Protein kinase D regulates RhoA activity via rhotekin phosphorylation

Journal of Biological Chemistry

Volumn 287, Issue 12, 2012, Pages 9473-9483

  Pusapati, Ganesh V ^a,d   Eiseler, Tim ^b   Rykx, An ^c,e   Vandoninck, Sandy ^c   Derua, Rita ^c   Waelkens, Etienne ^c   Van Lint, Johan ^c   Von Wichert, Götz ^a   Seufferlein, Thomas ^a,b  

^a UNIVERSITY OF ULM   (Germany)

^b MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^c UNIVERSITY OF LEUVEN   (Belgium)

^d STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e Movetis NV   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATED PROTEINS; ANGIOGENESIS; CELLULAR PROCESS; G PROTEIN COUPLED RECEPTORS; IN-VIVO; ISOFORMS; KINASE FAMILY; PHORBOL ESTERS; POTENTIAL SITES; PROTEIN KINASE D; RHOA GTPASE; STRESS FIBERS; VARIOUS SUBSTRATES; VESICLE TRAFFICKING;

AMINO ACIDS; CELL CULTURE; CELL DEATH; CELL MEMBRANES; ENZYMES; PHOSPHORYLATION; SIGNAL TRANSDUCTION; SUBSTRATES;

PROTEINS;

ACTIN; BINDING PROTEIN; PROTEIN KINASE D; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; RHOTEKIN; SERINE; UNCLASSIFIED DRUG;

ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME REGULATION; ENZYME SUBSTRATE; FIBROBLAST; HUMAN; HUMAN CELL; IN VIVO STUDY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; STRESS FIBER;

AMINO ACID MOTIFS; ANIMALS; HEK293 CELLS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; NIH 3T3 CELLS; PHOSPHORYLATION; PROTEIN KINASE C; RHOA GTP-BINDING PROTEIN;

EID: 84858605175     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.339564     Document Type: Article

References (49)

1. Manning, G., Whyte, D. B., Martinez, R., Hunter, T., and Sudarsanam, S. (2002) The protein kinase complement of the human genome. Science 298, 1912-1934 (Pubitemid 35425239)
2. Rykx, A., De Kimpe, L., Mikhalap, S., Vantus, T., Seufferlein, T., Vandenheede, J. R., and Van Lint, J. (2003) Protein kinase D: a family affair. FEBS Lett. 546, 81-86 (Pubitemid 36782285)
3. Valverde, A. M., Sinnett-Smith, J., Van Lint, J., and Rozengurt, E. (1994) Molecular cloning and characterization of protein kinase D. A target for diacylglycerol and phorbol esters with a distinctive catalytic domain. Proc. Natl. Acad. Sci. U.S.A. 91, 8572-8576 (Pubitemid 24273706)
4. Johannes, F. J., Prestle, J., Eis, S., Oberhagemann, P., and Pfizenmaier, K. (1994) PKCu is a novel, atypical member of the protein kinase C family. J. Biol. Chem. 269, 6140-6148 (Pubitemid 24243002)
5. Sturany, S., Van Lint, J., Muller, F., Wilda, M., Hameister, H., Hocker, M., Brey, A., Gern, U., Vandenheede, J., Gress, T., Adler, G., and Seufferlein, T. (2001) Molecular cloning and characterization of the human protein kinase D2. A novel member of the protein kinase D family of serine threonine kinases. J. Biol. Chem. 276, 3310-3318
6. Hayashi, A., Seki, N., Hattori, A., Kozuma, S., and Saito, T. (1999) PKCnu, a new member of the protein kinaseCfamily, composes a fourth subfamily with PKCmu. Biochim. Biophys. Acta 1450, 99-106 (Pubitemid 29199863)
7. Jamora, C., Yamanouye, N., Van Lint, J., Laudenslager, J., Vandenheede, J. R., Faulkner, D. J., and Malhotra, V. (1999) Gβγ-mediated regulation of Golgi organization is through the direct activation of protein kinase D. Cell 98, 59-68
8. Rozengurt, E., Rey, O., and Waldron, R. T. (2005) Protein kinase D signaling. J. Biol. Chem. 280, 13205-13208 (Pubitemid 40517202)
9. Johannessen, M., Delghandi, M. P., Rykx, A., Dragset, M., Vandenheede, J. R., Van Lint, J., and Moens, U. (2007) Protein kinase D induces transcription through direct phosphorylation of the cAMP-response elementbinding protein. J. Biol. Chem. 282, 14777-14787 (Pubitemid 47093365)
10. Carnegie, G. K., Soughayer, J., Smith, F. D., Pedroja, B. S., Zhang, F., Diviani, D., Bristow, M. R., Kunkel, M. T., Newton, A. C., Langeberg, L. K., and Scott, J. D. (2008) AKAP-Lbc mobilizes a cardiac hypertrophy signaling pathway. Mol. Cell 32, 169-179
11. Fielitz, J., Kim, M. S., Shelton, J. M., Qi, X., Hill, J. A., Richardson, J. A., Bassel-Duby, R., and Olson, E. N. (2008) Requirement of protein kinase D1 for pathological cardiac remodeling. Proc. Natl. Acad. Sci. U.S.A. 105, 3059-3063 (Pubitemid 351723667)
12. Ha, C. H., Wang, W., Jhun, B. S., Wong, C., Hausser, A., Pfizenmaier, K., McKinsey, T. A., Olson, E. N., and Jin, Z. (2008) 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. 283, 14590-14599
13. Azoitei, N., Pusapati, G. V., Kleger, A., Möller, P., Küfer, R., Genze, F., Wagner, M., van Lint, J., Carmeliet, P., Adler, G., and Seufferlein, T. (2010) Protein kinase D2 is a crucial regulator of tumour cell-endothelial cell communication in gastrointestinal tumors. Gut 59, 1316-1330
14. von Wichert, G., Edenfeld, T., von Blume, J., Krisp, H., Krndija, D., Schmid, H., Oswald, F., Lother, U., Walther, P., Adler, G., and Seufferlein, T. (2008) Protein kinase D2 regulates chromogranin A secretion in human BON neuroendocrine tumor cells. Cell. Signal. 20, 925-934
15. Sumara, G., Formentini, I., Collins, S., Sumara, I., Windak, R., Bodenmiller, B., Ramracheya, R., Caille, D., Jiang, H., Platt, K. A., Meda, P., Aebersold, R., Rorsman, P., and Ricci, R. (2009) Regulation of PKD by the MAPK p38δ in insulin secretion and glucose homeostasis. Cell 136, 235-248
16. Yeaman, C., Ayala, M. I., Wright, J. R., Bard, F., Bossard, C., Ang, A., Maeda, Y., Seufferlein, T., Mellman, I., Nelson, W. J., and Malhotra, V. (2004) Protein kinase D regulates basolateral membrane protein exit from trans-Golgi network. Nat. Cell Biol. 6, 106-112 (Pubitemid 38425709)
17. Matthews, S. A., Navarro, M. N., Sinclair, L. V., Emslie, E., Feijoo-Carnero, C., and Cantrell, D. A. (2010) Unique functions for protein kinase D1 and protein kinase D2 in mammalian cells. Biochem. J. 432, 153-163
18. Reid, T., Furuyashiki, T., Ishizaki, T., Watanabe, G., Watanabe, N., Fujisawa, K., Morii, N., Madaule, P., and Narumiya, S. (1996) Rhotekin, a new putative target for Rho bearing homology to a serine/threonine kinase, PKN, and rhophilin in the Rho-binding domain. J. Biol. Chem. 271, 13556-13560 (Pubitemid 26185401)
19. Fu, Q., Yu, L., Liu, Q., Zhang, J., Zhang, H., and Zhao, S. (2000) Genomics 332, 328-332
20. Liu, C. A., Wang, M. J., Chi, C. W., Wu, C. W., and Chen, J. Y. (2004) Rho/rhotekin-mediated NF-κB activation confers resistance to apoptosis. Oncogene 23, 8731-8742
21. Fan, J., Ma, L. J., Xia, S. J., Yu, L., Fu, Q., Wu, C. Q., Huang, X. H., Jiang, J. M., and Tang, X. D. (2005) Association between clinical characteristics and expression abundance of RTKN gene in human bladder carcinoma tissues from Chinese patients. J. Cancer Res. Clin. Oncol. 131, 157-162 (Pubitemid 40175009)
22. Ito, H., Iwamoto, I., Morishita, R., Nozawa, Y., Narumiya, S., Asano, T., and Nagata, K. (2005) Possible role of Rho/rhotekin signaling in mammalian septin organization. Oncogene 24, 7064-7072 (Pubitemid 41573635)
23. Reynaud, C., Fabre, S., and Jalinot, P. (2000) The PDZ protein TIP-1 interacts with the Rho effector rhotekin and is involved in Rho signaling to the serum response element. J. Biol. Chem. 275, 33962-33968
24. Ito, H., Iwamoto, I., Morishita, R., Nozawa, Y., Asano, T., and Nagata, K. (2006) Identification of a PDZ protein, PIST, as a binding partner for Rho effector rhotekin. Biochemical and cell-biological characterization of rhotekin- PIST interaction. Biochem. J. 397, 389-398 (Pubitemid 44187497)
25. Sudo, K., Ito, H., Iwamoto, I., Morishita, R., Asano, T., and Nagata, K. (2006) Identification of a cell polarity-related protein, Lin-7B, as a binding partner for a Rho effector, rhotekin, and their possible interaction in neurons. Neurosci. Res. 56, 347-355 (Pubitemid 44750262)
26. Nagata, K., Ito, H., Iwamoto, I., Morishita, R., and Asano, T. (2009) Interaction of a multidomain adaptor protein, vinexin, with a Rho effector, rhotekin. Med. Mol. Morphol. 42, 9-15
27. Pusapati, G. V., Krndija, D., Armacki, M., von Wichert, G., von Blume, J., Malhotra, V., Adler, G., and Seufferlein, T. (2010) Role of the second cysteine-rich domain and Pro-275 in protein kinase D2 interaction with ADP-ribosylation factor 1, trans-Golgi network recruitment, and protein transport. Mol. Biol. Cell 21, 1011-1022
28. Nishikawa, K., Toker, A., Johannes, F. J., Songyang, Z., and Cantley, L. C. (1997) Determination of the specific substrate sequence motifs of protein kinase C isozymes. J. Biol. Chem. 272, 952-960 (Pubitemid 27034586)
29. Wheeler, A. P., and Ridley, A. J. (2004) Why three Rho proteins? RhoA, RhoB, RhoC, and cell motility. Exp. Cell Res. 301, 43-49 (Pubitemid 39388895)
30. Schwartz, M. (2004) Rho signaling at a glance. J. Cell Sci. 117, 5457-5458
31. Hall, A. (1998) Rho GTPases and the actin cytoskeleton. Science 279, 509-514
32. 12/13 in NIH3T3 cells. Am. J. Physiol. Cell Physiol. 285, C1197-C1206
33. LaValle, C. R., George, K. M., Sharlow, E. R., Lazo, J. S., Wipf, P., and Wang, Q. J. (2010) Protein kinase D as a potential new target for cancer therapy. Biochim. Biophys. Acta 1806, 183-192
34. Hausser, A., Storz, P., Märtens, S., Link, G., Toker, A., and Pfizenmaier, K. (2005) Protein kinase D regulates vesicular transport by phosphorylating and activating phosphatidylinositol-4 kinase IIIβ at the Golgi complex. Nat. Cell Biol. 7, 880-886 (Pubitemid 41486288)
35. Jaggi, M., Rao, P. S., Smith, D. J., Wheelock, M. J., Johnson, K. R., Hemstreet, G. P., and Balaji, K. C. (2005) E-cadherin phosphorylation by protein kinase D1/protein kinase Cμ is associated with altered cellular aggregation and motility in prostate cancer. Cancer Res. 65, 483-492
36. Ding, G., Sonoda, H., Yu, H., Kajimoto, T., Goparaju, S. K., Jahangeer, S., Okada, T., and Nakamura, S. (2007) Protein kinase D-mediated phosphorylation and nuclear export of sphingosine kinase 2. J. Biol. Chem. 282, 27493-27502 (Pubitemid 47501982)
37. Fugmann, T., Hausser, A., Schöffler, P., Schmid, S., Pfizenmaier, K., and Olayioye, M. A. (2007) Regulation of secretory transport by protein kinase D-mediated phosphorylation of the ceramide transfer protein. J. Cell Biol. 178, 15-22 (Pubitemid 47026398)
38. Watkins, J. L., Lewandowski, K. T., Meek, S. E., Storz, P., Toker, A., and Piwnica-Worms, H. (2008) Phosphorylation of the Par-1 polarity kinase by protein kinase D regulates 14-3-3 binding and membrane association. Proc. Natl. Acad. Sci. U.S.A. 105, 18378-18383
39. Biliran, H., Jan, Y., Chen, R., Pasquale, E. B., and Ruoslahti, E. (2008) Protein kinase D is a positive regulator of Bit1 apoptotic function. J. Biol. Chem. 283, 28029-28037
40. De Kimpe, L., Janssens, K., Derua, R., Armacki, M., Goicoechea, S., Otey, C., Waelkens, E., Vandoninck, S., Vandenheede, J. R., Seufferlein, T., and Van Lint, J. (2009) Characterization of cortactin as an in vivo protein kinase D substrate. Interdependence of sites and potentiation by Src. Cell. Signal. 21, 253-263
41. Janssens, K., De Kimpe, L., Balsamo, M., Vandoninck, S., Vandenheede, J. R., Gertler, F., and Van Lint, J. (2009) Characterization of EVL-I as a protein kinase D substrate. Cell. Signal. 21, 282-292
42. Du, C., Jaggi, M., Zhang, C., and Balaji, K. C. (2009) Protein kinase D1- mediated phosphorylation and subcellular localization of beta-catenin. Cancer Res. 69, 1117-1124
43. Peterburs, P., Heering, J., Link, G., Pfizenmaier, K., Olayioye, M. A., and Hausser, A. (2009) Protein kinase D regulates cell migration by direct phosphorylation of the cofilin phosphatase slingshot 1-like. Cancer Res. 69, 5634-5638
44. Eiseler, T., Döppler, H., Yan, I. K., Kitatani, K., Mizuno, K., and Storz, P. (2009) Protein kinase D1 regulates cofilin-mediated F-actin reorganization and cell motility through slingshot. Nat. Cell Biol. 11, 545-556
45. Nhek, S., Ngo, M., Yang, X., Ng, M. M., Field, S. J., Asara, J. M., Ridgway, N. D., and Toker, A. (2010) Regulation of oxysterol-binding protein Golgi localization through protein kinase D-mediated phosphorylation. Mol. Biol. Cell 21, 2327-2337
46. Eiseler, T., Hausser, A., De Kimpe, L., Van Lint, J., and Pfizenmaier, K. (2010) Protein kinase D controls actin polymerization and cell motility through phosphorylation of cortactin. J. Biol. Chem. 285, 18672-18683
47. Song, J., Li, J., Lulla, A., Evers, B. M., and Chung, D. H. (2006) Protein kinase D protects against oxidative stress-induced intestinal epithelial cell injury via Rho/ROK/PKC-δ pathway activation. Am. J. Physiol. Cell Physiol. 290, C1469-C1476 (Pubitemid 43830786)
48. Li, J., O'Connor, K. L., Hellmich, M. R., Greeley, G. H., Jr., Townsend, C. M., Jr., and Evers, B. M. (2004) The role of protein kinase D in neurotensin secretion mediated by protein kinase C-α/-δ and Rho/Rho kinase. J. Biol. Chem. 279, 28466-28474 (Pubitemid 38900128)
49. Yuan, J., Slice, L. W., and Rozengurt, E. (2001) Activation of protein kinase D by signaling through Rho and the α subunit of the heterotrimeric G protein G13. J. Biol. Chem. 276, 38619-38627