Kallikrein-related peptidase-4 initiates tumor-stroma interactions in prostate cancer through protease-activated receptor-1

International Journal of Cancer

Volumn 126, Issue 3, 2010, Pages 599-610

  Wang, Wenbin ^a   Mize, Gregory J ^a   Zhang, Xiaotun ^a   Takayama, Thomas K ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

IL 6; KLK4; PAR 1; Prostate cancer; Signaling

Indexed keywords

CYTOKINE; GROWTH FACTOR; INTERLEUKIN 6; KALLIKREIN 4; KALLIKREIN 6; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEINASE ACTIVATED RECEPTOR 1; THROMBIN; UNCLASSIFIED DRUG;

ARTICLE; CANCER GROWTH; CELL PROLIFERATION; CELL STRAIN LNCAP; CELL SURFACE; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MYOFIBROBLAST; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FUNCTION; STROMA CELL; UPREGULATION;

ADENOCARCINOMA; CELL LINE, TUMOR; CELLS, CULTURED; CULTURE MEDIA, CONDITIONED; GENE KNOCKDOWN TECHNIQUES; HUMANS; INTERLEUKIN-6; KALLIKREINS; MALE; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; NEOPLASM PROTEINS; OLIGOPEPTIDES; PARACRINE COMMUNICATION; PROSTATIC NEOPLASMS; RECEPTOR, PAR-1; RNA, SMALL INTERFERING; STROMAL CELLS; THROMBIN;

EID: 73449094567     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.24904     Document Type: Article

References (65)

1. Jemal A, Siegel R, Ward E, Murray T, XuJ, ThunMJ. Cancer statistics, 2007. CA Cancer J Clin 2007;57:43-66.
2. Culig Z, Hobisch A, Cronauer MV, Radmayr C, TrapmanJ, HittmairA, BartschG, KlockerH. Androgen receptor activation in prostatic tumor cell lines by insulin-like growth factor-I, keratinocyte growth factor, and epidermal growth factor. Cancer Res 1994;54:5474-8.
3. Nazareth LV, Weigel NL. Activation of the human androgen receptor through a protein kinase A signaling pathway. J Biol Chem 1996;271:19900-7.
4. Ueda T, Mawji NR, Bruchovsky N, Sadar MD. Ligand-independent activation of the androgen receptor by IL-6 and the role of the coactivator SRC-1 in prostate cancer cells. J Biol Chem 2002;277:38087-94.
5. De Wever O, Demetter P, Mareel M, Bracke M. Stromal myofibroblasts are drivers of invasive cancer growth. Int J Cancer 2008;123:2229-38.
6. Chung LW, Chang SM, Bell C, Zhau HE, RoJY, von EschenbachAC. Co-inoculation of tumorigenic rat prostate mesenchymal cells with non-tumorigenic epithelial cells results in the development of carcinosarcoma in syngeneic and athymic animals. Int J Cancer 1989;43:1179-87.
7. Camps JL, Chang SM, Hsu TC, Freeman MR, HongSJ, ZhauHE, von EschenbachAC, ChungLW. Fibroblast-mediated acceleration of human epithelial tumor growth in vivo. Proc Natl Acad Sci USA 1990;87:75-9.
8. Kalluri R, Zeisberg M. Fibroblasts in cancer. Nat Rev Cancer 2006;6:392-401.
9. Orimo A, Gupta PB, Sgroi DC, Arenzana-Seisdedos F, DelaunayT, NaeemR, CareyVJ, RichardsonAL, WeinbergRA. Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/ CXCL12 secretion. Cell 2005;121:335-48.
10. Ao M, Franco OE, Park D, Raman D, WilliamsK, HaywardSW. Cross-talk between paracrine-acting cytokine and chemokine pathways promotes malignancy in benign human prostatic epithelium. Cancer Res 2007;67:4244-53.
11. Wilson TJ, Singh RK. Proteases as modulators of tumor-stromal interaction: primary tumors to bone metastases. Biochim Biophys Acta 2008;1785:85-95.
12. Lundwall A, Band V, Blaber M, Clements JA, CourtyY, DiamandisEP, FritzH, LiljaH, MalmJ, MaltaisLJ, OlssonAY, PetrakiC, et al. A comprehensive nomenclature for serine proteases with homology to tissue kallikreins. Biol Chem 2006;387:637-41.
13. Borgono CA, Diamandis EP. The emerging roles of human tissue kallikreins in cancer. Nat Rev Cancer 2004;4:876-90.
14. Clements JA, Willemsen NM, Myers SA, Dong Y. The tissue kallikrein family of serine proteases: functional roles in human disease and potential as clinical biomarkers. Crit Rev Clin Lab Sci 2004;41:265-312.
15. Takayama TK, McMullen BA, Nelson PS, Matsumura M, FujikawaK. 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;40:15341-8.
16. Ramsay AJ, Dong Y, Hunt ML, Linn M, SamaratungaH, ClementsJA, HooperJD. Kallikrein-related peptidase 4 (KLK4) initiates intracellular signaling via protease-activated receptors (PARs). KLK4 and PAR-2 are co-expressed during prostate cancer progression. J Biol Chem 2008;283:12293-304.
17. Oikonomopoulou K, Hansen KK, Saifeddine M, Tea I, BlaberM, BlaberSI, ScarisbrickI, Andrade-GordonP, CottrellGS, BunnettNW, DiamandisEP, HollenbergMD. Proteinase-activated receptors, targets for kallikrein signaling. J Biol Chem 2006;281:32095-112.
18. Mize GJ, Wang W, Takayama TK. Prostate-specific Kallikreins-2 and-4 enhance the proliferation of DU-145 prostate cancer cells through protease-activated receptors-1 and -2. Mol Cancer Res 2008;6:1043-51.
19. Coughlin SR. Thrombin signalling and protease-activated receptors. Nature 2000;407:258-64.
20. Leger AJ, Covic L, Kuliopulos A. Protease-activated receptors in cardiovascular diseases. Circulation 2006;114:1070-7.
21. Darmoul D, Gratio V, Devaud H, Lehy T, LaburtheM. Aberrant expression and activation of the thrombin receptor protease-activated receptor-1 induces cell proliferation and motility in human colon cancer cells. Am J Pathol 2003;162:1503-13.
22. Darmoul D, Gratio V, Devaud H, Laburthe M. Protease-activated receptor 2 in colon cancer: trypsin-induced MAPK phosphorylation and cell proliferation are mediated by epidermal growth factor receptor transactivation. J Biol Chem 2004;279:20927-34.
23. Caruso R, Pallone F, Fina D, Gioia V, PelusoI, CaprioliF, StolfiC, PerfettiA, SpagnoliLG, PalmieriG, MacdonaldTT, MonteleoneG. Protease-activated receptor-2 activation in gastric cancer cells promotes epidermal growth factor receptor transactivation and proliferation. Am J Pathol 2006;169:268-78.
24. Steinhoff M, Buddenkotte J, Shpacovitch V, Rattenholl A, MoormannC, VergnolleN, LugerTA, HollenbergMD. Proteinase-activated receptors: transducers of proteinase-mediated signaling in inflammation and immune response. Endocr Rev 2005;26:1-43.
25. McLaughlin JN, Patterson MM, Malik AB. Protease-activated receptor-3 (PAR3) regulates PAR1 signaling by receptor dimerization. Proc Natl Acad Sci USA 2007;104:5662-7.
26. Black PC, Mize GJ, Karlin P, Greenberg DL, HawleySJ, TrueLD, VessellaRL, TakayamaTK. Overexpression of protease-activated receptors-1,-2, and-4 (PAR-1, -2, and -4) in prostate cancer. Prostate 2007;67:743-56.
27. Greenberg DL, Mize GJ, Takayama TK. Protease-activated receptor mediated RhoA signaling and cytoskeletal reorganization in LNCaP cells. Biochemistry 2003;42:702-9.
28. Liu J, Schuff-Werner P, Steiner M. Thrombin/thrombin receptor (PAR-1)-mediated induction of IL-8 and VEGF expression in prostate cancer cells. Biochem Biophys Res Commun 2006;343:183-9.
29. Yin YJ, Salah Z, Maoz M, Ram SC, OchayonS, NeufeldG, KatzavS, Bar-ShavitR. Oncogenic transformation induces tumor angiogenesis: a role for PAR1 activation. FASEB J 2003;17:163-74.
30. Zhang X, Wang W, True LD, Vessella RL, TakayamaTK. Protease-activated receptor-1 is upregulated in reactive stroma of primary prostate cancer and bone metastasis. Prostate 2009;69:727-36.
31. Mize GJ, Harris JE, Takayama TK, Kulman JD. Regulated expression of active biotinylated G-protein coupled receptors in mammalian cells. Protein Expr Purif 2008;57:280-9.
32. Wang W, Zhang X, Mize GJ, Takayama TK. Protease-activated receptor-1 upregulates fibroblast growth factor 7 in stroma of benign prostatic hyperplasia. Prostate 2008;68:1064-75.
33. Blaszczyk N, Masri BA, Mawji NR, Ueda T, McAlindenG, DuncanCP, BruchovskyN, SchweikertHU, SchnabelD, JonesEC, SadarMD. Osteoblast-derived factors induce androgen-independent proliferation and expression of prostate-specific antigen in human prostate cancer cells. Clin Cancer Res 2004;10:1860-9.
34. Ishii K, Hein L, Kobilka B, Coughlin SR. Kinetics of thrombin receptor cleavage on intact cells. Relation to signaling. J Biol Chem 1993;268:9780-6.
35. Webber MM, Trakul N, Thraves PS, Bello-DeOcampo D, ChuWW, StortoPD, HuardTK, RhimJS, WilliamsDE. A human prostatic stromal myofibroblast cell line WPMY-1: a model for stromal-epithelial interactions in prostatic neoplasia. Carcinogenesis 1999;20:1185-92.
36. Azumi N, Battifora H. The distribution of vimentin and keratin in epithelial and nonepithelial neoplasms. A comprehensive immunohistochemical study on formalin-and alcohol-fixed tumors. Am J Clin Pathol 1987;88:286-96.
37. Saalbach A, Aneregg U, Bruns M, Schnabel E, HerrmannK, HausteinUF. Novel fibroblast-specific monoclonal antibodies: properties and specificities. J Invest Dermatol 1996;106:1314-9.
38. Hong DS, Angelo LS, Kurzrock R. Interleukin-6 and its receptor in cancer: implications for translational therapeutics. Cancer 2007;110:1911-28.
39. Culig Z, Steiner H, Bartsch G, Hobisch A. Interleukin-6 regulation of prostate cancer cell growth. J Cell Biochem 2005;95:497-505.
40. Hobisch A, Eder IE, Putz T, Horninger W, BartschG, KlockerH, CuligZ. Interleukin-6 regulates prostate-specific protein expression in prostate carcinoma cells by activation of the androgen receptor. Cancer Res 1998;58:4640-5.
41. Arora P, Ricks TK, Trejo J. Protease-activated receptor signalling, endocytic sorting and dysregulation in cancer. J Cell Sci 2007;120:921-8.
42. Tuxhorn JA, Ayala GE, Rowley DR. Reactive stroma in prostate cancer progression. J Urol 2001;166:2472-83.
43. Rowley DR. What might a stromal response mean to prostate cancer progression? Cancer Metastsis Rev 1998;17:411-9.
44. D'Andrea MR, Derian CK, Santulli RJ, Andrade-Gordon P. Differential expression of protease-activated receptors-1 and -2 in stromal fibroblasts of normal, benign, and malignant human tissues. Am J Pathol 2001;158:2031-41.
45. Salah Z, Maoz M, Cohen I, Pizov G, PodeD, RungeMS, Bar-ShavitR. Identification of a novel functional androgen response element within hPar1 promoter: implications to prostate cancer progression. FASEB J 2005;19:62-72.
46. Salah Z, Maoz M, Pizov G, Bar-Shavit R. Transcriptional regulation of human protease-activated receptor 1: a role for the early growth response-1 protein in prostate cancer. Cancer Res 2007;67:9835-43.
47. Shaw JL, Diamandis EP. Distribution of 15 human kallikreins in tissues and biological fluids. Clin Chem 2007;53:1423-32.
48. Wilson S, Greer B, Hooper J, Zijlstra A, WalkerB, QuigleyJ, HawthorneS. The membrane-anchored serine protease. TMPRSS2, activates PAR-2 in prostate cancer cells. Biochem J 2005;388:967-72.
49. Nelson PS, Gan L, Ferguson C, Moss P, GelinasR, HoodL, WangK. Molecular cloning and characterization of prostase, an androgen-regulated serine protease with prostate-restricted expression. Proc Natl Acad Sci USA 1999;96:3114-9.
50. Stephenson SA, Verity K, Ashworth LK, Clements JA. Localization of a new prostate-specific antigen-related serine protease gene. KLK4, is evidence for an expanded human kallikrein gene family cluster on chromosome 19q13.3-13.4. J Biol Chem 1999;274:23210-4.
51. Yousef GM, Obiezu CV, Luo LY, Black MH, DiamandisEP. 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;59:4252-6.
52. Hollenberg MD, Oikonomopoulou K, Hansen KK, Saifeddine M, RamachandranR, DiamandisEP. Kallikreins and proteinase-mediated signaling: proteinase-activated receptors (PARs) and the pathophysiology of inflammatory diseases and cancer. Biol Chem 2008;389:643-51.
53. Drachenberg DE, Elgamal AA, Rowbotham R, Peterson M, MurphyGP. Circulating levels of interleukin-6 in patients with hormone refractory prostate cancer. Prostate 1999;41:127-33.
54. Zerbini LF, Wang Y, Cho JY, Libermann TA. Constitutive activation of nuclear factor kappaB p50/p65 and Fra-1 and JunD is essential for deregulated interleukin 6 expression in prostate cancer. Cancer Res 2003;63:2206-15.
55. Ueda T, Bruchovsky N, Sadar MD. Activation of the androgen receptor N-terminal domain by interleukin-6 via MAPK and STAT3 signal transduction pathways. J Biol Chem 2002;277:7076-85.
56. Lin DL, Whitney MC, Yao Z, Keller ET. Interleukin-6 induces androgen responsiveness in prostate cancer cells through up-regulation of androgen receptor expression. Clin Cancer Res 2001;7:1773-81.
57. Lu Y, Zhang J, Dai J, Dehne LA, MizokamiA, YaoZ, KellerET. Osteoblasts induce prostate cancer proliferation and PSA expression through interleukin-6-mediated activation of the androgen receptor. Clin Exp Metastasis 2004;21:399-408.
58. Sivashanmugam P, Tang L, Daaka Y. Interleukin 6 mediates the lysophosphatidic acid-regulated cross-talk between stromal and epithelial prostate cancer cells. J Biol Chem 2004;279:21154-9.
59. Moore BB, Arenberg DA, Stoy K, Morgan T, AddisonCL, MorrisSB, GlassM, WilkeC, XueYY, SitterdingS, KunkelSL, BurdickMD, et al. Distinct CXC chemokines mediate tumorigenicity of prostate cancer cells. Am J Pathol 1999;154:1503-12.
60. Inoue K, Slaton JW, Eve BY, Kim SJ, PerrotteP, BalbayMD, YanoS, Bar-EliM, RadinskyR, PettawayCA, DinneyCP. Interleukin 8 expression regulates tumorigenicity and metastases in androgen-independent prostate cancer. Clin Cancer Res 2000;6:2104-19.
61. Kim SJ, Uehara H, Karashima T, McCarty M, ShihN, FidlerIJ. Expression of interleukin-8 correlates with angiogenesis, tumorigenicity, and metastasis of human prostate cancer cells implanted orthotopically in nude mice. Neoplasia 2001;3:33-42.
62. Lee LF, Louie MC, Desai SJ, Yang J, ChenHW, EvansCP, KungHJ. Interleukin-8 confers androgen-independent growth and migration of LNCaP: differential effects of tyrosine kinases Src and FAK. Oncogene 2004;23:2197-205.
63. Murphy C, McGurk M, Pettigrew J, Santinelli A, MazzucchelliR, JohnstonPG, MontironiR, WaughDJ. Nonapical and cytoplasmic expression of interleukin-8, CXCR1, and CXCR2 correlates with cell proliferation and microvessel density in prostate cancer. Clin Cancer Res 2005;11:4117-27.
64. Kim MS, Day CJ, Selinger CI, Magno CL, StephensSR, MorrisonNA. MCP-1-induced human osteoclast-like cells are tartrate-resistant acid phosphatase, NFATc1, and calcitonin receptor-positive but require receptor activator of NFk B ligand for bone resorption. J Biol Chem 2006;281:1274-85.
65. Lu Y, Xiao G, Galson DL, Nishio Y, MizokamiA, KellerET, YaoZ, ZhangJ. PTHrP-induced MCP-1 production by human bone marrow endothelial cells and osteoblasts promotes osteoclast differentiation and prostate cancer cell proliferation and invasion in vitro. Int J Cancer 2007;121:724-33.