Selective recapitulation of conserved and nonconserved regions of putative noxa1 protein activation domain confers isoform-specific inhibition of nox1 oxidase and attenuation of endothelial cell migration

Journal of Biological Chemistry

Volumn 288, Issue 51, 2013, Pages 36437-36450

  Ranayhossaini, Daniel J ^a,b   Rodriguez, Andres I ^a,b   Sahoo, Sanghamitra ^b   Chen, Beibei B ^c   Mallampalli, Rama K ^c,d   Kelley, Eric E ^a,b   Csanyi, Gabor ^a,b   Gladwin, Mark T ^a,c   Romero, Guillermo ^b   Pagano, Patrick J ^a,b  

^a Vascular Medicine Institute and Departments   (United States)

^b Pharmacology and Chemical Biology   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLON CARCINOMA; OXIDANT SOURCES; POTENTIAL THERAPIES; PROTEIN ACTIVATION; VASCULAR DISEASE;

DISEASE CONTROL; ENDOTHELIAL CELLS; OXIDANTS;

CHEMICAL ACTIVATION;

CYTOCHROME C; ENZYME INHIBITOR; NOXA1 PROTEIN; NOXA1DS PROTEIN; OXIDOREDUCTASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 5; SUPEROXIDE; UNCLASSIFIED DRUG; XANTHINE OXIDASE;

ARTERY ENDOTHELIUM; ARTICLE; CANCER CELL; CELL MEMBRANE; CELL MIGRATION; COLON ADENOCARCINOMA; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME INHIBITION; HUMAN; HUMAN CELL; HYPOXIA; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEIN SUBUNIT; PULMONARY ARTERY;

ENZYME INHIBITORS; ENZYME MECHANISMS; NADPH OXIDASE; NOX1; PEPTIDES; REACTIVE OXYGEN SPECIES (ROS);

ADAPTOR PROTEINS, VESICULAR TRANSPORT; AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CATALYTIC DOMAIN; CELL MEMBRANE; CELL MOVEMENT; CERCOPITHECUS AETHIOPS; CONSERVED SEQUENCE; COS CELLS; ENDOTHELIAL CELLS; ENZYME ACTIVATION; HT29 CELLS; HUMANS; ISOENZYMES; MOLECULAR SEQUENCE DATA; MUTATION; NADPH OXIDASE; PROTEIN BINDING; PULMONARY ARTERY; SUPEROXIDES;

EID: 84890935863     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.521344     Document Type: Article

References (57)

1. Al Ghouleh, I., Khoo, N. K., Knaus, U. G., Griendling, K. K., Touyz, R. M., Thannickal, V. J., Barchowsky, A., Nauseef, W. M., Kelley, E. E., Bauer, P. M., Darley-Usmar, V., Shiva, S., Cifuentes-Pagano, E., Freeman, B. A., Gladwin, M. T., and Pagano, P. J. (2011) Oxidases and peroxidases in cardiovascular and lung disease: Few concepts in reactive oxygen species signaling. Free Radic. Biol. Med. 51, 1271-1288
2. Kuzkaya, N., Weissmann, N., Harrison, D. G., and Dikalov, S. (2003) Interactions of peroxynitrite, tetrahydrobiopterin, ascorbic acid, and thiols: Implications for uncoupling endothelial nitric-oxide synthase. J. Biol. Chem. 278, 22546-22554
3. White, C. R., Brock, T. A., Chang, L. Y., Crapo, J., Briscoe, P., Ku, D., Bradley, W. A., Gianturco, S. H., Gore, J., Freeman, B. A., and et al. (1994) Superoxide and peroxynitrite in atherosclerosis. Proc. Natl. Acad. Sci. U.S.A. 91, 1044-1048
4. Beckman, J. S., Beckman, T. W., Chen, J., Marshall, P. A., and Freeman, B. A. (1990) Apparent hydroxyl radical production by peroxynitrite: Implications for endothelial injury from nitric oxide and superoxide. Proc. Natl. Acad. Sci. U.S.A. 87, 1620-1624
5. 2-mediated oxidation and inactivation of phosphatases in growth factor signaling. Proc. Natl. Acad. Sci. U.S.A. 105, 7147-7152
6. Cardey, B., Foley, S., and Enescu, M. (2007) Mechanism of thiol oxidation by the superoxide radical. J. Phys. Chem. A 111, 13046-13052
7. Winterbourn, C. C., and Metodiewa, D. (1999) Reactivity of biologically important thiol compounds with superoxide and hydrogen peroxide. Free Radic. Biol. Med. 27, 322-328
8. McCord, J. M., and Fridovich, I. (1969) Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J. Biol. Chem. 244, 6049-6055
9. Sedeek, M., Hébert, R. L., Kennedy, C. R., Burns, K. D., and Touyz, R. M. (2009) Molecular mechanisms of hypertension: Role of Nox family NADPH oxidases. Curr. Opin. Nephrol. Hypertens. 18, 122-127
10. Lassègue, B., and Clempus, R. E. (2003) Vascular NAD(P)H oxidases: Specific features, expression, and regulation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 285, R277-R297
11. Ambasta, R. K., Kumar, P., Griendling, K. K., Schmidt, H. H., Busse, R., and Brandes, R. P. (2004) Direct interaction of the novel Nox proteins with p22phox is required for the formation of a functionally active NADPH oxidase. J. Biol. Chem. 279, 45935-45941
12. Leto, T. L., Garrett, M. C., Fujii, H., and Nunoi, H. (1991) Characterization of neutrophil NADPH oxidase factors p47-phox and p67-phox from recombinant baculoviruses. J. Biol. Chem. 266, 19812-19818
13. 2+ activation of the NADPH oxidase 5 (NOX5). J. Biol. Chem. 279, 18583-18591
14. Lyle, A. N., Deshpande, N. N., Taniyama, Y., Seidel-Rogol, B., Pounkova, L., Du, P., Papaharalambus, C., Lassègue, B., and Griendling, K. K. (2009) Poldip2, a novel regulator of Nox4 and cytoskeletal integrity in vascular smooth muscle cells. Circ. Res. 105, 249-259
15. Bánfi, B., Clark, R. A., Steger, K., and Krause, K. H. (2003) Two novel proteins activate superoxide generation by the NADPH oxidase NOX1. J. Biol. Chem. 278, 3510-3513
16. Han, C. H., Freeman, J. L., Lee, T., Motalebi, S. A., and Lambeth, J. D. (1998) Regulation of the neutrophil respiratory burst oxidase. Identification of an activation domain in p67(phox). J. Biol. Chem. 273, 16663-16668
17. Ambasta, R. K., Schreiber, J. G., Janiszewski, M., Busse, R., and Brandes, R. P. (2006) Noxa1 is a central component of the smooth muscle NADPH oxidase in mice. Free Radic. Biol. Med. 41, 193-201
18. Maehara, Y., Miyano, K., Yuzawa, S., Akimoto, R., Takeya, R., and Sumimoto, H. (2010) A conserved region between the TPR and activation domains of p67phox participates in activation of the phagocyte NADPH oxidase. J. Biol. Chem. 285, 31435-31445
19. Suh, Y. A., Arnold, R. S., Lassegue, B., Shi, J., Xu, X., Sorescu, D., Chung, A. B., Griendling, K. K., and Lambeth, J. D. (1999) Cell transformation by the superoxide-generating oxidase Mox1. Nature 401, 79-82
20. Csányi, G., Taylor, W. R., and Pagano, P. J. (2009) NOX and inflammation in the vascular adventitia. Free Radic. Biol. Med. 47, 1254-1266
21. Corcionivoschi, N., Alvarez, L. A., Sharp, T. H., Strengert, M., Alemka, A., Mantell, J., Verkade, P., Knaus, U. G., and Bourke, B. (2012) Mucosal reactive oxygen species decrease virulence by disrupting Campylobacter jejuni phosphotyrosine signaling. Cell Host Microbe 12, 47-59
22. Arbiser, J. L., Petros, J., Klafter, R., Govindajaran, B., McLaughlin, E. R., Brown, L. F., Cohen, C., Moses, M., Kilroy, S., Arnold, R. S., and Lambeth, J. D. (2002) Reactive oxygen generated by Nox1 triggers the angiogenic switch. Proc. Natl. Acad. Sci. U.S.A. 99, 715-720
23. Ushio-Fukai, M., and Nakamura, Y. (2008) Reactive oxygen species and angiogenesis: NADPH oxidase as target for cancer therapy. Cancer Lett. 266, 37-52
24. Garrido-Urbani, S., Jemelin, S., Deffert, C., Carnesecchi, S., Basset, O., Szyndralewiez, C., Heitz, F., Page, P., Montet, X., Michalik, L., Arbiser, J., Rüegg, C., Krause, K. H., Imhof, B. A., and Imhof, B. (2011) Targeting vascular NADPH oxidase 1 blocks tumor angiogenesis through a PPARα mediated mechanism. PLoS One 6, e14665
25. Ardanaz, N., and Pagano, P. J. (2006) Hydrogen peroxide as a paracrine vascular mediator: Regulation and signaling leading to dysfunction. Exp. Biol. Med. 231, 237-251
26. Cascino, T., Csanyi, G., Al Ghouleh, I., Montezano, A. C., Touyz, R. M., Haurani, M. J., and Pagano, P. J. (2011) Adventitia-derived hydrogen peroxide impairs relaxation of the rat carotid artery via smooth muscle cell p38 mitogen-Activated protein kinase. Antioxid. Redox Signal. 15, 1507-1515
27. Csányi, G., Yao, M., Rodríguez, A. I., Al Ghouleh, I., Sharifi-Sanjani, M., Frazziano, G., Huang, X., Kelley, E. E., Isenberg, J. S., and Pagano, P. J. (2012) Thrombospondin-1 regulates blood flow via CD47 receptor-mediated activation of NADPH oxidase 1. Arterioscler. Thromb. Vasc. Biol. 32, 2966-2973
28. Jacobson, G. M., Dourron, H. M., Liu, J., Carretero, O. A., Reddy, D. J., Andrzejewski, T., and Pagano, P. J. (2003) Novel NAD(P)H oxidase inhibitor suppresses angioplasty-induced superoxide and neointimal hyperplasia of rat carotid artery. Circ. Res. 92, 637-643
29. Dikalova, A., Clempus, R., Lassègue, B., Cheng, G., McCoy, J., Dikalov, S., San Martin, A., Lyle, A., Weber, D. S., Weiss, D., Taylor, W. R., Schmidt, H. H., Owens, G. K., Lambeth, J. D., and Griendling, K. K. (2005) Nox1 overexpression potentiates angiotensin II-induced hypertension and vascular smooth muscle hypertrophy in transgenic mice. Circulation 112, 2668-2676
30. Zhang, X., Goncalves, R., and Mosser, D. M. (2008) Curr. Protoc. Immunol. Chapter 14, Unit 14.11
31. Cheng, G., Cao, Z., Xu, X., van Meir, E. G., and Lambeth, J. D. (2001) Homologs of gp91phox: Cloning and tissue expression of Nox3, Nox4, and Nox5. Gene 269, 131-140
32. Cheng, G., and Lambeth, J. D. (2004) NOXO1, regulation of lipid binding, localization, and activation of Nox1 by the Phox homology (PX) domain. J. Biol. Chem. 279, 4737-4742
33. Vilardaga, J. P., Nikolaev, V. O., Lorenz, K., Ferrandon, S., Zhuang, Z., and Lohse, M. J. (2008) Conformational cross-talk between α2A-Adrenergic and μ-opioid receptors controls cell signaling. Nat. Chem. Biol. 4, 126-131
34. Csányi, G., Cifuentes-Pagano, E., Al Ghouleh, I., Ranayhossaini, D. J., Egaña, L., Lopes, L. R., Jackson, H. M., Kelley, E. E., and Pagano, P. J. (2011) Nox2 B-loop peptide, Nox2ds, specifically inhibits the NADPH oxidase Nox2. Free Radic. Biol. Med. 51, 1116-1125
35. Molshanski-Mor, S., Mizrahi, A., Ugolev, Y., Dahan, I., Berdichevsky, Y., and Pick, E. (2007) Cell-free assays: The reductionist approach to the study of NADPH oxidase assembly, or "all you wanted to know about cell-free assays but did not dare to ask". Methods Mol. Biol. 412, 385-428
36. Nisimoto, Y., Jackson, H. M., Ogawa, H., Kawahara, T., and Lambeth, J. D. (2010) Constitutive NADPH-dependent electron transferase activity of the Nox4 dehydrogenase domain. Biochemistry 49, 2433-2442
37. Wheeler, D., Sneddon, W. B., Wang, B., Friedman, P. A., and Romero, G. (2007) NHERF-1 and the cytoskeleton regulate the traffic and membrane dynamics of G protein-coupled receptors. J. Biol. Chem. 282, 25076-25087
38. Chen, B. B., and Mallampalli, R. K. (2009) Masking of a nuclear signal motif by monoubiquitination leads to mislocalization and degradation of the regulatory enzyme cytidylyltransferase. Mol. Cell. Biol. 29, 3062-3075
39. Liang, C.-C., Park, A. Y., and Guan, J.-L. (2007) In vitro scratch assay: A convenient and inexpensive method for analysis of cell migration in vitro. Nat. Protoc. 2, 329-333
40. 558. J. Biol. Chem. 274, 22999-23005
41. Kellogg, E. W., 3rd, and Fridovich, I. (1975) Superoxide, hydrogen perox-ide, and singlet oxygen in lipid peroxidation by a xanthine oxidase system. J. Biol. Chem. 250, 8812-8817
42. Harrison, R. (2002) Structure and function of xanthine oxidoreductase: where are we now? Free Radic. Biol. Med. 33, 774-797
43. Gianni, D., Bohl, B., Courtneidge, S. A., and Bokoch, G. M. (2008) The involvement of the tyrosine kinase c-Src in the regulation of reactive oxygen species generation mediated by NADPH oxidase-1. Mol. Biol. Cell 19, 2984-2994
44. McGuire, J. J., Anderson, D. J., and Bennett, B. M. (1994) Inhibition of the biotransformation and pharmacological actions of glyceryl trinitrate by the flavoprotein inhibitor, diphenyleneiodonium sulfate. J. Pharmacol. Exp. Ther. 271, 708-714
45. Hancock, J. T., and Jones, O. T. (1987) The inhibition by diphenyleneiodonium and its analogues of superoxide generation by macrophages. Biochem. J. 242, 103-107
46. Gianni, D., Taulet, N., Zhang, H., DerMardirossian, C., Kister, J., Martinez, L., Roush, W. R., Brown, S. J., Bokoch, G. M., and Rosen, H. (2010) A novel and specific NADPH oxidase-1 (Nox1) small-molecule inhibitor blocks the formation of functional invadopodia in human colon cancer cells. ACS Chem. Biol. 5, 981-993
47. Gaggini, F., Laleu, B., Orchard, M., Fioraso-Cartier, L., Cagnon, L., Houngninou-Molango, S., Gradia, A., Duboux, G., Merlot, C., Heitz, F., Szyndralewiez, C., and Page, P. (2011) Design, synthesis and biological activity of original pyrazolo-pyrido-diazepine, -pyrazine and -oxazine dione derivatives as novel dual Nox4/Nox1 inhibitors. Bioorg. Med. Chem. 19, 6989-6999
48. Mishra, A., Lai, G. H., Schmidt, N. W., Sun, V. Z., Rodriguez, A. R., Tong, R., Tang, L., Cheng, J., Deming, T. J., Kamei, D. T., and Wong, G. C. (2011) Translocation of HIV TAT peptide and analogues induced by multiplexed membrane and cytoskeletal interactions. Proc. Natl. Acad. Sci. U.S.A. 108, 16883-16888
49. Rey, F. E., Cifuentes, M. E., Kiarash, A., Quinn, M. T., and Pagano, P. J. (2001) Novel competitive inhibitor of NAD(P)H oxidase assembly attenuates vascular O(2)(-) and systolic blood pressure in mice. Circ. Res. 89, 408-414
50. Poillot, C., Bichraoui, H., Tisseyre, C., Bahemberae, E., Andreotti, N., Sabatier, J. M., Ronjat, M., and De Waard, M. (2012) Small efficient cellpenetrating peptides derived from scorpion toxin maurocalcine. J. Biol. Chem. 287, 17331-17342
51. Dennis, K. E., Aschner, J. L., Milatovic, D., Schmidt, J. W., Aschner, M., Kaplowitz, M. R., Zhang, Y., and Fike, C. D. (2009) NADPH oxidases and reactive oxygen species at different stages of chronic hypoxia-induced pulmonary hypertension in newborn piglets. Am. J. Physiol. Lung Cell. Mol. Physiol. 297, L596-L607
52. Roos, D., Kuhns, D. B., Maddalena, A., Bustamante, J., Kannengiesser, C., de Boer, M., van Leeuwen, K., Köker, M. Y., Wolach, B., Roesler, J., Malech, H. L., Holland, S. M., Gallin, J. I., and Stasia, M. J. (2010) Hematologically important mutations: The autosomal recessive forms of chronic granulomatous disease (second update). Blood Cells Mol. Dis. 44, 291-299
53. Mittal, M., Roth, M., König, P., Hofmann, S., Dony, E., Goyal, P., Selbitz, A. C., Schermuly, R. T., Ghofrani, H. A., Kwapiszewska, G., Kummer, W., Klepetko, W., Hoda, M. A., Fink, L., Hänze, J., Seeger, W., Grimminger, F., Schmidt, H. H., and Weissmann, N. (2007) Hypoxia-dependent regulation of nonphagocytic NADPH oxidase subunit NOX4 in the pulmonary vasculature. Circ. Res. 101, 258-267
54. Schröder, K., Kohnen, A., Aicher, A., Liehn, E. A., Büchse, T., Stein, S., Weber, C., Dimmeler, S., and Brandes, R. P. (2009) NADPH oxidase Nox2 is required for hypoxia-induced mobilization of endothelial progenitor cells. Circ. Res. 105, 537-544
55. Kinoshita, M., and Hynynen, K. (2005) Intracellular delivery of Bak BH3 peptide by microbubble-enhanced ultrasound. Pharm. Res. 22, 716-720
56. Walensky, L. D., Kung, A. L., Escher, I., Malia, T. J., Barbuto, S., Wright, R. D., Wagner, G., Verdine, G. L., and Korsmeyer, S. J. (2004) Activation of apoptosis in vivo by a hydrocarbon-stapled BH3 helix. Science 305, 1466-1470
57. Tugyi, R., Uray, K., Iván, D., Fellinger, E., Perkins, A., and Hudecz, F. (2005) Partial D-Amino acid substitution: Improved enzymatic stability and preserved Ab recognition of a MUC2 epitope peptide. Proc. Natl. Acad. Sci. U.S.A. 102, 413-418.