Analysis of substrates of protein kinase C isoforms in human breast cells by the traceable kinase method

Biochemistry

Volumn 51, Issue 36, 2012, Pages 7087-7097

  Chen, Xiangyu ^a,b   Zhao, Xin ^a,b   Abeyweera, Thushara P ^a,b   Rotenberg, Susan A ^a  

^a CITY UNIVERSITY OF NEW YORK   (United States)

^b CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HUMAN BREAST; IN-VITRO; ISOFORMS; MEMBRANE-PERMEABLE; NONRADIOACTIVE; PHOSPHORYLATION REACTIONS; POTENTIAL SUBSTRATE; PROTEIN KINASE C; WESTERN BLOTTING;

ENZYMES; MASS SPECTROMETRY; PHOSPHORYLATION; PROTEINS; STOICHIOMETRY;

SUBSTRATES;

ADENOSINE TRIPHOSPHATE; CDC42 EFFECTOR PROTEIN 4; DIACYLGLYCEROL; ENZYME ANTIBODY; GUANOSINE TRIPHOSPHATASE; LACTONE; MUTANT PROTEIN; PROTEIN; PROTEIN KINASE C ALPHA; PROTEIN KINASE C DELTA; PROTEIN KINASE C ZETA; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BREAST CELL; CELL STRAIN MCF 7; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ANALYSIS; ENZYME ISOLATION; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE; ENZYME SUBSTRATE COMPLEX; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN EXPRESSION; STOICHIOMETRY; WESTERN BLOTTING;

AMINO ACID SEQUENCE; BREAST; CELL LINE, TUMOR; ENZYME ASSAYS; HUMANS; INTRACELLULAR SPACE; ISOENZYMES; MUTAGENESIS, SITE-DIRECTED; MUTATION; PHOSPHORYLATION; PLASMIDS; PROTEIN BINDING; PROTEIN KINASE C; RNA, SMALL INTERFERING;

EID: 84866090827     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi300999c     Document Type: Article

References (45)

1. Sun, X.-g. and Rotenberg, S. A. (1999) Over-expression of PKCα in MCF-10A human breast cells engenders dramatic alterations in morphology, proliferation and motility Cell Growth Differ. 10, 343-352 (Pubitemid 29242600)
2. Steinberg, S. F. (2008) Structural basis of protein kinase C isoform function Physiol. Rev. 88, 1341-1378
3. Teicher, B. A. (2006) Protein kinase C as a therapeutic target Clin. Cancer Res. 12, 5336-5345 (Pubitemid 44497246)
4. Konopatskaya, O. and Poole, A. W. (2010) Protein kinase Cα: Disease regulator and therapeutic target Trends Pharmacol. Sci. 31, 8-14
5. Larsson, C. (2006) Protein kinase C and regulation of the actin cytoskeleton Cell. Signalling 18, 276-284 (Pubitemid 41661343)
6. Ghoul, A., Serova, M., Benhadji, K. A., Cvitkovic, E., Faivre, S., Philips, E., Calvo, F., Lokiec, F., and Raymond, E. (2006) Protein kinase C α and δ are members of a large family of high potential for anticancer targeted therapy Targeted Oncology 1, 42-53 (Pubitemid 44088127)
7. Lonne, G. K., Cornmark, L., Zahirovic, I. O., Landberg, G., Jirstrom, K., and Larsson, C. (2010) PKCα expression is a marker for breast cancer aggressiveness Mol. Cancer 9, 76-90
8. Kerfoot, C., Huang, W., and Rotenberg, S. A. (2004) Immunohistochemical analysis of advanced human breast carcinomas reveals down-regulation of protein kinase Cα J. Histochem. Cytochem. 52, 419-422 (Pubitemid 38229108)
9. Kiley, S. C., Clark, K. J., Goodnough, M., Welch, D. R., and Jaken, S. (1999) Protein kinase δ involvement in mammary tumor cell metastasis Cancer Res. 59, 3230-3238 (Pubitemid 29316027)
10. McCracken, M. A., Miraglia, L. J., McKay, R. A., and Strobl, J. S. (2003) Protein kinase C δ is a pro-survival factor in human breast tumor cell lines Mol. Cancer Ther. 2, 273-281
11. Kruger, J. S. and Reddy, K. B. (2003) Distinct mechanisms mediate the initial and sustained phases of cell migration in epidermal growth factor receptor-overexpressing cells Mol. Cancer Res. 1, 801-809 (Pubitemid 37174451)
12. McKiernan, E., O'Brien, K., Grebenchtchikov, N., Geurts-Moespot, A., Sieuwerts, A. M., Martens, J. W., Magdolen, V., Evoy, D., McDermott, E., Crown, J., Sweep, F. C., and Duffy, M. J. (2008) Protein kinase Cδ expression in breast cancer as measured by real-time PCR, western blotting, and ELISA Br. J. Cancer 18, 1644-1650
13. Lonne, G. K., Masoumi, K. C., Lennartsson, J., and Larsson, C. (2009) Protein kinase Cδ supports survival of MDA-MB-231 breast cancer cells by suppressing the ERK1/2 pathway J. Biol. Chem. 284, 33456-33465
14. Urtreger, A. J., Grossoni, V. C., Falbo, K. B., Kazanietz, M. G., and Bal de Kier Joffe, E. D. (2005) Atypical protein kinase C-ζ modulates clonogenicity, motility, and secretion of proteolytic enzymes in murine mammary cells Mol. Carcinog. 42, 29-39 (Pubitemid 40041483)
15. Shah, K., Liu, Y., Deirmengian, C., and Shokat, K. M. (1997) Engineering unnatural nucleotide specificity for Rous sarcoma virus tyrosine kinase to uniquely label its direct substrates Proc. Natl. Acad. Sci. U.S.A. 94, 3565-3570 (Pubitemid 27180412)
16. Ting, A. Y., Witte, K., Shah, K., Kraybill, B., Shokat, K. M., and Schultz, P. G. (2001) Phage-display evolution of tyrosine kinases with altered nucleotide specificity Biopolymers 60, 220-228 (Pubitemid 34074176)
17. Shah, K. and Shokat, K. M. (2002) A chemical genetic screen for direct v-src substrates reveals ordered assembly of a retrograde signaling pathway Chem. Biol. 9, 35-47 (Pubitemid 34155863)
18. Witucki, L. A., Huang, X., Shah, K., Liu, Y., Kyin, S., Eck, M. J., and Shokat, K. M. (2002) Mutant tyrosine kinases with unnatural nucleotide specificity retain the structure and phosphoacceptor specificity of the wildtype enzyme Chem. Biol. 9, 25-33 (Pubitemid 34155862)
19. Habelhah, H., Shah, K., Huang, L., Burlingame, A. L., Shokat, K. M., and Ronai, Z. (2001) Identification of new JNK substrate using ATP pocket mutant JNK and a corresponding ATP analogue J. Biol. Chem. 276, 18090-18095
20. Eblen, S. T., Kumar, N. V., Shah, K., Henderson, M. J., Watts, C. K. W., Shokat, K. M., and Weber, M. J. (2003) Identification of novel ERK2 substrates through use of an engineered kinase and ATP analogs J. Biol. Chem. 278, 14926-14935 (Pubitemid 36799822)
21. Hindley, A. D., Park, S., Wang, L., Shah, K., Wang, Y., Hu, X., Shokat, K. M., Kolch, W., Sedivy, J. M., and Yeung, K. C. (2004) Engineering the serine/threonine protein kinase Raf-1 to utilize an orthogonal analogue of ATP substituted at the N6 position FEBS Lett. 556, 26-34 (Pubitemid 38058550)
22. Abeyweera, T. P. and Rotenberg, S. A. (2007) Design and characterization of a traceable protein kinase C-α Biochemistry 46, 2364-2370 (Pubitemid 46362410)
23. Abeyweera, T. P., Chen, X., and Rotenberg, S. A. (2009) Phosphorylation of α6-tubulin by protein kinase Cα activates motility of human breast cells J. Biol. Chem. 284, 17648-17656
24. Garcia-Bermejo, M. L., Leskow, F. C., Fuji, T., Wang, Q., Blumberg, P. M., Ohba, M., Kurok, T., Han, K. C., Lee, J., Marquez, V. E., and Kazanietz, M. G. (2002) Diacylglycerol (DAG)-lactones, a new class of protein kinase C (PKC) agonists, induce apoptosis in LNCaP prostate cancer cells by selective activation of PKCα J. Biol. Chem. 277, 645-655 (Pubitemid 34952103)
25. 2004, 279, 23846. (Erratum)
26. Soule, H. D., Maloney, T. M., Wolman, S. R., Peterson, W. D., Jr., Brenz, R., McGrath, C. M., Russo, J., Pauley, R. J., Jones, R. F., and Brooks, S. C. (1990) Isolation and characterization of a spontaneously immortalized human breast epithelial cell line, MCF-10 Cancer Res. 50, 6075-6086 (Pubitemid 20331424)
27. Peters, H. I., Chang, Y. W., and Traugh, J. A. (1995) Phosphorylation of elongation factor 1 (EF-1) by protein kinase C stimulates GDP/GTP-exchange activity Eur. J. Biochem. 234, 550-556
28. Bouzahzah, B., Albanese, C., Ahmed, F., Pixley, F., Lisanti, M. P., Segall, J. D., Condeelis, J., Joyce, D., Minden, A., Der, C. J., Chan, A., Symons, M., and Pestel, R. G. (2001) Rho family GTPases regulate mammary epithelium cell growth and metastasis through distinguishable pathways Mol. Med. 7, 816-830 (Pubitemid 34175305)
29. Tang, Y., Olufemi, L., Wang, M. T., and Nie, D. (2008) Role of rho GTPases in breast cancer Front. Biosci. 13, 759-776 (Pubitemid 351599780)
30. Wittman, T. and Waterman-Storer, C. M. (2005) Spatial regulation of CLASP affinity for microtubules by Rac1 and GSK3β in migrating epithelial cells J. Cell Biol. 169, 929-939 (Pubitemid 41002869)
31. Hirsch, D. S., Pirone, D. M., and Burbelo, P. D. (2001) A new family of cdc42 effector proteins, CEPs, function in fibroblast and epithelial cell shape changes J. Biol. Chem. 276, 875-883 (Pubitemid 32096504)
32. Joberty, G., Perlungher, R. R., and Macara, I. G. (1999) The Borgs, a new family of cdc42 and TC10 GTPase-interacting proteins Mol. Cell. Biol. 19, 6585-6597 (Pubitemid 29441843)
33. Jaken, S. and Parker, P. J. (2000) Protein kinase C binding partners BioEssays 22, 245-254 (Pubitemid 30144417)
34. Osmanagic-Myers, S. and Wiche, G. (2004) Plectin-RACK1 (receptor for activated C kinase 1) scaffolding: A novel mechanism to regulate protein kinase C activity J. Biol. Chem. 279, 18701-18710 (Pubitemid 38623294)
35. Fritz, G., Brachetti, C., Bahlmann, F., Schmidt, M., and Kaina, B. (2002) Rho GTPases in human breast tumours: Expression and mutation analyses and correlation with clinical parameters Br. J. Cancer 87, 635-644
36. Burbelo, P., Wellstein, A., and Pestell, R. G. (2004) Altered rho GTPase signaling pathways in breast cancer cells Breast Cancer Res. Treat. 84, 43-48 (Pubitemid 38388859)
37. Zuo, Y., Wu, Y., and Chakraborty, C. (2012) Cdc42 negatively regulates intrinsic migration of highly aggressive breast cancer cells J. Cell. Physiol. 227, 1399-1407
38. Arias-Romero, L. E., Villamar-Cruz, O., Pacheco, A., Kosoff, R., Huang, M., Muthuswamy, S. K., and Chernoff, J. (2010) A Rac-Pak signaling pathway is essential for ErbB2-mediated transformation of human breast epithelial cancer cells Oncogene 29, 5839-5849
39. Coniglio, S. J., Zavarella, S., and Symons, M. H. (2008) Pak1 and Pak2 mediate tumor cell invasion through distinct signaling mechanisms Mol. Cell. Biol. 28, 4162-4172 (Pubitemid 351812999)
40. Mehta, D., Rahman, A., and Malik, A. B. (2001) Protein kinase C-α signals rho-guanine nucleotide dissociation inhibitor phosphorylation and rho activation and regulates the endothelial cell barrier function J. Biol. Chem. 276, 22614-22620
41. Grohmanova, K., Schlaepfer, D., Hess, D., Gutierrez, P., Beck, M., and Kroschewski, R. (2004) Phosphorylation of IQGAP1 modulates its binding to cdc42, revealing a new type of Rho-GTPase regulator J. Biol. Chem. 279, 48495-48504 (Pubitemid 39625723)
42. Chitaley, K., Chen, L., Galler, A., Walter, U., Daum, G., and Clowes, A. W. (2004) Vasodilator-stimulated phosphoprotein is a substrate for protein kinase C FEBS Lett. 556, 211-215 (Pubitemid 38058581)
43. Ritter, B., Modregger, J., Paulsson, M., and Plomann, M. (1999) PACSIN 2, a novel member of the PACSIN family of cytoplasmic adapter proteins FEBS Lett. 454, 356-362 (Pubitemid 29304631)
44. Mori, A., Aizawa, H., Saido, T. C., Kawasaki, H., Mizuno, K., Murofushi, H., Suzuki, K., and Sakai, H. (1991) Site-specific phosphorylation by protein kinase C inhibits assembly-promoting activity of microtubule-associated protein 4 Biochemistry 30, 9341-9346
45. Xiao, H., Bai, X. H., Wang, Y., Kim, H., Mak, A. S., and Liu, M. (2012) MEK/ERK pathway mediates PKC activation-induced recruitment of PKCζ and MMP-9 to podosomes J. Cell. Physiol. DOI: 10.1002/jcp.24146