A naturally occurring isoform inhibits parathyroid hormone receptor trafficking and signaling

Journal of Bone and Mineral Research

Volumn 26, Issue 1, 2011, Pages 143-155

  Alonso, Verõnica ^a   Ardura, Juan A ^a   Wang, Bin ^a   Sneddon, W Bruce ^a,b   Friedman, Peter A ^a  

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

^b DUQUESNE UNIVERSITY   (United States)

Author keywords

ADENYLYL CYCLASE; ALTERNATIVE SPLICING; DOMINANT NEGATIVE; G PROTEIN COUPLED RECEPTORS; ISOFORM; MAP KINASE; MEMBRANE TRAFFICKING; PTH RECEPTOR

Indexed keywords

CYCLIC AMP; HETERODIMER; HETEROGENEOUS NUCLEAR RNA; ISOPROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PARATHYROID HORMONE; PARATHYROID HORMONE RECEPTOR;

ANIMAL CELL; ARTICLE; BASE PAIRING; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CELL MIGRATION; CELL SURFACE; CELLULAR DISTRIBUTION; CHEEK MUCOSA; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENZYME PHOSPHORYLATION; EXON; EXON SKIPPING; GENETIC TRANSFECTION; HORMONE RESISTANCE; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; INTRON; KIDNEY CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RAT; SIGNAL TRANSDUCTION;

CYCLIC AMP; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; EXONS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN TRANSPORT; RECEPTOR, PARATHYROID HORMONE, TYPE 1; SEQUENCE DELETION; SIGNAL TRANSDUCTION;

EID: 78650938286     PISSN: 08840431     EISSN: None     Source Type: Journal    
DOI: 10.1002/jbmr.167     Document Type: Article

References (51)

1. Harmar AJ., Family-B G-protein-coupled receptors. Genome Biol. 2001; 2: 3013.1-3013.10.
2. Mannstadt M, Juppner H, Gardella TJ., Receptors for PTH and PTHrP: their biological importance and functional properties. Am J Physiol. 1999; 277: F665-F675.
3. Schipani E, Karga H, Karaplis AC, et al. Identical complementary deoxyribonucleic acids encode a human renal and bone parathyroid hormone (PTH)/PTH-related peptide receptor. Endocrinology. 1993; 132: 2157-2165.
4. Kong X-F, Schipani E, Lanske B, et al. The rat, mouse and human genes encoding the receptor for parathyroid hormone and parathyroid hormone-related peptide are highly homologous. Biochem Biophys Res Commun. 1994; 200: 1290-1299.
5. Shyu JF, Inoue D, Baron R, Horne WC., The deletion of 14 amino acids in the seventh transmembrane domain of a naturally occurring calcitonin receptor isoform alters ligand binding and selectively abolishes coupling to phospholipase C. J Biol Chem. 1996; 271: 31127-31134.
6. Grammatopoulos DK, Dai Y, Randeva HS, et al. A novel spliced variant of the type 1 corticotropin-releasing hormone receptor with a deletion in the seventh transmembrane domain present in the human pregnant term myometrium and fetal membranes. Mol Endocrinol. 1999; 13: 2189-2202.
7. Grinninger C, Wang W, Oskoui KB, Voice JK, Goetzl EJ., A natural variant type II G protein-coupled receptor for vasoactive intestinal peptide with altered function. J Biol Chem. 2004; 279: 40259-40262.
8. Markovic D, Lehnert H, Levine MA, Grammatopoulos DK., Structural determinants critical for localization and signaling within the seventh transmembrane domain of the type 1 corticotropin releasing hormone receptor: lessons from the receptor variant R1d. Mol Endocrinol. 2008; 22: 2505-2519.
9. Urena P, Kong XF, Abou-Samra AB, et al. Parathyroid hormone (PTH)/PTH-related peptide receptor messenger ribonucleic acids are widely distributed in rat tissues. Endocrinology. 1993; 133: 617-623.
10. Jobert AS, Fernandes I, Turner G, et al. Expression of alternatively spliced isoforms of the parathyroid hormone (PTH)/PTH-related peptide receptor messenger RNA in human kidney and bone cells. Mol Endocrinol. 1996; 10: 1066-1076.
11. Amizuka N, Lee HS, Kwan MY, et al. Cell-specific expression of the parathyroid hormone (PTH)/PTH-related peptide receptor gene in kidney from kidney-specific and ubiquitous promoters. Endocrinology. 1997; 138: 469-481.
12. Ding C, Racusen LC, Wilson P, Burrow C, Levine MA., Identification of an alternatively spliced form of PTH/PTHrP receptor mRNA in immortalized renal tubular cells. J Bone Miner Res. 1995; 10 (Suppl 1): S484.
13. Schipani E, Weinstein LS, Bergwitz C, et al. Pseudohypoparathyroidism type Ib is not caused by mutations in the coding exons of the human parathyroid hormone (PTH)/PTH-related peptide receptor gene. J Clin Endocrinol Metab. 1995; 80: 1611-1621.
14. Fukumoto S, Suzawa M, Takeuchi Y, et al. Absence of mutations in parathyroid hormone (PTH) PTH-related protein receptor complementary deoxyribonucleic acid in patients with pseudohypoparathyroidism type Ib. J Clin Endocrinol Metab. 1996; 81: 2554-2558.
15. Suarez F, Lebrun JJ, Lecossier D, Escoubet B, Coureau C, Silve C., Expression and modulation of the parathyroid hormone (PTH)/PTH-related peptide receptor messenger ribonucleic acid in skin fibroblasts from patients with type Ib pseudohypoparathyroidism. J Clin Endocrinol Metab. 1995; 80: 965-970.
16. Bettoun JD, Minagawa M, Kwan MY, et al. Cloning and characterization of the promoter regions of the human parathyroid hormone (PTH)/PTH-related peptide receptor gene: analysis of deoxyribonucleic acid from normal subjects and patients with pseudohypoparathyroidism type 1b. J Clin Endocrinol Metab. 1997; 82: 1031-1040.
17. Racusen LC, Wilson PD, Hartz PA, Fivush BA, Burrow CR., Renal proximal tubular epithelium from patients with nephropathic cystinosis: immortalized cell lines as in vitro model systems. Kidney Int. 1995; 48: 536-543.
18. Racusen LC, Monteil C, Sgrignoli A, et al. Cell lines with extended in vitro growth potential from human renal proximal tubule: Characterization, response to inducers, and comparison with established cell lines. J Lab Clin Med. 1997; 129: 318-329.
19. Wang B, Bisello A, Yang Y, Romero GG, Friedman PA., NHERF1 regulates parathyroid hormone receptor membrane retention without affecting recycling. J Biol Chem. 2007; 282: 36214-36222.
20. Wang B, Yang Y, Friedman PA., Na/H Exchange regulator factor 1, a novel Akt-associating protein, regulates extracellular signal-related signaling through a B-Raf-mediated pathway. Mol Biol Cell. 2008; 19: 1637-1645.
21. Wang B, Yang Y., Generation of human PTH1R construct with Flag epitope located internally: comparison of two-fragment assembly by using PCR overlap extension or ligase. J Biomol Tech. 2009; 20: 195-200.
22. Ferrandon S, Feinstein TN, Castro M, et al. Sustained cyclic AMP production by parathyroid hormone receptor endocytosis. Nat Chem Biol. 2009; 5: 734-742.
23. Sneddon WB, Syme CA, Bisello A, et al. Activation-independent parathyroid hormone receptor internalization is regulated by NHERF1 (EBP50). J Biol Chem. 2003; 278: 43787-43796.
24. Bisello A, Greenberg Z, Behar V, Rosenblatt M, Suva LJ, Chorev M., Role of glycosylation in expression and function of the human parathyroid hormone parathyroid hormone-related protein receptor. Biochemistry. 1996; 35: 15890-15895.
25. Nikolaev VO, Bunemann M, Hein L, Hannawacker A, Lohse MJ., Novel single chain cAMP sensors for receptor-induced signal propagation. J Biol Chem. 2004; 37215-37218.
26. Vilardaga JP, Nikolaev VO, Lorenz K, Ferrandon S, Zhuang Z, Lohse MJ., Conformational cross-talk between α2A-adrenergic and mu-opioid receptors controls cell signaling. Nat Chem Biol. 2008; 4: 126-131.
27. Abramoff MD, Magelhaes PJ, Ram SJ., Image Processing with ImageJ. Biophotonics Int. 2004; 11: 36-42.
28. Krogh A, Larsson B, von Heijne G, Sonnhammer EL., Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol. 2001; 305: 567-580.
29. Bermak JC, Li M, Bullock C, Zhou QY., Regulation of transport of the dopamine D1 receptor by a new membrane-associated ER protein. Nat Cell Biol. 2001; 3: 492-498.
30. Schulein R, Hermosilla R, Oksche A, et al. A dileucine sequence and an upstream glutamate residue in the intracellular carboxyl terminus of the vasopressin V2 receptor are essential for cell surface transport in COS.M6 cells. Molecular Pharmacol. 1998; 54: 525-535.
31. Thielen A, Oueslati M, Hermosilla R, et al. The hydrophobic amino acid residues in the membrane-proximal C tail of the G protein-coupled vasopressin V2 receptor are necessary for transport-competent receptor folding. FEBS Lett. 2005; 579: 5227-5235.
32. Marchese A, Paing MM, Temple BR, Trejo J., G protein-coupled receptor sorting to endosomes and lysosomes. Annu Rev Pharmacol Toxicol. 2008; 48: 601-629.
33. Ulloa-Aguirre A, Conn PM., Targeting of G protein-coupled receptors to the plasma membrane in health and disease. Front Biosci. 2009; 14: 973-994.
34. B receptor heterodimerization. Neuron. 2000; 27: 97-106.
35. Poyner DR, Sexton PM, Marshall I, et al. International Union of Pharmacology. XXXII. The mammalian calcitonin gene-related peptides, adrenomedullin, amylin, and calcitonin receptors. Pharmacol Rev. 2002; 54: 233-246.
36. Rey A, Manen D, Rizzoli R, Caverzasio J, Ferrari SL., Proline-rich motifs in the PTH/PTHrP-receptor C-terminus mediate scaffolding of c-Src with Ã-arrestin2 for ERK1/2 activation. J Biol Chem. 2006; 38181-38188.
37. Pioszak AA, Harikumar KG, Parker NR, Miller LJ, Xu HE., Dimeric arrangement of the parathyroid hormone receptor and a structural mechanism for ligand-induced dissociation. J Biol Chem. 2010; [Epub ahead of print].
38. Seck T, Baron R, Horne WC., The alternatively spliced Îe13 transcript of the rabbit calcitonin receptor dimerizes with the C1a isoform and inhibits its surface expression. J Biol Chem. 2003; 278: 23085-23093.
39. Mahon MJ, Bonacci TM, Divieti P, Smrcka AV., A docking site for G protein βÎ subunits on the parathyroid hormone 1 receptor supports signaling through multiple pathways. Mol Endocrinol. 2006; 20: 136-146.
40. Huang Z, Chen Y, Nissenson RA., The cytoplasmic tail of the G-protein-coupled receptor for parathyroid hormone and parathyroid hormone-related protein contains positive and negative signals for endocytosis. J Biol Chem. 1995; 270: 151-156.
41. Weinman EJ, Hall RA, Friedman PA, Liu-Chen LY, Shenolikar S., The association of NHERF adaptor proteins with G protein-coupled receptors and receptor tyrosine kinases. Annu Rev Physiol. 2006; 68: 491-505.
42. + exchanger regulatory factor-1 (NHERF1) in rat osteosarcoma ROS 17/28 cells. Mol Endocrinol. 2008; 22: 1163-1170.
43. Wang B, Yang Y, Abou-Samra AB, Friedman PA., NHERF1 regulates parathyroid hormone receptor desensitization; interference with Ã-arrestin binding. Mol Pharmacol. 2009; 75: 1189-1197.
44. Bouley R, Lin HY, Raychowdhury MK, Marshansky V, Brown D, Ausiello DA., Downregulation of the vasopressin type 2 receptor after vasopressin-induced internalization: involvement of a lysosomal degradation pathway. Am J Physiol Cell Physiol. 2005; 288: C1390-C1401.
45. Meusser B, Hirsch C, Jarosch E, Sommer T., ERAD: the long road to destruction. Nat Cell Biol. 2005; 7: 766-772.
46. Schwieger I, Lautz K, Krause E, Rosenthal W, Wiesner B, Hermosilla R., Derlin-1 and p97/valosin-containing protein mediate the endoplasmic reticulum-associated degradation of human V2 vasopressin receptors. Mol Pharmacol. 2008; 73: 697-708.
47. van Ommen GJ, van Deutekom J, Aartsma-Rus A., The therapeutic potential of antisense-mediated exon skipping. Curr Opin Mol Ther. 2008; 10: 140-149.
48. Miriami E, Margalit H, Sperling R., Conserved sequence elements associated with exon skipping. Nucleic Acids Res. 2003; 31: 1974-1983.
49. Juppner H, Bastepe M., Different mutations within or upstream of the GNAS locus cause distinct forms of pseudohypoparathyroidism. J Pediatr Endocrinol Metab. 2006; 19 (Suppl 2): 641-646.
50. Bastepe M, Juppner H., GNAS locus and pseudohypoparathyroidism. Horm Res. 2005; 63: 65-74.
51. Mantovani G, de Sanctis L, Barbieri AM, et al. Pseudohypoparathyroidism and GNAS epigenetic defects: clinical evaluation of Albright hereditary osteodystrophy and molecular analysis in 40 patients. J Clin Endocrinol Metab. 2010; 95: 651-658.