Critical role of TXNIP in oxidative stress, DNA damage and retinal pericyte apoptosis under high glucose: Implications for diabetic retinopathy

Experimental Cell Research

Volumn 319, Issue 7, 2013, Pages 1001-1012

  Devi, Takhellambam S ^a   Hosoya, Ken Ichi ^b   Terasaki, Tetsuya ^c   Singh, Lalit P ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TOYAMA   (Japan)

^c TOHOKU UNIVERSITY   (Japan)

Author keywords

Chromatin break; Diabetic retinopathy; Hyperglycemia; Mitochondrial dysfunction; Oxidative stress; Pericyte apoptosis; TXNIP

Indexed keywords

ACETYLCYSTEINE; CASPASE 3; GLUCOSE; SMALL INTERFERING RNA; THIOREDOXIN INTERACTING PROTEIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; DIABETIC RETINOPATHY; DNA DAMAGE; ENZYME ACTIVATION; HYPERGLYCEMIA; NITROSYLATION; NONHUMAN; OXIDATIVE STRESS; PERICYTE; PRIORITY JOURNAL; RAT; RETINA; UPREGULATION;

RATTUS;

EID: 84874991065     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2013.01.012     Document Type: Article

References (62)

1. Cheung N., Mitchell P., Wong T.Y. Diabetic retinopathy. Lancet 2010, 376:124-136.
2. Robinson R., Barathi V.A., Chaurasia S.S., Wong T.Y., Kern T.S. Update on animal models of diabetic retinopathy: from molecular approaches to mice and higher mammals. Dis. Model. Mech. 2012, 5:444-456.
3. Tang J., Kern T.S. Inflammation in diabetic retinopathy. Prog. Retin. Eye Res. 2011, 30:343-358.
4. Frey T., Antonetti D.A. Alterations to the blood-retinal barrier in diabetes: cytokines and reactive oxygen species. Antioxid Redox Signal. 2011, 15:1271-1284.
5. Geraldes P., Hiraoka-Yamamoto J., Matsumoto M., Clermont A., Leitges M., Marette A., Aiello L.P., Kern T.S., King G.L. Activation of PKC-delta and SHP-1 by hyperglycemia causes vascular cell apoptosis and diabetic retinopathy. Nat. Med. 2009, 15:1298-1306.
6. Roy S., Nasser S., Yee Y., Graves D.T., Roy S S. A long-term siRNA strategy regulates fibronectin overexpression and improves vascular lesions in retinas of diabetic rats. Mol. Vis. 2011, 17:3166-3174.
7. Hammes H.P., Feng Y., Pfister F., Brownlee M. Diabetic retinopathy: targeting vasoregression. Diabetes 2011, 60:9-16.
8. Winkler E.A., Bell R.D., Zlokovic B.V. Central nervous system pericytes in health and disease. Nat. Neurosci. 2011, 14:1398-1405.
9. Puro D.G. Retinovascular physiology and pathophysiology: new experimental approach/new insights. Prog. Retin. Eye Res. 2012, 31:258-270.
10. Barber A.J., Gardner T.W., Abcouwer S.F. The significance of vascular and neural apoptosis to the pathology of diabetic retinopathy. Invest. Ophthalmol. Vis. Sci. 2011, 52:1156-1163.
11. Schulze P.C., Yoshioka J., Takahashi T., He Z., King G.L., Lee R.T. Hyperglycemia promotes oxidative stress through inhibition of thioredoxin function by thioredoxin-interacting protein. J. Biol. Chem. 2004, 279:30369-30374.
12. Forrester M.T., Seth D., Hausladen A., Eyler C.E., Foster M.W., Matsumoto A., Benhar M., Marshall H.E., Stamler J.S. Thioredoxin-interacting protein (Txnip) is a feedback regulator of S-nitrosylation. J. Biol. Chem. 2009, 284:36160-36166.
13. Perrone L., Devi T.S., Hosoya K.I., Terasaki T., Singh L.P. Thioredoxin interacting protein (TXNIP) induces inflammation through chromatin modification in retinal capillary endothelial cells under diabetic conditions. J. Cell Physiol. 2009, 221:262-272.
14. Perrone L., Devi T.S., Hosoya K.I., Terasaki T., Singh L.P. Inhibition of TXNIP expression in vivo blocks early pathologies of diabetic retinopathy. Cell Death Dis. 2010, 1:65. 10.1038/cddis.2010.42.
15. T.S. Devi, I. Lee, M. Hüttemann, A. Kumar, K.D. Nantwi, L.P. Singh, Txnip links innate host defense mechanisms to oxidative stress and inflammation in retinal Muller glia under chronic hyperglycemia: implications for diabetic retinopathy. Exp. Diabetes Res. (2012) 438238.
16. Benhar M., Forrester M.T., Hess D.T., Stamler J.S. Regulated protein denitrosylation by cytosolic and mitochondrial thioredoxins. Science 2008, 320:1050-1054.
17. Wu C., Parrott A.M., Fu C., Liu T., Marino S.M., Gladyshev V.N., Jain M.R., Baykal A.T., Li Q., Oka S., Sadoshima J., Beuve A., Simmons W.J., Li H. Thioredoxin 1-mediated post-translational modifications: reduction, transnitrosylation, denitrosylation, and related proteomics methodologies. Antioxid Redox Signal. 2011, 15:2565-2604.
18. Barglow K.T., Knutson C.G., Wishnok J.S., Tannenbaum S.R., Marletta M.A. Site-specific and redox-controlled S-nitrosation of thioredoxin. Proc. Nat. Acad. Sci. U.S.A. 2011, 108:E600-E606.
19. Zhou R., Tardivel A., Thorens B., Choi I., Tschopp J. Thioredoxin-interacting protein links oxidative stress to inflammasome activation. Nat. Immunol. 2010, 11:136-140.
20. Masters S.L., Dunne A., Subramanian S.L., Hull R.L., Tannahill G.M., Sharp F.A., Becker C., Franchi L., Yoshihara E., Chen Z., Mullooly N., Mielke L.A., Harris J., Coll R.C., Mills K.H., Mok K.H., Newsholme P., Nuñez G., Yodoi J., Kahn S.E., Lavelle E.C., O'Neill L.A. Activation of the NLRP3 inflammasome by islet amyloid polypeptide provides a mechanism for enhanced IL-1Β in type 2 diabetes. Nat. Immunol. 2010, 11:897-904.
21. Koenen T.B., Stienstra R., van Tits L.J., Graaf J.de, Stalenhoef A.F., Joosten L.A., Tack C.J., Netea M.G. Hyperglycemia activates caspase-1 and TXNIP-mediated IL-1Β transcription in human adipose tissue. Diabetes 2011, 60:517-524.
22. Trueblood K.E., Mohr S., Dubyak G.R. Purinergic regulation of high glucose-induced caspase-1 activation in the rMC-1 rat retinal Muller cell line. Am. J. Physiol. Cell. Physiol. 2011, 301:C1213-C1223.
23. Sbai O., Devi T.S., Melone M.A., Feron F., Khrestchatisky M., Singh L.P., Perrone L. RAGE-TXNIP axis is required for S100B-promoted Schwann cell migration, fibronectin expression and cytokine secretion. J. Cell Sci. 2010, 123:4332-4339.
24. Lerner A.G., Upton J.P., Praveen P.V., Ghosh R., Nakagawa Y., Igbaria A., Shen S., Nguyen V., Backes B.J., Heiman M., Heintz N., Greengard P., Hui S., Tang Q., Trusina A., Oakes S.A., Papa F.R. IRE1α induces thioredoxin-interacting protein to activate the NLRP3 inflammasome andpromote programmed cell death under irremediable ER stress. Cell Metab. 2012, 16:250-264.
25. Oslowski C.M., Hara T., O'Sullivan-Murphy B., Kanekura K., Lu S., Hara M., Ishigaki S., Zhu L.J., Hayashi E., Hui S.T., Greiner D., Kaufman R.J., Bortell R., Urano F. Thioredoxin-interacting protein mediates ER stress-induced Β cell death through initiation of the inflammasome. Cell Metab. 2012, 16:265-273.
26. Kondo T., Hosoya K., Hori S., Tomi M., Ohtsuki S., Takanaga H., Nakashima E., Iizasa H., Asashima T., Ueda M., Obinata M., Terasaki T. Establishment of conditionally immortalized rat retinal pericyte cell lines (TR-rPCT) and their application in a co-culture system using retinal capillary endothelial cell line (TR-iBRB2). Cell Struct. Funct. 2003, 28:145-153.
27. Kador P.F., Randazzo J., Blessing K., Makita J., Zhang P., Yu K., Hosoya K., Terasaki T. Polyol formation in cell lines of rat retinal capillary pericytes and endothelial cells (TR-rPCT and TR-iBRB). J. Ocul. Pharmacol. Ther. 2009, 25:299-308.
28. Adachi T., Yasuda H., Aida K., Kamiya T., Hara H., Hosoya K., Terasaki T., Ikeda T. Regulation of extracellular-superoxide dismutase in rat retina pericytes. Redox Rep. 2010, 15:250-258.
29. Makita J., Hosoya K., Zhang P., Kador P.F. Response of rat retinal capillary pericytes and endothelial cells to glucose. J. Ocul. Pharmacol. Ther. 2011, 27:7-15.
30. Singh L.P., Devi T.S., Nantwi K.D. Theophylline regulates inflammatory and neurotrophic factor signals in functional recovery after C2-hemisection in adult rats. Exp. Neurol. 2012, 238:79-88.
31. Hara M.R., Snyder S.H. Nitric oxide-GAPDH-Siah: a novel cell death cascade. Cell Mol. Neurobiol. 2006, 26:527-538.
32. Sen N., Snyder S.H. Neurotrophin-mediated degradation of histone methyltransferase by S-nitrosylation cascade regulates neuronal differentiation. Proc. Nat. Acad. Sci. U.S.A. 2011, 108:20178-20183.
33. Busik J.V., Mohr S., Grant M.B. Hyperglycemia-induced reactive oxygen species toxicity to endothelial cells is dependent on paracrine mediators. Diabetes 2008, 57:1952-1965.
34. Ackrell B.A. Cytopathies involving mitochondrial complex II. Mol. Aspects Med. 2002, 23:369-384.
35. Sandhir R., Sood A., Mehrotra A., Kamboj S.S. N-Acetylcysteine reverses mitochondrial dysfunctions and behavioral abnormalities in 3-nitropropionic acid-induced Huntington's disease. Neurodegener. Dis. 2012, 9:145-157.
36. Morán M., Moreno-Lastres D., Marín-Buera L., Arenas J., Martín M.A., Ugalde C. Mitochondrial respiratory chain dysfunction: implications in neurodegeneration. Free Radical Biol. Med. 2012, 53:595-609.
37. Pellegrino M.W., Nargund A.M., Haynes C.M. Signaling the mitochondrial unfolded protein response. Biochim. Biophys. Acta 2012 Mar, 14. [Epub ahead of print].
38. Cabezas R., El-Bachá R.S., González J., Barreto G.E. Mitochondrial functions in astrocytes: neuroprotective implications from oxidative damage by rotenone. Neurosci. Res. 2012 Aug 10, [Epub ahead of print].
39. Trudeau K., Molina A.J., Roy S. High glucose induces mitochondrial morphology and metabolic changes in retinal pericytes. Invest. Ophthalmol. Vis. Sci. 2011, 52:8657-8664.
40. Jelenik T., Roden M. Mitochondrial plasticity in obesity and diabetes mellitus. Antioxid Redox Signal. 2012 Sep 3, [Epub ahead of print].
41. Barot M., Gokulgandhi M.R., Mitra A.K. Mitochondrial dysfunction in retinal diseases. Curr. Eye Res. 2011, 36:1069-1077.
42. Zhong Q., Kowluru R.A. Diabetic retinopathy and damage to mitochondrial structure and transport machinery. Invest. Ophthalmol. Vis. Sci. 2011, 52:8739-8746.
43. T.S. Devi, L.P. Singh, K.I. Hosoya, T. Terasaki, GSK-3Β/CREB axis mediates IGF-1-induced ECM/adhesion molecule expression, cell cycle progression and monolayer permeability in retinal capillary endothelial cells: implications for diabetic retinopathy. Biochim. Biophys. Acta, Mol. Basis Dis. 1812 (2011) 1080-1088.
44. Cheng D.W., Jiang Y., Shalev A., Kowluru R., Crook E.D., Singh L.P. An analysis of high glucose and glucosamine-induced gene expression and oxidative stress in renal mesangial cells. Arch. Physiol. Biochem. 2006, 112:189-218.
45. Zhong Y., Wang J.J., Zhang S.X. Intermittent but not constant high glucose induces ER stress and inflammation in human retinal pericytes. Adv. Exp. Med. Biol. 2012, 723:285-292.
46. Jauhiainen A., Thomsen C., Strömbom L., Grundevik P., Andersson C., Danielsson A., Andersson M.K., Nerman O., Rörkvist L., Ståhlberg A., Åman P. Distinct cytoplasmic and nuclear functions of the stress induced protein DDIT3/CHOP/GADD153. PLoS One 2012, 7:e33208.
47. Awai M., Koga T., Inomata Y., Oyadomari S., Gotoh T., Mori M., Tanihara H. NMDA-induced retinal injury is mediated by an endoplasmic reticulum stress-related protein, CHOP/GADD153. J. Neurochem. 2006, 96:43-52.
48. Ikesugi K., Mulhern M.L., Madson C.J., Hosoya K., Terasaki T., Kador P.F., Shinohara T. Induction of endoplasmic reticulum stress in retinal pericytes by glucose deprivation. Curr. Eye Res. 2006, 31:947-953.
49. Saxena G., Chen J., Shalev A. Intracellular shuttling and mitochondrial function of thioredoxin-interacting protein. J. Biol. Chem. 2010, 285:3997-4005.
50. Al-Gayyar M.M., Abdelsaid M.A., Matragoon S., Pillai B.A., El-Remessy A.B. Thioredoxin interacting protein is a novel mediator of retinal inflammation and neurotoxicity. Br. J. Pharmacol. 2011, 164:170-180.
51. Munemasa Y., Kwong J.M., Kim S.H., Ahn J.H., Caprioli J., Piri N. Thioredoxins 1 and 2 protect retinal ganglion cells from pharmacologically induced oxidative stress, optic nerve transection and ocular hypertension. Adv. Exp. Med. Biol. 2010, 664:355-363.
52. Li Q., Verma A., Han P.Y., Nakagawa T., Johnson R.J., Grant M.B., Campbell-Thompson M., Jarajapu Y.P., Lei B., Hauswirth W.W. Diabetic eNOS-knockout mice develop accelerated retinopathy. Invest. Ophthalmol. Vis. Sci. 2010, 51:5240-5246.
53. Giove T.J., Deshpande M.M., Gagen C.S., Eldred W.D. Increased neuronal nitric oxide synthase activity in retinal neurons in early diabetic retinopathy. Mol. Vis. 2009, 15:2249-2258.
54. Mishra A., Newman E.A. Inhibition of inducible nitric oxide synthase reverses the loss of functional hyperemia in diabetic retinopathy. Glia 2010, 58:1996-2004.
55. Zheng L., Du Y., Miller C., Gubitosi-Klug R.A., Ball S., Berkowitz B.A., Kern T.S. Critical role of inducible nitric oxide synthase in degeneration of retinal capillaries in mice with streptozotocin-induced diabetes. Diabetologia 2007, 50:1987-1996.
56. Lai Y.C., Pan K.T., Chang G.F., Hsu C.H., Khoo K.H., Hung C.H., Jiang Y.J., Ho F.M., Meng T.C. Nitrite-mediated S-nitrosylation of caspase-3 prevents hypoxia-induced endothelial barrier dysfunction. Circ. Res. 2011, 109:1375-1386.
57. Tian J., Kim S.F., Hester L., Snyder S.H. S-nitrosylation/activation of COX-2 mediates NMDA neurotoxicity. Proc. Nat. Acad. Sci. U.S.A. 2008, 105:10537-10540.
58. Li F., Sonveaux P., Rabbani Z.N., Liu S., Yan B., Huang Q., Vujaskovic Z., Dewhirst M.W., Li C.Y. Regulation of HIF-1alpha stability through S-nitrosylation. Mol. Cell. 2007, 13:63-74.
59. Hara M.R., Snyder S.H. Nitric oxide-GAPDH-Siah: a novel cell death cascade. Cell. Mol. Neurobiol. 2006, 26:527-538.
60. Sen N., Snyder S.H. Neurotrophin-mediated degradation of histone methyltransferase by S-nitrosylation cascade regulates neuronal differentiation. Proc. Nat. Acad. Sci. U.S.A. 2011, 108:20178-20183.
61. Yoshioka J., Chutkow W.A., Lee S., Kim J.B., Yan J., Tian R., Lindsey M.L., Feener E.P., Seidman C.E., Seidman J.G., Lee R.T. Deletion of thioredoxin-interacting protein in mice impairs mitochondrial function but protects the myocardium from ischemia-reperfusion injury. J. Clin. Invest. 2012, 122:267-279.
62. Oka S., Liu W., Yoshihara E., Ahsan M.K., Ramos D.A., Son A., Okuyama H., Zhang L., Masutani H., Nakamura H., Yodoi J. Thioredoxin binding protein-2 mediates metabolic adaptation in response to lipopolysaccharide in vivo. Crit. Care Med. 2010, 38:2345-2351.