Raf Kinase inhibitory protein (RKIP) as a metastasis suppressor: Regulation of signaling networks in cancer

Critical Reviews in Oncogenesis

Volumn 19, Issue 6, 2014, Pages 447-454

  Yesilkanal, Ali E ^a   Rosner, Marsha Rich ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

BACH 1; Gene signature; HMGA 2; Metastasis; Raf 1; RKIP; Suppressor; Triple negative breast cancer

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLETHANOLAMINE BINDING PROTEIN; RAF PROTEIN; PEBP1 PROTEIN, HUMAN;

ARTICLE; CELL CYCLE PROGRESSION; CELL PROLIFERATION; DNA SYNTHESIS; HUMAN; M PHASE CELL CYCLE CHECKPOINT; METASTASIS; NONHUMAN; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; NEOPLASM; PATHOLOGY; PHYSIOLOGY; TRIPLE NEGATIVE BREAST CANCER; TUMOR SUPPRESSOR GENE;

GENE EXPRESSION REGULATION, NEOPLASTIC; GENE REGULATORY NETWORKS; GENES, TUMOR SUPPRESSOR; HUMANS; MAP KINASE SIGNALING SYSTEM; NEOPLASM METASTASIS; NEOPLASMS; PHOSPHATIDYLETHANOLAMINE BINDING PROTEIN; SIGNAL TRANSDUCTION; TRIPLE NEGATIVE BREAST NEOPLASMS;

EID: 84912051747     PISSN: 08939675     EISSN: 21626448     Source Type: Journal    
DOI: 10.1615/CritRevOncog.2014012000     Document Type: Article

References (53)

1. Chaffer CL, Weinberg RA. A perspective on cancer cell metastasis. Science. 2011; 331: 1559-64.
2. Comen E, Norton L, Massague J. Clinical implications of cancer self-seeding. Nat Rev Clin Oncol. 2011; 8: 369-77.
3. Brabletz T, Lyden D, Steeg PS, Werb Z. Roadblocks to translational advances on metastasis research. Nat Med. 2013; 19: 1104-9.
4. Liu W, Vivian CJ, Brinker AE, Hampton KR, Lianidou E, Welch DR. Microenvironmental Influences on Metastasis Suppressor Expression and Function during a Metastatic Cell's Journey. Cancer Microenviron. 2014; Epub ahead of print.
5. Vanharanta S, Massague J. Origins of metastatic traits. Cancer Cell. 2013; 24: 410-21.
6. Fu Z, Smith PC, Zhang L, Rubin MA, Dunn RL, Yao Z, Keller ET. Effects of raf kinase inhibitor protein expression on suppression of prostate cancer metastasis. J Natl Cancer Inst. 2003; 95: 878-89.
7. Dangi-Garimella S, Yun J, Eves EM, Newman M, Erkeland SJ, Hammond SM, Minn AJ, Rosner MR. Raf kinase inhibitory protein suppresses a metastasis signalling cascade involving LIN28 and let-7. EMBO J. 2009; 28: 347-58.
8. Martinho O, Pinto F, Granja S, Miranda-Goncalves V, Moreira MA, Ribeiro LF, di Loreto C, Rosner MR, Longatto-Filho A, Reis RM. RKIP inhibition in cervical cancer is associated with higher tumor aggressive behavior and resistance to cisplatin therapy. PLoS One. 2013; 8: e59104.
9. Martinho O, Granja S, Jaraquemada T, Caeiro C, Miranda-Goncalves V, Honavar M, Costa P, Damasceno M, Rosner MR, Lopes JM, Reis RM. Downregulation of RKIP is associated with poor outcome and malignant progression in gliomas. PLoS One. 2012; 7: e30769.
10. Al-Mulla F, Bitar MS, Thiery JP, Zea TT, Chatterjee D, Bennett L, Park S, Edwards J, Yeung KC. 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.
11. Doyle B, Hagan S, Al-Mulla F, Scott L, Harden S, Paul J, Mulcahy H, Murray GI, Sheahan K, O'Sullivan J, Kolch W. Raf kinase inhibitor protein expression combined with peritoneal involvement and lymphovascular invasion predicts prognosis in Dukes' B colorectal cancer patients. Histopathology. 2013; 62: 505-10.
12. Yeung K, Seitz T, Li S, Janosch P, McFerran B, Kaiser C, Fee F, Katsanakis KD, Rose DW, Mischak H, Sedivy JM, Kolch W. Suppression of Raf-1 kinase activity and MAP kinase signalling by RKIP. Nature. 1999; 401: 173-7.
13. Yeung K, Janosch P, McFerran B, Rose DW, Mischak H, Sedivy JM, Kolch W. Mechanism of suppression of the Raf/MEK/extracellular signal-regulated kinase pathway by the raf kinase inhibitor protein. Mol Cell Biol. 2000; 20: 3079-85.
14. Trakul N, Menard RE, Schade GR, Qian Z, Rosner MR. Raf kinase inhibitory protein regulates Raf-1 but not B-Raf kinase activation. J Biol Chem. 2005; 280: 24931-40.
15. Mason CS, Springer CJ, Cooper RG, Superti-Furga G, Marshall CJ, Marais R. Serine and tyrosine phosphorylations cooperate in Raf-1, but not B-Raf activation. Embo J. 1999; 18: 2137-48.
16. Rushworth LK, Hindley AD, O'Neill E, Kolch W. Regulation and role of Raf-1/B-Raf heterodimerization. Mol Cell Biol. 2006; 26: 2262-72.
17. Zeng L, Ehrenreiter K, Menon J, Menard R, Kern F, Nakazawa Y, Bevilacqua E, Imamoto A, Baccarini M, Rosner MR. RKIP regulates MAP kinase signaling in cells with defective B-Raf activity. Cell Signal. 2013; 25: 1156-65.
18. Weber CK, Slupsky JR, Kalmes HA, Rapp UR. Active Ras induces heterodimerization of cRaf and BRaf. Cancer Res. 2001; 61: 3595-8.
19. Park S, Yeung ML, Beach S, Shields JM, Yeung KC. RKIP downregulates B-Raf kinase activity in melanoma cancer cells. Oncogene. 2005; 24: 3535-40.
20. Parker PJ, Murray-Rust J. PKC at a glance. J Cell Sci. 2004; 117: 131-2.
21. Corbit KC, Trakul N, Eves EM, Diaz B, Marshall M, Rosner MR. Activation of Raf-1 signaling by protein kinase C through a Mechanism Involving Raf kinase inhibitory protein. J Biol Chem. 2003; 278: 13061-8.
22. 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.
23. Granovsky AE, Clark MC, McElheny D, Heil G, Hong J, Liu X, Kim Y, Joachimiak G, Joachimiak A, Koide S, Rosner MR. Raf kinase inhibitory protein function is regulated via a flexible pocket and novel phosphorylation-dependent mechanism. Mol Cell Biol. 2009; 29: 1306-20.
24. Ziogas A, Lorenz IC, Moelling K, Radziwill G. Mitotic Raf-1 is stimulated independently of Ras and is active in the cytoplasm. J Biol Chem. 1998; 273: 24108-14.
25. Hayne C, Tzivion G, Luo Z. Raf-1/MEK/MAPK pathway is necessary for the G2/M transition induced by nocodazole. J Biol Chem. 2000; 275: 31876-82.
26. Shapiro PS, Vaisberg E, Hunt AJ, Tolwinski NS, Whalen AM, McIntosh JR, Ahn NG. Activation of the MKK/ERK pathway during somatic cell mitosis: direct interactions of active ERK with kinetochores and regulation of the mitotic 3F3/2 phosphoantigen. J Cell Biol. 1998; 142: 1533-45.
27. Zecevic M, Catling AD, Eblen ST, Renzi L, Hittle JC, Yen TJ, Gorbsky GJ, Weber MJ. Active MAP kinase in mitosis: localization at kinetochores and association with the motor protein CENP-E. J Cell Biol. 1998; 142: 1547-58.
28. Eves EM, Shapiro P, Naik K, Klein UR, Trakul N, Rosner MR. Raf kinase inhibitory protein regulates aurora B kinase and the spindle checkpoint. Mol Cell. 2006; 23: 561-74.
29. Chatterjee D, Bai Y, Wang Z, Beach S, Mott S, Roy R, Braastad C, Sun Y, Mukhopadhyay A, Aggarwal BB, Darnowski J, Pantazis P, Wyche J, Fu Z, Kitagwa Y, Keller ET, Sedivy JM, Yeung KC. RKIP sensitizes prostate and breast cancer cells to drug-induced apoptosis. J Biol Chem. 2004; 279: 17515-23.
30. Johnson SM, Grosshans H, Shingara J, Byrom M, Jarvis R, Cheng A, Labourier E, Reinert KL, Brown D, Slack FJ. RAS is regulated by the let-7 microRNA family. Cell. 2005; 120: 635-47.
31. Johnson CD, Esquela-Kerscher A, Stefani G, Byrom M, Kelnar K, Ovcharenko D, Wilson M, Wang X, Shelton J, Shingara J, Chin L, Brown D, Slack FJ. The let-7 microRNA represses cell proliferation pathways in human cells. Cancer Res. 2007; 67: 7713-22.
32. Peter ME. Let-7 and miR-200 microRNAs: guardians against pluripotency and cancer progression. Cell Cycle. 2009; 8: 843-52.
33. Fedele M, Visone R, De Martino I, Troncone G, Palmieri D, Battista S, Ciarmiello A, Pallante P, Arra C, Melillo RM, Helin K, Croce CM, Fusco A. HMGA2 induces pituitary tumorigenesis by enhancing E2F1 activity. Cancer Cell. 2006; 9: 459-71.
34. Zaidi MR, Okada Y, Chada KK. Misexpression of full-length HMGA2 induces benign mesenchymal tumors in mice. Cancer Res. 2006; 66: 7453-9.
35. Mayr C, Hemann MT, Bartel DP. Disrupting the pairing between let-7 and Hmga2 enhances oncogenic transformation. Science. 2007; 315: 1576-9.
36. Thuault S, Valcourt U, Petersen M, Manfioletti G, Heldin CH, Moustakas A. Transforming growth factor-beta employs HMGA2 to elicit epithelial-mesenchymal transition. J Cell Biol. 2006; 174: 175-83.
37. Tavazoie SF, Alarcon C, Oskarsson T, Padua D, Wang Q, Bos PD, Gerald WL, Massague J. Endogenous human microRNAs that suppress breast cancer metastasis. Nature. 2008; 451: 147-52.
38. Ma L, Teruya-Feldstein J, Weinberg RA. Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature. 2007; 449: 682-8.
39. Yun J, Frankenberger CA, Kuo WL, Boelens MC, Eves EM, Cheng N, Liang H, Li WH, Ishwaran H, Minn AJ, Rosner MR. Signalling pathway for RKIP and Let-7 regulates and predicts metastatic breast cancer. EMBO J. 2011; 30: 4500-14.
40. Minn AJ, Bevilacqua E, Yun J, Rosner MR. Identification of novel metastasis suppressor signaling pathways for breast cancer. Cell Cycle. 2012; 11: 2452-7.
41. Kang Y, Siegel PM, Shu W, Drobnjak M, Kakonen SM, Cordon-Cardo C, Guise TA, Massague J. A multigenic program mediating breast cancer metastasis to bone. Cancer Cell. 2003; 3: 537-49.
42. Sun M, Gomes S, Chen P, Frankenberger CA, Sankarasharma D, Chung CH, Chada KK, Rosner MR. RKIP and HMGA2 regulate breast tumor survival and metastasis through lysyl oxidase and syndecan-2. Oncogene. 2013; 33: 3528-37.
43. Erler JT, Bennewith KL, Nicolau M, Dornhofer N, Kong C, Le QT, Chi JT, Jeffrey SS, Giaccia AJ. Lysyl oxidase is essential for hypoxia-induced metastasis. Nature. 2006; 440: 1222-6.
44. Park H, Kim Y, Lim Y, Han I, Oh ES. Syndecan-2 mediates adhesion and proliferation of colon carcinoma cells. J Biol Chem. 2002; 277: 29730-6.
45. Sun M, Song CX, Huang H, Frankenberger CA, Sankarasharma D, Gomes S, Chen P, Chen J, Chada KK, He C, Rosner MR. HMGA2/TET1/HOXA9 signaling pathway regulates breast cancer growth and metastasis. Proc Natl Acad Sci U S A. 2013; 110: 9920-5.
46. Paik S, Shak S, Tang G, Kim C, Baker J, Cronin M, Baehner FL, Walker MG, Watson D, Park T, Hiller W, Fisher ER, Wickerham DL, Bryant J, Wolmark N. A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer. N Engl J Med. 2004; 351: 2817-26.
47. van 't Veer LJ, Dai H, van de Vijver MJ, He YD, Hart AA, Mao M, Peterse HL, van der Kooy K, Marton MJ, Witteveen AT, Schreiber GJ, Kerkhoven RM, Roberts C, Linsley PS, Bernards R, Friend SH. Gene expression profiling predicts clinical outcome of breast cancer. Nature. 2002; 415: 530-6.
48. Lee U, Frankenberger C, Yun J, Bevilacqua E, Caldas C, Chin SF, Rueda OM, Reinitz J, Rosner MR. A prognostic gene signature for metastasis-free survival of triple negative breast cancer patients. PLoS One. 2013; 8: e82125.
49. Lee J, Lee J, Farquhar KS, Yun J, Frankenberger CA, Bevilacqua E, Yeung K, Kim EJ, Balazsi G, Rosner MR. Network of mutually repressive metastasis regulators can promote cell heterogeneity and metastatic transitions. Proc Natl Acad Sci U S A. 2014; 111: E364-73.
50. Al-Mulla F, Bitar MS, Taqi Z, Yeung KC. RKIP: much more than Raf kinase inhibitory protein. J Cell Physiol. 2013; 228: 1688-702.
51. Al-Mulla F, Bitar MS, Al-Maghrebi M, Behbehani AI, Al-Ali W, Rath O, Doyle B, Tan KY, Pitt A, Kolch W. Raf kinase inhibitor protein RKIP enhances signaling by glycogen synthase kinase-3beta. Cancer Res. 2011; 71: 1334-43.
52. Akinleye A, Furqan M, Mukhi N, Ravella P, Liu D. MEK and the inhibitors: from bench to bedside. J Hematol Oncol. 2013; 6: 27.
53. Duncan JS, Whittle MC, Nakamura K, Abell AN, Midland AA, Zawistowski JS, Johnson NL, Granger DA, Jordan NV, Darr DB, Usary J, Kuan PF, Smalley DM, Major B, He X, Hoadley KA, Zhou B, Sharpless NE, Perou CM, Kim WY, Gomez SM, Chen X, Jin J, Frye SV, Earp HS, Graves LM, Johnson GL. Dynamic reprogramming of the kinome in response to targeted MEK inhibition in triple-negative breast cancer. Cell. 2012; 149: 307-21.