γ-diketone axonopathy: Analyses of cytoskeletal motors and highways in CNS myelinated axons

Toxicological Sciences

Volumn 117, Issue 1, 2010, Pages 180-189

  Zhang, Lihai ^a   Gavin, Terrence ^b   DeCaprio, Anthony P ^c   LoPachin, Richard M ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b IONA COLLEGE   (United States)

^c FLORIDA INTERNATIONAL UNIVERSITY   (United States)

Author keywords

diketone neuropathy; Axon atrophy; Axonal cytoskeleton; Microtubule associated proteins; Neurofilament; Protein adduct

Indexed keywords

1,4 DIKETONE; ACETONYLACETONE; ALPHA TUBULIN; BETA TUBULIN; DYNEIN ADENOSINE TRIPHOSPHATASE; MEMBRANE PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; MICROTUBULE ASSOCIATED PROTEIN 1A; MICROTUBULE ASSOCIATED PROTEIN 2; MICROTUBULE ASSOCIATED PROTEIN 5; NEUROFILAMENT PROTEIN; PROTEIN KIF1A; PROTEIN KIF3; PROTEIN KIF5; TAU PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CYTOSKELETON; HEAVY CHAIN; IMMUNOBLOTTING; INTOXICATION; LIGHT CHAIN; MALE; MICROTUBULE; MOLECULAR WEIGHT; MOTOR NERVE CONDUCTION; MOTOR NEUROPATHY; MYELINATION; NERVE FIBER DEGENERATION; NONHUMAN; PROTEIN PROTEIN INTERACTION; RAT; SEDIMENTATION; SPINAL CORD;

ADENOSINE TRIPHOSPHATE; ANIMALS; AXONS; BODY WEIGHT; CENTRAL NERVOUS SYSTEM; CYTOSKELETON; KETONES; MALE; MOLECULAR MOTOR PROTEINS; MYELIN SHEATH; RATS; RATS, SPRAGUE-DAWLEY;

RATTUS;

EID: 77955860580     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfq176     Document Type: Article

References (61)

1. Ackerley, S., Thornhill, P., Grierson, A. J., Bronlees, J., Anerton, B. H., Leigh, P. N., Shaw, C. E., and Miller, C. C. J. (2003). Neurofilament heavy chain side arm phosphorylation regulates axonal transport of neurofilaments. J. Cell Biol. 161, 489-495.
2. Bocquet, A., Berges, R., Frank, R., Robert, P., Peterson, A. C., and Eyer, J. (2009). Neurofilaments bind tubulin and modulate its polymerization. J. Neurosci. 29, 11043-11054.
3. Boekelheide, K. (1987). 2,5-Hexanedione alters microtubule assembly. II. Enhanced polymerization of crosslinked tubulin. Toxicol. Appl. Pharmacol. 88, 383-396.
4. Carden, M. J., and Eagles, P. A. M. (1983). Neurofilaments from ox spinal nerves. Isolation, disassembly, reassembly and cross-linking properties. Biochem. J. 215, 227-237.
5. Carter, A. P., Garbarino, J. E., Wilson-Kubalek, E. M., Shipley, W. E., Cho, C., Milligan, R. A., Vale, R. D., and Gibbons, I. R. (2008). Structure and functional role of dynein's microtubule-binding domain. Science 322, 1691-1695.
6. Chen, J., Kanai, Y., Cowan, N. J., and Hirokawa, N. (1992). Projection domains of MAP2 and tau determine spacings between microtubules in dendrites and axons. Nature 360, 674-677.
7. Chiu, F. C., Opanashuk, L. A., He, D. K., Lehning, E. J., and LoPachin, R. M. (2000). γ-Diketone peripheral neuropathy. II. Neurofilament subunit content. Toxicol. Appl. Pharmacol. 165, 141-147.
8. Cohlberg, J. A., Hajarian, H., Tran, T., Alipourjeddi, P., and Noveen, A. (1995). Neurofilament protein heterotetramers as assembly intermediates. J. Biol. Chem. 270, 9334-9339.
9. Cuchillo-Ibanez, S. A., Byers, H. L., Leung, K., Ward, M. A., Anderton, B. H., and Hanger, D. P. (2008). Phosphorylation of tau regulates its axonal transport by controlling its binding to kinesin. FASEB J. 22, 3186-3195.
10. DeCaprio, A. P., and Fowke, J. H. (1992). Limited and selective adduction of carboxyl-terminal lysines in the high molecular weight neurofilament proteins by 2,5-hexanedione in vitro. Brain Res. 586, 219-228.
11. DeCaprio, A. P., Kinney, E. A., and Fowke, J. H. (1997). Regioselective binding of 2,5-hexanedione to high-molecular-weight rat neurofilament proteins in vitro. Toxicol. Appl. Pharmacol. 145, 211-217.
12. DeCaprio, A. P., Olajos, E. J., and Weber, P. (1982). Covalent binding of a neurotoxic n-hexane metabolite: conversion of primary amines to substituted pyrrole adducts by 2,5-hexanedione. Toxicol. Appl. Pharmacol. 65, 440-450.
13. DeCaprio, A. P., and O'Neill, E. A. (1985). Alterations in rat axonal cytoskeletal proteins induced by in vitro and in vivo 2,5-hexanedione exposure. Toxicol. Appl. Pharmacol. 78, 235-247.
14. Edelmann, W., Zervas, M., Costello, P., Roback, L., Fischer, I., Hammarback, J. A., Cowan, N., Davies, P., Wainer, B., and Kucherlapati, R. (1996). Neuronal abnormalities in microtubule-associated protein 1B mutant mice. Proc. Natl. Acad. Sci. U.S.A. 93, 1270-1275.
15. Gilbert, S. P., Webb, M. R., Brune, M., and Johnson, K. A. (1995). Pathway of processive ATP hydrolysis by kinesin. Nature 373, 671-676.
16. Gill, S. R., Schroer, T. A., Szilak, I., Steuer, E. R., Sheetz, M. P., and Cleveland, D. W. (1991). Dynactin, a conserved, ubiquitously expressed component of an activator of vesicle motility mediated by cytoplasmic dynein. J. Cell Biol. 115, 1639-1650.
17. Graham, D. G., Genter St. Clair, M. B., Amarnath, V., and Anthony, D. C. (1991). Molecular mechanisms of γ-diketone neuropathy. Adv. Exp. Med. Biol. 283, 427-431.
18. Grierson, A. J., Johnson, G. V. W., and Miller, C. C. J. (2001). Three different human tau isoforms and rat neurofilament light, middle and heavy chain proteins are cellular substrates for transglutaminase. Neurosci. Lett. 298, 9-12.
19. Gupta, R. P., Abdel-Rahman, A., Jensen, K. F., and Abou-Donia, M. B. (2000). Altered expression of neurofilament subunits in diisopropyl phosphorofluoridate-treated hen spinal cord and their presence in axonal aggregation. Brain Res. 878, 32-47.
20. Heijink, E., Scholten, S. W., Bolhuis, P. A., and de Wolff, F. A. (2000). Effects of 2,5-hexanedione on calpain-mediated degradation of human neurofilaments in vitro. Chem. Biol. Interact. 129, 231-247.
21. Hirokawa, N. (1994). Microtubule organization and dynamics dependent on microtubule-associated proteins. Curr. Opin. Cell Biol. 6, 74-81.
22. Ikegami, K., Heier, R. L., Taruishi, M., Takagi, H., Mukai, M., Shimma, S., Taka, S., Hatanaka, K., Morone, N., Yao, I., et al. (2007). Loss of α-tubulin polyglutamylation in ROSA22 mice is associated with abnormal targeting of KIF1A and modulated synaptic function. Proc. Natl. Acad. Sci. U.S.A. 104, 3213-3218.
23. Iwabata, J., Yoshida, M., and Komatsu, Y. (2005). Proteomic analysis of organspecific post-translational lysine-acetylation and -methylation in mice by use of anti-acetyllysine and -methyllysine mouse monoclonal antibodies. Proteomics 5, 4653-4664.
24. Karlsson, J.-E., Rosengren, L. E., and Haglid, K. G. (1991). Quantitative and qualitative alterations of neuronal and glial intermediate filaments in rat nervous system after exposure to 2,5-hexanedione. J. Neurochem. 57, 1437-1444.
25. Lehning, E. J., Dyer, K. S., Jortner, B. S., and LoPachin, R. M. (1995). Axonal atrophy is a specific component of 2,5-hexanedione peripheral neuropathy. Toxicol. Appl. Pharmacol. 135, 58-66.
26. Lehning, E. J., Jortner, B. S., Fox, J. H., Arezzo, J. C., Kitano, T., and LoPachin, R. M. (2000). γ-Diketone peripheral neuropathy. I. Quantitative morphometric analyses of axonal atrophy and swelling. Toxicol. Appl. Pharmacol. 165, 127-140.
27. Letterier, J. F., Kas, J., Hartwig, J., Vegners, R., and Janmey, P. A. (1996). Mechanical effects of neurofilament cross-bridges. Modulation by phosphorylation, lipids, and interactions with F-actin. J. Biol. Chem. 271, 15687-15694.
28. LoPachin, R. M., Barber, D. S., and Gavin, T. (2008). Molecular mechanisms of the conjugated a,b-unsaturated carbonyl derivatives: Relevance to neurotoxicity and neurodegenerative diseases. Toxicol. Sci. 104, 235-249.
29. LoPachin, R. M., and DeCaprio, A. P. (2004). γ-Diketone central neuropathy: axon atrophy and the role of cytoskeletal protein adduction. Toxicol. Appl. Pharmacol. 199, 20-34.
30. LoPachin, R. M., and DeCaprio, A. P. (2005). Protein adduct formation as a molecular mechanism in neurotoxicity. Toxicol. Sci. 86, 214-225.
31. LoPachin, R. M., He, D., Reid, M. L., and Opanashuk, L. A. (2004). 2,5-Hexanedione-induced changes in the monomeric neurofilament protein content of rat spinal cord fractions. Toxicol. Appl. Pharmacol. 198, 61-73.
32. LoPachin, R. M., Jortner, B. S., Reid, M. L., and Das, S. (2003). γ-Diketone central neuropathy: quantitative morphometric analysis of axons in rat spinal cord white matter regions and nerve roots. Toxicol. Appl. Pharmacol. 193, 29-46.
33. LoPachin, R. M., Jortner, B. S., Reid, M. L., and Monir, A. (2005). γ-Diketone central neuropathy: quantitative analyses of cytoskeletal components in myelinated axons of the rat rubrospinal tract. Neurotoxicology 26, 1021-1030.
34. LoPachin, R. M., and Lehning, E. J. (1997). The relevance of axonal swelling and atrophy to c-diketone neurotoxicity. Neurotoxicology 18, 7-22.
35. LoPachin, R. M., Lehning, E. J., Stack, E. C., Hussein, S. J., and Saubermann, A. J. (1994). 2,5-Hexanedione alters elemental composition and water content of rat peripheral nerve myelinated axons. J. Neurochem. 63, 2266-2278.
36. LoPachin, R. M., Ross, J. F., Reid, M. L., Das, S., Mansukhani, S., and Lehning, E. J. (2002). Neurological evaluation of toxic axonopathies in rats: acrylamide and 2,5-hexanedione. Neurotoxicology 23, 95-110.
37. Lorand, L., and Graham, R. M. (2003). Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat. Rev. Mol. Cell Biol. 4, 140-156.
38. Millecamps, S., Gowing, G., Corti, O., Mallet, J., and Julien, J. P. (2007). Conditional NF-L transgene expression in mice for in vivo analysis of turnover and transport rate of neurofilaments. J. Neurosci. 27, 4947-4956.
39. Miyasaka, H., Okabe, S., Ishiguro, K., Uchida, T., and Hirokawa, N. (1993). Interaction of the tail domain of high molecular weight subunits of neurofilaments with the COOH-terminal region of tubulin and its regulation by τ protein kinase II. J. Biol. Chem. 268, 22695-22702.
40. Monaco, S., Autilio-Gambetti, L., Lasek, R. J., Katz, M. J., and Gambetti, P. (1989). Experimental increase of neurofilament transport rate: decreases in neurofilament number and in axon diameter. J. Neuropathol. Exp. Neurol. 48, 23-32.
41. Mukouyama, S. B., Oguchi, M., Kodera, Y., Maeda, T., and Suzuki, H. (2004). Low pKa lysine residues at the active site of sarcosine oxidase from Corynebacterium sp. U-96. Biochem. Biophys. Commun. 320, 846-851.
42. Noble, M., Lewis, S. A., and Cowan, N. J. (1989). The microtubule binding domain of microtubule-associated protein MAP1B contains a repeated sequence motif unrelated to that of MAP2 and tau. J. Cell Biol. 109, 3367-3376.
43. Norlund, M. A., Lee, J. M., Zainelli, G. M., and Muma, N. A. (1999). Elevated transglutaminase-induced bonds in PHF tau in Alzheimer's disease. Brain Res. 851, 154-163.
44. Okada, Y., and Hirokawa, N. (2000). Mechanism of the single-headed processivity: diffusional anchoring between the K-loop of kinesin and the C terminus of tubulin. Proc. Natl. Acad. Sci. U.S.A. 97, 640-645.
45. Pfister, K. K., Wagner, M. C., Stenoien, D. L., Brady, S. T., and Bloom, G. S. (1989). Monoclonal antibodies to kinesin heavy and light chains stain vesicle-like structures, but not microtubules, in cultured cells. J. Cell Biol. 108, 1453-1463.
46. Sakaguchi, T., Okada, M., Kitamura, T., and Kawasaki, K. (1993). Reduced diameter and conduction velocity of myelinated fibers in the sciatic nerve of a neurofilament-deficient mutant quail. Neurosci. Lett. 153, 65-68.
47. Saxton, W. M. (1994). Isolation and analysis of microtubule motor proteins. Methods Cell Biol. 44, 279-288.
48. Scholey, J. M., Porter, M. E., Grissom, P. M., and McIntosh, J. R. (1985). Identification of kinesin in sea urchin eggs, and evidence for its localization in the mitotic spindle. Nature 318, 483-486.
49. Selkoe, D. J., Abaham, C., and Ihara, Y. (1982). Brain transglutaminase: in vitro crosslinking of human neurofilament proteins into insoluble polymers. Proc. Natl. Acad. Sci. U.S.A. 79, 6070-6074.
50. Shah, J. V., Flanagan, L. A., Janmey, P. A., and Leterrier, J.-F. (2000). Bidirectional translocation of neurofilaments along microtubules mediated in part by dynein/dynactin. Mol. Biol. Cell 11, 3495-3508.
51. Sickles, D. W., Pearson, J. K., Beall, A., and Testino, A. (1994). Toxic axonal degeneration occurs independent of neurofilament accumulation. J. Neurosci. Res. 39, 347-354.
52. Stone, J. D., Peterson, A. P., Eyer, J., Oblak, T. G., and Sickles, D. W. (2001). Neurofilaments are nonessential to the pathogenesis of toxicant-induced axonal degeneration. J. Neurosci. 21, 2278-2287.
53. Teng, J., Takei, Y., Harad, A., Nakata, T., Chen, J., and Hirokawa, N. (2001). Synergistic effects of MAP2 and MAP1B knockout in neuronal migration, dendritic outgrowth, and microtubule organization. J. Cell Biol. 155, 65-76.
54. Tshala-Katumbay, D., Monterroso, V., Kayton, R., Lasarev, M., Sabri, M., and Spencer, P. (2009). Probing mechanisms of axonopathy. Part II: protein targets of 2,5-hexanedione, the neurotoxic metabolite of the aliphatic solvent n-hexane. Toxicol. Sci. 107, 482-489.
55. Vallee, R. B. (1982). A taxol-dependent procedure for the isolation of microtubules and microtubule-associated proteins (MAPs). J. Cell Biol. 92, 435-442.
56. Wagner, O. I., Ascano, J., Tokito, M., Leterrier, J.-F., Janmey, P. A., and Holzbaur, E. L. F. (2004). The interaction of neurofilaments with the microtubule motor cytoplasmic dynein. Mol. Biol. Cell 15, 5092-5100.
57. Xia, C.-H., Roberts, E. A., Her, L.-S., Liu, X., Williams, D. S., Cleveland, D. W., and Goldstein, L. S. B. (2003). Abnormal neurofilament transport caused by targeted disruption of neuronal kinesin heavy chain KIF5A. J. Cell Biol. 161, 55-66.
58. ε-and O-aceltylation. EMBO Rep. 8, 556-562.
59. Yang, X.-J., and Seto, E. (2008). Lysine acetylation: Codified crosstalk with other posttranslational modifications. Cell 31, 449-461.
60. Yuan, A., Rao, M. V., Kumar, A., Julien, J.-P., and Nixon, R. A. (2003). Neurofilament transport in vivo minimally requires hetero-oligomer formation. J. Neurosci. 23, 9452-9458.
61. Yuan, A., Rao, M. V., Sasaki, T., Rao, M. V., Kumar, A., Kanumuri, V., Dunlop, D. S., Liem, R. K. H., and Nixon, R. A. (2009). Neurofilaments form a highly stable stationary cytoskeleton after researching a critical level in axons. J. Neurosci. 29, 11316-11329.