Functional genomic analysis unravels a metabolic-inflammatory interplay in adrenoleukodystrophy

Human Molecular Genetics

Volumn 21, Issue 5, 2012, Pages 1062-1077

  Schlüter, Agatha ^a,b   Espinosa, Lluís ^c   Fourcade, Stéphane ^a,b   Galino, Jorge ^a,b   Lśpez, Eva ^a,b   Ilieva, Ekaterina ^a,b   Morató, Laia ^a,b   Asheuer, Muriel ^d   Cook, Ted ^e   McLaren, Alistair ^e   Reid, Juliet ^e   Kelly, Fiona ^e   Bates, Stewart ^e   Aubourg, Patrick ^d   Galea, Elena ^f,g   Pujol, Aurora ^a,b,g  

^a HOSPITAL UNIVERSITARI DE BELLVITGE   (Spain)

^b CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED DE ENFERMEDADES RARAS CIBERER   (Spain)

^c HOSPITAL DEL MAR   (Spain)

^d INSERM   (France)

^e GLAXOSMITHKLINE   (United Kingdom)

^f INSTITUT DE NEUROCIÈNCIES   (Spain)

^g INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPOCYTOKINE; INSULIN; VERY LONG CHAIN FATTY ACID;

ADRENOLEUKODYSTROPHY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CEREBRAL ADRENOMYELONEUROPATHY; CONTROLLED STUDY; FUNCTIONAL GENOMICS; MALE; METABOLIC DISORDER; MOUSE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; SPINAL CORD; TRANSCRIPTOMICS; WESTERN BLOTTING;

ADIPOKINES; ADIPONECTIN; ADRENOLEUKODYSTROPHY; ADULT; ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BIOSYNTHETIC PATHWAYS; BRAIN; CHILD; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; FATTY ACIDS; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION STUDIES; HUMANS; I-KAPPA B KINASE; INSULIN; INSULIN RESISTANCE; LEPTIN; METABOLIC NETWORKS AND PATHWAYS; MICE; NF-KAPPA B; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; SIGNAL TRANSDUCTION; SPINAL CORD; TOLL-LIKE RECEPTORS; TRANSCRIPTOME;

EID: 84856955371     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddr536     Document Type: Article

References (57)

1. Ferrer, I., Aubourg, P. and Pujol, A. (2010) General aspects and neuropathology of X-linked adrenoleukodystrophy. Brain Pathol., 20, 817-830.
2. Mosser, J., Douar, A.M., Sarde, C.O., Kioschis, P., Feil, R., Moser, H., Poustka, A.M., Mandel, J.L. and Aubourg, P. (1993) Putative X-linked adrenoleukodystrophy gene shares unexpected homology with ABC transporters. Nature, 361, 726-730.
3. van Roermund, C.W., Visser, W.F., Ijlst, L., van Cruchten, A., Boek, M., Kulik, W., Waterham, H.R. and Wanders, R.J. (2008) The human peroxisomal ABC half transporter ALDP functions as a homodimer and accepts acyl-CoA esters. FASEB J., 22, 4201-4208.
4. Kemp, S., Pujol, A., Waterham, H.R., van Geel, B.M., Boehm, C.D., Raymond, G.V., Cutting, G.R., Wanders, R.J. and Moser, H.W. (2001) ABCD1 mutations and the X-linked adrenoleukodystrophy mutation database: role in diagnosis and clinical correlations. Hum. Mutat., 18, 499-515.
5. Moser, H., Smith, K.D., Watkins, P.A., Powers, J. and Moser, A.B. (2001) In Scriver, C. (ed.), The Metabolic and Molecular Bases of Inherited Disease. McGraw-Hill, New York, pp. 3257-3301.
6. Asheuer, M., Bieche, I., Laurendeau, I., Moser, A., Hainque, B., Vidaud, M. and Aubourg, P. (2005) Decreased expression of ABCD4 and BG1 genes early in the pathogenesis of X-linked adrenoleukodystrophy. Hum. Mol. Genet., 14, 1293-1303.
7. Cartier, N., Hacein-Bey-Abina, S., Bartholomae, C.C., Veres, G., Schmidt, M., Kutschera, I., Vidaud, M., Abel, U., Dal-Cortivo, L., Caccavelli, L. et al. (2009) Hematopoietic stem cell gene therapy with a lentiviral vector in X-linked adrenoleukodystrophy. Science, 326, 818-823.
8. Pujol, A., Ferrer, I., Camps, C., Metzger, E., Hindelang, C., Callizot, N., Ruiz, M., Pampols, T., Giros, M. and Mandel, J.L. (2004) Functional overlap between ABCD1 (ALD) and ABCD2 (ALDR) transporters: a therapeutic target for X-adrenoleukodystrophy. Hum. Mol. Genet., 13, 2997-3006.
9. Pujol, A., Hindelang, C., Callizot, N., Bartsch, U., Schachner, M. and Mandel, J.L. (2002) Late onset neurological phenotype of the X-ALD gene inactivation in mice: a mouse model for adrenomyeloneuropathy. Hum. Mol. Genet., 11, 499-505.
10. Forss-Petter, S., Werner, H., Berger, J., Lassmann, H., Molzer, B., Schwab, M.H., Bernheimer, H., Zimmermann, F. and Nave, K.A. (1997) Targeted inactivation of the X-linked adrenoleukodystrophy gene in mice. J. Neurosci. Res., 50, 829-843.
11. Lu, J.F., Lawler, A.M., Watkins, P.A., Powers, J.M., Moser, A.B., Moser, H.W. and Smith, K.D. (1997) A mouse model for X-linked adrenoleukodystrophy. Proc. Natl Acad. Sci. USA, 94, 9366-9371.
12. Singh, I. and Pujol, A. (2010) Pathomechanisms underlying X-adrenoleukodystrophy: a three-hit hypothesis. Brain Pathol., 20, 838-844.
13. Ashburner, M., Ball, C.A., Blake, J.A., Botstein, D., Butler, H., Cherry, J.M., Davis, A.P., Dolinski, K., Dwight, S.S., Eppig, J.T. et al. (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet., 25, 25-29.
14. Kanehisa, M. and Goto, S. (2000) KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res., 28, 27-30.
15. Eichler, F.S., Ren, J.Q., Cossoy, M., Rietsch, A.M., Nagpal, S., Moser, A.B., Frosch, M.P. and Ransohoff, R.M. (2008) Is microglial apoptosis an early pathogenic change in cerebral X-linked adrenoleukodystrophy? Ann. Neurol., 63, 729-742.
16. Tilg, H. and Moschen, A.R. (2006) Adipocytokines: mediators linking adipose tissue, inflammation and immunity. Nat. Rev. Immunol., 6, 772-783.
17. Wymann, M.P. and Schneiter, R. (2008) Lipid signalling in disease. Nat. Rev. Mol. Cell Biol., 9, 162-176.
18. Aguirre, V., Werner, E.D., Giraud, J., Lee, Y.H., Shoelson, S.E. and White, M.F. (2002) Phosphorylation of Ser307 in insulin receptor substrate-1 blocks interactions with the insulin receptor and inhibits insulin action. J. Biol. Chem., 277, 1531-1537.
19. Gao, Z., Hwang, D., Bataille, F., Lefevre, M., York, D., Quon, M.J. and Ye, J. (2002) Serine phosphorylation of insulin receptor substrate 1 by inhibitor kappa B kinase complex. J. Biol. Chem., 277, 48115-48121.
20. Tsukumo, D.M., Carvalho-Filho, M.A., Carvalheira, J.B., Prada, P.O., Hirabara, S.M., Schenka, A.A., Araujo, E.P., Vassallo, J., Curi, R., Velloso, L.A. et al. (2007) Loss-of-function mutation in Toll-like receptor 4 prevents diet-induced obesity and insulin resistance. Diabetes, 56, 1986-1998.
21. Um, S.H., Frigerio, F., Watanabe, M., Picard, F., Joaquin, M., Sticker, M., Fumagalli, S., Allegrini, P.R., Kozma, S.C., Auwerx, J. et al. (2004) Absence of S6K1 protects against age- and diet-induced obesity while enhancing insulin sensitivity. Nature, 431, 200-205.
22. Fourcade, S., Lopez-Erauskin, J., Galino, J., Duval, C., Naudi, A., Jove, M., Kemp, S., Villarroya, F., Ferrer, I., Pamplona, R. et al. (2008) Early oxidative damage underlying neurodegeneration in X-adrenoleukodystrophy. Hum. Mol. Genet., 17, 1762-1773.
23. Hein, S., Schonfeld, P., Kahlert, S. and Reiser, G. (2008) 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., 17, 1750-1761.
24. Galino, J., Ruiz, M., Fourcade, S., Schluter, A., Lopez-Erauskin, J., Guilera, C., Jove, M., Naudi, A., Garcia-Arumi, E., Andreu, A.L. et al. (2011) Oxidative damage compromises energy metabolism in the axonal degeneration mouse model of X-adrenoleukodystrophy. Antioxid. Redox Signal, 15, 2095-2107.
25. Lopez-Erauskin, J., Fourcade, S., Galino, J., Ruiz, M., Schluter, A., Naudi, A., Jove, M., Portero-Otin, M., Pamplona, R., Ferrer, I. et al. (2011) Antioxidants halt axonal degeneration in a mouse model of X-adrenoleukodystrophy. Ann. Neurol., 70, 84-92.
26. Hooijmans, C.R. and Kiliaan, A.J. (2008) Fatty acids, lipid metabolism and Alzheimer pathology. Eur. J. Pharmacol., 585, 176-196.
27. Starkov, A.A., Fiskum, G., Chinopoulos, C., Lorenzo, B.J., Browne, S.E., Patel, M.S. and Beal, M.F. (2004) Mitochondrial alpha-ketoglutarate dehydrogenase complex generates reactive oxygen species. J. Neurosci. Res., 24, 7779-7788.
28. Gilg, A.G., Singh, A.K. and Singh, I. (2000) Inducible nitric oxide synthase in the central nervous system of patients with X-adrenoleukodystrophy. J. Neuropathol. Exp. Neurol., 59, 1063-1069.
29. Powers, J.M., Pei, Z., Heinzer, A.K., Deering, R., Moser, A.B., Moser, H.W., Watkins, P.A. and Smith, K.D. (2005) Adreno-leukodystrophy: oxidative stress of mice and men. J. Neuropathol. Exp. Neurol., 64, 1067-1079.
30. Bernheimer, H., Budka, H. and Muller, P. (1983) Brain tissue immunoglobulins in adrenoleukodystrophy: a comparison with multiple sclerosis and systemic lupus erythematosus. Acta Neuropathol., 59, 95-102.
31. Ho, J.K., Moser, H., Kishimoto, Y. and Hamilton, J.A. (1995) Interactions of a very long chain fatty acid with model membranes and serum albumin: implications for the pathogenesis of adrenoleukodystrophy. J. Clin. Invest., 96, 1455-1463.
32. Powers, J.M. and Moser, H.W. (1998) Peroxisomal disorders: genotype, phenotype, major neuropathologic lesions, and pathogenesis. Brain Pathol., 8, 101-120.
33. Boden, G., She, P., Mozzoli, M., Cheung, P., Gumireddy, K., Reddy, P., Xiang, X., Luo, Z. and Ruderman, N. (2005) Free fatty acids produce insulin resistance and activate the proinflammatory nuclear factor-kappaB pathway in rat liver. Diabetes, 54, 3458-3465.
34. Griffin, M.E., Marcucci, M.J., Cline, G.W., Bell, K., Barucci, N., Lee, D., Goodyear, L.J., Kraegen, E.W., White, M.F. and Shulman, G.I. (1999) Free fatty acid-induced insulin resistance is associated with activation of protein kinase C theta and alterations in the insulin signaling cascade. Diabetes, 48, 1270-1274.
35. Evans, J.L., Maddux, B.A. and Goldfine, I.D. (2005) The molecular basis for oxidative stress-induced insulin resistance. Antioxid. Redox Signal, 7, 1040-1052.
36. Singh, J., Khan, M. and Singh, I. (2009) Silencing of Abcd1 and Abcd2 genes sensitizes astrocytes for inflammation: implication for X-adrenoleukodystrophy. J Lipid Res., 50, 135-147.
37. Henkel, J.S., Beers, D.R., Siklos, L. and Appel, S.H. (2006) The chemokine MCP-1 and the dendritic and myeloid cells it attracts are increased in the mSOD1 mouse model of ALS. Mol. Cell. Neurosci., 31, 427-437.
38. Henkel, J.S., Engelhardt, J.I., Siklos, L., Simpson, E.P., Kim, S.H., Pan, T., Goodman, J.C., Siddique, T., Beers, D.R. and Appel, S.H. (2004) Presence of dendritic cells, MCP-1, and activated microglia/macrophages in amyotrophic lateral sclerosis spinal cord tissue. Ann. Neurol., 55, 221-235.
39. Hotamisligil, G.S. (2006) Inflammation and metabolic disorders. Nature, 444, 860-867.
40. Shi, H., Kokoeva, M.V., Inouye, K., Tzameli, I., Yin, H. and Flier, J.S. (2006) TLR4 links innate immunity and fatty acid-induced insulin resistance. J. Clin. Invest., 116, 3015-3025.
41. Cartier, N. and Aubourg, P. (2010) Hematopoietic stem cell transplantation and hematopoietic stem cell gene therapy in X-linked adrenoleukodystrophy. Brain Pathol., 20, 857-862.
42. Paintlia, A.S., Gilg, A.G., Khan, M., Singh, A.K., Barbosa, E. and Singh, I. (2003) Correlation of very long chain fatty acid accumulation and inflammatory disease progression in childhood X-ALD: implications for potential therapies. Neurobiol. Dis., 14, 425-439.
43. Wolf, A.M., Wolf, D., Rumpold, H., Enrich, B. and Tilg, H. (2004) Adiponectin induces the anti-inflammatory cytokines IL-10 and IL-1RA in human leukocytes. Biochem. Biophys. Res. Commun., 323, 630-635.
44. Yamaguchi, N., Argueta, J.G., Masuhiro, Y., Kagishita, M., Nonaka, K., Saito, T., Hanazawa, S. and Yamashita, Y. (2005) Adiponectin inhibits Toll-like receptor family-induced signaling. FEBS Lett., 579, 6821-6826.
45. Spranger, J., Verma, S., Gohring, I., Bobbert, T., Seifert, J., Sindler, A.L., Pfeiffer, A., Hileman, S.M., Tschop, M. and Banks, W.A. (2006) Adiponectin does not cross the blood-brain barrier but modifies cytokine expression of brain endothelial cells. Diabetes, 55, 141-147.
46. Glezer, I., Lapointe, A. and Rivest, S. (2006) Innate immunity triggers oligodendrocyte progenitor reactivity and confines damages to brain injuries. FASEB J., 20, 750-752.
47. Fassbender, K., Walter, S., Kuhl, S., Landmann, R., Ishii, K., Bertsch, T., Stalder, A.K., Muehlhauser, F., Liu, Y., Ulmer, A.J. et al. (2004) The LPS receptor (CD14) links innate immunity with Alzheimer's disease. FASEB J., 18, 203-205.
48. Bate, C., Veerhuis, R., Eikelenboom, P. and Williams, A. (2004) Microglia kill amyloid-beta1-42 damaged neurons by a CD14-dependent process. Neuroreport, 15, 1427-1430.
49. Yuan, M., Konstantopoulos, N., Lee, J., Hansen, L., Li, Z.W., Karin, M. and Shoelson, S.E. (2001) Reversal of obesity- and diet-induced insulin resistance with salicylates or targeted disruption of Ikkbeta. Science, 293, 1673-1677.
50. Lunnon, K., Teeling, J.L., Tutt, A.L., Cragg, M.S., Glennie, M.J. and Perry, V.H. (2011) Systemic inflammation modulates Fc receptor expression on microglia during chronic neurodegeneration. J. Immunol., 186, 7215-7224.
51. Ferrer, I., Kapfhammer, J.P., Hindelang, C., Kemp, S., Troffer-Charlier, N., Broccoli, V., Callyzot, N., Mooyer, P., Selhorst, J., Vreken, P. et al. (2005) Inactivation of the peroxisomal ABCD2 transporter in the mouse leads to late-onset ataxia involving mitochondria, Golgi and endoplasmic reticulum damage. Hum. Mol. Genet., 14, 3565-3577.
52. Ghate, A., Befort, K., Becker, J.A., Filliol, D., Bole-Feysot, C., Demebele, D., Jost, B., Koch, M. and Kieffer, B.L. (2007) Identification of novel striatal genes by expression profiling in adult mouse brain. Neuroscience, 146, 1182-1192.
53. Gentleman, R.C., Carey, V.J., Bates, D.M., Bolstad, B., Dettling, M., Dudoit, S., Ellis, B., Gautier, L., Ge, Y., Gentry, J. et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol., 5, R80.
54. Smyth, G.K. (2005) In Gentleman, R., Carey, V., Dudoit, S., Irizarry, R. and Huber, W. (eds), Bioinformatics and Computational Biology Solutions using R and Bioconductor. Springer, New York, pp. 397-420.
55. Mootha, V.K., Lindgren, C.M., Eriksson, K.F., Subramanian, A., Sihag, S., Lehar, J., Puigserver, P., Carlsson, E., Ridderstrale, M., Laurila, E. et al. (2003) PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat. Genet., 34, 267-273.
56. Krassioukov, A.V., Ackery, A., Schwartz, G., Adamchik, Y., Liu, Y. and Fehlings, M.G. (2002) An in vitro model of neurotrauma in organotypic spinal cord cultures from adult mice. Brain Res. Brain Res. Protoc., 10, 60-68.
57. Rothstein, J.D., Jin, L., Dykes-Hoberg, M. and Kuncl, R.W. (1993) Chronic inhibition of glutamate uptake produces a model of slow neurotoxicity. Proc. Natl Acad. Sci. USA, 90, 6591-6595.