RKIP Inhibition in Cervical Cancer Is Associated with Higher Tumor Aggressive Behavior and Resistance to Cisplatin Therapy

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Martinho, Olga ^a,b,c   Pinto, Filipe ^a,b   Granja, Sara ^a,b   Miranda Gonçalves, Vera ^a,b   Moreira, Marise A R ^d   Ribeiro, Luis F J ^e   di Loreto, Celso ^f   Rosner, Marsha R ^g   Longatto Filho, Adhemar ^a,b,c,h   Reis, Rui Manuel ^a,b,c  

^a UNIVERSITY OF MINHO   (Portugal)

^b UNIVERSITY OF MINHO   (Portugal)

^c BARRETOS CANCER HOSPITAL   (Brazil)

^d FEDERAL UNIVERSITY OF GOIÁS   (Brazil)

^e Araujo Jorge Hospital   (Brazil)

^f INSTITUTO ADOLFO LUTZ   (Brazil)

^g UNIVERSITY OF CHICAGO   (United States)

^h Faculty of Veterinary Medicine   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CISPLATIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLETHANOLAMINE BINDING PROTEIN; SHORT HAIRPIN RNA;

ADULT; AGED; ANCHORAGE INDEPENDENT GROWTH; ARTICLE; CANCER GROWTH; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CELL VIABILITY; CERVICAL INTRAEPITHELIAL LESION; CHICK EMBRYO; COLONY FORMATION; CONTROLLED STUDY; DOWN REGULATION; DRUG RESISTANCE; EMBRYO; ENZYME ACTIVATION; FEMALE; G2 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MAJOR CLINICAL STUDY; MOLECULAR DYNAMICS; NONHUMAN; ONCOLOGICAL PARAMETERS; PROTEIN DEPLETION; PROTEIN EXPRESSION; TUMOR AGGRESSIVE BEHAVIOR; TUMOR VASCULARIZATION; UTERINE CERVICITIS; UTERINE CERVIX CARCINOMA; UTERINE CERVIX DISEASE;

ADULT; AGED; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CELL PROLIFERATION; DISEASE PROGRESSION; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE EXPRESSION; HUMANS; MAP KINASE SIGNALING SYSTEM; MIDDLE AGED; NEOVASCULARIZATION, PATHOLOGIC; PHOSPHATIDYLETHANOLAMINE BINDING PROTEIN; TREATMENT OUTCOME; UTERINE CERVICAL NEOPLASMS;

EID: 84875122880     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0059104     Document Type: Article

References (62)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E,et al. (2011) Global cancer statistics. CA Cancer J. Clin 61: 69-90. caac.20107 [pii];10.3322/caac.20107 [doi].
2. Castellsague X, Diaz M, de SS, Munoz N, Herrero R, et al. (2006) Worldwide human papillomavirus etiology of cervical adenocarcinoma and its cofactors: implications for screening and prevention. J Natl Cancer Inst 98: 303-315.
3. Bosch FX, de SS, (2007) The epidemiology of human papillomavirus infection and cervical cancer. Dis Markers 23: 213-227.
4. zur HH, (2002) Papillomaviruses and cancer: from basic studies to clinical application. Nat Rev Cancer 2: 342-350.
5. Davey DD, (2003) Cervical cytology classification and the Bethesda System. Cancer Journal 9: 327-334.
6. Martin AG (2007) Molecular biology of cervical cancer. Clin Transl Oncol 9: 347-354. DOI10.1007/s12094-007-0066-8.
7. Corbit KC, Trakul N, Eves EM, Diaz B, Marshall M, et al. (2003) Activation of Raf-1 signaling by protein kinase C through a mechanism involving Raf kinase inhibitory protein. J Biol Chem 278: 13061-13068. 10.1074/jbc.M210015200 [doi];M210015200 [pii].
8. Yeung K, Seitz T, Li S, Janosch P, McFerran B, et al. (1999) Suppression of Raf-1 kinase activity and MAP kinase signalling by RKIP. Nature 401: 173-177. 10.1038/43686 [doi].
9. Yeung K, Janosch P, McFerran B, Rose DW, Mischak H, et al. (2000) Mechanism of suppression of the Raf/MEK/extracellular signal-regulated kinase pathway by the raf kinase inhibitor protein. Mol Cell Biol 20: 3079-3085.
10. Akaishi J, Onda M, Asaka S, Okamoto J, Miyamoto S, et al. (2006) Growth-suppressive function of phosphatidylethanolamine-binding protein in anaplastic thyroid cancer. Anticancer Res 26: 4437-4442.
11. Zhang L, Fu Z, Binkley C, Giordano T, Burant CF, et al. (2004) Raf kinase inhibitory protein inhibits beta-cell proliferation. Surgery 136: 708-715. 10.1016/j.surg.2003.12.013 [doi];S0039606004000200 [pii].
12. Al-Mulla F, Bitar MS, Taqi Z, Rath O, Kolch W (2010) RAF kinase inhibitory protein (RKIP) modulates cell cycle kinetics and motility. Mol. Biosyst 7: 928-41. 10.1039/c0mb00208a [doi].
13. Bement WM (2005) A role for RKIP in cell motility. Chem Biol 12: 953-954. S1074-5521(05)00268-1 [pii];10.1016/j.chembiol.2005.08.012 [doi].
14. Baritaki S, Chapman A, Yeung K, Spandidos DA, Palladino M, et al. (2009) Inhibition of epithelial to mesenchymal transition in metastatic prostate cancer cells by the novel proteasome inhibitor, NPI-0052: pivotal roles of Snail repression and RKIP induction. Oncogene 28: 3573-3585. onc2009214 [pii];10.1038/onc.2009.214 [doi].
15. Hellmann J, Rommelspacher H, Muhlbauer E, Wernicke C (2010) Raf kinase inhibitor protein enhances neuronal differentiation in human SH-SY5Y cells. Dev Neurosci 32: 33-46. 000236595 [pii];10.1159/000236595 [doi].
16. Keller ET, Fu Z, Brennan M (2004) The role of Raf kinase inhibitor protein (RKIP) in health and disease. Biochem Pharmacol 68: 1049-1053. 10.1016/j.bcp.2004.04.024 [doi];S0006295204003600 [pii].
17. Keller ET, Fu Z, Yeung K, Brennan M, (2004) Raf kinase inhibitor protein: a prostate cancer metastasis suppressor gene. Cancer Lett 207: 131-137.
18. Martinho O, Simões K, Longatto-Filho A, Jacob CE, Zilberstein B, et al. (2013) Absence of RKIP expression is an independent prognostic biomarker in gastric cancer. Oncol Rep 29(2): 690-6. 10.3892/or.2012.2179 [doi].
19. Dangi-Garimella S, Yun J, Eves EM, Newman M, Erkeland SJ, et al. (2009) Raf kinase inhibitory protein suppresses a metastasis signalling cascade involving LIN28 and let-7. EMBO J 28: 347-358. emboj2008294 [pii];10.1038/emboj.2008.294 [doi].
20. Fu Z, Smith PC, Zhang L, Rubin MA, Dunn RL, et al. (2003) Effects of raf kinase inhibitor protein expression on suppression of prostate cancer metastasis. J Natl Cancer Inst 95: 878-889.
21. Hagan S, Al-Mulla F, Mallon E, Oien K, Ferrier R, et al. (2005) Reduction of Raf-1 kinase inhibitor protein expression correlates with breast cancer metastasis. Clin Cancer Res 11: 7392-7397. 11/20/7392 [pii];10.1158/1078-0432.CCR-05-0283 [doi].
22. Al-Mulla F, Hagan S, Behbehani AI, Bitar MS, George SS, et al. (2006) Raf kinase inhibitor protein expression in a survival analysis of colorectal cancer patients. J Clin Oncol. 24: 5672-5679.
23. Minoo P, Zlobec I, Baker K, Tornillo L, Terracciano L, et al. (2007) Loss of Raf-1 kinase inhibitor protein expression is associated with tumor progression and metastasis in colorectal cancer. Am J Clin Pathol. 127: 820-827.
24. Kim HS, Kim GY, Lim SJ, Kim YW (2010) Raf-1 kinase inhibitory protein expression in thyroid carcinomas. Endocr Pathol 21: 253-257. 10.1007/s12022-010-9131-x [doi].
25. Martinho O, Gouveia A, Silva P, Pimenta A, Reis RM, et al. (2009) Loss of RKIP expression is associated with poor survival in GISTs. Virchows Arch 455: 277-284. 10.1007/s00428-009-0821-z [doi].
26. Maresch J, Birner P, Zakharinov M, Toumangelova-Uzeir K, Natchev S, et al. (2010) Additive effect on survival of Raf kinase inhibitor protein and signal transducer and activator of transcription 3 in high-grade glioma. Cancer. 10.1002/cncr.25799 [doi].
27. Kim HS, Kim GY, Lim SJ, Kim YW (2010) Loss of Raf-1 kinase inhibitory protein in pancreatic ductal adenocarcinoma. Pathology 42: 655-660. 10.3109/00313025.2010.522172 [doi].
28. Xu YF, Yi Y, Qiu SJ, Gao Q, Li YW, et al. (2010) PEBP1 downregulation is associated to poor prognosis in HCC related to hepatitis B infection. J Hepatol 53: 872-879. S0168-8278(10)00618-5 [pii];10.1016/j.jhep.2010.05.019 [doi].
29. Zaravinos A, Chatziioannou M, Lambrou GI, Boulalas I, Delakas D, et al. (2010) Implication of RAF and RKIP Genes in Urinary Bladder Cancer. Pathol. Oncol. Res. 17: 181-90. 10.1007/s12253-010-9295-1 [doi].
30. Chatterjee D, Sabo E, Tavares R, Resnick MB (2008) 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 14: 2994-3001. 14/10/2994 [pii];10.1158/1078-0432.CCR-07-4496 [doi].
31. Houben R, Michel B, Vetter-Kauczok CS, Pfohler C, Laetsch B, et al. (2006) Absence of classical MAP kinase pathway signalling in Merkel cell carcinoma. J Invest Dermatol 126: 1135-1142. 5700170 [pii];10.1038/sj.jid.5700170 [doi].
32. Chen Y, Ouyang GL, Yi H, Li MY, Zhang PF, et al. (2008) Identification of RKIP as an invasion suppressor protein in nasopharyngeal carcinoma by proteomic analysis. J Proteome Res 7: 5254-5262.
33. Zlobec I, Baker K, Minoo P, Jass JR, Terracciano L, et al. (2008) Node-negative colorectal cancer at high risk of distant metastasis identified by combined analysis of lymph node status, vascular invasion, and raf-1 kinase inhibitor protein expression. Clin Cancer Res 14: 143-148.
34. Fu Z, Kitagawa Y, Shen R, Shah R, Mehra R, et al. (2006) Metastasis suppressor gene Raf kinase inhibitor protein (RKIP) is a novel prognostic marker in prostate cancer. Prostate 66: 248-256. 10.1002/pros.20319 [doi].
35. Biewenga P, Buist MR, Moerland PD, van Thernaat EVL, van Kampen AHC, et al. (2008) Gene expression in early stage cervical cancer. Gynecologic Oncology 108: 520-526. DOI10.1016/j.ygyno.2007.11.024.
36. Hu CJ, Zhou L, Zhang J, Huang C, Zhang GM, (2011) Immunohistochemical detection of Raf kinase inhibitor protein in normal cervical tissue and cervical cancer tissue. J Int Med Res 39: 229-237.
37. Eves EM, Shapiro P, Naik K, Klein UR, Trakul N, et al. (2006) Raf kinase inhibitory protein regulates aurora B kinase and the spindle checkpoint. Mol Cell 23: 561-574. S1097-2765(06)00496-5 [pii];10.1016/j.molcel.2006.07.015 [doi].
38. Logarinho E, Maffini S, Barisic M, Marques A, Toso A, et al. (2012) CLASPs prevent irreversible multipolarity by ensuring spindle-pole resistance to traction forces during chromosome alignment. Nat Cell Biol 14: 295-303. ncb2423 [pii];10.1038/ncb2423 [doi].
39. Cardeal LB, Boccardo E, Termini L, Rabachini T, Andreoli MA, et al. (2012) HPV16 oncoproteins induce MMPs/RECK-TIMP-2 imbalance in primary keratinocytes: possible implications in cervical carcinogenesis. PLoS One 7: e33585. 10.1371/journal.pone.0033585 [doi];PONE-D-12-01424 [pii].
40. Martinho O, Faloppa CC, Scapulatempo NC, Longatto-Filho A, Baiocchi G, et al. (2012) Loss of RKIP expression during the carcinogenic evolution of endometrial cancer. J. Clin. Pathol. 65: 122-8. jclinpath-2011-200358 [pii];10.1136/jclinpath-2011-200358 [doi].
41. Martinho O, Granja S, Jaraquemada T, Caeiro C, Miranda-Goncalves V, et al. (2012) Downregulation of RKIP Is Associated with Poor Outcome and Malignant Progression in Gliomas. PLoS One 7: e30769. 10.1371/journal.pone.0030769 [doi];PONE-D-11-15118 [pii].
42. Trakul N, Menard RE, Schade GR, Qian Z, Rosner MR (2005) Raf kinase inhibitory protein regulates Raf-1 but not B-Raf kinase activation. J Biol Chem 280: 24931-24940. M413929200 [pii];10.1074/jbc.M413929200 [doi].
43. Moniz S, Martinho O, Pinto F, Sousa B, Loureiro C, et al. (2013) Loss of WNK2 expression by promoter gene methylation occurs in adult gliomas and triggers Rac1-mediated tumour cell invasiveness. Hum Mol Genet. 22: 84-95.
44. Poomtavorn Y, Suwannarurk K, Thaweekul Y, Maireang K, (2011) Risk Factors for High-Grade Cervical Intraepithelial Neoplasia in Patients with Atypical Squamous Cells of Undetermined Significance (ASC-US) Papanicolaou Smears. Asian Pac J Cancer Prev 12: 235-238.
45. Li HZ, Wang Y, Gao Y, Shao J, Zhao XL, et al. (2008) Effects of raf kinase inhibitor protein expression on metastasis and progression of human epithelial ovarian cancer. Mol Cancer Res 6: 917-928. 6/6/917 [pii];10.1158/1541-7786.MCR-08-0093 [doi].
46. Zaravinos A, Kanellou P, Baritaki S, Bonavida B, Spandidos DA (2009) BRAF and RKIP are significantly decreased in cutaneous squamous cell carcinoma. Cell Cycle 8: 1402-1408. 8308 [pii].
47. Lorenz K, Lohse MJ, Quitterer U (2003) Protein kinase C switches the Raf kinase inhibitor from Raf-1 to GRK-2. Nature 426: 574-579. 10.1038/nature02158 [doi];nature02158 [pii].
48. Yeung KC, Rose DW, Dhillon AS, Yaros D, Gustafsson M, et al. (2001) Raf kinase inhibitor protein interacts with NF-kappaB-inducing kinase and TAK1 and inhibits NF-kappaB activation. Mol Cell Biol 21: 7207-7217. 10.1128/MCB.21.21.7207-7217.2001 [doi].
49. Al-Mulla F, Bitar MS, Al-Maghrebi M, Behbehani AI, Al-Ali W, et al. (2011) Raf Kinase Inhibitor Protein RKIP Enhances Signaling by Glycogen Synthase Kinase-3{beta}. Cancer Res. 15: 1334-43. 0008-5472.CAN-10-3102 [pii];10.1158/0008-5472.CAN-10-3102 [doi].
50. Shemon AN, Eves EM, Clark MC, Heil G, Granovsky A, et al. (2009) Raf Kinase Inhibitory Protein protects cells against locostatin-mediated inhibition of migration. PLoS One 4: e6028. 10.1371/journal.pone.0006028 [doi].
51. Lee HC, Tian B, Sedivy JM, Wands JR, Kim M (2006) Loss of Raf kinase inhibitor protein promotes cell proliferation and migration of human hepatoma cells. Gastroenterology 131: 1208-1217. S0016-5085(06)01537-X [pii];10.1053/j.gastro.2006.07.012 [doi].
52. Schuierer MM, Bataille F, Hagan S, Kolch W, Bosserhoff AK (2004) Reduction in Raf kinase inhibitor protein expression is associated with increased Ras-extracellular signal-regulated kinase signaling in melanoma cell lines. Cancer Res 64: 5186-5192. 10.1158/0008-5472.CAN-03-3861 [doi];64/15/5186 [pii].
53. Ruan L, Wang GL, Yi H, Chen Y, Tang CE, et al. (2010) Raf kinase inhibitor protein correlates with sensitivity of nasopharyngeal carcinoma to radiotherapy. J Cell Biochem 110: 975-981. 10.1002/jcb.22611 [doi].
54. Li HZ, Gao Y, Zhao XL, Liu YX, Sun BC, et al. (2009) Effects of raf kinase inhibitor protein expression on metastasis and progression of human breast cancer. Mol Cancer Res 7: 832-840. 1541-7786.MCR-08-0403 [pii];10.1158/1541-7786.MCR-08-0403 [doi].
55. Chatterjee D, Bai Y, Wang Z, Beach S, Mott S, et al. (2004) RKIP sensitizes prostate and breast cancer cells to drug-induced apoptosis. J Biol Chem 279: 17515-17523.
56. Wu K, Bonavida B (2009) The activated NF-kappaB-Snail-RKIP circuitry in cancer regulates both the metastatic cascade and resistance to apoptosis by cytotoxic drugs. Crit Rev Immunol 29: 241-254. 18841dcb1a005a88,0d4f451d6774e29d [pii].
57. Woods Ignatoski KM, Grewal NK, Markwart SM, Vellaichamy A, Chinnaiyan AM, et al. (2008) Loss of Raf kinase inhibitory protein induces radioresistance in prostate cancer. Int J Radiat Oncol Biol Phys 72: 153-160. S0360-3016(08)00835-3 [pii];10.1016/j.ijrobp.2008.04.072 [doi].
58. Chatterjee D, Bai Y, Wang Z, Beach S, Mott S, et al. (2004) RKIP sensitizes prostate and breast cancer cells to drug-induced apoptosis. J Biol Chem 279: 17515-17523. 10.1074/jbc.M313816200 [doi];M313816200 [pii].
59. Al-Mulla F, Bitar MS, Feng J, Park S, Yeung KC (2012) A new model for raf kinase inhibitory protein induced chemotherapeutic resistance. PLoS One 7: e29532. 10.1371/journal.pone.0029532 [doi];PONE-D-11-09100 [pii].
60. Zhu S, Mc Henry KT, Lane WS, Fenteany G, (2005) A chemical inhibitor reveals the role of Raf kinase inhibitor protein in cell migration. Chem Biol 12: 981-991.
61. Jazirehi AR, Vega MI, Chatterjee D, Goodglick L, Bonavida B, (2004) Inhibition of the Raf-MEK1/2-ERK1/2 signaling pathway, Bcl-xL down-regulation, and chemosensitization of non-Hodgkin's lymphoma B cells by Rituximab. Cancer Res 64: 7117-7126.
62. Bonavida B, Baritaki S, Huerta-Yepez S, Vega MI, Chatterjee D, et al. (2008) Novel therapeutic applications of nitric oxide donors in cancer: roles in chemo- and immunosensitization to apoptosis and inhibition of metastases. Nitric Oxide 19: 152-157.