Protein kinase D-mediated phosphorylation of polycystin-2 (TRPP2) is essential for its effects on cell growth and calcium channel activity

Molecular Biology of the Cell

Volumn 21, Issue 22, 2010, Pages 3853-3865

  Streets, Andrew J ^a   Needham, Andrew J ^a   Gill, Sharonjit K ^a   Ong, Albert C M ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM CHANNEL; CALCIUM ION; CATION CHANNEL; EPIDERMAL GROWTH FACTOR; POLYCYSTIN 2; PROTEIN KINASE D; SERINE;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CARBOXY TERMINAL SEQUENCE; CELL GROWTH; CELL PROLIFERATION; CELL STRAIN; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; HUMAN; HUMAN CELL; MOUSE; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; WILD TYPE;

ADENOSINE TRIPHOSPHATE; ANIMALS; BINDING SITES; BLOTTING, WESTERN; CALCIUM; CALCIUM CHANNELS; CELL LINE; CELL PROLIFERATION; ENDOPLASMIC RETICULUM; EPIDERMAL GROWTH FACTOR; FLUORESCENT ANTIBODY TECHNIQUE; HEK293 CELLS; HUMANS; MUTATION; PHOSPHORYLATION; PROTEIN KINASE C; RNA INTERFERENCE; SERINE; TRPP CATION CHANNELS;

EID: 78649637949     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E10-04-0377     Document Type: Article

References (48)

1. Ahmmed, G. U., Mehta, D., Vogel, S., Holinstat, M., Paria, B. C., Tiruppathi, C., and Malik, A. B. (2004). Protein kinase Cα phosphorylates the TRPC1 channel and regulates store-operated Ca2+ entry in endothelial cells. J. Biol. Chem. 279, 20941-20949.
2. Barker, G., and Simmons, N. L. (1981). Identification of two strains of cultured canine renal epithelial cells (MDCK cells) which display entirely different physiological properties. Q. J. Exp. Physiol. 66, 61-72.
3. Brandlin, I., et al. (2002). Protein kinase C (PKC)η-mediated PKCμ activation modulates ERK and JNK signal pathways. J. Biol. Chem. 277, 6490-6496.
4. Cai, Y., et al. (2004). Calcium dependence of polycystin-2 channel activity is modulated by phosphorylation at Ser812. J. Biol. Chem. 279, 19987-19995.
5. Cai, Y., Maeda, Y., Cedzich, A., Torres, V. E., Wu, G., Hayashi, T., Mochizuki, T., Park, J. H., Witzgall, R., and Somlo, S. (1999). Identification and characterization of polycystin-2, the PKD2 gene product. J. Biol. Chem. 274, 28557-28565.
6. Calvet, J. P., and Grantham, J. J. (2001). The genetics and physiology of polycystic kidney disease. Semin. Nephrol. 21, 107-123.
7. Chang, M. Y., Parker, E., Ibrahim, S., Shortland, J. R., Nahas, M. E., Haylor, J. L., and Ong, A. C. (2006). Haploinsufficiency of Pkd2 is associated with increased tubular cell proliferation and interstitial fibrosis in two murine Pkd2 models. Nephrol. Dial. Transplant. 21, 2078-2084.
8. Chen, J., Lu, G., and Wang, Q. J. (2005). Protein kinase C-independent effects of protein kinase D3 in glucose transport in L6 myotubes. Mol. Pharmacol. 67, 152-162.
9. Duncan, R. F., and Song, H. J. (1999). Striking multiplicity of eIF4E-BP1 phosphorylated isoforms identified by 2D gel electrophoresis regulation by heat shock. Eur. J. Biochem. 265, 728-743.
10. Feng, S., Okenka, G. M., Bai, C. X., Streets, A. J., Newby, L. J., DeChant, B. T., Tsiokas, L., Obara, T., and Ong, A. C. (2008). Identification and functional characterization of an N-terminal oligomerization domain for polycystin-2. J. Biol. Chem. 283, 28471-28479.
11. Frohlich, O., Klein, J. D., Smith, P. M., Sands, J. M., and Gunn, R. B. (2004). Urea transport in MDCK cells that are stably transfected with UT-A1. Am. J. Physiol. Cell Physiol. 286, C1264-C1270.
12. Gallagher, A. R., et al. (2006). A truncated polycystin-2 protein causes polycystic kidney disease and retinal degeneration in transgenic rats. J. Am. Soc. Nephrol. 17, 2719-2730.
13. Giamarchi, A., et al. (2010). A polycystin-2 (TRPP2) dimerization domain essential for the function of heteromeric polycystin complexes. EMBO J. 29, 1176-1191.
14. Grimm, D. H., Karihaloo, A., Cai, Y., Somlo, S., Cantley, L. G., and Caplan, M. J. (2006). Polycystin-2 regulates proliferation and branching morphogenesis in kidney epithelial cells. J. Biol. Chem. 281, 137-144.
15. Gschwendt, M., Dieterich, S., Rennecke, J., Kittstein, W., Mueller, H. J., and Johannes, F. J. (1996). Inhibition of protein kinase C mu by various inhibitors. Differentiation from protein kinase c isoenzymes. FEBS Lett. 392, 77-80.
16. Guinamard, R., Chatelier, A., Lenfant, J., and Bois, P. (2004). Activation of the Ca(2+)-activated nonselective cation channel by diacylglycerol analogues in rat cardiomyocytes. J. Cardiovasc. Electrophysiol. 15, 342-348.
17. Hanaoka, K., Qian, F., Boletta, A., Bhunia, A. K., Piontek, K., Tsiokas, L., Sukhatme, V. P., Guggino, W. B., and Germino, G. G. (2000). Co-assembly of polycystin-1 and -2 produces unique cation-permeable currents. Nature 408, 990-994.
18. Hellman, N. E., Greco, A. J., Rogers, K. K., Kanchagar, C., Balkovetz, D. F., and Lipschutz, J. H. (2005). Activated extracellular signal-regulated kinases are necessary and sufficient to initiate tubulogenesis in renal tubular MDCK strain I cell cysts. Am. J. Physiol. Renal Physiol. 289, F777-F785.
19. Ivison, S. M., Graham, N. R., Bernales, C. Q., Kifayet, A., Ng, N., Shobab, L. A., and Steiner, T. S. (2007). Protein kinase D interaction with TLR5 is required for inflammatory signaling in response to bacterial flagellin. J. Immunol. 178, 5735-5743.
20. Kottgen, M., et al. (2005). Trafficking of TRPP2 by PACS proteins represents a novel mechanism of ion channel regulation. EMBO J. 24, 705-716. (Pubitemid 40396101)
21. Koulen, P., Cai, Y., Geng, L., Maeda, Y., Nishimura, S., Witzgall, R., Ehrlich, B. E., and Somlo, S. (2002). Polycystin-2 is an intracellular calcium release channel. Nat. Cell Biol. 4, 191-197.
22. Laycock, S., Taylor, H. C., Haigh, C., Lee, A. T., Cooper, G. J., Ong, A. C., and Robson, L. (2009). A novel dephosphorylation-activated conductance in a mouse renal collecting duct cell line. Exp. Physiol. 94, 914-927.
23. Lemonnier, J., Ghayor, C., Guicheux, J., and Caverzasio, J. (2004). Protein kinase C-independent activation of protein kinase D is involved in BMP-2-induced activation of stress mitogen-activated protein kinases JNK and p38 and osteoblastic cell differentiation. J. Biol. Chem. 279, 259-264.
24. Li, Q., Dai, Y., Guo, L., Liu, Y., Hao, C., Wu, G., Basora, N., Michalak, M., and Chen, X. Z. (2003). Polycystin-2 associates with tropomyosin-1, an actin microfilament component. J. Mol. Biol. 325, 949-962.
25. Li, X., Luo, Y., Starremans, P. G., McNamara, C. A., Pei, Y., and Zhou, J. (2005). Polycystin-1 and polycystin-2 regulate the cell cycle through the helix-loophelix inhibitor Id2. Nat. Cell Biol. 7, 1102-1112.
26. Liang, G., Yang, J., Wang, Z., Li, Q., Tang, Y., and Chen, X. Z. (2008). Polycystin-2 down-regulates cell proliferation via promoting PERK-dependent phosphorylation of eIF2alpha. Hum. Mol. Genet. 17, 3254-3262.
27. Ma, R., Li, W. P., Rundle, D., Kong, J., Akbarali, H. I., and Tsiokas, L. (2005). PKD2 functions as an epidermal growth factor-activated plasma membrane channel. Mol. Cell Biol. 25, 8285-8298.
28. Mochizuki, T., et al. (1996). PKD2, a gene for polycystic kidney disease that encodes an integral membrane protein. Science 272, 1339-1342. (Pubitemid 26199975)
29. Nauli, S. M., et al. (2003). Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells. Nat. Genet. 33, 129-137.
30. Newby, L. J., Streets, A. J., Zhao, Y., Harris, P. C., Ward, C. J., and Ong, A. C. (2002). Identification, characterization, and localization of a novel kidney polycystin-1-polycystin-2 complex. J. Biol. Chem. 277, 20763-20773.
31. Nilius, B., Prenen, J., Tang, J., Wang, C., Owsianik, G., Janssens, A., Voets, T., and Zhu, M. X. (2005). Regulation of the Ca2+ sensitivity of the nonselective cation channel TRPM4. J. Biol. Chem. 280, 6423-6433.
32. 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.
33. Ong, A. C., and Harris, P. C. (2005). Molecular pathogenesis of ADPKD: the polycystin complex gets complex. Kidney Int. 67, 1234-1247.
34. Ong, A. C., Ward, C. J., Butler, R. J., Biddolph, S., Bowker, C., Torra, R., Pei, Y., and Harris, P. C. (1999). Coordinate expression of the autosomal dominant polycystic kidney disease proteins, polycystin-2 and polycystin-1, in normal and cystic tissue. Am. J. Pathol. 154, 1721-1729.
35. Ponnambalam, S., Rabouille, C., Luzio, J. P., Nilsson, T., and Warren, G. (1994). The TGN38 glycoprotein contains two non-overlapping signals that mediate localization to the trans-Golgi network. J. Cell Biol. 125, 253-268.
36. Prasad, S., McDaid, J. P., Tam, F. W., Haylor, J. L., and Ong, A. C. (2009). Pkd2 dosage influences cellular repair responses following ischemia-reperfusion injury. Am. J. Pathol. 175, 1493-1503.
37. Richardson, J. C., Scalera, V., and Simmons, N. L. (1981). Identification of two strains of MDCK cells which resemble separate nephron tubule segments. Biochim. Biophys. Acta 673, 26-36.
38. Rossetti, S., et al. (2007). Comprehensive molecular diagnostics in autosomal dominant polycystic kidney disease. J. Am. Soc. Nephrol. 18, 2143-2160.
39. Rozengurt, E., Rey, O., and Waldron, R. T. (2005). Protein kinase D signaling. J. Biol. Chem. 280, 13205-13208.
40. 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.
41. Sammels, E., Devogelaere, B., Mekahli, D., Bultynck, G., Missiaen, L., Parys, J. B., Cai, Y., Somlo, S., and De Smedt, H. (2010). Polycystin-2 activation by inositol 1,4,5-trisphosphate-induced Ca2+ release requires its direct association with the inositol 1,4,5-trisphosphate receptor in a signaling microdomain. J. Biol. Chem. 285, 18794-18805.
42. Streets, A. J., Moon, D. J., Kane, M. E., Obara, T., and Ong, A. C. (2006). Identification of an N-terminal glycogen synthase kinase 3 phosphorylation site which regulates the functional localization of polycystin-2 in vivo and in vitro. Hum. Mol. Genet. 15, 1465-1473.
43. Torres, V. E., and Harris, P. C. Mechanisms of Disease: autosomal dominant and recessive polycystic kidney diseases. Nat. Clin. Pract. Nephrol. 2, 40-55, 2006; quiz 55.
44. Wang, Q. J. (2006). PKD at the crossroads of DAG and PKC signaling. Trends Pharmacol. Sci. 27, 317-323.
45. Wegierski, T., Steffl, D., Kopp, C., Tauber, R., Buchholz, B., Nitschke, R., Kuehn, E. W., Walz, G., and Kottgen, M. (2009). TRPP2 channels regulate apoptosis through the Ca2+ concentration in the endoplasmic reticulum. EMBO J. 28, 490-499.
46. Wilson, P. D. (2004). Polycystic kidney disease: new understanding in the pathogenesis. Int. J. Biochem. Cell Biol. 36, 1868-1873.
47. Yao, X., Kwan, H. Y., and Huang, Y. (2005). Regulation of TRP channels by phosphorylation. Neurosignals 14, 273-280.
48. Zhang, W., Bergamaschi, D., Jin, B., and Lu, X. (2005). Posttranslational modifications of p27kip1 determine its binding specificity to different cyclins and cyclin-dependent kinases in vivo. Blood 105, 3691-3698. (Pubitemid 40628218)