Identification of novel TMPRSS2:ERG mechanisms in prostate cancer metastasis: Involvement of MMP9 and PLXNA2

Oncogene

Volumn 33, Issue 17, 2014, Pages 2204-2214

  Tian, T V ^a,b,c   Tomavo, N ^a,b,c   Huot, L ^b,c,d   Flourens, A ^a,b,c   Bonnelye, E ^e   Flajollet, S ^a,b,c   Hot, D ^b,c,d   Leroy, X ^c,f   De Launoit, Y ^a,b,c   Duterque Coquillaud, M ^a,b,c  

^a INSTITUT DE BIOLOGIE DE LILLE   (France)

^b INSTITUT PASTEUR DE LILLE   (France)

^c UNIV LILLE   (France)

^d INSERM U1019   (France)

^e University of Lyon Claude Bernard   (France)

^f LILLE UNIVERSITY HOSPITAL   (France)

Author keywords

invasion; migration; MMP9; PLXNA2; prostate cancer; TMPRSS2:ERG fusion

Indexed keywords

ANDROGEN RECEPTOR; COMPLEMENTARY DNA; MESSENGER RNA; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL; CELL CLONE; CELL MIGRATION; GENE; GENE EXPRESSION REGULATION; GENE FUSION; GENE SEQUENCE; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; METASTASIS; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROSTATE CANCER; TMPRSS2 ERG GENE; TUMOR INVASION;

CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; GENE EXPRESSION REGULATION; HUMANS; LYMPHATIC METASTASIS; MALE; MATRIX METALLOPROTEINASE 9; NERVE TISSUE PROTEINS; ONCOGENE PROTEINS, FUSION; PHENOTYPE; PROSTATIC NEOPLASMS; RECEPTORS, CELL SURFACE; TRANSCRIPTOME;

EID: 84899649184     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.176     Document Type: Article

References (80)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2012. CA Cancer J Clin 2012; 62: 10-29.
2. Squire JA, Park PC, Yoshimoto M, Alami J, Williams JL, Evans A et al. Prostate cancer as a model system for genetic diversity in tumors. Adv Cancer Res 2011; 112: 183-216.
3. Rubin MA, Maher CA, Chinnaiyan AM. Common gene rearrangements in prostate cancer. J Clin Oncol 2011; 29: 3659-3668.
4. Tomlins SA, Rhodes DR, Perner S, Dhanasekaran SM, Mehra R, Sun XW et al. Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science 2005; 310: 644-648.
5. Wang J, Cai Y, Ren C, Ittmann M. Expression of variant TMPRSS2/ERG fusion messenger RNAs is associated with aggressive prostate cancer. Cancer Res 2006; 66: 8347-8351.
6. FitzGerald LM, Agalliu I, Johnson K, Miller MA, Kwon EM, Hurtado-Coll A et al. Association of TMPRSS2-ERG gene fusion with clinical characteristics and outcomes: results from a population-based study of prostate cancer. BMC Cancer 2008; 8: 230.
7. Gopalan A, Leversha MA, Satagopan JM, Zhou Q, Al-Ahmadie HA, Fine SW et al. TMPRSS2-ERG gene fusion is not associated with outcome in patients treated by prostatectomy. Cancer Res 2009; 69: 1400-1406.
8. Hoogland AM, Jenster G, van Weerden WM, Trapman J, van der Kwast T, Roobol MJ et al. ERG immunohistochemistry is not predictive for PSA recurrence, local recurrence or overall survival after radical prostatectomy for prostate cancer. Mod Pathol 2012; 25: 471-479.
9. Hermans KG, Boormans JL, Gasi D, van Leenders GJ, Jenster G, Verhagen PC et al. Overexpression of prostate-specific TMPRSS2(exon 0)-ERG fusion transcripts corresponds with favorable prognosis of prostate cancer. Clin Cancer Res 2009; 15: 6398-6403.
10. Saramaki OR, Harjula AE, Martikainen PM, Vessella RL, Tammela TL, Visakorpi T. TMPRSS2:ERG fusion identifies a subgroup of prostate cancers with a favorable prognosis. Clin Cancer Res 2008; 14: 3395-3400.
11. Attard G, Clark J, Ambroisine L, Fisher G, Kovacs G, Flohr P et al. Duplication of the fusion of TMPRSS2 to ERG sequences identifies fatal human prostate cancer. Oncogene 2008; 27: 253-263.
12. Demichelis F, Fall K, Perner S, Andren O, Schmidt F, Setlur SR et al. TMPRSS2:ERG gene fusion associated with lethal prostate cancer in a watchful waiting cohort. Oncogene 2007; 26: 4596-4599.
13. Nam RK, Sugar L, Wang Z, Yang W, Kitching R, Klotz LH et al. Expression of TMPRSS2:ERG gene fusion in prostate cancer cells is an important prognostic factor for cancer progression. Cancer Biol Ther 2007; 6: 40-45.
14. Nam RK, Sugar L, Yang W, Srivastava S, Klotz LH, Yang LY et al. Expression of the TMPRSS2:ERG fusion gene predicts cancer recurrence after surgery for localised prostate cancer. Br J Cancer 2007; 97: 1690-1695.
15. Perner S, Demichelis F, Beroukhim R, Schmidt FH, Mosquera JM, Setlur S et al. TMPRSS2:ERG fusion-associated deletions provide insight into the heterogeneity of prostate cancer. Cancer Res 2006; 66: 8337-8341.
16. Mehra R, Tomlins SA, Yu J, Cao X, Wang L, Menon A et al. Characterization of TMPRSS2-ETS gene aberrations in androgen-independent metastatic prostate cancer. Cancer Res 2008; 68: 3584-3590.
17. Tomlins SA, Laxman B, Varambally S, Cao X, Yu J, Helgeson BE et al. Role of the TMPRSS2-ERG gene fusion in prostate cancer. Neoplasia 2008; 10: 177-188.
18. Klezovitch O, Risk M, Coleman I, Lucas JM, Null M, True LD et al. A causal role for ERG in neoplastic transformation of prostate epithelium. Proc Natl Acad Sci USA 2008; 105: 2105-2110.
19. Zong Y, Xin L, Goldstein AS, Lawson DA, Teitell MA, Witte ON. ETS family transcription factors collaborate with alternative signaling pathways to induce carcinoma from adult murine prostate cells. Proc Natl Acad Sci USA 2009; 106: 12465-12470.
20. King JC, Xu J, Wongvipat J, Hieronymus H, Carver BS, Leung DH et al. Cooperativity of TMPRSS2-ERG with PI3-kinase pathway activation in prostate oncogenesis. Nat Genet 2009; 41: 524-526.
21. Carver BS, Tran J, Gopalan A, Chen Z, Shaikh S, Carracedo A et al. Aberrant ERG expression cooperates with loss of PTEN to promote cancer progression in the prostate. Nat Genet 2009; 41: 619-624.
22. Yu J, Yu J, Mani RS, Cao Q, Brenner CJ, Cao X et al. An integrated network of androgen receptor, polycomb, and TMPRSS2-ERG gene fusions in prostate cancer progression. Cancer Cell 2010; 17: 443-454.
23. Wei GH, Badis G, Berger MF, Kivioja T, Palin K, Enge M et al. Genome-wide analysis of ETS-family DNA-binding in vitro and in vivo. Embo J 2010; 29: 2147-2160.
24. Chng KR, Chang CW, Tan SK, Yang C, Hong SZ, Sng NY et al. A transcriptional repressor co-regulatory network governing androgen response in prostate cancers. Embo J 2011; 31: 2810-2823.
25. Macintosh CA, Stower M, Reid N, Maitland NJ. Precise microdissection of human prostate cancers reveals genotypic heterogeneity. Cancer Res 1998; 58: 23-28.
26. Cheng L, Song SY, Pretlow TG, Abdul-Karim FW, Kung HJ, Dawson DV et al. Evidence of independent origin of multiple tumors from patients with prostate cancer. J Natl Cancer Inst 1998; 90: 233-237.
27. Andreoiu M, Cheng L. Multifocal prostate cancer: biologic, prognostic, and therapeutic implications. Hum Pathol 2010; 41: 781-793.
28. Mehra R, Han B, Tomlins SA, Wang L, Menon A, Wasco MJ et al. Heterogeneity of TMPRSS2 gene rearrangements in multifocal prostate adenocarcinoma: molecular evidence for an independent group of diseases. Cancer Res 2007; 67: 7991-7995.
29. Barry M, Perner S, Demichelis F, Rubin MA. TMPRSS2-ERG fusion heterogeneity in multifocal prostate cancer: clinical and biologic implications. Urology 2007; 70: 630-633.
30. Minner S, Gartner M, Freudenthaler F, Bauer M, Kluth M, Salomon G et al. Marked heterogeneity of ERG expression in large primary prostate cancers. Mod Pathol 2012; 26: 106-116.
31. Furusato B, Tan SH, Young D, Dobi A, Sun C, Mohamed AA et al. ERG oncoprotein expression in prostate cancer: clonal progression of ERG-positive tumor cells and potential for ERG-based stratification. Prostate Cancer Prostatic Dis 2010; 13: 228-237.
32. Fradet A, Sorel H, Deux B, Clé zardin P, Bonnelye E. A new murine model of osteoblastic/osteolytic lesions from human androgen-resistant prostate cancer. Bone 2010; 47(Special Issue): S289.
33. Scher HI, Morris MJ, Basch E, Heller G. End points and outcomes in castrationresistant prostate cancer: from clinical trials to clinical practice. J Clin Oncol 2011; 29: 3695-3704.
34. Clark J, Merson S, Jhavar S, Flohr P, Edwards S, Foster CS et al. Diversity of TMPRSS2-ERG fusion transcripts in the human prostate. Oncogene 2007; 26: 2667-2673.
35. Wang J, Cai Y, Yu W, Ren C, Spencer DM, Ittmann M. Pleiotropic biological activities of alternatively spliced TMPRSS2/ERG fusion gene transcripts. Cancer Res 2008; 68: 8516-8524.
36. Kunderfranco P, Mello-Grand M, Cangemi R, Pellini S, Mensah A, Albertini V et al. ETS transcription factors control transcription of EZH2 and epigenetic silencing of the tumor suppressor gene Nkx3.1 in prostate cancer. PLoS One 2010; 5: e10547.
37. 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.
38. Patrawala L, Calhoun T, Schneider-Broussard R, Li H, Bhatia B, Tang S et al. Highly purified CD44 prostate cancer cells from xenograft human tumors are enriched in tumorigenic and metastatic progenitor cells. Oncogene 2006; 25: 1696-1708.
39. Castellano G, Malaponte G, Mazzarino MC, Figini M, Marchese F, Gangemi P et al. Activation of the osteopontin/matrix metalloproteinase-9 pathway correlates with prostate cancer progression. Clin Cancer Res 2008; 14: 7470-7480.
40. Nese N, Kandiloglu AR, Simsek G, Lekili M, Ozdamar A, Catalkaya A et al. Comparison of the desmoplastic reaction and invading ability in invasive ductal carcinoma of the breast and prostatic adenocarcinoma based on the expression of heat shock protein 47 and fascin. Anal Quant Cytol Histol 2010; 32: 90-101.
41. Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009; 4: 44-57.
42. Steffan JJ, Koul S, Meacham RB, Koul HK. The transcription factor SPDEF suppresses prostate tumor metastasis. J Biol Chem 2012; 287: 29968-29978.
43. Himelstein BP, Lee EJ, Sato H, Seiki M, Muschel RJ. Transcriptional activation of the matrix metalloproteinase-9 gene in an H-ras and v-myc transformed rat embryo cell line. Oncogene 1997; 14: 1995-1998.
44. Franco M, Tamagnone L. Tyrosine phosphorylation in semaphorin signalling: shifting into overdrive. EMBO Rep 2008; 9: 865-871.
45. Capparuccia L, Tamagnone L. Semaphorin signaling in cancer cells and in cells of the tumor microenvironment-two sides of a coin. J Cell Sci 2009; 122: 1723-1736.
46. Wong OG, Nitkunan T, Oinuma I, Zhou C, Blanc V, Brown RS et al. Plexin-B1 mutations in prostate cancer. Proc Natl Acad Sci USA 2007; 104: 19040-19045.
47. Deryugina EI, Quigley JP. Matrix metalloproteinases and tumor metastasis. Cancer Metastasis Rev 2006; 25: 9-34.
48. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144: 646-674.
49. Dhanasekaran SM, Barrette TR, Ghosh D, Shah R, Varambally S, Kurachi K et al. Delineation of prognostic biomarkers in prostate cancer. Nature 2001; 412: 822-826.
50. Grasso CS, Wu YM, Robinson DR, Cao X, Dhanasekaran SM, Khan AP et al. The mutational landscape of lethal castration-resistant prostate cancer. Nature 2012; 487: 239-243.
51. Varambally S, Yu J, Laxman B, Rhodes DR, Mehra R, Tomlins SA et al. Integrative genomic and proteomic analysis of prostate cancer reveals signatures of metastatic progression. Cancer Cell 2005; 8: 393-406.
52. Mitelman F, Johansson B, Mertens F. The impact of translocations and gene fusions on cancer causation. Nat Rev Cancer 2007; 7: 233-245.
53. Leshem O, Madar S, Kogan-Sakin I, Kamer I, Goldstein I, Brosh R et al. TMPRSS2/ ERG promotes epithelial to mesenchymal transition through the ZEB1/ZEB2 axis in a prostate cancer model. PLoS One 2011; 6: e21650.
54. Attard G, Swennenhuis JF, Olmos D, Reid AH, Vickers E, A'Hern R et al. Characterization of ERG, AR and PTEN gene status in circulating tumor cells from patients with castration-resistant prostate cancer. Cancer Res 2009; 69: 2912-2918.
55. Stott SL, Lee RJ, Nagrath S, Yu M, Miyamoto DT, Ulkus L et al. Isolation and characterization of circulating tumor cells from patients with localized and metastatic prostate cancer. Sci Transl Med 2010; 2: 25ra3.
56. Guo CC, Wang Y, Xiao L, Troncoso P, Czerniak BA. The relationship of TMPRSS2- ERG gene fusion between primary and metastatic prostate cancers. Hum Pathol 2012; 43: 644-649.
57. Perner S, Svensson MA, Hossain RR, Day JR, Groskopf J, Slaughter RC et al. ERG rearrangement metastasis patterns in locally advanced prostate cancer. Urology 2010; 75: 762-767.
58. Polyak K, Weinberg RA. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer 2009; 9: 265-273.
59. Valastyan S, Weinberg RA. Tumor metastasis: molecular insights and evolving paradigms. Cell 2012; 147: 275-292.
60. Becker-Santos DD, Guo Y, Ghaffari M, Vickers ED, Lehman M, Altamirano-Dimas M et al. Integrin-linked kinase as a target for ERG-mediated invasive properties in prostate cancer models. Carcinogenesis 2012; 33: 2558-2567.
61. Kessenbrock K, Plaks V, Werb Z. Matrix metalloproteinases: regulators of the tumor microenvironment. Cell 2010; 141: 52-67.
62. Dos Reis ST, Pontes Jr J, Villanova FE, Borra PM, Antunes AA, Dall'oglio MF et al. Genetic polymorphisms of matrix metalloproteinases: susceptibility and prognostic implications for prostate cancer. J Urol 2009; 181: 2320-2325.
63. Nakamura Y, Esnault S, Maeda T, Kelly EA, Malter JS, Jarjour NN. Ets-1 regulates TNF-alpha-induced matrix metalloproteinase-9 and tenascin expression in primary bronchial fibroblasts. J Immunol 2004; 172: 1945-1952.
64. Hanzawa M, Shindoh M, Higashino F, Yasuda M, Inoue N, Hida K et al. Hepatocyte growth factor upregulates E1AF that induces oral squamous cell carcinoma cell invasion by activating matrix metalloproteinase genes. Carcinogenesis 2000; 21: 1079-1085.
65. Hance MW, Dole K, Gopal U, Bohonowych JE, Jezierska-Drutel A, Neumann CA et al. Secreted Hsp90 is a novel regulator of the epithelial to mesenchymal transition (EMT) in prostate cancer. J Biol Chem 2012; 287: 37732-37744.
66. Kato T, Fujita Y, Nakane K, Kojima T, Nozawa Y, Deguchi T et al. ETS1 promotes chemoresistance and invasion of paclitaxel-resistant, hormone-refractory PC3 prostate cancer cells by up-regulating MDR1 and MMP9 expression. Biochem Biophys Res Commun 2012; 417: 966-971.
67. Bergers G, Brekken R, McMahon G, Vu TH, Itoh T, Tamaki K et al. Matrix metalloproteinase- 9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol 2000; 2: 737-744.
68. Hiratsuka S, Nakamura K, Iwai S, Murakami M, Itoh T, Kijima H et al. MMP9 induction by vascular endothelial growth factor receptor-1 is involved in lungspecific metastasis. Cancer Cell 2002; 2: 289-300.
69. Kolodkin AL, Matthes DJ, Goodman CS. The semaphorin genes encode a family of transmembrane and secreted growth cone guidance molecules. Cell 1993; 75: 1389-1399.
70. Biankin AV, Waddell N, Kassahn KS, Gingras MC, Muthuswamy LB, Johns AL et al. Pancreatic cancer genomes reveal aberrations in axon guidance pathway genes. Nature 2012; 491: 399-405.
71. Blanc V, Nariculam J, Munson P, Freeman A, Klocker H, Masters J et al. A role for class 3 semaphorins in prostate cancer. Prostate 2011; 71: 649-658.
72. Zhou C, Wong OG, Masters JR, Williamson M. Effect of cancer-associated mutations in the PlexinB1 gene. Mol Cancer 2012; 11: 11.
73. Vlaeminck-Guillem V, Carrere S, Dewitte F, Stehelin D, Desbiens X, Duterque- Coquillaud M. The Ets family member Erg gene is expressed in mesodermal tissues and neural crests at fundamental steps during mouse embryogenesis. Mech Dev 2000; 91: 331-335.
74. Brown CB, Feiner L, Lu MM, Li J, Ma X, Webber AL et al. PlexinA2 and semaphorin signaling during cardiac neural crest development. Development 2001; 128: 3071-3080.
75. Toyofuku T, Yoshida J, Sugimoto T, Yamamoto M, Makino N, Takamatsu H et al. Repulsive and attractive semaphorins cooperate to direct the navigation of cardiac neural crest cells. Dev Biol 2008; 321: 251-262.
76. Dhordain P, Dewitte F, Desbiens X, Stehelin D, Duterque-Coquillaud M. Mesodermal expression of the chicken erg gene associated with precartilaginous condensation and cartilage differentiation. Mech Dev 1995; 50: 17-28.
77. Kodo K, Nishizawa T, Furutani M, Arai S, Yamamura E, Joo K et al. GATA6 mutations cause human cardiac outflow tract defects by disrupting semaphorin-plexin signaling. Proc Natl Acad Sci USA 2009; 106: 13933-13938.
78. Le Jeune M, Tomavo N, Tian TV, Flourens A, Marchand N, Camuzeaux B et al. Identification of four alternatively spliced transcripts of the Ucma/GRP gene, encoding a new Gla-containing protein. Exp Cell Res 2010; 316: 203-215.
79. Sakurai-Yageta M, Recchi C, Le Dez G, Sibarita JB, Daviet L, Camonis J et al. The interaction of IQGAP1 with the exocyst complex is required for tumor cell invasion downstream of Cdc42 and RhoA. J Cell Biol 2008; 181: 985-998.
80. Flajollet S, Poras I, Carosella ED, Moreau P. RREB-1 is a transcriptional repressor of HLA-G. J Immunol 2009; 183: 6948-6959.