Ectopic Norrin induces growth of ocular capillaries and restores normal retinal angiogenesis in Norrie disease mutant mice

Journal of Neuroscience

Volumn 25, Issue 7, 2005, Pages 1701-1710

  Ohlmann, Andreas ^a   Scholz, Michael ^a   Goldwich, Andreas ^a   Chauhan, Bharesh K ^b   Hudl, Kristiane ^c   Ohlmann, Anne V ^a   Zrenner, Eberhart ^c   Berger, Wolfgang ^d   Cvekl, Aleš ^b   Seeliger, Mathias W ^c   Tamm, Ernst R ^a,e  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^d UNIVERSITY OF ZURICH   (Switzerland)

^e UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

Angiogenesis; Frizzled 4; Norrie disease; PIGF; Retina; VEGF

Indexed keywords

CELL PROTEIN; NORRIN; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; ELECTRON MICROSCOPY; ELECTRORETINOGRAPHY; EMBRYO; ENDOTHELIUM CELL; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; NORRIE DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA CAPILLARY; TRANSGENIC MOUSE;

ANIMALS; BETA-CRYSTALLINS; CAPILLARIES; CELL COUNT; CELL DIVISION; CELLS, CULTURED; CHICKENS; COCULTURE TECHNIQUES; ELECTRORETINOGRAPHY; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; EYE PROTEINS; GENE EXPRESSION REGULATION; HUMANS; LENS, CRYSTALLINE; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; NEOVASCULARIZATION, PHYSIOLOGIC; NERVE TISSUE PROTEINS; PROMOTER REGIONS (GENETICS); RECOMBINANT FUSION PROTEINS; RETINA; RETINAL GANGLION CELLS; RETINAL VESSELS; RNA, MESSENGER; SKIN;

EID: 20044387404     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4756-04.2005     Document Type: Article

References (41)

1. Ash JD, Overbeek PA (2000) Lens-specific VEGF-A expression induces angioblast migration and proliferation and stimulates angiogenic remodeling. Dev Biol 223:383-398.
2. Berger W (1998) Molecular dissection of Norrie disease. Acta Anat (Basel) 162:95-100.
3. Berger W, van de PD, Warburg M, Gal A, Bleeker-Wagemakers L, de Silva H, Meindl A, Meitinger T, Cremers F, Ropers HH (1992) Mutations in the candidate gene for Norrie disease. Hum Mol Genet 1:461-465.
4. Berger W, van de PD, Bachner D, Oerlemans F, Winkens H, Hameister H, Wieringa B, Hendriks W, Ropers HH (1996) An animal model for Norrie disease (ND): gene targeting of the mouse ND gene. Hum Mol Genet 5:51-59.
5. Cepko CL, Austin CP, Yang X, Alexiades M, Ezzeddine D (1996) Cell fate determination in the vertebrate retina. Proc Natl Acad Sci USA 93:589-595.
6. Connolly SE, Hores TA, Smith LE, D'Amore PA (1988) Characterization of vascular development in the mouse retina. Microvasc Res 36:275-290.
7. Duhamel RC, Johnson DA (1985) Use of nonfat dry milk to block nonspecific nuclear and membrane staining by avidin conjugates. J Histochem Cytochem 33:711-714.
8. Duncan MK, Roth HJ, Thompson M, Kantorow M, Piatigorsky J (1995) Chicken βB1 crystallin: gene sequence and evidence for functional conservation of promoter activity between chicken and mouse. Biochim Biophys Acta 1261:68-76.
9. Duncan MK, Li X, Ogino H, Yasuda K, Piatigorsky J (1996) Developmental regulation of the chicken βB1-crystallin promoter in transgenic mice. Mech Dev 57:79-89.
10. Favre CJ, Mancuso M, Maas K, McLean JW, Baluk P, McDonald DM (2003) Expression of genes involved in vascular development and angiogenesis in endothelial cells of adult lung. Am J Physiol Heart Circ Physiol 285:H1917-H1938.
11. Feeney SA, Simpson DA, Gardiner TA, Boyle C, Jamison P, Stitt AW (2003) Role of vascular endothelial growth factor and placental growth factors during retinal vascular development and hyaloid regression. Invest Ophthalmol Vis Sci 44:839-847.
12. Flügel-Koch C, Ohlmann A, Piatigorsky J, Tamm ER (2002) Overexpression of TGF-β1 alters early development of cornea and lens in transgenic mice. Dev Dyn 225:111-125.
13. Fruttiger M (2002) Development of the mouse retinal vasculature: angiogenesis versus vasculogenesis. Invest Ophthalmol Vis Sci 43:522-527.
14. Inatani M, Tanihara H (2002) Proteoglycans in retina. Prog Retin Eye Res 21:429-447.
15. Ito M, Yoshioka M (1999) Regression of the hyaloid vessels and pupillary membrane of the mouse. Anat Embryol (Berl) 200:403-411.
16. Ito S, Karnovsky MJ (1968) Formaldehyde-glutaraldehyde fixatives containing trinitro compounds. J Cell Biol 39:168A-169A.
17. Lindahl P, Johansson BR, Leveen P, Betsholtz C (1997) Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science 277:242-245.
18. Meindl A, Berger W, Meitinger T, van de PD, Achatz H, Dorner C, Haasemann M, Hellebrand H, Gal A, Cremers F (1992) Norrie disease is caused by mutations in an extracellular protein resembling C-terminal globular domain of mucins. Nat Genet 2:139-143.
19. Meitinger T, Meindl A, Bork P, Rost B, Sander C, Haasemann M, Murken J ( 1993) Molecular modelling of the Norrie disease protein predicts a cystine knot growth factor tertiary structure. Nat Genet 5:376-380.
20. Möller A, Eysteinsson T, Steingrímsson E (2004) Electroretinographic assessment of retinal function in microphthalmia mutant mice. Exp Eye Res 78:837-848.
21. Neufeld G, Cohen T, Gengrinovitch S, Poltorak Z (1999) Vascular endothelial growth factor (VEGF) and its receptors. FASEB J 13:9-22.
22. Ohlmann AV, Adamek E, Ohlmann A, Lütjen-Drecoll E (2004) Norrie gene product is necessary for regression of hyaloid vessels. Invest Ophthalmol Vis Sci 45:2384-2390.
23. Okamoto N, Tobe T, Hackett SF, Ozaki H, Vinores MA, LaRochelle W, Zack DJ, Campochiaro PA (1997) Transgenic mice with increased expression of vascular endothelial growth factor in the retina: a new model of intraretinal and subretinal neovascularization. Am J Pathol 151:281-291.
24. Perez-Vilar J, Hill RL (1997) Norrie disease protein (norrin) forms disulfide-linked oligomers associated with the extracellular matrix. J Biol Chem 272:33410-33415.
25. Provis JM (2001) Development of the primate retinal vasculature. Prog Retin Eye Res 20:799-821.
26. Rehm HL, Zhang DS, Brown MC, Burgess B, Halpin C, Berger W, Morton CC, Corey DP, Chen ZY (2002) Vascular defects and sensorineural deafness in a mouse model of Norrie disease. J Neurosci 22:4286-4292.
27. Richter M, Gottanka J, May CA, Welge-Lüssen U, Berger W, Lütjen-Drecoll E (1998) Retinal vasculature changes in Norrie disease mice. Invest Ophthalmol Vis Sci 39:2450-2457.
28. Robinson GS, Ju M, Shih SC, Xu X, McMahon G, Caldwell RB, Smith LE (2001) Nonvascular role for VEGF: VEGFR-1, 2 activity is critical for neural retinal development. FASEB J 15:1215-1217.
29. Robitaille J, MacDonald ML, Kaykas A, Sheldahl LC, Zeisler J, Dube MP, Zhang LH, Singaraja RR, Guernsey DL, Zheng B, Siebert LF, Hoskin-Mott A, Trese MT, Pimstone SN, Shastry BS, Moon RT, Hayden MR, Goldberg YP, Samuels ME (2002) Mutant frizzled-4 disrupts retinal angiogenesis in familial exudative vitreoretinopathy. Nat Genet 32:326-330.
30. Ruether K, van de Pol D, Jaissle G, Berger W, Tornow RP, Zrenner E (1997) Retinoschisislike alterations in the mouse eye caused by gene targeting of the Norrie disease gene. Invest Ophthalmol Vis Sci 38:710-718.
31. Schägger H, von Jagow G (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 166:368-379.
32. Seeliger MW, Grimm C, Stahlberg F, Friedburg C, Jaissle G, Zrenner E, Guo H, Reme CE, Humphries P, Hofmann F, Biel M, Fariss RN, Redmond TM, Wenzel A (2001) New views on RPE65 deficiency: the rod system is the source of vision in a mouse model of Leber congenital amaurosis. Nat Genet 29:70-74.
33. Stone J, Itin A, Alon T, Pe'er J, Gnessin H, Chan-Ling T, Keshet E (1995) Development of retinal vasculature is mediated by hypoxia-induced vascular endothelial growth factor (VEGF) expression by neuroglia. J Neurosci 15:4738-4747.
34. Tazawa Y, Seaman AJ (1972) The electroretinogram of the living extracorporeal bovine eye. The influence of anoxia and hypothermia. Invest Ophthalmol 11:691-698.
35. Tobe T, Okamoto N, Vinores MA, Derevjanik NL, Vinores SA, Zack DJ, Campochiaro PA (1998) Evolution of neovascularization in mice with overexpression of vascular endothelial growth factor in photoreceptors. Invest Ophthalmol Vis Sci 39:180-188.
36. Vinores SA, Seo MS, Derevjanik NL, Campochiaro PA (2003) Photoreceptor-specific overexpression of platelet-derived growth factor induces proliferation of endothelial cells, pericytes, and glial cells and aberrant vascular development: an ultrastructural and immunocytochemical study. Brain Res Dev Brain Res 140:169-183.
37. Wang Y, Huso D, Cahill H, Ryugo D, Nathans J (2001) Progressive cerebellar, auditory, and esophageal dysfunction caused by targeted disruption of the frizzled-4 gene. J Neurosci 21:4761-4771.
38. Weber BH, Schrewe H, Molday LL, Gehrig A, White KL, Seeliger MW, Jaissle GB, Friedburg C, Tamm E, Molday RS (2002) Inactivation of the murine X-linked juvenile retinoschisis gene, Rs1h, suggests a role of retinoschisin in retinal cell layer organization and synaptic structure. Proc Natl Acad Sci USA 99:6222-6227.
39. Xu Q, Wang Y, Dabdoub A, Smallwood PM, Williams J, Woods C, Kelley MW, Jiang L, Tasman W, Zhang K, Nathans J (2004) Vascular development in the retina and inner ear: control by Norrin and Frizzled-4, a high-affinity ligand-receptor pair. Cell 116:883-895.
40. Young RW (1984) Cell death during differentiation of the retina in the mouse. J Comp Neurol 229:362-373.
41. Yourey PA, Gohari S, Su JL, Alderson RF (2000) Vascular endothelial cell growth factors promote the in vitro development of rat photoreceptor cells. J Neurosci 20:6781-6788.