RKIP: Much more than Raf Kinase inhibitory protein

Journal of Cellular Physiology

Volumn 228, Issue 8, 2013, Pages 1688-1702

  Al Mulla, Fahd ^a   Bitar, Milad S ^a   Taqi, Zainab ^a   Yeung, Kam C ^b  

^a KUWAIT UNIVERSITY   (Kuwait)

^b MEDICAL COLLEGE OF OHIO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATIDYLETHANOLAMINE BINDING PROTEIN;

APOPTOSIS; CELL CYCLE REGULATION; CELL GROWTH; CELL INVASION; CELL MOTILITY; CELLULAR DISTRIBUTION; GENOMICS; GROWTH; GROWTH REGULATION; HUMAN; INTRACELLULAR SIGNALING; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; REVIEW;

ANIMALS; APOPTOSIS; BASE SEQUENCE; CATTLE; CELL MOVEMENT; CELL PROLIFERATION; DRUG RESISTANCE; GENOME, HUMAN; HUMANS; MAP KINASE SIGNALING SYSTEM; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHOSPHATIDYLETHANOLAMINE BINDING PROTEIN; RAF KINASES;

BOVINAE;

EID: 84876743828     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.24335     Document Type: Review

References (192)

1. Adams RR, Carmena M, Earnshaw WC. 2001. Chromosomal passengers and the (aurora) ABCs of mitosis. Trends Cell Biol 11:49-54.
2. Allen DB, Maguire JJ, Mahdavian M, Wicke C, Marcocci L, Scheuenstuhl H, Chang M, Le AX, Hopf HW, Hunt TK. 1997. Wound hypoxia and acidosis limit neutrophil bacterial killing mechanisms. Arch Surg 132:991-996.
3. Al-Mulla F. 2012a. Novel flavonoid didymin inhibits neuroblastomas-Letter. Cancer Prev Res (Phila) 5:883.
4. Al-Mulla F. 2012b. RKIP and cellular motility. J Cell Physiol 227:2969-2970.
5. Al-Mulla F, Keith WN, Pickford IR, Going JJ, Birnie GD. 1999. Comparative genomic hybridization analysis of primary colorectal carcinomas and their synchronous metastases. Genes Chromosomes Cancer 24:306-314.
6. Al-Mulla F, AlFadhli S, Al-Hakim AH, Going JJ, Bitar MS. 2006a. Metastatic recurrence of early-stage colorectal cancer is linked to loss of heterozygosity on chromosomes 4 and 14q. J Clin Pathol 59:624-630.
7. Al-Mulla F, Behbehani AI, Bitar MS, Varadharaj G, Going JJ. 2006b. Genetic profiling of stage I and II colorectal cancer may predict metastatic relapse. Mod Pathol 19:648-658.
8. Al-Mulla F, Hagan S, Behbehani AI, Bitar MS, George SS, Going JJ, Garcia JJ, Scott L, Fyfe N, Murray GI, Kolch W. 2006c. Raf kinase inhibitor protein expression in a survival analysis of colorectal cancer patients. J Clin Oncol 24:5672-5679.
9. Al-Mulla F, Hagan S, Al-Ali W, Jacob SP, Behbehani AI, Bitar MS, Dallol A, Kolch W. 2008. Raf kinase inhibitor protein: Mechanism of loss of expression and association with genomic instability. J Clin Pathol 61:524-529.
10. Al-Mulla F, Bitar MS, Al-Maghrebi M, Behbehani AI, Al-Ali W, Rath O, Doyle B, Tan KY, Pitt A, Kolch W. 2011a. Raf kinase inhibitor protein RKIP enhances signaling by glycogen synthase kinase-3beta. Cancer Res 71:1334-1343.
11. Al-Mulla F, Bitar MS, Taqi Z, Rath O, Kolch W. 2011b. RAF kinase inhibitory protein (RKIP) modulates cell cycle kinetics and motility. Mol Biosyst 7:928-941.
12. 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.
13. Antoun G, Bouchard-Cannon P, Cheng HY. 2012. Regulation of MAPK/ERK signaling and photic entrainment of the suprachiasmatic nucleus circadian clock by Raf kinase inhibitor protein. J Neurosci 32:4867-4877.
14. Banfield MJ, Brady RL. 2000. The structure of Antirrhinum centroradialis protein (CEN) suggests a role as a kinase regulator. J Mol Biol 297:1159-1170.
15. Banfield MJ, Barker JJ, Perry AC, Brady RL. 1998. Function from structure? The crystal structure of human phosphatidylethanolamine-binding protein suggests a role in membrane signal transduction. Structure 6:1245-1254.
16. Baritaki S, Katsman A, Chatterjee D, Yeung KC, Spandidos DA, Bonavida B. 2007. Regulation of tumor cell sensitivity to TRAIL-induced apoptosis by the metastatic suppressor Raf kinase inhibitor protein via Yin Yang 1 inhibition and death receptor 5 up-regulation. J Immunol 179:5441-5453.
17. Baritaki S, Chapman A, Yeung K, Spandidos DA, Palladino M, Bonavida B. 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.
18. Baritaki S, Huerta-Yepez S, Sahakyan A, Karagiannides I, Bakirtzi K, Jazirehi A, Bonavida B. 2010. Mechanisms of nitric oxide-mediated inhibition of EMT in cancer: Inhibition of the metastasis-inducer Snail and induction of the metastasis-suppressor RKIP. Cell Cycle 9:4931-4940.
19. Baylin SB, Herman JG. 2000. DNA hypermethylation in tumorigenesis: Epigenetics joins genetics. Trends Genet 16:168-174.
20. Beach S, Tang H, Park S, Dhillon AS, Keller ET, Kolch W, Yeung KC. 2008. Snail is a repressor of RKIP transcription in metastatic prostate cancer cells. Oncogene 27:2243-2248.
21. Bernier I, Jolles P. 1984. Purification and characterization of a basic 23kDa cytosolic protein from bovine brain. Biochim Biophys Acta 790:174-181.
22. Beshir AB, Ren G, Magpusao AN, Barone LM, Yeung KC, Fenteany G. 2010. Raf kinase inhibitor protein suppresses nuclear factor-kappaB-dependent cancer cell invasion through negative regulation of matrix metalloproteinase expression. Cancer Lett 299:137-149.
23. Birner P, Jesch B, Schultheis A, Schoppmann SF. 2012. RAF-kinase inhibitor protein (RKIP) downregulation in esophageal cancer and its metastases. Clin Exp Metastasis 29:551-559.
24. Bitar MS, Al-Mulla F. 2012. ROS constitute a convergence nexus in the development of IGF1 resistance and impaired wound healing in a rat model of type 2 diabetes. Dis Model Mech 5:375-388.
25. Bitar MS, Al-Saleh E, Al-Mulla F. 2005. Oxidative stress-mediated alterations in glucose dynamics in a genetic animal model of type II diabetes. Life Sci 77:2552-2573.
26. Bollengier F, Mahler A. 1988. Localization of the novel neuropolypeptide h3 in subsets of tissues from different species. J Neurochem 50:1210-1214.
27. Bonavida B, Baritaki S. 2011. Dual role of NO donors in the reversal of tumor cell resistance and EMT: Downregulation of the NF-kappaB/Snail/YY1/RKIP circuitry. Nitric Oxide 24:1-7.
28. Bonavida B, Baritaki S, Huerta-Yepez S, Vega MI, Chatterjee D, Yeung K. 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.
29. Bruun AW, Svendsen I, Sorensen SO, Kielland-Brandt MC, Winther JR. 1998. A high-affinity inhibitor of yeast carboxypeptidase Y is encoded by TFS1 and shows homology to a family of lipid binding proteins. Biochemistry 37:3351-3357.
30. Cano A, Perez-Moreno MA, Rodrigo I, Locascio A, Blanco MJ, del Barrio MG, Portillo F, Nieto MA. 2000. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol 2:76-83.
31. 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. 2004. RKIP sensitizes prostate and breast cancer cells to drug-induced apoptosis. J Biol Chem 279:17515-17523.
32. Chen Y, Tang CE, Ouyang GL, Ruan L, Li MY, Zhang PF, Li C, Yi H, Peng F, Li JL, Chen ZC, Xiao ZQ. 2009. Identification of RKIP as a differentially tyrosine-phosphorylated protein in nasopharyngeal carcinoma and normal nasopharyngeal epithelial tissues by phosphoproteomic approach. Med Oncol 26:463-470.
33. Ciarmela P, Marzioni D, Islam MS, Gray PC, Terracciano L, Lorenzi T, Todros T, Petraglia F, Castellucci M. 2012. Possible role of RKIP in cytotrophoblast migration: Immunohistochemical and in vitro studies. J Cell Physiol 227:1821-1828.
34. Corbit KC, Trakul N, Eves EM, Diaz B, Marshall M, Rosner MR. 2003. Activation of Raf-1 signaling by protein kinase C through a mechanism involving Raf kinase inhibitory protein. J Biol Chem 278:13061-13068.
35. Dangi-Garimella S, Yun J, Eves EM, Newman M, Erkeland SJ, Hammond SM, Minn AJ, Rosner MR. 2009. Raf kinase inhibitory protein suppresses a metastasis signalling cascade involving LIN28 and let-7. EMBO J 28:347-358.
36. Das SK, Bhutia SK, Sokhi UK, Azab B, Su ZZ, Boukerche H, Anwar T, Moen EL, Chatterjee D, Pellecchia M, Sarkar D, Fisher PB. 2012. Raf kinase inhibitor RKIP inhibits MDA-9/syntenin-mediated metastasis in melanoma. Cancer Res 72:6217-6226.
37. Deiss K, Kisker C, Lohse MJ, Lorenz K. 2012. Raf kinase inhibitor protein (RKIP) dimer formation controls its target switch from Raf1 to G protein-coupled receptor kinase (GRK) 2. J Biol Chem 287:23407-23417.
38. Dephoure N, Zhou C, Villen J, Beausoleil SA, Bakalarski CE, Elledge SJ, Gygi SP. 2008. A quantitative atlas of mitotic phosphorylation. Proc Natl Acad Sci USA 105:10762-10767.
39. Dyson HJ, Komives EA. 2012. Role of disorder in IkappaB-NFkappaB interaction. IUBMB Life 64:499-505.
40. Eickholt BJ, Walsh FS, Doherty P. 2002. An inactive pool of GSK-3 at the leading edge of growth cones is implicated in Semaphorin 3A signaling. J Cell Biol 157:211-217.
41. Emanuele MJ, Elia AE, Xu Q, Thoma CR, Izhar L, Leng Y, Guo A, Chen YN, Rush J, Hsu PW, Yen HC, Elledge SJ. 2011. Global identification of modular cullin-RING ligase substrates. Cell 147:459-474.
42. Etienne-Manneville S, Hall A. 2003. Cdc42 regulates GSK-3beta and adenomatous polyposis coli to control cell polarity. Nature 421:753-756.
43. Eves EM, Rosner MR. 2010. MAP kinase regulation of the mitotic spindle checkpoint. Methods Mol Biol 661:497-505.
44. Eves EM, Shapiro P, Naik K, Klein UR, Trakul N, Rosner MR. 2006. Raf kinase inhibitory protein regulates aurora B kinase and the spindle checkpoint. Mol Cell 23:561-574.
45. Farooqui R, Zhu S, Fenteany G. 2006. Glycogen synthase kinase-3 acts upstream of ADP-ribosylation factor 6 and Rac1 to regulate epithelial cell migration. Exp Cell Res 312:1514-1525.
46. Frayne JIC, Love S, Hall L. 1999. Localisation of phosphatidylethanolamine-binding protein in the brain and other tissues of the rat. Cell Tissue Res 298:415-423.
47. Fu Z, Smith PC, Zhang L, Rubin MA, Dunn RL, Yao Z, Keller ET. 2003. Effects of raf kinase inhibitor protein expression on suppression of prostate cancer metastasis. J Natl Cancer Inst 95:878-889.
48. Fu Z, Kitagawa Y, Shen R, Shah R, Mehra R, Rhodes D, Keller PJ, Mizokami A, Dunn R, Chinnaiyan AM, Yao Z, Keller ET. 2006. Metastasis suppressor gene Raf kinase inhibitor protein (RKIP) is a novel prognostic marker in prostate cancer. Prostate 66:248-256.
49. Fujimori Y, Inokuchi M, Takagi Y, Kato K, Kojima K, Sugihara K. 2012. Prognostic value of RKIP and p-ERK in gastric cancer. J Exp Clin Cancer Res 31:30.
50. Gao C, Pang L, Ren C, Ma T. 2012. Prognostic value of raf kinase inhibitor protein in esophageal squamous cell carcinoma. Pathol Oncol Res 18:471-477.
51. Gherardi E, Birchmeier W, Birchmeier C, Vande Woude G. 2012. Targeting MET in cancer: Rationale and progress. Nat Rev Cancer 12:89-103.
52. Gimenez M, Souza VC, Izumi C, Barbieri MR, Chammas R, Oba-Shinjo SM, Uno M, Marie SK, Rosa JC. 2010. Proteomic analysis of low- to high-grade astrocytomas reveals an alteration of the expression level of raf kinase inhibitor protein and nucleophosmin. Proteomics 10:2812-2821.
53. Goumon Y, Angelone T, Schoentgen F, Chasserot-Golaz S, Almas B, Fukami MM, Langley K, Welters ID, Tota B, Aunis D, Metz-Boutigue MH. 2004. The hippocampal cholinergic neurostimulating peptide, the N-terminal fragment of the secreted phosphatidylethanolamine-binding protein, possesses a new biological activity on cardiac physiology. J Biol Chem 279:13054-13064.
54. Granovsky AE, Rosner MR. 2008. Raf kinase inhibitory protein: A signal transduction modulator and metastasis suppressor. Cell Res 18:452-457.
55. Granovsky AE, Clark MC, McElheny D, Heil G, Hong J, Liu X, Kim Y, Joachimiak G, Joachimiak A, Koide S, Rosner MR. 2009. Raf kinase inhibitory protein function is regulated via a flexible pocket and novel phosphorylation-dependent mechanism. Mol Cell Biol 29:1306-1320.
56. Guo W, Dong Z, Guo Y, Lin X, Chen Z, Kuang G, Yang Z. 2012a. Aberrant methylation and loss expression of RKIP is associated with tumor progression and poor prognosis in gastric cardia adenocarcinoma. Clin Exp Metastasis DOI 10.1007/s10585-012-9533-x
57. Guo W, Dong Z, Lin X, Zhang M, Kuang G, Zhu T. 2012b. Decreased expression and aberrant methylation of Raf kinase inhibitory protein gene in esophageal squamous cell carcinoma. Cancer Invest 30:703-711.
58. Hagan S, Al-Mulla F, Mallon E, Oien K, Ferrier R, Gusterson B, Garcia JJ, Kolch W. 2005. Reduction of Raf-1 kinase inhibitor protein expression correlates with breast cancer metastasis. Clin Cancer Res 11:7392-7397.
59. Hagan S, Garcia R, Dhillon A, Kolch W. 2006. Raf kinase inhibitor protein regulation of raf and MAPK signaling. Methods Enzymol 407:248-259.
60. Han NK, Kim BC, Lee HC, Lee YJ, Park MJ, Chi SG, Ko YG, Lee JS. 2012. Secretome analysis of ionizing radiation-induced senescent cancer cells reveals that secreted RKIP plays a critical role in neighboring cell migration. Proteomics 12:2822-2832.
61. Hellmann J, Rommelspacher H, Wernicke C. 2009. Long-term ethanol exposure impairs neuronal differentiation of human neuroblastoma cells involving neurotrophin-mediated intracellular signaling and in particular protein kinase C. Alcohol Clin Exp Res 33:538-550.
62. 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.
63. Herranz N, Pasini D, Diaz VM, Franci C, Gutierrez A, Dave N, Escriva M, Hernandez-Munoz I, Di Croce L, Helin K, Garcia de Herreros A, Peiro S. 2008. Polycomb complex 2 is required for E-cadherin repression by the Snail1 transcription factor. Mol Cell Biol 28:4772-4781.
64. Hochstrasser DF, Frutiger S, Paquet N, Bairoch A, Ravier F, Pasquali C, Sanchez JC, Tissot JD, Bjellqvist B, Vargas R, et al. 1992. Human liver protein map: A reference database established by microsequencing and gel comparison. Electrophoresis 13:992-1001.
65. Houben R, Vetter-Kauczok CS, Ortmann S, Rapp UR, Broecker EB, Becker JC. 2008. Phospho-ERK staining is a poor indicator of the mutational status of BRAF and NRAS in human melanoma. J Invest Dermatol 128:2003-2012.
66. Hsu YL, Chen CY, Lin IP, Tsai EM, Kuo PL, Hou MF. 2012. 4-Shogaol, an active constituent of dietary ginger, inhibits metastasis of MDA-MB-231 human breast adenocarcinoma cells by decreasing the repression of NF-kappaB/Snail on RKIP. J Agric Food Chem 60:852-861.
67. Huang L, Dai T, Lin X, Zhao X, Chen X, Wang C, Li X, Shen H, Wang X. 2012. MicroRNA-224 targets RKIP to control cell invasion and expression of metastasis genes in human breast cancer cells. Biochem Biophys Res Commun 425:127-133.
68. Huerta-Yepez S, Yoon NK, Hernandez-Cueto A, Mah V, Rivera-Pazos CM, Chatterjee D, Vega MI, Maresh EL, Horvath S, Chia D, Bonavida B, Goodglick L. 2011. Expression of phosphorylated raf kinase inhibitor protein (pRKIP) is a predictor of lung cancer survival. BMC Cancer 11:259.
69. Jazirehi AR, Bonavida B. 2005. Cellular and molecular signal transduction pathways modulated by rituximab (rituxan, anti-CD20 mAb) in non-Hodgkin's lymphoma: Implications in chemosensitization and therapeutic intervention. Oncogene 24:2121-2143.
70. 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.
71. Jia B, Liu H, Kong Q, Li B. 2012. RKIP expression associated with gastric cancer cell invasion and metastasis. Tumour Biol 33:919-925.
72. Jiang T, Chen N, Zhao F, Wang XJ, Kong B, Zheng W, Zhang DD. 2010. High levels of Nrf2 determine chemoresistance in type II endometrial cancer. Cancer Res 70:5486-5496.
73. Julien S, Puig I, Caretti E, Bonaventure J, Nelles L, van Roy F, Dargemont C, de Herreros AG, Bellacosa A, Larue L. 2007. Activation of NF-kappaB by Akt upregulates Snail expression and induces epithelium mesenchyme transition. Oncogene 26:7445-7456.
74. Kang Y, Siegel PM, Shu W, Drobnjak M, Kakonen SM, Cordon-Cardo C, Guise TA, Massague J. 2003. A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 3:537-549.
75. Karin M, Cao Y, Greten FR, Li ZW. 2002. NF-kappaB in cancer: From innocent bystander to major culprit. Nat Rev Cancer 2:301-310.
76. Keller ET, Fu Z, Yeung K, Brennan M. 2004. Raf kinase inhibitor protein: A prostate cancer metastasis suppressor gene. Cancer Lett 207:131-137.
77. Kim SO, Kim MR. 2013. (-)-Epigallocatechin 3-gallate inhibits invasion by inducing the expression of Raf kinase inhibitor protein in AsPC1 human pancreatic adenocarcinoma cells through the modulation of histone deacetylase activity. Int J Oncol 42:349-358.
78. Kim HS, Kim GY, Lim SJ, Kim YW. 2010. Loss of Raf-1 kinase inhibitory protein in pancreatic ductal adenocarcinoma. Pathology 42:655-660.
79. Kim W, Bennett EJ, Huttlin EL, Guo A, Li J, Possemato A, Sowa ME, Rad R, Rush J, Comb MJ, Harper JW, Gygi SP. 2011. Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol Cell 44:325-340.
80. Kim HS, Lee SH, Won KY, Kim GY, Park YK, Kim YW. 2012a. Expression of Raf-1 kinase inhibitory protein in carcinoma of the ampulla of Vater. Virchows Arch 460:61-68.
81. Kim HS, Won KY, Kim GY, Kim SC, Park YK, Kim YW. 2012b. Reduced expression of Raf-1 kinase inhibitory protein predicts regional lymph node metastasis and shorter survival in esophageal squamous cell carcinoma. Pathol Res Pract 208:292-299.
82. Kim SO, Ives KL, Wang X, Davey RA, Chao C, Hellmich MR. 2012c. Raf-1 kinase inhibitory protein (RKIP) mediates ethanol-induced sensitization of secretagogue signaling in pancreatic acinar cells. J Biol Chem 287:33377-33388.
83. Kleer CG, Cao Q, Varambally S, Shen R, Ota I, Tomlins SA, Ghosh D, Sewalt RG, Otte AP, Hayes DF, Sabel MS, Livant D, Weiss SJ, Rubin MA, Chinnaiyan AM. 2003. EZH2 is a marker of aggressive breast cancer and promotes neoplastic transformation of breast epithelial cells. Proc Natl Acad Sci USA 100:11606-11611.
84. Koch WJ, Rockman HA, Samama P, Hamilton RA, Bond RA, Milano CA, Lefkowitz RJ. 1995. Cardiac function in mice overexpressing the beta-adrenergic receptor kinase or a beta ARK inhibitor. Science 268:1350-1353.
85. Kondo Y, Shen L, Cheng AS, Ahmed S, Boumber Y, Charo C, Yamochi T, Urano T, Furukawa K, Kwabi-Addo B, Gold DL, Sekido Y, Huang TH, Issa JP. 2008. Gene silencing in cancer by histone H3 lysine 27 trimethylation independent of promoter DNA methylation. Nat Genet 40:741-750.
86. Kristensen LS, Nielsen HM, Hansen LL. 2009. Epigenetics and cancer treatment. Eur J Pharmacol 625:131-142.
87. Krueger JS, Keshamouni VG, Atanaskova N, Reddy KB. 2001. Temporal and quantitative regulation of mitogen-activated protein kinase (MAPK) modulates cell motility and invasion. Oncogene 20:4209-4218.
88. Kurdistani SK. 2011. Histone modifications in cancer biology and prognosis. Prog Drug Res 67:91-106.
89. 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.
90. Leong AS, Leong TY. 2011. Standardization in immunohistology. Methods Mol Biol 724:37-68.
91. Li HZ, Wang Y, Gao Y, Shao J, Zhao XL, Deng WM, Liu YX, Yang J, Yao Z. 2008. Effects of raf kinase inhibitor protein expression on metastasis and progression of human epithelial ovarian cancer. Mol Cancer Res 6:917-928.
92. Libra M, Torrisi E. 2009. BRAF and RKIP aberrations in actinic keratosis and non-melanoma skin cancers. Cell Cycle 8:1305.
93. Liotta LA, Kohn EC. 2001. The microenvironment of the tumour-host interface. Nature 411:375-3379.
94. 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.
95. Lujambio A, Lowe SW. 2012. The microcosmos of cancer. Nature 482:347-355.
96. Ma J, Li F, Liu L, Cui D, Wu X, Jiang X, Jiang H. 2009. Raf kinase inhibitor protein inhibits cell proliferation but promotes cell migration in rat hepatic stellate cells. Liver Int 29:567-574.
97. Mandili G, Khadjavi A, Gallo V, Minero VG, Bessone L, Carta F, Giribaldi G, Turrini F. 2012. Characterization of the protein ubiquitination response induced by Doxorubicin. FEBS J 279:2182-2191.
98. Maresch J, Birner P, Zakharinov M, Toumangelova-Uzeir K, Natchev S, Guentchev M. 2011. Additive effect on survival of Raf kinase inhibitor protein and signal transducer and activator of transcription 3 in high-grade glioma. Cancer 117:2499-2504.
99. Margueron R, Reinberg D. 2011. The Polycomb complex PRC2 and its mark in life. Nature 469:343-349.
100. Martinho O, Gouveia A, Silva P, Pimenta A, Reis RM, Lopes JM. 2009. Loss of RKIP expression is associated with poor survival in GISTs. Virchows Arch 455:277-284.
101. Martinho O, Faloppa CC, Neto CS, Longatto-Filho A, Baiocchi G, da Cunha IW, Soares FA, Fregnani JH, Reis RM. 2012a. Loss of RKIP expression during the carcinogenic evolution of endometrial cancer. J Clin Pathol 65:122-128.
102. Martinho O, Granja S, Jaraquemada T, Caeiro C, Miranda-Goncalves V, Honavar M, Costa P, Damasceno M, Rosner MR, Lopes JM, Reis RM. 2012b. Downregulation of RKIP is associated with poor outcome and malignant progression in gliomas. PLoS ONE 7:e30769.
103. Matallanas D, Birtwistle M, Romano D, Zebisch A, Rauch J, von Kriegsheim A, Kolch W. 2011. Raf family kinases: Old dogs have learned new tricks. Genes Cancer 2:232-260.
104. Minn AJ, Bevilacqua E, Yun J, Rosner MR. 2012. Identification of novel metastasis suppressor signaling pathways for breast cancer. Cell Cycle 11:2452-2457.
105. Minoo P, Baker K, Goswami R, Chong G, Foulkes WD, Ruszkiewicz AR, Barker M, Buchanan D, Young J, Jass JR. 2006. Extensive DNA methylation in normal colorectal mucosa in hyperplastic polyposis. Gut 55:1467-1474.
106. Minoo P, Zlobec I, Baker K, Tornillo L, Terracciano L, Jass JR, Lugli A. 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.
107. Mitake S, Ojika K, Katada E, Otsuka Y, Matsukawa N, Fujimori O. 1995. Accumulation of hippocampal cholinergic neurostimulating peptide (HCNP)-related components in Hirano bodies. Neuropathol Appl Neurobiol 21:35-40.
108. Mitake S, Katada E, Otsuka Y, Matsukawa N, Iwase T, Tsugu T, Fujimori O, Ojika K. 1996a. Possible implication of hippocampal cholinergic neurostimulating peptide (HCNP)-related components in Hirano body formation. Neuropathol Appl Neurobiol 22:440-445.
109. Mitake S, Ojika K, Katada E, Otsuka Y, Matsukawa N, Fujimori O. 1996b. Distribution of hippocampal cholinergic neurostimulating peptide (HCNP) immunoreactivity in the central nervous system of the rat. Brain Res 706:57-70.
110. Moen EL, Wen S, Anwar T, Cross-Knorr S, Brilliant K, Birnbaum F, Rahaman S, Sedivy JM, Moss SF, Chatterjee D. 2012. Regulation of RKIP function by Helicobacter pylori in gastric cancer. PLoS ONE 7:e37819.
111. Moffit JS, Boekelheide K, Sedivy JM, Klysik J. 2007. Mice lacking Raf kinase inhibitor protein-1 (RKIP-1) have altered sperm capacitation and reduced reproduction rates with a normal response to testicular injury. J Androl 28:883-890.
112. Moon A, Park JY, Sung JY, Park YK, Kim YW. 2012. Reduced expression of Raf-1 kinase inhibitory protein in renal cell carcinoma: A significant prognostic marker. Pathology 44:534-539.
113. Morey L, Helin K. 2010. Polycomb group protein-mediated repression of transcription. Trends Biochem Sci 35:323-332.
114. Morgan C, LaCourse EJ, Rushbrook BJ, Greetham D, Hamilton JV, Barrett J, Bailey K, Brophy PM. 2006. Plasticity demonstrated in the proteome of a parasitic nematode within the intestine of different host strains. Proteomics 6:4633-4645.
115. Murga-Zamalloa CA, Ghosh AK, Patil SB, Reed NA, Chan LS, Davuluri S, Peranen J, Hurd TW, Rachel RA, Khanna H. 2011. Accumulation of the Raf-1 kinase inhibitory protein (Rkip) is associated with Cep290-mediated photoreceptor degeneration in ciliopathies. J Biol Chem 286:28276-28286.
116. Nguyen DX, Bos PD, Massague J. 2009. Metastasis: From dissemination to organ-specific colonization. Nat Rev Cancer 9:274-284.
117. Notarbartolo M, Giannitrapani L, Vivona N, Poma P, Labbozzetta M, Florena AM, Porcasi R, Muggeo VM, Sandonato L, Cervello M, Montalto G, D'Alessandro N. 2011. Frequent alteration of the Yin Yang 1/Raf-1 kinase inhibitory protein ratio in hepatocellular carcinoma. OMICS 15:267-272.
118. Odabaei G, Chatterjee D, Jazirehi AR, Goodglick L, Yeung K, Bonavida B. 2004. Raf-1 kinase inhibitor protein: Structure, function, regulation of cell signaling, and pivotal role in apoptosis. Adv Cancer Res 91:169-200.
119. Ohta T, Iijima K, Miyamoto M, Nakahara I, Tanaka H, Ohtsuji M, Suzuki T, Kobayashi A, Yokota J, Sakiyama T, Shibata T, Yamamoto M, Hirohashi S. 2008. Loss of Keap1 function activates Nrf2 and provides advantages for lung cancer cell growth. Cancer Res 68:1303-1309.
120. Park S, Yeung ML, Beach S, Shields JM, Yeung KC. 2005. RKIP downregulates B-Raf kinase activity in melanoma cancer cells. Oncogene 24:3535-3540.
121. Park S, Rath O, Beach S, Xiang X, Kelly SM, Luo Z, Kolch W, Yeung KC. 2006. Regulation of RKIP binding to the N-region of the Raf-1 kinase. FEBS Lett 580:6405-6412.
122. Park S, Ahn ES, Lee S, Jung M, Park JH, Yi SY, Yeom CH. 2009. Proteomic analysis reveals upregulation of RKIP in S-180 implanted BALB/C mouse after treatment with ascorbic acid. J Cell Biochem 106:1136-1145.
123. Perry AC. 1994. Sequence analysis of a mammalian phospholipid-binding protein from testis and epididymis and its distribution between spermatozoa and extracellular secretions. Biochem J 301:235-242.
124. Poma P, Labbozzetta M, Vivona N, Porcasi R, D'Alessandro N, Notarbartolo M. 2012. Analysis of possible mechanisms accounting for raf-1 kinase inhibitor protein downregulation in hepatocellular carcinoma. OMICS 16:579-588.
125. Ponten F, Jirstrom K, Uhlen M. 2008. The human protein atlas-A tool for pathology. J Pathol 216:387-393.
126. Poste G, Fidler IJ. 1980. The pathogenesis of cancer metastasis. Nature 283:139-146.
127. Raake PW, Vinge LE, Gao E, Boucher M, Rengo G, Chen X, DeGeorge BR, Jr., Matkovich S, Houser SR, Most P, Eckhart AD, Dorn GW II, Koch WJ. 2008. G protein-coupled receptor kinase 2 ablation in cardiac myocytes before or after myocardial infarction prevents heart failure. Circ Res 103:413-422.
128. Rautureau G, Jouvensal L, Vovelle F, Schoentgen F, Locker D, Decoville M. 2009. Expression and characterization of the PEBP homolog genes from Drosophila. Arch Insect Biochem Physiol 71:55-69.
129. Rayasam GV, Tulasi VK, Sodhi R, Davis JA, Ray A. 2009. Glycogen synthase kinase 3: More than a namesake. Br J Pharmacol 156:885-898.
130. Ren G, Baritaki S, Marathe H, Feng J, Park S, Beach S, Bazeley PS, Beshir AB, Fenteany G, Mehra R, Daignault S, Al-Mulla F, Keller E, Bonavida B, de la Serna I, Yeung KC. 2012. Polycomb protein EZH2 regulates tumor invasion via the transcriptional repression of the metastasis suppressor RKIP in breast and prostate cancer. Cancer Res 72:3091-3104.
131. Reumer A, Bogaerts A, Van Loy T, Husson SJ, Temmerman L, Choi C, Clynen E, Hassan B, Schoofs L. 2009. Unraveling the protective effect of a Drosophila phosphatidylethanolamine-binding protein upon bacterial infection by means of proteomics. Dev Comp Immunol 33:1186-1195.
132. Ribas C, Penela P, Murga C, Salcedo A, Garcia-Hoz C, Jurado-Pueyo M, Aymerich I, Mayor F, Jr. 2007. The G protein-coupled receptor kinase (GRK) interactome: Role of GRKs in GPCR regulation and signaling. Biochim Biophys Acta 1768:913-922.
133. Roos A, Boron WF. 1981. Intracellular pH. Physiol Rev 61:296-434.
134. Saunders PT, McKinnell C, Millar MR, Gaughan J, Turner KJ, Jegou B, Syed V, Sharpe RM. 1995. Phosphatidylethanolamine binding protein is an abundant secretory product of haploid testicular germ cells in the rat. Mol Cell Endocrinol 107:221-230.
135. Schoentgen F, Saccoccio F, Jolles J, Bernier I, Jolles P. 1987. Complete amino acid sequence of a basic 21-kDa protein from bovine brain cytosol. Eur J Biochem 166:333-338.
136. Schoentgen F, Seddiqi N, Bucquoy S, Jolles P, Lemesle-Varloot L, Provost K, Mornon JP. 1992. Main structural and functional features of the basic cytosolic bovine 21kDa protein delineated through hydrophobic cluster analysis and molecular modelling. Protein Eng 5:295-303.
137. 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.
138. Schuierer MM, Bataille F, Weiss TS, Hellerbrand C, Bosserhoff AK. 2006. Raf kinase inhibitor protein is downregulated in hepatocellular carcinoma. Oncol Rep 16:451-456.
139. Schwanhausser B, Gossen M, Dittmar G, Selbach M. 2009. Global analysis of cellular protein translation by pulsed SILAC. Proteomics 9:205-209.
140. Seddiqi N, Bollengier F, Alliel PM, Perin JP, Bonnet F, Bucquoy S, Jolles P, Schoentgen F. 1994. Amino acid sequence of the Homo sapiens brain 21-23-kDa protein (neuropolypeptide h3), comparison with its counterparts from Rattus norvegicus and Bos taurus species, and expression of its mRNA in different tissues. J Mol Evol 39:655-660.
141. Seddiqi N, Segretain D, Bucquoy S, Pineau C, Jegou B, Jolles P, Schoentgen F. 1996. Characterization and localization of the rat, mouse and human testicular phosphatidylethanolamine binding protein. Experientia 52:101-110.
142. Selbach M, Schwanhausser B, Thierfelder N, Fang Z, Khanin R, Rajewsky N. 2008. Widespread changes in protein synthesis induced by microRNAs. Nature 455:58-63.
143. Sells MA, Boyd JT, Chernoff J. 1999. p21-activated kinase 1 (Pak1) regulates cell motility in mammalian fibroblasts. J Cell Biol 145:837-849.
144. Serrano CV, Jr., Fraticelli A, Paniccia R, Teti A, Noble B, Corda S, Faraggiana T, Ziegelstein RC, Zweier JL, Capogrossi MC. 1996. pH dependence of neutrophil-endothelial cell adhesion and adhesion molecule expression. Am J Physiol 271:C962-C970.
145. Serre L, Vallee B, Bureaud N, Schoentgen F, Zelwer C. 1998. Crystal structure of the phosphatidylethanolamine-binding protein from bovine brain: A novel structural class of phospholipid-binding proteins. Structure 6:1255-1265.
146. Serre L, Pereira de Jesus K, Zelwer C, Bureaud N, Schoentgen F, Benedetti H. 2001. Crystal structures of YBHB and YBCL from Escherichia coli, two bacterial homologues to a Raf kinase inhibitor protein. J Mol Biol 310:617-634.
147. Sethi N, Kang Y. 2011. Unravelling the complexity of metastasis-Molecular understanding and targeted therapies. Nat Rev Cancer 11:735-748.
148. Shemon AN, Eves EM, Clark MC, Heil G, Granovsky A, Zeng L, Imamoto A, Koide S, Rosner MR. 2009. Raf Kinase Inhibitory Protein protects cells against locostatin-mediated inhibition of migration. PLoS ONE 4:e6028.
149. Shemon AN, Heil GL, Granovsky AE, Clark MM, McElheny D, Chimon A, Rosner MR, Koide S. 2010. Characterization of the Raf kinase inhibitory protein (RKIP) binding pocket: NMR-based screening identifies small-molecule ligands. PLoS ONE 5:e10479.
150. Shoushtari AN, Szmulewitz RZ, Rinker-Schaeffer CW. 2011. Metastasis-suppressor genes in clinical practice: Lost in translation? Nat Rev Clin Oncol 8:333-342.
151. Simister PC, Banfield MJ, Brady RL. 2002. The crystal structure of PEBP-2, a homologue of the PEBP/RKIP family. Acta Crystallogr D Biol Crystallogr 58:1077-1080.
152. Singhal J, Nagaprashantha LD, Vatsyayan R, Ashutosh Awasthi S, Singhal SS. 2012. Didymin induces apoptosis by inhibiting N-Myc and upregulating RKIP in neuroblastoma. Cancer Prev Res (Phila) 5:473-483.
153. Solis LM, Behrens C, Dong W, Suraokar M, Ozburn NC, Moran CA, Corvalan AH, Biswal S, Swisher SG, Bekele BN, Minna JD, Stewart DJ, Wistuba II. 2010. Nrf2 and Keap1 abnormalities in non-small cell lung carcinoma and association with clinicopathologic features. Clin Cancer Res 16:3743-3753.
154. Song SP, Zhang SB, Li ZH, Zhou YS, Li B, Bian ZW, Liao QD, Zhang YD. 2012. Reduced expression of Raf kinase inhibitor protein correlates with poor prognosis in pancreatic cancer. Clin Transl Oncol 14:848-852.
155. Stacy DR, Ely K, Massion PP, Yarbrough WG, Hallahan DE, Sekhar KR, Freeman ML. 2006. Increased expression of nuclear factor E2 p45-related factor 2 (NRF2) in head and neck squamous cell carcinomas. Head Neck 28:813-818.
156. Su AI, Wiltshire T, Batalov S, Lapp H, Ching KA, Block D, Zhang J, Soden R, Hayakawa M, Kreiman G, Cooke MP, Walker JR, Hogenesch JB. 2004. A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci USA 101:6062-6067.
157. Sun H, Zhu T, Ding F, Hu N, Gu X. 2009. Proteomic studies of rat tibialis anterior muscle during postnatal growth and development. Mol Cell Biochem 332:161-171.
158. Tang H, Park S, Sun SC, Trumbly R, Ren G, Tsung E, Yeung KC. 2010. RKIP inhibits NF-kappaB in cancer cells by regulating upstream signaling components of the IkappaB kinase complex. FEBS Lett 584:662-668.
159. Tavel L, Jaquillard L, Karsisiotis AI, Saab F, Jouvensal L, Brans A, Delmas AF, Schoentgen F, Cadene M, Damblon C. 2012. Ligand binding study of human PEBP1/RKIP: Interaction with nucleotides and Raf-1 peptides evidenced by NMR and mass spectrometry. PLoS ONE 7:e36187.
160. Theroux S, Pereira M, Casten KS, Burwell RD, Yeung KC, Sedivy JM, Klysik J. 2007. Raf kinase inhibitory protein knockout mice: Expression in the brain and olfaction deficit. Brain Res Bull 71:559-567.
161. Thongboonkerd V, Barati MT, McLeish KR, Benarafa C, Remold-O'Donnell E, Zheng S, Rovin BH, Pierce WM, Epstein PN, Klein JB. 2004. Alterations in the renal elastin-elastase system in type 1 diabetic nephropathy identified by proteomic analysis. J Am Soc Nephrol 15:650-662.
162. Thornton TM, Pedraza-Alva G, Deng B, Wood CD, Aronshtam A, Clements JL, Sabio G, Davis RJ, Matthews DE, Doble B, Rincon M. 2008. Phosphorylation by p38 MAPK as an alternative pathway for GSK3beta inactivation. Science 320:667-670.
163. Trakul N, Rosner MR. 2005. Modulation of the MAP kinase signaling cascade by Raf kinase inhibitory protein. Cell Res 15:19-23.
164. 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.
165. Tsukamoto Y, Nakada C, Noguchi T, Tanigawa M, Nguyen LT, Uchida T, Hijiya N, Matsuura K, Fujioka T, Seto M, Moriyama M. 2010. MicroRNA-375 is downregulated in gastric carcinomas and regulates cell survival by targeting PDK1 and 14-3-3zeta. Cancer Res 70:2339-2349.
166. Valadao M, Braggio D, Santos AF, Pimenta-Inada HK, Linhares E, Goncalves R, Romano S, Vilhena B, Small I, Cubero D, Cruz F, Oliveira AT, Martinho O, Reis RM, Guimaraes DP, Ferreira CG. 2012. Involvement of signaling molecules in the prediction of response to imatinib treatment in metastatic GIST patients. J Surg Res 178:288-293.
167. Vallee BS, Tauc P, Brochon JC, Maget-Dana R, Lelievre D, Metz-Boutigue MH, Bureaud N, Schoentgen F. 2001. Behaviour of bovine phosphatidylethanolamine-binding protein with model membranes. Evidence of affinity for negatively charged membranes. Eur J Biochem 268:5831-5841.
168. Varambally S, Dhanasekaran SM, Zhou M, Barrette TR, Kumar-Sinha C, Sanda MG, Ghosh D, Pienta KJ, Sewalt RG, Otte AP, Rubin MA, Chinnaiyan AM. 2002. The polycomb group protein EZH2 is involved in progression of prostate cancer. Nature 419:624-629.
169. Venugopal R, Jaiswal AK. 1996. Nrf1 and Nrf2 positively and c-Fos and Fra1 negatively regulate the human antioxidant response element-mediated expression of NAD(P)H:quinone oxidoreductase1 gene. Proc Natl Acad Sci USA 93:14960-14965.
170. Walker EJ, Rosenberg SA, Wands JR, Kim M. 2011. Role of Raf kinase inhibitor protein in hepatocellular carcinoma. For Immunopathol Dis Therap 2:195-204.
171. Wang Y, Yang J, Gao Y, Zhao XL, Li HZ, Yao Z. 2009. [Relationship between raf kinase inhibitor protein and metastasis of ovarian carcinoma]. Zhonghua Fu Chan Ke Za Zhi 44:522-528.
172. Woods Ignatoski KM, Grewal NK, Markwart SM, Vellaichamy A, Chinnaiyan AM, Yeung K, Ray ME, Keller ET. 2008. Loss of Raf kinase inhibitory protein induces radioresistance in prostate cancer. Int J Radiat Oncol Biol Phys 72:153-160.
173. 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.
174. Wu XH, Wang SX, Yang YJ, Li JK, Xu Z, Tang RF. 2011. [Expression of Raf kinase inhibitor protein and its significance in invasion and metastasis of hepatocellular carcinoma]. Zhonghua Zhong Liu Za Zhi 33:358-362.
175. Xinzhou H, Ning Y, Ou W, Xiaodan L, Fumin Y, Huitu L, Wei Z. 2011. RKIp inhibits the migration and invasion of human prostate cancer PC-3M cells through regulation of extracellular matrix. Mol Biol (Mosk) 45:1004-1011.
176. Xu YF, Yi Y, Qiu SJ, Gao Q, Li YW, Dai CX, Cai MY, Ju MJ, Zhou J, Zhang BH, Fan J. 2010. PEBP1 downregulation is associated to poor prognosis in HCC related to hepatitis B infection. J Hepatol 53:872-879.
177. Yasuda H, Terada M, Maeda K, Kogawa S, Sanada M, Haneda M, Kashiwagi A, Kikkawa R. 2003. Diabetic neuropathy and nerve regeneration. Prog Neurobiol 69:229-285.
178. Yeung K, Seitz T, Li S, Janosch P, McFerran B, Kaiser C, Fee F, Katsanakis KD, Rose DW, Mischak H, Sedivy JM, Kolch W. 1999. Suppression of Raf-1 kinase activity and MAP kinase signalling by RKIP. Nature 401:173-177.
179. Yeung K, Janosch P, McFerran B, Rose DW, Mischak H, Sedivy JM, Kolch W. 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.
180. Yeung KC, Rose DW, Dhillon AS, Yaros D, Gustafsson M, Chatterjee D, McFerran B, Wyche J, Kolch W, Sedivy JM. 2001. Raf kinase inhibitor protein interacts with NF-kappaB-inducing kinase and TAK1 and inhibits NF-kappaB activation. Mol Cell Biol 21:7207-7217.
181. Yook JI, Li XY, Ota I, Fearon ER, Weiss SJ. 2005. Wnt-dependent regulation of the E-cadherin repressor snail. J Biol Chem 280:11740-11748.
182. Yun J, Frankenberger CA, Kuo WL, Boelens MC, Eves EM, Cheng N, Liang H, Li WH, Ishwaran H, Minn AJ, Rosner MR. 2011. Signalling pathway for RKIP and Let-7 regulates and predicts metastatic breast cancer. EMBO J 30:4500-4514.
183. 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.
184. Zebisch A, Wolfler A, Fried I, Wolf O, Lind K, Bodner C, Haller M, Drasche A, Pirkebner D, Matallanas D, Rath O, Blyth K, Delwel R, Taskesen E, Quehenberger F, Kolch W, Troppmair J, Sill H. 2012. Frequent loss of RAF kinase inhibitor protein expression in acute myeloid leukemia. Leukemia 26:1842-1849.
185. Zeng L, Imamoto A, Rosner MR. 2008. Raf kinase inhibitory protein (RKIP): A physiological regulator and future therapeutic target. Expert Opin Ther Targets 12:1275-1287.
186. Zhang D, Tai LK, Wong LL, Putti TC, Sethi SK, Teh M, Koay ES. 2008. Proteomic characterization of differentially expressed proteins in breast cancer: Expression of hnRNP H1, RKIP and GRP78 is strongly associated with HER-2/neu status. Proteomics Clin Appl 2:99-107.
187. Zhang H, Wu J, Keller JM, Yeung K, Keller ET, Fu Z. 2012. Transcriptional regulation of RKIP expression by androgen in prostate cells. Cell Physiol Biochem 30:1340-1350.
188. Zhang XM, Gu H, Yan L, Zhang GY. 2013. RKIP inhibits the malignant phenotypes of gastric cancer cells. Neoplasma 60:196-202.
189. 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.
190. Zlobec I, Baker K, Minoo P, Jass JR, Terracciano L, Lugli A. 2008a. 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.
191. Zlobec I, Baker K, Terracciano L, Peter S, Degen L, Beglinger C, Lugli A. 2008b. Two-marker protein profile predicts poor prognosis in patients with early rectal cancer. Br J Cancer 99:1712-1717.
192. Zlobec I, Bihl M, Foerster A, Rufle A, Lugli A. 2011. Comprehensive analysis of CpG island methylator phenotype (CIMP)-high, -low, and -negative colorectal cancers based on protein marker expression and molecular features. J Pathol 225:336-343.