Ataxia and Hypogonadism: a Review of the Associated Genes and Syndromes.
Ataxia
Gordon Holmes syndrome
Hypogonadism
NGS
Journal
Cerebellum (London, England)
ISSN: 1473-4230
Titre abrégé: Cerebellum
Pays: United States
ID NLM: 101089443
Informations de publication
Date de publication:
Apr 2024
Apr 2024
Historique:
accepted:
20
03
2023
pubmed:
31
3
2023
medline:
31
3
2023
entrez:
30
3
2023
Statut:
ppublish
Résumé
The association of hypogonadism and cerebellar ataxia was first recognized in 1908 by Gordon Holmes. Since the seminal description, several heterogeneous phenotypes have been reported, differing for age at onset, associated features, and gonadotropins levels. In the last decade, the genetic bases of these disorders are being progressively uncovered. Here, we review the diseases associating ataxia and hypogonadism and the corresponding causative genes. In the first part of this study, we focus on clinical syndromes and genes (RNF216, STUB1, PNPLA6, AARS2, SIL1, SETX) predominantly associated with ataxia and hypogonadism as cardinal features. In the second part, we mention clinical syndromes and genes (POLR3A, CLPP, ERAL1, HARS, HSD17B4, LARS2, TWNK, POLG, ATM, WFS1, PMM2, FMR1) linked to complex phenotypes that include, among other features, ataxia and hypogonadism. We propose a diagnostic algorithm for patients with ataxia and hypogonadism, and we discuss the possible common etiopathogenetic mechanisms.
Identifiants
pubmed: 36997834
doi: 10.1007/s12311-023-01549-x
pii: 10.1007/s12311-023-01549-x
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
688-701Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Holmes GA. Form of familial degeneration of the cerebellum. Brain. 1908;30:466–89.
doi: 10.1093/brain/30.4.466
De Michele G, Filla A. Other autosomal recessive and childhood ataxias. Handb Clin Neurol. 2012;103:343–57. https://doi.org/10.1016/B978-0-444-51892-7.00021-8 .
doi: 10.1016/B978-0-444-51892-7.00021-8
pubmed: 21827899
Galatolo D, Tessa A, Filla A, Santorelli FM. Clinical application of next generation sequencing in hereditary spinocerebellar ataxia: increasing the diagnostic yield and broadening the ataxia-spasticity spectrum. A retrospective anal. Neurogenetics. 2018;19:1–8. https://doi.org/10.1007/s10048-017-0532-6 .
doi: 10.1007/s10048-017-0532-6
Margolin DH, Kousi M, Chan YM, Lim ET, Schmahmann JD, Hadjivassiliou M, Hall JE, Adam I, Dwyer A, Plummer L, Aldrin SV, O’Rourke J, Kirby A, Lage K, Milunsky A, Milunsky JM, Chan J, Hedley-Whyte ET, Daly MJ, et al. Ataxia, dementia, and hypogonadotropism caused by disordered ubiquitination. N Engl J Med. 2013;23(368):1992–2003. https://doi.org/10.1056/NEJMoa1215993 .
doi: 10.1056/NEJMoa1215993
Alqwaifly M, Bohlega S. Ataxia and hypogonadotropic hypogonadism with intrafamilial variability caused by RNF216 mutation. Neurol Int. 2016;8:6444. https://doi.org/10.4081/ni.2016.6444 .
doi: 10.4081/ni.2016.6444
pubmed: 27441066
pmcid: 4935815
Santens P, Van Damme T, Steyaert W, Willaert A, Sablonnière B, De Paepe A, Coucke PJ, Dermaut B. RNF216 mutations as a novel cause of autosomal recessive Huntington-like disorder. Neurology. 2015;84:1760–6. https://doi.org/10.1212/WNL.0000000000001521 .
doi: 10.1212/WNL.0000000000001521
pubmed: 25841028
Calandra CR, Mocarbel Y, Vishnopolska SA, et al. Gordon Holmes syndrome caused by RNF216 novel mutation in 2 Argentinean siblings. Mov Disord Clin Pract. 2019;6:259–62. https://doi.org/10.1002/mdc3.12721 .
doi: 10.1002/mdc3.12721
pubmed: 30949559
pmcid: 6417841
Chen KL, Zhao GX, Wang H, et al. A novel de novo RNF216 mutation associated with autosomal recessive Huntington-like disorder. Ann Clin Transl Neurol. 2020;7:860–4. https://doi.org/10.1002/acn3.51047 .
doi: 10.1002/acn3.51047
pubmed: 32358900
pmcid: 7261743
Lieto M, Galatolo D, Roca A, Cocozza S, Pontillo G, Fico T, Pane C, Saccà F, De Michele G, Santorelli FM, Filla A. Overt hypogonadism may not be a sentinel sign of RING finger protein 216: two novel mutations associated with ataxia, chorea, and fertility. Mov Disord Clin Pract. 2019;6:724–6. https://doi.org/10.1002/mdc3.12839 .
doi: 10.1002/mdc3.12839
pubmed: 31745488
pmcid: 6856465
Chen KL, Wang H, Zhao GX, Wei L, Huang YY, Chen SD, Sun J, Dong Q, Cui M, Yu JT. Whole-exome sequencing identified a novel mutation in RNF216 in a family with Gordon Holmes syndrome. J Mol Neurosci. 2022;72:691–4. https://doi.org/10.1007/s12031-021-01953-0 .
doi: 10.1007/s12031-021-01953-0
pubmed: 35088240
Shi CH, Schisler JC, Rubel CE, Tan S, Song B, McDonough H, Xu L, Portbury AL, Mao CY, True C, Wang RH, Wang QZ, Sun SL, Seminara SB, Patterson C, Xu YM. Ataxia and hypogonadism caused by the loss of ubiquitin ligase activity of the U box protein CHIP. Hum Mol Genet. 2014;23:1013–24. https://doi.org/10.1093/hmg/ddt497 .
doi: 10.1093/hmg/ddt497
pubmed: 24113144
De Michele G, Galatolo D, Barghigiani M, Dello Iacovo D, Trovato R, Tessa A, Salvatore E, Filla A, De Michele G, Santorelli FM. Spinocerebellar ataxia type 48: last but not least. Neurol Sci. 2020;41:2423–32. https://doi.org/10.1007/s10072-020-04408-3 .
doi: 10.1007/s10072-020-04408-3
pubmed: 32342324
Heimdal K, Sanchez-Guixé M, Aukrust I, Bollerslev J, Bruland O, Jablonski GE, Erichsen AK, Gude E, Koht JA, Erdal S, Fiskerstrand T, Haukanes BI, Boman H, Bjørkhaug L, Tallaksen CM, Knappskog PM, Johansson S. STUB1 mutations in autosomal recessive ataxias - evidence for mutation-specific clinical heterogeneity. Orphanet J Rare Dis. 2014;9:146. https://doi.org/10.1186/s13023-014-0146-0 .
doi: 10.1186/s13023-014-0146-0
pubmed: 25258038
pmcid: 4181732
Synofzik M, Hufnagel RB, Züchner S. PNPLA6-related disorders. GeneReviews®; 2014.
Jokanović M. Neurotoxic effects of organophosphorus pesticides and possible association with neurodegenerative diseases in man: a review. Toxicology. 2018;410:125–31. https://doi.org/10.1016/j.tox.2018.09.009 .
doi: 10.1016/j.tox.2018.09.009
pubmed: 30266654
Rainier S, Bui M, Mark E, Thomas D, Tokarz D, Ming L, Delaney C, Richardson RJ, Albers JW, Matsunami N, Stevens J, Coon H, Leppert M, Fink JK. Neuropathy target esterase gene mutations cause motor neuron disease. Am J Hum Genet. 2008;82:780–5. https://doi.org/10.1016/j.ajhg.2007.12.018 .
doi: 10.1016/j.ajhg.2007.12.018
pubmed: 18313024
pmcid: 2427280
Synofzik M, Gonzalez MA, Lourenco CM, Coutelier M, Haack TB, Rebelo A, Hannequin D, Strom TM, Prokisch H, Kernstock C, Durr A, Schols L, Lima-Martinez MM, Farooq A, Schule R, Stevanin G, Marques W Jr, Zuchner S. PNPLA6 mutations cause Boucher–Neuhauser and Gordon Holmes syndromes as part of a broad neurodegenerative spectrum. Brain. 2014;137:69–77. https://doi.org/10.1093/brain/awt326 .
doi: 10.1093/brain/awt326
pubmed: 24355708
Teive HAG, Camargo CHF, Sato MT, Shiokawa N, Boguszewski CL, Raskin S, Buck C, Seminara SB, Munhoz RP. Different cerebellar ataxia phenotypes associated with mutations of the PNPLA6 gene in Brazilian patients with recessive ataxias. Cerebellum. 2018;17:380–5. https://doi.org/10.1007/s12311-017-0909-y .
doi: 10.1007/s12311-017-0909-y
pubmed: 29248984
pmcid: 5970027
Sen K, Finau M, Ghosh P. Bi-allelic variants in PNPLA6 possibly associated with Parkinsonian features in addition to spastic paraplegia phenotype. J Neurol. 2020;267:2749–53. https://doi.org/10.1007/s00415-020-10028-w .
doi: 10.1007/s00415-020-10028-w
pubmed: 32623594
Nanetti L, Di Bella D, Magri S, et al. Multifaceted and age-dependent phenotypes associated with biallelic PNPLA6 gene variants: eight novel cases and review of the literature. Front Neurol. 2022;12:793547. https://doi.org/10.3389/fneur.2021.793547 .
doi: 10.3389/fneur.2021.793547
pubmed: 35069422
pmcid: 8770815
Gotz A, Tyynismaa H, Euro L, et al. Exome sequencing identifies mitochondrial alanyl-tRNA synthetase mutations in infantile mitochondrial cardiomyopathy. Am J Hum Genet. 2011;88:635–42. https://doi.org/10.1016/j.ajhg.2011.04.006 .
doi: 10.1016/j.ajhg.2011.04.006
pubmed: 21549344
pmcid: 3146718
Dallabona C, Diodato D, Kevelam SH, et al. Novel (ovario) leukodystrophy related to AARS2 mutations. Neurology. 2014;82:2063–71. https://doi.org/10.1212/WNL.0000000000000497 .
doi: 10.1212/WNL.0000000000000497
pubmed: 24808023
pmcid: 4118500
Wang X, Wang Q, Tang H, Chen B, Dong X, Niu S, Li S, Shi Y, Shan W, Zhang Z. Novel alanyl-tRNA synthetase 2 pathogenic variants in leukodystrophies. Front Neurol. 2019;10:1321. https://doi.org/10.3389/fneur.2019.01321 .
doi: 10.3389/fneur.2019.01321
pubmed: 31920941
pmcid: 6928200
Lakshmanan R, Adams ME, Lynch DS, Kinsella JA, Phadke R, Schott JM, Murphy E, Rohrer JD, Chataway J, Houlden H, Fox NC, Davagnanam I. Redefining the phenotype of ALSP and AARS2 mutation-related leukodystrophy. Neurol Genet. 2017;3:e135. https://doi.org/10.1212/NXG.0000000000000135 .
doi: 10.1212/NXG.0000000000000135
pubmed: 28243630
pmcid: 5312114
De Michele G, Galatolo D, Lieto M, Maione L, Cocozza S, Santorelli FM, Filla A. New AARS2 mutations in two siblings with tremor, downbeat nystagmus, and primary amenorrhea: a benign phenotype without leukoencephalopathy. Mov Disord Clin Pract. 2020;7:684–7. https://doi.org/10.1002/mdc3.12991 .
doi: 10.1002/mdc3.12991
pubmed: 32775515
pmcid: 7396852
Kuo ME, Antonellis A, Shakkottai VG. Alanyl-tRNA synthetase 2 (AARS2)-related ataxia without leukoencephalopathy. Cerebellum. 2020;19:154–60. https://doi.org/10.1007/s12311-019-01080-y .
doi: 10.1007/s12311-019-01080-y
pubmed: 31705293
pmcid: 6982554
Fine AS, Nemeth CL, Kaufman ML, et al. Mitochondrial aminoacyl-tRNA synthetase disorders: an emerging group of developmental disorders of myelination. J Neurodev Disord. 2019;11:29. https://doi.org/10.1186/s11689-019-9292-y .
doi: 10.1186/s11689-019-9292-y
pubmed: 31839000
pmcid: 6913031
Anttonen AK, Mahjneh I, Hämäläinen RH, Lagier-Tourenne C, Kopra O, Waris L, Anttonen M, Joensuu T, Kalimo H, Paetau A, Tranebjaerg L, Chaigne D, Koenig M, Eeg-Olofsson O, Udd B, Somer M, Somer H, Lehesjoki AE. The gene disrupted in Marinesco-Sjögren syndrome encodes SIL1, an HSPA5 cochaperone. Nat Genet. 2005;37:1309–11. https://doi.org/10.1038/ng1677 .
doi: 10.1038/ng1677
pubmed: 16282978
Senderek J, Krieger M, Stendel C, Bergmann C, Moser M, Breitbach-Faller N, Rudnik-Schöneborn S, Blaschek A, Wolf NI, Harting I, North K, Smith J, Muntoni F, Brockington M, Quijano-Roy S, Renault F, Herrmann R, Hendershot LM, Schröder JM, et al. Mutations in SIL1 cause Marinesco-Sjögren syndrome, a cerebellar ataxia with cataract and myopathy. Nat Genet. 2005;37:1312–4. https://doi.org/10.1038/ng1678 .
doi: 10.1038/ng1678
pubmed: 16282977
Krieger M, Roos A, Stendel C, Claeys KG, Sonmez FM, Baudis M, Bauer P, Bornemann A, de Goede C, Dufke A, Finkel RS, Goebel HH, Häussler M, Kingston H, Kirschner J, Medne L, Muschke P, Rivier F, Rudnik-Schöneborn S, et al. SIL1 mutations and clinical spectrum in patients with Marinesco-Sjogren syndrome. Brain. 2013;136:3634–44. https://doi.org/10.1093/brain/awt283 .
doi: 10.1093/brain/awt283
pubmed: 24176978
Inaguma Y, Hamada N, Tabata H, Iwamoto I, Mizuno M, Nishimura YV, Ito H, Morishita R, Suzuki M, Ohno K, Kumagai T, Nagata K. SIL1, a causative cochaperone gene of Marinesco-Söjgren syndrome, plays an essential role in establishing the architecture of the developing cerebral cortex. EMBO Mol Med. 2014;6:414–29. https://doi.org/10.1002/emmm.201303069 .
doi: 10.1002/emmm.201303069
pubmed: 24473200
pmcid: 3958314
Lavin MF, Yeo AJ, Becherel OJ. Senataxin protects the genome: implications for neurodegeneration and other abnormalities. Rare Dis. 2013;6(1):e25230. https://doi.org/10.4161/rdis.25230 .
doi: 10.4161/rdis.25230
Criscuolo C, Chessa L, Di Giandomenico S, Mancini P, Saccà F, Grieco GS, Piane M, Barbieri F, De Michele G, Banfi S, Pierelli F, Rizzuto N, Santorelli FM, Gallosti L, Filla A, Casali C. Ataxia with oculomotor apraxia type 2: a clinical, pathologic, and genetic study. Neurology. 2006;66:1207–10. https://doi.org/10.1212/01.wnl.0000208402.10512.4a .
doi: 10.1212/01.wnl.0000208402.10512.4a
pubmed: 16636238
Moreira MC, Koenig M. Ataxia with Oculomotor Apraxia Type 2. 2004 Nov 15 [Updated 2018 Jul 12]. In: Adam MP, Ardinger HH, Pagon RA, et al., editors. GeneReviews® [Internet]. Seattle (WA): University of Washington, Seattle;1993-2020. Available from: https://www.ncbi.nlm.nih.gov/books/NBK1154/
Ronsin S, Hannoun S, Thobois S, Petiot P, Vighetto A, Cotton F, Tilikete C. A new MRI marker of ataxia with oculomotor apraxia. Eur J Radiol. 2019;110:187-192. doi: https://doi.org/10.1016/j.ejrad.2018.11.035 .
Cocozza S, Pontillo G, De Michele G, Di Stasi M, Guerriero E, Perillo T, Pane C, De Rosa A, Ugga L, Brunetti A. Conventional MRI findings in hereditary degenerative ataxias: a pictorial review. Neuroradiology. 2021;63:983–99. https://doi.org/10.1007/s00234-021-02682-2 .
doi: 10.1007/s00234-021-02682-2
pubmed: 33733696
pmcid: 8213578
Gazulla J, Benavente I, López-Fraile IP, Modrego P, Koenig M. Sensorimotor neuronopathy in ataxia with oculomotor apraxia type 2. Muscle Nerve. 2009;40:481–5. https://doi.org/10.1002/mus.21328 .
doi: 10.1002/mus.21328
pubmed: 19618424
Anheim M, Monga B, Fleury M, Charles P, Barbot C, Salih M, Delaunoy JP, Fritsch M, Arning L, Synofzik M, Schöls L, Sequeiros J, Goizet C, Marelli C, Le Ber I, Koht J, Gazulla J, De Bleecker J, Mukhtar M, Drouot N, Ali-Pacha L, Benhassine T, Chbicheb M, M’Zahem A, Hamri A, Chabrol B, Pouget J, Murphy R, Watanabe M, Coutinho P, Tazir M, Durr A, Brice A, Tranchant C, Koenig M. Ataxia with oculomotor apraxia type 2: clinical, biological and genotype/phenotype correlation study of a cohort of 90 patients. Brain. 2009;132:2688-2698. doi: https://doi.org/10.1093/brain/awp211 .
Catford SR, O’Bryan MK, RI ML, Delatycki MB, Rombauts L. Germ cell arrest associated with aSETX mutation in ataxia oculomotor apraxia type 2. Reprod Biomed Online. 2019;38:961–5. https://doi.org/10.1016/j.rbmo.2018.12.042 .
doi: 10.1016/j.rbmo.2018.12.042
pubmed: 30642639
Becherel OJ, Fogel BL, Zeitlin SI, Samaratunga H, Greaney J, Homer H, Lavin MF. Disruption of spermatogenesis and infertility in ataxia with oculomotor apraxia type 2 (AOA2). Cerebellum. 2019;18:448–56. https://doi.org/10.1007/s12311-019-01012-w .
doi: 10.1007/s12311-019-01012-w
pubmed: 30778901
pmcid: 6520128
Bernard G, Vanderver A. POLR3-related leukodystrophy. 2012 Aug 2 [Updated 2017 May 11]. In: Adam MP, Ardinger HH, Pagon RA, et al., editors. GeneReviews® [Internet]. Seattle (WA): University of Washington, Seattle;1993–2020. Available from: https://www.ncbi.nlm.nih.gov/books/NBK99167/
La Piana R, Tonduti D, Gordish Dressman H, Schmidt JL, Murnick J, Brais B, Bernard G, Vanderver A. Brain magnetic resonance imaging (MRI) pattern recognition in Pol III-related leukodystrophies. J Child Neurol. 2014;29:214–20. https://doi.org/10.1177/0883073813503902 .
Wolf NI, Vanderver A, van Spaendonk RM, et al. Clinical spectrum of 4H leukodystrophy caused by POLR3A and POLR3B mutations. Neurology. 2014;83:1898–905. https://doi.org/10.1212/WNL.0000000000001002 .
doi: 10.1212/WNL.0000000000001002
pubmed: 25339210
pmcid: 4248461
La Piana R, Cayami FK, Tran LT, Guerrero K, van Spaendonk R, Õunap K, Pajusalu S, Haack T, Wassmer E, Timmann D, Mierzewska H, Poll-Thé BT, Patel C, Cox H, Atik T, Onay H, Ozkınay F, Vanderver A, van der Knaap MS, et al. Diffuse hypomyelination is not obligate for POLR3-related disorders. Neurology. 2016;86:1622–6. https://doi.org/10.1212/WNL.0000000000002612 .
doi: 10.1212/WNL.0000000000002612
pubmed: 27029625
pmcid: 4844237
Minnerop M, Kurzwelly D, Wagner H, Soehn AS, Reichbauer J, Tao F, Rattay TW, Peitz M, Rehbach K, Giorgetti A, Pyle A, Thiele H, Altmüller J, Timmann D, Karaca I, Lennarz M, Baets J, Hengel H, Synofzik M, et al. Hypomorphic mutations in POLR3A are a frequent cause of sporadic and recessive spastic ataxia. Brain. 2017;140:1561–78. https://doi.org/10.1093/brain/awx095 .
doi: 10.1093/brain/awx095
pubmed: 28459997
pmcid: 6402316
Battini R, Bertelloni S, Astrea G, Casarano M, Travaglini L, Baroncelli G, Pasquariello R, Bertini E, Cioni G. Longitudinal follow up of a boy affected by Pol III-related leukodystrophy: a detailed phenotype description. BMC Med Genet. 2015;16:53. https://doi.org/10.1186/s12881-015-0203-0 .
doi: 10.1186/s12881-015-0203-0
pubmed: 26204956
pmcid: 4557838
Lerat J, Jonard L, Loundon N, Christin-Maitre S, Lacombe D, Goizet C, Rouzier C, Van Maldergem L, Gherbi S, Garabedian EN, Bonnefont JP, Touraine P, Mosnier I, Munnich A, Denoyelle F, Marlin S. An application of NGS for molecular investigations in Perrault syndrome: study of 14 families and review of the literature. Hum Mutat. 2016;37:1354–62. https://doi.org/10.1002/humu.23120 .
doi: 10.1002/humu.23120
pubmed: 27650058
Newman WG, Friedman TB, Conway GS, et al. Perrault syndrome. 2014 Sep 25 [Updated 2018 Sep 6]. In: Adam MP, Ardinger HH, Pagon RA, et al., editors. GeneReviews® [Internet]. Seattle (WA): University of Washington, Seattle;1993-2020. Available from: https://www.ncbi.nlm.nih.gov/books/NBK242617/
Jenkinson EM, Clayton-Smith J, Mehta S, Bennett C, Reardon W, Green A, Pearce SH, De Michele G, Conway GS, Cilliers D, Moreton N, Davis JR, Trump D, Newman WG. Perrault syndrome: further evidence for genetic heterogeneity. J Neurol. 2012;259:974–6. https://doi.org/10.1007/s00415-011-6285-5 .
doi: 10.1007/s00415-011-6285-5
pubmed: 22037954
van der Knaap MS, Bugiani M, Mendes MI, Riley LG, Smith DEC, Rudinger-Thirion J, Frugier M, Breur M, Crawford J, van Gaalen J, Schouten M, Willems M, Waisfisz Q, Mau-Them FT, Rodenburg RJ, Taft RJ, Keren B, Christodoulou J, Depienne C, et al. Biallelic variants in LARS2 and KARS cause deafness and (ovario)leukodystrophy. Neurology. 2019;92:e1225–37. https://doi.org/10.1212/WNL.0000000000007098 .
doi: 10.1212/WNL.0000000000007098
pubmed: 30737337
pmcid: 9281382
Lines MA, Jobling R, Brady L, Marshall CR, Scherer SW, Rodriguez AR, Lee L, Lang AE, Mestre TA, Wanders RJ, Ferdinandusse S, Tarnopolsky MA. Canadian Pediatric Genetic Disorders Sequencing Consortium (FORGE Canada). Peroxisomal D-bifunctional protein deficiency: three adults diagnosed by whole-exome sequencing. Neurology. 2014;82:963–8. https://doi.org/10.1212/WNL.0000000000000219 .
doi: 10.1212/WNL.0000000000000219
pubmed: 24553428
pmcid: 3963001
Theunissen TE, Szklarczyk R, Gerards M, Hellebrekers DM, Mulder-Den Hartog EN, Vanoevelen J, Kamps R, de Koning B, Rutledge SL, Schmitt-Mechelke T, van Berkel CG, van der Knaap MS, de Coo IF, Smeets HJ. Specific MRI abnormalities reveal severe Perrault syndrome due to CLPP defects. Front Neurol. 2016;7:203. https://doi.org/10.3389/fneur.2016.00203 .
doi: 10.3389/fneur.2016.00203
pubmed: 27899912
pmcid: 5110515
Domínguez-Ruiz M, García-Martínez A, Corral-Juan M, Pérez-Álvarez ÁI, Plasencia AM, Villamar M, Moreno-Pelayo MA, Matilla-Dueñas A, Menéndez-González M, Del Castillo I. Perrault syndrome with neurological features in a compound heterozygote for two TWNK mutations: overlap of TWNK-related recessive disorders. J Transl Med. 2019;17:290. https://doi.org/10.1186/s12967-019-2041-x .
doi: 10.1186/s12967-019-2041-x
pubmed: 31455392
pmcid: 6712801
Ołdak M, Oziębło D, Pollak A, Stępniak I, Lazniewski M, Lechowicz U, Kochanek K, Furmanek M, Tacikowska G, Plewczynski D, Wolak T, Płoski R, Skarżyński H. Novel neuro-audiological findings and further evidence for TWNK involvement in Perrault syndrome. J Transl Med. 2017;15:25. https://doi.org/10.1186/s12967-017-1129-4 .
doi: 10.1186/s12967-017-1129-4
pubmed: 28178980
pmcid: 5299684
Cohen BH, Chinnery PF, Copeland WC. POLG-related disorders. 2010 Mar 16 [Updated 2018 Mar 1]. In: Adam MP, Ardinger HH, Pagon RA, et al., editors. GeneReviews® [Internet]. Seattle (WA): University of Washington, Seattle. p. 1993–2020.
Luoma P, Melberg A, Rinne JO, Kaukonen JA, Nupponen NN, Chalmers RM, Oldfors A, Rautakorpi I, Peltonen L, Majamaa K, Somer H, Suomalainen A. Parkinsonism, premature menopause, and mitochondrial DNA polymerase gamma mutations: clinical and molecular genetic study. Lancet. 2004;364:875–82. https://doi.org/10.1016/S0140-6736(04)16983-3 .
doi: 10.1016/S0140-6736(04)16983-3
pubmed: 15351195
Tzoulis C, Neckelmann G, Mørk SJ, Engelsen BE, Viscomi C, Moen G, Ersland L, Zeviani M, Bindoff LA. Localized cerebral energy failure in DNA polymerase gamma-associated encephalopathy syndromes. Brain. 2010;133:1428–37. https://doi.org/10.1093/brain/awq067 .
doi: 10.1093/brain/awq067
pubmed: 20400524
Béreau M, Anheim M, Echaniz-Laguna A, Magot A, Verny C, Goideau-Sevrain M, Barth M, Amati-Bonneau P, Allouche S, Ayrignac X, Bédat-Millet AL, Guyant-Maréchal L, Kuntzer T, Ochsner F, Petiot P, Vial C, Omer S, Sole G, Taieb G, et al. The wide POLG-related spectrum: an integrated view. J Neurol Sci. 2016;368:70–6. https://doi.org/10.1016/j.jns.2016.06.062 .
doi: 10.1016/j.jns.2016.06.062
pubmed: 27538604
Filosto M, Mancuso M, Nishigaki Y, Pancrudo J, Harati Y, Gooch C, Mankodi A, Bayne L, Bonilla E, Shanske S, Hirano M, DiMauro S. Clinical and genetic heterogeneity in progressive external ophthalmoplegia due to mutations in polymerase-gamma. Arch. Neurol. 2003;60:1279–84.
doi: 10.1001/archneur.60.9.1279
pubmed: 12975295
Amirifar P, Ranjouri MR, Yazdani R, Abolhassani H, Aghamohammadi A. Ataxia-telangiectasia: a review of clinical features and molecular pathology. Pediatr Allergy Immunol. 2019;30:277–88. https://doi.org/10.1111/pai.13020 .
doi: 10.1111/pai.13020
pubmed: 30685876
Tavani F, Zimmerman RA, Berry GT, Sullivan K, Gatti R, Bingham P. Ataxia-telangiectasia: the pattern of cerebellar atrophy on MRI. Neuroradiology. 2003;45:315–9. https://doi.org/10.1007/s00234-003-0945-9 .
doi: 10.1007/s00234-003-0945-9
pubmed: 12740724
Lin DD, Barker PB, Lederman HM, Crawford TO. Cerebral abnormalities in adults with ataxia-telangiectasia. AJNR Am J Neuroradiol. 2014;35:119–23. https://doi.org/10.3174/ajnr.A3646 .
doi: 10.3174/ajnr.A3646
pubmed: 23886747
pmcid: 4106125
Hamer G, Kal HB, Westphal CH, Ashley T, de Rooij DG. Ataxia telangiectasia mutated expression and activation in the testis. Biol Reprod. 2004;70:1206–12. https://doi.org/10.1095/biolreprod.103.024950 .
doi: 10.1095/biolreprod.103.024950
pubmed: 14681204
Nissenkorn A, Levy-Shraga Y, Banet-Levi Y, Lahad A, Sarouk I, Modan-Moses D. Endocrine abnormalities in ataxia telangiectasia: findings from a national cohort. Pediatr Res. 2016;79:889–94. https://doi.org/10.1038/pr.2016.19 .
doi: 10.1038/pr.2016.19
pubmed: 26891003
Zatyka M, Ricketts C, Xavier GS, Minton J, Fenton S, Hofman-Thiel S, Rutter GA, Barrett TG. Sodium- potassium ATPase β1 subunit is a molecular partner of wolframin, and endoplasmic reticulum protein involved in ER stress. Hum Mol Genet. 2008;17:190–200.
doi: 10.1093/hmg/ddm296
pubmed: 17947299
Hofmann S, Philbrook C, Gerbitz KD, Bauer MF. Wolfram syndrome: structural and functional analyses of mutant and wild-type wolframin, the WFS1 gene product. Hum Mol Genet. 2003;12:2003–12. https://doi.org/10.1093/hmg/ddg214 .
doi: 10.1093/hmg/ddg214
pubmed: 12913071
Galluzzi P, Filosomi G, Vallone IM, Bardelli AM, Venturi C. MRI of Wolfram syndrome (DIDMOAD). Neuroradiology. 1999;41:729–31. https://doi.org/10.1007/s002340050832 .
doi: 10.1007/s002340050832
pubmed: 10552021
Gocmen R, Guler E. Teaching NeuroImages: MRI of brain findings of Wolfram (DIDMOAD) syndrome. Neurology. 2014;83:e213–4. https://doi.org/10.1212/WNL.0000000000001082 .
doi: 10.1212/WNL.0000000000001082
pubmed: 25488999
Samara A, Lugar HM, Hershey T, Shimony JS. Longitudinal assessment of neuroradiologic features in Wolfram syndrome. AJNR Am J Neuroradiol. 2020;41:2364–9. https://doi.org/10.3174/ajnr.A6831 .
doi: 10.3174/ajnr.A6831
pubmed: 33122205
pmcid: 7963228
Medlej R, Wasson J, Baz P, Azar S, Salti I, Loiselet J, Permutt A, Halaby G. Diabetes mellitus and optic atrophy: a study of Wolfram syndrome in the Lebanese population. J Clin Endocrinol Metab. 2004;89:1656–61. https://doi.org/10.1210/jc.2002-030015 .
doi: 10.1210/jc.2002-030015
pubmed: 15070927
Schiff M, Roda C, Monin ML, Arion A, Barth M, Bednarek N, Bidet M, Bloch C, Boddaert N, Borgel D, Brassier A, Brice A, Bruneel A, Buissonnière R, Chabrol B, Chevalier MC, Cormier-Daire V, De Barace C, De Maistre E, et al. Clinical, laboratory and molecular findings and long-term follow-up data in 96 French patients with PMM2-CDG (phosphomannomutase 2-congenital disorder of glycosylation) and review of the literature. J Med Genet. 2017;54:843–51. https://doi.org/10.1136/jmedgenet-2017-104903 .
doi: 10.1136/jmedgenet-2017-104903
pubmed: 28954837
Brum JM, Rizzo IM, Mello WD, Speck-Martins CE. Congenital disorder of glycosylation type Ia: a non-progressive encephalopathy associated with multisystemic involvement. Arq Neuropsiquiatr. 2008;66:545–8. https://doi.org/10.1590/s0004-282x2008000400021 .
doi: 10.1590/s0004-282x2008000400021
pubmed: 18813717
Kristiansson B, Stibler H, Wide L. Gonadal function and glycoprotein hormones in the carbohydrate-deficient glycoprotein (CDG) syndrome. Acta Paediatr. 1995;84:655–9. https://doi.org/10.1111/j.1651-2227.1995.tb13720.x .
doi: 10.1111/j.1651-2227.1995.tb13720.x
pubmed: 7670249
Sparks SE, Krasnewich DM. PMM2-CDG (CDG-Ia) 2005 Aug 15 [Updated 2015 Oct 29]. In: Adam MP, Ardinger HH, Pagon RA, et al., editors. GeneReviews® [Internet]. Seattle (WA): University of Washington, Seattle; 1993-2021.
Nielsen KB, Tommerup N, Dyggve HV, Schou C. Macroorchidism and fragile X in mentally retarded males. Clinical, cytogenetic, and some hormonal investigations in mentally retarded males, including two with the fragile site at Xq28, fra(X)(q28). Hum Genet. 1982;61:113–7. https://doi.org/10.1007/BF00274199 .
doi: 10.1007/BF00274199
pubmed: 6215327
Hunter JE, Berry-Kravis E, Hipp H, Todd PK. FMR1 Disorders. 1998 Jun 16 [updated 2019 Nov 21]. In: Adam MP, Ardinger HH, Pagon RA, Wallace SE, Bean LJH, Stephens K, Amemiya A, editors. GeneReviews® [Internet]. Seattle (WA): University of Washington, Seattle; 1993–2020.
Muzar Z, Lozano R. Current research, diagnosis, and treatment of fragile X-associated tremor/ataxia syndrome. Intractable Rare Dis Res. 2014;3:101–9. https://doi.org/10.5582/irdr.2014.01029 .
doi: 10.5582/irdr.2014.01029
pubmed: 25606360
pmcid: 4298640
Saldarriaga-Gil W, Rodriguez-Guerrero T, Fandiño-Losada A, Ramirez-Cheyne J. Tremor-Ataxia syndrome and primary ovarian insufficiency in an FMR1 premutation carrier. Colomb Med (Cali). 2017 ;48(3):148-151. https://doi.org/10.25100/cm.v48i3.3019 . PMID: 29299012; PMCID: PMC5687867.
Sheshpari S, Shahnazi M, Mobarak H, Ahmadian S, Bedate AM, Nariman-Saleh-Fam Z, Nouri M, Rahbarghazi R, Mahdipour M. Ovarian function and reproductive outcome after ovarian tissue transplantation: a systematic review. J Transl Med. 2019;17:396. https://doi.org/10.1186/s12967-019-02149-2 .
doi: 10.1186/s12967-019-02149-2
pubmed: 31783875
pmcid: 6883646
Akassoglou K, Malester B, Xu J, Tessarollo L, Rosenbluth J, Chao MV. Brain-specific deletion of neuropathy target esterase/swisscheese results in neurodegeneration. Proc Natl Acad Sci U S A. 2004;101:5075–80. https://doi.org/10.1073/pnas.0401030101 .
doi: 10.1073/pnas.0401030101
pubmed: 15051870
pmcid: 387376
Hedges VL, Ebner TJ, Meisel RL, Mermelstein PG. The cerebellum as a target for estrogen action. Front Neuroendocrinol. 2012;33:403–11. https://doi.org/10.1016/j.yfrne.2012.08.005 .
doi: 10.1016/j.yfrne.2012.08.005
pubmed: 22975197
pmcid: 3496070
Sakamoto H, Mezaki Y, Shikimi H, Ukena K, Tsutsui K. Dendritic growth and spine formation in response to estrogen in the developing Purkinje cell. Endocrinology. 2003;144:4466–77. https://doi.org/10.1210/en.2003-0307 .
doi: 10.1210/en.2003-0307
pubmed: 12960093
Azcoitia I, Yague JG, Garcia-Segura LM. Estradiol synthesis within the human brain. Neuroscience. 2011;191:139–47. https://doi.org/10.1016/j.neuroscience.2011.02.012 .
doi: 10.1016/j.neuroscience.2011.02.012
pubmed: 21320576
Hedges VL, Chen G, Yu L, Krentzel AA, Starrett JR, Zhu JN, Suntharalingam P, Remage-Healey L, Wang JJ, Ebner TJ, Mermelstein PG. Local estrogen synthesis regulates parallel fiber-Purkinje cell neurotransmission within the cerebellar cortex. Endocrinology. 2018;159:1328–38. https://doi.org/10.1210/en.2018-00039 .
doi: 10.1210/en.2018-00039
pubmed: 29381778
pmcid: 5839732
Manto M, Hampe CS. Endocrine disorders and the cerebellum: from neurodevelopmental injury to late-onset ataxia. Handb Clin Neurol. 2018;155:353–68. https://doi.org/10.1016/B978-0-444-64189-2.00023-8 .
doi: 10.1016/B978-0-444-64189-2.00023-8
pubmed: 29891071