Cancer Letters
Volume 224, Issue 1 , Pages 1-22 , 16 June 2005

Human tissue kallikrein gene family: applications in cancer

  • Christina V. Obiezu

      Affiliations

    • Department of Pathology and Laboratory Medicine, Mount Sinai Hospital, 600 University Avenue, Toronto, Ont., Canada M5G 1X5
    • Department of Laboratory Medicine and Pathobiology, University of Toronto, 100 College Street, Toronto, Ont., Canada M5G 1L5
    • ,
  • Eleftherios P. Diamandis

      Affiliations

    • Department of Pathology and Laboratory Medicine, Mount Sinai Hospital, 600 University Avenue, Toronto, Ont., Canada M5G 1X5
    • Department of Laboratory Medicine and Pathobiology, University of Toronto, 100 College Street, Toronto, Ont., Canada M5G 1L5
    • Corresponding Author InformationCorresponding author. Address: Department of Pathology and Laboratory Medicine, Mount Sinai Hospital, 600 University Avenue, Toronto, Ont., Canada M5G 1X5. Tel.: +1 416 586 8443; fax: +1 416 586 8628.

Received 7 September 2004 ,Accepted 15 September 2004.

References 

  1. Walker B, Lynas JF. Strategies for the inhibition of serine proteases. Cell. Mol. Life Sci. 2001;58:596–624
  2. Rawlings ND, Barrett AJ. Evolutionary families of peptidases. Biochem. J. 1993;290(Pt 1):205–218
  3. Puente XS, Sanchez LM, Overall CM, Lopez-Otin C. Human and mouse proteases: a comparative genomic approach. Nat. Rev. Genet. 2003;4:544–558
  4. Puente XS, Lopez-Otin C. A genomic analysis of rat proteases and protease inhibitors. Genome Res. 2004;14:609–622
  5. Abbott A. Biologists take degrading route to tackle cancer. Nature. 2004;429:794
  6. Schedlich LJ, Bennetts BH, Morris BJ. Primary structure of a human glandular kallikrein gene. DNA. 1987;6:429–437
  7. Riegman PH, Vlietstra RJ, Klaassen P, van der Korput JA, Geurts van Kessel A, Romijn JC, et al. The prostate-specific antigen gene and the human glandular kallikrein-1 gene are tandemly located on chromosome 19. Fed. Eur. Biochem. Soc. Lett. 1989;247:123–126
  8. Fiedler F, Betz G, Hinz H, Lottspeich F, Raidoo DM, Bhoola KD. Not more than three tissue kallikreins identified from organs of the guinea pig. Biol. Chem. 1999;380:63–73
  9. Murray SR, Chao J, Chao L. Evolution of the kallikrein gene family. Agents Actions Suppl. 1992;38:26–33
  10. Venter JC, Adams MD, Myers EW, Li PW, Mural RJ, Sutton GG, et al. The sequence of the human genome. Science. 2001;291:1304–1351
  11. Liu XL, Wazer DE, Watanabe K, Band V. Identification of a novel serine protease-like gene, the expression of which is down-regulated during breast cancer progression. Cancer Res. 1996;56:3371–3379
  12. Anisowicz A, Sotiropoulou G, Stenman G, Mok SC, Sager R. A novel protease homolog differentially expressed in breast and ovarian cancer. Mol. Med. 1996;2:624–636
  13. Little SP, Dixon EP, Norris F, Buckley W, Becker GW, Johnson M, et al. Zyme, a novel and potentially amyloidogenic enzyme cDNA isolated from Alzheimer's disease brain. J. Biol. Chem. 1997;272:25135–25142
  14. Yamashiro K, Tsuruoka N, Kodama S, Tsujimoto M, Yamamura Y, Tanaka T, et al. Molecular cloning of a novel trypsin-like serine protease (neurosin) preferentially expressed in brain. Biochim. Biophys. Acta. 1997;1350:11–14
  15. Yoshida S, Taniguchi M, Hirata A, Shiosaka S. Sequence analysis and expression of human neuropsin cDNA and gene. Gene. 1998;213:9–16
  16. Underwood LJ, Tanimoto H, Wang Y, Shigemasa K, Parmley TH, O'Brien TJ. Cloning of tumor-associated differentially expressed gene-14, a novel serine protease overexpressed by ovarian carcinoma. Cancer Res. 1999;59:4435–4439
  17. Yoshida S, Taniguchi M, Suemoto T, Oka T, He X, Shiosaka S. cDNA cloning and expression of a novel serine protease, TLSP. Biochim. Biophys. Acta. 1998;1399:225–228
  18. Mitsui S, Yamada T, Okui A, Kominami K, Uemura H, Yamaguchi N. A novel isoform of a kallikrein-like protease, TLSP/hippostasin (PRSS20), is expressed in the human brain and prostate. Biochem. Biophys. Res. Commun. 2000;272:205–211
  19. Hansson L, Stromqvist M, Backman A, Wallbrandt P, Carlstein A, Egelrud T. Cloning, expression, and characterization of stratum corneum chymotryptic enzyme. A skin-specific human serine proteinase. J. Biol. Chem. 1994;269:19420–19426
  20. Brattsand M, Egelrud T. Purification, molecular cloning, and expression of a human stratum corneum trypsin-like serine protease with possible function in desquamation. J. Biol. Chem. 1999;274:30033–30040
  21. Yousef GM, Chang A, Scorilas A, Diamandis EP. Genomic organization of the human kallikrein gene family on chromosome 19q13.3–q13.4. Biochem. Biophys. Res. Commun. 2000;276:125–133
  22. Yousef GM, Luo LY, Diamandis EP. Identification of novel human kallikrein-like genes on chromosome 19q13.3–q13.4. Anticancer Res. 1999;19:2843–2852
  23. Yousef GM, Diamandis EP. The expanded human kallikrein gene family: locus characterization and molecular cloning of a new member, KLK-L3 (KLK9). Genomics. 2000;65:184–194
  24. Yousef GM, Borgono CA, Michael IP, Diamandis EP. Cloning of a novel kallikrein pseudogene. Tumour Biol. 2004;in press
  25. Grimwood J, Gordon LA, Olsen A, Terry A, Schmutz J, Lamerdin J, et al. The DNA sequence and biology of human chromosome 19. Nature. 2004;428:529–535
  26. Yousef GM, Kopolovic AD, Elliott MB, Diamandis EP. Genomic overview of serine proteases. Biochim. Biophys. Acta. 2003;305:28–36
  27. Diamandis EP, Yousef GM, Luo LY, Magklara A, Obiezu CV. The new human kallikrein gene family: implications in carcinogenesis. Trends Endocrinol. Metab. 2000;11:54–60
  28. Yousef GM, Diamandis M, Jung K, Diamandis EP. Molecular cloning of a novel human acid phosphatase gene (acpt) that is highly expressed in the testis. Genomics. 2001;74:385–395
  29. Yousef GM, Borgono CA, Michael IP, Davidian C, Stephan C, Jung K, et al. Molecular cloning of a new gene which is differentially expressed in breast and prostate cancers. Tumour Biol. 2004;25(3):122–133
  30. Foussias G, Yousef GM, Diamandis EP. Identification and molecular characterization of a novel member of the siglec family (SIGLEC9). Genomics. 2000;67:171–178
  31. Olsson AY, Lilja H, Lundwall A. Taxon-specific evolution of glandular kallikrein genes and identification of a progenitor of prostate-specific antigen. Genomics. 2004;84:147–156
  32. Olsson AY, Lundwall A. Organization and evolution of the glandular kallikrein locus in Mus musculus. Biochem. Biophys. Res. Commun. 2002;299:305–311
  33. Evans BA, Drinkwater CC, Richards RI. Mouse glandular kallikrein genes. Structure and partial sequence analysis of the kallikrein gene locus. J. Biol. Chem. 1987;262:8027–8034
  34. Borgono CA, Michael IP, Diamandis EP. Human tissue kallikreins: physiologic roles and applications in cancer. Mol. Cancer Res. 2004;2:257–280
  35. Diamandis EP, Yousef GM, Olsson AY. An update on human and mouse glandular kallikreins. Clin. Biochem. 2004;37:258–260
  36. Yousef GM, Diamandis EP. An overview of the kallikrein gene families in humans and other species: emerging candidate tumour markers. Clin. Biochem. 2003;36:443–452
  37. Yousef GM, Diamandis EP. Human kallikreins: common structural features, sequence analysis and evolution. Curr. Genom. 2003;4:147–165
  38. Yousef GM, Diamandis EP. The new human tissue kallikrein gene family: structure, function, and association to disease. Endocrinol. Rev. 2001;22:184–204
  39. Betz SF. Disulfide bonds and the stability of globular proteins. Protein Sci. 1993;2:1551–1558
  40. Rittenhouse HG, Finlay JA, Mikolajczyk SD, Partin AW. Human Kallikrein 2 (hK2) and prostate-specific antigen (PSA): two closely related, but distinct, kallikreins in the prostate. Crit. Rev. Clin. Lab. Sci. 1998;35:275–368
  41. Diamandis EP, Yousef GM, Clements J, Ashworth LK, Yoshida S, Egelrud T, et al. New nomenclature for the human tissue kallikrein gene family. Clin. Chem. 2000;46:1855–1858
  42. Clements JA. The glandular kallikrein family of enzymes: tissue-specific expression and hormonal regulation. Endocrinol. Rev. 1989;10:393–419
  43. Xiong W, Wang J, Chao L, Chao J. Tissue-specific expression and promoter analyses of the human tissue kallikrein gene in transgenic mice. Biochem. J. 1997;325(Pt 1):111–116
  44. Chapdelaine P, Paradis G, Tremblay RR, Dube JY. High level of expression in the prostate of a human glandular kallikrein mRNA related to prostate-specific antigen. Fed. Eur. Biochem. Soc. Lett. 1988;236:205–208
  45. Henttu P, Lukkarinen O, Vihko P. Expression of the gene coding for human prostate-specific antigen and related hGK-1 in benign and malignant tumors of the human prostate. Int. J. Cancer. 1990;45:654–660
  46. Henttu P, Vihko P. Prostate-specific antigen and human glandular kallikrein: two kallikreins of the human prostate. Ann. Med. 1994;26:157–164
  47. Nelson PS, Gan L, Ferguson C, Moss P, Gelinas R, Hood L, et al. Molecular cloning and characterization of prostase, an androgen-regulated serine protease with prostate-restricted expression. Proc. Natl Acad. Sci. USA. 1999;96:3114–3119
  48. Yousef GM, Obiezu CV, Luo LY, Black MH, Diamandis EP. Prostase/KLK-L1 is a new member of the human kallikrein gene family, is expressed in prostate and breast tissues, and is hormonally regulated. Cancer Res. 1999;59:4252–4256
  49. Aumuller G, Seitz J, Lilja H, Abrahamsson PA, von der Kammer H, Scheit KH. Species- and organ-specificity of secretory proteins derived from human prostate and seminal vesicles. Prostate. 1990;17:31–40
  50. Wang MC, Papsidero LD, Kuriyama M, Valenzuela LA, Murphy GP, Chu TM. Prostate antigen: a new potential marker for prostatic cancer. Prostate. 1981;2:89–96
  51. Wang MC, Valenzuela LA, Murphy GP, Chu TM. Purification of a human prostate specific antigen. Invest. Urol. 1979;17:159–163
  52. Cumming AD, Walsh T, Wojtacha D, Fleming S, Thomson D, Jenkins DA. Expression of tissue kallikrein in human kidney. Clin. Sci. (Colch.). 1994;87:5–11
  53. Diamandis EP, Yousef GM. Human tissue kallikreins: a family of new cancer biomarkers. Clin. Chem. 2002;48:1198–1205
  54. Clements J, Mukhtar A, Ehrlich A, Yap B. Glandular kallikrein gene expression in the human uterus. Braz. J. Med. Biol. Res. 1994;27:1855–1863
  55. Miller DH, Lindley JG, Margolius HS. Tissue kallikrein levels and synthesis rates are not changed by an acute physiological dose of aldosterone. Proc. Soc. Exp. Biol. Med. 1985;180:121–125
  56. Miller DH, Chao J, Margolius HS. Tissue kallikrein synthesis and its modification by testosterone or low dietary sodium. Biochem. J. 1984;218:37–43
  57. Guo Y, Pili R, Passaniti A. Regulation of prostate-specific antigen gene expression in LNCaP human prostatic carcinoma cells by growth, dihydrotestosterone, and extracellular matrix. Prostate. 1994;24:1–10
  58. Montgomery BT, Young CY, Bilhartz DL, Andrews PE, Prescott JL, Thompson NF, et al. Hormonal regulation of prostate-specific antigen (PSA) glycoprotein in the human prostatic adenocarcinoma cell line, LNCaP. Prostate. 1992;21:63–73
  59. Young CY, Andrews PE, Montgomery BT, Tindall DJ. Tissue-specific and hormonal regulation of human prostate-specific glandular kallikrein. Biochemistry. 1992;31:818–824
  60. Young CY, Andrews PE, Tindall DJ. Expression and androgenic regulation of human prostate-specific kallikreins. J. Androl. 1995;16:97–99
  61. Zarghami N, Grass L, Diamandis EP. Steroid hormone regulation of prostate-specific antigen gene expression in breast cancer. Br. J. Cancer. 1997;75:579–588
  62. Cleutjens KB, van Eekelen CC, van der Korput HA, Brinkmann AO, Trapman J. Two androgen response regions cooperate in steroid hormone regulated activity of the prostate-specific antigen promoter. J. Biol. Chem. 1996;271:6379–6388
  63. Cleutjens KB, van der Korput HA, van Eekelen CC, van Rooij HC, Faber PW, Trapman J. An androgen response element in a far upstream enhancer region is essential for high, androgen-regulated activity of the prostate-specific antigen promoter. Mol. Endocrinol. 1997;11:148–161
  64. Riegman PH, Vlietstra RJ, van der Korput JA, Brinkmann AO, Trapman J. The promoter of the prostate-specific antigen gene contains a functional androgen responsive element. Mol. Endocrinol. 1991;5:1921–1930
  65. Murtha P, Tindall DJ, Young CY. Androgen induction of a human prostate-specific kallikrein, hKLK2: characterization of an androgen response element in the 5′ promoter region of the gene. Biochemistry. 1993;32:6459–6464
  66. Cleutjens CB, Steketee K, van Eekelen CC, van der Korput JA, Brinkmann AO, Trapman J. Both androgen receptor and glucocorticoid receptor are able to induce prostate-specific antigen expression, but differ in their growth-stimulating properties of LNCaP cells. Endocrinology. 1997;138:5293–5300
  67. Cleutjens KB, van der Korput HA, Ehren-van Eekelen CC, Sikes RA, Fasciana C, Chung LW, et al. A 6-kb promoter fragment mimics in transgenic mice the prostate-specific and androgen-regulated expression of the endogenous prostate-specific antigen gene in humans. Mol. Endocrinol. 1997;11:1256–1265
  68. Magklara A, Grass L, Diamandis EP. Differential steroid hormone regulation of human glandular kallikrein (hK2) and prostate-specific antigen (PSA) in breast cancer cell lines. Breast Cancer Res. Treat. 2000;59:263–270
  69. Wolf DA, Schulz P, Fittler F. Transcriptional regulation of prostate kallikrein-like genes by androgen. Mol. Endocrinol. 1992;6:753–762
  70. Magklara A, Brown TJ, Diamandis EP. Characterization of androgen receptor and nuclear receptor co-regulator expression in human breast cancer cell lines exhibiting differential regulation of kallikreins 2 and 3. Int. J. Cancer. 2002;100:507–514
  71. Diamandis EP. New diagnostic applications and physiological functions of prostate specific antigen. Scand. J. Clin. Lab. Invest. Suppl. 1995;221:105–112
  72. Jemal A, Tiwari RC, Murray T, Ghafoor A, Samuels A, Ward E, et al. Cancer statistics, 2004. CA Cancer J. Clin. 2004;54:8–29
  73. Dong Y, Kaushal A, Bui L, Chu S, Fuller PJ, Nicklin J, et al. Human kallikrein 4 (KLK4) is highly expressed in serous ovarian carcinomas. Clin. Cancer Res. 2001;7:2363–2371
  74. Obiezu CV, Scorilas A, Katsaros D, Massobrio M, Yousef GM, Fracchioli S, et al. Higher human kallikrein gene 4 (klk4) expression indicates poor prognosis of ovarian cancer patients. Clin. Cancer Res. 2001;7:2380–2386
  75. Kim H, Scorilas A, Katsaros D, Yousef GM, Massobrio M, Fracchioli S, et al. Human kallikrein gene 5 (KLK5) expression is an indicator of poor prognosis in ovarian cancer. Br. J. Cancer. 2001;84:643–650
  76. Dong Y, Kaushal A, Brattsand M, Nicklin J, Clements JA. Differential splicing of KLK5 and KLK7 in epithelial ovarian cancer produces novel variants with potential as cancer biomarkers. Clin. Cancer Res. 2003;9:1710–1720
  77. Kyriakopoulou LG, Yousef GM, Scorilas A, Katsaros D, Massobrio M, Fracchioli S, et al. Prognostic value of quantitatively assessed KLK7 expression in ovarian cancer. Clin. Biochem. 2003;36:135–143
  78. Tanimoto H, Underwood LJ, Shigemasa K, Parmley TH, O'Brien TJ. Increased expression of protease M in ovarian tumors. Tumour Biol. 2001;22:11–18
  79. Ni X, Zhang W, Huang KC, Wang Y, Ng SK, Mok SC, et al. Characterisation of human kallikrein 6/protease M expression in ovarian cancer. Br. J. Cancer. 2004;91:725–731
  80. Santin AD, Zhan F, Bellone S, Palmieri M, Cane S, Bignotti E, et al. Gene expression profiles in primary ovarian serous papillary tumors and normal ovarian epithelium: identification of candidate molecular markers for ovarian cancer diagnosis and therapy. Int. J. Cancer. 2004;112:14–25
  81. Magklara A, Scorilas A, Katsaros D, Massobrio M, Yousef GM, Fracchioli S, et al. The human KLK8 (neuropsin/ovasin) gene: identification of two novel splice variants and its prognostic value in ovarian cancer. Clin. Cancer Res. 2001;7:806–811
  82. Shigemasa K, Tian X, Gu L, Tanimoto H, Underwood LJ, O'Brien TJ, et al. Human kallikrein 8 (hK8/TADG-14) expression is associated with an early clinical stage and favorable prognosis in ovarian cancer. Oncol. Rep. 2004;11:1153–1159
  83. Yousef GM, Kyriakopoulou LG, Scorilas A, Fracchioli S, Ghiringhello B, Zarghooni M, et al. Quantitative expression of the human kallikrein gene 9 (KLK9) in ovarian cancer: a new independent and favorable prognostic marker. Cancer Res. 2001;61:7811–7818
  84. Shvartsman HS, Lu KH, Lee J, Lillie J, Deavers MT, Clifford S, et al. Overexpression of kallikrein 10 in epithelial ovarian carcinomas. Gynecol. Oncol. 2003;90:44–50
  85. Shigemasa K, Gu L, Tanimoto H, O'Brien TJ, Ohama K. Human kallikrein gene 11 (KLK11) mRNA overexpression is associated with poor prognosis in patients with epithelial ovarian cancer. Clin. Cancer Res. 2004;10:2766–2770
  86. Yousef GM, Magklara A, Chang A, Jung K, Katsaros D, Diamandis EP. Cloning of a new member of the human kallikrein gene family, KLK14, which is down-regulated in different malignancies. Cancer Res. 2001;61:3425–3431
  87. Yousef GM, Fracchioli S, Scorilas A, Borgono CA, Iskander L, Puopolo M, et al. Steroid hormone regulation and prognostic value of the human kallikrein gene 14 in ovarian cancer. Am. J. Clin. Pathol. 2003;119:346–355
  88. Yousef GM, Scorilas A, Katsaros D, Fracchioli S, Iskander L, Borgono C, et al. Prognostic value of the human kallikrein gene 15 expression in ovarian cancer. J. Clin. Oncol. 2003;21:3119–3126
  89. Yousef GM, Polymeris ME, Yacoub GM, Scorilas A, Soosaipillai A, Popalis C, et al. Parallel overexpression of seven kallikrein genes in ovarian cancer. Cancer Res. 2003;63:2223–2227
  90. Adib TR, Henderson S, Perrett C, Hewitt D, Bourmpoulia D, Ledermann J, et al. Predicting biomarkers for ovarian cancer using gene-expression microarrays. Br. J. Cancer. 2004;90:686–692
  91. Hibbs K, Skubitz KM, Pambuccian SE, Casey RC, Burleson KM, Oegema TR, et al. Differential gene expression in ovarian carcinoma: identification of potential biomarkers. Am. J. Pathol. 2004;165:397–414
  92. Welsh JB, Sapinoso LM, Kern SG, Brown DA, Liu T, Bauskin AR, et al. Large-scale delineation of secreted protein biomarkers overexpressed in cancer tissue and serum. Proc. Natl Acad. Sci. USA. 2003;100:3410–3415
  93. Guppy AE, Rustin GJ. CA125 response: can it replace the traditional response criteria in ovarian cancer?. Oncologist. 2002;7:437–443
  94. Ghosh S, Wu Y, Stack MS. Ovarian cancer-associated proteinases. Cancer Treat. Res. 2002;107:331–351
  95. Stack MS, Ellerbroek SM, Fishman DA. The role of proteolytic enzymes in the pathology of epithelial ovarian carcinoma. Int. J. Oncol. 1998;12:569–576
  96. Yousef GM, Diamandis EP. Kallikreins, steroid hormones and ovarian cancer: is there a link?. Minerva Endocrinol. 2002;27:157–166
  97. Xi Z, Kaern J, Davidson B, Klokk TI, Risberg B, Trope C, et al. Kallikrein 4 is associated with paclitaxel resistance in ovarian cancer. Gynecol. Oncol. 2004;94:80–85
  98. Yousef GM, Polymeris ME, Grass L, Soosaipillai A, Chan PC, Scorilas A, et al. Human kallikrein 5: a potential novel serum biomarker for breast and ovarian cancer. Cancer Res. 2003;63:3958–3965
  99. Diamandis EP, Borgono CA, Scorilas A, Yousef GM, Harbeck N, Dorn J, et al. Immunofluorometric quantification of human kallikrein 5 expression in ovarian cancer cytosols and its association with unfavorable patient prognosis. Tumour Biol. 2003;24:299–309
  100. Diamandis EP, Yousef GM, Soosaipillai AR, Bunting P. Human kallikrein 6 (zyme/protease M/neurosin): a new serum biomarker of ovarian carcinoma. Clin. Biochem. 2000;33:579–583
  101. Diamandis EP, Scorilas A, Fracchioli S, Van Gramberen M, De Bruijn H, Henrik A, et al. Human kallikrein 6 (hK6): a new potential serum biomarker for diagnosis and prognosis of ovarian carcinoma. J. Clin. Oncol. 2003;21:1035–1043
  102. Hoffman BR, Katsaros D, Scorilas A, Diamandis P, Fracchioli S, Rigault de la Longrais IA, et al. Immunofluorometric quantitation and histochemical localisation of kallikrein 6 protein in ovarian cancer tissue: a new independent unfavourable prognostic biomarker. Br. J. Cancer. 2002;87:763–771
  103. Kishi T, Grass L, Soosaipillai A, Scorilas A, Harbeck N, Schmalfeldt B, et al. Human kallikrein 8, a novel biomarker for ovarian carcinoma. Cancer Res. 2003;63:2771–2774
  104. Kishi T, Grass L, Soosaipillai A, Shimizu-Okabe C, Diamandis EP. Human kallikrein 8: immunoassay development and identification in tissue extracts and biological fluids. Clin. Chem. 2003;49:87–96
  105. Goyal J, Smith KM, Cowan JM, Wazer DE, Lee SW, Band V. The role for NES1 serine protease as a novel tumor suppressor. Cancer Res. 1998;58:4782–4786
  106. Luo L, Herbrick JA, Scherer SW, Beatty B, Squire J, Diamandis EP. Structural characterization and mapping of the normal epithelial cell-specific 1 gene. Biochem. Biophys. Res. Commun. 1998;247:580–586
  107. Luo LY, Katsaros D, Scorilas A, Fracchioli S, Piccinno R, Rigault de la Longrais IA, et al. Prognostic value of human kallikrein 10 expression in epithelial ovarian carcinoma. Clin. Cancer Res. 2001;7:2372–2379
  108. Luo L, Bunting P, Scorilas A, Diamandis EP. Human kallikrein 10: a novel tumor marker for ovarian carcinoma?. Clin. Chim. Acta. 2001;306:111–118
  109. Luo LY, Katsaros D, Scorilas A, Fracchioli S, Bellino R, van Gramberen M, et al. The serum concentration of human kallikrein 10 represents a novel biomarker for ovarian cancer diagnosis and prognosis. Cancer Res. 2003;63:807–811
  110. Scorilas A, Borgono CA, Harbeck N, Dorn J, Schmalfeldt B, Schmitt M, et al. Human kallikrein 13 protein in ovarian cancer cytosols: a new favorable prognostic marker. J. Clin. Oncol. 2004;22:678–685
  111. Borgoño CA, Fracchioli S, Yousef GM, Luo L-Y, Katsaros D, Scorilas A, et al. Favourable prognostic value of human kallikrein 11 (hK11) in patients with ovarian carcinoma. Int. J. Cancer. 2003;106:605–610
  112. Yousef GM, Scorilas A, Kyriakopoulou LG, Rendl L, Diamandis M, Ponzone R, et al. Human kallikrein gene 5 (KLK5) expression by quantitative PCR: an independent indicator of poor prognosis in breast cancer. Clin. Chem. 2002;48:1241–1250
  113. Talieri M, Diamandis EP, Gourgiotis D, Mathioudaki K, Scorilas A. Expression analysis of the human kallikrein 7 (KLK7) in breast tumors: a new potential biomarker for prognosis of breast carcinoma. Thromb. Haemost. 2004;91:180–186
  114. Yousef G, Scorilas A, Nakamura T, Ellatif MA, Ponzone R, Biglia N, et al. The prognostic value of the human kallikrein gene 9 (KLK9) in breast cancer. Breast Cancer Res. Treat. 2003;78:149–158
  115. Dhar S, Bhargava R, Yunes M, Li B, Goyal J, Naber SP, et al. Analysis of normal epithelial cell specific-1 (NES1)/Kallikrein 10 mRNA expression by in situ hybridization, a novel marker for breast cancer. Clin. Cancer Res. 2001;7:3393–3398
  116. Yunes MJ, Neuschatz AC, Bornstein LE, Naber SP, Band V, Wazer DE. Loss of expression of the putative tumor suppressor NES1 gene in biopsy-proven ductal carcinoma in situ predicts for invasive carcinoma at definitive surgery. Int. J. Radiat. Oncol. Biol. Phys. 2003;56:653–657
  117. Li B, Goyal J, Dhar S, Dimri G, Evron E, Sukumar S, et al. CpG methylation as a basis for breast tumor-specific loss of NES1/kallikrein 10 expression. Cancer Res. 2001;61:8014–8021
  118. Chang A, Yousef GM, Scorilas A, Grass L, Sismondi P, Ponzone R, et al. Human kallikrein gene 13 (KLK13) expression by quantitative RT-PCR: an independent indicator of favourable prognosis in breast cancer. Br. J. Cancer. 2002;86:1457–1464
  119. Yousef GM, Magklara A, Diamandis EP. KLK12 is a novel serine protease and a new member of the human kallikrein gene family differential expression in breast cancer. Genomics. 2000;69:331–341
  120. Yousef GM, Borgono CA, Scorilas A, Ponzone R, Biglia N, Iskander L, et al. Quantitative analysis of human kallikrein gene 14 expression in breast tumours indicates association with poor prognosis. Br. J. Cancer. 2002;87:1287–1293
  121. Yousef GM, Scorilas A, Magklara A, Memari N, Ponzone R, Sismondi P, et al. The androgen-regulated gene human kallikrein 15 (KLK15) is an independent and favourable prognostic marker for breast cancer. Br. J. Cancer. 2002;87:1294–1300
  122. Yousef GM, Yacoub GM, Polymeris ME, Popalis C, Soosaipillai A, Diamandis EP. Kallikrein gene downregulation in breast cancer. Br. J. Cancer. 2004;90:167–172
  123. Borgono CA, Grass L, Soosaipillai A, Yousef GM, Petraki CD, Howarth DH, et al. Human kallikrein 14: a new potential biomarker for ovarian and breast cancer. Cancer Res. 2003;63:9032–9041
  124. Sauter ER, Daly M, Linahan K, Ehya H, Engstrom PF, Bonney G, et al. Prostate-specific antigen levels in nipple aspirate fluid correlate with breast cancer risk. Cancer Epidemiol. Biomarkers Prev. 1996;5:967–970
  125. Sauter ER, Lininger J, Magklara A, Hewett JE, Diamandis EP. Association of kallikrein expression in nipple aspirate fluid with breast cancer risk. Int. J. Cancer. 2004;108:588–591
  126. Luo LY, Diamandis EP, Look MP, Soosaipillai AP, Foekens JA. Higher expression of human kallikrein 10 in breast cancer tissue predicts tamoxifen resistance. Br. J. Cancer. 2002;86:1790–1796
  127. Gretzer MB, Partin AW. PSA markers in prostate cancer detection. Urol. Clin. North Am. 2003;30:677–686
  128. de Koning HJ, Auvinen A, Berenguer Sanchez A, Calais da Silva F, Ciatto S, Denis L, et al. Large-scale randomized prostate cancer screening trials: program performances in the European randomized screening for prostate cancer trial and the prostate, lung, colorectal and ovary cancer trial. Int. J. Cancer. 2002;97:237–244
  129. Yousef GM, Scorilas A, Chang A, Rendl L, Diamandis M, Jung K, et al. Down-regulation of the human kallikrein gene 5 (KLK5) in prostate cancer tissues. Prostate. 2002;51:126–132
  130. Bharaj BS, Luo L-Y, Jung K, Stephan C, Diamandis EP. Identification of single nucleotide polymorphism in the human kallikrein 10 (KLK10) gene and their association with prostate, breast, testicular and ovarian cancers. Prostate. 2002;51:35–41
  131. Nakamura T, Mitsui S, Okui A, Kominami K, Nomoto T, Ukimura O, et al Alternative splicing isoforms of hippostasin (PRSS20/KLK11) in prostate cancer cell lines. Prostate. 2001;49:72–78
  132. Nakamura T, Stephan C, Scorilas A, Yousef GM, Jung K, Diamandis EP. Quantitative analysis of hippostasin/KLK11 gene expression in cancerous and noncancerous prostatic tissues. Urology. 2003;61:1042–1046
  133. Nakamura T, Mitsui S, Okui A, Miki T, Yamaguchi N. Molecular cloning and expression of a variant form of hippostasin/KLK11 in prostate. Prostate. 2003;54:299–305
  134. Yousef GM, Stephan C, Scorilas A, Ellatif MA, Jung K, Kristiansen G, et al. Differential expression of the human kallikrein gene 14 (KLK14) in normal and cancerous prostatic tissues. Prostate. 2003;56:287–292
  135. Yousef GM, Scorilas A, Jung K, Ashworth LK, Diamandis EP. Molecular cloning of the human kallikrein 15 gene (KLK15). Up-regulation in prostate cancer. J. Biol. Chem. 2001;276:53–61
  136. Stephan C, Yousef GM, Scorilas A, Jung K, Jung M, Kristiansen G, et al. Quantitative analysis of kallikrein 15 gene expression in prostate tissue. J. Urol. 2003;169:361–364
  137. Obiezu CV, Soosaipillai A, Jung K, Stephan C, Scorilas A, Howarth DH, et al. Detection of human kallikrein 4 in healthy and cancerous prostatic tissues by immunofluorometry and immunohistochemistry. Clin. Chem. 2002;48:1232–1240
  138. Xi Z, Klokk TI, Korkmaz K, Kurys P, Elbi C, Risberg B, et al. Kallikrein 4 is a predominantly nuclear protein and is overexpressed in prostate cancer. Cancer Res. 2004;64:2365–2370
  139. Day CH, Fanger GR, Retter MW, Hylander BL, Penetrante RB, Houghton RL, et al. Characterization of KLK4 expression and detection of KLK4-specific antibody in prostate cancer patient sera. Oncogene. 2002;21:7114–7120
  140. Diamandis EP, Okui A, Mitsui S, Luo LY, Soosaipillai A, Grass L, et al. Human kallikrein 11: a new biomarker of prostate and ovarian carcinoma. Cancer Res. 2002;62:295–300
  141. Nakamura T, Scorilas A, Stephan C, Jung K, Soosaipillai AR, Diamandis EP. The usefulness of serum human kallikrein 11 for discriminating between prostate cancer and benign prostatic hyperplasia. Cancer Res. 2003;63:6543–6546
  142. Luo LY, Yousef G, Diamandis EP. Human tissue kallikreins and testicular cancer. Apmis. 2003;111:225–232discussion 232–233
  143. Huyghe E, Matsuda T, Thonneau P. Increasing incidence of testicular cancer worldwide: a review. J. Urol. 2003;170:5–11
  144. Yousef GM, Diamandis EP. The new kallikrein-like gene, KLK-L2. Molecular characterization, mapping, tissue expression, and hormonal regulation. J. Biol. Chem. 1999;274:37511–37516
  145. Yousef GM, Obiezu CV, Jung K, Stephan C, Scorilas A, Diamandis EP. Differential expression of kallikrein gene 5 in cancerous and normal testicular tissues. Urology. 2002;60:714–718
  146. Luo LY, Rajpert-De Meyts ER, Jung K, Diamandis EP. Expression of the normal epithelial cell-specific 1 (NES1; KLK10) candidate tumour suppressor gene in normal and malignant testicular tissue. Br. J. Cancer. 2001;85:220–224
  147. Chang A, Yousef GM, Jung K, Meyts ER, Diamanids EP. Identification and molecular characterization of five novel kallikrein gene 13 (KLK13; KLK-L4) splice variants: differential expression in human testis and testicular cancer. Anticancer Res. 2001;21:3147–3152
  148. Lundstrom A, Egelrud T. Stratum corneum chymotryptic enzyme: a proteinase which may be generally present in the stratum corneum and with a possible involvement in desquamation. Acta Derm. Venereol. 1991;71:471–474
  149. Egelrud T. Purification and preliminary characterization of stratum corneum chymotryptic enzyme: a proteinase that may be involved in desquamation. J. Invest. Dermatol. 1993;101:200–204
  150. Caubet C, Jonca N, Brattsand M, Guerrin M, Bernard D, Schmidt R, et al. Degradation of corneodesmosome proteins by two serine proteases of the kallikrein family, SCTE/KLK5/hK5 and SCCE/KLK7/hK7. J. Invest. Dermatol. 2004;122:1235–1244
  151. Santin AD, Cane S, Bellone S, Bignotti E, Palmieri M, De Las Casas LE, et al. The serine protease stratum corneum chymotryptic enzyme (kallikrein 7) is highly overexpressed in squamous cervical cancer cells. Gynecol. Oncol. 2004;94:283–288
  152. Cane S, Bignotti E, Bellone S, Palmieri M, De las Casas L, Roman JJ, et al. The novel serine protease tumor-associated differentially expressed gene-14 (KLK8/Neuropsin/Ovasin) is highly overexpressed in cervical cancer. Am. J. Obstet. Gynecol. 2004;190:60–66
  153. Yousef GM, Borgono CA, Popalis C, Yacoub GM, Polymeris ME, Soosaipillai A, et al. In-silico analysis of kallikrein gene expression in pancreatic and colon cancers. Anticancer Res. 2004;24:43–51
  154. Iacobuzio-Donahue CA, Ashfaq R, Maitra A, Adsay NV, Shen-Ong GL, Berg K, et al. Highly expressed genes in pancreatic ductal adenocarcinomas: a comprehensive characterization and comparison of the transcription profiles obtained from three major technologies. Cancer Res. 2003;63:8614–8622
  155. Ignatenko NA, Zhang H, Watts GS, Skovan BA, Stringer DE, Gerner EW. The chemopreventive agent alpha-difluoromethylornithine blocks Ki-ras-dependent tumor formation and specific gene expression in Caco-2 cells. Mol. Carcinog. 2004;39:221–233
  156. Takeuchi S, Bartram CR, Wada M, Reiter A, Hatta Y, Seriu T, et al. Allelotype analysis of childhood acute lymphoblastic leukemia. Cancer Res. 1995;55:5377–5382
  157. Roman-Gomez J, Jimenez-Velasco A, Agirre X, Castillejo JA, Barrios M, Andreu EJ, et al. The normal epithelial cell-specific 1 (NES1) gene, a candidate tumor suppressor gene on chromosome 19q13.3–4, is downregulated by hypermethylation in acute lymphoblastic leukemia. Leukemia. 2004;18:362–365
  158. Bhattacharjee A, Richards WG, Staunton J, Li C, Monti S, Vasa P, et al. Classification of human lung carcinomas by mRNA expression profiling reveals distinct adenocarcinoma subclasses. Proc. Natl Acad. Sci. USA. 2001;98:13790–13795
  159. Garber ME, Troyanskaya OG, Schluens K, Petersen S, Thaesler Z, Pacyna-Gengelbach M, et al. Diversity of gene expression in adenocarcinoma of the lung. Proc. Natl Acad. Sci. USA. 2001;98:13784–13789
  160. Chung CH, Parker JS, Karaca G, Wu J, Funkhouser WK, Moore D, et al. Molecular classification of head and neck squamous cell carcinomas using patterns of gene expression. Cancer Cell. 2004;5:489–500
  161. Hart PS, Hart TC, Michalec MD, Ryu OH, Simmons D, Hong S, et al. Mutation in kallikrein 4 causes autosomal recessive hypomaturation amelogenesis imperfecta. J. Med. Genet. 2004;41:545–549
  162. Hu JC, Zhang C, Sun X, Yang Y, Cao X, Ryu O, et al. Characterization of the mouse and human PRSS17 genes, their relationship to other serine proteases, and the expression of PRSS17 in developing mouse incisors. Gene. 2000;251:1–8
  163. Hu JC, Sun X, Zhang C, Liu S, Bartlett JD, Simmer JP. Enamelysin and kallikrein-4 mRNA expression in developing mouse molars. Eur. J. Oral Sci. 2002;110:307–315
  164. Okui A, Kominami K, Uemura H, Mitsui S, Yamaguchi N. Characterization of a brain-related serine protease, neurosin (human kaillikrein 6), in human cerebrospinal fluid. Neuroreport. 2001;12:1345–1350
  165. Yamanaka H, He X, Matsumoto K, Shiosaka S, Yoshida S. Protease M/neurosin mRNA is expressed in mature oligodendrocytes. Brain Res. Mol. Brain Res. 1999;71:217–224
  166. Diamandis EP, Yousef GM, Soosaipillai AR, Grass L, Porter A, Little S, et al. Immunofluorometric assay of human kallikrein 6 (zyme/protease M/neurosin) and preliminary clinical applications. Clin. Biochem. 2000;33:369–375
  167. Bernett MJ, Blaber SI, Scarisbrick IA, Dhanarajan P, Thompson SM, Blaber M. Crystal structure and biochemical characterization of human kallikrein 6 reveals that a trypsin-like kallikrein is expressed in the central nervous system. J. Biol. Chem. 2002;277:24562–24570
  168. Blaber SI, Scarisbrick IA, Bernett MJ, Dhanarajan P, Seavy MA, Jin Y, et al. Enzymatic properties of rat myelencephalon-specific protease. Biochemistry. 2002;41:1165–1173
  169. Scarisbrick IA, Towner MD, Isackson PJ. Nervous system-specific expression of a novel serine protease: regulation in the adult rat spinal cord by excitotoxic injury. J. Neurosci. 1997;17:8156–8168
  170. Scarisbrick IA, Blaber SI, Lucchinetti CF, Genain CP, Blaber M, Rodriguez M. Activity of a newly identified serine protease in CNS demyelination. Brain. 2002;125:1283–1296
  171. Blaber SI, Ciric B, Christophi GP, Bernett MJ, Blaber M, Rodriguez M, et al. Targeting kallikrein 6 proteolysis attenuates CNS inflammatory disease. Fed. Am. Soc. Exp. Biol. J. 2004;18:920–922
  172. Zarghooni M, Soosaipillai A, Grass L, Scorilas A, Mirazimi N, Diamandis EP. Decreased concentration of human kallikrein 6 in brain extracts of Alzheimer's disease patients. Clin. Biochem. 2002;35:225–231
  173. Diamandis EP, Yousef GM, Petraki C, Soosaipillai AR. Human kallikrein 6 as a biomarker of Alzheimer's disease. Clin. Biochem. 2000;33:663–667
  174. Mitsui S, Okui A, Uemura H, Mizuno T, Yamada T, Yamamura Y, et al. Decreased cerebrospinal fluid levels of neurosin (KLK6), an aging-related protease, as a possible new risk factor for Alzheimer's disease. Ann. NY Acad. Sci. 2002;977:216–223
  175. Ogawa K, Yamada T, Tsujioka Y, Taguchi J, Takahashi M, Tsuboi Y, et al. Localization of a novel type trypsin-like serine protease, neurosin, in brain tissues of Alzheimer's disease and Parkinson's disease. Psychiatry Clin. Neurosci. 2000;54:419–426
  176. Iwata A, Maruyama M, Akagi T, Hashikawa T, Kanazawa I, Tsuji S, et al. Alpha-synuclein degradation by serine protease neurosin: implication for pathogenesis of synucleinopathies. Hum. Mol. Genet. 2003;12:2625–2635
  177. Aston C, Jiang L, Sokolov BP. Transcriptional profiling reveals evidence for signaling and oligodendroglial abnormalities in the temporal cortex from patients with major depressive disorder. Mol. Psychiatry. 2004;
  178. Diamandis EP, Scorilas A, Kishi T, Blennow K, Luo LY, Soosaipillai A, et al. Altered kallikrein 7 and 10 concentrations in cerebrospinal fluid of patients with Alzheimer's disease and frontotemporal dementia. Clin. Biochem. 2004;37:230–237
  179. Shimizu-Okabe C, Yousef GM, Diamandis EP, Yoshida S, Shiosaka S, Fahnestock M. Expression of the kallikrein gene family in normal and Alzheimer's disease brain. Neuroreport. 2001;12:2747–2751
  180. Mitsui S, Tsuruoka N, Yamashiro K, Nakazato H, Yamaguchi N. A novel form of human neuropsin, a brain-related serine protease, is generated by alternative splicing and is expressed preferentially in human adult brain. Eur. J. Biochem. 1999;260:627–634
  181. Komatsu N, Takata M, Otsuki N, Toyama T, Ohka R, Takehara K, et al. Expression and localization of tissue kallikrein mRNAs in human epidermis and appendages. J. Invest. Dermatol. 2003;121:542–549
  182. Poblete MT, Reynolds NJ, Figueroa CD, Burton JL, Muller-Esterl W, Bhoola KD. Tissue kallikrein and kininogen in human sweat glands and psoriatic skin. Br. J. Dermatol. 1991;124:236–241
  183. Schremmer-Danninger E, Hermann A, Fink E, Fritz H, Roscher AA. Identification and occurrence of mRNAs for components of the kallikrein–kinin system in human skin and in skin diseases. Immunopharmacology. 1999;43:287–291
  184. Hansson L, Backman A, Ny A, Edlund M, Ekholm E, Ekstrand Hammarstrom B, et al. Epidermal overexpression of stratum corneum chymotryptic enzyme in mice: a model for chronic itchy dermatitis. J. Invest. Dermatol. 2002;118:444–449
  185. Ekholm E, Egelrud T. Stratum corneum chymotryptic enzyme in psoriasis. Arch Dermatol. Res. 1999;291:195–200
  186. Ekholm E, Egelrud T. The expression of stratum corneum chymotryptic enzyme in human anagen hair follicles: further evidence for its involvement in desquamation-like processes. Br. J. Dermatol. 1998;139:585–590
  187. Ekholm IE, Brattsand M, Egelrud T. Stratum corneum tryptic enzyme in normal epidermis: a missing link in the desquamation process?. J. Invest. Dermatol. 2000;114:56–63
  188. Vasilopoulos Y, Cork MJ, Murphy R, Williams HC, Robinson DA, Duff GW, et al. Genetic association between an AACC insertion in the 3′UTR of the stratum corneum chymotryptic enzyme gene and atopic dermatitis. J. Invest. Dermatol. 2004;123:62–66
  189. Kuwae K, Matsumoto-Miyai K, Yoshida S, Sadayama T, Yoshikawa K, Hosokawa K, et al. Epidermal expression of serine protease, neuropsin (KLK8) in normal and pathological skin samples. Mol. Pathol. 2002;55:235–241
  190. Pejovic T. Genetic changes in ovarian cancer. Ann. Med. 1995;27:73–78
  191. Johansson B, Fioretos T, Mitelman F. Cytogenetic and molecular genetic evolution of chronic myeloid leukemia. Acta Haematol. 2002;107:76–94
  192. Casalone R, Albini A, Righi R, Granata P, Toniolo A. Nonrandom chromosome changes in Kaposi sarcoma: cytogenetic and FISH results in a new cell line (KS-IMM) and literature review. Cancer Genet. Cytogenet. 2001;124:16–19
  193. Webber MM, Waghray A, Bello D. Prostate-specific antigen, a serine protease, facilitates human prostate cancer cell invasion. Clin. Cancer Res. 1995;1:1089–1094
  194. Deperthes D, Frenette G, Brillard-Bourdet M, Bourgeois L, Gauthier F, Tremblay RR, et al. Potential involvement of kallikrein hK2 in the hydrolysis of the human seminal vesicle proteins after ejaculation. J. Androl. 1996;17:659–665
  195. Magklara A, Mellati AA, Wasney GA, Little SP, Sotiropoulou G, Becker GW, et al. Characterization of the enzymatic activity of human kallikrein 6: autoactivation, substrate specificity, and regulation by inhibitors. Biochem. Biophys. Res. Commun. 2003;307:948–955
  196. Takayama TK, Fujikawa K, Davie EW. Characterization of the precursor of prostate-specific antigen. Activation by trypsin and by human glandular kallikrein. J. Biol. Chem. 1997;272:21582–21588
  197. Takayama TK, Carter CA, Deng T. Activation of prostate-specific antigen precursor (pro-PSA) by prostin, a novel human prostatic serine protease identified by degenerate PCR. Biochemistry. 2001;40:1679–1687
  198. Takayama TK, McMullen BA, Nelson PS, Matsumura M, Fujikawa K. Characterization of hK4 (Prostase), a prostate-specific serine protease: activation of the precursor of prostate specific antigen (pro-PSA) and single-chain urokinase-type plasminogen activator and degradation of prostatic acid phosphatase. Biochemistry. 2001;40:15341–15348
  199. Lovgren J, Rajakoski K, Karp M, Lundwall A, Lilja H. Activation of the zymogen form of prostate-specific antigen by human glandular kallikrein 2. Biochem. Biophys. Res. Commun. 1997;238:549–555
  200. Fortier AH, Nelson BJ, Grella DK, Holaday JW. Antiangiogenic activity of prostate-specific antigen. J. Natl Cancer Inst. 1999;91:1635–1640
  201. Fortier AH, Holaday JW, Liang H, Dey C, Grella DK, Holland-Linn J, et al. Recombinant prostate specific antigen inhibits angiogenesis in vitro and in vivo. Prostate. 2003;56:212–219
  202. Papadopoulos I, Sivridis E, Giatromanolaki A, Koukourakis MI. Tumor angiogenesis is associated with MUC1 overexpression and loss of prostate-specific antigen expression in prostate cancer. Clin. Cancer Res. 2001;7:1533–1538
  203. Aimes RT, Zijlstra A, Hooper JD, Ogbourne SM, Sit ML, Fuchs S, et al. Endothelial cell serine proteases expressed during vascular morphogenesis and angiogenesis. Thromb. Haemost. 2003;89:561–572
  204. Tanimoto H, Underwood LJ, Shigemasa K, Yan Yan MS, Clarke J, Parmley TH, et al. The stratum corneum chymotryptic enzyme that mediates shedding and desquamation of skin cells is highly overexpressed in ovarian tumor cells. Cancer. 1999;86:2074–2082
  205. Black MH, Diamandis EP. The diagnostic and prognostic utility of prostate-specific antigen for diseases of the breast. Breast Cancer Res Treat. 2000;59:1–14
  206. Magklara A, Scorilas A, Catalona WJ, Diamandis EP. The combination of human glandular kallikrein and free prostate-specific antigen (PSA) enhances discrimination between prostate cancer and benign prostatic hyperplasia in patients with moderately increased total PSA. Clin Chem. 1999;45:1960–1966
  207. Partin AW, Catalona WJ, Finlay JA, Darte C, Tindall DJ, Young CY, et al. Use of human glandular kallikrein 2 for the detection of prostate cancer: preliminary analysis. Urology. 1999;54:839–845

PII: S0304-3835(04)00730-X

doi: 10.1016/j.canlet.2004.09.024

Cancer Letters
Volume 224, Issue 1 , Pages 1-22 , 16 June 2005

Article Tools