Insulin receptor signaling in cones

Journal of Biological Chemistry

Volumn 288, Issue 27, 2013, Pages 19503-19515

  Rajala, Ammaji ^a,c   Dighe, Radhika ^a,c   Agbaga, Martin Paul ^a,c   Anderson, Robert E ^a,b,c   Rajala, Raju V S ^a,b,c  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF OKLAHOMA HEALTH SCIENCES CENTER   (United States)

^c UNIVERSITY OF OKLAHOMA HEALTH SCIENCES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGE-RELATED MACULAR DEGENERATION; DIABETIC RETINOPATHY; INSULIN RECEPTORS; LEUCINE ZIPPERS; PHOSPHOINOSITIDE 3-KINASE; RETINITIS PIGMENTOSA; SIGNALING PROTEINS; SYSTEMIC ADMINISTRATION;

CELL DEATH; EYE PROTECTION; INSULIN;

MAMMALS;

CONE OPSIN; INSULIN RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN P85; PROTEIN P85 ALPHA; RHODOPSIN; TRANSDUCIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; MOUSE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RETINA CONE; RETINA DEGENERATION; RETINA ROD; SIGNAL TRANSDUCTION; SURVIVAL;

CELL DEATH; CONE PHOTORECEPTORS; INSULIN; INSULIN RECEPTOR; NEURODEGENERATION; NEUROPROTECTION; PHOSPHATIDYLINOSITOL 3-KINASE; PHOTORECEPTOR DEGENERATION; PHOTORECEPTORS;

ANIMALS; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CELL COMMUNICATION; CELL SURVIVAL; EYE PROTEINS; HUMANS; MACULAR DEGENERATION; MICE; MICE, KNOCKOUT; PHOSPHATIDYLINOSITOL 3-KINASES; RECEPTOR, INSULIN; RETINAL CONE PHOTORECEPTOR CELLS; RETINAL ROD PHOTORECEPTOR CELLS; RETINITIS PIGMENTOSA; SIGNAL TRANSDUCTION;

EID: 84880048696     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.469064     Document Type: Article

References (76)

1. Fliesler, S. J. and Anderson, R. E. (1983) in Progress in Lipid Research (Holman, R.T., ed) pp. 79-131, Pergamon Press, Inc., Elmsford, NY
2. Zhou, F., Qu, L., Lv, K., Chen, H., Liu, J., Liu, X., Li, Y., and Sun, X. (2011) Luteolin protects against reactive oxygen species-mediated cell death induced by zinc toxicity via the PI3K-Akt-NF-κB-ERK-dependent pathway. J. Neurosci. Res. 89, 1859-1868
3. Cheng, Z., Tseng, Y., and White, M. F. (2010) Insulin signaling meets mitochondria in metabolism. Trends Endocrinol. Metab. 21, 589-598
4. Gao, Y., Dong, C., Yin, J., Shen, J., Tian, J., and Li, C. (2012) Neuroprotective effect of fucoidan on H2O2-induced apoptosis in PC12 cells via activation of PI3K/Akt pathway. Cell. Mol. Neurobiol. 32, 523-529
5. Sanghera, K. P., Mathalone, N., Baigi, R., Panov, E., Wang, D., Zhao, X., Hsu, H., Wang, H., Tropepe, V., Ward, M., and Boyd, S. R. (2011) The PI3K/Akt/mTOR pathway mediates retinal progenitor cell survival under hypoxic and superoxide stress. Mol. Cell. Neurosci. 47, 145-153
6. Havrankova, J., Roth, J., and Brownstein, M. (1978) Insulin receptors are widely distributed in the central nervous system of the rat. Nature 272, 827-829
7. Baskin, D. G., Figlewicz Lattemann, D., Seeley, R. J., Woods, S. C., Porte, D., Jr., and Schwartz, M. W. (1999) Insulin and leptin. Dual adiposity signals to the brain for the regulation of food intake and body weight. Brain Res. 848, 114-123
8. Schwartz, M. W., Sipols, A. J., Marks, J. L., Sanacora, G., White, J. D., Scheurink, A., Kahn, S. E., Baskin, D. G., Woods, S. C., and Figlewicz, D. P. (1992) Inhibition of hypothalamic neuropeptide Y gene expression by insulin. Endocrinology 130, 3608-3616
9. Heidenreich, K. A. (1993) Insulin and IGF-I receptor signaling in cultured neurons. Ann. N.Y. Acad. Sci. 692, 72-88
10. Robinson, L. J., Leitner, W., Draznin, B., and Heidenreich, K. A. (1994) Evidence that p21ras mediates the neurotrophic effects of insulin and insulin-like growth factor I in chick forebrain neurons. Endocrinology 135, 2568-2573
11. Takahashi, M., Yamada, T., Tooyama, I., Moroo, I., Kimura, H., Yamamoto, T., and Okada, H. (1996) Insulin receptor mRNA in the substantia nigra in Parkinson's disease. Neurosci. Lett. 204, 201-204
12. Frölich, L., Blum-Degen, D., Bernstein, H. G., Engelsberger, S., Humrich, J., Laufer, S., Muschner, D., Thalheimer, A., Türk, A., Hoyer, S., Zöchling, R., Boissl, K. W., Jellinger, K., and Riederer, P. (1998) Brain insulin and insulin receptors in aging and sporadic Alzheimer's disease. J. Neural. Transm. 105, 423-438
13. Barber, A. J., Nakamura, M., Wolpert, E. B., Reiter, C. E., Seigel, G. M., Antonetti, D. A., and Gardner, T. W. (2001) 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
14. Brüning, J. C., Gautam, D., Burks, D. J., Gillette, J., Schubert, M., Orban, P. C., Klein, R., Krone, W., Müller-Wieland, D., and Kahn, C. R. (2000) Role of brain insulin receptor in control of body weight and reproduction. Science 289, 2122-2125
15. Rajala, A., Tanito, M., Le, Y. Z., Kahn, C. R., and Rajala, R. V. (2008) Loss of neuroprotective survival signal in mice lacking insulin receptor gene in rod photoreceptor cells. J. Biol. Chem. 283, 19781-19792
16. Carter-Dawson, L. D., and LaVail, M. M. (1979) Rods and cones in the mouse retina. II. Autoradiographic analysis of cell generation using tritiated thymidine. J. Comp. Neurol. 188, 263-272
17. Carter-Dawson, L. D., and LaVail, M. M. (1979) Rods and cones in the mouse retina. I. Structural analysis using light and electron microscopy. J. Comp. Neurol. 188, 245-262
18. Adler, R., Curcio, C., Hicks, D., Price, D., and Wong, F. (1999) Cell death in age-related macular degeneration. Mol. Vis. 5, 31
19. Stone, E. M., Braun, T. A., Russell, S. R., Kuehn, M. H., Lotery, A. J., Moore, P. A., Eastman, C. G., Casavant, T. L., and Sheffield, V. C. (2004) Missense variations in the fibulin 5 gene and age-related macular degeneration. N. Engl. J. Med. 351, 346-353
20. Shen, J., Yang, X., Dong, A., Petters, R. M., Peng, Y. W., Wong, F., and Campochiaro, P. A. (2005) Oxidative damage is a potential cause of cone cell death in retinitis pigmentosa. J. Cell Physiol. 203, 457-464
21. Cho, N. C., Poulsen, G. L., Ver Hoeve, J. N., and Nork, T. M. (2000) Selective loss of S-cones in diabetic retinopathy. Arch. Ophthalmol. 118, 1393-1400
22. Nork, T. M. (2000) Acquired color vision loss and a possible mechanism of ganglion cell death in glaucoma. Trans. Am. Ophthalmol. Soc. 98, 331-363
23. Hamel, C. P. (2007) Cone rod dystrophies. Orphanet. J. Rare. Dis. 2, 7
24. Kellner, U., and Foerster, M. H. (1993) Pattern of dysfunction in progressive cone dystrophies. An extended classification. Ger. J. Ophthalmol. 2, 170-177
25. Kohl, S. (2009) Genetic causes of hereditary cone and cone-rod dystrophies. Ophthalmologe 106, 109-115
26. Punzo, C., Xiong, W., and Cepko, C. L. (2012) Loss of daylight vision in retinal degeneration. Are oxidative stress and metabolic dysregulation to blame? J. Biol. Chem. 287, 1642-1648
27. Park, S. H., Park, J. W., Park, S. J., Kim, K. Y., Chung, J. W., Chun, M. H., and Oh, S. J. (2003) Apoptotic death of photoreceptors in the streptozotocin-induced diabetic rat retina. Diabetologia 46, 1260-1268
28. Reiter, C. E., Wu, X., Sandirasegarane, L., Nakamura, M., Gilbert, K. A., Singh, R. S., Fort, P. E., Antonetti, D. A., and Gardner, T. W. (2006) Diabetes reduces basal retinal insulin receptor signaling. Reversal with systemic and local insulin. Diabetes 55, 1148-1156
29. Punzo, C., Kornacker, K., and Cepko, C. L. (2009) Stimulation of the insulin/mTOR pathway delays cone death in a mouse model of retinitis pigmentosa. Nat. Neurosci. 12, 44-52
30. Ivanovic, I., Anderson, R. E., Le, Y. Z., Fliesler, S. J., Sherry, D. M., and Rajala, R. V. (2011) Deletion of the p85α regulatory subunit of phosphoinositide 3-kinase in cone photoreceptor cells results in cone photoreceptor degeneration. Invest. Ophthalmol. Vis. Sci. 52, 3775-3783
31. Ivanovic, I., Allen, D. T., Dighe, R., Le, Y. Z., Anderson, R. E., and Rajala, R. V. (2011) Phosphoinositide 3-kinase signaling in retinal rod photoreceptors. Invest. Ophthalmol. Vis. Sci. 52, 6355-6362
32. Linton, J. D., Holzhausen, L. C., Babai, N., Song, H., Miyagishima, K. J., Stearns, G. W., Lindsay, K., Wei, J., Chertov, A. O., Peters, T. A., Caffe, R., Pluk, H., Seeliger, M. W., Tanimoto, N., Fong, K., Bolton, L., Kuok, D. L., Sweet, I. R., Bartoletti, T. M., Radu, R. A., Travis, G. H., Zagotta, W. N., Townes-Anderson, E., Parker, E., Van der Zee, C. E., Sampath, A. P., Sokolov, M., Thoreson, W. B., and Hurley, J. B. (2010) Flow of energy in the outer retina in darkness and in light. Proc. Natl. Acad. Sci. U.S.A. 107, 8599-8604
33. Okawa, H., Sampath, A. P., Laughlin, S. B., and Fain, G. L. (2008) ATP consumption by mammalian rod photoreceptors in darkness and in light. Curr. Biol. 18, 1917-1921
34. Li, G., Anderson, R. E., Tomita, H., Adler, R., Liu, X., Zack, D. J., and Rajala, R. V. (2007) Nonredundant role of Akt2 for neuroprotection of rod photoreceptor cells from light-induced cell death. J. Neurosci. 27, 203-211
35. Mears, A. J., Kondo, M., Swain, P. K., Takada, Y., Bush, R. A., Saunders, T. L., Sieving, P. A., and Swaroop, A. (2001) Nrl is required for rod photoreceptor development. Nat. Genet. 29, 447-452
36. Yang, Y., Mohand-Said, S., Danan, A., Simonutti, M., Fontaine, V., Clerin, E., Picaud, S., Léveillard, T., and Sahel, J. A. (2009) Functional cone rescue by RdCVF protein in a dominant model of retinitis pigmentosa. Mol. Ther. 17, 787-795
37. Tan, E., Ding, X. Q., Saadi, A., Agarwal, N., Naash, M. I., and Al-Ubaidi, M. R. (2004) Expression of cone-photoreceptor-specific antigens in a cell line derived from retinal tumors in transgenic mice. Invest. Ophthalmol. Vis. Sci. 45, 764-768
38. Luo, J., McMullen, J. R., Sobkiw, C. L., Zhang, L., Dorfman, A. L., Sherwood, M. C., Logsdon, M. N., Horner, J. W., DePinho, R. A., Izumo, S., and Cantley, L. C. (2005) Class IA phosphoinositide 3-kinase regulates heart size and physiological cardiac hypertrophy. Mol. Cell. Biol. 25, 9491-9502
39. Le, Y. Z., Ash, J. D., Al-Ubaidi, M. R., Chen, Y., Ma, J. X., and Anderson, R. E. (2004) Targeted expression of Cre recombinase to cone photoreceptors in transgenic mice. Mol. Vis. 10, 1011-1018
40. Kryger, Z., Galli-Resta, L., Jacobs, G. H., and Reese, B. E. (1998) The topography of rod and cone photoreceptors in the retina of the ground squirrel. Vis. Neurosci. 15, 685-691
41. Stuck, M. W., Conley, S. M., and Naash, M. I. (2012) Defects in the outer limiting membrane are associated with rosette development in the Nrl-/- retina. PLoS ONE 7, e32484
42. Elias, R. V., Sezate, S. S., Cao, W., and McGinnis, J. F. (2004) Temporal kinetics of the light/dark translocation and compartmentation of arrestin and α-transducin in mouse photoreceptor cells. Mol. Vis. 10, 672-681
43. Majewski, N., Nogueira, V., Bhaskar, P., Coy, P. E., Skeen, J. E., Gottlob, K., Chandel, N. S., Thompson, C. B., Robey, R. B., and Hay, N. (2004) Hexokinase-mitochondria interaction mediated by Akt is required to inhibit apoptosis in the presence or absence of Bax and Bak. Mol. Cell 16, 819-830
44. Naash, M. I., Hollyfield, J. G., al-Ubaidi, M. R., and Baehr, W. (1993) Simulation of human autosomal dominant retinitis pigmentosa in transgenic mice expressing a mutated murine opsin gene. Proc. Natl. Acad. Sci. U.S.A. 90, 5499-5503
45. Nikonov, S. S., Brown, B. M., Davis, J. A., Zuniga, F. I., Bragin, A., Pugh, E. N., Jr., and Craft, C. M. (2008) Mouse cones require an arrestin for normal inactivation of phototransduction. Neuron 59, 462-474
46. Zhu, X., Brown, B., Li, A., Mears, A. J., Swaroop, A., and Craft, C. M. (2003) GRK1-dependent phosphorylation of S andMopsins and their binding to cone arrestin during cone phototransduction in the mouse retina. J. Neurosci. 23, 6152-6160
47. Nikonov, S. S., Daniele, L. L., Zhu, X., Craft, C. M., Swaroop, A., and Pugh, E. N., Jr. (2005) Photoreceptors of Nrl-/- mice coexpress functional Sand M-cone opsins having distinct inactivation mechanisms. J. Gen. Physiol. 125, 287-304
48. Daniele, L. L., Lillo, C., Lyubarsky, A. L., Nikonov, S. S., Philp, N., Mears, A. J., Swaroop, A., Williams, D. S., and Pugh, E. N., Jr. (2005) Cone-like morphological, molecular, and electrophysiological features of the photoreceptors of the Nrl knockout mouse. Invest. Ophthalmol. Vis. Sci. 46, 2156-2167
49. Feathers, K. L., Lyubarsky, A. L., Khan, N. W., Teofilo, K., Swaroop, A., Williams, D. S., Pugh, E. N., Jr., and Thompson, D. A. (2008) Nrl-knockout mice deficient in Rpe65 fail to synthesize 11-cis-retinal and cone outer segments. Invest. Ophthalmol. Vis. Sci. 49, 1126-1135
50. Gómez-Vicente, V., Donovan, M., and Cotter, T. G. (2005) Multiple death pathways in retina-derived 661W cells following growth factor deprivation. Cross-talk between caspases and calpains. Cell Death Differ. 12, 796-804
51. Bowes, C., Li, T., Danciger, M., Baxter, L. C., Applebury, M. L., and Farber, D. B. (1990) Retinal degeneration in the rd mouse is caused by a defect in the β subunit of rod cGMP-phosphodiesterase. Nature 347, 677-680
52. Lem, J., Krasnoperova, N. V., Calvert, P. D., Kosaras, B., Cameron, D. A., Nicolò, M., Makino, C. L., and Sidman, R. L. (1999) Morphological, physiological, and biochemical changes in rhodopsin knockout mice. Proc. Natl. Acad. Sci. U.S.A. 96, 736-741
53. Tsang, S. H., Gouras, P., Yamashita, C. K., Kjeldbye, H., Fisher, J., Farber, D. B., and Goff, S. P. (1996) Retinal degeneration in mice lacking the β subunit of the rod cGMP phosphodiesterase. Science 272, 1026-1029
54. Masure, S., Haefner, B., Wesselink, J. J., Hoefnagel, E., Mortier, E., Verhasselt, P., Tuytelaars, A., Gordon, R., and Richardson, A. (1999) Molecular cloning, expression, and characterization of the human serine/threonine kinase Akt-3. Eur. J. Biochem. 265, 353-360
55. Staal, S. P. (1987) Molecular cloning of the akt oncogene and its human homologues AKT1 and AKT2. Amplification of AKT1 in a primary human gastric adenocarcinoma. Proc. Natl. Acad. Sci. U.S.A. 84, 5034-5037
56. Brodbeck, D., Cron, P., and Hemmings, B. A. (1999) A human protein kinase Bγ with regulatory phosphorylation sites in the activation loop and in the C-terminal hydrophobic domain. J. Biol. Chem. 274, 9133-9136
57. Jones, P. F., Jakubowicz, T., and Hemmings, B. A. (1991) Molecular cloning of a second form of rac protein kinase. Cell Regul. 2, 1001-1009
58. Jones, P. F., Jakubowicz, T., Pitossi, F. J., Maurer, F., and Hemmings, B. A. (1991) Molecular cloning and identification of a serine/threonine protein kinase of the second-messenger subfamily. Proc. Natl. Acad. Sci. U.S.A. 88, 4171-4175
59. Nakatani, K., Sakaue, H., Thompson, D. A., Weigel, R. J., and Roth, R. A. (1999) Identification of a human Akt3 (protein kinase B γ) which contains the regulatory serine phosphorylation site. Biochem. Biophys. Res. Commun. 257, 906-910
60. Coffer, P. J., and Woodgett, J. R. (1991) Molecular cloning and characterisation of a novel putative protein-serine kinase related to the cAMP-dependent and protein kinase C families. Eur. J. Biochem. 201, 475-481
61. Li, G., Rajala, A., Wiechmann, A. F., Anderson, R. E., and Rajala, R. V. (2008) Activation and membrane binding of retinal protein kinase Bα/Akt1 is regulated through light-dependent generation of phosphoinositides. J. Neurochem. 107, 1382-1397
62. Hay, N., and Sonenberg, N. (2004) Upstream and downstream of mTOR. Genes Dev. 18, 1926-1945
63. Gingras, A. C., Raught, B., and Sonenberg, N. (2001) Regulation of translation initiation by FRAP/mTOR. Genes Dev. 15, 807-826
64. Dennis, P. B., Jaeschke, A., Saitoh, M., Fowler, B., Kozma, S. C., and Thomas, G. (2001) Mammalian TOR. A homeostatic ATP sensor. Science 294, 1102-1105
65. Sarbassov, D. D., Ali, S. M., and Sabatini, D. M. (2005) Growing roles for the mTOR pathway. Curr. Opin. Cell Biol. 17, 596-603
66. Sengupta, S., Peterson, T. R., and Sabatini, D. M. (2010) Regulation of the mTOR complex 1 pathway by nutrients, growth factors, and stress. Mol. Cell 40, 310-322
67. Schmelzle, T., and Hall, M. N. (2000) TOR, a central controller of cell growth. Cell 103, 253-262
68. Chiang, G. G., and Abraham, R. T. (2005) Phosphorylation of mammalian target of rapamycin (mTOR) at Ser-2448 is mediated by p70S6 kinase. J. Biol. Chem. 280, 25485-25490
69. Wang, X., and Proud, C. G. (2006) The mTOR pathway in the control of protein synthesis. Physiology 21, 362-369
70. Gingras, A. C., Kennedy, S. G., O'Leary, M. A., Sonenberg, N., and Hay, N. (1998) 4E-BP1, a repressor of mRNA translation, is phosphorylated and inactivated by the Akt(PKB) signaling pathway. Genes Dev. 12, 502-513
71. Rehen, S. K., Neves, D. D., Fragel-Madeira, L., Britto, L. R., and Linden, R. (1999) Selective sensitivity of early postmitotic retinal cells to apoptosis induced by inhibition of protein synthesis. Eur. J. Neurosci. 11, 4349-4356
72. Morris, J. Z., Tissenbaum, H. A., and Ruvkun, G. (1996) A phosphatidylinositol- 3-OH kinase family member regulating longevity and diapause in Caenorhabditis elegans. Nature 382, 536-539
73. Kimura, K. D., Tissenbaum, H. A., Liu, Y., and Ruvkun, G. (1997) daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 277, 942-946
74. Wu, X., Reiter, C. E., Antonetti, D. A., Kimball, S. R., Jefferson, L. S., and Gardner, T. W. (2004) Insulin promotes rat retinal neuronal cell survival in a p70S6K-dependent manner. J. Biol. Chem. 279, 9167-9175
75. Liu, Y., Liu, F., Grundke-Iqbal, I., Iqbal, K., and Gong, C. X. (2011) Deficient brain insulin signalling pathway in Alzheimer's disease and diabetes. J. Pathol. 225, 54-62
76. Deng, Y., Li, B., Liu, Y., Iqbal, K., Grundke-Iqbal, I., and Gong, C. X. (2009) Dysregulation of insulin signaling, glucose transporters, O-GlcNAcylation, and phosphorylation of tau and neurofilaments in the brain. Implication for Alzheimer's disease. Am. J. Pathol. 175, 2089-2098