Targeting prolyl-isomerase Pin1 prevents mitochondrial oxidative stress and vascular dysfunction: Insights in patients with diabetes

European Heart Journal

Volumn 36, Issue 13, 2015, Pages 817-828

  Paneni, Francesco ^a,b,c   Costantino, Sarah ^a,b   Castello, Lorenzo ^d   Battista, Rodolfo ^e   Capretti, Giuliana ^d   Chiandotto, Sergio ^d   D'Amario, Domenico ^f   Scavone, Giuseppe ^f   Villano, Angelo ^f   Rustighi, Alessandra ^g   Crea, Filippo ^f   Pitocco, Dario ^f   Lanza, Gaetano ^f   Volpe, Massimo ^c,d   Del Sal, Giannino ^g   Lüscher, Thomas F ^a   Cosentino, Francesco ^a,b  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^c IRCCS NEUROMED   (Italy)

^d SAPIENZA UNIVERSITY OF ROME   (Italy)

^e Civile Hospital   (Italy)

^f CATHOLIC UNIVERSITY   (Italy)

^g UNIVERSITY OF TRIESTE   (Italy)

Author keywords

Diabetes mellitus; Endothelial function; Inflammation; Oxidative stress

Indexed keywords

CAVEOLIN 1; CELL ADHESION MOLECULE; CYTOCHROME C; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUCOSE; INTERCELLULAR ADHESION MOLECULE 1; MONOCYTE CHEMOTACTIC PROTEIN 1; NITRIC OXIDE; PEPTIDYLPROLYL ISOMERASE PIN1; PROTEIN P66; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR RELA; VASCULAR CELL ADHESION MOLECULE 1; CCL2 PROTEIN, HUMAN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NIMA-INTERACTING PEPTIDYLPROLYL ISOMERASE; NITRIC OXIDE SYNTHASE; NOS3 PROTEIN, HUMAN; PEPTIDYLPROLYL ISOMERASE; PROTEIN SHC; SHC1 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; AORTA; ARTICLE; CELL DISRUPTION; CELL ISOLATION; CELL ORGANELLE; CLINICAL ARTICLE; CONTROLLED STUDY; DIABETES MELLITUS; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; ENZYME PHOSPHORYLATION; GENE DELETION; GENE SILENCING; HUMAN; HUMAN CELL; HYPERGLYCEMIA; MALE; MITOCHONDRION; MONOCYTE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN SECRETION; UPREGULATION; VASCULAR DISEASE; VASCULITIS; ANALYSIS OF VARIANCE; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; C57BL MOUSE; CASE CONTROL STUDY; CELL CULTURE; DIABETIC ANGIOPATHIES; METABOLISM; MITOCHONDRIAL DISEASES; PATHOPHYSIOLOGY; PHYSIOLOGY; VASCULAR ENDOTHELIUM;

ANALYSIS OF VARIANCE; ANIMALS; AORTA; CASE-CONTROL STUDIES; CELLS, CULTURED; CHEMOKINE CCL2; CYTOCHROMES C; DIABETIC ANGIOPATHIES; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; GENE KNOCKDOWN TECHNIQUES; GLUCOSE; HUMANS; HYPERGLYCEMIA; INTERCELLULAR ADHESION MOLECULE-1; MALE; MICE, INBRED C57BL; MITOCHONDRIAL DISEASES; NF-KAPPA B; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE III; OXIDATIVE STRESS; PEPTIDYLPROLYL ISOMERASE; REACTIVE OXYGEN SPECIES; SHC SIGNALING ADAPTOR PROTEINS; UP-REGULATION; VASCULAR CELL ADHESION MOLECULE-1; VASCULITIS;

EID: 84926674364     PISSN: 0195668X     EISSN: 15229645     Source Type: Journal    
DOI: 10.1093/eurheartj/ehu179     Document Type: Article

References (41)

1. Beckman JA, Paneni F, Cosentino F, Creager MA. Diabetes and vascular disease: pathophysiology, clinical consequences, and medical therapy: part II. Eur Heart J 2013;34:2444-2452.
2. Paneni F, Beckman JA, Creager MA, Cosentino F. Diabetes and vascular disease: pathophysiology, clinical consequences, and medical therapy: part I. Eur Heart J 2013;34:2436-2443.
3. Lu KP, Zhou XZ. The prolyl isomerase PIN1: a pivotal new twist in phosphorylation signalling and disease. Nat Rev Mol Cell Biol 2007;8:904-916.
4. Lee TH, Pastorino L, Lu KP. Peptidyl-prolyl cis-trans isomerase Pin1 in ageing, cancer and Alzheimer disease. Expert Rev Mol Med 2011;13:e21.
5. Girardini JE, Napoli M, Piazza S, Rustighi A, Marotta C, Radaelli E, Capaci V, Jordan L, Quinlan P, Thompson A, Mano M, Rosato A, Crook T, Scanziani E, Means AR, Lozano G, Schneider C, Del Sal G. A Pin1/mutant p53 axis promotes aggressiveness in breast cancer. Cancer Cell 2011;20:79-91.
6. Tan X, Zhou F, Wan J, Hang J, Chen Z, Li B, Zhang C, Shao K, Jiang P, Shi S, Feng X, Lv N, Wang Z, Ling Y, Zhao X, Ding D, Sun J, Xiong M, He J. Pin1 expression contributes to lung cancer: prognosis and carcinogenesis. Cancer Biol Ther 2010;9: 111-119.
7. Fukuchi M, Fukai Y, Kimura H, Sohda M, Miyazaki T, Nakajima M, Masuda N, Tsukada K, Kato H, Kuwano H. Prolyl isomerase Pin1 expression predicts prognosis in patients with esophageal squamous cell carcinoma and correlates with cyclinD1 expression. Int J Oncol 2006;29:329-334.
8. 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 2003;12:1413-1426.
9. AtkinsonGP, Nozell SE, HarrisonDK, Stonecypher MS, Chen D, Benveniste EN. The prolyl isomerase Pin1 regulates the NF-kappaB signaling pathway and interleukin-8 expression in glioblastoma. Oncogene 2009;28:3735-3745.
10. Wang J, Ray PS, Sim MS, Zhou XZ, Lu KP, Lee AV, Lin X, Bagaria SP, Giuliano AE, Cui X. FOXC1 regulates the functions of human basal-like breast cancer cells by activating NF-kappaB signaling. Oncogene 2012;31:4798-4802.
11. Pinton P, Rimessi A, Marchi S, Orsini F, Migliaccio E, Giorgio M, Contursi C, Minucci S, Mantovani F, Wieckowski MR, Del Sal G, Pelicci PG, Rizzuto R. Protein kinaseCbeta and prolyl isomerase 1 regulate mitochondrial effects of the life-span determinant p66Shc. Science 2007;315:659-663.
12. Sun L, Xiao L, Nie J, Liu FY, Ling GH, Zhu XJ, Tang WB, Chen WC, Xia YC, Zhan M, Ma MM, Peng YM, Liu H, Liu YH, Kanwar YS. p66Shc mediates high-glucose and angiotensin II-induced oxidative stress renal tubular injury via mitochondrialdependent apoptotic pathway. Am J Physiol Renal Physiol 2010;299:F1014-F1025.
13. Sorrentino G, Mioni M, Giorgi C, RuggeriN, Pinton P, Moll U, Mantovani F, Del Sal G. The prolyl-isomerase Pin1 activates the mitochondrial death program of p53. Cell Death Differ 2013;20:198-208.
14. Grison A, Mantovani F, Comel A, Agostoni E, Gustincich S, Persichetti F, Del Sal G. Ser46 phosphorylation and prolyl-isomerase Pin1-mediated isomerization of p53 are key events in p53-dependent apoptosis induced by mutant huntingtin. Proc Natl Acad Sci USA 2011;108:17979-17984.
15. Ruan L, Torres CM, Qian J, Chen F, Mintz JD, SteppDW, Fulton D, Venema RC. Pin1 prolyl isomerase regulates endothelial nitric oxide synthase. Arterioscler Thromb Vasc Biol 2011;31:392-398.
16. Camici GG, Schiavoni M, Francia P, Bachschmid M, Martin-Padura I, Hersberger M, Tanner FC, Pelicci P, Volpe M, Anversa P, Luscher TF, Cosentino F. Genetic deletion of p66(Shc) adaptor protein prevents hyperglycemia-induced endothelial dysfunction and oxidative stress. Proc Natl Acad Sci USA 2007;104:5217-5222.
17. Paneni F, Mocharla P, Akhmedov A, Costantino S, Osto E, Volpe M, Luscher TF, Cosentino F. Gene silencing of the mitochondrial adaptor p66(Shc) suppresses vascular hyperglycemic memory in diabetes. Circ Res 2012;111:278-289.
18. Giacco F, Brownlee M. Oxidative stress and diabetic complications. Circ Res 2010; 107:1058-1070.
19. Ramsey JJ, Tran D, Giorgio M, Griffey SM, Koehne A, Laing ST, Taylor SL, Kim K, Cortopassi GA, Lloyd KC, Hagopian K, Tomilov AA, Migliaccio E, Pelicci PG, McDonald RB. The Influence of Shc Proteins on Life Span in Mice. J Gerontol A Biol Sci Med Sci 2013. doi:10.1093/gerona/glt198.
20. Pagnin E, Fadini G, de Toni R, Tiengo A, Calo L, Avogaro A. Diabetes induces p66shc gene expression in human peripheral blood mononuclear cells: relationship to oxidative stress. J Clin Endocrinol Metab 2005;90:1130-1136.
21. Forstermann U, Munzel T. Endothelial nitric oxide synthase in vascular disease: from marvel to menace. Circulation 2006;113:1708-1714.
22. TabitCE, ChungWB, HamburgNM, Vita JA. Endothelial dysfunction in diabetes mellitus: molecular mechanisms and clinical implications. Rev Endocr Metab Disord 2010; 11:61-74.
23. Tabit CE, Shenouda SM, Holbrook M, Fetterman JL, Kiani S, Frame AA, Kluge MA, Held A, Dohadwala MM, Gokce N, Farb MG, Rosenzweig J, Ruderman N, Vita JA, Hamburg NM. Protein kinase C-beta contributes to impaired endothelial insulin signaling in humans with diabetes mellitus. Circulation 2013;127:86-95.
24. Kouroedov A, Eto M, Joch H, VolpeM, Luscher TF, Cosentino F. Selective inhibition of protein kinaseCbeta2 prevents acute effects of high glucose on vascular cell adhesion molecule-1 expression in human endothelial cells. Circulation 2004;110:91-96.
25. Baker RG, Hayden MS, Ghosh S. NF-kappaB, inflammation, and metabolic disease. Cell Metab 2011;13:11-22.
26. PaneniF, VolpeM, LuscherTF, CosentinoF. SIRT1, p66Shc, and Set7/9invascularhyperglycemic memory: bringing all the strands together. Diabetes 2013;62:1800-1807.
27. Shenouda SM, Widlansky ME, Chen K, Xu G, Holbrook M, Tabit CE, Hamburg NM, Frame AA, Caiano TL, Kluge MA, Duess MA, Levit A, Kim B, Hartman ML, Joseph L, Shirihai OS, Vita JA. Altered mitochondrial dynamics contributes to endothelial dysfunction in diabetes mellitus. Circulation 2011;124:444-453.
28. Li C, Ruan L, Sood SG, Papapetropoulos A, Fulton D, Venema RC. Role of eNOS phosphorylation at Ser-116 in regulation of eNOS activity in endothelial cells. Vascul Pharmacol 2007;47:257-264.
29. LuKP. Phosphorylation-dependent prolyl isomerization: a novel cell cycle regulatory mechanism. Prog Cell Cycle Res 2000;4:83-96.
30. Napoli M, Girardini JE, Piazza S, Del Sal G. Wiring the oncogenic circuitry: Pin1 unleashes mutant p53. Oncotarget 2011;2:654-656.
31. Fadini GP, Albiero M, Menegazzo L, Boscaro E, Pagnin E, Iori E, Cosma C, Lapolla A, Pengo V, Stendardo M, Agostini C, Pelicci PG, Giorgio M, Avogaro A. The redox enzyme p66Shc contributes to diabetes and ischemia-induced delay in cutaneous wound healing. Diabetes 2010;59:2306-2314.
32. Menini S, Amadio L, Oddi G, Ricci C, Pesce C, Pugliese F, Giorgio M, Migliaccio E, Pelicci P, Iacobini C, Pugliese G. Deletion of p66Shc longevity gene protects against experimental diabetic glomerulopathy by preventing diabetes-induced oxidative stress. Diabetes 2006;55:1642-1650.
33. Kluge MA, Fetterman JL, Vita JA. Mitochondria and endothelial function. Circ Res 2013;112:1171-1188.
34. Mount PF, Kemp BE, Power DA. Regulation of endothelial and myocardial NO synthesis by multi-site eNOS phosphorylation. J Mol Cell Cardiol 2007;42:271-279.
35. Frank PG, Woodman SE, Park DS, LisantiMP. Caveolin, caveolae, and endothelial cell function. Arterioscler Thromb Vasc Biol 2003;23:1161-1168.
36. Ki SH, Lee JW, Lim SC, Hien TT, Im JH, Oh WK, Lee MY, Ji YH, Kim YG, Kang KW. Protective effect of nectandrin B, a potent AMPK activator on neointima formation: inhibition of Pin1 expression through AMPK activation. Br J Pharmacol 2013;168: 932-945.
37. Lv L, Zhang J, Zhang L, Xue G, Wang P, Meng Q, LiangW. Essential role of Pin1 via STAT3 signalling and mitochondria-dependent pathways in restenosis in type 2 diabetes. J Cell Mol Med 2013;17:989-1005.
38. Chiasson VL, Munshi N, Chatterjee P, Young KJ, Mitchell BM. Pin1 deficiency causes endothelial dysfunction and hypertension. Hypertension 2011;58:431-438.
39. Toko H, Konstandin MH, Doroudgar S, Ormachea L, Joyo E, Joyo AY, Din S, Gude NA, Collins B, Volkers M, Thuerauf DJ, Glembotski CC, Chen CH, Lu KP, Muller OJ, Uchida T, Sussman MA. Regulation of cardiac hypertrophic signaling by prolyl isomerase Pin1. Circ Res 2013;112:1244-1252.
40. Paneni F, Costantino S, Volpe M, Luscher TF, Cosentino F. Epigenetic signatures and vascular risk in type 2 diabetes: a clinical perspective. Atherosclerosis 2013;230: 191-197.
41. Handy DE, CastroR, Loscalzo J. Epigenetic modifications: basic mechanisms and role in cardiovascular disease. Circulation 2011;123:2145-2156.