Peripheral neuropathy in the Twitcher mouse involves the activation of axonal Caspase 3

ASN Neuro

Volumn 3, Issue 4, 2011, Pages 213-222

  Smith, Benjamin ^a   Galbiati, Francesca ^a   Castelvetri, Ludovico Cantuti ^a   Givogri, Maria I ^a   Lopez Rosas, Aurora ^a   Bongarzone, Ernesto R ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

Author keywords

Apoptosis; Caspase 3; Dying back pathology; Krabbe disease; Leukodystrophies; Myelin; Twitcher mouse

Indexed keywords

CASPASE 3; PSYCHOSINE; CERAMIDE; ISOPROTEIN; MYELIN BASIC PROTEIN; N CAPROYLSPHINGOSINE; N-CAPROYLSPHINGOSINE; NEUROFILAMENT PROTEIN; NEUROFILAMENT PROTEIN L;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CELL MUTANT; CONTROLLED STUDY; DEMYELINATION; DISEASE ACTIVITY; DISEASE COURSE; ENZYME ACTIVATION; ENZYME LOCALIZATION; GLIA; GLOBOID CELL LEUKODYSTROPHY; IN VITRO STUDY; MOTONEURON; MOUSE; MOUSE STRAIN; MYELINATION; NERVE FIBER DEGENERATION; NONHUMAN; PATHOPHYSIOLOGY; PERIPHERAL NEUROPATHY; SCIATIC NERVE; SPINAL CORD NERVE CELL; TWITCHER MOUSE; ANIMAL; C57BL MOUSE; CELL LINE; DISEASE MODEL; DNA FRAGMENTATION; DOSE RESPONSE; DRUG EFFECT; GENETICS; METABOLISM; MOUSE MUTANT; NERVE CONDUCTION; NERVE FIBER; NEWBORN; PATHOLOGY; PHYSIOLOGY; REVIEW; SPINAL CORD;

ANIMALS; ANIMALS, NEWBORN; AXONS; CASPASE 3; CELL LINE, TRANSFORMED; CERAMIDES; DISEASE MODELS, ANIMAL; DNA FRAGMENTATION; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME ACTIVATION; LEUKODYSTROPHY, GLOBOID CELL; MICE; MICE, INBRED C57BL; MICE, NEUROLOGIC MUTANTS; MOTOR NEURONS; MYELIN BASIC PROTEINS; NEURAL CONDUCTION; NEUROFILAMENT PROTEINS; PERIPHERAL NERVOUS SYSTEM DISEASES; PROTEIN ISOFORMS; PSYCHOSINE; SCIATIC NERVE; SPINAL CORD;

EID: 80054923275     PISSN: None     EISSN: 17590914     Source Type: Journal    
DOI: 10.1042/AN20110019     Document Type: Article

References (67)

1. Ahmed Z, Doward AI, Pryce G, Taylor DL, Pocock JM, Leonard JP, Baker D, Cuzner ML (2002) A role for caspase-1 and -3 in the pathology of experimental allergic encephalomyelitis: inflammation versus degeneration. Am J Pathol 161:1577-1586.
2. Aicardi J (1993) The inherited leukodystrophies: a clinical overview. J Inherit Metab Dis 16:733-743.
3. Barbarese E, Carson JH, Braun PE (1978) Accumulation of the four myelin basic proteins in mouse brain during development. J Neurochem 31:779-782.
4. Bird TD, Farrell DF, Sumi SM (1978) Brain lipid composition of the shiverer mouse: genetic defect in myelin development. J Neurochem 31:387-391.
5. Bjartmar C, Yin X, Trapp BD (1999) Axonal pathology in myelin disorders. J Neurocytol 28:383-395.
6. Boggs JM (2006) Myelin basic protein: a multifunctional protein. Cell Mol Life Sci 63:1945-1961.
7. Burguillos MA, Deierborg T, Kavanagh E, Persson A, Hajji N, Garcia-Quintanilla A, Cano J, Brundin P, Englund E, Venero JL, Joseph B (2011) Caspase signalling controls microglia activation and neurotoxicity. Nature 472: 319-324.
8. Castelvetri LC, Givogri MI, Zhu H, Smith B, Lopez-Rosas A, Qiu X, van Breemen R, Bongarzone ER (2011) Axonopathy is a compounding factor in the pathogenesis of Krabbe disease. Acta Neuropathol (Berl) 122:35-48.
9. Chan PH (2001) Reactive oxygen radicals in signaling and damage in the ischemic brain. J Cereb Blood Flow Metab 21:2-14.
10. Chen XH, Siman R, Iwata A, Meaney DF, Trojanowski JQ, Smith DH (2004) Long-term accumulation of amyloid-beta, beta-secretase, presenilin-1, and caspase-3 in damaged axons following brain trauma. Am J Pathol 165:357-371.
11. Chiba A, Ohta Y, Oshio K, Inase M (2003) Motor evoked potentials in rats with congenital hydrocephalus. Neurol Res 25:305-308.
12. Culmsee C, Landshamer S (2006) Molecular insights into mechanisms of the cell death program: role in the progression of neurodegenerative disorders. Curr Alzheimer Res 3:269-283.
13. de Ferra F, Engh H, Hudson L, Kamholz J, Puckett C, Molineaux S, Lazzarini RA (1985) Alternative splicing accounts for the four forms of myelin basic protein. Cell 43:721-727.
14. Dolcetta D, Amadio S, Guerrini U, Givogri MI, Perani L, Galbiati F, Sironi L, Del Carro U, Roncarolo MG, Bongarzone E (2005) Myelin deterioration in Twitcher mice: motor evoked potentials and magnetic resonance imaging as in vivo monitoring tools. J Neurosci Res 81:597-604.
15. Dolcetta D, Perani L, Givogri MI, Galbiati F, Amadio S, del Carro U, Finocchiaro G, Fanzani A, Marchesini S, Naldini L, Roncarolo MG, Bongarzone E (2006) Design and optimization of lentiviral vectors for transfer of GALC expression in Twitcher brain. J Gene Med 8:962-971.
16. Dutta R, Trapp BD (2007) Pathogenesis of axonal and neuronal damage in multiple sclerosis. Neurology 68:S22-S31; discussion S43-S54.
17. Escolar ML, Poe MD, Smith JK, Gilmore JH, Kurtzberg J, Lin W, Styner M (2009) Diffusion tensor imaging detects abnormalities in the corticospinal tracts of neonates with infantile Krabbe disease. AJNR Am J Neuroradiol 30:1017-1021.
18. Galbiati F, Basso V, Cantuti L, Givogri MI, Lopez-Rosas A, Perez N, Vasu C, Cao H, van Breemen R, Mondino A, Bongarzone ER (2007a) Autonomic denervation of lymphoid organs leads to epigenetic immune atrophy in a mouse model of Krabbe disease. J Neurosci 27:13730-13738.
19. Galbiati F, Clementi G, Superchi D, Givogri MI, Bongarzone ER (2007b) Effects of irradiation on the postnatal development of the brain in a genetic mouse model of globoid cell leukodystrophy. Neurochem Res 32:377-388.
20. Galbiati F, Givogri MI, Cantuti L, Rosas AL, Cao H, van Breemen R, Bongarzone ER (2009) Combined hematopoietic and lentiviral gene-transfer therapies in newborn Twitcher mice reveal contemporaneous neurodegeneration and demyelination in Krabbe disease. J Neurosci Res 87:1748-1759.
21. Gamblin TC, Chen F, Zambrano A, Abraha A, Lagalwar S, Guillozet AL, Lu M, Fu Y, Garcia-Sierra F, LaPointe N, Miller R, Berry RW, Binder LI, Cryns VL (2003) Caspase cleavage of tau: linking amyloid and neurofibrillary tangles in Alzheimer's disease. Proc Natl Acad Sci USA 100:10032-10037.
22. Gendelman HE, Pezeshkpour GH, Pressman NJ, Wolinsky JS, Quarles RH, Dobersen MJ, Trapp BD, Kitt CA, Aksamit A, Johnson RT (1985) A quantitation of myelin-associated glycoprotein and myelin basic protein loss in different demyelinating diseases. Ann Neurol 18:324-328.
23. Giri S, Khan M, Rattan R, Singh I, Singh AK (2006) Krabbe disease: psychosine-mediated activation of phospholipase A2 in oligodendrocyte cell death. J Lipid Res 47:1478-1492.
24. Giri S, Khan M, Nath N, Singh I, Singh AK (2008) The role of AMPK in psychosine mediated effects on oligodendrocytes and astrocytes: implication for Krabbe disease. J Neurochem 105:1820-1833.
25. Harauz G, Ladizhansky V, Boggs JM (2009) Structural polymorphism and multifunctionality of myelin basic protein. Biochemistry 48:8094-8104.
26. Hofling AA, Kim JH, Fantz CR, Sands MS, Song SK (2009) Diffusion tensor imaging detects axonal injury and demyelination in the spinal cord and cranial nerves of a murine model of globoid cell leukodystrophy. NMR Biomed 22:1100-1106.
27. Hogan GR, Gutmann L, Chou SM (1969) The peripheral neuropathy of Krabbe's (globoid) leukodystrophy. Neurology 19:1094-1100.
28. Igisu H, Suzuki K (1984) Progressive accumulation of toxic metabolite in a genetic leukodystrophy. Science 224:753-755.
29. Jacobs JM, Scaravilli F, de Aranda FT (1982) The pathogenesis of globoid cell leucodystrophy in peripheral nerve of the mouse mutant Twitcher. J Neurol Sci 55:285-304.
30. Kobayashi T, Yamanaka T, Jacobs JM, Teixeira F, Suzuki K (1980) The Twitcher mouse: an enzymatically authentic model of human globoid cell leukodystrophy (Krabbe disease). Brain Res 202:479-483.
31. Kobayashi S, Katayama M, Satoh J, Suzuki K (1988) The Twitcher mouse. An alteration of the unmyelinated fibers in the PNS. Am J Pathol 131:308-319.
32. Komiyama A, Suzuki K (1994) Progressive dysfunction of Twitcher Schwann cells is evaluated better in vitro than in vivo. Brain Res 637:106-113.
33. Kondo Y, Adams JM, Vanier MT, Duncan ID (2011) Macrophages counteract demyelination in a mouse model of globoid cell leukodystrophy. J Neurosci 31:3610-3624.
34. Krabbe K (1916) A new familial infantile form of diffuse brain sclerosis. Brain 39:74-114.
35. Kurnellas MP, Nicot A, Shull GE, Elkabes S (2005) Plasma membrane calcium ATPase deficiency causes neuronal pathology in the spinal cord: a potential mechanism for neurodegeneration in multiple sclerosis and spinal cord injury. FASEB J 19:298-300.
36. Ludolph AC, Hugon J, Spencer PS (1987) Non-invasive assessment of the pyramidal tract and motor pathway of primates. Electroencephalogr Clin Neurophysiol 67:63-67.
37. Martin LJ (1999) Neuronal death in amyotrophic lateral sclerosis is apoptosis: possible contribution of a programmed cell death mechanism. J Neuropathol Exp Neurol 58:459-471.
38. Mikoshiba K, Fujishiro M, Kohsaka S, Okano H, Takamatsu K, Tsukada Y (1985) Disorders in myelination in the Twitcher mutant: immunohistochemical and biochemical studies. Neurochem Res 10:1129-1141.
39. Morfini G, Pigino G, Opalach K, Serulle Y, Moreira JE, Sugimori M, Llinas RR, Brady ST (2007) 1-Methyl-4-phenylpyridinium affects fast axonal transport by activation of caspase and protein kinase C. Proc Natl Acad Sci USA 104:2442-2447.
40. Nagara H, Kobayashi T, Suzuki K (1982) The Twitcher mouse: normal pattern of early myelination in the spinal cord. Brain Res 244:289-294.
41. Nikolaev A, McLaughlin T, O'Leary DD, Tessier-Lavigne M (2009) APP binds DR6 to trigger axon pruning and neuron death via distinct caspases. Nature 457:981-989.
42. Ohno M, Komiyama A, Martin PM, Suzuki K (1993) Proliferation of microglia/macrophages in the demyelinating CNS and PNS of Twitcher mouse. Brain Res 602:268-274.
43. Okouchi M, Ekshyyan O, Maracine M, Aw TY (2007) Neuronal apoptosis in neurodegeneration. Antioxid Redox Signal 9:1059-1096.
44. Olmstead CE (1987) Neurological and neurobehavioral development of the mutant 'Twitcher' mouse. Behav Brain Res 25:143-153.
45. Orrenius S, Zhivotovsky B, Nicotera P (2003) Regulation of cell death: the calcium-apoptosis link. Nat Rev Mol Cell Biol 4:552-565.
46. Polster BM, Fiskum G (2004) Mitochondrial mechanisms of neural cell apoptosis. J Neurochem 90:1281-1289.
47. Ramakrishnan H, Hedayati KK, Lullmann-Rauch R, Wessig C, Fewou SN, Maier H, Goebel HH, Gieselmann V, Eckhardt M (2007) Increasing sulfatide synthesis in myelin-forming cells of arylsulfatase A-deficient mice causes demyelination and neurological symptoms reminiscent of human metachromatic leukodystrophy. J Neurosci 27:9482-9490.
48. Ravid T, Tsaba A, Gee P, Rasooly R, Medina EA, Goldkorn T (2003) Ceramide accumulation precedes caspase-3 activation during apoptosis of A549 human lung adenocarcinoma cells. Am J Physiol Lung Cell Mol Physiol 284:L1082-L1092.
49. Reeves TM, Greer JE, Vanderveer AS, Phillips LL (2010) Proteolysis of submembrane cytoskeletal proteins ankyrin-G and alphaII-spectrin following diffuse brain injury: a role in white matter vulnerability at Nodes of Ranvier. Brain Pathol 20:1055-1068.
50. Rohn TT, Rissman RA, Davis MC, Kim YE, Cotman CW, Head E (2002) Caspase-9 activation and caspase cleavage of tau in the Alzheimer's disease brain. Neurobiol Dis 11:341-354.
51. Schoenmann Z, Assa-Kunik E, Tiomny S, Minis A, Haklai-Topper L, Arama E, Yaron A (2010) Axonal degeneration is regulated by the apoptotic machinery or a NAD+-sensitive pathway in insects and mammals. J Neurosci 30:6375-6386.
52. Shinoda H, Kobayashi T, Katayama M, Goto I, Nagara H (1987) Accumulation of galactosylsphingosine (psychosine) in the Twitcher mouse: determination by HPLC. J Neurochem 49:92-99.
53. Spinedi A, Amendola A, di Bartolomeo S, Piacentini M (1998) Ceramideinduced apoptosis is mediated by caspase activation independently from retinoblastoma protein post-translational modification. Biochem Biophys Res Commun 243:852-857.
54. Suzuki K (1998) Twenty five years of the 'psychosine hypothesis': a personal perspective of its history and present status. Neurochem Res 23:251-259.
55. Takahashi H, Suzuki K (1984) Demyelination in the spinal cord of murine globoid cell leukodystrophy (the Twitcher mouse). Acta Neuropathol 62:298-308.
56. Tanaka K, Nagara H, Kobayashi T, Goto I, Suzuki K (1989) The Twitcher mouse: attenuated processes of Schwann cells in unmyelinated fibers. Brain Res 503:160-162.
57. Taniike M, Mohri I, Eguchi N, Irikura D, Urade Y, Okada S, Suzuki K (1999) An apoptotic depletion of oligodendrocytes in the Twitcher, a murine model of globoid cell leukodystrophy. J Neuropathol Exp Neurol 58:644-653.
58. Taniike M, Suzuki K (1994) Spacio-temporal progression of demyelination in Twitcher mouse: with clinico-pathological correlation. Acta Neuropathol 88:228-236.
59. Toyoshima E, Yeager AM, Brennan S, Santos GW, Moser HW, Mayer RF (1986) Nerve conduction studies in the Twitcher mouse (murine globoid cell leukodystrophy). J Neurol Sci 74:307-318.
60. Turmel H, Hartmann A, Parain K, Douhou A, Srinivasan A, Agid Y, Hirsch EC (2001) Caspase-3 activation in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-treated mice. Mov Disord 16:185-189.
61. Ugawa Y, Rothwell JC, Day BL, Thompson PD, Marsden, CD (1991) Percutaneous electrical stimulation of corticospinal pathways at the level of the pyramidal decussation in humans. Ann Neurol 29:418-427.
62. Wenger DA, Rafi MA, Luzi P, Datto J, Costantino-Ceccarini E (2000) Krabbe disease: genetic aspects and progress toward therapy. Mol Genet Metab 70:1-9.
63. Westphal D, Sytnyk V, Schachner M, Leshchyns'ka I (2010) Clustering of the NCAM (neural cell adhesion molecule) at the neuronal cell surface induces caspase-8- and -3-dependent changes of the spectrin meshwork required for NCAM-mediated neurite outgrowth. J Biol Chem 285:42046-42057.
64. White AB, Givogri MI, Lopez-Rosas A, Cao H, van Breemen R, Thinakaran G, Bongarzone ER (2009) Psychosine accumulates in membrane microdomains in the brain of Krabbe patients, disrupting the raft architecture. J Neurosci 29:6068-6077.
65. White AB, Galbiati F, Givogri MI, Lopez Rosas A, Qiu X, van Breemen R, Bongarzone ER (2011) Persistence of psychosine in brain lipid rafts is a limiting factor in the therapeutic recovery of a mouse model for Krabbe disease. J Neurosci Res 89:352-364.
66. Whitfield PD, Sharp PC, Taylor R, Meikle P (2001) Quantification of galactosylsphingosine in the Twitcher mouse using electrospray ionization-tandem mass spectrometry. J Lipid Res 42:2092-2095.
67. Yamada H, Martin P, Suzuki K (1996) Impairment of protein kinase C activity in Twitcher Schwann cells in vitro. Brain Res 718:138-144.