Update on CD164 and LMX1A genes to strengthen their causative role in autosomal dominant hearing loss.
Journal
Human genetics
ISSN: 1432-1203
Titre abrégé: Hum Genet
Pays: Germany
ID NLM: 7613873
Informations de publication
Date de publication:
Apr 2022
Apr 2022
Historique:
received:
14
12
2021
accepted:
18
02
2022
pubmed:
8
3
2022
medline:
27
4
2022
entrez:
7
3
2022
Statut:
ppublish
Résumé
Novel hearing loss (HL) genes are constantly being discovered, and evidence from independent studies is essential to strengthen their position as causes of hereditary HL. To address this issue, we searched our genetic data of families with autosomal dominant HL (ADHL) who had been tested with high-throughput DNA sequencing methods. For CD164, only one pathogenic variant in one family has so far been reported. For LMX1A, just two previous studies have revealed its involvement in ADHL. In this study we found two families with the same pathogenic variant in CD164 and one family with a novel variant in LMX1A (c.686C>A; p.(Ala229Asp)) that impairs its transcriptional activity. Our data show recurrence of the same CD164 variant in two HL families of different geographic origin, which strongly suggests it is a mutational hotspot. We also provide further evidence for haploinsufficiency as the pathogenic mechanism underlying LMX1A-related ADHL.
Identifiants
pubmed: 35254497
doi: 10.1007/s00439-022-02443-y
pii: 10.1007/s00439-022-02443-y
doi:
Substances chimiques
CD164 protein, human
0
Endolyn
0
LIM-Homeodomain Proteins
0
LMX1A protein, human
0
Transcription Factors
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
445-453Subventions
Organisme : Narodowe Centrum Nauki
ID : 2016/22/E/NZ5/00470
Organisme : Ministry of Health and Welfare
ID : HI20C0285
Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Adzhubei I, Jordan DM, Sunyaev SR (2013) Predicting functional effect of human missense mutations using PolyPhen-2. Curr Protoc Hum Genet Chapter 7(Unit7):20. https://doi.org/10.1002/0471142905.hg0720s76
doi: 10.1002/0471142905.hg0720s76
Ahmadmehrabi S, Brant J, Epstein DJ, Ruckenstein MJ, Rader DJ (2021) Genetics of postlingual sensorineural hearing loss. Laryngoscope 131:401–409. https://doi.org/10.1002/lary.28646
doi: 10.1002/lary.28646
pubmed: 32243624
Bongers EM, de Wijs IJ, Marcelis C, Hoefsloot LH, Knoers NV (2008) Identification of entire LMX1B gene deletions in nail patella syndrome: evidence for haploinsufficiency as the main pathogenic mechanism underlying dominant inheritance in man. Eur J Hum Genet 16:1240–1244. https://doi.org/10.1038/ejhg.2008.83
doi: 10.1038/ejhg.2008.83
pubmed: 18414507
Chun S, Fay JC (2009) Identification of deleterious mutations within three human genomes. Genome Res 19:1553–1561. https://doi.org/10.1101/gr.092619.109
doi: 10.1101/gr.092619.109
pubmed: 19602639
pmcid: 2752137
Davydov EV, Goode DL, Sirota M, Cooper GM, Sidow A, Batzoglou S (2010) Identifying a high fraction of the human genome to be under selective constraint using GERP++. PLoS Comput Biol 6:e1001025. https://doi.org/10.1371/journal.pcbi.1001025
doi: 10.1371/journal.pcbi.1001025
pubmed: 21152010
pmcid: 2996323
Doucet-Beaupre H, Ang SL, Levesque M (2015) Cell fate determination, neuronal maintenance and disease state: the emerging role of transcription factors Lmx1a and Lmx1b. FEBS Lett 589:3727–3738. https://doi.org/10.1016/j.febslet.2015.10.020
doi: 10.1016/j.febslet.2015.10.020
pubmed: 26526610
German MS, Wang J, Fernald AA, Espinosa R 3rd, Le Beau MM, Bell GI (1994) Localization of the genes encoding two transcription factors, LMX1 and CDX3, regulating insulin gene expression to human chromosomes 1 and 13. Genomics 24:403–404. https://doi.org/10.1006/geno.1994.1639
doi: 10.1006/geno.1994.1639
pubmed: 7698771
Hildebrand MS, DeLuca AP, Taylor KR, Hoskinson DP, Hur IA, Tack D, McMordie SJ, Huygen PL, Casavant TL, Smith RJ (2009) A contemporary review of AudioGene audioprofiling: a machine-based candidate gene prediction tool for autosomal dominant nonsyndromic hearing loss. Laryngoscope 119:2211–2215. https://doi.org/10.1002/lary.20664
doi: 10.1002/lary.20664
pubmed: 19780026
pmcid: 2783729
Hildebrand MS, Morin M, Meyer NC, Mayo F, Modamio-Hoybjor S, Mencia A, Olavarrieta L, Morales-Angulo C, Nishimura CJ, Workman H, DeLuca AP, del Castillo I, Taylor KR, Tompkins B, Goodman CW, Schrauwen I, Wesemael MV, Lachlan K, Shearer AE, Braun TA, Huygen PL, Kremer H, Van Camp G, Moreno F, Casavant TL, Smith RJ, Moreno-Pelayo MA (2011) DFNA8/12 caused by TECTA mutations is the most identified subtype of nonsyndromic autosomal dominant hearing loss. Hum Mutat 32:825–834. https://doi.org/10.1002/humu.21512
doi: 10.1002/humu.21512
pubmed: 21520338
pmcid: 3326665
Ioannidis NM, Rothstein JH, Pejaver V, Middha S, McDonnell SK, Baheti S, Musolf A, Li Q, Holzinger E, Karyadi D, Cannon-Albright LA, Teerlink CC, Stanford JL, Isaacs WB, Xu J, Cooney KA, Lange EM, Schleutker J, Carpten JD, Powell IJ, Cussenot O, Cancel-Tassin G, Giles GG, MacInnis RJ, Maier C, Hsieh CL, Wiklund F, Catalona WJ, Foulkes WD, Mandal D, Eeles RA, Kote-Jarai Z, Bustamante CD, Schaid DJ, Hastie T, Ostrander EA, Bailey-Wilson JE, Radivojac P, Thibodeau SN, Whittemore AS, Sieh W (2016) REVEL: an ensemble method for predicting the pathogenicity of rare missense variants. Am J Hum Genet 99:877–885. https://doi.org/10.1016/j.ajhg.2016.08.016
doi: 10.1016/j.ajhg.2016.08.016
pubmed: 27666373
pmcid: 5065685
Kim BJ, Kim AR, Han JH, Lee C, Oh DY, Choi BY (2017) Discovery of MYH14 as an important and unique deafness gene causing prelingually severe autosomal dominant nonsyndromic hearing loss. J Gene Med. https://doi.org/10.1002/jgm.2950
doi: 10.1002/jgm.2950
pubmed: 28221712
Kircher M, Witten DM, Jain P, O’Roak BJ, Cooper GM, Shendure J (2014) A general framework for estimating the relative pathogenicity of human genetic variants. Nat Genet 46:310–315. https://doi.org/10.1038/ng.2892
doi: 10.1038/ng.2892
pubmed: 24487276
pmcid: 3992975
Kobayashi M, Miyagawa M, Nishio SY, Moteki H, Fujikawa T, Ohyama K, Sakaguchi H, Miyanohara I, Sugaya A, Naito Y, Morita SY, Kanda Y, Takahashi M, Ishikawa K, Nagano Y, Tono T, Oshikawa C, Kihara C, Takahashi H, Noguchi Y, Usami SI (2018) WFS1 mutation screening in a large series of Japanese hearing loss patients: massively parallel DNA sequencing-based analysis. PLoS ONE 13:e0193359. https://doi.org/10.1371/journal.pone.0193359
doi: 10.1371/journal.pone.0193359
pubmed: 29529044
pmcid: 5846739
Kumar P, Henikoff S, Ng PC (2009) Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nat Protoc 4:1073–1081. https://doi.org/10.1038/nprot.2009.86
doi: 10.1038/nprot.2009.86
pubmed: 19561590
Lee CG, Jang J, Jin HS (2018) A novel missense mutation in the ACTG1 gene in a family with congenital autosomal dominant deafness: a case report. Mol Med Rep 17:7611–7617. https://doi.org/10.3892/mmr.2018.8837
doi: 10.3892/mmr.2018.8837
pubmed: 29620237
pmcid: 5983957
Lee SY, Han JH, Carandang M, Kim MY, Kim B, Yi N, Kim J, Kim BJ, Oh DY, Koo JW, Lee JH, Oh SH, Choi BY (2020) Novel genotype-phenotype correlation of functionally characterized LMX1A variants linked to sensorineural hearing loss. Hum Mutat 41:1877–1883. https://doi.org/10.1002/humu.24095
doi: 10.1002/humu.24095
pubmed: 32840933
McGuirt WT, Prasad SD, Griffith AJ, Kunst HP, Green GE, Shpargel KB, Runge C, Huybrechts C, Mueller RF, Lynch E, King MC, Brunner HG, Cremers CW, Takanosu M, Li SW, Arita M, Mayne R, Prockop DJ, Van Camp G, Smith RJ (1999) Mutations in COL11A2 cause non-syndromic hearing loss (DFNA13). Nat Genet 23:413–419. https://doi.org/10.1038/70516
doi: 10.1038/70516
pubmed: 10581026
McIntosh I, Dreyer SD, Clough MV, Dunston JA, Eyaid W, Roig CM, Montgomery T, Ala-Mello S, Kaitila I, Winterpacht A, Zabel B, Frydman M, Cole WG, Francomano CA, Lee B (1998) Mutation analysis of LMX1B gene in nail-patella syndrome patients. Am J Hum Genet 63:1651–1658. https://doi.org/10.1086/302165
doi: 10.1086/302165
pubmed: 9837817
pmcid: 1377636
Naito T, Nishio SY, Iwasa Y, Yano T, Kumakawa K, Abe S, Ishikawa K, Kojima H, Namba A, Oshikawa C, Usami S (2013) Comprehensive genetic screening of KCNQ4 in a large autosomal dominant nonsyndromic hearing loss cohort: genotype-phenotype correlations and a founder mutation. PLoS ONE 8:e63231. https://doi.org/10.1371/journal.pone.0063231
doi: 10.1371/journal.pone.0063231
pubmed: 23717403
pmcid: 3662675
Nyegaard M, Rendtorff ND, Nielsen MS, Corydon TJ, Demontis D, Starnawska A, Hedemand A, Buniello A, Niola F, Overgaard MT, Leal SM, Ahmad W, Wikman FP, Petersen KB, Cruger DG, Oostrik J, Kremer H, Tommerup N, Frodin M, Steel KP, Tranebjaerg L, Borglum AD (2015) A Novel Locus Harbouring a Functional CD164 Nonsense Mutation Identified in a Large Danish Family with Nonsyndromic Hearing Impairment. PLoS Genet 11:e1005386. https://doi.org/10.1371/journal.pgen.1005386
doi: 10.1371/journal.pgen.1005386
pubmed: 26197441
pmcid: 4510537
Oza AM, DiStefano MT, Hemphill SE, Cushman BJ, Grant AR, Siegert RK, Shen J, Chapin A, Boczek NJ, Schimmenti LA, Murry JB, Hasadsri L, Nara K, Kenna M, Booth KT, Azaiez H, Griffith A, Avraham KB, Kremer H, Rehm HL, Amr SS, Abou Tayoun AN, ClinGen Hearing Loss Clinical Domain Working G (2018) Expert specification of the ACMG/AMP variant interpretation guidelines for genetic hearing loss. Hum Mutat 39:1593–1613. https://doi.org/10.1002/humu.23630
doi: 10.1002/humu.23630
pubmed: 30311386
pmcid: 6188673
Ozieblo D, Pazik J, Stepniak I, Skarzynski H, Oldak M (2020) Two novel pathogenic variants confirm RMND1 causative role in Perrault syndrome with renal involvement. Genes (basel). https://doi.org/10.3390/genes11091060
doi: 10.3390/genes11091060
Papadopoulos JS, Agarwala R (2007) COBALT: constraint-based alignment tool for multiple protein sequences. Bioinformatics 23:1073–1079. https://doi.org/10.1093/bioinformatics/btm076
doi: 10.1093/bioinformatics/btm076
pubmed: 17332019
Ramzan K, Al-Owain M, Al-Numair NS, Afzal S, Al-Ageel S, Al-Amer S, Al-Baik L, Al-Otaibi GF, Hashem A, Al-Mashharawi E, Basit S, Al-Mazroea AH, Softah A, Sogaty S, Imtiaz F (2020) Identification of TMC1 as a relatively common cause for nonsyndromic hearing loss in the Saudi population. Am J Med Genet B Neuropsychiatr Genet 183:172–180. https://doi.org/10.1002/ajmg.b.32774
doi: 10.1002/ajmg.b.32774
pubmed: 31854501
Richards S, Aziz N, Bale S, Bick D, Das S, Gastier-Foster J, Grody WW, Hegde M, Lyon E, Spector E, Voelkerding K, Rehm HL, Committee ALQA (2015) Standards and guidelines for the interpretation of sequence variants: a joint consensus recommendation of the American College of Medical Genetics and Genomics and the Association for Molecular Pathology. Genet Med 17:405–424. https://doi.org/10.1038/gim.2015.30
doi: 10.1038/gim.2015.30
pubmed: 25741868
pmcid: 4544753
Salam AA, Hafner FM, Linder TE, Spillmann T, Schinzel AA, Leal SM (2000) A novel locus (DFNA23) for prelingual autosomal dominant nonsyndromic hearing loss maps to 14q21-q22 in a Swiss German kindred. Am J Hum Genet 66:1984–1988. https://doi.org/10.1086/302931
doi: 10.1086/302931
pubmed: 10777717
pmcid: 1378045
Schrauwen I, Chakchouk I, Liaqat K, Jan A, Nasir A, Hussain S, Nickerson DA, Bamshad MJ, Ullah A, Ahmad W, Leal SM (2018) A variant in LMX1A causes autosomal recessive severe-to-profound hearing impairment. Hum Genet 137:471–478. https://doi.org/10.1007/s00439-018-1899-7
doi: 10.1007/s00439-018-1899-7
pubmed: 29971487
pmcid: 6094940
Schwarz JM, Cooper DN, Schuelke M, Seelow D (2014) MutationTaster2: mutation prediction for the deep-sequencing age. Nat Methods 11:361–362. https://doi.org/10.1038/nmeth.2890
doi: 10.1038/nmeth.2890
pubmed: 24681721
Shearer A, Hildebrand M, Smith R (1999) Hereditary Hearing Loss and Deafness Overview. University of Washington. https://www.ncbi.nlm.nih.gov/books/NBK1434/ . 2019
Stritt S, Nurden P, Turro E, Greene D, Jansen SB, Westbury SK, Petersen R, Astle WJ, Marlin S, Bariana TK, Kostadima M, Lentaigne C, Maiwald S, Papadia S, Kelly AM, Stephens JC, Penkett CJ, Ashford S, Tuna S, Austin S, Bakchoul T, Collins P, Favier R, Lambert MP, Mathias M, Millar CM, Mapeta R, Perry DJ, Schulman S, Simeoni I, Thys C, Consortium B-B, Gomez K, Erber WN, Stirrups K, Rendon A, Bradley JR, van Geet C, Raymond FL, Laffan MA, Nurden AT, Nieswandt B, Richardson S, Freson K, Ouwehand WH, Mumford AD (2016) A gain-of-function variant in DIAPH1 causes dominant macrothrombocytopenia and hearing loss. Blood 127:2903–2914. https://doi.org/10.1182/blood-2015-10-675629
doi: 10.1182/blood-2015-10-675629
pubmed: 26912466
Vona B, Muller T, Nanda I, Neuner C, Hofrichter MA, Schroder J, Bartsch O, Lassig A, Keilmann A, Schraven S, Kraus F, Shehata-Dieler W, Haaf T (2014) Targeted next-generation sequencing of deafness genes in hearing-impaired individuals uncovers informative mutations. Genet Med 16:945–953. https://doi.org/10.1038/gim.2014.65
doi: 10.1038/gim.2014.65
pubmed: 24875298
pmcid: 4262760
Wang H, Wu K, Yu L, Xie L, Xiong W, Wang D, Guan J, Wang Q (2017) A novel dominant GJB2 (DFNA3) mutation in a Chinese family. Sci Rep 7:34425. https://doi.org/10.1038/srep34425
doi: 10.1038/srep34425
pubmed: 28102197
pmcid: 5244381
Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ (2009) Jalview Version 2–a multiple sequence alignment editor and analysis workbench. Bioinformatics 25:1189–1191. https://doi.org/10.1093/bioinformatics/btp033
doi: 10.1093/bioinformatics/btp033
pubmed: 19151095
pmcid: 2672624
Wesdorp M, de Koning Gans PAM, Schraders M, Oostrik J, Huynen MA, Venselaar H, Beynon AJ, van Gaalen J, Piai V, Voermans N, van Rossum MM, Hartel BP, Lelieveld SH, Wiel L, Verbist B, Rotteveel LJ, van Dooren MF, Lichtner P, Kunst HPM, Feenstra I, Admiraal RJC, Consortium D, Yntema HG, Hoefsloot LH, Pennings RJE, Kremer H (2018) Heterozygous missense variants of LMX1A lead to nonsyndromic hearing impairment and vestibular dysfunction. Hum Genet 137:389–400. https://doi.org/10.1007/s00439-018-1880-5
doi: 10.1007/s00439-018-1880-5
pubmed: 29754270
pmcid: 5973959