Wnt5a-Induced Wnt1-Inducible secreted protein-1 suppresses vascular smooth muscle cell apoptosis induced by oxidative stress

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 34, Issue 11, 2014, Pages 2449-2456

  Mill, Carina ^a   Monk, Bethan Alice ^a   Williams, Helen ^a   Simmonds, Steven John ^a   Jeremy, Jamie Yancey ^a   Johnson, Jason Lee ^a   George, Sarah Jane ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Apoptosis; Atherosclerosis; WISP 1 protein; Wnt proteins

Indexed keywords

BETA CATENIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; HYDROGEN PEROXIDE; MESSENGER RNA; PEPTIDES AND PROTEINS; SMALL INTERFERING RNA; T CELL FACTOR PROTEIN; UNCLASSIFIED DRUG; WNT1 INDUCIBLE SECRETED PROTEIN 1; WNT5A PROTEIN; CCN PROTEIN; ONCOPROTEIN; WISP1 PROTEIN, HUMAN; WISP1 PROTEIN, MOUSE; WNT PROTEIN; WNT5A PROTEIN, HUMAN; WNT5A PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; AORTA MEDIA; APOPTOSIS; ARTICLE; ATHEROSCLEROTIC PLAQUE; CELL SURVIVAL; CONTROLLED STUDY; CORONARY ARTERY; CORONARY ARTERY ATHEROSCLEROSIS; DISEASE COURSE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; MOUSE; NONHUMAN; OXIDATIVE STRESS; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; SURVIVAL FACTOR; UPREGULATION; WNT SIGNALING PATHWAY; ANIMAL; CELL CULTURE; DRUG EFFECTS; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; VASCULAR SMOOTH MUSCLE;

ANIMALS; APOPTOSIS; BETA CATENIN; CCN INTERCELLULAR SIGNALING PROTEINS; CELL SURVIVAL; CELLS, CULTURED; HUMANS; HYDROGEN PEROXIDE; MICE; MUSCLE, SMOOTH, VASCULAR; OXIDATIVE STRESS; PROTO-ONCOGENE PROTEINS; SIGNAL TRANSDUCTION; TCF TRANSCRIPTION FACTORS; WNT PROTEINS;

EID: 84911934768     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.114.303922     Document Type: Article

References (51)

1. Wight TN. The extracellular matrix an d atherosclerosis. Curr Opin Lipidol. 1995;6:326-334.
2. Davies MJ, Richardson PD, Woolf N, Katz DR, Mann J. Risk of thrombosis in human atherosclerotic plaques: role of extracellular lipid, macrophage, and smooth muscle cell content. Br Heart J. 1993;69:377-381.
3. Virmani R, Kolodgie FD, Burke AP, Farb A, Schwartz SM. Lessons from sudden coronary death: a comprehensive morpholo gical classification scheme for atherosclerotic lesions. Arterioscler Thromb Vasc Biol. 2000;20:1262-1275.
4. Dhume AS, Soundararajan K, Hunter WJ 3rd, Agrawal DK. Comparison of vascular smooth m uscle cell apoptosis and fibrous cap morphology in symptomatic and asymptomatic carotid artery disease. Ann Vasc Surg. 2003;17:1-8.
5. Madamanchi NR,Vendrov A,Runge MS. Oxidative stress and vascular disease. Arterioscler Thromb Vasc Biol. 2005;25:29-38.
6. Irani K. Oxidant signaling in vascular cell growth, death, and survival: a review of the roles of reactive oxygen species in smooth muscle and endo thelial cell mitogenic and apoptotic signaling. Circ Res. 2000;87:179-183.
7. Kockx MM, De Meyer GR, Muhring J, Jacob W, Bult H, Herman AG. Apoptosis and related proteins in different stages of human atherosclerotic plaques. Circulation. 1998;97:2307-2315.
8. Bjö rkerud S, Björkerud B. Apoptosis is abundant in human atherosclerotic lesions, especially in inflammatory cells (macrophages and T cells), and may contribute to the accumulation of gruel and plaque instability. Am J Pathol. 1996;149:367-380.
9. Geng YJ, Libby P. Evidence for apoptosis in advanced human atheroma. Colocalization with interleukin-1 beta-converting enzyme. Am J Pathol. 1995;147:251-266.
10. Han DK, Haudenschild CC, Hong MK, Tinkle BT, Leon MB, Liau G. Evidence for apoptosis in human atherogenesis and in a rat vascular injury model. Am J Pathol. 1995;147:267-277.
11. Bauriedel G, Hutter R, Welsch U, Bach R, Sievert H, Lü deritz B. Role of smooth muscle cell death in advanced coronary primary lesions: implications for plaque instability. Cardiovasc Res. 1999;41:480-488.
12. von der Thü sen JH, van Vlijmen BJ, Hoeben RC, Kockx MM, Havekes LM, van Berkel TJ, Biessen EA. Induction of atherosclerotic plaque rupture in apolipoprotein E-/-mice after adenovirus-mediated tra nsfer of p53. Circulation. 2002;105:2064-2070.
13. Zadelaar AS, von der Thü sen JH, Boesten LS, Hoeben RC, Kockx MM, Versnel MA, van Berkel TJ, Havekes LM, Biessen EA, van Vlijm en BJ. Increased vulnerability of pre-existing atherosclerosis in ApoEdeficient mice following adenovirus-mediated Fas ligand gene transfer. Atherosclerosis. 2005;183:244-250.
14. Clarke MC, Figg N, Maguire JJ, Davenport AP, Goddard M, Littlewood TD, Bennett MR. Apoptosis of vascular smooth muscle cells induces features of plaque vulnerability in atherosclerosis. Nat Med. 2006;12:1075-1080.
15. Clarke MC, Littlewood TD, Figg N, Maguire JJ, Davenport AP, Goddard M, Bennett MR. Chronic apoptosis of vascular smooth muscle cells accelerates atherosclerosis and promotes calcification and medial degeneration. Circ Res. 2008;102:1529-1538.
16. Flynn PD, Byrne CD, Baglin TP, Weissberg PL, Bennett MR. Thrombin generation by apoptotic vascular smooth muscle cells. Blood. 1997;89:4378-4384.
17. Schaub FJ, Han DK, Liles WC, Adams LD, Coats SA, Ramachandran RK, Seifert RA, Schwartz SM, Bowen-Pope DF. Fas/FADD-mediated activation of a specific program of inflammatory gene expression in vascular smooth muscle cells. Nat Med. 2000;6:790-796.
18. Proudfoot D, Skepper JN, Hegyi L, Bennett MR, Shanahan CM, Weissberg PL. Apoptosis regulates human vascular calcification in vitro: evidence for initiation of vascular calcification by apoptotic bodies. Circ Res. 2000;87:1055-1062.
19. Kü hl M, Sheldahl LC, Park M, Miller JR, Moon RT. The Wnt/Ca2+ pathway: a new vertebrate Wnt signaling pathway takes shape. Trends Genet. 2000;16:279-283.
20. Katoh M. WNT/PCP signaling pathway and human cancer. Oncol Rep 2005;14:1583-1588.
21. Katoh M. WNT signaling in stem cell biology and regenerative medicine. Curr Drug Targets. 2008;9:565-570.
22. Chien AJ, Conrad WH, Moon RT. A Wnt survival guide: from flies to human disease. J Invest Dermatol. 2009;129:1614-1627.
23. Papkoff J. Regulation of complexed and free catenin pools by distinct mechanisms. Differential effects of Wnt-1 and v-Src. J Biol Chem. 1997;272:4536-4543.
24. Daniels DL, Weis WI. Beta-catenin directly displaces Groucho/TLE repressors from Tcf/Lef in Wnt-mediated transcription activation. Nat Struct Mol Biol. 2005;12:364-371.
25. Christman MA 2nd, Goetz DJ, Dickerson E, McCall KD, Lewis CJ, Benencia F, Silver MJ, Kohn LD, Malgor R. Wnt5a is expressed in murine and human atherosclerotic lesions. Am J Physiol Heart Circ Physiol. 2008;294:H2864-H2870.
26. Kim J,Kim J,Kim DW,Ha Y,Ihm MH,Kim H,Song K,Lee I.Wnt5a induces endothelial inflammation via beta-catenin-independent signaling. J Immunol. 2010; 185: 1274-1282.
27. Tsaousi A, Williams H, Lyon CA, Taylor V, Swain A, Johnson JL, George SJ. Wnt4/?-catenin signaling induces VSMC proliferation and is associated with intim al thickening. Circ Res. 2011;108:427-436.
28. Xu L, Corcoran RB, Welsh JW, Pennica D, Levine AJ. WISP-1 is a Wnt-1-and beta-catenin-responsive oncogene. Genes Dev. 2000;14:585-595.
29. Masckauchá n TN, Shawber CJ, Funahashi Y, Li CM, Kitajewski J. Wnt/beta-catenin signaling induces proliferation, survival and interleukin-8 in human endothelial cells. Angiogenesis. 2005; 8:43-51.
30. Almeida M, Han L, Bellido T, Manolagas SC, Kousteni S. Wnt proteins prevent apoptosis of both uncommitted osteoblast progenitors and differentiated osteoblasts by beta-catenin-dependent a nd-independent signaling cascades involving Src/ERK and phosphatidylinositol 3-kinase/AKT. J Biol Chem. 2005;280:41342-41351.
31. Tapia JC, Torres VA, Rodriguez DA, Leyton L, Quest AF. Casein kinase 2 (CK2) increases survivin expression via enhanced beta-catenin-T cell factor/lymphoid enhancer binding factor-dependent transcription. Proc Natl Acad Sci USA. 2006;103:15079-15084.
32. Gandhirajan RK, Staib PA, Minke K, Gehrke I, Plickert G, Schlö sser A, Schmitt EK, Hallek M, Kreuzer KA. Small molecule inhibitors of Wnt/beta-catenin/lef-1 signaling induces apoptosis in chronic lymphocytic leukemia cells in vitro and in vivo. Neoplasia. 2010;12:326-335.
33. Gille JJ, Joenje H. Cell culture models for oxidative stress: superoxide and hydrogen peroxide versus normobaric hyperoxia. Mutat Res. 1992;275:405-414.
34. Lin CL, Wang JY, Huang YT, Kuo YH, Surendran K, Wang FS. Wnt/betacatenin signaling modulates survival of high glucose-stressed mesangial cells. J Am Soc Nephrol. 2006;17:28 12-2820.
35. Chen S, Guttridge DC, You Z, Zhang Z, Fribley A, Mayo MW, Kitajewski J, Wang CY. Wnt-1 signaling inhibits apoptosis by activating beta-catenin/T cell factor-mediated transcription. J Cell Biol. 2001;152:87-96.
36. Ueda Y, Hijikata M, Takagi S, Takada R, Takada S, Chiba T, Shimotohno K. Wnt/beta-catenin signaling suppresses apoptosis in low serum medium and induces morphologic change in rodent fibroblasts. Int J Cancer. 2002;99:681-688.
37. Hwang SG, Ryu JH, Kim IC, Jho EH, Jung HC, Kim K, Kim SJ, Chun JS. Wnt-7a causes loss of differentiated phenotype and inh ibits apoptosis of articular chondrocytes via different mechanisms. J Biol Chem. 2004;279:26597-26604.
38. Dehner M, Hadjihannas M, Weiske J, Huber O, Behrens J. Wnt signaling inhibits Forkhe ad box O3a-induced transcription and apoptosis through up-regulation of serum-and glucocorticoid-inducible kinase 1. J Biol Chem. 2008;283:19201-19210.
39. Shin SY, Chin BR, Lee YH, Kim JH. Invol vement of glycogen synthase kinase-3beta in hydrogen peroxide-induced suppression of Tcf/Lefdependent transcriptional activity. Cell Signal. 2006;18:601-607.
40. Almeida M, Han L, Martin-Millan M, O'B rien CA, Manolagas SC. Oxidative stress antagonizes Wnt signaling in osteoblast precursors by diverting beta-catenin from T cell factor-to forkhead box O-mediated transcription. J Biol Chem. 2007;282:27298-27305.
41. Hoogeboom D, Essers MA, Polderman PE, Voets E, Smits LM, Burgering BM. Interaction of FOXO with beta-catenin inhibits beta-catenin/T cell factor activity. J Biol Chem. 2008;283:9224-9230.
42. Su F, Overholtzer M, Besser D, Levine AJ. WISP-1 attenuates p53-mediated apoptosis in response to DNA damage through activation of the Akt kinase. Genes Dev. 2002;16:46-57.
43. You Z, Saims D, Chen S, Zhang Z, Guttridge DC, Guan KL, MacDougald OA, Brown AM, Evan G, Kitajewski J, Wang CY. Wnt signaling promotes oncogenic transformation by inhibiting c-Myc-induced apoptosis. J Ce ll Biol. 2002;157:429-440.
44. Venkatesan B, Prabhu SD, Venkatachalam K, Mummidi S, Valente AJ, Clark RA, Delafontaine P, Chandrasekar B. WNT1-inducible signaling pathway protein-1 acti vates diverse cell survival pathways and blocks doxorubicin-induced cardiomyocyte death. Cell Signal. 2010;22:809-820.
45. Wang S, Chong ZZ, Shang YC, Maiese K. WISP1 (CCN4) autoregulates its ex pression and nuclear trafficking of?-catenin during oxidant stress with limited effects upon neuronal autophagy. Curr Neurovasc Res. 2012;9:91-101.
46. Reddy VS, Valente AJ, Delafontaine P, Chandras ekar B. Interleukin-18/WNT1-inducible signaling pathway protein-1 signaling mediates human saphenous vein smooth muscle cell proliferation. J Cell Physiol. 2011;226:3303-3315.
47. Pennica D,Swanson TA,Welsh JW,Roy MA,et al. WISP genes are members of the connective tissue growth factor family that are up-regulated in wnt-1-transformed cells and aberrantly expressed in human colon tumors. Proc Natl Acad Sci USA. 1998;95:14717-14722.
48. Leu SJ, Lam SC, Lau LF. Pro-angiogenic activities of CYR61 (CCN1) mediated through integrins alphavbeta3 and alpha6beta1 in human umbilical vein endothelial cells. J Biol Chem. 2002;2 77:46248-46255.
49. Lin CG, Chen CC, Leu SJ, Grzeszkiewicz TM, Lau LF. Integrin-dependent functions of the angiogenic inducer NOV (CCN3): implication in wound healing. J Biol Chem. 2005;280:8229-8237.
50. Hoshijima M, Hattori T, Inoue M, Araki D, Hanagata H , Miyauchi A, Takigawa M. CT domain of CCN2/CTGF directly interacts with fibronectin and enhances cell adhesion of chondrocytes through integrin alpha-5beta1. FEBS Lett. 2006;580:1376-1382.
51. Ono M , Inkson CA, Kilts TM, Young MF. WISP-1/CCN4 regulates osteogenesis by enhancing BMP-2 activity. J Bone Miner Res. 2011;26:193-208.