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Adapting the Foreign Soil: Factors Promoting Tumor Metastasis

  • Ramish RiazEmail author
  • Shah Rukh Abbas
  • Maria Shabbir
Chapter
  • 30 Downloads

Abstract

Majority of the deaths associated with cancer are attributed to metastasis. Till now there had been no cure of metastasis. Metastatic cells are usually resistant to conventional radiotherapy and chemotherapeutic agents. Metastasis can occur even after decades of treatment of primary tumor. Insights into the molecular mechanisms promoting metastasis could help in developing novel techniques that will prevent development of metastasis. The chapter discusses the major molecular mechanisms that support metastasis. It highlights the mechanisms involved in metastatic dormancy, immunomodulation, and mechano-transduction and their possible role in establishment of metastasis. It gives in-depth review of tumor microenvironment and how microenvironment plays role in supporting micrometastasis. It also discusses the mechanisms and factors which help the micrometastasis to escape the immune response and develop overt metastasis.

Keywords

Metastasis Tumor microenvironment Immune modulation Mechano-transduction Chemotherapeutic agents 

References

  1. 1.
    Patel P, Chen EI (2012) Cancer stem cells, tumor dormancy, and metastasis. Front Endocrinol 3:125CrossRefGoogle Scholar
  2. 2.
    Smith BN, Bhowmick NA (2016) Role of EMT in metastasis and therapy resistance. J Clin Med 5(2):E17CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Chaffer CL, San Juan BP, Lim E, Weinberg RA (2016) EMT, cell plasticity and metastasis. Cancer Metastasis Rev 35(4):645–654CrossRefGoogle Scholar
  4. 4.
    Jablonska-Trypuc A, Matejczyk M, Rosochacki S (2016) Matrix metalloproteinases (MMPs), the main extracellular matrix (ECM) enzymes in collagen degradation, as a target for anticancer drugs. J Enzyme Inhib Med Chem 31(suppl 1):177–183CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Jiang WG, Sanders AJ, Katoh M, Ungefroren H, Gieseler F, Prince M et al (2015) Tissue invasion and metastasis: molecular, biological and clinical perspectives. Semin Cancer Biol 35(Suppl):S244–SS75CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Lambert AW, Pattabiraman DR, Weinberg RA (2017) Emerging biological principles of metastasis. Cell 168(4):670–691CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Aguirre-Ghiso JA (2007) Models, mechanisms and clinical evidence for cancer dormancy. Nat Rev Cancer 7(11):834–846CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Lipworth S, Hammond RJ, Baron VO, Hu Y, Coates A, Gillespie SH (2016) Defining dormancy in mycobacterial disease. Tuberculosis 99:131–142CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Sosa MS, Bragado P, Aguirre-Ghiso JA (2014) Mechanisms of disseminated cancer cell dormancy: an awakening field. Nat Rev Cancer 14(9):611–622CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Manjili MH (2017) Tumor dormancy and relapse: from a natural byproduct of evolution to a disease state. Cancer Res 77(10):2564–2569CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Hadfield G (1954) The dormant cancer cell. Br Med J 2(4888):607–610CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Hosseini H, Obradovic MMS, Hoffmann M, Harper KL, Sosa MS, Werner-Klein M et al (2016) Early dissemination seeds metastasis in breast cancer. Nature 540(7634):552–558CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Gao XL, Zhang M, Tang YL, Liang XH (2017) Cancer cell dormancy: mechanisms and implications of cancer recurrence and metastasis. Onco Targets Ther 10:5219–5228CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Gomis RR, Gawrzak S (2017) Tumor cell dormancy. Mol Oncol 11(1):62–78CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Aguirre-Ghiso JA, Estrada Y, Liu D, Ossowski L (2003) ERK(MAPK) activity as a determinant of tumor growth and dormancy; regulation by p38(SAPK). Cancer Res 63(7):1684–1695PubMedPubMedCentralGoogle Scholar
  16. 16.
    Gay LJ, Malanchi I (2017) The sleeping ugly: tumour microenvironment’s act to make or break the spell of dormancy. Biochim Biophys Acta Rev Cancer 1868(1):231–238CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Sosa MS, Avivar-Valderas A, Bragado P, Wen HC, Aguirre-Ghiso JA (2011) ERK1/2 and p38alpha/beta signaling in tumor cell quiescence: opportunities to control dormant residual disease. Clin Cancer Res 17(18):5850–5857CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Jo H, Jia Y, Subramanian KK, Hattori H, Luo HR (2008) Cancer cell-derived clusterin modulates the phosphatidylinositol 3′-kinase-Akt pathway through attenuation of insulin-like growth factor 1 during serum deprivation. Mol Cell Biol 28(13):4285–4299CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Vera-Ramirez L (2019) Cell-intrinsic survival signals. The role of autophagy in metastatic dissemination and tumor cell dormancy. Semin Cancer Biol.  https://doi.org/10.1016/j.semcancer.2019.07.027. [Epub ahead of print]
  20. 20.
    Prunier C, Baker D, ten Dijke P, Ritsma L (2019) TGF-β family signaling pathways in cellular dormancy. Trends Cancer 5(1):66–78CrossRefGoogle Scholar
  21. 21.
    Kobayashi A, Okuda H, Xing F, Pandey PR, Watabe M, Hirota S et al (2011) Bone morphogenetic protein 7 in dormancy and metastasis of prostate cancer stem-like cells in bone. J Exp Med 208(13):2641–2655CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Seidi K, Manjili MH, Jahanban-Esfahlan R, Javaheri T (2018) Tumor cell dormancy: threat or opportunity in the fight against cancer. Cancer 11(8):1207Google Scholar
  23. 23.
    Wang H-F, Wang S-S, Huang M-C, Liang X-H, Tang Y-J, Tang Y-L (2019) Targeting immune-mediated dormancy: a promising treatment of cancer. Front Oncol 9:498CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Osisami M, Keller ET (2013) Mechanisms of metastatic tumor dormancy. J Clin Med 2(3):136–150CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Saudemont A, Hamrouni A, Marchetti P, Liu J, Jouy N, Hetuin D et al (2007) Dormant tumor cells develop cross-resistance to apoptosis induced by CTLs or imatinib mesylate via methylation of suppressor of cytokine signaling 1. Cancer Res 67(9):4491–4498CrossRefGoogle Scholar
  26. 26.
    Zhou Y, Su Y, Zhu H, Wang X, Li X, Dai C et al (2019) Interleukin-23 receptor signaling mediates cancer dormancy and radioresistance in human esophageal squamous carcinoma cells via the Wnt/Notch pathway. J Mol Med 97(2):177–188CrossRefGoogle Scholar
  27. 27.
    Yadav AS, Pandey PR, Butti R, Radharani NNV, Roy S, Bhalara SR et al (2018) The biology and therapeutic implications of tumor dormancy and reactivation. Front Oncol 8:72CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Senft D, Ze Ronai A (2016) Immunogenic, cellular, and angiogenic drivers of tumor dormancy-a melanoma view. Pigment Cell Melanoma Res 29(1):27–42CrossRefGoogle Scholar
  29. 29.
    Straume O, Shimamura T, Lampa MJ, Carretero J, Oyan AM, Jia D et al (2012) Suppression of heat shock protein 27 induces long-term dormancy in human breast cancer. Proc Natl Acad Sci U S A 109(22):8699–8704CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Ghajar CM, Peinado H, Mori H, Matei IR, Evason KJ, Brazier H et al (2013) The perivascular niche regulates breast tumour dormancy. Nat Cell Biol 15(7):807–817CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Hofstetter CP, Burkhardt JK, Shin BJ, Gursel DB, Mubita L, Gorrepati R et al (2012) Protein phosphatase 2A mediates dormancy of glioblastoma multiforme-derived tumor stem-like cells during hypoxia. PLoS One 7(1):e30059CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Weidenfeld K, Schif-Zuck S, Abu-Tayeh H, Kang K, Kessler O, Weissmann M et al (2016) Dormant tumor cells expressing LOXL2 acquire a stem-like phenotype mediating their transition to proliferative growth. Oncotarget 7(44):71362–71377CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Endo H, Inoue M (2019) Dormancy in cancer. Cancer Sci 110(2):474–480CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Alison MR, Islam S, Wright NA (2010) Stem cells in cancer: instigators and propagators? J Cell Sci 123(Pt 14):2357–2368CrossRefGoogle Scholar
  35. 35.
    Chaffer CL, Brueckmann I, Scheel C, Kaestli AJ, Wiggins PA, Rodrigues LO et al (2011) Normal and neoplastic nonstem cells can spontaneously convert to a stem-like state. Proc Natl Acad Sci U S A 108(19):7950–7955CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Liang J, Shao SH, Xu ZX, Hennessy B, Ding Z, Larrea M et al (2007) The energy sensing LKB1-AMPK pathway regulates p27(kip1) phosphorylation mediating the decision to enter autophagy or apoptosis. Nat Cell Biol 9(2):218–224CrossRefGoogle Scholar
  37. 37.
    Sinha G, Sherman LS, Sandiford OA, Williams LM, Ayer S, Walker ND et al (2016) Mesenchymal stem cell-breast cancer stem cell: relevance to dormancy. J Cancer Stem Cell Res 4:1CrossRefGoogle Scholar
  38. 38.
    Psaila B, Lyden D (2009) The metastatic niche: adapting the foreign soil. Nat Rev Cancer 9(4):285–293CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Peinado H, Zhang H, Matei IR, Costa-Silva B, Hoshino A, Rodrigues G et al (2017) Pre-metastatic niches: organ-specific homes for metastases. Nat Rev Cancer 17(5):302–317CrossRefGoogle Scholar
  40. 40.
    Kaplan RN, Riba RD, Zacharoulis S, Bramley AH, Vincent L, Costa C et al (2005) VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 438(7069):820–827CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Liu Y, Cao X (2016) Characteristics and Significance of the pre-metastatic Niche. Cancer Cell 30(5):668–681CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Costa-Silva B, Aiello NM, Ocean AJ, Singh S, Zhang H, Thakur BK et al (2015) Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver. Nat Cell Biol 17(6):816–826CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Guise T (2010) Examining the metastatic niche: targeting the microenvironment. Semin Oncol 37(Suppl 2):S2–S14CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Gupta GP, Nguyen DX, Chiang AC, Bos PD, Kim JY, Nadal C et al (2007) Mediators of vascular remodelling co-opted for sequential steps in lung metastasis. Nature 446(7137):765–770CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Hiratsuka S, Goel S, Kamoun WS, Maru Y, Fukumura D, Duda DG et al (2011) Endothelial focal adhesion kinase mediates cancer cell homing to discrete regions of the lungs via E-selectin up-regulation. Proc Natl Acad Sci U S A 108(9):3725–3730CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Qian BZ, Li J, Zhang H, Kitamura T, Zhang J, Campion LR et al (2011) CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature 475(7355):222–225CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Labelle M, Begum S, Hynes RO (2014) Platelets guide the formation of early metastatic niches. Proc Natl Acad Sci U S A 111(30):E3053–E3061CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Hoshino A, Costa-Silva B, Shen TL, Rodrigues G, Hashimoto A, Tesic Mark M et al (2015) Tumour exosome integrins determine organotropic metastasis. Nature 527(7578):329–335CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Lukanidin E, Sleeman JP (2012) Building the niche: the role of the S100 proteins in metastatic growth. Semin Cancer Biol 22(3):216–225CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Lu X, Kang Y (2007) Organotropism of breast cancer metastasis. J Mammary Gland Biol Neoplasia 12(2-3):153–162CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Sharma SK, Chintala NK, Vadrevu SK, Patel J, Karbowniczek M, Markiewski MM (2015) Pulmonary alveolar macrophages contribute to the premetastatic niche by suppressing antitumor T cell responses in the lungs. J Immunol 194(11):5529–5538CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Malanchi I, Santamaria-Martinez A, Susanto E, Peng H, Lehr HA, Delaloye JF et al (2011) Interactions between cancer stem cells and their niche govern metastatic colonization. Nature 481(7379):85–89CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Deng X, Ao S, Hou J, Li Z, Lei Y, Lyu G (2019) Prognostic significance of periostin in colorectal cancer. Chin J Cancer Res 31(3):547–556CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Kudo A (2011) Periostin in fibrillogenesis for tissue regeneration: periostin actions inside and outside the cell. Cell Mol Life Sci 68(19):3201–3207CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Kim S, Takahashi H, Lin WW, Descargues P, Grivennikov S, Kim Y et al (2009) Carcinoma-produced factors activate myeloid cells through TLR2 to stimulate metastasis. Nature 457(7225):102–106CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Erler JT, Bennewith KL, Cox TR, Lang G, Bird D, Koong A et al (2009) Hypoxia-induced lysyl oxidase is a critical mediator of bone marrow cell recruitment to form the premetastatic niche. Cancer Cell 15(1):35–44CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Xiong A, Liu Y (2017) Targeting hypoxia inducible factors-1α as a novel therapy in fibrosis. Front Pharmacol 8:326CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Cox TR, Bird D, Baker AM, Barker HE, Ho MW, Lang G et al (2013) LOX-mediated collagen crosslinking is responsible for fibrosis-enhanced metastasis. Cancer Res 73(6):1721–1732CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Ahn GO, Brown JM (2008) Matrix metalloproteinase-9 is required for tumor vasculogenesis but not for angiogenesis: role of bone marrow-derived myelomonocytic cells. Cancer Cell 13(3):193–205CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Casbon A-J, Reynaud D, Park C, Khuc E, Gan DD, Schepers K et al (2015) Invasive breast cancer reprograms early myeloid differentiation in the bone marrow to generate immunosuppressive neutrophils. Proc Natl Acad Sci U S A 112(6):E56–E75CrossRefGoogle Scholar
  61. 61.
    Wu CF, Andzinski L, Kasnitz N, Kroger A, Klawonn F, Lienenklaus S et al (2015) The lack of type I interferon induces neutrophil-mediated pre-metastatic niche formation in the mouse lung. Int J Cancer 137(4):837–847CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Wculek SK, Malanchi I (2015) Neutrophils support lung colonization of metastasis-initiating breast cancer cells. Nature 528(7582):413–417CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Valiente M, Obenauf AC, Jin X, Chen Q, Zhang XH, Lee DJ et al (2014) Serpins promote cancer cell survival and vascular co-option in brain metastasis. Cell 156(5):1002–1016CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Massague J, Obenauf AC (2016) Metastatic colonization by circulating tumour cells. Nature 529(7586):298–306CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Oh M, Nor JE (2015) The perivascular niche and self-renewal of stem cells. Front Physiol 6:367CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Ding L, Saunders TL, Enikolopov G, Morrison SJ (2012) Endothelial and perivascular cells maintain haematopoietic stem cells. Nature 481(7382):457–462CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Celia-Terrassa T, Kang Y (2018) Metastatic niche functions and therapeutic opportunities. Nat Cell Biol 20(8):868–877CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Borovski T, De Sousa EMF, Vermeulen L, Medema JP (2011) Cancer stem cell niche: the place to be. Cancer Res 71(3):634–639CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Doherty MJ, Ashton BA, Walsh S, Beresford JN, Grant ME, Canfield AE (1998) Vascular pericytes express osteogenic potential in vitro and in vivo. J Bone Miner Res 13(5):828–838CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Plaks V, Kong N, Werb Z (2015) The cancer stem cell niche: how essential is the niche in regulating stemness of tumor cells? Cell Stem Cell 16(3):225–238CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Ting Koh Y, Luz García-Hernández M, Martin Kast W (2006) Tumor immune escape mechanisms. In: Teicher BA (ed) Cancer drug resistance. Humana Press, Totowa, pp 577–602CrossRefGoogle Scholar
  72. 72.
    Johansen LL, Lock-Andersen J, Hviid TVF (2016) The pathophysiological impact of HLA class Ia and HLA-G expression and regulatory T cells in malignant melanoma: a review. J Immunol Res 2016:6829283CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Fiore E, Fusco C, Romero P, Stamenkovic I (2002) Matrix metalloproteinase 9 (MMP-9/gelatinase B) proteolytically cleaves ICAM-1 and participates in tumor cell resistance to natural killer cell-mediated cytotoxicity. Oncogene 21(34):5213–5223CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Dong H, Strome SE, Salomao DR, Tamura H, Hirano F, Flies DB et al (2002) Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat Med 8(8):793–800CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Choi IH, Zhu G, Sica GL, Strome SE, Cheville JC, Lau JS et al (2003) Genomic organization and expression analysis of B7-H4, an immune inhibitory molecule of the B7 family. J Immunol 171(9):4650–4654CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Garg AD, Coulie PG, Van den Eynde BJ, Agostinis P (2017) Integrating next-generation dendritic cell vaccines into the current cancer immunotherapy landscape. Trends Immunol 38(8):577–593CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Loro LL, Ohlsson M, Vintermyr OK, Liavaag PG, Jonsson R, Johannessen AC (2001) Maintained CD40 and loss of polarised CD40 ligand expression in oral squamous cell carcinoma. Anticancer Res 21(1a):113–117PubMedPubMedCentralGoogle Scholar
  78. 78.
    Disis ML (2010) Immune regulation of cancer. J Clin Oncol 28(29):4531–4538CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Gonzalez H, Hagerling C, Werb Z (2018) Roles of the immune system in cancer: from tumor initiation to metastatic progression. Genes Dev 32(19-20):1267–1284CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Albini A, Bruno A, Noonan DM, Mortara L (2018) Contribution to tumor angiogenesis from innate immune cells within the tumor microenvironment: implications for immunotherapy. Front Immunol 9:527CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Multhoff G, Molls M, Radons J (2011) Chronic inflammation in cancer development. Front Immunol 2:98PubMedPubMedCentralGoogle Scholar
  82. 82.
    Yan C, Theodorescu D (2018) RAL GTPases: biology and potential as therapeutic targets in cancer. Pharmacol Rev 70(1):1–11CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Liu T, Zhang L, Joo D, Sun S-C (2017) NF-κB signaling in inflammation. Signal Transduct Target Ther 2:17023CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Liu J, Lin PC, Zhou BP (2015) Inflammation fuels tumor progress and metastasis. Curr Pharm Des 21(21):3032–3040CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Rivera-Cruz CM, Shearer JJ, Figueiredo Neto M, Figueiredo ML (2017) The immunomodulatory effects of mesenchymal stem cell polarization within the tumor microenvironment niche. Stem Cells Int 2017:4015039CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    Bouchlaka MN, Hematti P, Capitini CM (2017) Therapeutic purposes and risks of ex vivo expanded mesenchymal stem/stromal cells. In: Mesenchymal stromal cells as tumor stromal modulators. Elsevier, AmsterdamGoogle Scholar
  87. 87.
    Ribeiro A, Laranjeira P, Mendes S, Velada I, Leite C, Andrade P et al (2013) Mesenchymal stem cells from umbilical cord matrix, adipose tissue and bone marrow exhibit different capability to suppress peripheral blood B, natural killer and T cells. Stem Cell Res Ther 4(5):125CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Liu WH, Liu JJ, Wu J, Zhang LL, Liu F, Yin L et al (2018) Retraction: novel mechanism of inhibition of dendritic cells maturation by mesenchymal stem cells via interleukin-10 and the JAK1/STAT3 signaling pathway. PLoS One 13(3):e0194455CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Zhao ZG, Xu W, Sun L, Li WM, Li QB, Zou P (2012) The characteristics and immunoregulatory functions of regulatory dendritic cells induced by mesenchymal stem cells derived from bone marrow of patient with chronic myeloid leukaemia. Eur J Cancer 48(12):1884–1895CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    Knowles RG, Moncada S (1994) Nitric oxide synthases in mammals. Biochem J 298(Pt 2):249–258CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    Choudhari SK, Chaudhary M, Bagde S, Gadbail AR, Joshi V (2013) Nitric oxide and cancer: a review. World J Surg Oncol 11:118CrossRefGoogle Scholar
  92. 92.
    Eyler CE, Wu Q, Yan K, MacSwords JM, Chandler-Militello D, Misuraca KL et al (2011) Glioma stem cell proliferation and tumor growth are promoted by nitric oxide synthase-2. Cell 146(1):53–66CrossRefPubMedPubMedCentralGoogle Scholar
  93. 93.
    Lu G, Zhang R, Geng S, Peng L, Jayaraman P, Chen C et al (2015) Myeloid cell-derived inducible nitric oxide synthase suppresses M1 macrophage polarization. Nat Commun 6:6676CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Molon B, Ugel S, Del Pozzo F, Soldani C, Zilio S, Avella D et al (2011) Chemokine nitration prevents intratumoral infiltration of antigen-specific T cells. J Exp Med 208(10):1949–1962CrossRefPubMedPubMedCentralGoogle Scholar
  95. 95.
    Gehad AE, Lichtman MK, Schmults CD, Teague JE, Calarese AW, Jiang Y et al (2012) Nitric oxide-producing myeloid-derived suppressor cells inhibit vascular E-selectin expression in human squamous cell carcinomas. J Invest Dermatol 132(11):2642–2651CrossRefPubMedPubMedCentralGoogle Scholar
  96. 96.
    Douguet L, Bod L, Lengagne R, Labarthe L, Kato M, Avril MF et al (2016) Nitric oxide synthase 2 is involved in the pro-tumorigenic potential of gammadelta17 T cells in melanoma. Oncoimmunology 5(8):e1208878CrossRefPubMedPubMedCentralGoogle Scholar
  97. 97.
    Salimian Rizi B, Achreja A, Nagrath D (2017) Nitric oxide: the forgotten child of tumor metabolism. Trends Cancer 3(9):659–672CrossRefPubMedPubMedCentralGoogle Scholar
  98. 98.
    Huber V, Camisaschi C, Berzi A, Ferro S, Lugini L, Triulzi T et al (2017) Cancer acidity: an ultimate frontier of tumor immune escape and a novel target of immunomodulation. Semin Cancer Biol 43:74–89CrossRefPubMedPubMedCentralGoogle Scholar
  99. 99.
    Nakagawa Y, Negishi Y, Shimizu M, Takahashi M, Ichikawa M, Takahashi H (2015) Effects of extracellular pH and hypoxia on the function and development of antigen-specific cytotoxic T lymphocytes. Immunol Lett 167(2):72–86CrossRefPubMedPubMedCentralGoogle Scholar
  100. 100.
    Lotzova E, Savary CA, Herberman RB (1987) Induction of NK cell activity against fresh human leukemia in culture with interleukin 2. J Immunol 138(8):2718–2727PubMedGoogle Scholar
  101. 101.
    Rocca YS, Roberti MP, Arriaga JM, Amat M, Bruno L, Pampena MB et al (2013) Altered phenotype in peripheral blood and tumor-associated NK cells from colorectal cancer patients. Innate Immun 19(1):76–85CrossRefGoogle Scholar
  102. 102.
    Dong H, Bullock TN (2014) Metabolic influences that regulate dendritic cell function in tumors. Front Immunol 5:24CrossRefPubMedPubMedCentralGoogle Scholar
  103. 103.
    Cao TM, Takatani T, King MR (2013) Effect of extracellular pH on selectin adhesion: theory and experiment. Biophys J 104(2):292–299CrossRefPubMedPubMedCentralGoogle Scholar
  104. 104.
    Bellocq A, Suberville S, Philippe C, Bertrand F, Perez J, Fouqueray B et al (1998) Low environmental pH is responsible for the induction of nitric-oxide synthase in macrophages. Evidence for involvement of nuclear factor-kappa B activation. J Biol Chem 273(9):5086–5092CrossRefGoogle Scholar
  105. 105.
    Kinoshita H, Yashiro M, Fukuoka T, Hasegawa T, Morisaki T, Kasashima H et al (2015) Diffuse-type gastric cancer cells switch their driver pathways from FGFR2 signaling to SDF1/CXCR4 axis in hypoxic tumor microenvironments. Carcinogenesis 36(12):1511–1520PubMedGoogle Scholar
  106. 106.
    Ohue Y, Nishikawa H (2019) Regulatory T (Treg) cells in cancer: can Treg cells be a new therapeutic target? Cancer Sci 110(7):2080–2089CrossRefPubMedPubMedCentralGoogle Scholar
  107. 107.
    Wei SC, Yang J (2016) Forcing through tumor metastasis: the interplay between tissue rigidity and epithelial-mesenchymal transition. Trends Cell Biol 26(2):111–120CrossRefGoogle Scholar
  108. 108.
    El-Haibi CP, Bell GW, Zhang J, Collmann AY, Wood D, Scherber CM et al (2012) Critical role for lysyl oxidase in mesenchymal stem cell-driven breast cancer malignancy. Proc Natl Acad Sci U S A 109(43):17460–17465CrossRefPubMedPubMedCentralGoogle Scholar
  109. 109.
    Riaz M, Sieuwerts AM, Look MP, Timmermans MA, Smid M, Foekens JA et al (2012) High TWIST1 mRNA expression is associated with poor prognosis in lymph node-negative and estrogen receptor-positive human breast cancer and is co-expressed with stromal as well as ECM related genes. Breast Cancer Res 14(5):R123CrossRefPubMedPubMedCentralGoogle Scholar
  110. 110.
    Calvo F, Ege N, Grande-Garcia A, Hooper S, Jenkins RP, Chaudhry SI et al (2013) Mechanotransduction and YAP-dependent matrix remodelling is required for the generation and maintenance of cancer-associated fibroblasts. Nat Cell Biol 15(6):637–646CrossRefPubMedPubMedCentralGoogle Scholar
  111. 111.
    Hebner C, Weaver VM, Debnath J (2008) Modeling morphogenesis and oncogenesis in three-dimensional breast epithelial cultures. Annu Rev Pathol 3:313–339CrossRefPubMedPubMedCentralGoogle Scholar
  112. 112.
    Northcott JM, Dean IS, Mouw JK, Weaver VM (2018) Feeling stress: the mechanics of cancer progression and aggression. Front Cell Dev Biol 6:17CrossRefPubMedPubMedCentralGoogle Scholar
  113. 113.
    Broders-Bondon F, Nguyen Ho-Bouldoires TH, Fernandez-Sanchez ME, Farge E (2018) Mechanotransduction in tumor progression: the dark side of the force. J Cell Biol 217(5):1571–1587CrossRefPubMedPubMedCentralGoogle Scholar
  114. 114.
    DuFort CC, Paszek MJ, Weaver VM (2011) Balancing forces: architectural control of mechanotransduction. Nat Rev Mol Cell Biol 12(5):308–319CrossRefPubMedPubMedCentralGoogle Scholar
  115. 115.
    Kou C-TJ, Kandpal RP (2018) Differential expression patterns of Eph receptors and ephrin ligands in human cancers. Biomed Res Int 2018:23Google Scholar
  116. 116.
    Ehrlicher AJ, Nakamura F, Hartwig JH, Weitz DA, Stossel TP (2011) Mechanical strain in actin networks regulates FilGAP and integrin binding to filamin A. Nature 478(7368):260–263CrossRefPubMedPubMedCentralGoogle Scholar
  117. 117.
    Iwamoto DV, Calderwood DA (2015) Regulation of integrin-mediated adhesions. Curr Opin Cell Biol 36:41–47CrossRefPubMedPubMedCentralGoogle Scholar
  118. 118.
    Zhang K, Corsa CA, Ponik SM, Prior JL, Piwnica-Worms D, Eliceiri KW et al (2013) The collagen receptor discoidin domain receptor 2 stabilizes SNAIL1 to facilitate breast cancer metastasis. Nat Cell Biol 15(6):677–687CrossRefPubMedPubMedCentralGoogle Scholar
  119. 119.
    Tsai JH, Yang J (2013) Epithelial-mesenchymal plasticity in carcinoma metastasis. Genes Dev 27(20):2192–2206CrossRefPubMedPubMedCentralGoogle Scholar
  120. 120.
    Scott LE, Weinberg SH, Lemmon CA (2019) Mechanochemical signaling of the extracellular matrix in epithelial-mesenchymal transition. Front Cell Dev Biol 7:135CrossRefPubMedPubMedCentralGoogle Scholar
  121. 121.
    Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C et al (2004) Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117(7):927–939CrossRefPubMedPubMedCentralGoogle Scholar
  122. 122.
    Scarpa E, Szabo A, Bibonne A, Theveneau E, Parsons M, Mayor R (2015) Cadherin switch during EMT in neural crest cells leads to contact inhibition of locomotion via repolarization of forces. Dev Cell 34(4):421–434CrossRefPubMedPubMedCentralGoogle Scholar
  123. 123.
    Basu S, Cheriyamundath S, Ben-Ze’ev A (2018) Cell-cell adhesion: linking Wnt/β-catenin signaling with partial EMT and stemness traits in tumorigenesis. F1000Res 7:488CrossRefGoogle Scholar
  124. 124.
    Gomez EW, Chen QK, Gjorevski N, Nelson CM (2010) Tissue geometry patterns epithelial-mesenchymal transition via intercellular mechanotransduction. J Cell Biochem 110(1):44–51PubMedPubMedCentralGoogle Scholar
  125. 125.
    Zanetti D, Llenbach R, Plodinec M, Oertle P, Redling K et al (2018) Length scale matters: real-time elastography versus nanomechanical profiling by atomic force microscopy for the diagnosis of breast lesions. Biomed Res Int 2018:12Google Scholar
  126. 126.
    Lopez JI, Kang I, You WK, McDonald DM, Weaver VM (2011) In situ force mapping of mammary gland transformation. Integr Biol 3(9):910–921CrossRefGoogle Scholar
  127. 127.
    Affo S, Yu LX, Schwabe RF (2017) The role of cancer-associated fibroblasts and fibrosis in liver cancer. Annu Rev Pathol 12:153–186CrossRefPubMedPubMedCentralGoogle Scholar
  128. 128.
    Panera N, Crudele A, Romito I, Gnani D, Alisi A (2017) Focal adhesion kinase: insight into molecular roles and functions in hepatocellular carcinoma. Int J Mol Sci 18(1):99CrossRefGoogle Scholar
  129. 129.
    Celià-Terrassa T, Kang Y (2016) Distinctive properties of metastasis-initiating cells. Genes Dev 30(8):892–908CrossRefPubMedPubMedCentralGoogle Scholar
  130. 130.
    Valastyan S, Weinberg RA (2011) Tumor metastasis: molecular insights and evolving paradigms. Cell 147(2):275–292CrossRefPubMedPubMedCentralGoogle Scholar
  131. 131.
    Cooper J, Giancotti FG (2019) Integrin signaling in cancer: mechanotransduction, stemness, epithelial plasticity, and therapeutic resistance. Cancer Cell 35(3):347–367CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2020

Authors and Affiliations

  1. 1.Atta Ur Rahman School of Applied Biosciences, NUSTIslamabadPakistan
  2. 2.Pakistan Institute of Medical SciencesIslamabadPakistan
  3. 3.Department of Industrial BiotechnologyAtta Ur Rahman School of Applied Biosciences, NUSTIslamabadPakistan
  4. 4.Department of Healthcare BiotechnologyAtta Ur Rahman School of Applied Biosciences, NUSTIslamabadPakistan

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