Gitelman-Like Syndrome Caused by Pathogenic Variants in mtDNA.
Adolescent
Adult
Aged
Base Sequence
Child
Child, Preschool
DNA, Mitochondrial
/ genetics
Female
Genotype
Gitelman Syndrome
/ genetics
HEK293 Cells
Humans
Infant
Kidney
/ metabolism
Male
Middle Aged
Mitochondria
/ metabolism
Models, Biological
Mutation
Nucleic Acid Conformation
Pedigree
Phenotype
Polymorphism, Single Nucleotide
RNA, Transfer, Ile
/ chemistry
RNA, Transfer, Phe
/ chemistry
Solute Carrier Family 12, Member 3
/ genetics
Young Adult
Gitelman-s syndrome
Na transport
blood pressure
chronic kidney disease
chronic kidney failure
epithelial sodium transport
genetic renal disease
human genetics
ion transport
mitochondria
Journal
Journal of the American Society of Nephrology : JASN
ISSN: 1533-3450
Titre abrégé: J Am Soc Nephrol
Pays: United States
ID NLM: 9013836
Informations de publication
Date de publication:
02 2022
02 2022
Historique:
received:
03
05
2021
accepted:
06
09
2021
pubmed:
6
10
2021
medline:
5
3
2022
entrez:
5
10
2021
Statut:
ppublish
Résumé
Gitelman syndrome is the most frequent hereditary salt-losing tubulopathy characterized by hypokalemic alkalosis and hypomagnesemia. Gitelman syndrome is caused by biallelic pathogenic variants in We identified mitochondrial DNA (mtDNA) variants in three families with Gitelman-like electrolyte abnormalities, then investigated 156 families for variants in Genetic investigations revealed four mtDNA variants in 13 families: m.591C>T ( Pathogenic mtDNA variants in
Sections du résumé
BACKGROUND
Gitelman syndrome is the most frequent hereditary salt-losing tubulopathy characterized by hypokalemic alkalosis and hypomagnesemia. Gitelman syndrome is caused by biallelic pathogenic variants in
METHODS
We identified mitochondrial DNA (mtDNA) variants in three families with Gitelman-like electrolyte abnormalities, then investigated 156 families for variants in
RESULTS
Genetic investigations revealed four mtDNA variants in 13 families: m.591C>T (
CONCLUSION
Pathogenic mtDNA variants in
Identifiants
pubmed: 34607911
pii: 00001751-202202000-00007
doi: 10.1681/ASN.2021050596
pmc: PMC8819995
doi:
Substances chimiques
DNA, Mitochondrial
0
RNA, Transfer, Ile
0
RNA, Transfer, Phe
0
SLC12A3 protein, human
0
Solute Carrier Family 12, Member 3
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
305-325Subventions
Organisme : Department of Health
Pays : United Kingdom
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Cancer Research UK
Pays : United Kingdom
Organisme : Medical Research Council
Pays : United Kingdom
Commentaires et corrections
Type : CommentIn
Informations de copyright
Copyright © 2022 by the American Society of Nephrology.
Références
Simon DB, Nelson-Williams C, Bia MJ, Ellison D, Karet FE, Molina AM, et al.: Gitelman’s variant of Bartter’s syndrome, inherited hypokalaemic alkalosis, is caused by mutations in the thiazide-sensitive Na-Cl cotransporter. Nat Genet 12: 24–30, 1996
Blanchard A, Bockenhauer D, Bolignano D, Calò LA, Cosyns E, Devuyst O, et al.: Gitelman syndrome: consensus and guidance from a Kidney Disease: Improving Global Outcomes (KDIGO) Controversies Conference. Kidney Int 91: 24–33, 2017
Vargas-Poussou R, Dahan K, Kahila D, Venisse A, Riveira-Munoz E, Debaix H, et al.: Spectrum of mutations in Gitelman syndrome. J Am Soc Nephrol 22: 693–703, 2011
Downie ML, Lopez Garcia SC, Kleta R, Bockenhauer D: Inherited tubulopathies of the kidney: insights from genetics. Clin J Am Soc Nephrol 16: 620–630, 2020
Viering DHHM, de Baaij JHF, Walsh SB, Kleta R, Bockenhauer D: Genetic causes of hypomagnesemia, a clinical overview. Pediatr Nephrol 32: 1123–1135, 2017
van der Made CI, Hoorn EJ, de la Faille R, Karaaslan H, Knoers NV, Hoenderop JG, et al.: Hypomagnesemia as first clinical manifestation of ADTKD-HNF1B: a case series and literature review. Am J Nephrol 42: 85–90, 2015
Chinnery PF: Primary Mitochondrial disorders overview. In: GeneReviews®, edited by Adam MP AH, Pagon RA, et al.: Seattle, Washington, University of Washington, 2000
Goto Y, Itami N, Kajii N, Tochimaru H, Endo M, Horai S: Renal tubular involvement mimicking Bartter syndrome in a patient with Kearns-Sayre syndrome. J Pediatr 116: 904–910, 1990
Wilson FH, Hariri A, Farhi A, Zhao H, Petersen KF, Toka HR, et al.: A cluster of metabolic defects caused by mutation in a mitochondrial tRNA. Science 306: 1190–1194, 2004
Giordano C, Powell H, Leopizzi M, De Curtis M, Travaglini C, Sebastiani M, et al.: Fatal congenital myopathy and gastrointestinal pseudo-obstruction due to POLG1 mutations. Neurology 72: 1103–1105, 2009
Zhou Y, Zhong C, Yang Q, Zhang G, Yang H, Li Q, et al.: Novel SARS2 variants identified in a Chinese girl with HUPRA syndrome. Mol Genet Genomic Med 9: e1650, 2021
Connor TM, Hoer S, Mallett A, Gale DP, Gomez-Duran A, Posse V, et al.: Mutations in mitochondrial DNA causing tubulointerstitial kidney disease. PLoS Genet 13: e1006620, 2017
Li H, Durbin R: Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26: 589–595, 2010
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al.; 1000 Genome Project Data Processing Subgroup: The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078–2079, 2009
Martin AR, Williams E, Foulger RE, Leigh S, Daugherty LC, Niblock O, et al.: PanelApp crowdsources expert knowledge to establish consensus diagnostic gene panels. Nat Genet 51: 1560–1565, 2019
Ekici AB, Hackenbeck T, Morinière V, Pannes A, Buettner M, Uebe S, et al.: Renal fibrosis is the common feature of autosomal dominant tubulointerstitial kidney diseases caused by mutations in mucin 1 or uromodulin. Kidney Int 86: 589–599, 2014
Yarham JW, McFarland R, Taylor RW, Elson JL: A proposed consensus panel of organisms for determining evolutionary conservation of mt-tRNA point mutations. Mitochondrion 12: 533–538, 2012
Wong LC, Chen T, Wang J, Tang S, Schmitt ES, Landsverk M, et al.: Interpretation of mitochondrial tRNA variants. Genet Med 22: 917–926, 2020
Ellard S, Baple E, Callaway A, Berry I, Forrester N, Turnbull C, et al.: ACGS Best Practice Guidelines for Variant Classification in Rare Disease 2020, ACGS, 2020. Accessed March 1, 2021.
Bech AP, Wetzels JFM, Nijenhuis T: Reference values of renal tubular function tests are dependent on age and kidney function. Physiol Rep 5: e13542, 2017
Colussi G, Bettinelli A, Tedeschi S, De Ferrari ME, Syrén ML, Borsa N, et al.: A thiazide test for the diagnosis of renal tubular hypokalemic disorders. Clin J Am Soc Nephrol 2: 454–460, 2007
Rodenburg RJT: Biochemical diagnosis of mitochondrial disorders. J Inherit Metab Dis 34: 283–292, 2011
Panneman DM, Wortmann SB, Haaxma CA, van Hasselt PM, Wolf NI, Hendriks Y, et al.: Variants in NGLY1 lead to intellectual disability, myoclonus epilepsy, sensorimotor axonal polyneuropathy and mitochondrial dysfunction. Clin Genet 97: 556–566, 2020
Yépez VA, Kremer LS, Iuso A, Gusic M, Kopajtich R, Koňaříková E, et al.: OCR-Stats: robust estimation and statistical testing of mitochondrial respiration activities using Seahorse XF Analyzer. PLoS One 13: e0199938, 2018
Pedersen NB, Hofmeister MV, Rosenbaek LL, Nielsen J, Fenton RA: Vasopressin induces phosphorylation of the thiazide-sensitive sodium chloride cotransporter in the distal convoluted tubule. Kidney Int 78: 160–169, 2010
Ashton EJ, Legrand A, Benoit V, Roncelin I, Venisse A, Zennaro MC, et al.: Simultaneous sequencing of 37 genes identified causative mutations in the majority of children with renal tubulopathies. Kidney Int 93: 961–967, 2018
World Health Organization: Global Status Report on Noncommunicable Diseases 2014, 2014. Available at: http://apps.who.int/iris/bitstream/handle/10665/148114/9789241564854_eng.pdf;jsessionid=51B6533AF532336F82399400471FA2AD?sequence=1 . Accessed July 12, 2021.
World Health Organization: Global Health Risks: Mortality and Burden of Disease Attributable to Selected Major Risks, 2009. Available at: https://www.who.int/healthinfo/global_burden_disease/GlobalHealthRisks_report_full.pdf .. Accessed July 12, 2021.
Walsh PR, Tse Y, Ashton E, Iancu D, Jenkins L, Bienias M, et al.: Clinical and diagnostic features of Bartter and Gitelman syndromes. Clin Kidney J 11: 302–309, 2018
, et al. Kidney Disease: Improving Global Outcomes: Autosomal dominant tubulointerstitial kidney disease: Diagnosis, classification, and management. https://kdigo.org/wp-content/uploads/2017/02/KDIGO_ADTKD-2015.pdf. Accessed March 15, 2021
Kunz WS, Kudin A, Vielhaber S, Elger CE, Attardi G, Villani G: Flux control of cytochrome c oxidase in human skeletal muscle. J Biol Chem 275: 27741–27745, 2000
Gnaiger E: Mitochondrial Pathways and Respiratory Control: An Introduction to OXPHOS Analysis. Mitochondr Physiol Network 19.12, Innsbruck, OROBOROS MiPNet Publications, 2014
Reilly RF, Ellison DH: Mammalian distal tubule: Physiology, pathophysiology, and molecular anatomy. Physiol Rev 80: 277–313, 2000
Belostotsky R, Ben-Shalom E, Rinat C, Becker-Cohen R, Feinstein S, Zeligson S, et al.: Mutations in the mitochondrial seryl-tRNA synthetase cause hyperuricemia, pulmonary hypertension, renal failure in infancy and alkalosis, HUPRA syndrome. Am J Hum Genet 88: 193–200, 2011
Hanna MG, Nelson IP, Morgan-Hughes JA, Wood NW: MELAS: A new disease associated mitochondrial DNA mutation and evidence for further genetic heterogeneity. J Neurol Neurosurg Psychiatry 65: 512–517, 1998
Goto Y, Nonaka I, Horai S: A mutation in the tRNA(Leu)(UUR) gene associated with the MELAS subgroup of mitochondrial encephalomyopathies. Nature 348: 651–653, 1990
Melone MA, Tessa A, Petrini S, Lus G, Sampaolo S, di Fede G, et al.: Revelation of a new mitochondrial DNA mutation (G12147A) in a MELAS/MERFF phenotype. Arch Neurol 61: 269–272, 2004
Giordano C, Perli E, Orlandi M, Pisano A, Tuppen HA, He L, et al.: Cardiomyopathies due to homoplasmic mitochondrial tRNA mutations: Morphologic and molecular features. Hum Pathol 44: 1262–1270, 2013
Cox R, Platt J, Chen LC, Tang S, Wong LJ, Enns GM: Leigh syndrome caused by a novel m.4296G>A mutation in mitochondrial tRNA isoleucine. Mitochondrion 12: 258–261, 2012
Gutiérrez Cortés N, Pertuiset C, Dumon E, Börlin M, Hebert-Chatelain E, Pierron D, et al.: Novel mitochondrial DNA mutations responsible for maternally inherited nonsyndromic hearing loss. Hum Mutat 33: 681–689, 2012
Schaller A, Desetty R, Hahn D, Jackson CB, Nuoffer JM, Gallati S, et al.: Impairment of mitochondrial tRNAIle processing by a novel mutation associated with chronic progressive external ophthalmoplegia. Mitochondrion 11: 488–496, 2011
Tzen C-Y, Tsai J-D, Wu T-Y, Chen B-F, Chen M-L, Lin S-P, et al.: Tubulointerstitial nephritis associated with a novel mitochondrial point mutation. Kidney Int 59: 846–854, 2001
D’Aco KE, Manno M, Clarke C, Ganesh J, Meyers KE, Sondheimer N: Mitochondrial tRNA(Phe) mutation as a cause of end-stage renal disease in childhood. Pediatr Nephrol 28: 515–519, 2013
Lorenz R, Ahting U, Betzler C, Heimering S, Borggrafe I, Lange-Sperandio B: Homoplasmy of the mitochondrial DNA mutation m.616T>C leads to mitochondrial tubulointerstitial kidney disease and encephalopathia. Nephron 144:156-160, 2020
Riedhammer KM, Braunisch MC, Günthner R, Wagner M, Hemmer C, Strom TM, et al.: Exome sequencing and identification of phenocopies in patients with clinically presumed hereditary nephropathies. Am J Kidney Dis 76: 460–470, 2020
Zhang C, Wang L, Zhang J, Su XT, Lin DH, Scholl UI, et al.: KCNJ10 determines the expression of the apical Na-Cl cotransporter (NCC) in the early distal convoluted tubule (DCT1). Proc Natl Acad Sci U S A 111: 11864–11869, 2014
Wang MX, Cuevas CA, Su XT, Wu P, Gao ZX, Lin DH, et al.: Potassium intake modulates the thiazide-sensitive sodium-chloride cotransporter (NCC) activity via the Kir4.1 potassium channel. Kidney Int 93: 893–902, 2018
Terker AS, Zhang C, McCormick JA, Lazelle RA, Zhang C, Meermeier NP, et al.: Potassium modulates electrolyte balance and blood pressure through effects on distal cell voltage and chloride. Cell Metab 21: 39–50, 2015
Bockenhauer D, Feather S, Stanescu HC, Bandulik S, Zdebik AA, Reichold M, et al.: Epilepsy, ataxia, sensorineural deafness, tubulopathy, and KCNJ10 mutations. N Engl J Med 360: 1960–1970, 2009
Konrad M, Vollmer M, Lemmink HH, VAN DEN Heuvel LPWJ, Jeck N, Vargas-Poussou R, et al.: Mutations in the chloride channel gene CLCNKB as a cause of classic Bartter syndrome. J Am Soc Nephrol 11: 1449–1459, 2000
Schlingmann KP, Renigunta A, Hoorn EJ, Forst AL, Renigunta V, Atanasov V, et al.: Defects in KCNJ16 cause a novel tubulopathy with hypokalemia, salt wasting, disturbed acid-base homeostasis, and sensorineural deafness. J Am Soc Nephrol 32: 1498–1512, 2021
Cuevas CA, Su X-T, Wang M-X, Terker AS, Lin D-H, McCormick JA, et al.: Potassium sensing by renal distal tubules requires Kir4.1. J Am Soc Nephrol 28: 1814–1825, 2017
Janssen AG, Scholl U, Domeyer C, Nothmann D, Leinenweber A, Fahlke C: Disease-causing dysfunctions of barttin in Bartter syndrome type IV. J Am Soc Nephrol 20: 145–153, 2009
Chen J-C, Lo Y-F, Lin Y-W, Lin S-H, Huang C-L, Cheng C-J: WNK4 kinase is a physiological intracellular chloride sensor. Proc Natl Acad Sci U S A 116: 4502–4507, 2019
Grimm PR, Coleman R, Delpire E, Welling PA: Constitutively active SPAK causes hyperkalemia by activating NCC and remodeling distal tubules. J Am Soc Nephrol 28: 2597–2606, 2017
Yang S-S, Fang Y-W, Tseng M-H, Chu P-Y, Yu IS, Wu H-C, et al.: Phosphorylation regulates NCC stability and transporter activity in vivo. J Am Soc Nephrol 24: 1587–1597, 2013
Hansell P, Welch WJ, Blantz RC, Palm F: Determinants of kidney oxygen consumption and their relationship to tissue oxygen tension in diabetes and hypertension. Clin Exp Pharmacol Physiol 40: 123–137, 2013
McCormick JA, Ellison DH: Distal convoluted tubule. Compr Physiol 5: 45–98, 2015
Hall AM, Rhodes GJ, Sandoval RM, Corridon PR, Molitoris BA: In vivo multiphoton imaging of mitochondrial structure and function during acute kidney injury. Kidney Int 83: 72–83, 2013
Bagnasco S, Good D, Balaban R, Burg M: Lactate production in isolated segments of the rat nephron. Am J Physiol 248: F522–F526, 1985
Meij IC, Koenderink JB, De Jong JC, De Pont JJ, Monnens LA, Van Den Heuvel LP, et al.: Dominant isolated renal magnesium loss is caused by misrouting of the Na + ,K + -ATPase γ -subunit. Ann N Y Acad Sci 986: 437–443, 2003
Franken GAC, Adella A, Bindels RJM, de Baaij JHF: Mechanisms coupling sodium and magnesium reabsorption in the distal convoluted tubule of the kidney. Acta Physiol (Oxf) 231: e13528, 2021
Geven WB, Monnens LA, Willems HL, Buijs WC, ter Haar BG: Renal magnesium wasting in two families with autosomal dominant inheritance. Kidney Int 31: 1140–1144, 1987
Schlingmann KP, Bandulik S, Mammen C, Tarailo-Graovac M, Holm R, Baumann M, et al.: Germline de novo mutations in ATP1A1 cause renal hypomagnesemia, refractory seizures, and intellectual disability. Am J Hum Genet 103: 808–816, 2018
de Baaij JH, Dorresteijn EM, Hennekam EA, Kamsteeg EJ, Meijer R, Dahan K, et al.: Recurrent FXYD2 p.Gly41Arg mutation in patients with isolated dominant hypomagnesaemia. Nephrol Dial Transplant 30: 952–957, 2015
Adalat S, Hayes WN, Bryant WA, Booth J, Woolf AS, Kleta R, et al.: HNF1B mutations are associated with a Gitelman-like tubulopathy that develops during childhood. Kidney Int Rep 4: 1304–1311, 2019
Kompatscher A, de Baaij JHF, Aboudehen K, Hoefnagels APWM, Igarashi P, Bindels RJM, et al.: Loss of transcriptional activation of the potassium channel Kir5.1 by HNF1 β drives autosomal dominant tubulointerstitial kidney disease. Kidney Int 92: 1145–1156, 2017
Ferrè S, Veenstra GJ, Bouwmeester R, Hoenderop JG, Bindels RJ: HNF-1B specifically regulates the transcription of the γ a-subunit of the Na + /K + -ATPase. Biochem Biophys Res Commun 404: 284–290, 2011
Bech AP, Wetzels JF, Bongers EMHF, Nijenhuis T: Thiazide responsiveness testing in patients with renal magnesium wasting and correlation with genetic analysis: A diagnostic test study. Am J Kidney Dis 68: 168–170, 2016
Nozu K, Iijima K, Kanda K, Nakanishi K, Yoshikawa N, Satomura K, et al.: The pharmacological characteristics of molecular-based inherited salt-losing tubulopathies. J Clin Endocrinol Metab 95: E511–E518, 2010
Jeck N, Konrad M, Peters M, Weber S, Bonzel KE, Seyberth HW: Mutations in the chloride channel gene, CLCNKB, leading to a mixed Bartter-Gitelman phenotype. Pediatr Res 48: 754–758, 2000
Reilly RF, Huang CL: The mechanism of hypocalciuria with NaCl cotransporter inhibition. Nat Rev Nephrol 7: 669–674, 2011
Kovacikova J, Winter C, Loffing-Cueni D, Loffing J, Finberg KE, Lifton RP, et al.: The connecting tubule is the main site of the furosemide-induced urinary acidification by the vacuolar H + -ATPase. Kidney Int 70: 1706–1716, 2006
Roshan M, Kabekkodu SP, Vijaya PH, Manjunath K, Graw J: Analysis of mitochondrial DNA variations in Indian patients with congenital cataract. Mol Vis 18: 181–193, 2012
Elisaf M, Panteli K, Theodorou J, Siamopoulos KC: Fractional excretion of magnesium in normal subjects and in patients with hypomagnesemia. Magnes Res 10: 315–320, 1997