Renal phosphate wasting in the absence of adenylyl cyclase 6

Journal of the American Society of Nephrology

Volumn 25, Issue 12, 2014, Pages 2822-2834

  Fenton, Robert A ^a   Murray, Fiona ^b   Dominguez Rieg, Jessica A ^c   Tang, Tong ^d   Levi, Moshe ^e   Rieg, Timo ^b,d  

^a AARHUS UNIVERSITY   (Denmark)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^e UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; ADENYLYL CYCLASE 6; CALCIUM SENSING RECEPTOR; CREATININE; CYCLIC AMP; FIBROBLAST GROWTH FACTOR 23; FIBROBLAST GROWTH FACTOR RECEPTOR; FORSKOLIN; NPT2A PROTEIN; NPT2C PROTEIN; PARATHYROID HORMONE; PHOSPHATE; PROTEIN; TECALCET; UNCLASSIFIED DRUG; FIBROBLAST GROWTH FACTOR; SLC34A1 PROTEIN, MOUSE; SODIUM PHOSPHATE COTRANSPORTER 2A;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CONFOCAL LASER MICROSCOPY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CREATININE URINE LEVEL; CYCLIC AMP URINE LEVEL; FEMALE; GENOTYPE; HYPERPARATHYROIDISM; HYPERPHOSPHATEMIA; IMMUNOGOLD ELECTRON MICROSCOPY; IMMUNOGOLD LABELING; IMMUNOHISTOCHEMISTRY; KIDNEY CLEARANCE; KIDNEY PROXIMAL TUBULE; LYSOSOME; MALE; MICROVILLUS; MOUSE; NONHUMAN; PARATHYROID HORMONE BLOOD LEVEL; PHOSPHATE BLOOD LEVEL; PHOSPHATE EXCRETION; PHOSPHATE INTAKE; PHOSPHATE URINE LEVEL; PRIORITY JOURNAL; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; SECONDARY HYPERPARATHYROIDISM; URINARY EXCRETION; ANIMAL; CHEMISTRY; GENETICS; HOMEOSTASIS; KIDNEY; KIDNEY DISEASE; METABOLISM; PHENOTYPE; PROTEIN TRANSPORT; TRANSGENIC MOUSE; URINE;

ADENYLYL CYCLASES; ANIMALS; CYCLIC AMP; FEMALE; FIBROBLAST GROWTH FACTORS; HOMEOSTASIS; HYPERPARATHYROIDISM; HYPERPHOSPHATEMIA; IMMUNOHISTOCHEMISTRY; KIDNEY; KIDNEY DISEASES; LYSOSOMES; MALE; MICE; MICE, TRANSGENIC; PARATHYROID HORMONE; PHENOTYPE; PHOSPHATES; PROTEIN TRANSPORT; SODIUM-PHOSPHATE COTRANSPORTER PROTEINS, TYPE IIA;

EID: 84921514415     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2013101102     Document Type: Article

References (62)

1. Levi M, Blaine J, Breusegem S, Takahashi H, Sorribas V, Barry N: Renal phosphate-wasting disorders. Adv Chronic Kidney Dis 13: 155-165, 2006
2. Bergwitz C, Jüppner H: Regulation of phosphate homeostasis by PTH, vitamin D, and FGF23. Annu Rev Med 61: 91-104, 2010
3. Forster IC, Hernando N, Biber J, Murer H: Phosphate transporters of the SLC20 and SLC34 families. Mol Aspects Med 34: 386-395, 2013
4. Bacic D, Lehir M, Biber J, Kaissling B, Murer H, Wagner CA: The renal Na+/phosphate cotransporter NaPi-IIa is internalized via the receptor-mediated endocytic route in response to parathyroid hormone. Kidney Int 69: 495-503, 2006
5. Segawa H, Yamanaka S, Onitsuka A, Tomoe Y, Kuwahata M, Ito M, Taketani Y, Miyamoto K: Parathyroid hormone-dependent endocytosis of renal type IIc Na-Pi cotransporter. Am J Physiol Renal Physiol 292: F395-F403, 2007
6. Picard N, Capuano P, Stange G, Mihailova M, Kaissling B, Murer H, Biber J, Wagner CA: Acute parathyroid hormone differentially regulates renal brush bordermembrane phosphate cotransporters. Pflugers Arch 460: 677-687, 2010
7. Guo J, Song L, Liu M, Segawa H, Miyamoto K, Bringhurst FR, Kronenberg HM, Jüppner H: 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. Endocrinology 154: 1680-1689, 2013
8. Iida-Klein A, Guo J, Drake MT, Kronenberg HM, Abou-Samra AB, Bringhurst FR, Segre GV: Structural requirements of parathyroid hormone/parathyroid hormone-related peptide receptors for phospholipase C activation and regulation of phosphate uptake. Miner Electrolyte Metab 21: 177-179, 1995
9. Iida-Klein A, Guo J, Takemura M, Drake MT, Potts JT Jr., Abou-Samra A, Bringhurst FR, Segre GV: 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, 1997
10. Bacic D, Schulz N, Biber J, Kaissling B, Murer H, Wagner CA: Involvement of the MAPK-kinase pathway in the PTH-mediated regulation of the proximal tubule type IIa Na+/Pi cotransporter in mouse kidney. Pflugers Arch 446: 52-60, 2003
11. Lederer ED, Sohi SS, McLeish KR: Parathyroid hormone stimulates extracellular signal-regulated kinase (ERK) activity through two independent signal transduction pathways: Role of ERK in sodium-phosphate cotransport. J Am Soc Nephrol 11: 222-231, 2000
12. Gattineni J, Bates C, Twombley K, Dwarakanath V, Robinson ML, Goetz R, Mohammadi M, Baum M: FGF23 decreases renal NaPi-2a and NaPi-2c expression and induces hypophosphatemia in vivo predominantly via FGF receptor 1. Am J Physiol Renal Physiol 297: F282-F291, 2009
13. Biber J, Hernando N, Forster I, Murer H: Regulation of phosphate transport in proximal tubules. Pflugers Arch 458: 39-52, 2009
14. Madjdpour C, Bacic D, Kaissling B, Murer H, Biber J: Segment-specific expression of sodium-phosphate cotransporters NaPi-IIa and-IIc and interacting proteins in mouse renal proximal tubules. Pflugers Arch 448: 402-410, 2004
15. Nie X, Arrighi I, Kaissling B, Pfaff I, Mann J, Barhanin J, Vallon V: Expression and insights on function of potassium channel TWIK-1 in mouse kidney. Pflugers Arch 451: 479-488, 2005
16. Giral H, Lanzano L, Caldas Y, Blaine J, Verlander JW, Lei T, Gratton E, Levi M: Role of PDZK1 protein in apicalmembrane expression of renal sodium-coupled phosphate transporters. J Biol Chem 286: 15032-15042, 2011
17. Segawa H, Yamanaka S, Ito M, Kuwahata M, Shono M, Yamamoto T, Miyamoto K: Internalization of renal type IIc Na-Pi cotransporter in response to a high-phosphate diet. Am J Physiol Renal Physiol 288: F587-F596, 2005
18. Yu S, Yu D, Lee E, Eckhaus M, Lee R, Corria Z, Accili D, Westphal H, Weinstein LS: Variable and tissue-specific hormone resistance in heterotrimeric Gs protein alpha-subunit (Gsalpha) knockout mice is due to tissue-specific imprinting of the gsalpha gene. Proc Natl Acad Sci U S A 95: 8715-8720, 1998
19. Germain-Lee EL, Schwindinger W, Crane JL, Zewdu R, Zweifel LS, Wand G, Huso DL, Saji M, Ringel MD, Levine MA: A mouse model of albright hereditary osteodystrophy generated by targeted disruption of exon 1 of the Gnas gene. Endocrinology 146: 4697-4709, 2005
20. Liu J, Litman D, Rosenberg MJ, Yu S, Biesecker LG, Weinstein LS: A GNAS1 imprinting defect in pseudohypoparathyroidism type IB. J Clin Invest 106: 1167-1174, 2000
21. Rieg T, Kohan DE: Regulation of nephron water and electrolyte transport by adenylyl cyclases. Am J Physiol Renal Physiol 306: F701-F709, 2014
22. Shen T, Suzuki Y, Poyard M, Miyamoto N, Defer N, Hanoune J: Expression of adenylyl cyclase mRNAs in the adult, in developing, and in the Brattleboro rat kidney. Am J Physiol 273: C323-C330, 1997
23. Bek MJ, Zheng S, Xu J, Yamaguchi I, Asico LD, Sun XG, Jose PA: Differential expression of adenylyl cyclases in the rat nephron. Kidney Int 60: 890-899, 2001
24. Defer N, Best-Belpomme M, Hanoune J: Tissue specificity and physiological relevance of various isoforms of adenylyl cyclase. Am J Physiol Renal Physiol 279: F400-F416, 2000
25. Wu CS, Lin JT, Chien CL, Chang WC, Lai HL, Chang CP, Chern Y: Type VI adenylyl cyclase regulates neurite extension by binding to Snapin and Snap25. Mol Cell Biol 31: 4874-4886, 2011
26. Rieg T, Tang T, Uchida S, Hammond HK, Fenton RA, Vallon V: Adenylyl cyclase6 enhances NKCC2 expressionandmediates vasopressin-induced phosphorylation of NKCC2 and NCC. Am J Pathol 182: 96-106, 2013
27. Rieg T, Tang T, Murray F, Schroth J, Insel PA, Fenton RA, Hammond HK, Vallon V: Adenylate cyclase 6 determines cAMP formation and aquaporin-2 phosphorylation and trafficking in inner medulla. J Am Soc Nephrol 21: 2059-2068, 2010
28. Roos KP, Strait KA, Raphael KL, Blount MA, Kohan DE: Collecting duct-specific knockout of adenylyl cyclase type VI causes a urinary concentration defect in mice. Am J Physiol Renal Physiol 302: F78-F84, 2012
29. Roos KP, Bugaj V, Mironova E, Stockand JD, Ramkumar N, Rees S, Kohan DE: Adenylyl cyclase VI mediates vasopressin-stimulated ENaC activity. J Am Soc Nephrol 24: 218-227, 2013
30. Chien CL, Wu YS, Lai HL, Chen YH, Jiang ST, Shih CM, Lin SS, Chang C, Chern Y: Impaired water reabsorption in mice deficient in the type VI adenylyl cyclase (AC6). FEBS Lett 584: 2883-2890, 2010
31. Chabardès D, Firsov D, Aarab L, Clabecq A, Bellanger AC, Siaume-Perez S, Elalouf JM: Localization of mRNAs encoding Ca2+-inhibitable adenylyl cyclases along the renal tubule. Functional consequences for regulation of the cAMP content. J Biol Chem 271: 19264-19271, 1996
32. Radanovic T, Wagner CA, Murer H, Biber J: Regulation of intestinal phosphate transport. I. Segmental expression and adaptation to low-P (i) diet of the type IIb Na(+)-P(i) cotransporter in mouse small intestine. Am J Physiol Gastrointest Liver Physiol 288: G496-G500, 2005
33. Neary NM, El-Maouche D, Hopkins R, Libutti SK, Moses AM, Weinstein LS: Development and treatment of tertiary hyperparathyroidism in patients with pseudohypoparathyroidism type 1B. J Clin Endocrinol Metab 97: 3025-3030, 2012
34. Kawata T, Imanishi Y, Kobayashi K, Kenko T, Wada M, Ishimura E, Miki T, Nagano N, Inaba M, Arnold A, Nishizawa Y: Relationship between parathyroid calcium-sensing receptor expression and potency of the calcimimetic, cinacalcet, in suppressing parathyroid hormone secretion in an in vivo murine model of primary hyperparathyroidism. Eur J Endocrinol 153: 587-594, 2005
35. Hruska KA, Moskowitz D, Esbrit P, Civitelli R, Westbrook S, Huskey M: Stimulation of inositol trisphosphate and diacylglycerol production in renal tubular cells by parathyroid hormone. J Clin Invest 79: 230-239, 1987
36. Farrow EG, Summers LJ, Schiavi SC, McCormick JA, Ellison DH, White KE: Altered renal FGF23-mediated activity involving MAPK and Wnt: Effects of the Hyp mutation. J Endocrinol 207: 67-75, 2010
37. Gattineni J, Alphonse P, Zhang Q, Mathews N, Bates CM, Baum M: Regulation of renal phosphate transport by FGF23 is mediated by FGFR1 and FGFR4. Am J Physiol Renal Physiol 306: F351-F358, 2014
38. Urakawa I, Yamazaki Y, Shimada T, Iijima K, Hasegawa H, Okawa K, Fujita T, Fukumoto S, Yamashita T: Klotho converts canonical FGF receptor into a specific receptor for FGF23. Nature 444: 770-774, 2006
39. Keusch I, Traebert M, Lötscher M, Kaissling B, Murer H, Biber J: Parathyroid hormone and dietary phosphate provoke a lysosomal routing of the proximal tubular Na/Pi-cotransporter type II. Kidney Int 54: 1224-1232, 1998
40. Wagner CA, Loffing-Cueni D, Yan Q, Schulz N, Fakitsas P, Carrel M, Wang T, Verrey F, Geibel JP, Giebisch G, Hebert SC, Loffing J: Mouse model of type II Bartter's syndrome. II. Altered expression of renal sodium- and water-transporting proteins. Am J Physiol Renal Physiol 294: F1373-F1380, 2008
41. Kwon TH, Laursen UH, Marples D, Maunsbach AB, Knepper MA, Frokiaer J, Nielsen S: Altered expression of renal AQPs and Na(+) transporters in rats with lithium-induced NDI. Am J Physiol Renal Physiol 279: F552-F564, 2000
42. Lanzano L, Lei T, Okamura K, Giral H, Caldas Y, Masihzadeh O, Gratton E, Levi M, Blaine J: Differential modulation of the molecular dynamics of the type IIa and IIc sodium phosphate cotransporters by parathyroid hormone. Am J Physiol Cell Physiol 301: C850-C861, 2011
43. Breusegem SY, Takahashi H, Giral-Arnal H, Wang X, Jiang T, Verlander JW, Wilson P, Miyazaki-Anzai S, Sutherland E, Caldas Y, Blaine JT, Segawa H, Miyamoto K, Barry NP, Levi M: Differential regulation of the renal sodium-phosphate cotransporters NaPi-IIa, NaPi-IIc, and PiT-2 in dietary potassium deficiency. Am J Physiol Renal Physiol 297: F350-F361, 2009
44. Rhee Y, Bivi N, Farrow E, Lezcano V, Plotkin LI, White KE, Bellido T: Parathyroid hormone receptor signaling in osteocytes increases the expression of fibroblast growth factor-23 in vitro and in vivo. Bone 49: 636-643, 2011
45. Brown WW, Jüppner H, Langman CB, Price H, Farrow EG, White KE, McCormick KL: Hypophosphatemia with elevations in serum fibroblast growth factor 23 in a child with Jansen's metaphyseal chondrodysplasia. J Clin Endocrinol Metab 94: 17-20, 2009
46. Burnett-Bowie SM, Henao MP, Dere ME, Lee H, Leder BZ: Effects of hPTH (1-34) infusion on circulating serum phosphate, 1,25-dihydroxyvitamin D, and FGF23 levels in healthy men. J Bone Miner Res 24: 1681-1685, 2009
47. Smith RC, O'Bryan LM, Farrow EG, Summers LJ, Clinkenbeard EL, Roberts JL, Cass TA, Saha J, Broderick C, Ma YL, Zeng QQ, Kharitonenkov A, Wilson JM, Guo Q, Sun H, Allen MR, Burr DB, Breyer MD, White KE: Circulating a Klotho influences phosphate handling by controlling FGF23 production. J Clin Invest 122: 4710-4715, 2012
48. Sabbagh Y, O'Brien SP, Song W, Boulanger JH, Stockmann A, Arbeeny C, Schiavi SC: Intestinal npt2b plays a major role in phosphate absorption and homeostasis. J Am Soc Nephrol 20: 2348-2358, 2009
49. Lötscher M, Scarpetta Y, Levi M, Halaihel N, Wang H, Zajicek HK, Biber J, Murer H, Kaissling B: Rapid downregulation of rat renal Na/P(i) cotransporter in response to parathyroid hormone involves microtubule rearrangement. J Clin Invest 104: 483-494, 1999
50. Nagai S, Okazaki M, Segawa H, Bergwitz C, Dean T, Potts JT Jr., Mahon MJ, Gardella TJ, Jüppner H: Acute down-regulation of sodium-dependent phosphate transporter NPT2a involves predominantly the cAMP/PKA pathway as revealed by signaling-selective parathyroid hormone analogs. J Biol Chem 286: 1618-1626, 2011
51. Bellorin-Font E, Martin KJ: Regulation of the PTH-receptor-cyclase system of canine kidney: Effects of calcium, magnesium, and guanine nucleotides. Am J Physiol 241: F364-F373, 1981
52. Traebert M, Roth J, Biber J, Murer H, Kaissling B: Internalization of proximal tubular type II Na-P(i) cotransporter by PTH: Immunogold electronmicroscopy. Am J Physiol Renal Physiol 278: F148-F154, 2000
53. Tang T, Gao MH, Lai NC, Firth AL, Takahashi T, Guo T, Yuan JXJ, Roth DM, Hammond HK: Adenylyl cyclase type 6 deletion decreases left ventricular function via impaired calcium handling. Circulation 117: 61-69, 2008
54. Weiss J, Sos ML, Seidel D, Peifer M, Zander T, Heuckmann JM, Ullrich RT, Menon R, Maier S, Soltermann A, Moch H, Wagener P, Fischer F, Heynck S, Koker M, Schöttle J, Leenders F, Gabler F, DabowI, Querings S, Heukamp LC, Balke-Want H, Ansén S, Rauh D, Baessmann I, Altmüller J, Wainer Z, Conron M, Wright G, Russell P, Solomon B, Brambilla E, Brambilla C, Lorimier P, Sollberg S, Brustugun OT, Engel-Riedel W, Ludwig C, Petersen I, Sänger J, Clement J, Groen H, Timens W, Sietsma H, Thunnissen E, Smit E, Heideman D, Cappuzzo F, Ligorio C, Damiani S, Hallek M, Beroukhim R, Pao W, Klebl B, Baumann M, Buettner R, Ernestus K, Stoelben E, Wolf J, Nürnberg P, Perner S, Thomas RK: Frequent and focal FGFR1 amplification associates with therapeutically tractable FGFR1 dependency in squamous cell lung cancer. Sci Transl Med 2: 62ra93, 2010
55. Wöhrle S, Bonny O, Beluch N, Gaulis S, Stamm C, Scheibler M, Müller M, Kinzel B, Thuery A, Brueggen J, Hynes NE, Sellers WR, Hofmann F, Graus-Porta D: FGF receptors control vitamin D and phosphate homeostasis by mediating renal FGF-23 signaling and regulating FGF-23 expression in bone. J Bone Miner Res 26: 2486-2497, 2011
56. + excretion. Am J Physiol Regul Integr Comp Physiol 301: R510-R518, 2011
57. Rieg T, Richter K, Osswald H, Vallon V: Kidney function in mice: Thiobutabarbital versus alpha-chloralose anesthesia. Naunyn Schmiedebergs Arch Pharmacol 370: 320-323, 2004
58. Rieg T, Bundey RA, Chen Y, Deschenes G, Junger W, Insel PA, Vallon V: Mice lacking P2Y2 receptors have salt-resistant hypertension and facilitated renal Na+ and water reabsorption. FASEB J 21: 3717-3726, 2007
59. Rieg T, Pothula K, Schroth J, Satriano J, Osswald H, Schnermann J, Insel PA, Bundey RA, Vallon V: Vasopressin regulation of inner medullary collecting ducts and compensatory changes in mice lacking adenosine A1 receptors. Am J Physiol Renal Physiol 294: F638-F644, 2008
60. Guder WG: Stimulation of renal gluconeogenesis by angiotensin II. Biochim Biophys Acta 584: 507-519, 1979
61. Moeller HB, Knepper MA, Fenton RA: Serine 269 phosphorylated aquaporin-2 is targeted to the apical membrane of collecting duct principal cells. Kidney Int 75: 295-303, 2009
62. Sandberg MB, Maunsbach AB, McDonough AA: Redistribution of distal tubule Na+-Cl- cotransporter (NCC) in response to a high-salt diet. Am J Physiol Renal Physiol 291: F503-F508, 2006