The heme precursor delta-aminolevulinate blocks peripheral myelin formation

Journal of Neurochemistry

Volumn 106, Issue 5, 2008, Pages 2068-2079

  Felitsyn, Natalia ^a   McLeod, Colin ^a   Shroads, Albert L ^a   Stacpoole, Peter W ^a   Notterpek, Lucia ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

Delta aminolevulinate; Demyelination; Dichloroacetate; Oxidative stress; Peripheral neuropathy; Schwann cells

Indexed keywords

AMINOLEVULINIC ACID; DICHLOROACETIC ACID; PERIPHERAL MYELIN PROTEIN 22;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ISOLATION; DEMYELINATION; GLIA CELL; NONHUMAN; OXIDATIVE STRESS; PERIPHERAL NEUROPATHY; PORPHYRIA; PRIORITY JOURNAL; PROTEIN CARBONYLATION; PROTEIN EXPRESSION; RAT; SCHWANN CELL; SENSORY NERVE CELL; TYROSINEMIA;

AMINOLEVULINIC ACID; ANIMALS; AXONS; CELLS, CULTURED; COCULTURE TECHNIQUES; DICHLOROACETATE; DOSE-RESPONSE RELATIONSHIP, DRUG; FREE RADICALS; GANGLIA, SPINAL; HEME; MICE; MYELIN PROTEINS; MYELIN SHEATH; NERVE FIBERS, MYELINATED; NEURONS, AFFERENT; NEUROTOXINS; OXIDATIVE STRESS; PERIPHERAL NERVES; PERIPHERAL NERVOUS SYSTEM DISEASES; RATS; SCHWANN CELLS;

ANIMALIA;

EID: 49549108230     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2008.05552.x     Document Type: Article

References (71)

1. Adhikari A., Penatti C. A., Resende R. R., Ulrich H., Britto L. R. Bechara E. J. (2006) 5-Aminolevulinate and 4, 5-dioxovalerate ions decrease GABA(A) receptor density in neuronal cells, synaptosomes and rat brain. Brain Res. 1093, 95 104.
2. Ammini C. V., Fernandez-Canon J., Shroads A. L., Cornett R., Cheung J., James M. O., Henderson G. N., Grompe M. Stacpoole P. W. (2003) Pharmacologic or genetic ablation of maleylacetoacetate isomerase increases levels of toxic tyrosine catabolites in rodents. Biochem. Pharmacol. 66, 2029 2038.
3. Archelos J. J., Roggenbuck K., Schneider-Schaulies J., Linington C., Toyka K. V. Hartung H. P. (1993) Production and characterization of monoclonal antibodies to the extracellular domain of P0. J. Neurosci. Res. 35, 46 53.
4. Audesirk G. (1985) Effects of lead exposure on the physiology of neurons. Prog. Neurobiol. 24, 199 231.
5. Bartzokis G. (2004) Age-related myelin breakdown: a developmental model of cognitive decline and Alzheimer's disease. Neurobiol. Aging 25, 5 18 author reply 49-62.
6. Beal M. F. (2004) Mitochondrial dysfunction and oxidative damage in Alzheimer's and Parkinson's diseases and coenzyme Q10 as a potential treatment. J. Bioenerg. Biomembr. 36, 381 386.
7. Bechara E. J., Dutra F., Cardoso V. E., Sartori A., Olympio K. P., Penatti C. A., Adhikari A. Assuncao N. A. (2007) The dual face of endogenous alpha-aminoketones: pro-oxidizing metabolic weapons. Comp Biochem Physiol C Toxicol Pharmacol 146, 88 110.
8. Becker D. M. Kramer S. (1977) The neurological manifestations of porphyria: a review. Medicine (Baltimore) 56, 411 423.
9. Bondy S. C. LeBell C. P. (1991) Oxygen radical generation as an index of neurotoxic damage. Biomed. Environ. Sci. 4, 217 223.
10. Capel F., Buffiere C., Patureau Mirand P. Mosoni L. (2004) Differential variation of mitochondrial H2O2 release during aging in oxidative and glycolytic muscles in rats. Mech. Ageing Dev. 125, 367 373.
11. Carneiro R. C. Reiter R. J. (1998) Melatonin protects against lipid peroxidation induced by delta-aminolevulinic acid in rat cerebellum, cortex and hippocampus. Neuroscience 82, 293 299.
12. Coria F., Berciano M. T., Berciano J. Lafarga M. (1984) Axon membrane remodeling in the lead-induced demyelinating neuropathy of the rat. Brain Res. 291, 369 372.
13. Demasi M., Penatti C. A., DeLucia R. Bechara E. J. (1996) The prooxidant effect of 5-aminolevulinic acid in the brain tissue of rats: implications in neuropsychiatric manifestations in porphyrias. Free Radic. Biol. Med. 20, 291 299.
14. Dowling V., Hoarau P. C., Romeo M., O'Halloran J., van Pelt F., O'Brien N. Sheehan D. (2006) Protein carbonylation and heat shock response in Ruditapes decussatus following p,p'-dichlorodiphenyldichloroethylene (DDE) exposure: a proteomic approach reveals that DDE causes oxidative stress. Aquat Toxicol 77, 11 18.
15. Dreyfus H., Guerold B., Freysz L. Hicks D. (1997) Successive isolation and separation of the major lipid fractions including gangliosides from single biological samples. Anal Biochem. 249, 67 78.
16. Einheber S., Milner T. A., Giancotti F. Salzer J. L. (1993) Axonal regulation of Schwann cell integrin expression suggests a role for alpha 6 beta 4 in myelination. J. Cell Biol. 123, 1223 1236.
17. Felitsyn N., Stacpoole P. W. Notterpek L. (2007) Dichloroacetate causes reversible demyelination in vitro: potential mechanism for its neuropathic effect. J. Neurochem. 100, 429 436.
18. Floderus Y., Sardh E., Moller C., Andersson C., Rejkjaer L., Andersson D. E. Harper P. (2006) Variations in porphobilinogen and 5-aminolevulinic acid concentrations in plasma and urine from asymptomatic carriers of the acute intermittent porphyria gene with increased porphyrin precursor excretion. Clin. Chem. 52, 701 707.
19. Flugel K. A. Druschky K. F. (1977) Electromyogram and nerve conduction in patients with acute intermittent porphyria. J. Neurol. 214, 267 279.
20. Gibson J. B. Goldberg A. (1956) The neuropathology of acute porphyria. J. Pathol. Bacteriol. 71, 495 509.
21. Gorchein A. Webber R. (1987) delta-Aminolaevulinic acid in plasma, cerebrospinal fluid, saliva and erythrocytes: studies in normal, uraemic and porphyric subjects. Clin. Sci. (Lond) 72, 103 112.
22. Hermes-Lima M., Castilho R. F., Valle V. G., Bechara E. J. Vercesi A. E. (1992) Calcium-dependent mitochondrial oxidative damage promoted by 5-aminolevulinic acid. Biochim. Biophys. Acta 1180, 201 206.
23. Hollander J., Bejma J., Ookawara T., Ohno H. Ji L. L. (2000) Superoxide dismutase gene expression in skeletal muscle: fiber-specific effect of age. Mech. Ageing Dev. 116, 33 45.
24. Iida H., Schmeichel A. M., Wang Y., Schmelzer J. D. Low P. A. (2004) Schwann cell is a target in ischemia-reperfusion injury to peripheral nerve. Muscle Nerve 30, 761 766.
25. Juknat A. A., Kotler M. L., Quaglino A., Carrillo N. M. Hevor T. (2003) Necrotic cell death induced by delta-aminolevulinic acid in mouse astrocytes. Protective role of melatonin and other antioxidants. J. Pineal Res. 35, 1 11.
26. Juurlink B. H., Thorburne S. K. Hertz L. (1998) Peroxide-scavenging deficit underlies oligodendrocyte susceptibility to oxidative stress. Glia 22, 371 378.
27. Kaufmann P., Engelstad K., Wei Y. et al. (2006) Dichloroacetate causes toxic neuropathy in MELAS: a randomized, controlled clinical trial. Neurology 66, 324 330.
28. LeBel C. P. Bondy S. C. (1991) Oxygen radicals: common mediators of neurotoxicity. Neurotoxicol. Teratol. 13, 341 346.
29. Lindberg R. L., Martini R., Baumgartner M., Erne B., Borg J., Zielasek J., Ricker K., Steck A., Toyka K. V. Meyer U. A. (1999) Motor neuropathy in porphobilinogen deaminase-deficient mice imitates the peripheral neuropathy of human acute porphyria. J. Clin. Invest. 103, 1127 1134.
30. Mitchell G., Larochelle J., Lambert M. et al. (1990) Neurologic crises in hereditary tyrosinemia. N. Engl. J. Med. 322, 432 437.
31. Mitsumoto A., Takeuchi A., Okawa K. Nakagawa Y. (2002) A subset of newly synthesized polypeptides in mitochondria from human endothelial cells exposed to hydroperoxide stress. Free Radic. Biol. Med. 32, 22 37.
32. Monteiro H. P., Abdalla D. S., Faljoni-Alario A. Bechara E. J. (1986) Generation of active oxygen species during coupled autoxidation of oxyhemoglobin and delta-aminolevulinic acid. Biochim. Biophys. Acta 881, 100 106.
33. Morell P. (1984) Myelin. Plenum Press, New York.
34. Morell P. Toews A. D. (1996) Schwann cells as targets for neurotoxicants. Neurotoxicology 17, 685 695.
35. Morrison M. L., Williamson K., Arthur K., Price G. J., Hamilton P. W. Maxwell P. (2005) Phenotypic changes in mitochondrial membrane potential (Delta psi(m)) during valinomycin-induced depolarisation and apoptosis. Cell Oncol. 27, 231 236.
36. Moser V. C., Phillips P. M., McDaniel K. L. MacPhail R. C. (1999) Behavioral evaluation of the neurotoxicity produced by dichloroacetic acid in rats. Neurotoxicol. Teratol. 21, 719 731.
37. Mronga T., Stahnke T., Goldbaum O. Richter-Landsberg C. (2004) Mitochondrial pathway is involved in hydrogen-peroxide-induced apoptotic cell death of oligodendrocytes. Glia 46, 446 455.
38. Muzyka V. I. Bogovskii L. A. (1985) [Interrelation of delta-aminolevulinic acid and brain myelin proteins as affected by benzene and lead]. Biull. Eksp. Biol. Med. 100, 447 449.
39. Muzyka V. I. Moks M. A. (1984) [Binding of delta-aminolevulinic acid by myelin proteins]. Biokhimiia 49, 1647 1649.
40. Nave K. A. Salzer J. L. (2006) Axonal regulation of myelination by neuregulin 1. Curr. Opin. Neurobiol. 16, 492 500.
41. Noriega G. O., Tomaro M. L. del Batlle A. M. (2003) Bilirubin is highly effective in preventing in vivo delta-aminolevulinic acid-induced oxidative cell damage. Biochim. Biophys. Acta 1638, 173 178.
42. Notterpek L., Snipes G. J. Shooter E. M. (1999) Temporal expression pattern of peripheral myelin protein 22 during in vivo and in vitro myelination. Glia 25, 358 369.
43. Ojano-Dirain C., Pumford N. R., Iqbal M., Wing T., Cooper M. Bottje W. G. (2005) Biochemical evaluation of mitochondrial respiratory chain in duodenum of low and high feed efficient broilers. Poult. Sci. 84, 1926 1934.
44. Onuki J., Chen Y., Teixeira P. C., Schumacher R. I., Medeiros M. H., Van Houten B. Di Mascio P. (2004) Mitochondrial and nuclear DNA damage induced by 5-aminolevulinic acid. Arch. Biochem. Biophys. 432, 178 187.
45. Pantoni L., Garcia J. H. Gutierrez J. A. (1996) Cerebral white matter is highly vulnerable to ischemia. Stroke 27, 1641 1646 discussion 1647.
46. Pipinos I. I., Swanson S. A., Zhu Z., Nella A. A., Weiss D. J., Gutti T. L., McComb R. D., Baxter B. T., Lynch T. G. Casale G. P. (2008) Chronically ischemic mouse skeletal muscle exhibits myopathy in association with mitochondrial dysfunction and oxidative damage. Am. J. Physiol. Regul. Integr. Comp. Physiol. 295, R290 296.
47. Powell H. C., Myers R. R. Lampert P. W. (1982) Changes in Schwann cells and vessels in lead neuropathy. Am. J. Pathol. 109, 193 205.
48. Princ F. G., Juknat A. A., Maxit A. G., Cardalda C. Batlle A. (1997) Melatonin's antioxidant protection against delta-aminolevulinic acid-induced oxidative damage in rat cerebellum. J. Pineal Res. 23, 40 46.
49. Princ F. G., Juknat A. A., Amitrano A. A. Batlle A. (1998) Effect of reactive oxygen species promoted by delta-aminolevulinic acid on porphyrin biosynthesis and glucose uptake in rat cerebellum. Gen. Pharmacol. 31, 143 148.
50. Reers M., Smith T. W. Chen L. B. (1991) J-aggregate formation of a carbocyanine as a quantitative fluorescent indicator of membrane potential. Biochemistry 30, 4480 4486.
51. Romero F. J., Segura-Aguilar J., Monsalve E., Hermenegildo C., Nies E., Puertas F. J. Roma J. (1990) Antioxidant and glutathione-related enzymatic activities in rat sciatic nerve. Neurotoxicol. Teratol. 12, 603 605.
52. Romero F. J., Monsalve E., Hermenegildo C., Puertas F. J., Higueras V., Nies E., Segura-Aguilar J. Roma J. (1991) Oxygen toxicity in the nervous tissue: comparison of the antioxidant defense of rat brain and sciatic nerve. Neurochem. Res. 16, 157 161.
53. Russo P. A., Mitchell G. A. Tanguay R. M. (2001) Tyrosinemia: a review. Pediatr. Dev. Pathol. 4, 212 221.
54. Sakai T. (2000) Biomarkers of lead exposure. Ind. Health 38, 127 142.
55. Sakai T. Morita Y. (1996) delta-Aminolevulinic acid in plasma or whole blood as a sensitive indicator of lead effects, and its relation to the other heme-related parameters. Int. Arch. Occup. Environ. Health 68, 126 132.
56. Sakai T., Morita Y., Araki T., Kano M. Yoshida T. (2000) Relationship between delta-aminolevulinic acid dehydratase genotypes and heme precursors in lead workers. Am. J. Ind. Med. 38, 355 360.
57. Shroads A. L., Guo X., Dixit V., Liu H. P., James M. O. Stacpoole P. W. (2008) Age-dependent kinetics and metabolism of dichloroacetate: possible relevance to toxicity. J. Pharmacol. Exp. Ther. 324, 1163 1171.
58. Silbergeld E. K. (1992) Mechanisms of lead neurotoxicity, or looking beyond the lamppost. FASEB J. 6, 3201 3206.
59. Smith K. J., Kapoor R. Felts P. A. (1999) Demyelination: the role of reactive oxygen and nitrogen species. Brain Pathol. 9, 69 92.
60. Spruijt L., Naviaux R. K., McGowan K. A., Nyhan W. L., Sheean G., Haas R. H. Barshop B. A. (2001) Nerve conduction changes in patients with mitochondrial diseases treated with dichloroacetate. Muscle Nerve 24, 916 924.
61. Stacpoole P. W. (1989) The pharmacology of dichloroacetate. Metabolism 38, 1124 1144.
62. Stacpoole P. W., Henderson G. N., Yan Z. M., Cornett R. James M. O. (1998) Pharmacokinetics, metabolism, and toxicology of dichloroacetate. Drug Metab. Rev. 30, 499 539.
63. Stacpoole P. W., Kerr D. S., Barnes C. et al. (2006) Controlled clinical trial of dichloroacetate for treatment of congenital lactic acidosis in children. Pediatrics 117, 1519 1531.
64. Stahnke T., Stadelmann C., Netzler A., Bruck W. Richter-Landsberg C. (2007) Differential upregulation of heme oxygenase-1 (HSP32) in glial cells after oxidative stress and in demyelinating disorders. J. Mol. Neurosci. 32, 25 37.
65. Trajkovic K., Dhaunchak A. S., Goncalves J. T., Wenzel D., Schneider A., Bunt G., Nave K. A. Simons M. (2006) Neuron to glia signaling triggers myelin membrane exocytosis from endosomal storage sites. J. Cell Biol. 172, 937 948.
66. deVellis J. Carpenter E. (2006) Development, in Basic Neurochemistry (Siegel G. J., Albeerts R. W., Brady S. T. Price D. L., eds), pp. 4347 4458. Elseviere Academic Press, Burlington, Massachusetts.
67. 2+ and and membrane protein thiols. Biochim. Biophys. Acta. 1188, 86 92.
68. Wada R. Yagihashi S. (2005) Role of advanced glycation end products and their receptors in development of diabetic neuropathy. Ann. NY Acad. Sci. 1043, 598 604.
69. Weinmaster G. Lemke G. (1990) Cell-specific cyclic AMP-mediated induction of the PDGF receptor. EMBO J. 9, 915 920.
70. Whetsell W. O. Jr, Sassa S. Kappas A. (1984) Porphyrin-heme biosynthesis in organotypic cultures of mouse dorsal root ganglia. Effects of heme and lead on porphyrin synthesis and peripheral myelin. J. Clin. Invest. 74, 600 607.
71. Zimmer S., Taub H. Marks G. S. (1980) A comparison of the porphyrin-inducing activity of barbiturates and benzodiazepines in chick embryo liver cells. Can. J. Physiol. Pharmacol. 58, 991 995.