Origins and Spread of Machado-Joseph Disease Ancestral Mutations Events

Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1049)

Abstract

Machado-Joseph disease (MJD) is the most common autosomal dominant spinocerebellar ataxia reported worldwide, but it shows marked geographic differences in prevalence. The study of ancestral origins and spreading routes of MJD mutational events has contributed to explain such differences. During human evolution, at least two independent de novo MJD expansions occurred in distinct haplotype backgrounds: TTACAC and GTGGCA (named Joseph and Machado lineages). The most ancient Joseph lineage, probably of Asian origin, has been introduced recently in Europe, where founder effects are responsible for the high MJD prevalence, as occurs in the Portuguese/Azorean island of Flores and Northeastern mainland. The Machado lineage is geographically more restricted, with most known families in Portugal (island of São Miguel and along the Tagus valley). The hypothesis of other mutational origins has been raised, namely to explain the disease among Australian aborigines; however, a comprehensive haplotype study suggested the introduction of the Joseph lineage in that community via Asia. Also, additional SNP-based haplotypes (TTAGAC, TTGGAC and GTGCCA) were observed in other MJD families, but phylogenetic analysis with more polymorphic flanking markers did not point to independent mutational events, reinforcing the hypothesis of a very low mutation rate underlying this repeat expansion locus.

Keywords

MJD SCA3 Mutational origins Haplotype Geographic clusters Prevalence 

References

  1. 1.
    Nakano KK, Dawson DM, Spence A (1972) Machado disease. A hereditary ataxia in Portuguese emigrants to Massachusetts. Neurology 22:49–55CrossRefGoogle Scholar
  2. 2.
    Woods BT, Schaumburg HH (1972) Nigro-spino-dentatal degeneration with nuclear ophthalmoplegia. A unique and partially treatable clinico-pathological entity. J Neurol Sci 17:149–166CrossRefGoogle Scholar
  3. 3.
    Rosenberg RN, Nyhan WL, Bay C, Shore P (1976) Autosomal dominant striatonigral degeneration. A clinical, pathologic, and biochemical study of a new genetic disorder. Neurology 26:703–714CrossRefGoogle Scholar
  4. 4.
    IJDF: International Joseph Diseases Newsletter (1978)Google Scholar
  5. 5.
    Coutinho P (1992) Doença de Machado-Joseph- Tentativa de definição. University of Porto PortugalGoogle Scholar
  6. 6.
    Coutinho P, Andrade C (1978) Autosomal dominant system degeneration in Portuguese families of the Azores Islands. A new genetic disorder involving cerebellar, pyramidal, extrapyramidal and spinal cord motor functions. Neurology 28:703–709CrossRefGoogle Scholar
  7. 7.
    Romanul FC, Fowler HL, Radvany J, Feldman RG, Feingold M (1977) Azorean disease of the nervous system. N Engl J Med 296:1505–1508CrossRefGoogle Scholar
  8. 8.
    Lima L, Coutinho P (1980) Clinical criteria for diagnosis of Machado-Joseph disease: report of a non-Azorean Portuguese family. Neurology 30:319–322CrossRefGoogle Scholar
  9. 9.
    Healton EB, Brust JC, Kerr DL, Resor S, Penn A (1980) Presumably Azorean disease in a presumably non-Portuguese family. Neurology 30:1084–1089CrossRefGoogle Scholar
  10. 10.
    Ishino H, Sato M, Mii T, Terano A, Hayahara T (1971) [An autopsy case of Marie’s hereditary ataxia]. Seishin shinkeigaku zasshi = Psychiatria et neurologia Japonica 73:747–757Google Scholar
  11. 11.
    Sakai T, Ohta M, Ishino H (1983) Joseph disease in a non-Portuguese family. Neurology 33:74–80CrossRefGoogle Scholar
  12. 12.
    Yuasa T, Ohama E, Harayama H, Yamada M, Kawase Y, Wakabayashi M, Atsumi T, Miyatake T (1986) Joseph’s disease: clinical and pathological studies in a Japanese family. Ann Neurol 19:152–157CrossRefGoogle Scholar
  13. 13.
    Bharucha NE, Bharucha EP, Bhabha SK (1986) Machado-Joseph-Azorean disease in India. Arch Neurol 43:142–144CrossRefGoogle Scholar
  14. 14.
    Zhao JB, Wang TL, Wang GX (1994) [The pathology of Joseph’s disease in a Chinese family: a report of two autopsy cases]. Zhonghua bing li xue za zhi = Chin J Pathol 23:232–234Google Scholar
  15. 15.
    Burt T, Blumbergs P, Currie B (1993) A dominant hereditary ataxia resembling Machado-Joseph disease in Arnhem Land, Australia. Neurology 43:1750–1752CrossRefGoogle Scholar
  16. 16.
    Goldberg-Stern H, D’Jaldetti R, Melamed E, Gadoth N (1994) Machado-Joseph (Azorean) disease in a Yemenite Jewish family in Israel. Neurology 44:1298–1301CrossRefGoogle Scholar
  17. 17.
    Sequeiros J, Coutinho P (1993) Epidemiology and clinical aspects of Machado-Joseph disease. Adv Neurol 61:139–153PubMedPubMedCentralGoogle Scholar
  18. 18.
    Fergunson F, Critchley M (1929) A clinical study of an heredo-familial disease resembling disseminated sclerosis. Brain 52:203–225CrossRefGoogle Scholar
  19. 19.
    Harding AE (1982) The clinical features and classification of the late onset autosomal dominant cerebellar ataxias. A study of 11 families, including descendants of the ‘the Drew family of Walworth’. Brain 105:1–28CrossRefGoogle Scholar
  20. 20.
    Giunti P, Sweeney MG, Harding AE (1995) Detection of the Machado-Joseph disease/spinocerebellar ataxia three trinucleotide repeat expansion in families with autosomal dominant motor disorders, including the Drew family of Walworth. Brain 118(Pt 5):1077–1085CrossRefGoogle Scholar
  21. 21.
    Wang J, Shen L, Lei L, Xu Q, Zhou J, Liu Y, Guan W, Pan Q, Xia K, Tang B et al (2011) Spinocerebellar ataxias in mainland China: an updated genetic analysis among a large cohort of familial and sporadic cases. Zhong nan da xue xue bao Yi xue ban = J Cent S Univ Med Sci 36:482–489Google Scholar
  22. 22.
    de Castilhos RM, Furtado GV, Gheno TC, Schaeffer P, Russo A, Barsottini O, Pedroso JL, Salarini DZ, Vargas FR, de Lima MA et al (2014) Spinocerebellar ataxias in Brazil–frequencies and modulating effects of related genes. Cerebellum 13:17–28CrossRefGoogle Scholar
  23. 23.
    Vale J, Bugalho P, Silveira I, Sequeiros J, Guimaraes J, Coutinho P (2010) Autosomal dominant cerebellar ataxia: frequency analysis and clinical characterization of 45 families from Portugal. Eur J Neurol 17:124–128CrossRefGoogle Scholar
  24. 24.
    Boonkongchuen P, Pongpakdee S, Jindahra P, Papsing C, Peerapatmongkol P, Wetchaphanphesat S, Paiboonpol S, Dejthevaporn C, Tanprawate S, Nudsasarn A et al (2014) Clinical analysis of adult-onset spinocerebellar ataxias in Thailand. BMC Neurol 14:75CrossRefGoogle Scholar
  25. 25.
    Schols L, Amoiridis G, Buttner T, Przuntek H, Epplen JT, Riess O (1997) Autosomal dominant cerebellar ataxia: phenotypic differences in genetically defined subtypes? Ann Neurol 42:924–932CrossRefGoogle Scholar
  26. 26.
    Zhao Y, Tan EK, Law HY, Yoon CS, Wong MC, Ng I (2002) Prevalence and ethnic differences of autosomal-dominant cerebellar ataxia in Singapore. Clin Genet 62:478–481CrossRefGoogle Scholar
  27. 27.
    Tsai HF, Liu CS, Leu TM, Wen FC, Lin SJ, Liu CC, Yang DK, Li C, Hsieh M (2004) Analysis of trinucleotide repeats in different SCA loci in spinocerebellar ataxia patients and in normal population of Taiwan. Acta Neurol Scand 109:355–360CrossRefGoogle Scholar
  28. 28.
    Stevanin G, Durr A, David G, Didierjean O, Cancel G, Rivaud S, Tourbah A, Warter JM, Agid Y, Brice A (1997) Clinical and molecular features of spinocerebellar ataxia type 6. Neurology 49:1243–1246CrossRefGoogle Scholar
  29. 29.
    Maruyama H, Izumi Y, Morino H, Oda M, Toji H, Nakamura S, Kawakami H (2002) Difference in disease-free survival curve and regional distribution according to subtype of spinocerebellar ataxia: a study of 1,286 Japanese patients. Am J Med Genet 114:578–583CrossRefGoogle Scholar
  30. 30.
    van de Warrenburg BP, Sinke RJ, Verschuuren-Bemelmans CC, Scheffer H, Brunt ER, Ippel PF, Maat-Kievit JA, Dooijes D, Notermans NC, Lindhout D et al (2002) Spinocerebellar ataxias in the Netherlands: prevalence and age at onset variance analysis. Neurology 58:702–708Google Scholar
  31. 31.
    Paradisi I, Ikonomu V, Arias S (2016) Spinocerebellar ataxias in Venezuela: genetic epidemiology and their most likely ethnic descent. J Hum Genet 61:215–222CrossRefGoogle Scholar
  32. 32.
    Moseley ML, Benzow KA, Schut LJ, Bird TD, Gomez CM, Barkhaus PE, Blindauer KA, Labuda M, Pandolfo M, Koob MD et al (1998) Incidence of dominant spinocerebellar and Friedreich triplet repeats among 361 ataxia families. Neurology 51:1666–1671CrossRefGoogle Scholar
  33. 33.
    Pujana MA, Corral J, Gratacos M, Combarros O, Berciano J, Genis D, Banchs I, Estivill X, Volpini V (1999) Spinocerebellar ataxias in Spanish patients: genetic analysis of familial and sporadic cases (The Ataxia Study Group). Hum Genet 104:516–522CrossRefGoogle Scholar
  34. 34.
    Koutsis G, Kladi A, Karadima G, Houlden H, Wood NW, Christodoulou K, Panas M (2014) Friedreich’s ataxia and other hereditary ataxias in Greece: an 18-year perspective. J Neurol Sci 336:87–92CrossRefGoogle Scholar
  35. 35.
    Bauer PO, Zumrova A, Matoska V, Marikova T, Krilova S, Boday A, Singh B, Goetz P (2005) Absence of spinocerebellar ataxia type 3/Machado-Joseph disease within ataxic patients in the Czech population. Eur J Neurol 12:851–857CrossRefGoogle Scholar
  36. 36.
    Votsi C, Zamba-Papanicolaou E, Georghiou A, Kyriakides T, Papacostas S, Kleopa KA, Pantzaris M, Christodoulou K (2012) Investigation of SCA10 in the Cypriot population: further exclusion of SCA dynamic repeat mutations. J Neurol Sci 323:154–157CrossRefGoogle Scholar
  37. 37.
    Sumathipala DS, Abeysekera GS, Jayasekara RW, Tallaksen CM, Dissanayake VH (2013) Autosomal dominant hereditary ataxia in Sri Lanka. BMC Neurol 13:39CrossRefGoogle Scholar
  38. 38.
    Sulek-Piatkowska A, Zdzienicka E, Raczynska-Rakowicz M, Krysa W, Rajkiewicz M, Szirkowiec W, Zaremba J (2010) The occurrence of spinocerebellar ataxias caused by dynamic mutations in Polish patients. Neurol Neurochir Pol 44:238–245PubMedGoogle Scholar
  39. 39.
    Juvonen V, Hietala M, Kairisto V, Savontaus ML (2005) The occurrence of dominant spinocerebellar ataxias among 251 Finnish ataxia patients and the role of predisposing large normal alleles in a genetically isolated population. Acta Neurol Scand 111:154–162CrossRefGoogle Scholar
  40. 40.
    Dragasevic NT, Culjkovic B, Klein C, Ristic A, Keckarevic M, Topisirovic I, Vukosavic S, Svetel M, Kock N, Stefanova E et al (2006) Frequency analysis and clinical characterization of different types of spinocerebellar ataxia in Serbian patients. Mov Disord: Official J Mov Disord Soc 21:187–191CrossRefGoogle Scholar
  41. 41.
    Pazarci P, Kasap H, Koc AF, Altunbasak S, Erkoc MA (2015) Mutation analysis of 6 spinocerebellar ataxia (SCA) types in patients from southern Turkey. Turk J Med Sci 45:1228–1233CrossRefGoogle Scholar
  42. 42.
    Smith DC, Greenberg LJ, Bryer A (2016) The hereditary ataxias: where are we now? Four decades of local research. S Afr Med J = Suid-Afrikaanse tydskrif vir geneeskunde 106:S38–41CrossRefGoogle Scholar
  43. 43.
    Gaspar C, Lopes-Cendes I, Hayes S, Goto J, Arvidsson K, Dias A, Silveira I, Maciel P, Coutinho P, Lima M et al (2001) Ancestral origins of the Machado-Joseph disease mutation: a worldwide haplotype study. Am J Hum Genet 68:523–528CrossRefGoogle Scholar
  44. 44.
    Nachman MW, Crowell SL (2000) Estimate of the mutation rate per nucleotide in humans. Genetics 156:297–304PubMedPubMedCentralGoogle Scholar
  45. 45.
    Rubinsztein DC, Leggo J, Coetzee GA, Irvine RA, Buckley M, Ferguson-Smith MA (1995) Sequence variation and size ranges of CAG repeats in the Machado-Joseph disease, spinocerebellar ataxia type 1 and androgen receptor genes. Hum Mol Genet 4:1585–1590CrossRefGoogle Scholar
  46. 46.
    Limprasert P, Nouri N, Heyman RA, Nopparatana C, Kamonsilp M, Deininger PL, Keats BJ (1996) Analysis of CAG repeat of the Machado-Joseph gene in human, chimpanzee and monkey populations: a variant nucleotide is associated with the number of CAG repeats. Hum Mol Genet 5:207–213CrossRefGoogle Scholar
  47. 47.
    Djian P, Hancock JM, Chana HS (1996) Codon repeats in genes associated with human diseases: fewer repeats in the genes of nonhuman primates and nucleotide substitutions concentrated at the sites of reiteration. Proc Natl Acad Sci USA 93:417–421CrossRefGoogle Scholar
  48. 48.
    Martins S, Calafell F, Gaspar C, Wong VC, Silveira I, Nicholson GA, Brunt ER, Tranebjaerg L, Stevanin G, Hsieh M et al (2007) Asian origin for the worldwide-spread mutational event in Machado-Joseph disease. Arch Neurol 64:1502–1508CrossRefGoogle Scholar
  49. 49.
    Sequeiros J (1989) Análise genética das causas da vairiação fenotípica na doença de Machado-Joseph. Ph.D. thesis, Universidade do PortoGoogle Scholar
  50. 50.
    Martins S, Soong BW, Wong VC, Giunti P, Stevanin G, Ranum LP, Sasaki H, Riess O, Tsuji S, Coutinho P et al (2012) Mutational origin of Machado-Joseph disease in the Australian Aboriginal communities of Groote Eylandt and Yirrkala. Arch Neurol 69:746–751CrossRefGoogle Scholar
  51. 51.
    Chakravarty A, Mukherjee SC (2002) Autosomal dominant cerebellar ataxias in ethnic Bengalees in West Bengal—an Eastern Indian state. Acta Neurol Scand 105:202–208CrossRefGoogle Scholar
  52. 52.
    Jayadev S, Michelson S, Lipe H, Bird T (2006) Cambodian founder effect for spinocerebellar ataxia type 3 (Machado-Joseph disease). J Neurol Sci 250:110–113CrossRefGoogle Scholar
  53. 53.
    Bhargava A, Fuentes FF (2010) Mutational dynamics of microsatellites. Mol Biotechnol 44:250–266CrossRefGoogle Scholar
  54. 54.
    Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462PubMedPubMedCentralGoogle Scholar
  55. 55.
    Putman AI, Carbone I (2014) Challenges in analysis and interpretation of microsatellite data for population genetic studies. Ecol Evol 4:4399–4428PubMedPubMedCentralGoogle Scholar
  56. 56.
    Illarioshkin SN, Slominsky PA, Ovchinnikov IV, Markova ED, Miklina NI, Klyushnikov SA, Shadrina M, Vereshchagin NV, Limborskaya SA, Ivanova-Smolenskaya IA (1996) Spinocerebellar ataxia type 1 in Russia. J Neurol 243:506–510CrossRefGoogle Scholar
  57. 57.
    Saber S, Rostami M, Dehghan MM, Hooshiar KB, Banoie M, Houshmand M (2006) Molecular investigation SCA in 26 patients suspected to SCA in Iran. Eur J Hum Genet 14:275Google Scholar
  58. 58.
    Kiloh LG, Lethlean AK, Morgan G, Cawte JE, Harris M (1980) An endemic neurological disorder in tribal Australian aborigines. J Neurol Neurosurg Psychiatry 43:661–668CrossRefGoogle Scholar
  59. 59.
    Burt T, Currie B, Kilburn C, Lethlean AK, Dempsey K, Blair I, Cohen A, Nicholson G (1996) Machado-Joseph disease in east Arnhem Land, Australia: chromosome 14q32.1 expanded repeat confirmed in four families. Neurology 46:1118–1122CrossRefGoogle Scholar
  60. 60.
    Buhmann C, Bussopulos A, Oechsner M (2003) Dopaminergic response in Parkinsonian phenotype of Machado-Joseph disease. Mov Disord: Official J Mov Disord Soc 18:219–221CrossRefGoogle Scholar
  61. 61.
    Subramony SH, Hernandez D, Adam A, Smith-Jefferson S, Hussey J, Gwinn-Hardy K, Lynch T, McDaniel O, Hardy J, Farrer M et al (2002) Ethnic differences in the expression of neurodegenerative disease: Machado-Joseph disease in Africans and Caucasians. Mov Disord: Official J Mov Disord Soc 17:1068–1071CrossRefGoogle Scholar
  62. 62.
    Ogun SA, Martins S, Adebayo PB, Dawodu CO, Sequeiros J, Finkel MF (2015) Machado-Joseph disease in a Nigerian family: mutational origin and review of the literature. Eur J Hum Genet: EJHG 23:271–273CrossRefGoogle Scholar
  63. 63.
    Gwinn-Hardy K, Singleton A, O’Suilleabhain P, Boss M, Nicholl D, Adam A, Hussey J, Critchley P, Hardy J, Farrer M (2001) Spinocerebellar ataxia type 3 phenotypically resembling Parkinson disease in a black family. Arch Neurol 58:296–299CrossRefGoogle Scholar
  64. 64.
    Sequeiros J, Suite ND (1986) Spinopontine atrophy disputed as a separate entity: the first description of Machado-Joseph disease. Neurology 36:1408CrossRefGoogle Scholar
  65. 65.
    Taniguchi R, Konigsmark BW (1971) Dominant spino-pontine atrophy. Report of a family through three generations. Brain 94:349–358CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2018

Authors and Affiliations

  1. 1.IPATIMUP - Institute of Molecular Pathology and ImmunologyUniversidade do PortoPortoPortugal
  2. 2.i3S - Instituto de Investigação e Inovação em SaúdeUniversidade do PortoPortoPortugal
  3. 3.IBMC - Institute for Molecular and Cell BiologyUniversidade do PortoPortoPortugal
  4. 4.ICBAS - Instituto de Ciências Biomédicas de Abel SalazarUniversidade do PortoPortoPortugal

Personalised recommendations