In vivo modelling of ATP1A3 G316S-induced ataxia in C. Elegans using CRISPR/Cas9-mediated homologous recombination reveals dominant loss of function defects

PLoS ONE

Volumn 11, Issue 12, 2016, Pages

  Sorkaç, Altar ^a   Alcantara, Ivan C ^a   Hart, Anne C ^a  

^a BROWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ALDICARB; ATP1A3 PROTEIN, HUMAN;

ADULT; ALLELE; AMINO ACID SUBSTITUTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATAXIA; ATP1A3 GENE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; CRISPR CAS SYSTEM; DISEASE MODEL; EAT 6 GENE; GENE; GENE DOSAGE; GENE FUNCTION; HETEROZYGOTE; HOMOLOGOUS RECOMBINATION; IN VIVO STUDY; LOSS OF FUNCTION MUTATION; NEUROMUSCULAR JUNCTION; NONHUMAN; RNA EDITING; YOUNG ADULT; ANIMAL; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; DOMINANT GENE; GENETICS; HUMAN; MUTATION;

ALLELES; ANIMALS; CAENORHABDITIS ELEGANS; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; GENES, DOMINANT; HETEROZYGOTE; HOMOLOGOUS RECOMBINATION; HUMANS; MUTATION; SODIUM-POTASSIUM-EXCHANGING ATPASE;

EID: 85004011277     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0167963     Document Type: Article

References (24)

1. Gahl WA, Markello TC, Toro C, Fajardo KF, Sincan M, Gill F, et al. The National Institutes of Health Undiagnosed Diseases Program: insights into rare diseases. Genet Med. 2012; 14(1):51-9. PubMed Central PMCID: PMCPMC4098846. doi: 10.1038/gim.0b013e318232a005 PMID: 22237431
2. Sweadner KJ, Toro C, Whitlow CT, Snively BM, Cook JF, Ozelius LJ, et al. ATP1A3 Mutation in Adult Rapid-Onset Ataxia. PloS one. 2016; 11(3):e0151429. PubMed Central PMCID: PMCPMC4798776. doi: 10.1371/journal.pone.0151429 PMID: 26990090
3. Bottger P, Tracz Z, Heuck A, Nissen P, Romero-Ramos M, Lykke-Hartmann K. Distribution of Na/K-ATPase alpha 3 isoform, a sodium-potassium P-type pump associated with rapid-onset of dystonia parkinsonism (RDP) in the adult mouse brain. The Journal of comparative neurology. 2011; 519(2):376-404. doi: 10.1002/cne.22524 PMID: 21165980
4. Heinzen EL, Arzimanoglou A, Brashear A, Clapcote SJ, Gurrieri F, Goldstein DB, et al. Distinct neurological disorders with ATP1A3 mutations. The Lancet Neurology. 2014; 13(5):503-14. PubMed Central PMCID: PMC4238309. doi: 10.1016/S1474-4422(14)70011-0 PMID: 24739246
5. de Carvalho Aguiar P, Sweadner KJ, Penniston JT, Zaremba J, Liu L, Caton M, et al. Mutations in the Na+/K+ -ATPase alpha3 gene ATP1A3 are associated with rapid-onset dystonia parkinsonism. Neuron. 2004; 43(2):169-75. doi: 10.1016/j.neuron.2004.06.028 PMID: 15260953
6. Heinzen EL, Swoboda KJ, Hitomi Y, Gurrieri F, Nicole S, de Vries B, et al. De novo mutations in ATP1A3 cause alternating hemiplegia of childhood. Nat Genet. 2012; 44(9):1030-4. PubMed Central PMCID: PMC3442240. doi: 10.1038/ng.2358 PMID: 22842232
7. Dimitriadi M, Hart AC. Neurodegenerative disorders: insights from the nematode Caenorhabditis elegans. Neurobiol Dis. 2010; 40(1):4-11. PubMed Central PMCID: PMCPMC2926245. doi: 10.1016/j. nbd.2010.05.012 PMID: 20493260
8. Link CD. Expression of human beta-amyloid peptide in transgenic Caenorhabditis elegans. Proc Natl Acad Sci U S A. 1995; 92(20):9368-72. PubMed Central PMCID: PMCPMC40986. PMID: 7568134
9. Faber PW, Alter JR, MacDonald ME, Hart AC. Polyglutamine-mediated dysfunction and apoptotic death of a Caenorhabditis elegans sensory neuron. Proc Natl Acad Sci U S A. 1999; 96(1):179-84. PubMed Central PMCID: PMCPMC15113. PMID: 9874792
10. Kraemer BC, Zhang B, Leverenz JB, Thomas JH, Trojanowski JQ, Schellenberg GD. Neurodegeneration and defective neurotransmission in a Caenorhabditis elegans model of tauopathy. Proc Natl Acad Sci U S A. 2003; 100(17):9980-5. PubMed Central PMCID: PMCPMC187908. doi: 10.1073/pnas. 1533448100 PMID: 12872001
11. Wang J, Farr GW, Hall DH, Li F, Furtak K, Dreier L, et al. An ALS-linked mutant SOD1 produces a locomotor defect associated with aggregation and synaptic dysfunction when expressed in neurons of Caenorhabditis elegans. PLoS genetics. 2009; 5(1):e1000350. PubMed Central PMCID: PMCPMC2621352. doi: 10.1371/journal.pgen.1000350 PMID: 19165329
12. Lakso M, Vartiainen S, Moilanen AM, Sirvio J, Thomas JH, Nass R, et al. Dopaminergic neuronal loss and motor deficits in Caenorhabditis elegans overexpressing human alpha-synuclein. Journal of neurochemistry. 2003; 86(1):165-72. PMID: 12807436
13. Avery L. The genetics of feeding in Caenorhabditis elegans. Genetics. 1993; 133(4):897-917. PubMed Central PMCID: PMC1205408. PMID: 8462849
14. Davis MW, Somerville D, Lee RY, Lockery S, Avery L, Fambrough DM. Mutations in the Caenorhabditis elegans Na,K-ATPase alpha-subunit gene, eat-6, disrupt excitable cell function. J Neurosci. 1995; 15 (12):8408-18. PMID: 8613772
15. Doi M, Iwasaki K. Na+/K+ ATPase regulates the expression and localization of acetylcholine receptors in a pump activity-independent manner. Molecular and cellular neurosciences. 2008; 38(4):548-58. PubMed Central PMCID: PMC2569892. doi: 10.1016/j.mcn.2008.05.003 PMID: 18599311
16. Govorunova EG, Moussaif M, Kullyev A, Nguyen KC, McDonald TV, Hall DH, et al. A homolog of FHM2 is involved in modulation of excitatory neurotransmission by serotonin in C. elegans. PloS one. 2010; 5 (4):e10368. PubMed Central PMCID: PMCPMC2860991. doi: 10.1371/journal.pone.0010368 PMID: 20442779
17. Friedland AE, Tzur YB, Esvelt KM, Colaiacovo MP, Church GM, Calarco JA. Heritable genome editing in C. elegans via a CRISPR-Cas9 system. Nature methods. 2013; 10(8):741-3. PubMed Central PMCID: PMC3822328. doi: 10.1038/nmeth.2532 PMID: 23817069
18. Dickinson DJ, Ward JD, Reiner DJ, Goldstein B. Engineering the Caenorhabditis elegans genome using Cas9-triggered homologous recombination. Nature methods. 2013; 10(10):1028-34. PubMed Central PMCID: PMC3905680. doi: 10.1038/nmeth.2641 PMID: 23995389
19. Arribere JA, Bell RT, Fu BX, Artiles KL, Hartman PS, Fire AZ. Efficient marker-free recovery of custom genetic modifications with CRISPR/Cas9 in Caenorhabditis elegans. Genetics. 2014; 198(3):837-46. PubMed Central PMCID: PMC4224173. doi: 10.1534/genetics.114.169730 PMID: 25161212
20. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. A programmable dual-RNAguided DNA endonuclease in adaptive bacterial immunity. Science. 2012; 337(6096):816-21. doi: 10. 1126/science.1225829 PMID: 22745249
21. Fu Y, Foden JA, Khayter C, Maeder ML, Reyon D, Joung JK, et al. High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat Biotechnol. 2013; 31(9):822-6. PubMed Central PMCID: PMCPMC3773023. doi: 10.1038/nbt.2623 PMID: 23792628
22. Shima Y, Tada Y, Furuki M, Hara Y, Ohta H. A missense mutation of the gene for Na+,K(+)-ATPase alpha-subunit causes abnormal feeding behavior in Caenorhabditis elegans. Biochem Biophys Res Commun. 1998; 248(3):778-82. doi: 10.1006/bbrc.1998.8981 PMID: 9704004
23. Ward JD. Rapid and precise engineering of the Caenorhabditis elegans genome with lethal mutation co-conversion and inactivation of NHEJ repair. Genetics. 2015; 199(2):363-77. PubMed Central PMCID: PMCPMC4317648. doi: 10.1534/genetics.114.172361 PMID: 25491644
24. Frokjaer-Jensen C, Davis MW, Hopkins CE, Newman BJ, Thummel JM, Olesen SP, et al. Single-copy insertion of transgenes in Caenorhabditis elegans. Nat Genet. 2008; 40(11):1375-83. PubMed Central PMCID: PMC2749959. doi: 10.1038/ng.248 PMID: 18953339