Prkc-ζ expression promotes the aggressive phenotype of human prostate cancer cells and is a novel target for therapeutic intervention

Genes and Cancer

Volumn 1, Issue 5, 2010, Pages 444-464

  Yao, Sheng ^a   Bee, Alix ^a   Brewer, Daniel ^b   Dodson, Andrew ^a   Beesley, Carol ^a   Ke, Youqiang ^a   Ambroisine, Laurence ^c   Fisher, Gabrielle ^c   Møller, Heinrich ^d   Dickinson, Tim ^a   Gerard, Patricia ^a   Lian, Lu Yu ^a   Risk, Janet ^a   Lane, Brian ^a   Smith, Paul ^a   Reuter, Victor ^e   Berney, Daniel ^f   Gosden, Christine ^a   Scardino, Peter ^e   Cuzick, Jack ^c   Djamgoz, Mustafa B A ^g   Cooper, Colin ^b   Foster, Christopher S ^a   more..

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^c QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^d KING'S COLLEGE LONDON   (United Kingdom)

^e MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^f QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^g IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

PRKC ; Prostate cancer; siRNA

Indexed keywords

HEAT SHOCK PROTEIN 27; INHIBITOR OF DIFFERENTIATION 1; PROTEIN KINASE C ZETA; RAD51 PROTEIN; SMALL INTERFERING RNA;

ADULT; AGED; ARTICLE; CANCER CELL; CONTROLLED STUDY; DRUG TARGETING; GENE EXPRESSION; GENE REGULATORY NETWORK; GENE SILENCING; GENETIC ASSOCIATION; GENETIC IDENTIFICATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; KNOCKOUT GENE; MAJOR CLINICAL STUDY; MALE; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION;

EID: 79952848971     PISSN: 19476019     EISSN: 19476027     Source Type: Journal    
DOI: 10.1177/1947601910376079     Document Type: Article

References (94)

1. Jemal A, Siegel R, Ward E, et al. Cancer statistics 2008. CA Cancer J Clin 2008;58:71-96.
2. Cancer Research UK. Cancer stats, key facts on prostate cancer- November 2008. Available from: http://www.cancerresearchuk.org/cancerstats/types/prostatecancer. Accessed April 2009.
3. Easton DF, Eeles RA. Genome-wide association studies in cancer. Hum Mol Genet 2008;17:R109-R15.
4. Al Olama AA, Kote-Jarai Z, Giles GG, et al. Multiple loci on 8q24 associated with prostate cancer susceptibility. Nat Genet 2009;41:1058-60.
5. Eeles RA, Kote-Jarai Z, Al-Olama AA, et al. Identification of seven new prostate cancer susceptibility loci through a genome-wide association study. Nat Genet 2009;41:1116-21.
6. Foster CS, Cooper CS. Urgent need to develop independent biomarkers for functional, diagnostic and prognostic application in oncology research. Biomarkers Med 2009;3:329-33.
7. Cuzick J, Fisher G, Kattan MW, et al. Long-term outcome among men with conservatively treated localised prostate cancer. Br J Cancer 2006;95:1186-94.
8. Cornford P, Evans J, Dodson AR, et al. Protein kinase C isoenzyme patterns characteristically modulated in early prostate cancer. Am J Pathol 1999;154:137-44.
9. Sun R, Gao P, Chen L, et al. Protein kinase C zeta is required for epidermal growth factor-induced chemotaxis of human breast cancer cells. Cancer Res 2005;65:1433-41.
10. Galvez AS, Duran A, Linares JF, et al. Protein kinase Cζ represses the interleukin-6 promoter and impairs tumorigenesis in vivo. Mol Cell Biol 2009;29:104-15.
11. Liu Y, Wang B, Wang J, et al. Down-regulation of PKC zeta expression inhibits chemotaxis signal transduction in human lung cancer cells. Lung Cancer 2009;63:210-8.
12. Evans JD, Cornford PA, Dodson A, Neoptolemos JP, Foster CS. Expression patterns of protein kinase C isoenzymes are characteristically modulated in chronic pancreatitis and pancreatic cancer. Am J Clin Pathol 2003;119:392-402.
13. Laudanna C, Sorio C, Tecchio C, et al. Motility analysis of pancreatic adenocarcinoma cells reveals a role for the atypical zeta isoform of protein kinase C in cancer cell movement. Lab Invest 2003;83:1155-63.
14. Pearson M, Hurley JH. Structure, function and membrane interactions of C1 domains. In: Protein kinase C. 2nd ed. Kluwer Academic/Plenum: 2004. p. 9-15.
15. Masso-Welch PA, Verstovsek G, Ip MM. Alterations in the expression and localization of protein kinase C isoforms during mammary gland differentiation. Eur J Cell Biol 1999;78:497-510.
16. Muscella A, Storelli C, Marsigliante S. Atypical PKC-zeta and PKCiota mediate opposing effects on MCF-7 Na+/K+ ATPase activity. J Cell Physiol 2005;205:278-85.
17. Park JW, Kim HP, Lee SJ, et al. Protein kinase C alpha and zeta differentially regulate death-inducing signaling complex formation in cigarette smoke extract-induced apoptosis. J Immunol 2008;180:4668-78.
18. Guo H, Gu F, Li W, et al. Reduction of protein kinase Cζ inhibits migration and invasion of human glioblastoma cells. J Neurochem 2009;109:203-13.
19. Kela I, Harmelin A, Waks T, Orr-Urtreger A, Domany E, Eshhar Z. Interspecies comparison of prostate cancer gene-expression profiles reveals genes associated with aggressive tumors. Prostate 2009;69:1034-44.
20. Cooper CS, Foster CS. Concepts of epigenetics in prostate cancer development. Br J Cancer 2009;100:240-5.
21. Morgan EA, Forootan SS, Adamson J, et al. Expression of cutaneous fatty acid-binding protein (C-FABP) in prostate cancer: potential prognostic marker and target for tumourigenicity-suppression. Int J Oncol 2008;32:767-75.
22. Bee A, Ke Y, Forootan S, et al. Ribosomal protein L19 is a prognostic marker for human prostate cancer. Clin Cancer Res 2006;12:2061-5.
23. Forootan SS, Wong Y-C, Dodson A, et al. Increased Id-1 expression is significantly associated with poor survival of patients with prostate cancer. Hum Pathol 2007;38:1321-9.
24. Mitra A, Jameson C, Barbachano Y, et al. Over-expression of RAD51 occurs in aggressive prostate cancer. Histopathology 2009;55:696-704.
25. Foster CS, Dodson AR, Ambroisine L, et al. Hsp-27 expression at diagnosis predicts poor clinical outcome in prostate cancer independent of ETS-gene rearrangement. Br J Cancer 2009;101:1137-44.
26. Smith P, Rhodes NP, Shortland AP, et al. Sodium channel protein expression enhances the invasiveness of rat and human prostate cancer cells. FEBS Lett 1998;423:19-24.
27. Diss JK, Stewart D, Pani F, et al. A potential novel marker for human prostate cancer: voltage-gated sodium channel expression in vivo. Pros Cancer Pros Dis 2005;8:266-73.
28. Grimes JA, Fraser SP, Stephens GJ, et al. Differential expression of voltage-activated Na+ currents in two prostatic tumour cell lines: contribution to invasiveness in vitro. FEBS Lett 1995;369:290-4.
29. Fraser SP, Ding Y, Liu A, Foster CS, Djamgoz MBA. Tetrodotoxin suppresses morphological enhancement of the metastatic MAT-LyLu rat prostate cancer cell line. Cell Tissue Res 1999;295:505-12.
30. de Albuquerque Garcia Redondo P, Nakamura CV, de Souza W, Morgado-Diaz JA. Differential expression of sialic acid and N-acetylgalactosamine residues on the cell surface of intestinal epithelial cells according to normal or metastatic potential. J Histochem Cytochem 2004;52:629-40.
31. Wang FL, Cui SX, Sun LP, et al. High expression of alpha 2, 3-linked sialic acid residues is associated with the metastatic potential of human gastric cancer. Cancer Detect Prev 2009;32:437-43.
32. Barthel SR, Wiese GK, Cho J, et al. Alpha 1,3 fucosyltransferases are master regulators of prostate cancer cell trafficking. Proc Nat Acad Sci U S A 2009;106:19491-6.
33. Liu S, Meng L, Moremen KW, Prestegard JH. Nuclear magnetic resonance structural characterization of substrates bound to the alpha-2,6- sialyltransferase, ST7Gal-I. Biochemistry (Mosc) 2009;48:11211-9.
34. + channel activity in human prostate cancer cell lines of markedly different metastatic potential: distinguishing characteristics of PC-3 and LNCaP cells. Prostate 2001;46:262-74.
35. Smith P, Rhodes NP, Shortland AP, et al. Upregulation of sodium channel protein expression correlates with increase in invasiveness of rat and human prostate cancer cell lines. FEBS Lett 1998;423: 19-24.
36. Foster CS, Dodson A, Karavana V, Smith PH, Ke Y. Prostatic stem cells. J Pathol 2002;197:551-65.
37. Fraser S, Grimes JA, Djamgoz MBA. Effects of voltage-gated ion channel modulators on rat prostatic cancer cell proliferation: comparison of strongly and weakly metastatic cell lines. Prostate 2000;44:61-76.
38. Khaitan D, Sankpal UT, Weksler B, et al. Role of KCNMA1 gene in breast cancer invasion and metastasis to brain. BMC Cancer 2009;9:258.
39. Lian WN, Wu TW, Dao Rl, Chen YJ, Lin CH. Deglycosylation of Na+/ K+-ATPase causes the basolateral protein to undergo apical targeting in polarized hepatic cells. J Cell Sci 2006;119:11-22.
40. Vagin O, Turdikulova S, Tokhtaeva E. Polarized membrane distribution of potassium-dependent ion pumps in epithelial cells: different roles of the N-glycans of their beta subunits. Cell Biochem Biophys 2007;47:376-91.
41. Foster CS. Functional aspects of glycoprotein N-linked oligosaccharide processing by human tumors. Br J Cancer 1990;62:57-63.
42. Wu J, Zhang B, Wu M, et al. Screening of a PKC zeta-specific kinase inhibitor PKCz1257.3 which inhibits EGF-induced breast cancer cell chemotaxis. Invest New Drugs Mar 27 2009. [Epub ahead of print]
43. Coghlan MP, Chou MM, Carpenter CL. Atypical protein kinases Cλ and - ζ associate with the GTP-binding protein Cdc42 and mediate stress fiber loss. Mol Cell Biol 2000;20:2880-9.
44. Liu XJ, Yang C, Gupta N, Zuo J, Chang YS, Fang FD. Protein kinase C-zeta regulation of GLUT4 translocation through actin remodelling in CHO cells. J Mol Med 2007;85:851-61.
45. Wang HR, Zhang Y, Ozdamar B, et al. Regulation of cell polarity and protrusion formation by targeting RhoA for degradation. Science 2003;302:1775-9.
46. Even-Faitelson L, Ravid S. PAK1 and a PKCzeta regulate myosin II-B phosphorylation: a novel signaling pathway regulating filament assembly. Mol Biol Cell 2006;17:2869-81.
47. Etienne-Manneville S. Polarity proteins in migration and invasion. Oncogene 2008;27:6970-80.
48. Suzuki A, Ohno S. The PAR-aPKC system: lessons in polarity. J Cell Sci 2006;119:979-87.
49. Etienne-Manneville S, Manneville JB, Nicholls S, Ferenczi MA, Hall A. Cdc42 and Par6-PKCzeta regulate the spatially localized association of Dig1 and APC to control cell polarization. J Cell Biol 2005;170:895-901.
50. Wang J, Wan W, Sun R, et al. Reduction of Akt2 expression inhibits chemotaxis signal transduction in human breast cancer cells. Cell Signal 2008;20:1025-34.
51. Ozdamar B, Bose R, Barrios-Rodiles M, Wang HR, Zhang Y, Wrana JL. Regulation of the polarity protein Par6 by TGFbeta receptors controls epithelial cell plasticity. Science 2005;307:1603-9.
52. Rodriguez EM, Dunham EE, Martin GS. Atypical protein kinase C activity is required for extracellular matrix degradation and invasion by Src-transformed cells. J Cell Physiol 2009;221:171-82.
53. Tak H, Jang E, Kim SB, et al. 14-3-3epsilon inhibits MK5-mediated cell migration by disturbing F-actin polymerization. Cell Signal 2007;19:2379-87.
54. Doshi BM, Hightower LE, Lee J. The role of Hsp27 and actin in the regulation of movement in human cancer cells responding to heat shock. Cell Stress Chaperones 2009;14:445-57.
55. Gomez-Casero E, San-Antonio B, Iniquez MA, Fresno M. Cot/Tpl2 and PKCzeta cooperate in the regulation of the transcriptional activity of NFATc2 through the phosphorylation of its amino-terminal domain. Cell Signal 2007;19:1652-61.
56. Teusch N, Lombardo E, Eddleston J, Knaus UG. The low molecular weight GTPase RhoA and atypical protein kinase Czeta are required for TLR2-mediated gene transcription. J Immunol 2004;173:507-14.
57. Singh AP, Bafna S, Chaudhary K, et al. Genome-wide expression profiling reveals transcriptomic variation and perturbed gene networks in androgen-dependent and androgen-independent prostate cancer cells. Cancer Lett 2008;259:28-38.
58. Wang L, Tang H, Thayanithy V, et al. Gene networks and microRNAs implicated in aggressive prostate cancer. Cancer Res 2009;69:9490-7.
59. Boskovic J, Coloma J, Aparicio T, et al. Molecular architecture of the human GINS complex. EMBO Rep 2007;8:678-84.
60. Barkley LR, Song IY, Zou Y, Vaziri C. Reduced expression of GINS complex members induces hallmarks of pre-malignancy in primary untransformed human cells. Cell Cycle 2009;8:1577-88.
61. Truhlar SM, Torpey JW, Komives EA. Regions of IkappaBalpha that are critical for its inhibition of NF-kappaB. DNA interaction fold upon binding to NF-kappaB. Proc Nat Acad Sci U S A 2006; 103:18951-6.
62. Guy M, Kote-Jarai Z, Giles GG, et al. Identification of new genetic risk factors for prostate cancer. Asian J Androl 2009;11:49-55.
63. Forootan SS, Bao ZZ, Forootan FS, et al. Atelocollagen-delivered siRNA targeting the FABP5 gene as an experimental therapy for prostate cancer in mouse xenografts. Int J Oncol 2009;36:69-76.
64. Goekjian PG, Jirousek MR. Protein kinase C inhibitors as novel anticancer drugs. Expert Opin Investig Drugs 2001;10:2117-40.
65. Gonelli A, Mischiati C, Guerrini R, Voltan R, Salvadori S, Zauli G. Perspectives of protein kinase C (PKC) inhibitors as anti-cancer agents. Mini Rev Med Chem 2009;9:498-509.
66. Herbst R, Oh Y, Wagle A, Lahn M. Enzastaurin, a protein kinase Cβ- selective inhibitor, and its potential application as an anticancer agent in lung cancer. Clin Cancer Res 2007;13:4641s-6s.
67. Fields AP, Frederick LA, Regala RP. Targeting the oncogenic protein kinase C iota signalling pathway for the treatment of cancer. Biochem Soc Trans 2007;35:996-1000.
68. Whitson EL, Bugni TS, Chockalingam PS, et al. Spheciosterol sulfates, PKCzeta inhibitors from a Philippine sponge Spheciospongia sp. J Nat Prod 2008;71:1213-7.
69. Yuan L, Seo JS, Kang NS, et al. Identification of 3-hydroxy-2-(3- hydroxyphenyl)-4H-1-benzopyran-4-ones as isoform-selective PKCzeta inhibitors and potential therapeutics for psychostimulant abuse. Mol Biosyst 2009;5:927-30.
70. Tatsuda Y, Iguchi K, Usui S, Suzui M, Hirano K. Protein kinase C is inhibited by bisphosphonates in prostate cancer PC-3 cells. Eur J Pharmacol 2010;627:348-53.
71. Roffey J, Rosse C, Linch M, Hibbert A, McDonald NQ, Parker PJ. Protein kinase C intervention: the state of play. Curr Opin Cell Biol 2009;21:268-79.
72. Spurdle AB, Couch FJ, Hogervorst FB, Radice P, Sinilnikova OM; IARC Unclassified Genetic Variants Working Group. Prediction and assessment of splicing alterations: implications for clinical testing. Hum Mutat 2008;29:1304-13.
73. Wulff H, Castle NA, Pardo LA. Voltage-gated potassium channels as therapeutic targets. Nat Rev Drug Discov 2009;8:982-1001.
74. Faratian D, Langdon SP, Harrison DJ. How can systems pathology help us personalize cancer therapy? Discov Med 2009;8:81-6.
75. Honma Y, Akimoto M. Therapeutic strategy using phenotypic modulation of cancer cells by differentiation-inducing agents. Cancer Sci 2007;98:1643-51.
76. Monks NR, Pardee AB. Targeting the NF-kappa B pathway in estrogen receptor negative MDA-MB-231 breast cancer cells using small inhibitory RNAs. J Cell Biochem 2006;98:221-33.
77. Nadiminty N, Dutt S, Tepper C, Gao AC. Microarray analysis reveals potential target genes of NF-kappaB2/p52 in LNCaP prostate cancer cells. Prostate 2010;70:276-87.
78. Eastham MA, Kattan MW, Fearn P, et al. Local progression among men with conservatively treated localized prostate cancer: results from the Transatlantic Prostate Group. Eur Urol 2008;53:347-54.
79. van Diest PJ, van Dam P, Henzen-Logmans SC, et al. A scoring system for immunohistochemical staining: consensus report of the task force for basic research of the EORTC-GCCG. J Clin Pathol 1997; 50:801-4.
80. Berney DM, Gopalan A, Kudahetti S, et al. Ki-67 and outcome in clinically localised prostate cancer: analysis of conservatively treated prostate cancer patients from the Trans-Atlantic Prostate Group study. Br J Cancer 2009;100:888-93.
81. Smith P, Rhodes NP, Beesley C, Ke Y, Foster CS. Prostatic stromal cell phenotype is directly modulated by norepinephrine. Urology 1998;51:663-70.
82. Jing C, Beesley C, Foster CS, et al. Identification of the messenger RNA for human cutaneous fatty acid-binding protein as a metastasisinducer. Cancer Res 2000;60:2390-8.
83. Olsen MW, Ley CD, Junker N, Hansen AJ, Lund EL, Kristiansen PE. Angiopoietin-4 inhibits angiogenesis and reduces interstitial fluid pressure. Neoplasia 2006;8:364-72.
84. Steck PA, Nicolson GL. Cell surface properties of spontaneously metastasizing rat mammary adenocarcinoma cell clones. Transplant Proc 1984;16:355-60.
85. Guo HB, Lee I, Bryan BT, Pierce M. Deletion of mouse embryo fibroblast N-acetylglucosaminyltransferase V stimulates alpha5beta1 integrin expression mediated by the protein kinase C signaling pathway. J Biol Chem 2005;280:8332-42.
86. Shaaban AM, O'Neill PA, Davies MPA, et al. Declining estrogen receptor beta expression defines malignant progression of human breast neoplasia. Am J Surg Pathol 2003;27:1502-12.
87. Bashir I, Sikora K, Foster CS. Cell-surface oligosaccharides expressed by phenotypically distinct sublines of the Dunning 3327 rat prostate cancer. Biochem Soc Trans 1990;18:968-9.
88. Sharpe JC, Abel PD, Gilbertson JA, Brawn P, Foster CS. Modulated expression of human leukocyte antigen class I and class II determinants in hyperplastic and malignant human prostatic epithelium. Br J Urol 1994;74:609-16.
89. Ritchie ME, Silver J, Oshlack A, et al. A comparison of background correction methods for two-colour microarrays. Bioinformatics 2007;23:2700-7.
90. Smyth GK, Speed T. Normalization of cDNA microarray data. Methods 2003;31:265-73.
91. Gentleman RC, Carey VJ, Bates DM, et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 2004;5:R80.
92. Smyth G. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004;3:Article 3.
93. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Stat Soc Ser B 1995;57:289-300.
94. Falcon S, Gentleman RC. Using GOstats to test gene lists for GO term association. Bioinformatics 2007;23:257-8.