Protein kinase D1 inhibits cell proliferation through matrix metalloproteinase-2 and matrix metalloproteinase-9 secretion in prostate cancer

Cancer Research

Volumn 70, Issue 5, 2010, Pages 2095-2104

  Biswas, M Helal Uddin ^a   Du, Cheng ^a   Zhang, Chuanyou ^a   Straubhaar, Juerg ^a   Languino, Lucia R ^a   Balaji, K C ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMITOTIC AGENT; ANTINEOPLASTIC AGENT; BETA INTEGRIN; GELATINASE A; GELATINASE B; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE D 1; RECOMBINANT MATRIX METALLOPROTEINASE 2; RECOMBINANT MATRIX METALLOPROTEINASE 9; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; UVOMORULIN;

ARTICLE; BIOINFORMATICS; CELL PROLIFERATION; COMPUTER MODEL; CONTROLLED STUDY; DNA MICROARRAY; ELECTROPHORESIS; ENZYME PHOSPHORYLATION; ENZYME RELEASE; ENZYME SYNTHESIS; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOPRECIPITATION; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; SIGNAL TRANSDUCTION; ZYMOGRAPHY;

CADHERINS; CELL GROWTH PROCESSES; CELL LINE, TUMOR; DOWN-REGULATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; INTEGRIN BETA3; MALE; MAP KINASE SIGNALING SYSTEM; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PROSTATIC NEOPLASMS; PROTEIN KINASE C; TRANSFECTION;

EID: 77950232143     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-09-4155     Document Type: Article

References (50)

1. Frisch SM, Ruoslahti E. Integrins and anoikis. Curr Opin Cell Biol 1997;9:701-706
2. Kantak SS, Kramer RH. E-cadherin regulates anchorage-independent growth and survival in oral squamous cell carcinoma cells. J Biol Chem 1998;273:16953-16961
3. Alexander CM, Howard EW, Bissell MJ, Werb Z. Rescue of mammary epithelial cell apoptosis and entactin degradation by a tissue inhibitor of metalloproteinases-1 transgene. J Cell Biol 1996;135:1669-1677
4. Stetler-Stevenson WG, Krutzsch HC, Wacher MP, Margulies IM, Liotta LA. The activation of human type IV collagenase proenzyme. Sequence identification of the major conversion product following organomercurial activation. J Biol Chem 1989;264:1353-1356
5. McCawley LJ, Matrisian LM. Matrix metalloproteinases: they're not just for matrix anymore!. Curr Opin Cell Biol 2001;13:534-540
6. Puente XS, Sanchez LM, Overall CM, Lopez-Otin C. Human and mouse proteases: a comparative genomic approach. Nat Rev Genet 2003;4:544-558
7. Egeblad M, Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer 2002;2:161-174
8. Kayagaki N, Kawasaki A, Ebata T, et al. Metalloproteinase-mediated release of human Fas ligand. J Exp Med 1995;182:1777-1783
9. Witty JP, Lempka T, Coffey RJ, Jr., Matrisian LM. Decreased tumor formation in 7,12-dimethylbenzanthracene-treated stromelysin-1 transgenic mice is associated with alterations in mammary epithelial cell apoptosis. Cancer Res 1995;55:1401-1406
10. Powell WC, Fingleton B, Wilson CL, Boothby M, Matrisian LM. The metalloproteinase matrilysin proteolytically generates active soluble Fas ligand and potentiates epithelial cell apoptosis. Curr Biol 1999;9:1441-1447
11. Sheu BC, Hsu SM, Ho HN, Lien HC, Huang SC, Lin RH. A novel role of metalloproteinase in cancer-mediated immunosuppression. Cancer Res 2001;61:237-242
12. Balbin M, Fueyo A, Tester AM, et al. Loss of collagenase-2 confers increased skin tumor susceptibility to male mice. Nat Genet 2003;35:252-257
13. Hartland SN, Murphy F, Aucott RL, et al. Active matrix metalloproteinase- 2 promotes apoptosis of hepatic stellate cells via the cleavage of cellular N-cadherin. Liver Int 2009;29:966-978
14. Wielockx B, Lannoy K, Shapiro SD, et al. Inhibition of matrix metalloproteinases blocks lethal hepatitis and apoptosis induced by tumor necrosis factor and allows safe antitumor therapy. Nat Med 2001;7:1202-1208
15. Lokeshwar BL. MMP inhibition in prostate cancer. Ann N Y Acad Sci 1999;878:271-289
16. Jaggi M, Du C, Zhang W, Balaji KC. Protein kinase D1: a protein of emerging translational interest. Front Biosci 2007;12:3757-3767
17. Schwartz MA, Baron V. Interactions between mitogenic stimuli, or, a thousand and one connections. Curr Opin Cell Biol 1999;11:197-202.
18. Shattil SJ. Signaling through platelet integrin αIIbβ3: inside-out, outside- in, and sideways. Thromb Haemost 1999;82:318-325
19. Woods AJ, White DP, Caswell PT, Norman JC. PKD1/PKCmu promotes αvβ3 integrin recycling and delivery to nascent focal adhesions. EMBO J 2004;23:2531-2543
20. Medeiros RB, Dickey DM, Chung H, et al. Protein kinase D1 and the β1 integrin cytoplasmic domain control β1 integrin function via regulation of Rap1 activation. Immunity 2005;23:213-226
21. Jaggi M, Rao PS, Smith DJ, Hemstreet GP, Balaji KC. Protein kinase Cμ is down-regulated in androgen-independent prostate cancer. Biochem Biophys Res Commun 2003;307:254-260
22. Jaggi M, Rao PS, Smith DJ, et al. E-cadherin phosphorylation by protein kinase D1/protein kinase Cμ is associated with altered cellular aggregation and motility in prostate cancer. Cancer Res 2005;65:483-492
23. Syed V, Mak P, Du C, Balaji KC. β-catenin mediates alteration in cell proliferation, motility and invasion of prostate cancer cells by differential expression of E-cadherin and protein kinase D1. J Cell Biochem 2008;104:82-95.
24. Gumbiner BM. Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell 1996;84:345-357
25. Takeichi M. Cadherin cell adhesion receptors as a morphogenetic regulator. Science 1991;251:1451-1455
26. Steinhusen U, Weiske J, Badock V, Tauber R, Bommert K, Huber O. Cleavage and shedding of E-cadherin after induction of apoptosis. J Biol Chem 2001;276:4972-4980
27. Fouquet S, Lugo-Martinez VH, Faussat AM, et al. Early loss of E-cadherin from cell-cell contacts is involved in the onset of Anoikis in enterocytes. J Biol Chem 2004;279:43061-43069
28. Noe V, Fingleton B, Jacobs K, et al. Release of an invasion promoter E-cadherin fragment by matrilysin and stromelysin-1. J Cell Sci 2001;114:111-118
29. Du C, Jaggi M, Zhang C, Balaji KC. Protein kinase D1-mediated phosphorylation and subcellular localization of β-catenin. Cancer Res 2009;69:1117-1124
30. Hassan S, Biswas MH, Zhang C, Du C, Balaji KC. Heat shock protein 27 mediates repression of androgen receptor function by protein kinase D1 in prostate cancer cells. Oncogene 2009.
31. Ruhul Amin AR, Uddin Biswas MH, Senga T, et al. A role for SHPS-1/ SIRPα in concanavalin A-dependent production of MMP-9. Genes Cells 2007;12:1023-1033
32. Mak P, Jaggi M, Syed V, et al. Protein kinase D1 (PKD1) influences androgen receptor (AR) function in prostate cancer cells. Biochem Biophys Res Commun 2008;373:618-623
33. Biswas MH, Hasegawa HH, Rahman MA, et al. SHP-2-Erk signaling regulates concanavalin A-dependent production of TIMP-2. Biochem Biophys Res Commun 2006;348:1145-1149
34. Gentleman RC, Carey VJ, Bates DM, et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 2004;5:R80.
35. Liu E, Thant AA, Kikkawa F, et al. The Ras-mitogen-activated protein kinase pathway is critical for the activation of matrix metalloproteinase secretion and the invasiveness in v-crk-transformed 3Y1. Cancer Res 2000;60:2361-2364
36. Zheng DQ, Woodard AS, Tallini G, Languino LR. Substrate specificity of α(v)β(3) integrin-mediated cell migration and phosphatidylinositol 3-kinase/AKT pathway activation. J Biol Chem 2000;275:24565-24574
37. Eliceiri BP, Klemke R, Stromblad S, Cheresh DA. Integrin αvβ3 requirement for sustained mitogen-activated protein kinase activity during angiogenesis. J Cell Biol 1998;140:1255-1263
38. Ito K, Okamoto I, Araki N, et al. Calcium influx triggers the sequential proteolysis of extracellular and cytoplasmic domains of E-cadherin, leading to loss of β-catenin from cell-cell contacts. Oncogene 1999; 18:7080-7090
39. Lopez-Otin C, Palavalli LH, Samuels Y. Protective roles of matrix metalloproteinases: from mouse models to human cancer. Cell Cycle 2009;8.
40. Lopez-Otin C, Matrisian LM. Emerging roles of proteases in tumour suppression. Nat Rev Cancer 2007;7:800-808
41. Cauwe B, Van den Steen PE, Opdenakker G. The biochemical, biological, and pathological kaleidoscope of cell surface substrates processed by matrix metalloproteinases. Crit Rev Biochem Mol Biol 2007;42:113-185
42. Protheroe AS, Banks RE, Mzimba M, et al. Urinary concentrations of the soluble adhesion molecule E-cadherin and total protein in patients with bladder cancer. Br J Cancer 1999;80:273-278
43. Kuefer R, Hofer MD, Gschwend JE, et al. The role of an 80 kDa fragment of E-cadherin in the metastatic progression of prostate cancer. Clin Cancer Res 2003;9:6447-6452
44. Zheng G, Lyons JG, Tan TK, et al. Disruption of E-cadherin by matrix metalloproteinase directly mediates epithelial-mesenchymal transition downstream of transforming growth factor-β1 in renal tubular epithelial cells. Am J Pathol 2009;175:580-591
45. Marambaud P, Shioi J, Serban G, et al. A presenilin-1/γ-secretase cleavage releases the E-cadherin intracellular domain and regulates disassembly of adherens junctions. EMBO J 2002;21:1948-1956
46. Klucky B, Mueller R, Vogt I, et al. Kallikrein 6 induces E-cadherin shedding and promotes cell proliferation, migration, and invasion. Cancer Res 2007;67:8198-8206
47. Lee KH, Choi EY, Hyun MS, et al. Association of extracellular cleavage of E-cadherin mediated by MMP-7 with HGF-induced in vitro invasion in human stomach cancer cells. Eur Surg Res 2007;39:208-215
48. Munshi HG, Stack MS. Reciprocal interactions between adhesion receptor signaling and MMP regulation. Cancer Metastasis Rev 2006;25:45-56.
49. Scorilas A, Karameris A, Arnogiannaki N, et al. Overexpression of matrix-metalloproteinase-9 in human breast cancer: a potential favourable indicator in node-negative patients. Br J Cancer 2001;84:1488-1496
50. Takeha S, Fujiyama Y, Bamba T, Sorsa T, Nagura H, Ohtani H. Stromal expression of MMP-9 and urokinase receptor is inversely associated with liver metastasis and with infiltrating growth in human colorectal cancer: a novel approach from immune/inflammatory aspect. Jpn J Cancer Res 1997;88:72-81.