Protein Never in Mitosis Gene A Interacting-1 (PIN1) regulates degradation of inducible nitric oxide synthase in endothelial cells

American Journal of Physiology - Cell Physiology

Volumn 295, Issue 3, 2008, Pages

  Liu, Tongzheng ^a   Huang, Yongcheng ^a   Likhotvorik, Rostislav I ^a   Keshvara, Lakhu ^a   Hoyt, Dale G ^a,b  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Calpain; Endothelium; Endotoxin; Interferon

Indexed keywords

CALPASTATIN; CYCLOHEXIMIDE; EPOXOMICIN; GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; LIPOPOLYSACCHARIDE; MESSENGER RNA; N(G) NITROARGININE METHYL ESTER; PEPTIDYLPROLYL ISOMERASE PIN1; SHORT HAIRPIN RNA; CALPAIN; CALPAIN INHIBITOR III; DIPEPTIDE; ENZYME INHIBITOR; LIPOPOLYSACCHARIDE, ESCHERICHIA COLI 0111 B4; NIMA INTERACTING PEPTIDYLPROLYL ISOMERASE; NIMA-INTERACTING PEPTIDYLPROLYL ISOMERASE; NITRIC OXIDE; NOS2 PROTEIN, MOUSE; OLIGOPEPTIDE; PEPTIDYLPROLYL ISOMERASE; PROTEASOME; RECOMBINANT PROTEIN; SMALL INTERFERING RNA;

AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL GENE; CONTROLLED STUDY; CYTOTOXICITY; ENDOTHELIUM CELL; ESCHERICHIA COLI; EXPERIMENTAL ANIMAL; GENE INTERACTION; IMMUNOPRECIPITATION; MITOSIS; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN INTERACTION; PROTEIN METABOLISM; PROTEIN STABILITY; STATISTICAL SIGNIFICANCE; WILD TYPE; ANIMAL; CELL CULTURE; CELL SURVIVAL; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; GENETICS; METABOLISM; MOUSE; PROTEIN BINDING; PROTEIN PROCESSING; RNA INTERFERENCE; TIME;

ESCHERICHIA COLI; MURINAE;

ANIMALS; CALPAIN; CELL SURVIVAL; CELLS, CULTURED; DIPEPTIDES; ENDOTHELIAL CELLS; ENZYME INHIBITORS; INTERFERON TYPE II; LIPOPOLYSACCHARIDES; MICE; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; OLIGOPEPTIDES; PEPTIDYLPROLYL ISOMERASE; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECOMBINANT PROTEINS; RNA INTERFERENCE; RNA, MESSENGER; RNA, SMALL INTERFERING; TIME FACTORS;

EID: 53449102657     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00366.2007     Document Type: Article

References (51)

1. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254, 1976.
2. Cuzzocrea S, Mazzon E, Di Paola R, Esposito E, Macarthur H, Matuschak GM, Salvemini D. A role for nitric oxide-mediated peroxynitrite formation in a model of endotoxin-induced shock. J Pharmacol Exp Ther 319: 73-81, 2006.
3. Du Q, Park KS, Guo Z, He P, Nagashima M, Shao L, Sahai R, Geller DA, Hussain SP. Regulation of human nitric oxide synthase 2 expression by Wnt beta-catenin signaling. Cancer Res 66: 7024-7031, 2006.
4. Esnault S, Braun RK, Shen ZJ, Xiang Z, Heninger E, Love RB, Sandor M, Malter JS. Pin1 modulates the type 1 immune response. PLoS ONE 2: e226, 2007.
5. Esnault S, Shen ZJ, Whitesel E, Malter JS. The peptidyl-prolyl isomerase Pin1 regulates granulocyte-macrophage colony-stimulating factor mRNA stability in T lymphocytes. J Immunol 177: 6999-7006, 2006.
6. Goll DE, Thompson VF, Li H, Wei W, Cong J. The calpain system. Physiol Rev 83: 731-801, 2003.
7. Gross SS, Wolin MS. Nitric oxide: pathophysiological mechanisms. Annu Rev Physiol 57: 737-769, 1995.
8. Hausel P, Latado H, Courjault-Gautier F, Felley-Bosco E. Src-mediated phosphorylation regulates subcellular distribution and activity of human inducible nitric oxide synthase. Oncogene 25: 198-206, 2006.
9. Hemmrich K, Kroncke KD, Suschek CV, Kolb-Bachofen V. What sense lies in antisense inhibition of inducible nitric oxide synthase expression? Nitric Oxide 12: 183-199, 2005.
10. Huang H, Liu T, Rose JL, Stevens RL, Hoyt DG. Sensitivity of mice to lipopolysaccharide is increased by a high saturated fat and cholesterol diet. J Inflamm 4: 22, 2007.
11. Huang H, McIntosh J, Hoyt D. An efficzient, nonenzymatic method for isolation and culture of murine aortic endothelial cells and their response to inflammatory stimuli. In Vitro Cell Dev Biol Anim 39: 43-50, 2003.
12. Huang H, Rose JL, Hoyt DG. p38 Mitogen-activated protein kinase mediates synergistic induction of inducible nitric-oxide synthase by lipopolysaccharide and interferon-γ through signal transducer and activator of transcription 1 Ser727 phosphorylation in murine aortic endothelial cells. Mol Pharmacol 66: 302-311, 2004.
13. Huang Y, Magdaleno S, Hopkins R, Slaughter C, Curran T, Keshvara L. Tyrosine phosphorylated Disabled 1 recruits Crk family adapter proteins. Biochem Biophys Res Commun 318: 204-212, 2004.
14. Ilsley JL, Sudol M, Winder SJ. The WW domain: linking cell signalling to the membrane cytoskeleton. Cell Signal 14: 183-189, 2002.
15. Janas J, Skowronski J, Van Aelst L. Lentiviral delivery of RNAi in hippocampal neurons. Methods Enzymol 406: 593-605, 2006.
16. Javesghani D, Hussain SN, Scheidel J, Quinn MT, Magder SA. Superoxide production in the vasculature of lipopolysaccharide-treated rats and pigs. Shock 19: 486-493, 2003.
17. Kleinert H, Pautz A, Linker K, Schwarz PM. Regulation of the expression of inducible nitric oxide synthase. Eur J Pharmacol 500: 255-266, 2004.
18. Kok RJ, Schraa AJ, Bos EJ, Moorlag HE, Asgeirsdottir SA, Everts M, Meijer DK, Molema G. Preparation and functional evaluation of RGD-modified proteins as alpha(v)beta(3) integrin directed therapeutics. Bioconjug Chem 13: 128-135, 2002.
19. Kolodziejski PJ, Musial A, Koo JS, Eissa NT. Ubiquitination of inducible nitric oxide synthase is required for its degradation. Proc Natl Acad Sci USA 99: 12315-12320, 2002.
20. Kroncke KD, Fehsel K, Kolb-Bachofen V. Nitric oxide: cytotoxicity versus cytoprotection-how, why, when, and where? Nitric Oxide 1: 107-120, 1997.
21. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685, 1970.
22. Lu KP, Liou YC, Zhou XZ. Pinning down proline-directed phosphorylation signaling. Trends Cell Biol 12: 164-172, 2002.
23. Lu KP, Zhou XZ. The prolyl isomerase PIN1: a pivotal new twist in phosphorylation signalling and disease. Nat Rev Mol Cell Biol 8: 904-916, 2007.
24. Lundberg AS, Randell SH, Stewart SA, Elenbaas B, Hartwell KA, Brooks MW, Fleming MD, Olsen JC, Miller SW, Weinberg RA, Hahn WC. Immortalization and transformation of primary human airway epithelial cells by gene transfer. Oncogene 21: 4577-4586, 2002.
25. Mei JM, Hord NG, Winterstein DF, Donald SP, Phang JM. Expression of prostaglandin endoperoxide H synthase-2 induced by nitric oxide in conditionally immortalized murine colonic epithelial cells. FASEB J 14: 1188-1201, 2000.
26. Meng L, Mohan R, Kwok BH, Elofsson M, Sin N, Crews CM. Epoxomicin, a potent and selective proteasome inhibitor, exhibits in vivo antiinflammatory activity. Proc Natl Acad Sci USA 96: 10403-10408, 1999.
27. Moffat J, Grueneberg DA, Yang X, Kim SY, Kloepfer AM, Hinkle G, Piqani B, Eisenhaure TM, Luo B, Grenier JK, Carpenter AE, Foo SY, Stewart SA, Stockwell BR, Hacohen N, Hahn WC, Lander ES, Sabatini DM, Root DE. A lentiviral RNAi library for human and mouse genes applied to an arrayed viral high-content screen. Cell 124: 1283-1298, 2006.
28. Monje P, Hernandez-Losa J, Lyons RJ, Castellone MD, Gutkind JS. Regulation of the transcriptional activity of c-Fos by ERK. A novel role for the prolyl isomerase PIN1. J Biol Chem 280: 35081-35084, 2005.
29. Morikawa A, Koide N, Kato Y, Sugiyama T, Chakravortty D, Yoshida T, Yokochi T. Augmentation of nitric oxide production by gamma interferon in a mouse vascular endothelial cell line and its modulation by tumor necrosis factor alpha and lipopolysaccharide. Infect Immun 68: 6209-6214, 2000.
30. Musial A, Eissa NT. Inducible nitric-oxide synthase is regulated by the proteasome degradation pathway. J Biol Chem 276: 24268-24273, 2001.
31. Muzaffar S, Jeremy JY, Angelini GD, Stuart-Smith K, Shukla N. Role of the endothelium and nitric oxide synthases in modulating superoxide formation induced by endotoxin and cytokines in porcine pulmonary arteries. Thorax 58: 598-604, 2003.
32. Pacher P, Beckman JS, Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol Rev 87: 315-424, 2007.
33. Rose JL, Reeves KC, Likhotvorik RI, Hoyt DG. Base excision repair proteins are required for integrin-mediated suppression of bleomycin-induced DNA breakage in murine lung endothelial cells. J Pharmacol Exp Ther 321: 318-326, 2007.
34. Ryo A, Nakamura M, Wulf G, Liou YC, Lu KP. Pin1 regulates turnover and subcellular localization of beta-catenin by inhibiting its interaction with APC. Nat Cell Biol 3: 793-801, 2001.
35. Ryo A, Suizu F, Yoshida Y, Perrem K, Liou YC, Wulf G, Rottapel R, Yamaoka S, Lu KP. Regulation of NF-kappaB signaling by Pin1-dependent prolyl isomerization and ubiquitin-mediated proteolysis of p65/RelA. Mol Cell 12: 1413-1426, 2003.
36. Shelton JL, Wang L, Cepinskas G, Sandig M, Scott JA, North ML, Inculet R, Mehta S. Inducible NO synthase (iNOS) in human neutrophils but not pulmonary microvascular endothelial cells (PMVEC) mediates septic protein leak in vitro. Microvasc Res 74: 23-31, 2007.
37. Shen M, Stukenberg PT, Kirschner MW, Lu KP. The essential mitotic peptidyl-prolyl isomerase Pin1 binds and regulates mitosis-specific phosphoproteins. Genes Dev 12: 706-720, 1998.
38. Shen ZJ, Esnault S, Malter JS. The peptidyl-prolyl isomerase Pin1 regulates the stability of granulocyte-macrophage colony-stimulating factor mRNA in activated eosinophils. Nat Immunol 6: 1280-1287, 2005.
39. Smallwood HS, Shi L, Squier TC. Increases in calmodulin abundance and stabilization of activated inducible nitric oxide synthase mediate bacterial killing in RAW 264.7 macrophages. Biochemistry 45: 9717-9726, 2006.
40. Snedecor GW. Statistical Methods. Ames, IA: Iowa State University Press, 1980.
41. Stewart SA, Dykxhoorn DM, Palliser D, Mizuno H, Yu EY, An DS, Sabatini DM, Chen IS, Hahn WC, Sharp PA, Weinberg RA, Novina CD. Lentivirus-delivered stable gene silencing by RNAi in primary cells. RNA 9: 493-501, 2003.
42. Walker G, Pfeilschifter J, Kunz D. Mechanisms of suppression of inducible nitric-oxide synthase (iNOS) expression in interferon (IFN)-gamma-stimulated RAW 264.7 cells by dexamethasone evidence for glucocorticoid-induced degradation of iNOS protein by calpain as a key step in post-transcriptional regulation. J Biol Chem 272: 16679-16687, 1997.
43. Walker G, Pfeilschifter J, Otten U, Kunz D. Proteolytic cleavage of inducible nitric oxide synthase (iNOS) by calpain I. Biochim Biophys Acta 1568: 216-224, 2001.
44. Wulf G, Finn G, Suizu F, Lu KP. Phosphorylation-specific prolyl isomerization: is there an underlying theme? Nat Cell Biol 7: 435-441, 2005.
45. Wulf GM, Ryo A, Wulf GG, Lee SW, Niu T, Petkova V, Lu KP. Pin1 is overexpressed in breast cancer and cooperates with Ras signaling in increasing the transcriptional activity of c-Jun towards cyclin D1. EMBO J 20: 3459-3472, 2001.
46. Xia Y, Zweier JL. Superoxide and peroxynitrite generation from inducible nitric oxide synthase in macrophages. Proc Natl Acad Sci USA 94: 6954-6958, 1997.
47. Xie QW, Whisnant R, Nathan C. Promoter of the mouse gene encoding calcium-independent nitric oxide synthase confers inducibility by interferon gamma and bacterial lipopolysaccharide. J Exp Med 177: 1779-1784, 1993.
48. Yaffe MB, Schutkowski M, Shen M, Zhou XZ, Stukenberg PT, Rahfeld JU, Xu J, Kuang J, Kirschner MW, Fischer G, Cantley LC, Lu KP. Sequence-specific and phosphorylation-dependent proline isomerization: a potential mitotic regulatory mechanism. Science 278: 1957-1960, 1997.
49. Yeh E, Cunningham M, Arnold H, Chasse D, Monteith T, Ivaldi G, Hahn WC, Stukenberg PT, Shenolikar S, Uchida T, Counter CM, Nevins JR, Means AR, Sears R. A signalling pathway controlling c-Myc degradation that impacts oncogenic transformation of human cells. Nat Cell Biol 6: 308-318, 2004.
50. Yeh ES, Means AR. PIN1, the cell cycle and cancer. Nat Rev Cancer 7: 381-388, 2007.
51. Yoshida M, Xia Y. Heat shock protein 90 as an endogenous protein enhancer of inducible nitric-oxide synthase. J Biol Chem 278: 36953-36958, 2003.