The G protein a subunit variant XLαs promotes inositol 1,4,5-trisphosphate signaling and mediates the renal actions of parathyroid hormone in vivo

Science Signaling

Volumn 8, Issue 391, 2015, Pages ra84-

  He, Qing ^a   Zhu, Yan ^a   Corbin, Braden A ^a   Plagge, Antonius ^b   Bastepe, Murat ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

1,25 DIHYDROXYERGOCALCIFEROL; CYCLIC AMP; G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; INOSITOL 1,4,5 TRISPHOSPHATE; PARATHYROID HORMONE; PHOSPHATE; SODIUM PHOSPHATE COTRANSPORTER; THROMBIN; VITAMIN D; CHROMOGRANIN; GNAS PROTEIN, MOUSE; SLC34A1 PROTEIN, MOUSE; SODIUM PHOSPHATE COTRANSPORTER 2A; STIMULATORY GUANINE NUCLEOTIDE BINDING PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD LEVEL; CONTROLLED STUDY; HEK293 CELL LINE; HUMAN; HUMAN CELL; HYPERPHOSPHATEMIA; HYPOCALCEMIA; KIDNEY; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE EPITHELIUM; MOUSE; NONHUMAN; PARATHYROID HORMONE BLOOD LEVEL; PERINATAL PERIOD; PHENOTYPE; PHOSPHATE BLOOD LEVEL; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; SECOND MESSENGER; SIGNAL TRANSDUCTION; URINALYSIS; VITAMIN BLOOD LEVEL; ANIMAL; CYTOLOGY; DRUG EFFECTS; GENETICS; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY;

MUS;

ANIMALS; CHROMOGRANINS; CYCLIC AMP; GTP-BINDING PROTEIN ALPHA SUBUNITS, GQ-G11; GTP-BINDING PROTEIN ALPHA SUBUNITS, GS; HEK293 CELLS; HUMANS; INOSITOL 1,4,5-TRISPHOSPHATE; KIDNEY TUBULES, PROXIMAL; MICE; MICE, KNOCKOUT; PARATHYROID HORMONE; SECOND MESSENGER SYSTEMS; SODIUM-PHOSPHATE COTRANSPORTER PROTEINS, TYPE IIA;

EID: 84940373916     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.aaa9953     Document Type: Article

References (59)

1. S. Turan, M. Bastepe, The GNAS complex locus and human diseases associated with loss-of-function mutations or epimutations within this imprinted gene. Horm. Res. Paediatr. 80, 229-241 (2013).
2. A. Plagge, G. Kelsey, E. L. Germain-Lee, Physiological functions of the imprinted Gnas locus and its protein variants Gas and XLas in human and mouse. J. Endocrinol. 196, 193-214 (2008).
3. L. S. Weinstein, S. Yu, D. R. Warner, J. Liu, Endocrine manifestations of stimulatory G protein a-subunit mutations and the role of genomic imprinting. Endocr. Rev. 22, 675-705 (2001).
4. R. H. Ke hlenbach, J. Matthey, W. B. Huttner, XLas is a new type of G protein. Nature 372, 804-809 (1994).
5. S. Yu, D. Yu, E. Lee, M. Eckhaus, R. Lee, Z. Corria, D. Accili, H.West phal, L. S.Weinstein, Variable and tissue-specific hormone resistance in heterotrimeric Gs protein a-subunit (Gsa) knockout mice is due to tissue-specific imprinting of the Gsa gene. Proc. Natl. Acad. Sci. U.S.A. 95, 8715-8720 (19 98).
6. B. E. Hayward, M. Kamiya, L. Strain, V. Moran, R. Campbell, Y. Hayashizaki, D. T. Bonthron, The human GNAS1 gene is imprinted and encodes distinct paternally and biallelically expressed G proteins. Proc. Natl. Acad. Sci. U.S.A. 95, 10038-10043 (1998).
7. J. Peters, S. F.Wroe, C. A. Wells, H. J. Miller, D. Bodle, C. V. Beechey, C. M.Williamson, G. Kelsey, A cluster of oppositely imprinted transcripts at the Gnas locus in the distal imprinting region of mouse chromosome 2. Proc. Natl. Acad. Sci. U.S.A. 96, 3830-3835 (1999).
8. N. Richard, A. Molin, N. Coudray, P. Rault-Guillaume, H. Jüppner, M. L. Kottler, Paternal GNAS mutations lead to severe intrauterine growth retardation (IUGR) and provide evidence for a role of XLas in fetal development. J. Clin. Endocrinol. Metab. 98, E1549-E1556 (2013).
9. A. Plagge, E. Gordon, W. Dean, R. Boiani, S. Cinti, J. Peters, G. Kelsey, The imprinted signaling protein XLas is required for postnatal adaptation to feeding. Nat. Genet. 36, 818-826 (2004).
10. D. Geneviève, D. Sanlaville, L. Faivre, M. L. Kottler,M. Jambou, P. Gosset, D. Boustani-Samara, G. Pinto, C. Ozilou, G. Abeguilé, A. Munnich, S. Romana, O. Raoul, V. Cormier-Daire, M. Vekemans, Paternal deletion of the GNAS imprinted locus (including Gnasxl) in two girls presenting with severe pre-and post-natal growth retardation and intractable feeding difficulties. Eur. J. Hum. Genet. 13, 1033-1039 (2005).
11. M. A. Aldred, S. Aftimos, C. Hall, K. S. Waters, R. V. Thakker, R. C. Trembath, L. Brueton, Constitutional deletion of chromosome 20q in two patients affected with albright hereditary osteodystrophy. Am. J. Med. Genet. 113, 167-172 (2002).
12. B. Izzi, I. Francois, V. Labarque, C. Thys, C. Wittevrongel, K. Devriendt, E. Legius, A. Van Den Bruel, M. D'Hooghe, D. Lambrechts, F. De Zegher, C. Van Geet, K. Freson, Methylation defect in imprinted genes detected in patients with an Albright's hereditary osteodystrophy like phenotype and platelet Gs hypofunction. PLOS One 7, e38579 (2012).
13. I. Garcia-Murillas, R. Sharpe, A. Pearson, J. Campbell, R. Natrajan, A. Ashworth, N. C. Turner, An siRNA screen identifies the GNAS locus as a driver in 20q amplified breast cancer. Oncogene 33, 2478-2486 (2014).
14. E. Ferná ndez-Rebollo, A. Maeda, M. Reyes, S. Turan, L. F. Fröhlich, A. Plagge, G. Kelsey, H. Jüppner, M. Bastepe, Loss of XLas (extra-large as) imprinting results in early postnatal hypoglycemia and lethality in a mouse model of pseudohypoparathyroidism Ib. Proc. Natl. Acad. Sci. U.S.A. 109, 6638-6643 (2012).
15. M. Klemke, H. A. Pasolli, R. H. Kehlenbach, S. Offermanns, G. Schultz, W. B. Huttner, Characterization of the extra-large G protein a-subunit XLas: II. Signal transduction properties. J. Biol. Chem. 275, 33633-33640 (2000).
16. M. Bastepe, Y. Gunes, B. Perez-Villamil, J. Hunzelman, L. S. Weinstein, H. Jüppner, Receptor-mediated adenylyl cyclase activation through XLas, the extra-large variant of the s timulatory G protein a-subunit. Mol. Endocrinol. 16, 1912-1919 (2002).
17. T. Xie, A. Plagge, O. Gavrilova, S. Pack, W. Jou, E. W. Lai, M. Frontera, G. Kelsey, L. S. Weinstein, The alternative stimulatory G protein a-subunit XLas is a critical regulator of energy and glucose metabolism and sympathetic nerve activity in adult mice. J. Biol. Chem. 281, 18989-18999 (2006).
18. H. A. Pasolli, M. Klemke, R. H. Kehlenbach, Y. Wang, W. B. Huttner, Characterization of the extra-large G protein a-subunit XLas: I. Tissue distribution and subcellular localization. J. Biol. Chem. 275, 33622-33632 (2000).
19. M. Klemke, R. H. Kehlenbach, W. B. Huttner, Two overlapping reading frames in a single exon encode interacting proteins-A novel way of gene usage. EMBO J. 20, 3849-3860 (2001).
20. C. Aydin, N. Aytan, M. J. Mahon, H. A. Tawfeek, N.W. Kowall, A. Dedeoglu, M. Bastepe, Extralarge XLas (XXLas), a variant of stimulatory G protein a-subunit (Gsa), is a distinct, membrane-anchored GNAS product that can mimic Gsa. Endocrinology 150, 3567-3575 (2009).
21. J. Abramowitz, D. Grenet, M. Birnbaumer, H. N. Torres, L. Birnbaumer, XLas, the extralong form of the a-subunit of the Gs G protein, is significan tly longer than suspected, and so is its companion Alex. Proc. Natl. Acad. Sci. U.S.A. 101, 8366-8371 (2004).
22. H. Kronenberg, R. H. Williams, Williams Textbook of Endocrinology (Saunders/Elsevier, Philadelphia, 2008), p. xix, 1911 pp.
23. F. R. Bringhurst, H. Juppner, J. Guo, P. Urena, J. T. Potts Jr., H. M. Kronenberg, A.B. Abou-Samra, G. V. Segre, Cloned, stably expressed parathyroid hormone (PTH)/PTHrelated peptide receptors activate multiple messenger signals and biological responses in LLC-PK1 kidney cells. Endocrinology 132, 2090-2098 (1993).
24. Z. Liu, S. Turan, V. L. Wehbi, J. P. Vilardaga, M. Bastepe, Extra-long Gas variant XLas protein escapes activation-induced subcellular redistribution and is able to provide sustained signaling. J. Biol. Chem. 286, 38558-38569 (2011).
25. Z. Liu,H.S egawa, C.Aydin,M.Reyes, R. G. Erben, L. S.Weinstein, M. Chen,V.Marshansky, L. F. Fröhlich, M. Bastepe, Transgenic overexpression of the extra-large Gsa variant XLas enhances Gsa-mediated responses in the mouse renal proximal tu bule in vivo. Endocrinology 152, 1222-1233 (2011).
26. T. Shimada, H. Hasegawa, Y. Yamazaki, T.Muto, R. Hino, Y. Takeuchi, T. Fujita, K. Nakahara, S. Fukumoto, T. Yamash ita, FGF-23 is a potent regulator of vitamin D metabolism and phosphate homeostasis. J. Bone Miner. Res. 19, 429-435 (2004).
27. H. L. Brenza, C. Kimmel-Jehan, F. Jehan, T. Shinki, S. Wakino, H. Anazawa, T. Suda, H. F. DeLuca, Parathyroid hormone activation of the 25-hydroxyvitamin D3-1a-hydroxylase gene promoter. Proc. Natl. Acad. Sci. U.S.A. 95, 1387-1391 (1998).
28. H. Murer, M. Lötscher, B. Kaissling, M. Levi, S. A. Kempson, J. Biber, Renal brush border membrane Na/Pi-cotransport: Molecular aspects in PTH-dependent and dietary regulation. Kidney Int. 49, 1769-1773 (1996).
29. L. R. Chase, G. L. Melson, G. D. Aurbach, Pseudohypoparathyroidism: Defective excretion of 3?,5?-AMP in response to parathyroid hormone. J. Clin. Invest. 48, 1832-1844 (1969).
30. R. DunlayK. Hruska PTH receptor coupling to phospholipase C is an alternate pathway of signal transduction in bone and kidney. Am. J. Physiol. 258 F223-F231 1990).
31. J. Guo, L. Song, M. Liu, H. Segawa, K. Miyamoto, F. R. Bringhurst, H. M. Kronenberg, H. Jüppner, Activation of a non-cAMP/PKA signaling pathway downstream of the PTH/PTHrP receptor is essential for a sustained hypophosphatemic response to PTH infusion in male mice. En docrinology 154, 1680-1689 (2013).
32. J. Gattineni, C. Bates, K. Twombley, V. Dwarakanath, M. L. Robinson, R. Goetz, M. Mohammadi, M. Baum, FGF23 decreases renal NaPi-2a and Na Pi-2c expression and induces hypophosphatemia in vivo predominantly via FGF receptor 1. Am. J. Physiol. Renal Physiol. 297, F282-F291 (2009).
33. T. Shimada, M. Kakitani, Y. Yamazaki, H. Hasegawa, Y. T akeuchi, T. Fujita, S. Fukumoto, K. Tomizuka, T. Yamashita, Targeted ablation of Fgf23 demonstrates an essential physiological role of FGF23 in phosphate and vitamin D metabolism. J. Clin. Invest. 113, 561-568 (2004).
34. Y. Ma, M. Samaraweera, S. Cooke-Hubley, B. J. Kirby, A. C. Karaplis, B. Lanske, C. S. Kovacs, Neither absence nor excess of FGF23 disturbs murine fetal-placental phosphorus homeostasis or prenatal skel etal development and mineralization. Endocrinology 155, 1596-1605 (2014).
35. A. Murayama, K. Takeyama, S. Kitanaka, Y. Kodera, Y. Kawaguchi, T. Hosoya, S. Kato, Positive and n egative regulations of the renal 25-hydroxyvitamin D3 1a-hydroxylase gene by parathyroid hormone, calcitonin, and 1a,25(OH)2D3 in intact animals. Endocrinology 140, 2224-2231 (1999).
36. C. S. Kovacs, The role of vitamin D in pregnancy and lactation: Insights from animal models and clinical studies. Annu. Rev. Nutr. 32, 97-123 (2012).
37. P. Capuano, D. Bacic, M. Roos, S. M. Gisler, G. Stange, J. Biber, B. Kaissling, E. J.Weinman, S. Shenolikar, C. A. Wagner, H. Murer, Defective coupling of apical PTH receptors to phospholipase C prevents internalization of the Na+-phosphate cotransporter NaPi-IIa in Nherf1-deficient mice. Am. J. Physiol. Cell Physiol. 292, C927-C934 (2007).
38. M. Traebert, H. Völkl, J. Biber, H. Murer, B. Kaissling, Luminal and contraluminal action o f 1-34 and 3-34 PTH peptides on renal type IIa Na-Pi cotransporter. Am. J. Physiol. Renal Physiol. 278, F792-F798 (2000).
39. I. C. Forster, N. Hernando, J. Biber, H. Murer, Proximal tubular handling of phosphate: A molecular perspective. Kidney Int. 70, 1548-1559 (2006).
40. M. Minagawa, T. Yasuda, Y. Kobayashi, H. Niimi, Transient pseudohypoparathyroidism of the neonate. Eur. J. Endocrinol. 133, 151-155 (1995).
41. S. Manzar, Transient pseudohypoparathyroidism and neonatal seizure. J. Trop. Pediatr. 47, 113-114 (2001).
42. L. R. Carraro-Lacroix, G. Malnic, A. C. Girardi, Regulation of Na+/H+ exchanger NHE3 by glucagon-like peptide 1 receptor agonist exendin-4 in renal proximal tubule cells. Am. J. Physiol. Renal Physiol. 297, F164 7-F1655 (2009).
43. Y. J. Lee, M. O. Kim, J. M. Ryu, H. J. Han, Regulation of SGLT expression and localization through Epac/PKA-dependent caveolin-1 and F-actin activation in renal proximal tubule cells. Biochim. Biophys. Acta 1823, 971-982 (2012).
44. K. J. Honegger, P. Capuano, C. Winter, D. Bacic, G. Stange, C. A. Wagner, J. Biber, H. Murer, N. Hernando, Regulation of sodium-proto n exchanger isoform 3 (NHE3) by PKA and exchange protein directly activated by cAMP (EPAC). Proc. Natl. Acad. Sci. U.S.A. 103, 803-808 (2006).
45. L. F. Brass, J. A. Hoxie, T. Kieber-Emmons, D. R. Manning, M. Poncz, M. Woolkalis, Agonist receptors and G proteins as mediators of platelet activation. Adv. Exp. Med. Biol. 344, 17-36 (1993).
46. C. K. Billington, R. B. Penn, Signaling and regulation of G protein-coupled receptors in airway smooth muscle. Respir. Res. 4, 2 (2003).
47. M. Chen, O. Gavrilova, J. Liu, T. Xie, C. Deng, A. T. Nguyen, L. M. Nackers, J. Lorenzo, L. Shen, L. S. Weinstein, Alternative Gnas gene products have opposite effects on glucose and lipid metabolism. Proc. Natl. Acad. Sci. U.S.A. 102, 7386-7391 (2005).
48. X. Hui, G. Reither, L. Kaestner, P. Lipp, Targeted activation of conventional and novel protein kinases C through differential translocation patterns. Mol. Cell Biol. 34, 2370-2381 (2014).
49. S. Verrall, M. Ishii, M. Chen, L. Wang , T. Tram, S. R. Coughlin, The thrombin receptor second cytoplasmic loop confers coupling to Gq-like G proteins in chimeric receptors: Additional evidence for a common transmembrane signaling and G protein coupling mechanism in G protein-coup led receptors. J. Biol. Chem. 272, 6898-6902 (1997).
50. M. Gschwendt, Protein kinase Cd. Eur. J. Biochem. 259, 555-564 (1999).
51. T. Hirai K. Chida Protein kinase Cz (PKCz): Activation mechanisms and cellular functions, J. Biochem. 133 1-7(2003).
52. H Takasu, J Guo, FR Bringhurst, Dual signaling and ligand selectivity of the human PTH/PTHrP receptor. J. Bone Miner. Res. 14, 11-20 (1999).
53. S. A. Eaton, C. M. Williamson, S. T. Ball, C. V. Beechey, L. Moir, J. Edwards, L. Teboul, M. Maconochie, J. Peters, New mutations at the impri nted Gnas cluster show gene dosage effects of Gsa in postnatal growth and implicate XLas in bone and fat metabolism but not in suckling. Mol. Cell Biol. 32, 1017-1029 (2012).
54. Q. He, X. Yang, Y. Gong , D. Kovalenko, E. Canalis, C. J. Rosen, R. E. Friesel, Deficiency of Sef is associated with increased postnatal cortical bone mass by regulating Runx2 activity. J. Bone Miner. Res. 29, 1217-1231 (2014).
55. J. Biber, B. Stieger, G. Stange, H. Murer, Isolation of renal proximal tubular brushborder membranes. Nat. Protoc. 2, 1356-1359 (2007).
56. M. Masuda, H. Yamamoto, M. Kozai, S. Tanaka, M. Ishiguro, Y. Takei, O. Nakahashi, S. Ikeda, T. Uebanso, Y. Taketani, H. Segawa, K. Miyamoto, E. Takeda, Regulation of renal sodium-depe ndent phosphate co-transporter genes (Npt2a and Npt2c) by alltrans-retinoic acid and its receptors. Biochem. J. 429, 583-592 (2010).
57. R. B. Doctor, J. Chen, L. L. Peters, S. E. Lux, L. J. Mandel, Distribution of epithelial ankyrin (Ank3) spliceoforms in renal proximal and distal tubules. Am. J. Physiol. 274, F129-F138 (1998).
58. P. H. Carter, T. Dean, B. Bhayana, A. Khatri, R. R ajur, T. J. Gardella, Actions of the small molecule ligands SW106 and AH-3960 on the type-1 parathyroid hormone receptor. Mol. Endocrinol. 29, 307-321 (2015).
59. D. Yang, J. Guo, P. Divieti, F. R. Bringhurst, Parathyroid hormone activates PKC-d and regulates osteoblastic differentiation via a PLC-independent pathway. Bone 38, 485-496 (2006).