Genome-Wide Association Study of Chronic Dizziness in the Elderly Identifies Loci Implicating MLLT10, BPTF, LINC01224, and ROS1.

Dizziness Genome-wide association studies Human Imbalance Vertigo

Journal

Journal of the Association for Research in Otolaryngology : JARO
ISSN: 1438-7573
Titre abrégé: J Assoc Res Otolaryngol
Pays: United States
ID NLM: 100892857

Informations de publication

Date de publication:
30 Nov 2023
Historique:
received: 06 02 2023
accepted: 12 11 2023
medline: 1 12 2023
pubmed: 1 12 2023
entrez: 30 11 2023
Statut: aheadofprint

Résumé

Chronic age-related imbalance is a common cause of falls and subsequent death in the elderly and can arise from dysfunction of the vestibular system, an elegant neuroanatomical group of pathways that mediates human perception of acceleration, gravity, and angular head motion. Studies indicate that 27-46% of the risk of age-related chronic imbalance is genetic; nevertheless, the underlying genes remain unknown. The cohort consisted of 50,339 cases and 366,900 controls in the Million Veteran Program. The phenotype comprised cases with two ICD diagnoses of vertigo or dizziness at least 6 months apart, excluding acute or recurrent vertiginous syndromes and other non-vestibular disorders. Genome-wide association studies were performed as individual logistic regressions on European, African American, and Hispanic ancestries followed by trans-ancestry meta-analysis. Downstream analysis included case-case-GWAS, fine mapping, probabilistic colocalization of significant variants and genes with eQTLs, and functional analysis of significant hits. Two significant loci were identified in Europeans, another in the Hispanic population, and two additional in trans-ancestry meta-analysis, including three novel loci. Fine mapping revealed credible sets of intronic single nucleotide polymorphisms (SNPs) in MLLT10 - a histone methyl transferase cofactor, BPTF - a subunit of a nucleosome remodeling complex implicated in neurodevelopment, and LINC01224 - a proto-oncogene receptor tyrosine kinase. Despite the difficulties of phenotyping the nature of chronic imbalance, we replicated two loci from previous vertigo GWAS studies and identified three novel loci. Findings suggest candidates for further study and ultimate treatment of this common elderly disorder.

Identifiants

pubmed: 38036714
doi: 10.1007/s10162-023-00917-y
pii: 10.1007/s10162-023-00917-y
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : NIH HHS
ID : R01DC020052
Pays : United States
Organisme : NIH HHS
ID : R01GM140287
Pays : United States

Investigateurs

Sumitra Muralidhar (S)
Jennifer Moser (J)
Jennifer E Deen (JE)
Philip S Tsao (PS)
J Michael Gaziano (JM)
Elizabeth Hauser (E)
Amy Kilbourne (A)
Shiuh-Wen Luoh (SW)
Michael Matheny (M)
Dave Oslin (D)
Lori Churby (L)
Stacey B Whitbourne (SB)
Jessica V Brewer (JV)
Shahpoor Alex Shayan (SA)
Luis E Selva (LE)
Saiju Pyarajan (S)
Kelly Cho (K)
Scott L DuVall (SL)
Mary T Brophy (MT)
Brady Stephens (B)
Todd Connor (T)
Dean P Argyres (DP)
Tim Assimes (T)
Adriana Hung (A)
Henry Kranzler (H)
Samuel Aguayo (S)
Sunil Ahuja (S)
Kathrina Alexander (K)
Xiao M Androulakis (XM)
Prakash Balasubramanian (P)
Zuhair Ballas (Z)
Jean Beckham (J)
Sujata Bhushan (S)
Edward Boyko (E)
David Cohen (D)
Louis Dellitalia (L)
L Christine Faulk (LC)
Joseph Fayad (J)
Daryl Fujii (D)
Saib Gappy (S)
Frank Gesek (F)
Jennifer Greco (J)
Michael Godschalk (M)
Todd W Gress (TW)
Samir Gupta (S)
Salvador Gutierrez (S)
John Harley (J)
Kimberly Hammer (K)
Mark Hamner (M)
Adriana Hung (A)
Robin Hurley (R)
Pran Iruvanti (P)
Frank Jacono (F)
Darshana Jhala (D)
Scott Kinlay (S)
Jon Klein (J)
Michael Landry (M)
Peter Liang (P)
Suthat Liangpunsakul (S)
Jack Lichy (J)
C Scott Mahan (CS)
Ronnie Marrache (R)
Stephen Mastorides (S)
Elisabeth Mates (E)
Kristin Mattocks (K)
Paul Meyer (P)
Jonathan Moorman (J)
Timothy Morgan (T)
Maureen Murdoch (M)
James Norton (J)
Olaoluwa Okusaga (O)
Kris Ann Oursler (KA)
Ana Palacio (A)
Samuel Poon (S)
Emily Potter (E)
Michael Rauchman (M)
Richard Servatius (R)
Satish Sharma (S)
River Smith (R)
Peruvemba Sriram (P)
Patrick Strollo (P)
Neeraj Tandon (N)
Gerardo Villareal (G)
Agnes Wallbom (A)
Jessica Walsh (J)
John Wells (J)
Jeffrey Whittle (J)
Mary Whooley (M)
Allison E Williams (AE)
Peter Wilson (P)
Junzhe Xu (J)
Shing Shing Yeh (SS)
Daniel Dochtermann (D)
Poornima Devineni (P)

Informations de copyright

© 2023. This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply.

Références

Ekvall Hansson E, Magnusson M (2013) Vestibular asymmetry predicts falls among elderly patients with multi- sensory dizziness. BMC Geriatr 13.  https://doi.org/10.1186/1471-2318-13-77
Harun A, Semenov YR, Agrawal Y (2015) Vestibular function and activities of daily living: analysis of the 1999 to 2004 National Health and Nutrition Examination Surveys. Gerontol Geriatr Med 1:2333721415607124. https://doi.org/10.1177/2333721415607124 . Epub 2015 Sep 21. PMID: 26753170; PMCID: PMC4706363. https://doi.org/10.1177/2333721415607124
Kippenbrock T, Soja ME (2007) Preventing falls in the elderly: interviewing patients who have fallen. Researchers attempt to identify fall-risk factors from the patients’ point of view. Geriatr Nurs 14:205–9
Fernández L, Breinbauer HA, Delano PH (2015) Vertigo and dizziness in the elderly. Front Neurol 6:144
pubmed: 26167157 pmcid: 4481149 doi: 10.3389/fneur.2015.00144
Cutson TM (1994) Falls in the elderly. Am Fam Physician 49:149–156
pubmed: 8273713
Teixeira AR, Wender MH, Gonçalves AK, Freitas CDLR, dos Santos AMPV, Soldera CLC (2016) Dizziness, physical exercise, falls, and depression in adults and the elderly. Int Arch Otorhinolaryngol 20:124–131
pubmed: 27096016
Mitchell AJ, Vaze A, Rao S (2009) Clinical diagnosis of depression in primary care: a meta-analysis. Lancet 374:609–619
pubmed: 19640579 doi: 10.1016/S0140-6736(09)60879-5
Furman JM, Redfern MS (2001) Effect of aging on the otolith-ocular reflex. J Vestib Res 11:91–103
pubmed: 11847453 doi: 10.3233/VES-2001-11204
Baloh RW, Jacobson KM, Socotch TM (1993) The effect of aging on visual-vestibuloocular responses. Exp Brain Res 95:509–516
pubmed: 8224077 doi: 10.1007/BF00227144
Matheson AJ, Darlington CL, Smith PF (1999) Further evidence for age-related deficits in human postural function. J Vestib Res 9:261–264
pubmed: 10472038 doi: 10.3233/VES-1999-9403
Rauch SD, Velazquez-Villaseñor L, Dimitri PS, Merchant SN (2001) Decreasing hair cell counts in aging humans. Ann N Y Acad Sci 942:220–227
pubmed: 11710464 doi: 10.1111/j.1749-6632.2001.tb03748.x
Jang YS, Hwang CH, Shin JY, Bae WY, Kim LS (2006) Age-related changes on the morphology of the otoconia. Laryngoscope 116:996–1001
pubmed: 16735917 doi: 10.1097/01.mlg.0000217238.84401.03
Walther LE, Westhofen M (2007) Presbyvertigo-aging of otoconia and vestibular sensory cells. J Vestib Res 17:89–92
pubmed: 18413901 doi: 10.3233/VES-2007-172-303
Maes L, Dhooge I, D’haenens W, Bockstael A, Keppler H, Philips B, Swinnen F, Vinck BM (2010) The effect of age on the sinusoidal harmonic acceleration test, pseudorandom rotation test, velocity step test, caloric test, and vestibular-evoked myogenic potential test. Ear Hear 31:84–94
Tanioka H, Tanioka S, Kaga K (2020) Vestibular aging process from 3D physiological imaging of the membranous labyrinth. Published Online First. https://doi.org/10.1038/s41598-020-66520-w
doi: 10.1038/s41598-020-66520-w
Wagner H, Melhus H, Pedersen NL, Michaëlsson K (2009) Heritability of impaired balance: a nationwide cohort study in twins. Osteoporosis Int 20:577–583
doi: 10.1007/s00198-008-0710-3
El Haber N, Hill KD, Cassano A-MT, Paton LM, Macinnis RJ, Cui JS, Hopper JL, Wark JD (2006) Genetic and environmental influences on variation in balance performance among female twin pairs aged 21–82 years. Am J Epidemiol 164:246–56
Skuladottir ATh, Bjornsdottir G, Nawaz MS, Petersen H, Rognvaldsson S, Moore KHS, Olafsson PI, Magnusson SH, Bjornsdottir A, Sveinsson OA, Sigurdardottir GR, Saevarsdottir S, Ivarsdottir EV, Stefansdottir L, Gunnarsson B, Muhlestein JB, Knowlton KU, Jones DA, Nadauld LD, Hartmann AM, Rujescu D, Strupp M, Walters GB, Thorgeirsson TE, Jonsdottir I, Holm H, Thorleifsson G, Gudbjartsson DF, Sulem P, Stefansson H, Stefansson K (2021) A genome-wide meta-analysis uncovers six sequence variants conferring risk of vertigo. Commun Biol 4:1148
pubmed: 34620984 pmcid: 8497462 doi: 10.1038/s42003-021-02673-2
Xiao AY, Tan ML, Plana MN, Yadav D, Zamora J, Petrov MS (2018) The use of international classification of diseases codes to identify patients with pancreatitis: a systematic review and meta-analysis of diagnostic accuracy studies. Clin Transl Gastroenterol 9.  https://doi.org/10.1038/s41424-018-0060-1
Foley HE, Knight JC, Ploughman M, Asghari S, Audas R (2020) Identifying cases of chronic pain using health administrative data: a validation study. Can J Pain 4:252–267
pubmed: 33987504 pmcid: 7967902 doi: 10.1080/24740527.2020.1820857
Wassermann A, Finn S, Axer H (2022) Age-associated characteristics of patients with chronic dizziness and vertigo. J Geriatr Psychiatry Neurol 35:580–585
pubmed: 34338064 doi: 10.1177/08919887211036185
Müller KJ, Becker-Bense S, Strobl R, Grill E, Dieterich M (2022) Chronic vestibular syndromes in the elderly: presbyvestibulopathy—an isolated clinical entity? Eur J Neurol 29:1825–1835
pubmed: 35239246 doi: 10.1111/ene.15308
Ji L, Zhai S (2018) Aging and the peripheral vestibular system. J Otol 13:138–140
pubmed: 30671091 pmcid: 6335476 doi: 10.1016/j.joto.2018.11.006
Yetiser S (2020) Review of the pathology underlying benign paroxysmal positional vertigo. J Int Med Res 48:300060519892370
pubmed: 31885315 doi: 10.1177/0300060519892370
Fang H, Hui Q, Lynch J, Honerlaw J, Assimes TL, Huang J, Vujkovic M, Damrauer SM, Pyarajan S, Gaziano JM, DuVall SL, O’Donnell CJ, Cho K, Chang K-M, Wilson PWF, Tsao PS, Sun YV, Tang H, Gaziano JM, Ramoni R, Breeling J, Chang K-M, Huang G, Muralidhar S, O’Donnell CJ, Tsao PS, Muralidhar S, Moser J, Whitbourne SB, Brewer J V., Concato J, Warren S, Argyres DP, Stephens B, Brophy MT, Humphries DE, Do N, Shayan S, Nguyen X-MT, Pyarajan S, Cho K, Hauser E, Sun Y, Zhao H, Wilson P, McArdle R, Dellitalia L, Harley J, Whittle J, Beckham J, Wells J, Gutierrez S, Gibson G, Kaminsky L, Villareal G, Kinlay S, Xu J, Hamner M, Haddock KS, Bhushan S, Iruvanti P, Godschalk M, Ballas Z, Buford M, Mastorides S, Klein J, Ratcliffe N, Florez H, Swann A, Murdoch M, Sriram P, Yeh SS, Washburn R, Jhala D, Aguayo S, Cohen D, Sharma S, Callaghan J, Oursler KA, Whooley M, Ahuja S, Gutierrez A, Schifman R, Greco J, Rauchman M, Servatius R, Oehlert M, Wallbom A, Fernando R, Morgan T, Stapley T, Sherman S, Anderson G, Sonel E, Boyko E, Meyer L, Gupta S, Fayad J, Hung A, Lichy J, Hurley R, Robey B, Striker R (2019) Harmonizing genetic ancestry and self-identified race/ethnicity in genome-wide association studies. Am J Human Gen 105:763–72
Hunter-Zinck H, Shi Y, Li M, Gorman BR, Ji SG, Sun N, Webster T, Liem A, Hsieh P, Devineni P, Karnam P, Gong X, Radhakrishnan L, Schmidt J, Assimes TL, Huang J, Pan C, Humphries D, Brophy M, Moser J, Muralidhar S, Huang GD, Przygodzki R, Concato J, Gaziano JM, Gelernter J, O’Donnell CJ, Hauser ER, Zhao H, O’Leary TJ, Tsao PS, Pyarajan S (2020) Genotyping array design and data quality control in the Million Veteran Program. Am J Hum Genet 106:535–548
pubmed: 32243820 pmcid: 7118558 doi: 10.1016/j.ajhg.2020.03.004
Chang CC, Chow CC, Tellier LCAM, Vattikuti S, Purcell SM, Lee JJ (2015) Second-generation PLINK: rising to the challenge of larger and richer datasets. Gigascience 4:1–16
doi: 10.1186/s13742-015-0047-8
Zhou W, Nielsen JB, Fritsche LG, Dey R, Maiken E, Wolford BN, Lefaive J, Vandehaar P, Sarah A, Gifford A, Bastarache LA, Wei W, Denny JC, Hveem K, Kang HM, Abecasis GR, Willer CJ (2019) Efficiently controlling for case-control imbalance and sample relatedness in large-scale genetic association studies. Nat Genetics 50:1335–1341
doi: 10.1038/s41588-018-0184-y
Patterson N, Price AL, Reich D (2006) Population structure and eigenanalysis. PLoS Genet 2:190
doi: 10.1371/journal.pgen.0020190
Mbatchou J, Barnard L, Backman J, Marcketta A, Kosmicki JA, Ziyatdinov A, Benner C, O’Dushlaine C, Barber M, Boutkov B, Habegger L, Ferreira M, Baras A, Reid J, Abecasis G, Maxwell E, Marchini J (2021) Computationally efficient whole-genome regression for quantitative and binary traits. Nat Genet 53. https://doi.org/10.1038/s41588-021-00870-7
Willer CJ, Li Y, Abecasis GR (2010) METAL: fast and efficient meta-analysis of genomewide association scans. Bioinformatics 26:2190–2191
pubmed: 20616382 pmcid: 2922887 doi: 10.1093/bioinformatics/btq340
Bulik-Sullivan BK, Loh P-R, Finucane HK, Ripke S, Yang J, Patterson N, Daly MJ, Price AL, Neale BM (2015) LD Score regression distinguishes confounding from polygenicity in genome-wide association studies. Nat Genet 47:291–295
pubmed: 25642630 pmcid: 4495769 doi: 10.1038/ng.3211
Pruim RJ, Welch RP, Sanna S, Teslovich TM, Chines PS, Gliedt TP, Boehnke M, Abecasis GR, Willer CJ (2010) LocusZoom: regional visualization of genome-wide association scan results. Bioinformatics 26(18):2336–2337.  https://doi.org/10.1093/bioinformatics/btq419
Finucane, H, Bulik-Sullivan B, Gusev A, Trynka G, Reshef Y et al (2015) Partitioning heritability by functional annotation using genome-wide association summary statistics. Nat Genet 47:1228–35
Wells HRR, Freidin MB, Zainul Abidin FN et al (2019) GWAS identifies 44 independent associated genomic loci for self-reported adult hearing difficulty in UK Biobank. Am J Hum Genet 105(4):788–802. https://doi.org/10.1016/j.ajhg.2019.09.008
doi: 10.1016/j.ajhg.2019.09.008 pubmed: 31564434 pmcid: 6817556
Clifford RE, Maihofer AX, Stein MB, Ryan AF, Nievergelt CM (2020) Novel risk loci in tinnitus and causal inference with neuropsychiatric disorders among adults of European ancestry. JAMA Otolaryngol Head Neck Surg 146:1015–1025
pubmed: 32970095 pmcid: 7516809 doi: 10.1001/jamaoto.2020.2920
Peyrot WJ, Price AL (2021) Identifying loci with different allele frequencies among cases of eight psychiatric disorders using CC-GWAS. Nat Genet 53:445–454
pubmed: 33686288 pmcid: 8038973 doi: 10.1038/s41588-021-00787-1
Hukku A, Pividori M, Luca F, Pique-Regi R, Im HK, Wen X (2021) Probabilistic colocalization of genetic variants from complex and molecular traits: promise and limitations. Am J Hum Genet 108:25–35
pubmed: 33308443 doi: 10.1016/j.ajhg.2020.11.012
Pividori M, Rajagopal PS, Barbeira A, Liang Y, Melia O, Bastarache L, Park Y, GTEx Consortium, Wen X, Im HK (2020) PhenomeXcan: mapping the genome to the phenome through the transcriptome. Sci Adv 6. https://doi.org/10.1126/sciadv.aba2083
GTEx Consortium (2020) The GTEx Consortium atlas of genetic regulatory effects across human tissues. Science (1979) 369:1318–30
Berisa T, Pickrell JK (2016) Approximately independent linkage disequilibrium blocks in human populations. Bioinformatics 32(2):283–285. https://doi.org/10.1093/bioinformatics/btv546
doi: 10.1093/bioinformatics/btv546 pubmed: 26395773
Zou Y, Carbonetto P, Wang G, Stephens M (2022) Fine-mapping from summary data with the ‘Sum of Single Effects’ model. Published Online First. https://doi.org/10.1371/journal.pgen.1010299
doi: 10.1371/journal.pgen.1010299
Wang G, Sarkar A, Carbonetto P, Stephens M (2020) A simple new approach to variable selection in regression, with application to genetic fine mapping. J R Stat Soc Series B Stat Methodol 82(5):1273–1300. https://doi.org/10.1111/rssb.12388
doi: 10.1111/rssb.12388 pubmed: 37220626 pmcid: 10201948
Watanabe K, Taskesen E, van Bochoven A, Posthuma D (2017) Functional mapping and annotation of genetic associations with FUMA. Nat Commun 8:1826
pubmed: 29184056 pmcid: 5705698 doi: 10.1038/s41467-017-01261-5
de Leeuw CA, Mooij JM, Heskes T, Posthuma D (2015) MAGMA: generalized gene-set analysis of GWAS data. PLoS Comput Biol 11:e1004219
pubmed: 25885710 pmcid: 4401657 doi: 10.1371/journal.pcbi.1004219
Rentzsch P, Witten D, Cooper GM, Shendure J, Kircher M (2019) CADD: predicting the deleteriousness of variants throughout the human genome. Nucleic Acids Res 47. https://doi.org/10.1093/nar/gky1016
Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T, Telling A, Amit I, Lajoie BR, Sabo PJ, Dorschner MO, Sandstrom R, Bernstein B, Bender MA, Groudine M, Gnirke A, Stamatoyannopoulos J, Mirny LA, Lander ES, Dekker J (1979) Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 2009(326):289–293
Orvis J, Gottfried B, Kancherla J, Adkins RS, Song Y, Dror AA, Olley D, Rose K, Chrysostomou E, Kelly MC, Milon B, Matern MS, Azaiez H, Herb B, Colantuoni C, Carter RL, Ament SA, Kelley MW, White O, Bravo HC, Mahurkar A, Hertzano R (2021) gEAR: Gene Expression Analysis Resource portal for community-driven, multi-omic data exploration. Nat Methods 18:843–844
pubmed: 34172972 pmcid: 8996439 doi: 10.1038/s41592-021-01200-9
Watanabe K, Stringer S, Frei O, Umićević Mirkov M, de Leeuw C, Polderman TJC, van der Sluis S, Andreassen OA, Neale BM, Posthuma D (2019) A global overview of pleiotropy and genetic architecture in complex traits. Nat Genet 51:1339–1348
pubmed: 31427789 doi: 10.1038/s41588-019-0481-0
Hromatka BS, Tung JY, Kiefer AK, Do CB, Hinds DA, Eriksson N (2015) Genetic variants associated with motion sickness point to roles for inner ear development, neurological processes and glucose homeostasis. Hum Mol Genet 24:2700–2708
pubmed: 25628336 pmcid: 4383869 doi: 10.1093/hmg/ddv028
Rujescu D, Hartmann AM, Giegling I, Konte B, Herrling M, Himmelein S, Strupp M (2018) Genome-wide association study in vestibular neuritis: involvement of the host factor for HSV-1 replication. Front Neurol 9:1–9
doi: 10.3389/fneur.2018.00591
Strupp M, Maul S, Konte B, Hartmann AM, Giegling I, Wollenteit S, Feil K, Rujescu D (2020) A variation in FGF14 is associated with downbeat nystagmus in a genome-wide association study. Cerebellum 19:348–357
pubmed: 32157568 doi: 10.1007/s12311-020-01113-x
Vietri Rudan M, Barrington C, Henderson S, Ernst C, Odom DT, Tanay A, Hadjur S (2015) Comparative Hi-C reveals that CTCF underlies evolution of chromosomal domain architecture. Cell Rep 10:1297–1309
pubmed: 25732821 pmcid: 4542312 doi: 10.1016/j.celrep.2015.02.004
Vidović T, Ewald CY (2022) Longevity-promoting pathways and transcription factors respond to and control extracellular matrix dynamics during aging and disease. Front Aging 3. https://doi.org/10.3389/fragi.2022.935220
Rudnicki A, Isakov O, Ushakov K, Shivatzki S, Weiss I, Friedman LM, Shomron N, Avraham KB (2014) Next-generation sequencing of small RNAs from inner ear sensory epithelium identifies microRNAs and defines regulatory pathways. BMC Genomics 15:1–12
doi: 10.1186/1471-2164-15-484
Shen J, Scheffer DI, Kwan KY, Corey DP (2015) SHIELD: an integrative gene expression database for inner ear research. Database 2015:1–9
doi: 10.1093/database/bav071
Cai N, Revez JA, Adams MJ et al (2020) Minimal phenotyping yields genome-wide association signals of low specificity for major depression. Nat Genet 52(4):437–447. https://doi.org/10.1038/s41588-020-0594-5
doi: 10.1038/s41588-020-0594-5 pubmed: 32231276 pmcid: 7906795
Agrawal Y, Carey JP, della Santina CC, Schubert MC, Minor LB. (2009) Disorders of balance and vestibular function in US adults: data from the National Health and Nutrition Examination Survey, 2001–2004. Arch Intern Med 169:938–944
pubmed: 19468085 doi: 10.1001/archinternmed.2009.66
Agrawal Y, van de Berg R, Wuyts F, Walther L, Magnusson M, Oh E, Sharpe M, Strupp M (2019) Presbyvestibulopathy: diagnostic criteria consensus document of the classification committee of the Bárány Society. J Vestib Res 29:161–170
pubmed: 31306146 pmcid: 9249286 doi: 10.3233/VES-190672
Kalmanson O, Foster CA (2023) Cupulolithiasis: a critical reappraisal. OTO Open 7. https://doi.org/10.1002/oto2.38
Sessoms PH, Gottshall KR, Sturdy J, Viirre E (2015) Head stabilization measurements as a potential evaluation tool for comparison of persons with TBI and vestibular dysfunction with healthy controls. Mil Med 180:135–142
pubmed: 25747644 doi: 10.7205/MILMED-D-14-00386
Fu W, Zhao J, Hu W, Dai L, Jiang Z, Zhong S, Deng B, Huang Y, Wu W, Yin J (2021) LINC01224/ZNF91 promote stem cell-like properties and drive radioresistance in non-small cell lung cancer. Cancer Manag Res 13:5671–5681
pubmed: 34285587 pmcid: 8286114 doi: 10.2147/CMAR.S313744
Edwards SL, Beesley J, French JD, Dunning AM (2013) Beyond GWASs: illuminating the dark road from association to function. Am J Hum Genet 93(5):779–97.  https://doi.org/10.1016/j.ajhg.2013.10.012 . PMID: 24210251; PMCID: PMC3824120
He D, Wu D, Muller S, Wang L, Saha P, Ahanger SH, Liu SJ, Cui M, Hong SJ, Jain M, Olson HE, Akeson M, Costello JF, Diaz A, Lim DA (2021) miRNA-independent function of long noncoding pri-miRNA loci. Proc Natl Acad Sci 118.  https://doi.org/10.1073/pnas.2017562118
Hunt SE, McLaren W, Gil L, Thormann A, Schuilenburg H, Sheppard D, Parton A, Armean IM, Trevanion SJ, Flicek P, Cunningham F (2018) Ensembl variation resources. Database (Oxford) 2018:bay119. https://doi.org/10.1093/database/bay119
Walsh KM, Zhang C, Calvocoressi L, Hansen HM, Berchuck A, Schildkraut JM, Bondy ML, Wrensch M, Wiemels JL, Claus EB (2022) Pleiotropic MLLT10 variation confers risk of meningioma and estrogen-mediated cancers. Neurooncol Adv 4. https://doi.org/10.1093/noajnl/vdac044
Stankiewicz P, Khan TN, Szafranski P, Slattery L, Streff H, Vetrini F, Bernstein JA, Brown CW, Rosenfeld JA, Rednam S, Scollon S, Bergstrom KL, Parsons DW, Plon SE, Vieira MW, Quaio CRDC, Baratela WAR, Acosta Guio JC, Armstrong R, Mehta SG, Rump P, Pfundt R, Lewandowski R, Fernandes EM, Shinde DN, Tang S, Hoyer J, Zweier C, Reis A, Bacino CA, Xiao R, Breman AM, Smith JL, Katsanis N, Bostwick B, Popp B, Davis EE, Yang Y (2017) Haploinsufficiency of the chromatin remodeler BPTF causes syndromic developmental and speech delay, postnatal microcephaly, and dysmorphic features. Am J Hum Genet 101:503–515
pubmed: 28942966 doi: 10.1016/j.ajhg.2017.08.014
Schmoker AM, Weinert JL, Markwood JM, Albretsen KS, Lunde ML, Weir ME, Ebert AM, Hinkle KL, Ballif BA (2020) FYN and ABL regulate the interaction networks of the DCBLD receptor family. Mol Cell Proteomics 19:1586–1601
pubmed: 32606017 pmcid: 8015000 doi: 10.1074/mcp.RA120.002163

Auteurs

Royce Clifford (R)

Department of Otolaryngology-Head and Neck Surgery, University of California San Diego, La Jolla, CA, 92093, USA. r2clifford@health.ucsd.edu.
Research Dept, Veteran Administration Hospitals, San Diego, CA, 92161, USA. r2clifford@health.ucsd.edu.

Daniel Munro (D)

Dept. of Psychiatry, University of California San Diego, La Jolla, CA, 92093, USA.
Dept. of Integrative Structural and Computational Biology, Scripps Research, La Jolla, CA, 92093, USA.

Daniel Dochtermann (D)

Veterans Administrations Hospitals, Million Veteran Program, Boston, MA, 02130, USA.

Poornima Devineni (P)

Veterans Administrations Hospitals, Million Veteran Program, Boston, MA, 02130, USA.

Saiju Pyarajan (S)

Veterans Administrations Hospitals, Million Veteran Program, Boston, MA, 02130, USA.

Francesca Telese (F)

Dept. of Psychiatry, University of California San Diego, La Jolla, CA, 92093, USA.

Abraham A Palmer (AA)

Dept. of Psychiatry, University of California San Diego, La Jolla, CA, 92093, USA.
Institute for Genomic Medicine, University of California San Diego, La Jolla, CA, 92093, USA.

Pejman Mohammadi (P)

Center for Immunity and Immunotherapies, Seattle Children's Research Institute, Seattle, WA, 98101, USA.
Department of Pediatrics, University of Washington School of Medicine, Seattle, WA, 98195, USA.

Rick Friedman (R)

Department of Otolaryngology-Head and Neck Surgery, University of California San Diego, La Jolla, CA, 92093, USA.

Classifications MeSH