ErbB2-enhanced invasiveness of H-Ras MCF10A breast cells requires MMP-13 and uPA upregulation via p38 MAPK signaling

International Journal of Oncology

Volumn 36, Issue 2, 2010, Pages 501-507

  Yong, Hae Young ^a   Kim, In Young ^b   Kim, Jong Suk ^a   Moon, Aree ^a  

^a Duksung Women's University   (South Korea)

^b Korea Food and Drug Administration   (South Korea)

Author keywords

Breast cancer; ErbB2; Matrix metalloproteinase 13; p38 MAPK; Urokinase type plasminogen activator

Indexed keywords

COLLAGENASE 3; EPIDERMAL GROWTH FACTOR RECEPTOR 2; MITOGEN ACTIVATED PROTEIN KINASE P38; UROKINASE RECEPTOR;

ARTICLE; BREAST CARCINOMA; BREAST CELL; CANCER GROWTH; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; EPITHELIUM CELL; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; ONCOGENE H RAS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; UPREGULATION;

BLOTTING, WESTERN; BREAST NEOPLASMS; CELL LINE; CELL MOVEMENT; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENES, RAS; HUMANS; MATRIX METALLOPROTEINASE 13; NEOPLASM INVASIVENESS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RECEPTOR, ERBB-2; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; UP-REGULATION; UROKINASE-TYPE PLASMINOGEN ACTIVATOR;

EID: 75449085701     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo-00000524     Document Type: Article

References (53)

1. Bargmann L, Hung MC and Weinberg RA: The neu oncogene encodes an epidermal growth factor receptor-related protein. Nature 319: 226-230, 1986.
2. Holbro T, Civenni G and Hynes NE: The ErbB receptors and their role in cancer progression. Exp Cell Res 284: 99-110, 2003.
3. Satoh T, Endo M, Nakafuku M, Akiyama T, Yamamoto T and Kaziro Y: Accumulation of p21ras. GTP in response to stimulation with epidermal growth factor and oncogene products with tyrosine kinase activity. Proc Natl Acad Sci USA 87: 7926-7929, 1990.
4. Von Lintig FC, Dreilinger AD, Varki NM, Wallace AM, Casteel DE and Boss GR: Ras activation in human breast cancer. Breast Cancer Res Treat 62: 51-62, 2000.
5. Yarden Y: Biology of HER2 and its importance in breast cancer. Oncology 61: 1-13, 2001.
6. Denhardt DT: Oncogene-initiated aberrant signaling engenders the metastatic phenotype: synergistic transcription factor interactions are targets for cancer therapy. Crit Rev Oncog 7: 261-291, 1996.
7. Algül H, Wagner M, Lesina M and Schmid RM: Over-expression of ErbB2 in the exocrine pancreas induces an inflammatory response but not increased proliferation. Int J Cancer 121: 1410-1416, 2007.
8. Slamon DJ, Godolphin W, Jones LA, Holt JA, Wong SG, Keith DE, Levin WJ, Stuart SO, Udove J, Ullrich A and McGuire WL: Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer. Science 244: 707-712, 1989.
9. Tan M, Yao J and Yu D: Overexpression of the c-erbB-2 gene enhanced intrinsic metastasis potential in human breast cancer cells without increasing their transformation abilities. Cancer Res 57: 1199-1205, 1997.
10. Bange EZ and Ullrich A: Molecular targets for breast cancer therapy and prevention. Nat Med 7: 548-552, 2001.
11. Anders CK, Hsu DS, Broadwater G, Acharya CR, Foekens JA, Zhang Y, Wang Y, Marcom PK, Marks JR, Febbo PG, Nevins JR, Potti A and Blackwell KL: Young age at diagnosis correlates with worse prognosis and defines a subset of breast cancers with shared patterns of gene expression. Young age at diagnosis correlates with worse prognosis and defines a subset of breast cancers with shared patterns of gene expression. J Clin Oncol 26: 324-330, 2008.
12. Kawa S, Matsushita H, Ohbayashi H, Semba K and Yamamoto T: A novel mouse monoclonal antibody targeting ErbB2 suppresses breast cancer growth. Biochem Biophys Res Commun 284: 329-333, 2009.
13. Kedrin D, Wyckoff J, Boimel PJ, Coniglio SJ, Hynes NE, Arteaga CL and Segall JE: ERBB1 and ERBB2 have distinct functions in tumor cell invasion and intravasation Clin Cancer Res 15: 3733-3739, 2009.
14. MacDougall JR and Matrisian LM: Contributions of tumor and stromal matrix metalloproteinases to tumor progression, invasion and metastasis. Cancer Metastasis Rev 14: 351-362, 1995.
15. Liotta LA and Kohn EC: Stromal therapy: the next step in ovarian cancer treatment. J Natl Cancer Inst 94: 1113-1114, 2002.
16. Deryugina EI and Quigley JP: Matrix metalloproteinases and tumor metastasis. Cancer Metastasis Rev 25: 9-34, 2006.
17. Tryggvason K, Hoyhtya M and Pyke C: Type IV collagenases in invasive tumors. Breast Cancer Res Treat 24: 209-218, 1993.
18. Sato H, Takino T, Okada Y, Cao J, Shinagawa A, Yamamoto E and Seiki MA: Matrix metalloproteinase expressed on the surface of invasive tumour cells. Nature 370: 61-65, 1994.
19. Cazorla M, Hernández L, Nadal A, Balbín M, López JM, Vizoso F, Fernández PL, Iwata K, Cardesa A, López-Otín C and Campo E: Collagenase-3 expression is associated with advanced local invasion in human squamous cell carcinomas of the larynx. J Pathol 186: 144-150, 1997.
20. Culhaci N, Metin K, Copcu E and Dikicioglu E: Elevated expression of MMP-13 and TIMP-1 in head and neck squamous cell carcinomas may reflect increased tumor invasiveness. BMC Cancer 3: 4-42, 2004.
21. Chapman HA: Plasminogen activators, integrins, and the coordinated regulation of cell adhesion and migration. Curr Opin Cell Biol 9: 714-724, 1997.
22. Andreasen PA, Kjoller L, Christensen L and Duffy MJ: The urokinase-type plasminogen activator system in cancer metastasis, a review. Int J Cancer 72: 1-22, 1997.
23. Moons L, Shi C, Ploplis V, Plow E, Haber E, Collen D and Carmeliet P: Reduced transplant arteriosclerosis in plasminogen-deficient mice. J Clin Invest 102: 1788-1797, 1998.
24. Lijnen HR, van Hoef B, Lupu F, Moons L, Carmeliet P and Collen D: Function of the plasminogen/plasmin and matrix metalloproteinase systems after vascular injury in mice with targeted inactivation of fibrinolytic system genes. Arterioscler Thromb Vasc Biol 18: 1035-1045, 1998.
25. Urban P, Vuaroqueaux V, Labuhn M, Delorenzi M, Wirapati P, Wight E, Senn HJ, Benz C, Eppenberger U and Eppenberger-Castori S: Increased expression of urokinase-type plasminogen activator mRNA determines adverse prognosis in ErbB2-positive primary breast cancer. J Clin Oncol 24: 4245-4253, 2006.
26. Bosc DG, Goueli BS and Janknecht R: HER2/Neu-mediated activation of the ETS transcription factor ER81 and its target gene MMP-1. Oncogene 20: 6215-6224, 2001.
27. Gum R, Wang SW, Lengyel E, Yu D, Hung MC, Juarez J and Boyd D: Up-regulation of urokinase-type plasminogen activator expression by the HER2/neu proto oncogene. Anticancer Res 15: 1167-1172, 1995.
28. Ke Z, Lin H, Fan Z, Cai TQ, Kaplan RA, Ma C, Bower KA, Shi X and Luo J: MMP-2 mediates ethanol-induced invasion of mammary epithelial cells overexpressing ErbB2. Int J Cancer 119: 8-16, 2006.
29. Rocca GL, Pucci-Minafra I, Marrazzo A, Taormina P and Minafra S: Zymographic detection and clinical correlations of MMP-2 and MMP-9 in breast cancer sera. Br J Cancer 90: 1414-1421, 2004.
30. Pellikainen JM, Ropponen KM, Kataja VV, Kellokoski JK, Eskelinen MJ and Kosma VM: Expression of matrix metallo-proteinase (MMP)-2 and MMP-9 in breast cancer with a special reference tovactivator protein-2, HER2, and prognosis. Clin Cancer Res 10: 7621-7628, 2004.
31. Urban P, Vuaroqueaux V, Labuhn M, Delorenzi M, Wirapati P, Wight E, Senn HJ, Benz C, Eppenberger U and Eppenberger-Castori S: Increased expression of urokinase-type plasminogen activator mRNA determines adverse prognosis in ErbB2-positive primary breast cancer. J Clin Oncol 24: 245-253, 2006.
32. Kim IY, Yong HY, Kang KW and Moon A: Overexpression of ErbB2 induces invasion of MCF10A human breast epithelial cells via MMP-9. Cancer Lett 275: 227-233, 2009.
33. Kiaris H and Spandidos DA: Mutations of ras genes in human tumours. Int J Oncol 7: 413-421, 1995.
34. Clark GJ and Der CJ: Aberrant function of the Ras signal transduction pathway in human breast cancer. Breast Cancer Res Treat 35: 133-144, 1995.
35. Watson DM, Elton RA, Jack WJ, Dixon JM, Chetty U and Miller WR: The H-ras oncogene product p21 and prognosis in human breast cancer. Breast Cancer Res Treat 17: 161-169, 1991.
36. Franks LM and Teich NM: Cellular and Molecular Biology of Cancer. Oxford University Press, 1997.
37. Moon A, Kim MS, Kim TG, Kim SH, Kim HE, Chen YQ and Choi Kim HR: H-ras, but not N-ras, induces an invasive phenotype in human breast epithelial cells: a role for MMP-2 in the H-ras-induced invasive phenotype. Int J Cancer 85: 176-181, 2000.
38. Kim MS, Lee EJ, Choi Kim HR and Moon A: p38 kinase is a key signaling molecule for H-ras-induced cell motility and invasive phenotype in human breast epithelial cell. Cancer Res 63: 5454-5461, 2003.
39. Song H, Ki SH, Kim SG and Moon A: Activating transcription factor 2 mediates matrix metalloproteinase-2 transcriptional activation induced by p38 in breast epithelial cells. Cancer Res 66: 10487-10496, 2006.
40. Lee JY, Han CY, Yang JW, Smith C, Kim SK, Lee EY, Kim SG and Kang KW: Induction of glutathione transferase in insulin-like growth factor type I receptor-overexpressed hepatoma cells. Mol Pharmacol 72: 1082-1093, 2007.
41. Benard V, Bohl BP and Bokoch GM: Characterization of Rac and Cdc42 activation in chemoattractant-stimulated human neutrophils using a novel assay for active GTPases. J Biol Chem 274: 3198-3204, 1999.
42. Moon A, Yong HY, Song JI, Cukovic D, Salagrama S, Kaplan D, Putt D, Kim H, Dombkowski A and Kim HR: Global gene expression profiling unveils S100A8/A9 as candidate markers in H-Ras-mediated human breast epithelial cell invasion. Mol Cancer Res 6: 1544-1553, 2008.
43. Downward J: Targeting RAS signalling pathways in cancer therapy. Nat Rev Cancer 3: 11-22, 2003.
44. Tal-Or P, Erlich S, Porat-Shliom N, Goldshmit Y, Ben-Baruch G, Shaharabani E, Kloog Y and Pinkas-Kramarski R: Ligand-independent regulation of ErbB4 receptor phosphorylation by activated Ras. J Cell Biochem 98: 1482-1494, 2006.
45. Eckert LB, Repasky GA, Ulkü AS, McFall A, Zhou H, Sartor CI and Der CJ: Involvement of Ras activation in human breast cancer cell signaling, invasion, and anoikis. Cancer Res 64: 4585-4592, 2004.
46. Kruszewski W, Kowara R, Rzepko R, Warezak C, Zielinski J, Gryglewski G, Kopacz A, Jastrzebski T and Pawelczyk T: K-RAS point mutation, and amplification of c-myc and C-ERBB2 in colon adenocarcinoma. Folia Histochem Cytobiol 42: 173-179, 2004.
47. O-charoenrat P, Rhys-Evans PH, Archer DJ and Eccles SA: C-erbB receptors in squamous cell carcinomas of the head and neck: clinical significance and correlation with matrix metallo-proteinases and vascular endothelial growth factors. Oral Oncol 38: 73-80, 2002.
48. Meng S, Tripathy D, Shete S, Ashfaq R, Saboorian H, Haley B, Frenkel E, Euhus D, Leitch M, Osborne C, Clifford E, Perkins S, Beitsch P, Khan A, Morrison L, Herlyn D, Terstappen LW, Lane N, Wang J and Uhr J: uPAR and HER-2 gene status in individual breast cancer cells from blood and tissues. Proc Natl Acad Sci USA 103: 7361-17365, 2006.
49. Zhang B, Cao X, Liu Y, Cao W, Zhang F, Zhang S, Li H, Ning L, Fu L, Niu Y, Niu R, Sun B and Hao X: Tumor-derived matrix metalloproteinase-13 (MMP-13) correlates with poor prognoses of invasive breast cancer. BMC Cancer 28:8:83, 2008.
50. Shin I, Kim S, Song H, Kim HR and Moon A: H-Ras-specific activation of Rac MKK3/6-p38 pathway: its critical role in invasion and migration of breast epithelial cells. J Biol Chem 280: 14675-14683, 2005.
51. Ravanti L, Heino J, López-Otín C and Kähäri VM: Induction of collagenase-3 (MMP-13) expression in human skin fibroblasts by three-dimensional collagen is mediated by p38 mitogen-activated protein kinase. J Biol Chem 274: 2446-2455, 1999.
52. Johansson N, Ala-aho R, Uitto V, Grénman R, Fusenig NE, López-Otín C and Kähäri VM: Expression of collagenase-3 (MMP-13) and collagenase-1 (MMP-1) by transformed keratinocytes is dependent on the activity of p38 mitogen activated protein kinase. Cell Sci 113: 227-235, 2000.
53. Estrella VC, Eder AM, Liu S, Pustilnik TB, Tabassam FH, Claret FX, Gallick GE, Mills GB and Wiener JR: Lysophosphatidic acid induction of urokinase plasminogen activator secretion requires activation of the p38MAPK pathway. Int J Oncol 31: 441-449, 2007.