N-CAM exhibits a regulatory function in pathological angiogenesis in oxygen induced retinopathy

PLoS ONE

Volumn 6, Issue 10, 2011, Pages

  Håkansson, Joakim ^a,e   Ståhlberg, Anders ^a,b   Wolfhagen Sand, Fredrik ^a,c   Gerhardt, Holger ^a,d   Semb, Henrik ^a,c  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b TATAA Biocenter   (Sweden)

^c LUND UNIVERSITY   (Sweden)

^d IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^e PharmaSurgics in Sweden AB   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; NERVE CELL ADHESION MOLECULE; VASCULOTROPIN A;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BIOACCUMULATION; CELL LEVEL; CELL PROLIFERATION; CONTROLLED STUDY; ENDOTHELIUM CELL; EPIRETINAL MEMBRANE; MOUSE; NEWBORN; NONHUMAN; OXYGEN INDUCED RETINOPATHY; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; RETINA NEOVASCULARIZATION; RETINOPATHY;

ANIMALS; ANOXIA; CELL PROLIFERATION; DIABETIC RETINOPATHY; ENDOTHELIAL CELLS; MICE; NEOVASCULARIZATION, PATHOLOGIC; NEURAL CELL ADHESION MOLECULES; RETINAL NEOVASCULARIZATION; RETINAL VESSELS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 80054746929     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0026026     Document Type: Article

References (47)

1. Kahn HA, Hiller R, (1974) Blindness caused by diabetic retinopathy. Am J Ophthalmol 78: 58-67.
2. Gibson DL, Sheps SB, Uh SH, Schechter MT, McCormick AQ, (1990) Retinopathy of prematurity-induced blindness: birth weight-specific survival and the new epidemic. Pediatrics 86: 405-412.
3. Smith LE, Wesolowski E, McLellan A, Kostyk SK, D'Amato R, et al. (1994) Oxygen-induced retinopathy in the mouse. Invest Ophthalmol Vis Sci 35: 101-111.
4. Stone J, Itin A, Alon T, Pe'er J, Gnessin H, et al. (1995) Development of retinal vasculature is mediated by hypoxia-induced vascular endothelial growth factor (VEGF) expression by neuroglia. J Neurosci 15: 4738-4747.
5. Stone J, Chan-Ling T, Pe'er J, Itin A, Gnessin H, et al. (1996) Roles of vascular endothelial growth factor and astrocyte degeneration in the genesis of retinopathy of prematurity. Invest Ophthalmol Vis Sci 37: 290-299.
6. Gospodarowicz D, Abraham JA, Schilling J, (1989) Isolation and characterization of a vascular endothelial cell mitogen produced by pituitary-derived folliculo stellate cells. Proc Natl Acad Sci U S A 86: 7311-7315.
7. Connolly DT, (1991) Vascular permeability factor: a unique regulator of blood vessel function. J Cell Biochem 47: 219-223.
8. Ferrara N, Houck KA, Jakeman LB, Winer J, Leung DW, (1991) The vascular endothelial growth factor family of polypeptides. J Cell Biochem 47: 211-218.
9. Gerhardt H, Golding M, Fruttiger M, Ruhrberg C, Lundkvist A, et al. (2003) VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol 161: 1163-1177.
10. Bartsch U, Kirchhoff F, Schachner M, (1990) Highly sialylated N-CAM is expressed in adult mouse optic nerve and retina. J Neurocytol 19: 550-565.
11. Sawaguchi A, Idate Y, Ide S, Kawano J, Nagaike R, et al. (1999) Multistratified expression of polysialic acid and its relationship to VAChT-containing neurons in the inner plexiform layer of adult rat retina. J Histochem Cytochem 47: 919-928.
12. Wojciechowski AB, Englund U, Lundberg C, Warfvinge K, (2004) Migratory capacity of the cell line RN33B and the host glial cell response after subretinal transplantation to normal adult rats. Glia 47: 58-67.
13. Liepe BA, Stone C, Koistinaho J, Copenhagen DR, (1994) Nitric oxide synthase in Muller cells and neurons of salamander and fish retina. J Neurosci 14: 7641-7654.
14. Paulson OB, Newman EA, (1987) Does the release of potassium from astrocyte endfeet regulate cerebral blood flow? Science 237: 896-898.
15. Flower RW, McLeod DS, Lutty GA, Goldberg B, Wajer SD, (1985) Postnatal retinal vascular development of the puppy. Invest Ophthalmol Vis Sci 26: 957-968.
16. Newman E, Reichenbach A, (1996) The Muller cell: a functional element of the retina. Trends Neurosci 19: 307-312.
17. Stone J, Dreher Z, (1987) Relationship between astrocytes, ganglion cells and vasculature of the retina. J Comp Neurol 255: 35-49.
18. Fruttiger M, (2002) Development of the mouse retinal vasculature: angiogenesis versus vasculogenesis. Invest Ophthalmol Vis Sci 43: 522-527.
19. Xian X, Hakansson J, Stahlberg A, Lindblom P, Betsholtz C, et al. (2006) Pericytes limit tumor cell metastasis. J Clin Invest 116: 642-651.
20. Ishida S, Usui T, Yamashiro K, Kaji Y, Amano S, et al. (2003) VEGF164-mediated inflammation is required for pathological, but not physiological, ischemia-induced retinal neovascularization. J Exp Med 198: 483-489.
21. Kuwabara K, Ogawa S, Matsumoto M, Koga S, Clauss M, et al. (1995) Hypoxia-mediated induction of acidic/basic fibroblast growth factor and platelet-derived growth factor in mononuclear phagocytes stimulates growth of hypoxic endothelial cells. Proc Natl Acad Sci U S A 92: 4606-4610.
22. Cao R, Brakenhielm E, Pawliuk R, Wariaro D, Post MJ, et al. (2003) Angiogenic synergism, vascular stability and improvement of hind-limb ischemia by a combination of PDGF-BB and FGF-2. Nat Med 9: 604-613.
23. Bohnsack BL, Hirschi KK, (2004) Red light, green light: signals that control endothelial cell proliferation during embryonic vascular development. Cell Cycle 3: 1506-1511.
24. Smith LE, Shen W, Perruzzi C, Soker S, Kinose F, et al. (1999) Regulation of vascular endothelial growth factor-dependent retinal neovascularization by insulin-like growth factor-1 receptor. Nat Med 5: 1390-1395.
25. Smith LE, (2005) IGF-1 and retinopathy of prematurity in the preterm infant. Biol Neonate 88: 237-244.
26. Williams EJ, Furness J, Walsh FS, Doherty P, (1994) Activation of the FGF receptor underlies neurite outgrowth stimulated by L1, N-CAM, and N-cadherin. Neuron 13: 583-594.
27. Povlsen GK, Berezin V, Bock E, (2008) Neural cell adhesion molecule-180-mediated homophilic binding induces epidermal growth factor receptor (EGFR) down-regulation and uncouples the inhibitory function of EGFR in neurite outgrowth. J Neurochem 104: 624-639.
28. Gardiner TA, Gibson DS, de Gooyer TE, de la Cruz VF, McDonald DM, et al. (2005) Inhibition of Tumor Necrosis Factor-{alpha} Improves Physiological Angiogenesis and Reduces Pathological Neovascularization in Ischemic Retinopathy. Am J Pathol 166: 637-644.
29. Ruhrberg C, Gerhardt H, Golding M, Watson R, Ioannidou S, et al. (2002) Spatially restricted patterning cues provided by heparin-binding VEGF-A control blood vessel branching morphogenesis. Genes Dev 16: 2684-2698.
30. Miller JW, Adamis AP, Shima DT, D'Amore PA, Moulton RS, et al. (1994) Vascular endothelial growth factor/vascular permeability factor is temporally and spatially correlated with ocular angiogenesis in a primate model. Am J Pathol 145: 574-584.
31. Pe'er J, Shweiki D, Itin A, Hemo I, Gnessin H, et al. (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.
32. Shima DT, Adamis AP, Ferrara N, Yeo KT, Yeo TK, et al. (1995) Hypoxic induction of endothelial cell growth factors in retinal cells: identification and characterization of vascular endothelial growth factor (VEGF) as the mitogen. Mol Med 1: 182-193.
33. Pierce EA, Foley ED, Smith LE, (1996) Regulation of vascular endothelial growth factor by oxygen in a model of retinopathy of prematurity. Arch Ophthalmol 114: 1219-1228.
34. Shima DT, Kuroki M, Deutsch U, Ng YS, Adamis AP, et al. (1996) The mouse gene for vascular endothelial growth factor. Genomic structure, definition of the transcriptional unit, and characterization of transcriptional and post-transcriptional regulatory sequences. J Biol Chem 271: 3877-3883.
35. McColm JR, Geisen P, Hartnett ME, (2004) VEGF isoforms and their expression after a single episode of hypoxia or repeated fluctuations between hyperoxia and hypoxia: relevance to clinical ROP. Mol Vis 10: 512-520.
36. Brooks SE, Gu X, Samuel S, Marcus DM, Bartoli M, et al. (2001) Reduced severity of oxygen-induced retinopathy in eNOS-deficient mice. Invest Ophthalmol Vis Sci 42: 222-228.
37. Knowles RG, Moncada S, (1994) Nitric oxide synthases in mammals. Biochem J 298 (Pt 2): 249-258.
38. Christopherson KS, Bredt DS, (1997) Nitric oxide in excitable tissues: physiological roles and disease. J Clin Invest 100: 2424-2429.
39. Fulton D, Gratton JP, McCabe TJ, Fontana J, Fujio Y, et al. (1999) Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature 399: 597-601.
40. Murohara T, Asahara T, Silver M, Bauters C, Masuda H, et al. (1998) Nitric oxide synthase modulates angiogenesis in response to tissue ischemia. J Clin Invest 101: 2567-2578.
41. Chiarugi V, Ruggiero M, Magnelli L, (2000) Molecular polarity in endothelial cells and tumor-induced angiogenesis. Oncol Res 12: 1-4.
42. Hedin U, Roy J, Tran PK, Lundmark K, Rahman A, (1999) Control of smooth muscle cell proliferation-the role of the basement membrane. Thromb Haemost 82 (Suppl 1): 23-26.
43. Stupack DG, Cheresh DA, (2003) Apoptotic cues from the extracellular matrix: regulators of angiogenesis. Oncogene 22: 9022-9029.
44. Edvardsen K, Chen W, Rucklidge G, Walsh FS, Obrink B, et al. (1993) Transmembrane neural cell-adhesion molecule (NCAM), but not glycosyl-phosphatidylinositol-anchored NCAM, down-regulates secretion of matrix metalloproteinases. Proc Natl Acad Sci U S A 90: 11463-11467.
45. Cremer H, Lange R, Christoph A, Plomann M, Vopper G, et al. (1994) Inactivation of the N-CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning. Nature 367: 455-459.
46. Jones CA, London NR, Chen H, Park KW, Sauvaget D, et al. (2008) Robo4 stabilizes the vascular network by inhibiting pathologic angiogenesis and endothelial hyperpermeability. Nat Med 14: 448-453.
47. Stahlberg A, Hakansson J, Xian X, Semb H, Kubista M, (2004) Properties of the reverse transcription reaction in mRNA quantification. Clin Chem 50: 509-515.