Von Hippel-Lindau protein regulates transition from the fetal to the adult circulatory system in retina

Development

Volumn 137, Issue 9, 2010, Pages 1563-1571

  Kurihara, Toshihide ^a,b,f   Kubota, Yoshiaki ^a   Ozawa, Yoko ^a   Takubo, Keiyo ^a   Noda, Kousuke ^a,c   Simon, M Celeste ^d   Johnson, Randall S ^b   Suematsu, Makoto ^a   Tsubota, Kazuo ^a   Ishida, Susumu ^a,c   Goda, Nobuhito ^e   Suda, Toshio ^a   Okano, Hideyuki ^a  

^a KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

^e WASEDA UNIVERSITY   (Japan)

^f SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Angiogenesis; Circulatory system; Hypoxia inducible factor 1; Mouse

Indexed keywords

OXYGEN; UBIQUITIN PROTEIN LIGASE E3; VON HIPPEL LINDAU PROTEIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; VASCULOTROPIN A;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIOVASCULAR SYSTEM; CONTROLLED STUDY; DISEASE COURSE; DOWN REGULATION; NONHUMAN; OXYGEN SENSING; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA; RETINA BLOOD VESSEL; RETINA DEGENERATION; RETINA DEVELOPMENT; ANIMAL; BLOOD VESSEL; C57BL MOUSE; CONFOCAL MICROSCOPY; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MACROPHAGE; METABOLISM; MOUSE; PATHOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

MUS;

ANIMALS; BLOOD VESSELS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MACROPHAGES; MICE; MICE, INBRED C57BL; MICROSCOPY, CONFOCAL; RETINA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VON HIPPEL-LINDAU TUMOR SUPPRESSOR PROTEIN;

EID: 77951248799     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.049015     Document Type: Article

References (43)

1. Brown, D. M. and Regillo, C. D. (2007). Anti-VEGF agents in the treatment of neovascular age-related macular degeneration: applying clinical trial results to the treatment of everyday patients. Am. J. Ophthalmol. 144, 627-637.
2. Chen, J., Connor, K. M., Aderman, C. M. and Smith, L. E. (2008). Erythropoietin deficiency decreases vascular stability in mice. J. Clin. Invest. 118, 526-533. (Pubitemid 351206543)
3. Claxton, S. and Fruttiger, M. (2005). Oxygen modifies artery differentiation and network morphogenesis in the retinal vasculature. Dev. Dyn. 233, 822-828. (Pubitemid 40853458)
4. Fischer, C., Jonckx, B., Mazzone, M., Zacchigna, S., Loges, S., Pattarini, L., Chorianopoulos, E., Liesenborghs, L., Koch, M., De Mol, M. et al. (2007). Anti-PlGF inhibits growth of VEGF(R)-inhibitor-resistant tumors without affecting healthy vessels. Cell 131, 463-475. (Pubitemid 350007692)
5. Forsythe, J. A., Jiang, B. H., Iyer, N. V., Agani, F., Leung, S. W., Koos, R. D. and Semenza, G. L. (1996). Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol. Cell. Biol. 16, 4604-4613. (Pubitemid 26272112)
6. Fruttiger, M., Calver, A. R., Kruger, W. H., Mudhar, H. S., Michalovich, D., Takakura, N., Nishikawa, S. and Richardson, W. D. (1996). PDGF mediates a neuron-astrocyte interaction in the developing retina. Neuron 17, 1117-1131. (Pubitemid 27021098)
7. Gerhardt, H., Golding, M., Fruttiger, M., Ruhrberg, C., Lundkvist, A., Abramsson, A., Jeltsch, M., Mitchell, C., Alitalo, K., Shima, D. et al. (2003). VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J. Cell Biol. 161, 1163-1177. (Pubitemid 36870177)
8. Gnarra, J. R., Ward, J. M., Porter, F. D., Wagner, J. R., Devor, D. E., Grinberg, A., Emmert-Buck, M. R., Westphal, H., Klausner, R. D. and Linehan, W. M. (1997). Defective placental vasculogenesis causes embryonic lethality in VHL-deficient mice. Proc. Natl. Acad. Sci. USA 94, 9102-9107. (Pubitemid 27357789)
9. Gruber, M., Hu, C. J., Johnson, R. S., Brown, E. J., Keith, B. and Simon, M. C. (2007). Acute postnatal ablation of Hif-2alpha results in anemia. Proc. Natl. Acad. Sci. USA 104, 2301-2306. (Pubitemid 46391392)
10. Haase, V. H., Glickman, J. N., Socolovsky, M. and Jaenisch, R. (2001). Vascular tumors in livers with targeted inactivation of the von Hippel-Lindau tumor suppressor. Proc. Natl. Acad. Sci. USA 98, 1583-1588. (Pubitemid 32165542)
11. Hammes, H. P., Lin, J., Wagner, P., Feng, Y., Vom Hagen, F., Krzizok, T., Renner, O., Breier, G., Brownlee, M. and Deutsch, U. (2004). Angiopoietin-2 causes pericyte dropout in the normal retina: evidence for involvement in diabetic retinopathy. Diabetes 53, 1104-1110. (Pubitemid 38436625)
12. Hayreh, S. S. (2007). Neovascular glaucoma. Prog. Retin. Eye Res. 26, 470-485.
13. Hellstrom, M., Phng, L. K., Hofmann, J. J., Wallgard, E., Coultas, L., Lindblom, P., Alva, J., Nilsson, A. K., Karlsson, L., Gaiano, N. et al. (2007). Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature 445, 776-780. (Pubitemid 46279716)
14. Hu, C. J., Wang, L. Y., Chodosh, L. A., Keith, B. and Simon, M. C. (2003). Differential roles of hypoxia-inducible factor 1alpha (HIF-1alpha) and HIF-2alpha in hypoxic gene regulation. Mol. Cell. Biol. 23, 9361-9374. (Pubitemid 37499822)
15. Kapitsinou, P. P. and Haase, V. H. (2008). The VHL tumor suppressor and HIF: insights from genetic studies in mice. Cell Death Differ. 15, 650-659.
16. Kawamoto, S., Niwa, H., Tashiro, F., Sano, S., Kondoh, G., Takeda, J., Tabayashi, K. and Miyazaki, J. (2000). A novel reporter mouse strain that expresses enhanced green fluorescent protein upon Cre-mediated recombination. FEBS Lett. 470, 263-268. (Pubitemid 30169275)
17. Kubota, Y., Hirashima, M., Kishi, K., Stewart, C. L. and Suda, T. (2008). Leukemia inhibitory factor regulates microvessel density by modulating oxygen-dependent VEGF expression in mice. J. Clin. Invest. 118, 2393-2403. (Pubitemid 351949769)
18. Kubota, Y., Takubo, K., Shimizu, T., Ohno, H., Kishi, K., Shibuya, M., Saya, H. and Suda, T. (2009). M-CSF inhibition selectively targets pathological angiogenesis and lymphangiogenesis. J. Exp. Med. 206, 1089-1102.
19. Kurihara, T., Ozawa, Y., Shinoda, K., Nagai, N., Inoue, M., Oike, Y., Tsubota, K., Ishida, S. and Okano, H. (2006). Neuroprotective effects of angiotensin II type 1 receptor (AT1R) blocker, telmisartan, via modulating AT1R and AT2R signaling in retinal inflammation. Invest. Ophthalmol. Vis. Sci. 47, 5545-5552. (Pubitemid 46723808)
20. Lang, R. A. (1997). Apoptosis in mammalian eye development: lens morphogenesis, vascular regression and immune privilege. Cell Death Differ. 4, 12-20.
21. Lang, R. A. and Bishop, J. M. (1993). Macrophages are required for cell death and tissue remodeling in the developing mouse eye. Cell 74, 453-462.
22. Lobov, I. B., Rao, S., Carroll, T. J., Vallance, J. E., Ito, M., Ondr, J. K., Kurup, S., Glass, D. A., Patel, M. S., Shu, W. et al. (2005). WNT7b mediates macrophage-induced programmed cell death in patterning of the vasculature. Nature 437, 417-421. (Pubitemid 41613504)
23. Marquardt, T., Ashery-Padan, R., Andrejewski, N., Scardigli, R., Guillemot, F. and Gruss, P. (2001). Pax6 is required for the multipotent state of retinal progenitor cells. Cell 105, 43-55. (Pubitemid 32323915)
24. Maxwell, P. H., Wiesener, M. S., Chang, G. W., Clifford, S. C., Vaux, E. C., Cockman, M. E., Wykoff, C. C., Pugh, C. W., Maher, E. R. and Ratcliffe, P. J. (1999). The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399, 271-275.
25. Merkle, E. M. and Gilkeson, R. C. (2005). Remnants of fetal circulation: appearance on MDCT in adults. Am. J. Roentgenol. 185, 541-549.
26. Mitchell, C. A., Rutland, C. S., Walker, M., Nasir, M., Foss, A. J., Stewart, C., Gerhardt, H., Konerding, M. A., Risau, W. and Drexler, H. C. (2006). Unique vascular phenotypes following over-expression of individual VEGFA isoforms from the developing lens. Angiogenesis 9, 209-224.
27. Nicholson, D. H., Green, W. R. and Kenyon, K. R. (1976). Light and electron microscopic study of early lesions in angiomatosis retinae. Am. J. Ophthalmol. 82, 193-204.
28. Ohh, M., Yauch, R. L., Lonergan, K. M., Whaley, J. M., Stemmer-Rachamimov, A. O., Louis, D. N., Gavin, B. J., Kley, N., Kaelin, W. G., Jr and Iliopoulos, O. (1998). The von Hippel-Lindau tumor suppressor protein is required for proper assembly of an extracellular fibronectin matrix. Mol. Cell 1, 959-968. (Pubitemid 128379257)
29. Ozawa, Y., Nakao, K., Shimazaki, T., Takeda, J., Akira, S., Ishihara, K., Hirano, T., Oguchi, Y. and Okano, H. (2004). Downregulation of STAT3 activation is required for presumptive rod photoreceptor cells to differentiate in the postnatal retina. Mol. Cell. Neurosci. 26, 258-270. (Pubitemid 38781083)
30. Ozawa, Y., Nakao, K., Shimazaki, T., Shimmura, S., Kurihara, T., Ishida, S., Yoshimura, A., Tsubota, K. and Okano, H. (2007). SOCS3 is required to temporally fine-tune photoreceptor cell differentiation. Dev. Biol. 303, 591-600. (Pubitemid 46341283)
31. Phng, L. K., Potente, M., Leslie, J. D., Babbage, J., Nyqvist, D., Lobov, I., Ondr, J. K., Rao, S., Lang, R. A., Thurston, G. et al. (2009). Nrarp coordinates endothelial Notch and Wnt signaling to control vessel density in angiogenesis. Dev. Cell 16, 70-82.
32. Rankin, E. B., Biju, M. P., Liu, Q., Unger, T. L., Rha, J., Johnson, R. S., Simon, M. C., Keith, B. and Haase, V. H. (2007). Hypoxia-inducible factor-2 (HIF-2) regulates hepatic erythropoietin in vivo. J. Clin. Invest. 117, 1068-1077. (Pubitemid 46556763)
33. Rao, S., Lobov, I. B., Vallance, J. E., Tsujikawa, K., Shiojima, I., Akunuru, S., Walsh, K., Benjamin, L. E. and Lang, R. A. (2007). Obligatory participation of macrophages in an angiopoietin 2-mediated cell death switch. Development 134, 4449-4458.
34. Rodesch, F., Simon, P., Donner, C. and Jauniaux, E. (1992). Oxygen measurements in endometrial and trophoblastic tissues during early pregnancy. Obstet. Gynecol. 80, 283-285.
35. Ruhrberg, C., Gerhardt, H., Golding, M., Watson, R., Ioannidou, S., Fujisawa, H., Betsholtz, C. and Shima, D. T. (2002). Spatially restricted patterning cues provided by heparin-binding VEGF-A control blood vessel branching morphogenesis. Genes Dev. 16, 2684-2698.
36. Ryan, H. E., Poloni, M., McNulty, W., Elson, D., Gassmann, M., Arbeit, J. M. and Johnson, R. S. (2000). Hypoxia-inducible factor-1alpha is a positive factor in solid tumor growth. Cancer Res. 60, 4010-4015. (Pubitemid 30636574)
37. Saint-Geniez, M., Maldonado, A. E. and D'Amore, P. A. (2006). VEGF expression and receptor activation in the choroid during development and in the adult. Invest. Ophthalmol. Vis. Sci. 47, 3135-3142. (Pubitemid 351639793)
38. Saint-Geniez, M., Maharaj, A. S., Walshe, T. E., Tucker, B. A., Sekiyama, E., Kurihara, T., Darland, D. C., Young, M. J. and D'Amore, P. A. (2008). Endogenous VEGF is required for visual function: evidence for a survival role on muller cells and photoreceptors. PLoS ONE 3, e3554.
39. Sears, J. E., Hoppe, G., Ebrahem, Q. and Anand-Apte, B. (2008). Prolyl hydroxylase inhibition during hyperoxia prevents oxygen-induced retinopathy. Proc. Natl. Acad. Sci. USA 105, 19898-19903.
40. Stalmans, I., Ng, Y. S., Rohan, R., Fruttiger, M., Bouche, A., Yuce, A., Fujisawa, H., Hermans, B., Shani, M., Jansen, S. et al. (2002). Arteriolar and venular patterning in retinas of mice selectively expressing VEGF isoforms. J. Clin. Invest. 109, 327-336. (Pubitemid 34141806)
41. Tang, N., Mack, F., Haase, V. H., Simon, M. C. and Johnson, R. S. (2006). pVHL function is essential for endothelial extracellular matrix deposition. Mol. Cell. Biol. 26, 2519-2530.
42. Yu, D. Y. and Cringle, S. J. (2001). Oxygen distribution and consumption within the retina in vascularised and avascular retinas and in animal models of retinal disease. Prog. Retin. Eye Res. 20, 175-208.
43. Yun, Z., Maecker, H. L., Johnson, R. S. and Giaccia, A. J. (2002). Inhibition of PPAR gamma 2 gene expression by the HIF-1-regulated gene DEC1/Stra13: a mechanism for regulation of adipogenesis by hypoxia. Dev. Cell 2, 331-341. (Pubitemid 34266118)