Insulin signaling in retinal neurons is regulated within cholesterol-enriched membrane microdomains

American Journal of Physiology - Endocrinology and Metabolism

Volumn 300, Issue 3, 2011, Pages

  Fox, Todd E ^a   Young, Megan M ^a   Pedersen, Michelle M ^a   Giambuzzi Tussey, Sarah ^a   Kester, Mark ^a   Gardner, Thomas W ^b  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Akt; Diabetes; Diabetic retinopathy; Protein kinase C

Indexed keywords

CHOLESTEROL; INSULIN; INSULIN RECEPTOR SUBSTRATE 2; PHORBOL ESTER; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B;

ANIMAL CELL; ARTICLE; BLOOD VESSEL PERMEABILITY; CELL SURVIVAL; CONTROLLED STUDY; DIABETIC RETINOPATHY; IMMUNOPRECIPITATION; INSULIN RESISTANCE; LIPID RAFT; NERVE CELL NECROSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RETINA NERVE CELL; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

BLOTTING, WESTERN; CELL LINE; CHOLESTEROL; DIABETIC RETINOPATHY; ENZYME ACTIVATION; HUMANS; INSULIN; LIPID METABOLISM; MEMBRANE MICRODOMAINS; ONCOGENE PROTEIN V-AKT; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN KINASE C; RETINAL NEURONS; SIGNAL TRANSDUCTION; SUBCELLULAR FRACTIONS;

EID: 79952131184     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00641.2010     Document Type: Article

References (48)

1. Aiello LP, Clermont A, Arora V, Davis MD, Sheetz MJ, Bursell SE. Inhibition of PKC beta by oral administration of ruboxistaurin is well tolerated and ameliorates diabetes-induced retinal hemodynamic abnormalities in patients. Invest Ophthalmol Vis Sci 47: 86-92, 2006. (Pubitemid 46780799)
2. Antonetti DA, Barber AJ, Bronson SK, Freeman WM, Gardner TW, Jefferson LS, Kester M, Kimball SR, Krady JK, LaNoue KF, Norbury CC, Quinn PG, Sandirasegarane L, Simpson IA. Diabetic retinopathy: seeing beyond glucose-induced microvascular disease. Diabetes 55: 2401-2411, 2006.
3. Barber AJ, Antonetti DA, Kern TS, Reiter CE, Soans RS, Krady JK, Levison SW, Gardner TW, Bronson SK. The Ins2Akita mouse as a model of early retinal complications in diabetes. Invest Ophthalmol Vis Sci 46: 2210-2218, 2005.
4. 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 102: 783-791, 1998. (Pubitemid 28399611)
5. Barber AJ, Nakamura M, Wolpert EB, Reiter CE, Seigel GM, Antonetti DA, Gardner TW. Insulin rescues retinal neurons from apoptosis by a phosphatidylinositol 3-kinase/Akt-mediated mechanism that reduces the activation of caspase-3. J Biol Chem 276: 32814-32821, 2001.
6. Bhattacharya S, Dey D, Roy SS. Molecular mechanism of insulin resistance. J Biosci 32: 405-413, 2007. (Pubitemid 46708735)
7. Bourbon NA, Sandirasegarane L, Kester M. Ceramide-induced inhibition of Akt is mediated through protein kinase Czeta: implications for growth arrest. J Biol Chem 277: 3286-3292, 2002. (Pubitemid 34953194)
8. Bourbon NA, Yun J, Kester M. Ceramide directly activates protein kinase C zeta to regulate a stress-activated protein kinase signaling complex. J Biol Chem 275: 35617-35623, 2000.
9. Chen H, Nystrom FH, Dong LQ, Li Y, Song S, Liu F, Quon MJ. Insulin stimulates increased catalytic activity of phosphoinositide-dependent kinase-1 by a phosphorylation-dependent mechanism. Biochemistry 40: 11851-11859, 2001. (Pubitemid 32906046)
10. Cohen AW, Razani B, Wang XB, Combs TP, Williams TM, Scherer PE, Lisanti MP. Caveolin-1-deficient mice show insulin resistance and defective insulin receptor protein expression in adipose tissue. Am J Physiol Cell Physiol 285: C222-C235, 2003. (Pubitemid 36736354)
11. Das Evcimen N, King GL. The role of protein kinase C activation and the vascular complications of diabetes. Pharmacol Res 55: 498-510, 2007. (Pubitemid 46962309)
12. Fox TE, Han X, Kelly S, Merrill AH 2nd, Martin RE, Anderson RE, Gardner TW, Kester M. Diabetes alters sphingolipid metabolism in the retina: a potential mechanism of cell death in diabetic retinopathy. Diabetes 55: 3573-3580, 2006. (Pubitemid 44923619)
13. Fox TE, Houck KL, O'Neill SM, Nagarajan M, Stover TC, Pomianowski PT, Unal O, Yun JK, Naides SJ, Kester M. Ceramide recruits and activates protein kinase C zeta (PKC zeta) within structured membrane microdomains. J Biol Chem 282: 12450-12457, 2007. (Pubitemid 47100622)
14. Ganapathi SB, Fox TE, Kester M, Elmslie KS. Ceramide modulates HERG potassium channel gating by translocation into lipid rafts. Am J Physiol Cell Physiol 299: C74-C86, 2010.
15. Gosbell AD, Favilla I, Baxter KM, Jablonski P. Insulin receptor and insulin receptor substrate-I in rat retinae. Clin Experiment Ophthalmol 28: 212-215, 2000.
16. Gosbell AD, Favilla I, Jablonski P. The location of insulin receptors in bovine retina and isolated retinal cells. Clin Experiment Ophthalmol 30: 124-130, 2002. (Pubitemid 34467112)
17. Hajduch E, Turban S, Le Liepvre X, Le Lay S, Lipina C, Dimopoulos N, Dugail I, Hundal HS. Targeting of PKCzeta and PKB to caveolin-enriched microdomains represents a crucial step underpinning the disruption in PKB-directed signalling by ceramide. Biochem J 410: 369-379, 2008. (Pubitemid 351346195)
18. Hammes HP, Du X, Edelstein D, Taguchi T, Matsumura T, Ju Q, Lin J, Bierhaus A, Nawroth P, Hannak D, Neumaier M, Bergfeld R, Giardino I, Brownlee M. Benfotiamine blocks three major pathways of hyperglycemic damage and prevents experimental diabetic retinopathy. Nat Med 9: 294-299, 2003. (Pubitemid 36362784)
19. Hoehn KL, Summers SA. Assaying AKT/protein kinase B activity. Methods Mol Med 83: 137-144, 2003.
20. Inokuchi J. Insulin resistance as a membrane microdomain disorder. Biol Pharm Bull 29: 1532-1537, 2006. (Pubitemid 44166346)
21. Kabayama K, Sato T, Kitamura F, Uemura S, Kang BW, Igarashi Y, Inokuchi J. TNFalpha-induced insulin resistance in adipocytes as a membrane microdomain disorder: involvement of ganglioside GM3. Glycobiology 15: 21-29, 2005. (Pubitemid 40202036)
22. Kim YH, Kim YS, Kang SS, Noh HS, Kim HJ, Cho GJ, Choi WS. Expression of 14-3-3 zeta and interaction with protein kinase C in the rat retina in early diabetes. Diabetologia 48: 1411-1415, 2005. (Pubitemid 41186109)
23. Ozes ON, Akca H, Mayo LD, Gustin JA, Maehama T, Dixon JE, Donner DB. A phosphatidylinositol 3-kinase/Akt/mTOR pathway mediates and PTEN antagonizes tumor necrosis factor inhibition of insulin signaling through insulin receptor substrate-1. Proc Natl Acad Sci USA 98: 4640-4645, 2001. (Pubitemid 32295029)
24. Parpal S, Karlsson M, Thorn H, Stralfors P. Cholesterol depletion disrupts caveolae and insulin receptor signaling for metabolic control via insulin receptor substrate-1, but not for mitogen-activated protein kinase control. J Biol Chem 276: 9670-9678, 2001.
25. Paz K, Hemi R, LeRoith D, Karasik A, Elhanany E, Kanety H, Zick Y. A molecular basis for insulin resistance. Elevated serine/threonine phosphorylation of IRS-1 and IRS-2 inhibits their binding to the juxta-membrane region of the insulin receptor and impairs their ability to undergo insulin-induced tyrosine phosphorylation. J Biol Chem 272: 29911-29918, 1997.
26. Pike LJ. Rafts defined: a report on the Keystone Symposium on Lipid Rafts and Cell Function. J Lipid Res 47: 1597-1598, 2006. (Pubitemid 44079915)
27. PKC-DRS Study Group. The effect of ruboxistaurin on visual loss in patients with moderately severe to very severe nonproliferative diabetic retinopathy: initial results of the Protein Kinase C beta Inhibitor Diabetic Retinopathy Study (PKC-DRS) multicenter randomized clinical trial. Diabetes 54: 2188-2197, 2005.
28. Powell DJ, Hajduch E, Kular G, Hundal HS. Ceramide disables 3-phosphoinositide binding to the pleckstrin homology domain of protein kinase B (PKB)/Akt by a PKCzeta-dependent mechanism. Mol Cell Biol 23: 7794-7808, 2003. (Pubitemid 37271476)
29. Rajala A, Tanito M, Le YZ, Kahn CR, Rajala RV. Loss of neuroprotective survival signal in mice lacking insulin receptor gene in rod photoreceptor cells. J Biol Chem 283: 19781-19792, 2008.
30. Rajala RV, McClellan ME, Chan MD, Tsiokas L, Anderson RE. Interaction of the retinal insulin receptor beta-subunit with the p85 subunit of phosphoinositide 3-kinase. Biochemistry 43: 5637-5650, 2004. (Pubitemid 38623598)
31. Rajala RV, Tanito M, Neel BG, Rajala A. Enhanced retinal insulin receptor-activated neuroprotective survival signal in mice lacking the protein-tyrosine phosphatase-1B gene. J Biol Chem 285: 8894-8904, 2010.
32. Rajala RV, Wiskur B, Tanito M, Callegan M, Rajala A. Diabetes reduces autophosphorylation of retinal insulin receptor and increases protein-tyrosine phosphatase-1B activity. Invest Ophthalmol Vis Sci 50: 1033-1040, 2009.
33. Reiter CE, Sandirasegarane L, Wolpert EB, Klinger M, Simpson IA, Barber AJ, Antonetti DA, Kester M, Gardner TW. Characterization of insulin signaling in rat retina in vivo and ex vivo. Am J Physiol Endocrinol Metab 285: E763-E774, 2003. (Pubitemid 37176427)
34. Reiter CE, Wu X, Sandirasegarane L, Nakamura M, Gilbert KA, Singh RS, Fort PE, Antonetti DA, Gardner TW. Diabetes reduces basal retinal insulin receptor signaling: reversal with systemic and local insulin. Diabetes 55: 1148-1156, 2006. (Pubitemid 44100194)
35. Rodrigues M, Waldbillig RJ, Rajagopalan S, Hackett J, LeRoith D, Chader GJ. Retinal insulin receptors: localization using a polyclonal anti-insulin receptor antibody. Brain Res 443: 389-394, 1988. (Pubitemid 18062813)
36. Rölz W, Xin C, Ren S, Pfeilschifter J, Huwiler A. Interleukin-1 inhibits angiotensin II-stimulated protein kinase B pathway in renal mesangial cells via the inducible nitric oxide synthase. Eur J Pharmacol 442: 195-203, 2002. (Pubitemid 34626194)
37. Rui L, Aguirre V, Kim JK, Shulman GI, Lee A, Corbould A, Dunaif A, White MF. Insulin/IGF-1 and TNF-alpha stimulate phosphorylation of IRS-1 at inhibitory Ser307 via distinct pathways. J Clin Invest 107: 181-189, 2001. (Pubitemid 32096834)
38. Sandirasegarane L, Kester M. Enhanced stimulation of Akt-3/protein kinase B-gamma in human aortic smooth muscle cells. Biochem Biophys Res Commun 283: 158-163, 2001. (Pubitemid 32912552)
39. Seigel GM. Establishment of an E1A-immortalized retinal cell culture. In Vitro Cell Dev Biol Anim 32: 66-68, 1996. (Pubitemid 26075291)
40. Shiba T, Inoguchi T, Sportsman JR, Heath WF, Bursell S, King GL. Correlation of diacylglycerol level and protein kinase C activity in rat retina to retinal circulation. Am J Physiol Endocrinol Metab 265: E783-E793, 1993.
41. Shin T, Kim S, Ahn M, Kim H. An immunohistochemical study of protein kinase C in the bovine retina. J Vet Med Sci 68: 71-74, 2006. (Pubitemid 43208156)
42. Song KS, Li S, Okamoto T, Quilliam LA, Sargiacomo M, Lisanti MP. Co-purification and direct interaction of Ras with caveolin, an integral membrane protein of caveolae microdomains. Detergent-free purification of caveolae microdomains. J Biol Chem 271: 9690-9697, 1996.
43. Tanti JF, Jager J. Cellular mechanisms of insulin resistance: role of stress-regulated serine kinases and insulin receptor substrates (IRS) serine phosphorylation. Curr Opin Pharmacol 9: 753-762, 2009.
44. Tikhonenko M, Lydic TA, Wang Y, Chen W, Opreanu M, Sochacki A, McSorley KM, Renis RL, Kern T, Jump DB, Reid GE, Busik JV. Remodeling of retinal Fatty acids in an animal model of diabetes: a decrease in long-chain polyunsaturated fatty acids is associated with a decrease in fatty acid elongases Elovl2 and Elovl4. Diabetes 59: 219-227, 2010.
45. Van Horn DJ, Myers MG Jr, Backer JM. Direct activation of the phosphatidylinositol 3′-kinase by the insulin receptor. J Biol Chem 269: 29-32, 1994.
46. Wood JP, McCord RJ, Osborne NN. Retinal protein kinase C. Neurochem Int 30: 119-136, 1997.
47. Wu X, Reiter CE, Antonetti DA, Kimball SR, Jefferson LS, Gardner TW. Insulin promotes rat retinal neuronal cell survival in a p70S6K-dependent manner. J Biol Chem 279: 9167-9175, 2004. (Pubitemid 38295980)
48. Yi X, Schubert M, Peachey NS, Suzuma K, Burks DJ, Kushner JA, Suzuma I, Cahill C, Flint CL, Dow MA, Leshan RL, King GL, White MF. Insulin receptor substrate 2 is essential for maturation and survival of photoreceptor cells. J Neurosci 25: 1240-1248, 2005. (Pubitemid 40268967)