TWIST1 is an ERK1/2 effector that promotes invasion and regulates MMP-1 expression in human melanoma cells

Cancer Research

Volumn 72, Issue 24, 2012, Pages 6382-6392

  Weiss, Michele B ^a   Abel, Ethan V ^a,b   Mayberry, Melanie M ^a   Basile, Kevin J ^a,b   Berger, Adam C ^a   Aplin, Andrew E ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERSTITIAL COLLAGENASE; MATRIGEL; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; TRANSCRIPTION FACTOR TWIST; TRANSCRIPTION FACTOR TWIST1; UNCLASSIFIED DRUG;

ARTICLE; CANCER INVASION; CANCER STAGING; CELL ASSAY; CELL CYCLE; CELL DEATH; CELL GROWTH; CELL LEVEL; CONCENTRATION RESPONSE; EPITHELIAL MESENCHYMAL TRANSITION; MELANOMA CELL; METASTASIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SPHEROID OUTGROWTH; THREE DIMENSIONAL DERMAL MIMETIC ASSAY; TUMOR CELL LINE;

CELL PROLIFERATION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MAP KINASE SIGNALING SYSTEM; MATRIX METALLOPROTEINASE 1; MELANOMA; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; NEOPLASM INVASIVENESS; NUCLEAR PROTEINS; PROTO-ONCOGENE PROTEINS B-RAF; RNA, SMALL INTERFERING; SKIN NEOPLASMS; SPHEROIDS, CELLULAR; TUMOR CELLS, CULTURED; TWIST TRANSCRIPTION FACTOR;

EID: 84871234148     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-1033     Document Type: Article

References (46)

1. Friedl P, Wolf K. Tumour-cell invasion and migration: diversity and escape mechanisms. Nat Rev Cancer 2003;3:362-74. (Pubitemid 37328856)
2. Vernon AE, LaBonne C. Tumor metastasis: a new twist on epithelial-mesenchymal transitions. Curr Biol 2004;14:R719-21. (Pubitemid 39290047)
3. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell 2009;139:871-90.
4. Castanon I, Baylies MK. A Twist in fate: evolutionary comparison of Twist structure and function. Gene 2002;287:11-22. (Pubitemid 34460565)
5. O'Rourke MP, Tam PP. Twist functions in mouse development. Int J Dev Biol 2002;46:401-13. (Pubitemid 36841007)
6. Fuchtbauer EM. Expression of M-twist during postimplantation development of the mouse. Dev Dyn 1995;204:316-22.
7. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, et al. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 2004;117:927-39. (Pubitemid 38798858)
8. Ansieau S, Bastid J, Doreau A, Morel AP, Bouchet BP, Thomas C, et al. Induction of EMT by twist proteins as a collateral effect of tumor-promoting inactivation of premature senescence. Cancer Cell 2008;14:79-89. (Pubitemid 351890463)
9. Kwok WK, Ling MT, Lee TW, Lau TC, Zhou C, Zhang X, et al. Upregulation of TWIST in prostate cancer and its implication as a therapeutic target. Cancer Res 2005;65:5153-62. (Pubitemid 40827324)
10. Maestro R, Dei Tos AP, Hamamori Y, Krasnokutsky S, Sartorelli V, Kedes L, et al. Twist is a potential oncogene that inhibits apoptosis. Genes Dev 1999;13:2207-17. (Pubitemid 29426726)
11. Yang Z, Zhang X, Gang H, Li X, Li Z, Wang T, et al. Up-regulation of gastric cancer cell invasion by Twist is accompanied by N-cadherin and fibronectin expression. Biochem Biophys Res Commun 2007;358:925-30. (Pubitemid 46802478)
12. Lee TK, Poon RT, Yuen AP, Ling MT, Kwok WK, Wang XH, et al. Twist overexpression correlates with hepatocellular carcinoma metastasis through induction of epithelial-mesenchymal transition. Clin Cancer Res 2006;12:5369-76. (Pubitemid 44497250)
13. Koefinger P, Wels C, Joshi S, Damm S, Steinbauer E, Beham-Schmid C, et al. The cadherin switch in melanoma instigated by HGF is mediated through epithelial-mesenchymal transition regulators. Pigment Cell Melanoma Res 2011;24:382-5.
14. Hoek K, Rimm DL, Williams KR, Zhao H, Ariyan S, Lin A, et al. Expression profiling reveals novel pathways in the transformation of melanocytes to melanomas. Cancer Res 2004;64:5270-82. (Pubitemid 39006547)
15. Miller AJ, Mihm MC Jr. Melanoma. N Engl J Med 2006;355:51-65.
16. Russo AE, Torrisi E, Bevelacqua Y, Perrotta R, Libra M, McCubrey JA, et al. Melanoma: molecular pathogenesis and emerging target therapies (Review). Int J Oncol 2009;34:1481-9.
17. Breslow A. Thickness, cross-sectional areas and depth of invasion in the prognosis of cutaneous melanoma. Ann Surg 1970;172:902-8.
18. Elder DE, Gimotty PA, Guerry D. Cutaneous melanoma: estimating survival and recurrence risk based on histopathologic features. Dermatol Ther 2005;18:369-85. (Pubitemid 43096610)
19. Thomas NE. BRAF somatic mutations in malignant melanoma and melanocytic naevi. Melanoma Res 2006;16:97-103. (Pubitemid 44090041)
20. Sumimoto H, Miyagishi M, Miyoshi H, Yamagata S, Shimizu A, Taira K, et al. Inhibition of growth and invasive ability of melanoma by inactivation of mutated BRAF with lentivirus-mediated RNA interference. Oncogene 2004;23:6031-9. (Pubitemid 39178855)
21. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001;29:e45.
22. Carriere A, Cargnello M, Julien LA, Gao H, Bonneil E, Thibault P, et al. Oncogenic MAPK signaling stimulates mTORC1 activity by promoting RSK-mediated raptor phosphorylation. Curr Biol 2008;18:1269-77.
23. Cheng GZ, Zhang WZ, Sun M, Wang Q, Coppola D, Mansour M, et al. Twist is transcriptionally induced by activation of STAT3 and mediates STAT3 oncogenic function. J Biol Chem 2008;283:14665-73.
24. Hong J, Zhou J, Fu J, He T, Qin J, Wang L, et al. Phosphorylation of serine 68 of Twist1 by MAPKs stabilizes Twist1 protein and promotes breast cancer cell invasiveness. Cancer Res 2011;71:3980-90.
25. Arozarena I, Sanchez-Laorden B, Packer L, Hidalgo-Carcedo C, Hayward R, Viros A, et al. Oncogenic BRAF induces melanoma cell invasion by downregulating the cGMP-specific phosphodiesterase PDE5A. Cancer Cell 2011;19:45-57.
26. Vial E, Sahai E, Marshall CJ. ERK-MAPK signaling coordinately regulates activity of Rac1 and RhoA for tumor cell motility. Cancer Cell 2003;4:67-79. (Pubitemid 36904162)
27. Klein RM, Aplin AE. Rnd3 regulation of the actin cytoskeleton promotes melanoma migration and invasive outgrowth in three dimensions. Cancer Res 2009;69:2224-33.
28. Smalley KS, Haass NK, Brafford PA, Lioni M, Flaherty KT, Herlyn M. Multiple signaling pathways must be targeted to overcome drug resistance in cell lines derived from melanoma metastases. Mol Cancer Ther 2006;5:1136-44. (Pubitemid 43881305)
29. Ridky TW, Chow JM, Wong DJ, Khavari PA. Invasive three-dimensional organotypic neoplasia from multiple normal human epithelia. Nat Med 2010;16:1450-5.
30. Weaver VM, Petersen OW, Wang F, Larabell CA, Briand P, Damsky C, et al. Reversion of the malignant phenotype of human breast cells in three-dimensional culture and in vivo by integrin blocking antibodies. J Cell Biol 1997;137:231-45. (Pubitemid 27167310)
31. Shiota M, Izumi H, Onitsuka T, Miyamoto N, Kashiwagi E, Kidani A, et al. Twist and p53 reciprocally regulate target genes via direct interaction. Oncogene 2008;27:5543-53.
32. Benbow U, Schoenermark MP, Mitchell TI, Rutter JL, Shimokawa K, Nagase H, et al. A novel host/tumor cell interaction activates matrix metalloproteinase 1 and mediates invasion through type I collagen. J Biol Chem 1999;274:25371-8.
33. Durko M, Navab R, Shibata HR, Brodt P. Suppression of basement membrane type IV collagen degradation and cell invasion in human melanoma cells expressing an antisense RNA for MMP-1. Biochim Biophys Acta 1997;1356:271-80. (Pubitemid 27226732)
34. Huntington JT, Shields JM, Der CJ, Wyatt CA, Benbow U, Slingluff CL Jr, et al. Overexpression of collagenase 1 (MMP-1) is mediated by the ERK pathway in invasive melanoma cells: role of BRAF mutation and fibroblast growth factor signaling. J Biol Chem 2004;279:33168-76. (Pubitemid 39062961)
35. Ryu B, Moriarty WF, Stine MJ, DeLuca A, Kim DS, Meeker AK, et al. Global analysis of BRAFV600E target genes in human melanocytes identifies matrix metalloproteinase-1 as a critical mediator of melanoma growth. J Invest Dermatol 2011;131:1579-83.
36. Airola K, Karonen T, Vaalamo M, Lehti K, Lohi J, Kariniemi AL, et al. Expression of collagenases-1 and -3 and their inhibitors TIMP-1 and -3 correlates with the level of invasion in malignant melanomas. Br J Cancer 1999;80:733-43. (Pubitemid 29209836)
37. Blackburn JS, Rhodes CH, Coon CI, Brinckerhoff CE. RNA interference inhibition of matrix metalloproteinase-1 prevents melanoma metastasis by reducing tumor collagenase activity and angiogenesis. Cancer Res 2007;67:10849-58. (Pubitemid 350145914)
38. Kessenbrock K, Plaks V, Werb Z. Matrix metalloproteinases: regulators of the tumor microenvironment. Cell 2010;141:52-67.
39. Blackburn JS, Liu I, Coon CI, Brinckerhoff CE. A matrix metalloproteinase-1/protease activated receptor-1 signaling axis promotes melanoma invasion and metastasis. Oncogene 2009;28:4237-48.
40. Cantwell-Dorris ER, O'Leary JJ, Sheils OM. BRAFV600E: implications for carcinogenesis and molecular therapy. Mol Cancer Ther 2011;10:385-94.
41. Shields JM, Thomas NE, Cregger M, Berger AJ, Leslie M, Torrice C, et al. Lack of extracellular signal-regulated kinase mitogen-activated protein kinase signaling shows a new type of melanoma. Cancer Res 2007;67:1502-12. (Pubitemid 46389241)
42. Eckert MA, Lwin TM, Chang AT, Kim J, Danis E, Ohno-Machado L, et al. Twist1-induced invadopodia formation promotes tumor metastasis. Cancer Cell 2011;19:372-86.
43. Pollock PM, Harper UL, Hansen KS, Yudt LM, Stark M, Robbins CM, et al. High frequency of BRAF mutations in nevi. Nat Genet 2003;33:19-20. (Pubitemid 36068675)
44. Uribe P, Andrade L, Gonzalez S. Lack of association between BRAF mutation and MAPK ERK activation in melanocytic nevi. J Invest Dermatol 2006;126:161-6. (Pubitemid 43336108)
45. Nikkola J, Vihinen P, Vuoristo MS, Kellokumpu-Lehtinen P, Kahari VM, Pyrhonen S. High serum levels of matrix metalloproteinase-9 and matrix metalloproteinase-1 are associated with rapid progression in patients with metastatic melanoma. Clin Cancer Res 2005;11:5158-66. (Pubitemid 41003701)
46. Coussens LM, Fingleton B, Matrisian LM. Matrix metalloproteinase inhibitors and cancer: trials and tribulations. Science 2002;295:2387-92. (Pubitemid 34270240)