TMPRSS4 regulates levels of integrin 5 in NSCLC through miR-205 activity to promote metastasis

British Journal of Cancer

Volumn 110, Issue 3, 2014, Pages 764-774

  Larzabal, L ^a   De Aberasturi, A L ^a,b   Redrado, M ^a   Rueda, P ^c   Rodriguez, M J ^c   Bodegas, M E ^b   Montuenga, L M ^a,b   Calvo, A ^a,b  

^a UNIVERSITY OF NAVARRA   (Spain)

^b UNIVERSITY OF NAVARRA   (Spain)

^c Inmunologia y Genetica Aplicada SA   (Spain)

Author keywords

integrin a5; lung cancer; metastasis; miRNAs; TMPRSS4

Indexed keywords

CADHERINS; CARCINOMA, NON-SMALL-CELL LUNG; CELL CYCLE; CELL MOVEMENT; CELL PROLIFERATION; FIBRONECTINS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INTEGRIN ALPHA5; LUNG NEOPLASMS; MEMBRANE PROTEINS; MICRORNAS; NEOPLASM METASTASIS; SERINE ENDOPEPTIDASES; SIGNAL TRANSDUCTION;

EID: 84893805986     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2013.761     Document Type: Article

References (50)

1. Adachi M, Taki T, Higashiyama M, Kohno N, Inufusa H, Miyake M (2000) Significance of integrin alpha5 gene expression as a prognostic factor in node-negative non-small cell lung cancer. Clin Cancer Res 6(1): 96-101.
2. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116(2): 281-297.
3. Betel D, Wilson M, Gabow A, Marks DS, Sander C (2008) The microRNA.org resource: targets and expression. Nucleic Acids Res 36(Database issue): D149-D153.
4. Bracken CP, Gregory PA, Khew-Goodall Y, Goodall GJ (2009) The role of microRNAs in metastasis and epithelial-mesenchymal transition. Cell Mol Life Sci 66(10): 1682-1699.
5. Caldas C, Brenton JD (2005) Sizing up miRNAs as cancer genes. Nat Med 11(7): 712-714.
6. Cheadle C, Vawter MP, Freed WJ, Becker KG (2003) Analysis of microarray data using Z score transformation. J Mol Diagn 5(2): 73-81.
7. Chen CZ (2005) MicroRNAs as oncogenes and tumor suppressors. N Engl J Med 353(17): 1768-1771.
8. Dingemans AM, van den Boogaart V, Vosse BA, van Suylen RJ, Griffioen AW, Thijssen VL (2010) Integrin expression profiling identifies integrin alpha5 and beta1 as prognostic factors in early stage non-small cell lung cancer. Mol Cancer 9: 152.
9. Friedman RC, Farh KK, Burge CB, Bartel DP (2009) Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19(1): 92-105.
10. Gandellini P, Folini M, Longoni N, Pennati M, Binda M, Colecchia M, Salvioni R, Supino R, Moretti R, Limonta P, Valdagni R, Daidone MG, Zaffaroni N (2009) miR-205 Exerts tumor-suppressive functions in human prostate through down-regulation of protein kinase Cepsilon. Cancer Res 69(6): 2287-2295.
11. Giancotti FG, Ruoslahti E (1999) Integrin signaling. Science 285(5430): 1028-1032.
12. Gibbons DL, Lin W, Creighton CJ, Zheng S, Berel D, Yang Y, Raso MG, Liu DD, Wistuba II, Lozano G, Kurie JM (2009) Expression signatures of metastatic capacity in a genetic mouse model of lung adenocarcinoma. PLoS One 4(4): e5401.
13. Gogali A, Charalabopoulos K, Constantopoulos S (2004) Integrin receptors in primary lung cancer. Exp Oncol 26(2): 106-110.
14. Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G, Vadas MA, Khew-Goodall Y, Goodall GJ (2008) The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 10(5): 593-601.
15. Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ (2008) miRBase: tools for microRNA genomics. Nucleic Acids Res 36(Database issue): D154-D158.
16. Hamamoto J, Soejima K, Yoda S, Naoki K, Nakayama S, Satomi R, Terai H, Ikemura S, Sato T, Yasuda H, Hayashi Y, Sakamoto M, Takebayashi T, Betsuyaku T (2013) Identification of microRNAs differentially expressed between lung squamous cell carcinoma and lung adenocarcinoma. Mol Med Rep 8(2): 456-462.
17. Hood JD, Cheresh DA (2002) Role of integrins in cell invasion and migration. Nat Rev Cancer 2(2): 91-100.
18. Hooper JD, Clements JA, Quigley JP, Antalis TM (2001) Type II transmembrane serine proteases. Insights into an emerging class of cell surface proteolytic enzymes. J Biol Chem 276(2): 857-860.
19. Iorio MV, Casalini P, Piovan C, Di Leva G, Merlo A, Triulzi T, Menard S, Croce CM, Tagliabue E (2009) microRNA-205 regulates HER3 in human breast cancer. Cancer Res 69(6): 2195-2200.
20. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP (2003) Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 31(4): e15.
21. Jemal A, Siegel R, Xu J, Ward E (2010) Cancer statistics, 2010. CA Cancer J Clin 60(5): 277-300.
22. Jiang M, Zhang P, Hu G, Xiao Z, Xu F, Zhong T, Huang F, Kuang H, Zhang W (2013) Relative expression of miR-205-5p and miR-205-3p, and miR-21 in tissues and serum of non-small cell lung cancer patients. Mol Cell Biochem 383(1-2): 67-75.
23. Jung H, Lee KP, Park SJ, Park JH, Jang YS, Choi SY, Jung JG, Jo K, Park DY, Yoon JH, Lim DS, Hong GR, Choi C, Park YK, Lee JW, Hong HJ, Kim S, Park YW (2008) TMPRSS4 promotes invasion, migration and metastasis of human tumor cells by facilitating an epithelial-mesenchymal transition. Oncogene 27(18): 2635-2647.
24. Kebebew E, Peng M, Reiff E, Duh QY, Clark OH, McMillan A (2005) ECM1 and TMPRSS4 are diagnostic markers of malignant thyroid neoplasms and improve the accuracy of fine needle aspiration biopsy. Ann Surg 242(3): 353-361 (discussion 361-3).
25. Kim S, Kang HY, Nam EH, Choi MS, Zhao XF, Hong CS, Lee JW, Lee JH, Park YK (2010) TMPRSS4 induces invasion and epithelial-mesenchymal transition through upregulation of integrin alpha5 and its signaling pathways. Carcinogenesis 31(4): 597-606.
26. Kloosterman WP, Plasterk RH (2006) The diverse functions of microRNAs in animal development and disease. Dev Cell 11(4): 441-450.
27. Larzabal L, Nguewa PA, Pio R, Blanco D, Sanchez B, Rodriguez MJ, Pajares MJ, Catena R, Montuenga LM, Calvo A (2011) Overexpression of TMPRSS4 in non-small cell lung cancer is associated with poor prognosis in patients with squamous histology. Br J Cancer 105(10): 1608-1614.
28. Lebanony D, Benjamin H, Gilad S, Ezagouri M, Dov A, Ashkenazi K, Gefen N, Izraeli S, Rechavi G, Pass H, Nonaka D, Li J, Spector Y, Rosenfeld N, Chajut A, Cohen D, Aharonov R, Mansukhani M (2009) Diagnostic assay based on hsa-miR-205 expression distinguishes squamous from nonsquamous non-small-cell lung carcinoma. J Clin Oncol 27(12): 2030-2037.
29. Lim LP, Lau NC, Garrett-Engele P, Grimson A, Schelter JM, Castle J, Bartel DP, Linsley PS, Johnson JM (2005) Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433(7027): 769-773.
30. Lujambio A, Calin GA, Villanueva A, Ropero S, Sanchez-Cespedes M, Blanco D, Montuenga LM, Rossi S, Nicoloso MS, Faller WJ, Gallagher WM, Eccles SA, Croce CM, Esteller M (2008) A microRNA DNA methylation signature for human cancer metastasis. Proc Natl Acad Sci USA 105(36): 13556-13561.
31. Majid S, Saini S, Dar AA, Hirata H, Shahryari V, Tanaka Y, Yamamura S, Ueno K, Zaman MS, Singh K, Chang I, Deng G, Dahiya R (2011) MicroRNA-205 inhibits Src-mediated oncogenic pathways in renal cancer. Cancer Res 71(7): 2611-2621.
32. Markou A, Tsaroucha EG, Kaklamanis L, Fotinou M, Georgoulias V, Lianidou ES (2008) Prognostic value of mature microRNA-21 and microRNA-205 overexpression in non-small cell lung cancer by quantitative real-time RT-PCR. Clin Chem 54(10): 1696-1704.
33. Maschler S, Wirl G, Spring H, Bredow DV, Sordat I, Beug H, Reichmann E (2005) Tumor cell invasiveness correlates with changes in integrin expression and localization. Oncogene 24(12): 2032-2041.
34. Matsushima K, Isomoto H, Yamaguchi N, Inoue N, Machida H, Nakayama T, Hayashi T, Kunizaki M, Hidaka S, Nagayasu T, Nakashima M, Ujifuku K, Mitsutake N, Ohtsuru A, Yamashita S, Korpal M, Kang Y, Gregory PA, Goodall GJ, Kohno S, Nakao K (2011) MiRNA-205 modulates cellular invasion and migration via regulating zinc finger E-box binding homeobox 2 expression in esophageal squamous cell carcinoma cells. J Transl Med 9: 30.
35. Nam EH, Lee Y, Park YK, Lee JW, Kim S (2012) ZEB2 upregulates integrin alpha5 expression through cooperation with Sp1 to induce invasion during epithelial-mesenchymal transition of human cancer cells. Carcinogenesis 33(3): 563-571.
36. Netzel-Arnett S, Hooper JD, Szabo R, Madison EL, Quigley JP, Bugge TH, Antalis TM (2003) Membrane anchored serine proteases: a rapidly expanding group of cell surface proteolytic enzymes with potential roles in cancer. Cancer Metastasis Rev 22(2-3): 237-258.
37. Park SM, Gaur AB, Lengyel E, Peter ME (2008) The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev 22(7): 894-907.
38. Ponz-Sarvise M, Nguewa PA, Pajares MJ, Agorreta J, Lozano MD, Redrado M, Pio R, Behrens C, Wistuba II, Garcia-Franco CE, Garcia-Foncillas J, Montuenga LM, Calvo A, Gil-Bazo I (2011) Inhibitor of differentiation-1 as a novel prognostic factor in NSCLC patients with adenocarcinoma histology and its potential contribution to therapy resistance. Clin Cancer Res 17(12): 4155-4166.
39. Ramirez RD, Sheridan S, Girard L, Sato M, Kim Y, Pollack J, Peyton M, Zou Y, Kurie JM, Dimaio JM, Milchgrub S, Smith AL, Souza RF, Gilbey L, Zhang X, Gandia K, Vaughan MB, Wright WE, Gazdar AF, Shay JW, Minna JD (2004) Immortalization of human bronchial epithelial cells in the absence of viral oncoproteins. Cancer Res 64(24): 9027-9034.
40. Roman J, Ritzenthaler JD, Roser-Page S, Sun X, Han S (2010) alpha5beta1-integrin expression is essential for tumor progression in experimental lung cancer. Am J Respir Cell Mol Biol 43(6): 684-691.
41. Roy R, Yang J, Moses MA (2009) Matrix metalloproteinases as novel biomarkers and potential therapeutic targets in human cancer. J Clin Oncol 27(31): 5287-5297.
42. Sawada K, Mitra AK, Radjabi AR, Bhaskar V, Kistner EO, Tretiakova M, Jagadeeswaran S, Montag A, Becker A, Kenny HA, Peter ME, Ramakrishnan V, Yamada SD, Lengyel E (2008) Loss of E-cadherin promotes ovarian cancer metastasis via alpha 5-integrin, which is a therapeutic target. Cancer Res 68(7): 2329-2339.
43. Song H, Bu G (2009) MicroRNA-205 inhibits tumor cell migration through down-regulating the expression of the LDL receptor-related protein 1. Biochem Biophys Res Commun 388(2): 400-405.
44. Szabo R, Bugge TH (2008) Type II transmembrane serine proteases in development and disease. Int J Biochem Cell Biol 40(6-7): 1297-1316.
45. Tellez CS, Juri DE, Do K, Bernauer AM, Thomas CL, Damiani LA, Tessema M, Leng S, Belinsky SA (2011) EMT and stem cell-like properties associated with miR-205 and miR-200 epigenetic silencing are early manifestations during carcinogen-induced transformation of human lung epithelial cells. Cancer Res 71(8): 3087-3097.
46. Valencia K, Ormazabal C, Zandueta C, Luis-Ravelo D, Anton I, Pajares MJ, Agorreta J, Montuenga LM, Martinez-Canarias S, Leitinger B, Lecanda F (2012) Inhibition of collagen receptor discoidin domain receptor-1 (DDR1) reduces cell survival, homing, and colonization in lung cancer bone metastasis. Clin Cancer Res 18(4): 969-980.
47. Wallrapp C, Hahnel S, Muller-Pillasch F, Burghardt B, Iwamura T, Ruthenburger M, Lerch MM, Adler G, Gress TM (2000) A novel transmembrane serine protease (TMPRSS3) overexpressed in pancreatic cancer. Cancer Res 60(10): 2602-2606.
48. Wu H, Mo YY (2009) Targeting miR-205 in breast cancer. Expert Opin Ther Targets 13(12): 1439-1448.
49. Wu H, Zhu S, Mo YY (2009) Suppression of cell growth and invasion by miR-205 in breast cancer. Cell Res 19(4): 439-448.
50. Yanaihara N, Caplen N, Bowman E, Seike M, Kumamoto K, Yi M, Stephens RM, Okamoto A, Yokota J, Tanaka T, Calin GA, Liu CG, Croce CM, Harris CC (2006) Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell 9(3): 189-198