Isolation and function of mouse tissue resident vascular precursors marked by myelin protein zero

Journal of Experimental Medicine

Volumn 208, Issue 5, 2011, Pages 949-960

  Kubota, Yoshiaki ^a   Takubo, Keiyo ^a   Hirashima, Masanori ^b   Nagoshi, Narihito ^a   Kishi, Kazuo ^a   Okuno, Yuji ^a   Nakamura Ishizu, Ayako ^a   Sano, Keigo ^b   Murakami, Masato ^c   Ema, Masatsugu ^d   Omatsu, Yoshiki ^e   Takahashi, Satoru ^d   Nagasawa, Takashi ^e   Shibuya, Masabumi ^c   Okano, Hideyuki ^a   Suda, Toshio ^a  

^a KEIO UNIVERSITY   (Japan)

^b KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^d UNIVERSITY OF TSUKUBA   (Japan)

^e KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CD31 ANTIGEN; CD45 ANTIGEN; CHEMOKINE RECEPTOR CXCR4; MYELIN; MYELIN PROTEIN ZERO; NOTCH RECEPTOR; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL EXPANSION; CELL FUNCTION; CELL ISOLATION; CELL POPULATION; CELL SURFACE; CONTROLLED STUDY; ENDOTHELIUM CELL; HEMANGIOBLAST; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA; SCHWANN CELL; SIGNAL TRANSDUCTION; SPINDLE CELL; STEM CELL; VASCULAR PRECURSOR CELL; VASCULARIZATION;

ANIMALS; ANTIGENS, DIFFERENTIATION; CELL LINE, TUMOR; CHEMOKINE CXCL12; ENDOTHELIAL CELLS; MICE; MICE, TRANSGENIC; MYELIN P0 PROTEIN; NEOVASCULARIZATION, PHYSIOLOGIC; RECEPTORS, CXCR4; RECEPTORS, NOTCH; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; RETINA; STEM CELLS; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 79956101403     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20102187     Document Type: Article

References (50)

1. Albuquerque, R.J., T. Hayashi, W.G. Cho, M.E. Kleinman, S. Dridi, A. Takeda, J.Z. Baffi, K. Yamada, H. Kaneko, M.G. Green, et al. 2009. Alternatively spliced vascular endothelial growth factor receptor-2 is an essential endogenous inhibitor of lymphatic vessel growth. Nat. Med. 15:1023-1030.
2. Asahara, T., T. Murohara, A. Sullivan, M. Silver, R. van der Zee, T. Li, B. Witzenbichler, G. Schatteman, and J.M. Isner. 1997. Isolation of putative progenitor endothelial cells for angiogenesis. Science. 275:964-967.
3. Ashton, N. 1970. Retinal angiogenesis in the human embryo. Br. Med. Bull. 26:103-106.
4. Beltrami, A.P., L. Barlucchi, D. Torella, M. Baker, F. Limana, S. Chimenti, H. Kasahara, M. Rota, E. Musso, K. Urbanek, et al. 2003. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell. 114:763-776
5. Carmeliet, P. 2003. Angiogenesis in health and disease. Nat. Med. 9:653-660.
6. Ceradini, D.J., A.R. Kulkarni, M.J. Callaghan, O.M. Tepper, N. Bastidas, M.E. Kleinman, J.M. Capla, R.D. Galiano, J.P. Levine, and G.C. Gurtner. 2004. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat. Med. 10:858-864.
7. Danielian, P.S., D. Muccino, D.H. Rowitch, S.K. Michael, and A.P. McMahon. 1998. Modification of gene activity in mouse embryos in utero by a tamoxifen-inducible form of Cre recombinase. Curr. Biol. 8:1323-1326.
8. Ema, M., T. Yokomizo, A. Wakamatsu, T. Terunuma, M. Yamamoto, and S. Takahashi. 2006. Primitive erythropoiesis from mesodermal precursors expressing VE-cadherin, PECAM-1, Tie2, endoglin, and CD34 in the mouse embryo. Blood. 108:4018-4024
9. Etchevers, H.C., C. Vincent, N.M. Le Douarin, and G.F. Couly. 2001. The cephalic neural crest provides pericytes and smooth muscle cells to all blood vessels of the face and forebrain. Development. 128:1059-1068.
10. Fruttiger, M. 2002. Development of the mouse retinal vasculature: angiogenesis versus vasculogenesis. Invest. Ophthalmol. Vis. Sci. 43:522-527.
11. Gage, P.J., W. Rhoades, S.K. Prucka, and T. Hjalt. 2005. Fate maps of neural crest and mesoderm in the mammalian eye. Invest. Ophthalmol. Vis. Sci. 46:4200-4208.
12. Gao, D., D.J. Nolan, A.S. Mellick, K. Bambino, K. McDonnell, and V. Mittal. 2008. Endothelial progenitor cells control the angiogenic switch in mouse lung metastasis. Science. 319:195-198.
13. Gariano, R.F., and T.W. Gardner. 2005. Retinal angiogenesis in development and disease. Nature. 438:960-966.
14. Gerhardt, H., M. Golding, M. Fruttiger, C. Ruhrberg, A. Lundkvist, A. Abramsson, M. Jeltsch, C. Mitchell, K. Alitalo, D. Shima, and C. Betsholtz. 2003. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J. Cell Biol. 161:1163-1177.
15. Giese, K.P., R. Martini, G. Lemke, P. Soriano, and M. Schachner. 1992. Mouse P0 gene disruption leads to hypomyelination, abnormal expression of recognition molecules, and degeneration of myelin and axons. Cell. 71:565-576.
16. Grenier, G., A. Scimè, F. Le Grand, A. Asakura, C. Perez-Iratxeta, M.A. Andrade-Navarro, P.A. Labosky, and M.A. Rudnicki. 2007. Resident endothelial precursors in muscle, adipose, and dermis contribute to postnatal vasculogenesis. Stem Cells. 25:3101-3110.
17. Guo, Y., B. Graham-Evans, and H.E. Broxmeyer. 2006. Murine embryonic stem cells secrete cytokines/growth modulators that enhance cell survival/anti-apoptosis and stimulate colony formation of murine hematopoietic progenitor cells. Stem Cells. 24:850-856.
18. Hellström, M., L.K. Phng, J.J. Hofmann, E. Wallgard, L. Coultas, P. Lindblom, J. Alva, A.K. Nilsson, L. Karlsson, N. Gaiano, et al. 2007. Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature. 445:776-780.
19. Henking, P., and L.F. De Oliveira. 1967. Development of retinal vessels in the rat. Invest. Ophthalmol. 6:520-530.
20. Jakobsson, L., C.A. Franco, K. Bentley, R.T. Collins, B. Ponsioen, I.M. Aspalter, I. Rosewell, M. Busse, G. Thurston, A. Medvinsky, et al. 2010. Endothelialcells dynamically compete for the tip cell position during angiogenic sprouting. Nat. Cell Biol. 12:943-953.
21. Jiang, Y., B. Vaessen, T. Lenvik, M. Blackstad, M. Reyes, and C.M. Verfaillie. 2002. Multipotent progenitor cells can be isolated from postnatal murine bone marrow, muscle, and brain. Exp. Hematol. 30:896-904.
22. Jin, D.K., K. Shido, H.G. Kopp, I. Petit, S.V. Shmelkov, L.M. Young, A.T. Hooper, H. Amano, S.T. Avecilla, B. Heissig, et al. 2006. Cytokinemediated deployment of SDF-1 induces revascularization through recruitment of CXCR4+ hemangiocytes. Nat. Med. 12:557-567.
23. Kawamoto, S., H. Niwa, F. Tashiro, S. Sano, G. Kondoh, J. Takeda, K. Tabayashi, and J. Miyazaki. 2000. A novel reporter mouse strain that expresses enhanced green fluorescent protein upon Cre-mediated recombination. FEBS Lett. 470:263-268.
24. Kubota, Y., M. Hirashima, K. Kishi, C.L. Stewart, and T. Suda. 2008. Leukemia inhibitory factor regulates microvessel density by modulating oxygendependent VEGF expression in mice. J. Clin. Invest. 118:2393-2403.
25. Lawson, N.D., A.M. Vogel, and B.M. Weinstein. 2002. sonic hedgehog and vascular endothelial growth factor act upstream of the Notch pathway during arterial endothelial differentiation. Dev. Cell. 3:127-136.
26. Lemke, G., and R. Axel. 1985. Isolation and sequence of a cDNA encoding the major structural protein of peripheral myelin. Cell. 40:501-508.
27. McLeod, D.S., T. Hasegawa, T. Prow, C. Merges, and G. Lutty. 2006. The initial fetal human retinal vasculature develops by vasculogenesis. Dev. Dyn. 235:3336-3347.
28. Millauer, B., S. Wizigmann-Voos, H. Schnürch, R. Martinez, N.P. Møller, W. Risau, and A. Ullrich. 1993. High affinity VEGF binding and developmental expression suggest Flk-1 as a major regulator of vasculogenesis and angiogenesis. Cell. 72:835-846.
29. Morikawa, S., Y. Mabuchi, K. Niibe, S. Suzuki, N. Nagoshi, T. Sunabori, S. Shimmura, Y. Nagai, T. Nakagawa, H. Okano, and Y. Matsuzaki. 2009. Development of mesenchymal stem cells partially originate from the neural crest. Biochem. Biophys. Res. Commun. 379:1114-1119.
30. Nagoshi, N., S. Shibata, Y. Kubota, M. Nakamura, Y. Nagai, E. Satoh, S. Morikawa, Y. Okada, Y. Mabuchi, H. Katoh, et al. 2008. Ontogeny and multipotency of neural crest-derived stem cells in mouse bone marrow, dorsal root ganglia, and whisker pad. Cell Stem Cell. 2:392-403.
31. Noguera-Troise, I., C. Daly, N.J. Papadopoulos, S. Coetzee, P. Boland, N.W. Gale, H.C. Lin, G.D. Yancopoulos, and G. Thurston. 2006. Blockade of Dll4 inhibits tumour growth by promoting non-productive angiogenesis. Nature. 444:1032-1037.
32. Phng, L.K., M. Potente, J.D. Leslie, J. Babbage, D. Nyqvist, I. Lobov, J.K. Ondr, S. Rao, R.A. Lang, G. Thurston, and H. Gerhardt. 2009. Nrarp coordinates endothelial Notch and Wnt signaling to control vessel density in angiogenesis. Dev. Cell. 16:70-82.
33. Pietri, T., O. Eder, M. Blanche, J.P. Thiery, and S. Dufour. 2003. The human tissue plasminogen activator-Cre mouse: a new tool for targeting specifically neural crest cells and their derivatives in vivo. Dev. Biol. 259: 176-187.
34. Planat-Benard, V., J.S. Silvestre, B. Cousin, M. André, M. Nibbelink, R. Tamarat, M. Clergue, C. Manneville, C. Saillan-Barreau, M. Duriez, et al. 2004. Plasticity of human adipose lineage cells toward endothelial cells: physiological and therapeutic perspectives. Circulation. 109:656-663.
35. Purhonen, S., J. Palm, D. Rossi, N. Kaskenpää, I. Rajantie, S. Ylä-Herttuala, K. Alitalo, I.L. Weissman, and P. Salven. 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.
36. Ratajczak, M.Z., E.K. Zuba-Surma, B. Machalinski, J. Ratajczak, and M. Kucia. 2008. Very small embryonic-like (VSEL) stem cells: purification from adult organs, characterization, and biological significance. Stem Cell Rev. 4:89-99.
37. Ricci-Vitiani, L., R. Pallini, M. Biffoni, M. Todaro, G. Invernici, T. Cenci, G. Maira, E.A. Parati, G. Stassi, L.M. Larocca, and R. De Maria. 2010. Tumour vascularization via endothelial differentiation of glioblastoma stem-like cells. Nature. 468:824-828.
38. Ridgway, J., G. Zhang, Y. Wu, S. Stawicki, W.C. Liang, Y. Chanthery, J. Kowalski, R.J. Watts, C. Callahan, I. Kasman, et al. 2006. Inhibition of Dll4 signalling inhibits tumour growth by deregulating angiogenesis. Nature. 444:1083-1087.
39. Risau, W. 1997. Mechanisms of angiogenesis. Nature. 386:671-674.
40. Sato, Y., T. Watanabe, D. Saito, T. Takahashi, S. Yoshida, J. Kohyama, E. Ohata, H. Okano, and Y. Takahashi. 2008. Notch mediates the segmental specification of angioblasts in somites and their directed migration toward the dorsal aorta in avian embryos. Dev. Cell. 14:890-901.
41. Schuh, A.C., P. Faloon, Q.L. Hu, M. Bhimani, and K. Choi. 1999. In vitro hematopoietic and endothelial potential of flk-1(-/-) embryonic stem cells and embryos. Proc. Natl. Acad. Sci. USA. 96:2159-2164.
42. Shalaby, F., J. Rossant, T.P. Yamaguchi, M. Gertsenstein, X.F. Wu, M.L. Breitman, and A.C. Schuh. 1995. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature. 376:62-66.
43. Stern, C.D., and S.E. Fraser. 2001. Tracing the lineage of tracing cell lineages. Nat. Cell Biol. 3:E216-E218.
44. Suchting, S., C. Freitas, F. le Noble, R. Benedito, C. Bréant, A. Duarte, and A. Eichmann. 2007. The Notch ligand Delta-like 4 negatively regulatesendothelial tip cell formation and vessel branching. Proc. Natl. Acad. Sci. USA. 104:3225-3230.
45. Tamamura, H., A. Omagari, K. Hiramatsu, K. Gotoh, T. Kanamoto, Y. Xu, E. Kodama, M. Matsuoka, T. Hattori, N. Yamamoto, et al. 2001. Development of specific CXCR4 inhibitors possessing high selectivity indexes as well as complete stability in serum based on an anti-HIV peptide T140. Bioorg. Med. Chem. Lett. 11:1897-1902.
46. Tammela, T., G. Zarkada, E. Wallgard, A. Murtomäki, S. Suchting, M. Wirzenius, M. Waltari, M. Hellström, T. Schomber, R. Peltonen, et al. 2008. Blocking VEGFR-3 suppresses angiogenic sprouting and vascular network formation. Nature. 454:656-660.
47. Vodyanik, M.A., J. Yu, X. Zhang, S. Tian, R. Stewart, J.A. Thomson, and I.I. Slukvin. 2010. A mesoderm-derived precursor for mesenchymal stem and endothelial cells. Cell Stem Cell. 7:718-729.
48. Wang, R., K. Chadalavada, J. Wilshire, U. Kowalik, K.E. Hovinga, A. Geber, B. Fligelman, M. Leversha, C. Brennan, and V. Tabar. 2010. Glioblastoma stem-like cells give rise to tumour endothelium. Nature. 468:829-833.
49. Wurmser, A.E., K. Nakashima, R.G. Summers, N. Toni, K.A. D'Amour, D.C. Lie, and F.H. Gage. 2004. Cell fusion-independent differentiation of neural stem cells to the endothelial lineage. Nature. 430:350-356.
50. Yamauchi, Y., K. Abe, A. Mantani, Y. Hitoshi, M. Suzuki, F. Osuzu, S. Kuratani, and K. Yamamura. 1999. A novel transgenic technique that allows specific marking of the neural crest cell lineage in mice. Dev. Biol. 212:191-203.