Identification and characterization of a resident vascular stem/progenitor cell population in preexisting blood vessels

EMBO Journal

Volumn 31, Issue 4, 2012, Pages 842-855

  Naito, Hisamichi ^a   Kidoya, Hiroyasu ^a   Sakimoto, Susumu ^a   Wakabayashi, Taku ^a   Takakura, Nobuyuki ^a,b  

^a OSAKA UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

angiogenesis; endothelium; side population; somatic stem cell

Indexed keywords

CELL SURFACE MARKER; HOE 33342;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD FLOW; BLOOD VESSEL; CAPILLARY ENDOTHELIUM; CELL HETEROGENEITY; CELL POPULATION; CELLULAR DISTRIBUTION; COLONY FORMING UNIT; CONTROLLED STUDY; DORMANCY; ENDOTHELIAL PROGENITOR CELL; GENE EXPRESSION PROFILING; LIMB ISCHEMIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; STEM CELL TRANSPLANTATION;

ANIMALS; BLOOD VESSELS; ENDOTHELIUM, VASCULAR; GENE EXPRESSION PROFILING; HUMANS; INFANT, NEWBORN; MICE; NEOVASCULARIZATION, PATHOLOGIC; STEM CELLS;

EID: 84857040086     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2011.465     Document Type: Article

References (48)

1. Arai F, Hirao A, Ohmura M, Sato H, Matsuoka S, Takubo K, Ito K, Koh GY, Suda T (2004) Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell 118: 149-161 (Pubitemid 38962572)
2. Asahara T, Murohara T, Sullivan A, Silver M, Van der Zee R, Li T, Witzenbichler B, Schatteman G, Isner JM (1997) Isolation of putative progenitor endothelial cells for angiogenesis. Science 275: 964-967 (Pubitemid 27087709)
3. Asahara T, Takahashi T, Masuda H, Kalka C, Chen D, Iwaguro H, Inai Y, Silver M, Isner JM (1999) VEGF contributes to postnatal neovascularization by mobilizing bone marrow-derived endothelial progenitor cells. EMBO J 18: 3964-3972 (Pubitemid 29335849)
4. Boisset JC, van Cappellen W, Andrieu-Soler C, Galjart N, Dzierzak E, Robin C (2010) In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium. Nature 464: 116-120
5. Bruscia EM, Ziegler EC, Price JE, Weiner S, Egan ME, Krause DS (2006) Engraftment of donor-derived epithelial cells in multiple organs following bone marrow transplantation into newborn mice. Stem Cells 24: 2299-2308 (Pubitemid 44527484)
6. Bunting KD, Zhou S, Lu T, Sorrentino BP (2000) Enforced Pglycoprotein pump function in murine bone marrow cells results in expansion of side population stem cells in vitro and repopulating cells in vivo. Blood 96: 902-909 (Pubitemid 30616854)
7. Cao G, Savani RC, Fehrenbach M, Lyons C, Zhang L, Coukos G, Delisser HM (2006) Involvement of endothelial CD44 during in vivo angiogenesis. Am J Pathol 169: 325-336
8. Challen GA, Little MH (2006) A side order of stem cells: the SP phenotype. Stem Cells 24: 3-12
9. Choi K, Kennedy M, Kazarov A, Papadimitriou JC, Keller G (1998) A common precursor for hematopoietic and endothelial cells. Development 125: 725-732 (Pubitemid 28108096)
10. Cotsarelis G, Sun TT, Lavker RM (1990) Label-retaining cells reside in the bulge area of pilosebaceous unit: implications for follicular stem cells, hair cycle, and skin carcinogenesis. Cell 61: 1329-1337
11. De Bock K, De Smet F, Leite De Oliveira R, Anthonis K, Carmeliet P (2009) Endothelial oxygen sensors regulate tumor vessel abnormalization by instructing phalanx endothelial cells. J Mol Med 87: 561-569
12. Feinberg RN, Beebe DC (1983) Hyaluronate in vasculogenesis. Science 220: 1177-1179 (Pubitemid 13097206)
13. Gerhardt H, Golding M, Fruttiger M, Ruhrberg C, Lundkvist A, Abramsson A, Jeltsch M, Mitchell C, Alitalo K, Shima D, Betsholtz C (2003) VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol 161: 1163-1177 (Pubitemid 36870177)
14. Golebiewska A, Brons NH, Bjerkvig R, Niclou SP (2011) Critical appraisal of the side population assay in stem cell and cancer stem cell research. Cell Stem Cell 8: 136-147
15. Goodell MA, Brose K, Paradis G, Conner AS, Mulligan RC (1996) Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med 183: 1797-1806 (Pubitemid 26134320)
16. Gothert JR, Gustin SE, van Eekelen JA, Schmidt U, Hall MA, Jane SM, Green AR, Gottgens B, Izon DJ, Begley CG (2004) Genetically tagging endothelial cells in vivo: bone marrow-derived cells do not contribute to tumor endothelium. Blood 104: 1769-1777 (Pubitemid 39202286)
17. Gothot A, Pyatt R, McMahel J, Rice S, Srour EF (1997) Functional heterogeneity of human CD34(+) cells isolated in subcompartments of the G0/G1 phase of the cell cycle. Blood 90: 4384-4393 (Pubitemid 27508444)
18. Hooper AT, Butler JM, Nolan DJ, Kranz A, Iida K, Kobayashi M, Kopp HG, Shido K, Petit I, Yanger K, James D, Witte L, Zhu Z, Wu Y, Pytowski B, Rosenwaks Z, Mittal V, Sato TN, Rafii S (2009) Engraftment and reconstitution of hematopoiesis is dependent on VEGFR2-mediated regeneration of sinusoidal endothelial cells. Cell Stem Cell 4: 263-274
19. Hou Z, Bailey JP, Vomachka AJ, Matsuda M, Lockefeer JA, Horseman ND (2000) Glycosylation-dependent cell adhesion molecule 1 (GlyCAM 1) is induced by prolactin and suppressed by progesterone in mammary epithelium. Endocrinology 141: 4278-4283
20. Hu Y, Zhang Z, Torsney E, Afzal AR, Davison F, Metzler B, Xu Q (2004) Abundant progenitor cells in the adventitia contribute to atherosclerosis of vein grafts in ApoE-deficient mice. J Clin Invest 113: 1258-1265 (Pubitemid 39069924)
21. Kalabis J, Oyama K, Okawa T, Nakagawa H, Michaylira CZ, Stairs DB, Figueiredo JL, Mahmood U, Diehl JA, Herlyn M, Rustgi AK (2008) A subpopulation of mouse esophageal basal cells has properties of stem cells with the capacity for selfrenewal and lineage specification. J Clin Invest 118: 3860-3869
22. Kidoya H, Naito H, Takakura N (2010) Apelin induces enlarged and nonleaky blood vessels for functional recovery from ischaemia. Blood 115: 3166-3174
23. Mahmoud M, Allinson KR, Zhai Z, Oakenfull R, Ghandi P, Adams RH, Fruttiger M, Arthur HM (2010) Pathogenesis of arteriovenous malformations in the absence of endoglin. Circ Res 106: 1425-1433
24. Mazzone M, Dettori D, Leite de Oliveira R, Loges S, Schmidt T, Jonckx B, Tian YM, Lanahan AA, Pollard P, Ruiz de Almodovar C, De Smet F, Vinckier S, Aragones J, Debackere K, Luttun A, Wyns S, Jordan B, Pisacane A, Gallez B, Lampugnani MG et al (2009) Heterozygous deficiency of PHD2 restores tumor oxygenation and inhibits metastasis via endothelial normalization. Cell 136: 839-851
25. Medici D, Shore EM, Lounev VY, Kaplan FS, Kalluri R, Olsen BR (2010) Conversion of vascular endothelial cells into multipotent stem-like cells. Nat Med 16: 1400-1406
26. Miller DS (2010) Regulation of P-glycoprotein and other ABC drug transporters at the blood-brain barrier. Trends Pharmacol Sci 31: 246-254
27. Mizrak D, Brittan M, Alison MR (2008) CD133: molecule of the moment. J Pathol 214: 3-9
28. Morita Y, Ema H, Yamazaki S, Nakauchi H (2006) Non-side-population hematopoietic stem cells in mouse bone marrow. Blood 108: 2850-2856
29. Nagahama Y, Ueno M, Miyamoto S, Morii E, Minami T, Mochizuki N, Saya H, Takakura N (2010) PSF1, a DNA replication factor expressed widely in stem and progenitor cells, drives tumorigenic and metastatic properties. Cancer Res 70: 1215-1224
30. Nishikawa SI, Nishikawa S, Kawamoto H, Yoshida H, Kizumoto M, Kataoka H, Katsura Y (1998) In vitro generation of lymphohematopoietic cells from endothelial cells purified from murine embryos. Immunity 8: 761-769 (Pubitemid 28294523)
31. Nolan DJ, Ciarrocchi A, Mellick AS, Jaggi JS, Bambino K, Gupta S, Heikamp E, McDevitt MR, Scheinberg DA, Benezra R, Mittal V (2007) Bone marrow-derived endothelial progenitor cells are a major determinant of nascent tumor neovascularization. Genes Dev 21: 1546-1558 (Pubitemid 46955726)
32. Okuno Y, Nakamura-Ishizu A, Kishi K, Suda T, Kubota Y (2011) Bone marrow-derived cells serve as proangiogenic macrophages but not endothelial cells in wound healing. Blood 117: 5264-5272
33. Onrust SV, Hartl PM, Rosen SD, Hanahan D (1996) Modulation of L-selectin ligand expression during an immune response accompanying tumorigenesis in transgenic mice. J Clin Invest 97: 54-64 (Pubitemid 26021694)
34. Osawa M, Hanada K, Hamada H, Nakauchi H (1996) Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science 273: 242-245 (Pubitemid 26285891)
35. Passman JN, Dong XR, Wu SP, Maguire CT, Hogan KA, Bautch VL, Majesky MW (2008) A sonic hedgehog signaling domain in the arterial adventitia supports resident Sca1+ smooth muscle progenitor cells. Proc Natl Acad Sci USA 105: 9349-9354
36. 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 (Pubitemid 40460552)
37. 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 (Pubitemid 351754556)
38. Risau W (1995) Differentiation of endothelium. FASEB J 9: 926-933
39. Risau W (1997) Mechanisms of angiogenesis. Nature 386: 671-674 (Pubitemid 27193480)
40. Sainz J, Al Haj Zen A, Caligiuri G, Demerens C, Urbain D, Lemitre M, Lafont A (2006) Isolation of 'side population' progenitor cells from healthy arteries of adult mice. Arterioscler Thromb Vasc Biol 26: 281-286 (Pubitemid 43732188)
41. Shantsila E, Watson T, Lip GY (2007) Endothelial progenitor cells in cardiovascular disorders. J Am Coll Cardiol 49: 741-752
42. Summers YJ, Heyworth CM, de Wynter EA, Hart CA, Chang J, Testa NG (2004) AC133+ G0 cells from cord blood show a high incidence of long-term culture-initiating cells and a capacity for more than 100 million-fold amplification of colony-forming cells in vitro. Stem Cells 22: 704-715 (Pubitemid 39166928)
43. Takahashi T, Kalka C, Masuda H, Chen D, Silver M, Kearney M, Magner M, Isner JM, Asahara T (1999) Ischemia-and cytokineinduced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat Med 5: 434-438 (Pubitemid 29180584)
44. Takakura N, Huang XL, Naruse T, Hamaguchi I, Dumont DJ, Yancopoulos GD, Suda T (1998) Critical role of the TIE2 endothelial cell receptor in the development of definitive hematopoiesis. Immunity 9: 677-686 (Pubitemid 28557596)
45. Takakura N, Watanabe T, Suenobu S, Yamada Y, Noda T, Ito Y, Satake M, Suda T (2000) A role for hematopoietic stem cells in promoting angiogenesis. Cell 102: 199-209
46. Walter DH, Haendeler J, Reinhold J, Rochwalsky U, Seeger F, Honold J, Hoffmann J, Urbich C, Lehmann R, Arenzana-Seisdesdos F, Aicher A, Heeschen C, Fichtlscherer S, Zeiher AM, Dimmeler S (2005) Impaired CXCR4 signaling contributes to the reduced neovascularization capacity of endothelial progenitor cells from patients with coronary artery disease. Circ Res 97: 1142-1151
47. 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 (Pubitemid 43732967)
48. Zhang XQ, Takakura N, Oike Y, Inada T, Gale NW, Yancopoulos GD, Suda T (2001) Stromal cells expressing ephrin-B2 promote the growth and sprouting of ephrin-B2(+) endothelial cells. Blood 98: 1028-1037