Motor neuron pathology in experimental autoimmune encephalomyelitis: Studies in THY1-YFP transgenic mice

Brain

Volumn 128, Issue 8, 2005, Pages 1877-1886

  Bannerman, P G ^a   Hahn, A ^a   Ramirez, S ^a   Morley, M ^a   Bonnemann C ^a   Yu, S ^b   Zhang, G X ^b   Rostami, A ^b   Pleasure, D ^a  

^a CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^b THOMAS JEFFERSON UNIVERSITY HOSPITAL   (United States)

Author keywords

Axonal degeneration; Dendrite; Experimental autoimmune encephalomyelitis (EAE); Motor neuron; Multiple sclerosis

Indexed keywords

MYELIN OLIGODENDROCYTE GLYCOPROTEIN; NEUROFILAMENT PROTEIN; YELLOW FLUORESCENT PROTEIN; MYELIN ASSOCIATED GLYCOPROTEIN; NEUROFILAMENT PROTEIN H; OLIGODENDROCYTE MYELIN GLYCOPROTEIN; OLIGODENDROCYTE-MYELIN GLYCOPROTEIN;

ALLERGIC ENCEPHALOMYELITIS; AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AXONAL INJURY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DEMYELINATION; DENDRITE; DISEASE COURSE; FEMALE; IMMUNOREACTIVITY; LUMBOSACRAL SPINE; MALE; MOTONEURON; MOTOR NEURON DISEASE; MOUSE; MULTIPLE SCLEROSIS; MYELITIS; NONHUMAN; PERIKARYON; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SEQUENCE ANALYSIS; SPINAL CORD ATROPHY; TRANSGENE; TRANSGENIC MOUSE; ANIMAL; ATROPHY; C57BL MOUSE; DEMYELINATING DISEASE; NERVE FIBER; PATHOLOGY; PHENOTYPE; PHOSPHORYLATION; SPINAL CORD;

ANIMALS; ATROPHY; AXONS; DEMYELINATING AUTOIMMUNE DISEASES, CNS; DENDRITES; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOTOR NEURONS; MYELIN-ASSOCIATED GLYCOPROTEIN; NEUROFILAMENT PROTEINS; PHENOTYPE; PHOSPHORYLATION; SPINAL CORD;

EID: 23444441299     PISSN: 00068950     EISSN: None     Source Type: Journal    
DOI: 10.1093/brain/awh550     Document Type: Article

References (58)

1. Ackerley S, Grierson AJ, Brownlees J, Thornhill P, Anderton BH, Leigh PN, et al. Glutamate slows axonal transport of neurofilaments in transfected neurons. J Cell Biol 2000; 150: 165-75.
2. Ackerley S, Grierson AJ, Banner S, Perkinton MS, Brownlees J, Byers HL, et al. p38α stress-activated protein kinase phosphorylates neurofilaments and is associated with neurofilament pathology in amyotrophic lateral sclerosis. Mol Cell Neurosci 2004; 26: 354-64.
3. Ahmed Z, Doward AI, Pryce G, Taylor DL, Pocock JM, Leonard JP, et al. A role for caspase-1 and 3 in the pathology of experimental allergic encephalomyelitis. Inflammation versus degeneration. Am J Pathol 2002; 161: 1577-86.
4. Bjartmar C, Kidd G, Mork S, Rudick R, Trapp BD. Neurological disabuity correlates with spinal cord axonal loss and reduced N-acetyl aspartate in chronic multiple sclerosis patients. Ann Neurol 2000; 48: 893-901.
5. Bjartmar C, Wujek JR, Trapp BD. Axonal loss in the pathology of multiple sclerosis: consequences for understanding the progressive phase of the disease. J Neurol Sci 2003; 206: 165-71.
6. Brownlees J, Yates A, Bajaj NP, Davis D, Anderton BH, Leigh PN, et al. Phosphorylation of neurofilament heavy chain side-arms by stress activated protein kinase-1b/Jun N-terminal kinase-3. J Cell Sci 2000; 113: 401-7.
7. Carriedo SG, Yin HZ, Weiss JH. Motor neurons are selectively vulnerable to AMPA/kainate receptor-mediated injury in vitro. J Neurosci 1996; 16: 4069-79.
8. Charcot JM. Lectures on the diseases of the nervous system delivered at La Salpetriere (translated by G. Sigerson). London: New Sydenham Society; 1877.
9. Chaudhuri A, Behan PO. Fatigue in neurological disorders. Lancet 2004; 363: 978-88.
10. Craner MJ, Hains BC, Lo AC, Black JA, Waxman SG. Co-localization of sodium channel Nav1.6 and the sodium-calcium exchanger at sites of axonal injury in the spinal cord in EAE. Brain 2004; 127: 294-303.
11. de Haan A, de Ruiter CJ, van der Woude, LHV, Jongen PJH. Contractile properties and fatigue of quadriceps muscles in multiple sclerosis. Muscle Nerve 2000; 23: 1534-41.
12. De Stefano N, Matthews PM, Fu L, Narayanan S, Stanley J, Francis GS, et al. Axonal damage correlates with disability in patients with relapsing-remitting multiple sclerosis. Results of a longitudinal magnetic resonance spectroscopy study. Brain 1998; 121: 1469-77.
13. De Stefano N, Narayanan S, Francis GS, Arnaoutelis R, Tartaglia MC, Antel JP, et al. Evidence of axonal damage in the early stages of multiple sclerosis and its relevance to disability. Arch Neurol 2001; 58: 65-70.
14. Diem R, Hobom M, Maier K, Weissert R, Storch MK, Meyer R, Bahr M. Methylprednisolone increases neuronal apoptosis during autoimmune CNS inflammation by inhibition of an endogenous neuroprotective pathway. J Neurosci 2003; 23: 6993-7000.
15. Edwards SG, Gong QY, Liu C, Zvartau ME, Jaspan T, Roberts N, Blumhardt LD. Infratentorial atrophy on magnetic resonance imaging and disability in multiple sclerosis. Brain 1999; 122: 291-301.
16. Evangelou N, Konz D, Esiri MM, Smith S, Palace J, Matthews PM. Size-selective neuronal changes in the anterior optic pathways suggest a differential susceptibility to injury in multiple sclerosis. Brain 2001; 124: 1813-20.
17. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, Wallace M, et al. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 2000; 28: 41-51.
18. Filippi M, Bozzali M, Rovaris M, Gonen O, Kesavadas C, Ghezzi A, et al. Evidence for widespread axonal damage at the earliest clinical stage of multiple sclerosis. Brain 2003; 126: 433-7.
19. Fisher M, Long RR, Drachman DA. Hand muscle atrophy in multiple sclerosis. Arch Neurol 1983; 40: 811-5.
20. Gavrieli Y, Sherman Y, Ben-Sasson SA. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 1992; 119: 493-501.
21. Gran B, Zhang G-X, Yu S, Li J, Chen X-H, Ventura ES, et al. IL-12p35-deficient mice are susceptible to experimental autoimmune encephalomyelitis: evidence for redundancy in the IL-12 system in the induction of central nervous system autoimmune demyelination. J Immunol 2002; 169: 7104-10.
22. Hardin-Pouzet H, Krakowski M, Bourbonniere L, Didier-Bazes M, Tran E, Owens T. Glutamate metabolism is down-regulated in astrocytes during experimental allergic encephalomyelitis. Glia 1997; 20: 79-85.
23. Hobom M, Storch MK, Weissert R, Maier K, Radhakrishnan A, Kramer B, et al. Mechanisms and time course of neuronal degeneration in experimental autoimmune encephalomyelitis. Brain Pathol 2004; 14: 148-57.
24. Kanwar JR, Kanwar RK, Krissansen GW. Simultaneous neuroprotection and blockade of inflammation reverses autoimmune encephalomyelitis. Brain 2004; 127: 1313-31.
25. Kornek B, Storch MK, Bauer J, Djamshidian A, Weissert R, Wallstroem E, et al. Distribution of a calcium channel subunit in dystrophic axons in multiple sclerosis and experimental autoimmune encephalomyelitis. Brain 2001; 124: 1114-24.
26. Lee VM-Y, Carden MJ, Schlaepfer WW, Trojanowski JQ. Monoclonal antibodies distinguish several differentially phosphorylated states of the two largest rat neurofilament subunits (NF-H and NF-M) and demonstrate their existence in the normal nervous system of the adult rat. J Neurosci 1987; 7: 3474-88.
27. Lin X, Blumhardt LD, Constantinescu CS. The relationship of brain and cervical cord volume to disability in clinical subtypes of multiple sclerosis: a three-dimensional MRI study. Acta Neurol Scand 2003; 108: 401-6.
28. Lin X, Tench CR, Evangelou N, Jaspan T, Constantiescu CS. Measurement of spinal cord atrophy in multiple sclerosis. J Neuroimaging 2004; 20S-26S.
29. Matute C, Alberdi E, Domercq M, Perez-Cerda F, Perez-Samartin A, Sanchez-Gomez MV. The link between excitotoxic oligodendroglial death and demyelinating diseases. Trends Neurosci 2001; 24: 224-30.
30. McPhail LT, Fernandes KJ, Chan CC, Vanderluit JL, Tetzlaff W. Axonal reinjury reveals the survival and re-expression of regeneration-associated genes in chronically axotomized adult motoneurons. Exp Neurol 2004; 188: 331-40.
31. Meyer R, Weissert R, Diem R, Storch MK, de Graaf KL, Kramer B, Bahr M. Acute neuronal apoptosis in a rat model of multiple sclerosis. J Neurosci 2001; 21: 6214-20.
32. Miller DH, Barkhof F, Frank JA, Parker GJM, Thompson AJ. Measurement of atrophy in multiple sclerosis: pathological basis, methodological aspects and clinical relevance. Brain 2002; 125: 1676-95.
33. Onuki M, Ayers MM, Bernard CC, Orian JM. Axonal degeneration is an early pathological feature in autoimmune-mediated demyelination in mice. Microsc Res Tech 2001; 15: 731-9.
34. Papandrikopoulou A, Doll T, Tucker RP, Garner GC, Matus A. Embryonic MAP2 lacks the cross-linking sidearm sequences and dendritic targeting signal of adult MAP2. Nature 1989; 340: 650-2.
35. Perry VH, Anthony DC. Axon damage and repair in multiple sclerosis. Philos Trans R Soc Lond B Biol Sci 1999; 354: 1641-7.
36. Petajan JH. Electromyographic findings in multiple sclerosis: remitting signs of denervation. Muscle Nerve 1982; 5: S157-60.
37. Peterson JW, Bo L, Mork S, Chang A, Trapp BD. Transected neurites, apoptotic neurons, and reduced inflammation in cortical multiple sclerosis lesions. Ann Neurol 2001; 50: 389-400.
38. Pitt D, Werner P, Raine CS. Glutamate excitotoxicity in a model of multiple sclerosis. Nature Med 2000; 6: 67-70.
39. Ray SK, Schaecher KE, Shields DC, Hogan EL, Banik NL. Combined TUNEL and double immunofluorescent labeling for detection of apoptotic mononuclear phagocytes in autoimmune demyelinating disease. Brain Res Brain Res Protoc 2000; 5: 305-11.
40. Riederer BM, Draberova E, Viklicky V, Draber P. Changes of MAP2 phosphorylation during brain development. J Histochem Cytochem 1995; 43: 1269-84.
41. Ritz LA, Bailey SM, Murray CR, Sparkes ML. Organizational and morphological features of cat sacrocaudal motoneurons. J Comp Neurol 1992; 318: 209-21.
42. Shefner JM, Mackin GA, Dawson DM. Lower motor neuron dysfunction in patients with multiple sclerosis. Muscle Nerve 1992; 15: 1265-70.
43. Slavin A, Ewing C, Liu J, Ichikawa M, Slavin J, Bernard CC. Induction of a multiple sclerosis-like disease in mice with an immunodominant epitope of myelin oligodendrocyte glycoprotein. Autoimmunity 1998; 28: 109-20.
44. Smith T, Groom A, Zhu B, Turski L. Autoimmune encephalomyelitis ameliorated by AMPA antagonists. Nature Med 2000; 6: 62-6.
45. Snider WD, Palavali V. Early axon and dendritic outgrowth of spinal accessory motor neurons studied with DiI in fixed tissues. J Comp Neurol 1990; 297: 227-38.
46. Sternberger LA, Sternberger NH. Monoclonal antibodies distinguish phosphorylated and nonphosphorylated forms of neurofilaments in situ. Proc Natl Acad Sci USA 1983; 80: 6126-30.
47. Stys PK. Axonal degeneration in multiple sclerosis: is it time for neuroprotective strategies? Ann Neurol 2004; 55: 601-3.
48. Sun D, Leung CL, Liem RKH. Phosphorylation of the high molecular weight neurofilament protein (NF-H) by Cdk5 and p35. J Biol Chem 1996; 271: 14245-51.
49. Trapp BD, Peterson J, Ransohoff RM, Rudick R, Mork S, Bo L. Axonal transection in the lesions of multiple sclerosis. New Engl J Med 1998; 338: 278-85.
50. Tsang YM, Chiong F, Kuznetsov D, Karaskis E, Geula C. Motor neurons are rich in non-phosphorylated neurofilaments: cross-species comparison and alterations in ALS. Brain Res 2000; 861: 45-58.
51. Ukkonen M, Dastidar P, Heinonen T, Laasonen E, Elovaara I. Volumetric quantitation by MRI in primary progressive multiple sclerosis: volumes of plaques and atrophy correlated with neurological disability. Eur J Neurol 2003; 10: 663-9.
52. Vanderhorst VG, Holstege G. Organization of lumbosacral motoneuronal cell groups innervating hindlimb, pelvic floor and axial muscles in the cat. J Comp Neurol 1997; 382: 46-76.
53. Veeranna, Amin ND, Ahn NG, Jaffe H, Winters CA, Grant P, Pant HC. Mitogen-activated protein kinases (Erk1,2) phosphorylate Lys-Ser-Pro (KSP) repeats in neurofilament proteins NF-H and NF-M. J Neurosci 1998; 18: 4008-21.
54. Villarroya H, Marie Y, Ouallet JC, Le Saux F, Tchelingerian JL, Baumann N. Expression of TNF alpha in central neurons of Lewis rat spinal cord after EAE induction. J Neurosci Res 1997; 49: 592-9.
55. Werner P, Pitt D, Raine CS. Multiple sclerosis: altered glutamate homeostasis in lesions correlates with oligodendrocyte and axonal damage. Ann Neurol 2001; 50: 169-80.
56. Yasuda M, Umemura S, Osamura RY, Kenjo T, Tsutsumi Y. Apoptotic cells in the human endometrium and placental villi: pitfalls in applying the TUNEL method. Arch Histol Cytol 1995; 58: 185-90.
57. Zhang GX, Yu S, Gran B, Li J, Siglienti I, Chen X, et al. Role of IL-12 receptor beta 1 in regulation of T cell response by APC in experimental autoimmune encephalomyelitis. J Immunol 2003; 171: 4485-92.
58. Zhu B, Luo L, Moore GR, Paty DW, Cynader MS. Dendritic and synaptic pathology in experimental autoimmune encephalomyelitis. Am J Pathol 2003; 162: 1639-50.