Functional role of the NPxxY motif in internalization of the type 2 vasopressin receptor in LLC-PK1 cells

American Journal of Physiology - Cell Physiology

Volumn 285, Issue 4 54-4, 2003, Pages

  Bouley, Richard ^a,b   Sun, Tian Xiao ^a   Chenard, Melissa ^a   McLaughlin, Margaret ^a   McKee, Mary ^a   Lin, Herbert Y ^a   Brown, Dennis ^a   Ausiello, Dennis A ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Polarized cell culture; Protein traffic; Tyrosine motif; 1b adaptor motif

Indexed keywords

ADENYLATE CYCLASE; CLATHRIN; CYCLIC AMP; G PROTEIN COUPLED RECEPTOR; PHENYLALANINE; TYROSINE; VASOPRESSIN V2 RECEPTOR;

ANIMAL CELL; APICAL MEMBRANE; ARTICLE; BASOLATERAL MEMBRANE; CELL POLARITY; CELL SURFACE; COATED PIT; CONTROLLED STUDY; EPITHELIUM CELL; IMMUNOFLUORESCENCE; IMMUNOGOLD ELECTRON MICROSCOPY; INTERNALIZATION; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN TRANSPORT; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 0141568143     PISSN: 03636143     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpcell.00477.2002     Document Type: Article

References (68)

1. Andersen-Beckh B, Dehe M, Schulein R, Wiesner B, Rutz C, Liebenhoff U, Rosenthal W, and Oksche A. Polarized expression of the vasopressin V2 receptor in Madin-Darby canine kidney cells. Kidney Int 56: 517-527, 1999.
2. Ausiello DA, Holtzman EJ, Gronich J, and Ercolani L. Cell signalling. In: The Kidney: Physiology and Pathophysiology (2nd ed.), edited by Seldin DW and Giebisch G. New York: Raven, 1995, p. 645-706.
3. Bakris G, Bursztyn M, Gavras I, Bresnahan M, and Gavras H. Role of vasopressin in essential hypertension: racial differences. J Hypertens 15: 545-550, 1997.
4. Barak LS, Menard L, Ferguson SS, Colapietro AM, and Caron MG. The conserved seven-transmembrane sequence NP(X)2,3Y of the G-protein-coupled receptor superfamily regulates multiple properties of the beta 2-adrenergic receptor. Biochemistry 34: 15407-15414, 1995.
5. Barak LS, Tiberi M, Freedman NJ, Kwatra MM, Lefkowitz RJ, and Caron MG. A highly conserved tyrosine residue in G protein-coupled receptors is required for agonist-mediated beta 2-adrenergic receptor sequestration. J Biol Chem 269: 2790-2795, 1994.
6. Becker BN, Cheng HF, Burns KD, and Harris RC. Polarized rabbit type 1 angiotensin II receptors manifest differential rates of endocytosis and recycling. Am J Physiol Cell Physiol 269: C1048-C1056, 1995.
7. Birnbaumer M, Antaramian A, Themmen AP, and Gilbert S. Desensitization of the human V2 vasopressin receptor. Homologous effects in the absence of heterologous desensitization. J Biol Chem 267: 11783-11788, 1992.
8. s/adenylyl cyclase system. Mol Endocrinol 8: 886-894, 1994.
9. Bohm SK, Khitin LM, Smeekens SP, Grady EF, Payan DG, and Bunnett NW. Identification of potential tyrosine-containing endocytic motifs in the carboxyl-tail and seventh transmembrane domain of the neurokinin 1 receptor. J Biol Chem 272: 2363-2372, 1997.
10. Bouley R, Breton S, Sun T, McLaughlin M, Nsumu NN, Lin HY, Ausiello DA, and Brown D. Nitric oxide and atrial natriuretic factor stimulate cGMP-dependent membrane insertion of aquaporin 2 in renal epithelial cells. J Clin Invest 106: 1115-1126, 2000.
11. Bowen-Pidgeon D, Innamorati G, Sadeghi HM, and Birnbaumer M. Arrestin effects on internalization of vasopressin receptors. Mol Pharmacol 59: 1395-1401, 2001.
12. Bremnes T, Paasche JD, Mehlum A, Sandberg C, Bremnes B, and Attramadal H. Regulation and intracellular trafficking pathways of the endothelin receptors. J Biol Chem 275: 17596-17604, 2000.
13. Brown D and Nielsen S. Cell biology of vasopressin action. In: Brenner and Rector's the Kidney (6th ed.), edited by Brenner BM. Boston: Saunders, 2000, p. 575-594.
14. Carman CV, Lisanti MP, and Benovic JL. Regulation of G protein-coupled receptor kinases by caveolin. J Biol Chem 274: 8858-8864, 1999.
15. Chun M, Liyanage UK, Lisanti MP, and Lodish HF. Signal transduction of a G protein-coupled receptor in caveolae: colocalization of endothelin and its receptor with caveolin. Proc Natl Acad Sci USA 91: 11728-11732, 1994.
16. Cowley AW Jr, Cushman WC, and Quillen EW Jr, Skelton MM, and Langford HG. Vasopressin elevation in essential hypertension and increased responsiveness to sodium intake. Hypertension 3: I93-I100, 1981.
17. Dale LB, Bhattacharya M, Seachrist JL, Anborgh PH, and Ferguson SS. Agonist-stimulated and tonic internalization of metabotropic glutamate receptor 1a in human embryonic kidney 293 cells: agonist-stimulated endocytosis is beta-arrestin1 isoform-specific. Mol Pharmacol 60: 1243-1253, 2001.
18. 1 MF-2 smooth muscle cells. J Biol Chem 272: 17858-17866, 1997.
19. Dessy C, Kelly RA, Balligand JL, and Feron O. Dynamin mediates caveolar sequestration of muscarinic cholinergic receptors and alteration in NO signaling. EMBO J 19: 4272-4280, 2000.
20. Folsch H, Ohno H, Bonifacino JS, and Mellman I. A novel clathrin adaptor complex mediates basolateral targeting in polarized epithelial cells. Cell 99: 189-198, 1999.
21. Gan Y, McGraw TE, and Rodriguez-Boulan E. The epithelial-specific adaptor AP1B mediates post-endocytic recycling to the basolateral membrane. Nat Cell Biol 4: 605-609, 2002.
22. Garcia-Perez A and Smith WL. Apical-basolateral membrane asymmetry in canine cortical collecting tubule cells. Bradykinin, arginine vasopressin, prostaglandin E2 interrelationships. J Clin Invest 74: 63-74, 1984.
23. Hashimoto J, Imai Y, Minami N, Munakata M, and Abe K. Effects of vasopressin V1 and V2 receptor antagonists on the development of salt-induced hypertension in Dahl rats. J Cardiovasc Pharmacol 26: 548-554, 1995.
24. Hashimoto Y, Ozaki J, Yasuhara M, Hori R, Suga S, Itoh H, Nakao K, and Inui K. Functional evidence for an apical ANP receptor in LLC-PK1 kidney epithelial cells. Eur J Pharmacol 268: 443-445, 1994.
25. Hayes G, Forgo J, Bringhurst FR, Segre G, and Murer H. Expression of parathyroid hormone receptors in MDCK and LLC-PK1 cells. Pflügers Arch 430: 636-644, 1995.
26. Henley JR, Krueger EW, Oswald BJ, and McNiven MA. Dynamin-mediated internalization of caveolae. J Cell Biol 141: 85-99, 1998.
27. 2 receptor in Madin Darby canine kidney epithelial cells. Mol Pharmacol 60: 1031-1039, 2001.
28. Hocher B, Merker HJ, Durr JA, Schiller S, Gross P, and Hensen J. Internalization of V2-vasopressin receptors in LLC-PK1-cells: evidence for receptor-mediated endocytosis. Biochem Biophys Res Commun 186: 1376-1383, 1992.
29. Hunyady L, Bor M, Baukal AJ, Balla T, and Catt KJ. A conserved NPLFY sequence contributes to agonist binding and signal transduction but is not an internalization signal for the type 1 angiotensin II receptor. J Biol Chem 270: 16602-16609, 1995.
30. Igarashi J and Michel T. Agonist-modulated targeting of the EDG-1 receptor to plasmalemmal caveolae. eNOS activation by sphingosine 1-phosphate and the role of caveolin-1 in sphingo-lipid signal transduction. J Biol Chem 275: 32363-32370, 2000.
31. Innamorati G, Le Gouill C, Balamotis M, and Birnbaumer M. The long and the short cycle. Alternative intracellular routes for trafficking of G-protein coupled receptors. J Biol Chem 276: 13096-13103, 2001.
32. Innamorati G, Sadeghi H, Eberle AN, and Birnbaumer M. Phosphorylation of the V2 vasopressin receptor. J Biol Chem 272: 2486-2492, 1997.
33. Innamorati G, Sadeghi HM, Tran NT, and Birnbaumer M. A serine cluster prevents recycling of the V2 vasopressin receptor. Proc Natl Acad Sci USA 95: 2222-2226, 1998.
34. Ishizaka N, Griendling KK, Lassegue B, and Alexander RW. Angiotensin II type 1 receptor: relationship with caveolae and caveolin after initial agonist stimulation. Hypertension 32: 459-466, 1998.
35. Jans DA and Hemmings BA. cAMP-dependent protein kinase activation affects vasopressin V2-receptor number and internalization in LLC-PK1 renal epithelial cells. FEBS Lett 281: 267-271, 1991.
36. Jurzak M, Jans DA, Haase W, Peters R, and Fahrenholz F. Generation of anti-idiotypic monoclonal antibodies recognizing vasopressin receptors in cultured cells and kidney sections. Exp Cell Res 203: 182-191, 1992.
37. Kim JK, Summer SN, and Schrier RW. Arginine vasopressin receptor internalization and recycling in rat renal collecting tubules. J Recept Res 14: 139-152, 1994.
38. Kirk KL. Binding and internalization of a fluorescent vasopressin analogue by collecting duct cells. Am J Physiol Cell Physiol 255: C622-C632, 1988.
39. Kramer HK, Andria ML, Kushner SA, Esposito DH, Hiller JM, and Simon EJ. Mutation of tyrosine 318 (Y318F) in the delta-opioid receptor attenuates tyrosine phosphorylation, agonist-dependent receptor internalization, and mitogen-activated protein kinase activation. Brain Res Mol Brain Res 79: 55-66, 2000.
40. Krisch B, Feindt J, and Mentlein R. Immunoelectronmicroscopic analysis of the ligand-induced internalization of the somatostatin receptor subtype 2 in cultured human glioma cells. J Histochem Cytochem 46: 1233-1242, 1998.
41. Laporte SA, Servant G, Richard DE, Escher E, Guillemette G, and Leduc R. The tyrosine within the NPXnY motif of the human angiotensin II type 1 receptor is involved in mediating signal transduction but is not essential for internalization. Mol Pharmacol 49: 89-95, 1996.
42. Lefkowitz RJ. G protein-coupled receptors. III. New roles for receptor kinases and beta-arrestins in receptor signaling and desensitization. J Biol Chem 273: 18677-18680, 1998.
43. LeVier DG, McCoy DE, and Spielman WS. Functional localization of adenosine receptor-mediated pathways in the LLC-PK1 renal cell line. Am J Physiol Cell Physiol 263: C729-C735, 1992.
44. Lolait SJ, O'Carroll AM, McBride OW, Konig M, Morel A, and Brownstein MJ. Cloning and characterization of a vasopressin V2 receptor and possible link to nephrogenic diabetes insipidus. Nature 357: 336-339, 1992.
45. Lutz W and Kumar R. Hypertonic sucrose treatment enhances second messenger accumulation in vasopressin-sensitive cells. Am J Physiol Renal Fluid Electrolyte Physiol 264: F228-F233, 1993.
46. Lutz W, Sanders M, Salisbury J, and Kumar R. Internalization of vasopressin analogs in kidney and smooth muscle cells: evidence for receptor-mediated endocytosis in cells with V2 or V1 receptors. Proc Natl Acad Sci USA 87: 6507-6511, 1990.
47. Matter K, Hunziker W, and Mellman I. Basolateral sorting of LDL receptor in MDCK cells: the cytoplasmic domain contains two tyrosine-dependent targeting determinants. Cell 71: 741-753, 1992.
48. Mimura Y, Ogura T, Kataoka H, Oishi T, Asano N, Kishida M, Yamauchi T, Ogawa N, and Makino H. Alterations of renal V1 and V2 receptors in spontaneously hypertensive rats and DOCA-salt hypertensive rats using computerized quantification for macro-autoradiogram. Res Commun Mol Pathol Pharmacol 95: 43-56, 1997.
49. Nonoguchi H, Owada A, Kobayashi N, Takayama M, Terada Y, Koike J, Ujiie K, Marumo F, Sakai T. and Tomita K. Immunohistochemical localization of V2 vasopressin receptor along the nephron and functional role of luminal V2 receptor in terminal inner medullary collecting ducts. J Clin Invest 96: 1768-1778, 1995.
50. Oakley RH, Laporte SA, Holt JA, Barak LS, and Caron MG. Association of beta-arrestin with G protein-coupled receptors during clathrin-mediated endocytosis dictates the profile of receptor resensitization. J Biol Chem 274: 32248-32257, 1999.
51. Oakley RH, Laporte SA, Holt JA, Caron MG, and Barak LS. Differential affinities of visual arrestin, beta arrestin1, and beta arrestin2 for G protein-coupled receptors delineate two major classes of receptors. J Biol Chem 275: 17201-17210, 2000.
52. Odorizzi G and Trowbridge IS. Structural requirements for basolateral sorting of the human transferrin receptor in the biosynthetic and endocytic pathways of Madin-Darby canine kidney cells. J Cell Biol 137: 1255-1264, 1997.
53. Pfaller W, Gstraunthaler G, and Loidl P. Morphology of the differentiation and maturation of LLC-PK1 epithelia. J Cell Physiol 142: 247-254, 1990.
54. Pfeiffer R, Kirsch J, and Fahrenholz F. Agonist and antagonist-dependent internalization of the human vasopressin V2 receptor. Exp Cell Res 244: 327-339, 1998.
55. Ravid R, Swaab DF, and Pool CW. Immunocytochemical localization of vasopressin-binding sites in the rat kidney. J Endocrinol 105: 133-140, 1985.
56. Roseberry AG and Hosey MM. Internalization of the M2 muscarinic acetylcholine receptor proceeds through an atypical pathway in HEK293 cells that is independent of clathrin and caveolae. J Cell Sci 114: 739-746, 2001.
57. Rosendorff A, Ebersole BJ, and Sealfon SC. Conserved helix 7 tyrosine functions as an activation relay in the serotonin 5HT(2C) receptor. Brain Res Mol Brain Res 84: 90-96, 2000.
58. Salas PJ, Misek DE, Vega-Salas DE, Gundersen D, Cereijido M, and Rodriguez-Boulan E. Microtubules and actin filaments are not critically involved in the biogenesis of epithelial cell surface polarity. J Cell Biol 102: 1853-1867, 1986.
59. Saunders C, Keefer JR, Bonner CA, and Limbird LE. Targeting of G protein-coupled receptors to the basolateral surface of polarized renal epithelial cells involves multiple, non-contiguous structural signals. J Biol Chem 273: 24196-24206, 1998.
60. Sawyer WH and Manning M. The development of potent and specific vasopressin antagonists. Kidney Int Suppl 26: S34-S37, 1988.
61. Schulein R, Lorenz D, Oksche A, Wiesner B, Hermosilla R, Ebert J, and Rosenthal W. Polarized cell surface expression of the green fluorescent protein-tagged vasopressin V2 receptor in Madin Darby canine kidney cells. FEBS Lett 441: 170-176, 1998.
62. Schwencke C, Okumura S, Yamamoto M, Geng YJ, and Ishikawa Y. Colocalization of beta-adrenergic receptors and caveolin within the plasma membrane. J Cell Biochem 75: 64-72, 1999.
63. Segredo V, Burford NT, Lameh J, and Sadee W. A constitutively internalizing and recycling mutant of the μ-opioid receptor. J Neurochem 68: 2395-2404, 1997.
64. Simpson JC, Smith DC, Roberts LM, and Lord JM. Expression of mutant dynamin protects cells against diphtheria toxin but not against ricin. Exp Cell Res 239: 293-300, 1998.
65. Slice LW, Wong HC, Sternini C, Grady EF, Bunnett NW, and Walsh JH. The conserved NPXnY motif present in the gastrin-releasing peptide receptor is not a general sequestration sequence. J Biol Chem 269: 21755-21761, 1994.
66. Von Bonsdorff CH, Fuller SD, and Simons K. Apical and basolateral endocytosis in Madin-Darby canine kidney (MDCK) cells grown on nitrocellulose filters. EMBO J 4: 2781-2792, 1985.
67. Whistler JL, Enquist J, Marley A, Fong J, Gladher F, Tsuruda P, Murray SR, and Von Zastrow M. Modulation of postendocytic sorting of G protein-coupled receptors. Science 297: 615-620, 2002.
68. Yeaman C, Heinflink M, Falck-Pedersen E, Rodriguez-Boulan E, and Gershengorn MC. Polarity of TRH receptors in transfected MDCK cells is independent of endocytosis signals and G protein coupling. Am J Physiol Cell Physiol 270: C753-C762, 1996.