Skip to main content
SpringerLink
Log in

Spectrum of DNA variants for non-syndromic deafness in a large cohort from multiple continents

  • Original Investigation
  • Published:
Human Genetics Aims and scope Submit manuscript

Abstract

Hearing loss is the most common sensory deficit in humans with causative variants in over 140 genes. With few exceptions, however, the population-specific distribution for many of the identified variants/genes is unclear. Until recently, the extensive genetic and clinical heterogeneity of deafness precluded comprehensive genetic analysis. Here, using a custom capture panel (MiamiOtoGenes), we undertook a targeted sequencing of 180 genes in a multi-ethnic cohort of 342 GJB2 mutation-negative deaf probands from South Africa, Nigeria, Tunisia, Turkey, Iran, India, Guatemala, and the United States (South Florida). We detected causative DNA variants in 25 % of multiplex and 7 % of simplex families. The detection rate varied between 0 and 57 % based on ethnicity, with Guatemala and Iran at the lower and higher end of the spectrum, respectively. We detected causative variants within 27 genes without predominant recurring pathogenic variants. The most commonly implicated genes include MYO15A, SLC26A4, USH2A, MYO7A, MYO6, and TRIOBP. Overall, our study highlights the importance of family history and generation of databases for multiple ethnically discrete populations to improve our ability to detect and accurately interpret genetic variants for pathogenicity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Ahmed ZM, Masmoudi S, Kalay E, Belyantseva IA, Mosrati MA, Collin RW, Riazuddin S, Hmani-Aifa M, Venselaar H, Kawar MN, Tlili A, van der Zwaag B, Khan SY, Ayadi L, Riazuddin SA, Morell RJ, Griffith AJ, Charfedine I, Caylan R, Oostrik J, Karaguzel A, Ghorbel A, Riazuddin S, Friedman TB, Ayadi H, Kremer H (2008) Mutations of LRTOMT, a fusion gene with alternative reading frames, cause nonsyndromic deafness in humans. Nat Genet 40:1335–1340. doi:10.1038/ng.245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amendola LM, Jarvik GP, Leo MC, McLaughlin HM, Akkari Y, Amaral MD, Berg JS, Biswas S, Bowling KM, Conlin LK, Cooper GM, Dorschner MO, Dulik MC, Ghazani AA, Ghosh R, Green RC, Hart R, Horton C, Johnston JJ, Lebo MS, Milosavljevic A, Ou J, Pak CM, Patel RY, Punj S, Richards CS, Salama J, Strande NT, Yang Y, Plon SE, Biesecker LG, Rehm HL (2016) Performance of ACMG-AMP variant-interpretation guidelines among nine laboratories in the Clinical Sequencing Exploratory Research Consortium. Am J Hum Genet 98:1067–1076. doi:10.1016/j.ajhg.2016.03.024

    Article  CAS  PubMed  Google Scholar 

  • Angeli S, Lin X, Liu XZ (2012) Genetics of hearing and deafness. Anat Rec (Hoboken) 295:1812–1829. doi:10.1002/ar.22579

    Article  CAS  Google Scholar 

  • Aronson SJ, Rehm HL (2015) Building the foundation for genomics in precision medicine. Nature 526:336–342. doi:10.1038/nature15816

    Article  CAS  PubMed  Google Scholar 

  • Babanejad M, Fattahi Z, Bazazzadegan N, Nishimura C, Meyer N, Nikzat N, Sohrabi E, Najmabadi A, Jamali P, Habibi F, Smith RJ, Kahrizi K, Najmabadi H (2012) A comprehensive study to determine heterogeneity of autosomal recessive nonsyndromic hearing loss in Iran. Am J Med Genet A 158A:2485–2492. doi:10.1002/ajmg.a.35572

    Article  PubMed  Google Scholar 

  • Bademci G, Foster J 2nd, Mahdieh N, Bonyadi M, Duman D, Cengiz FB, Menendez I, Diaz-Horta O, Shirkavand A, Zeinali S, Subasioglu A, Tokgoz-Yilmaz S, Huesca-Hernandez F, de la Luz Arenas-Sordo M, Dominguez-Aburto J, Hernandez-Zamora E, Montenegro P, Paredes R, Moreta G, Vinueza R, Villegas F, Mendoza-Benitez S, Guo S, Bozan N, Tos T, Incesulu A, Sennaroglu G, Blanton SH, Ozturkmen-Akay H, Yildirim-Baylan M, Tekin M (2016) Comprehensive analysis via exome sequencing uncovers genetic etiology in autosomal recessive nonsyndromic deafness in a large multiethnic cohort. Genet Med 18:364–371. doi:10.1038/gim.2015.89

    Article  CAS  PubMed  Google Scholar 

  • Baux D, Larrieu L, Blanchet C, Hamel C, Ben Salah S, Vielle A, Gilbert-Dussardier B, Holder M, Calvas P, Philip N, Edery P, Bonneau D, Claustres M, Malcolm S, Roux AF (2007) Molecular and in silico analyses of the full-length isoform of usherin identify new pathogenic alleles in Usher type II patients. Hum Mutat 28:781–789. doi:10.1002/humu.20513

    Article  CAS  PubMed  Google Scholar 

  • Baux D, Blanchet C, Hamel C, Meunier I, Larrieu L, Faugere V, Vache C, Castorina P, Puech B, Bonneau D, Malcolm S, Claustres M, Roux AF (2014) Enrichment of LOVD-USHbases with 152 USH2A genotypes defines an extensive mutational spectrum and highlights missense hotspots. Hum Mutat 35:1179–1186. doi:10.1002/humu.22608

    Article  CAS  PubMed  Google Scholar 

  • Borck G, Ur Rehman A, Lee K, Pogoda HM, Kakar N, von Ameln S, Grillet N, Hildebrand MS, Ahmed ZM, Nurnberg G, Ansar M, Basit S, Javed Q, Morell RJ, Nasreen N, Shearer AE, Ahmad A, Kahrizi K, Shaikh RS, Ali RA, Khan SN, Goebel I, Meyer NC, Kimberling WJ, Webster JA, Stephan DA, Schiller MR, Bahlo M, Najmabadi H, Gillespie PG, Nurnberg P, Wollnik B, Riazuddin S, Smith RJ, Ahmad W, Muller U, Hammerschmidt M, Friedman TB, Riazuddin S, Leal SM, Ahmad J, Kubisch C (2011) Loss-of-function mutations of ILDR1 cause autosomal-recessive hearing impairment DFNB42. Am J Hum Genet 88:127–137. doi:10.1016/j.ajhg.2010.12.011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brownstein Z, Friedman LM, Shahin H, Oron-Karni V, Kol N, Abu Rayyan A, Parzefall T, Lev D, Shalev S, Frydman M, Davidov B, Shohat M, Rahile M, Lieberman S, Levy-Lahad E, Lee MK, Shomron N, King MC, Walsh T, Kanaan M, Avraham KB (2011) Targeted genomic capture and massively parallel sequencing to identify genes for hereditary hearing loss in Middle Eastern families. Genome Biol 12:R89. doi:10.1186/gb-2011-12-9-r89

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chu CW, Chen YJ, Lee YH, Jaung SJ, Lee FP, Huang HM (2015) Government-funded universal newborn hearing screening and genetic analyses of deafness predisposing genes in Taiwan. Int J Pediatr Otorhinolaryngol 79:584–590. doi:10.1016/j.ijporl.2015.01.033

    Article  PubMed  Google Scholar 

  • Davis A (1995) Hearing in adults: the prevalence and distribution of hearing impairment and reported hearing disability in the MRC Institute of Hearing Research’s National Study of Hearing. Whurr Publisher, London

    Google Scholar 

  • Delmaghani S, del Castillo FJ, Michel V, Leibovici M, Aghaie A, Ron U, Van Laer L, Ben-Tal N, Van Camp G, Weil D, Langa F, Lathrop M, Avan P, Petit C (2006) Mutations in the gene encoding pejvakin, a newly identified protein of the afferent auditory pathway, cause DFNB59 auditory neuropathy. Nat Genet 38:770–778. doi:10.1038/ng1829

    Article  CAS  PubMed  Google Scholar 

  • Eudy JD, Weston MD, Yao S, Hoover DM, Rehm HL, Ma-Edmonds M, Yan D, Ahmad I, Cheng JJ, Ayuso C, Cremers C, Davenport S, Moller C, Talmadge CB, Beisel KW, Tamayo M, Morton CC, Swaroop A, Kimberling WJ, Sumegi J (1998) Mutation of a gene encoding a protein with extracellular matrix motifs in Usher syndrome type IIa. Science 280:1753–1757

    Article  CAS  PubMed  Google Scholar 

  • Fugazzola L, Cerutti N, Mannavola D, Crino A, Cassio A, Gasparoni P, Vannucchi G, Beck-Peccoz P (2002) Differential diagnosis between Pendred and pseudo-Pendred syndromes: clinical, radiologic, and molecular studies. Pediatr Res 51:479–484. doi:10.1203/00006450-200204000-00013

    Article  CAS  PubMed  Google Scholar 

  • Garrison E, Marth G (2012) Haplotype-based variant detection from short-read sequencing. arXiv preprint arXiv:1207.3907

  • Gorlin RJ, Toriello HV, Cohen MM (1995) Hereditary hearing loss and its syndromes. Oxford University Press, Oxford

    Google Scholar 

  • Gu X, Guo L, Ji H, Sun S, Chai R, Wang L, Li H (2015) Genetic testing for sporadic hearing loss using targeted massively parallel sequencing identifies 10 novel mutations. Clin Genet 87:588–593. doi:10.1111/cge.12431

    Article  CAS  PubMed  Google Scholar 

  • Hutchin TP, Parker MJ, Young ID, Davis AC, Pulleyn LJ, Deeble J, Lench NJ, Markham AF, Mueller RF (2000) A novel mutation in the mitochondrial tRNA(Ser(UCN)) gene in a family with non-syndromic sensorineural hearing impairment. J Med Genet 37:692–694

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • King PJ, Ouyang X, Du L, Yan D, Angeli SI, Liu XZ (2012) Etiologic diagnosis of nonsyndromic genetic hearing loss in adult vs pediatric populations. Otolaryngol Head Neck Surg 147:932–936. doi:10.1177/0194599812453553

    Article  PubMed  PubMed Central  Google Scholar 

  • Kothiyal P, Cox S, Ebert J, Husami A, Kenna MA, Greinwald JH, Aronow BJ, Rehm HL (2010) High-throughput detection of mutations responsible for childhood hearing loss using resequencing microarrays. BMC Biotechnol 10:10. doi:10.1186/1472-6750-10-10

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee HK, Song MH, Kang M, Lee JT, Kong KA, Choi SJ, Lee KY, Venselaar H, Vriend G, Lee WS, Park HJ, Kwon TK, Bok J, Kim UK (2009) Clinical and molecular characterizations of novel POU3F4 mutations reveal that DFN3 is due to null function of POU3F4 protein. Physiol Genomics 39:195–201. doi:10.1152/physiolgenomics.00100.2009

    Article  PubMed  Google Scholar 

  • Li H, Durbin R (2010) Fast and accurate long-read alignment with Burrows–Wheeler transform. Bioinformatics 26:589–595. doi:10.1093/bioinformatics/btp698

    Article  PubMed  PubMed Central  Google Scholar 

  • Maddalena A, Bale S, Das S, Grody W, Richards S, Committee ALQA (2005) Technical standards and guidelines: molecular genetic testing for ultra-rare disorders. Genet Med 7:571–583. doi:10.1097/01.GIM.0000182738.95726.ca

    Article  PubMed  Google Scholar 

  • Mosrati MA, Hammami B, Rebeh IB, Ayadi L, Dhouib L, Ben Mahfoudh K, Hakim B, Charfeddine I, Mnif J, Ghorbel A, Masmoudi S (2011) A novel dominant mutation in SIX1, affecting a highly conserved residue, result in only auditory defects in humans. Eur J Med Genet 54:e484–e488. doi:10.1016/j.ejmg.2011.06.001

    Article  PubMed  Google Scholar 

  • Nance WE (2003) The genetics of deafness. Ment Retard Dev Disabil Res Rev 9:109–119. doi:10.1002/mrdd.10067

    Article  PubMed  Google Scholar 

  • Naz S, Giguere CM, Kohrman DC, Mitchem KL, Riazuddin S, Morell RJ, Ramesh A, Srisailpathy S, Deshmukh D, Riazuddin S, Griffith AJ, Friedman TB, Smith RJ, Wilcox ER (2002) Mutations in a novel gene, TMIE, are associated with hearing loss linked to the DFNB6 locus. Am J Hum Genet 71:632–636. doi:10.1086/342193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Naz S, Alasti F, Mowjoodi A, Riazuddin S, Sanati MH, Friedman TB, Griffith AJ, Wilcox ER, Riazuddin S (2003) Distinctive audiometric profile associated with DFNB21 alleles of TECTA. J Med Genet 40:360–363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nord AS, Lee M, King MC, Walsh T (2011) Accurate and exact CNV identification from targeted high-throughput sequence data. BMC Genom 12:184. doi:10.1186/1471-2164-12-184

    Article  CAS  Google Scholar 

  • Rehman AU, Gul K, Morell RJ, Lee K, Ahmed ZM, Riazuddin S, Ali RA, Shahzad M, Jaleel AU, Andrade PB, Khan SN, Khan S, Brewer CC, Ahmad W, Leal SM, Riazuddin S, Friedman TB (2011) Mutations of GIPC3 cause nonsyndromic hearing loss DFNB72 but not DFNB81 that also maps to chromosome 19p. Hum Genet 130:759–765. doi:10.1007/s00439-011-1018-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riahi Z, Bonnet C, Zainine R, Louha M, Bouyacoub Y, Laroussi N, Chargui M, Kefi R, Jonard L, Dorboz I, Hardelin JP, Salah SB, Levilliers J, Weil D, McElreavey K, Boespflug OT, Besbes G, Abdelhak S, Petit C (2014) Whole exome sequencing identifies new causative mutations in Tunisian families with non-syndromic deafness. PLoS One 9:e99797. doi:10.1371/journal.pone.0099797

    Article  PubMed  PubMed Central  Google Scholar 

  • Richards CS, Bale S, Bellissimo DB, Das S, Grody WW, Hegde MR, Lyon E, Ward BE, Molecular Subcommittee of the ALQAC (2008) ACMG recommendations for standards for interpretation and reporting of sequence variations: revisions 2007. Genet Med 10:294–300. doi:10.1097/GIM.0b013e31816b5cae

    Article  CAS  PubMed  Google Scholar 

  • 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. doi:10.1038/gim.2015.30

    Article  PubMed  PubMed Central  Google Scholar 

  • Schrauwen I, Sommen M, Corneveaux JJ, Reiman RA, Hackett NJ, Claes C, Claes K, Bitner-Glindzicz M, Coucke P, Van Camp G, Huentelman MJ (2013) A sensitive and specific diagnostic test for hearing loss using a microdroplet PCR-based approach and next generation sequencing. Am J Med Genet A 161A:145–152. doi:10.1002/ajmg.a.35737

    Article  PubMed  Google Scholar 

  • Shearer AE, Smith RJ (2015) Massively parallel sequencing for genetic diagnosis of hearing loss: the new standard of care. Otolaryngol Head Neck Surg 153:175–182. doi:10.1177/0194599815591156

    Article  PubMed  PubMed Central  Google Scholar 

  • Shearer AE, DeLuca AP, Hildebrand MS, Taylor KR, Gurrola J 2nd, Scherer S, Scheetz TE, Smith RJ (2010) Comprehensive genetic testing for hereditary hearing loss using massively parallel sequencing. Proc Natl Acad Sci USA 107:21104–21109. doi:10.1073/pnas.1012989107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shearer AE, Black-Ziegelbein EA, Hildebrand MS, Eppsteiner RW, Ravi H, Joshi S, Guiffre AC, Sloan CM, Happe S, Howard SD, Novak B, Deluca AP, Taylor KR, Scheetz TE, Braun TA, Casavant TL, Kimberling WJ, Leproust EM, Smith RJ (2013) Advancing genetic testing for deafness with genomic technology. J Med Genet 50:627–634. doi:10.1136/jmedgenet-2013-101749

    Article  CAS  PubMed  Google Scholar 

  • Shearer AE, Eppsteiner RW, Booth KT, Ephraim SS, Gurrola J 2nd, Simpson A, Black-Ziegelbein EA, Joshi S, Ravi H, Giuffre AC, Happe S, Hildebrand MS, Azaiez H, Bayazit YA, Erdal ME, Lopez-Escamez JA, Gazquez I, Tamayo ML, Gelvez NY, Leal GL, Jalas C, Ekstein J, Yang T, Usami S, Kahrizi K, Bazazzadegan N, Najmabadi H, Scheetz TE, Braun TA, Casavant TL, LeProust EM, Smith RJ (2014) Utilizing ethnic-specific differences in minor allele frequency to recategorize reported pathogenic deafness variants. Am J Hum Genet 95:445–453. doi:10.1016/j.ajhg.2014.09.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sloan-Heggen CM, Babanejad M, Beheshtian M, Simpson AC, Booth KT, Ardalani F, Frees KL, Mohseni M, Mozafari R, Mehrjoo Z, Jamali L, Vaziri S, Akhtarkhavari T, Bazazzadegan N, Nikzat N, Arzhangi S, Sabbagh F, Otukesh H, Seifati SM, Khodaei H, Taghdiri M, Meyer NC, Daneshi A, Farhadi M, Kahrizi K, Smith RJ, Azaiez H, Najmabadi H (2015) Characterising the spectrum of autosomal recessive hereditary hearing loss in Iran. J Med Genet 52:823–829. doi:10.1136/jmedgenet-2015-103389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tchernitchko D, Goossens M, Wajcman H (2004) In silico prediction of the deleterious effect of a mutation: proceed with caution in clinical genetics. Clin Chem 50:1974–1978. doi:10.1373/clinchem.2004.036053

    Article  CAS  PubMed  Google Scholar 

  • Tekin D, Yan D, Bademci G, Feng Y, Guo S, Foster J 2nd, Blanton S, Tekin M, Liu X (2016) A next-generation sequencing gene panel (MiamiOtoGenes) for comprehensive analysis of deafness genes. Hear Res 333:179–184. doi:10.1016/j.heares.2016.01.018

    Article  CAS  PubMed  Google Scholar 

  • Thusberg J, Vihinen M (2009) Pathogenic or not? And if so, then how? Studying the effects of missense mutations using bioinformatics methods. Hum Mutat 30:703–714. doi:10.1002/humu.20938

    Article  CAS  PubMed  Google Scholar 

  • Tsai AC, Liu X (2014) Toward best practice in using molecular diagnosis to guide medical management, are we there yet? N Am J Med Sci (Boston) 7:199–200

    Google Scholar 

  • Usami S, Abe S, Weston MD, Shinkawa H, Van Camp G, Kimberling WJ (1999) Non-syndromic hearing loss associated with enlarged vestibular aqueduct is caused by PDS mutations. Hum Genet 104:188–192

    Article  CAS  PubMed  Google Scholar 

  • Weston MD, Kelley PM, Overbeck LD, Wagenaar M, Orten DJ, Hasson T, Chen ZY, Corey D, Mooseker M, Sumegi J, Cremers C, Moller C, Jacobson SG, Gorin MB, Kimberling WJ (1996) Myosin VIIA mutation screening in 189 Usher syndrome type 1 patients. Am J Hum Genet 59:1074–1083

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu CC, Lu YC, Chen PJ, Yeh PL, Su YN, Hwu WL, Hsu CJ (2010) Phenotypic analyses and mutation screening of the SLC26A4 and FOXI1 genes in 101 Taiwanese families with bilateral nonsyndromic enlarged vestibular aqueduct (DFNB4) or Pendred syndrome. Audiol Neurootol 15:57–66. doi:10.1159/000231567

    Article  CAS  PubMed  Google Scholar 

  • Yan D, Liu XZ (2008) Cochlear molecules and hereditary deafness. Front Biosci 13:4972–4983

    Article  CAS  PubMed  Google Scholar 

  • Yan D, Tekin M, Blanton SH, Liu XZ (2013) Next-generation sequencing in genetic hearing loss. Genet Test Mol Biomarkers 17:581–587. doi:10.1089/gtmb.2012.0464

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang T, Wei X, Chai Y, Li L, Wu H (2013) Genetic etiology study of the non-syndromic deafness in Chinese Hans by targeted next-generation sequencing. Orphanet J Rare Dis 8:85. doi:10.1186/1750-1172-8-85

    Article  PubMed  PubMed Central  Google Scholar 

  • Yoshimura H, Iwasaki S, Nishio SY, Kumakawa K, Tono T, Kobayashi Y, Sato H, Nagai K, Ishikawa K, Ikezono T, Naito Y, Fukushima K, Oshikawa C, Kimitsuki T, Nakanishi H, Usami S (2014) Massively parallel DNA sequencing facilitates diagnosis of patients with Usher syndrome type 1. PLoS One 9:e90688. doi:10.1371/journal.pone.0090688

    Article  PubMed  PubMed Central  Google Scholar 

  • Yoshinaga-Itano C (2000) Successful outcomes for deaf and hard-of-hearing children. Semin Hear 21:309–326. doi:10.1055/s-2000-13462

    Article  Google Scholar 

Download references

Acknowledgments

This study was supported by R01 DC05575, R01 DC01246, 2P50DC000422-Sub-Project 6432, and R01 DC012115 from the National Institutes of Health/National Institute on Deafness and Other Communication Disorders to Xuezhong Liu and R01DC09645 and R01DC012836 to Mustafa Tekin; University of Pretoria RDP fund to RI Kabahuma.

Author information

Authors and Affiliations

  1. Department of Otolaryngology (D-48), University of Miami Miller School of Medicine, 1666 NW 12th Avenue, Miami, FL, 33136, USA

    Denise Yan, Demet Tekin, Joseph Foster II, Abhiraami Kannan-Sundhari, Rahul Mittal, Bing Zou, Mhamed Grati, Susan H. Blanton, Xue Z. Liu & Mustafa Tekin

  2. Department of Human Genetics, John P. Hussman Institute for Human Genomics, University of Miami, 1501 NW 10th Avenue, BRB-610 (M-860), Miami, FL, 33136, USA

    Guney Bademci, Joseph Foster II, F. Basak Cengiz, Shengru Guo, Ibis Menendez, Susan H. Blanton, Xue Z. Liu & Mustafa Tekin

  3. Department of Otorhinolaryngology, Steve Biko Academic Hospital, University of Pretoria, Cnr Malan and Steve Biko Road, Gezina, Pretoria, South Africa

    Rosemary I. Kabahuma

  4. Madras ENT Research Foundation (MERF), No-1, 1st Cross Street, Off. II Main Road, Raja Annamalai Puram, Chennai, 600028, Tamil Nadu, India

    Mohan Kameswaran

  5. Department of Otorhinolaryngology, College of Medicine, University of Ibadan, Ibadan, Nigeria

    Taye J. Lasisi, Waheed A. Adedeji & Akeem O. Lasisi

  6. Institute for Research on Genetic and Metabolic Diseases, INVEGEM, Guatemala City, Guatemala

    Marianna Herrera & Claudia Carranza

  7. Institute of Biomedical and Clinical Science, University of Exeter Medical School, RILD Wellcome Wolfson Centre, Exeter, UK

    Reza Maroofian & Andrew H. Crosby

  8. Laboratoire Procédés de Criblage Moléculaire et Cellulaire, Centre de Biotechnologie de Sfax, Université de Sfax, Sfax, Tunisia

    Mariem Bensaid & Saber Masmoudi

  9. Medical Genetics Laboratory of Genome, Isfahan, Iran

    Mahdiyeh Behnam

  10. Department of Medical Genetics, Mashhad University of Medical Sciences, Mashhad, Iran

    Majid Mojarrad

  11. Department of Otolaryngology, Xiangya Hospital, Central South University, Changsha, Hunan, China

    Yong Feng & Xue Z. Liu

  12. Division of Genetics, Department of Pediatrics, Ankara University School of Medicine, Ankara, Turkey

    Duygu Duman

  13. Department of Neurobiology, Physiology, and Behavior, Center for Neuroscience, UC Davis, Davis, CA, 95616, USA

    Alex M. Mawla & Alex S. Nord

  14. Department of Psychiatry and Behavioral Sciences, Center for Neuroscience, UC Davis, Davis, CA, 95616, USA

    Alex M. Mawla & Alex S. Nord

  15. Dr. John T. Macdonald Department of Human Genetics, University of Miami Miller School of Medicine, Miami, FL, 33136, USA

    Susan H. Blanton & Mustafa Tekin

Authors
  1. Denise Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Demet Tekin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Guney Bademci
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Joseph Foster II
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. F. Basak Cengiz
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Abhiraami Kannan-Sundhari
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Shengru Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Rahul Mittal
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Bing Zou
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Mhamed Grati
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Rosemary I. Kabahuma
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Mohan Kameswaran
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Taye J. Lasisi
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Waheed A. Adedeji
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Akeem O. Lasisi
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Ibis Menendez
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Marianna Herrera
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Claudia Carranza
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Reza Maroofian
    View author publications

    You can also search for this author in PubMed Google Scholar

  20. Andrew H. Crosby
    View author publications

    You can also search for this author in PubMed Google Scholar

  21. Mariem Bensaid
    View author publications

    You can also search for this author in PubMed Google Scholar

  22. Saber Masmoudi
    View author publications

    You can also search for this author in PubMed Google Scholar

  23. Mahdiyeh Behnam
    View author publications

    You can also search for this author in PubMed Google Scholar

  24. Majid Mojarrad
    View author publications

    You can also search for this author in PubMed Google Scholar

  25. Yong Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

  26. Duygu Duman
    View author publications

    You can also search for this author in PubMed Google Scholar

  27. Alex M. Mawla
    View author publications

    You can also search for this author in PubMed Google Scholar

  28. Alex S. Nord
    View author publications

    You can also search for this author in PubMed Google Scholar

  29. Susan H. Blanton
    View author publications

    You can also search for this author in PubMed Google Scholar

  30. Xue Z. Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  31. Mustafa Tekin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Xue Z. Liu or Mustafa Tekin.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yan, D., Tekin, D., Bademci, G. et al. Spectrum of DNA variants for non-syndromic deafness in a large cohort from multiple continents. Hum Genet 135, 953–961 (2016). https://doi.org/10.1007/s00439-016-1697-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00439-016-1697-z

Keywords

Search

Navigation