The initial fetal human retinal vasculature develops by vasculogenesis

Developmental Dynamics

Volumn 235, Issue 12, 2006, Pages 3336-3347

  McLeod, D Scott ^a   Hasegawa, Takuya ^a   Prow, Tarl ^a   Merges, Carol ^a   Lutty, Gerard ^a,b  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b JOHNS HOPKINS HOSPITAL   (United States)

Author keywords

Angioblasts; Astrocyte precursor cells; Astrocytes; Endothelial cells; Progenitors; Proliferation; Vasculogenesis

Indexed keywords

ANTIBODY; APYRASE; CD31 ANTIGEN; CD34 ANTIGEN; CD39 ANTIGEN; CHEMOKINE RECEPTOR CXCR4; KI 67 ANTIGEN;

ANGIOGENESIS; ARTICLE; BLOOD CELL; CELL FUNCTION; CELL PROLIFERATION; CONFOCAL MICROSCOPY; DOWN REGULATION; EMBRYO; ENDOTHELIAL PROGENITOR CELL; ENDOTHELIUM CELL; GESTATIONAL AGE; HEMANGIOBLAST; HUMAN; HUMAN TISSUE; IMMUNOASSAY; IMMUNOHISTOCHEMISTRY; NERVE CELL; NEUROBLAST; PRIORITY JOURNAL; RETINA DEVELOPMENT; SPECTROSCOPY; STEM CELL;

ANTIGENS, CD; ANTIGENS, CD31; ANTIGENS, CD34; APYRASE; ASTROCYTES; CELL DIFFERENTIATION; CELL PROLIFERATION; EMBRYONIC STEM CELLS; ENDOTHELIAL CELLS; GESTATIONAL AGE; HUMANS; IMMUNOHISTOCHEMISTRY; KI-67 ANTIGEN; RECEPTORS, CXCR4; RETINA; RETINAL GANGLION CELLS; RETINAL VESSELS;

EID: 33845355387     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.20988     Document Type: Article

References (49)

1. Asahara T, Masuda H, Takahashi T, Kalka C, Pastore C, Silver M, Kearne M, Magner M, Isner JM. 1999. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res 85:221-228.
2. Ashton N. 1970. Retinal angiogenesis in the human embryo. Brit Med Bull 26:103-106.
3. Beck L, D'amore PA. 1997. Vascular development: cellular and molecular regulation. FASEB J 11:365-373.
4. Bhutto IA., Kim SY, Mcleod DS, Merges CA, Fukai N, Olsen BR, Lutty GA. 2004. Retinal and choroidal localization of collagen XVIII and the endostatin portion of collagen XVIII in aged human control and in age-related macular degeneration subjects. Invest Ophthalmol Vis Sci 45:1544-1552.
5. Chalasani S, Baribaud F, Coughlan C, Sunshine M, Lee V, Doms R, Littman DR, Raper JA. 2003. The chemokine stromal cell-derived factor-1 promotes the survival of embryonic retinal ganglion cells. J Neurosci 23:4601-4612.
6. Chan-Ling T, Mcleod DS, Hughes S, Baxter L, Chu Y, Hasegawa T, Lutty GA. 2004. Astrocyte-endothelial cell relationships during human retinal vascular development. Invest Ophthalmol Vis Sci 45:2020-2032.
7. Chu Y, Hughes S, Chan-Ling T. 2001. Differentiation and migration of astrocyte precursor cells and astrocytes in human fetal retina: relevance to optic nerve coloboma. FASEB J 15:2013-2015.
8. Civin C, Strauss LC, Brovall C, Fackler MJ, Schwartz J, Shaper J. 1984. Antigenic analysis of hematopoiesis. III. A hematopoietic progenitor cell surface antigen denned by a monoclonal antibody raised against KG-1a cells. J Immunol 133:157-165.
9. Crosby J, Kaminski W, Schatteman G, Martin P, Raines E, Seifert R, Bowen-Pope DF. 2000. Endothelial cells of hematopoietic origin make a significant contribution to adult blood vessel formation. Circ Res 87:728-730.
10. Drake C, Fleming P. 2000. Vasculogenesis in the day 6.5 to 9.5 mouse embryo. Blood 95:1671-1679.
11. Eltzschig H, Ibla J, Furuta GT, Leonard M, Jacobson K, Enjyoji K, Robson S, Colgan S. 2003. Coordinated adenine nucleotide phosphohydrolysis and nucleoside signaling in posthypoxic endothelium: role of ectonucleotidases and adenosine A2B receptors. J Exp Med 198:783-796.
12. Fina L, Molgaard H, Robertson D, Bradley N, Monaghan P, Delia D, Sutherland D, Baker MA., Greaves MF. 1990. Expression of the CD34 gene in vascular endothelial cells. Blood 75:2417-2426.
13. Fruttiger M. 2002. Development of the mouse retinal vasculature: angiogenesis versus vasculogenesis. Invest Ophthalmol Vis Sci 43:522-527.
14. Goepfert C, Sundberg C, Sevigny J, Enjyoji K, Hoshi T, Csizmadia E, Robson S. 2001. Disordered cellular migration and angiogenesis in cd39-null mice. Circulation 104:3109-3115.
15. Grant MB, Caballero S, Brown GA, Guthrie SM, Mames RN, Vaught T, Scott EW. 2003. The contribution of adult hematopoietic stem cells to retinal neovascularization. Adv Exp Med Biol 522:37-45.
16. Guo H, Fang B, Liao L, Zhao Z, Liu J, Chen H, Hsu S, Cui Q, Zhao R. 2003. Hemangioblastic characteristics of fetal bone marrow-derived Flk1(+)CD31(-)CD34(-) cells. Exp Hematol 31:650-658.
17. Hughes S, Yang H, Chan-Ling T. 2000. Vascularization of the human fetal retina: roles of vasculogenesis and angiogenesis. Invest Ophthalmol Vis Sci 41:1217-1228.
18. Imhof BA, Dunon D. 1995. Leukocyte migration and adhesion. Adv Immunol 58:345-416.
19. Juarez J, Bendall L, Bradstock K. 2004. Chemokines and their receptors as therapeutic targets: the role of the SDF-1/CXCR4 axis. Curr Pharm Des 10:1245-1259.
20. Kaczmarek E, Koziak K, Sevigny J, Siegel JB, Anrather J, Beaudoin A, Bach F, Robson S. 1996. Identification and characterization of CD39/vascular ATP diphosphohydrolase. J Biol Chem 271:33116-33122.
21. Labastie M, Cortes F, Romeo PH, Dulac C, Peault B. 1998. Molecular identity of hematopoietic precursor cells emerging in the human embryo. Blood 92:3624-3635.
22. Lazarini F, Tham TO, Casanova P, Arenzana-Seisdedos F, Dubois-Dalcq M. 2003. Role of the a-chemokine stromal cell-derived factor (SDF-1) in the developing and mature central nervous system. Glia 42:139-148.
23. Lutty GA, McLeod DS. 1992. A new technique for visualization of the human retinal vasculature. Arch Ophthalmol 110:267-276.
24. Lutty GA, McLeod DS. 2003. Retinal vascular development and oxygen-induced retinopathy: a role for adenosine. Prog Ret Eye Res 22:95-111.
25. Lutty GA, McLeod DS. 2005. Phosphatase enzyme histochemistry for studying vascular hierarchy, pathology, and endothelial cell dysfunction in retina and choroid. Vision Res 45:3504-3511.
26. Lutty GA, Merges C, Threlkeld AB, Crone S, McLeod DS. 1993. Heterogeneity in localization of isoforms of TGF-b in human retina, vitreous, and choroid. Invest Ophthalmol Vis Sci 34:477-487.
27. Lutty G, McLeod D, Pachnis A, Costantini F, Fabry M, Nagel R. 1994. Retinal and choroidal neovascularization in a transgenic mouse model of sickle cell disease. Am J Pathol 145:490-497.
28. Lutty GA, Phelan A, McLeod DS, Fabry ME, Nagel RL. 1996. A rat model for sickle cell-mediated vaso-occlusion in retina. Microvascular Res 52:270-280.
29. Lutty GA, Merges C, Grebe R, Prow T, McLeod DS. 2006. Canine retinal angioblasts are multipotent. Exp Eye Res 83:183-193.
30. Mann IC. 1928. The development of the human eye. Cambridge: University Press.
31. McLeod DS, Lutty GA, Wajer SD, Flower RW. 1987. Visualization of a developing vasculature. Microvasc Res 33:257-269.
32. McLeod D, Goldberg M, Lutty G. 1993. Dual perspective analysis of vascular formations in sickle cell retinopathy. Arch Ophthalmol 111:1234-1245.
33. McLeod DS, Brownstein R, Lutty GA. 1996a. Vaso-obliteration in the canine model of oxygen-induced retinopathy. Invest Ophthalmol Vis Sci 37:300-311.
34. McLeod D, Crone SN, Lutty GA. 1996b. Vasoproliferation in the neonatal dog model of oxygen-induced retinopathy. Invest Ophthalmol Vis Sci 37:1322-1333.
35. McLeod, DS, Merges C, Fukushima A, Goldberg MF, Lutty GA. 1997. Histopathological features of neovascularization in sickle cell retinopathy. Am J Ophthalmol 124:473-487.
36. Mhaskar R, Agarwal N, Takkar D, Buckshee K, Deorari A. 1989. Fetal foot length: a new parameter for assessment of gestational age. Int J Gynaecol Obstet 29:35-38.
37. Newman PJ. 1997. The biology of PECAM-1. J Clin Invest 100:S25-29.
38. Otani A, Kinder K, Ewalt K, Otero FJ, Schimmel P, Friedlander M. 2002. Bone marrow-derived stem cells target retinal astrocytes and can promote or inhibit retinal angiogenesis. Nat Med 8:1004-1010.
39. Peichev M, Naiyer AJ, Pereira D, Zhu Z, Lane WJ, Williams M, Oz MC, Hicklin DJ, Witte L, Moore MA., Rafii S. 2000. Expression of VEGFR-2 and AC133 by circulating human CD34(+) cells identifies a population of functional endothelial precursors. Blood 95:952-958.
40. Provis JM. 2001. Development of the primate retina. Prog Retin Eye Res 20:799-821.
41. Rhodes R. 1979. A light microscopic study of the developing human neural retina. Am J Anat 154:195-209.
42. Risau W. 1997. Mechanisms of angiogenesis. Nature 386:671-674.
43. Risau W. 1998. Development and differentiation of endothelium. Kidney Int 54(Suppl):S3-S6.
44. Risau W, Flamme I. 1995. Vasculogenesis. Ann Rev Cell Dev Biol 11:73-91.
45. Sandercoe TM, Madigan MC, Billson FA, Penfold PL, Provis JM. 1999. Astrocyte proliferation during development of the human retinal vasculature. Exp Eye Res 69:511-523.
46. Sengupta N, Caballero S, Mames RN, Butler JM, Scott EW, Grant MB. 2003. The role of adult bone marrow-derived stem cells in choroidal neovascularization. Invest Ophthalmol Vis Sci 44:4908-4913.
47. Taomoto M, McLeod DS, Merges C, Lutty GA. 2000. Localization of adenosine A2a receptor in retinal development and oxygen-induced retinopathy. Invest Ophthalmol Vis Sci 41:230-243.
48. Tavian M, Coulombel L, Luton D, Clemente H, Dieterlen-Lievre F, Peault B. 1996. Aorta-associated CD34+ hematopoietic cells in the early human embryo. Blood 87:67-72.
49. Yong K, Watts M, Shaun Thomas N, Sullivan A, Ings S, Linch DC. 1998. Transmigration of CD34+ cells across specialized and nonspecialized endothelium requires prior activation by growth factors and is mediated by PECAM-1 (CD31). Blood 91:1196-1205.