NOX5: From basic biology to signaling and disease

Free Radical Biology and Medicine

Volumn 52, Issue 4, 2012, Pages 725-734

  Bedard, Karen ^a   Jaquet, Vincent ^b   Krause, Karl Heinz ^b  

^a DALHOUSIE UNIVERSITY   (Canada)

^b UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

Author keywords

Free radicals; NADPH oxidase; NOX5; Reactive oxygen species

Indexed keywords

NOX 5 PROTEIN; OXIDOREDUCTASE; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; BARRETT ESOPHAGUS; BIOCHEMISTRY; BIOLOGY; CANCER CELL; CARDIOVASCULAR SYSTEM; DISEASE ASSOCIATION; ENDOTHELIUM CELL; ENZYME ACTIVITY; EVOLUTION; FETUS DEVELOPMENT; FIBROBLAST; HEALTH; HUMAN; IN SITU HYBRIDIZATION; LYMPH NODE; NEOPLASM; NONHUMAN; PANCREAS; PLACENTA; PREGNANCY; PRIORITY JOURNAL; PROSTATE; PROSTATE ADENOCARCINOMA; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; SMOOTH MUSCLE FIBER; SPERMATOGENESIS; SPLEEN; TESTIS; UMBILICAL CORD; UTERUS;

AMINO ACID SEQUENCE; ANIMALS; EVOLUTION, MOLECULAR; HUMANS; ISOENZYMES; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; NADPH OXIDASE; ORGAN SPECIFICITY; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEIN STRUCTURE, TERTIARY; SUPEROXIDES;

MAMMALIA; MUS; RATTUS;

EID: 84856224124     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2011.11.023     Document Type: Review

References (88)

1. O. Warburg Beobachtungen uber die Oxydationsprozesse im Seeigelei Z. Physiol. Chem. 57 1908 1 16
2. C.W. Baldridge, and R.W. Gerard The extra respiration of phagocytosis Am. J. Physiol. 103 1933
3. J. MacLeod The role of oxygen in the metabolism and motility of human spermatozoa Am. J. Physiol. 138 1943 512 518
4. B.M. Babior, J.D. Lambeth, and W. Nauseef The neutrophil NADPH oxidase Arch. Biochem. Biophys. 397 2002 342 344 (Pubitemid 34852301)
5. K. Bedard, and K.H. Krause The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology Physiol. Rev. 87 2007 245 313 (Pubitemid 46209993)
6. W.M. Nauseef Nox enzymes in immune cells Semin. Immunopathol. 30 2008 195 208
7. H. Sumimoto Structure, regulation and evolution of Nox-family NADPH oxidases that produce reactive oxygen species FEBS J. 275 2008 3249 3277 (Pubitemid 351813551)
8. Y.A. Suh, R.S. Arnold, B. Lassegue, J. Shi, X. Xu, D. Sorescu, A.B. Chung, K.K. Griendling, and J.D. Lambeth Cell transformation by the superoxide-generating oxidase Mox1 Nature 401 1999 79 82
9. + channel generated through alternative splicing of the NADPH oxidase homolog NOH-1 Science 287 2000 138 142 (Pubitemid 30033238)
10. B. Banfi, B. Malgrange, J. Knisz, K. Steger, M. Dubois-Dauphin, and K.H. Krause NOX3, a superoxide-generating NADPH oxidase of the inner ear J. Biol. Chem. 279 2004 46065 46072 (Pubitemid 39491600)
11. G. Cheng, Z. Cao, X. Xu, E.G. van Meir, and J.D. Lambeth Homologs of gp91phox: cloning and tissue expression of Nox3, Nox4, and Nox5 Gene 269 2001 131 140 (Pubitemid 32488913)
12. J.D. Lambeth, G. Cheng, R.S. Arnold, and W.A. Edens Novel homologs of gp91phox Trends Biochem. Sci. 25 2000 459 461
13. M. Geiszt, J.B. Kopp, P. Varnai, and T.L. Leto Identification of renox, an NAD(P)H oxidase in kidney Proc. Natl. Acad. Sci. U. S. A. 97 2000 8010 8014 (Pubitemid 30460764)
14. A. Shiose, J. Kuroda, K. Tsuruya, M. Hirai, H. Hirakata, S. Naito, M. Hattori, Y. Sakaki, and H. Sumimoto A novel superoxide-producing NAD(P)H oxidase in kidney J. Biol. Chem. 276 2001 1417 1423 (Pubitemid 32096573)
15. 2+-activated NADPH oxidase in testis, spleen, and lymph nodes J. Biol. Chem. 276 2001 37594 37601
16. X. De Deken, D. Wang, M.C. Many, S. Costagliola, F. Libert, G. Vassart, J.E. Dumont, and F. Miot Cloning of two human thyroid cDNAs encoding new members of the NADPH oxidase family J. Biol. Chem. 275 2000 23227 23233 (Pubitemid 30646220)
17. C. Dupuy, R. Ohayon, A. Valent, M.S. Noel-Hudson, D. Deme, and A. Virion Purification of a novel flavoprotein involved in the thyroid NADPH oxidase: cloning of the porcine and human cDNAs J. Biol. Chem. 274 1999 37265 37269
18. B. Banfi, R.A. Clark, K. Steger, and K.H. Krause Two novel proteins activate superoxide generation by the NADPH oxidase NOX1 J. Biol. Chem. 278 2003 3510 3513 (Pubitemid 36801072)
19. M. Geiszt, K. Lekstrom, J. Witta, and T.L. Leto Proteins homologous to p47phox and p67phox support superoxide production by NAD(P)H oxidase 1 in colon epithelial cells J. Biol. Chem. 278 2003 20006 20012 (Pubitemid 36799193)
20. N. Ueno, R. Takeya, K. Miyano, H. Kikuchi, and H. Sumimoto The NADPH oxidase Nox3 constitutively produces superoxide in a p22phox-dependent manner: its regulation by oxidase organizers and activators J. Biol. Chem. 280 2005 23328 23339 (Pubitemid 40853246)
21. L. Serrander, L. Cartier, K. Bedard, B. Banfi, B. Lardy, O. Plastre, A. Sienkiewicz, L. Forro, W. Schlegel, and K.H. Krause NOX4 activity is determined by mRNA levels and reveals a unique pattern of ROS generation Biochem. J. 406 2007 105 114 (Pubitemid 47264740)
22. J. Aguirre, and J.D. Lambeth Nox enzymes from fungus to fly to fish and what they tell us about Nox function in mammals Free Radic. Biol. Med. 49 2010 1342 1353
23. T. Kawahara, M.T. Quinn, and J.D. Lambeth Molecular evolution of the reactive oxygen-generating NADPH oxidase (Nox/Duox) family of enzymes BMC Evol. Biol. 7 2007 109
24. K. Bedard, B. Lardy, and K.H. Krause NOX family NADPH oxidases: not just in mammals Biochimie 89 2007 1107 1112 (Pubitemid 47248001)
25. B. Lardy, M. Bof, L. Aubry, M.H. Paclet, F. Morel, M. Satre, and G. Klein NADPH oxidase homologs are required for normal cell differentiation and morphogenesis in Dictyostelium discoideum Biochim. Biophys. Acta 1744 2005 199 212 (Pubitemid 40798925)
26. H.M. Wain, E.A. Bruford, R.C. Lovering, M.J. Lush, M.W. Wright, and S. Povey Guidelines for human gene nomenclature Genomics 79 2002 464 470 (Pubitemid 34274283)
27. K. Bedard, H. Attar, J. Bonnefont, V. Jaquet, C. Borel, O. Plastre, M.J. Stasia, S.E. Antonarakis, and K.H. Krause Three common polymorphisms in the CYBA gene form a haplotype associated with decreased ROS generation Hum. Mutat. 30 2009 1123 1133
28. 2+ activation of the NADPH oxidase 5 (NOX5) J. Biol. Chem. 279 2004 18583 18591 (Pubitemid 38623279)
29. D.J.R. Fulton Nox5 and the regulation of cellular function Antioxid. Redox Signal 11 2009 2443 2452
30. A. El Chemaly, Y. Okochi, M. Sasaki, S. Arnaudeau, Y. Okamura, and N. Demaurex VSOP/Hv1 proton channels sustain calcium entry, neutrophil migration, and superoxide production by limiting cell depolarization and acidification J. Exp. Med. 207 2010 129 139
31. 2+-dependent high-affinity complex formation between calmodulin and melittin Biochem. J. 209 1983 269 272 (Pubitemid 13153662)
32. R.F. Steiner, and L. Norris The interaction of melittin with troponin C Arch. Biochem. Biophys. 254 1987 342 352 (Pubitemid 17068826)
33. C.C. Wei, N. Motl, K. Levek, L.Q. Chen, Y.P. Yang, T. Johnson, L. Hamilton, and D.J. Stuehr Conformational states and kinetics of the calcium binding domain of NADPH oxidase 5 Open Biochem. J. 4 2010 59 67
34. Z. Grabarek Insights into modulation of calcium signaling by magnesium in calmodulin, troponin C and related EF-hand proteins Biochim. Biophys. Acta 1813 2011 913 921
35. F. Tirone, L. Radu, C.T. Craescu, and J.A. Cox Identification of the binding site for the regulatory calcium-binding domain in the catalytic domain of NOX5 Biochemistry 49 2010 761 771
36. D. Jagnandan, J.E. Church, B. Banfi, D.J. Stuehr, M.B. Marrero, and D.J.R. Fulton Novel mechanism of activation of NADPH oxidase 5-calcium sensitization via phosphorylation J. Biol. Chem. 282 2007 6494 6507 (Pubitemid 47100887)
37. L. Serrander, V. Jaquet, K. Bedard, O. Plastre, O. Hartley, S. Arnaudeau, N. Demaurex, W. Schlegel, and K.H. Krause NOX5 is expressed at the plasma membrane and generates superoxide in response to protein kinase C activation Biochimie 89 2007 1159 1167 (Pubitemid 47248008)
38. G.M. Bokoch, B. Diebold, J.S. Kim, and D. Gianni Emerging evidence for the importance of phosphorylation in the regulation of NADPH oxidases Antioxid. Redox Signal 11 2009 2429 2441
39. D. Pandey, and D.J. Fulton Molecular regulation of NADPH oxidase 5 via the MAPK pathway Am. J. Physiol. Heart Circ. Physiol. 300 2011 H1336 1344
40. D. Pandey, J.P. Gratton, R. Rafikov, S.M. Black, and D. Fulton Calcium/calmodulin-dependent kinase II mediates the phosphorylation and activation of NADPH oxidase 5 Mol. Pharmacol. 80 2011 407 415
41. F. Tirone, and J.A. Cox NADPH oxidase 5 (NOX5) interacts with and is regulated by calmodulin FEBS Lett. 581 2007 1202 1208 (Pubitemid 46385949)
42. A.C. Montezano, D. Burger, T.M. Paravicini, A.Z. Chignalia, H. Yusuf, M. Almasri, Y. He, G.E. Callera, G. He, K.H. Krause, D. Lambeth, M.T. Quinn, and R.M. Touyz Nicotinamide adenine dinucleotide phosphate reduced oxidase 5 (Nox5) regulation by angiotensin II and endothelin-1 is mediated via calcium/calmodulin-dependent, Rac-1-independent pathways in human endothelial cells Circ. Res. 106 2010 1363 1373
43. A. El Jamali, A.J. Valente, J.D. Lechleiter, M.J. Gamez, D.W. Pearson, W.M. Nauseef, and R.A. Clark Novel redox-dependent regulation of NOX5 by the tyrosine kinase c-Abl Free Radic. Biol. Med. 44 2008 868 881
44. T. Kawahara, and J.D. Lambeth Phosphatidylinositol (4,5)-bisphosphate modulates Nox5 localization via an N-terminal polybasic region Mol. Biol. Cell 19 2008 4020 4031
45. T. Kawahara, H.M. Jackson, S.M. Smith, P.D. Simpson, and J.D. Lambeth Nox5 forms a functional oligomer mediated by self-association of its dehydrogenase domain Biochemistry 50 2011 2013 2025
46. T.J. Guzik, W. Chen, M.C. Gongora, B. Guzik, H.E. Lob, D. Mangalat, N. Hoch, S. Dikalov, P. Rudzinski, B. Kapelak, J. Sadowski, and D.G. Harrison Calcium-dependent NOX5 nicotinamide adenine dinucleotide phosphate oxidase contributes to vascular oxidative stress in human coronary artery disease J. Am. Coll. Cardiol. 52 2008 1803 1809
47. S.S. Brar, Z. Corbin, T.P. Kennedy, R. Hemendinger, L. Thornton, B. Bommarius, R.S. Arnold, A.R. Whorton, A.B. Sturrock, T.P. Huecksteadt, M.T. Quinn, K. Krenitsky, K.G. Ardie, J.D. Lambeth, and J.R. Hoidal NOX5 NAD(P)H oxidase regulates growth and apoptosis in DU 145 prostate cancer cells Am. J. Physiol. Cell Physiol. 285 2003 C353 C369
48. X.Y. Fu, D.G. Beer, J. Behar, J. Wands, D. Lambeth, and W.B. Cao cAMP-response element-binding protein mediates acid-induced NADPH oxidase NOX5-S expression in Barrett esophageal adenocarcinoma cells J. Biol. Chem. 281 2006 20368 20382 (Pubitemid 44065811)
49. A.S. Kamiguti, L. Serrander, K. Lin, R.J. Harris, J.C. Cawley, D.J. Allsup, J.R. Slupsky, K.H. Krause, and M. Zuzel Expression and activity of NOX5 in the circulating malignant B cells of hairy cell leukemia J. Immunol. 175 2005 8424 8430 (Pubitemid 41798410)
50. J. Tosic, and A. Walton Formation of hydrogen peroxide by spermatozoa and its inhibitory effect of respiration Nature 158 1946 485
51. R.J. Aitken, and B.J. Curry Redox regulation of human sperm function: from the physiological control of sperm capacitation to the etiology of infertility and DNA damage in the germ line Antioxid. Redox Signal 14 2011 367 381
52. I. Bize, G. Santander, P. Cabello, D. Driscoll, and C. Sharpe Hydrogen peroxide is involved in hamster sperm capacitation in vitro Biol. Reprod. 44 1991 398 403
53. R.J. Aitken, M.A. Baker, G.N. De Iuliis, and B. Nixon New insights into sperm physiology and pathology Handb. Exp. Pharmacol. 198 2010 99 115
54. P.V. Lishko, I.L. Botchkina, A. Fedorenko, and Y. Kirichok Acid extrusion from human spermatozoa is mediated by flagellar voltage-gated proton channel Cell 140 2010 327 337
55. M. Capasso, T.E. DeCoursey, and M.J. Dyer pH regulation and beyond: unanticipated functions for the voltage-gated proton channel, HVCN1 Trends Cell Biol. 21 2010 20 28
56. P.V. Lishko, and Y. Kirichok The role of Hv1 and CatSper channels in sperm activation J. Physiol. 588 2010 4667 4672
57. R.J. Aitken, D.W. Buckingham, and K.M. West Reactive oxygen species and human spermatozoa: analysis of the cellular mechanisms involved in luminol- and lucigenin-dependent chemiluminescence J. Cell. Physiol. 151 1992 466 477
58. P. Vernet, N. Fulton, C. Wallace, and R.J. Aitken Analysis of reactive oxygen species generating systems in rat epididymal spermatozoa Biol. Reprod. 65 2001 1102 1113 (Pubitemid 32927575)
59. A.J. Koppers, G.N. De Iuliis, J.M. Finnie, E.A. McLaughlin, and R.J. Aitken Significance of mitochondrial reactive oxygen species in the generation of oxidative stress in spermatozoa J. Clin. Endocrinol. Metab. 93 2008 3199 3207
60. K. Whittington, and W.C. Ford Relative contribution of leukocytes and of spermatozoa to reactive oxygen species production in human sperm suspensions Int. J. Androl. 22 1999 229 235 (Pubitemid 29361236)
61. I. Oborna, H. Fingerova, J. Novotny, J. Brezinova, M. Svobodova, and N. Aziz Reactive oxygen species in human semen in relation to leukocyte contamination Biomed. Pap. Med. Fac. Univ. Palacky Olomouc Czech Repub. 153 2009 53 57
62. E. Gomez, D.W. Buckingham, J. Brindle, F. Lanzafame, D.S. Irvine, and R.J. Aitken Development of an image analysis system to monitor the retention of residual cytoplasm by human spermatozoa: correlation with biochemical markers of the cytoplasmic space, oxidative stress, and sperm function J. Androl. 17 1996 276 287
63. M.R. Moein, V.O. Dehghani, N. Tabibnejad, and S. Vahidi Reactive oxygen species (ROS) level in seminal plasma of infertile men and healthy donors Iran. J. Reprod. Med. 5 2007 51 55
64. K.S. Athayde, M. Cocuzza, A. Agarwal, N. Krajcir, A.M. Lucon, M. Srougi, and J. Hallak Development of normal reference values for seminal reactive oxygen species and their correlation with leukocytes and semen parameters in a fertile population J. Androl. 28 2007 613 620 (Pubitemid 47057045)
65. R.J. Aitken, and G.N. De Iuliis Role of oxidative stress in the etiology of sperm DNA damage A. Zini, A. Agarwal, Sperm Chromatin 2011 Springer New York 277 293
66. L. Myatt, and X. Cui Oxidative stress in the placenta Histochem. Cell Biol. 122 2004 369 382 (Pubitemid 39506594)
67. X.L. Cui, B.J. Chang, and L. Myatt Expression and distribution of NADPH oxidase isoforms in human myometrium-role in angiotensin II-induced hypertrophy Biol. Reprod. 82 2010 305 312
68. J. Si, J. Hong, J. Behar, J.R. Wands, R.F. Souza, S.J. Spechler, J.D. Lambeth, and W.B. Cao NADPH oxidase NOX5-S mediates cyclin D1 expression in Barrett's esophageal adenocarcinoma cells Gastroenterology 134 2008 A441
69. R.S. BelAiba, T. Djordjevic, A. Petry, K. Diemer, S. Bonello, B. Banfi, J. Hess, A. Pogrebniak, C. Bickel, and A. Gorlach NOX5 variants are functionally active in endothelial cells Free Radic. Biol. Med. 42 2007 446 459 (Pubitemid 46162114)
70. R.P. Brandes, N. Weissmann, and K. Schroder NADPH oxidases in cardiovascular disease Free Radic. Biol. Med. 49 2010 687 706
71. M. Sedeek, R.L. Hebert, C.R. Kennedy, K.D. Burns, and R.M. Touyz Molecular mechanisms of hypertension: role of Nox family NADPH oxidases Curr. Opin. Nephrol. Hypertens. 18 2009 122 127
72. D.G. Harrison, and M.C. Gongora Oxidative stress and hypertension Med. Clin. North Am. 93 2009 621 635
73. S. Selemidis, C.G. Sobey, K. Wingler, H.H. Schmidt, and G.R. Drummond NADPH oxidases in the vasculature: molecular features, roles in disease and pharmacological inhibition Pharmacol. Ther. 120 2008 254 291
74. G. San Jose, A. Fortuno, O. Beloqui, J. Diez, and G. Zalba NADPH oxidase CYBA polymorphisms, oxidative stress and cardiovascular diseases Clin. Sci. (London) 114 2008 173 182 (Pubitemid 351293993)
75. B. Lassegue, and K.K. Griendling NADPH oxidases: functions and pathologies in the vasculature Arterioscler. Thromb. Vasc. Biol. 30 2010 653 661
76. M.C. Alvarez, C. Caldiz, J.C. Fantinelli, C.D. Garciarena, G.M. Console, G.E. Chiappe de Cingolani, and S.M. Mosca Is cardiac hypertrophy in spontaneously hypertensive rats the cause or the consequence of oxidative stress? Hypertens. Res. 31 2008 1465 1476
77. F. Lacy, M.T. Kailasam, D.T. O'Connor, G.W. Schmid-Schonbein, and R.J. Parmer Plasma hydrogen peroxide production in human essential hypertension: role of heredity, gender, and ethnicity Hypertension 36 2000 878 884
78. R.M. Touyz, and E.L. Schiffrin Increased generation of superoxide by angiotensin II in smooth muscle cells from resistance arteries of hypertensive patients: role of phospholipase D-dependent NAD(P)H oxidase-sensitive pathways J. Hypertens. 19 2001 1245 1254 (Pubitemid 32595280)
79. R.E. Clempus, D. Sorescu, A.E. Dikalova, L. Pounkova, P. Jo, G.P. Sorescu, H.H. Schmidt, B. Lassegue, and K.K. Griendling Nox4 is required for maintenance of the differentiated vascular smooth muscle cell phenotype Arterioscler. Thromb. Vasc. Biol. 27 2007 42 48 (Pubitemid 46360379)
80. G. Gavazzi, B. Banfi, C. Deffert, L. Fiette, M. Schappi, F. Herrmann, and K.H. Krause Decreased blood pressure in NOX1-deficient mice FEBS Lett. 580 2006 497 504 (Pubitemid 43089678)
81. K. Matsuno, H. Yamada, K. Iwata, D. Jin, M. Katsuyama, M. Matsuki, S. Takai, K. Yamanishi, M. Miyazaki, H. Matsubara, and C. Yabe-Nishimura Nox1 is involved in angiotensin II-mediated hypertension: a study in Nox1-deficient mice Circulation 112 2005 2677 2685 (Pubitemid 41532605)
82. D.B. Jay, C.A. Papaharalambus, B. Seidel-Rogol, A.E. Dikalova, B. Lassegue, and K.K. Griendling Nox5 mediates PDGF-induced proliferation in human aortic smooth muscle cells Free Radic. Biol. Med. 45 2008 329 335
83. B. van Loon, E. Markkanen, and U. Hubscher Oxygen as a friend and enemy: how to combat the mutational potential of 8-oxo-guanine DNA Repair (Amsterdam) 9 2010 604 616
84. B. Kumar, S. Koul, L. Khandrika, R.B. Meacham, and H.K. Koul Oxidative stress is inherent in prostate cancer cells and is required for aggressive phenotype Cancer Res. 68 2008 1777 1785 (Pubitemid 351416563)
85. J. Hong, M. Resnick, J. Behar, L.J. Wang, J. Wands, R.A. DeLellis, R.F. Souza, S.J. Spechler, and W.B. Cao Acid-induced p16 hypermethylation contributes to development of esophageal adenocarcinoma via activation of NADPH oxidase NOX5-S Am. J. Physiol. Gastrointest. Liver Physiol. 299 2010 G697 G706
86. A. Juhasz, Y. Ge, S. Markel, A. Chiu, L. Matsumoto, J. van Balgooy, K. Roy, and J.H. Doroshow Expression of NADPH oxidase homologues and accessory genes in human cancer cell lines, tumours and adjacent normal tissues Free Radic. Res. 43 2009 523 532
87. V. Jaquet, J. Marcoux, E. Forest, K.G. Leidal, S. McCormick, Y. Westermaier, R. Perozzo, O. Plastre, L. Fioraso-Cartier, B. Diebold, L. Scapozza, W.M. Nauseef, F. Fieschi, K.H. Krause, and K. Bedard NADPH oxidase (NOX) isoforms are inhibited by celastrol with a dual mode of action Br. J. Pharmacol. 164 2011 507 520
88. S. Wind, K. Beuerlein, T. Eucker, H. Muller, P. Scheurer, M.E. Armitage, H. Ho, H.H. Schmidt, and K. Wingler Comparative pharmacology of chemically distinct NADPH oxidase inhibitors Br. J. Pharmacol. 161 2010 885 898