. APMIS : acta pathologica, microbiologica, et immunologica Scandinavica 112(7–8):508–525. doi:10.1111/j.1600-0463.2004.apm11207-0810.x
Pulford E, Hocking A, Griggs K, McEvoy J, Bonder C, Henderson DW, Klebe S (2016) Vasculogenic mimicry in malignant mesothelioma: an experimental and immunohistochemical analysis. Pathology 48(7):650–659. doi:10.1016/j.pathol.2016.07.009
Wang H, Lin H, Pan J, Mo C, Zhang F, Huang B, Wang Z, Chen X, Zhuang J, Wang D, Qiu S (2016) Vasculogenic mimicry in prostate cancer: the roles of EphA2 and PI3K. J Cancer 7(9):1114–1124. doi:10.7150/jca.14120
Shirakawa K, Kobayashi H, Heike Y, Kawamoto S, Brechbiel MW, Kasumi F, Iwanaga T, Konishi F, Terada M, Wakasugi H (2002) Hemodynamics in vasculogenic mimicry and angiogenesis of inflammatory breast cancer xenograft. Cancer Res 62(2):560–566
Paulis YW, Soetekouw PM, Verheul HM, Tjan-Heijnen VC, Griffioen AW (2010) Signalling pathways in vasculogenic mimicry. Biochim Biophys Acta 1806(1):18–28. doi:10.1016/j.bbcan.2010.01.001
Maniotis AJ, Folberg R, Hess A, Seftor EA, Gardner LM, Pe’er J, Trent JM, Meltzer PS, Hendrix MJ (1999) Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am J Pathol 155(3):739–752. doi:10.1016/s0002-9440(10)65173-5
Seftor RE, Hess AR, Seftor EA, Kirschmann DA, Hardy KM, Margaryan NV, Hendrix MJ (2012) Tumor cell vasculogenic mimicry: from controversy to therapeutic promise. Am J Pathol 181(4):1115–1125. doi:10.1016/j.ajpath.2012.07.013
Postovit LM, Margaryan NV, Seftor EA, Kirschmann DA, Lipavsky A, Wheaton WW, Abbott DE, Seftor RE, Hendrix MJ (2008) Human embryonic stem cell microenvironment suppresses the tumorigenic phenotype of aggressive cancer cells. Proc Natl Acad Sci U S A 105(11):4329–4334. doi:10.1073/pnas.0800467105
Mihic-Probst D, Ikenberg K, Tinguely M, Schraml P, Behnke S, Seifert B, Civenni G, Sommer L, Moch H, Dummer R (2012) Tumor cell plasticity and angiogenesis in human melanomas. PLoS One 7(3):e33571. doi:10.1371/journal.pone.0033571
De Bock K, Mazzone M, Carmeliet P (2011) Antiangiogenic therapy, hypoxia, and metastasis: risky liaisons, or not? Nat Rev Clin Oncol 8(7):393–404. doi:10.1038/nrclinonc.2011.83
Benizri E, Ginouves A, Berra E (2008) The magic of the hypoxia-signaling cascade. Cell Mol Life Sci 65(7–8):1133–1149. doi:10.1007/s00018-008-7472-0
Ivan M, Kondo K, Yang H, Kim W, Valiando J, Ohh M, Salic A, Asara JM, Lane WS, Kaelin WG Jr (2001) HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science (New York, NY) 292(5516):464–468. doi:10.1126/science.1059817
Fernandez-Barral A, Orgaz JL, Gomez V, del Peso L, Calzada MJ, Jimenez B (2012) Hypoxia negatively regulates antimetastatic PEDF in melanoma cells by a hypoxia inducible factor-independent, autophagy dependent mechanism. PLoS One 7(3):e32989. doi:10.1371/journal.pone.0032989
Andrews S, Ford D, Martin P (2012) Knockdown of osteopontin reduces the inflammatory response and subsequent size of postsurgical adhesions in a murine model. Am J Pathol 181(4):1165–1172. doi:10.1016/j.ajpath.2012.06.027
Vartanian A, Stepanova E, Grigorieva I, Solomko E, Baryshnikov A, Lichinitser M (2011) VEGFR1 and PKCalpha signaling control melanoma vasculogenic mimicry in a VEGFR2 kinase-independent manner. Melanoma Res 21(2):91–98. doi:10.1097/CMR.0b013e328343a237
Comito G, Calvani M, Giannoni E, Bianchini F, Calorini L, Torre E, Migliore C, Giordano S, Chiarugi P (2011) HIF-1alpha stabilization by mitochondrial ROS promotes met-dependent invasive growth and vasculogenic mimicry in melanoma cells. Free Radic Biol Med 51(4):893–904. doi:10.1016/j.freeradbiomed.2011.05.042
Conley SJ, Gheordunescu E, Kakarala P, Newman B, Korkaya H, Heath AN, Clouthier SG, Wicha MS (2012) Antiangiogenic agents increase breast cancer stem cells via the generation of tumor hypoxia. Proc Natl Acad Sci U S A 109(8):2784–2789. doi:10.1073/pnas.1018866109
Ju RJ, Li XT, Shi JF, Li XY, Sun MG, Zeng F, Zhou J, Liu L, Zhang CX, Zhao WY, Lu WL (2014) Liposomes, modified with PTD(HIV-1) peptide, containing epirubicin and celecoxib, to target vasculogenic mimicry channels in invasive breast cancer. Biomaterials 35(26):7610–7621. doi:10.1016/j.biomaterials.2014.05.040
Serwe A, Rudolph K, Anke T, Erkel G (2012) Inhibition of TGF-beta signaling, vasculogenic mimicry and proinflammatory gene expression by isoxanthohumol. Investig New Drugs 30(3):898–915. doi:10.1007/s10637-011-9643-3
Frank NY, Schatton T, Kim S, Zhan Q, Wilson BJ, Ma J, Saab KR, Osherov V, Widlund HR, Gasser M, Waaga-Gasser AM, Kupper TS, Murphy GF, Frank MH (2011) VEGFR-1 expressed by malignant melanoma-initiating cells is required for tumor growth. Cancer Res 71(4):1474–1485. doi:10.1158/0008-5472.can-10-1660
Folkman J (2007) Angiogenesis: an organizing principle for drug discovery? Nat Rev Drug Discov 6(4):273–286. doi:10.1038/nrd2115
Senger DR, Galli SJ, Dvorak AM, Perruzzi CA, Harvey VS, Dvorak HF (1983) Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science (New York, NY) 219(4587):983–985
Ferrara N, Henzel WJ (1989) Pituitary follicular cells secrete a novel heparin-binding growth factor specific for vascular endothelial cells. Biochem Biophys Res Commun 161(2):851–858
Olsson AK, Dimberg A, Kreuger J, Claesson-Welsh L (2006) VEGF receptor signalling - in control of vascular function. Nat Rev Mol Cell Biol 7(5):359–371. doi:10.1038/nrm1911
Tie J, Desai J (2012) Antiangiogenic therapies targeting the vascular endothelia growth factor signaling system. Crit Rev Oncog 17(1):51–67
Dvorak HF (2002) Vascular permeability factor/vascular endothelial growth factor: a critical cytokine in tumor angiogenesis and a potential target for diagnosis and therapy. J Clin Oncol 20(21):4368–4380. doi:10.1200/jco.2002.10.088
Hicklin DJ, Ellis LM (2005) Role of the vascular endothelial growth factor pathway in tumor growth and angiogenesis. J Clin Oncol 23(5):1011–1027. doi:10.1200/jco.2005.06.081
Shalaby F, Rossant J, Yamaguchi TP, Gertsenstein M, Wu XF, Breitman ML, Schuh AC (1995) Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 376(6535):62–66. doi:10.1038/376062a0
Takahashi T, Yamaguchi S, Chida K, Shibuya M (2001) A single autophosphorylation site on KDR/Flk-1 is essential for VEGF-A-dependent activation of PLC-gamma and DNA synthesis in vascular endothelial cells. EMBO J 20(11):2768–2778. doi:10.1093/emboj/20.11.2768
Matsumoto T, Bohman S, Dixelius J, Berge T, Dimberg A, Magnusson P, Wang L, Wikner C, Qi JH, Wernstedt C, Wu J, Bruheim S, Mugishima H, Mukhopadhyay D, Spurkland A, Claesson-Welsh L (2005) VEGF receptor-2 Y951 signaling and a role for the adapter molecule TSAd in tumor angiogenesis. EMBO J 24(13):2342–2353. doi:10.1038/sj.emboj.7600709
Zeng H, Sanyal S, Mukhopadhyay D (2001) Tyrosine residues 951 and 1059 of vascular endothelial growth factor receptor-2 (KDR) are essential for vascular permeability factor/vascular endothelial growth factor-induced endothelium migration and proliferation, respectively. J Biol Chem 276(35):32714–32719. doi:10.1074/jbc.M103130200
Dougher M, Terman BI (1999) Autophosphorylation of KDR in the kinase domain is required for maximal VEGF-stimulated kinase activity and receptor internalization. Oncogene 18(8):1619–1627. doi:10.1038/sj.onc.1202478
Dunk C, Ahmed A (2001) Vascular endothelial growth factor receptor-2-mediated mitogenesis is negatively regulated by vascular endothelial growth factor receptor-1 in tumor epithelial cells. Am J Pathol 158(1):265–273. doi:10.1016/s0002-9440(10)63965-x
Hiratsuka S, Minowa O, Kuno J, Noda T, Shibuya M (1998) Flt-1 lacking the tyrosine kinase domain is sufficient for normal development and angiogenesis in mice. Proc Natl Acad Sci U S A 95(16):9349–9354
Kaipainen A, Korhonen J, Mustonen T, van Hinsbergh VW, Fang GH, Dumont D, Breitman M, Alitalo K (1995) Expression of the fms-like tyrosine kinase 4 gene becomes restricted to lymphatic endothelium during development. Proc Natl Acad Sci U S A 92(8):3566–3570
Jussila L, Alitalo K (2002) Vascular growth factors and lymphangiogenesis. Physiol Rev 82(3):673–700. doi:10.1152/physrev.00005.2002
Valtola R, Salven P, Heikkila P, Taipale J, Joensuu H, Rehn M, Pihlajaniemi T, Weich H, deWaal R, Alitalo K (1999) VEGFR-3 and its ligand VEGF-C are associated with angiogenesis in breast cancer. Am J Pathol 154(5):1381–1390. doi:10.1016/s0002-9440(10)65392-8
Partanen TA, Alitalo K, Miettinen M (1999) Lack of lymphatic vascular specificity of vascular endothelial growth factor receptor 3 in 185 vascular tumors. Cancer 86(11):2406–2412
He Y, Kozaki K, Karpanen T, Koshikawa K, Yla-Herttuala S, Takahashi T, Alitalo K (2002) Suppression of tumor lymphangiogenesis and lymph node metastasis by blocking vascular endothelial growth factor receptor 3 signaling. J Natl Cancer Inst 94(11):819–825
Wang JF, Zhang X, Groopman JE (2004) Activation of vascular endothelial growth factor receptor-3 and its downstream signaling promote cell survival under oxidative stress. J Biol Chem 279(26):27088–27097. doi:10.1074/jbc.M314015200
Makinen T, Veikkola T, Mustjoki S, Karpanen T, Catimel B, Nice EC, Wise L, Mercer A, Kowalski H, Kerjaschki D, Stacker SA, Achen MG, Alitalo K (2001) Isolated lymphatic endothelial cells transduce growth, survival and migratory signals via the VEGF-C/D receptor VEGFR-3. EMBO J 20(17):4762–4773. doi:10.1093/emboj/20.17.4762
Cascone T, Heymach JV (2012) Targeting the angiopoietin/Tie2 pathway: cutting tumor vessels with a double-edged sword? J Clin Oncol 30(4):441–444. doi:10.1200/jco.2011.38.7621
Tadros A, Hughes DP, Dunmore BJ, Brindle NP (2003) ABIN-2 protects endothelial cells from death and has a role in the antiapoptotic effect of angiopoietin-1. Blood 102(13):4407–4409. doi:10.1182/blood-2003-05-1602
Kim I, Kim HG, So JN, Kim JH, Kwak HJ, Koh GY (2000) Angiopoietin-1 regulates endothelial cell survival through the phosphatidylinositol 3′-kinase/Akt signal transduction pathway. Circ Res 86(1):24–29
Papapetropoulos A, Fulton D, Mahboubi K, Kalb RG, O’Connor DS, Li F, Altieri DC, Sessa WC (2000) Angiopoietin-1 inhibits endothelial cell apoptosis via the Akt/survivin pathway. J Biol Chem 275(13):9102–9105
Wu F, Yang LY, Li YF, Ou DP, Chen DP, Fan C (2009) Novel role for epidermal growth factor-like domain 7 in metastasis of human hepatocellular carcinoma. Hepatology 50(6):1839–1850. doi:10.1002/hep.23197
Saharinen P, Eklund L, Miettinen J, Wirkkala R, Anisimov A, Winderlich M, Nottebaum A, Vestweber D, Deutsch U, Koh GY, Olsen BR, Alitalo K (2008) Angiopoietins assemble distinct Tie2 signalling complexes in endothelial cell-cell and cell-matrix contacts. Nat Cell Biol 10(5):527–537. doi:10.1038/ncb1715
Fukuhara S, Sako K, Minami T, Noda K, Kim HZ, Kodama T, Shibuya M, Takakura N, Koh GY, Mochizuki N (2008) Differential function of Tie2 at cell-cell contacts and cell-substratum contacts regulated by angiopoietin-1. Nat Cell Biol 10(5):513–526. doi:10.1038/ncb1714
Gale NW, Thurston G, Hackett SF, Renard R, Wang Q, McClain J, Martin C, Witte C, Witte MH, Jackson D, Suri C, Campochiaro PA, Wiegand SJ, Yancopoulos GD (2002) Angiopoietin-2 is required for postnatal angiogenesis and lymphatic patterning, and only the latter role is rescued by angiopoietin-1. Dev Cell 3(3):411–423
Fagiani E, Christofori G (2013) Angiopoietins in angiogenesis. Cancer Lett 328(1):18–26. doi:10.1016/j.canlet.2012.08.018
Hansen TM, Singh H, Tahir TA, Brindle NP (2010) Effects of angiopoietins-1 and -2 on the receptor tyrosine kinase Tie2 are differentially regulated at the endothelial cell surface. Cell Signal 22(3):527–532. doi:10.1016/j.cellsig.2009.11.007
Seegar TC, Eller B, Tzvetkova-Robev D, Kolev MV, Henderson SC, Nikolov DB, Barton WA (2010) Tie1-Tie2 interactions mediate functional differences between angiopoietin ligands. Mol Cell 37(5):643–655. doi:10.1016/j.molcel.2010.02.007
Tsutsui S, Inoue H, Yasuda K, Suzuki K, Takeuchi H, Nishizaki T, Higashi H, Era S, Mori M (2006) Angiopoietin 2 expression in invasive ductal carcinoma of the breast: its relationship to the VEGF expression and microvessel density. Breast Cancer Res Treat 98(3):261–266. doi:10.1007/s10549-005-9157-9
Danza K, Pilato B, Lacalamita R, Addati T, Giotta F, Bruno A, Paradiso A, Tommasi S (2013) Angiogenetic axis angiopoietins/Tie2 and VEGF in familial breast cancer. European journal of human genetics : EJHG 21(8):824–830. doi:10.1038/ejhg.2012.273
Lorger M, Felding-Habermann B (2010) Capturing changes in the brain microenvironment during initial steps of breast cancer brain metastasis. Am J Pathol 176(6):2958–2971. doi:10.2353/ajpath.2010.090838
Hashizume H, Falcon BL, Kuroda T, Baluk P, Coxon A, Yu D, Bready JV, Oliner JD, McDonald DM (2010) Complementary actions of inhibitors of angiopoietin-2 and VEGF on tumor angiogenesis and growth. Cancer Res 70(6):2213–2223. doi:10.1158/0008-5472.can-09-1977
Schulz P, Fischer C, Detjen KM, Rieke S, Hilfenhaus G, von Marschall Z, Bohmig M, Koch I, Kehrberger J, Hauff P, Thierauch KH, Alves F, Wiedenmann B, Scholz A (2011) Angiopoietin-2 drives lymphatic metastasis of pancreatic cancer. FASEB J 25(10):3325–3335. doi:10.1096/fj.11-182287
Tian S, Hayes AJ, Metheny-Barlow LJ, Li LY (2002) Stabilization of breast cancer xenograft tumour neovasculature by angiopoietin-1. Br J Cancer 86(4):645–651. doi:10.1038/sj.bjc.6600082
Stoeltzing O, Ahmad SA, Liu W, McCarty MF, Wey JS, Parikh AA, Fan F, Reinmuth N, Kawaguchi M, Bucana CD, Ellis LM (2003) Angiopoietin-1 inhibits vascular permeability, angiogenesis, and growth of hepatic colon cancer tumors. Cancer Res 63(12):3370–3377
Hawighorst T, Skobe M, Streit M, Hong YK, Velasco P, Brown LF, Riccardi L, Lange-Asschenfeldt B, Detmar M (2002) Activation of the tie2 receptor by angiopoietin-1 enhances tumor vessel maturation and impairs squamous cell carcinoma growth. Am J Pathol 160(4):1381–1392. doi:10.1016/s0002-9440(10)62565-5
Holopainen T, Huang H, Chen C, Kim KE, Zhang L, Zhou F, Han W, Li C, Yu J, Wu J, Koh GY, Alitalo K, He Y (2009) Angiopoietin-1 overexpression modulates vascular endothelium to facilitate tumor cell dissemination and metastasis establishment. Cancer Res 69(11):4656–4664. doi:10.1158/0008-5472.can-08-4654
Cao Y, Sonveaux P, Liu S, Zhao Y, Mi J, Clary BM, Li CY, Kontos CD, Dewhirst MW (2007) Systemic overexpression of angiopoietin-2 promotes tumor microvessel regression and inhibits angiogenesis and tumor growth. Cancer Res 67(8):3835–3844. doi:10.1158/0008-5472.can-06-4056
Kunz P, Hoffend J, Altmann A, Dimitrakopoulou-Strauss A, Koczan D, Eisenhut M, Bonaterra GA, Dengler TJ, Mier W, Haberkorn U, Kinscherf R (2006) Angiopoietin-2 overexpression in morris hepatoma results in increased tumor perfusion and induction of critical angiogenesis-promoting genes. J Nuclear Med 47(9):1515–1524
Ahmad SA, Liu W, Jung YD, Fan F, Wilson M, Reinmuth N, Shaheen RM, Bucana CD, Ellis LM (2001) The effects of angiopoietin-1 and -2 on tumor growth and angiogenesis in human colon cancer. Cancer Res 61(4):1255–1259
Oliner J, Min H, Leal J, Yu D, Rao S, You E, Tang X, Kim H, Meyer S, Han SJ, Hawkins N, Rosenfeld R, Davy E, Graham K, Jacobsen F, Stevenson S, Ho J, Chen Q, Hartmann T, Michaels M, Kelley M, Li L, Sitney K, Martin F, Sun JR, Zhang N, Lu J, Estrada J, Kumar R, Coxon A, Kaufman S, Pretorius J, Scully S, Cattley R, Payton M, Coats S, Nguyen L, Desilva B, Ndifor A, Hayward I, Radinsky R, Boone T, Kendall R (2004) Suppression of angiogenesis and tumor growth by selective inhibition of angiopoietin-2. Cancer Cell 6(5):507–516. doi:10.1016/j.ccr.2004.09.030
Coxon A, Bready J, Min H, Kaufman S, Leal J, Yu D, Lee TA, Sun JR, Estrada J, Bolon B, McCabe J, Wang L, Rex K, Caenepeel S, Hughes P, Cordover D, Kim H, Han SJ, Michaels ML, Hsu E, Shimamoto G, Cattley R, Hurh E, Nguyen L, Wang SX, Ndifor A, Hayward IJ, Falcon BL, McDonald DM, Li L, Boone T, Kendall R, Radinsky R, Oliner JD (2010) Context-dependent role of angiopoietin-1 inhibition in the suppression of angiogenesis and tumor growth: implications for AMG 386, an angiopoietin-1/2-neutralizing peptibody. Mol Cancer Ther 9(10):2641–2651. doi:10.1158/1535-7163.mct-10-0213
O’Sullivan B, Brierley J International union against cancer UICC manual of clinical oncology. Ninth edition edn
Lindahl P, Johansson BR, Leveen P, Betsholtz C (1997) Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science 277(5323):242–245
Paulsson J, Sjoblom T, Micke P, Ponten F, Landberg G, Heldin CH, Bergh J, Brennan DJ, Jirstrom K, Ostman A (2009) Prognostic significance of stromal platelet-derived growth factor beta-receptor expression in human breast cancer. Am J Pathol 175(1):334–341. doi:10.2353/ajpath.2009.081030
Pinto MP, Dye WW, Jacobsen BM, Horwitz KB (2014) Malignant stroma increases luminal breast cancer cell proliferation and angiogenesis through platelet-derived growth factor signaling. BMC Cancer 14:735. doi:10.1186/1471-2407-14-735
Stuelten CH, DaCosta BS, Arany PR, Karpova TS, Stetler-Stevenson WG, Roberts AB (2005) Breast cancer cells induce stromal fibroblasts to express MMP-9 via secretion of TNF-alpha and TGF-beta. J Cell Sci 118(Pt 10):2143–2153. doi:10.1242/jcs.02334
Shao ZM, Nguyen M, Barsky SH (2000) Human breast carcinoma desmoplasia is PDGF initiated. Oncogene 19(38):4337–4345. doi:10.1038/sj.onc.1203785
Banerjee S, Sengupta K, Dhar K, Mehta S, D’Amore PA, Dhar G, Banerjee SK (2006) Breast cancer cells secreted platelet-derived growth factor-induced motility of vascular smooth muscle cells is mediated through neuropilin-1. Mol Carcinog 45(11):871–880. doi:10.1002/mc.20248
Erber R, Thurnher A, Katsen AD, Groth G, Kerger H, Hammes HP, Menger MD, Ullrich A, Vajkoczy P (2004) Combined inhibition of VEGF and PDGF signaling enforces tumor vessel regression by interfering with pericyte-mediated endothelial cell survival mechanisms. FASEB J 18(2):338–340. doi:10.1096/fj.03-0271fje
Escudier B, Eisen T, Stadler WM, Szczylik C, Oudard S, Siebels M, Negrier S, Chevreau C, Solska E, Desai AA, Rolland F, Demkow T, Hutson TE, Gore M, Freeman S, Schwartz B, Shan M, Simantov R, Bukowski RM (2007) Sorafenib in advanced clear-cell renal-cell carcinoma. N Engl J Med 356 (2):125–134. doi:10.1056/NEJMoa060655
Llovet JM, Ricci S, Mazzaferro V, Hilgard P, Gane E, Blanc JF, de Oliveira AC, Santoro A, Raoul JL, Forner A, Schwartz M, Porta C, Zeuzem S, Bolondi L, Greten TF, Galle PR, Seitz JF, Borbath I, Haussinger D, Giannaris T, Shan M, Moscovici M, Voliotis D, Bruix J (2008) Sorafenib in advanced hepatocellular carcinoma. N Engl J Med 359(4):378–390. doi:10.1056/NEJMoa0708857
Motzer RJ, Hutson TE, Tomczak P, Michaelson MD, Bukowski RM, Rixe O, Oudard S, Negrier S, Szczylik C, Kim ST, Chen I, Bycott PW, Baum CM, Figlin RA (2007) Sunitinib versus interferon alfa in metastatic renal-cell carcinoma. N Engl J Med 356 (2):115–124. doi:10.1056/NEJMoa065044
Raymond E, Dahan L, Raoul JL, Bang YJ, Borbath I, Lombard-Bohas C, Valle J, Metrakos P, Smith D, Vinik A, Chen JS, Horsch D, Hammel P, Wiedenmann B, Van Cutsem E, Patyna S, Lu DR, Blanckmeister C, Chao R, Ruszniewski P (2011) Sunitinib malate for the treatment of pancreatic neuroendocrine tumors. N Engl J Med 364(6):501–513. doi:10.1056/NEJMoa1003825
Motzer RJ, Hutson TE, Cella D, Reeves J, Hawkins R, Guo J, Nathan P, Staehler M, de Souza P, Merchan JR, Boleti E, Fife K, Jin J, Jones R, Uemura H, De Giorgi U, Harmenberg U, Wang J, Sternberg CN, Deen K, McCann L, Hackshaw MD, Crescenzo R, Pandite LN, Choueiri TK (2013) Pazopanib versus sunitinib in metastatic renal-cell carcinoma. N Engl J Med 369(8):722–731. doi:10.1056/NEJMoa1303989
Schutz FA, Choueiri TK, Sternberg CN (2011) Pazopanib: clinical development of a potent anti-angiogenic drug. Crit Rev Oncol Hematol 77(3):163–171. doi:10.1016/j.critrevonc.2010.02.012
Strumberg D, Schultheis B (2012) Regorafenib for cancer. Expert Opin Investig Drugs 21(6):879–889. doi:10.1517/13543784.2012.684752
Chiorean EG, Sweeney C, Youssoufian H, Qin A, Dontabhaktuni A, Loizos N, Nippgen J, Amato R (2014) A phase I study of olaratumab, an anti-platelet-derived growth factor receptor alpha (PDGFRalpha) monoclonal antibody, in patients with advanced solid tumors. Cancer Chemother Pharmacol 73(3):595–604. doi:10.1007/s00280-014-2389-9
Presta M, Dell’Era P, Mitola S, Moroni E, Ronca R, Rusnati M (2005) Fibroblast growth factor/fibroblast growth factor receptor system in angiogenesis. Cytokine Growth Factor Rev 16(2):159–178. doi:10.1016/j.cytogfr.2005.01.004
Bottcher RT, Niehrs C (2005) Fibroblast growth factor signaling during early vertebrate development. Endocr Rev 26 (1):63–77. doi:10.1210/er.2003-0040
Carmeliet P, Jain RK (2000) Angiogenesis in cancer and other diseases. Nature 407(6801):249–257. doi:10.1038/35025220
Dow JK, deVere WRW (2000) Fibroblast growth factor 2: its structure and property, paracrine function, tumor angiogenesis, and prostate-related mitogenic and oncogenic functions. Urology 55(6):800–806
Shing Y, Folkman J, Sullivan R, Butterfield C, Murray J, Klagsbrun M (1984) Heparin affinity: purification of a tumor-derived capillary endothelial cell growth factor. Science 223(4642):1296–1299
Desbaillets I, Ziegler U, Groscurth P, Gassmann M (2000) Embryoid bodies: an in vitro model of mouse embryogenesis. Exp Physiol 85(6):645–651
Stegmann TJ (1999) New approaches to coronary heart disease: induction of neovascularisation by growth factors. BioDrugs 11(5):301–308
Cross MJ, Claesson-Welsh L (2001) FGF and VEGF function in angiogenesis: signalling pathways, biological responses and therapeutic inhibition. Trends Pharmacol Sci 22(4):201–207
Yu P, Wilhelm K, Dubrac A, Tung JK, Alves TC, Fang JS, Xie Y, Zhu J, Chen Z, De Smet F, Zhang J, Jin SW, Sun L, Sun H, Kibbey RG, Hirschi KK, Hay N, Carmeliet P, Chittenden TW, Eichmann A, Potente M, Simons M (2017) FGF-dependent metabolic control of vascular development. Nature 545(7653):224–228. doi:10.1038/nature22322
Seghezzi G, Patel S, Ren CJ, Gualandris A, Pintucci G, Robbins ES, Shapiro RL, Galloway AC, Rifkin DB, Mignatti P (1998) Fibroblast growth factor-2 (FGF-2) induces vascular endothelial growth factor (VEGF) expression in the endothelial cells of forming capillaries: an autocrine mechanism contributing to angiogenesis. J Cell Biol 141(7):1659–1673
Moscatelli D, Presta M, Joseph-Silverstein J, Rifkin DB (1986) Both normal and tumor cells produce basic fibroblast growth factor. J Cell Physiol 129(2):273–276. doi:10.1002/jcp.1041290220
Kandel J, Bossy-Wetzel E, Radvanyi F, Klagsbrun M, Folkman J, Hanahan D (1991) Neovascularization is associated with a switch to the export of bFGF in the multistep development of fibrosarcoma. Cell 66(6):1095–1104. doi:0092-8674(91)90033-U [pii]
Li VW, Folkerth RD, Watanabe H, Yu C, Rupnick M, Barnes P, Scott RM, Black PM, Sallan SE, Folkman J (1994) Microvessel count and cerebrospinal fluid basic fibroblast growth factor in children with brain tumours. Lancet 344(8915):82–86
Baird A, Mormede P, Bohlen P (1986) Immunoreactive fibroblast growth factor (FGF) in a transplantable chondrosarcoma: inhibition of tumor growth by antibodies to FGF. J Cell Biochem 30(1):79–85. doi:10.1002/jcb.240300109
Gross JL, Herblin WF, Dusak BA, Czerniak P, Diamond MD, Sun T, Eidsvoog K, Dexter DL, Yayon A (1993) Effects of modulation of basic fibroblast growth factor on tumor growth in vivo. J Natl Cancer Inst 85(2):121–131
Hori A, Sasada R, Matsutani E, Naito K, Sakura Y, Fujita T, Kozai Y (1991) Suppression of solid tumor growth by immunoneutralizing monoclonal antibody against human basic fibroblast growth factor. Cancer Res 51(22):6180–6184
Czubayko F, Liaudet-Coopman ED, Aigner A, Tuveson AT, Berchem GJ, Wellstein A (1997) A secreted FGF-binding protein can serve as the angiogenic switch in human cancer. Nat Med 3(10):1137–1140
Rak J, Kerbel RS (1997) bFGF and tumor angiogenesis--back in the limelight? Nat Med 3(10):1083–1084
Auguste P, Gursel DB, Lemiere S, Reimers D, Cuevas P, Carceller F, Di Santo JP, Bikfalvi A (2001) Inhibition of fibroblast growth factor/fibroblast growth factor receptor activity in glioma cells impedes tumor growth by both angiogenesis-dependent and -independent mechanisms. Cancer Res 61(4):1717–1726
Polnaszek N, Kwabi-Addo B, Peterson LE, Ozen M, Greenberg NM, Ortega S, Basilico C, Ittmann M (2003) Fibroblast growth factor 2 promotes tumor progression in an autochthonous mouse model of prostate cancer. Cancer Res 63(18):5754–5760
Liang J, Chen P, Hu Z, Zhou X, Chen L, Li M, Wang Y, Tang J, Wang H, Shen H (2008) Genetic variants in fibroblast growth factor receptor 2 (FGFR2) contribute to susceptibility of breast cancer in Chinese women. Carcinogenesis 29(12):2341–2346. doi:10.1093/carcin/bgn235
Agarwal D, Pineda S, Michailidou K, Herranz J, Pita G, Moreno LT, Alonso MR, Dennis J, Wang Q, Bolla MK, Meyer KB, Menendez-Rodriguez P, Hardisson D, Mendiola M, Gonzalez-Neira A, Lindblom A, Margolin S, Swerdlow A, Ashworth A, Orr N, Jones M, Matsuo K, Ito H, Iwata H, Kondo N, Hartman M, Hui M, Lim WY, Iau PT, Sawyer E, Tomlinson I, Kerin M, Miller N, Kang D, Choi J, Park SK, Noh D, Hopper JL, Schmidt DF, Makalic E, Southey MC, Teo SH, Yip CH, Sivanandan K, Tay W, Brauch H, Bruning T, Hamann U, Dunning AM, Shah M, Andrulis IL, Knight JA, Glendon G, Tchatchou S, Schmidt MK, Broeks A, Rosenberg EH, van’t Veer LJ, Fasching PA, Renner SP, Ekici AB, Beckmann MW, Shen C, Hsiung C, Yu J, Hou M, Blot W, Cai Q, Wu AH, Tseng C, Van Den Berg D, Stram DO, Cox A, Brock IW, Reed MW, Muir K, Lophatananon A, Stewart-Brown S, Siriwanarangsan P, Zheng W, Deming-Halverson S, Shrubsole MJ, Long J, Shu X, Lu W, Gao Y, Zhang B, Radice P, Peterlongo P, Manoukian S, Mariette F, Sangrajrang S, McKay J, Couch FJ, Toland AE, Yannoukakos D, Fletcher O, Johnson N, dos Santos SI, Peto J, Marme F, Burwinkel B, Guenel P, Truong T, Sanchez M, Mulot C, Bojesen SE, Nordestgaard BG, Flyer H, Brenner H, Dieffenbach AK, Arndt V, Stegmaier C, Mannermaa A, Kataja V, Kosma V, Hartikainen JM, Lambrechts D, Yesilyurt BT, Floris G, Leunen K, Chang-Claude J, Rudolph A, Seibold P, Flesch-Janys D, Wang X, Olson JE, Vachon C, Purrington K, Giles GG, Severi G, Baglietto L, Haiman CA, Henderson BE, Schumacher F, Marchand LL, Simard J, Dumont M, Goldberg MS, Labreche F, Winqvist R, Pylkas K, Jukkola-Vuorinen A, Grip M, Devilee P, Tollenaar RA, Seynaeve C, Garcia-Closas M, Chanock SJ, Lissowska J, Figueroa JD, Czene K, Eriksson M, Humphreys K, Darabi H, Hooning MJ, Kriege M, Collee JM, Tilanus-Linthorst M, Li J, Jakubowska A, Lubinski J, Jaworska-Bieniek K, Durda K, Nevanlinna H, Muranen TA, Aittomaki K, Blomqvist C, Bogdanova N, Dork T, Hall P, Chenevix-Trench G, Easton DF, Pharroah PD, Arias-Perez JI, Zamora P, Benitez J, Milne RL (2014) FGF receptor genes and breast cancer susceptibility: results from the Breast Cancer Association Consortium. Br J Cancer 110(4):1088–1100. doi:10.1038/bjc.2013.769
Yamamoto Y, Matsui J, Matsushima T, Obaishi H, Miyazaki K, Nakamura K, Tohyama O, Semba T, Yamaguchi A, Hoshi SS, Mimura F, Haneda T, Fukuda Y, Kamata J, Takahashi K, Matsukura M, Wakabayashi T, Asada M, Nomoto K, Watanabe T, Dezso Z, Yoshimatsu K, Funahashi Y, Tsuruoka A (2014) Lenvatinib, an angiogenesis inhibitor targeting VEGFR/FGFR, shows broad antitumor activity in human tumor xenograft models associated with microvessel density and pericyte coverage. Vasc Cell 6:18. doi:10.1186/2045-824X-6-18
Schneider BP, Miller KD (2005) Angiogenesis of breast cancer. J Clin Oncol 23(8):1782–1790. doi:10.1200/jco.2005.12.017
Bareschino MA, Schettino C, Colantuoni G, Rossi E, Rossi A, Maione P, Ciardiello F, Gridelli C (2011) The role of antiangiogenetic agents in the treatment of breast cancer. Curr Med Chem 18(33):5022–5032
Khosravi Shahi P, Soria Lovelle A, Perez Manga G (2009) Tumoral angiogenesis and breast cancer. Clin Transl Oncol 11(3):138–142
Zhang HT, Craft P, Scott PA, Ziche M, Weich HA, Harris AL, Bicknell R (1995) Enhancement of tumor growth and vascular density by transfection of vascular endothelial cell growth factor into MCF-7 human breast carcinoma cells. J Natl Cancer Inst 87(3):213–219
Chen W, Wang S, Tian T, Bai J, Hu Z, Xu Y, Dong J, Chen F, Wang X, Shen H (2009) Phenotypes and genotypes of insulin-like growth factor 1, IGF-binding protein-3 and cancer risk: evidence from 96 studies. Eur J Hum Genet 17(12):1668–1675. doi:10.1038/ejhg.2009.86
Fox SB, Generali DG, Harris AL (2007) Breast tumour angiogenesis. Breast Cancer Res 9(6):216. doi:10.1186/bcr1796
Toffoli S, Roegiers A, Feron O, Van Steenbrugge M, Ninane N, Raes M, Michiels C (2009) Intermittent hypoxia is an angiogenic inducer for endothelial cells: role of HIF-1. Angiogenesis 12(1):47–67. doi:10.1007/s10456-009-9131-y
Naumov GN, Bender E, Zurakowski D, Kang SY, Sampson D, Flynn E, Watnick RS, Straume O, Akslen LA, Folkman J, Almog N (2006) A model of human tumor dormancy: an angiogenic switch from the nonangiogenic phenotype. J Natl Cancer Inst 98(5):316–325. doi:10.1093/jnci/djj068
Hyder SM (2006) Sex-steroid regulation of vascular endothelial growth factor in breast cancer. Endocr Relat Cancer 13(3):667–687. doi:10.1677/erc.1.00931
Rubanyi GM, Johns A, Kauser K (2002) Effect of estrogen on endothelial function and angiogenesis. Vasc Pharmacol 38(2):89–98
Greb RR, Heikinheimo O, Williams RF, Hodgen GD, Goodman AL (1997) Vascular endothelial growth factor in primate endometrium is regulated by oestrogen-receptor and progesterone-receptor ligands in vivo. Hum Reprod 12(6):1280–1292
Morales DE, McGowan KA, Grant DS, Maheshwari S, Bhartiya D, Cid MC, Kleinman HK, Schnaper HW (1995) Estrogen promotes angiogenic activity in human umbilical vein endothelial cells in vitro and in a murine model. Circulation 91(3):755–763
Kim-Schulze S, McGowan KA, Hubchak SC, Cid MC, Martin MB, Kleinman HK, Greene GL, Schnaper HW (1996) Expression of an estrogen receptor by human coronary artery and umbilical vein endothelial cells. Circulation 94(6):1402–1407
Thomas T, Rhodin J, Clark L, Garces A (2003) Progestins initiate adverse events of menopausal estrogen therapy. Climacteric 6(4):293–301
Kerbel RS (2012) Strategies for improving the clinical benefit of antiangiogenic drug based therapies for breast cancer. J Mammary Gland Biol Neoplasia 17(3–4):229–239. doi:10.1007/s10911-012-9266-0
Mackey J, Gelmon K, Martin M, McCarthy N, Pinter T, Rupin M, Youssoufian H (2009) TRIO-012: a multicenter, multinational, randomized, double-blind phase III study of IMC-1121B plus docetaxel versus placebo plus docetaxel in previously untreated patients with HER2-negative, unresectable, locally recurrent or metastatic breast cancer. Clin Breast Cancer 9(4):258–261. doi:10.3816/CBC.2009.n.044
Munoz R, Shaked Y, Bertolini F, Emmenegger U, Man S, Kerbel RS (2005) Anti-angiogenic treatment of breast cancer using metronomic low-dose chemotherapy. Breast 14(6):466–479. doi:10.1016/j.breast.2005.08.026
Colleoni M, Rocca A, Sandri MT, Zorzino L, Masci G, Nole F, Peruzzotti G, Robertson C, Orlando L, Cinieri S, de BF, Viale G, Goldhirsch A (2002) Low-dose oral methotrexate and cyclophosphamide in metastatic breast cancer: antitumor activity and correlation with vascular endothelial growth factor levels. Ann Oncol 13 (1):73–80
Rossari JR, Metzger-Filho O, Paesmans M, Saini KS, Gennari A, de Azambuja E, Piccart-Gebhart M (2012) Bevacizumab and breast cancer: a meta-analysis of first-line phase III studies and a critical reappraisal of available evidence. J Oncol 2012:417673. doi:10.1155/2012/417673
Montero AJ, Vogel C (2012) Fighting fire with fire: rekindling the bevacizumab debate. N Engl J Med 366(4):374–375. doi:10.1056/NEJMe1113368
Sikov WM, Berry DA, Perou CM, Singh B, Cirrincione CT, Tolaney SM, Kuzma CS, Pluard TJ, Somlo G, Port ER, Golshan M, Bellon JR, Collyar D, Hahn OM, Carey LA, Hudis CA, Winer EP (2015) Impact of the addition of carboplatin and/or bevacizumab to neoadjuvant once-per-week paclitaxel followed by dose-dense doxorubicin and cyclophosphamide on pathologic complete response rates in stage II to III triple-negative breast cancer: CALGB 40603 (Alliance). J Clin Oncol 33(1):13–21. doi:10.1200/JCO.2014.57.0572
von Minckwitz G, Eidtmann H, Rezai M, Fasching PA, Tesch H, Eggemann H, Schrader I, Kittel K, Hanusch C, Kreienberg R, Solbach C, Gerber B, Jackisch C, Kunz G, Blohmer JU, Huober J, Hauschild M, Fehm T, Muller BM, Denkert C, Loibl S, Nekljudova V, Untch M (2012) Neoadjuvant chemotherapy and bevacizumab for HER2-negative breast cancer. N Engl J Med 366(4):299–309. doi:10.1056/NEJMoa1111065
Cameron D, Brown J, Dent R, Jackisch C, Mackey J, Pivot X, Steger GG, Suter TM, Toi M, Parmar M, Laeufle R, Im YH, Romieu G, Harvey V, Lipatov O, Pienkowski T, Cottu P, Chan A, Im SA, Hall PS, Bubuteishvili-Pacaud L, Henschel V, Deurloo RJ, Pallaud C, Bell R (2013) Adjuvant bevacizumab-containing therapy in triple-negative breast cancer (BEATRICE): primary results of a randomised, phase 3 trial. Lancet Oncol 14(10):933–942. doi:10.1016/s1470-2045(13)70335-8
Fuchs CS, Tomasek J, Yong CJ, Dumitru F, Passalacqua R, Goswami C, Safran H, dos Santos LV, Aprile G, Ferry DR, Melichar B, Tehfe M, Topuzov E, Zalcberg JR, Chau I, Campbell W, Sivanandan C, Pikiel J, Koshiji M, Hsu Y, Liepa AM, Gao L, Schwartz JD, Tabernero J (2014) Ramucirumab monotherapy for previously treated advanced gastric or gastro-oesophageal junction adenocarcinoma (REGARD): an international, randomised, multicentre, placebo-controlled, phase 3 trial. Lancet (London, England) 383(9911):31–39. doi:10.1016/s0140-6736(13)61719-5
Wilke H, Muro K, Van Cutsem E, Oh SC, Bodoky G, Shimada Y, Hironaka S, Sugimoto N, Lipatov O, Kim TY, Cunningham D, Rougier P, Komatsu Y, Ajani J, Emig M, Carlesi R, Ferry D, Chandrawansa K, Schwartz JD, Ohtsu A (2014) Ramucirumab plus paclitaxel versus placebo plus paclitaxel in patients with previously treated advanced gastric or gastro-oesophageal junction adenocarcinoma (RAINBOW): a double-blind, randomised phase 3 trial. Lancet Oncol 15(11):1224–1235. doi:10.1016/s1470-2045(14)70420-6
Hoar FJ, Chaudhri S, Wadley MS, Stonelake PS (2003) Co-expression of vascular endothelial growth factor C (VEGF-C) and c-erbB2 in human breast carcinoma. Eur J Cancer 39(12):1698–1703
Dieras V, Wildiers H, Jassem J, Dirix LY, Guastalla JP, Bono P, Hurvitz SA, Goncalves A, Romieu G, Limentani SA, Jerusalem G, Lakshmaiah KC, Roche H, Sanchez-Rovira P, Pienkowski T, Segui Palmer MA, Li A, Sun YN, Pickett CA, Slamon DJ (2015) Trebananib (AMG 386) plus weekly paclitaxel with or without bevacizumab as first-line therapy for HER2-negative locally recurrent or metastatic breast cancer: a phase 2 randomized study. Breast (Edinburgh, Scotland) 24(3):182–190. doi:10.1016/j.breast.2014.11.003
Robert NJ, Dieras V, Glaspy J, Brufsky AM, Bondarenko I, Lipatov ON, Perez EA, Yardley DA, Chan SY, Zhou X, Phan SC, O’Shaughnessy J (2011) RIBBON-1: randomized, double-blind, placebo-controlled, phase III trial of chemotherapy with or without bevacizumab for first-line treatment of human epidermal growth factor receptor 2-negative, locally recurrent or metastatic breast cancer. J Clin Oncol 29(10):1252–1260. doi:10.1200/jco.2010.28.0982
Kerbel RS, Benezra R, Lyden DC, Hattori K, Heissig B, Nolan DJ, Mittal V, Shaked Y, Dias S, Bertolini F, Rafii S (2008) Endothelial progenitor cells are cellular hubs essential for neoangiogenesis of certain aggressive adenocarcinomas and metastatic transition but not adenomas. Proceedings of the National Academy of Sciences of the United States of America 105 (34):E54; author reply E55. doi:10.1073/pnas.0804876105
Folkman J (2006) Antiangiogenesis in cancer therapy--endostatin and its mechanisms of action. Exp Cell Res 312(5):594–607. doi:10.1016/j.yexcr.2005.11.015
Fernandez PM, Rickles FR (2002) Tissue factor and angiogenesis in cancer. Curr Opin Hematol 9(5):401–406
Satchi-Fainaro R, Puder M, Davies JW, Tran HT, Sampson DA, Greene AK, Corfas G, Folkman J (2004) Targeting angiogenesis with a conjugate of HPMA copolymer and TNP-470. Nat Med 10(3):255–261. doi:10.1038/nm1002
Sakurai T, Kudo M (2011) Signaling pathways governing tumor angiogenesis. Oncology 81(Suppl 1):24–29. doi:10.1159/000333256
Burstein HJ, Chen YH, Parker LM, Savoie J, Younger J, Kuter I, Ryan PD, Garber JE, Chen H, Campos SM, Shulman LN, Harris LN, Gelman R, Winer EP (2008) VEGF as a marker for outcome among advanced breast cancer patients receiving anti-VEGF therapy with bevacizumab and vinorelbine chemotherapy. Clin Cancer Res 14(23):7871–7877. doi:10.1158/1078-0432.ccr-08-0593
Schneider BP, Wang M, Radovich M, Sledge GW, Badve S, Thor A, Flockhart DA, Hancock B, Davidson N, Gralow J, Dickler M, Perez EA, Cobleigh M, Shenkier T, Edgerton S, Miller KD (2008) Association of vascular endothelial growth factor and vascular endothelial growth factor receptor-2 genetic polymorphisms with outcome in a trial of paclitaxel compared with paclitaxel plus bevacizumab in advanced breast cancer: ECOG 2100. J Clin Oncol 26(28):4672–4678. doi:10.1200/jco.2008.16.1612
Kim DH, Xu W, Kamel-Reid S, Liu X, Jung CW, Kim S, Lipton JH (2010) Clinical relevance of vascular endothelial growth factor (VEGFA) and VEGF receptor (VEGFR2) gene polymorphism on the treatment outcome following imatinib therapy. Ann Oncol 21(6):1179–1188. doi:10.1093/annonc/mdp452
Smith ER, Zurakowski D, Saad A, Scott RM, Moses MA (2008) Urinary biomarkers predict brain tumor presence and response to therapy. Clinical cancer research : an official journal of the American Association for Cancer Research 14(8):2378–2386. doi:10.1158/1078-0432.ccr-07-1253
Moses MA, Wiederschain D, Loughlin KR, Zurakowski D, Lamb CC, Freeman MR (1998) Increased incidence of matrix metalloproteinases in urine of cancer patients. Cancer Res 58(7):1395–1399
Burstein HJ, Elias AD, Rugo HS, Cobleigh MA, Wolff AC, Eisenberg PD, Lehman M, Adams BJ, Bello CL, DePrimo SE, Baum CM, Miller KD (2008) Phase II study of sunitinib malate, an oral multitargeted tyrosine kinase inhibitor, in patients with metastatic breast cancer previously treated with an anthracycline and a taxane. Journal of clinical oncology : official journal of the American Society of Clinical Oncology 26(11):1810–1816. doi:10.1200/jco.2007.14.5375
Jain RK (2005) Antiangiogenic therapy for cancer: current and emerging concepts. Oncology (Williston Park) 19(4 Suppl 3):7–16
Kallman RF, Dorie MJ (1986) Tumor oxygenation and reoxygenation during radiation therapy: their importance in predicting tumor response. Int J Radiat Oncol Biol Phys 12(4):681–685. doi:0360-3016(86)90080-5 [pii]
Cao Y, Arbiser J, D’Amato RJ, D’Amore PA, Ingber DE, Kerbel R, Klagsbrun M, Lim S, Moses MA, Zetter B, Dvorak H, Langer R (2011) Forty-year journey of angiogenesis translational research. Sci Transl Med 3(114):114rv113. doi:10.1126/scitranslmed.3003149
Lu H, Shu XO, Cui Y, Kataoka N, Wen W, Cai Q, Ruan ZX, Gao YT, Zheng W (2005) Association of genetic polymorphisms in the VEGF gene with breast cancer survival. Cancer Res 65(12):5015–5019. doi:10.1158/0008-5472.CAN-04-2786
Jin Q, Hemminki K, Enquist K, Lenner P, Grzybowska E, Klaes R, Henriksson R, Chen B, Pamula J, Pekala W, Zientek H, Rogozinska-Szczepka J, Utracka-Hutka B, Hallmans G, Forsti A (2005) Vascular endothelial growth factor polymorphisms in relation to breast cancer development and prognosis. Clin Cancer Res 11(10):3647–3653. doi:10.1158/1078-0432.CCR-04-1803
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This work has been supported by grants from the National Key R&D Program (2016YFC1302301) by National Natural Science Foundation of China (81672738, U1601223).
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Zhou, Z., Yao, H., Hu, H. (2017). Disrupting Tumor Angiogenesis and “the Hunger Games” for Breast Cancer. In: Song, E., Hu, H. (eds) Translational Research in Breast Cancer. Advances in Experimental Medicine and Biology, vol 1026. Springer, Singapore. https://doi.org/10.1007/978-981-10-6020-5_8
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