Wnt signalling in smooth muscle cells and its role in cardiovascular disorders

Cardiovascular Research

Volumn 95, Issue 2, 2012, Pages 233-240

  Mill, Carina ^a   George, Sarah Jane ^a  

^a BRISTOL ROYAL INFIRMARY   (United Kingdom)

Author keywords

Apoptosis; Migration; Proliferation; Vascular smooth muscle; Wnt

Indexed keywords

BETA CATENIN; FRIZZLED PROTEIN; WNT PROTEIN;

APOPTOSIS; ATHEROSCLEROSIS; BLOOD VESSEL; CARDIOVASCULAR DISEASE; CELL FUNCTION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CELL TYPE; DROSOPHILA; EMBRYO DEVELOPMENT; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RESTENOSIS; REVIEW; SMOOTH MUSCLE FIBER;

ANIMALS; CARDIOVASCULAR DISEASES; CELL MOVEMENT; CELL PROLIFERATION; HUMANS; MYOCYTES, SMOOTH MUSCLE; WNT SIGNALING PATHWAY;

EID: 84863644232     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvs141     Document Type: Review

References (106)

1. Dahlof B. Cardiovascular disease risk factors: epidemiology and risk assessment. Am J Cardiol 2010;105:3A-9A.
2. Burke AP, Virmani R. Pathophysiology of acute myocardial infarction. Med Clin N Am 2007;91:553.
3. Newby AC, George SJ. Proliferation, migration, matrix turnover and death of smooth muscle cells in native coronary and vein graft atherosclerosis. Curr Opin Cardiol 1996;11:574-582. (Pubitemid 26401805)
4. Thyberg J, Blomgren K, Roy J, Tran PK, Hedin U. Phenotypic modulation of smooth muscle cells after arterial injury is associated with changes in the distribution of laminin and fibronectin. J Histochem Cytochem 1997;45:837-846. (Pubitemid 27248799)
5. Owens GK, Kumar MS, Wamhoff BR. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev 2003;84:767-801.
6. Schwartz SM, deBlois D, O'Brien ERM. The intima. Soil for atherosclerosis and restenosis. Circ Res 1995;77:445-465.
7. Bennett MR. Apoptosis of vascular smooth muscle cells in vascular remodelling and atherosclerotic plaque rupture. Cardiovasc Res 1999;41:361-368. (Pubitemid 29087332)
8. Bauriedel G, Hutter R, Welsch U, Bach R, Sievert H, Lüderitz B. Role of smooth muscle cell death in advanced coronary primary lesions: implications for plaque stability. Cardiovasc Res 1999;41:480-488. (Pubitemid 29087345)
9. Lopez-Candales A, Holmes D, Liao S, Scott M, Wickline S, RW T. Decreased vascular smooth muscle cell density in medial degeneration of human abdominal aortic aneurysms. Am J Pathol 1997;150:993-1007. (Pubitemid 27106171)
10. Golledge J, Muller J, Daugherty A, Norman P. Abdominal aortic aneurysm-Pathogenesis and implications for management. Arterioscler Thromb Vasc Biol 2006;26: 2605-2613.
11. Deak II. Thoracic duplications in the mutant wingless of Drosophila and their effect on muscles and nerves. Dev Biol 1978;66:422-441. (Pubitemid 9043814)
12. Nusse R, Brown A, Papkoff J, Scambler P, Shackleford G, McMahon A et al. A new nomenclature for int-1 and related genes: the Wnt gene family. Cell 1991;64:231.
13. Chien AJ, Conrad WH, Moon RT. A Wnt survival guide: from flies to human disease. J Invest Dermatol 2009;129:1614-1627.
14. van Amerongen R, Berns A. Knockout mouse models to study Wnt signal transduction. Trends Genet 2006;22:678-689. (Pubitemid 44738131)
15. Mikels AJ, Nusse R. Purified Wnt5a protein activates or inhibits b-catenin-TCF signaling depending on receptor context. PLos Biol 2006;4:e115.
16. Tetsu O, McCormick F. b-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 1999;398:422-426. (Pubitemid 29180374)
17. He TC, Sparks AB, Rago C, Hermeking H, Zawel L, da Costa LT et al. Identification of c-MYC as a target of the APC pathway. Science 1998;281:1509-1512. (Pubitemid 28425575)
18. Zhang T, Otevrel T, Gao Z, Gao Z, Ehrlich SM, Fields JZ et al. Evidence that APC regulates survivin expression: a possible mechanism contributing to the stem cell origin of colon cancer. Cancer Res 2001;61:8664-8667. (Pubitemid 34013874)
19. 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.
20. Longo KA, Kennell JA, Ochocinska MJ, Ross SE, Wright WS, MacDougald OA. Wnt signaling protects 3T3-L1 preadipocytes from apoptosis through induction of insulinlike growth factors. J Biol Chem 2002;277:38239-38244. (Pubitemid 35154678)
21. Gradl D, Kuhl M, Wedlich D. The Wnt/Wg signal transducer b-catenin controls fibronectin expression. Mol Cell Biol 1999;19:5576-5587. (Pubitemid 29339915)
22. Rahmani M, Read J, Carthy J, Luo Z, Luo H, Si X et al. Versican promoter is a target for the b-catenin/TCF-4 transcription factor via protein kinase B/glycognen synthase kinase-3b signaling in vascular smooth muscle cells. Cardiovasc Pathol 2004;13:S56.
23. Brabletz T, Jung A, Dag S, Hlubek F, Kirchner T. beta-catenin regulates the expression of the matrix metalloproteinase-7 in human colorectal cancer. Am J Pathol 1999; 155:1033-1038. (Pubitemid 29488909)
24. Crawford HC, Fingleton BM, Rudolph-Owen LA, Goss KJ, Rubinfeld B, Polakis P et al. The metalloproteinase matrilysin is a target of beta-catenin transactivation in intestinal tumors. Oncogene 1999;18:2883-2891. (Pubitemid 29250878)
25. Wu B, Crampton SP, Hughes CCW. Wnt signaling induces matrix metalloproteinase expression and regulates T Cell transmigration. Immunity 2007;26:227-239. (Pubitemid 46329437)
26. Blavier L, Lazaryev A, Shi XH, Dorey FJ, Shackleford GM, DeClerck YA. Stromelysin-1 (MMP-3) is a target and a regulator of Wnt1-induced epithelialmesenchymal transition (EMT). Cancer Biol Ther 2010;10:198-208.
27. Ye S, Wang J, Yang S, Xu W, Xie M, Han K et al. Specific inhibitory protein Dkk-1 blocking Wnt/b-catenin signaling pathway improve protectives effect on the extracellular matrix. J Huazhong Univ Sci Technol Med Sci 2011;31:657-662.
28. Kim K, Lu Z, Hay ED. Direct evidence for a role of b-catenin/LEF-1 signaling pathway in induction of EMT. Cell Biol Int 2002;26:463-476. (Pubitemid 34762099)
29. Marchenko ND, Marchenko GN, Weinreb RN, Lindsey JD, Kyshtoobayeva A, Crawford HC et al. [beta]-Catenin regulates the gene of MMP-26, a novel matrix metalloproteinase expressed both in carcinomas and normal epithelial cells. Int J Biochem Cell Biol 2004;36:942.
30. Johnson JL. Matrix metalloproteinases: influence on smooth muscle cells and atherosclerotic plaque stability. Expert Rev Cardiovasc Ther 2007;5:265-282. (Pubitemid 46488141)
31. Williams H, Johnson J, Jackson C, White S, George S. MMP-7 mediates cleavage of N-cadherin and promotes smooth muscle cell apoptosis. Cardiovasc Res 2010;87: 137-146.
32. De A. Wnt/Ca(2+) signaling pathway: a brief overview. Acta Biochim Biophys Sin 2011;43:745-756.
33. Hoang BH, Thomas JT, Abdul-Karim FW, Correia KM, Conlon RA, Luyten FP et al. Expression pattern of two Frizzled-related genes, Frzb-1 and Sfrp-1, during mouse embryogenesis suggests a role for modulating action of Wnt family members. Dev Dyn 1998;212:364-372. (Pubitemid 28294865)
34. Hsieh JC, Kodjabachian L, Rebbert ML, Rattner A, Smallwood PM, Samos CH et al. A new secreted protein that binds to Wnt proteins and inhibits their activities. Nature 1999;398:431-436. (Pubitemid 29180376)
35. Fedi P, Bafico A, Nieto Soria A, Burgess WH, Miki T, Bottaro DP et al. Isolation and biochemical characterization of the human Dkk-1 homologue, a novel inhibitor of mammalian Wnt signaling. J Biol Chem 1999;274:19465-19472.
36. Lyon C, Mill C, Tsaousi A, Williams H, George S. Regulation of VSMC behavior by the cadherin-catenin complex. Front Biosci 2011;16:644-673.
37. Quasnichka H, Slater S, Beeching C, Boehm M, Sala-Newby G, George S. Regulation of smooth muscle cell proliferation by b-catenin/TCF signaling involves modulation of cyclin D1 and p21 expression. Circ Res 2006;99:1329-1337. (Pubitemid 44949668)
38. Bedel A, Negre-Salvayre A, Heeneman S, Grazide M-H, Thiers J-C, Salvayre R et al. E-Cadherin/{beta}-Catenin/T-cell factor pathway is involved in smooth muscle cell proliferation elicited by oxidized low-density lipoprotein. Circ Res 2008;103: 694-701.
39. Wang X, Xiao Y, Mou Y, Zhao Y, Blankesteijn M, Hall JL. A role for the b-catenin/T-cell factor signaling cascade in vascular remodeling. Circ Res 2002;90:340-347. (Pubitemid 34633936)
40. Uglow EB, Slater S, Sala-Newby GB, Aguilera-Garcia CM, Angelini GD, Newby AC et al. Dismantling of cadherin-mediated cell-cell contacts modulates smooth muscle proliferation. Circ Res 2003;92:1314-1321. (Pubitemid 36773473)
41. Slater SC, Koutsouki E, Jackson CL, Bush RC, Angelini GD, Newby AC et al. R-cadherin:b-catenin complex and its association with vascular smooth muscle cell proliferation. Arterioscler Thromb Vasc Biol 2004;24:1204-1210. (Pubitemid 38880009)
42. Wang X, Adhikari N, Li Q, Hall JL. The LDL receptor related protein LRP6 regulates proliferation and survival through the Wnt cascade in vascular smooth muscle cells. Am J Physiol Heart Circ Physiol 2004;287:H2376-H2383. (Pubitemid 39557105)
43. Ezan J, Leroux L, Barandon L, Dufourcq P, Jaspard B, Moreau C et al. FrzA/sFRP-1, a secreted antagonist of the Wnt-Frizzled pathway, controls vascular cell proliferation in vitro and in vivo. Cardiovasc Res 2004;63:731-738. (Pubitemid 39078687)
44. Marchand A, Atassi F, Gaaya A, Leprince P, Le Feuvre C, Soubrier F et al. The Wnt/beta-catenin pathway is activated during advanced arterial aging in humans. Aging Cell 2011;10:220-232.
45. Tsaousi A, Williams H, Lyon C, Taylor V, Swain A, Johnson J et al. Wnt4/b-catenin signalling induces VSMC proliferation and is associated with intimal thickening. Circ Res 2011;108:427-436.
46. Reddy VS, Valente AJ, Delafontaine P, Chandrasekar 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. Karpurapu M, Wang D, Van Quyen D, Kim T-K, Kundumani-Sridharan V, Pulusani S et al. Cyclin D1 Is a bona fide target gene of NFATc1 and is sufficient in the mediation of injury-induced vascular wall remodeling. J Biol Chem 2010;285:3510-3523.
48. Cipolletta E, Monaco S, Maione AS, Vitiello L, Campiglia P, Pastore L et al. Calmodulin-dependent kinase II mediates vascular smooth muscle cell proliferation and is potentiated by extracellularly regulated kinase. Endocrinology 2010;151: 2747-2759.
49. Hu Y, Cheng L, Hochleitner B-W, Xu Q. Activation of mitogen-activated protein kinases (ERK/JNK) and AP-1 transcription factor in rat carotid arteries after balloon injury. Arterioscler Thromb Vasc Biol 1997;17:2808-2816. (Pubitemid 28016025)
50. de Jesus Perez VA, Ali Z, Alastalo T-P, Ikeno F, Sawada H, Lai Y-J et al. BMP promotes motility and represses growth of smooth muscle cells by activation of tandem Wnt pathways. J Cell Biol 2011;192:171-188.
51. Mao C, Malek T-BO, Pueyo ME, Steg PG, Soubrier F. Differentitial expression of rat frizzled-related frzb-1 and frizzled receptor fz1 and fz2 genes in the rat aorta after balloon injury. Arterioscler Thromb Vasc Biol 2000;20:43-51. (Pubitemid 30048345)
52. Glaw JT, Skalak TC, Peirce SM. Inhibition of canonical Wnt signaling increases microvascular hemorrhaging and venular remodeling in adult rats. Microcirculation 2010;17: 348-357.
53. Tanaka SS, Kojima Y, Yamaguchi YL, Nishinakamura R, Tam PPL. Impact of WNT signaling on tissue lineage differentiation in the early mouse embryo. Dev Growth Differ 2011;53:843-856.
54. Tickenbrock L, Schwable J, Strey A, Sargin B, Hehn S, Baas M et al. Wnt signaling regulates transendothelial migration of monocytes. J Leukoc Biol 2006;79:1306-1313. (Pubitemid 44835566)
55. Cheng C-w, Yeh J-c, Fan T-P, Smith SK, Charnock-Jones DS. Wnt5a-mediated noncanonical Wnt signalling regulates human endothelial cell proliferation and migration. Biochem Biophys Res Comm 2007;365:285-290.
56. Williams H, Tsaousi A, George S. WNT/beta-catenin signalling regulates intimal thickening and smooth muscle cell migration. Atherosclerosis 2010;213:e15.
57. Chow W, Hou G, Bendeck MP. Glycogen synthase kinase 3[beta] regulation of nuclear factor of activated T-cells isoform c1 in the vascular smooth muscle cell response to injury. Exp Cell Res 2008;314:2919-2929.
58. Pauly RR, Bilato C, Sollott SJ, Monticone R, Kelly PT, Lakatta EG et al. Role of calcium/calmodulin-dependent protein kinase II in the regulation of vascular smooth muscle cell migration. Circulation 1995;91:1107-1115.
59. Hsieh CC, Yen MH, Yen CH, Lau YT. Oxidized low density lipoprotein induces apoptosis via generation of reactive oxygen species in vascular smooth muscle cells. Cardiovasc Res 2001;49:135-145.
60. Li PF, Dietz R, von Harsdorf R. Reactive oxygen species induce apoptosis of vascular smooth muscle cell. FEBS Lett 1997;404:249-252. (Pubitemid 27113462)
61. Dimmeler S, Zeiher AM. Reactive oxygen species and vascular cell apoptosis in response to angiotensin II and pro-atherosclerotic factors. Regul Pept 2000;90:19-25. (Pubitemid 30331005)
62. Walford G, Loscalzo J. Nitric oxide in vascular biology. J Thromb Haemost 2003;1: 2112-2118.
63. Geng YJ, Wu Q, Muszynski M, Hansson GK, Libby P. Apoptosis of vascular smooth muscle cells induced by in vitro stimulation with interferon-gamma, tumor necrosis factor-alpha, and interleukin-1 beta. Arterioscler Thromb Vasc Biol 1996;16:19-27. (Pubitemid 26026927)
64. Jovinge S, Crisby M, Thyberg J, Nilsson J. DNA fragmentation and ultrastructural changes of degenerating cells in atherosclerotic lesions and smooth muscle cells exposed to oxidized LDL in vitro. Arterioscler Thromb Vasc Biol 1997;17:2225-2231. (Pubitemid 28057125)
65. Okura Y, Brink M, Itabe H, Scheidegger KJ, Kalangos A, Delafontaine P. Oxidized low-density lipoprotein is associated with apoptosis of vascular smooth muscle cells in human atherosclerotic plaques. Circulation 2000;102:2680-2686.
66. Mill C, Jeremy JY, George SJ. YIA 4 Wnt5a signalling promotes VSMC survival via WISP-1: consequences for VSMC viability in atherosclerotic plaques. Heart 2011; 97:e7.
67. Lv L, Zhou Z, Huang X, Zhao Y, Zhang L, Shi Y et al. Inhibition of peptidyl-prolyl cis/trans isomerase Pin1 induces cell cycle arrest and apoptosis in vascular smooth muscle cells. Apoptosis 2010;15:41-54.
68. Shin M, Nagai H, Sheng G. Notch mediates Wnt and BMP signals in the early separation of smooth muscle progenitors and blood/endothelial common progenitors. Development 2009;136:595-603.
69. Shafer SL, Towler DA. Transcriptional regulation of SM22a by Wnt3a: convergence with TGFb1/Smad signaling at a novel regulatory element. J Mol Cell Cardiol 2009;46: 621-635.
70. Wang Z, ShuW, Lu MM, Morrisey EE. Wnt7b activates canonical signaling in epithelial and vascular smooth muscle cells through interactions with Fzd1, Fzd10, and LRP5. Mol Cell Biol 2005;25:5022-5030. (Pubitemid 40781102)
71. Shu WG, Jiang YQ, Lu MM, Morrisey EE. Wnt7b regulates mesehchymal proliferation and vascular development in the lung. Development 2002;129:4831-4842. (Pubitemid 35277208)
72. Christman MA II, Goetz DJ, Dickerson E, McCall KD, Lewis CJ, Benencia F et al. Wnt5a is expressed in murine and human atherosclerotic lesions. Am J Physiol Heart Circ Physiol 2008;294:H2864-H2870.
73. Mill C, Tsaousi A, Woodward E, Johnson J, George S. Increased expression of Wnt5A in unstable atherosclerotic plaques is associated with increased MMP expression and may contribute to instability. Atherosclerosis 2010;213:e12.
74. Mani A, Radhakrishnan J, Wang H, Mani A, Mani MA, Nelson-Williams C et al. LRP6 mutation in a family with early coronary disease and metabolic risk factors. Science 2007;315:1278-1282. (Pubitemid 46364265)
75. Magoori K, Kang MJ, Ito MR, Kakuuchi H, Ioka RX, Kamataki A et al. Severe hypercholesterolemia, impaired fat tolerance, and advanced atherosclerosis in mice lacking both low density lipoprotein receptor-related protein 5 and apolipoprotein E. J Biol Chem 2003;278:11331-11336. (Pubitemid 36792690)
76. Sarzani R, Salvi F, Bordicchia M, Guerra F, Battistoni I, Pagliariccio G et al. Carotid artery atherosclerosis in hypertensive patients with a functional LDL receptorrelated protein 6 gene variant. Nutr Metab Cardiovasc Dis 2009;21:150-156.
77. Ueland T, Otterdal K, Lekva T, Halvorsen B, Gabrielsen A, Sandberg WJ et al. Dickkopf-1 enhances inflammatory interaction between platelets and endothelial cells and shows increased expression in atherosclerosis. Arterioscler Thromb Vasc Biol 2009;29:1228-1234.
78. Osada M, Park HL, Nagakawa Y, Begum S, Yamashita K, Wu GJ et al. A novel response element confers p63-and p73-specific activation of the WNT4 promoter. Biochem Biophys Res Commun 2006;339:1120-1128. (Pubitemid 41790580)
79. Sim EUH, Smith A, Szilagi E, Rae F, Ioannou P, Lindsay MH et al. Wnt-4 regulation by the Wilms' tumour suppressor gene, WT1. Oncogene 2002;21:2948-2960. (Pubitemid 34522894)
80. Devgan V, Mammucari C, Millar SE, Brisken C, Dotto GP. P21(WAF1/Cip1) is a negative transcriptional regulator of Wnt4 expression downstream of Notch1 activation. Genes Dev 2005;19:1485-1495. (Pubitemid 41003015)
81. Wan XY, Ji W, Mei X, Zhou JG, Liu JX, Fang CC et al. Negative feedback regulation of Wnt4 signaling by EAF1 and EAF2/U19. PLoS ONE 2010;5e9118.
82. Katoh M. Transcriptional mechanisms of WNT5A based on NF-kappa B, Hedgehog, TGF beta, and Notch signaling cascades. Int J Mol Med 2009;23:763-769.
83. Wang ZP, Xu L, Zhu XP, Cui WG, Sun Y, Nishijo H et al. Demethylation of specific Wnt/beta-Catenin pathway genes and its upregulation in rat brain induced by prenatal valproate exposure. Anat Rec 2010;293:1947-1953.
84. Deng G, Li ZQ, Zhao C, Yuan YA, Niu CC, Pan J et al. WNT5A expression is regulated by the status of its promoter methylation in leukaemia and can inhibit leukemic cell malignant proliferation. Oncol Rep 2011;25:367-376.
85. Gupta S, Iljin K, Sara H, Mpindi JP, Mirtti T, Vainio P et al. FZD4 as a mediator of ERG oncogene-induced Wnt signaling and epithelial-to-mesenchymal transition in human prostate cancer cells. Cancer Res 2010;70:6735-6745.
86. Scharer CD, McCabe CD, Ali-Seyed M, Berger MF, Bulyk ML, Moreno CS. Genomewide promoter analysis of the SOX4 transcriptional network in prostate cancer cells. Cancer Res 2009;69:709-717.
87. Katoh Y, Katoh M. Conserved POU-binding site linked to SP1-binding site within FZD5 promoter: transcriptional mechanisms of FZD5 in undifferentiated human ES cells, fetal liver/spleen, adult colon, pancreatic islet, and diffuse-type gastric cancer. Int J Oncol 2007;30:751-755.
88. Katoh Y, Katoh M. Comparative genomics on Fzd8 orthologs. Oncol Rep 2005;13: 993-997.
89. Katoh M. Comparative integromics on FZD7 orthologs: conserved binding sites for PU.1, SP1, CCAAT-box and TCF/LEF/SOX transcription factors within 5'-promoter region of mammalian FZD7 orthologs. Int J Mol Med 2007;19:529-533.
90. Schuuring E, van Deemter L, Roelink H, Nusse R. Transient expression of the protooncogene int-1 during differentiation of P19 embryonal carcinoma cells. Mol Cell Biol 1989;9:1357-1361. (Pubitemid 19071706)
91. Ingraham CA, Park GC, Makarenkova HP, Crossin KL. Matrix metalloproteinase (MMP)-9 induced by wnt signaling increases the proliferation and migration of embryonic neural stem cells at low O2 levels. J Biol Chem 2011;286:17649-17657.
92. Pereira C, Schaer DJ, Bachli EB, Kurrer MO, Schoedon G. Wnt5A/CaMKII Signaling contributes to the inflammatory response of macrophages and is a target for the antiinflammatory action of activated protein C and interleukin-10. Arterioscler Thromb Vasc Biol 2008;28:504-510.
93. Borrell-Pages M, Romero JC, Juan-Babot O, Badimon L. Wnt pathway activation, cell migration, and lipid uptake is regulated by low-density lipoprotein receptor-related protein 5 in human macrophages. Eur Heart J 2011;32:2841-2850.
94. Gonsalves FC, Klein K, Carson BB, Katz S, Ekas LA, Evans S et al. An RNAi-based chemical genetic screen identifies three small-molecule inhibitors of the Wnt/wingless signaling pathway. Proc Natl Acad Sci USA 2011;108:5954-5963.
95. Lepourcelet M, Chen Y-NP, France DS, Wang H, Crews P, Petersen F et al. Smallmolecule antagonists of the oncogenic Tcf/b-catenin protein complex. Cancer Cell 2004;5:91-102. (Pubitemid 38121599)
96. Wang W, Liu H, Wang S, Hao X, Li L. A diterpenoid derivative 15-oxospiramilactone inhibits Wnt/[beta]-catenin signaling and colon cancer cell tumorigenesis. Cell Res 2011;21:730-740.
97. Chen M,Wang J, Lu J, Bond MC, Ren X-R, Lyerly HK et al. The anti-helminthic niclosamide inhibits Wnt/Frizzled1 signaling. Biochemistry 2009;48:10267-10274.
98. Emami KH, Nguyen C, Ma H, Kim DH, Jeong KW, Eguchi M et al. A small molecule inhibitor of b-catenin/cyclic AMP response element-binding protein transcription. Proc Natl Acad Sci USA 2004;101:12682-12687. (Pubitemid 39122083)
99. Huang S-MA, Mishina YM, Liu S, Cheung A, Stegmeier F, Michaud GA et al. Tankyrase inhibition stabilizes axin and antagonizes Wnt signalling. Nature 2009;461: 614-620.
100. Chen Z, Venkatesan AM, Dehnhardt CM, Santos OD, Santos ED, Ayral-Kaloustian S et al. 2,4-Diamino-quinazolines as inhibitors of b-catenin/Tcf-4 pathway: potential treatment for colorectal cancer. Bioorg Med Chem Lett 2009;19:4980-4983.
101. Thorne CA, Hanson AJ, Schneider J, Tahinci E, Orton D, Cselenyi CS et al. Smallmolecule inhibition of Wnt signaling through activation of casein kinase 1a. Nat Chem Biol 2010;6:829-836.
102. Ewan K, Pajak B, Stubbs M, Todd H, Barbeau O, Quevedo C et al. A useful approach to identify novel small-molecule inhibitors of Wnt-dependent transcription. Cancer Res 2010;70:5963-5973.
103. Laeremans H, Hackeng TM, van Zandvoort MAMJ, Thijssen VLJL, Janssen BJA, Ottenheijm HCJ et al. Blocking of Frizzled signaling with a homologous peptide fragment of Wnt3a/Wnt5a reduces infarct expansion and prevents the development of heart failure after myocardial infarction/clinical perspective. Circulation 2011;124: 1626-1635.
104. Shan J, Shi D-L, Wang J, Zheng J. Identification of a specific inhibitor of the Dishevelled PDZ domain. Biochemistry 2005;44:15495-15503. (Pubitemid 41706133)
105. Park CH, Chang JY, Hahm ER, Park S, Kim H-K, Yang CH. Quercetin, a potent inhibitor against b-catenin/Tcf signaling in SW480 colon cancer cells. Biochem Biophys Res Comm 2005;328:227-234. (Pubitemid 40164659)
106. Chen B, Dodge ME, Tang W, Lu J, Ma Z, Fan C-W et al. Small molecule-mediated disruption of Wnt-dependent signaling in tissue regeneration and cancer. Nat Chem Biol 2009;5:100-107.