Hydrogen peroxide regulates osteopontin expression through activation of transcriptional and translational pathways

Journal of Biological Chemistry

Volumn 289, Issue 1, 2014, Pages 275-285

  Lyle, Alicia N ^a   Remus, Ebony W ^a   Fan, Aaron E ^a   Lassègue, Bernard ^a   Walter, Grant A ^a   Kiyosue, Arihiro ^d   Griendling, Kathy K ^a   Robert Taylor, W ^a,b,c  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Emory University   (United States)

^c ATLANTA VA MEDICAL CENTER   (United States)

^d UNIVERSITY OF TOKYO HOSPITAL   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROGEN PEROXIDE; OXYGEN; PROTEINS; TRANSCRIPTION;

EUKARYOTIC INITIATION FACTOR; IN-VITRO; OSTEOPONTIN; PROMOTER ACTIVITIES; PROTEIN EXPRESSIONS; REACTIVE OXYGEN; SMOOTH MUSCLE CELLS; TRANSLATIONAL REGULATION;

PEROXIDES;

HYDROGEN PEROXIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INITIATION FACTOR 4E; INITIATION FACTOR 4E BINDING PROTEIN 1; MESSENGER RNA; OSTEOPONTIN; REACTIVE OXYGEN METABOLITE; SERINE; TRANSCRIPTION FACTOR AP 1; CARRIER PROTEIN; EIF4EBP1 PROTEIN, RAT; OXIDIZING AGENT; PHOSPHOPROTEIN; SPP1 PROTEIN, RAT;

ANIMAL CELL; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SENSITIVITY ANALYSIS; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; TRANSCRIPTION INITIATION; TRANSLATION INITIATION; UPREGULATION; ANIMAL; BIOSYNTHESIS; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MUTATION; PHOSPHORYLATION; PHYSIOLOGY; POLYSOME; PROTEIN SYNTHESIS;

ANIMALS; CARRIER PROTEINS; CELLS, CULTURED; EUKARYOTIC INITIATION FACTOR-4E; GENE EXPRESSION REGULATION; HYDROGEN PEROXIDE; MUTATION; MYOCYTES, SMOOTH MUSCLE; OSTEOPONTIN; OXIDANTS; PHOSPHOPROTEINS; PHOSPHORYLATION; POLYRIBOSOMES; PROTEIN BIOSYNTHESIS; RATS; TRANSCRIPTION, GENETIC;

EID: 84891715978     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.489641     Document Type: Article

References (37)

1. Bruemmer, D., Collins, A. R., Noh, G., Wang, W., Territo, M., Arias-Magallona, S., Fishbein, M. C., Blaschke, F., Kintscher, U., Graf, K., Law, R. E., and Hsueh, W. A. (2003) Angiotensin II-accelerated atherosclerosis and aneurysm formation is attenuated in osteopontin-deficient mice. J. Clin. Invest. 112, 1318-1331 (Pubitemid 38057686)
2. Matsui, Y., Rittling, S. R., Okamoto, H., Inobe, M., Jia, N., Shimizu, T., Akino, M., Sugawara, T., Morimoto, J., Kimura, C., Kon, S., Denhardt, D., Kitabatake, A., and Uede, T. (2003) Osteopontin deficiency attenuates atherosclerosis in female apolipoprotein E-deficient mice. Arterioscler. Thromb. Vasc. Biol. 23, 1029-1034 (Pubitemid 36713556)
3. Ström, A., Franzén, A., Wängnerud, C., Knutsson, A. K., Heinegård, D., and Hultgårdh-Nilsson, A. (2004) Altered vascular remodeling in osteopontindeficient atherosclerotic mice. J. Vasc. Res. 41, 314-322 (Pubitemid 39370274)
4. Kurata, M., Okura, T., Irita, J., Enomoto, D., Nagao, T., Jotoku, M., Miyoshi, K., Desilva, V. R., and Higaki, J. (2011) Angiotensin II receptor blockade with valsartan decreases plasma osteopontin levels in patients with essential hypertension. J. Hum. Hypertens. 25, 334-339
5. Lorenzen, J. M., Neunhöffer, H., David, S., Kielstein, J. T., Haller, H., and Fliser, D. (2010) Angiotensin II receptor blocker and statins lower elevated levels of osteopontin in essential hypertension. Results from the EUTOPIA trial. Atherosclerosis 209, 184-188
6. Duvall, C. L., Taylor, W. R., Weiss, D., Wojtowicz, A. M., and Guldberg, R. E. (2007) Impaired angiogenesis, early callus formation, and late stage remodeling in fracture healing of osteopontin-deficient mice. J. Bone Miner. Res. 22, 286-297 (Pubitemid 46167799)
7. Duvall, C. L., Weiss, D., Robinson, S. T., Alameddine, F. M., Guldberg, R. E., and Taylor, W. R. (2008) The role of osteopontin in recovery from hind limb ischemia. Arterioscler. Thromb. Vasc. Biol. 28, 290-295 (Pubitemid 351161202)
8. Umekawa, T., Tsuji, H., Uemura, H., and Khan, S. R. (2009) Superoxide from NADPH oxidase as second messenger for the expression of osteopontin and monocyte chemoattractant protein-1 in renal epithelial cells exposed to calcium oxalate crystals. BJU Int. 104, 115-120
9. Brown, D. I., and Griendling, K. K. (2009) Nox proteins in signal transduction. Free Radic. Biol. Med. 47, 1239-1253
10. Lyle, A. N., and Griendling, K. K. (2006) Modulation of vascular smooth muscle signaling by reactive oxygen species. Physiology 21, 269-280 (Pubitemid 44156859)
11. Kaul, G., Pattan, G., and Rafeequi, T. (2011) Eukaryotic elongation factor-2 (eEF2). Its regulation and peptide chain elongation. Cell Biochem. Funct. 29, 227-234
12. Heesom, K. J., and Denton, R. M. (1999) Dissociation of the eukaryotic initiation factor-4E/4E-BP1 complex involves phosphorylation of 4E-BP1 by an mTOR-associated kinase. FEBS Lett. 457, 489-493 (Pubitemid 29414749)
13. Abe, K., Nakashima, H., Ishida, M., Miho, N., Sawano, M., Soe, N. N., Kurabayashi, M., Chayama, K., Yoshizumi, M., and Ishida, T. (2008) Angiotensin II-induced osteopontin expression in vascular smooth muscle cells involves Gq/11, Ras, ERK, Src and Ets-1. Hypertens. Res. 31, 987-998 (Pubitemid 351895043)
14. Hur, W., and Gray, N. S. (2011) Small molecule modulators of antioxidant response pathway. Curr. Opin. Chem. Biol. 15, 162-173
15. Redpath, N. T., and Proud, C. G. (1989) The tumour promoter okadaic acid inhibits reticulocyte-lysate protein synthesis by increasing the net phosphorylation of elongation factor 2. Biochem. J. 262, 69-75 (Pubitemid 19220932)
16. Brasier, A. R., Jamaluddin, M., Han, Y., Patterson, C., and Runge, M. S. (2000) Angiotensin II induces gene transcription through cell-type-dependent effects on the nuclear factor-κB (NF-κB) transcription factor. Mol. Cell Biochem. 212, 155-169
17. Sun, Y., and Oberley, L. W. (1996) Redox regulation of transcriptional activators. Free Radic. Biol. Med. 21, 335-348 (Pubitemid 26271723)
18. Hu, T., Luan, R., Zhang, H., Lau, W. B., Wang, Q., Zhang, Y., Wang, H. C., and Tao, L. (2009) Hydrogen peroxide enhances osteopontin expression and matrix metalloproteinase activity in aortic vascular smooth muscle cells. Clin. Exp. Pharmacol. Physiol. 36, 626-630
19. De Haro, C., Méndez, R., and Santoyo, J. (1996) The eIF-2α kinases and the control of protein synthesis. FASEB J. 10, 1378-1387 (Pubitemid 26347872)
20. Paravicini, T. M., and Touyz, R. M. (2006) Redox signaling in hypertension. Cardiovasc. Res. 71, 247-258
21. Gloire, G., Legrand-Poels, S., and Piette, J. (2006) NF-κB activation by reactive oxygen species. Fifteen years later. Biochem. Pharmacol. 72, 1493-1505 (Pubitemid 44666727)
22. Halliwell, B. (1999) Antioxidant defence mechanisms. From the beginning to the end (of the beginning). Free Radic. Res. 31, 261-272 (Pubitemid 29452853)
23. Gauer, S., Hauser, I. A., Obermüller, N., Holzmann, Y., Geiger, H., and Goppelt-Struebe, M. (2008) Synergistic induction of osteopontin by aldosterone and inflammatory cytokines in mesangial cells. J. Cell. Biochem. 103, 615-623 (Pubitemid 351171932)
24. Grant, C. M. (2011) Regulation of translation by hydrogen peroxide. Antioxid. Redox Signal. 15, 191-203
25. Kuwano, Y., Kim, H. H., Abdelmohsen, K., Pullmann, R., Jr., Martindale, J. L., Yang, X., and Gorospe, M. (2008) MKP-1 mRNA stabilization and translational control by RNA-binding proteins HuR and NF90. Mol. Cell. Biol. 28, 4562-4575 (Pubitemid 351977754)
26. Rocic, P., Seshiah, P., and Griendling, K. K. (2003) Reactive oxygen species sensitivity of angiotensin II-dependent translation initiation in vascular smooth muscle cells. J. Biol. Chem. 278, 36973-36979 (Pubitemid 37140033)
27. Garrido, A. M., and Griendling, K. K. (2009) NADPH oxidases and angiotensin II receptor signaling. Mol. Cell. Endocrinol. 302, 148-158
28. Griendling, K. K., Taubman, M. B., Akers, M., Mendlowitz, M., and Alexander, R. W. (1991) Characterization of phosphatidylinositol-specific phospholipase C from cultured vascular smooth muscle cells. J. Biol. Chem. 266, 15498-15504 (Pubitemid 21907676)
29. Collins, A. R., Schnee, J., Wang, W., Kim, S., Fishbein, M. C., Bruemmer, D., Law, R. E., Nicholas, S., Ross, R. S., and Hsueh, W. A. (2004) Osteopontin modulates angiotensin II-induced fibrosis in the intact murine heart. J. Am. Coll. Cardiol. 43, 1698-1705 (Pubitemid 38561355)
30. 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
31. Muddashetty, R. S., Kelic, S., Gross, C., Xu, M., and Bassell, G. J. (2007) Dysregulated metabotropic glutamate receptor-dependent translation of AMPA receptor and postsynaptic density-95 mRNAs at synapses in a mouse model of fragile X syndrome. J. Neurosci. 27, 5338-5348 (Pubitemid 46790157)
32. Stefani, G., Fraser, C. E., Darnell, J. C., and Darnell, R. B. (2004) Fragile X mental retardation protein is associated with translating polyribosomes in neuronal cells. J. Neurosci. 24, 7272-7276 (Pubitemid 39100696)
33. Bidder, M., Shao, J. S., Charlton-Kachigian, N., Loewy, A. P., Semenkovich, C. F., and Towler, D. A. (2002) Osteopontin transcription in aortic vascular smooth muscle cells is controlled by glucose-regulated upstream stimulatory factor and activator protein-1 activities. J. Biol. Chem. 277, 44485-44496 (Pubitemid 36157883)
34. Zhao, W., Wang, L., Zhang, M., Wang, P., Zhang, L., Yuan, C., Qi, J., Qiao, Y., Kuo, P. C., and Gao, C. (2011) NF-κB- and AP-1-mediated DNA looping regulates osteopontin transcription in endotoxin-stimulated murine macrophages. J. Immunol. 186, 3173-3179
35. Kimball, S. R. (1999) Eukaryotic initiation factor eIF2. Int. J. Biochem. Cell Biol. 31, 25-29 (Pubitemid 29094786)
36. Williams, E. S., Wilson, E., and Ramos, K. S. (2012) NF-κB and matrix-dependent regulation of osteopontin promoter activity in allylamine-activated vascular smooth muscle cells. Oxid. Med. Cell Longev. 2012, 496540
37. Shinohara, M. L., Kim, H. J., Kim, J. H., Garcia, V. A., and Cantor, H. (2008) Alternative translation of osteopontin generates intracellular and secreted isoforms that mediate distinct biological activities in dendritic cells. Proc. Natl. Acad. Sci. U. S. A. 105, 7235-7239 (Pubitemid 351754461)