Dopamine D3 receptor inhibits the ubiquitin-specific peptidase 48 to promote NHE3 degradation

FASEB Journal

Volumn 28, Issue 3, 2014, Pages 1422-1434

  Armando, Ines ^a   Van Villar, Anthony M ^a   Jones, John E ^a   Lee, Hewang ^a   Wang, Xiaoyan ^a   Asico, Laureano D ^a   Yu, Peiying ^a   Yang, Jian ^a   Escano Jr , Crisanto S ^a   Pascua Crusan, Annabelle M ^a   Felder, Robin A ^b   Jose, Pedro A ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Blood pressure; C57Bl 6 mice; Kidney; Renal proximal tubule cells

Indexed keywords

3,4,4A,10B TETRAHYDRO 4 PROPYL 2H,5H [1]BENZOPYRANO[4,3 B][1,4]OXAZIN 9 OL; DEUBIQUITINASE; DOPAMINE 3 RECEPTOR; SMALL INTERFERING RNA; SODIUM PROTON EXCHANGE PROTEIN 3; UBIQUITIN SPECIFIC PEPTIDASE 48; UNCLASSIFIED DRUG; PRIMER DNA; PROTEINASE; SODIUM PROTON EXCHANGE PROTEIN; SODIUM-HYDROGEN EXCHANGER 3; UBIQUITIN ISOPEPTIDASE;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ENZYME INHIBITION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; KIDNEY HOMOGENATE; KIDNEY PROXIMAL TUBULE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SODIUM TRANSPORT; UBIQUITINATION; BLOOD PRESSURE; C57BL/6 MICE; CELL CULTURE; CYTOLOGY; KIDNEY; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; POLYMERASE CHAIN REACTION; RENAL PROXIMAL TUBULE CELLS; TWO HYBRID SYSTEM;

BLOOD PRESSURE; C57BL/6 MICE; KIDNEY; RENAL PROXIMAL TUBULE CELLS;

BASE SEQUENCE; CELLS, CULTURED; DNA PRIMERS; ENDOPEPTIDASES; HUMANS; KIDNEY TUBULES, PROXIMAL; POLYMERASE CHAIN REACTION; PROTEOLYSIS; RECEPTORS, DOPAMINE D3; SODIUM-HYDROGEN ANTIPORTER; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84899553522     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-243840     Document Type: Article

References (59)

1. Felder, R. A., Seikaly, M. G., Cody, P., Eisner, G. M., and Jose, P. A. (1990) Attenuated renal response to dopaminergic drugs in spontaneously hypertensive rats. Hypertension 15, 560-569
2. Chen, C. J., and Lokhandwala, M. F. (1992) An impairment of renal tubular DA-1 receptor function as the causative factor for diminished natriuresis to volume expansion in spontaneously hypertensive rats. Clin. Exp. Hypertens. A. 14, 615-628
3. Luippold, G., Küster, E., Joos, T. O., and Mühlbauer, B. (1998) Dopamine D3 receptor activation modulates renal function in anesthetized rats. Naunyn Schmiedebergs Arch. Pharmacol. 358, 690-693
4. Ladines, C. A., Zeng, C., Asico, L. D., Sun, X., Pocchiari, F., Semeraro, C., Pisegna, J., Wank, S., Yamaguchi, I., Eisner, G. M., and Jose, P. A. (2001) Impaired renal D1-like and D2-like dopamine receptor interaction in the spontaneously hypertensive rat. Am. J. Physiol. Regul. Integr. Comp. Physiol. 281, R1071-R1078
5. Sibley, D. R. (1999) New insights into dopaminergic receptor function using antisense and genetically altered animals. Annu. Rev. Pharmacol. Toxicol. 39, 313-314
6. Brismar, H., Holtbäck, U., and Aperia, A. (2000) Mechanisms by which intrarenal dopamine and ANP interact to regulate sodium metabolism. Clin. Exp. Hypertens. 22, 303-307
7. Carey, R. M. (1992) Theodore Cooper lecture: renal dopamine system: paracrine regulator of sodium homeostasis and blood pressure. Hypertension 38, 297-302
8. Hussain, T., and Lokhandwala, M. F. (2003) Renal dopamine receptors and hypertension. Exp. Biol. Med. (Maywood) 228, 134-142
9. Zeng, C., Armando, I., Luo, Y., Eisner, G. M., Felder, R. A., and Jose, P. A. (2008) Dysregulation of dopamine-dependent mechanisms as a determinant of hypertension: studies in dopamine receptor knockout mice. Am. J. Physiol. Heart Circ. Physiol. 294, H551-H569
10. Felder, R. A., Sanada, H., Xu, J., Yu, P. Y., Wang, Z., Watanabe, H., Asico, L. D., Wang, W., Zheng, S., Yamaguchi, I., Williams, S. M., Gainer, J., Brown, N. J., Hazen-Martin, D., Wong, L. J., Robillard, J. E., Carey, R. M., Eisner, G. M., and Jose, P. A. (2002) G protein-coupled receptor kinase 4 gene variants in human essential hypertension. Proc. Natl. Acad. Sci. U. S. A. 99, 3872-38777
11. Harris, R. C. (2012) Abnormalities in renal dopamine signaling and hypertension: the role of GRK4. Curr. Opin. Nephrol. Hypertens. 21, 61-65
12. Ueda, A., Ozono, R., Oshima, T., Yano, A., Kambe, M., Teranishi, Y., Katsuki, M., and Chayama, K. (2003) Disruption of the type 2 dopamine receptor gene causes a sodium-dependent increase in blood pressure in mice. Am. J. Hypertens. 16, 853-858
13. Asico, L. D., Ladines, C., Fuchs, S., Accili, D., Carey, R. M., Semeraro, C., Pocchiari, F., Felder, R. A., Eisner, G. M., and Jose, P. A. (1998) Disruption of the dopamine D3 receptor gene produces renin-dependent hypertension. J. Clin. Invest. 102, 493-498
14. Luippold, G., Zimmermann, C., Mai, M., Kloor, D., Starck, D., Gross, G., and Mühlbauer, B. (2001) Dopamine D3 receptors and salt-dependent hypertension. J. Am. Soc. Nephrol. 12, 2272-2279
15. Zeng, C., Eisner, G. M., Felder, R. A., and Jose, P. A. (2006) D3 dopamine receptor and essential hypertension. Curr. Hypertens. Rev. 2, 247-253
16. Yang, Z., Asico, L. D., Yu, P., Wang, Z., Jones, J. E., Escano, C. S., Wang, X., Quinn, M. T., Sibley, D. R., Romero, G. G., Felder, R. A., and Jose, P. A. (2006) D5 dopamine receptor regulation of reactive oxygen species production, NADPH oxidase, and blood pressure. Am. J. Physiol. Regul. Integr. Comp. Physiol. 290, R96-R104
17. Felder, R. A., and Jose, P. A. (2006) Mechanisms of disease: the role of GRK4 in the etiology of essential hypertension and salt sensitivity. Nat. Clin. Pract. Nephrol. 2, 637-650
18. Ortiz, P. A., and Garvin, J. L. (2001) Intrarenal transport and vasoactive substances in hypertension. Hypertension 38, 621-624
19. Zeng, C., Liu, Y., Wang, Z., He, D., Huang, L., Yu, P., Zheng, S., Jones, J. E., Asico, L. D., Hopfer, U., Eisner, G. M., Felder, R. A., and Jose, P. A. (2006) Activation of D3 dopamine receptor decreases angiotensin II type 1 receptor expression in rat renal proximal tubule cells. Circ. Res. 99, 494-500
20. Kaneko, S., Albrecht, F., Asico, L. D., Eisner, G. M., Robillard, J. E., and Jose, P. A. (1992) Ontogeny of DA1 receptor-mediated natriuresis in the rat: in vivo and in vitro correlations. Am. J. Physiol. 263, R631-R638
21. Kaneko, S., Eisner, G. M., and Jose, P. A. (1990) Effect of pramipexole, a dopamine-1/dopamine-2 receptor agonist, on sodium excretion and blood pressure in spontaneously hypertensive rats. J. Auton. Pharmacol. 10, s53-s60
22. Zeng, C., Asico, L. D., Yu, C., Villar, V. A., Shi, W., Luo, Y., Wang, Z., He, D., Liu, Y., Huang, L., Yang, C., Wang, X., Hopfer, U., Eisner, G. M., and Jose, P. A. (2008) Renal D3 dopamine receptor stimulation induces natriuresis via an ETB endothelin receptor mechanism. Kidney Int. 74, 750-759
23. Pedrosa, R., Gomes, P., Hopfer, U., Jose, P. A., and Soares-da-Silva, P. (2004) Giβ3 protein-coupled dopamine D3 receptormediated inhibition of renal NHE3 activity in SHR proximal tubular cells is a PLC-PKC-mediated event. Am. J. Physiol. Renal Physiol. 287, F1059-F1066
24. +/Hα exchanger activity in normotensive and spontaneously hypertensive rat proximal tubular epithelial cells. Br. J. Pharmacol. 142, 1343-1353
25. +-K-ATPase activity is dependent on the opening of Kα channels. Am. J. Physiol. Renal Physiol. 283, F114-F123
26. Flegelova, H., Haguenauer-Tsapis, R., and Sychrova, H. (2006) Heterologous expression of mammalian Na/H antiporters in Saccharomyces cerevisiae. Biochim. Biophys. Acta 1760, 504-516
27. +/Hα exchanger NHE3 by dopamine: Translational and post-Translational mechanisms. Am. J. Physiol. Renal Physiol. 304, F1169-F1180
28. Wilkinson, K. D. (1999) Regulation of ubiquitin-dependent processes by deubiquitinating enzymes. FASEB J. 11, 1245-1256
29. Lockhart, P. J., Hulihan, M., Lincoln, S., Hussey, J., Skipper, L., Bisceglio, G., Wilkes, K., and Farrer, M. J. (2004) Identification of the human ubiquitin specific protease 31 (USP31) gene: structure, sequence and expression analysis. DNA Seq. 15, 9-14
30. Quesada, V., Diaz-Perales, A., Gutierrez-Fernandez, A., Garabaya, C., Cal, S., and Lopez-Otin, C. L. (2004) Cloning and enzymatic analysis of 22 novel human ubiquitin-specific proteases. Biochem. Biophys. Res. Commun. 314, 54-62
31. Villar, V. A., Jones, J. E., Armando, I., Palmes-Saloma, C., Yu, P., Pascua, A. M., Keever, L., Arnaldo, F. B., Wang, Z., Luo, Y., Felder, R. A., and Jose, P. A. (2009) G protein-coupled receptor kinase 4 (GRK4) regulates the phosphorylation and function of the dopamine D3 receptor. J. Biol. Chem. 284, 21425-21434
32. Li, H., Armando, I., Yu, P., Escano, C., Mueller, S. C., Asico, L., Pascua, A., Lu, Q., Wang, X., Villar, V. A., Jones, J. E., Wang, Z., Periasamy, A., Lau, Y. S., Soares-da-Silva, P., Creswell, K., Guillemette, G., Sibley, D. R., Eisner, G., Gildea, J. J., Felder, R. A., and Jose, P. A. (2008) Dopamine 5 receptor mediates Ang II type 1 receptor degradation via a ubiquitin-proteasome pathway in mice and human cells. J. Clin. Invest. 118, 2180-2189
33. Day, C. A., and Kenworthy, A. K. (2012) Mechanisms underlying the confined diffusion of cholera toxin B-subunit in intact cell membranes. PLoS ONE 7, e34923
34. Song, K. S., Li, S., Okamoto, T., Quilliam, L. A., Sargiacomo, M., and Lisanti, M. P. (1996) Co-purification and direct interaction of Ras with caveolin, an integral membrane protein of caveolae microdomains: detergent-free purification of caveolae microdomains. J. Biol. Chem. 271, 9690-9697
35. Yu, P., Villar, V. A., and Jose, P. A. (2013) Methods for the study of dopamine receptors within lipid rafts of kidney cells. Methods Mol. Biol. 964, 15-24
36. Fernández-Montalván, A., Bouwmeester, T., Joberty, G., Mader, R., Mahnke, M., Pierrat, B., Schlaeppi, J. M., Worpenberg, S., and Gerhartz, B. (2007) Biochemical characterization of USP7 reveals post-Translational modification sites and structural requirements for substrate processing and subcellular localization. FEBS J. 274, 4256-42570
37. Ladasky, J. J., Boyle, S., Seth, M., Li, H., Pentcheva, T., Abe, F., Steinberg, S. J., and Edidin, M. (2006) Bap31 enhances the endoplasmic reticulum export and quality control of human class I MHC molecules. J. Immunol. 177, 6172-6181
38. Cuevas, S., Zhang, Y., Yang, Y., Escano, C., Asico, L., Jones, J. E., Armando, I., and Jose, P. A. (2012) Role of renal DJ-1 in the pathogenesis of hypertension associated with increased reactive oxygen species production. Hypertension 59, 446-452
39. Zhang, Y., Cuevas, S., Asico, L. D., Escano, C., Yang, Y., Pascua, A. M., Wang, X., Jones, J. E., Grandy, D., Eisner, G., Jose, P. A., and Armando, I. (2012) Deficient dopamine D2 receptor function causes renal inflammation independently of high blood pressure. PLoS ONE 7, e38745
40. Villar, V. A., Jones, J. E., Armando, I., Asico, L. D., Escano, C. S. Jr., Lee, H., Wang, X., Yang, Y., Pascua-Crusan, A. M., Palmes-Saloma, C. P., Felder, R. A., and Jose, P. A. (2013) Sorting nexin 1 loss results in D5 dopamine receptor dysfunction in human renal proximal tubule cells and hypertension in mice. J. Biol. Chem. 288, 152-163
41. Villar, V. A., Armando, I., Sanada, H., Frazer, L. C., Russo, C. M., Notario, P. M., Lee, H., Comisky, L., Russell, H. A., Yang, Y., Jurgens, J. A., Jose, P. A., and Jones, J. E. (2013) Novel role of sorting nexin 5 in renal D1 dopamine receptor trafficking and function: implications for hypertension. FASEB J. 27, 1808-1819
42. +-Hα exchanger 3 (NHE3) is present in lipid rafts in the rabbit ileal brush border: a role for rafts in trafficking and rapid stimulation of NHE3. J. Physiol. 537, 537-552
43. +/Hα exchanger NHE3 activity and trafficking are lipid raft-dependent. J. Biol. Chem. 281,17845-17855
44. Kenworthy, A. K., Petranova, N., and Edidin, M. (2000) Highresolution FRET microscopy of cholera toxin B-subunit and GPI-Anchored proteins in cell plasma membranes. Mol. Biol. Cell 11, 1645-1655
45. Mikhalyov, I., and Samsonov, A. (2011) Lipid raft detecting in membranes of live erythrocytes. Biochim. Biophys. Acta. 1808, 1930-1929
46. Moe, O. W. (1997) Sodium-hydrogen exchange in renal epithelia: mechanisms of acute regulation. Curr. Opin. Nephrol. Hypertens. 6, 440-446
47. Donowitz, M., and Li, X. (2007) Regulatory binding partners and complexes of NHE3. Physiol. Rev. 87, 825-872
48. McDonough, A. A. (2010) Mechanisms of proximal tubule sodium transport regulation that link extracellular fluid volume and blood pressure. Am. J. Physiol. Regul. Integr. Comp. Physiol. 298, R851-R861
49. Bezerra, C. N., Girardi, A. C., Carraro-Lacroix, R., and Rebouças, N. A. (2008) Mechanisms underlying the long-Term regulation of NHE3 by parathyroid hormone. Am. J. Physiol. Renal Physiol. 294, F1232-F1237
50. +/Hα exchanger 3: biphasic response and glucocorticoid dependence. Am. J. Physiol. Renal Physiol. 283, F532-F539
51. +/Hα exchanger NHE3 by chronic exposure to angiotensin II in renal epithelial cells. Biochem. Biophys. Res. Commun. 409, 470-4761
52. Di Sole, F., Hu, M. C., Zhang, J., Babich, V., Bobulescu, I. A., Shi, M., McLeroy, P., Rogers, T. E., and Moe, O. W. (2011) The reduction of Na/H exchanger-3 protein and transcript expression in acute ischemia-reperfusion injury is mediated by extractable tissue factor(s). Kidney Int. 80, 822-831
53. Morales, P., Díaz, E. S., and Kong, M. (2007) Proteasome activity and its relationship with protein phosphorylation during capacitation and acrosome reaction in human spermatozoa. Soc. Reprod. Fertil. Suppl. 65, 269-273
54. Wojcikiewicz, R. J. (2004) Regulated ubiquitination of proteins in GPCR-initiated signaling pathways. Trends Pharmacol. Sci. 25, 35-41
55. Nalepa, G., Rolfe, M., and Harper, J. W. (2006) Drug discovery in the ubiquitin-proteasome system. Nat. Rev. Drug Discov. 5, 596-613
56. Kessler, B. M., and Edelmann, M. J. (2011) PTMs in conversation: activity and function of deubiquitinating enzymes regulated via post-Translational modifications. Cell Biochem. Biophys. 60, 21-38
57. Yao, T., Song, L., Jin, J., Cai, Y., Takahashi, H., Swanson, S. K., Washburn, M. P., Florens, L., Conaway, R. C., Cohen, R. E., and Conaway, J. W. (2008) Distinct modes of regulation of the Uch37 deubiquitinating enzyme in the proteasome and in the INo980 chromatin-remodeling complex. Mol. Cell. 31, 909-917
58. Jose, P. A., Eisner, G. M., and Felder, R. A. (1998) Renal dopamine receptors in health and hypertension. Pharmacol. Ther. 80, 149-182
59. +/Hα exchanger. Nat. Genet. 19, 282-285