Protein kinase D1 regulates matrix metalloproteinase expression and inhibits breast cancer cell invasion

Breast Cancer Research

Volumn 11, Issue 1, 2009, Pages

  Eiseler, Tim ^a   Döppler, Heike ^a   Yan, Irene K ^a   Goodison, Steve ^b   Storz, Peter ^a  

^a MAYO CLINIC   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGENASE 3; GELATINASE A; GELATINASE B; MATRILYSIN; MATRIX METALLOPROTEINASE; MATRIX METALLOPROTEINASE 14; MATRIX METALLOPROTEINASE 15; PROTEIN KINASE D; PROTEIN KINASE D1; PROTEIN SERINE THREONINE KINASE; SHORT HAIRPIN RNA; STROMELYSIN 2; STROMELYSIN 3; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 2; TUMOR MARKER; UNCLASSIFIED DRUG; MESSENGER RNA; PROTEIN KINASE C;

ARTICLE; BREAST CANCER; CANCER INVASION; CONTROLLED STUDY; DNA METHYLATION; ENZYME ACTIVITY; EPIGENETICS; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; BREAST TUMOR; CELL ADHESION; CELL MOTION; CELL PROLIFERATION; CULTURE TECHNIQUE; ENZYME IMMUNOASSAY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOPRECIPITATION; LYMPH NODE METASTASIS; METABOLISM; METASTASIS; MULTICELLULAR SPHEROID; PAGET NIPPLE DISEASE; PATHOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL LINE; WESTERN BLOTTING;

BLOTTING, WESTERN; BREAST NEOPLASMS; CARCINOMA, DUCTAL, BREAST; CELL ADHESION; CELL CULTURE TECHNIQUES; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOENZYME TECHNIQUES; IMMUNOPRECIPITATION; LYMPHATIC METASTASIS; MATRIX METALLOPROTEINASES; NEOPLASM INVASIVENESS; PROTEIN KINASE C; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SPHEROIDS, CELLULAR;

EID: 67549112510     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/bcr2232     Document Type: Article

References (49)

1. Storz P, Doppler H, Toker A. Protein kinase D mediates mitochondrion-to-nucleus signaling and detoxification from mitochondrial reactive oxygen species. Mol Cell Biol 2005, 25:8520-8530. 1265746, 16166634, 10.1128/MCB.25.19.8520-8530.2005.
2. Rykx A, De Kimpe L, Mikhalap S, Vantus T, Seufferlein T, Vandenheede JR, Van Lint J. Protein kinase D: a family affair. FEBS letters 2003, 546:81-86. 10.1016/S0014-5793(03)00487-3, 12829240.
3. Hausser A, Storz P, Martens S, Link G, Toker A, Pfizenmaier K. Protein kinase D regulates vesicular transport by phosphorylating and activating phosphatidylinositol-4 kinase IIIbeta at the Golgi complex. Nat Cell Biol 2005, 7:880-886. 1458033, 16100512, 10.1038/ncb1289.
4. Bowden ET, Barth M, Thomas D, Glazer RI, Mueller SC. An invasion-related complex of cortactin, paxillin and PKCmu associates with invadopodia at sites of extracellular matrix degradation. Oncogene 1999, 18:4440-4449. 10.1038/sj.onc.1202827, 10442635.
5. Endo K, Oki E, Biedermann V, Kojima H, Yoshida K, Johannes FJ, Kufe D, Datta R. Proteolytic cleavage and activation of protein kinase C μ by caspase-3 in the apoptotic response of cells to 1-beta-D-arabinofuranosylcytosine and other genotoxic agents. J Biol Chem 2000, 275:18476-18481. 10.1074/jbc.M002266200, 10764790.
6. Palmantier R, Roberts JD, Glasgow WC, Eling T, Olden K. Regulation of the adhesion of a human breast carcinoma cell line to type IV collagen and vitronectin: roles for lipoxygenase and protein kinase C. Cancer Res 1996, 56:2206-2212.
7. Rozengurt E, Rey O, Waldron RT. Protein kinase D signaling. J Biol Chem 2005, 280:13205-13208. 10.1074/jbc.R500002200, 15701647.
8. Storz P, Toker A. Protein kinase D mediates a stress-induced NF-kappaB activation and survival pathway. EMBO journal 2003, 22:109-120. 140053, 12505989, 10.1093/emboj/cdg009.
9. Storz P. Reactive oxygen species in tumor progression. Front Biosci 2005, 10:1881-1896. 10.2741/1667, 15769673.
10. Eiseler T, Schmid MA, Topbas F, Pfizenmaier K, Hausser A. PKD is recruited to sites of actin remodelling at the leading edge and negatively regulates cell migration. FEBS letters 2007, 581:4279-4287. 10.1016/j.febslet.2007.07.079, 17707375.
11. Song J, Li J, Lulla A, Evers BM, Chung DH. Protein kinase D protects against oxidative stress-induced intestinal epithelial cell injury via Rho/ROK/PKC-δ pathway activation. Am J Physiol Cell Physiol 2006, 290:C1469-C1476. 2613753, 16421204, 10.1152/ajpcell.00486.2005.
12. Simpson KJ, Dugan AS, Mercurio AM. Functional analysis of the contribution of RhoA and RhoC GTPases to invasive breast carcinoma. Cancer Res 2004, 64:8694-8701. 10.1158/0008-5472.CAN-04-2247, 15574779.
13. Wang W, Eddy R, Condeelis J. The cofilin pathway in breast cancer invasion and metastasis. Nat Rev Cancer 2007, 7:429-440. 10.1038/nrc2148, 17522712.
14. Jaggi M, Rao PS, Smith DJ, Hemstreet GP, Balaji KC. Protein kinase C mu is down-regulated in androgen-independent prostate cancer. Biochem Biophys Res Commun 2003, 307:254-260. 10.1016/S0006-291X(03)01161-6, 12859948.
15. Kim M, Jang HR, Kim JH, Noh SM, Song KS, Cho JS, Jeong HY, Norman JC, Caswell PT, Kang GH, Kim SY, Yoo HS, Kim YS. Epigenetic inactivation of protein kinase D1 in gastric cancer and its role in gastric cancer cell migration and invasion. Carcinogenesis 2008, 29:629-637. 10.1093/carcin/bgm291, 18283041.
16. Egeblad M, Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer 2002, 2:161-174. 10.1038/nrc745, 11990853.
17. Sternlicht MD, Lochter A, Sympson CJ, Huey B, Rougier JP, Gray JW, Pinkel D, Bissell MJ, Werb Z. The stromal proteinase MMP3/stromelysin-1 promotes mammary carcinogenesis. Cell 1999, 98:137-146. 10.1016/S0092-8674(00)81009-0, 10428026.
18. Coussens LM, Fingleton B, Matrisian LM. Matrix metalloproteinase inhibitors and cancer: trials and tribulations. Science 2002, 295:2387-2392. 10.1126/science.1067100, 11923519.
19. Chabottaux V, Noel A. Matrix metalloproteinases to predict breast cancer metastases. Clin Lab Int 2007, 8-10.
20. Duffy MJ, Maguire TM, Hill A, McDermott E, O'Higgins N. Metalloproteinases: role in breast carcinogenesis, invasion and metastasis. Breast Cancer Res 2000, 2:252-257. 138784, 11250717, 10.1186/bcr65.
21. Martin M, Matrisian L. Matrix metalloproteinases as prognostic factors for cancer. Clin Lab Int 2004, 16-18.
22. Zhang B, Cao X, Liu Y, Cao W, Zhang F, Zhang S, Li H, Ning L, Fu L, Niu Y, Niu R, Sun B, Hao X. Tumor-derived matrix metalloproteinase-13 (MMP-13) correlates with poor prognoses of invasive breast cancer. BMC Cancer 2008, 8:83. 2362123, 18373849, 10.1186/1471-2407-8-83.
23. Matrisian LM. Metalloproteinases and their inhibitors in matrix remodeling. Trends Genet 1990, 6:121-125. 10.1016/0168-9525(90)90126-Q, 2132731.
24. Turpeenniemi-Hujanen T. Gelatinases (MMP-2 and -9) and their natural inhibitors as prognostic indicators in solid cancers. Biochimie 2005, 87:287-297. 10.1016/j.biochi.2005.01.014, 15781315.
25. Minn AJ, Gupta GP, Siegel PM, Bos PD, Shu W, Giri DD, Viale A, Olshen AB, Gerald WL, Massague J. Genes that mediate breast cancer metastasis to lung. Nature 2005, 436:518-524. 1283098, 16049480, 10.1038/nature03799.
26. Gupta GP, Nguyen DX, Chiang AC, Bos PD, Kim JY, Nadal C, Gomis RR, Manova-Todorova K, Massague J. Mediators of vascular remodelling co-opted for sequential steps in lung metastasis. Nature 2007, 446:765-770. 10.1038/nature05760, 17429393.
27. Nelson KK, Melendez JA. Mitochondrial redox control of matrix metalloproteinases. Free Radic Biol Med 2004, 37:768-784. 10.1016/j.freeradbiomed.2004.06.008, 15304253.
28. Thomas P, Khokha R, Shepherd FA, Feld R, Tsao MS. Differential expression of matrix metalloproteinases and their inhibitors in non-small cell lung cancer. J Pathol 2000, 190:150-156. 10.1002/(SICI)1096-9896(200002)190:2<150::AID-PATH510>3.0.CO;2-W, 10657012.
29. Westermarck J, Kahari VM. Regulation of matrix metalloproteinase expression in tumor invasion. Faseb J 1999, 13:781-792.
30. Liu LT, Chang HC, Chiang LC, Hung WC. Histone deacetylase inhibitor up-regulates RECK to inhibit MMP-2 activation and cancer cell invasion. Cancer Res 2003, 63:3069-3072.
31. Klampfer L, Huang J, Shirasawa S, Sasazuki T, Augenlicht L. Histone deacetylase inhibitors induce cell death selectively in cells that harbor activated kRasV12: The role of signal transducers and activators of transcription 1 and p21. Cancer Res 2007, 67:8477-8485. 10.1158/0008-5472.CAN-07-0210, 17875686.
32. Bartsch JE, Staren ED, Appert HE. Matrix metalloproteinase expression in breast cancer. J Surg Res 2003, 110:383-392. 10.1016/S0022-4804(03)00007-6, 12788669.
33. Jauliac S, Lopez-Rodriguez C, Shaw LM, Brown LF, Rao A, Toker A. The role of NFAT transcription factors in integrin-mediated carcinoma invasion. Nature Cell Biol 2002, 4:540-544. 10.1038/ncb816, 12080349.
34. Leber TM, Balkwill FR. Zymography: a single-step staining method for quantitation of proteolytic activity on substrate gels. Anal Biochem 1997, 249:24-28. 10.1006/abio.1997.2170, 9193704.
35. Storz P. Mitochondrial ROS - radical detoxification, mediated by protein kinase D. Trends Cell Biol 2007, 17:13-18. 10.1016/j.tcb.2006.11.003, 17126550.
36. Wang F, Hansen RK, Radisky D, Yoneda T, Barcellos-Hoff MH, Petersen OW, Turley EA, Bissell MJ. Phenotypic reversion or death of cancer cells by altering signaling pathways in three-dimensional contexts. J Natl Cancer Inst 2002, 94:1494-1503.
37. Hegedus L, Cho H, Xie X, Eliceiri GL. Additional MDA-MB-231 breast cancer cell matrix metalloproteinases promote invasiveness. J Cell Physiol 2008, 216:480-485. 10.1002/jcp.21417, 18286480.
38. Hotary K, Li XY, Allen E, Stevens SL, Weiss SJ. A cancer cell metalloprotease triad regulates the basement membrane transmigration program. Genes Dev 2006, 20:2673-2686. 1578694, 16983145, 10.1101/gad.1451806.
39. Ramos-DeSimone N, Hahn-Dantona E, Sipley J, Nagase H, French DL, Quigley JP. Activation of matrix metalloproteinase-9 (MMP-9) via a converging plasmin/stromelysin-1 cascade enhances tumor cell invasion. J Biol Chem 1999, 274:13066-13076. 10.1074/jbc.274.19.13066, 10224058.
40. Farina AR, Tacconelli A, Cappabianca L, Gulino A, Mackay AR. Inhibition of human MDA-MB-231 breast cancer cell invasion by matrix metalloproteinase 3 involves degradation of plasminogen. Eur J Biochem 2002, 269:4476-4483. 10.1046/j.1432-1033.2002.03142.x, 12230559.
41. Farmer P, Bonnefoi H, Becette V, Tubiana-Hulin M, Fumoleau P, Larsimont D, Macgrogan G, Bergh J, Cameron D, Goldstein D, Duss S, Nicoulaz AL, Brisken C, Fiche M, Delorenzi M, Iggo R. Identification of molecular apocrine breast tumours by microarray analysis. Oncogene 2005, 24:4660-4671. 10.1038/sj.onc.1208561, 15897907.
42. Perou CM, Sorlie T, Eisen MB, Rijn M, Jeffrey SS, Rees CA, Pollack JR, Ross DT, Johnsen H, Akslen LA, Fluge O, Pergamenschikov A, Williams C, Zhu SX, Lønning PE, Børresen-Dale AL, Brown PO, Botstein D. Molecular portraits of human breast tumours. Nature 2000, 406:747-752. 10.1038/35021093, 10963602.
43. Vijver MJ, He YD, van't Veer LJ, Dai H, Hart AA, Voskuil DW, Schreiber GJ, Peterse JL, Roberts C, Marton MJ, Parrish M, Atsma D, Witteveen A, Glas A, Delahaye L, Velde T, Bartelink H, Rodenhuis S, Rutgers ET, Friend SH, Bernards R. A gene-expression signature as a predictor of survival in breast cancer. N Engl J Med 2002, 347:1999-2009. 10.1056/NEJMoa021967, 12490681.
44. van 't Veer LJ, Dai H, Vijver MJ, He YD, Hart AA, Mao M, Peterse HL, Kooy K, Marton MJ, Witteveen AT, Schreiber GJ, Kerkhoven RM, Roberts C, Linsley PS, Bernards R, Friend SH. Gene expression profiling predicts clinical outcome of breast cancer. Nature 2002, 415:530-536. 10.1038/415530a, 11823860.
45. Turashvili G, Bouchal J, Baumforth K, Wei W, Dziechciarkova M, Ehrmann J, Klein J, Fridman E, Skarda J, Srovnal J, Hajduch M, Murray P, Kolar Z. Novel markers for differentiation of lobular and ductal invasive breast carcinomas by laser microdissection and microarray analysis. BMC Cancer 2007, 7:55. 1852112, 17389037, 10.1186/1471-2407-7-55.
46. Poola I, DeWitty RL, Marshalleck JJ, Bhatnagar R, Abraham J, Leffall LD. Identification of MMP-1 as a putative breast cancer predictive marker by global gene expression analysis. Nat Med 2005, 11:481-483. 10.1038/nm1243, 15864312.
47. Chen J, Deng F, Singh SV, Wang QJ. Protein kinase D3 (PKD3) contributes to prostate cancer cell growth and survival through a PKCepsilon/PKD3 pathway downstream of Akt and ERK 1/2. Cancer Res 2008, 68:3844-3853. 10.1158/0008-5472.CAN-07-5156, 18483269.
48. Yoeli-Lerner M, Yiu GK, Rabinovitz I, Erhardt P, Jauliac S, Toker A. Akt blocks breast cancer cell motility and invasion through the transcription factor NFAT. Mol Cell 2005, 20:539-550. 10.1016/j.molcel.2005.10.033, 16307918.
49. Ha CH, Wang W, Jhun BS, Wong C, Hausser A, Pfizenmaier K, McKinsey TA, Olson EN, Jin ZG. Protein kinase D-dependent phosphorylation and nuclear export of histone deacetylase 5 mediates vascular endothelial growth factor-induced gene expression and angiogenesis. J Biol Chem 2008, 283:14590-14599. 10.1074/jbc.M800264200, 18332134.