Phagocyte-like NADPH oxidase [Nox2] in cellular dysfunction in models of glucolipotoxicity and diabetes

Biochemical Pharmacology

Volumn 88, Issue 3, 2014, Pages 275-283

  Kowluru, Anjaneyulu ^a,b   Kowluru, Renu A ^c,d  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b WAYNE STATE UNIVERSITY   (United States)

^c WAYNE STATE UNIVERSITY   (United States)

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

Author keywords

Cell death; Complications; Diabetes; Nox2; Rac1

Indexed keywords

4 AMINO 6 [2 [[4 (DIETHYLAMINO) 1 METHYLBUTYL]AMINO] 6 METHYL 4 PYRIMIDINYL] 2 METHYLQUINOLINE; GLYCOPROTEIN GP 91; PROTEIN P22; PROTEIN P40; PROTEIN P47; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2;

CELL DAMAGE; CELL MEMBRANE PERMEABILITY; CYTOSOL; DIABETES MELLITUS; DIABETIC CARDIOMYOPATHY; DIABETIC RETINOPATHY; ENDOTHELIUM CELL; HEART MUSCLE CELL; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INSULIN RELEASE; INSULIN RESISTANCE; LIPOTOXICITY; NONHUMAN; OXIDATIVE STRESS; PANCREAS ISLET BETA CELL; PHAGOCYTE; PRIORITY JOURNAL; RETINA; REVIEW;

CELL DEATH; COMPLICATIONS; DIABETES; NOX2; RAC1;

ANIMALS; CELL LINE; DIABETES MELLITUS; DIABETIC CARDIOMYOPATHIES; DIABETIC RETINOPATHY; ENZYME ACTIVATION; FATTY ACIDS; GLUCOSE; HUMANS; INSULIN; INSULIN RESISTANCE; INSULIN-SECRETING CELLS; MEMBRANE GLYCOPROTEINS; NADPH OXIDASE; OXIDATIVE STRESS; PHAGOCYTES;

EID: 84897008089     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2014.01.017     Document Type: Note

References (71)

1. IDF International Diabetes Federation - Diabetes Atlas 6th ed. 2013 1 160
2. V. Poitout, and R.P. Robertson Glucolipotoxicity: fuel excess and beta-cell dysfunction Endocr Rev 29 2008 351 366 (Pubitemid 351679704)
3. R. Blake, and I.A. Trounce Mitochondrial dysfunction and complications associated with diabetes Biochim Biophys Acta 2013 10.1016/j.bbagen.2013.11.007
4. S. Supale, N. Li, T. Brun, and P. Maechler Mitochondrial dysfunction in pancreatic beta-cells Trends Endocrinol Metab 23 2012 477 487
5. P. Newsholme, C. Gaidel, and M. Krause Mitochondria and diabetes. An intriguing pathogenetic role Adv Exp Med Biol 942 2012 235 247
6. K. Syeda, A.M. Mohammed, D.K. Arora, and A. Kowluru Glucotoxic conditions induce endoplasmic reticulum stress to cause caspase 3 mediated lamin B degradation in pancreatic β-cells: protection by nifedipine Biochem Pharmacol 86 2013 1338 1346
7. T. Kuijpers, and R. Lutter Inflammation and repeated infections in CGID: two sides of a coin Cell Mol Life Sci 69 2012 7 15
8. R.S. Frey, M. Ushio-Fukai, and A.B. Malik NADPH oxidase-dependent signaling in endothelial cells: role in physiology and pathophysiology Antioxid Redox Signal 11 2009 791 810
9. A. Kowluru Small G proteins in islet beta-cell function Endocr Rev 31 2010 52 78
10. P. Newsholme, E.P. Haber, S.M. Hirabara, E.L.O. Rebelato, J. Procopio, and D. Morgan et al. Diabetes associated cell stress and dysfunction: role of mitochondrial and nonmitochondrial ROS production and activity J Physiol 583 2007 9 24 (Pubitemid 47244241)
11. R. Veluthakal, S.V. Madathilperambil, P. McDonald, L.K. Olson, and A. Kowluru Regulatory roles for Tiam1, a guanine nucleotide exchange factor for Rac1, in glucose-stimulated insulin secretion in pancreatic beta-cells Biochem Pharmacol 77 2009 101 113
12. I. Syed, C.N. Kyathanahalli, and A. Kowluru Phagocyte-like NADPH oxidase generates ROS in INS 832/13 cells and rat islets: role of protein prenylation Am J Physiol Regul Integr Comp Physiol 300 2011 R756 R762
13. A. Matti, C. Kyathanahalli, and A. Kowluru Protein farnesylation is requisite for mitochondrial fuel-induced insulin release: further evidence to link reactive oxygen species generation to insulin secretion in pancreatic beta-cells Islets 4 2012 74 77
14. I. Syed, B. Jayaram, W. Subasinghe, and A. Kowluru Tiam1/Rac1 signaling pathway mediates palmitate-induced, ceramide-sensitive generation of superoxides and lipid peroxides and the loss of mitochondrial membrane potential in pancreatic beta-cells Biochem Pharmacol 80 2010 874 883
15. A. Kowluru Friendly, and not so friendly, roles of Rac1 in islet β-cell function: lessons learnt from pharmacological and molecular biological approaches Biochem Pharmacol 81 2011 965 975
16. W. Subasinghe, I. Syed, and A. Kowluru Phagocyte-like NADPH oxidase promotes cytokine-induced mitochondrial dysfunction in pancreatic β-cells: evidence for regulation by Rac1 Am J Physiol Regul Integr Comp Physiol 300 2011 R12 R20
17. H. Yuan, Y. Lu, X. Huang, Q. He, Y. Man, and Y. Zhou et al. Suppression of NADPH oxidase 2 substantially restores glucose-induced dysfunction of pancreatic NIT-1 cells FEBS J 277 2010 5061 5071
18. I. Syed, C.N. Kyathanahalli, B. Jayaram, S. Govind, C.J. Rhodes, and R.A. Kowluru et al. Increased phagocyte-like NADPH oxidase and ROS generation in type 2 diabetic ZDF rat and human islets: role of Rac1-JNK1/2 signaling pathway in mitochondrial dysregulation in the diabetic islet Diabetes 60 2011 2843 2852
19. E. Shen, Y. Li, Y. Li, L. Shan, H. Zhu, and Q. Feng et al. Rac1 is required for cardiomyocyte apoptosis during hyperglycemia Diabetes 58 2009 2386 2395
20. J. Li, H. Zhu, E. Shen, L. Wan, J.M. Arnold, and T. Peng Deficiency of rac1 blocks NADPH oxidase activation, inhibits endoplasmic reticulum stress, and reduces myocardial remodeling in a mouse model of type 1 diabetes Diabetes 59 2010 2033 2042
21. W. Yu, J. Wu, F. Cai, J. Xiang, W. Zha, and D. Fan et al. Curcumin alleviates diabetic cardiomyopathy in experimental diabetic rats PLOS ONE 7 2012 E52013
22. H.E. Tawfik, A.B. El-Remessy, S. Matragoon, G. Ma, R.B. Caldwell, and R.W. Caldwell Simvastatin improves diabetes-induced coronary endothelial dysfunction J Pharmacol Exp Ther 319 2006 386 395 (Pubitemid 44455146)
23. S.A. Metz, M.E. Rabaglia, J.B. Stock, and A. Kowluru Modulation of insulin secretion from normal rat islets by inhibitors of the post-translational modifications of GTP-binding proteins Biochem J 295 1993 31 40 (Pubitemid 23298304)
24. M. Al-Shabrawey, M. Rojas, T. Sanders, A. Behzadian, A. El-Remessy, and M. Bartoli et al. Role of NADPH oxidase in retinal vascular inflammation Invest Ophthalmol Vis Sci 49 2008 3239 3244
25. A. Othman, S. Ahmad, S. Megyerdi, R. Mussell, K. Choksi, and K.R. Maddipati et al. 12/15-lipoxygenase-derived lipid metabolites induce retinal endothelial barrier dysfunction: contribution of NADPH oxidase PLOS ONE 8 2 2013 e57254 10.1371/journal.pone.0057254
26. M. He, H. Pan, C. Xiao, and M. Pu Roles for redox signaling by NADPH oxidase in hyperglycemia-induced heme oxygenase-1 expression in the diabetic retina Invest Ophthalmol Vis Sci 54 2013 4092 4101
27. Y. Du, A. Veenstra, K. Palczewski, and T.S. Kern Photoreceptor cells are major contributors to oxidative stress and local inflammation in the retina Proc Natl Acad Sci U S A 110 2013 16586 16591
28. R. Kowluru, A. Kowluru, G. Mohammad, I. Syed, J.M. Santos, and R. Veluthakal Tiam1-Rac1 signaling axis mediated activation of NADPH oxidase-2 initiates mitochondrial damage in the development of diabetic retinopathy Diabetologia 2014 [in press]
29. P. Sukumar, H. Viswambharan, H. Imrie, R.M. Cubbon, N. Yuldasheva, and M. Gage et al. Nox2 NADPH oxidase has a critical role in insulin resistance-related endothelial cell dysfunction Diabetes 62 2013 2130 2134
30. Y. Gorin, and K. Block Nox as a target for diabetic complications Clin Sci (Lond) 125 2013 361 382
31. D.A. Taylor-Fishwick NOX, NOX who is there? The contribution of NADPH oxidase one to beta cell dysfunction Front Endocrinol (Lausanne) 4 2013 1 8
32. E. Cifuentes-Pagano, D.N. Meijles, and P.J. Pagano Sly as a Nox: the challenges, triumphs and pitfalls of selective NADPH Oxidase inhibition Antioxid Redox Signal 2013 10.1089/ars.2013.5620 [ahead of print]
33. J. El-Benna, P.M. Dang, and A. Périanin Towards specific NADPH oxidase inhibition by small synthetic peptides Cell Mol Life Sci 69 2012 2307 2314
34. J. El-Benna, P.M. Dang, and A. Périanin Peptide-based inhibitors of the phagocyte NADPH oxidase Biochem Pharmacol 80 2010 778 785
35. H.C. Williams, and K.K. Griendling NADPH oxidase inhibitors: new antihypertensive agents? J Cardiovasc Pharmacol 50 2007 9 16 (Pubitemid 47220441)
36. H.K. Bid, R.D. Roberts, P.K. Manchanda, and P.J. Houghton RAC1: an emerging therapeutic option for targeting cancer angiogenesis and metastasis Mol Cancer Ther 12 2013 1925 1934
37. A. Kowluru Protein prenylation in glucose-induced insulin secretion from the pancreatic islet beta-cell: a perspective J Cell Mol Med 12 2008 164 173
38. R. Veluthakal, H. Kaur, M. Goalstone, and A. Kowluru Dominant negative alpha subunit of farnesyl and geranyltransferase inhibits glucose-stimulated, but not KCl-stimulated insulin secretion in INS 832/13 cells Diabetes 56 2007 204 210
39. A. Kowluru, R. Veluthakal, C.J. Rhodes, V. Kamath, I. Syed, and B.J. Koch Protein farnesylation-dependent Raf/extracellular signal-related kinase signaling links to cytoskeletal remodeling to facilitate glucose-induced insulin secretion in pancreatic beta-cells Diabetes 59 2010 967 977
40. H.Q. Chen, M. Tannous, R. Veluthakal, R. Amin, and A. Kowluru Novel roles for palmitoylation of Ras in IL-1β-induced nitric oxide release and caspase-3 activation in insulin-secreting β-cells Biochem Pharmacol 66 2003 1681 1694 (Pubitemid 37249313)
41. I. Navarro-Lérida, S. Sánchez-Perales, M. Calvo, C. Rentero, Y. Zheng, and C. Enrich et al. A palmitoylation switch mechanism regulates Rac1 function and membrane organization EMBO J 31 2012 534 551
42. M.J. Bijlmakers, and M. Marsh The on-off story of protein palmitoylation Trends Cell Biol 13 2003 32 42 (Pubitemid 35453893)
43. S. Blaskovic, M. Blanc, and F.G. van der Goot What does S-palmitoylation do to membrane proteins FEBS J 280 2013 2766 2774
44. A.M. Mohammed, F. Chen, and A. Kowluru The two faces of protein palmitoylation in islet beta-cell function: potential implications in the pathophysiology of islet metabolic dysregulation and diabetes Recent Pat Endocr Metab Immune Drug Discov 7 2013 203 212
45. S.G. Straub, H. Yajima, M. Komatsu, T. Aizawa, and G.W. Sharp The effects of cerulenin, an inhibitor of protein acylation, on the two phases of glucose-stimulated insulin secretion Diabetes 51 Suppl. 1 2002 S91 S95
46. H. Yajima, M. Komatsu, S. Yamada, S.G. Straub, T. Kaneko, and Y. Sato et al. Cerulenin, an inhibitor of protein acylation, selectively attenuates nutrient stimulation of insulin release: a study in rat pancreatic islets Diabetes 49 2000 712 717 (Pubitemid 30339985)
47. L.D. Falo Jr., B. Benacerraf, L. Rothstein, and K.L. Rock Cerulenin is a potent inhibitor of antigen processing by antigen-presenting cells J Immunol 139 1987 3918 3923 (Pubitemid 18013677)
48. H.J. Gabius, M. van de Wouwer, S. Andre, and A. Villabolo Down regulation of epidermal growth factor receptor by altering N-glycosylation: emerging role for beta1,4-galactosyltransferases Anti Cancer Res 32 2012 1565 1572
49. B.C. Jennings, M.J. Nadolski, Y. Ling, M.B. Baker, M.L. Harrison, and R.J. Deschenes et al. 2-Bromopalmitate and 2-(2-hydroxy-5-nitro-benzylidene)- benzo[b]thiophen-3-one inhibit DHHC-mediated palmitoylation in vitro J Lipid Res 50 2009 233 242
50. A.M. Mohammed, K. Syeda, T. Hadden, and A. Kowluru Upregulation of phagocyte-like NADPH oxidase by cytokines in pancreatic beta-cells: attenuation of oxidative and nitrosative stress by 2-bromopalmitate Biochem Pharmacol 85 2013 109 114
51. A.C. Baldwin, C.D. Green, L.K. Olson, M.A. Moxley, and J.A. Corbett A role for aberrant protein palmitoylation in FFA-induced ER stress and β-cell death Am J Physiol Endocrinol Metab 302 2010 E1390 E1398
52. J. Tong, L. Li, B. Ballermann, and Z. Wang Phosphorylation of Rac1 T108 by ERK in response to EGF: a novel mechanism to regulate Rac1 function Mol Cell Biol 33 2013 4538 4551
53. T. Kwon, D.Y. Kwon, J. Chun, J.H. Kim, and S.S. Kang Akt protein kinase inhibits Rac1-GTP binding through phosphorylation at serine 71 of Rac1 J Biol Chem 275 2000 423 428 (Pubitemid 30039001)
54. J. Schwarz, J. Proff, A. Hävemeier, M. Ladwein, K. Rottner, and B. Barlag et al. Serine-71 phosphorylation of Rac1 modulates downstream PLOS ONE 7 2012 e44358
55. J. Schoentaube, A. Olling, H. Tatge, I. Just, and R. Gerhard Serine-71 phosphorylation of Rac1/Cdc42 diminishes the pathogenic effect of Clostridium difficile toxin A Cell Microbiol 11 2009 1816 1826
56. V. Brandes, I. Schelle, S. Brinkmann, F. Schulz, J. Schwarz, and R. Gerhard et al. Protection from Clostridium difficile toxin B-catalysed Rac1/Cdc42 glucosylation by tauroursodeoxycholic acid-induced Rac1/Cdc42 phosphorylation Biol Chem 393 2012 77 84
57. F. Chang, C. Lemmon, D. Lietha, M. Eck, and L. Romer Tyrosine phosphorylation of Rac1: a role in regulation of cell spreading PLoS ONE 6 2011 e28587
58. phox phosphorylation and Nox2 mobilization to the plasma membrane Semi Immunopathol 30 2008 279 289
59. F.R. Sheppard, M.R. Kelher, E.E. Moore, N.J. McLaughlin, A. Banerjee, and C.C. Silliman Structural organization of the neutrophil NADPH oxidase: phosphorylation and translocation during priming J Leukoc Biol 78 2005 1025 1042 (Pubitemid 41572466)
60. J. El-Benna, P.M. Dang, M.A. Gougerot-Pocidalo, J.C. Marie, and F. Braut-Boucher p47phox, the phagocyte NADPH oxidase/NOX2 organizer: structure, phosphorylation and implication in disease Exp Mol Med 41 2009 217 225
61. Y. Gao, J.B. Dickerson, F. Guo, J. Zheng, and Y. Zheng Rational design and characterization of a Rac GTPase-specific small molecule inhibitor Proc Natl Acad Sci U S A 101 2004 7618 7623 (Pubitemid 38658078)
62. B.L. Montalvo-Ortiz, L. Castillo-Pichardo, E. Hernandez, T. Humphries-Bickley, A. De la Mota-Peynado, and L.A. Cubano et al. Characterization of Ehop-016, a novel small molecule inhibitor of Rac GTPase J Biol Chem 287 2012 13228 13238
63. F.E. Rey, M.E. Cifuentes, A. Kiarash, M.T. Quinn, and P.J. Pagano Novel competitive inhibitor of NAD(P)H oxidase assembly attenuates vascular O(2)(-) and systolic blood pressure in mice Circ Res 89 2001 408 414 (Pubitemid 34132656)
64. E.E. Bosco, S. Kumar, F. Marchioni, J. Biesiada, M. Kordos, and K. Szczur et al. Rational design of small molecule inhibitors targeting the Rac GTPase-p67(phox) signaling axis in inflammation Chem Biol 19 2012 228 242
65. C.M. de Faria, A.C. Nazare, M.S. Petronio, L.C. Paracatu, M.L. Zeraic, and L.O. Regasini et al. Protocatechuic acid alkyl esters: hydrophobicity as a determinant factor for inhibition of NADPH oxidase Curr Med Chem 19 2012 4885 4893
66. M.E. Macías-Pérez, F. Martínez-Ramos, I.I. Padilla-Martínez, J. Correa-Basurto, L. Kispert, and J.E. Mendieta-Wejebe et al. Ethers and esters derived from apocynin avoid the interaction between p47phox and p22phox subunits of NADPH oxidase: evaluation in vitro and in silico Biosci Rep 33 4 2013
67. S. Suzuki, P. Pitchakarn, S. Sato, T. Shirai, and S. Takahashi Apocynin, an NADPH oxidase inhibitor, suppresses progression of prostate cancer via Rac1 dephosphorylation Exp Toxicol Pathol 65 2013 1035 1041
68. M. Levay, K.A. Krobert, K. Wittig, N. Voigt, M. Bermudez, and G. Wolber et al. NSC23766, a widely used inhibitor of Rac1 activation, additionally acts as a competitive antagonist at muscarinic acetylcholine receptors J Pharmacol Exp Ther 347 2013 69 79
69. M.P. Pedro, A.A. Vilcaes, V.M. Tomatis, R.G. Oliveira, and G.A. Gomez et al. 2-Bromopalmitate reduces protein deacylation by inhibition of acyl-protein thioesterase enzymatic activities PLOS ONE 8 2013 e75232
70. Y.H. You, S. Okada, S. Ly, K. Jandeleit-Dahm, D. Barit, and T. Namikoshi et al. Role of Nox2 in diabetic kidney disease Am J Physiol Renal Physiol 304 2013 F840 F848
71. M. Sedeek, R. Nasrallah, R.M. Touyz, and R.L. Hebert NADPH oxidases, reactive oxygen species, and the kidney: friend or foe J Am Soc Nephrol 24 2013 1512 1518