Neurovascular crosstalk between interneurons and capillaries is required for vision

Journal of Clinical Investigation

Volumn 125, Issue 6, 2015, Pages 2335-2346

  Usui, Yoshihiko ^a   Westenskow, Peter D ^a,b   Kurihara, Toshihide ^a   Aguilar, Edith ^a   Sakimoto, Susumu ^a   Paris, Liliana P ^a   Wittgrove, Carli ^a   Feitelberg, Daniel ^a   Friedlander, Mollie S H ^a   Moreno, Stacey K ^a   Dorrell, Michael I ^b   Friedlander, Martin ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b Division of Basic Science   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIPHTHERIA TOXIN; MESSENGER RNA; MICROTUBULE ASSOCIATED PROTEIN 2; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR 1A CRE; UNCLASSIFIED DRUG; VASCULOTROPIN A;

ALLELE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CAPILLARY; CONTROLLED STUDY; EXTRACELLULAR MATRIX; GENE EXPRESSION PROFILING; GENETIC MODEL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INTERNEURON; MOUSE; NERVE FIBER; NEUROFILAMENT; NONHUMAN; PRIORITY JOURNAL; RETINA AMACRINE CELL; RETINA HORIZONTAL NERVE CELL; RETINA NERVE CELL; RETINAL INTERNEURON; TUNEL ASSAY; UPREGULATION; VISION; ANIMAL; CYTOLOGY; METABOLISM; PHOTORECEPTOR CELL; PHYSIOLOGY; RETINA BLOOD VESSEL; TRANSGENIC MOUSE;

AMACRINE CELLS; ANIMALS; CAPILLARIES; MICE; MICE, TRANSGENIC; PHOTORECEPTOR CELLS, VERTEBRATE; RETINAL HORIZONTAL CELLS; RETINAL VESSELS; VISION, OCULAR;

EID: 84930408306     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI80297     Document Type: Article

References (42)

1. Storkebaum E, Quaegebeur A, Vikkula M, Carmeliet P. Cerebrovascular disorders: Molecular insights and therapeutic opportunities. Nat Neurosci. 2011;14(11): 1390-1397.
2. Stanimirovic DB, Friedman A. Pathophysiology of the neurovascular unit: Disease cause or consequence? J Cereb Blood Flow Metab. 2012;32(7): 1207-1221.
3. Sapieha P. Eyeing central neurons in vascular growth and reparative angiogenesis. Blood. 2012;120(11): 2182-2194.
4. Fruttiger M. Development of the retinal vasculature. Angiogenesis. 2007;10(2): 77-88.
5. Caprara C, Thiersch M, Lange C, Joly S, Samardzija M, Grimm C. HIF1A is essential for the development of the intermediate plexus of the retinal vasculature. Invest Ophthalmol Vis Sci. 2011;52(5): 2109-2117.
6. Grimm C, et al. Neuroprotection by hypoxic preconditioning: HIF-1 and erythropoietin protect from retinal degeneration. Semin Cell Dev Biol. 2005;16(4-5): 531-538.
7. Yu DY, Yu PK, Cringle SJ, Kang MH, Su EN. Functional and morphological characteristics of the retinal and choroidal vasculature. Prog Retin Eye Res. 2014;40: 53-93.
8. Nakamura-Ishizu A, et al. The formation of an angiogenic astrocyte template is regulated by the neuroretina in a HIF-1-dependent manner. Dev Biol. 2012;363(1): 106-114.
9. Dorrell MI, Aguilar E, Scheppke L, Barnett FH, Friedlander M. Combination angiostatic therapy completely inhibits ocular and tumor angiogenesis. Proc Natl Acad Sci U S A. 2007;104(3): 967-972.
10. Stone J, Dreher Z. Relationship between astrocytes, ganglion cells and vasculature of the retina. J Comp Neurol. 1987;255(1): 35-49.
11. Ma Y, et al. Quantitative analysis of retinal vessel attenuation in eyes with retinitis pigmentosa. Invest Ophthalmol Vis Sci. 2012;53(7): 4306-4314.
12. Stahl A, et al. The mouse retina as an angiogenesis model. Invest Ophthalmol Vis Sci. 2010;51(6): 2813-2826.
13. Fujitani Y, et al. Ptf1a determines horizontal and amacrine cell fates during mouse retinal development. Development. 2006;133(22): 4439-4450.
14. Muzumdar MD, Tasic B, Miyamichi K, Li L, Luo L. A global double-fluorescent Cre reporter mouse. Genesis. 2007;45(9): 593-605.
15. Chien CL, Liem RK. The neuronal intermediate filament, alpha-internexin is transiently expressed in amacrine cells in the developing mouse retina. Exp Eye Res. 1995;61(6): 749-756.
16. Gerber HP, et al. VEGF is required for growth and survival in neonatal mice. Development. 1999;126(6): 1149-1159.
17. Okabe K, et al. Neurons limit angiogenesis by titrating VEGF in retina. Cell. 2014;159(3): 584-596.
18. Cringle SJ, Yu PK, Su EN, Yu DY. Oxygen distribution and consumption in the developing rat retina. Invest Ophthalmol Vis Sci. 2006;47(9): 4072-4076.
19. Stone J, et al. Development of retinal vasculature is mediated by hypoxia-induced vascular endothelial growth factor (VEGF) expression by neuroglia. J Neurosci. 1995;15(7): 4738-4747.
20. Bai Y, et al. Muller cell-derived VEGF is a significant contributor to retinal neovascularization. J Pathol. 2009;219(4): 446-454.
21. Park HY, Kim JH, Park CK. Neuronal cell death in the inner retina and the influence of vascular endothelial growth factor inhibition in a diabetic rat model. Am J Pathol. 2014;184(6): 1752-1762.
22. Grunwald JE, et al. Risk of geographic atrophy in the comparison of age-related macular degeneration treatments trials. Ophthalmology. 2014;121(1): 150-161.
23. Kurihara T, Westenskow PD, Bravo S, Aguilar E, Friedlander M. Targeted deletion of Vegfa in adult mice induces vision loss. J Clin Invest. 2012;122(11): 4213-4217.
24. Saint-Geniez M, Kurihara T, Sekiyama E, Maldonado AE, D'Amore PA. An essential role for RPE-derived soluble VEGF in the maintenance of the choriocapillaris. Proc Natl Acad Sci U S A. 2009;106(44): 18751-18756.
25. Vinores SA, et al. Blood-retinal barrier breakdown in retinitis pigmentosa: Light and electron microscopic immunolocalization. Histol Histopathol. 1995;10(4): 913-923.
26. Klaassen I, Van Noorden CJ, Schlingemann RO. Molecular basis of the inner blood-retinal barrier and its breakdown in diabetic macular edema and other pathological conditions. Prog Retin Eye Res. 2013;34: 19-48.
27. Stem MS, Gardner TW. Neurodegeneration in the pathogenesis of diabetic retinopathy: Molecular mechanisms and therapeutic implications. Curr Med Chem. 2013;20(26): 3241-3250.
28. Barber AJ, Lieth E, Khin SA, Antonetti DA, Buchanan AG, Gardner TW. Neural apoptosis in the retina during experimental and human diabetes. Early onset and effect of insulin. J Clin Invest. 1998;102(4): 783-791.
29. Otani A, et al. Rescue of retinal degeneration by intravitreally injected adult bone marrow-derived lineage-negative hematopoietic stem cells. J Clin Invest. 2004;114(6): 765-774.
30. Kawaguchi Y, Cooper B, Gannon M, Ray M, MacDonald RJ, Wright CV. The role of the transcriptional regulator Ptf1a in converting intestinal to pancreatic progenitors. Nat Genet. 2002;32(1): 128-134.
31. Haase VH, Glickman JN, Socolovsky M, Jaenisch R. Vascular tumors in livers with targeted inactivation of the von Hippel-Lindau tumor suppressor. Proc Natl Acad Sci U S A. 2001;98(4): 1583-1588.
32. Ryan HE, et al. Hypoxia-inducible factor-1alpha is a positive factor in solid tumor growth. Cancer Res. 2000;60(15): 4010-4015.
33. Gruber M, Hu CJ, Johnson RS, Brown EJ, Keith B, Simon MC. Acute postnatal ablation of Hif-2alpha results in anemia. Proc Natl Acad Sci U S A. 2007;104(7): 2301-2306.
34. Buch T, et al. A Cre-inducible diphtheria toxin receptor mediates cell lineage ablation after toxin administration. Nat Methods. 2005;2(6): 419-426.
35. Madisen L, et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat Neurosci. 2010;13(1): 133-140.
36. Westenskow PD, et al. Ras pathway inhibition prevents neovascularization by repressing endothelial cell sprouting. J Clin Invest. 2013;123(11): 4900-4908.
37. Kurihara T, et al. von Hippel-Lindau protein regulates transition from the fetal to the adult circulatory system in retina. Development. 2010;137(9): 1563-1571.
38. Alvarez-Bolado G, Zhou X, Voss AK, Thomas T, Gruss P. Winged helix transcription factor Foxb1 is essential for access of mammillothalamic axons to the thalamus. Development. 2000;127(5): 1029-1038.
39. Kubota Y, et al. M-CSF inhibition selectively targets pathological angiogenesis and lymphangiogenesis. J Exp Med. 2009;206(5): 1089-1102.
40. Zhang L, et al. Different effects of glucose starvation on expression and stability of VEGF mRNA isoforms in murine ovarian cancer cells. Biochem Biophys Res Commun. 2002;292(4): 860-868.
41. Murakami Y, et al. Receptor interacting protein kinase mediates necrotic cone but not rod cell death in a mouse model of inherited degeneration. Proc Natl Acad Sci U S A. 2012;109(36): 14598-14603.
42. Prusky GT, Alam NM, Beekman S, Douglas RM. Rapid quantification of adult and developing mouse spatial vision using a virtual optomotor system. Invest Ophthalmol Vis Sci. 2004;45(12): 4611-4616.