Basolateral Mg2+ Extrusion via CNNM4 Mediates Transcellular Mg2+ Transport across Epithelia: A Mouse Model

PLoS Genetics

Volumn 9, Issue 12, 2013, Pages

  Yamazaki, Daisuke ^a   Funato, Yosuke ^a   Miura, Jiro ^b   Sato, Sunao ^b   Toyosawa, Satoru ^b   Furutani, Kazuharu ^b   Kurachi, Yoshihisa ^b   Omori, Yoshihiro ^b,c   Furukawa, Takahisa ^b,c   Tsuda, Tetsuya ^b   Kuwabata, Susumu ^b   Mizukami, Shin ^b   Kikuchi, Kazuya ^b   Miki, Hiroaki ^a  

^a OSAKA UNIVERSITY   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN M4; CYCLINE; MAGNESIUM; SODIUM; UNCLASSIFIED DRUG; CATION TRANSPORT PROTEIN; CNNM4 PROTEIN, HUMAN;

AMELOBLAST; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASOLATERAL MEMBRANE; CONTROLLED STUDY; FEMALE; HYPOMAGNESEMIA; INTESTINE ABSORPTION; INTRACELLULAR TRANSPORT; ION EXCHANGE; ION TRANSPORT; MAGNESIUM METABOLISM; MISSENSE MUTATION; MOLECULAR IMAGING; MOUSE; NONHUMAN; POINT MUTATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; TOOTH DEVELOPMENT; AMELOGENESIS IMPERFECTA; ANIMAL; DISEASE MODEL; EPITHELIUM; GENETICS; HUMAN; HYPERTRICHOSIS; KNOCKOUT MOUSE; LEBER CONGENITAL AMAUROSIS; METABOLISM; PATHOLOGY; RETINITIS PIGMENTOSA; TRANSPORT AT THE CELLULAR LEVEL;

AMELOGENESIS IMPERFECTA; ANIMALS; BIOLOGICAL TRANSPORT; CATION TRANSPORT PROTEINS; DISEASE MODELS, ANIMAL; EPITHELIUM; HUMANS; HYPERTRICHOSIS; LEBER CONGENITAL AMAUROSIS; MAGNESIUM; MICE; MICE, KNOCKOUT; MUTATION, MISSENSE; RETINITIS PIGMENTOSA;

EID: 84892689931     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003983     Document Type: Article

References (45)

1. Simon DB, Lu Y, Choate KA, Velazquez H, Al-Sabban E, et al. (1999) Paracellin-1, a renal tight junction protein required for paracellular Mg2+ resorption. Science 285: 103-106.
2. Konrad M, Schaller A, Seelow D, Pandey AV, Waldegger S, et al. (2006) Mutations in the tight-junction gene claudin 19 (CLDN19) are associated with renal magnesium wasting, renal failure, and severe ocular involvement. Am J Hum Genet 79: 949-957.
3. Hou J, Paul DL, Goodenough DA, (2005) Paracellin-1 and the modulation of ion selectivity of tight junctions. J Cell Sci 118: 5109-5118.
4. Schlingmann KP, Weber S, Peters M, Niemann Nejsum L, Vitzthum H, et al. (2002) Hypomagnesemia with secondary hypocalcemia is caused by mutations in TRPM6, a new member of the TRPM gene family. Nat Genet 31: 166-170.
5. Walder RY, Landau D, Meyer P, Shalev H, Tsolia M, et al. (2002) Mutation of TRPM6 causes familial hypomagnesemia with secondary hypocalcemia. Nat Genet 31: 171-174.
6. Voets T, Nilius B, Hoefs S, van der Kemp AW, Droogmans G, et al. (2004) TRPM6 forms the Mg2+ influx channel involved in intestinal and renal Mg2+ absorption. J Biol Chem 279: 19-25.
7. Ryazanova LV, Rondon LJ, Zierler S, Hu Z, Galli J, et al. (2010) TRPM7 is essential for Mg(2+) homeostasis in mammals. Nat Commun 1: 109.
8. Teramoto T, Lambie EJ, Iwasaki K, (2005) Differential regulation of TRPM channels governs electrolyte homeostasis in the C. elegans intestine. Cell Metab 1: 343-354.
9. Teramoto T, Sternick LA, Kage-Nakadai E, Sajjadi S, Siembida J, et al. (2010) Magnesium excretion in C. elegans requires the activity of the GTL-2 TRPM channel. PLoS One 5: e9589.
10. Wang CY, Shi JD, Yang P, Kumar PG, Li QZ, et al. (2003) Molecular cloning and characterization of a novel gene family of four ancient conserved domain proteins (ACDP). Gene 306: 37-44.
11. Meyer TE, Verwoert GC, Hwang SJ, Glazer NL, Smith AV, et al. (2010) Genome-wide association studies of serum magnesium, potassium, and sodium concentrations identify six Loci influencing serum magnesium levels. PLoS Genet 6: e1001045.
12. Stuiver M, Lainez S, Will C, Terryn S, Günzel D, et al. (2011) CNNM2, encoding a basolateral protein required for renal Mg2+ handling, is mutated in dominant hypomagnesemia. Am J Hum Genet 88: 333-343.
13. Gibson MM, Bagga DA, Miller CG, Maguire ME, (1991) Magnesium transport in Salmonella typhimurium: the influence of new mutations conferring Co2+ resistance on the CorA Mg2+ transport system. Mol Microbiol 5: 2753-2762.
14. Goytain A, Quamme GA, (2005) Functional characterization of ACDP2 (ancient conserved domain protein), a divalent metal transporter. Physiol Genomics 22: 382-389.
15. Sponder G, Svidova S, Schweigel M, Vormann J, Kolisek M, (2010) Splice-variant 1 of the ancient domain protein 2 (ACDP2) complements the magnesium-deficient growth phenotype of Salmonella enterica sv. typhimurium strain MM281. Magnes Res 23: 105-114.
16. Parry DA, Mighell AJ, El-Sayed W, Shore RC, Jalili IK, et al. (2009) Mutations in CNNM4 cause Jalili syndrome, consisting of autosomal-recessive cone-rod dystrophy and amelogenesis imperfecta. Am J Hum Genet 84: 266-273.
17. Polok B, Escher P, Ambresin A, Chouery E, Bolay S, et al. (2009) Mutations in CNNM4 cause recessive cone-rod dystrophy with amelogenesis imperfecta. Am J Hum Genet 84: 259-265.
18. de Baaij JH, Stuiver M, Meij IC, Lainez S, Kopplin K, et al. (2012) Membrane topology and intracellular processing of cyclin M2 (CNNM2). J Biol Chem 287: 13644-13655.
19. Casaletto JB, Saotome I, Curto M, McClatchey AI, (2011) Ezrin-mediated apical integrity is required for intestinal homeostasis. Proc Natl Acad Sci USA 108: 11924-11929.
20. Su L, Shen L, Clayburgh DR, Nalle SC, Sullivan EA, et al. (2009) Targeted epithelial tight junction dysfunction causes immune activation and contributes to development of experimental colitis. Gastroenterology 136: 551-563.
21. Kucharski LM, Lubbe WJ, Maguire ME, (2000) Cation hexaammines are selective and potent inhibitors of the CorA magnesium transport system. J Biol Chem 275: 16767-16773.
22. Kolisek M, Launay P, Beck A, Sponder G, Serafini N, et al. (2008) SLC41A1 is a novel mammalian Mg2+ carrier. J Biol Chem 283: 16235-16247.
23. Smith CE, (1998) Cellular and chemical events during enamel maturation. Crit Rev Oral Biol Med 9: 128-161.
24. Inai T, Sengoku A, Hirose E, Iida H, Shibata Y, (2008) Differential expression of the tight junction proteins, claudin-1, claudin-4, occludin, ZO-1, and PAR3, in the ameloblasts of rat upper incisors. Anat Rec 291: 577-585.
25. Meindl A, Dry K, Herrmann K, Manson F, Ciccodicola A, et al. (1996) A gene (RPGR) with homology to the RCC1 guanine nucleotide exchange factor is mutated in X-linked retinitis pigmentosa (RP3). Nat Genet 13: 35-42.
26. Hong DH, Pawlyk BS, Shang J, Sandberg MA, Berson EL, et al. (2000) A retinitis pigmentosa GTPase regulator (RPGR)-deficient mouse model for X-linked retinitis pigmentosa (RP3). Proc Natl Acad Sci USA 97: 3649-3654.
27. Günther T, (2006) Mechanisms, regulation and pathologic significance of Mg2+ efflux from erythrocytes. Magnes Res 19: 190-198.
28. Günther T, (2007) Na+/Mg2+ antiport in non-erythrocyte vertebrate cells. Magnes Res 20: 89-99.
29. Kolisek M, Nestler A, Vormann J, Schweigel-Röntgen M, (2012) Human gene SLC41A1 encodes for the Na+/Mg2+ exchanger. Am J Physiol Cell Physiol 302: C318-326.
30. Wabakken T, Rian E, Kveine M, Aasheim HC, (2003) The human solute carrier SLC41A1 belongs to a novel eukaryotic subfamily with homology to prokaryotic MgtE Mg2+ transporters. Biochem Biophys Res Commun 306: 718-724.
31. Hurd TW, Otto EA, Mishima E, Gee HY, Inoue H, et al. (2013) Mutation of the Mg2+ transporter SLC41A1 results in a nephronophthisis-like phenotype. J Am Soc Nephrol 24: 967-977.
32. Navarro-González JF, Mora-Fernández C, García-Pérez J, (2009) Clinical implications of disordered magnesium homeostasis in chronic renal failure and dialysis. Semin Dial 22: 37-44.
33. Konrad M, Schlingmann KP, Gudermann T, (2004) Insights into the molecular nature of magnesium homeostasis. Am J Physiol Renal Physiol 286: F599-605.
34. Dimke H, Hoenderop JG, Bindels RJ, (2011) Molecular basis of epithelial Ca2+ and Mg2+ transport: insights from the TRP channel family. J Physiol 589: 1535-1542.
35. Jälevik B, Odelius H, Dietz W, Norén J, (2001) Secondary ion mass spectrometry and X-ray microanalysis of hypomineralized enamel in human permanent first molars. Arch Oral Biol 46: 239-247.
36. Itoh M, Yonemura S, Nagafuchi A, Tsukita S, Tsukita S, (1991) 220-kD undercoat-constitutive protein: its specific localization at cadherin-based cell-cell adhesion sites. J Cell Biol 115: 1449-1462.
37. Koike C, Obara T, Uriu Y, Numata T, Sanuki R, et al. (2010) TRPM1 is a component of the retinal ON bipolar cell transduction channel in the mGluR6 cascade. Proc Natl Acad Sci USA 107: 332-337.
38. Omori Y, Chaya T, Katoh K, Kajimura N, Sato S, et al. (2010) Negative regulation of ciliary length by ciliary male germ cell-associated kinase (Mak) is required for retinal photoreceptor survival. Proc Natl Acad Sci USA 107: 22671-22676.
39. Sato S, Omori Y, Katoh K, Kondo M, Kanagawa M, et al. (2008) Pikachurin, a dystroglycan ligand, is essential for photoreceptor ribbon synapse formation. Nat Neurosci 11: 923-931.
40. Fujita T, Hirooka K, Nakamura T, Itano T, Nishiyama A, et al. (2012) Neuroprotective effects of angiotensin II type 1 receptor (AT1-R) blocker via modulating AT1-R signaling and decreased extracellular glutamate levels. Invest Ophthalmol Vis Sci 53: 4099-4110.
41. Hibino H, Kurachi Y, (2007) Distinct detergent-resistant membrane microdomains (lipid rafts) respectively harvest K(+) and water transport systems in brain astroglia. Eur J Neurosci 26: 2539-2555.
42. Günther T, (2006) Concentration, compartmentation and metabolic function of intracellular free Mg2+. Magnes Res 19: 225-236.
43. Schilling T, Eder C, (2004) A novel physiological mechanism of glycine-induced immunomodulation: Na+-coupled amino acid transporter currents in cultured brain macrophages. J Physiol 559: 35-40.
44. Leone FA, Baranauskas JA, Furriel RP, Borin IA, (2005) SigrafW: An easy-to-use program for fitting enzyme kinetic data. Biochem Mol Biol Educ 33: 399-403.
45. Tsuda T, Nemoto N, Kawakami K, Mochizuki E, Kishida S, et al. (2011) SEM observation of wet biological specimens pretreated with room-temperature ionic liquid. Chembiochem 12: 2547-2550.