Functional analysis of H. sapiens DNA polymerase γ spacer mutation W748S with and without common variant E1143G

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1802, Issue 6, 2010, Pages 545-551

  Palin, Eino J H ^a   Lesonen, Annamari ^a   Farr, Carol L ^b   Euro, Liliya ^a   Suomalainen, Anu ^a,c   Kaguni, Laurie S ^b  

^a UNIVERSITY OF HELSINKI   (Finland)

^b Michigan State University   (United States)

^c HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

Author keywords

Alpers; Ataxia; DNA polymerase ; MIRAS; POLG; POLG1

Indexed keywords

DNA DIRECTED DNA POLYMERASE GAMMA; MITOCHONDRIAL DNA;

AMINO ACID SUBSTITUTION; ARTICLE; ATAXIA; BINDING AFFINITY; CELL MUTANT; CELL VIABILITY; CONTROLLED STUDY; DISEASE SEVERITY; DNA BINDING; ENZYME ACTIVITY; GENE DOSAGE; GENE MUTATION; GENETIC DISORDER; GENETIC VARIABILITY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; MITOCHONDRIAL RECESSIVE ATAXIA SYNDROME; PHENOTYPE; PRIORITY JOURNAL; WILD TYPE;

AMINO ACID SUBSTITUTION; CATALYTIC DOMAIN; CELLS, CULTURED; DNA PRIMERS; DNA, INTERGENIC; DNA, MITOCHONDRIAL; DNA-DIRECTED DNA POLYMERASE; GENES, RECESSIVE; GENETIC VARIATION; HUMANS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; MUTATION, MISSENSE; PROTEIN SUBUNITS; RECOMBINANT PROTEINS; SPINOCEREBELLAR DEGENERATIONS; SYNDROME;

ANIMALIA; HOMO SAPIENS;

EID: 77952237939     PISSN: 09254439     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbadis.2010.02.003     Document Type: Article

References (34)

1. Kaguni L.S. DNA polymerase gamma, the mitochondrial replicase. Annu. Rev. Biochem. 2004, 73:293-320.
2. Spelbrink J.N., Li F.Y., Tiranti V., Nikali K., Yuan Q.P., Tariq M., Wanrooij S., Garrido N., Comi G., Morandi L., Santoro L., Toscano A., Fabrizi G.M., Somer H., Croxen R., Beeson D., Poulton J., Suomalainen A., Jacobs H.T., Zeviani M., Larsson C. Human mitochondrial DNA deletions associated with mutations in the gene encoding Twinkle, a phage T7 gene 4-like protein localized in mitochondria. Nat. Genet. 2001, 28:223-231.
3. Korhonen J.A., Pham X.H., Pellegrini M., Falkenberg M. Reconstitution of a minimal mtDNA replisome in vitro. EMBO J. 2004, 23:2423-2429.
4. Tiranti V., Rocchi M., DiDonato S., Zeviani M. Cloning of human and rat cDNAs encoding the mitochondrial single-stranded DNA-binding protein (SSB). Gene 1993, 126:219-225.
5. Fan L., Kim S., Farr C., Schaefer K., Randolph K., Tainer J., Kaguni L. A novel processive mechanism for DNA synthesis revealed by structure, modeling and mutagenesis of the accessory subunit of human mitochondrial DNA polymerase. J. Mol. Biol. 2006, 358:1229-1243.
6. Yakubovskaya E., Chen Z., Carrodeguas J.A., Kisker C., Bogenhagen D.F. Functional human mitochondrial DNA polymerase gamma forms a heterotrimer. J. Biol. Chem. 2005, 281:374-382.
7. Luo N., Kaguni L.S. Mutations in the spacer region of Drosophila mitochondrial DNA polymerase affect DNA binding, processivity, and the balance between Pol and Exo function. J. Biol. Chem. 2005, 280:2491-2497.
8. Lamantea E., Tiranti V., Bordoni A., Toscano A., Bono F., Servidei S., Papadimitriou A., Spelbrink H., Silvestri L., Casari G., Comi G.P., Zeviani M. Mutations of mitochondrial DNA polymerase gammaA are a frequent cause of autosomal dominant or recessive progressive external ophthalmoplegia. Ann. Neurol. 2002, 52:211-219.
9. Van Goethem G., Dermaut B., Löfgren A., Martin J.J., Van Broeckhoven C. Mutation of POLG is associated with progressive external ophthalmoplegia characterized by mtDNA deletions. Nat. Genet. 2001, 28:211-212.
10. Van Goethem G., Luoma P., Rantamäki M., Al Memar A., Kaakkola S., Hackman P., Krahe R., Löfgren A., Martin J.J., De Jonghe P., Suomalainen A., Udd B., Van Broeckhoven C. POLG mutations in neurodegenerative disorders with ataxia but no muscle involvement. Neurology 2004, 63:1251-1257.
11. Van Goethem G., Martin J.J., Dermaut B., Löfgren A., Wibail A., Ververken D., Tack P., Dehaene I., Van Zandijcke M., Moonen M., Ceuterick C., De Jonghe P., Van Broeckhoven C. Recessive POLG mutations presenting with sensory and ataxic neuropathy in compound heterozygote patients with progressive external ophthalmoplegia. Neuromuscul. Disord. 2003, 13:133-142.
12. Hakonen A.H., Heiskanen S., Juvonen V., Lappalainen I., Luoma P.T., Rantamaki M., Goethem G.V., Lofgren A., Hackman P., Paetau A., Kaakkola S., Majamaa K., Varilo T., Udd B., Kaariainen H., Bindoff L.A., Suomalainen A. Mitochondrial DNA polymerase W748S mutation: a common cause of autosomal recessive ataxia with ancient European origin. Am. J. Hum. Genet. 2005, 77:430-441.
13. Rantamäki M., Krahe R., Paetau A., Cormand B., Mononen I., Udd B. Adult-onset autosomal recessive ataxia with thalamic lesions in a Finnish family. Neurology 2001, 57:1043-1049.
14. Hakonen A.H., Isohanni P., Paetau A., Herva R., Suomalainen A., Lönnqvist T. Recessive Twinkle mutations in early onset encephalopathy with mtDNA depletion. Brain 2007, 130:3032-3040.
15. Campuzano V., Montermini L., Moltò M.D., Pianese L., Cossée M., Cavalcanti F., Monros E., Rodius F., Duclos F., Monticelli A., Zara F., Cañizares J., Koutnikova H., Bidichandani S.I., Gellera C., Brice A., Trouillas P., De Michele G., Filla A., De Frutos R., Palau F., Patel P.I., Di Donato S., Mandel J.L., Cocozza S., Koenig M., Pandolfo M. Friedreich's ataxia: autosomal recessive disease caused by an intronic GAA triplet repeat expansion. Science 1996, 271:1423-1427.
16. Foury F., Cazzalini O. Deletion of the yeast homologue of the human gene associated with Friedreich's ataxia elicits iron accumulation in mitochondria. FEBS Lett. 1997, 411:373-377.
17. A.H. Hakonen, S. Goffart, S. Marjavaara, A. Paetau, H. Cooper, K. Mattila, M. Lampinen, A. Sajantila, T. Lönnqvist, J.N. Spelbrink, A. Suomalainen, Infantile-onset spinocerebellar ataxia and mitochondrial recessive ataxia syndrome are associated with neuronal complex I defect and mtDNA depletion, Hum. Mol. Genet. 17 (2008) 3822-3835.
18. Chan S.S.L., Longley M.J., Copeland W.C. The common A467T mutation in the human mitochondrial DNA polymerase (POLG) compromises catalytic efficiency and interaction with the accessory subunit. J. Biol. Chem. 2005, 280:31341-31346.
19. Chan S.S.L., Longley M.J., Copeland W.C. Modulation of the W748S mutation in DNA polymerase gamma by the E1143G polymorphism in mitochondrial disorders. Hum. Mol. Genet. 2006, 15:3473-3483.
20. P.T. Luoma, N. Luo, W.N. Löscher, C.L. Farr, R. Horvath, J. Wanschitz, S. Kiechl, L.S. Kaguni, A. Suomalainen, Functional defects due to spacer-region mutations of human mitochondrial DNA polymerase in a family with an ataxia-myopathy syndrome, Hum. Mol. Genet. 14 (2005) 1907-1920.
21. Naviaux R.K., Nguyen K.V. POLG mutations associated with Alpers' syndrome and mitochondrial DNA depletion. Ann. Neurol. 2004, 55:706-712.
22. Nguyen K.V., Ostergaard E., Ravn S.H., Balslev T., Danielsen E.R., Vardag A., McKiernan P.J., Gray G., Naviaux R.K. POLG mutations in Alpers syndrome. Neurology 2005, 65:1493-1495.
23. Longley M., Ropp P., Lim S., Copeland W. Characterization of the native and recombinant catalytic subunit of human DNA polymerase gamma: identification of residues critical for exonuclease activity and dideoxynucleotide sensitivity. Biochemistry 1998, 37:10529-10539.
24. Lee Y.-S., Kennedy W.D., Yin Y.W. Structural insight into processive human mitochondrial DNA synthesis and disease-related polymerase mutations. Cell 2009, 139:312-324.
25. P. Luoma, A. Melberg, J.O. Rinne, J.A. Kaukonen, N.N. Nupponen, R.M. Chalmers, A. Oldfors, I. Rautakorpi, L. Peltonen, K. Majamaa, H. Somer, A. Suomalainen, Parkinsonism, premature menopause, and mitochondrial DNA polymerase gamma mutations: clinical and molecular genetic study, Lancet 364 (2004) 875-882.
26. Baruffini E., Ferrero I., Foury F. Mitochondrial DNA defects in Saccharomyces cerevisiae caused by functional interactions between DNA polymerase gamma mutations associated with disease in human. Biochim. Biophys. Acta 2007, 1772:1225-1235.
27. Hakonen A.H., Davidzon G., Salemi R., Bindoff L.A., Van Goethem G., Dimauro S., Thorburn D.R., Suomalainen A. Abundance of the POLG disease mutations in Europe, Australia, New Zealand, and the United States explained by single ancient European founders. Eur. J. Hum. Genet. 2007, 15:779-783.
28. Nikali K., Suomalainen A., Saharinen J., Kuokkanen M., Spelbrink J.N., Lönnqvist T., Peltonen L. Infantile onset spinocerebellar ataxia is caused by recessive mutations in mitochondrial proteins Twinkle and Twinky. Hum. Mol. Genet. 2005, 14:2981-2990.
29. Wang Y., Kaguni L. Baculovirus expression reconstitutes Drosophila mitochondrial DNA polymerase. J. Biol. Chem. 1999, 274:28972-28977.
30. Fan L., Sanschagrin P.C., Kaguni L.S., Kuhn L.A. The accessory subunit of mtDNA polymerase shares structural homology with aminoacyl-tRNA synthetases: implications for a dual role as a primer recognition factor and processivity clamp. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:9527-9532.
31. Wernette C., Kaguni L. A mitochondrial DNA polymerase from embryos of Drosophila melanogaster. Purification, subunit structure, and partial characterization. J. Biol. Chem. 1986, 261:14764-14770.
32. Boulet L., Karpati G., Shoubridge E.A. Distribution and threshold expression of the tRNA(Lys) mutation in skeletal muscle of patients with myoclonic epilepsy and ragged-red fibers (MERRF). Am. J. Hum. Genet. 1992, 51:1187-1200.
33. W. Humphrey, A. Dalke, K. Schulten, VMD: visual molecular dynamics, Journal of molecular graphics 14 (1996) 33-38, 27-38.
34. Brieba L.G., Eichman B.F., Kokoska R.J., Doublié S., Kunkel T.A., Ellenberger T. Structural basis for the dual coding potential of 8-oxoguanosine by a high-fidelity DNA polymerase. EMBO J. 2004, 23:3452-3461.