Dysregulated protease activated receptor 1 (PAR1) promotes metastatic phenotype in breast cancer through HMGA2

Oncogene

Volumn 35, Issue 12, 2016, Pages 1529-1540

  Yang, E ^a   Cisowski, J ^a   Nguyen, N ^a   O'Callaghan, K ^a   Xu, J ^a   Agarwal, A ^a   Kuliopulos, A ^a   Covic, L ^a  

^a TUFTS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESTROGEN RECEPTOR; HIGH MOBILITY GROUP A2 PROTEIN; PROTEINASE ACTIVATED RECEPTOR 1; UVOMORULIN; VIMENTIN;

ADVANCED CANCER; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASAL CELL CARCINOMA; BREAST CARCINOMA; BREAST METASTASIS; CELL SELF-RENEWAL; CONTROLLED STUDY; DOWN REGULATION; ECTOPIC EXPRESSION; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; MCF 7 CELL LINE; MESENCHYME CELL; MOUSE; MUTANT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TUMOR INVASION; UPREGULATION; BREAST TUMOR; METABOLISM; METASTASIS; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

BREAST NEOPLASMS; FEMALE; HMGA2 PROTEIN; HUMANS; MCF-7 CELLS; NEOPLASM METASTASIS; PHENOTYPE; RECEPTOR, PAR-1; VIMENTIN;

EID: 84957922704     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2015.217     Document Type: Article

References (54)

1. Vu T-KH, Hung DT, Wheaton VI, Coughlin SR. Molecular cloning of a functional thrombin receptor reveals a novel proteolytic mechanism of receptor action. Cell 1991; 64: 1057-1068
2. Even-Ram S, Uziely B, Cohen P, Grisaru-Granovsky S, Maoz M, Ginzburg Y, et al. Thrombin receptor overexpression in malignant and physiological invasion processes. Nat Med 1998; 4: 909-914
3. Henrikson KP, Salazar SL, Fenton JW, Pentecost BT. Role of thrombin receptor in breast cancer invasiveness. Br J Cancer 1999; 79: 401-406
4. Cisowski J, O'Callaghan K, Kuliopulos A, Yang J, Nguyen N, Deng Q, et al. Targeting protease-activated receptor-1 with cell-penetrating pepducins in lung cancer. Am J Pathol 2011; 179: 513-523
5. Rudroff C, Seibold S, Kaufmann R, Zetina CC, Reise K, Schafer U, et al. Expression of the thrombin receptor PAR-1 correlates with tumour cell differentiation of pancreatic adenocarcinoma in vitro. Clin Exp Metastasis 2002; 19: 181-189
6. Nierodzik ML, Chen K, Takeshita K, Li JJ, Huang YQ, Feng XS, et al. Proteaseactivated receptor 1 (PAR-1) is required and rate-limiting for thrombin-enhanced experimental pulmonary metastasis. Blood 1998; 92: 3694-3700
7. Even-Ram SC, Maoz M, Pokroy E, Reich R, Katz B-Z, Gutwein P, et al. Tumor cell invasion is promoted by activation of protease activated receptor-1 in cooperation with the alpha vbeta 5 integrin. J Biol Chem 2001; 276: 10952-10962
8. Tellez C, Bar-Eli M. Role and regulation of the thrombin receptor (PAR-1) in human melanoma. Oncogene 2003; 22: 3130-3137
9. Whitehead I, Kirk H, Kay R. Expression cloning of oncogenes by retroviral transfer of cDNA libraries. Mol Cell Biol 1995; 15: 704-710
10. Martin CB, Mahon GM, Klinger MB, Kay RJ, Symons M, Der CJ, et al. The thrombin receptor, PAR-1, causes transformation by activation of Rho-mediated signaling pathways. Oncogene 2001; 20: 1953-1963
11. Korkola JE, DeVries S, Fridlyand J, Hwang ES, Estep ALH, Chen Y-Y, et al. Differentiation of lobular versus ductal breast carcinomas by expression microarray analysis. Cancer Res 2003; 63: 7167-7175
12. Boire A, Covic L, Agarwal A, Jacques S, Sharifi S, Kuliopulos A. PAR1 is a matrix metalloprotease-1 receptor that promotes invasion and tumorigenesis of breast cancer cells. Cell 2005; 120: 303-313
13. Agarwal A, Covic L, Sevigny LM, Kaneider NC, Lazarides K, Azabdaftari G, et al. Targeting a metalloprotease-PAR1 signaling system with cell-penetrating pepducins inhibits angiogenesis, ascites, and progression of ovarian cancer. Mol Cancer Ther 2008; 7: 2746-2757
14. Nguyen N, Kuliopulos A, Graham RA, Covic L. Tumor-derived Cyr61(CCN1) promotes stromal matrix metalloprotease-1 production and protease-activated receptor 1-dependent migration of breast cancer cells. Cancer Res 2006; 66: 2658-2665
15. Yang E, Boire A, Agarwal A, Nguyen N, O'Callaghan K, Tu P, et al. Blockade of PAR1 signaling with cell-penetrating pepducins inhibits Akt survival pathways in breast cancer cells and suppresses tumor survival and metastasis. Cancer Res 2009; 69: 6223-6231
16. Perou CM, Sorlie T, Eisen MB, Van De Rijn M, Jeffrey SS, Rees CA, et al. Molecular portraits of human breast tumours. Nature 2000; 406: 747-752
17. Thiery JP, Sleeman JP. Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 2006; 7: 131-142
18. Slofstra SH, Bijlsma MF, Groot AP, Reitsma PH, Lindhout T, ten Cate H, et al. Protease-activated receptor-4 inhibition protects from multiorgan failure in a murine model of systemic inflammation. Blood 2007; 110: 3176-3182
19. Satelli A, Li S. Vimentin in cancer and its potential as a molecular target for cancer therapy. Cell Mol Life Sci 2011; 68: 3033-3046
20. 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
21. Aigner K, Dampier B, Descovich L, Mikula M, Sultan A, Schreiber M, et al. The transcription factor ZEB1 (deltaEF1) promotes tumour cell dedifferentiation by repressing master regulators of epithelial polarity. Oncogene 2007; 26: 6979-6988
22. Bolos V, Peinado H, Perez-Moreno MA, Fraga MF, Esteller M, Cano A. The transcription factor Slug represses E-cadherin expression and induces epithelial to mesenchymal transitions: a comparison with Snail and E47 repressors. J Cell Sci 2003; 116: 499-511
23. Cano A, Perez-Moreno MA, Rodrigo I, Locascio A, Blanco MJ, del Barrio MG, et al. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol 2000; 2: 76-83
24. Tallini G, Dal Cin P, Rhoden KJ, Chiapetta G, Manfioletti G, Giancotti V, et al. Expression of HMGI-C and HMGI(Y) in ordinary lipoma and atypical lipomatous tumors: immunohistochemical reactivity correlates with karyotypic alterations. Am J Pathol 1997; 151: 37-43
25. Medeiros F, Erickson-Johnson MR, Keeney GL, Clayton AC, Nascimento AG, Wang X, et al. Frequency and characterization of HMGA2 and HMGA1 rearrangements in mesenchymal tumors of the lower genital tract. Genes Chromosomes Cancer 2007; 46: 981-990
26. Peluso S, Chiappetta G. High-mobility group A (HMGA) proteins and breast cancer. Breast Care (Basel) 2010; 5: 81-85
27. Pegoraro S, Ros G, Piazza S, Sommaggio R, Ciani Y, Rosato A, et al. HMGA1 promotes metastatic processes in basal-like breast cancer regulating EMT and stemness. Oncotarget 2013; 4: 1293-1308
28. Reeves R. Nuclear functions of the HMG proteins. Biochim Biophys Acta 2010; 1799: 3-14
29. Sgarra R, Zammitti S, Lo Sardo A, Maurizio E, Arnoldo L, Pegoraro S, et al. HMGA molecular network: From transcriptional regulation to chromatin remodeling. Biochim Biophys Acta 2010; 1799: 37-47
30. Chen JQ, Russo J. ERalpha-negative and triple negative breast cancer: molecular features and potential therapeutic approaches. Biochim Biophys Acta 2009; 1796: 162-175
31. Kuliopulos A, Covic L, Seeley SK, Sheridan PJ, Helin J, Costello CE. Plasmin desensitization of the PAR1 thrombin receptor: kinetics, sites of truncation, and implications for thrombolytic therapy. Biochemistry 1999; 38: 4572-4585
32. Nelson WJ, Traub P. Proteolysis of vimentin and desmin by the Ca2+-activated proteinase specific for these intermediate filament proteins. Mol Cell Biol 1983; 3: 1146-1156
33. Lahat G, Zhu QS, Huang KL, Wang S, Bolshakov S, Liu J, et al. Vimentin is a novel anti-cancer therapeutic target; insights from in vitro and in vivo mice xenograft studies. PLoS One 2010; 5: e10105
34. Sun JM, Spencer VA, Li L, Yu Chen H, Yu J, Davie JR. Estrogen regulation of trefoil factor 1 expression by estrogen receptor alpha and Sp proteins. Exp Cell Res 2005; 302: 96-107
35. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, et al. The epithelialmesenchymal transition generates cells with properties of stem cells. Cell 2008; 133: 704-715
36. Cleynen I, Brants JR, Peeters K, Deckers R, Debiec-Rychter M, Sciot R, et al. HMGA2 regulates transcription of the Imp2 gene via an intronic regulatory element in cooperation with nuclear factor-kappaB. Mol Cancer Res 2007; 5: 363-372
37. Tallini G, Dal Cin P. HMGI(Y) and HMGI-C dysregulation: a common occurrence in human tumors. Adv Anat Pathol 1999; 6: 237-246
38. Salah Z, Maoz M, Cohen I, Pizov G, Pode D, Runge MS, et al. Identification of a novel functional androgen response element within hPar1 promoter: implications to prostate cancer progression. FASEB J 2005; 19: 62-72
39. Salah Z, Uziely B, Jaber M, Maoz M, Cohen I, Hamburger T, et al. Regulation of human protease-activated receptor 1 (hPar1) gene expression in breast cancer by estrogen. FASEB J 2012; 26: 2031-2042
40. Ferguson M, Henry PA, Currie RA. Histone deacetylase inhibition is associated with transcriptional repression of the Hmga2 gene. Nucleic Acids Res 2003; 31: 3123-3133
41. Kumar MS, Armenteros-Monterroso E, East P, Chakravorty P, Matthews N, Winslow MM, et al. HMGA2 functions as a competing endogenous RNA to promote lung cancer progression. Nature 2014; 505: 212-217
42. Sheen YS, Liao YH, Lin MH, Chu CY, Ho BY, Hsieh MC, et al. IMP-3 promotes migration and invasion of melanoma cells by modulating the expression of HMGA2 and predicts poor prognosis in melanoma. J Invest Dermatol 2014; 135: 1065-1073
43. Li Y, Zhao Z, Xu C, Zhou Z, Zhu Z, You T. HMGA2 induces transcription factor Slug expression to promote epithelial-to-mesenchymal transition and contributes to colon cancer progression. Cancer Lett 2014; 355: 130-140
44. Xi YN, Xin XY, Ye HM. Effects of HMGA2 on malignant degree, invasion, metastasis, proliferation and cellular morphology of ovarian cancer cells. Asian Pac J Trop Med 2014; 7: 289-292
45. Thuault S, Tan EJ, Peinado H, Cano A, Heldin CH, Moustakas A. HMGA2 and Smads co-regulate SNAIL1 expression during induction of epithelial-to-mesenchymal transition. J Biol Chem 2008; 283: 33437-33446
46. Becker RC, Moliterno DJ, Jennings LK, Pieper KS, Pei J, Niederman A, et al. Safety and tolerability of SCH 530348 in patients undergoing non-urgent percutaneous coronary intervention: a randomised, double-blind, placebo-controlled phase II study. Lancet 2009; 373: 919-928
47. Morrow DA, Braunwald E, Bonaca MP, Ameriso SF, Dalby AJ, Fish MP, et al. Vorapaxar in the secondary prevention of atherothrombotic events. N Engl J Med 2012; 366: 1404-1413
48. Tricoci P, Huang Z, Held C, Moliterno DJ, Armstrong PW, Van De Werf F, et al. Thrombin-receptor antagonist vorapaxar in acute coronary syndromes. N Engl J Med 2012; 366: 20-33
49. Zhang P, Gruber A, Kasuda S, Kimmelstiel C, O'Callaghan K, Cox DH, et al. Suppression of arterial thrombosis without affecting hemostatic parameters with a cell-penetrating PAR1 pepducin. Circulation 2012; 126: 83-91
50. Covic L, Misra M, Badar J, Singh C, Kuliopulos A. Pepducin-based intervention of thrombin receptor signaling and systemic platelet activation. Nat Med 2002; 8: 1161-1165
51. Hatziapostolou M, Polytarchou C, Panutsopulos D, Covic L, Tsichlis PN. Proteinaseactivated receptor-1-triggered activation of tumor progression locus-2 promotes actin cytoskeleton reorganization and cell migration. Cancer Res 2008; 68: 1851-1861
52. Covic L, Gresser AL, Kuliopulos A. Biphasic kinetics of activation and signaling for PAR1 and PAR4 thrombin receptors in platelets. Biochemistry 2000; 39: 5458-5467
53. Kamath L, Meydani A, Foss F, Kuliopulos A. Signaling from protease-activated receptor-1 inhibits migration and invasion of breast cancer cells. Cancer Res 2001; 61: 5933-5940
54. Fillmore CM, Gupta PB, Rudnick JA, Caballero S, Keller PJ, Lander ES, et al. Estrogen expands breast cancer stem-like cells through paracrine FGF/Tbx3 signaling. Proc Natl Acad Sci USA 2010; 107: 21737-21742