Protein kinase D2 regulates migration and invasion of U87MG glioblastoma cells in vitro

Experimental Cell Research

Volumn 319, Issue 13, 2013, Pages 2037-2048

  Bernhart, Eva ^a   Damm, Sabine ^a   Wintersperger, Andrea ^a   DeVaney, Trevor ^a   Zimmer, Andreas ^b   Raynham, Tony ^c   Ireson, Christopher ^c   Sattler, Wolfgang ^a  

^a MEDICAL UNIVERSITY OF GRAZ   (Austria)

^b UNIVERSITY OF GRAZ   (Austria)

^c Cancer Research Technology Ltd   (United Kingdom)

Author keywords

C Jun; Glioblastoma; Invasion; MAPK; PRKD2; Sphingosine 1 phosphate

Indexed keywords

ALPHA2 INTEGRIN; ALPHA4 INTEGRIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERSTITIAL COLLAGENASE; MITOGENIC AGENT; PLASMINOGEN ACTIVATOR; PROTEIN C JUN; PROTEIN KINASE D; PROTEIN KINASE D2; SPHINGOSINE 1 PHOSPHATE; UNCLASSIFIED DRUG; UROKINASE; UROKINASE RECEPTOR;

ARTICLE; AUTOPHOSPHORYLATION; CELL INVASION; CELL MIGRATION; CELL MOTILITY; CHEMOTAXIS; DOWN REGULATION; ENZYME ACTIVATION; GENE EXPRESSION; GLIOBLASTOMA; GLIOMA CELL; IN VITRO STUDY; MICROSCOPY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

EID: 84879883626     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2013.03.029     Document Type: Article

References (73)

1. Stupp R., Mason W.P., van den Bent M.J., Weller M., Fisher B., Taphoorn M.J., Belanger K., Brandes A.A., Marosi C., Bogdahn U., Curschmann J., Janzer R.C., Ludwin S.K., Gorlia T., Allgeier A., Lacombe D., Cairncross J.G., Eisenhauer E., Mirimanoff R.O. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N. Engl. J. Med. 2005, 352:987-996.
2. Parsons D.W., Jones S., Zhang X., Lin J.C., Leary R.J., Angenendt P., Mankoo P., Carter H., Siu I.M., Gallia G.L., Olivi A., McLendon R., Rasheed B.A., Keir S., Nikolskaya T., Nikolsky Y., Busam D.A., Tekleab H., Diaz L.A., Hartigan J., Smith D.R., Strausberg R.L., Marie S.K., Shinjo S.M., Yan H., Riggins G.J., Bigner D.D., Karchin R., Papadopoulos N., Parmigiani G., Vogelstein B., Velculescu V.E., Kinzler K.W. An integrated genomic analysis of human glioblastoma multiforme. Science 2008, 321:1807-1812.
3. The Cancer Genome Atlas Research Network, Comprehensive genomic characterization defines human glioblastoma genes and core pathways, Nature 455 (2008) 1061-1068.
4. Hadjipanayis C.G., Van Meir E.G. Tumor initiating cells in malignant gliomas: biology and implications for therapy. J. Mol. Med. (Berl) 2009, 87:363-374.
5. Friedl P., Locker J., Sahai E., Segall J.E. Classifying collective cancer cell invasion. Nat. Cell Biol. 2012, 14:777-783.
6. Reardon D.A., Rich J.N., Friedman H.S., Bigner D.D. Recent advances in the treatment of malignant astrocytoma. J. Clin. Oncol. 2006, 24:1253-1265.
7. Onishi M., Ichikawa T., Kurozumi K., Date I. Angiogenesis and invasion in glioma. Brain Tumor Pathol. 2011, 28:13-24.
8. Griner E.M., Kazanietz M.G. Protein kinase C and other diacylglycerol effectors in cancer. Nat. Rev. Cancer 2007, 7:281-294.
9. Fu Y., Rubin C.S. Protein kinase D: coupling extracellular stimuli to the regulation of cell physiology. EMBO Rep. 2011, 12:785-796.
10. LaValle C.R., George K.M., Sharlow E.R., Lazo J.S., Wipf P., Wang Q.J. Protein kinase D as a potential new target for cancer therapy. Biochim. Biophys. Acta 1806, 2010:183-192.
11. Trauzold A., Schmiedel S., Sipos B., Wermann H., Westphal S., Roder C., Klapper W., Arlt A., Lehnert L., Ungefroren H., Johannes F.J., Kalthoff H. PKCmu prevents CD95-mediated apoptosis and enhances proliferation in pancreatic tumour cells. Oncogene 2003, 22:8939-8947.
12. Ochi N., Tanasanvimon S., Matsuo Y., Tong Z., Sung B., Aggarwal B.B., Sinnett-Smith J., Rozengurt E., Guha S. Protein kinase D1 promotes anchorage-independent growth, invasion, and angiogenesis by human pancreatic cancer cells. J. Cell Physiol. 2011, 226:1074-1081.
13. Harikumar K.B., Kunnumakkara A.B., Ochi N., Tong Z., Deorukhkar A., Sung B., Kelland L., Jamieson S., Sutherland R., Raynham T., Charles M., Bagherzadeh A., Foxton C., Boakes A., Farooq M., Maru D., Diagaradjane P., Matsuo Y., Sinnett-Smith J., Gelovani J., Krishnan S., Aggarwal B.B., Rozengurt E., Ireson C.R., Guha S. A novel small-molecule inhibitor of protein kinase D blocks pancreatic cancer growth in vitro and in vivo. Mol. Cancer Ther. 2010, 9:1136-1146.
14. Chen J., Deng F., Singh S.V., Wang Q.J. 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.
15. Zou Z., Zeng F., Xu W., Wang C., Ke Z., Wang Q.J., Deng F. PKD2 and PKD3 Promote Prostate Cancer Cell Invasion via uPA by Shifting Balance Between NF-kappaB and HDAC1. J. Cell Sci. 2012, 125:4800-4811.
16. Mihailovic T., Marx M., Auer A., Van Lint J., Schmid M., Weber C., Seufferlein T. Protein kinase D2 mediates activation of nuclear factor kappaB by Bcr-Abl in Bcr-Abl+ human myeloid leukemia cells. Cancer Res. 2004, 64:8939-8944.
17. Kovalevska L.M., Yurchenko O.V., Shlapatska L.M., Berdova G.G., Mikhalap S.V., Van Lint J., Sidorenko S.P. Immunohistochemical studies of protein kinase D (PKD) 2 expression in malignant human lymphomas. Exp. Oncol. 2006, 28:225-230.
18. Azoitei N., Kleger A., Schoo N., Thal D.R., Brunner C., Pusapati G.V., Filatova A., Genze F., Moller P., Acker T., Kuefer R., Van Lint J., Baust H., Adler G., Seufferlein T. Protein kinase D2 is a novel regulator of glioblastoma growth and tumor formation. Neuro. Oncol. 2011, 13:710-724.
19. Prigozhina N.L., Waterman-Storer C.M. Protein kinase D-mediated anterograde membrane trafficking is required for fibroblast motility. Curr. Biol. 2004, 14:88-98.
20. Woods A.J., White D.P., Caswell P.T., Norman J.C. PKD1/PKCmu promotes alphavbeta3 integrin recycling and delivery to nascent focal adhesions. EMBO J. 2004, 23:2531-2543.
21. De Kimpe L., Janssens K., Derua R., Armacki M., Goicoechea S., Otey C., Waelkens E., Vandoninck S., Vandenheede J.R., Seufferlein T., Van Lint J. Characterization of cortactin as an in vivo protein kinase D substrate: interdependence of sites and potentiation by Src. Cell Signal. 2009, 21:253-263.
22. Eiseler T., Doppler H., Yan I.K., Kitatani K., Mizuno K., Storz P. Protein kinase D1 regulates cofilin-mediated F-actin reorganization and cell motility through slingshot. Nat. Cell Biol. 2009, 11:545-556.
23. Watkins J.L., Lewandowski K.T., Meek S.E., Storz P., Toker A., Piwnica-Worms H. Phosphorylation of the Par-1 polarity kinase by protein kinase D regulates 14-3-3 binding and membrane association. Proc. Natl. Acad. Sci. USA 2008, 105:18378-18383.
24. Eiseler T., Doppler H., Yan I.K., Goodison S., Storz P. Protein kinase D1 regulates matrix metalloproteinase expression and inhibits breast cancer cell invasion. Breast Cancer Res.: 2009, 11:R13.
25. Anand M., Van Meter T.E., Fillmore H.L. Epidermal growth factor induces matrix metalloproteinase-1 (MMP-1) expression and invasion in glioma cell lines via the MAPK pathway. J. Neurooncol. 2011, 104:679-687.
26. Pyne N.J., Pyne S. Sphingosine 1-phosphate and cancer. Nat. Rev. Cancer 2010, 10:489-503.
27. Van Brocklyn J., Letterle C., Snyder P., Prior T. Sphingosine-1-phosphate stimulates human glioma cell proliferation through Gi-coupled receptors: role of ERK MAP kinase and phosphatidylinositol 3-kinase beta. Cancer Lett. 2002, 181:195-204.
28. Van Brocklyn J.R., Young N., Roof R. Sphingosine-1-phosphate stimulates motility and invasiveness of human glioblastoma multiforme cells. Cancer Lett. 2003, 199:53-60.
29. Annabi B., Lachambre M.P., Plouffe K., Sartelet H., Beliveau R. Modulation of invasive properties of CD133+ glioblastoma stem cells: a role for MT1-MMP in bioactive lysophospholipid signaling. Mol. Carcinog. 2009, 48:910-919.
30. Young N., Pearl D.K., Van Brocklyn J.R. Sphingosine-1-phosphate regulates glioblastoma cell invasiveness through the urokinase plasminogen activator system and CCN1/Cyr61. Mol. Cancer Res. 2009, 7:23-32.
31. Bryan L., Paugh B.S., Kapitonov D., Wilczynska K.M., Alvarez S.M., Singh S.K., Milstien S., Spiegel S., Kordula T. Sphingosine-1-phosphate and interleukin-1 independently regulate plasminogen activator inhibitor-1 and urokinase-type plasminogen activator receptor expression in glioblastoma cells: implications for invasiveness. Mol. Cancer Res. 2008, 6:1469-1477.
32. Guha S., Tanasanvimon S., Sinnett-Smith J., Rozengurt E. Role of protein kinase D signaling in pancreatic cancer. Biochem. Pharmacol. 2010, 80:1946-1954.
33. Hao Q., Wang L., Zhao Z.J., Tang H. Identification of protein kinase D2 as a pivotal regulator of endothelial cell proliferation, migration, and angiogenesis. J. Biol. Chem. 2009, 284:799-806.
34. Azoitei N., Pusapati G.V., Kleger A., Moller P., Kufer R., Genze F., Wagner M., van Lint J., Carmeliet P., Adler G., Seufferlein T. Protein kinase D2 is a crucial regulator of tumour cell-endothelial cell communication in gastrointestinal tumours. Gut 2010, 59:1316-1330.
35. M. Armacki, G. Joodi, S.C. Nimmagadda, L. de Kimpe, G.V. Pusapati, S. Vandoninck, J. Van Lint, A. Illing and T. Seufferlein. A novel splice variant of calcium and integrin-binding protein 1 mediates protein kinase D2-stimulated tumour growth by regulating angiogenesis, Oncogene, http://dx.doi.org/10.1038/onc.2013.43.
36. Pfaffl M.W., Horgan G.W., Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 2002, 30:e36.
37. Leppa S., Saffrich R., Ansorge W., Bohmann D. Differential regulation of c-Jun by ERK and JNK during PC12 cell differentiation. EMBO J. 1998, 17:4404-4413.
38. Kim R.H., Takabe K., Milstien S., Spiegel S. Export and functions of sphingosine-1-phosphate. Biochim. Biophys. Acta 1791, 2009:692-696.
39. Van Brocklyn J.R., Jackson C.A., Pearl D.K., Kotur M.S., Snyder P.J., Prior T.W. Sphingosine kinase-1 expression correlates with poor survival of patients with glioblastoma multiforme: roles of sphingosine kinase isoforms in growth of glioblastoma cell lines. J. Neuropathol. Exp. Neurol. 2005, 64:695-705.
40. Yoshida Y., Nakada M., Sugimoto N., Harada T., Hayashi Y., Kita D., Uchiyama N., Yachie A., Takuwa Y., Hamada J. Sphingosine-1-phosphate receptor type 1 regulates glioma cell proliferation and correlates with patient survival. Int. J. Cancer 2010, 126:2341-2352.
41. Natarajan J., Berrar D., Dubitzky W., Hack C., Zhang Y., DeSesa C., Van Brocklyn J.R., Bremer E.G. Text mining of full-text journal articles combined with gene expression analysis reveals a relationship between sphingosine-1-phosphate and invasiveness of a glioblastoma cell line. BMC Bioinf. 2006, 7:373.
42. Kalluri R., Weinberg R.A. The basics of epithelial-mesenchymal transition. J. Clin. Invest. 2009, 119:1420-1428.
43. Karam M., Legay C., Auclair C., Ricort J.M. Protein kinase D1 stimulates proliferation and enhances tumorigenesis of MCF-7 human breast cancer cells through a MEK/ERK-dependent signaling pathway. Exp. Cell Res. 2012, 318:558-569.
44. Kim do Y., Jung M.S., Park Y.G., Yuan H.D., Quan H.Y., Chung S.H. Ginsenoside Rh2(S) induces the differentiation and mineralization of osteoblastic MC3T3-E1 cells through activation of PKD and p38 MAPK pathways. BMB Rep. 2011, 44:659-664.
45. Sinnett-Smith J., Zhukova E., Rey O., Rozengurt E. Protein kinase D2 potentiates MEK/ERK/RSK signaling, c-Fos accumulation and DNA synthesis induced by bombesin in Swiss 3T3 cells. J. Cell Physiol. 2007, 211:781-790.
46. Lin C.W., Shen S.C., Chien C.C., Yang L.Y., Shia L.T., Chen Y.C. 12-O-tetradecanoylphorbol-13-acetate-induced invasion/migration of glioblastoma cells through activating PKCalpha/ERK/NF-kappaB-dependent MMP-9 expression. J. Cell Physiol. 2010, 225:472-481.
47. Lai C.F., Chaudhary L., Fausto A., Halstead L.R., Ory D.S., Avioli L.V., Cheng S.L. Erk is essential for growth, differentiation, integrin expression, and cell function in human osteoblastic cells. J. Biol. Chem. 2001, 276:14443-14450.
48. Huang C., Jacobson K., Schaller M.D. MAP kinases and cell migration. J. Cell Sci. 2004, 117:4619-4628.
49. Vial E., Sahai E., Marshall C.J. ERK-MAPK signaling coordinately regulates activity of Rac1 and RhoA for tumor cell motility. Cancer Cell 2003, 4:67-79.
50. Botta G.P., Reginato M.J., Reichert M., Rustgi A.K., Lelkes P.I. Constitutive K-RasG12D activation of ERK2 specifically regulates 3D invasion of human pancreatic cancer cells via MMP-1. Mol. Cancer Res. 2012, 10:183-196.
51. Eke I., Storch K., Kastner I., Vehlow A., Faethe C., Mueller-Klieser W., Taucher-Scholz G., Temme A., Schackert G., Cordes N. Three-dimensional Invasion of human glioblastoma cells remains unchanged by X-ray and carbon ion irradiation in vitro. Int. J. Radiat. Oncol. Biol. Phys. 2012, 84:e515-523.
52. Matsuda K., Sato A., Okada M., Shibuya K., Seino S., Suzuki K., Watanabe E., Narita Y., Shibui S., Kayama T., Kitanaka C. Targeting JNK for therapeutic depletion of stem-like glioblastoma cells. Sc. Rep. 2012, 2:516.
53. Yoon C.H., Kim M.J., Kim R.K., Lim E.J., Choi K.S., An S., Hwang S.G., Kang S.G., Suh Y., Park M.J., Lee S.J. c-Jun N-terminal kinase has a pivotal role in the maintenance of self-renewal and tumorigenicity in glioma stem-like cells. Oncogene 2012, 31:4655-4666.
54. Kozuka-Hata H., Nasu-Nishimura Y., Koyama-Nasu R., Ao-Kondo H., Tsumoto K., Akiyama T., Oyama M. Phosphoproteome of human glioblastoma initiating cells reveals novel signaling regulators encoded by the transcriptome. PLoS One 2012, 7:e43398.
55. Karin M. The regulation of AP-1 activity by mitogen-activated protein kinases. J. Biol. Chem. 1995, 270:16483-16486.
56. Han J., Jiang Y., Li Z., Kravchenko V.V., Ulevitch R.J. Activation of the transcription factor MEF2C by the MAP kinase p38 in inflammation. Nature 1997, 386:296-299.
57. Musti A.M., Treier M., Bohmann D. Reduced ubiquitin-dependent degradation of c-Jun after phosphorylation by MAP kinases. Science 1997, 275:400-402.
58. Lopez-Bergami P., Huang C., Goydos J.S., Yip D., Bar-Eli M., Herlyn M., Smalley K.S., Mahale A., Eroshkin A., Aaronson S., Ronai Z. Rewired ERK-JNK signaling pathways in melanoma. Cancer Cell 2007, 11:447-460.
59. Waldron R.T., Whitelegge J.P., Faull K.F., Rozengurt E. Identification of a novel phosphorylation site in c-jun directly targeted in vitro by protein kinase D. Biochem. Biophys. Res. Commun. 2007, 356:361-367.
60. Blau L., Knirsh R., Ben-Dror I., Oren S., Kuphal S., Hau P., Proescholdt M., Bosserhoff A.K., Vardimon L. Aberrant expression of c-Jun in glioblastoma by internal ribosome entry site (IRES)-mediated translational activation. Proc. Natl. Acad. Sci. USA 2012, 109:E2875-2884.
61. Eriksson M., Arminen L., Karjalainen-Lindsberg M.L., Leppa S. AP-1 regulates alpha2beta1 integrin expression by ERK-dependent signals during megakaryocytic differentiation of K562 cells. Exp. Cell Res. 2005, 304:175-186.
62. Amos S., Redpath G.T., Dipierro C.G., Carpenter J.E., Hussaini I.M. Epidermal growth factor receptor-mediated regulation of urokinase plasminogen activator expression and glioblastoma invasion via C-SRC/MAPK/AP-1 signaling pathways. J. Neuropathol. Exp. Neurol. 2010, 69:582-592.
63. Mittelstadt M.L., Patel R.C. AP-1 mediated transcriptional repression of matrix metalloproteinase-9 by recruitment of histone deacetylase 1 in response to interferon beta. PLoS One 2012, 7:e42152.
64. Desgrosellier J.S., Cheresh D.A. Integrins in cancer: biological implications and therapeutic opportunities. Nat. Rev. Cancer 2010, 10:9-22.
65. Ou J., Luan W., Deng J., Sa R., Liang H. alphaV integrin induces multicellular radioresistance in human nasopharyngeal carcinoma via activating SAPK/JNK pathway. PLoS One 2012, 7:e38737.
66. Naci D., El Azreq M.A., Chetoui N., Lauden L., Sigaux F., Charron D., Al-Daccak R., Aoudjit F. alpha2beta1 integrin promotes chemoresistance against doxorubicin in cancer cells through extracellular signal-regulated kinase (ERK). J. Biol. Chem. 2012, 287:17065-17076.
67. Chamberlain M.C., Cloughsey T., Reardon D.A., Wen P.Y. A novel treatment for glioblastoma: integrin inhibition. Expert Rev. Neurother. 2012, 12:421-435.
68. Reardon D.A., Fink K.L., Mikkelsen T., Cloughesy T.F., O'Neill A., Plotkin S., Glantz M., Ravin P., Raizer J.J., Rich K.M., Schiff D., Shapiro W.R., Burdette-Radoux S., Dropcho E.J., Wittemer S.M., Nippgen J., Picard M., Nabors L.B. Randomized phase II study of cilengitide, an integrin-targeting arginine-glycine-aspartic acid peptide, in recurrent glioblastoma multiforme. J. Clin. Oncol. 2008, 26:5610-5617.
69. Salajegheh M., Rudnicki A., Smith T.W. Expression of urokinase-type plasminogen activator receptor (uPAR) in primary central nervous system neoplasms. Appl. Immunohistochem. Mol. Morphol. 2005, 13:184-189.
70. Blasi F., Carmeliet P. uPAR: a versatile signalling orchestrator. Nat. Rev. Mol. Cell Biol. 2002, 3:932-943.
71. Raghu H., Gondi C.S., Dinh D.H., Gujrati M., Rao J.S. Specific knockdown of uPA/uPAR attenuates invasion in glioblastoma cells and xenografts by inhibition of cleavage and trafficking of Notch -1 receptor. Mol. Cancer 2011, 10:130.
72. Stojic J., Hagemann C., Haas S., Herbold C., Kuhnel S., Gerngras S., Roggendorf W., Roosen K., Vince G.H. Expression of matrix metalloproteinases MMP-1, MMP-11 and MMP-19 is correlated with the WHO-grading of human malignant gliomas. Neurosci. Res. 2008, 60:40-49.
73. Navarro M.N., Sinclair L.V., Feijoo-Carnero C., Clarke R., Matthews S.A., Cantrell D.A. Protein kinase D2 has a restricted but critical role in T-cell antigen receptor signalling in mature T-cells. Biochem. J. 2012, 442:649-659.