The axon guidance molecule netrin-4 is expressed by müller cells and contributes to angiogenesis in the retina

GLIA

Volumn 60, Issue 10, 2012, Pages 1567-1578

  Lange, Johannes ^a,b   Yafai, Yousef ^a   Noack, André ^a   Yang, Xiu Mei ^a,d   Munk, Anne Britta ^a   Krohn, Sandra ^a   Iandiev, Ianors ^a   Wiedemann, Peter ^a   Reichenbach, Andreas ^c   Eichler, Wolfram ^a,c  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b STAVANGER UNIVERSITY HOSPITAL   (Norway)

^c Paul Flechsig Institute for Brain Research   (Germany)

^d FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Angiogenesis; Cytokine; M ller cell; Netrins; Retina

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 3; NETRIN; NETRIN 4; UNCLASSIFIED DRUG; VASCULOTROPIN; VIMENTIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; COLORECTAL CANCER; CONTROLLED STUDY; ENDOTHELIUM CELL; GLIA CELL; IMMUNOFLUORESCENCE; MUELLER CELL; NERVE CELL; NERVE FIBER; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; RETINA; RETINA CELL;

ANIMALS; ANIMALS, NEWBORN; CATTLE; CELL HYPOXIA; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTHELIAL CELLS; ENZYME-LINKED IMMUNOSORBENT ASSAY; GUINEA PIGS; NEOVASCULARIZATION, PATHOLOGIC; NERVE GROWTH FACTORS; NEUROGLIA; PHOSPHORYLATION; RATS; RATS, LONG-EVANS; RECEPTORS, CELL SURFACE; RECEPTORS, RETINOIC ACID; RETINA; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEINS; UP-REGULATION;

EID: 84865338014     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22376     Document Type: Article

References (57)

1. Adamis AP, Shima DT. 2005. The role of vascular endothelial growth factor in ocular health and disease. Retina 25: 111-118.
2. Bauch H, Stier H, Schlosshauer B. 1998. Axonal versus dendritic outgrowth is differentially affected by radial glia in discrete layers of the retina. J Neurosci 18: 1774-1785.
3. 2+ and pH, and activated by protein kinase A. Glia 19: 311-323.
4. Bringmann A, Pannicke T, Grosche J, Francke M, Wiedemann P, Skatchkov SN, Osborne NN, Reichenbach A. 2006. Müller cells in the healthy and diseased retina. Prog Retin Eye Res 25: 397-424.
5. Bringmann A, Iandiev I, Pannicke T, Wurm A, Hollborn M, Wiedemann P, Osborne NN, Reichenbach A. 2009. Cellular signaling and factors involved in Müller cell gliosis: Neuroprotective and detrimental effects. Prog Retin Eye Res 28: 423-451.
6. Bullard LE, Qi X, Penn JS. 2003. Role for extracellular signal-responsive kinase-1 and -2 in retinal angiogenesis. Invest Ophthalmol Vis Sci 44: 1722-1731.
7. Carmeliet P, Tessier-Lavigne M. 2005. Common mechanisms of nerve and blood vessel wiring. Nature 436: 193-200.
8. Carmeliet P. 2003. Blood vessels and nerves: Common signals, pathways and diseases. Nat Rev Genet 4: 710-720.
9. Cirulli V, Yebra M. 2007. Netrins: Beyond the brain. Nat Rev Mol Cell Biol 8: 296-306.
10. Ciulla TA, Rosenfeld PJ. 2009. Anti-vascular endothelial growth factor therapy for neovascular ocular diseases other than age-related macular degeneration. Curr Opin Ophthalmol 20: 166-174.
11. Cross MJ, Dixelius J, Matsumoto T, Claesson-Welsh L. 2003. VEGF receptor signal transduction. Trends Biochem Sci 28: 488-489.
12. De la Torre JR, Höpker VH, Ming GL, Poo MM, Tessier-Lavigne M, Hemmati-Brivanlou A, Holt CE. 1997. Turning of retinal growth cones in a netrin-1 gradient mediated by the netrin receptor DCC. Neuron 19: 1211-1224.
13. Eichler W, Yafai Y, Kuhrt H, Gräter R, Hoffmann S, Wiedemann P, Reichenbach A. 2001. Hypoxia: Modulation of endothelial cell proliferation by soluble factors released by retinal cells. Neuroreport 12: 4103-4108.
14. Eichler W, Yafai Y, Wiedemann P, Reichenbach A. 2004. Angiogenesis-related factors derived from retinal glial (Müller) cells in hypoxia. Neuroreport 15: 1633-1637.
15. Eveno C, Broqueres-You D, Feron JG, Rampanou A, Tijeras-Raballand A, Ropert S, Leconte L, Levy BI, Pocard M. 2011. Netrin-4 delays colorectal cancer carcinomatosis by inhibiting tumor angiogenesis. Am J Pathol 178: 1861-1869.
16. Ferrara N, Gerber HP, LeCouter J. 2003. The biology of VEGF and its receptors. Nat Med 9: 669-676.
17. Folkman J. 1995. Angiogenesis in cancer, vascular, rheumatoid, and other diseases. Nat Med 1: 27-31.
18. Forcet C, Stein E, Pays L, Corset V, Llambi F, Tessier-Lavigne M, Mehlen P. 2002. Netrin-1-mediated axon outgrowth requires deleted in colorectal cancer-dependent MAPK activation. Nature 417: 443-447.
19. Freitas C, Larrivée B, Eichmann A. 2008. Netrins and UNC5 receptors in angiogenesis. Angiogenesis 11: 23-29.
20. Gao G, Li Y, Zhang D, Gee S, Crosson C, Ma J. 2001. Unbalanced expression of VEGF and PEDF in ischemia-induced retinal neovascularization. FEBS Lett 489: 270-276.
21. Gariano RF. 2003. Cellular mechanisms in retinal vascular development. Prog Retin Eye Res 22: 295-306.
22. Hoang S, Liauw J, Choi M, Choi M, Guzman RG, Steinberg GK. 2009. Netrin-4 enhances angiogenesis and neurologic outcome after cerebral ischemia. J Cereb Blood Flow Metab 29: 385-397.
23. Huang C, Jacobson K, Schaller MD. 2004. MAP kinases and cell migration. J Cell Sci 117: 4619-4628.
24. Ishibashi T, Hata Y, Yoshikawa H, Nakagawa K, Sueishi K, Inomata H. 1997. Expression of vascular endothelial growth factor in experimental choroidal neovascularization. Graefe's Arch Clin Exp Ophthalmol 235: 159-167.
25. Kwak N, Okamoto N, Wood JM, Campochiaro PA. 2000. VEGF is major stimulator in model of choroidal neovascularization. Invest Ophthalmol Vis Sci 41: 3158-3164.
26. Lambert E, Coissieux MM, Laudet V, Mehlen P. 2012. Netrin-4 acts as a pro-angiogenic factor during zebrafish development. J Biol Chem 287: 3987-3999.
27. Larrieu-Lahargue F, Welm AL, Thomas KR, Li DY. 2010. Netrin-4 induces lymphangiogenesis in vivo. Blood 115: 5418-5426.
28. Larrivée B, Freitas C, Suchting S, Brunet I, Eichmann A. 2009. Guidance of vascular development: Lessons from the nervous system. Circ Res 104: 428-441.
29. Lejmi E, Leconte L, Pédron-Mazoyer S, Ropert S, Raoul W, Lavalette S, Bouras I, Feron JG, Maitre-Boube M, Assayag F, Feumi C, Alemany M, Jie TX, Merkulova T, Poupon MF, Ruchoux MM, Tobelem G, Sennlaub F, Plouët J. 2008. Netrin-4 inhibits angiogenesis via binding to neogenin and recruitment of Unc5B. Proc Natl Acad Sci USA 105: 12491-12496.
30. Levy AP, Levy NS, Wegner S, Goldberg MA. 1995. Transcriptional regulation of the rat vascular endothelial growth factor gene by hypoxia. J Biol Chem 270: 13333-13340.
31. Li YN, Pinzón-Duarte G, Dattilo M, Claudepierre T, Koch M, Brunken WJ. 2012. The expression and function of netrin-4 in murine ocular tissues. Exp Eye Res 96: 24-35.
32. Liu Y, Cox SR, Morita T, Kourembanas S. 1995. Hypoxia regulates vascular endothelial growth factor gene expression in endothelial cells. Identification of a 5′ enhancer. Circ Res 77: 638-643.
33. Liu Y, Stein E, Oliver T, Li Y, Brunken WJ, Koch M, Tessier-Lavigne M, Hogan BL. 2004. Novel role for Netrins in regulating epithelial behaviour during lung branching morphogenesis. Curr Biol 14: 897-905.
34. Lu X, Le Noble F, Yuan L, Jiang Q, De Lafarge B, Sugiyama D, Bréant C, Claes F, De Smet F, Thomas JL, Autiero M, Carmeliet P, Tessier-Lavigne M, Eichmann A. 2004. The Netrin receptor UNC5B mediates guidance events controlling morphogenesis of the vascular system. Nature 432: 179-186.
35. Millauer B, Wizigmann-Voos S, Schnürch H, Martinez R, Møller NP, Risau W, Ullrich A. 1993. High affinity VEGF binding and developmental expression suggest Flk-1 as a major regulator of vasculogenesis and angiogenesis. Cell 72: 835-846.
36. Ming GL, Wong ST, Henley J, Yuan XB, Song HJ, Spitzer NC, Poo MM. 2002. Adaptation in the chemotactic guidance of nerve growth cones. Nature 417: 411-418.
37. Moore SW, Tessier-Lavigne M, Kennedy TE. 2007. Netrins and their receptors. Adv Exp Med Biol 621: 17-31.
38. Nacht M, St Martin TB, Byrne A, Klinger KW, Teicher BA, Madden SL, Jiang Y. 2009. Netrin-4 regulates angiogenic responses and tumor cell growth. Exp Cell Res 315: 784-794.
39. Newman E, Reichenbach A. 1996. The Müller cells: A functional element of the retina. Trends Neurosci 19: 307-312.
40. Nguyen A, Cai H. 2006. Netrin-1 induces angiogenesis via a DCC-dependent ERK1/2-eNOS feed-forward mechanism. Proc Natl Acad Sci USA 103: 6530-6535.
41. Nishijima K, Ng YS, Zhong L, Bradley J, Schubert W, Jo N, Akita J, Samuelsson SJ, Robinson GS, Adamis AP, Shima DT. 2007. Vascular endothelial growth factor-A is a survival factor for retinal neurons and a critical neuroprotectant during the adaptive response to ischemic injury. Am J Pathol 171: 53-67.
42. Park KW, Crouse D, Lee M, Karnik SK, Sorensen LK, Murphy KJ, Kuo CJ, Li DY. 2004. The axonal attractant Netrin-1 is an angiogenic factor. Proc Natl Acad Sci USA 101: 16210-16215.
43. Pe'er J, Shweiki D, Itin A, Hemo I, Gnessin H, Keshet E. 1995. Hypoxia-induced expression of vascular endothelial growth factor by retinal cells is a common factor in neovascularizing ocular diseases. Lab Invest 72: 638-645.
44. Pe'er J, Folberg R, Itin A, Gnessin H, Hemo I, Keshet E. 1996. Upregulated expression of vascular endothelial growth factor in proliferative diabetic retinopathy. Br J Ophthalmol 80: 241-245.
45. Petrova TV, Makinen T, Alitalo K. 1999. Signaling via vascular endothelial growth factor receptors. Exp Cell Res 253: 117-130.
46. Pierce EA, Avery RL, Foley ED, Aiello LP, Smith LE. 1995. Vascular endothelial growth factor/vascular permeability factor expression in a mouse model of retinal neovascularization. Proc Natl Acad Sci USA 92: 905-909.
47. Reichenbach A, Stolzenburg JU, Wolburg H, Härtig W, El-Hifnawi E, Martin H. 1995. Effects of enhanced extracellular ammonia concentration on cultured mammalian retinal glial (Müller) cells. Glia 13: 195-208.
48. Risau W. 1997. Mechanisms of angiogenesis. Nature 386: 671-674.
49. Rosenberger P, Schwab JM, Mirakaj V, Masekowsky E, Mager A, Morote-Garcia JC, Unertl K, Eltzschig HK. 2009. Hypoxia-inducible factor-dependent induction of Netrin-1 dampens inflammation caused by hypoxia. Nat Immunol 10: 195-202.
50. Schneiders FI, Maertens B, Böse K, Li Y, Brunken WJ, Paulsson M, Smyth N, Koch M. 2007. Binding of Netrin-4 to laminin short arms regulates basement membrane assembly. J Biol Chem 282: 23750-23758.
51. Semenza GL. 2007. Vasculogenesis, angiogenesis, and arteriogenesis: Mechanisms of blood vessel formation and remodeling. J Cell Biochem 102: 840-847.
52. Srinivasan K, Strickland P, Valdes A, Shin G, Hinck, L. 2003. Netrin-1/neogenin interaction stabilizes multipotent progenitor cap cells during mammary gland morphogenesis. Dev Cell 4: 371-382.
53. Stone J, Itin A, Alon A, Pe'er J, Gnessin H, Keshet E. 1995. Development of retinal vasculature is mediated by hypoxia-induced vascular endothelial growth factor (VEGF) expression by neuroglia. Neuroscience 5: 4738-4747.
54. Wang W, Reeves WB, Ramesh G. 2009. Netrin-1 increases proliferation and migration of renal proximal tubular epithelial cells via the UNC5B receptor. Am J Physiol Renal Physiol. 296:F723-F729.
55. Wilson BD, Ii M, Park KW, Suli A, Sorensen LK, Larrieu-Lahargue F, Urness LD, Suh W, Asai J, Kock GA, Thorne T, Silver M, Thomas KR, Chien CB, Losordo DW, Li DY. 2006. Netrins promote developmental and therapeutic angiogenesis. Science 313: 640-644.
56. Yafai Y, Lange J, Wiedemann P, Reichenbach A, Eichler W. 2007. Pigment epithelium-derived factor acts as an opponent of growth-stimulatory factors in retinal glial-endothelial cell interactions. Glia 55: 642-651.
57. Yi X, Mai LC, Uyama M, Yew DT. 1998. Time-course expression of vascular endothelial growth factor as related to the development of the retinochoroidal vasculature in rats. Exp Brain Res 118: 155-160.