Advertisement

NAD metabolism and the SLC34 family: evidence for a liver-kidney axis regulating inorganic phosphate

  • Sawako Tatsumi
  • Kanako Katai
  • Ichiro Kaneko
  • Hiroko Segawa
  • Ken-ichi Miyamoto
Invited Review

Abstract

The solute carrier 34 (SLC34) family of membrane transporters is a major contributor to Pi homeostasis. Many factors are involved in regulating the SLC34 family. The roles of the bone mineral metabolism factors parathyroid hormone (PTH) and fibroblast growth factor 23 (FGF23) in Pi homeostasis are well studied. Intracellular Pi is thought to be involved in energy metabolism, such as ATP production. Under certain conditions of altered energy metabolism, plasma Pi concentrations are affected by the regulation of a Pi shift into cells or release from the tissues. We recently investigated the mechanism of hepatectomy-related hypophosphatemia, which is thought to involve an unknown phosphaturic factor. Hepatectomy-related hypophosphatemia is due to impaired nicotinamide adenine dinucleotide (NAD) metabolism through its effects on the SLC34 family in the liver-kidney axis. The oxidized form of NAD, NAD+, is an essential cofactor in various cellular biochemical reactions. Levels of NAD+ and its reduced form NADH vary with the availability of dietary energy and nutrients. Nicotinamide phosphoribosyltransferase (Nampt) generates a key NAD+ intermediate, nicotinamide mononucleotide, from nicotinamide and 5-phosphoribosyl 1-pyrophosphate. The liver, an important organ of NAD metabolism, is thought to release metabolic products such as nicotinamide and may control NAD metabolism in other organs. Moreover, NAD is an important regulator of the circadian rhythm. Liver-specific Nampt-deficient mice and heterozygous Nampt mice have abnormal daily plasma Pi concentration oscillations. These data indicate that NAD metabolism in the intestine, liver, and kidney is closely related to Pi metabolism through the SLC34 family. Here, we review the relationship between the SLC34 family and NAD metabolism based on our recent studies.

Keywords

SLC34 Phosphate NAD Nampt Liver Kidney 

Abbreviations

Nampt

Nicotinamide phosphoribosyltransferase

NAM

Nicotinamide

NAD+

Nicotinamide adenine dinucleotide

MNA

N1-methylnicotinamide

2-Py

N1-methyl-2-pyridone-5-carboxamide

4-Py

N1-methyl-4-pyridine-3-carboxamide

ZT

Zeitgeber time

PH

Partial hepatectomy

References

  1. 1.
    Bai P, Canto C, Oudart H, Brunyanszki A, Cen Y, Thomas C, Yamamoto H, Huber A, Kiss B, Houtkooper RH, Schoonjans K, Schreiber V, Sauve AA, Menissier-de Murcia J, Auwerx J (2011) PARP-1 inhibition increases mitochondrial metabolism through SIRT1 activation. Cell Metab 13:461–468.  https://doi.org/10.1016/j.cmet.2011.03.004 CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Beck L, Karaplis AC, Amizuka N, Hewson AS, Ozawa H, Tenenhouse HS (1998) Targeted inactivation of Npt2 in mice leads to severe renal phosphate wasting, hypercalciuria, and skeletal abnormalities. Proc Natl Acad Sci U S A 95:5372–5377CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Becker GJ, Walker RG, Hewitson TD, Pedagogos E (2009) Phosphate levels--time for a rethink? Nephrol Dialysis Trans 24:2321–2324.  https://doi.org/10.1093/ndt/gfp220 CrossRefGoogle Scholar
  4. 4.
    Bender DA, Olufunwa R (1988) Utilization of tryptophan, nicotinamide and nicotinic acid as precursors for nicotinamide nucleotide synthesis in isolated rat liver cells. Br J Nutr 59:279–287CrossRefPubMedGoogle Scholar
  5. 5.
    Bergwitz C, Roslin NM, Tieder M, Loredo-Osti JC, Bastepe M, Abu-Zahra H, Frappier D, Burkett K, Carpenter TO, Anderson D, Garabedian M, Sermet I, Fujiwara TM, Morgan K, Tenenhouse HS, Juppner H (2006) SLC34A3 mutations in patients with hereditary hypophosphatemic rickets with hypercalciuria predict a key role for the sodium-phosphate cotransporter NaPi-IIc in maintaining phosphate homeostasis. Am J Hum Genet 78:179–192.  https://doi.org/10.1086/499409 CrossRefGoogle Scholar
  6. 6.
    Berndt TJ, Knox FG, Kempson SA, Dousa TP (1981) Nicotinamide adenine dinucleotide and renal response to parathyroid hormone. Endocrinology 108:2005–2007.  https://doi.org/10.1210/endo-108-5-2005 CrossRefPubMedGoogle Scholar
  7. 7.
    Bielesz B, Bacic D, Honegger K, Biber J, Murer H, Wagner CA (2006) Unchanged expression of the sodium-dependent phosphate cotransporter NaPi-IIa despite diurnal changes in renal phosphate excretion. Arch Eur J Physiol 452:683–689.  https://doi.org/10.1007/s00424-006-0087-0 CrossRefGoogle Scholar
  8. 8.
    Block GA, Klassen PS, Lazarus JM, Ofsthun N, Lowrie EG, Chertow GM (2004) Mineral metabolism, mortality, and morbidity in maintenance hemodialysis. J Am Soc Nephrol : JASN 15:2208–2218.  https://doi.org/10.1097/01.ASN.0000133041.27682.A2 CrossRefPubMedGoogle Scholar
  9. 9.
    Bose S, French S, Evans FJ, Joubert F, Balaban RS (2003) Metabolic network control of oxidative phosphorylation: multiple roles of inorganic phosphate. J Biol Chem 278:39155–39165.  https://doi.org/10.1074/jbc.M306409200 CrossRefPubMedGoogle Scholar
  10. 10.
    Buell JF, Berger AC, Plotkin JS, Kuo PC, Johnson LB (1998) The clinical implications of hypophosphatemia following major hepatic resection or cryosurgery. Arch Surg 133:757–761CrossRefPubMedGoogle Scholar
  11. 11.
    Campbell PI, al-Mahrouq HA, Abraham MI, Kempson SA (1989) Specific inhibition of rat renal Na+/phosphate cotransport by picolinamide. J Pharmacol Exp Ther 251:188–192PubMedGoogle Scholar
  12. 12.
    Canto C, Auwerx J (2009) Caloric restriction, SIRT1 and longevity. Trends Endocrinol Metab 20:325–331.  https://doi.org/10.1016/j.tem.2009.03.008 CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Canto C, Houtkooper RH, Pirinen E, Youn DY, Oosterveer MH, Cen Y, Fernandez-Marcos PJ, Yamamoto H, Andreux PA, Cettour-Rose P, Gademann K, Rinsch C, Schoonjans K, Sauve AA, Auwerx J (2012) The NAD(+) precursor nicotinamide riboside enhances oxidative metabolism and protects against high-fat diet-induced obesity. Cell Metab 15:838–847.  https://doi.org/10.1016/j.cmet.2012.04.022 CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Canto C, Jiang LQ, Deshmukh AS, Mataki C, Coste A, Lagouge M, Zierath JR, Auwerx J (2010) Interdependence of AMPK and SIRT1 for metabolic adaptation to fasting and exercise in skeletal muscle. Cell Metab 11:213–219.  https://doi.org/10.1016/j.cmet.2010.02.006 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Canto C, Menzies KJ, Auwerx J (2015) NAD(+) metabolism and the control of energy homeostasis: a balancing act between mitochondria and the nucleus. Cell Metab 22:31–53.  https://doi.org/10.1016/j.cmet.2015.05.023 CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Caverzasio J, Rizzoli R, Bonjour JP (1986) Sodium-dependent phosphate transport inhibited by parathyroid hormone and cyclic AMP stimulation in an opossum kidney cell line. J Biol Chem 261:3233–3237PubMedGoogle Scholar
  17. 17.
    Chang AR, Grams ME (2014) Serum phosphorus and mortality in the third National Health and nutrition examination survey (NHANES III): effect modification by fasting. Am J Kidney Dis 64:567–573.  https://doi.org/10.1053/j.ajkd.2014.04.028 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Cheng SC, Young DO, Huang Y, Delmez JA, Coyne DW (2008) A randomized, double-blind, placebo-controlled trial of niacinamide for reduction of phosphorus in hemodialysis patients. Clin J Am Soc Nephrol : CJASN 3:1131–1138.  https://doi.org/10.2215/CJN.04211007 CrossRefPubMedGoogle Scholar
  19. 19.
    Coskun R, Gundogan K, Baldane S, Guven M, Sungur M (2014) Refeeding hypophosphatemia: a potentially fatal danger in the intensive care unit. Turkish J Med Sci 44:369–374CrossRefGoogle Scholar
  20. 20.
    Costford SR, Bajpeyi S, Pasarica M, Albarado DC, Thomas SC, Xie H, Church TS, Jubrias SA, Conley KE, Smith SR (2010) Skeletal muscle NAMPT is induced by exercise in humans. Am J Phys Endocrinol Metab 298:E117–E126.  https://doi.org/10.1152/ajpendo.00318.2009 CrossRefGoogle Scholar
  21. 21.
    Datta HK, Malik M, Neely RD (2007) Hepatic surgery-related hypophosphatemia. Clinica Chim Acta 380:13–23.  https://doi.org/10.1016/j.cca.2007.01.027 CrossRefGoogle Scholar
  22. 22.
    Dhingra R, Sullivan LM, Fox CS, Wang TJ, D'Agostino RB Sr, Gaziano JM, Vasan RS (2007) Relations of serum phosphorus and calcium levels to the incidence of cardiovascular disease in the community. Arch Intern Med 167:879–885.  https://doi.org/10.1001/archinte.167.9.879 CrossRefPubMedGoogle Scholar
  23. 23.
    Dominguez JH, Pitts TO, Brown T, Puschett DB, Schuler F, Chen TC, Puschett JB (1984) Prostaglandin E2 and parathyroid hormone: comparisons of their actions on the rabbit proximal tubule. Kidney Int 26:404–410CrossRefPubMedGoogle Scholar
  24. 24.
    Dousa TP (1996) Modulation of renal Na-pi cotransport by hormones acting via genomic mechanism and by metabolic factors. Kidney Int 49:997–1004CrossRefPubMedGoogle Scholar
  25. 25.
    Eddington H, Hoefield R, Sinha S, Chrysochou C, Lane B, Foley RN, Hegarty J, New J, O'Donoghue DJ, Middleton RJ, Kalra PA (2010) Serum phosphate and mortality in patients with chronic kidney disease. Clin J Am Soc Nephrol : CJASN 5:2251–2257.  https://doi.org/10.2215/CJN.00810110 CrossRefPubMedGoogle Scholar
  26. 26.
    Eto N, Miyata Y, Ohno H, Yamashita T (2005) Nicotinamide prevents the development of hyperphosphataemia by suppressing intestinal sodium-dependent phosphate transporter in rats with adenine-induced renal failure. Nephrol Dialysis Trans 20:1378–1384.  https://doi.org/10.1093/ndt/gfh781 CrossRefGoogle Scholar
  27. 27.
    Farrow EG, White KE (2010) Recent advances in renal phosphate handling. Nat Rev Nephrol 6:207–217.  https://doi.org/10.1038/nrneph.2010.17 CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Ferris GM, Clark JB (1971) Nicotinamide nucleotide synthesis in regenerating rat liver. Biochem J 121:655–662CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Ferris GM, Clark JB (1972) The control of nucleic acid and nicotinamide nucleotide synthesis in regenerating rat liver. Biochem J 128:869–877CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Giovannini I, Chiarla C, Giuliante F, Ardito F, Vellone M, Nuzzo G (2006) Hepatic resection-related hypophosphatemia is of renal origin as manifested by isolated hyperphosphaturia. Ann Surg 243:429; author reply 429.  https://doi.org/10.1097/01.sla.0000202002.17260.c4 CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Giovannini I, Chiarla C, Nuzzo G (2002) Pathophysiologic and clinical correlates of hypophosphatemia and the relationship with sepsis and outcome in postoperative patients after hepatectomy. Shock 18:111–115CrossRefPubMedGoogle Scholar
  32. 32.
    Goldsweig BK, Carpenter TO (2015) Hypophosphatemic rickets: lessons from disrupted FGF23 control of phosphorus homeostasis. Curr Osteoporosis Rep 13:88–97.  https://doi.org/10.1007/s11914-015-0259-y CrossRefGoogle Scholar
  33. 33.
    Gopal E, Fei YJ, Miyauchi S, Zhuang L, Prasad PD, Ganapathy V (2005) Sodium-coupled and electrogenic transport of B-complex vitamin nicotinic acid by slc5a8, a member of the Na/glucose co-transporter gene family. Biochem J 388:309–316.  https://doi.org/10.1042/BJ20041916 CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Hattenhauer O, Traebert M, Murer H, Biber J (1999) Regulation of small intestinal Na-P(i) type IIb cotransporter by dietary phosphate intake. Am J Phys 277:G756–G762Google Scholar
  35. 35.
    Hernando N, Myakala K, Simona F, Knopfel T, Thomas L, Murer H, Wagner CA, Biber J (2015) Intestinal depletion of NaPi-IIb/Slc34a2 in mice: renal and hormonal adaptation. J Bone Mineral Res 30:1925–1937.  https://doi.org/10.1002/jbmr.2523 CrossRefGoogle Scholar
  36. 36.
    Hernando N, Wagner CA (2018) Mechanisms and regulation of intestinal phosphate absorption. Compr Physiol 8:1065–1090.  https://doi.org/10.1002/cphy.c170024 CrossRefPubMedGoogle Scholar
  37. 37.
    Hershberger KA, Martin AS, Hirschey MD (2017) Role of NAD(+) and mitochondrial sirtuins in cardiac and renal diseases. Nat Rev Nephrol 13:213–225.  https://doi.org/10.1038/nrneph.2017.5 CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Higgins GM, Anderson RM (1931) Experimental pathology of the liver: I Restoration of the liver in the white rat following partial remova. ArchPathol 12:186–202Google Scholar
  39. 39.
    Hilfiker H, Hattenhauer O, Traebert M, Forster I, Murer H, Biber J (1998) Characterization of a murine type II sodium-phosphate cotransporter expressed in mammalian small intestine. Proc Natl Acad Sci U S A 95:14564–14569CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Hruska KA, Mathew S, Lund R, Qiu P, Pratt R (2008) Hyperphosphatemia of chronic kidney disease. Kidney Int 74:148–157.  https://doi.org/10.1038/ki.2008.130 CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Ichikawa S, Sorenson AH, Imel EA, Friedman NE, Gertner JM, Econs MJ (2006) Intronic deletions in the SLC34A3 gene cause hereditary hypophosphatemic rickets with hypercalciuria. J Clin Endocrinol Metab 91:4022–4027.  https://doi.org/10.1210/jc.2005-2840 CrossRefPubMedGoogle Scholar
  42. 42.
    Ikuta K, Segawa H, Sasaki S, Hanazaki A, Fujii T, Kushi A, Kawabata Y, Kirino R, Sasaki S, Noguchi M, Kaneko I, Tatsumi S, Ueda O, Wada NA, Tateishi H, Kakefuda M, Kawase Y, Ohtomo S, Ichida Y, Maeda A, Jishage KI, Horiba N, Miyamoto KI (2017) Effect of Npt2b deletion on intestinal and renal inorganic phosphate (pi) handling. Clin Exp Nephrol 22:517–528.  https://doi.org/10.1007/s10157-017-1497-3 CrossRefPubMedGoogle Scholar
  43. 43.
    Imai S (2009) The NAD world: a new systemic regulatory network for metabolism and aging--Sirt1, systemic NAD biosynthesis, and their importance. Cell Biochem Biophys 53:65–74.  https://doi.org/10.1007/s12013-008-9041-4 CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Imai S (2010) "clocks" in the NAD world: NAD as a metabolic oscillator for the regulation of metabolism and aging. Biochim Biophys Acta 1804:1584–1590.  https://doi.org/10.1016/j.bbapap.2009.10.024 CrossRefPubMedGoogle Scholar
  45. 45.
    Imai S, Guarente L (2014) NAD+ and sirtuins in aging and disease. Trends Cell Biol 24:464–471.  https://doi.org/10.1016/j.tcb.2014.04.002 CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Isakova T, Block G (2018) The phosphate bucket list. Kidney Int 93:1033–1035.  https://doi.org/10.1016/j.kint.2018.01.010 CrossRefPubMedGoogle Scholar
  47. 47.
    Isakova T, Xie H, Barchi-Chung A, Smith K, Sowden N, Epstein M, Collerone G, Keating L, Juppner H, Wolf M (2012) Daily variability in mineral metabolites in CKD and effects of dietary calcium and calcitriol. Clin J Am Soc Nephrol : CJASN 7:820–828.  https://doi.org/10.2215/CJN.11721111 CrossRefPubMedGoogle Scholar
  48. 48.
    Ix JH, Anderson CA, Smits G, Persky MS, Block GA (2014) Effect of dietary phosphate intake on the circadian rhythm of serum phosphate concentrations in chronic kidney disease: a crossover study. Am J Clin Nutr 100:1392–1397.  https://doi.org/10.3945/ajcn.114.085498 CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Jubiz W, Canterbury JM, Reiss E, Tyler FH (1972) Circadian rhythm in serum parathyroid hormone concentration in human subjects: correlation with serum calcium, phosphate, albumin, and growth hormone levels. J Clin Invest 51:2040–2046.  https://doi.org/10.1172/JCI107010 CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Katai K, Miyamoto K, Kishida S, Segawa H, Nii T, Tanaka H, Tani Y, Arai H, Tatsumi S, Morita K, Taketani Y, Takeda E (1999) Regulation of intestinal Na+−dependent phosphate co-transporters by a low-phosphate diet and 1,25-dihydroxyvitamin D3. Biochem J 343(Pt 3):705–712CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Katai K, Tanaka H, Tatsumi S, Fukunaga Y, Genjida K, Morita K, Kuboyama N, Suzuki T, Akiba T, Miyamoto K, Takeda E (1999) Nicotinamide inhibits sodium-dependent phosphate cotransport activity in rat small intestine. Nephrol Dialysis Trans 14:1195–1201CrossRefGoogle Scholar
  52. 52.
    Kawai M, Kinoshita S, Shimba S, Ozono K, Michigami T (2014) Sympathetic activation induces skeletal Fgf23 expression in a circadian rhythm-dependent manner. J Biol Chem 289:1457–1466.  https://doi.org/10.1074/jbc.M113.500850 CrossRefPubMedGoogle Scholar
  53. 53.
    Kemp GJ, Blumsohn A, Morris BW (1992) Circadian changes in plasma phosphate concentration, urinary phosphate excretion, and cellular phosphate shifts. Clin Chem 38:400–402PubMedGoogle Scholar
  54. 54.
    Kempson SA, Colon-Otero G, Ou SY, Turner ST, Dousa TP (1981) Possible role of nicotinamide adenine dinucleotide as an intracellular regulator of renal transport of phosphate in the rat. J Clin Invest 67:1347–1360CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Kempson SA, Shah SV, Werness PG, Berndt T, Lee PH, Smith LH, Knox FG, Dousa TP (1980) Renal brush border membrane adaptation to phosphorus deprivation: effects of fasting versus low-phosphorus diet. Kidney Int 18:36–47CrossRefPubMedGoogle Scholar
  56. 56.
    Kishikawa T, Takahashi H, Shimazawa E, Ogata E (1980) Diurnal changes in calcium and phosphate metabolism in rats. Hormone and metabolic research = Hormon- und Stoffwechselforschung = Hormones et metabolisme 12:545–551.  https://doi.org/10.1055/s-2007-999195 CrossRefPubMedGoogle Scholar
  57. 57.
    Kraus D, Yang Q, Kong D, Banks AS, Zhang L, Rodgers JT, Pirinen E, Pulinilkunnil TC, Gong F, Wang YC, Cen Y, Sauve AA, Asara JM, Peroni OD, Monia BP, Bhanot S, Alhonen L, Puigserver P, Kahn BB (2014) Nicotinamide N-methyltransferase knockdown protects against diet-induced obesity. Nature 508:258–262.  https://doi.org/10.1038/nature13198 CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Kuboyama N, Watanabe Y, Yamaguchi M, Sato K, Suzuki T, Akiba T (1999) Effects of niceritrol on faecal and urinary phosphate excretion in normal rats. Nephrol Dialysis Trans 14:610–614CrossRefGoogle Scholar
  59. 59.
    Lederer E (2014) Regulation of serum phosphate. J Physiol 592:3985–3995.  https://doi.org/10.1113/jphysiol.2014.273979 CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Lederer E, Miyamoto K (2012) Clinical consequences of mutations in sodium phosphate cotransporters. Clin J Am Soc Nephrol : CJASN 7:1179–1187.  https://doi.org/10.2215/CJN.09090911 CrossRefPubMedGoogle Scholar
  61. 61.
    Lenglet A, Liabeuf S, Guffroy P, Fournier A, Brazier M, Massy ZA (2013) Use of nicotinamide to treat hyperphosphatemia in dialysis patients. Drugs in R&D 13:165–173.  https://doi.org/10.1007/s40268-013-0024-6 CrossRefGoogle Scholar
  62. 62.
    Lepage R, Legare G, Racicot C, Brossard JH, Lapointe R, Dagenais M, D'Amour P (1999) Hypocalcemia induced during major and minor abdominal surgery in humans. J Clin Endocrinol Metab 84:2654–2658.  https://doi.org/10.1210/jcem.84.8.5889 CrossRefPubMedGoogle Scholar
  63. 63.
    Lin LF, Henderson LM (1972) Pyridinium precursors of pyridine nucleotides in perfused rat kidney and in the testis. J Biol Chem 247:8023–8030PubMedGoogle Scholar
  64. 64.
    Lorenz-Depiereux B, Benet-Pages A, Eckstein G, Tenenbaum-Rakover Y, Wagenstaller J, Tiosano D, Gershoni-Baruch R, Albers N, Lichtner P, Schnabel D, Hochberg Z, Strom TM (2006) Hereditary hypophosphatemic rickets with hypercalciuria is caused by mutations in the sodium-phosphate cotransporter gene SLC34A3. Am J Hum Genet 78:193–201.  https://doi.org/10.1086/499410 CrossRefPubMedGoogle Scholar
  65. 65.
    Marinella MA (2003) The refeeding syndrome and hypophosphatemia. Nutr Rev 61:320–323CrossRefPubMedGoogle Scholar
  66. 66.
    Marinella MA (2005) Refeeding syndrome and hypophosphatemia. J Intensive Care Med 20:155–159.  https://doi.org/10.1177/0885066605275326 CrossRefPubMedGoogle Scholar
  67. 67.
    Martin A, David V, Quarles LD (2012) Regulation and function of the FGF23/klotho endocrine pathways. Physiol Rev 92:131–155.  https://doi.org/10.1152/physrev.00002.2011 CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Martin PR, Shea RJ, Mulks MH (2001) Identification of a plasmid-encoded gene from Haemophilus ducreyi which confers NAD independence. J Bacteriol 183:1168–1174.  https://doi.org/10.1128/JB.183.4.1168-1174.2001 CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Masri S (2015) Sirtuin-dependent clock control: new advances in metabolism, aging and cancer. Current opinion in clinical nutrition and metabolic care 18:521–527.  https://doi.org/10.1097/MCO.0000000000000219 CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Masri S, Sassone-Corsi P (2014) Sirtuins and the circadian clock: bridging chromatin and metabolism. Sci Signal 7:re6.  https://doi.org/10.1126/scisignal.2005685 CrossRefPubMedGoogle Scholar
  71. 71.
    Menon V, Greene T, Pereira AA, Wang X, Beck GJ, Kusek JW, Collins AJ, Levey AS, Sarnak MJ (2005) Relationship of phosphorus and calcium-phosphorus product with mortality in CKD. Am J Kidney Dis 46:455–463.  https://doi.org/10.1053/j.ajkd.2005.05.025 CrossRefPubMedGoogle Scholar
  72. 72.
    Miyagawa A, Tatsumi S, Takahama W, Fujii O, Nagamoto K, Kinoshita E, Nomura K, Ikuta K, Fujii T, Hanazaki A, Kaneko I, Segawa H, Miyamoto KI (2018) The sodium phosphate cotransporter family and nicotinamide phosphoribosyltransferase contribute to the daily oscillation of plasma inorganic phosphate concentration. Kidney Int 93:1073–1085.  https://doi.org/10.1016/j.kint.2017.11.022 CrossRefPubMedGoogle Scholar
  73. 73.
    Miyamoto K, Haito-Sugino S, Kuwahara S, Ohi A, Nomura K, Ito M, Kuwahata M, Kido S, Tatsumi S, Kaneko I, Segawa H (2011) Sodium-dependent phosphate cotransporters: lessons from gene knockout and mutation studies. J Pharm Sci 100:3719–3730.  https://doi.org/10.1002/jps.22614 CrossRefPubMedGoogle Scholar
  74. 74.
    Miyamoto K, Ito M, Tatsumi S, Kuwahata M, Segawa H (2007) New aspect of renal phosphate reabsorption: the type IIc sodium-dependent phosphate transporter. Am J Nephrol 27:503–515.  https://doi.org/10.1159/000107069 CrossRefPubMedGoogle Scholar
  75. 75.
    Murer H, Hernando N, Forster I, Biber J (2000) Proximal tubular phosphate reabsorption: molecular mechanisms. Physiol Rev 80:1373–1409CrossRefPubMedGoogle Scholar
  76. 76.
    Murer H, Hernando N, Forster L, Biber J (2001) Molecular mechanisms in proximal tubular and small intestinal phosphate reabsorption (plenary lecture). Mol Membr Biol 18:3–11CrossRefPubMedGoogle Scholar
  77. 77.
    Nafidi O, Lapointe RW, Lepage R, Kumar R, D'Amour P (2009) Mechanisms of renal phosphate loss in liver resection-associated hypophosphatemia. Ann Surg 249:824–827.  https://doi.org/10.1097/SLA.0b013e3181a3e562 CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Nafidi O, Lepage R, Lapointe RW, D'Amour P (2007) Hepatic resection-related hypophosphatemia is of renal origin as manifested by isolated hyperphosphaturia. Ann Surg 245:1000–1002.  https://doi.org/10.1097/SLA.0b013e31805d0882 CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Nakahata Y, Kaluzova M, Grimaldi B, Sahar S, Hirayama J, Chen D, Guarente LP, Sassone-Corsi P (2008) The NAD+−dependent deacetylase SIRT1 modulates CLOCK-mediated chromatin remodeling and circadian control. Cell 134:329–340.  https://doi.org/10.1016/j.cell.2008.07.002 CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Nakahata Y, Sahar S, Astarita G, Kaluzova M, Sassone-Corsi P (2009) Circadian control of the NAD+ salvage pathway by CLOCK-SIRT1. Science 324:654–657.  https://doi.org/10.1126/science.1170803 CrossRefPubMedGoogle Scholar
  81. 81.
    Nomura K, Tatsumi S, Miyagawa A, Shiozaki Y, Sasaki S, Kaneko I, Ito M, Kido S, Segawa H, Sano M, Fukuwatari T, Shibata K, Miyamoto K (2014) Hepatectomy-related hypophosphatemia: a novel phosphaturic factor in the liver-kidney axis. J Am Soc Nephrol : JASN 25:761–772.  https://doi.org/10.1681/ASN.2013060569 CrossRefPubMedGoogle Scholar
  82. 82.
    O'Seaghdha CM, Hwang SJ, Muntner P, Melamed ML, Fox CS (2011) Serum phosphorus predicts incident chronic kidney disease and end-stage renal disease. Nephrol Dialysis Trans 26:2885–2890.  https://doi.org/10.1093/ndt/gfq808 CrossRefGoogle Scholar
  83. 83.
    Ohi A, Hanabusa E, Ueda O, Segawa H, Horiba N, Kaneko I, Kuwahara S, Mukai T, Sasaki S, Tominaga R, Furutani J, Aranami F, Ohtomo S, Oikawa Y, Kawase Y, Wada NA, Tachibe T, Kakefuda M, Tateishi H, Matsumoto K, Tatsumi S, Kido S, Fukushima N, Jishage K, Miyamoto K (2011) Inorganic phosphate homeostasis in sodium-dependent phosphate cotransporter Npt2b(+)/(−) mice. Am J Physiol Ren Physiol 301:F1105–F1113.  https://doi.org/10.1152/ajprenal.00663.2010 CrossRefGoogle Scholar
  84. 84.
    Orozco-Solis R, Sassone-Corsi P (2014) Circadian clock: linking epigenetics to aging. Curr Opin Genet Dev 26:66–72.  https://doi.org/10.1016/j.gde.2014.06.003 CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Ou SY, Kempson SA, Dousa TP (1981) Relationship between rate of gluconeogenesis and content of nicotinamide adenine dinucleotide in renal cortex. Life Sci 29:1195–1202CrossRefPubMedGoogle Scholar
  86. 86.
    Palmer SC, Hayen A, Macaskill P, Pellegrini F, Craig JC, Elder GJ, Strippoli GF (2011) Serum levels of phosphorus, parathyroid hormone, and calcium and risks of death and cardiovascular disease in individuals with chronic kidney disease: a systematic review and meta-analysis. Jama 305:1119–1127.  https://doi.org/10.1001/jama.2011.308 CrossRefPubMedGoogle Scholar
  87. 87.
    Palmese S, Pezza M, De Robertis E (2005) Hypophosphatemia and metabolic acidosis. Minerva Anestesiol 71:237–242PubMedGoogle Scholar
  88. 88.
    Pirinen E, Canto C, Jo YS, Morato L, Zhang H, Menzies KJ, Williams EG, Mouchiroud L, Moullan N, Hagberg C, Li W, Timmers S, Imhof R, Verbeek J, Pujol A, van Loon B, Viscomi C, Zeviani M, Schrauwen P, Sauve AA, Schoonjans K, Auwerx J (2014) Pharmacological inhibition of poly(ADP-ribose) polymerases improves fitness and mitochondrial function in skeletal muscle. Cell Metab 19:1034–1041.  https://doi.org/10.1016/j.cmet.2014.04.002 CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Pomposelli JJ, Pomfret EA, Burns DL, Lally A, Sorcini A, Gordon FD, Lewis WD, Jenkins R (2001) Life-threatening hypophosphatemia after right hepatic lobectomy for live donor adult liver transplantation. Liver Trans 7:637–642.  https://doi.org/10.1053/jlts.2001.26287 CrossRefGoogle Scholar
  90. 90.
    Portale AA, Halloran BP, Morris RC Jr (1987) Dietary intake of phosphorus modulates the circadian rhythm in serum concentration of phosphorus. Implications for the renal production of 1,25-dihydroxyvitamin D. J Clin Invest 80:1147–1154.  https://doi.org/10.1172/JCI113172 CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    Pronicka E, Ciara E, Halat P, Janiec A, Wojcik M, Rowinska E, Rokicki D, Pludowski P, Wojciechowska E, Wierzbicka A, Ksiazyk JB, Jacoszek A, Konrad M, Schlingmann KP, Litwin M (2017) Biallelic mutations in CYP24A1 or SLC34A1 as a cause of infantile idiopathic hypercalcemia (IIH) with vitamin D hypersensitivity: molecular study of 11 historical IIH cases. J Appl Genet 58:349–353.  https://doi.org/10.1007/s13353-017-0397-2 CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Radanovic T, Wagner CA, Murer H, Biber J (2005) 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.  https://doi.org/10.1152/ajpgi.00167.2004 CrossRefPubMedGoogle Scholar
  93. 93.
    Ramsey KM, Yoshino J, Brace CS, Abrassart D, Kobayashi Y, Marcheva B, Hong HK, Chong JL, Buhr ED, Lee C, Takahashi JS, Imai S, Bass J (2009) Circadian clock feedback cycle through NAMPT-mediated NAD+ biosynthesis. Science 324:651–654.  https://doi.org/10.1126/science.1171641 CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Revollo JR, Grimm AA, Imai S (2004) The NAD biosynthesis pathway mediated by nicotinamide phosphoribosyltransferase regulates Sir2 activity in mammalian cells. J Biol Chem 279:50754–50763.  https://doi.org/10.1074/jbc.M408388200 CrossRefPubMedGoogle Scholar
  95. 95.
    Revollo JR, Korner A, Mills KF, Satoh A, Wang T, Garten A, Dasgupta B, Sasaki Y, Wolberger C, Townsend RR, Milbrandt J, Kiess W, Imai S (2007) Nampt/PBEF/Visfatin regulates insulin secretion in beta cells as a systemic NAD biosynthetic enzyme. Cell Metab 6:363–375.  https://doi.org/10.1016/j.cmet.2007.09.003 CrossRefPubMedPubMedCentralGoogle Scholar
  96. 96.
    Sabbagh Y, O'Brien SP, Song W, Boulanger JH, Stockmann A, Arbeeny C, Schiavi SC (2009) Intestinal npt2b plays a major role in phosphate absorption and homeostasis. J Am Soc Nephrol : JASN 20:2348–2358.  https://doi.org/10.1681/ASN.2009050559 CrossRefPubMedGoogle Scholar
  97. 97.
    Salem RR, Tray K (2005) Hepatic resection-related hypophosphatemia is of renal origin as manifested by isolated hyperphosphaturia. Ann Surg 241:343–348CrossRefPubMedPubMedCentralGoogle Scholar
  98. 98.
    Sampathkumar K, Selvam M, Sooraj YS, Gowthaman S, Ajeshkumar RN (2006) Extended release nicotinic acid - a novel oral agent for phosphate control. Int Urol Nephrol 38:171–174.  https://doi.org/10.1007/s11255-006-0001-x CrossRefPubMedGoogle Scholar
  99. 99.
    Sampathkumar K, Sooraj YS, Ajeshkumar RP (2006) Extended release nicotinic acid is a promising agent for phosphate control in hemodialysis. Kidney Int 69:1281.  https://doi.org/10.1038/sj.ki.5000258 CrossRefPubMedGoogle Scholar
  100. 100.
    Schiavi SC, Tang W, Bracken C, O'Brien SP, Song W, Boulanger J, Ryan S, Phillips L, Liu S, Arbeeny C, Ledbetter S, Sabbagh Y (2012) Npt2b deletion attenuates hyperphosphatemia associated with CKD. J Am Soc Nephrol : JASN 23:1691–1700.  https://doi.org/10.1681/ASN.2011121213 CrossRefPubMedGoogle Scholar
  101. 101.
    Schlingmann KP, Kaufmann M, Weber S, Irwin A, Goos C, John U, Misselwitz J, Klaus G, Kuwertz-Broking E, Fehrenbach H, Wingen AM, Guran T, Hoenderop JG, Bindels RJ, Prosser DE, Jones G, Konrad M (2011) Mutations in CYP24A1 and idiopathic infantile hypercalcemia. N Engl J Med 365:410–421.  https://doi.org/10.1056/NEJMoa1103864 CrossRefGoogle Scholar
  102. 102.
    Schlingmann KP, Ruminska J, Kaufmann M, Dursun I, Patti M, Kranz B, Pronicka E, Ciara E, Akcay T, Bulus D, Cornelissen EA, Gawlik A, Sikora P, Patzer L, Galiano M, Boyadzhiev V, Dumic M, Vivante A, Kleta R, Dekel B, Levtchenko E, Bindels RJ, Rust S, Forster IC, Hernando N, Jones G, Wagner CA, Konrad M (2016) Autosomal-recessive mutations in SLC34A1 encoding sodium-phosphate cotransporter 2A cause idiopathic infantile hypercalcemia. J Am Soc Nephrol : JASN 27:604–614.  https://doi.org/10.1681/ASN.2014101025 CrossRefPubMedGoogle Scholar
  103. 103.
    Segawa H, Kaneko I, Yamanaka S, Ito M, Kuwahata M, Inoue Y, Kato S, Miyamoto K (2004) Intestinal Na-P(i) cotransporter adaptation to dietary P(i) content in vitamin D receptor null mice. Am J Physiol Ren Physiol 287:F39–F47.  https://doi.org/10.1152/ajprenal.00375.2003 CrossRefGoogle Scholar
  104. 104.
    Segawa H, Onitsuka A, Furutani J, Kaneko I, Aranami F, Matsumoto N, Tomoe Y, Kuwahata M, Ito M, Matsumoto M, Li M, Amizuka N, Miyamoto K (2009) Npt2a and Npt2c in mice play distinct and synergistic roles in inorganic phosphate metabolism and skeletal development. Am J Physiol Ren Physiol 297:F671–F678.  https://doi.org/10.1152/ajprenal.00156.2009 CrossRefGoogle Scholar
  105. 105.
    Segawa H, Onitsuka A, Kuwahata M, Hanabusa E, Furutani J, Kaneko I, Tomoe Y, Aranami F, Matsumoto N, Ito M, Matsumoto M, Li M, Amizuka N, Miyamoto K (2009) Type IIc sodium-dependent phosphate transporter regulates calcium metabolism. J Am Soc Nephrol : JASN 20:104–113.  https://doi.org/10.1681/ASN.2008020177 CrossRefPubMedGoogle Scholar
  106. 106.
    Shimoda K, Akiba T, Matsushima T, Rai T, Abe K, Hoshino M (1998) Niceritrol decreases serum phosphate levels in chronic hemodialysis patients. Nihon Jinzo Gakkai shi 40:1–7PubMedGoogle Scholar
  107. 107.
    Shinoda H, Seto H (1985) Diurnal rhythms in calcium and phosphate metabolism in rodents and their relations to lighting and feeding schedules. Miner Electrolyte Metab 11:158–166PubMedGoogle Scholar
  108. 108.
    Sim JJ, Bhandari SK, Smith N, Chung J, Liu IL, Jacobsen SJ, Kalantar-Zadeh K (2013) Phosphorus and risk of renal failure in subjects with normal renal function. Am J Med 126:311–318.  https://doi.org/10.1016/j.amjmed.2012.08.018 CrossRefPubMedGoogle Scholar
  109. 109.
    Suzuki S, Egi M, Schneider AG, Bellomo R, Hart GK, Hegarty C (2013) Hypophosphatemia in critically ill patients. J Crit Care 28(536):e539–e519.  https://doi.org/10.1016/j.jcrc.2012.10.011 CrossRefGoogle Scholar
  110. 110.
    Takahashi Y, Tanaka A, Nakamura T, Fukuwatari T, Shibata K, Shimada N, Ebihara I, Koide H (2004) Nicotinamide suppresses hyperphosphatemia in hemodialysis patients. Kidney Int 65:1099–1104.  https://doi.org/10.1111/j.1523-1755.2004.00482.x CrossRefPubMedGoogle Scholar
  111. 111.
    Tatsumi S, Miyagawa A, Kaneko I, Shiozaki Y, Segawa H, Miyamoto K (2016) Regulation of renal phosphate handling: inter-organ communication in health and disease. J Bone Miner Metab 34:1–10.  https://doi.org/10.1007/s00774-015-0705-z CrossRefPubMedGoogle Scholar
  112. 112.
    Tenenhouse HS, Chu YL (1982) Hydrolysis of nicotinamide-adenine dinucleotide by purified renal brush-border membranes. Mechanism of NAD+ inhibition of brush-border membrane phosphate-transport activity. Biochem J 204:635–638CrossRefPubMedPubMedCentralGoogle Scholar
  113. 113.
    Tonelli M, Sacks F, Pfeffer M, Gao Z, Curhan G (2005) Relation between serum phosphate level and cardiovascular event rate in people with coronary disease. Circulation 112:2627–2633.  https://doi.org/10.1161/CIRCULATIONAHA.105.553198 CrossRefPubMedGoogle Scholar
  114. 114.
    Tran MT, Zsengeller ZK, Berg AH, Khankin EV, Bhasin MK, Kim W, Clish CB, Stillman IE, Karumanchi SA, Rhee EP, Parikh SM (2016) PGC1alpha drives NAD biosynthesis linking oxidative metabolism to renal protection. Nature 531:528–532.  https://doi.org/10.1038/nature17184 CrossRefPubMedPubMedCentralGoogle Scholar
  115. 115.
    Verdin E (2015) NAD(+) in aging, metabolism, and neurodegeneration. Science 350:1208–1213.  https://doi.org/10.1126/science.aac4854 CrossRefGoogle Scholar
  116. 116.
    Wagner CA, Rubio-Aliaga I, Hernando N (2017) Renal phosphate handling and inherited disorders of phosphate reabsorption: an update. Pediatr Nephrol.  https://doi.org/10.1007/s00467-017-3873-3
  117. 117.
    Wang T, Zhang X, Bheda P, Revollo JR, Imai S, Wolberger C (2006) Structure of Nampt/PBEF/visfatin, a mammalian NAD+ biosynthetic enzyme. Nat Struct Mol Biol 13:661–662.  https://doi.org/10.1038/nsmb1114 CrossRefPubMedGoogle Scholar
  118. 118.
    Weinman EJ, Lederer ED (2012) PTH-mediated inhibition of the renal transport of phosphate. Exp Cell Res 318:1027–1032.  https://doi.org/10.1016/j.yexcr.2012.02.037 CrossRefPubMedPubMedCentralGoogle Scholar
  119. 119.
    Woller A, Duez H, Staels B, Lefranc M (2016) A mathematical model of the liver circadian clock linking feeding and fasting cycles to clock function. Cell Rep 17:1087–1097.  https://doi.org/10.1016/j.celrep.2016.09.060 CrossRefPubMedGoogle Scholar
  120. 120.
    Xu H, Bai L, Collins JF, Ghishan FK (2002) Age-dependent regulation of rat intestinal type IIb sodium-phosphate cotransporter by 1,25-(OH)(2) vitamin D. Am J Physiol Cell Physiol 282(3):C487–C493.  https://doi.org/10.1152/ajpcell.00412.2001 CrossRefGoogle Scholar
  121. 121.
    Yamaguchi S, Yoshino J (2017) Adipose tissue NAD(+) biology in obesity and insulin resistance: from mechanism to therapy. BioEssays 39.  https://doi.org/10.1002/bies.201600227 CrossRefGoogle Scholar
  122. 122.
    Yamamoto T, Michigami T, Aranami F, Segawa H, Yoh K, Nakajima S, Miyamoto K, Ozono K (2007) Hereditary hypophosphatemic rickets with hypercalciuria: a study for the phosphate transporter gene type IIc and osteoblastic function. J Bone Miner Metab 25:407–413.  https://doi.org/10.1007/s00774-007-0776-6 CrossRefPubMedGoogle Scholar
  123. 123.
    Yang SJ, Choi JM, Kim L, Park SE, Rhee EJ, Lee WY, Oh KW, Park SW, Park CY (2014) Nicotinamide improves glucose metabolism and affects the hepatic NAD-sirtuin pathway in a rodent model of obesity and type 2 diabetes. J Nutr Biochem 25:66–72.  https://doi.org/10.1016/j.jnutbio.2013.09.004 CrossRefPubMedGoogle Scholar
  124. 124.
    Yoshino J, Mills KF, Yoon MJ, Imai S (2011) Nicotinamide mononucleotide, a key NAD(+) intermediate, treats the pathophysiology of diet- and age-induced diabetes in mice. Cell Metab 14:528–536.  https://doi.org/10.1016/j.cmet.2011.08.014 CrossRefPubMedPubMedCentralGoogle Scholar
  125. 125.
    Zheng J, Glezerman IG, Sadot E, McNeil A, Zarama C, Gonen M, Creasy J, Pak LM, Balachandran VP, D'Angelica MI, Allen PJ, DeMatteo RP, Kingham TP, Jarnagin WR, Jaimes EA (2017) Hypophosphatemia after hepatectomy or pancreatectomy: role of the nicotinamide Phosphoribosyltransferase. J Am Coll Surg 225(488–497 e482):488–497.e2.  https://doi.org/10.1016/j.jamcollsurg.2017.06.012 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Sawako Tatsumi
    • 1
    • 2
  • Kanako Katai
    • 3
  • Ichiro Kaneko
    • 1
  • Hiroko Segawa
    • 1
  • Ken-ichi Miyamoto
    • 1
  1. 1.Department of Molecular Nutrition, Institution of Biomedical ScienceTokushima University Graduate SchoolTokushimaJapan
  2. 2.Department of Food Science and Nutrition, School of Human CulturesThe University of Shiga PrefectureHikoneJapan
  3. 3.Faculty of Human Life and Science, Department of Food Science and NutritionDoshisha Women’s College of Liberal ArtsKyotoJapan

Personalised recommendations