Pharmacoperones and the calcium sensing receptor: Exogenous and endogenous regulators

Pharmacological Research

Volumn 83, Issue , 2014, Pages 30-37

  Breitwieser, Gerda E ^a  

^a WEIS CENTER FOR RESEARCH   (United States)

Author keywords

Calcilytics; Calcimimetics; Calcium sensing receptor; Membrane protein biosynthesis; Pharmacologic chaperone; Pharmacoperones

Indexed keywords

CALCIUM; CALNEXIN; CALRETICULIN; DIHYDROPYRIDINE DERIVATIVE; GLUTATHIONE; MAGNESIUM; NEURONAL CALCIUM SENSOR; 1,4-DIHYDROPYRIDINE; CALCIUM SENSING RECEPTOR;

AMINO ACID SEQUENCE; BINDING SITE; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; DIMERIZATION; DISULFIDE BOND; ENDOPLASMIC RETICULUM; HUMAN; HYDROPHOBIC HELICAL INTERACTION; MOLECULAR INTERACTION; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; REVIEW; SIGNAL TRANSDUCTION; UPREGULATION; ALLOSTERISM; ANIMAL; DRUG DEVELOPMENT; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MUTATION;

ALLOSTERIC REGULATION; ANIMALS; CALCIUM; DIHYDROPYRIDINES; DRUG DISCOVERY; GENE EXPRESSION REGULATION; GLUTATHIONE; HUMANS; MUTATION; PROTEIN BIOSYNTHESIS; PROTEIN FOLDING; PROTEIN TRANSPORT; RECEPTORS, CALCIUM-SENSING;

EID: 84901936219     PISSN: 10436618     EISSN: 10961186     Source Type: Journal    
DOI: 10.1016/j.phrs.2013.11.006     Document Type: Review

References (94)

1. Z. Saidak, M. Brazier, S. Kamel, and R. Mentaverri Agonists and allosteric modulators of the calcium-sensing receptor and their therapeutic applications Mol Pharmacol 76 6 2009 1131 1144
2. E.M. Brown The calcium-sensing receptor: physiology, pathophysiology and CaR-based therapeutics Subcell Biochem 45 2007 129 167
3. P.E. Harringon, and C. Fotsch Calcium sensing receptor activators: calcimimetics Curr Med Chem 14 28 2007 3027 3034 (Pubitemid 350226971)
4. E.F. Nemeth Calcimimetic and calcilytic drugs: just for parathyroid cells? Cell Calcium 35 3 2004 283 289 (Pubitemid 38292372)
5. 2+-sensing receptor interact with overlapping but not identical binding sites in the transmembrane domain J Biol Chem 279 18 2004 18990 18997 (Pubitemid 38623329)
6. S.U. Miedlich, L. Gama, K. Seuwen, R.M. Wolf, and G.E. Breitwieser Homology modeling of the transmembrane domain of the human calcium sensing receptor and localization of an allosteric binding site J Biol Chem 279 8 2004 725 763
7. 2+-sensing receptor J Biol Chem 278 49 2003 49487 49494
8. P. Messa, C. Alfieri, and B. Brezzi Clinical utilization of cinacalcet in hypercalcemic conditions Expert Opin Drug Metab Toxicol 7 4 2011 517 528
9. O.I. Egbuna, and E.M. Brown Hypercalcaemic and hypocalcaemic conditions due to calcium sensing receptor mutations Best Pract Res Clin Rheumatol 22 1 2008 129 148 (Pubitemid 351325733)
10. B.K. Ward, A.L. Magno, J.P. Walsh, and T. Ratajczak The role of the calcium sensing receptor in human disease Clin Biochem 45 12 2012 943 953
11. S.C. Brennan, U. Thiem, S. Roth, A. Aggarwal, I.Sh. Fetahu, and S. Tennakoon et al. Calcium sensing receptor signalling in physiology and cancer Biochim Biophys Acta 1833 7 2013 1732 1744
12. B. Chakravarti, N. Chattophdhyay, and E.M. Brown Signaling through the extracellular calcium-sensing receptor (CaSR) Adv Exp Med Biol 740 2012 103 142
13. S. Pidasheva, L. Canaff, W.F. Simonds, S.J. Marx, and G.N. Hendy Impaired cotranslational processing of the calcium sensing receptor due to signal peptide missense mutations in familial hypocalciuric hypercalcemia Hum Mol Genet 14 12 2005 1679 1690 (Pubitemid 40895520)
14. S.M. Pidasheva, L. Canaff, O. Ercan, U. Kumar, and G.N. Hendy Calcium-sensing receptor dimerizes in the endoplasmic reticulum: biochemical and biophysical characterization of CASR mutants retained intracellularly Hum Mol Genet 15 14 2006 2200 2209 (Pubitemid 43985511)
15. Y. Huang, and G.E. Breitwieser Rescue of calcium-sensing receptor mutants by allosteric modulators reveals a conformational checkpoint in receptor biogenesis J Biol Chem 282 13 2007 9517 9525 (Pubitemid 47104573)
16. E. White, J. McKenna, A. Cavanaugh, and G.E. Breitwieser Pharmacochaperone-mediated rescue of calcium-sensing receptor loss-of-function mutants Mol Endocrinol 23 7 2009 1115 1123
17. M.P. Grant, A. Stepanchick, and G.E. Breitwieser Calcium signaling regulates trafficking of familial hypocalciuric hypercalcemia (FHH) mutants of the calcium sensing receptor Mol Endocrinol 26 12 2012 2081 2091
18. A. Cavanaugh, Y. Huang, and G.E. Breitwieser Behind the curtain: cellular mechanisms for allosteric modulation of calcium-sensing receptor Br J Pharmacol 165 2012 1670 1677
19. K. Leach, A. Wen, A.E. Davey, P.M. Sexton, A.D. Conigrave, and A. Christopoulos Identification of molecular phenotypes and biased signaling induced by naturally occurring mutations of the calcium-sensing receptor Endocrinology 153 9 2012 4304 4316
20. K. Leach, A. Wen, A.E. Cook, P.M. Sexton, A.D. Congrave, and A. Christopoulos Impact of clinically relevant mutations on the pharmacoregulation and signaling bias of the calcium-sensing receptor by positive and negative allosteric modulators Endocrinology 154 3 2013 1105 1116
21. 2+ receptor is essential for its expression at the cell surface Endocrinology 138 4 1997 1916 1922 (Pubitemid 27180807)
22. K. Ray, P. Clapp, P.K. Goldsmith, and A.M. Spiegel Identification of the sites of N-linked glycosylation on the human calcium receptor and assessment of their role in cell surface expression and signal transduction J Biol Chem 273 51 1998 34558 34567 (Pubitemid 29008938)
23. Y. Huang, A. Cavanaugh, and G.E. Breitwieser Regulation of stability and trafficking of calcium-sensing receptors by pharmacologic chaperones R. Richard, Neubig Advances in Pharmacology vol. 62 2011 Academic Press Burlington 43 173
24. X. Zhuang, S. Chowdhury, J.K. Northup, and K. Ray Sar1-dependent trafficking of the human calcium receptor to the cell surface Biochem Biophys Res Commun 396 4 2010 874 880
25. Z.C. Ryan, T.A. Craig, S.Y. Venyaminov, J.R. Thompson, and R. Kumar Biophysical properties of the extracellular domain of the calcium-sensing receptor Biochem Biophys Res Commun 349 1 2006 339 344 (Pubitemid 44331797)
26. Z. Zhang, S. Sun, S.J. Quinn, E.M. Brown, and M. Bai The extracellular calcium sensing receptor dimerizes through multiple types of intermolecular interactions J Biol Chem 276 7 2001 5316 5322
27. A.J. Pace, L. Gama, and G.E. Breitwieser Dimerization of the calcium-sensing receptor occurs within the extracellular domain and is eliminated by Cys to Ser mutations at Cys 101 and Cys236 J Biol Chem 274 17 1999 11629 11634
28. J.T. Tuusa, T.T. Leskela, and U.E. Petaja-Repo Human delta opioid receptor biogenesis is regulated via interactions with SERCA2b and calnexin FEBS J 277 13 2010 2815 2819
29. 2+-pump SERCA2b interacts with G protein-coupled receptors and enhances their expression at the cell surface J Mol Biol 371 3 2007 622 638 (Pubitemid 47087814)
30. M. Narayan Disulfide bonds: protein folding and subcellular protein trafficking FEBS J 279 13 2012 2272 2282
31. 2+-sensing receptor in growth plate chondrocytes Endocrinology 146 12 2005 5294 5303 (Pubitemid 41653042)
32. L. Komuves, Y. Oda, C.L. Tu, W.H. Chang, C.L. Ho-Pao, and T. Mauro et al. Epidermal expression of the full-length extracellular calcium-sensing receptor is required for normal keratinocyte differentiation J Cell Physiol 192 1 2002 45 54 (Pubitemid 34587386)
33. Y. Oda, C.L. Tu, W. Chang, D. Crumrine, L. Komuves, and T. Mauro et al. The calcium sensing receptor and its alternatively spliced form in murine epidermal differentiation J Biol Chem 275 2 2000 1183 1190 (Pubitemid 30051170)
34. B. Finney, W.J. Wilkinson, L. Searchfield, M. Cole, S. Bailey, and P.J. Kemp et al. An exon 5-less variant of the extracellular calcium-sensing receptor rescues absence of the full-length receptor in the developing mouse lung Exp Lung Res 37 4 2011 269 278
35. W. Chang, C. Tu, T.H. Chen, D. Bikle, and D. Shoback The extracellular calcium-sensing receptor (CaSR) is a critical modulator of skeletal development Sci Signal 1 35 2008 ra1
36. C. Ho, D.A. Conner, M.R. Pollak, D.J. Ladd, O. Kifor, and H.B. Warren et al. A mouse model of human familial hypocalciuric hypercalcemia and neonatal severe hyperparathyroidism Nat Genet 11 4 1995 389 394
37. Q. Tu, M. Pi, G. Karsenty, L. Simpson, S. Liu, and L.D. Quarles Rescue of the skeletal phenotype in CaSR-deficient mice by transfer onto the Gcm2 null background J Clin Invest 111 2003 1029 1037 (Pubitemid 36397479)
38. C.H. Kos, A.C. Karaplis, J.B. Peng, M.A. Hediger, D. Goltzman, and K.S. Mohammad et al. The calcium-sensing receptor is required for normal calcium homeostasis independent of parathyroid hormone J Clin Invest 111 2003 1021 1028 (Pubitemid 36397478)
39. G.E. Breitwieser Minireview: the intimate link between calcium sensing receptor trafficking and signaling: implications for disorders of calcium homeostasis Mol Endocrinol 26 9 2012 1482 1495
40. G.E. Breitwieser The calcium sensing receptor life cycle: trafficking, cell surface expression, and degradation Best Pract Res Clin Endocrinol Metab 27 2013 303 313
41. M.P. Grant, A. Stepanchick, A. Cavanaugh, and G.E. Breitwieser Agonist-driven maturation and plasma membrane insertion of calcium-sensing receptors dynamically control signal amplitude Sci Signal 4 200 2011 ra78
42. A. Cavanaugh, J. McKenna, A. Stepanchick, and G.E. Breitwieser Calcium-sensing receptor biosynthesis includes a cotranslational conformation checkpoint and endoplasmic reticulum retention J Biol Chem 285 26 2010 19854 19864
43. A. Stepanchick, J. McKenna, O. McGovern, Y. Huang, and G.E. Breitwieser Calcium sensing receptor mutations implicated in pancreatitis and idiopathic epilepsy syndrome disrupt an arginine-rich retention motif Cell Physiol Biochem 26 3 2010 363 374
44. M.P. Conn, A. Ulloa-Aguirre, and J.A. Janovick Pharmacoperone: what's in a word? Pharmacol Res 83 2014 1 2
45. J.A. Janovick, B.S. Park, and P.M. Conn Therapeutic rescue of misfolded mutants: validation of primary high throughput screens for identification of pharmacoperone drugs PLoS ONE 6 7 2011 e22784
46. Y. Liu, and Y. Ye Proteostasis regulation at the endoplasmic reticulum: a new perturbation site for targeted cancer therapy Cell Res 21 6 2011 867 883
47. N. Vij, S. Fang, and P.L. Zeitlin Selective inhibition of endoplasmic reticulum-associated degradation rescues DeltaF508-cystic fibrosis transmembrane conductance regulator and suppresses interleukin-8 levels: therapeutic implications J Biol Chem 281 25 2006 17369 17378
48. Y. Huang, J. Niwa, G. Sobue, and G.E. Breitwieser Calcium-sensing receptor ubiquitination and degradation mediated by the E3 ubiquitin ligase dorfin J Biol Chem 281 17 2006 11610 11617 (Pubitemid 43855418)
49. A. Stepanchick, and G.E. Breitwieser The cargo receptor p24A facilitates calcium sensing receptor maturation and stabilization in the early secretory pathway Biochem Biophys Res Commun 395 1 2010 136 140
50. T. Bouschet, S. Martin, and J.M. Henley Receptor-activity-modifying proteins are required for forward trafficking of the calcium sensing receptor to the plasma membrane J Cell Sci 118 20 2005 4709 4720 (Pubitemid 41646381)
51. Y. Imanishi, M. Inaba, T. Kawata, and Y. Nishizawa Cinacalcet in hyperfunctioning parathyroid diseases Ther Apher Dial 13 Suppl. 1 2009 S7 S11
52. C.M. Reh, G.N. Hendy, D.E. Cole, and D.D. Jeandron Neonatal hyperparathyroidism with a heterozygous calcium-sensing receptor (CASR) R185Q mutation: clinical benefit from cinacalcet J Clin Endocrinol Metab 96 4 2011 E707 E712
53. A. Wilhelm-Bals, P. Parvex, C. Magdelaine, and E. Girardin Successful use of bisphosphonate and calcimimetic in neonatal severe primary hyperparathyroidism Pediatrics 129 3 2012 e812 e816
54. E. Garcia Soblechero, M.T. Ferrer Castillo, B. Jimenez Crespo, M.L. Dominguez Quintero, and C. Gonzalez Futentes Neonatal hypercalcemia due to a homozygous mutation in the calcium-sensing receptor: failure of cinacalcet Neonatology 104 2 2013 104 108
55. A. Nakamura, T. Hotsubo, K. Kobayashi, H. Mochizuki, K. Ishizu, and T. Tajima Loss-of-function and gain-of-function mutations of calcium-sensing receptor: functional analysis and the effect of allosteric modulators NPS R-568 and NPS 2143 J Clin Endocrinol Metab 98 10 2013 E1692 E1701
56. J.Y.L. Lu, Y. Yang, G. Gnacadja, A. Christopoulos, and J.D. Reagan Effect of the calcimimetic R-568 [3-(2-chlorophenyl)-N-((1R)-1-(3-methoxypheyl)ethyl)- 1-propanamine] on correcting inactivating mutations in the human calcium-sensing receptor J Pharmacol Exp Ther 331 3 2009 775 786
57. R. Rus, C. Haag, C. Bumke-Vogt, V. Bahr, B. Mayr, and M. Mohlig et al. Novel inactivating mutations of the calcium-sensing receptor: the calcimimetic NPS R-568 improves signal transduction of mutant receptors J Clin Endocrinol Metab 93 12 2008 4797 4803
58. S. Tonack, C. Tang, and S. Offermanns Endogenous metabolites as ligands for G protein-coupled receptors modulating risk factors for metabolic and cardiovascular disease Am J Physiol Heart Circ Physiol 304 4 2013 H501 H513
59. V. Kumar, P.G. Fahey, Y.J. Jong, N. Ramanan, and K.L. O'Malley Activation of intracellular metabotropic glutamate receptor 5 in striatal neurons leads to up-regulation of genes associated with sustained synaptic transmission including Arc/Arg3.1 protein J Biol Chem 287 8 2012 5412 5425
60. 2+ release J Biol Chem 283 20 2008 14072 14083
61. 2+ handling in excitable cells in health and disease Pharmacol Rev 63 3 2011 700 727
62. M. Csala, E. Kereszturi, J. Mandl, and G. Banhegyi The endoplasmic reticulum as the extracellular space inside the cell: role in protein folding and glycosylation Antiox Redox Signal 16 10 2012 1100 1108
63. G.K. Broadhead, H.C. Mun, V.A. Avlani, O. Jourdon, W.B. Church, and A. Christopoulos et al. Allosteric modulation of the calcium-sensing receptor by gamma-glutamyl peptides: inhibition of PTH secretion, suppression of intracellular cAMP levels, and a common mechanism of action with amino acids J Biol Chem 286 11 2011 8786 8797
64. M. Wang, Y. Yao, D. Juang, and D.R. Hampson Activation of family C G-protein-coupled receptors by the tripeptide glutathione J Biol Chem 281 13 2006 8864 8870 (Pubitemid 43847993)
65. Y. Maruyama, R. Yasuda, M. Kuroda, and Y. Eto Kokumi substances, enhancers of basic tastes, induce responses in calcium-sensing receptor expressing taste cells PLoS ONE 7 4 2012 e34489
66. 2+ receptor J Biol Chem 277 21 2002 18908 18913 (Pubitemid 34952451)
67. C. Dubois, F. Vanden Abeele, P. Sehgal, C. Olesen, S. Junker, and S.B. Christensen et al. Differential effects of thapsigargin analogs on apoptosis of prostate cancer cells: complex regulation by intracellular calcium FEBS J 280 21 2013 5430 5440
68. R. Bravo, V. Parra, D. Gatica, A.E. Rodriguez, N. Torrealba, and F. Paredes et al. Endoplasmic reticulum and the unfolded protein response: dynamics and metabolic integration Int Rev Cell Mol Biol 301 2013 215 290
69. T.H. Tang, C.T. Chang, H.J. Wang, J.D. Erickson, R.A. Reichard, and A.G. Martin et al. Oxidative stress disruption of receptor-mediated calcium signaling mechanisms J Biomed Sci 20 1 2013 48
70. M. Hagiwara, and K. Nagata Redox-dependent protein quality control in the endoplasmic reticulum: folding to degradation Antioxid Redox Signal 16 10 2012 1119 1128
71. C.L. Grek, J. Zhang, Y. Manevich, D.M. Townsend, and K.D. Tew Causes and consequences of cysteine S-glutathionylation J Biol Chem 288 37 2013 26497 26504
72. Z. Cai, and L.J. Yan Protein oxidative modifications: beneficial roles in disease and health J Biochem Pharmacol Res 1 1 2013 15 26
73. S. Pidasheva, L. D'Souza-Li, L. Canaff, D.E. Cole, and G.N. Hendy CASRdb: calcium-sensing receptor locus-specific database for mutation causing familial (benign) hypocalciuric hypercalcemia, neonatal severe hyperparathyroidism, and autosomal dominant hypocalcemia Hum Mutat 24 2 2004 107 111 (Pubitemid 39006589)
74. 2+-sensing receptor's venus flytrap domain that selectively disables l-amino acid sensing J Biol Chem 280 32 2005 29067 29072 (Pubitemid 41161356)
75. V. Tzovaras, V. Tsimihodimos, C. Kostara, Z. Mitrogianni, and M. Elisaf Aminoglycoside-induced nephrotoxicity studied by proton magnetic resonance spectroscopy of urine Nephrol Dial Transplant 26 10 2011 3219 3224
76. P.P. Parsons, H.O. Garland, E.S. Harpur, and S. Old Acute gentamycin-induced hypercalciuria and hypermagnesiuria in the rat: dose-response relationship and role of renal tubular injury Br J Pharmacol 122 3 1997 570 576 (Pubitemid 27429735)
77. D.T. Ward, D. Maldonado-Perez, L. Hollins, and D. Riccardi Aminoglycosides induce acute cell signaling and chronic cell death in renal cells that express the calcium-sensing receptor J Am Soc Nephrol 16 5 2005 1236 1244 (Pubitemid 41716508)
78. S. McLarnon, D. Holden, D. Ward, M. Jones, A. Elliot, and D. Riccardi Aminoglycoside antibiotics induce pH-sensitive activation of the calcium-sensing receptor Biochem Biophys Res Commun 297 1 2002 71 77
79. 2+-sensing receptors in pulmonary arterial smooth muscle cells Circ Res 112 4 2013 640 650
80. 2+-sensing receptor function in idiopathic pulmonary arterial hypertension Circ Res 111 4 2012 469 481
81. G. Liu, X. Hu, L. Premkumar, and S. Chakrabarty Nifedipine synergizes with calcium in activating calcium sensing receptor, suppressing the expression of thymidylate synthase and survivin and promoting sensitivity to fluorouracil in human colon carcinoma cells Mol Carcinog 50 12 2011 922 930
82. S.A. Khedkar, and P.B. Auti 1,4-Dihydropyridines: a class of pharmacologically important molecules Mini Rev Med Chem 2013 PMID: 23621638 [Epub ahead of print]
83. P. Ioan, E. Carosati, M. Micucci, G. Cruciani, F. Broccatelli, and B.S. Zhorov et al. 1,4-Dihydropyridine scaffold in medicinal chemistry, the story so far and perspectives (part 1): action in ion channels and GPCRs Curr Med Chem 18 32 2012 4901 4922
84. E. Carosati, P. Ioan, M. Micucci, F. Broccatelli, G. Cruciani, and B.S. Zhorov et al. 1,4-Dihydropyridine scaffold in medicinal chemistry, the story so far and perspectives (part 2): action in other targets and antitargets Curr Med Chem 19 25 2012 4306 4323
85. 2+-sensing receptor rescues pulmonary hypertension in rats and mice Hypertens Res 2013 10.1038/hr.2013.129 [Epub ahead of print]
86. A.L. Firth, J. Mandel, and J.X.J. Yuan Idiopathic pulmonary arterial hypertension Dis Mod Mech 3 2010 268 273
87. G. Molostvov, S. Fletcher, R. Bland, and D. Zehnder Extracellular calcium-sensing receptor mediated signalling is involved in human vascular smooth muscle cell proliferation and apoptosis Cell Physiol Biochem 22 5-6 2008 413 422
88. M. Harel-Raviv, M. Eckler, K. Lalani, E. Raviv, and M. Gornitsky Nifedipine-induced gingival hyperplasia. A comprehensive review and analysis Oral Surg Oral Med Oral pathol Orad Radiol Endod 79 6 1995 15 22
89. N. Nakib, and S.S. Ashrafi Drug-induced gingival overgrowth Dis Mon 57 4 2011 224 230
90. T. Hattori, T. Ara, and Y. Fujinami Pharmacological evidences for the stimulation of calcium-sensing receptors by nifedipine in gingival fibroblasts J Pharmacol Pharmacother 2 1 2011 30 35
91. S. Fatherazi, C.M. Belton, S. Cai, S. Zarif, P.C. Goodwin, and R.J. Larmont et al. Calcium receptor message: expression and function decrease in differentiating keratinocytes Pflugers Arch 448 1 2004 93 104 (Pubitemid 38657210)
92. 2+-sensing in salivary ductal cells J Biol Chem 287 36 2012 30305 30316
93. A.E. Davey, K. Leach, C. Valant, A.D. Conigrave, P.M. Sexton, and A. Christopoulos Positive, negative allosteric modulators promote biased signaling at the calcium sensing receptor Endocrinology 153 3 2012 4304 4316
94. K. Leach, P.M. Sexton, A. Christopoulos, and A.D. Conigrave Engendering biased signalling from the calcium-sensing receptor for the pharmacotherapy of diverse disorders Br J Pharmacol 2013 10.1111/bph.12420 [Epub ahead of print]