The pathology of X-linked adrenoleukodystrophy: tissue specific changes as a clue to pathophysiology.
ABCD1
Adrenoleukodystrophy
Adrenomyeloneuropathy
Cerebral ALD
Immunohistochemistry
Pathology
Journal
Orphanet journal of rare diseases
ISSN: 1750-1172
Titre abrégé: Orphanet J Rare Dis
Pays: England
ID NLM: 101266602
Informations de publication
Date de publication:
28 Mar 2024
28 Mar 2024
Historique:
received:
18
10
2023
accepted:
23
02
2024
medline:
29
3
2024
pubmed:
29
3
2024
entrez:
29
3
2024
Statut:
epublish
Résumé
Although the pathology of X-linked adrenoleukodystrophy (ALD) is well described, it represents the end-stage of neurodegeneration. It is still unclear what cell types are initially involved and what their role is in the disease process. Revisiting the seminal post-mortem studies from the 1970s can generate new hypotheses on pathophysiology. This review describes (histo)pathological changes of the brain and spinal cord in ALD. It aims at integrating older works with current insights and at providing an overarching theory on the pathophysiology of ALD. The data point to an important role for axons and glia in the pathology of both the myelopathy and leukodystrophy of ALD. In-depth pathological analyses with new techniques could help further unravel the sequence of events behind the pathology of ALD.
Identifiants
pubmed: 38549180
doi: 10.1186/s13023-024-03105-0
pii: 10.1186/s13023-024-03105-0
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
138Subventions
Organisme : Nederlandse Organisatie voor Toegepast Natuurwetenschappelijk Onderzoek
ID : 016.196.310
Informations de copyright
© 2024. The Author(s).
Références
Moser HW, Moser AB, Frayer KK, Chen W, Schulman JD, O’Neill BP, Kishimoto Y. Adrenoleukodystrophy: increased plasma content of saturated very long chain fatty acids. Neurology. 1981;31(10):1241–9.
pubmed: 7202134
doi: 10.1212/WNL.31.10.1241
Berger J, Forss-Petter S, Eichler FS. Pathophysiology of X-linked adrenoleukodystrophy. Biochimie. 2014;98(100):135–42.
pubmed: 24316281
pmcid: 3988840
doi: 10.1016/j.biochi.2013.11.023
Powers JM, DeCiero DP, Ito M, Moser AB, Moser HW. Adrenomyeloneuropathy: a neuropathologic review featuring its noninflammatory myelopathy. J Neuropathol Exp Neurol. 2000;59(2):89–102.
pubmed: 10749098
doi: 10.1093/jnen/59.2.89
Igarashi M, Schaumburg HH, Powers J, Kishmoto Y, Kolodny E, Suzuki K. Fatty acid abnormality in adrenoleukodystrophy. J Neurochem. 1976;26(4):851–60.
pubmed: 965973
doi: 10.1111/j.1471-4159.1976.tb04461.x-i1
Singh I, Moser AE, Moser HW, Kishimoto Y. Adrenoleukodystrophy: impaired oxidation of very long chain fatty acids in white blood cells, cultured skin fibroblasts, and amniocytes. Pediatr Res. 1984;18(3):286–90.
pubmed: 6728562
doi: 10.1203/00006450-198403000-00016
Mosser J, Lutz Y, Stoeckel ME, Sarde CO, Kretz C, Douar AM, et al. The gene responsible for adrenoleukodystrophy encodes a peroxisomal membrane protein. Hum Mol Genet. 1994;3(2):265–71.
pubmed: 8004093
doi: 10.1093/hmg/3.2.265
Turk BR, Theda C, Fatemi A, Moser AB. X-linked adrenoleukodystrophy: Pathology, pathophysiology, diagnostic testing, newborn screening and therapies. Int J Dev Neurosci. 2020;80(1):52–72.
pubmed: 31909500
pmcid: 7041623
doi: 10.1002/jdn.10003
Hein S, Schönfeld P, Kahlert S, Reiser G. Toxic effects of X-linked adrenoleukodystrophy-associated, very long chain fatty acids on glial cells and neurons from rat hippocampus in culture. Hum Mol Genet. 2008;17(12):1750–61.
pubmed: 18344355
doi: 10.1093/hmg/ddn066
Ho JK, Moser H, Kishimoto Y, Hamilton JA. Interactions of a very long chain fatty acid with model membranes and serum albumin. Implications for the pathogenesis of adrenoleukodystrophy. J Clin Invest. 1995;96(3):1455–63.
pubmed: 7657817
pmcid: 185769
doi: 10.1172/JCI118182
Budka H, Sluga E, Heiss WD. Spastic paraplegia associated with Addison’s disease: adult variant of adreno-leukodystrophy. J Neurol. 1976;213(3):237–50.
pubmed: 61263
doi: 10.1007/BF00312873
Schaumburg HH, Powers JM, Raine CS, Suzuki K, Richardson EP. Jr. Adrenoleukodystrophy. A clinical and pathological study of 17 cases. Arch Neurol. 1975;32(9):577–91.
pubmed: 169765
doi: 10.1001/archneur.1975.00490510033001
Powers JM, Schaumberg HH. Adreno-leukodystrophy. Similar ultrastructural changes in adrenal cortical and Schwann cells. Arch Neurol. 1974;30(5):406–8.
pubmed: 4821786
doi: 10.1001/archneur.1974.00490350064011
Johnson AB, Schaumburg HH, Powers JM. Histochemical characteristics of the striated inclusions of adrenoleukodystrophy. J Histochem Cytochem. 1976;24(6):725–30.
pubmed: 59773
doi: 10.1177/24.6.59773
Powers JM, Schaumburg HH. The testis in adreno-leukodystrophy. Am J Pathol. 1981;102(1):90–8.
pubmed: 7468762
pmcid: 1903430
Strachan LR, Stevenson TJ, Freshner B, Keefe MD, Miranda Bowles D, Bonkowsky JL. A zebrafish model of X-linked adrenoleukodystrophy recapitulates key disease features and demonstrates a developmental requirement for abcd1 in oligodendrocyte patterning and myelination. Hum Mol Genet. 2017;26(18):3600–14.
pubmed: 28911205
pmcid: 5886093
doi: 10.1093/hmg/ddx249
Lu JF, Lawler AM, Watkins PA, Powers JM, Moser AB, Moser HW, Smith KD. A mouse model for X-linked adrenoleukodystrophy. Proc Natl Acad Sci U S A. 1997;94(17):9366–71.
pubmed: 9256488
pmcid: 23196
doi: 10.1073/pnas.94.17.9366
Moser HW, Moser AB, Kawamura N, Murphy J, Suzuki K, Schaumburg H, Kishimoto Y. Adrenoleukodystrophy: elevated C26 fatty acid in cultured skin fibroblasts. Ann Neurol. 1980;7(6):542–9.
pubmed: 7436359
doi: 10.1002/ana.410070607
Montoro R, Heine VM, Kemp S, Engelen M. Evolution of adrenoleukodystrophy model systems. J Inherit Metab Dis. 2021;44(3):544–53.
pubmed: 33373044
pmcid: 8248356
doi: 10.1002/jimd.12357
Contreras M, Mosser J, Mandel JL, Aubourg P, Singh I. The protein coded by the X-adrenoleukodystrophy gene is a peroxisomal integral membrane protein. FEBS Lett. 1994;344(2–3):211–5.
pubmed: 8187886
doi: 10.1016/0014-5793(94)00400-5
Liu LX, Janvier K, Berteaux-Lecellier V, Cartier N, Benarous R, Aubourg P. Homo- and heterodimerization of peroxisomal ATP-binding cassette half-transporters. J Biol Chem. 1999;274(46):32738–43.
pubmed: 10551832
doi: 10.1074/jbc.274.46.32738
Wiesinger C, Kunze M, Regelsberger G, Forss-Petter S, Berger J. Impaired very long-chain acyl-CoA β-oxidation in human X-linked adrenoleukodystrophy fibroblasts is a direct consequence of ABCD1 transporter dysfunction. J Biol Chem. 2013;288(26):19269–79.
pubmed: 23671276
pmcid: 3696697
doi: 10.1074/jbc.M112.445445
Netik A, Forss-Petter S, Holzinger A, Molzer B, Unterrainer G, Berger J. Adrenoleukodystrophy-related protein can compensate functionally for adrenoleukodystrophy protein deficiency (X-ALD): implications for therapy. Hum Mol Genet. 1999;8(5):907–13.
pubmed: 10196381
doi: 10.1093/hmg/8.5.907
Pujol A, Ferrer I, Camps C, Metzger E, Hindelang C, Callizot N, et al. Functional overlap between ABCD1 (ALD) and ABCD2 (ALDR) transporters: a therapeutic target for X-adrenoleukodystrophy. Hum Mol Genet. 2004;13(23):2997–3006.
pubmed: 15489218
doi: 10.1093/hmg/ddh323
Muneer Z, Wiesinger C, Voigtländer T, Werner HB, Berger J, Forss-Petter S. Abcd2 is a strong modifier of the metabolic impairments in peritoneal macrophages of ABCD1-deficient mice. PLoS ONE. 2014;9(9):e108655.
pubmed: 25255441
pmcid: 4177892
doi: 10.1371/journal.pone.0108655
Berger J, Albet S, Bentejac M, Netik A, Holzinger A, Roscher AA, et al. The four murine peroxisomal ABC-transporter genes differ in constitutive, inducible and developmental expression. Eur J Biochem. 1999;265(2):719–27.
pubmed: 10504404
doi: 10.1046/j.1432-1327.1999.00772.x
Maier EM, Mayerhofer PU, Asheuer M, Köhler W, Rothe M, Muntau AC, et al. X-linked adrenoleukodystrophy phenotype is independent of ABCD2 genotype. Biochem Biophys Res Commun. 2008;377(1):176–80.
pubmed: 18834860
doi: 10.1016/j.bbrc.2008.09.092
Kemp S, Valianpour F, Mooyer PA, Kulik W, Wanders RJ. Method for measurement of peroxisomal very-long-chain fatty acid beta-oxidation in human skin fibroblasts using stable-isotope-labeled tetracosanoic acid. Clin Chem. 2004;50(10):1824–6.
pubmed: 15388659
doi: 10.1373/clinchem.2004.038539
van Roermund CW, Visser WF, Ijlst L, van Cruchten A, Boek M, Kulik W, et al. The human peroxisomal ABC half transporter ALDP functions as a homodimer and accepts acyl-CoA esters. Faseb j. 2008;22(12):4201–8.
pubmed: 18757502
doi: 10.1096/fj.08-110866
Fourcade S, López-Erauskin J, Galino J, Duval C, Naudi A, Jove M, et al. Early oxidative damage underlying neurodegeneration in X-adrenoleukodystrophy. Hum Mol Genet. 2008;17(12):1762–73.
pubmed: 18344354
doi: 10.1093/hmg/ddn085
Barnett MH, Mathey E, Kiernan MC, Pollard JD. Axonal damage in central and peripheral nervous system inflammatory demyelinating diseases: common and divergent pathways of tissue damage. Curr Opin Neurol. 2016;29(3):213–21.
pubmed: 27058223
doi: 10.1097/WCO.0000000000000334
Low D, Ginhoux F. Recent advances in the understanding of microglial development and homeostasis. Cell Immunol. 2018;330:68–78.
pubmed: 29366562
doi: 10.1016/j.cellimm.2018.01.004
Singh I, Pujol A. Pathomechanisms underlying X-adrenoleukodystrophy: a three-hit hypothesis. Brain Pathol. 2010;20(4):838–44.
pubmed: 20626745
pmcid: 3021280
doi: 10.1111/j.1750-3639.2010.00392.x
Kim GH, Kim JE, Rhie SJ, Yoon S. The role of oxidative stress in neurodegenerative diseases. Exp Neurobiol. 2015;24(4):325–40.
pubmed: 26713080
pmcid: 4688332
doi: 10.5607/en.2015.24.4.325
Engelen M, Kemp S, Poll-The BT. X-linked adrenoleukodystrophy: pathogenesis and treatment. Curr Neurol Neurosci Rep. 2014;14(10):486.
pubmed: 25115486
doi: 10.1007/s11910-014-0486-0
Powers JM. Adreno-leukodystrophy (adreno-testiculo-leukomyelo-neuropathic-complex). Clin Neuropathol. 1985;4(5):181–99.
pubmed: 2998664
Fouquet F, Zhou JM, Ralston E, Murray K, Troalen F, Magal E, et al. Expression of the adrenoleukodystrophy protein in the human and mouse central nervous system. Neurobiol Dis. 1997;3(4):271–85.
pubmed: 9173925
doi: 10.1006/nbdi.1997.0127
Höftberger R, Kunze M, Weinhofer I, Aboul-Enein F, Voigtländer T, Oezen I, et al. Distribution and cellular localization of adrenoleukodystrophy protein in human tissues: implications for X-linked adrenoleukodystrophy. Neurobiol Dis. 2007;28(2):165–74.
pubmed: 17761426
doi: 10.1016/j.nbd.2007.07.007
Bugiani M, Plug BC, Man JHK, Breur M, van der Knaap MS. Heterogeneity of white matter astrocytes in the human brain. Acta Neuropathol. 2022;143(2):159–77.
pubmed: 34878591
doi: 10.1007/s00401-021-02391-3
Probst A, Ulrich J, Heitz PU, Herschkowitz N. Adrenomyeloneuropathy. A protracted, pseudosystematic variant of adrenoleukodystrophy. Acta Neuropathol. 1980;49(2):105–15.
pubmed: 6243840
doi: 10.1007/BF00690750
Schaumburg HH, Powers JM, Raine CS, Spencer PS, Griffin JW, Prineas JW, Boehme DM. Adrenomyeloneuropathy: a probable variant of adrenoleukodystrophy. II. General pathologic, neuropathologic, and biochemical aspects. Neurology. 1977;27(12):1114–9.
pubmed: 200862
doi: 10.1212/WNL.27.12.1114
Marino S, De Luca M, Dotti MT, Stromillo ML, Formichi P, Galluzzi P, et al. Prominent brain axonal damage and functional reorganization in pure adrenomyeloneuropathy. Neurology. 2007;69(12):1261–9.
pubmed: 17875914
doi: 10.1212/01.wnl.0000276945.92950.69
Powers JM, Schaumburg HH. Adreno-Leukodystrophy (sex-linked Schilder’s disease). A pathogenetic hypothesis based on ultrastructural lesions in adrenal cortex, peripheral nerve and testis. Am J Pathol. 1974;76(3):481–91.
pubmed: 4212914
pmcid: 1910882
van Geel BM, Koelman JH, Barth PG, Ongerboer de Visser BW. Peripheral nerve abnormalities in adrenomyeloneuropathy: a clinical and electrodiagnostic study. Neurology. 1996;46(1):112–8.
pubmed: 8559356
doi: 10.1212/WNL.46.1.112
Horn MA, Nilsen KB, Jørum E, Mellgren SI, Tallaksen CM. Small nerve fiber involvement is frequent in X-linked adrenoleukodystrophy. Neurology. 2014;82(19):1678–83.
pubmed: 24719486
doi: 10.1212/WNL.0000000000000415
Gong Y, Sasidharan N, Laheji F, Frosch M, Musolino P, Tanzi R, et al. Microglial dysfunction as a key pathological change in adrenomyeloneuropathy. Ann Neurol. 2017;82(5):813–27.
pubmed: 29059709
pmcid: 5725816
doi: 10.1002/ana.25085
Engelen M, Kemp S, de Visser M, van Geel BM, Wanders RJ, Aubourg P, Poll-The BT. X-linked adrenoleukodystrophy (X-ALD): clinical presentation and guidelines for diagnosis, follow-up and management. Orphanet J Rare Dis. 2012;7:51.
pubmed: 22889154
pmcid: 3503704
doi: 10.1186/1750-1172-7-51
Schaumburg HH, Powers JM, Suzuki K, Raine CS. Adreno-Leukodystrophy (sex-linked Schilder disease). Ultrastructural demonstration of specific cytoplasmic inclusions in the central nervous system. Arch Neurol. 1974;31(3):210–3.
pubmed: 4368379
doi: 10.1001/archneur.1974.00490390092013
Powers JM, Liu Y, Moser AB, Moser HW. The inflammatory myelinopathy of adreno-leukodystrophy: cells, effector molecules, and pathogenetic implications. J Neuropathol Exp Neurol. 1992;51(6):630–43.
pubmed: 1362438
doi: 10.1097/00005072-199211000-00007
Ito M, Blumberg BM, Mock DJ, Goodman AD, Moser AB, Moser HW, et al. Potential environmental and host participants in the early white matter lesion of adreno-leukodystrophy: morphologic evidence for CD8 cytotoxic T cells, cytolysis of oligodendrocytes, and CD1-mediated lipid antigen presentation. J Neuropathol Exp Neurol. 2001;60(10):1004–19.
pubmed: 11589421
doi: 10.1093/jnen/60.10.1004
Eichler FS, Ren JQ, Cossoy M, Rietsch AM, Nagpal S, Moser AB, et al. Is microglial apoptosis an early pathogenic change in cerebral X-linked adrenoleukodystrophy? Ann Neurol. 2008;63(6):729–42.
pubmed: 18571777
doi: 10.1002/ana.21391
van der Voorn JP, Pouwels PJ, Powers JM, Kamphorst W, Martin JJ, Troost D, et al. Correlating quantitative MR imaging with histopathology in X-linked adrenoleukodystrophy. AJNR Am J Neuroradiol. 2011;32(3):481–9.
pubmed: 21273354
pmcid: 8013090
doi: 10.3174/ajnr.A2327
Bergner CG, Genc N, Hametner S, Franz J, van der Meer F, Mitkovski M, et al. Concurrent axon and myelin destruction differentiates X-linked adrenoleukodystrophy from multiple sclerosis. Glia. 2021;69(10):2362–77.
pubmed: 34137074
doi: 10.1002/glia.24042
Weinhofer I, Rommer P, Gleiss A, Ponleitner M, Zierfuss B, Waidhofer-Söllner P, et al. Biomarker-based risk prediction for the onset of neuroinflammation in X-linked adrenoleukodystrophy. EBioMedicine. 2023;96:104781.
pubmed: 37683329
pmcid: 10497986
doi: 10.1016/j.ebiom.2023.104781
Selmaj KW, Raine CS. Tumor necrosis factor mediates myelin and oligodendrocyte damage in vitro. Ann Neurol. 1988;23(4):339–46.
pubmed: 3132891
doi: 10.1002/ana.410230405
Görtz AL, Peferoen LAN, Gerritsen WH, van Noort JM, Bugiani M, Amor S. Heat shock protein expression in cerebral X-linked adrenoleukodystrophy reveals astrocyte stress prior to myelin loss. Neuropathol Appl Neurobiol. 2018;44(4):363–76.
pubmed: 28319253
doi: 10.1111/nan.12399
Marchetti DP, Donida B, Jacques CE, Deon M, Hauschild TC, Koehler-Santos P, et al. Inflammatory profile in X-linked adrenoleukodystrophy patients: understanding disease progression. J Cell Biochem. 2018;119(1):1223–33.
pubmed: 28722826
doi: 10.1002/jcb.26295
Lannuzel A, Aubourg P, Tardieu M. Excessive production of tumour necrosis factor alpha by peripheral blood mononuclear cells in X-linked adrenoleukodystrophy. Eur J Paediatr Neurol. 1998;2(1):27–32.
pubmed: 10726843
doi: 10.1016/1090-3798(98)01002-7
Weinhofer I, Zierfuss B, Hametner S, Wagner M, Popitsch N, Machacek C, et al. Impaired plasticity of macrophages in X-linked adrenoleukodystrophy. Brain. 2018;141(8):2329–42.
pubmed: 29860501
pmcid: 6061697
doi: 10.1093/brain/awy127
Bergner CG, van der Meer F, Winkler A, Wrzos C, Türkmen M, Valizada E, et al. Microglia damage precedes major myelin breakdown in X-linked adrenoleukodystrophy and metachromatic leukodystrophy. Glia. 2019;67(6):1196–209.
pubmed: 30980503
pmcid: 6594046
doi: 10.1002/glia.23598
Cartier N, Lewis CA, Zhang R, Rossi FM. The role of microglia in human disease: therapeutic tool or target? Acta Neuropathol. 2014;128(3):363–80.
pubmed: 25107477
pmcid: 4131134
doi: 10.1007/s00401-014-1330-y
Aubourg P, Blanche S, Jambaqué I, Rocchiccioli F, Kalifa G, Naud-Saudreau C, et al. Reversal of early neurologic and neuroradiologic manifestations of X-linked adrenoleukodystrophy by bone marrow transplantation. N Engl J Med. 1990;322(26):1860–6.
pubmed: 2348839
doi: 10.1056/NEJM199006283222607
Cartier N, Hacein-Bey-Abina S, Bartholomae CC, Veres G, Schmidt M, Kutschera I, et al. Hematopoietic stem cell gene therapy with a lentiviral vector in X-linked adrenoleukodystrophy. Science. 2009;326(5954):818–23.
pubmed: 19892975
doi: 10.1126/science.1171242
Weber FD, Wiesinger C, Forss-Petter S, Regelsberger G, Einwich A, Weber WH, et al. X-linked adrenoleukodystrophy: very long-chain fatty acid metabolism is severely impaired in monocytes but not in lymphocytes. Hum Mol Genet. 2014;23(10):2542–50.
pubmed: 24363066
doi: 10.1093/hmg/ddt645
van Geel BM, Poll-The BT, Verrips A, Boelens JJ, Kemp S, Engelen M. Hematopoietic cell transplantation does not prevent myelopathy in X-linked adrenoleukodystrophy: a retrospective study. J Inherit Metab Dis. 2015;38(2):359–61.
pubmed: 25488625
doi: 10.1007/s10545-014-9797-1
Amor S, McNamara NB, Gerrits E, Marzin MC, Kooistra SM, Miron VE, Nutma E. White matter microglia heterogeneity in the CNS. Acta Neuropathol. 2022;143(2):125–41.
pubmed: 34878590
doi: 10.1007/s00401-021-02389-x
A O, U M, Lf B. Energy metabolism in childhood neurodevelopmental disorders. EBioMedicine. 2021;69:103474.
doi: 10.1016/j.ebiom.2021.103474
Lauer A, Da X, Hansen MB, Boulouis G, Ou Y, Cai X, et al. ABCD1 dysfunction alters white matter microvascular perfusion. Brain. 2017;140(12):3139–52.
pubmed: 29136088
pmcid: 5841142
doi: 10.1093/brain/awx262
Musolino PL, Gong Y, Snyder JM, Jimenez S, Lok J, Lo EH, et al. Brain endothelial dysfunction in cerebral adrenoleukodystrophy. Brain. 2015;138(Pt 11):3206–20.
pubmed: 26377633
pmcid: 4731416
doi: 10.1093/brain/awv250
Brown FR 3rd, Chen WW, Kirschner DA, Frayer KL, Powers JM, Moser AB, Moser HW. Myelin membrane from adrenoleukodystrophy brain white matter–biochemical properties. J Neurochem. 1983;41(2):341–8.
pubmed: 6875541
doi: 10.1111/j.1471-4159.1983.tb04748.x
Wilson R, Sargent JR. Lipid and fatty acid composition of brain tissue from adrenoleukodystrophy patients. J Neurochem. 1993;61(1):290–7.
pubmed: 8515276
doi: 10.1111/j.1471-4159.1993.tb03567.x
Buda A, Forss-Petter S, Hua R, Jaspers Y, Lassnig M, Waidhofer-Söllner P et al. ABCD1 Transporter Deficiency results in altered cholesterol homeostasis. Biomolecules. 2023;13(9).
Di Rocco M, Doria-Lamba L, Caruso U. Monozygotic twins with X-linked adrenoleukodystrophy and different phenotypes. Ann Neurol. 2001;50(3):424.
pubmed: 11558805
doi: 10.1002/ana.1220
Wiesinger C, Eichler FS, Berger J. The genetic landscape of X-linked adrenoleukodystrophy: inheritance, mutations, modifier genes, and diagnosis. Appl Clin Genet. 2015;8:109–21.
pubmed: 25999754
pmcid: 4427263
van Engen CE, Ofman R, Dijkstra IM, van Goethem TJ, Verheij E, Varin J, et al. CYP4F2 affects phenotypic outcome in adrenoleukodystrophy by modulating the clearance of very long-chain fatty acids. Biochim Biophys Acta. 2016;1862(10):1861–70.
pubmed: 27425035
doi: 10.1016/j.bbadis.2016.07.006
Ofman R, Dijkstra IM, van Roermund CW, Burger N, Turkenburg M, van Cruchten A, et al. The role of ELOVL1 in very long-chain fatty acid homeostasis and X-linked adrenoleukodystrophy. EMBO Mol Med. 2010;2(3):90–7.
pubmed: 20166112
pmcid: 3377275
doi: 10.1002/emmm.201000061
Kemp S, Berger J, Aubourg P. X-linked adrenoleukodystrophy: clinical, metabolic, genetic and pathophysiological aspects. Biochim Biophys Acta. 2012;1822(9):1465–74.
pubmed: 22483867
doi: 10.1016/j.bbadis.2012.03.012
Raas Q, van de Beek MC, Forss-Petter S, Dijkstra IM, Deschiffart A, Freshner BC et al. Metabolic rerouting via SCD1 induction impacts X-linked adrenoleukodystrophy. J Clin Invest. 2021;131(8).
van de Stadt SIW, Huffnagel IC, Turk BR, van der Knaap MS, Engelen M. Imaging in X-Linked adrenoleukodystrophy. Neuropediatrics. 2021;52(4):252–60.
pubmed: 34192790
doi: 10.1055/s-0041-1730937
Raymond GV, Seidman R, Monteith TS, Kolodny E, Sathe S, Mahmood A, Powers JM. Head trauma can initiate the onset of adreno-leukodystrophy. J Neurol Sci. 2010;290(1–2):70–4.
pubmed: 19945717
doi: 10.1016/j.jns.2009.11.005
Cartier N, Aubourg P. Hematopoietic stem cell transplantation and hematopoietic stem cell gene therapy in X-linked adrenoleukodystrophy. Brain Pathol. 2010;20(4):857–62.
pubmed: 20626747
pmcid: 8094635
doi: 10.1111/j.1750-3639.2010.00394.x
Orchard PJ, Nascene DR, Miller WP, Gupta A, Kenney-Jung D, Lund TC. Successful donor engraftment and repair of the blood-brain barrier in cerebral adrenoleukodystrophy. Blood. 2019;133(12):1378–81.
pubmed: 30635285
pmcid: 6440119
doi: 10.1182/blood-2018-11-887240
Schlüter A, Sandoval J, Fourcade S, Díaz-Lagares A, Ruiz M, Casaccia P, et al. Epigenomic signature of adrenoleukodystrophy predicts compromised oligodendrocyte differentiation. Brain Pathol. 2018;28(6):902–19.
pubmed: 29476661
pmcid: 6857458
doi: 10.1111/bpa.12595
Mallack EJ, Gao K, Engelen M, Kemp S. Structure and function of the ABCD1 variant database: 20 years, 940 pathogenic variants, and 3400 cases of Adrenoleukodystrophy. Cells. 2022;11(2).
Barnett SC, Linington C. Myelination: do astrocytes play a role? Neuroscientist. 2013;19(5):442–50.
pubmed: 23131748
doi: 10.1177/1073858412465655
Baarine M, Khan M, Singh A, Singh I. Functional characterization of IPSC-Derived brain cells as a model for X-Linked adrenoleukodystrophy. PLoS ONE. 2015;10(11):e0143238.
pubmed: 26581106
pmcid: 4651558
doi: 10.1371/journal.pone.0143238
van der Knaap MS, Bugiani M. Leukodystrophies: a proposed classification system based on pathological changes and pathogenetic mechanisms. Acta Neuropathol. 2017;134(3):351–82.
pubmed: 28638987
pmcid: 5563342
doi: 10.1007/s00401-017-1739-1