Altered agonist sensitivity of a mutant V2 receptor suggests a novel therapeutic strategy for nephrogenic diabetes insipidus

Molecular Endocrinology

Volumn 28, Issue 5, 2014, Pages 634-643

  Erdélyi, László Sándor ^a,b   Balla, András ^a,b   Patócs, Attila ^a   Tóth, Miklós ^a   Várnai, Péter ^a,b   Hunyady, László ^a,b  

^a SEMMELWEIS UNIVERSITY   (Hungary)

^b MTA SE Laboratory of Molecular Physiology   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

ARGIPRESSIN; BETA ARRESTIN; DESMOPRESSIN; HEMAGGLUTININ; VASOPRESSIN DERIVATIVE; VASOPRESSIN V1 RECEPTOR; VASOPRESSIN V2 RECEPTOR; ANTIDIURETIC AGENT; ARGIPRESSIN[1 DEAMINO]; AVP PROTEIN, HUMAN; CYCLIC AMP; NEUROPHYSIN; PROTEIN PRECURSOR; VASOPRESSIN RECEPTOR;

AGONIST; ARTICLE; BIOLUMINESCENCE RESONANCE ENERGY TRANSFER; BIOSENSOR; CASE REPORT; CELL SURFACE; CELLULAR DISTRIBUTION; CONFOCAL LASER MICROSCOPY; FLOW CYTOMETRY; HEK293 CELL LINE; HUMAN; MALE; MISSENSE MUTATION; MOUSE; NEPHROGENIC DIABETES INSIPIDUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; TREATMENT PLANNING; ADULT; AGONISTS; ANIMAL; DIABETES INSIPIDUS, NEPHROGENIC; ENDOPLASMIC RETICULUM; GENETICS; IN VITRO STUDY; METABOLISM; PHYSIOLOGY; RAT; SECOND MESSENGER;

ADULT; ANIMALS; ANTIDIURETIC AGENTS; CYCLIC AMP; DEAMINO ARGININE VASOPRESSIN; DIABETES INSIPIDUS, NEPHROGENIC; DNA MUTATIONAL ANALYSIS; ENDOPLASMIC RETICULUM; HEK293 CELLS; HUMANS; IN VITRO TECHNIQUES; MALE; MICE; MUTATION, MISSENSE; NEUROPHYSINS; PROTEIN PRECURSORS; RATS; RECEPTORS, VASOPRESSIN; SECOND MESSENGER SYSTEMS; VASOPRESSINS;

EID: 84899735563     PISSN: 08888809     EISSN: 19449917     Source Type: Journal    
DOI: 10.1210/me.2013-1424     Document Type: Article

References (46)

1. Lagerström MC, Schiöth HB. Structural diversity of G proteincoupled receptors and significance for drug discovery. Nat Rev Drug Discov. 2008; 7: 339-357.
2. Ma P, Zemmel R. Value of novelty? Nat Rev Drug Discov. 2002; 1: 571-572.
3. Schöneberg T, Schulz A, Biebermann H, Hermsdorf T, Römpler H, Sangkuhl K. Mutant G-protein-coupled receptors as a cause of human diseases. Pharmacol Ther. 2004; 104: 173-206.
4. Ala Y, Morin D, Mouillac B, et al. Functional studies of twelve mutant V2 vasopressin receptors related to nephrogenic diabetes insipidus: molecular basis of a mild clinical phenotype. J Am Soc Nephrol. 1998; 9: 1861-1872.
5. Tao YX. Inactivating mutations ofGprotein-coupled receptors and diseases: structure-function insights and therapeutic implications. Pharmacol Ther. 2006; 111: 949-973.
6. Arthus MF, Lonergan M, Crumley MJ, et al. Report of 33 novel AVPR2 mutations and analysis of 117 families with X-linked nephrogenic diabetes insipidus. J Am Soc Nephrol. 2000; 11: 1044-1054.
7. Moeller HB, Rittig S, Fenton RA. Nephrogenic diabetes insipidus: essential insights into the molecular background and potential therapies for treatment. Endocr Rev. 2013; 34: 278-301.
8. Ligeti E, Csepanyi-Komi R, Hunyady L. Physiological mechanisms of signal termination in biological systems. Acta Physiol (Oxf). 2012; 204: 469-478.
9. Rochdi MD, Vargas GA, Carpentier E, et al. Functional characterization of vasopressin type 2 receptor substitutions (R137H/C/L) leading to nephrogenic diabetes insipidus and nephrogenic syndrome of inappropriate antidiuresis: implications for treatments. Mol Pharmacol. 2010; 77: 836-845.
10. Böhm SK, Grady EF, Bunnett NW. Regulatory mechanisms that modulate signalling by G-protein-coupled receptors. Biochem J. 1997; 322(Pt 1): 1-18.
11. Luttrell LM, Lefkowitz RJ. The role of β-arrestins in the termina-tion and transduction of G-protein-coupled receptor signals. J Cell Sci. 2002; 115(Pt 3): 455-465.
12. Gáborik Z, Hunyady L. Intracellular trafficking of hormone receptors. Trends Endocrinol Metab. 2004; 15: 286-293.
13. Spanakis E, Milord E, Gragnoli C. AVPR2 variants and mutations in nephrogenic diabetes insipidus: review and missense mutation significance. J Cell Physiol. 2008; 217: 605-617.
14. Wesche D, Deen PM, Knoers NV. Congenital nephrogenic diabetes insipidus: the current state of affairs. Pediatr Nephrol. 2012; 27: 2183-2204.
15. Robben JH, Knoers NV, Deen PM. Cell biological aspects of the vasopressin type-2 receptor and aquaporin 2 water channel in nephrogenic diabetes insipidus. Am J Physiol Renal Physiol. 2006; 291: F257-F270.
16. Barak LS, Oakley RH, Laporte SA, Caron MG. Constitutive arrestin-mediated desensitization of a human vasopressin receptor mutant associated with nephrogenic diabetes insipidus. Proc Natl Acad Sci USA. 2001; 98: 93-98.
17. Morello JP, Salahpour A, Lapèrriere A, et al. Pharmacological chaperones rescue cell-surface expression and function of misfolded V2 vasopressin receptor mutants. J Clin Invest. 2000; 105: 887-895.
18. Robben JH, Sze M, Knoers NV, Deen PM. Functional rescue of vasopressin V2 receptor mutants inMDCKcells by pharmacochaperones: relevance to therapy of nephrogenic diabetes insipidus. Am J Physiol Renal Physiol. 2007; 292: F253-F260.
19. Wüller S, Wiesner B, Löffler A, et al. Pharmacochaperones posttranslationally enhance cell surface expression by increasing conformational stability of wild-type and mutant vasopressin V2 receptors. J Biol Chem. 2004; 279: 47254-47263.
20. Bernier V, Lagacé M, Lonergan M, Arthus MF, Bichet DG, Bouvier M. Functional rescue of the constitutively internalized V2 vasopressin receptor mutant R137H by the pharmacological chaperone action of SR49059. Mol Endocrinol. 2004; 18: 2074-2084.
21. Ranadive SA, Ersoy B, Favre H, Cheung CC, Rosenthal SM, Miller WL, Vaisse C. Identification, characterization and rescue of a novel vasopressin-2 receptor mutation causing nephrogenic diabetes insipidus. Clin Endocrinol (Oxf). 2009; 71: 388-393.
22. Robben JH, Kortenoeven ML, Sze M, et al. Intracellular activation of vasopressin V2 receptor mutants in nephrogenic diabetes insipidus by nonpeptide agonists. Proc Natl Acad Sci USA. 2009; 106: 12195-12200.
23. Jean-Alphonse F, Perkovska S, Frantz MC, et al. Biased agonist pharmacochaperones of the AVP V2 receptor may treat congenital nephrogenic diabetes insipidus. J Am Soc Nephrol. 2009; 20: 2190-2203.
24. Woo J, von Arnim AG. Mutational optimization of the coelenterazine-dependent luciferase from Renilla. Plant Methods. 2008; 4: 23.
25. Zacharias DA, Violin JD, Newton AC, Tsien RY. Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science. 2002; 296: 913-916.
26. Turu G, Szidonya L, Gáborik Z, et al. Differential β-arrestin binding of AT1 and AT2 angiotensin receptors. FEBS Lett. 2006; 580: 41-45.
27. Balla A, Tóth DJ, Soltész-Katona E, et al. Mapping of the localization of type 1 angiotensin receptor in membrane microdomains using bioluminescence resonance energy transfer-based sensors. J Biol Chem. 2012; 287: 9090-9099.
28. Klarenbeek JB, Goedhart J, Hink MA, Gadella TW, Jalink K. A mTurquoise-based cAMP sensor for both FLIM and ratiometric read-out has improved dynamic range. PLoS One. 2011; 6: e19170.
29. Takahashi K, Makita N, Manaka K, et al. V2 vasopressin receptor (V2R) mutations in partial nephrogenic diabetes insipidus highlight protean agonism of V2R antagonists. J Biol Chem. 2012; 287: 2099-2106.
30. Shenoy SK, Lefkowitz RJ. Trafficking patterns of β-arrestin and G protein-coupled receptors determined by the kinetics of β-arrestin deubiquitination. J Biol Chem. 2003; 278: 14498-14506.
31. Toth DJ, Toth JT, Gulyas G, et al. Acute depletion of plasma membrane phosphatidylinositol 4, 5-bisphosphate impairs specific steps in endocytosis of the G-protein-coupled receptor. J Cell Sci. 2012; 125(Pt 9): 2185-2197.
32. Sawyer WH, Acosta M, Balaspiri L, Judd J, Manning M. Structural changes in the arginine vasopressin molecule that enhance antidiuretic activity and specificity. Endocrinology. 1974; 94: 1106-1115.
33. Manning M, Lowbridge J, Stier CT Jr, Haldar J, Sawyer WH. [1-Deaminopenicillamine, 4-valine]-8-D-arginine-vasopressin, a highly potent inhibitor of the vasopressor response to argininevasopressin. J Med Chem. 1977; 20: 1228-1230.
34. Hase S, Sakakibara S, Wahrenburg M, Kirchberger M, Schwartz IL, Walter R. 1, 6-Aminosuberic acid analogs of lysine-and argininevasopressin and-vasotocin. Synthesis and biological properties. J Am Chem Soc. 1972; 94: 3590-3600.
35. Barak LS, Ménard L, Ferguson SS, Colapietro AM, Caron MG. The conserved seven-transmembrane sequence NP(X)2, 3Y of the Gprotein-coupled receptor superfamily regulates multiple properties of the β2-adrenergic receptor. Biochemistry. 1995; 34: 15407-15414.
36. Hunyady L, Bor M, Baukal AJ, Balla T, 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. 1995; 270: 16602-16609.
37. Rosenthal W, Antaramian A, Gilbert S, Birnbaumer M. Nephrogenic diabetes insipidus. A V2 vasopressin receptor unable to stimulate adenylyl cyclase. J Biol Chem. 1993; 268: 13030-13033.
38. Kocan M, See HB, Sampaio NG, Eidne KA, Feldman BJ, Pfleger KD. Agonist-independent interactions between β-arrestins and mutant vasopressin type II receptors associated with nephrogenic syndrome of inappropriate antidiuresis. Mol Endocrinol. 2009; 23: 559-571.
39. Hunyady L, Catt KJ. Pleiotropic AT1 receptor signaling pathways mediating physiological and pathogenic actions of angiotensin II. Mol Endocrinol. 2006; 20: 953-970.
40. Ehnis T, Hocher B, Abou-Rebyeh H, Oelkers W, Hensen J. Expression of vasopressin receptors (V2-subtype) on LLC-PK1 cells during cell culture. Eur J Clin Chem Clin Biochem. 1993; 31: 273-276.
41. Ferguson SS. Evolving concepts in G protein-coupled receptor endocytosis: the role in receptor desensitization and signaling. Pharmacol Rev. 2001; 53: 1-24.
42. Bichet DG. TMF: Nephrogenic Diabetes Insipidus. In Scriver's Online Metabolic and Molecular Bases of Inherited Disease; 2007. http://www. ommbid. com. Accessed 2010.
43. Manning M, Misicka A, Olma A, et al. Oxytocin and vasopressin agonists and antagonists as research tools and potential therapeutics. J Neuroendocrinol. 2012; 24: 609-628.
44. Koshimizu TA, Nakamura K, Egashira N, Hiroyama M, Nonoguchi H, Tanoue A. Vasopressin V1a and V1b receptors: from molecules to physiological systems. Physiol Rev. 2012; 92: 1813-1864.
45. Russell JA, Walley KR, Singer J, et al. Vasopressin versus norepinephrine infusion in patients with septic shock. N Engl J Med. 2008; 358: 877-887.
46. Czakó L, László F, Manning M. Treatment of diabetes insipidus with synthetic vasopressin derivatives (effect of 1-deamino-8-D-arginine vasopressin and 1-deamino-valine-8-D-arginine vasopressin) [in Hungarian]. Orv Hetil. 1980; 121: 773-778.