Toxic effects of X-linked adrenoleukodystrophy-associated, very long chain fatty acids on glial cells and neurons from rat hippocampus in culture

Human Molecular Genetics

Volumn 17, Issue 12, 2008, Pages 1750-1761

  Hein, Sabine ^a   Schönfeld, Peter ^b   Kahlert, Stefan ^a   Reiser, Georg ^a  

^a Institut für Neurobiochemie

^b OTTO VON GUERICKE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BEHENIC ACID; CALCIUM; FATTY ACID; HEXACOSANOIC ACID; LIGNOCERIC ACID; VERY LONG CHAIN FATTY ACID;

ADRENOLEUKODYSTROPHY; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CALCIUM CELL LEVEL; CALCIUM DEFICIENCY; CELL DEATH; CELL FUNCTION; CELL MEMBRANE DEPOLARIZATION; CONTROLLED STUDY; DEGENERATIVE DISEASE; DISORDERS OF PEROXISOMAL FUNCTIONS; GLIA CELL; HIPPOCAMPUS; MITOCHONDRIAL TOXICITY; MITOCHONDRION; NERVE CELL; NERVE CELL CULTURE; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; RAT; X CHROMOSOME LINKED DISORDER;

ADRENOLEUKODYSTROPHY; ANIMALS; ASTROCYTES; CALCIUM SIGNALING; CELL DEATH; CELLS, CULTURED; FATTY ACIDS; HIPPOCAMPUS; MITOCHONDRIA; NEUROGLIA; NEURONS; OLIGODENDROGLIA; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES;

ANIMALIA; RATTUS;

EID: 44849118490     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddn066     Document Type: Article

References (68)

1. Moser, A.B., Kreiter, N., Bezman, L., Lu, S., Raymond, G.V., Naidu, S. and Moser, H.W. (1999) Plasma very long chain fatty acids in 3,000 peroxisome disease patients and 29,000 controls. Ann. Neurol., 45, 100-110.
2. Moser, H.W. (1997) Adrenoleukodystrophy: Phenotype, genetics, pathogenesis and therapy. Brain, 120, 1485-1508.
3. van Geel, B.M., Assies, J., Weverling, G.J. and Barth, P.G. (1994) Predominance of the adrenomyeloneuropathy phenotype of X-linked adrenoleukodystrophy in The Netherlands: A survey of 30 kindreds. Neurology, 44, 2343-2346.
4. Aubourg, P. (1999) On the front of X-linked adrenoleukodystrophy. Neurochem. Res., 24, 515-520.
5. Aubourg, P. and Dubois-Dalcq, M. (2000) X-linked adrenoleukodystrophy enigma: How does the ALD peroxisomal transporter mutation affect CNS glia? Glia, 29, 186-190.
6. Igarashi, M., Schaumburg, H.H., Powers, J., Kishmoto, Y., Kolodny, E. and Suzuki, K. (1976) Fatty acid abnormality in adrenoleukodystrophy. J. Neurochem., 26, 851-860.
7. Singh, I., Moser, A.E., Moser, H.W. and Kishimoto, Y. (1984) Adrenoleukodystrophy: Impaired oxidation of very long chain fatty acids in white blood cells, cultured skin fibroblasts, and amniocytes. Pediatr. Res., 18, 286-290.
8. Valianpour, F., Selhorst, J.J., van Lint, L.E., van Gennip, A.H., Wanders, R.J. and Kemp, S. (2003) Analysis of very long-chain fatty acids using electrospray ionization mass spectrometry. Mol. Genet. Metab., 79, 189-196.
9. 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.
10. Wanders, R.J. and Tager, J.M. (1998) Lipid metabolism in peroxisomes in relation to human disease. Mol. Aspects Med., 19, 69-154.
11. Kemp, S., Wei, H.M., Lu, J.F., Braiterman, L.T., McGuinness, M.C., Moser, A.B., Watkins, P.A. and Smith, K.D. (1998) Gene redundancy and pharmacological gene therapy: Implications for X-linked adrenoleukodystrophy. Nat. Med., 4, 1261-1268.
12. Verhoeven, N.M., Roe, D.S., Kok, R.M., Wanders, R.J., Jakobs, C. and Roe, C.R. (1998) Phytanic acid and pristanic acid are oxidized by sequential peroxisomal and mitochondrial reactions in cultured fibroblasts. J. Lipid Res., 39, 66-74.
13. Fouquet, F., Zhou, J.M., Ralston, E., Murray, K., Troalen, F., Magal, E., Robain, O., Dubois-Dalcq, M. and Aubourg, P. (1997) Expression of the adrenoleukodystrophy protein in the human and mouse central nervous system. Neurobiol. Dis., 3, 271-285.
14. Gould, S.J. and Valle, D. (2000) Peroxisome biogenesis disorders: genetics and cell biology. Trends Genet., 16, 340-345.
15. Wanders, R.J. and Waterham, H.R. (2005) Peroxisomal disorders I: biochemistry and genetics of peroxisome biogenesis disorders. Clin. Genet., 67, 107-133.
16. Weller, S., Gould, S.J. and Valle, D. (2003) Peroxisome biogenesis disorders. Annu. Rev. Genomics Hum. Genet., 4, 165-211.
17. 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.
18. Powers, J.M. and Moser, H.W. (1998) Peroxisomal disorders: Genotype, phenotype, major neuropathologic lesions, and pathogenesis. Brain Pathol., 8, 101-120.
19. Dubois-Dalcq, M., Feigenbaum, V. and Aubourg, P. (1999) The neurobiology of X-linked adrenoleukodystrophy, a demyelinating peroxisomal disorder. Trends Neurosci., 22, 4-12.
20. Powers, J.M., Liu, Y., Moser, A.B. and Moser, H.W. (1992) The inflammatory myelinopathy of adreno-leukodystrophy: Cells, effector molecules, and pathogenetic implications. J. Neuropathol. Exp. Neurol., 51, 630-643.
21. Selmaj, K., Raine, C.S., Cannella, B. and Brosnan, C.F. (1991) Identification of lymphotoxin and tumor necrosis factor in multiple sclerosis lesions. J. Clin. Invest., 87, 949-954.
22. Takuma, K., Baba, A. and Matsuda, T. (2004) Astrocyte apoptosis: implications for neuroprotection. Prog. Neurobiol., 72, 111-127.
23. Blomgren, K., Zhu, C., Hallin, U. and Hagberg, H. (2003) Mitochondria and ischemic reperfusion damage in the adult and in the developing brain. Biochem. Biophys. Res. Commun., 304, 551-559.
24. Hunter, D.R., Haworth, R.A. and Southard, J.H. (1976) Relationship between configuration, function, and permeability in calcium-treated mitochondria. J. Biol. Chem., 251, 5069-5077.
25. 2+ homeostasis and mitochondria, and reduces cell viability in rat hippocampal astrocytes. Neurobiol. Dis., 18, 110-118.
26. Reiser, G., Schönfeld, P. and Kahlert, S. (2006) Mechanism of toxicity of the branched-chain fatty acid phytanic acid, a marker of Refsum disease, in astrocytes involves mitochondrial impairment. Int. J. Dev. Neurosci., 24, 113-122.
27. Schönfeld, P. and Struy, H. (1999) Refsum disease diagnostic marker phytanic acid alters the physical state of membrane proteins of liver mitochondria. FEBS Lett., 457, 179-183.
28. Schönfeld, P., Kahlert, S. and Reiser, G. (2004) In brain mitochondria the branched-chain fatty acid phytanic acid impairs energy transduction and sensitizes for permeability transition. Biochem. J. 383, 121-128.
29. Butt, A.M. (2006) Neurotransmitter-mediated calcium signalling in oligodendrocyte physiology and pathology. Glia, 54, 666-675.
30. Arundine, M. and Tymianski, M. (2004) Molecular mechanisms of glutamate-dependent neurodegeneration in ischemia and traumatic brain injury. Cell. Mol. Life Sci., 61, 657-668.
31. 2+ is coupled with reactive oxygen species generation in cultured hippocampal neurons but not in astrocytes. J. Neurosci. Res., 79, 262-271.
32. 2+ handling in adult control and ob/ob cardiomyocytes: Impact of mitochondrial reactive oxygen species. Diabetes, 56, 1136-1142.
33. Aitken, R.J., Wingate, J.K., De Iuliis, G.N., Koppers, A.J. and McLaughlin, E.A. (2006) Cis-insaturated fatty acids stimulate reactive oxygen species generation and lipid peroxidation in human spermatozoa. J. Clin. Endocrinol. Metab., 91, 4154-4163.
34. Korshunov, S.S., Skulachev, V.P. and Starkov, A.A. (1997) High Protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett., 416, 15-18.
35. m-Dependent and -independent production of reactive oxygen species by rat brain mitochondria. J. Neurochem., 79, 266-277.
36. Bernardi, P., Penzo, D. and Wojtczak, L. (2002) Mitochondrial energy dissipation by fatty acids. Mechanisms and implications for cell death. Vitam. Horm., 65, 97-126.
37. 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.
38. Bezman, L., Moser, A B., Raymond, G.V., Rinaldo, P., Watkins, P.A., Smith, K.D., Kass, N.E. and Moser, H.W. (2001) Adrenoleukodystrophy: incidence, new mutation rate, and results of extended family screening. Ann. Neurol., 49, 512-517.
39. Paik, M.J., Kim, K.R., Yoon, H.R and Kim, H.J. (2001) Diagnostic patterns of very-long-chain fatty acids in plasma of patients with X-linked adrenoleukodystrophy. J. Chromatogr. B. Biomed. Sci. Appl. 760, 149-157.
40. Wanders, R.J., van Roermund, C.W., Lageweg, W., Jacobs, B.S., Schutgens, R.B., Nijenhuis, A.A. and Tager, J.M. (1992) X-linked adrenoleukodystrophy: Biochemical diagnosis and enzyme defect. J. Inherit. Metab. Dis., 15, 634-644.
41. Lima, T.M., Kanunfre, C.C., Pompeia, C., Verlengia, R. and Curi, R. (2002) Ranking the toxicity of fatty acids on Jurcat and Raji cells by flow cytometric analysis. Toxicol. In Vitro, 16 741-747.
42. Smith, K.D., Kemp, S., Braiterman, L.T., Lu, J.P., Wei, H.M., Geraghty, M., Stetten G., Bergin, J.S., Pevsner, J. and Watkins, P.A. (1999) X-linked adrenoleukodystrophy: Genes, mutations, and phenotypes. Neurochem. Res. 24, 521-535.
43. Knoll, A., Salles, J., Sargueil, F., Cassagne, C. and Garbay, B. (2000) Peroxisomal beta-oxidation enzyme gene expression in the developing mouse brain. Neurosci. Lett., 285, 201-204.
44. Di Biase, A., Avellino, C., Pieroni, F., Quaresima, T., Grisolia, A., Cappa, M. and Salvati, S. (1997) Effects of exogenous hexacosanoic acid on biochemical myelin composition in weaning and post-weaning rats. Neurochem. Res., 22, 327-331.
45. Theda, C., Moser, A.B., Powers, J.M. and Moser, H.W. (1992) Phospholipids in X-linked adrenoleukodystrophy white matter: Fatty acid abnormalities before the onset of demyelination. J. Neurol. Sci., 110, 195-204.
46. 2+ uptake in apoptosis. Cell Calcium, 40, 553-560.
47. Halestrap, A.P. (2006) Calcium, mitochondria and reperfusion injury: A pore way to die. Biochem. Soc. Trans., 34, 232-237.
48. Baumgart, E., Vanhorebeek, I., Grabenbauer, M., Borgers, M., Declercq, P.E., Fahimi, H.D. and Baes, M. (2001) Mitochondrial alterations caused by defective peroxisomal biogenesis in a mouse model for Zellweger syndrome (PEX5 knockout mouse). Am. J. Pathol., 159, 1477-1494.
49. Goldfischer, S., Moore, C.L., Johnson, A.B., Spiro, A.J., Valsamis, M.P., Wisniewski, H.K., Ritch, R.H., Norton, W.T., Rapin, I. and Gartner, L.M. (1973) Peroxisomal and mitochondrial defects in the cerebro-hepato-renal syndrome. Science, 182, 62-64.
50. McGuinnes, M.C., Lu, J.F., Zhang, H.P., Dong, G.X., Heinzer, A.K., Watkins, P.A., Powers, J. and Smith, K.D. (2003) Role ot ALDP (ABCD1) and mitochondria in X-linked adrenoleukodystrophy. Mol. Cell. Biol. 23, 744-753.
51. Oezen, I., Roossmanith, W., Forss-Petter, S., Kemp, S., Voigtlander, T., Moser-Thier, K., Wanders, R.J., Bittner, R.E. and Berger, J. (2005) Accumulation of very long-chain fatty acids doses not affect mitochondrial function in adrenoleukodystrophy protien deficiency. Hum. Mol. Genet. 14, 1127-1137.
52. 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.
53. 2+ signalling in hippocampal astrocytes. Neuropharmacology, 37, 169-178.
54. i-inducing protease-activated receptors (PAR-1 and PAR-2) in rat astrocytes and C6 glioma cells. Neuroscience, 86, 597-609.
55. 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.
56. Al-Omar, M.A. (2006) The X-linked adrenoleukodystrophy (X-ALD) and oxidative stress. J. Herb. Pharmacother., 6, 125-134.
57. Schönfeld, P., Kahlert, S. and Reiser, G. (2006) A study of the cytotoxicity of branched-chain phytanic acid with mitochondria and rat brain astrocytes. Exp. Gerontol., 41, 688-696.
58. Schönfeld, P. and Wojtczak, L. (2007) Fatty acids decrease mitochondrial generation of reactive oxygen species at the reverse eclectron transport but increase it at the forward transport. Biochim. Biophys. Acta, 1767, 1032-1040.
59. Cocco, T., Di Paola, M., Papa, S. and Lorusso, M. (1999) Arachidonic acid interaction with the mitochondrial electron transport chain promotes reactive oxygen species generation. Free Radic. Biol. Med. 27, 51-59.
60. Schönfeld, P. and Reiser, G. (2006) Rotenone-like action of the branched-chain phytanic acid induces oxidative stress in mitochondria J. Biol. Chem., 281, 7136-7142.
61. Hamprecht, B. and Loffler, F. (1985) Primary glial cultures as a model for studying hormone action. Methods Enzymol., 109, 341-345.
62. Wang, Y., Luo, W., Stricker, R. and Reiser, G. (2006) Protease-activated receptor-1 protects rat astrocytes from apoptotic cell death via JNK-mediated release of the chemokine GRO/CINC-1. J. Neurochem., 98, 1046-1060.
63. McCarthy, K.D. and de Vellis, J. (1980) Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J. Cell Biol., 85, 890-902.
64. 2+ loads. J. Neurosci. Res., 66, 1019-1027.
65. Budd, S.L., Castilho, R.F. and Nicholls, D.G. (1997) Mitochondrial membrane potential and hydroethidine-monitored superoxide generation in cultured cerebellar granule cells. FEBS Lett., 415, 21-24.
66. Singh, I. and Kishimoto, Y. (1983) Effect of cyclodextrins on the solubilization of lignoceric acid, ceramide, and cerebroside, and on the enzymatic reactions involving these compounds. J. Lipid Res., 24, 662-665.
67. Hall, A.M., Wiczer, B.M., Herrmann, T., Stremmel, W. and Bernlohr, D.A. (2005) Enzymatic properties of purified murine fatty acid transport protein 4 and analysis of acyl-CoA synthetase activities in tissues from FATP4 null mice. J. Biol. Chem., 280, 1198-11954.
68. Liu, Y., Fiskum, G. and Schubert, D. (2002) Generation of reactive oxygen species by the mitochondrial electron transport chain. J. Neurochem., 80, 780-787.