The PI3K-PTEN tug-of-war, oxidative stress and retinal degeneration

Trends in Molecular Medicine

Volumn 15, Issue 5, 2009, Pages 191-198

  Kang, Kyung Hwa ^a   Lemke, Greg ^b   Kim, Jin Woo ^a  

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

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TOCOPHEROL; ANTIOXIDANT; ASCORBIC ACID; CYTOKINE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; RETINOID;

ARTICLE; BLOOD RETINA BARRIER; CYTOKINE PRODUCTION; ENZYME MECHANISM; ENZYME REGULATION; HISTOPATHOLOGY; HUMAN; HUMAN CELL; OXIDATIVE STRESS; PHOTORECEPTOR; PROTEIN PROTEIN INTERACTION; RETINA DEGENERATION; RETINA MACULA AGE RELATED DEGENERATION; RETINA PIGMENT EPITHELIOPATHY; SIGNAL PROCESSING;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; ANTIOXIDANTS; CELL POLARITY; CELL SURVIVAL; HUMANS; OXIDATIVE STRESS; PHOTORECEPTOR CELLS; PTEN PHOSPHOHYDROLASE; RETINAL DEGENERATION; RETINAL PIGMENT EPITHELIUM; SIGNAL TRANSDUCTION;

EID: 65549150446     PISSN: 14714914     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molmed.2009.03.005     Document Type: Article

References (100)

1. Algvere P.V., et al. Age-related maculopathy and the impact of blue light hazard. Acta Ophthalmol. Scand. 84 (2006) 4-15
2. Wenzel A., et al. Molecular mechanisms of light-induced photoreceptor apoptosis and neuroprotection for retinal degeneration. Prog. Retin. Eye Res. 24 (2005) 275-306
3. Winkler B.S., et al. Oxidative damage and age-related macular degeneration. Mol. Vis. 5 (1999) 32
4. Beatty S., et al. The role of oxidative stress in the pathogenesis of age-related macular degeneration. Surv. Ophthalmol. 45 (2000) 115-134
5. Cai J., et al. Oxidative damage and protection of the RPE. Prog. Retin. Eye Res. 19 (2000) 205-221
6. Liang F.Q., and Godley B.F. Oxidative stress-induced mitochondrial DNA damage in human retinal pigment epithelial cells: a possible mechanism for RPE aging and age-related macular degeneration. Exp. Eye Res. 76 (2003) 397-403
7. Pacione L.R., et al. Progress toward understanding the genetic and biochemical mechanisms of inherited photoreceptor degenerations. Annu. Rev. Neurosci. 26 (2003) 657-700
8. Zarbin M.A. Current concepts in the pathogenesis of age-related macular degeneration. Arch. Ophthalmol. 122 (2004) 598-614
9. Arshavsky V.Y., et al. G proteins and phototransduction. Annu. Rev. Physiol. 64 (2002) 153-187
10. Rando R.R. Molecular mechanisms in visual pigment regeneration. Photochem. Photobiol. 56 (1992) 1145-1156
11. Noell W.K. Possible mechanisms of photoreceptor damage by light in mammalian eyes. Vision Res. 20 (1980) 1163-1171
12. Komeima K., et al. Antioxidants slow photoreceptor cell death in mouse models of retinitis pigmentosa. J. Cell. Physiol. 213 (2007) 809-815
13. Tanito M., et al. Cytoprotective effect of thioredoxin against retinal photic injury in mice. Invest. Ophthalmol. Vis. Sci. 43 (2002) 1162-1167
14. Hogg R., and Chakravarthy U. AMD and micronutrient antioxidants. Curr. Eye Res. 29 (2004) 387-401
15. Gosbell A.D., et al. Retinal light damage: structural and functional effects of the antioxidant glutathione peroxidase-1. Invest. Ophthalmol. Vis. Sci. 47 (2006) 2613-2622
16. Winkler B.S. An hypothesis to account for the renewal of outer segments in rod and cone photoreceptor cells: renewal as a surrogate antioxidant. Invest. Ophthalmol. Vis. Sci. 49 (2008) 3259-3261
17. Imamura Y., et al. Drusen, choroidal neovascularization, and retinal pigment epithelium dysfunction in SOD1-deficient mice: a model of age-related macular degeneration. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 11282-11287
18. Saari J.C., et al. Reduction of all-trans-retinal limits regeneration of visual pigment in mice. Vision Res. 38 (1998) 1325-1333
19. Decanini A., et al. Changes in Select Redox Proteins of the Retinal Pigment Epithelium in Age-related Macular Degeneration. Am. J. Ophthalmol. 143 (2007) 607-615
20. Barnstable C.J., and Tombran-Tink J. Molecular mechanisms of neuroprotection in the eye. Adv. Exp. Med. Biol. 572 (2006) 291-295
21. Sakaguchi H., et al. Intense light exposure changes the crystallin content in retina. Exp. Eye Res. 76 (2003) 131-133
22. Rao N.A., et al. Elevated retina-specific expression of the small heat shock protein, αA-crystallin, is associated with photoreceptor protection in experimental uveitis. Invest. Ophthalmol. Vis. Sci. 49 (2008) 1161-1171
23. Doonan F., and Cotter T.G. Apoptosis: a potential therapeutic target for retinal degenerations. Curr. Neurovasc. Res. 1 (2004) 41-53
24. Li G., et al. Nonredundant role of Akt2 for neuroprotection of rod photoreceptor cells from light-induced cell death. J. Neurosci. 27 (2007) 203-211
25. Algvere P.V., and Seregard S. Age-related maculopathy: pathogenetic features and new treatment modalities. Acta Ophthalmol. Scand. 80 (2002) 136-143
26. Marmorstein A.D., et al. Morphogenesis of the retinal pigment epithelium: toward understanding retinal degenerative diseases. Ann. N. Y. Acad. Sci. 857 (1998) 1-12
27. Bharti K., et al. The other pigment cell: specification and development of the pigmented epithelium of the vertebrate eye. Pigment Cell Res. 19 (2006) 380-394
28. Sarangarajan R., and Apte S.P. Melanization and phagocytosis: implications for age related macular degeneration. Mol. Vis. 11 (2005) 482-490
29. Bonilha V.L., et al. Ezrin promotes morphogenesis of apical microvilli and basal infoldings in retinal pigment epithelium. J. Cell Biol. 147 (1999) 1533-1548
30. Jin M., et al. The role of interphotoreceptor retinoid-binding protein on the translocation of visual retinoids and function of cone photoreceptors. J. Neurosci. 29 (2009) 1486-1495
31. Bosch E., et al. Phagocytosis of outer segments by retinal pigment epithelium: phagosome-lysosome interaction. J. Histochem. Cytochem. 41 (1993) 253-263
32. Schraermeyer U., and Heimann K. Current understanding on the role of retinal pigment epithelium and its pigmentation. Pigment Cell Res. 12 (1999) 219-236
33. Bergmann M., et al. Inhibition of the ATP-driven proton pump in RPE lysosomes by the major lipofuscin fluorophore A2-E may contribute to the pathogenesis of age-related macular degeneration. FASEB J. 18 (2004) 562-564
34. Rozanowska M., et al. Blue light-induced reactivity of retinal age pigment. In vitro generation of oxygen-reactive species. J. Biol. Chem. 270 (1995) 18825-18830
35. Sparrow J.R., and Boulton M. RPE lipofuscin and its role in retinal pathobiology. Exp. Eye Res. 80 (2005) 595-606
36. Rizzolo L.J. Polarity and the development of the outer blood-retinal barrier. Histol. Histopathol. 12 (1997) 1057-1067
37. McKay B.S., et al. Cell-cell adhesion molecules and the development of an epithelial phenotype in cultured human retinal pigment epithelial cells. Exp. Eye Res. 65 (1997) 661-671
38. Luo Y., et al. Expression of JAM-A, AF-6, PAR-3 and PAR-6 during the assembly and remodeling of RPE tight junctions. Brain Res. 1110 (2006) 55-63
39. Tornquist P., et al. Permeability of ocular vessels and transport across the blood-retinal-barrier. Eye 4 (1990) 303-309
40. Comer F.I., and Parent C.A. Phosphoinositides specify polarity during epithelial organ development. Cell 128 (2007) 239-240
41. Rodriguez-Boulan E., et al. Organization of vesicular trafficking in epithelia. Nat. Rev. Mol. Cell Biol. 6 (2005) 233-247
42. Finnemann S.C., and Rodriguez-Boulan E. Macrophage and retinal pigment epithelium phagocytosis: apoptotic cells and photoreceptors compete for αvβ3 and αvβ5 integrins, and protein kinase C regulates αvβ5 binding and cytoskeletal linkage. J. Exp. Med. 190 (1999) 861-874
43. Gundersen D., et al. Apical polarity of Na,K-ATPase in retinal pigment epithelium is linked to a reversal of the ankyrin-fodrin submembrane cytoskeleton. J. Cell Biol. 112 (1991) 863-872
44. Gundersen D., et al. Apical polarization of N-CAM in retinal pigment epithelium is dependent on contact with the neural retina. J. Cell Biol. 121 (1993) 335-343
45. Mousa S.A., et al. Role of hypoxia and extracellular matrix-integrin binding in the modulation of angiogenic growth factors secretion by retinal pigmented epithelial cells. J. Cell. Biochem. 74 (1999) 135-143
46. Holtkamp G.M., et al. Retinal pigment epithelium-immune system interactions: cytokine production and cytokine-induced changes. Prog. Retin. Eye Res. 20 (2001) 29-48
47. Blaauwgeers H.G., et al. Polarized vascular endothelial growth factor secretion by human retinal pigment epithelium and localization of vascular endothelial growth factor receptors on the inner choriocapillaris. Evidence for a trophic paracrine relation. Am. J. Pathol. 155 (1999) 421-428
48. Slomiany M.G., and Rosenzweig S.A. IGF-1-induced VEGF and IGFBP-3 secretion correlates with increased HIF-1 α expression and activity in retinal pigment epithelial cell line D407. Invest. Ophthalmol. Vis. Sci 45 (2004) 2838-2847
49. Boulton M., and Dayhaw-Barker P. The role of the retinal pigment epithelium: topographical variation and ageing changes. Eye 15 (2001) 384-389
50. Cook H.L., et al. Age-related macular degeneration: diagnosis and management. Br. Med. Bull. 85 (2008) 127-149
51. Petrukhin K. New therapeutic targets in atrophic age-related macular degeneration. Expert Opin. Ther. Targets 11 (2007) 625-639
52. Lien S., and Lowman H.B. Therapeutic anti-VEGF antibodies. Handb. Exp. Pharmacol. 181 (2008) 131-150
53. Coleman H., and Chew E. Nutritional supplementation in age-related macular degeneration. Curr. Opin. Ophthalmol. 18 (2007) 220-223
54. Montezuma S.R., et al. Review of genetics in age related macular degeneration. Semin. Ophthalmol. 22 (2007) 229-240
55. Suter M., et al. Age-related macular degeneration. The lipofusion component N-retinyl-N-retinylidene ethanolamine detaches proapoptotic proteins from mitochondria and induces apoptosis in mammalian retinal pigment epithelial cells. J. Biol. Chem. 275 (2000) 39625-39630
56. Cross J.V., and Templeton D.J. Regulation of signal transduction through protein cysteine oxidation. Antioxid. Redox Signal. 8 (2006) 1819-1827
57. Rhee S.G., et al. Intracellular messenger function of hydrogen peroxide and its regulation by peroxiredoxins. Curr. Opin. Cell Biol. 17 (2005) 183-189
58. Xu D., et al. Oxidants painting the cysteine chapel: redox regulation of PTPs. Dev. Cell 2 (2002) 251-252
59. Chiarugi P. The redox regulation of LMW-PTP during cell proliferation or growth inhibition. IUBMB Life 52 (2001) 55-59
60. Meng T.C., et al. Regulation of insulin signaling through reversible oxidation of the protein-tyrosine phosphatases TC45 and PTP1B. J. Biol. Chem. 279 (2004) 37716-37725
61. Ross S.H., et al. Differential redox regulation within the PTP superfamily. Cell. Signal. 19 (2007) 1521-1530
62. Zhang J., et al. Myotubularin phosphoinositide phosphatases, protein phosphatases, and kinases: their roles in junction dynamics and spermatogenesis. J. Cell. Physiol. 204 (2005) 470-483
63. Herve J.C., and Sarrouilhe D. Modulation of junctional communication by phosphorylation: protein phosphatases, the missing link in the chain. Biol. Cell 94 (2002) 423-432
64. Alema S., and Salvatore A.M. p120 catenin and phosphorylation: Mechanisms and traits of an unresolved issue. Biochim. Biophys. Acta 1773 (2007) 47-58
65. Kotelevets L., et al. The lipid phosphatase activity of PTEN is critical for stabilizing intercellular junctions and reverting invasiveness. J. Cell Biol. 155 (2001) 1129-1135
66. Bailey T.A., et al. Oxidative stress affects the junctional integrity of retinal pigment epithelial cells. Invest. Ophthalmol. Vis. Sci. 45 (2004) 675-684
67. Kim J.W., et al. Retinal degeneration triggered by inactivation of PTEN in the retinal pigment epithelium. Genes Dev. 22 (2008) 3147-3157
68. Maehama T., and Dixon J.E. PTEN: a tumour suppressor that functions as a phospholipid phosphatase. Trends Cell Biol. 9 (1999) 125-128
69. Salmena L., et al. Tenets of PTEN tumor suppression. Cell 133 (2008) 403-414
70. Tamura M., et al. Inhibition of cell migration, spreading, and focal adhesions by tumor suppressor PTEN. Science 280 (1998) 1614-1617
71. Shen W.H., et al. Essential role for nuclear PTEN in maintaining chromosomal integrity. Cell 128 (2007) 157-170
72. Freeman D.J., et al. PTEN tumor suppressor regulates p53 protein levels and activity through phosphatase-dependent and -independent mechanisms. Cancer Cell 3 (2003) 117-130
73. Puc J., et al. Lack of PTEN sequesters CHK1 and initiates genetic instability. Cancer Cell 7 (2005) 193-204
74. Yin Y., and Shen W.H. PTEN: a new guardian of the genome. Oncogene 27 (2008) 5443-5453
75. Stiles B., et al. PTENless means more. Dev. Biol. 273 (2004) 175-184
76. Suzuki A., et al. Portrait of PTEN: messages from mutant mice. Cancer Sci. 99 (2008) 209-213
77. Cantley L.C. The phosphoinositide 3-kinase pathway. Science 296 (2002) 1655-1657
78. Fruman D.A., et al. Phosphoinositide kinases. Annu. Rev. Biochem. 67 (1998) 481-507
79. Vazquez F., et al. Phosphorylation of the PTEN tail regulates protein stability and function. Mol. Cell. Biol. 20 (2000) 5010-5018
80. Ambati J., et al. An animal model of age-related macular degeneration in senescent Ccl-2- or Ccr-2-deficient mice. Nat. Med. 9 (2003) 1390-1397
81. Kohli R., et al. Mitochondrial reactive oxygen species signal hepatocyte steatosis by regulating the phosphatidylinositol 3-kinase cell survival pathway. J. Biol. Chem. 282 (2007) 21327-21336
82. Seo J.H., et al. The major target of the endogenously generated reactive oxygen species in response to insulin stimulation is phosphatase and tensin homolog and not phosphoinositide-3 kinase (PI-3 kinase) in the PI-3 kinase/Akt pathway. Mol. Biol. Cell 16 (2005) 348-357
83. Leslie N.R., et al. Redox regulation of PI 3-kinase signalling via inactivation of PTEN. EMBO J. 22 (2003) 5501-5510
84. Ellson C., et al. PtdIns3P binding to the PX domain of p40phox is a physiological signal in NADPH oxidase activation. EMBO J. 25 (2006) 4468-4478
85. Hawkins P.T., et al. The role of PI3Ks in the regulation of the neutrophil NADPH oxidase. Biochem. Soc. Symp. 74 (2007) 59-67
86. Dinauer M.C. Regulation of neutrophil function by Rac GTPases. Curr. Opin. Hematol. 10 (2003) 8-15
87. Martin-Belmonte F., et al. PTEN-mediated apical segregation of phosphoinositides controls epithelial morphogenesis through Cdc42. Cell 128 (2007) 383-397
88. Mostov K.E., and Cardone M.H. Regulation of protein traffic in polarized epithelial cells. Bioessays 17 (1995) 129-138
89. Pinal N., et al. Regulated and polarized PtdIns(3,4,5)P3 accumulation is essential for apical membrane morphogenesis in photoreceptor epithelial cells. Curr. Biol. 16 (2006) 140-149
90. von Stein W., et al. Direct association of Bazooka/PAR-3 with the lipid phosphatase PTEN reveals a link between the PAR/aPKC complex and phosphoinositide signaling. Development 132 (2005) 1675-1686
91. Kotelevets L., et al. Implication of the MAGI-1b/PTEN signalosome in stabilization of adherens junctions and suppression of invasiveness. FASEB J. 19 (2005) 115-117
92. Vogelmann R., et al. TGFβ-induced downregulation of E-cadherin-based cell-cell adhesion depends on PI3-kinase and PTEN. J. Cell Sci. 118 (2005) 4901-4912
93. Xu K.P., and Yu F.S. Cross talk between c-Met and epidermal growth factor receptor during retinal pigment epithelial wound healing. Invest. Ophthalmol. Vis. Sci. 48 (2007) 2242-2248
94. Takahashi K., et al. Induction of tyrosine phosphorylation and association of β-catenin with EGF receptor upon tryptic digestion of quiescent cells at confluence. Oncogene 15 (1997) 71-78
95. Gaudry C.A., et al. Tyrosine-phosphorylated plakoglobin is associated with desmogleins but not desmoplakin after epidermal growth factor receptor activation. J. Biol. Chem. 276 (2001) 24871-24880
96. Monga S.P., et al. Hepatocyte growth factor induces Wnt-independent nuclear translocation of β-catenin after Met-β-catenin dissociation in hepatocytes. Cancer Res. 62 (2002) 2064-2071
97. Lilien J., and Balsamo J. The regulation of cadherin-mediated adhesion by tyrosine phosphorylation/dephosphorylation of β-catenin. Curr. Opin. Cell Biol. 17 (2005) 459-465
98. Taddei M.L., et al. β-catenin interacts with low-molecular-weight protein tyrosine phosphatase leading to cadherin-mediated cell-cell adhesion increase. Cancer Res. 62 (2002) 6489-6499
99. Wadham C., et al. The protein tyrosine phosphatase Pez is a major phosphatase of adherens junctions and dephosphorylates β-catenin. Mol. Biol. Cell 14 (2003) 2520-2529
100. Chiarugi P. PTPs versus PTKs: the redox side of the coin. Free Radic. Res. 39 (2005) 353-364