A docking site for G protein βγ subunits on the parathyroid hormone 1 receptor supports signaling through multiple pathways

Molecular Endocrinology

Volumn 20, Issue 1, 2006, Pages 136-146

  Mahon, Matthew J ^a   Bonacci, Tabetha M ^b   Divieti, Paola ^a   Smrcka, Alan V ^b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; AMINO ACID; CALCIUM ION; CYCLIC AMP; GLUTATHIONE TRANSFERASE; GUANINE NUCLEOTIDE BINDING PROTEIN BETA 1 SUBUNIT; GUANINE NUCLEOTIDE BINDING PROTEIN BETA SUBUNIT; GUANINE NUCLEOTIDE BINDING PROTEIN GAMMA 2 SUBUNIT; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PARATHYROID HORMONE RECEPTOR 1; PHOSPHOLIPASE C BETA1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOPLASM; EMBRYO; GENE MUTATION; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION;

ADENYLATE CYCLASE; AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CALCIUM; CELL LINE; CYCLIC AMP; DIMERIZATION; GTP-BINDING PROTEIN BETA SUBUNITS; GTP-BINDING PROTEIN GAMMA SUBUNITS; GUANOSINE 5'-O-(3-THIOTRIPHOSPHATE); HUMANS; ISOENZYMES; MAP KINASE SIGNALING SYSTEM; MICE; MOLECULAR SEQUENCE DATA; MUTATION; PHOSPHOLIPASE C; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; RECEPTOR, PARATHYROID HORMONE, TYPE 1; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 29444434762     PISSN: 08888809     EISSN: 08888809     Source Type: Journal    
DOI: 10.1210/me.2005-0169     Document Type: Article

References (56)

1. Kronenberg HM, Karaplis AC, Lanske B 1996 Role of parathyroid hormone-related protein in skeletal development. Ann NY Acad Sci 785:119-123
2. Qian J, Colbert MC, Witte D, Kuan CY, Gruenstein E, Osinska H, Lanske B, Kronenberg HM, Clemens TL 2003 Midgestational lethality in mice lacking the parathyroid hormone (PTH)/PTH-related peptide receptor is associated with abrupt cardiomyocyte death. Endocrinology 144:1053-1061
3. Abou-Samra AB, Jüppner H, Force T, Freeman MW, Kong XF, Schipani E, Urena P, Richards J, Bonventre JV, Potts Jr JT, Kronenberg HM, Segre GV 1992 Expression cloning of a common receptor for parathyroid hormone and parathyroid hormone-related peptide from rat osteoblast-like cells: a single receptor stimulates intracellular accumulation of both cAMP and inositol triphosphates and increases intracellular free calcium. Proc Natl Acad Sci USA 89:2732-2736
4. Bringhurst FR, Juppner H, Guo J, Urena P, Potts Jr JT, Kronenberg HM, Abou-Samra AB, Segre GV 1993 Cloned, stably expressed parathyroid hormone (PTH)/PTH-related peptide receptors activate multiple messenger signals and biological responses in LLC-PK1 kidney cells. Endocrinology 132:2090-2098
5. Offermanns S, Iida-Klein A, Segre GV, Simon MI 1996 Gαq family members couple parathyroid hormone (PTH)/PTH-related peptide and calcitonin receptors to phospholipase C in COS-7 cells. Mol Endocrinol 10:566-574
6. Reshkin SJ, Forgo J, Murer H 1991 Apical and basolateral effects of PTH in OK cells: transport inhibition, messenger production, effects of pertussis toxin, and interaction with a PTH analog. J Membr Biol 124:227-237
7. Mahon MJ, Donowitz M, Yun CC, Segre GV 2002 Na(+)/H(+)exchanger regulatory factor 2 directs parathyroid hormone 1 receptor signalling. Nature 417:858-861
8. Mahon MJ, Segre GV 2004 Stimulation by parathyroid hormone of a NHERF-1-assembled complex consisting of the parathyroid hormone I receptor, phospholipase Cbeta, and actin increases intracellular calcium in opossum kidney cells. J Biol Chem 279:23550-23558
9. Pines M, Santora A, Spiegel A 1986 Effects of phorbol esters and pertussis toxin on agonist-stimulated cyclic AMP production in rat osteosarcoma cells. Biochem Pharmacol 35:3639-3641
10. Rizzoli R, Bonjour JP 1988 Effect of pertussis toxin on parathyroid hormone-stimulated cyclic AMP production in cultured kidney cells. J Bone Miner Res 3:605-609
11. Abou-Samra AB, Jueppner H, Potts Jr JT, Segre GV 1989 Inactivation of pertussis toxin-sensitive guanyl nucleotide-binding proteins increase parathyroid hormone receptors and reverse agonist-induced receptor down-regulation in ROS 17/2.8 cells. Endocrinology 125:2594-2599
12. McKee RL, Caulfield MP, Rosenblatt M 1990 Treatment of bone-derived ROS 17/2.8 cells with dexamethasone and pertussis toxin enables detection of partial agonist activity for parathyroid hormone antagonists. Endocrinology 127:76-82
13. Fujimori A, Cheng SL, Avioli LV, Civitelli R 1991 Dissociation of second messenger activation by parathyroid hormone fragments in osteosarcoma cells. Endocrinology 128:3032-3039
14. Friedman PA, Coutermarsh BA, Kennedy SM, Gesek FA 1996 Parathyroid hormone stimulation of calcium transport is mediated by dual signaling mechanisms involving protein kinase A and protein kinase C. Endocrinology 137:13-20
15. Barry EL, Gesek FA, Yu AS, Lytton J, Friedman PA 1998 Distinct calcium channel isoforms mediate parathyroid hormone and chlorothiazide-stimulated calcium entry in transporting epithelial cells. J Membr Biol 161:55-64
16. Friedman PA, Gesek FA, Morley P, Whitfield JF, Willick GE 1999 Cell-specific signaling and structure-activity relations of parathyroid hormone analogs in mouse kidney cells. Endocrinology 140:301-309
17. Singh AT, Kunnel JG, Strieleman PJ, Stern PH 1999 Parathyroid hormone (PTH)-(1-34), [Nle(8,18), Tyr34]PTH-(3-34) amide, PTH-(1-31) amide, and PTH-related peptide-(1-34) stimulate phosphatidylcholine hydrolysis in UMR-106 osteoblastic cells: comparison with effects of phorbol 12,13-dibutyrate. Endocrinology 140:131-137
18. Suarez F, Silve C 1992 Effect of parathyroid hormone on arachidonic acid metabolism in mouse osteoblasts: permissive action of dexamethasone. Endocrinology 130:592-598
19. Cole JA 1999 Parathyroid hormone activates mitogenactivated protein kinase in opossum kidney cells. Endocrinology 140:5771-5779
20. Kalinowski L, Dobrucki LW, Malinski T 2001 Nitric oxide as a second messenger in parathyroid hormone-related protein signaling. J Endocrinol 170:433-440
21. Sutliff RL, Weber CS, Qian J, Miller ML, Clemens TL, Paul RJ 1999 Vasorelaxant properties of parathyroid hormone-related protein in the mouse: evidence for endothelium involvement independent of nitric oxide formation. Endocrinology 140:2077-2083
22. Cheung R, Erclik MS, Mitchell J 2005 Increased expression of G(11)α in osteoblastic cells enhances parathyroid hormone activation of phospholipase C and AP-1 regulation of matrix metalloproteinase-13 mRNA. J Cell Physiol 204:336-343
23. Singh AT, Gilchrist A, Voyno-Yasenetskaya T, Radeff-Huang JM, Stern PH, Kunnel JG, Strieleman PJ 2005 Gα12/Gα13 subunits of heterotrimeric G proteins mediate parathyroid hormone activation of phospholipase D in UMR-106 osteoblastic cells. Endocrinology 140:131-137
24. Hermans E 2003 Biochemical and pharmacological control of the multiplicity of coupling at G-protein-coupled receptors. Pharmacol Ther 99:25-44
25. Iida-Klein A, Guo J, Takemura M, Drake MT, Potts Jr JT, Abou-Samra A, Bringhurst FR, Segre GV 1997 Mutations in the second cytoplasmic loop of the rat parathyroid hormone (PTH)/PTH-related protein receptor result in selective loss of PTH-stimulated phospholipase C activity. J Biol Chem 272:6882-6889
26. Huang Z, Chen Y, Pratt S, Chen TH, Bambino T, Nissenson RA, Shoback DM 1996 The N-terminal region of the third intracellular loop of the parathyroid hormone (PTH)/PTH-related peptide receptor is critical for coupling to cAMP and inositol phosphate/Ca2+ signal transduction pathways. J Biol Chem 271:33382-33389
27. O'Dowd BF, Hnatowich M, Regan JW, Leader WM, Caron MG, Lefkowitz RJ 1988 Site-directed mutagenesis of the cytoplasmic domains of the human β2-adrenergic receptor. Localization of regions involved in G protein-receptor coupling. J Biol Chem 263:15985-15992
28. Huang Z, Chen Y, Pratt S, Chen TH, Bambino T, Shoback DM, Nissenson RA 1995 Mutational analysis of the cytoplasmic tail of the G protein-coupled receptor for parathyroid hormone (PTH) and PTH-related protein: effects on receptor expression and signaling. Mol Endocrinol 9:1240-1249
29. Iida-Klein A, Guo J, Xie LY, Juppner H, Potts Jr JT, Kronenberg HM, Bringhurst FR, Abou-Samra AB, Segre GV 1995 Truncation of the carboxyl-terminal region of the rat parathyroid hormone (PTH)/PTH-related peptide receptor enhances PTH stimulation of adenylyl cyclase but not phospholipase C. J Biol Chem 270:8458-8465
30. Mahon MJ, Shimada M 2005 Calmodulin interacts with the cytoplasmic tails of the parathyroid hormone 1 receptor and a sub-set of class b G-protein coupled receptors. FEBS Lett 579:803-807
31. O'Connor V, El Far O, Bofill-Cardona E, Nanoff C, Freissmuth M, Karschin A, Airas JM, Betz H, Boehm S 1999 Calmodulin dependence of presynaptic metabotropic glutamate receptor signaling. Science 286:1180-1184
32. El Far O, Bofill-Cardona E, Airas JM, O'Connor V, Boehm S, Freissmuth M, Nanoff C, Betz H 2001 Mapping of calmodulin and Gβγ binding domains within the C-terminal region of the metabotropic glutamate receptor 7A. J Biol Chem 276:30662-30669
33. Duchatelet S, Ostergaard E, Cortes D, Lemainque A, Julier C 2005 Recessive mutations in PTHR1 cause contrasting skeletal dysplasias in Eiken and Blomstrand syndromes. Hum Mol Genet 14:1-5
34. Divieti P, Lanske B, Kronenberg HM, Bringhurst FR 1998 Conditionally immortalized murine osteoblasts lacking the type 1 PTH/PTHrP receptor. J Bone Miner Res 13: 1835-1845
35. Gales C, Rebois RV, Hogue M, Trieu P, Breit A, Hebert TE, Bouvier M 2005 Real-time monitoring of receptor and G-protein interactions in living cells. Nat Methods 2:177-184
36. Kisselev O, Gautam N 1993 Specific interaction with rhodopsin is dependent on the γ subunit type in a G protein. J Biol Chem 268:24519-24522
37. Hoare S, Copland JA, Strakova Z, Ives K, Jeng YJ, Hellmich MR, Soloff MS 1999 The proximal portion of the COOH terminus of the oxytocin receptor is required for coupling to g(q), but not g(i). Independent mechanisms for elevating intracellular calcium concentrations from intracellular stores. J Biol Chem 274:28682-28689
38. Doi T, Sugimoto H, Arimoto I, Hiroaki Y, Fujiyoshi Y 1999 Interactions of endothelin receptor subtypes A and B with Gi, Go, and Gq in reconstituted phospholipid vesicles. Biochemistry 38:3090-3099
39. Gether U 2000 Uncovering molecular mechanisms involved in activation of G protein-coupled receptors. Endocr Rev 21:90-113
40. Marin EP, Krishna AG, Zvyaga TA, Isele J, Siebert F, Sakmar TP 2000 The amino terminus of the fourth cytoplasmic loop of rhodopsin modulates rhodopsin-transducin interaction. J Biol Chem 275:1930-1936
41. Taylor JM, Jacob-Mosier GG, Lawton RG, Remmers AE, Neubig RR 1994 Binding of an α2 adrenergic receptor third intracellular loop peptide to Gβ and the amino terminus of Gα. J Biol Chem 269:27618-27624
42. Taylor JM, Jacob-Mosier GG, Lawton RG, VanDort M, Neubig RR 1996 Receptor and membrane interaction sites on Gβ. A receptor-derived peptide binds to the carboxyl terminus. J Biol Chem 271:3336-3339
43. Wu G, Benovic JL, Hildebrandt JD, Lanier SM 1998 Receptor docking sites for G-protein βγ subunits. Implications for signal regulation. J Biol Chem 273:7197-7200
44. Wu G, Bogatkevich GS, Mukhin YV, Benovic JL, Hildebrandt JD, Lanier SM 2000 Identification of Gβγ binding sites in the third intracellular loop of the M(3)-muscarinic receptor and their role in receptor regulation. J Biol Chem 275:9026-9034
45. Robishaw JD, Berlot CH 2004 Translating G protein subunit diversity into functional specificity. Curr Opin Cell Biol 16:206-209
46. Kleuss C, Scherubl H, Hescheler J, Schultz G, Wittig B 1993 Selectivity in signal transduction determined by γ subunits of heterotrimeric G proteins. Science 259:832-834
47. Wang Q, Jolly JP, Surmeier JD, Mullah BM, Lidow MS, Bergson CM, Robishaw JD 2001 Differential dependence of the D1 and D5 dopamine receptors on the G protein γ 7 subunit for activation of adenylylcyclase. J Biol Chem 276:39386-39393
48. Wang Q, Mullah B, Hansen C, Asundi J, Robishaw JD 1997 Ribozyme-mediated suppression of the G protein γ7 subunit suggests a role in hormone regulation of adenylylcyclase activity. J Biol Chem 272:26040-26048
49. Richardson M, Robishaw JD, Daaka Y, Pitcher JA, Stoffel RH, Lefkowitz RJ 1999 The α2A-adrenergic receptor discriminates between Gi heterotrimers of different βγ subunit composition in Sf9 insect cell membranes. J Biol Chem 274:13525-13533
50. Lim WK, Myung CS, Garrison JC, Neubig RR 2001 Receptor-G protein γ specificity: γ11 shows unique potency for A(1) adenosine and 5-HT(1A) receptors. Biochemistry 40:10532-10541
51. Ford CE, Skiba NP, Bae H, Daaka Y, Reuveny E, Shekter LR, Rosal R, Weng G, Yang CS, Iyengar R, Miller RJ, Jan LY, Lefkowitz RJ, Hamm HE 1998 Molecular basis for interactions of G protein βγ subunits with effectors. Science 280:1271-1274
52. Li Y, Sternweis PM, Charnecki S, Smith TF, Gilman AG, Neer EJ, Kozasa T 1998 Sites for Gα binding on the G protein β subunit overlap with sites for regulation of phospholipase Cβ and adenylyl cyclase. J Biol Chem 273:16265-16272
53. Pitcher JA, Inglese J, Higgins JB, Arriza JL, Casey PJ, Kim C, Benovic JL, Kwatra MM, Caron MG, Lefkowitz RJ 1992 Role of βγ subunits of G proteins in targeting the β-adrenergic receptor kinase to membrane-bound receptors. Science 257:1264-1267
54. Touhara K, Inglese J, Pitcher JA, Shaw G, Lefkowitz RJ 1994 Binding of G protein βγ-subunits to pleckstrin homology domains. J Biol Chem 269:10217-10220
55. Kozasa T, Gilman AG 1995 Purification of recombinant G proteins from Sf9 cells by hexahistidine tagging of associated subunits. Characterization of α12 and inhibition of adenylyl cyclase by αz. J Biol Chem 270:1734-1741
56. Lavoie C, Mercier JF, Salahpour A, Umapathy D, Breit A, Villeneuve LR, Zhu WZ, Xiao RP, Lakatta EG, Bouvier M,Hebert TE 2002 β1/β2-adrenergic receptor heterodimerization regulates β2-adrenergic receptor internalization and ERK signaling efficacy. J Biol Chem 277:35402-35410