Brain lipotoxicity of phytanic acid and very long-chain fatty acids. Harmful cellular/mitochondrial activities in refsum disease and X-linked adrenoleukodystrophy

Aging and Disease

Volumn 7, Issue 2, 2016, Pages 136-149

  Schönfeld, Peter ^a   Reiser, Georg ^a  

^a OTTO VON GUERICKE UNIVERSITY   (Germany)

Author keywords

Adrenoleukodystrophy; Mitochondria; Neural cells; Peroxisomal disorder; Phytanic acid; Refsum disease; Very long chain fatty acids (VLCFA)

Indexed keywords

G PROTEIN COUPLED RECEPTOR 40; LIPOSOME; PHYTANIC ACID; VERY LONG CHAIN FATTY ACID;

APOPTOSIS; ASTROCYTE; CALCIUM SIGNALING; CELL DEATH; CELL VIABILITY; ELECTRON TRANSPORT; HUMAN; LIPID COMPOSITION; MITOCHONDRIAL BIOGENESIS; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL PERMEABILITY; MITOCHONDRIAL RESPIRATION; NEUROTOXICITY; NONHUMAN; OLIGODENDROGLIA; OXIDATIVE PHOSPHORYLATION; OXIDATIVE PHOSPHORYLATION UNCOUPLING; OXIDATIVE STRESS; PROTEIN DEGRADATION; REFSUM DISEASE; REVIEW;

EID: 85019076112     PISSN: None     EISSN: 21525250     Source Type: Journal    
DOI: 10.14336/AD.2015.0823     Document Type: Review

References (76)

1. Cermenati G, Mitro N, Audano M, Melcangi RC, Crestani M, De Fabiani E, et al. (2015). Lipids in the nervous system: from biochemistry and molecular biology to patho-physiology. Biochim Biophys Acta, 1851: 51-60
2. Müller CP, Reichel M, Muhle C, Rhein C, Gulbins E, Kornhuber J (2015). Brain membrane lipids in major depression and anxiety disorders. Biochim Biophys Acta, 1851: 1052-1065
3. Chaturvedi RK, Beal MF (2013). Mitochondria targeted therapeutic approaches in Parkinson's and Huntington's diseases. Mol Cell Neurosci, 55: 101-114
4. Aleshin S, Reiser G (2013). Role of the peroxisome proliferator-activated receptors (PPAR)-α, β/δ and γ triad in regulation of reactive oxygen species signaling in brain. Biol Chem, 394: 1553-1570
5. Aleshin S, Strokin M, Sergeeva M, Reiser G (2013). Peroxisome proliferator-activated receptor (PPAR)β/α, a possible nexus of PPARα-and PPARγ-dependent molecular pathways in neurodegenerative diseases: Review and novel hypotheses. Neurochem Int, 63: 322-330
6. Aleshin S, Grabeklis S, Hanck T, Sergeeva M, Reiser G (2009). Peroxisome proliferator-activated receptor (PPAR)-γ positively controls and PPARα negatively controls cyclooxygenase-2 expression in rat brain astrocytes through a convergence on PPARβ/δ via mutual control of PPAR expression levels. Mol Pharmacol, 76: 414-424
7. Ellinghaus P, Wolfrum C, Assmann G, Spener F, Seedorf U (1999). Phytanic acid activates the peroxisome proliferator-activated receptor alpha (PPARalpha) in sterol carrier protein 2-/sterol carrier protein x-deficient mice. J Biol Chem, 274: 2766-2772
8. Zomer AW, van Der Burg B, Jansen GA, Wanders RJ, Poll-The BT, van Der Saag PT (2000). Pristanic acid and phytanic acid: naturally occurring ligands for the nuclear receptor peroxisome proliferator-activated receptor α. J Lipid Res, 41: 1801-1807
9. Gloerich J, van Vlies N, Jansen GA, Denis S, Ruiter JP, van Werkhoven MA, et al. (2005). A phytol-enriched diet induces changes in fatty acid metabolism in mice both via PPARα-dependent and-independent pathways. J Lipid Res, 46: 716-726
10. Nakamura MT, Yudell BE, Loor JJ (2014). Regulation of energy metabolism by long-chain fatty acids. Prog Lipid Res, 53: 124-144
11. Kemp S, Berger J, Aubourg P (2012). X-linked adrenoleukodystrophy: clinical, metabolic, genetic and pathophysiological aspects. Biochim Biophys Acta, 1822: 1465-1474
12. Klenk E, Kahike W (1963). [On The Presence Of 3,7,11,15-Tetramethylhexadecanoic Acid (Phytanic Acid) In The Cholesterol Esters And Other Lipoid Fractions Of The Organs In A Case Of A Disease Of Unknown Origin (Possibly Heredopathia Atactica Polyneuritiformis, Refsum's Syndrome)]. Hoppe Seylers Z Physiol Chem, 333: 133-139
13. Kou J, Kovacs GG, Hoftberger R, Kulik W, Brodde A, Forss-Petter S, et al. (2011). Peroxisomal alterations in Alzheimer's disease. Acta neuropathol, 122: 271-283
14. Wojtczak L, Schönfeld P (1993). Effect of fatty acids on energy coupling processes in mitochondria. Biochim Biophys Acta, 1183: 41-57
15. Schönfeld P, Wojtczak L (2008). Fatty acids as modulators of the cellular production of reactive oxygen species. Free Radic Biol Med, 45: 231-241
16. Azarashvili T, Stricker R, Reiser G (2010). The mitochondria permeability transition pore complex in the brain with interacting proteins-promising targets for protection in neurodegenerative diseases. Biol Chem, 391: 619-629
17. Bernardi P (2013). The mitochondrial permeability transition pore: a mystery solved? Frontiers physiol, 4: 95
18. Schönfeld P, Reiser G (2013). Why does brain metabolism not favor burning of fatty acids to provide energy? Reflections on disadvantages of the use of free fatty acids as fuel for brain. J Cereb Blood Flow Metab, 33: 1493-1499
19. Speijer D (2011). Oxygen radicals shaping evolution: why fatty acid catabolism leads to peroxisomes while neurons do without it: FADH2/NADH flux ratios determining mitochondrial radical formation were crucial for the eukaryotic invention of peroxisomes and catabolic tissue differentiation. BioEssays, 33: 88-94
20. Yang SY, He XY, Schulz H (1987). Fatty acid oxidation in rat brain is limited by the low activity of 3-ketoacyl-coenzyme A thiolase. J Biol Chem, 262: 13027-13032
21. Price N, van der Leij F, Jackson V, Corstorphine C, Thomson R, Sorensen A, et al. (2002). A novel brain-expressed protein related to carnitine palmitoyltransferase I. Genomics, 80: 433-442
22. Wolfgang MJ, Kurama T, Dai Y, Suwa A, Asaumi M, Matsumoto S, et al. (2006). The brain-specific carnitine palmitoyltransferase-1c regulates energy homeostasis. Proc Natl Acad Sci U S A, 103: 7282-7287
23. Wanders RJ, Waterham HR (2006). Biochemistry of mammalian peroxisomes revisited. Annu Rev Biochem, 75: 295-332
24. Van Veldhoven PP (2010). Biochemistry and genetics of inherited disorders of peroxisomal fatty acid metabolism. J Lipid Res, 51: 2863-2895
25. Islinger M, Grille S, Fahimi HD, Schrader M (2012). The peroxisome: an update on mysteries. Histochem Cell Biol, 137: 547-574
26. Trompier D, Vejux A, Zarrouk A, Gondcaille C, Geillon F, Nury T, et al. (2014). Brain peroxisomes. Biochimie, 98: 102-110
27. Wanders RJ, Komen J, Ferdinandusse S (2011). Phytanic acid metabolism in health and disease. Biochim Biophys Acta, 1811: 498-507
28. Berger J, Forss-Petter S, Eichler FS (2014). Pathophysiology of X-linked adrenoleukodystrophy. Biochimie, 98: 135-142
29. Watkins PA, Naidu S, Moser HW (1987). Adrenoleukodystrophy: biochemical procedures in diagnosis, prevention and treatment. J Inherit Metab Dis, 10 Suppl 1: 46-53
30. Grings M, Tonin AM, Knebel LA, Zanatta A, Moura AP, Filho CS, et al. (2012). Phytanic acid disturbs mitochondrial homeostasis in heart of young rats: a possible pathomechanism of cardiomyopathy in Refsum disease. Mol Cell Biochem, 366: 335-343
31. Galea E, Launay N, Portero-Otin M, Ruiz M, Pamplona R, Aubourg P, et al. (2012). Oxidative stress underlying axonal degeneration in adrenoleukodystrophy: a paradigm for multifactorial neurodegenerative diseases? Biochim Biophys Acta, 1822: 1475-1488
32. Fourcade S, Lopez-Erauskin J, Ruiz M, Ferrer I, Pujol A (2014). Mitochondrial dysfunction and oxidative damage cooperatively fuel axonal degeneration in X-linked adrenoleukodystrophy. Biochimie, 98: 143-149
33. Hellgren LI (2010). Phytanic acid-an overlooked bioactive fatty acid in dairy fat? Ann N Y Acad Sci, 1190: 42-49
34. Jansen GA, Waterham HR, Wanders RJ (2004). Molecular basis of Refsum disease: sequence variations in phytanoyl-CoA hydroxylase (PHYH) and the PTS2 receptor (PEX7). Hum Mutat, 23: 209-218
35. Atshaves BP, McIntosh AM, Lyuksyutova OI, Zipfel W, Webb WW, Schroeder F (2004). Liver fatty acid-binding protein gene ablation inhibits branched-chain fatty acid metabolism in cultured primary hepatocytes. J Biol Chem, 279: 30954-30965
36. Atshaves BP, Storey SM, Petrescu A, Greenberg CC, Lyuksyutova OI, Smith R, 3rd, et al. (2002). Expression of fatty acid binding proteins inhibits lipid accumulation and alters toxicity in L cell fibroblasts. Am J Physiol Cell Physiol, 283: C688-703
37. Friedman KJ, Glick D (1982). Role of lipids in the Neurospora crassa membrane: IV. Biochemical and electrophysiological changes caused by growth on phytanic acid. J Membr Biol, 64: 1-9
38. Gutknecht J (1988). Proton conductance caused by long-chain fatty acids in phospholipid bilayer membranes. J Membr Biol, 106: 83-93
39. Schönfeld P, Struy H (1999). Refsum disease diagnostic marker phytanic acid alters the physical state of membrane proteins of liver mitochondria. FEBS Lett, 457: 179-183
40. Kihara A (2012). Very long-chain fatty acids: elongation, physiology and related disorders. J biochem, 152: 387-395
41. Kemp S, Wei HM, Lu JF, Braiterman LT, McGuinness MC, Moser AB, et al. (1998). Gene redundancy and pharmacological gene therapy: implications for X-linked adrenoleukodystrophy. Nat Med, 4: 1261-1268
42. Camões F, Bonekamp NA, Delille HK, Schrader M (2009). Organelle dynamics and dysfunction: A closer link between peroxisomes and mitochondria. J Inherit Metab Dis, 32: 163-180
43. Ho JK, Moser H, Kishimoto Y, Hamilton JA (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
44. Millar AA, Wrischer M, Kunst L (1998). Accumulation of very-long-chain fatty acids in membrane glycerolipids is associated with dramatic alterations in plant morphology. The Plant cell, 10: 1889-1902
45. Schönfeld P, Kahlert S, 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
46. Schönfeld P, Bohnensack R (1997). Fatty acid-promoted mitochondrial permeability transition by membrane depolarization and binding to the ADP/ATP carrier. FEBS Lett, 420: 167-170
47. Schönfeld P, Wieckowski MR, Wojtczak L (1997). Thyroid hormone-induced expression of the ADP/ATP carrier and its effect on fatty acid-induced uncoupling of oxidative phosphorylation. FEBS Lett, 416: 19-22
48. Brustovetsky N, Klingenberg M (1994). The reconstituted ADP/ATP carrier can mediate H+ transport by free fatty acids, which is further stimulated by mersalyl. J Biol Chem, 269: 27329-27336
49. Skulachev VP (1991). Fatty acid circuit as a physiological mechanism of uncoupling of oxidative phosphorylation. FEBS Lett, 294: 158-162
50. Komen JC, Distelmaier F, Koopman WJ, Wanders RJ, Smeitink J, Willems PH (2007). Phytanic acid impairs mitochondrial respiration through protonophoric action. Cell Mol Life Sci, 64: 3271-3281
51. Schönfeld P, Kahlert S, Reiser G (2006). A study of the cytotoxicity of branched-chain phytanic acid with mitochondria and rat brain astrocytes. Exp Gerontol, 41: 688-696
52. Zoratti M, Szabo I (1995). The mitochondrial permeability transition. Biochim Biophys Acta, 1241: 139-176
53. Brustovetsky N, Klingenberg M (1996). Mitochondrial ADP/ATP carrier can be reversibly converted into a large channel by Ca2+. Biochemistry, 35: 8483-8488
54. Schönfeld P, Reiser G (2006). Rotenone-like action of the branched-chain phytanic acid induces oxidative stress in mitochondria. J Biol Chem, 281: 7136-7142
55. Schönfeld P, Wojtczak L (2007). Fatty acids decrease mitochondrial generation of reactive oxygen species at the reverse electron transport but increase it at the forward transport. Biochim Biophys Acta, 1767: 1032-1040
56. Reiser G, Schönfeld P, 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
57. Kahlert S, Schönfeld P, Reiser G (2005). The Refsum disease marker phytanic acid, a branched chain fatty acid, affects Ca2+ homeostasis and mitochondria, and reduces cell viability in rat hippocampal astrocytes. Neurobiol Dis, 18: 110-118
58. Rönicke S, Kruska N, Kahlert S, Reiser G (2009). The influence of the branched-chain fatty acids pristanic acid and Refsum disease-associated phytanic acid on mitochondrial functions and calcium regulation of hippocampal neurons, astrocytes, and oligodendrocytes. Neurobiol Dis, 36: 401-410
59. Briscoe CP, Tadayyon M, Andrews JL, Benson WG, Chambers JK, Eilert MM, et al. (2003). The orphan G protein-coupled receptor GPR40 is activated by medium and long chain fatty acids. J Biol Chem, 278: 11303-11311
60. Itoh Y, Kawamata Y, Harada M, Kobayashi M, Fujii R, Fukusumi S, et al. (2003). Free fatty acids regulate insulin secretion from pancreatic β cells through GPR40. Nature, 422: 173-176
61. Fujiwara K, Maekawa F, Yada T (2005). Oleic acid interacts with GPR40 to induce Ca2+ signaling in rat islet β-cells: mediation by PLC and L-type Ca2+ channel and link to insulin release. Am J Physiol Endocrinol Metab, 289: E670-677
62. Suh HN, Huong HT, Song CH, Lee JH, Han HJ (2008). Linoleic acid stimulates gluconeogenesis via Ca2+/PLC, cPLA2, and PPAR pathways through GPR40 in primary cultured chicken hepatocytes. Am J Physiol Cell Physiol, 295: C1518-1527
63. Kruska N, Reiser G (2011). Phytanic acid and pristanic acid, branched-chain fatty acids associated with Refsum disease and other inherited peroxisomal disorders, mediate intracellular Ca2+ signaling through activation of free fatty acid receptor GPR40. Neurobiol Dis, 43: 465-472
64. Mosser J, Douar AM, Sarde CO, Kioschis P, Feil R, Moser H, et al. (1993). Putative X-linked adrenoleukodystrophy gene shares unexpected homology with ABC transporters. Nature, 361: 726-730
65. Hein S, Schönfeld P, Kahlert S, 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
66. Saab AS, Tzvetanova ID, Nave KA (2013). The role of myelin and oligodendrocytes in axonal energy metabolism. Curr Opin Neurobiol, 23: 1065-1072
67. Kruska N, Schönfeld P, Pujol A, Reiser G (2015). Astrocytes and mitochondria from adrenoleukodystrophy protein (ABCD1)-deficient mice reveal that the adrenoleukodystrophy-associated very long-chain fatty acids target several cellular energy-dependent functions. Biochim Biophys Acta, 1852: 925-936
68. McGuinness MC, Lu JF, Zhang HP, Dong GX, Heinzer AK, Watkins PA, et al. (2003). Role of ALDP (ABCD1) and mitochondria in X-linked adrenoleukodystrophy. Mol Cell Biol, 23: 744-753
69. Powers JM, DeCiero DP, Cox C, Richfield EK, Ito M, Moser AB, et al. (2001). The dorsal root ganglia in adrenomyeloneuropathy: neuronal atrophy and abnormal mitochondria. J Neuropathol Exp Neurol, 60: 493-501
70. Oezen I, Rossmanith W, Forss-Petter S, Kemp S, Voigtlander T, Moser-Thier K, et al. (2005). Accumulation of very long-chain fatty acids does not affect mitochondrial function in adrenoleukodystrophy protein deficiency. Hum Mol Genet, 14: 1127-1137
71. Lopez-Erauskin J, Galino J, Ruiz M, Cuezva JM, Fabregat I, Cacabelos D, et al. (2013). Impaired mitochondrial oxidative phosphorylation in the peroxisomal disease X-linked adrenoleukodystrophy. Hum Mol Genet, 22: 3296-3305
72. Morató L, Galino J, Ruiz M, Calingasan NY, Starkov AA, Dumont M, et al. (2013). Pioglitazone halts axonal degeneration in a mouse model of X-linked adrenoleukodystrophy. Brain, 136: 2432-2443
73. Busanello EN, Zanatta A, Tonin AM, Viegas CM, Vargas CR, Leipnitz G, et al. (2013). Marked inhibition of Na+, K+-ATPase activity and the respiratory chain by phytanic acid in cerebellum from young rats: possible underlying mechanisms of cerebellar ataxia in Refsum disease. J Bioenerg Biomembr, 45: 137-144
74. Nagai K (2015). Phytanic acid induces Neuro2a cell death via histone deacetylase activation and mitochondrial dysfunction. Neurotoxicol teratol, 48: 33-39
75. Baarine M, Beeson C, Singh A, Singh I (2015). ABCD1 deletion-induced mitochondrial dysfunction is corrected by SAHA: implication for adrenoleukodystrophy. J Neurochem, 133: 380-396
76. Zündorf G, Reiser G (2011). Calcium dysregulation and homeostasis of neural calcium in the molecular mechanisms of neurodegenerative diseases provide multiple targets for neuroprotection. Antioxid Redox Signal, 14: 1275-1288