RKIP inhibits local breast cancer invasion by antagonizing the transcriptional activation of MMP13

PLoS ONE

Volumn 10, Issue 8, 2015, Pages

  Datar, Ila ^a   Feng, Jingwei ^a   Qiu, Xiaoliang ^a   Lewandowski, John ^a   Yeung, Miranda ^a   Ren, Gang ^a   Aras, Shweta ^a   Al Mulla, Fahd ^b   Cui, Hongjuan ^c   Trumbly, Robert ^a   Arudra, Sri Krishna Chaitanya ^a   De Las Casas, Luis E ^a   De La Serna, Ivana ^a   Bitar, Milad S ^b   Yeung, Kam C ^a  

^a MEDICAL COLLEGE OF OHIO   (United States)

^b KUWAIT UNIVERSITY   (Kuwait)

^c State Key Laboratory of Silkworm Genome Biology(SWU)   (China)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGENASE 3; INTERSTITIAL COLLAGENASE; MITOGEN ACTIVATED PROTEIN KINASE 1; PHOSPHATIDYLETHANOLAMINE BINDING PROTEIN; STROMELYSIN; STROMELYSIN 2; MAPK1 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; BREAST CANCER CELL LINE; CANCER INHIBITION; CONTROLLED STUDY; DNA MICROARRAY; ENZYME INHIBITION; GAIN OF FUNCTION MUTATION; GENE EXPRESSION; GENE REPRESSION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LOSS OF FUNCTION MUTATION; LUNG METASTASIS; MAJOR CLINICAL STUDY; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN TARGETING; RECURRENCE FREE SURVIVAL; TRANSCRIPTION INITIATION; TUMOR INVASION; ANIMAL; BREAST TUMOR; CELL TRANSFORMATION; DISEASE FREE SURVIVAL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; METASTASIS; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; DISEASE-FREE SURVIVAL; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MATRIX METALLOPROTEINASE 13; MICE; MITOGEN-ACTIVATED PROTEIN KINASE 1; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; PHOSPHATIDYLETHANOLAMINE BINDING PROTEIN; SIGNAL TRANSDUCTION; TRANSCRIPTIONAL ACTIVATION;

EID: 84943303362     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0134494     Document Type: Article

References (41)

1. Yeung KC, Rose DW, Dhillon AS, Yaros D, Gustafsson M, Chatterjee D, et al. Raf kinase inhibitor protein interacts with NF-κB-inducing kinase and TAK1 and inhibits NF-κB activation. Mol Cell Biol. 2001; 21:7207-17. PMID: 11585904
2. Al-Mulla F, Bitar MS, Al-Maghrebi M, Behbehani AI, Al-Ali W, Rath O, et al. Raf kinase inhibitor protein RKIP enhances signaling by glycogen synthase kinase-3beta. Cancer Res. 2011; 71:1334-43. doi: 10.1158/0008-5472.CAN-10-3102 PMID: 21303975
3. Al-Mulla F, Bitar MS, Feng J, Park S, Yeung KC. A new model for raf kinase inhibitory protein induced chemotherapeutic resistance. PLoS One. 2012; 7:e29532. doi: 10.1371/journal.pone.0029532 PMID: 22279539
4. Yousuf S, Duan M, Moen EL, Cross-Knorr S, Brilliant K, Bonavida B, et al. Raf kinase inhibitor protein (RKIP) blocks signal transducer and activator of transcription 3 (STAT3) activation in breast and prostate cancer. PLoS One. 2014; 9:e92478. doi: 10.1371/journal.pone.0092478 PMID: 24658061
5. Lorenz K, Lohse MJ, Quitterer U. Protein kinase C switches the Raf kinase inhibitor from Raf-1 to GRK- 2. Nature. 2003; 426:574-9. PMID: 14654844
6. Al-Mulla F, Hagan S, Behbehani AI, Bitar MS, George SS, Going JJ, et al. Raf kinase inhibitor protein expression in a survival analysis of colorectal cancer patients. J Clin Oncol. 2006; 24:5672-9. PMID: 17179102
7. Chatterjee D, Bai Y, Wang Z, Beach S, Mott S, Roy R, et al. RKIP sensitizes prostate and breast cancer cells to drug-induced apoptosis. J Biol Chem. 2004; 279:17515-23. PMID: 14766752
8. Fu Z, Smith PC, Zhang L, Rubin MA, Dunn RL, Yao Z, et al. Effects of raf kinase inhibitor protein expression on suppression of prostate cancer metastasis. J Natl Cancer Inst. 2003; 95:878-89. PMID: 12813171
9. Hegan S, Al-Mulla F, Mallon E, Oien KA, Ferrier R, Gusterson B, et al. Reducton of Raf-1 kinase inhibitor protein (RKIP) expression in breast cancer metastases. Clinical cancer research. 2005.
10. Lee HC, Tian B, Sedivy JM, Wands JR, Kim M. Loss of Raf kinase inhibitor protein promotes cell proliferation and migration of human hepatoma cells. Gastroenterology. 2006; 131:1208-17. PMID: 17030190
11. Schuierer MM, Bataille F, Hagan S, Kolch W, Bosserhoff AK. Reduction in Raf kinase inhibitor protein expression is associated with increased Ras-extracellular signal- regulated kinase signaling in melanoma cell lines. Cancer Res. 2004; 64:5186-92. PMID: 15289323
12. Schuierer MM, Bataille F, Weiss TS, Hellerbrand C, Bosserhoff AK. Raf kinase inhibitor protein is downregulated in hepatocellular carcinoma. Oncol Rep. 2006; 16:451-6. PMID: 16865242
13. Zhang L, Fu Z, Binkley C, Giordano T, Burant CF, Logsdon CD, et al. Raf kinase inhibitory protein inhibits beta-cell proliferation. Surgery. 2004; 136:708-15. PMID: 15349122
14. Li HZ, Gao Y, Zhao XL, Liu YX, Sun BC, Yang J, et al. Effects of raf kinase inhibitor protein expression on metastasis and progression of human breast cancer. Mol Cancer Res. 2009; 7:832-40. doi: 10.1158/1541-7786.MCR-08-0403 PMID: 19531568
15. Beshir AB, Ren G, Magpusao AN, Barone LM, Yeung KC, Fenteany G. Raf kinase inhibitor protein suppresses nuclear factor-kB-dependent cancer cell invasion through negative regulation of matrix metalloproteinase expression. Cancer Lett. 2010; 299:137-49. doi: 10.1016/j.canlet.2010.08.012 PMID: 20855151
16. Dangi-Garimella S, Yun J, Eves EM, Newman M, Erkeland SJ, Hammond SM, et al. Raf kinase inhibitory protein suppresses a metastasis signalling cascade involving LIN28 and let-7. EMBO J. 2009; 28:347-58. doi: 10.1038/emboj.2008.294 PMID: 19153603
17. Al-Mulla F, Bitar MS, Thiery JP, Zea TT, Chatterjee D, Bennett L, et al. Clinical implications for loss or diminution of expression of Raf-1 kinase inhibitory protein and its phosphorylated form in ductal breast cancer. Am J Cancer Res. 2013; 3:446-64. PMID: 24224123
18. Fu Z, Kitagawa Y, Shen R, Shah R, Mehra R, Rhodes D, et al. Metastasis suppressor gene Raf kinase inhibitor protein (RKIP) is a novel prognostic marker in prostate cancer. The Prostate. 2005; 66:248-56.
19. Yun J, Frankenberger CA, Kuo WL, Boelens MC, Eves EM, Cheng N, et al. Signalling pathway for RKIP and Let-7 regulates and predicts metastatic breast cancer. EMBO J. 2011; 30:4500-14. doi: 10.1038/emboj.2011.312 PMID: 21873975
20. Valastyan S, Weinberg RA. Tumor metastasis: molecular insights and evolving paradigms. Cell. 2011; 147:275-92. doi: 10.1016/j.cell.2011.09.024 PMID: 22000009
21. Egeblad M, Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer. 2002; 2:161-74. PMID: 11990853
22. Brinckerhoff CE, Matrisian LM. Matrix metalloproteinases: a tail of a frog that became a prince. Nat Rev Mol Cell Biol. 2002; 3:207-14. PMID: 11994741
23. Coussens LM, Fingleton B, Matrisian LM. Matrix metalloproteinase inhibitors and cancer: trials and tribulations. Science. 2002; 295:2387-92. PMID: 11923519
24. Deryugina EI, Quigley JP. Matrix metalloproteinases and tumor metastasis. Cancer Metastasis Rev. 2006; 25:9-34. PMID: 16680569
25. Kang Y. Analysis of cancer stem cell metastasis in xenograft animal models. Methods Mol Biol. 2009; 568:7-19. doi: 10.1007/978-1-59745-280-9-2 PMID: 19582418
26. Aslakson CJ, Miller FR. Selective events in the metastatic process defined by analysis of the sequential dissemination of subpopulations of a mouse mammary tumor. Cancer Res. 1992; 52:1399-405. PMID: 1540948
27. Zhang B, Cao X, Liu Y, Cao W, Zhang F, Zhang S, et al. Tumor-derived matrix metalloproteinase-13 (MMP-13) correlates with poor prognoses of invasive breast cancer. BMC Cancer. 2008; 8:83. doi: 10.1186/1471-2407-8-83 PMID: 18373849
28. Desmedt C, Piette F, Loi S, Wang Y, Lallemand F, Haibe-Kains B, et al. Strong time dependence of the 76-gene prognostic signature for node-negative breast cancer patients in the TRANSBIG multicenter independent validation series. Clin Cancer Res. 2007; 13:3207-14. PMID: 17545524
29. Wang Y, Klijn JG, Zhang Y, Sieuwerts AM, Look MP, Yang F, et al. Gene- expression profiles to predict distant metastasis of lymph-node-negative primary breast cancer. Lancet. 2005; 365:671-9. PMID: 15721472
30. Al-Mulla F, Marafie M, Zea Tan T, Paul Thiery J. Raf kinase inhibitory protein role in the molecular subtyping of breast cancer. J Cell Biochem. 2014; 115:488-97. doi: 10.1002/jcb.24682 PMID: 24123286
31. Yeung K, Seitz T, Li S, Janosch P, McFerran B, Kaiser C, et al. Suppression of Raf- 1 kinase activity and MAP kinase signalling by RKIP. Nature. 1999; 401:173-7. PMID: 10490027
32. Bond M, Chase AJ, Baker AH, Newby AC. Inhibition of transcription factor NF-κB reduces matrix metalloproteinase- 1, -3 and -9 production by vascular smooth muscle cells. Cardiovascular research. 2001; 50:556-65. PMID: 11376631
33. Kim D, Kim S, Koh H, Yoon SO, Chung AS, Cho KS, et al. Akt/PKB promotes cancer cell invasion via increased motility and metalloproteinase production. FASEB J. 2001; 15:1953-62. PMID: 11532975
34. Xie TX, Wei D, Liu M, Gao AC, Ali-Osman F, Sawaya R, et al. Stat3 activation regulates the expression of matrix metalloproteinase-2 and tumor invasion and metastasis. Oncogene. 2004; 23:3550-60. PMID: 15116091
35. Cui C, Shi Q, Zhang X, Liu X, Bai Y, Li J, et al. CRP promotes MMP-10 expression via c-Raf/MEK/ERK and JAK1/ERK pathways in cardiomyocytes. Cell Signal. 2012; 24:810-8. doi: 10.1016/j.cellsig.2011.11.019 PMID: 22142512
36. Shin S, Dimitri CA, Yoon SO, Dowdle W, Blenis J. ERK2 but not ERK1 induces epithelial-to-mesenchymal transformation via DEF motif-dependent signaling events. Mol Cell. 2010; 38:114-27. doi: 10.1016/j.molcel.2010.02.020 PMID: 20385094
37. 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. PMID: 15184373
38. Nguyen DX, Massague J. Genetic determinants of cancer metastasis. Nat Rev Genet. 2007; 8:341-52. PMID: 17440531
39. Delassus GS, Cho H, Park J,Eliceiri GL. New pathway links from cancer- progression determinants to gene expression of matrix metalloproteinases in breast cancer cells. J Cell Physiol. 2008; 217:739-44. doi: 10.1002/jcp.21548 PMID: 18651563
40. Chatterjee D, Sabo E, Tavares R, Resnick MB. Inverse association between Raf Kinase Inhibitory Protein and signal transducers and activators of transcription 3 expression in gastric adenocarcinoma patients: implications for clinical outcome. Clin Cancer Res. 2008; 14:2994-3001. doi: 10.1158/1078-0432.CCR-07-4496 PMID: 18483365
41. Mengshol JA, Vincenti MP, Brinckerhoff CE. IL-1 induces collagenase-3 (MMP-13) promoter activity in stably transfected chondrocytic cells: requirement for Runx-2 and activation by p38 MAPK and JNK pathways. Nucleic Acids Res. 2001; 29:4361-72. PMID: 11691923