Novel role of sorting nexin 5 in renal D1 dopamine receptor trafficking and function: Implications for hypertension

FASEB Journal

Volumn 27, Issue 5, 2013, Pages 1808-1819

  Villar, Van Anthony M ^a,b   Armando, Ines ^a,b   Sanada, Hironobu ^c,d   Frazer, Lauren C ^b   Russo, Christen M ^b   Notario, Patricia M ^b   Lee, Hewang ^a,b   Comisky, Lauren ^b   Russell, Holly Ann ^b   Yang, Yu ^a   Jurgens, Julie A ^a   Jose, Pedro A ^a,b   Jones, John E ^a,b  

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

^b GEORGETOWN UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c FUKUSHIMA MEDICAL UNIVERSITY   (Japan)

^d NATIONAL VETERINARY ASSAY LABORATORY   (Japan)

Author keywords

cAMP; GRK4; Kidney; Natriuresis; Receptor trafficking

Indexed keywords

CREATININE; CYCLIC AMP; DOPAMINE 1 RECEPTOR; G PROTEIN COUPLED RECEPTOR KINASE 4; NEXIN 5; PROTEIN; SODIUM; TRANSFER RNA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; ENDOSOME; EPITHELIUM CELL; HOMEOSTASIS; HUMAN; HUMAN CELL; HYPERTENSION; INTERNALIZATION; KIDNEY EPITHELIUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; RAT; SODIUM EXCRETION; SPONTANEOUSLY HYPERTENSIVE RAT; SYSTOLIC BLOOD PRESSURE;

ANIMALS; ENDOCYTOSIS; G-PROTEIN-COUPLED RECEPTOR KINASE 4; HEK293 CELLS; HUMANS; HYPERTENSION; KIDNEY; MALE; PROTEIN TRANSPORT; RATS; RATS, INBRED SHR; RECEPTORS, DOPAMINE D1; RNA, SMALL INTERFERING; SORTING NEXINS;

MAMMALIA; RATTUS;

EID: 84877111389     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-208439     Document Type: Article

References (54)

1. Vassilatis, D. K., Hohmann, J. G., Zeng, H., Li, F., Ranchalis, J. E., Mortrud, M. T., Brown, A., Rodriguez, S. S., Weller, J. R., Wright, A. C., Bergmann, J. E., and Gaitanaris, G. A. (2003) The G protein-coupled receptor repertoires of human and mouse. Proc. Natl. Acad. Sci. U. S. A. 100, 4903-4908
2. Foord, S. M., Bonner, T. I., Neubig, R. R., Rosser, E. M., Pin, J. P., Davenport, A. P., Spedding, M., and Harmar, A. J. (2005) International Union of Pharmacology. XLVI. G protein-coupled receptor list. Pharmacol. Rev. 57, 279-288
3. Missale, C., Nash, S. R., Robinson, S. W., Jaber, M., and Caron, M. G. (1998) Dopamine receptors: from structure to function. Physiol. Rev. 78, 189-225
4. Aperia, A. C. (2000) Intrarenal dopamine: a key signal in the interactive regulation of sodium metabolism. Annu. Rev. Physiol. 62, 621-647
5. Banday, A. A., and Lokhandwala, M. F. (2008) Dopamine receptors and hypertension. Curr. Hypertens. Rep. 10, 268-e75
6. Jose, P. A., Soares-da-Silva, P., Eisner, G. M., and Felder, R. A. (2010) Dopamine and G protein-coupled receptor kinase 4 in the kidney: role in blood pressure regulation. Biochim. Biophys. Acta 1802, 1259-1267
7. Albrecht, F. E., Drago, J., Felder, R. A., Printz, M. P., Eisner, G. M., Robillard, J. E., Sibley, D. R., and Jose, P. A. (1996) Role of the D-1A dopamine receptor in the pathogenesis of essential hypertension. J. Clin. Invest. 97, 2283-2288
8. Gardner, B., Liu, Z. F., Jiang, D., and Sibley, D. R. (2001) The role of phosphorylation/dephosphorylation in agonist-induced desensitization of D1 dopamine receptor function: evidence for a novel pathway for receptor dephosphorylation. Mol. Pharmacol. 59, 310-321
9. Kim, O-J., Gardner, B. R., Williams, D. B., Marinec, P. S., Cabrera, D. M., Peters, J. D., Mak, C. C., Kim, K-M., and Sibley, D. R. (2004) The role of phosphorylation in D1 dopamine receptor desensitization. J. Biol. Chem. 279, 7999-8010
10. Krupnick, J. G., and Benovic, J. L. (1998) The role of receptor kinase and arrestins in G protein-coupled receptor regulation. Annu. Rev. Pharmacol. Toxicol. 38, 289-319
11. Lefkowitz, R. J. (1998) G protein coupled receptors: new roles for receptor kinases and-arrestins in receptor signaling and desensitization. J. Biol. Chem. 273, 18677-18680
12. Watanabe, H., Xu, J., Bengra, C., Jose, P. A., and Felder, R. A. (2002) Desensitization of human renal D1 dopamine receptors by G protein-coupled receptor kinase 4 Kidney Int. 62, 790-798
13. Brismar, H., Hua, X., Adachi, S., and Holtback, U. (2006) The role of endocytosis in renal dopamine D1 receptor signaling. Pflügers Arch. 451, 793-802
14. Drake, M. T., Shenoy, S. K., and Lefkowitz, R. J. (2006) Trafficking of G protein-coupled receptors. Circ. Res. 99, 570-582
15. Teasdale, R. D., Loci, D., Houghton, F., Karlsson, L., and Gleeson, P. A. (2001) A large family of endosome-localized proteins related to sorting nexin Biochem. J. 358, 7-16
16. Carlton, J., Bujny, M., Peter, B. J., Oorschot, V. M., Rutherford, A., Mellor, H., Klumperman, J., McMahon, H. T., and Cullen, P. J. (2004) Sorting nexin-1 mediates tubular endosome-to-TGN transport through coincidence sensing of high-curvature membranes and 3-phosphoinositides. Curr. Biol. 14, 1791-1800
17. Peter, B. J., Kent, H. M., Mills, I. G., Vallis, Y., Butler, P. J. G., Evans, P. R., and McMahon, H. T. (2004) BAR domains as sensors of membrane curvature: The amphiphysin BAR structure. Science 303, 495-499
18. Habermann, B. (2004) The BAR-domain family of proteins: a case of bending and binding? EMBO Rep. 5, 250-255
19. Wassmer, T., Attar, N., Bujny, M., Oakley, J., Traer, C. J., and Cullen, P. J. (2007) A loss-of-function screen reveals SNX5 and SNX6 as potential components of the mammalian retromer. J. Cell Sci. 120, 45-54
20. Yoo, K-W., Kim, E-H., Jung, S-H., Rhee, M., Koo, B.-K., Yoon, K-J., Kong, Y-Y., and Kim, C-H. (2006) Snx5, as a Mind bombbinding protein, is expressed in hematopoietic and endothelial precursor cells in zebrafish. FEBS Lett. 580, 4409-4416
21. Kurten, R. C., Cadena, D. L., and Gill, G. N. (1996) Enhanced degradation of EGF receptors by a sorting nexin, SNX1. Science 272, 1008-1010
22. Kaelin, W. G., Pallas, D. C., DeCaprio, J. A., Kaye, F. J., and Livingston, D. M. (1991) Identification of cellular proteins that can interact specifically with the T/E1A-binding region of the retinoblastoma gene product. Cell 64, 521-532
23. Costa, M. Z., Bacchi, C. E., and Franco, M. (2006) Histogenesis of the acquired cystic kidney disease: an immunohistochemical study. Appl. Immunohistochem. Mol. Morphol. 14, 348-352
24. Li, H., Li, H. F., Felder, R. A., Periasamy, A., and Jose, P. A. (2008) Rab4 and Rab11 coordinately regulate the recycling of angiotensin II type I receptor as demonstrated by fluorescence resonance energy transfer microscopy. J. Biomed. Opt. 13, 031206
25. Sun, Y., Day, R. N., Periasamy, A. (2011) Investigating proteinprotein interactions in living cells using fluorescence lifetime imaging microscopy. Nat. Protoc. 6, 1324-1340
26. Yu, P., Han, W., Villar, V. A., Li, H., Arnaldo, F. B., Concepcion, G. P., Felder, R. A., Quinn, M. T., and Jose, P. A. (2011) Dopamine D1 receptor-mediated inhibition of NADPH oxidase activity in human kidney cells occurs via protein kinase A-protein kinase C cross talk. Free Radic. Biol. Med. 50, 832-840
27. 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, 3872-3877
28. Yatabe, J., Sanada, H., Midorikawa, S., Hashimoto, S., Watanabe, T., Andrews, P. M., Armando, I., Wang, X., Felder, R. A., and Jose, P. A. (2008) Effects of decreased renal cortical expression of G protein-coupled receptor kinase 4 and angiotensin type 1 receptors in rats. Hypertens. Res. 31, 1455-1464
29. Yoneda, M., Sanada, H., Yatabe, J., Midorikawa, S., Hashimoto, S., Sasaki, M., Katoh, T., Watanabe, T., Andrews, P. M., Jose, P. A., and Felder. R. A. (2005) Differential effects of angiotensin II type-1 receptor antisense oligonucleotides on renal function in spontaneously hypertensive rats. Hypertension 46, 58-65
30. Brana, C., Caille, I., Pellevoisin, C., Charron, G., Aubert, I., Caron, M. G., Carles, D., Vital, C., and Bloch, B. (1996) Ontogeny of the striatal neurons expressing the D1 dopamine receptor in humans. J. Comp. Neurol. 370, 23-34
31. Tiberi, M., Nash, S. R., Bertrand, L., Lefkowitz, R. J., and Caron, M. G. (1996) Differential regulation of dopamine D1A receptor responsiveness by various G protein-coupled receptor kinases. J. Biol. Chem. 271, 3771-3778
32. Rankin, M. L., Marinec, P. S., Cabrera, D. M., Wang, Z., Jose, P. A., and Sibley, D. R. (2006) The D1 dopamine receptor is constitutively phosphorylated by G protein-coupled receptor kinase4. Mol. Pharmacol. 69, 759-769
33. Sanada, H., Yatabe, J., Midorikawa, S., Katoh, T., Hashimoto, S., Watanabe, T., Xu, J., Luo, Y., Wang, X., Zeng, C., Armando, I., Felder, R. A., and Jose, P. A. (2006) Amelioration of genetic hypertension by suppression of renal G protein-coupled receptor kinase type 4 expression. Hypertension 47, 1131-1139
34. Marchese, A., Paing, M. M., Temple, B. R., and Trejo, J. (2008) G protein-coupled receptor sorting to endosomes and lysosomes. Annu. Rev. Pharmacol. Toxicol. 48, 601-629
35. Brismar, H., Asghar, M., Carey, R. M., Greengard, P., and Aperia, A. (1998) Dopamine-induced recruitment of dopamine D1 receptors to the plasma membrane. Proc. Natl. Acad. Sci. U. S. A. 95, 5573-5578
36. Vickery, R. G., and von Zastrow, M. (1999) Distinct dynamindependent and-independent mechanisms target structurally homologous dopamine receptors to different endocytic membranes. J. Cell Biol. 144, 31-43
37. Rapacciuolo, A., Suvarna, S., Barki-Harrington, L., Luttrell, L. M., Cong, M., Lefkowitz, R. J., and Rockman, H. A. (2003) Protein kinase A and G protein-coupled receptor kinase phosphorylation mediates 1 adrenergic receptor endocytosis through different pathways. J. Biol. Chem. 278, 35403-35411
38. Kong, M. M., Hasbi, A., Mattocks, M., Fan, T., ODowd, B. F., and George, S. R. (2007) Regulation of D1 dopamine receptor trafficking and signaling by caveolin-1. Mol. Pharmacol. 72, 1157-1170
39. Yu, P., Yang, Z., Jones, J. E., Wang, Z., Owens, S. A., Mueller, S. C., Felder, R. A., and Jose, P. A. (2004) D1 dopamine receptor signaling involves caveolin-2 in HEK-293 cells. Kidney Int. 66, 2167-2180
40. Shih, M., Lin, F., Scott, J. D., Wang, H. Y., and Malbon, C. C. (1999) Dynamic complexes of 2-adrenergic receptors with protein kinases and phosphatases and the role of gravin. J. Biol. Chem. 274, 1588-1595
41. He, Y., Yu, L. P., and Jin, G. Z. (2009) Differential distributions and trafficking properties of dopamine D1 and D5 receptors in nerve cells. Neurosci. Bull. 25, 43-53
42. Premont, R. T., Macrae, A. D., Stoffel, R. H., Chung, N., Pitcher, J. A., Ambrose, C., Inglese, J., MacDonald, M. E., and Lefkowitz, R. J. (1996) Characterization of the G protein-coupled receptor kinase GRK4. Identification of four splice variants. J. Biol. Chem. 271, 6403-6410
43. 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
44. Ostrom, R. S., Liu, X., Head, B. P., Gregorian, C., Seasholtz, T. M., and Insel, P. A. (2002) Localization of adenylyl cyclase isoforms and G protein-coupled receptors in vascular smooth muscle cells: expression in caveolin-rich and noncaveolin domains. Mol. Pharmacol. 62, 983-992
45. Oh, P., and Schnitzer, J. E. (2001) Segregation of heterotrimeric G proteins in cell surface microdomains. Gq binds caveolin to concentrate in caveolae, whereas Gi and Gs target lipid rafts by default. Mol. Biol. Cell 12, 685-698
46. Felder, C. C., Campbell, T., Albrecht, F., and Jose, P. A. (1990) Dopamine inhibits Na-H exchanger activity in renal BBMV by stimulation of adenylate cyclase. Am. J. Physiol. 59, F297-F303
47. Ng, G. Y., Trogadis, J., Stevens, J., Bouvier, M., ODowd, B. F., and George, S. R. (1995) Agonist-induced desensitization of dopamine D1 receptor-stimulated adenylyl cyclase activity is temporally and biochemically separated from D1 receptor internalization. Proc. Natl. Acad. Sci. U. S. A. 92, 10157-10161
48. Trivedi, M., Narkar, V. A., Hussain, T., and Lokhandwala, M. F. (2004) Dopamine recruits D1A receptors to NaK-ATPaserich caveolar plasma membranes in rat renal proximal tubules. Am. J. Physiol. Renal. Physiol. 287, F921-F931
49. Vargas, G. A., and Von Zastrow, M. (2004) Identification of a novel endocytic recycling signal in the D1 dopamine receptor. J. Biol. Chem. 279, 37461-37469
50. Guo, Y., Jose, P. A. (2011) C-terminal di-leucine motif of dopamine D1 receptor plays an important role in its plasma membrane trafficking. PLoS One 6, e29204
51. Lamey, M., Thompson, M., Varghese, G., Chi, H., Sawzdargo, M., George, S. R., and ODowd, B. F. (2002) Distinct residues in the carboxyl tail mediate agonist-induced desensitization and internalization of the human dopamine D1 receptor. J. Biol. Chem. 277, 9415-9421
52. Jackson, A., Iwasiow, R. M., Chaar, Z. Y., Nantel, M-F., and Tiberi, M. (2002) Homologous regulation of the heptahelical D1A receptor responsiveness: specific cytoplasmic tail regions mediate dopamine-induced phosphorylation, desensitization and endocytosis. J. Neurochem. 82, 683-697
53. Zhang, M. Z., Yao, B., Wang, S., Fan, X., Wu, G., Yang, H., Yin, H., Yang, S., and Harris, R. C. (2011) Intrarenal dopamine deficiency leads to hypertension and decreased longevity in mice. J. Clin. Invest. 121, 2845-2854
54. Jiang, D., and Sibley, D. R. (1999) Regulation of D1 dopamine receptors with mutations of protein kinase phosphorylation sites: attenuation of the rate of agonist-induced desensitization. Mol. Pharmacol. 56, 675-683