Sustained inflammation after pericyte depletion induces irreversible blood-retina barrier breakdown

JCI Insight

Volumn 2, Issue 3, 2017, Pages

  Ogura, Shuntaro ^a   Kurata, Kaori ^a   Hattori, Yuki ^b   Takase, Hiroshi ^a   Ishiguro Oonuma, Toshina ^c   Hwang, Yoonha ^d   Ahn, Soyeon ^d   Park, Inwon ^d   Ikeda, Wataru ^e   Kusuhara, Sentaro ^f   Fukushima, Yoko ^g   Nara, Hiromi ^h   Sakai, Hideto ^h   Fujiwara, Takashi ⁱ   Matsushita, Jun ^j   Ema, Masatsugu ^j   Hirashima, Masanori ^f   Minami, Takashi ^k   Shibuya, Masabumi ^l   Takakura, Nobuyuki ^m   Kim, Pilhan ^d   Miyata, Takaki ^b   Ogura, Yuichiro ^a   Uemura, Akiyoshi ^a   more..

^a NAGOYA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICAL SCIENCES   (Japan)

^b NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c IWATE UNIVERSITY   (Japan)

^d Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^e Kobe MI R and D Center   (Japan)

^f KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^g OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^h ASTELLAS PHARMA INC   (Japan)

ⁱ Kure University   (Japan)

^j SHIGA UNIVERSITY OF MEDICAL SCIENCE   (Japan)

^k KUMAMOTO UNIVERSITY   (Japan)

^l JOBU UNIVERSITY   (Japan)

^m OSAKA UNIVERSITY   (Japan)

more..

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85019656342     PISSN: None     EISSN: 23793708     Source Type: Journal    
DOI: 10.1172/jci.insight.90905     Document Type: Article

References (58)

1. Armulik A, Genové G, Betsholtz C. Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev Cell. 2011;21(2):193–215.
2. Daneman R, Prat A. The blood-brain barrier. Cold Spring Harb Perspect Biol. 2015;7(1):a020412.
3. Zhao Z, Nelson AR, Betsholtz C, Zlokovic BV. Establishment and Dysfunction of the Blood-Brain Barrier. Cell. 2015;163(5):1064–1078.
4. Cogan DG, Toussaint D, Kuwabara T. Retinal vascular patterns. IV. Diabetic retinopathy. Arch Ophthalmol. 1961;66:366–378.
5. Antonetti DA, Klein R, Gardner TW. Diabetic retinopathy. N Engl J Med. 2012;366(13):1227–1239.
6. Uemura A, Kusuhara S, Katsuta H, Nishikawa S. Angiogenesis in the mouse retina: a model system for experimental manipulation. Exp Cell Res. 2006;312(5):676–683.
7. Uemura A, et al. Recombinant angiopoietin-1 restores higher-order architecture of growing blood vessels in mice in the absence of mural cells. J Clin Invest. 2002;110(11):1619–1628.
8. Diabetic Retinopathy Clinical Research Network, et al. Randomized trial evaluating ranibizumab plus prompt or deferred laser or triamcinolone plus prompt laser for diabetic macular edema. Ophthalmology. 2010;117(6):1064–1077.e35.
9. Koch S, Claesson-Welsh L. Signal transduction by vascular endothelial growth factor receptors. Cold Spring Harb Perspect Med. 2012;2(7):a006502.
10. Dejana E, Tournier-Lasserve E, Weinstein BM. The control of vascular integrity by endothelial cell junctions: molecular basis and pathological implications. Dev Cell. 2009;16(2):209–221.
11. Shibuya M. VEGFR and type-V RTK activation and signaling. Cold Spring Harb Perspect Biol. 2013;5(10):a009092.
12. Aiello LP, et al. Vascular endothelial growth factor in ocular fluid of patients with diabetic retinopathy and other retinal disorders. N Engl J Med. 1994;331(22):1480–1487.
13. Khaliq A, et al. Increased expression of placenta growth factor in proliferative diabetic retinopathy. Lab Invest. 1998;78(1):109–116.
14. McAuley AK, et al. Vitreous biomarkers in diabetic retinopathy: a systematic review and meta-analysis. J Diabetes Complicat. 2014;28(3):419–425.
15. Campochiaro PA. Molecular pathogenesis of retinal and choroidal vascular diseases. Prog Retin Eye Res. 2015;49:67–81.
16. Augustin HG, Koh GY, Thurston G, Alitalo K. Control of vascular morphogenesis and homeostasis through the angiopoietin-Tie system. Nat Rev Mol Cell Biol. 2009;10(3):165–177.
17. Mandriota SJ, Pepper MS. Regulation of angiopoietin-2 mRNA levels in bovine microvascular endothelial cells by cytokines and hypoxia. Circ Res. 1998;83(8):852–859.
18. Oh H, Takagi H, Suzuma K, Otani A, Matsumura M, Honda Y. Hypoxia and vascular endothelial growth factor selectively upregulate angiopoietin-2 in bovine microvascular endothelial cells. J Biol Chem. 1999;274(22):15732–15739.
19. Daly C, et al. Angiopoietin-1 modulates endothelial cell function and gene expression via the transcription factor FKHR (FOXO1). Genes Dev. 2004;18(9):1060–1071.
20. Kim I, Kim JH, Moon SO, Kwak HJ, Kim NG, Koh GY. Angiopoietin-2 at high concentration can enhance endothelial cell survival through the phosphatidylinositol 3′-kinase/Akt signal transduction pathway. Oncogene. 2000;19(39):4549–4552.
21. Daly C, et al. Angiopoietin-2 functions as an autocrine protective factor in stressed endothelial cells. Proc Natl Acad Sci U S A. 2006;103(42):15491–15496.
22. Kim M, et al. Opposing actions of angiopoietin-2 on Tie2 signaling and FOXO1 activation. J Clin Invest. 2016;126(9):3511–3525.
23. Korhonen EA, et al. Tie1 controls angiopoietin function in vascular remodeling and inflammation. J Clin Invest. 2016;126(9):3495–3510.
24. Yabkowitz R, Meyer S, Black T, Elliott G, Merewether LA, Yamane HK. Inflammatory cytokines and vascular endothelial growth factor stimulate the release of soluble tie receptor from human endothelial cells via metalloprotease activation. Blood. 1999;93(6):1969–1979.
25. Watanabe D, et al. Vitreous levels of angiopoietin 2 and vascular endothelial growth factor in patients with proliferative diabetic retinopathy. Am J Ophthalmol. 2005;139(3):476–481.
26. Gerhardt H, et al. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol. 2003;161(6):1163–1177.
27. Vestweber D. How leukocytes cross the vascular endothelium. Nat Rev Immunol. 2015;15(11):692–704.
28. Inai T, et al. Inhibition of vascular endothelial growth factor (VEGF) signaling in cancer causes loss of endothelial fenestrations, regression of tumor vessels, and appearance of basement membrane ghosts. Am J Pathol. 2004;165(1):35–52.
29. Motoike T, et al. Universal GFP reporter for the study of vascular development. Genesis. 2000;28(2):75–81.
30. Kusuhara S, et al. Arhgef15 promotes retinal angiogenesis by mediating VEGF-induced Cdc42 activation and potentiating RhoJ inactivation in endothelial cells. PLoS One. 2012;7(9):e45858.
31. Minami T, et al. The Down syndrome critical region gene 1 short variant promoters direct vascular bed-specific gene expression during inflammation in mice. J Clin Invest. 2009;119(8):2257–2270.
32. Minami T. Calcineurin-NFAT activation and DSCR-1 auto-inhibitory loop: how is homoeostasis regulated? J Biochem. 2014;155(4):217–226.
33. Minami T, et al. The calcineurin-NFAT-angiopoietin-2 signaling axis in lung endothelium is critical for the establishment of lung metastases. Cell Rep. 2013;4(4):709–723.
34. Miyamoto K, et al. Prevention of leukostasis and vascular leakage in streptozotocin-induced diabetic retinopathy via intercellular adhesion molecule-1 inhibition. Proc Natl Acad Sci U S A. 1999;96(19):10836–10841.
35. Sedgwick JD, Schwender S, Imrich H, Dörries R, Butcher GW, ter Meulen V. Isolation and direct characterization of resident microglial cells from the normal and inflamed central nervous system. Proc Natl Acad Sci U S A. 1991;88(16):7438–7442.
36. Jung S, et al. Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol Cell Biol. 2000;20(11):4106–4114.
37. Okabe K, et al. Neurons limit angiogenesis by titrating VEGF in retina. Cell. 2014;159(3):584–596.
38. Nakayama M, et al. Spatial regulation of VEGF receptor endocytosis in angiogenesis. Nat Cell Biol. 2013;15(3):249–260.
39. Ishitobi H, et al. Flk1-GFP BAC Tg mice: an animal model for the study of blood vessel development. Exp Anim. 2010;59(5):615–622.
40. Matsumoto K, et al. Study of normal and pathological blood vessel morphogenesis in Flt1-tdsRed BAC Tg mice. Genesis. 2012;50(7):561–571.
41. Hiratsuka S, Minowa O, Kuno J, Noda T, Shibuya M. Flt-1 lacking the tyrosine kinase domain is sufficient for normal development and angiogenesis in mice. Proc Natl Acad Sci U S A. 1998;95(16):9349–9354.
42. Holash J, et al. VEGF-Trap: a VEGF blocker with potent antitumor effects. Proc Natl Acad Sci U S A. 2002;99(17):11393–11398.
43. Felcht M, et al. Angiopoietin-2 differentially regulates angiogenesis through TIE2 and integrin signaling. J Clin Invest. 2012;122(6):1991–2005.
44. Baer C, Squadrito ML, Iruela-Arispe ML, De Palma M. Reciprocal interactions between endothelial cells and macrophages in angiogenic vascular niches. Exp Cell Res. 2013;319(11):1626–1634.
45. Han S, et al. Amelioration of sepsis by TIE2 activation-induced vascular protection. Sci Transl Med. 2016;8(335):335ra55.
46. Weinl C, et al. Endothelial SRF/MRTF ablation causes vascular disease phenotypes in murine retinae. J Clin Invest. 2013;123(5):2193–2206.
47. Franco CA, et al. SRF selectively controls tip cell invasive behavior in angiogenesis. Development. 2013;140(11):2321–2333.
48. Adamis AP, Berman AJ. Immunological mechanisms in the pathogenesis of diabetic retinopathy. Semin Immunopathol. 2008;30(2):65–84.
49. Betsholtz C, Lindblom P, Bjarnegard M, Enge M, Gerhardt H, Lindahl P. Role of platelet-derived growth factor in mesangium development and vasculopathies: lessons from platelet-derived growth factor and platelet-derived growth factor receptor mutations in mice. Curr Opin Nephrol Hypertens. 2004;13(1):45–52.
50. Yang WJ, Hu J, Uemura A, Tetzlaff F, Augustin HG, Fischer A. Semaphorin-3C signals through Neuropilin-1 and PlexinD1 receptors to inhibit pathological angiogenesis. EMBO Mol Med. 2015;7(10):1267–1284.
51. Hanaichi T, Sato T, Iwamoto T, Malavasi-Yamashiro J, Hoshino M, Mizuno N. A stable lead by modification of Sato’s method. J Electron Microsc (Tokyo). 1986;35(3):304–306.
52. Fujiwara T, Uehara Y. The cytoarchitecture of the medial layer in rat thoracic aorta: a scanning electron-microscopic study. Cell Tissue Res. 1992;270(1):165–172.
53. Lee JY, et al. In vivo fluorescence retinal imaging following AAV2-mediated gene delivery in the rat retina. Invest Ophthalmol Vis Sci. 2016;57(7):3390–3396.
54. Guizar-Sicairos M, Thurman ST, Fienup JR. Efficient subpixel image registration algorithms. Opt Lett. 2008;33(2):156–158.
55. Tsujino K, et al. Establishment of TSH β real-time monitoring system in mammalian photoperiodism. Genes Cells. 2013;18(7):575–588.
56. + populations in ES cell differentiation culture identifies genes involved in differentiation of mesoderm and mesenchyme including ARID3b that is essential for development of embryonic mesenchymal cells. Dev Biol. 2006;293(1):25–37.
57. Li C, Wong WH. Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc Natl Acad Sci U S A. 2001;98(1):31–36.
58. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A. 2001;98(9):5116–5121.