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Progenitor Cell Mobilization from Extramedullary Organs

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Stem Cell Mobilization

Part of the book series: Methods in Molecular Biology ((MIMB,volume 904))

Abstract

The course of various pathological conditions relies on the mobilization of stem cells and partially differentiated progenitor cells. Bone marrow transplantation studies have demonstrated that medullary hematopoietic and endothelial progenitors can undergo mobilization and trafficking. While the ability of the bone marrow to boost its resources in fighting disease or repairing injury declines with age, other organs have surfaced as reservoirs of various progenitor cell populations. This chapter discusses our current understanding of non-bone marrow-derived progenitor pools, focusing on mesenchymal stem cells. The evidence for the extramedullary progenitor mobilization, with a specific emphasis on white adipose tissue, is presented.

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References

  1. Laird DJ, von Andrian UH, Wagers AJ (2008) Stem cell trafficking in tissue development, growth, and disease. Cell 132:612–630

    Article  PubMed  CAS  Google Scholar 

  2. Kolonin MG, Simmons PJ (2009) Combi­natorial stem cell mobilization. Nat Biotechnol 27:252–253

    Article  PubMed  CAS  Google Scholar 

  3. Papayannopoulou T, Scadden DT (2008) Stem-cell ecology and stem cells in motion. Blood 111:3923–3930

    Article  PubMed  CAS  Google Scholar 

  4. Pelus LM (2008) Peripheral blood stem cell mobilization: new regimens, new cells, where do we stand. Curr Opin Hematol 15:285–292

    Article  PubMed  Google Scholar 

  5. Cottler-Fox MH, Lapidot T, Petit I, Kollet O, DiPersio JF, Link D, Devine S (2003) Stem cell mobilization. Hematology Am Soc Hematol Educ Program 419–437

    Google Scholar 

  6. Levesque JP, Winkler IG (2008) Mobilization of hematopoietic stem cells: state of the art. Curr Opin Organ Transplant 13:53–58

    Article  PubMed  Google Scholar 

  7. 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 14:263–273

    Article  PubMed  CAS  Google Scholar 

  8. Mancuso P, Antoniotti P, Quarna J, Calleri A, Rabascio C, Tacchetti C, Braidotti P, Wu HK, Zurita AJ, Saronni L, Cheng JB, Shalinsky DR, Heymach JV, Bertolini F (2009) Validation of a standardized method for enumerating circulating endothelial cells and progenitors: flow cytometry and molecular and ultrastructural analyses. Clin Cancer Res 15:267–273

    Article  PubMed  CAS  Google Scholar 

  9. Pitchford SC, Furze RC, Jones CP, Wengner AM, Rankin SM (2009) Differential mobilization of subsets of progenitor cells from the bone marrow. Cell Stem Cell 4:62–72

    Article  PubMed  CAS  Google Scholar 

  10. Hall B, Dembinski J, Sasser AK, Studeny M, Andreeff M, Marini F (2007) Mesenchymal stem cells in cancer: tumor-associated fibroblasts and cell-based delivery vehicles. Int J Hematol 86:8–16

    Article  PubMed  CAS  Google Scholar 

  11. Mancuso P, Martin-Padura I, Calleri A, Marighetti P, Quarna J, Rabascio C, Braidotti P, Bertolini F (2011) Circulating perivascular progenitors: a target of PDGFR inhibition. Int J Cancer 129:1344–1350

    Article  PubMed  CAS  Google Scholar 

  12. Bellows CF, Zhang Y, Chen J, Frazier ML, Kolonin MG (2011) Circulation of progenitor cells in obese and lean colorectal cancer patients. Cancer Epidemiol Biomarkers Prev 20:2461–2468

    Article  PubMed  CAS  Google Scholar 

  13. Pilling D, Fan T, Huang D, Kaul B, Gomer RH (2009) Identification of markers that distinguish monocyte-derived fibrocytes from monocytes, macrophages, and fibroblasts. PLoS One 4:e7475

    Article  PubMed  Google Scholar 

  14. Kucia M, Reca R, Campbell FR, Zuba-Surma E, Majka M, Ratajczak J, Ratajczak MZ (2006) A population of very small embryonic-like (VSEL) CXCR4(+)SSEA-1(+)Oct-4+ stem cells identified in adult bone marrow. Leukemia 20:857–869

    Article  PubMed  CAS  Google Scholar 

  15. Tilki D, Hohn HP, Ergun B, Rafii S, Ergun S (2009) Emerging biology of vascular wall progenitor cells in health and disease. Trends Mol Med 15:501–509

    Article  PubMed  CAS  Google Scholar 

  16. Kopp HG, Ramos CA, Rafii S (2006) Contribution of endothelial progenitors and proangiogenic hematopoietic cells to vascularization of tumor and ischemic tissue. Curr Opin Hematol 13:175–181

    Article  PubMed  CAS  Google Scholar 

  17. Du R, Lu KV, Petritsch C, Liu P, Ganss R, Passegue E, Song H, Vandenberg S, Johnson RS, Werb Z, Bergers G (2008) HIF1alpha induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion. Cancer Cell 13:206–220

    Article  PubMed  CAS  Google Scholar 

  18. Minana MD, Carbonell-Uberos F, Mirabet V, Marin S, Encabo A (2008) Identification of hemangioblasts in the adult human adipose ­tissue. Stem Cells 26:2696–2704

    Article  PubMed  Google Scholar 

  19. Han J, Koh YJ, Moon HR, Ryoo HG, Cho CH, Kim I, Koh GY (2010) Adipose tissue is an extramedullary reservoir for functional hematopoietic stem and progenitor cells. Blood 115:957–964

    Article  PubMed  CAS  Google Scholar 

  20. Cristofanilli M, Budd GT, Ellis MJ, Stopeck A, Matera J, Miller MC, Reuben JM, Doyle GV, Allard WJ, Terstappen LW, Hayes DF (2004) Circulating tumor cells, disease progression, and survival in metastatic breast cancer. N Engl J Med 351:781–791

    Article  PubMed  CAS  Google Scholar 

  21. Paterlini-Brechot P, Benali NL (2007) Circulating tumor cells (CTC) detection: clinical impact and future directions. Cancer Lett 253:180–204

    Article  PubMed  CAS  Google Scholar 

  22. Jin SW, Patterson C (2009) The opening act: vasculogenesis and the origins of circulation. Arterioscler Thromb Vasc Biol 29:623–629

    Article  PubMed  CAS  Google Scholar 

  23. Shaked Y, Ciarrocchi A, Franco M, Lee CR, Man S, Cheung AM, Hicklin DJ, Chaplin D, Foster FS, Benezra R, Kerbel RS (2006) Therapy-induced acute recruitment of ­circulating endothelial progenitor cells to tumors. Science 313:1785–1787

    Article  PubMed  CAS  Google Scholar 

  24. Lyden D, Hattori K, Dias S, Costa C, Blaikie P, Butros L, Chadburn A, Heissig B, Marks W, Witte L, Wu Y, Hicklin D, Zhu Z, Hackett NR, Crystal RG, Moore MA, Hajjar KA, Manova K, Benezra R, Rafii S (2001) Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nat Med 7:1194–1201

    Article  PubMed  CAS  Google Scholar 

  25. Peters BA, Diaz LA, Polyak K, Meszler L, Romans K, Guinan EC, Antin JH, Myerson D, Hamilton SR, Vogelstein B, Kinzler KW, Lengauer C (2005) Contribution of bone marrow-derived endothelial cells to human tumor vasculature. Nat Med 11:261–262

    Article  PubMed  CAS  Google Scholar 

  26. Kaplan RN, Riba RD, Zacharoulis S, Bramley AH, Vincent L, Costa C, MacDonald DD, Jin DK, Shido K, Kerns SA, Zhu Z, Hicklin D, Wu Y, Port JL, Altorki N, Port ER, Ruggero D, Shmelkov SV, Jensen KK, Rafii S, Lyden D (2005) VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 438:820–827

    Article  PubMed  CAS  Google Scholar 

  27. Purhonen S, Palm J, Rossi D, Kaskenpaa N, Rajantie I, Yla-Herttuala S, Alitalo K, Weissman IL, Salven P (2008) Bone marrow-derived circulating endothelial precursors do not contribute to vascular endothelium and are not needed for tumor growth. Proc Natl Acad Sci USA 105:6620–6625

    Article  PubMed  CAS  Google Scholar 

  28. Kim SJ, Kim JS, Papadopoulos J, Wook Kim S, Maya M, Zhang F, He J, Fan D, Langley R, Fidler IJ (2009) Circulating monocytes expressing CD31: implications for acute and chronic angiogenesis. Am J Pathol 174:1972–1980

    Article  PubMed  CAS  Google Scholar 

  29. Alessandri G, Girelli M, Taccagni G, Colombo A, Nicosia R, Caruso A, Baronio M, Pagano S, Cova L, Parati E (2001) Human vasculogenesis ex vivo: embryonal aorta as a tool for isolation of endothelial cell progenitors. Lab Invest 81:875–885

    Article  PubMed  CAS  Google Scholar 

  30. Ingram DA, Mead LE, Moore DB, Woodard W, Fenoglio A, Yoder MC (2005) Vessel ­wall-derived endothelial cells rapidly proliferate because they contain a complete hierarchy of endothelial progenitor cells. Blood 105:2783–2786

    Article  PubMed  CAS  Google Scholar 

  31. Zengin E, Chalajour F, Gehling UM, Ito WD, Treede H, Lauke H, Weil J, Reichenspurner H, Kilic N, Ergun S (2006) Vascular wall resident progenitor cells: a source for postnatal vasculogenesis. Development 133:1543–1551

    Article  PubMed  CAS  Google Scholar 

  32. Aicher A, Rentsch M, Sasaki K, Ellwart JW, Fandrich F, Siebert R, Cooke JP, Dimmeler S, Heeschen C (2007) Nonbone marrow-derived circulating progenitor cells contribute to postnatal neovascularization following tissue ischemia. Circ Res 100:581–589

    Article  PubMed  CAS  Google Scholar 

  33. da Silva Meirelles L, Chagastelles PC, Nardi NB (2006) Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J Cell Sci 119:2204–2213

    Article  PubMed  Google Scholar 

  34. Bianco P, Robey PG, Simmons PJ (2008) Mesenchymal stem cells: revisiting history, concepts, and assays. Cell Stem Cell 2:313–319

    Article  PubMed  CAS  Google Scholar 

  35. Bissell MJ, Radisky D (2001) Putting tumours in context. Nat Rev Cancer 1:46–54

    Article  PubMed  CAS  Google Scholar 

  36. Wels J, Kaplan RN, Rafii S, Lyden D (2008) Migratory neighbors and distant invaders: tumor-associated niche cells. Genes Dev 22:559–574

    Article  PubMed  CAS  Google Scholar 

  37. Mishra PJ, Mishra PJ, Glod JW, Banerjee D (2009) Mesenchymal stem cells: flip side of the coin. Cancer Res 69:1255–1258

    Article  PubMed  CAS  Google Scholar 

  38. Zhang Y, Daquinag A, Traktuev DO, Amaya F, Simmons PJ, March KL, Pasqualini R, Arap W, Kolonin MG (2009) White adipose tissue cells are recruited by experimental tumors and promote cancer progression in mouse models. Cancer Res 69:5259–5266

    Article  PubMed  CAS  Google Scholar 

  39. Campagnolo P, Cesselli D, Al Haj Zen A, Beltrami AP, Krankel N, Katare R, Angelini G, Emanueli C, Madeddu P (2010) Human adult vena saphena contains perivascular progenitor cells endowed with clonogenic and proangiogenic potential. Circulation 121:1735–1745

    Article  PubMed  Google Scholar 

  40. Hausman DB, DiGirolamo M, Bartness TJ, Hausman GJ, Martin RJ (2001) The biology of white adipocyte proliferation. Obes Rev 2:239–254

    Article  PubMed  CAS  Google Scholar 

  41. Crandall DL, Hausman GJ, Kral JG (1997) A review of the microcirculation of adipose tissue: anatomic, metabolic, and angiogenic perspectives. Microcirculation 4:211–232

    Article  PubMed  CAS  Google Scholar 

  42. Hausman GJ, Richardson RL (2004) Adipose tissue angiogenesis. J Anim Sci 82:925–934

    PubMed  CAS  Google Scholar 

  43. Kolonin MG, Saha PK, Chan L, Pasqualini R, Arap W (2004) Reversal of obesity by targeted ablation of adipose tissue. Nat Med 10:625–632

    Article  PubMed  CAS  Google Scholar 

  44. Rodeheffer MS, Birsoy K, Friedman JM (2008) Identification of white adipocyte progenitor cells in vivo. Cell 135:240–249

    Article  PubMed  CAS  Google Scholar 

  45. Gimble JM, Katz AJ, Bunnell BA (2007) Adipose-derived stem cells for regenerative medicine. Circ Res 100:1249–1260

    Article  PubMed  CAS  Google Scholar 

  46. Traktuev D, Merfeld-Clauss S, Li J, Kolonin M, Arap W, Pasqualini R, Johnstone BH, March KL (2008) A population of multipotent CD34-positive adipose stromal cells share ­pericyte and mesenchymal surface markers, reside in a periendothelial location, and stabilize endothelial networks. Circ Res 102:77–85

    Article  PubMed  CAS  Google Scholar 

  47. Tang W, Zeve D, Suh JM, Bosnakovski D, Kyba M, Hammer RE, Tallquist MD, Graff JM (2008) White fat progenitor cells reside in the adipose vasculature. Science 322:583–586

    Article  PubMed  CAS  Google Scholar 

  48. Cai L, Johnstone BH, Cook TG, Tan J, Fishbein MC, Chen PS, March KL (2009) Human adipose tissue-derived stem cells induce angiogenesis and nerve sprouting following myocardial infarction, in conjunction with potent preservation of cardiac function. Stem Cells 27:230–237

    Article  PubMed  CAS  Google Scholar 

  49. Abe R, Donnelly SC, Peng T, Bucala R, Metz CN (2001) Peripheral blood fibrocytes: differentiation pathway and migration to wound sites. J Immunol 166:7556–75562

    PubMed  CAS  Google Scholar 

  50. Hartlapp I, Abe R, Saeed RW, Peng T, Voelter W, Bucala R, Metz CN (2001) Fibrocytes induce an angiogenic phenotype in cultured endothelial cells and promote angiogenesis in vivo. FASEB J 15:2215–2224

    Article  PubMed  CAS  Google Scholar 

  51. Bellows CF, Zhang Y, Simmons PJ, Khalsa AS, Kolonin MG (2011) Influence of BMI on level of circulating progenitor cells. Obesity 19:1722–1726

    Article  PubMed  Google Scholar 

  52. Mullen JT, Moorman DW, Davenport DL (2009) The obesity paradox: body mass index and outcomes in patients undergoing nonbariatric general surgery. Ann Surg 250:166–172

    Article  PubMed  Google Scholar 

  53. Daquinag AC, Zhang Y, Amaya-Manzanares F, Simmons PJ, Kolonin MG (2011) An isoform of decorin is a resistin receptor on the surface of adipose progenitor cells. Cell Stem Cell 9:74–86

    Article  PubMed  CAS  Google Scholar 

  54. Groenewegen HC, Onuta G, Goris M, Zandvoort A, Zijlstra F, van Gilst WH, Rozing J, de Smet BJ, Roks AJ, Hillebrands JL (2008) Non-bone marrow origin of neointimal smooth muscle cells in experimental in-stent restenosis in rats. J Vasc Res 45:493–502

    Article  PubMed  Google Scholar 

  55. Goon PK, Lip GY, Boos CJ, Stonelake PS, Blann AD (2006) Circulating endothelial cells, endothelial progenitor cells, and endothelial microparticles in cancer. Neoplasia 8:79–88

    Article  PubMed  CAS  Google Scholar 

  56. McDonald DM, Foss AJ (2000) Endothelial cells of tumor vessels: abnormal but not absent. Cancer Metastasis Rev 19:109–120

    Article  PubMed  CAS  Google Scholar 

  57. Bertolini F, Shaked Y, Mancuso P, Kerbel RS (2006) The multifaceted circulating endothelial cell in cancer: towards marker and target identification. Nat Rev Cancer 6:835–845

    Article  PubMed  CAS  Google Scholar 

  58. Conejo-Garcia JR, Benencia F, Courreges MC, Kang E, Mohamed-Hadley A, Buckanovich RJ, Holtz DO, Jenkins A, Na H, Zhang L, Wagner DS, Katsaros D, Caroll R, Coukos G (2004) Tumor-infiltrating dendritic cell precursors recruited by a beta-defensin contribute to vasculogenesis under the influence of Vegf-A. Nat Med 10:950–958

    Article  PubMed  CAS  Google Scholar 

  59. De Palma M, Venneri MA, Galli R, Sergi Sergi L, Politi LS, Sampaolesi M, Naldini L (2005) Tie2 identifies a hematopoietic lineage of proangiogenic monocytes required for tumor vessel formation and a mesenchymal population of pericyte progenitors. Cancer Cell 8:211–226

    Article  PubMed  Google Scholar 

  60. Grunewald M, Avraham I, Dor Y, Bachar-Lustig E, Itin A, Jung S, Chimenti S, Landsman L, Abramovitch R, Keshet E (2006) VEGF-induced adult neovascularization: recruitment, retention, and role of accessory cells. Cell 124:175–189

    Article  PubMed  CAS  Google Scholar 

  61. Lumeng CN, Bodzin JL, Saltiel AR (2007) Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest 117:175–184

    Article  PubMed  CAS  Google Scholar 

  62. Kerkis I, Kerkis A, Dozortsev D, Stukart-Parsons GC, Gomes Massironi SM, Pereira LV, Caplan AI, Cerruti HF (2006) Isolation and characterization of a population of immature dental pulp stem cells expressing OCT-4 and other embryonic stem cell markers. Cells Tissues Organs 184:105–116

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

Supported by Komen for the Cure (KG080782), American Heart Association (0835434N), Cancer Prevention and Research Institute of Texas (RP100400), NIH Prostate SPORE (CA140388) and American Cancer Society (CNE-119003) awards to MGK.

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Authors and Affiliations

  1. Institute of Molecular Medicine, University of Texas Health Science Center at Houston, Houston, TX, USA

    Mikhail G. Kolonin

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  1. Mikhail G. Kolonin
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Correspondence to Mikhail G. Kolonin .

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  1. Science Center at Houston, Inst. Molecular Medicine, University of Texas, Pressler Street 1825, Houston, 77030, Texas, USA

    Mikhail G. Kolonin

  2. Health Science Center, Houston, Inst. Molecular Medicine, University of Texas, Pressler Street 1825, Houston, 77030, Texas, USA

    Paul J. Simmons

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Kolonin, M.G. (2012). Progenitor Cell Mobilization from Extramedullary Organs. In: Kolonin, M., Simmons, P. (eds) Stem Cell Mobilization. Methods in Molecular Biology, vol 904. Humana Press, Totowa, NJ. https://doi.org/10.1007/978-1-61779-943-3_20

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  • DOI: https://doi.org/10.1007/978-1-61779-943-3_20

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  • Publisher Name: Humana Press, Totowa, NJ

  • Print ISBN: 978-1-61779-942-6

  • Online ISBN: 978-1-61779-943-3

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