Suppression of protein kinase C-ζ attenuates vascular leakage via prevention of tight junction protein decrease in diabetic retinopathy

Biochemical and Biophysical Research Communications

Volumn 444, Issue 1, 2014, Pages 63-68

  Kim, Jeong Hun ^a,b   Song, Hyun Beom ^a,b   Jun, Hyoung Oh ^a   Kim, Jin Hyoung ^a   Yu, Young Suk ^a,b   Kim, Kyu Won ^b  

^a Seoul National University Hospital   (South Korea)

^b Seoul National University   (South Korea)

Author keywords

Diabetic retinopathy; Protein kinase C ; Tight junction protein; Vascular leakage

Indexed keywords

DIABETIC RETINOPATHY; PROTEIN KINASE C-Ζ; TIGHT JUNCTION PROTEIN; VASCULAR LEAKAGE;

ANIMALS; BLOOD-RETINAL BARRIER; CAPILLARY PERMEABILITY; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC RETINOPATHY; ENDOTHELIAL CELLS; GLYCOSYLATION END PRODUCTS, ADVANCED; HUMANS; MICE; MICE, INBRED C57BL; PROTEIN KINASE C; RETINAL VESSELS; RNA, SMALL INTERFERING; TIGHT JUNCTION PROTEINS; TIGHT JUNCTIONS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84893849857     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2014.01.002     Document Type: Article

References (35)

1. D.S. Fong, L.P. Aiello, F.L. Ferris 3rd, and R. Klein Diabetic retinopathy Diabetes Care 27 2004 2540 2553 (Pubitemid 39281419)
2. B.E. Klein Overview of epidemiologic studies of diabetic retinopathy Ophthalmic Epidemiol. 14 2007 179 183 (Pubitemid 47493723)
3. A.C. Ho, I.U. Scott, S.J. Kim, G.C. Brown, M.M. Brown, M.S. Ip, and F.M. Recchia Anti-vascular endothelial growth factor pharmacotherapy for diabetic macular edema: a report by the American Academy of Ophthalmology Ophthalmology 119 2012 2179 2188
4. R. Klein, B.E. Klein, S.E. Moss, and K.J. Cruickshanks The Wisconsin Epidemiologic Study of Diabetic Retinopathy. XV. The long-term incidence of macular edema Ophthalmology 102 1995 7 16
5. H. Funatsu, H. Yamashita, T. Ikeda, T. Mimura, S. Eguchi, and S. Hori Vitreous levels of interleukin-6 and vascular endothelial growth factor are related to diabetic macular edema Ophthalmology 110 2003 1690 1696 (Pubitemid 37025424)
6. Q. Nguyen, S. Tatlipinar, S. Shah, J. Haller, E. Quinlan, J. Sung, I. Zimmer-Galler, D. Do, and P. Campochiaro Vascular endothelial growth factor is a critical stimulus for diabetic macular edema Am. J. Ophthalmol. 142 2006 961 969
7. N. Bhagat, R.A. Grigorian, A. Tutela, and M.A. Zarbin Diabetic macular edema: pathogenesis and treatment Surv. Ophthalmol. 54 2009 1 32
8. Y. Ono, S. Aoki, K. Ohnishi, T. Yasuda, K. Kawano, and Y. Tsukada Increased serum levels of advanced glycation end-products and diabetic complications Diabetes Res. Clin. Pract. 41 1998 131 137 (Pubitemid 28459016)
9. B.O. Boehm, S. Schilling, S. Rosinger, G.E. Lang, G.K. Lang, R. Kientsch-Engel, and P. Stahl Elevated serum levels of N(epsilon)-carboxymethyl- lysine, an advanced glycation end product, are associated with proliferative diabetic retinopathy and macular oedema Diabetologia 47 2004 1376 1379 (Pubitemid 39232422)
10. A. Augustin, A. Loewenstein, and B.D. Kuppermann Macular edema. General pathophysiology Dev. Ophthalmol. 47 2010 10 26
11. A. Armulik, A. Abramsson, and C. Betsholtz Endothelial/pericyte interactions Circ. Res. 97 2005 512 523 (Pubitemid 41361741)
12. J.H. Kim, J.H. Kim, H.O. Jun, Y.S. Yu, and K.W. Kim Inhibition of protein kinase C delta attenuates blood-retinal barrier breakdown in diabetic retinopathy Am. J. Pathol. 176 2010 1517 1524
13. J.H. Kim, Y.S. Yu, C.S. Cho, and K.W. Kim Blockade of angiotensin II attenuates VEGF-mediated blood-retinal barrier breakdown in diabetic retinopathy J. Cereb. Blood Flow Metab. 29 2009 621 628
14. J.H. Kim, Y.S. Yu, K.W. Kim, and J.H. Kim Impaired retinal vascular development in anencephalic human fetus Histochem. Cell Biol. 134 2010 277 284
15. N.S. Harhaj, E.A. Felinski, E.B. Wolpert, J.M. Sundstrom, T.W. Gardner, and D.A. Antonetti VEGF activation of protein kinase C stimulates occludin phosphorylation and contributes to endothelial permeability Invest. Ophthalmol. Vis. Sci. 47 2006 5106 5115 (Pubitemid 46586418)
16. L. González-Mariscal, R. Tapia, and D. Chamorro Crosstalk of tight junction components with signaling pathways Biochim. Biophys. Acta 1778 2008 729 756 (Pubitemid 351317800)
17. M. Brownlee The pathobiology of diabetic complications: a unifying mechanism Diabetes 54 2005 1615 1625 (Pubitemid 40770750)
18. H. Mellor, and P.J. Parker The extended protein kinase C superfamily Biochem. J. 332 Pt 2 1998 281 292 (Pubitemid 28271856)
19. H. Ishii, M.R. Jirousek, D. Koya, C. Takagi, P. Xia, A. Clermont, S.E. Bursell, T.S. Kern, L.M. Ballas, W.F. Heath, L.E. Stramm, E.P. Feener, and G.L. King Amelioration of vascular dysfunctions in diabetic rats by an oral PKC beta inhibitor Science 272 1996 728 731 (Pubitemid 26000279)
20. H. Haller, W. Ziegler, C. Lindschau, and F. Luft Endothelial cell tyrosine kinase receptor and G protein-coupled receptor activation involves distinct protein kinase C isoforms Arterioscler. Thromb. Vasc. Biol. 16 1996 678 686 (Pubitemid 26153113)
21. M. Wellner, C. Maasch, C. Kupprion, C. Lindschau, F. Luft, and H. Haller The proliferative effect of vascular endothelial growth factor requires protein kinase C-alpha and protein kinase C-zeta Arterioscler. Thromb. Vasc. Biol. 19 1999 178 185 (Pubitemid 29031927)
22. C. Aveleira, C.-M. Lin, S. Abcouwer, A. Ambrósio, and D. Antonetti TNF-α signals through PKCζ/NF-κB to alter the tight junction complex and increase retinal endothelial cell permeability Diabetes 59 2010 2872 2882
23. X. Li, C.N. Hahn, M. Parsons, J. Drew, M.A. Vadas, and J.R. Gamble Role of protein kinase Czeta in thrombin-induced endothelial permeability changes: inhibition by angiopoietin-1 Blood 104 2004 1716 1724 (Pubitemid 39202279)
24. P. Titchenell, C.-M. Lin, J. Keil, J. Sundstrom, C. Smith, and D. Antonetti Novel atypical PKC inhibitors prevent vascular endothelial growth factor-induced blood-retinal barrier dysfunction Biochem. J. 446 2012 455 467
25. M.E. Kleinman, K. Yamada, A. Takeda, V. Chandrasekaran, M. Nozaki, J.Z. Baffi, R.J. Albuquerque, S. Yamasaki, M. Itaya, Y. Pan, B. Appukuttan, D. Gibbs, Z. Yang, K. Kariko, B.K. Ambati, T.A. Wilgus, L.A. DiPietro, E. Sakurai, K. Zhang, J.R. Smith, E.W. Taylor, and J. Ambati Sequence- and target-independent angiogenesis suppression by siRNA via TLR3 Nature 452 2008 591 597 (Pubitemid 351483358)
26. T. Murata, T. Ishibashi, A. Khalil, Y. Hata, H. Yoshikawa, and H. Inomata Vascular endothelial growth factor plays a role in hyperpermeability of diabetic retinal vessels Ophthalmic Res. 27 1995 48 52
27. X. Xu, Q. Zhu, X. Xia, S. Zhang, Q. Gu, and D. Luo Blood-retinal barrier breakdown induced by activation of protein kinase C via vascular endothelial growth factor in streptozotocin-induced diabetic rats Curr. Eye Res. 28 2004 251 256 (Pubitemid 38491318)
28. A. Goldin, J.A. Beckman, A.M. Schmidt, and M.A. Creager Advanced glycation end products: sparking the development of diabetic vascular injury Circulation 114 2006 597 605 (Pubitemid 44199649)
29. J.Y. Park, N. Takahara, A. Gabriele, E. Chou, K. Naruse, K. Suzuma, T. Yamauchi, S.W. Ha, M. Meier, C.J. Rhodes, and G.L. King Induction of endothelin-1 expression by glucose: an effect of protein kinase C activation Diabetes 49 2000 1239 1248 (Pubitemid 30439101)
30. P.E. Spoerri, A. Afzal, S. Li Calzi, L.C. Shaw, J. Cai, H. Pan, M. Boulton, and M.B. Grant Effects of VEGFR-1, VEGFR-2, and IGF-IR hammerhead ribozymes on glucose-mediated tight junction expression in cultured human retinal endothelial cells Mol. Vis. 12 2006 32 42 (Pubitemid 43072829)
31. I. Klaassen, C.J. Van Noorden, and R.O. Schlingemann Molecular basis of the inner blood-retinal barrier and its breakdown in diabetic macular edema and other pathological conditions Prog. Retin. Eye Res. 34 2013 19 48
32. T. Murakami, T. Frey, C. Lin, and D.A. Antonetti Protein kinase cbeta phosphorylates occludin regulating tight junction trafficking in vascular endothelial growth factor-induced permeability in vivo Diabetes 61 2012 1573 1583
33. R. Stuart, and S. Nigam Regulated assembly of tight junctions by protein kinase C Proc. Nat. Acad. Sci. U.S.A. 92 1995 6072 6076
34. V. Dodane, and B. Kachar Identification of isoforms of G proteins and PKC that colocalize with tight junctions J. Membr. Biol. 149 1996 199 209 (Pubitemid 26076105)
35. R. Minshall, E. Vandenbroucke, M. Holinstat, A. Place, C. Tiruppathi, S. Vogel, G. van Nieuw Amerongen, D. Mehta, and A. Malik Role of protein kinase Czeta in thrombin-induced RhoA activation and inter-endothelial gap formation of human dermal microvessel endothelial cell monolayers Microvasc. Res. 80 2010 240 249