Familial hypomagnesaemia with hypercalciuria and nephrocalcinosis: Clinical and molecular characteristics

Clinical Kidney Journal

Volumn 8, Issue 6, 2015, Pages 656-664

  Claverie Martin, Felix ^a  

^a HOSPITAL UNIVERSITARIO NUESTRA SEÑORA DE CANDELARIA   (Spain)

Author keywords

Claudin 16; Claudin 19; Genetic disease; Magnesium; Renal tubulopathy

Indexed keywords

CALCIUM; CLAUDIN; CLAUDIN 16; CLAUDIN 19; MAGNESIUM; MOLECULAR MARKER; THIAZIDE DIURETIC AGENT; UNCLASSIFIED DRUG; VITAMIN D;

CHRONIC KIDNEY FAILURE; CLINICAL FEATURE; COLOBOMA; END STAGE RENAL DISEASE; FAMILIAL HYPOMAGNESAEMIA WITH HYPERCALCIURIA AND NEPHROCALCINOSIS; GENE MUTATION; HUMAN; HYPOCALCIURIA; KIDNEY CALCIFICATION; KIDNEY TRANSPLANTATION; KIDNEY TUBULE DISORDER; MACULAR COLOBAMATA; MAGNESIUM BLOOD LEVEL; MYOPIA; NERVE CELL; NONHUMAN; NYSTAGMUS; PATHOPHYSIOLOGY; PIGMENT EPITHELIUM; PRIORITY JOURNAL; RARE DISEASE; REVIEW;

EID: 84959375565     PISSN: 20488505     EISSN: 20488513     Source Type: Journal    
DOI: 10.1093/ckj/sfv081     Document Type: Review

References (86)

1. Jahnen-Dechent W, Ketteler M. Magnesium basics. Clin Kidney 2012; 5(Suppl 1): i3-i14
2. deBaaij JH, Hoenderop JG, Bindels RJ. Magnesiuminman: implications for health and disease. Physiol Rev 2015; 95: 1-46
3. de Baaij JH, Hoenderop JG, Bindels RJ. Regulation of magnesium balance: lessons learned from human genetic diseases. Clin Kidney J 2012; 5(Suppl 1): i15-i24
4. Konrad M, Schlingmann KP. Inherited disorders of renal hypomagnesaemia. Nephrol Dial Transplant 2014; 29(Suppl 4): iv63-iv71
5. Michelis MF, Drash AL, Linarelli LG et al. Decreased bicarbonate threshold and renal magnesiumwastinginasibship with distal renal tubular acidosis. (Evaluation of the pathophysio-logical role of parathyroid hormone). Metabolism 1972; 21: 905-920
6. Manz F, Schärer K, Janka P et al. Renal magnesium wasting, incomplete tubular acidosis, hypercalciuria and nephrocalci-nosis in siblings. Eur J Pediatr 1978; 128: 67-79
7. Ulmann A, Hadj S, Lacour B et al. Renal magnesium and phosphate wastage in a patient with hypercalciuria and nephro-calcinosis: effect of oral phosphorus and magnesium supplements. Nephron 1985; 40: 83-87
8. Rodríguez-Soriano J, Vallo A, García-Fuentes M. Hypomag-nesaemia of hereditary renal origin. Pediatr Nephrol 1987; 1: 465-472
9. Nicholson JC, Jones CL, Powell HR et al. Familial hypomagnes-aemia-hypercalciuria leading to end-stage renal failure. Pediatr Nephrol 1995; 9: 74-76
10. Praga M, Vara J, González-Parra E et al. Familial hypomagnes-emia with hypercalciuria and nephrocalcinosis. Kidney Int 1995; 47: 1419-1425
11. Cole DE, Quamme GA. Inherited disorders of renal magnesium handling. J Am Soc Nephrol 2000; 11: 1937-1947.
12. Mount DB. Thick ascending limb of the loop of Henle. Clin J Am Soc Nephrol 2014; 9: 1974-1986.
13. 2+ resorption. Science 1999; 285: 103-106
14. Konrad M, Schaller A, Seelow D et al. 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 2006; 79: 949-957
15. Günzel D, Yu AS. Claudins and the modulation of tight junction permeability. Physiol Rev 2013; 93: 525-569
16. Benigno V, Canonica CS, Bettinelli A et al. Hypomagnes-aemia-hypercalciuria-nephrocalcinosis: a report of nine cases and a review. Nephrol Dial Transplant 2000; 15: 605-610
17. Weber S, Schneider L, Peters M et al. Novel paracellin-1 mutations in 25 families with familial hypomagnesemia with hy-percalciuria and nephrocalcinosis. J Am Soc Nephrol 2001; 12: 1872-1881
18. Blanchard A, Jeunemaitre X, Coudol P et al. Paracellin-1is critical for magnesium and calcium reabsorption in the human thick ascending limb of Henle. Kidney Int 2001; 59: 2206-2215
19. Godron A, Harambat J, Boccio V et al. Familial hypomagnes-emia with hypercalciuria and nephrocalcinosis: phenotype-genotype correlation and outcome in 32 patients with CLDN16 or CLDN19 mutations. Clin J Am Soc Nephrol 2012; 7: 801-809
20. Weber S, Hoffmann K, Jeck N et al. Familial hypomagnes-aemia with hypercalciuria and nephrocalcinosis maps to chromosome 3q27 and is associated with mutations in the PCLN-1 gene. Eur J Hum Genet 2000; 8: 414-422
21. Tajima T, Nakae J, Fujieda K. Two heterozygous mutations of CLDN16 in a Japanese patient with FHHNC. Pediatr Nephrol 2003; 18: 1280-1282
22. Müller D, Kausalya PJ, Claverie-Martin F et al. A novel claudin 16 mutation associated with childhood hypercalciuria abolishes binding to ZO-1 and results in lysosomal mistar-geting. Am J Hum Genet 2003; 73: 1293-1301
23. Müller D, Kausalya PJ, Bockenhauer D et al. Unusual clinical presentation and possible rescueofa novel claudin-16 mutation. J Clin Endocrinol Metab 2006; 91: 3076-3079
24. Müller D, Kausalya PJ, Meij IC et al. Familial hypomagnesemia with hypercalciuria and nephrocalcinosis: blocking endo-cytosis restores surface expression of a novel Claudin-16 mutant that lacks the entire C-terminal cytosolic tail. Hum Mol Genet 2006; 15: 1049-1058
25. 2+ transport function of Claudin-16. J Clin Invest 2006; 116: 878-891
26. Kang JH, Choi HJ, Cho HY et al. Familial hypomagnesemia with hypercalciuria and nephrocalcinosis associated with CLDN16 mutations. Pediatr Nephrol 2005; 20: 1490-1493
27. Kutluturk F, Temel B, Uslu B et al. An unusual patient with hy-percalciuria, recurrent nephrolithiasis, hypomagnesemia and G227R mutation of Paracellin-1. An unusual patient with hypercalciuria and hypomagnesemia unresponsive to thiazide diuretics. Horm Res 2006; 66: 175-181
28. Sanjad SA, Hariri A, Habbal ZM et al. A novel PCLN-1 gene mutation in familial hypomagnesemia with hypercalciuria and atypical phenotype. Pediatr Nephrol 2007; 22: 503-508
29. Staiger K, Staiger H, Haas C et al. Hypomagnesemia and ne-phrocalcinosisinapatient with two heterozygous mutations in the CLDN16 gene. J Nephrol 2007; 20: 107-110
30. Hampson G, Konrad MA, Scoble J. Familial hypomagnes-aemia with hypercalciuria and nephrocalcinosis (FHHNC): compound heterozygous mutation in the claudin 16 (CLDN16) gene. BMC Nephrol 2008; 9: 12
31. Konrad M, Hou J, Weber S et al. CLDN16 genotype predicts renal decline in familial hypomagnesemia with hypercal-ciuria and nephrocalcinosis. J Am Soc Nephrol 2008; 19: 171-181
32. Guran T, Akcay T, Bereket A et al. Clinical and molecular characterization of Turkish patients with familial hypomagnes-aemia: novel mutations in TRPM6 and CLDN16 genes. Nephrol Dial Transplant 2012; 27: 667-673
33. Kasapkara CS, Tumer L, Okur I et al. A novel mutation of the claudin 16 gene in familial hypomagnesemia with hypercal-ciuria and nephrocalcinosis mimicking rickets. Genet Couns 2011; 22: 187-192
34. Seeley HH, Loomba-Albrecht LA, Nagel M et al. Familial hypo-magnesemia with hypercalciuria and nephrocalcinosis in three siblings having the same genetic lesion but different clinical presentations. World J Pediatr 2012; 8: 177-180
35. Deeb A, Abood SA, Simon J et al. AnovelCLDN16 mutationina large family with familial hypomagnesaemia with hypercal-ciuria and nephrocalcinosis. BMC Res Notes 2013; 6: 527
36. Nadarajah L, Khosravi M, Dumitriu S et al. A novel claudin-16 mutation, severe bone disease, and nephrocalcinosis. Lancet 2014; 383: 98
37. Claverie-Martin F, Garcia-Nieto V, Loris C et al. Claudin-19 mutations and clinical phenotype in Spanish patients with familial hypomagnesemia with hypercalciuria and nephro-calcinosis. PLoS One 2013; 8: e53151
38. Hou J, Renigunta A, Konrad M et al. Claudin-16 and claudin-19 interact and form a cation-selective tight junction complex. J Clin Invest 2008; 118: 619-628
39. Naeem M, Hussain S, Akhtar N. Mutation in the tight-junction gene claudin 19 (CLDN19) and familial hypomagnes-emia, hypercalciuria, nephrocalcinosis (FHHNC) and severe ocular disease. Am J Nephrol 2011; 34: 241-248
40. Ekinci Z, Karabaş L, Konrad M. Hypomagnesemia-hypercal-ciuria-nephrocalcinosis and ocular findings: a new claudin-19 mutation. Turk J Pediatr 2012; 54: 168-170
41. Yuan T, Pang Q, Xing X et al. First report of a novel missense CLDN19 mutations causing familial hypomagnesemia with hypercalciuria and nephrocalcinosis in a Chinese family. Calcif Tissue Int 2015; 96: 265-273
42. Arteaga ME, Hunziker W, Teo AS et al. Familial hypomagnes-emia with hypercalciuria and nephrocalcinosis: variable phenotypic expression in three affected sisters from Mexican ancestry. Ren Fail 2015; 37: 180-183
43. Faguer S, Chauveau D, Cintas P et al. Renal, ocular, and neuro-muscular involvements in patients with CLDN19 mutations. Clin J Am Soc Nephrol 2011; 6: 355-360
44. Schaeffer C, Creatore A, Rampoldi L. Protein trafficking defects in inherited kidney diseases. Nephrol Dial Transplant 2014; 29(Suppl 4): iv33-iv44
45. Claverie-Martin F, Acosta-Herrera M, González-Paredes FJ et al. Missense and synonymous mutations in kidney disease-associated genes can cause mRNA defects. Pediatr Nephrol 2011; 26: 1573
46. Furuse M. Molecular basis of the core structure of tight junctions. Cold Spring Harb Perspect Biol 2010; 2: a002907
47. Mineta K, Yamamoto Y, Yamazaki Y et al. Predicted expansion of the claudin multigene family. FEBS Lett 2011; 585: 606-612
48. Hou J, Paul DL, Goodenough DA. Paracellin-1 and the modulation of ion selectivity of tight junctions. J Cell Sci 2005; 118: 5109-5118
49. Angelow S, El-Husseini R, Kanzawa SA et al. Renal localization and function of the tight junction protein claudin-19. Am J Physiol Renal Physiol 2007; 293: F166-F177
50. Colegio OR, Van Itallie C, Rahner C et al. Claudin extracellular domains determine paracellular charge selectivity and resistance but not tight junction fibril architecture. Am J Physiol Cell Physiol 2003; 284: C1346-C1354
51. Piontek J, Winkler L, Wolburg H et al. Formation of tight junction: determinants of homophilic interaction between classic claudins. FASEB J 2008; 22: 146-158
52. Piehl C, Piontek J, Cording J et al. Participation of the second extracellular loop of claudin-5 in paracellular tightening against ions, small and large molecules. Cell Mol Life Sci 2010; 67: 2131-2140
53. Suzuki H, Nishizawa T, Tani K et al. Crystal structure of aclau-din provides insight into the architecture of tight junctions. Science 2014; 344: 304-307
54. Suzuki H, Tani K, Tamura A et al. Model for the architecture of claudin-based paracellular ion channels through tight junctions. J Mol Biol 2015; 427: 291-297
55. Van Itallie CM, Mitic LL, Anderson JM. Claudin-2 forms homodimers and is a component of a high molecular weight protein complex. J Biol Chem 2011; 286: 3442-3450
56. - secretion in MDCK cells. J Physiol 2009; 587: 3777-3793
57. Van Itallie CM, Colegio OR, Anderson JM. The cytoplasmic tails of claudins can influence tight junction barrier properties through effects on protein stability. J Membr Biol 2004; 199: 29-38
58. Ikari A, Matsumoto S, Harada H et al. Dysfunction of paracel-lin-1 by dephosphorylation in Dahl salt-sensitive hypertensive rats. J Physiol Sci 2006; 56: 379-383
59. Ikari A, Hirai N, Shiroma M et al. Association of paracellin-1 with ZO-1 augments the reabsorption of divalent cations in renal epithelial cells. J Biol Chem 2004; 279: 54826-54832
60. Itoh M, Furuse M, Morita K et al. Direct binding of three tight junction-associated MAGUKs, ZO-1, ZO-2, and ZO-3, with the COOH termini of claudins. J Cell Biol 1999; 147: 1351-1363
61. Lee NP, Tong MK, Leung PP et al. Kidney claudin-19: localization in distal tubules and collecting ducts and dysregulation in polycystic renal disease. FEBS Lett 2006; 580: 923-931
62. Peng S, Adelman RA, Rizzolo LJ. Minimal effects of VEGF and anti-VEGF drugs on the permeability or selectivity of RPE tight junctions. Invest Ophthalmol Vis Sci 2010; 51: 3216-3225.
63. Hou J, Renigunta A, Gomes AS et al. Claudin-16 and claudin-19 interaction is required for their assembly into tight junctions and for renal reabsorption of magnesium. Proc Natl Acad Sci USA 2009; 106: 15350-15355
64. Yu AS. Claudins and the kidney. J Am Soc Nephrol 2015; 26: 11-19
65. Miyamoto T, Morita K, Takemoto D et al. Tight junctions in Schwann cells of peripheral myelinated axons: a lesson from claudin-19-deficient mice. J Cell Biol 2005; 169: 527-538
66. Hou J, Shan Q, Wang T et al. Transgenic RNAi depletion of claudin-16 and the renal handling of magnesium. J Biol Chem 2007; 282: 17114-17122
67. Peng S, Rao VS, Adelman RA et al. Claudin-19 and the barrier properties of the human retinal pigment epithelium. Invest Ophthalmol Vis Sci 2011; 52: 1392-1403
68. Riccardi D, Kemp PJ. The calcium-sensing receptor beyond extracellular calcium homeostasis: conception, development, adult physiology, and disease. Annu Rev Physiol 2012; 74: 271-297
69. ++ transport in response to CaSR signaling via a novel microRNA pathway. EMBO J 2012; 31: 1999-2012
70. Thorleifsson G, Holm H, Edvardsson V et al. Sequence variants in the CLDN14 gene associate with kidney stones and bone mineral density. Nat Genet 2009; 41: 926-930
71. Wilcox ER, Burton QL, Naz S et al. Mutations in the gene encoding tight junction claudin-14 cause autosomal recessive deafness DFNB29. Cell 2001; 104: 165-172
72. ++ metabolism via NFAT-microRNA-based mechanisms. J Am Soc Nephrol 2014; 25: 745-760
73. Toka HR, Al-Romaih K, Koshy JM et al. Deficiency of the calcium-sensing receptor in the kidney causes parathyroid hormone-independent hypocalciuria. J Am Soc Nephrol 2012; 23: 1879-1890
74. Dimke H, Desai P, Borovac J et al. Activation of the Ca(2+)-sensing receptor increases renal claudin-14 expression and urinary Ca(2+) excretion. Am J Physiol Renal Physiol 2013; 304: F761-F769
75. Gong Y, Himmerkus N, Plain A et al. Epigenetic regulation of microRNAs controlling CLDN14 expression as a mechanism for renal calcium handling. J Am Soc Nephrol 2015; 26: 663-676
76. Mulay SR, Kulkarni OP, Rupanagudi KV et al. Calcium oxalate crystals induce renal inflammation by NLRP3-mediated IL-1β secretion. J Clin Invest 2013; 123: 236-246
77. Knauf F, Asplin JR, Granja I et al. NALP3-mediated inflammation is a principal cause of progressive renal failure in oxalate nephropathy. Kidney Int 2013; 84: 895-901
78. Chang A, Ko K, Clark MR. The emerging role of the inflamma-some in kidney diseases. Curr Opin Nephrol Hypertens 2014; 23: 204-210
79. Lee DB, Huang E, Ward HJ. Tight junction biology and kidney dysfunction. Am J Physiol Renal Physiol 2006; 290: F20-F34
80. Hirano T, Kobayashi N, Itoh T et al. Null mutation of PCLN-1/claudin-16 results in bovine chronic interstitial nephritis. Genome Res 2000; 10: 659-663
81. Ohba Y, Kitagawa H, Kitoh K et al. A deletion of the paracellin-1 gene is responsible for renal tubular dysplasia in cattle. Genomics 2000; 68: 229-236
82. Sugiyama A, Ozaki K, Miyazaki et al. Renal dysplasia unrelated to claudin-16 deficiency in Japanese Black cattle. J Comp Pathol 2007; 137: 71-77
83. Sikora P, Zaniew M, Haisch L et al. Retrospective cohort study of familial hypomagnesaemia with hypercalciuria and nephrocalcinosis due to CLDN16 mutations. Nephrol Dial Transplant 2015; 30: 636-644
84. Claverie-Martín F, Vargas-Poussou R, Müller D et al. Clinical utility gene card for: familial hypomagnesemia with hypercalciuria and nephrocalcinosis with/without severe ocular involvement. Eur J Hum Genet 2015; 23: doi:10.1038/ejhg.2014.176
85. Martin-Nuñez E, Cordoba-Lanus E, Gonzalez-Acosta H et al. Haplotype analysis of CLDN19 single nucleotide polymorphisms in Spanish patients with familial hypomagnesemia with hypercalciuria and nephrocalcinosis. World J Pediatr 2015; 11: 272-275
86. Shroff R, Aitkenhead H, Costa N et al. Normal 25-hydroxyvi-tamin D Levels are associated with less proteinuria and attenuate renal failure progression in children with CKD. J Am Soc Nephrol 2015; doi: 10.1681/ASN.2014090947