Nitration of tyrosine 247 inhibits protein kinase G-1α activity by attenuating cyclic guanosine monophosphate binding

Journal of Biological Chemistry

Volumn 289, Issue 11, 2014, Pages 7948-7961

  Aggarwal, Saurabh ^a   Gross, Christine M ^a   Rafikov, Ruslan ^a   Kumar, Sanjiv ^a   Fineman, Jeffrey R ^b,c   Ludewig, Britta ^d   Jonigk, Danny ^a   Black, Stephen M ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; ENZYMES; MASS SPECTROMETRY; NITRIC OXIDE; PROTEINS;

HOMOLOGY MODELING; NATRIURETIC PEPTIDES; NITROSATIVE STRESS; OVER-EXPRESSION; PULMONARY ARTERY SMOOTH MUSCLE CELLS; PULMONARY HYPERTENSION; TYROSINE NITRATION; VASCULAR DISEASE;

NITRATION;

CELL MARKER; CYCLIC GMP; CYCLIC GMP DEPENDENT PROTEIN KINASE 1; PHENYLALANINE; TYROSINE;

AMINO ACID ANALYSIS; ANIMAL CELL; ARTERY MUSCLE; ARTICLE; BINDING AFFINITY; BLOOD VESSEL; CARDIOVASCULAR DISEASE; CATALYSIS; CELL DIFFERENTIATION; CELL LEVEL; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REGULATION; FEMALE; HUMAN; HUMAN TISSUE; LAMB; MALE; MOLECULAR MECHANICS; MUSCLE FIBER CONTRACTION; NITRATION; NITROSATIVE STRESS; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PULMONARY ARTERY; PULMONARY HYPERTENSION; SMOOTH MUSCLE FIBER;

CYCLIC GMP (CGMP); ENZYME CATALYSIS; MASS SPECTROMETRY (MS); MOLECULAR MODELING; PEROXYNITRITE; PROTEIN KINASE G (PKG);

ADULT; ANIMALS; AORTA; CARDIOVASCULAR DISEASES; CATALYTIC DOMAIN; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CYCLIC GMP; CYCLIC GMP-DEPENDENT PROTEIN KINASE TYPE I; FEMALE; HEK293 CELLS; HUMANS; MALE; MASS SPECTROMETRY; MIDDLE AGED; MODELS, MOLECULAR; MYOCYTES, SMOOTH MUSCLE; NITROGEN; PEROXYNITROUS ACID; PROTEIN BINDING; SHEEP; TYROSINE; YOUNG ADULT;

EID: 84896300144     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.534313     Document Type: Article

References (55)

1. Aggarwal, S., Gross, C. M., Kumar, S., Datar, S., Oishi, P., Kalkan, G., Schreiber, C., Fratz, S., Fineman, J. R., and Black, S. M. (2011) Attenuated vasodilatation in lambs with endogenous and exogenous activation of cGMP signaling. Role of protein kinase G nitration. J. Cell. Physiol. 226, 3104-3113
2. Negash, S., Gao, Y., Zhou, W., Liu, J., Chinta, S., and Raj, J. U. (2007) Regulation of cGMP-dependent protein kinase-mediated vasodilation by hypoxia-induced reactive species in ovine fetal pulmonary veins. Am. J. Physiol. Lung Cell Mol. Physiol. 293, L1012-L1020 (Pubitemid 47572249)
3. Zhao, Y. Y., Zhao, Y. D., Mirza, M. K., Huang, J. H., Potula, H. H., Vogel, S. M., Brovkovych, V., Yuan, J. X., Wharton, J., and Malik, A. B. (2009) Persistent eNOS activation secondary to caveolin-1 deficiency induces pulmonary hypertension in mice and humans through PKG nitration. J. Clin. Invest. 119, 2009-2018
4. Garbers, D. L. (1992) Guanylyl cyclase receptors and their endocrine, paracrine, and autocrine ligands. Cell 71, 1-4
5. Feil, S., Zimmermann, P., Knorn, A., Brummer, S., Schlossmann, J., Hofmann, F., and Feil, R. (2005) Distribution of cGMP-dependent protein kinase type I and its isoforms in the mouse brain and retina. Neuroscience 135, 863-868 (Pubitemid 41407748)
6. Uhler, M. D. (1993) Cloning and expression of a novel cyclic GMP-dependent protein kinase from mouse brain. J. Biol. Chem. 268, 13586-13591
7. Vaandrager, A. B., Hogema, B. M., and de Jonge, H. R. (2005) Molecular properties and biological functions of cGMP-dependent protein kinase II. Front. Biosci. 10, 2150-2164 (Pubitemid 40905289)
8. Wolfe, L., and Corbin, J. D. (1989) Cyclic nucleotides and disease. Curr. Opin. Cell Biol. 1, 215-219 (Pubitemid 19172762)
9. Wolfe, L., Corbin, J. D., and Francis, S. H. (1989) Characterization of a novel isozyme of cGMP-dependent protein kinase from bovine aorta. J. Biol. Chem. 264, 7734-7741 (Pubitemid 19119197)
10. Takio, K., Wade, R. D., Smith, S. B., Krebs, E. G., Walsh, K. A., and Titani, K. (1984) Guanosine cyclic 3′,5′-phosphate dependent protein kinase, a chimeric protein homologous with two separate protein families. Biochemistry 23, 4207-4218
11. 1HNMR and circular dichroism studies of the N-terminal domain of cyclic GMP dependent protein kinase. A leucine/isoleucine zipper. Biochemistry 30, 9387-9395
12. Zhao, J., Trewhella, J., Corbin, J., Francis, S., Mitchell, R., Brushia, R., and Walsh, D. (1997) Progressive cyclic nucleotide-induced conformational changes in the cGMP-dependent protein kinase studied by small angle x-ray scattering in solution. J. Biol. Chem. 272, 31929-31936 (Pubitemid 28013347)
13. Chu, D. M., Francis, S. H., Thomas, J. W., Maksymovitch, E. A., Fosler, M., and Corbin, J. D. (1998) Activation by autophosphorylation or cGMP binding produces a similar apparent conformational change in cGMP-dependent protein kinase. J. Biol. Chem. 273, 14649-14656 (Pubitemid 28319191)
14. Hofmann, F., Gensheimer, H. P., and Göbel, C. (1983) Autophosphorylation of cGMP-dependent protein kinase is stimulated only by occupancy of one of the two cGMP binding sites. FEBS Lett. 164, 350-354
15. Hofmann, F., Gensheimer, H. P., and Göbel, C. (1985) cGMP-dependent protein kinase. Autophosphorylation changes the characteristics of binding site 1. Eur. J. Biochem. 147, 361-365 (Pubitemid 15137272)
16. Reed, R. B., Sandberg, M., Jahnsen, T., Lohmann, S. M., Francis, S. H., and Corbin, J. D. (1996) Fast and slow cyclic nucleotide-dissociation sites in cAMP-dependent protein kinase are transposed in type Ibeta cGMP-dependent protein kinase. J. Biol. Chem. 271, 17570-17575 (Pubitemid 26244326)
17. Corbin, J. D., and Døskeland, S. O. (1983) Studies of two different intrachain cGMP-binding sites of cGMP-dependent protein kinase. J. Biol. Chem. 258, 11391-11397 (Pubitemid 13021285)
18. Reddy, V. M., Meyrick, B., Wong, J., Khoor, A., Liddicoat, J. R., Hanley, F. L., and Fineman, J. R. (1995) In utero placement of aortopulmonary shunts. A model of postnatal pulmonary hypertension with increased pulmonary blood flow in lambs. Circulation 92, 606-613
19. Jonigk, D., Golpon, H., Bockmeyer, C. L., Maegel, L., Hoeper, M. M., Gottlieb, J., Nickel, N., Hussein, K., Maus, U., Lehmann, U., Janciauskiene, S., Welte, T., Haverich, A., Rische, J., Kreipe, H., and Laenger, F. (2011) Plexiform lesions in pulmonary arterial hypertension composition, architecture, and microenvironment. Am. J. Pathol. 179, 167-179
20. Wedgwood, S., McMullan, D. M., Bekker, J. M., Fineman, J. R., and Black, S. M. (2001) Role for endothelin-1-induced superoxide and peroxynitrite production in rebound pulmonary hypertension associated with inhaled nitric oxide therapy. Circ. Res. 89, 357-364 (Pubitemid 34132675)
21. Sud, N., Sharma, S., Wiseman, D. A., Harmon, C., Kumar, S., Venema, R. C., Fineman, J. R., and Black, S. M. (2007) Nitric oxide and superoxide generation from endothelial NOS. Modulation by HSP90. Am. J. Physiol. Lung Cell Mol. Physiol. 293, L1444-L1453 (Pubitemid 350255027)
22. Sharma, S., Sud, N., Wiseman, D. A., Carter, A. L., Kumar, S., Hou, Y., Rau, T., Wilham, J., Harmon, C., Oishi, P., Fineman, J. R., and Black, S. M. (2008) Altered carnitine homeostasis is associated with decreased mitochondrial function and altered nitric oxide signaling in lambs with pulmonary hypertension. Am. J. Physiol. Lung Cell Mol. Physiol. 294, L46-L56 (Pubitemid 351380317)
23. Venselaar, H., Joosten, R. P., Vroling, B., Baakman, C. A., Hekkelman, M. L., Krieger, E., and Vriend, G. (2010) Homology modelling and spectroscopy, a never-ending love story. Eur. Biophys. J. 39, 551-563
24. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. (1997) Gapped BLAST and PSI-BLAST. A new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402 (Pubitemid 27359211)
25. King, R. D., and Sternberg, M. J. (1996) Identification and application of the concepts important for accurate and reliable protein secondary structure prediction. Protein Sci. 5, 2298-2310 (Pubitemid 26384468)
26. Kawashima, S., Yamashita, T., Ozaki, M., Ohashi, Y., Azumi, H., Inoue, N., Hirata, K., Hayashi, Y., Itoh, H., and Yokoyama, M. (2001) Endothelial NO synthase overexpression inhibits lesion formation in mouse model of vascular remodeling. Arterioscler. Thromb. Vasc. Biol. 21, 201-207 (Pubitemid 32125366)
27. Rudic, R. D., Shesely, E. G., Maeda, N., Smithies, O., Segal, S. S., and Sessa, W. C. (1998) Direct evidence for the importance of endothelium-derived nitric oxide in vascular remodeling. J. Clin. Invest. 101, 731-736 (Pubitemid 28096068)
28. Pilz, R. B., and Broderick, K. E. (2005) Role of cyclic GMP in gene regulation. Front. Biosci. 10, 1239-1268
29. Casteel, D. E., Smith-Nguyen, E. V., Sankaran, B., Roh, S. H., Pilz, R. B., and Kim, C. (2010) A crystal structure of the cyclic GMP-dependent protein kinase Iβ dimerization/docking domain reveals molecular details of isoform-specific anchoring. J. Biol. Chem. 285, 32684-32688
30. Osborne, B. W., Wu, J., McFarland, C. J., Nickl, C. K., Sankaran, B., Casteel, D. E., Woods, V. L., Jr., Kornev, A. P., Taylor, S. S., and Dostmann, W. R. (2011) Crystal structure of cGMP-dependent protein kinase reveals novel site of interchain communication. Structure 19, 1317-1327
31. Kim, J. J., Casteel, D. E., Huang, G., Kwon, T. H., Ren, R. K., Zwart, P., Headd, J. J., Brown, N. G., Chow, D. C., Palzkill, T., and Kim, C. (2011) Co-crystal structures of PKG Iβ (92-227) with cGMP and cAMP reveal the molecular details of cyclic-nucleotide binding. PLoS One 6, e18413
32. Herranz, B., Marquez, S., Guijarro, B., Aracil, E., Aicart-Ramos, C., Rodriguez-Crespo, I., Serrano, I., Rodríguez-Puyol, M., Zaragoza, C., and Saura, M. (2012) Integrin-linked kinase regulates vasomotor function by preventing endothelial nitric oxide synthase uncoupling. Role in atherosclerosis. Circ. Res. 110, 439-449
33. Lincoln, T. M., Dey, N. B., Boerth, N. J., Cornwell, T. L., and Soff, G. A. (1998) Nitric oxide-cyclic GMP pathway regulates vascular smooth muscle cell phenotypic modulation. Implications in vascular diseases. Acta. Physiol. Scand. 164, 507-515 (Pubitemid 29015669)
34. Acampora, K. B., Nagatomi, J., Langan, E. M., 3rd, and LaBerge, M. (2010) Increased synthetic phenotype behavior of smooth muscle cells in response to in vitro balloon angioplasty injury model. Ann. Vasc. Surg. 24, 116-126
35. Negash, S., Narasimhan, S. R., Zhou, W., Liu, J., Wei, F. L., Tian, J., and Raj, J. U. (2009) Role of cGMP-dependent protein kinase in regulation of pulmonary vascular smooth muscle cell adhesion and migration. Effect of hypoxia. Am. J. Physiol. Heart Circ. Physiol. 297, H304-H312
36. Dusserre, E., Bourdillon, M. C., Pulcini, T., and Berthezene, F. (1994) Decrease in high density lipoprotein binding sites is associated with decrease in intracellular cholesterol efflux in dedifferentiated aortic smooth muscle cells. Biochim. Biophys. Acta 1212, 235-244 (Pubitemid 24181664)
37. Klemm, D. J., Majka, S. M., Crossno, J. T., Jr., Psilas, J. C., Reusch, J. E., and Garat, C. V. (2011) Reduction of reactive oxygen species prevents hypoxia-induced CREB depletion in pulmonary artery smooth muscle cells. J. Cardiovasc. Pharmacol. 58, 181-191
38. Madamanchi, N. R., Moon, S. K., Hakim, Z. S., Clark, S., Mehrizi, A., Patterson, C., and Runge, M. S. (2005) Differential activation of mitogenic signaling pathways in aortic smooth muscle cells deficient in superoxide dismutase isoforms. Arterioscler. Thromb. Vasc. Biol. 25, 950-956 (Pubitemid 40627838)
39. Wang, J. N., Shi, N., and Chen, S. Y. (2012) Manganese superoxide dismutase inhibits neointima formation through attenuation of migration and proliferation of vascular smooth muscle cells. Free Radic. Biol. Med. 52, 173-181
40. Nisbet, R. E., Graves, A. S., Kleinhenz, D. J., Rupnow, H. L., Reed, A. L., Fan, T. H., Mitchell, P. O., Sutliff, R. L., and Hart, C. M. (2009) The role of NADPH oxidase in chronic intermittent hypoxia-induced pulmonary hypertension in mice. Am. J. Respir. Cell Mol. Biol. 40, 601-609
41. 2+ sensitization in pulmonary vascular smooth muscle through superoxide-dependent stimulation of RhoA. Am. J. Physiol. Lung Cell Mol. Physiol. 298, L232-L242
42. Nozik-Grayck, E., and Stenmark, K. R. (2007) Role of reactive oxygen species in chronic hypoxia-induced pulmonary hypertension and vascular remodeling. Adv. Exp. Med. Biol. 618, 101-112
43. Cruz, J. A., Bauer, E. M., Rodriguez, A. I., Gangopadhyay, A., Zeineh, N. S., Wang, Y., Shiva, S., Champion, H. C., and Bauer, P. M. (2012) Chronic hypoxia induces right heart failure in caveolin-1-/- mice. Am. J. Physiol. Heart Circ. Physiol. 302, H2518-H2527
44. Ischiropoulos, H. (2003) Biological selectivity and functional aspects of protein tyrosine nitration. Biochem. Biophys. Res. Commun. 305, 776-783
45. Corbin, J. D., Ogreid, D., Miller, J. P., Suva, R. H., Jastorff, B., and Døskeland, S. O. (1986) Studies of cGMP analog specificity and function of the two intrasubunit binding sites of cGMP-dependent protein kinase. J. Biol. Chem. 261, 1208-1214 (Pubitemid 16103928)
46. Redondo-Horcajo, M., Romero, N., Martínez-Acedo, P., Martínez-Ruiz, A., Quijano, C., Lourenço, C. F., Movilla, N., Enríquez, J. A., Rodríguez-Pascual, F., Rial, E., Radi, R., Vázquez, J., and Lamas, S. (2010) Cyclosporine A-induced nitration of tyrosine 34 MnSOD in endothelial cells. Role of mitochondrial superoxide. Cardiovasc. Res. 87, 356-365
47. Savvides, S. N., Scheiwein, M., Bohme, C. C., Arteel, G. E., Karplus, P. A., Becker, K., and Schirmer, R. H. (2002) Crystal structure of the antioxidant enzyme glutathione reductase inactivated by peroxynitrite. J. Biol. Chem. 277, 2779-2784 (Pubitemid 34953308)
48. Nie, H., Wu, J. L., Zhang, M., Xu, J., and Zou, M. H. (2006) Endothelial nitric oxide synthase-dependent tyrosine nitration of prostacyclin synthase in diabetes in vivo. Diabetes 55, 3133-3141 (Pubitemid 44923653)
49. Francis, S. H., Smith, J. A., Colbran, J. L., Grimes, K., Walsh, K. A., Kumar, S., and Corbin, J. D. (1996) Arginine 75 in the pseudosubstrate sequence of type Iβ cGMP-dependent protein kinase is critical for autoinhibition, although autophosphorylated serine 63 is outside this sequence. J. Biol. Chem. 271, 20748-20755 (Pubitemid 26281859)
50. Heil, W. G., Landgraf, W., and Hofmann, F. (1987) A catalytically active fragment of cGMP-dependent protein kinase. Occupation of its cGMP-binding sites does not affect its phosphotransferase activity. Eur. J. Biochem. 168, 117-121
51. Chu, D. M., Corbin, J. D., Grimes, K. A., and Francis, S. H. (1997) Activation by cyclic GMP binding causes an apparent conformational change in cGMP-dependent protein kinase. J. Biol. Chem. 272, 31922-31928 (Pubitemid 28013346)
52. Smith, J. A., Francis, S. H., Walsh, K. A., Kumar, S., and Corbin, J. D. (1996) Autophosphorylation of type Iβ cGMP-dependent protein kinase increases basal catalytic activity and enhances allosteric activation by cGMP or cAMP. J. Biol. Chem. 271, 20756-20762 (Pubitemid 26281860)
53. Hofmann, F., Bernhard, D., Lukowski, R., and Weinmeister, P. (2009) cGMP regulated protein kinases (cGK). Handb. Exp. Pharmacol. 2009, 137-162
54. Busch, J. L., Bessay, E. P., Francis, S. H., and Corbin, J. D. (2002) A conserved serine juxtaposed to the pseudosubstrate site of type I cGMP-dependent protein kinase contributes strongly to autoinhibition and lower cGMP affinity. J. Biol. Chem. 277, 34048-34054
55. Aitken, A., Hemmings, B. A., and Hofmann, F. (1984) Identification of the residues on cyclic GMP-dependent protein kinase that are autophosphorylated in the presence of cyclic AMP and cyclic GMP. Biochim. Biophys. Acta 790, 219-225 (Pubitemid 15221887)