Suppressor of cytokine signaling 1-derived peptide inhibits janus kinase/signal transducers and activators of transcription pathway and improves inflammation and atherosclerosis in diabetic mice

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 34, Issue 9, 2014, Pages 1953-1960

  Recio, Carlota ^a,b   Oguiza, Ainhoa ^a,b   Lazaro, Iolanda ^a   Mallavia, Beñat ^a   Egido, Jesus ^a,b   Gomez Guerrero, Carmen ^a,b  

^a Instituto de Investigación Sanitaria Fundación Jiménez Díaz   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

atherosclerosis; cytokines; lipopeptides

Indexed keywords

CHEMOKINE; COLLAGEN; CYTOKINE; JANUS KINASE; STAT PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 1; SUPPRESSOR OF CYTOKINE SIGNALING 1 DERIVED PEPTIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; CELL MIGRATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVATION; INFLAMMATION; LIPID STORAGE; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; T LYMPHOCYTE; VASCULAR SMOOTH MUSCLE;

ATHEROSCLEROSIS; CYTOKINES; LIPOPEPTIDES;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE; CIRCULAR DICHROISM; DIABETES MELLITUS, EXPERIMENTAL; DISEASE PROGRESSION; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG EVALUATION, PRECLINICAL; ENZYME ACTIVATION; INFLAMMATION; INTERFERON-GAMMA; INTERLEUKIN-6; JANUS KINASES; MACROPHAGES; MICE; MOLECULAR SEQUENCE DATA; MOLECULAR TARGETED THERAPY; MYOCYTES, SMOOTH MUSCLE; PEPTIDE FRAGMENTS; PLAQUE, ATHEROSCLEROTIC; PROTEIN CONFORMATION; PROTEIN KINASE INHIBITORS; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR; STAT3 TRANSCRIPTION FACTOR; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS;

EID: 84906940549     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.114.304144     Document Type: Article

References (51)

1. Libby P, Ridker PM, Hansson GK. Progress and challenges in translating the biology of atherosclerosis. Nature. 2011;473:317-325.
2. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature. 2001;414:813-820.
3. Beckman JA, Creager MA, Libby P. Diabetes and atherosclerosis: epidemiology, pathophysiology, and management. JAMA. 2002;287:2570-2581.
4. Harvey EJ, Ramji DP. Interferon-gamma and atherosclerosis: pro- or antiatherogenic? Cardiovasc Res. 2005;67:11-20.
5. Schuett H, Luchtefeld M, Grothusen C, Grote K, Schieffer B. How much is too much? Interleukin-6 and its signalling in atherosclerosis. Thromb Haemost. 2009;102:215-222.
6. Ait-Oufella H, Taleb S, Mallat Z, Tedgui A. Recent advances on the role of cytokines in atherosclerosis. Arterioscler Thromb Vasc Biol. 2011;31:969-979.
7. Kiu H, Nicholson SE. Biology and significance of the JAK/STAT signalling pathways. Growth Factors. 2012;30:88-106.
8. Miklossy G, Hilliard TS, Turkson J. Therapeutic modulators of STAT signalling for human diseases. Nat Rev Drug Discov. 2013;12:611-629.
9. Marrero MB. Introduction to JAK/STAT signaling and the vasculature. Vascul Pharmacol. 2005;43:307-309.
10. Tamiya T, Kashiwagi I, Takahashi R, Yasukawa H, Yoshimura A. Suppressors of cytokine signaling (SOCS) proteins and JAK/STAT pathways: regulation of T-cell inflammation by SOCS1 and SOCS3. Arterioscler Thromb Vasc Biol. 2011;31:980-985.
11. Gharavi NM, Alva JA, Mouillesseaux KP, Lai C, Yeh M, Yeung W, Johnson J, Szeto WL, Hong L, Fishbein M, Wei L, Pfeffer LM, Berliner JA. Role of the Jak/STAT pathway in the regulation of interleukin-8 transcription by oxidized phospholipids in vitro and in atherosclerosis in vivo. J Biol Chem. 2007;282:31460-31468.
12. Agrawal S, Febbraio M, Podrez E, Cathcart MK, Stark GR, Chisolm GM. Signal transducer and activator of transcription 1 is required for optimal foam cell formation and atherosclerotic lesion development. Circulation. 2007;115:2939-2947.
13. Lim WS, Timmins JM, Seimon TA, Sadler A, Kolodgie FD, Virmani R, Tabas I. Signal transducer and activator of transcription-1 is critical for apoptosis in macrophages subjected to endoplasmic reticulum stress in vitro and in advanced atherosclerotic lesions in vivo. Circulation. 2008;117:940-951.
14. Ortiz-Munoz G, Martin-Ventura JL, Hernandez-Vargas P, Mallavia B, Lopez-Parra V, Lopez-Franco O, Munoz-Garcia B, Fernandez-Vizarra P, Ortega L, Egido J, Gomez-Guerrero C. Suppressors of cytokine signaling modulate JAK/STAT-mediated cell responses during atherosclerosis. Arterioscler Thromb Vasc Biol. 2009;29:525-531.
15. Taleb S, Romain M, Ramkhelawon B, Uyttenhove C, Pasterkamp G, Herbin O, Esposito B, Perez N, Yasukawa H, Van Snick J, Yoshimura A, Tedgui A, Mallat Z. Loss of SOCS3 expression in T cells reveals a regulatory role for interleukin-17 in atherosclerosis. J Exp Med. 2009;206:2067-2077.
16. Qin L, Huang Q, Zhang H, Liu R, Tellides G, Min W, Yu L. SOCS1 prevents graft arteriosclerosis by preserving endothelial cell function. J Am Coll Cardiol. 2014;63:21-29.
17. Torella D, Curcio A, Gasparri C, Galuppo V, De Serio D, Surace FC, Cavaliere AL, Leone A, Coppola C, Ellison GM, Indolfi C. Fludarabine prevents smooth muscle proliferation in vitro and neointimal hyperplasia in vivo through specific inhibition of STAT-1 activation. Am J Physiol Heart Circ Physiol. 2007;292:H2935-H2943.
18. Daniel JM, Dutzmann J, Bielenberg W, Widmer-Teske R, Gunduz D, Hamm CW, Sedding DG. Inhibition of STAT3 signaling prevents vascular smooth muscle cell proliferation and neointima formation. Basic Res Cardiol. 2012;107:261.
19. Gomez-Guerrero C, Mallavia B, Egido J. Targeting inflammation in cardiovascular diseases. still a neglected field? Cardiovasc Ther. 2012;30:e189-e197.
20. Marrero MB, Banes-Berceli AK, Stern DM, Eaton DC. Role of the JAK/STAT signaling pathway in diabetic nephropathy. Am J Physiol Renal Physiol. 2006;290:F762-F768.
21. Ronn SG, Billestrup N, Mandrup-Poulsen T. Diabetes and suppressors of cytokine signaling proteins. Diabetes. 2007;56:541-548.
22. Suchy D, ?abuzek K, Machnik G, Koz?owski M, Okopie? B. SOCS and diabetes-ups and downs of a turbulent relationship. Cell Biochem Funct. 2013;31:181-195.
23. Yoshimura A, Naka T, Kubo M. SOCS proteins, cytokine signalling and immune regulation. Nat Rev Immunol. 2007;7:454-465.
24. Trengove MC, Ward AC. SOCS proteins in development and disease. Am J Clin Exp Immunol. 2013;2:1-29.
25. Recinos A 3rd, LeJeune WS, Sun H, Lee CY, Tieu BC, Lu M, Hou T, Boldogh I, Tilton RG, Brasier AR. Angiotensin II induces IL-6 expression and the Jak-STAT3 pathway in aortic adventitia of LDL receptor-deficient mice. Atherosclerosis. 2007;194:125-133.
26. Ortiz-Munoz G, Lopez-Parra V, Lopez-Franco O, Fernandez-Vizarra P, Mallavia B, Flores C, Sanz A, Blanco J, Mezzano S, Ortiz A, Egido J, Gomez-Guerrero C. Suppressors of cytokine signaling abrogate diabetic nephropathy. J Am Soc Nephrol. 2010;21:763-772.
27. Hernandez-Vargas P, Lopez-Franco O, Sanjuan G, Ruperez M, Ortiz- Munoz G, Suzuki Y, Aguado-Roncero P, Perez-Tejerizo G, Blanco J, Egido J, Ruiz-Ortega M, Gomez-Guerrero C. Suppressors of cytokine signaling regulate angiotensin II-activated Janus kinase-signal transducers and activators of transcription pathway in renal cells. J Am Soc Nephrol. 2005;16:1673-1683.
28. Lopez-Parra V, Mallavia B, Lopez-Franco O, Ortiz-Munoz G, Oguiza A, Recio C, Blanco J, Nimmerjahn F, Egido J, Gomez-Guerrero C. Fc? receptor deficiency attenuates diabetic nephropathy. J Am Soc Nephrol. 2012;23:1518-1527.
29. Sasi W, Jiang WG, Sharma A, Mokbel K. Higher expression levels of SOCS 1,3,4,7 are associated with earlier tumour stage and better clinical outcome in human breast cancer. BMC Cancer. 2010;10:178.
30. Liang X, He M, Chen T, Liu Y, Tian YL, Wu YL, Zhao Y, Shen Y, Yuan ZY. Multiple roles of SOCS proteins: differential expression of SOCS1 and SOCS3 in atherosclerosis. Int J Mol Med. 2013;31:1066-1074.
31. Rastmanesh MM, Bluyssen HA, Joles JA, Boer P, Willekes N, Braam B. Increased expression of SOCS3 in monocytes and SOCS1 in lymphocytes correlates with progressive loss of renal function and cardiovascular risk factors in chronic kidney disease. Eur J Pharmacol. 2008;593:99-104.
32. Grothusen C, Schuett H, Hillmer A, Lumpe S, Grote K, Ballmaier M, Bleich A, Glage S, Tietge UJ, Luchtefeld M, Schieffer B. Role of suppressor of cytokine signaling-1 in murine atherosclerosis. PLoS One. 2012;7:e51608.
33. Carow B, Ye Xq, Gavier-Widen D, Bhuju S, Oehlmann W, Singh M, Skold M, Ignatowicz L, Yoshimura A, Wigzell H, Rottenberg ME. Silencing suppressor of cytokine signaling-1 (SOCS1) in macrophages improves Mycobacterium tuberculosis control in an interferon-gamma (IFNgamma)- dependent manner. J Biol Chem. 2011;286:26873-26887.
34. Tajiri K, Imanaka-Yoshida K, Matsubara A, Tsujimura Y, Hiroe M, Naka T, Shimojo N, Sakai S, Aonuma K, Yasutomi Y. Suppressor of cytokine signaling 1 DNA administration inhibits inflammatory and pathogenic responses in autoimmune myocarditis. J Immunol. 2012;189:2043-2053.
35. Kawazoe Y, Naka T, Fujimoto M, Kohzaki H, Morita Y, Narazaki M, Okumura K, Saitoh H, Nakagawa R, Uchiyama Y, Akira S, Kishimoto T. Signal transducer and activator of transcription (STAT)-induced STAT inhibitor 1 (SSI-1)/suppressor of cytokine signaling 1 (SOCS1) inhibits insulin signal transduction pathway through modulating insulin receptor substrate 1 (IRS-1) phosphorylation. J Exp Med. 2001;193:263-269.
36. Chong MM, Chen Y, Darwiche R, Dudek NL, Irawaty W, Santamaria P, Allison J, Kay TW, Thomas HE. Suppressor of cytokine signaling-1 overexpression protects pancreatic beta cells from CD8+ T cell-mediated autoimmune destruction. J Immunol. 2004;172:5714-5721.
37. Flodstrom-Tullberg M, Yadav D, Hagerkvist R, Tsai D, Secrest P, Stotland A, Sarvetnick N. Target cell expression of suppressor of cytokine signaling- 1 prevents diabetes in the NOD mouse. Diabetes. 2003;52:2696-2700.
38. Mujtaba MG, Flowers LO, Patel CB, Patel RA, Haider MI, Johnson HM. Treatment of mice with the suppressor of cytokine signaling-1 mimetic peptide, tyrosine kinase inhibitor peptide, prevents development of the acute form of experimental allergic encephalomyelitis and induces stable remission in the chronic relapsing/remitting form. J Immunol. 2005;175:5077-5086.
39. Ahmed CM, Dabelic R, Waiboci LW, Jager LD, Heron LL, Johnson HM. SOCS-1 mimetics protect mice against lethal poxvirus infection: identification of a novel endogenous antiviral system. J Virol. 2009;83:1402-1415.
40. Waiboci LW, Ahmed CM, Mujtaba MG, Flowers LO, Martin JP, Haider MI, Johnson HM. Both the suppressor of cytokine signaling 1 (SOCS-1) kinase inhibitory region and SOCS-1 mimetic bind to JAK2 autophosphorylation site: implications for the development of a SOCS-1 antagonist. J Immunol. 2007;178:5058-5068.
41. Jager LD, Dabelic R, Waiboci LW, Lau K, Haider MS, Ahmed CM, Larkin J 3rd, David S, Johnson HM. The kinase inhibitory region of SOCS-1 is sufficient to inhibit T-helper 17 and other immune functions in experimental allergic encephalomyelitis. J Neuroimmunol. 2011;232:108-118.
42. Madonna S, Scarponi C, Doti N, Carbone T, Cavani A, Scognamiglio PL, Marasco D, Albanesi C. Therapeutical potential of a peptide mimicking the SOCS1 kinase inhibitory region in skin immune responses. Eur J Immunol. 2013;43:1883-1895.
43. Girolami EI, Bouhy D, Haber M, Johnson H, David S. Differential expression and potential role of SOCS1 and SOCS3 in Wallerian degeneration in injured peripheral nerve. Exp Neurol. 2010;223:173-182.
44. Giordanetto F, Kroemer RT. A three-dimensional model of suppressor of cytokine signalling 1 (SOCS-1). Protein Eng. 2003;16:115-124.
45. Pfender NA, Grosch S, Roussel G, Koch M, Trifilieff E, Greer JM. Route of uptake of palmitoylated encephalitogenic peptides of myelin proteolipid protein by antigen-presenting cells: importance of the type of bond between lipid chain and peptide and relevance to autoimmunity. J Immunol. 2008;180:1398-1404.
46. Halvorsen B, Otterdal K, Dahl TB, Skjelland M, Gullestad L, Oie E, Aukrust P. Atherosclerotic plaque stability-what determines the fate of a plaque? Prog Cardiovasc Dis. 2008;51:183-194.
47. Springall R, Amezcua-Guerra LM, Gonzalez-Pacheco H, Furuzawa- Carballeda J, Gomez-Garcia L, Marquez-Velasco R, Mejia-Dominguez AM, Cossio-Aranda J, Martinez-Sanchez C, Bojalil R. Interferon-gamma increases the ratio of matrix metalloproteinase-9/tissue inhibitor of metalloproteinase- 1 in peripheral monocytes from patients with coronary artery disease. PLoS One. 2013;8:e72291.
48. Meng L, Park J, Cai Q, Lanting L, Reddy MA, Natarajan R. Diabetic conditions promote binding of monocytes to vascular smooth muscle cells and their subsequent differentiation. Am J Physiol Heart Circ Physiol. 2010;298:H736-H745.
49. Nareika A, Sundararaj KP, Im YB, Game BA, Lopes-Virella MF, Huang Y. High glucose and interferon gamma synergistically stimulate MMP-1 expression in U937 macrophages by increasing transcription factor STAT1 activity. Atherosclerosis. 2009;202:363-371.
50. Palmer DC, Restifo NP. Suppressors of cytokine signaling (SOCS) in T cell differentiation, maturation, and function. Trends Immunol. 2009;30:592-602.
51. Swirski FK, Libby P, Aikawa E, Alcaide P, Luscinskas FW, Weissleder R, Pittet MJ. Ly-6Chi monocytes dominate hypercholesterolemia-associated monocytosis and give rise to macrophages in atheromata. J Clin Invest. 2007;117:195-205.