The kallikrein 14 gene is down-regulated by androgen receptor signalling and harbours genetic variation that is associated with prostate tumour aggressiveness

Biological Chemistry

Volumn 393, Issue 5, 2012, Pages 403-412

  Lose, Felicity ^a,b   Lawrence, Mitchell G ^b,f   Srinivasan, Srilakshmi ^b   O'Mara, Tracy ^a,b   Marquart, Louise ^a   Chambers, Suzanne ^c,d,e   Gardiner, Robert A ^e   Aitken, Joanne F ^c,d   Spurdle, Amanda B ^a   Batra, Jyotsna ^a,b   Clements, Judith A ^b  

^a QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^b QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

^c GRIFFITH UNIVERSITY   (Australia)

^d CANCER COUNCIL QUEENSLAND   (Australia)

^e UNIVERSITY OF QUEENSLAND   (Australia)

^f MONASH UNIVERSITY   (Australia)

Author keywords

Androgen regulation; Gleason score; Kallikreins; KLK14; Prostate cancer; Single nucleotide polymorphisms (SNPs)

Indexed keywords

ANDROGEN RECEPTOR; KALLIKREIN; KALLIKREIN 14; UNCLASSIFIED DRUG;

CANCER CELL; CANCER PROGNOSIS; CANCER RISK; CONFERENCE PAPER; CONTROLLED STUDY; DISEASE COURSE; DOWN REGULATION; GENE EXPRESSION; GENE LOCUS; GENETIC VARIABILITY; HUMAN; HUMAN CELL; IN VITRO STUDY; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; PROSTATE CANCER; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM;

ADULT; AGED; AGED, 80 AND OVER; CASE-CONTROL STUDIES; CELL LINE, TUMOR; DOWN-REGULATION; GENETIC PREDISPOSITION TO DISEASE; HUMANS; KALLIKREINS; MALE; MIDDLE AGED; POLYMORPHISM, SINGLE NUCLEOTIDE; PROSTATIC NEOPLASMS; RECEPTORS, ANDROGEN; SIGNAL TRANSDUCTION;

EID: 84859843770     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/hsz-2011-0268     Document Type: Conference Paper

References (69)

1. Adzhubei, I.A., Schmidt, S., Peshkin, L., Ramensky, V.E., Gerasimova, A., Bork, P., Kondrashov, A.S., and Sunyaev, S.R. (2010). A method and server for predicting damaging missense mutations. Nat. Methods. 7, 248-249.
2. Akamatsu, S., Takata, R., Ashikawa, K., Hosono, N., Kamatani, N., Fujioka, T., Ogawa, O., Kubo, M., Nakamura, Y., and Nakagawa, H. (2010). A functional variant in NKX3.1 associated with prostate cancer susceptibility down-regulates NKX3.1 expression. Hum. Mol. Genet. 19, 4265-4272.
3. Amigo, J., Salas, A., Phillips, C., and Carracedo, A. (2008). SPSmart: adapting population based SNP genotype databases for fast and comprehensive web access. BMC Bioinformatics 9, 428.
4. Baade, P.D., Aitken, J.F., Ferguson, M., Gardiner, R.A., and Chambers, S.K. (2010). Diagnostic and treatment pathways for men with prostate cancer in Queensland: investigating spatial and demographic inequalities. BMC Cancer 10, 452.
5. Barrett, J.C., Fry, B., Maller, J., and Daly, M.J. (2005). Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21, 263-265. (Pubitemid 40202029)
6. Bendtsen, J.D., Nielsen, H., Von Heijne, G., and Brunak, S. (2004). Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340, 783-795. (Pubitemid 38829638)
7. Bolton, E.C., So, A.Y., Chaivorapol, C., Haqq, C.M., Li, H., and Yamamoto, K.R. (2007). Cell- and gene-specific regulation of primary target genes by the androgen receptor. Genes Dev. 21, 2005-2017. (Pubitemid 47267287)
8. Borgono, C.A., Grass, L., Soosaipillai, A., Yousef, G.M., Petraki, C.D., Howarth, D.H., Fracchioli, S., Katsaros, D., and Diamandis, E.P. (2003). Human kallikrein 14: a new potential biomarker for ovarian and breast cancer. Cancer Res. 63, 9032-9041. (Pubitemid 38064085)
9. Borgono, C.A., Michael, I.P., Shaw, J.L., Luo, L.Y., Ghosh, M.C., Soosaipillai, A., Grass, L., Katsaros, D., and Diamandis, E.P. (2007). Expression and functional characterization of the cancer- related serine protease, human tissue kallikrein 14. J. Biol. Chem. 282, 2405-2422. (Pubitemid 47076761)
10. Brattsand, M., Stefansson, K., Lundh, C., Haasum, Y., and Egelrud, T. (2005). A proteolytic cascade of kallikreins in the stratum corneum. J. Invest. Dermatol. 124, 198-203. (Pubitemid 40100969)
11. Brown, M.B. and Forsythe, A.B. (1974). Robust tests for equality of variances. J. Am. Stat. Assoc. 69, 364-367.
12. Clegg, N., Eroglu, B., Ferguson, C., Arnold, H., Moorman, A., and Nelson, P.S. (2002). Digital expression profiles of the prostate androgen-response program. J. Steroid. Biochem. Mol. Biol. 80, 13-23. (Pubitemid 34178407)
13. Clements, J.A., Willemsen, N.M., Myers, S.A., and Dong, Y. (2004). The tissue kallikrein family of serine proteases: functional roles in human disease and potential as clinical biomarkers. Crit. Rev. Clin. Lab. Sci. 41, 265-312. (Pubitemid 38888061)
14. Duggan, D., Zheng, S.L., Knowlton, M., Benitez, D., Dimitrov, L., Wiklund, F., Robbins, C., Isaacs, S.D., Cheng, Y., Li, G., et al. (2007). Two genome-wide association studies of aggressive prostate cancer implicate putative prostate tumor suppressor gene DAB2IP. J. Natl. Cancer Inst. 99, 1836-1844. (Pubitemid 351767196)
15. Eeles, R.A., Kote-Jarai, Z., Giles, G.G., Olama, A.A., Guy, M., Jugurnauth, S.K., Mulholland, S., Leongamornlert, D.A., Edwards, S.M., Morrison, J., et al. (2008). Multiple newly identified loci associated with prostate cancer susceptibility. Nat Genet. 40, 316-321. (Pubitemid 351311772)
16. Eeles, R.A., Kote-Jarai, Z., Al Olama, A.A., Giles, G.G., Guy, M., Severi, G., Muir, K., Hopper, J.L., Henderson, B.E., Haiman, C.A., et al. (2009). Identification of seven new prostate cancer susceptibility loci through a genome-wide association study. Nat. Genet. 41, 1116-1121.
17. Emami, N. and Diamandis, E.P. (2008). Human kallikrein-related peptidase 14 (KLK14) is a new activator component of the KLK proteolytic cascade. Possible function in seminal plasma and skin. J. Biol. Chem. 283, 3031-3041.
18. Emami, N. and Diamandis, E.P. (2010). Potential role of multiple members of the kallikrein-related peptidase family of serine proteases in activating latent TGFβ1 in semen. Biol. Chem. 391, 85-95.
19. Emami, N., Deperthes, D., Malm, J., and Diamandis, E.P. (2008). Major role of human KLK14 in seminal clot liquefaction. J. Biol. Chem. 283, 19561-19569.
20. Fitzgerald, L.M., Kwon, E.M., Conomos, M.P., Kolb, S., Holt, S.K., Levine, D., Feng, Z., Ostrander, E.A., and Stanford, J.L. (2011). Genome-wide association study identifies a genetic variant associated with risk for more aggressive prostate cancer. Cancer Epidemiol. Biomarkers Prev. 20, 1196-1203.
21. Goard, C.A., Bromberg, I.L., Elliott, M.B., and Diamandis, E.P. (2007). A consolidated catalogue and graphical annotation of dbSNP polymorphisms in the human tissue kallikrein (KLK) locus. Mol. Oncol. 1, 303-312. (Pubitemid 350181644)
22. Grabe, N. 2000. AliBaba2.1 [Online]. Available: www.gene-regulation. com/pub/programs/alibaba2/index.html [Accessed August 2011].
23. Gratio, V., Loriot, C., Virca, G.D., Oikonomopoulou, K., Walker, F., Diamandis, E.P., Hollenberg, M.D., and Darmoul, D. (2011). Kallikrein-related peptidase 14 acts on proteinase-activated receptor 2 to induce signaling pathway in colon cancer cells. Am. J. Pathol. 179, 2625-2636.
24. Grosse, A., Bartsch, S., and Baniahmad, A. (2012). Androgen receptor- mediated gene repression. Mol. Cell Endocrinol. 352, 46-56.
25. Hodgson, M.C., Astapova, I., Hollenberg, A.N., and Balk, S.P. (2007). Activity of androgen receptor antagonist bicalutamide in prostate cancer cells is independent of NCoR and SMRT corepressors. Cancer Res. 67, 8388-8395. (Pubitemid 47395178)
26. Holzbeierlein, J., Lal, P., Latulippe, E., Smith, A., Satagopan, J., Zhang, L., Ryan, C., Smith, S., Scher, H., Scardino, P., et al. (2004). Gene expression analysis of human prostate carcinoma during hormonal therapy identifies androgen-responsive genes and mechanisms of therapy resistance. Am. J. Pathol. 164, 217-227. (Pubitemid 38364606)
27. Hooper, J.D., Bui, L.T., Rae, F.K., Harvey, T.J., Myers, S.A., Ashworth, L.K., and Clements, J.A. (2001). Identification and characterization of KLK14, a novel kallikrein serine protease gene located on human chromosome 19q13.4 and expressed in prostate and skeletal muscle. Genomics 73, 117-122. (Pubitemid 32382394)
28. Jia, L., Shen, H.C., Wantroba, M., Khalid, O., Liang, G., Wang, Q., Gentzschein, E., Pinski, J.K., Stanczyk, F.Z., Jones, P.A., et al. (2006). Locus-wide chromatin remodeling and enhanced androgen receptor-mediated transcription in recurrent prostate tumor cells. Mol. Cell. Biol. 26, 7331-7341. (Pubitemid 44477706)
29. Jia, L., Berman, B.P., Jariwala, U., Yan, X., Cogan, J.P., Walters, A., Chen, T., Buchanan, G., Frenkel, B., and Coetzee, G.A. (2008). Genomic androgen receptor-occupied regions with different functions, defined by histone acetylation, coregulators and transcriptional capacity. PLoS ONE 3, e3645.
30. Johnson, A.D., Handsaker, R.E., Pulit, S.L., Nizzari, M.M., O'Donnell, C.J., and De Bakker, P.I. (2008). SNAP: a webbased tool for identification and annotation of proxy SNPs using HapMap. Bioinformatics 24, 2938-2939.
31. Kader, A.K., Sun, J., Isaacs, S.D., Wiley, K.E., Yan, G., Kim, S.T., Fedor, H., Demarzo, A.M., Epstein, J.I., Walsh, P.C., et al. (2009). Individual and cumulative effect of prostate cancer riskassociated variants on clinicopathologic variables in 5,895 prostate cancer patients. Prostate 69, 1195-1205.
32. Kennedy, B.A., Gao, W., Huang, T.H., and Jin, V.X. (2010). HRTBLDb: an informative data resource for hormone receptors target binding loci. Nucleic Acids Res. 38, D676-681.
33. Klein, R.J., Hallden, C., Cronin, A.M., Ploner, A., Wiklund, F., Bjartell, A.S., Stattin, P., Xu, J., Scardino, P.T., Offit, K., et al. (2010). Blood biomarker levels to aid discovery of cancer-related single-nucleotide polymorphisms: kallikreins and prostate cancer. Cancer Prev. Res. (Phila.) 3, 611-619.
34. Kojima, S., Mulholland, D.J., Ettinger, S., Fazli, L., Nelson, C.C., and Gleave, M.E. (2006). Differential regulation of IGFBP-3 by the androgen receptor in the lineage-related androgen-dependent LNCaP and androgen-independent C4-2 prostate cancer models. Prostate 66, 971-986. (Pubitemid 43853069)
35. Kote-Jarai, Z., Amin Al Olama, A., Leongamornlert, D., Tymrakiewicz, M., Saunders, E., Guy, M., Giles, G.G., Severi, G., Southey, M., Hopper, J.L., et al. (2011). Identification of a novel prostate cancer susceptibility variant in the KLK3 gene transcript. Hum. Genet. 129, 687-694.
36. Lai, J., Kedda, M.A., Hinze, K., Smith, R.L., Yaxley, J., Spurdle, A.B., Morris, C.P., Harris, J., and Clements, J.A. (2007). PSA/KLK3 AREI promoter polymorphism alters androgen receptor binding and is associated with prostate cancer susceptibility. Carcinogenesis 28, 1032-1039. (Pubitemid 47072187)
37. Lawrence, M.G., Lai, J., and Clements, J.A. (2010). Kallikreins on steroids: structure, function, and hormonal regulation of prostatespecific antigen and the extended kallikrein locus. Endocr. Rev. 31, 407-446.
38. Lin, D.W., Fitzgerald, L.M., Fu, R., Kwon, E.M., Zheng, S.L., Kolb, S., Wiklund, F., Stattin, P., Isaacs, W.B., Xu, J., et al. (2011). Genetic variants in the LEPR, CRY1, RNASEL, IL4, and ARVCF genes are prognostic markers of prostate cancerspecific mortality. Cancer Epidemiol. Biomarkers Prev. 20, 1928-1936.
39. Lose, F., Nagle, C.M., O'mara, T., Batra, J., Bolton, K.L., Song, H., Ramus, S.J., Gentry-Maharaj, A., Menon, U., Gayther, S.A., et al. (2010). Vascular endothelial growth factor gene polymorphisms and ovarian cancer survival. Gynecol. Oncol. 119, 479-483.
40. Lose, F., Batra, J., O'mara, T., Fahey, P., Marquart, L., Eeles, R.A., Easton, D.F., Al Olama, A.A., Kote-Jarai, Z., Guy, M., et al. (2011). Common variation in kallikrein genes KLK5, KLK6, KLK12, and KLK13 and risk of prostate cancer and tumor aggressiveness. Urol Oncol.
41. Lubahn, J., Berndt, S.I., Jin, C.H., Klim, A., Luly, J., Wu, W.S., Isaacs, S., Wiley, K., Isaacs, W.B., Suarez, B.K., et al. (2010). Association of CASP8 D302H polymorphism with reduced risk of aggressive prostate carcinoma. Prostate 70, 646-653.
42. Mavridis, K. and Scorilas, A. (2010). Prognostic value and biological role of the kallikrein-related peptidases in human malignancies. Future Oncol. 6, 269-285.
43. Mostaghel, E.A., Page, S.T., Lin, D.W., Fazli, L., Coleman, I.M., True, L.D., Knudsen, B., Hess, D.L., Nelson, C.C., Matsumoto, A.M., et al. (2007). Intraprostatic androgens and androgen-regulated gene expression persist after testosterone suppression: therapeutic implications for castration-resistant prostate cancer. Cancer Res. 67, 5033-5041. (Pubitemid 46910214)
44. Nakai, K. and Horton, P. (1999). PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization. Trends Biochem. Sci. 24, 34-36.
45. Ng, P.C. and Henikoff, S. (2001). Predicting deleterious amino acid substitutions. Genome Res. 11, 863-874. (Pubitemid 32447869)
46. Oikonomopoulou, K., Hansen, K.K., Saifeddine, M., Vergnolle, N., Tea, I., Blaber, M., Blaber, S.I., Scarisbrick, I., Diamandis, E.P., and Hollenberg, M.D. (2006). Kallikrein-mediated cell signalling: targeting proteinase-activated receptors (PARs). Biol. Chem. 387, 817-824. (Pubitemid 43964807)
47. Oon, S.F., Pennington, S.R., Fitzpatrick, J.M., and Watson, R.W. (2011). Biomarker research in prostate cancer - towards utility, not futility. Nat. Rev. Urol. 8, 131-138.
48. Paliouras, M. and Diamandis, E.P. (2007). Coordinated steroid hormone-dependent and independent expression of multiple kallikreins in breast cancer cell lines. Breast Cancer Res. Treat. 102, 7-18. (Pubitemid 46294962)
49. Paliouras, M. and Diamandis, E.P. (2008a). Androgens act synergistically to enhance estrogen-induced upregulation of human tissue kallikreins 10, 11, and 14 in breast cancer cells via a membrane bound androgen receptor. Mol. Oncol. 1, 413-424.
50. Paliouras, M. and Diamandis, E.P. (2008b). Intracellular signaling pathways regulate hormone-dependent kallikrein gene expression. Tumour Biol. 29, 63-75.
51. Parikh, H., Wang, Z., Pettigrew, K.A., Jia, J., Daugherty, S., Yeager, M., Jacobs, K.B., Hutchinson, A., Burdett, L., Cullen, M., et al. (2011). Fine mapping the KLK3 locus on chromosome 19q13.33 associated with prostate cancer susceptibility and PSA levels. Hum. Genet. 129, 675-685.
52. Prescott, J., Jariwala, U., Jia, L., Cogan, J.P., Barski, A., Pregizer, S., Shen, H.C., Arasheben, A., Neilson, J.J., Frenkel, B., et al. (2007). Androgen receptor-mediated repression of novel target genes. Prostate 67, 1371-1383. (Pubitemid 47435785)
53. Rabien, A., Fritzsche, F., Jung, M., Diamandis, E.P., Loening, S.A., Dietel, M., Jung, K., Stephan, C., and Kristiansen, G. (2008). High expression of KLK14 in prostatic adenocarcinoma is associated with elevated risk of prostate-specific antigen relapse. Tumour Biol. 29, 1-8. (Pubitemid 351733214)
54. Rajapakse, S. and Takahashi, T. (2007). Expression and enzymatic characterization of recombinant human kallikrein 14. Zool. Sci. 24, 774-780. (Pubitemid 350076993)
55. Riva, A. and Kohane, I.S. (2004). A SNP-centric database for the investigation of the human genome. BMC Bioinformatics 5, 33.
56. Sandelin, A. and Wasserman, W.W. (2005). Prediction of nuclear hormone receptor response elements. Mol. Endocrinol. 19, 595-606. (Pubitemid 40349434)
57. Sankpal, U.T., Goodison, S., Abdelrahim, M., and Basha, R. (2011). Targeting sp1 transcription factors in prostate cancer therapy. Med. Chem. 7, 518-525.
58. Shaw, J.L. and Diamandis, E.P. (2008). Regulation of human tissue kallikrein-related peptidase expression by steroid hormones in 32 cell lines. Biol. Chem. 389, 1409-1419.
59. Sherry, S.T., Ward, M.H., Kholodov, M., Baker, J., Phan, L., Smigielski, E.M., and Sirotkin, K. (2001). dbSNP: the NCBI database of genetic variation. Nucleic Acids Res. 29, 308-311. (Pubitemid 32054478)
60. Smith, P.J., Zhang, C., Wang, J., Chew, S.L., Zhang, M.Q., and Krainer, A.R. (2006). An increased specificity score matrix for the prediction of SF2/ASF-specific exonic splicing enhancers. Hum. Mol. Genet. 15, 2490-2508. (Pubitemid 44288702)
61. Stefansson, K., Brattsand, M., Roosterman, D., Kempkes, C., Bocheva, G., Steinhoff, M., and Egelrud, T. (2008). Activation of proteinase-activated receptor-2 by human kallikrein-related peptidases. J. Invest. Dermatol. 128, 18-25. (Pubitemid 350249381)
62. Thompson, V.C., Morris, T.G., Cochrane, D.R., Cavanagh, J., Wafa, L.A., Hamilton, T., Wang, S., Fazli, L., Gleave, M.E., and Nelson, C.C. (2006). Relaxin becomes upregulated during prostate cancer progression to androgen independence and is negatively regulated by androgens. Prostate 66, 1698-1709. (Pubitemid 44893896)
63. Veveris-Lowe, T.L., Kruger, S.J., Walsh, T., Gardiner, R.A., and Clements, J.A. (2007). Seminal fluid characterization for male fertility and prostate cancer: kallikrein-related serine proteases and whole proteome approaches. Semin. Thromb. Hemost. 33, 87-99. (Pubitemid 46184036)
64. Witte, J.S. (2009). Prostate cancer genomics: towards a new understanding. Nat. Rev. Genet. 10, 77-82.
65. Yeager, M., Orr, N., Hayes, R.B., Jacobs, K.B., Kraft, P., Wacholder, S., Minichiello, M.J., Fearnhead, P., Yu, K., Chatterjee, N., et al. (2007). Genome-wide association study of prostate cancer identifies a second risk locus at 8q24. Nat. Genet. 39, 645-649. (Pubitemid 46676108)
66. Yoon, H., Laxmikanthan, G., Lee, J., Blaber, S.I., Rodriguez, A., Kogot, J.M., Scarisbrick, I.A., and Blaber, M. (2007). Activation profiles and regulatory cascades of the human kallikrein-related peptidases. J. Biol. Chem. 282, 31852-31864. (Pubitemid 350106429)
67. Yousef, G.M., Magklara, A., Chang, A., Jung, K., Katsaros, D., and Diamandis, E.P. (2001). Cloning of a new member of the human kallikrein gene family, KLK14, which is down-regulated in different malignancies. Cancer Res. 61, 3425-3431. (Pubitemid 32695036)
68. Yousef, G.M., Fracchioli, S., Scorilas, A., Borgono, C.A., Iskander, L., Puopolo, M., Massobrio, M., Diamandis, E.P., and Katsaros, D. (2003a). Steroid hormone regulation and prognostic value of the human kallikrein gene 14 in ovarian cancer. Am. J. Clin. Pathol. 119, 346-355. (Pubitemid 37047856)
69. Yousef, G.M., Stephan, C., Scorilas, A., Ellatif, M.A., Jung, K., Kristiansen, G., Jung, M., Polymeris, M.E., and Diamandis, E.P. (2003b). Differential expression of the human kallikrein gene 14 (KLK14) in normal and cancerous prostatic tissues. Prostate 56, 287-292. (Pubitemid 36988749)