Microglia/macrophages migrate through retinal epithelium barrier by a transcellular route in diabetic retinopathy: Role of PKCζ in the Goto Kakizaki rat model

American Journal of Pathology

Volumn 179, Issue 2, 2011, Pages 942-953

  Omri, Samy ^a   Behar Cohen, Francine ^a,b   De Kozak, Yvonne ^a   Sennlaub, Florian ^a   Mafra Verissimo, Lourena ^c   Jonet, Laurent ^a   Savoldelli, Michle ^a,b   Omri, Boubaker ^a   Crisanti, Patricia ^a  

^a CENTRE DE RECHERCHE DES CORDELIERS   (France)

^b HÔTEL DIEU   (France)

^c UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN 1; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; PROTEIN KINASE C ZETA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ADHESION; CELL VACUOLE; CHOROID; CONTROLLED STUDY; DIABETIC RETINOPATHY; GOTO KAKIZAKI RAT; HYPERGLYCEMIA; IMMUNOHISTOCHEMISTRY; INFLAMMATORY CELL; MACROPHAGE; MACROPHAGE MIGRATION; MICROGLIA; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PHOTORECEPTOR OUTER SEGMENT; PIGMENT EPITHELIUM; PRIORITY JOURNAL; RAT; TRANSCELLULAR CELL MIGRATION;

ANIMALS; BLOOD GLUCOSE; CELL MOVEMENT; DIABETIC RETINOPATHY; EPITHELIAL CELLS; INFLAMMATION; INTERCELLULAR ADHESION MOLECULE-1; LYMPHOCYTES; MACROPHAGES; MICROGLIA; MICROSCOPY, CONFOCAL; PROTEIN KINASE C; RATS; RATS, WISTAR; RETINA;

EID: 80052430852     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2011.04.018     Document Type: Article

References (49)

1. T.A. Ciulla, A.G. Amador, and B. Zinman Diabetic retinopathy and diabetic macular edema: pathophysiology, screening, and novel therapies Diabetes Care 26 2003 2653 2664 (Pubitemid 37055447)
2. T.W. Gardner, and D.A. Antonetti Novel potential mechanisms for diabetic macular edema: leveraging new investigational approaches Curr Diab Rep 8 2008 263 269
3. N. Miyamoto, Y. de Kozak, N. Normand, Y. Courtois, J.C. Jeanny, D. Benezra, and F. Behar-Cohen PlGF-1 and VEGFR-1 pathway regulation of the external epithelial hemato-ocular barrier A model for retinal edema Ophthalmic Res 40 2008 203 207 (Pubitemid 351562904)
4. K.E. Wellen, and G.S. Hotamisligil Inflammation, stress, and diabetes J Clin Invest 115 2005 1111 1119 (Pubitemid 40629025)
5. H. Xu, M. Chen, and J.V. Forrester Para-inflammation in the aging retina Prog Retin Eye Res 28 2009 348 368
6. R. Simo, M. Villarroel, L. Corraliza, C. Hernandez, and M. Garcia-Ramirez The retinal pigment epithelium: something more than a constituent of the blood-retinal barrierimplications for the pathogenesis of diabetic retinopathy J Biomed Biotechnol 2010 2010 190724 10.1155/2010/190724
7. W.F. Hickey, and H. Kimura Perivascular microglial cells of the CNS are bone marrow-derived and present antigen in vivo Science 239 1988 290 292 (Pubitemid 18061496)
8. V.H. Perry, and S. Gordon Macrophages and microglia in the nervous system Trends Neurosci 11 1988 273 277
9. W.J. Streit, M.B. Graeber, and G.W. Kreutzberg Functional plasticity of microglia: a review Glia 1 1988 301 307
10. H. Lassmann, M. Schmied, K. Vass, and W.F. Hickey Bone marrow derived elements and resident microglia in brain inflammation Glia 7 1993 19 24
11. E.A. Ling, and W.C. Wong The origin and nature of ramified and amoeboid microglia: a historical review and current concepts Glia 7 1993 9 18
12. E.A. Ling Monocytic origin of ramified microglia in the corpus callosum in postnatal rat Neuropathol Appl Neurobiol 20 1994 182 183
13. X.X. Zeng, Y.K. Ng, and E.A. Ling Neuronal and microglial response in the retina of streptozotocin-induced diabetic rats Vis Neurosci 17 2000 463 471
14. H.Y. Zeng, W.R. Green, and M.O. Tso Microglial activation in human diabetic retinopathy Arch Ophthalmol 126 2008 227 232 (Pubitemid 351240852)
15. C. Combadiere, C. Feumi, W. Raoul, N. Keller, M. Rodero, A. Pezard, S. Lavalette, M. Houssier, L. Jonet, E. Picard, P. Debre, M. Sirinyan, P. Deterre, T. Ferroukhi, S.Y. Cohen, D. Chauvaud, J.C. Jeanny, S. Chemtob, F. Behar-Cohen, and F. Sennlaub CX3CR1-dependent subretinal microglia cell accumulation is associated with cardinal features of age-related macular degeneration J Clin Invest 117 2007 2920 2928 (Pubitemid 47529622)
16. H. Xu, M. Chen, A. Manivannan, N. Lois, and J.V. Forrester Age-dependent accumulation of lipofuscin in perivascular and subretinal microglia in experimental mice Aging Cell 7 2008 58 68
17. A.D. Meleth, E. Agron, C.C. Chan, G.F. Reed, K. Arora, G. Byrnes, K.G. Csaky, F.L. Ferris 3rd, and E.Y. Chew Serum inflammatory markers in diabetic retinopathy Invest Ophthalmol Vis Sci 46 2005 4295 4301 (Pubitemid 44264635)
18. D. Gaucher, J.A. Chiappore, M. Paques, M. Simonutti, C. Boitard, J.A. Sahel, P. Massin, and S. Picaud Microglial changes occur without neural cell death in diabetic retinopathy Vision Res 47 2007 612 623 (Pubitemid 46242159)
19. T.S. Kern Contributions of inflammatory processes to the development of the early stages of diabetic retinopathy Exp Diabetes Res 2007 2007 95103
20. H. Xu, M. Chen, E.J. Mayer, J.V. Forrester, and A.D. Dick Turnover of resident retinal microglia in the normal adult mouse Glia 55 2007 1189 1198 (Pubitemid 47204210)
21. W. Ma, L. Zhao, A.M. Fontainhas, R.N. Fariss, and W.T. Wong Microglia in the mouse retina alter the structure and function of retinal pigmented epithelial cells: a potential cellular interaction relevant to AMD PLoS One 4 2009 e7945
22. J.K. Krady, A. Basu, C.M. Allen, Y. Xu, K.F. LaNoue, T.W. Gardner, and S.W. Levison Minocycline reduces proinflammatory cytokine expression, microglial activation, and caspase-3 activation in a rodent model of diabetic retinopathy Diabetes 54 2005 1559 1565 (Pubitemid 40586690)
23. J. Millan, L. Hewlett, M. Glyn, D. Toomre, P. Clark, and A.J. Ridley Lymphocyte transcellular migration occurs through recruitment of endothelial ICAM-1 to caveola- and F-actin-rich domains Nat Cell Biol 8 2006 113 123
24. C.V. Carman, and T.A. Springer A transmigratory cup in leukocyte diapedesis both through individual vascular endothelial cells and between them J Cell Biol 167 2004 377 388 (Pubitemid 39435079)
25. L. Yang, R.M. Froio, T.E. Sciuto, A.M. Dvorak, R. Alon, and F.W. Luscinskas ICAM-1 regulates neutrophil adhesion and transcellular migration of TNF-alpha-activated vascular endothelium under flow Blood 106 2005 584 592 (Pubitemid 40981255)
26. S. Marmon, J. Hinchey, P. Oh, M. Cammer, C.J. de Almeida, L. Gunther, C.S. Raine, and M.P. Lisanti Caveolin-1 expression determines the route of neutrophil extravasation through skin microvasculature Am J Pathol 174 2009 684 692
27. Y. de Kozak, B. Omri, J.R. Smith, M.C. Naud, B. Thillaye-Goldenberg, and P. Crisanti Protein kinase Czeta (PKCzeta) regulates ocular inflammation and apoptosis in endotoxin-induced uveitis (EIU): signaling molecules involved in EIU resolution by PKCzeta inhibitor and interleukin-13 Am J Pathol 170 2007 1241 1257 (Pubitemid 47339332)
28. A. Banan, L. Zhang, J.Z. Fields, A. Farhadi, D.A. Talmage, and A. Keshavarzian PKC-zeta prevents oxidant-induced iNOS upregulation and protects the microtubules and gut barrier integrity Am J Physiol Gastrointest Liver Physiol 283 2002 G909 G922
29. C.W. Park, J.H. Kim, J.H. Lee, Y.S. Kim, H.J. Ahn, Y.S. Shin, S.Y. Kim, E.J. Choi, Y.S. Chang, and B.K. Bang High glucose-induced intercellular adhesion molecule-1 (ICAM-1) expression through an osmotic effect in rat mesangial cells is PKC-NF-kappa B-dependent Diabetologia 43 2000 1544 1553 (Pubitemid 32734862)
30. Y. Du, V.P. Sarthy, and T.S. Kern Interaction between NO and COX pathways in retinal cells exposed to elevated glucose and retina of diabetic rats Am J Physiol Regul Integr Comp Physiol 287 2004 R735 R741
31. A.M. Abu El-Asrar, S. Desmet, A. Meersschaert, L. Dralands, L. Missotten, and K. Geboes Expression of the inducible isoform of nitric oxide synthase in the retinas of human subjects with diabetes mellitus Am J Ophthalmol 132 2001 551 556 (Pubitemid 32904579)
32. Y. Du, M.A. Smith, C.M. Miller, and T.S. Kern Diabetes-induced nitrative stress in the retina, and correction by aminoguanidine J Neurochem 80 2002 771 779 (Pubitemid 34809229)
33. R.A. Kowluru, R.L. Engerman, and T.S. Kern Abnormalities of retinal metabolism in diabetes or experimental galactosemia VIII Prevention by aminoguanidine Curr Eye Res 21 2000 814 819 (Pubitemid 32099432)
34. R.A. Kowluru Retinal metabolic abnormalities in diabetic mouse: comparison with diabetic rat Curr Eye Res 24 2002 123 128 (Pubitemid 34775530)
35. R.A. Kowluru Effect of reinstitution of good glycemic control on retinal oxidative stress and nitrative stress in diabetic rats Diabetes 52 2003 818 823 (Pubitemid 36323591)
36. E. Dejana The transcellular railway: insights into leukocyte diapedesis Nat Cell Biol 8 2006 105 107
37. A. Rahman, and F. Fazal Hug tightly and say goodbye: role of endothelial ICAM-1 in leukocyte transmigration Antioxid Redox Signal 11 2009 823 839
38. S. Camelo, L. Lajavardi, A. Bochot, B. Goldenberg, M.C. Naud, E. Fattal, F. Behar-Cohen, and Y. de Kozak Ocular and systemic bio-distribution of rhodamine-conjugated liposomes loaded with VIP injected into the vitreous of Lewis rats Mol Vis 13 2007 2263 2274 (Pubitemid 350268733)
39. N. Oka, M. Yamamoto, C. Schwencke, J. Kawabe, T. Ebina, S. Ohno, J. Couet, M.P. Lisanti, and Y. Ishikawa Caveolin interaction with protein kinase C Isoenzyme-dependent regulation of kinase activity by the caveolin scaffolding domain peptide J Biol Chem 272 1997 33416 33421 (Pubitemid 28023695)
40. A.L. Wang, A.C. Yu, Q.H. He, X. Zhu, and M.O. Tso AGEs mediated expression and secretion of TNF alpha in rat retinal microglia Exp Eye Res 84 2007 905 913 (Pubitemid 46613882)
41. E. Rungger-Brandle, A.A. Dosso, and P.M. Leuenberger Glial reactivity, an early feature of diabetic retinopathy Invest Ophthalmol Vis Sci 41 2000 1971 1980 (Pubitemid 30354375)
42. Li J, Jin HB, Sun YM, Su Y, Wang LF: KB-R7943 inhibits high glucose-induced endothelial ICAM-1 expression and monocyte-endothelial adhesion. Biochem Biophys Res Commun 392:516519
43. Hirano Y, Sakurai E, Matsubara A, Ogura Y: Suppression of ICAM-1 in retinal and choroidal endothelial cells by plasmid small-interfering RNAs in vivo. Invest Ophthalmol Vis Sci 51:508515
44. S. Marmon, J. Hinchey, C.S. Raine, and M.P. Lisanti Chemokine transport and leukocyte extravasation through dermal microvasculature in the absence of caveolae J Dermatol Sci 53 2009 225 228
45. A. Mantovani, A. Sica, S. Sozzani, P. Allavena, A. Vecchi, and M. Locati The chemokine system in diverse forms of macrophage activation and polarization Trends Immunol 25 2004 677 686 (Pubitemid 39457982)
46. S. Gopalakrishnan, M.A. Hallett, S.J. Atkinson, and J.A. Marrs aPKC-PAR complex dysfunction and tight junction disassembly in renal epithelial cells during ATP depletion Am J Physiol Cell Physiol 292 2007 C1094 C1102
47. S. Etienne-Manneville, and A. Hall Cell polarity: par6, aPKC and cytoskeletal crosstalk Curr Opin Cell Biol 15 2003 67 72 (Pubitemid 36044717)
48. T.E. Fox, K.L. Houck, S.M. O'Neill, M. Nagarajan, T.C. Stover, P.T. Pomianowski, O. Unal, J.K. Yun, S.J. Naides, and M. Kester Ceramide recruits and activates protein kinase C zeta (PKC zeta) within structured membrane microdomains J Biol Chem 282 2007 12450 12457 (Pubitemid 47100622)
49. Aveleira CA, Lin CM, Abcouwer SF, Ambrosio AF, Antonetti DA: TNF-alpha signals through PKCzeta/NF-kappaB to alter the tight junction complex and increase retinal endothelial cell permeability. Diabetes 59:28722882