Potential role of microglia in retinal blood vessel formation

Investigative Ophthalmology and Visual Science

Volumn 47, Issue 8, 2006, Pages 3595-3602

  Checchin, Daniella ^a,b   Sennlaub, Florian ^a,c   Levavasseur, Etienne ^c   Leduc, Martin ^a   Chemtob, Sylvain ^a,b  

^a Research Center   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANT; CD18 ANTIBODY; CD18 ANTIGEN; CHEMOKINE RECEPTOR CX3CR1; CLODRONIC ACID; GREEN FLUORESCENT PROTEIN; LECTIN; LIPOSOME; MONOCLONAL ANTIBODY; CHEMOKINE RECEPTOR; CX3CR1 PROTEIN, MOUSE; OXYGEN;

ANGIOGENESIS; ARTICLE; DISEASE MODEL; ENDOTHELIUM CELL; EXPLANT; FETUS; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPERCAPNIA; HYPEROXIA; IMMUNOCOMPETENT CELL; MICROGLIA; NONHUMAN; PRIORITY JOURNAL; PROLIFERATIVE RETINOPATHY; PROMOTER REGION; RAT; RETINA BLOOD VESSEL; RETROLENTAL FIBROPLASIA; ANIMAL; C57BL MOUSE; CYTOLOGY; MACROPHAGE; METABOLISM; MORPHOGENESIS; MOUSE; NEWBORN; PATHOPHYSIOLOGY; PHYSIOLOGY; PRENATAL DEVELOPMENT; RETINA; SPRAGUE DAWLEY RAT;

ANIMALS; ANTIGENS, CD18; CLODRONIC ACID; GREEN FLUORESCENT PROTEINS; HUMANS; HYPERCAPNIA; HYPEROXIA; INFANT, NEWBORN; LIPOSOMES; MACROPHAGES; MICE; MICE, INBRED C57BL; MICROGLIA; MORPHOGENESIS; OXYGEN; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, CHEMOKINE; RETINA; RETINAL VESSELS; RETINOPATHY OF PREMATURITY;

EID: 33748096137     PISSN: 01460404     EISSN: None     Source Type: Journal    
DOI: 10.1167/iovs.05-1522     Document Type: Article

References (63)

1. Chan-Ling T, Gock B, Stone J. The effect of oxygen on vasoformative cell division: evidence that 'physiological hypoxia' is the stimulus for normal retinal vasculogenesis. Invest Ophthalmol Vis Sci. 1995;36:1201-1214.
2. Watanabe T, Raff MC. Retinal astrocytes are immigrants from the optic nerve. Nature. 1988;332:834-837.
3. Ling TL, Mitrofanis J, Stone J. Origin of retinal astrocytes in the rat: evidence of migration from the optic nerve. J Comp Neurol. 1989;286:345-352.
4. Jiang B, Bezhadian MA, Caldwell RB. Astrocytes modulate retinal vasculogenesis: effects on endothelial cell differentiation. Glia. 1995;15:1-10.
5. Gerhardt H, Golding M, Fruttiger M, et al. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol. 2003;161:1163-1177.
6. Streit WJ. Microglia and macrophages in the developing CNS. Neurotoxicology. 2001;22:619-624.
7. Penfold PL, Provis JM, Liew SC. Human retinal microglia express phenotypic characteristics in common with dendritic antigen-presenting cells. J Neuroimmunol. 1993;45:183-191.
8. Provis JM, Penfold PL, Edwards AJ, van Driel D. Human retinal microglia: expression of immune markers and relationship to the glia limitans. Glia. 1995;14:243-256.
9. Diaz-Araya CM, Provis JM, Penfold PL. Ontogeny and cellular expression of MHC and leucocyte antigens in human retina. Glia. 1995;15:458-470.
10. Provis JM, Diaz CM, Penfold PL. Microglia in human retina: a heterogeneous population with distinct ontogenies. Perspect Dev Neurobiol. 1996;3:213-222.
11. Ashwell KW, Hollander H, Streit W, Stone J. The appearance and distribution of microglia in the developing retina of the rat. Vis Neurosci. 1989;2:437-448.
12. Ling EA. A light microscopic demonstration of amoeboid microglia and microglial cells in the retina of rats of various ages. Arch Histol Jpn. 1982;45:37-44.
13. Pennell NA, Streit WJ. Colonization of neural allografts by host microglial cells: relationship to graft neovascularization. Cell Transplant. 1997;6:221-230.
14. Lingen MW. Role of leukocytes and endothelial cells in the development of angiogenesis in inflammation and wound healing. Arch Pathol Lab Med. 2001;125:67-71.
15. Polverini PJ, Cotran PS, Gimbrone MA Jr, Unanue ER. Activated macrophages induce vascular proliferation. Nature. 1977;269:804-806.
16. Sunderkotter C, Goebeler M, Schulze-Osthoff K, Bhardwaj R, Sorg C. Macrophage-derived angiogenesis factors. Pharmacol Ther. 1991;51:195-216.
17. Crowther M, Brown NJ, Bishop ET, Lewis CE. Microenvironmental influence on macrophage regulation of angiogenesis in wounds and malignant tumors. J Leukoc Biol. 2001;70:478-490.
18. Knighton DR, Hunt TK, Scheuenstuhl H, et al. Oxygen tension regulates the expression of angiogenesis factor by macrophages. Science. 1983;221:1283-1285.
19. Lu YZ, Lin CH, Cheng FC, Hsueh CM. Molecular mechanisms responsible for microglia-derived protection of Sprague-Dawley rat brain cells during in vitro ischemia. Neurosci Lett. 2005;373:159-164.
20. Shimojo M, Nakajima K, Takei N, Hamanoue M, Kohsaka S. Production of basic fibroblast growth factor in cultured rat brain microglia. Neurosci Lett. 1991;123:229-231.
21. Liu X, Mashour GA, Webster HF, Kurtz A. Basic FGF and FGF receptor 1 are expressed in microglia during experimental autoimmune encephalomyelitis: temporally distinct expression of midkine and pleiotrophin. Glia. 1998;24:390-397.
22. Cross AK, Woodroofe MN. Chemokine modulation of matrix metalloproteinase and TIMP production in adult rat brain microglia and a human microglial cell line in vitro. Glia. 1999;28:183-189.
23. Gottschall PE, Deb S. Regulation of matrix metalloproteinase expressions in astrocytes, microglia and neurons. Neuroimmunomodulation. 1996;3:69-75.
24. Nagai A, Nakagawa E, Hatori K, et al. Generation and characterization of immortalized human microglial cell lines: expression of cytokines and chemokines. Neurobiol Dis. 2001;8:1057-1068.
25. Chao CC, Hu S, Close K, et al. Cytokine release from microglia: differential inhibition by pentoxifylline and dexamethasone. J Infect Dis. 1992;166:847-853.
26. Carter DA, Dick AD. CD200 maintains microglial potential to migrate in adult human retinal explant model. Curr Eye Res. 2004;28:427-436.
27. Jung S, Aliberti J, Graemmel P, et al. Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol Cell Biol. 2000;20:4106-4114.
28. Smith LE, Wesolowski E, McLellan A, et al. Oxygen-induced retinopathy in the mouse. Invest Ophthalmol Vis Sci. 1994;35:101-111.
29. Shohat M, Reisner SH, Krikler R, et al. Retinopathy of prematurity: incidence and risk factors. Pediatrics. 1983;72:159-163.
30. Holmes JM, Leske DA, Zhang S. The effect of raised inspired carbon dioxide on normal retinal vascular development in the neonatal rat. Curr Eye Res. 1997;16:78-81.
31. Checchin D, Sennlaub F, Sirinyan M, et al. Hypercapnia prevents neovascularization via nitrative stress. Free Radic Biol Med. 2006;40:543-553.
32. Altshuler D, Lo Turco JJ, Rush J, Cepko C. Taurine promotes the differentiation of a vertebrate retinal cell type in vitro. Development. 1993;119:1317-1328.
33. Hatakeyama J, Kageyama R. Retrovirus-mediated gene transfer to retinal explants. Methods. 2002;28:387-395.
34. Kermorvant-Duchemin E, Sennlaub F, Sirinyan M, et al. Transarachidonic acids generated during nitrative stress induce a thrombospondin-1-dependent microvascular degeneration. Nat Med. 2005;11:1339-1345.
35. Naito M, Nagai H, Kawano S, et al. Liposome-encapsulated dichloromethylene diphosphonate induces macrophage apoptosis in vivo and in vitro. J Leukoc Biol. 1996;60:337-344.
36. Schmidt-Weber CB, Rittig M, Buchner E, et al. Apoptotic cell death in activated monocytes following incorporation of clodronate-liposomes. J Leukoc Biol. 1996;60:230-244.
37. Bogers WM, Stad RK, Janssen DJ, et al. Kupffer cell depletion in vivo results in clearance of large-sized IgA aggregates in rats by liver endothelial cells. Clin Exp Immunol. 1991;85:128-136.
38. Diez-Roux G, Lang RA. Macrophages induce apoptosis in normal cells in vivo. Development. 1997;124:3633-3638.
39. Van Rooijen N, Sanders A. Liposome mediated depletion of macrophages: mechanism of action, preparation of liposomes and applications. J Immunol Methods. 1994;174:83-93.
40. Lahaie I, Hardy P, Hou X, et al. A novel mechanism for vasoconstrictor action of 8-isoprostaglandin F2 alpha on retinal vessels. Am J Physiol. 1998;274:R1406-R1416.
41. Armstrong RC. Isolation and characterization of immature oligodendrocyte lineage cells. Methods. 1998;16:282-292.
42. Huitinga I, Damoiseaux JG, van Rooijen N, Dopp EA, Dijkstra CD. Liposome mediated affection of monocytes. Immunobiology. 1992;185:11-19.
43. Hardy P, Dumont I, Bhattacharya M, et al. Oxidants, nitric oxide and prostanoids in the developing ocular vasculature: a basis for ischemic retinopathy. Cardiovasc Res. 2000;47:489-509.
44. Beauchamp MH, Sennlaub F, Speranza G, et al. Redox-dependent effects of nitric oxide on microvascular integrity in oxygen-induced retinopathy. Free Radic Biol Med. 2004;37:1885-1894.
45. Masson MJ, Uetrecht JP. Tolerance induced by low dose D-penicillamine in the brown Norway rat model of drug-induced autoimmunity is immune-mediated. Chem Res Toxicol. 2004;17:82-94.
46. Sunderkotter C, Steinbrink K, Goebeler M, Bhardwaj R, Sorg C. Macrophages and angiogenesis. J Leukoc Biol. 1994;55:410-422.
47. Polverini PJ. How the extracellular matrix and macrophages contribute to angiogenesis-dependent diseases. Eur J Cancer. 1996;32A:2430-2437.
48. Sakurai E, Anand A, Ambati BK, van Rooijen N, Ambati J. Macrophage depletion inhibits experimental choroidal neovascularization. Invest Ophthalmol Vis Sci. 2003;44:3578-3585.
49. Pollack A, Korte GE, Heriot WJ, Henkind P. Ultrastructure of Bruch's membrane after krypton laser photocoagulation, II: repair of Bruch's membrane and the role of macrophages. Arch Ophthalmol. 1986;104:1377-1382.
50. Penfold PL, Provis JM, Madigan MC, van Driel D, Billson FA. Angiogenesis in normal human retinal development: the involvement of astrocytes and macrophages. Graefes Arch Clin Exp Ophthalmol. 1990;228:255-263.
51. Diaz-Araya CM, Provis JM, Penfold PL, Billson FA. Development of microglial topography in human retina. J Comp Neurol. 1995;363:53-68.
52. Hume DA, Perry VH, Gordon S. Immunohistochemical localization of a macrophage-specific antigen in developing mouse retina: phagocytosis of dying neurons and differentiation of microglial cells to form a regular array in the plexiform layers. J Cell Biol. 1983;97:253-257.
53. Penfold PL, Provis JM. Cell death in the development of the human retina: phagocytosis of pyknotic and apoptotic bodies by retinal cells. Graefes Arch Clin Exp Ophthalmol. 1986;224:549-553.
54. Lin B, Ginsberg MD, Busto R, Dietrich WD. Sequential analysis of subacute and chronic neuronal, astrocytic and microglial alterations after transient global ischemia in rats. Acta Neuropathol (Berl). 1998;95:511-523.
55. Siren AL, McCarron R, Wang L, et al. Proinflammatory cytokine expression contributes to brain injury provoked by chronic monocyte activation. Mol Med. 2001;7:219-229.
56. Yossuck P, Yan Y, Tadesse M, Higgins RD. Dexamethasone alters TNF-alpha expression in retinopathy. Mol Genet Metab. 2001;72:164-167.
57. Yoshida S, Yoshida A, Ishibashi T. Induction of IL-8, MCP-1, and bFGF by TNF-alpha in retinal glial cells: implications for retinal neovascularization during post-ischemic inflammation. Graefes Arch Clin Exp Ophthalmol. 2004;242:409-413.
58. Forstreuter F, Lucius R, Mentlein R. Vascular endothelial growth factor induces chemotaxis and proliferation of microglial cells. J Neuroimmunol. 2002;132:93-98.
59. Lang RA, Bishop JM. Macrophages are required for cell death and tissue remodeling in the developing mouse eye. Cell. 1993;74:453-462.
60. Ishida S, Yamashiro K, Usui T, et al. Leukocytes mediate retinal vascular remodeling during development and vaso-obliteration in disease. Nat Med. 2003;9:781-788.
61. Duffield JS, Forbes SJ, Constandinou CM, et al. Selective depletion of macrophages reveals distinct, opposing roles during liver injury and repair. J Clin Invest. 2005;115:56-65.
62. Lobov IB, Rao S, Carroll TJ, et al. WNT7b mediates macrophage-induced programmed cell death in patterning of the vasculature. Nature. 2005;437:417-421.
63. Pe'er J, Shweiki D, Itin A, et al. Hypoxia-induced expression of vascular endothelial growth factor by retinal cells is a common factor in neovascularizing ocular diseases. Lab Invest. 1995;72:638-645.