WNT-5A triggers Cdc42 activation leading to an ERK1/2 dependent decrease in MMP9 activity and invasive migration of breast cancer cells

Molecular Oncology

Volumn 7, Issue 5, 2013, Pages 870-883

  Prasad, Chandra Prakash ^a   Chaurasiya, Shivendra Kumar ^a,b   Axelsson, Lena ^a   Andersson, Tommy ^a  

^a LUND UNIVERSITY   (Sweden)

^b INDIRA GANDHI NATIONAL TRIBAL UNIVERSITY   (India)

Author keywords

Breast cancer; Cdc42; ERK1 2; MMP9; WNT 5A

Indexed keywords

GELATINASE B; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN CDC42; RECOMBINANT PROTEIN; WNT5A PROTEIN;

ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; ENZYME ACTIVITY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; PRIORITY JOURNAL; ZYMOGRAPHY;

BREAST CANCER; CDC42; CELL DIVISION CONTROL PROTEIN 42 HOMOLOG; ERK1/2; MATRIX METALLOPROTEINASE; MMP; MMP9; PHOSPHORYLATION LYSIS BUFFER; PLB; RECOMBINANT MMP9; RECOMBINANT WNT-5A; RMMP9; RWNT-5A; WNT-5A;

BREAST NEOPLASMS; CDC42 GTP-BINDING PROTEIN; CELL LINE, TUMOR; CELL MOVEMENT; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOBLOTTING; MAP KINASE SIGNALING SYSTEM; MATRIX METALLOPROTEINASE 9; PROTO-ONCOGENE PROTEINS; WNT PROTEINS;

EID: 84884280193     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1016/j.molonc.2013.04.005     Document Type: Article

References (69)

1. Beliveau A., Mott J.D., Lo A., Chen E.I., Koller A.A., Yaswen P., Muschler J., Bissell M.J. Raf-induced MMP9 disrupts tissue architecture of human breast cells in three-dimensional culture and is necessary for tumor growth invivo. Genes Dev. 2010, 24:2800-2811.
2. Buechling T., Boutros M. Wnt signaling signaling at and above the receptor level. Curr. Top. Dev. Biol. 2011, 97:21-53.
3. Cadigan K.M., Nusse R. Wnt signaling: a common theme in animal development. Genes Dev. 1997, 11:3286-3305.
4. Chao T.S., Byron K.L., Lee K.M., Villereal M., Rosner M.R. Activation of MAP kinases by calcium-dependent and calcium-independent pathways. Stimulation by thapsigargin and epidermal growth factor. J.Biol. Chem. 1992, 267:19876-19883.
5. Chen H., Zhu G., Li Y., Padia R.N., Dong Z., Pan Z.K., Liu K., Huang S. Extracellular signal-regulated kinase signaling pathway regulates breast cancer cell migration by maintaining slug expression. Cancer Res. 2009, 69:9228-9235.
6. Clark C.C., Cohen I., Eichstetter I., Cannizzaro L.A., McPherson J.D., Wasmuth J.J., Iozzo R.V. Molecular cloning of the human proto-oncogene Wnt-5A and mapping of the gene (WNT5A) to chromosome 3p14-p21. Genomics 1993, 18:249-260.
7. Da Forno P.D., Pringle J.H., Hutchinson P., Osborn J., Huang Q., Potter L., Hancox R.A., Fletcher A., Saldanha G.S. WNT5A expression increases during melanoma progression and correlates with outcome. Clin. Cancer Res. 2008, 14:5825-5832.
8. Dale T.C. Signal transduction by the Wnt family of ligands. Biochem. J. 1998, 329(Pt 2):209-223.
9. Dejmek J., Dib K., Jonsson M., Andersson T. Wnt-5a and G-protein signaling are required for collagen-induced DDR1 receptor activation and normal mammary cell adhesion. Int. J. Cancer 2003, 103:344-351.
10. Dejmek J., Dejmek A., Safholm A., Sjolander A., Andersson T. Wnt-5a protein expression in primary dukes B colon cancers identifies a subgroup of patients with good prognosis. Cancer Res. 2005, 65:9142-9146.
11. Dejmek J., Leandersson K., Manjer J., Bjartell A., Emdin S.O., Vogel W.F., Landberg G., Andersson T. Expression and signaling activity of Wnt-5a/discoidin domain receptor-1 and Syk plays distinct but decisive roles in breast cancer patient survival. Clin. Cancer Res. 2005, 11:520-528.
12. 2+-induced NFAT activity is counteracted by Wnt-5a/Yes-Cdc42-casein kinase 1alpha signaling in human mammary epithelial cells. Mol. Cell. Biol. 2006, 26:6024-6036.
13. Deroanne C.F., Hamelryckx D., Ho T.T., Lambert C.A., Catroux P., Lapiere C.M., Nusgens B.V. Cdc42 downregulates MMP-1 expression by inhibiting the ERK1/2 pathway. J.Cell. Sci. 2005, 118:1173-1183.
14. Edlund S., Landstrom M., Heldin C.H., Aspenstrom P. Transforming growth factor-beta-induced mobilization of actin cytoskeleton requires signaling by small GTPases Cdc42 and RhoA. Mol. Biol. Cell. 2002, 13:902-914.
15. Ekstrom E.J., Sherwood V., Andersson T. Methylation and loss of Secreted Frizzled-Related Protein 3 enhances melanoma cell migration and invasion. PLoS One 2011, 6:e18674.
16. Estrada M., Espinosa A., Muller M., Jaimovich E. Testosterone stimulates intracellular calcium release and mitogen-activated protein kinases via a G protein-coupled receptor in skeletal muscle cells. Endocrinology 2003, 144:3586-3597.
17. Fritz G., Just I., Kaina B. Rho GTPases are over-expressed in human tumors. Int. J. Cancer 1999, 81:682-687.
18. Halleskog C., Dijksterhuis J.P., Kilander M.B., Becerril-Ortega J., Villaescusa J.C., Lindgren E., Arenas E., Schulte G. Heterotrimeric G protein-dependent WNT-5A signaling to ERK1/2 mediates distinct aspects of microglia proinflammatory transformation. J.Neuroinflammation 2012, 9:111.
19. Heasman S.J., Ridley A.J. Mammalian Rho GTPases: new insights into their functions from invivo studies. Nat. Rev. Mol. Cell. Biol. 2008, 9:690-701.
20. Huang C., Jacobson K., Schaller M.D. MAP kinases and cell migration. J.Cell. Sci. 2004, 117:4619-4628.
21. Jiang W., Crossman D.K., Mitchell E.H., Sohn P., Crowley M.R., Serra R. WNT5A inhibits metastasis and alters splicing of Cd44 in breast cancer cells. PLoS One 2013, 8:e58329.
22. Jonsson M., Andersson T. Repression of Wnt-5a impairs DDR1 phosphorylation and modifies adhesion and migration of mammary cells. J.Cell. Sci. 2001, 114:2043-2053.
23. Jonsson M., Dejmek J., Bendahl P.O., Andersson T. Loss of Wnt-5a protein is associated with early relapse in invasive ductal breast carcinomas. Cancer Res. 2002, 62:409-416.
24. Karlsson R., Pedersen E.D., Wang Z., Brakebusch C. Rho GTPase function in tumorigenesis. Biochim. Biophys. Acta 2009, 1796:91-98.
25. Kikuchi A., Yamamoto H., Sato A., Matsumoto S. Wnt5a: its signalling, functions and implication in diseases. Acta Physiol. (Oxf) 2011, 204:17-33.
26. Kleinman H.K., Martin G.R. Matrigel: basement membrane matrix with biological activity. Semin. Cancer Biol. 2005, 15:378-386.
27. Kremenevskaja N., von Wasielewski R., Rao A.S., Schofl C., Andersson T., Brabant G. Wnt-5a has tumor suppressor activity in thyroid carcinoma. Oncogene 2005, 24:2144-2154.
28. Kurayoshi M., Oue N., Yamamoto H., Kishida M., Inoue A., Asahara T., Yasui W., Kikuchi A. Expression of Wnt-5a is correlated with aggressiveness of gastric cancer by stimulating cell migration and invasion. Cancer Res. 2006, 66:10439-10448.
29. Lai S.L., Chien A.J., Moon R.T. Wnt/Fz signaling and the cytoskeleton: potential roles in tumorigenesis. Cell. Res. 2009, 19:532-545.
30. Leandersson K., Riesbeck K., Andersson T. Wnt-5a mRNA translation is suppressed by the Elav-like protein HuR in human breast epithelial cells. Nucleic Acids Res. 2006, 34:3988-3999.
31. Lee J., Cuddihy M.J., Kotov N.A. Three-dimensional cell culture matrices: state of the art. Tissue Eng. Part. B Rev. 2008, 14:61-86.
32. Liu X.H., Pan M.H., Lu Z.F., Wu B., Rao Q., Zhou Z.Y., Zhou X.J. Expression of Wnt-5a and its clinicopathological significance in hepatocellular carcinoma. Dig. Liver Dis. 2008, 40:560-567.
33. MacDonald B.T., Tamai K., He X. Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev. Cell. 2009, 17:9-26.
34. Medrek C., Landberg G., Andersson T., Leandersson K. Wnt-5a-CKI{alpha} signaling promotes {beta}-catenin/E-cadherin complex formation and intercellular adhesion in human breast epithelial cells. J.Biol. Chem. 2009, 284:10968-10979.
35. Melendez J., Grogg M., Zheng Y. Signaling role of Cdc42 in regulating mammalian physiology. J.Biol. Chem. 2010, 286:2375-2381.
36. 2+ pathways. Oncogene 1999, 18:7860-7872.
37. Moon R.T., Kohn A.D., De Ferrari G.V., Kaykas A. WNT and beta-catenin signalling: diseases and therapies. Nat. Rev. Genet. 2004, 5:691-701.
38. Moshal K.S., Sen U., Tyagi N., Henderson B., Steed M., Ovechkin A.V., Tyagi S.C. Regulation of homocysteine-induced MMP-9 by ERK1/2 pathway. Am. J. Physiol. Cell. Physiol. 2006, 290:C883-C891.
39. Nusse R. Wnt signaling and stem cell control. Cell. Res. 2008, 18:523-527.
40. Olson D.J., Papkoff J. Regulated expression of Wnt family members during proliferation of C57mg mammary cells. Cell. Growth Differ. 1994, 5:197-206.
41. Olson D.J., Gibo D.M., Saggers G., Debinski W., Kumar R. Reversion of uroepithelial cell tumorigenesis by the ectopic expression of human wnt-5a. Cell. Growth Differ. 1997, 8:417-423.
42. Osabe M., Negishi M. Active ERK1/2 protein interacts with the phosphorylated nuclear constitutive active/androstane receptor (CAR; NR1I3), repressing dephosphorylation and sequestering CAR in the cytoplasm. J.Biol. Chem. 2011, 286:35763-35769.
43. Pankov R., Endo Y., Even-Ram S., Araki M., Clark K., Cukierman E., Matsumoto K., Yamada K.M. A Rac switch regulates random versus directionally persistent cell migration. J.Cell. Biol. 2005, 170:793-802.
44. Procaccia S., Kraus S., Seger R. Determination of ERK activity: anti-phospho-ERK antibodies and invitro phosphorylation. Methods Mol. Biol. 2010, 661:39-58.
45. Pukrop T., Klemm F., Hagemann T., Gradl D., Schulz M., Siemes S., Trumper L., Binder C. Wnt 5a signaling is critical for macrophage-induced invasion of breast cancer cell lines. Proc. Natl. Acad. Sci. U S A 2006, 103:5454-5459.
46. Reddy K.B., Nabha S.M., Atanaskova N. Role of MAP kinase in tumor progression and invasion. Cancer Metastasis Rev. 2003, 22:395-403.
47. Ridley A.J., Allen W.E., Peppelenbosch M., Jones G.E. Rho family proteins and cell migration. Biochem. Soc. Symp. 1999, 65:111-123.
48. Roarty K., Serra R. Wnt5a is required for proper mammary gland development and TGF-beta-mediated inhibition of ductal growth. Development 2007, 134:3929-3939.
49. Rolli M., Fransvea E., Pilch J., Saven A., Felding-Habermann B. Activated integrin alphavbeta3 cooperates with metalloproteinase MMP-9 in regulating migration of metastatic breast cancer cells. Proc. Natl. Acad. Sci. U S A 2003, 100:9482-9487.
50. Roman-Gomez J., Jimenez-Velasco A., Cordeu L., Vilas-Zornoza A., San Jose-Eneriz E., Garate L., Castillejo J.A., Martin V., Prosper F., Heiniger A., Torres A., Agirre X. WNT5A, a putative tumour suppressor of lymphoid malignancies, is inactivated by aberrant methylation in acute lymphoblastic leukaemia. Eur. J. Cancer 2007, 43:2736-2746.
51. Safholm A., Leandersson K., Dejmek J., Nielsen C.K., Villoutreix B.O., Andersson T. A formylated hexapeptide ligand mimics the ability of Wnt-5a to impair migration of human breast epithelial cells. J.Biol. Chem. 2006, 281:2740-2749.
52. Safholm A., Tuomela J., Rosenkvist J., Dejmek J., Harkonen P., Andersson T. The Wnt-5a-derived hexapeptide Foxy-5 inhibits breast cancer metastasis invivo by targeting cell motility. Clin. Cancer Res. 2008, 14:6556-6563.
53. Schlessinger K., McManus E.J., Hall A. Cdc42 and noncanonical Wnt signal transduction pathways cooperate to promote cell polarity. J.Cell. Biol. 2007, 178:355-361.
54. Schulte G. International Union of Basic and clinical Pharmacology. LXXX. The class Frizzled receptors. Pharmacol. Rev. 2010, 62:632-667.
55. Senger D.R., Perruzzi C.A., Streit M., Koteliansky V.E., de Fougerolles A.R., Detmar M. The alpha(1)beta(1) and alpha(2)beta(1) integrins provide critical support for vascular endothelial growth factor signaling, endothelial cell migration, and tumor angiogenesis. Am. J. Pathol. 2002, 160:195-204.
56. Sheehy N.T., Cordes K.R., White M.P., Ivey K.N., Srivastava D. The neural crest-enriched microRNA miR-452 regulates epithelial-mesenchymal signaling in the first pharyngeal arch. Development 2010, 137:4307-4316.
57. Shimizu H., Julius M.A., Giarre M., Zheng Z., Brown A.M., Kitajewski J. Transformation by Wnt family proteins correlates with regulation of beta-catenin. Cell. Growth Differ. 1997, 8:1349-1358.
58. Stengel K., Zheng Y. Cdc42 in oncogenic transformation, invasion, and tumorigenesis. Cell. Signal. 2011, 23:1415-1423.
59. Szczur K., Xu H., Atkinson S., Zheng Y., Filippi M.D. Rho GTPase CDC42 regulates directionality and random movement via distinct MAPK pathways in neutrophils. Blood 2006, 108:4205-4213.
60. Tang Y., Olufemi L., Wang M.T., Nie D. Role of Rho GTPases in breast cancer. Front. Biosci. 2008, 13:759-776.
61. von Thun A., Birtwistle M., Kalna G., Grindlay J., Strachan D., Kolch W., von Kriegsheim A., Norman J.C. ERK2 drives tumour cell migration in three-dimensional microenvironments by suppressing expression of Rab17 and liprin-beta2. J.Cell. Sci. 2012, 125:1465-1477.
62. Weeraratna A.T., Jiang Y., Hostetter G., Rosenblatt K., Duray P., Bittner M., Trent J.M. Wnt5a signaling directly affects cell motility and invasion of metastatic melanoma. Cancer Cell 2002, 1:279-288.
63. Whale A., Hashim F.N., Fram S., Jones G.E., Wells C.M. Signalling to cancer cell invasion through PAK family kinases. Front. Biosci. 2011, 16:849-864.
64. Wong G.T., Gavin B.J., McMahon A.P. Differential transformation of mammary epithelial cells by Wnt genes. Mol. Cell. Biol. 1994, 14:6278-6286.
65. Yao J.S., Chen Y., Zhai W., Xu K., Young W.L., Yang G.Y. Minocycline exerts multiple inhibitory effects on vascular endothelial growth factor-induced smooth muscle cell migration: the role of ERK1/2, PI3K, and matrix metalloproteinases. Circ. Res. 2004, 95:364-371.
66. Ying J., Li H., Yu J., Ng K.M., Poon F.F., Wong S.C., Chan A.T., Sung J.J., Tao Q. WNT5A exhibits tumor-suppressive activity through antagonizing the Wnt/beta-catenin signaling, and is frequently methylated in colorectal cancer. Clin. Cancer Res. 2008, 14:55-61.
67. Zhu Y., Tian Y., Du J., Hu Z., Yang L., Liu J., Gu L. Dvl2-dependent activation of Daam1 and RhoA regulates Wnt5a-induced breast cancer cell migration. PLoS One 2012, 7:e37823.
68. Zugasti O., Rul W., Roux P., Peyssonnaux C., Eychene A., Franke T.F., Fort P., Hibner U. Raf-MEK-Erk cascade in anoikis is controlled by Rac1 and Cdc42 via Akt. Mol. Cell. Biol. 2001, 21:6706-6717.
69. Zuo Y., Wu Y., Chakraborty C. Cdc42 negatively regulates intrinsic migration of highly aggressive breast cancer cells. J.Cell. Physiol. 2011, 227:1399-1407.