Critical role of calpain in spinal cord degeneration in Parkinson's disease

Journal of Neurochemistry

Volumn 127, Issue 6, 2013, Pages 880-890

  Samantaray, Supriti ^a   Knaryan, Varduhi H ^a   Shields, Donald C ^b   Banik, Naren L ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

Author keywords

axonal degeneration; calpain; inflammation; neurodegeneration

Indexed keywords

CALPAIN 1; CALPAIN 2; CALPASTATIN; CHOLINE ACETYLTRANSFERASE; CYCLOOXYGENASE 2; NEUROFILAMENT PROTEIN;

AGED; ARTICLE; ASTROCYTOSIS; CERVICAL SPINAL CORD; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME INDUCTION; FEMALE; GLIOSIS; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; LUMBAR SPINAL CORD; LYMPHOCYTIC INFILTRATION; MALE; MOTONEURON; NERVE CELL NECROSIS; NERVE DEGENERATION; NERVE FIBER DEGENERATION; NERVOUS SYSTEM INFLAMMATION; PARKINSON DISEASE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SENSORY NERVE CELL; SPINAL CORD ATROPHY; T LYMPHOCYTE; THORACIC SPINAL CORD; TISSUE SECTION; VERY ELDERLY;

EID: 84890124327     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12374     Document Type: Article

References (66)

1. Banik N. L., Hogan E. L., Jenkins M. G., McDonald J. K., McAlhaney W. W., and, Sostek M. B., (1983) Purification of a calcium-activated neutral proteinase from bovine brain. Neurochem. Res. 8, 1389-1405.
2. Braak H., and, Del Tredici K., (2009) Neuroanatomy and pathology of sporadic Parkinson's disease. Adv. Anat. Embryol. Cell Biol. 201, 1-119.
3. Brochard V., Combadiere B., Prigent A., et al,. (2009) Infiltration of CD4+ lymphocytes into the brain contributes to neurodegeneration in a mouse model of Parkinson disease. J. Clin. Invest. 119, 182-192.
4. Burguillos M. A., Hajji N., Englund E., Persson A., Cenci A. M., Machado A., Cano J., Joseph B., and, Venero J. L., (2011) Apoptosis-inducing factor mediates dopaminergic cell death in response to LPS-induced inflammatory stimulus: evidence in Parkinson's disease patients. Neurobiol. Dis. 41, 177-188.
5. Butler J. T., Samantaray S., Beeson C. C., Ray S. K., and, Banik N. L., (2009) Involvement of calpain in the process of Jurkat T cell chemotaxis. J. Neurosci. Res. 87, 626-635.
6. Chera B., Schaecher K. E., Rocchini A., Imam S. Z., Sribnick E. A., Ray S. K., Ali S. F., and, Banik N. L., (2004) Immunofluorescent labeling of increased calpain expression and neuronal death in the spinal cord of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-treated mice. Brain Res. 1006, 150-156.
7. Choi D. H., Kim E. M., Son H. J., Joh T. H., Kim Y. S., Kim D., Flint Beal M., and, Hwang O., (2008) A novel intracellular role of matrix metalloproteinase-3 during apoptosis of dopaminergic cells. J. Neurochem. 106, 405-415.
8. Crocker S. J., Smith P. D., Jackson-Lewis V., et al,. (2003) Inhibition of calpains prevents neuronal and behavioral deficits in an MPTP mouse model of Parkinson's disease. J. Neurosci. 23, 4081-4091.
9. Czlonkowska A., Kohutnicka M., Kurkowska-Jastrzebska I., and, Czlonkowski A., (1996) Microglial reaction in MPTP (1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine) induced Parkinson's disease mice model. Neurodegeneration 5, 137-143.
10. Damier P., Hirsch E. C., Agid Y., and, Graybiel A. M., (1999) The substantia nigra of the human brain. II. Patterns of loss of dopamine-containing neurons in Parkinson's disease. Brain 122 (Pt 8), 1437-1448.
11. Del Tredici K., and, Braak H., (2012) Spinal cord lesions in sporadic Parkinson's disease. Acta Neuropathol. 124, 643-664.
12. Denson M. A., and, Wszolek Z. K., (1995) Familial parkinsonism: our experience and review. Parkinsonism Relat. Disord. 1, 35-46.
13. Dubois M., Strazielle C., Julien J. P., and, Lalonde R., (2005) Mice with the deleted neurofilament of low molecular weight (Nefl) gene: 2. Effects on motor functions and spatial orientation. J. Neurosci. Res. 80, 751-758.
14. Filley C. M., (2005) Neurobehavioral aspects of cerebral white matter disorders. Psychiatr. Clin. North Am. 28, 685-700.
15. Forno L. S., Sternberger L. A., Sternberger N. H., Strefling A. M., Swanson K., and, Eng L. F., (1986) Reaction of Lewy bodies with antibodies to phosphorylated and non-phosphorylated neurofilaments. Neurosci. Lett. 64, 253-258.
16. Galloway P. G., Grundke-Iqbal I., Iqbal K., and, Perry G., (1988) Lewy bodies contain epitopes both shared and distinct from Alzheimer neurofibrillary tangles. J. Neuropathol. Exp. Neurol. 47, 654-663.
17. Galvin J. E., Uryu K., Lee V. M., and, Trojanowski J. Q., (1999) Axon pathology in Parkinson's disease and Lewy body dementia hippocampus contains alpha-, beta-, and gamma-synuclein. Proc. Natl Acad. Sci. USA 96, 13450-13455.
18. Gotow T., (2000) Neurofilaments in health and disease. Med. Electron Microsc. 33, 173-199.
19. Hawkes C. H., Del Tredici K., and, Braak H., (2010) A timeline for Parkinson's disease. Parkinsonism Relat. Disord. 16, 79-84.
20. Hill W. D., Arai M., Cohen J. A., and, Trojanowski J. Q., (1993) Neurofilament mRNA is reduced in Parkinson's disease substantia nigra pars compacta neurons. J. Comp. Neurol. 329, 328-336.
21. Imai Y., and, Lu B., (2011) Mitochondrial dynamics and mitophagy in Parkinson's disease: disordered cellular power plant becomes a big deal in a major movement disorder. Curr. Opin. Neurobiol. 21, 935-941.
22. Kim Y. S., Kim S. S., Cho J. J., Choi D. H., Hwang O., Shin D. H., Chun H. S., Beal M. F., and, Joh T. H., (2005) Matrix metalloproteinase-3: a novel signaling proteinase from apoptotic neuronal cells that activates microglia. J. Neurosci. 25, 3701-3711.
23. Knaryan V. H., Samantaray S., Le Gal C., Ray S. K., and, Banik N. L., (2011) Tracking extranigral degeneration in animal models of Parkinson's disease: quest for effective therapeutic strategies. J. Neurochem. 118, 326-338.
24. Laurie C., Reynolds A., Coskun O., Bowman E., Gendelman H. E., and, Mosley R. L., (2007) CD4+ T cells from copolymer-1 immunized mice protect dopaminergic neurons in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of Parkinson's disease. J. Neuroimmunol. 183, 60-68.
25. Levesque S., Wilson B., Gregoria V., Thorpe L. B., Dallas S., Polikov V. S., Hong J. S., and, Block M. L,. (2010) Reactive microgliosis: extracellular micro-calpain and microglia-mediated dopaminergic neurotoxicity. Brain 133, 808-821.
26. Lezi E., and, Swerdlow R. H., (2012) Mitochondria in neurodegeneration. Adv. Exp. Med. Biol. 942, 269-286.
27. Lo E. H., Wang X., and, Cuzner M. L., (2002) Extracellular proteolysis in brain injury and inflammation: role for plasminogen activators and matrix metalloproteinases. J. Neurosci. Res. 69, 1-9.
28. Lorenzl S., Albers D. S., Narr S., Chirichigno J., and, Beal M. F., (2002) Expression of MMP-2, MMP-9, and MMP-1 and their endogenous counterregulators TIMP-1 and TIMP-2 in postmortem brain tissue of Parkinson's disease. Exp. Neurol. 178, 13-20.
29. Lorenzl S., Calingasan N., Yang L., et al,. (2004) Matrix metalloproteinase-9 is elevated in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine- induced parkinsonism in mice. NeuroMol. Med. 5, 119-132.
30. McGeer P. L., Itagaki S., Boyes B. E., and, McGeer E. G., (1988) Reactive microglia are positive for HLA-DR in the substantia nigra of Parkinson's and Alzheimer's disease brains. Neurology 38, 1285-1291.
31. Mouatt-Prigent A., Karlsson J. O., Yelnik J., Agid Y., and, Hirsch E. C., (2000) Calpastatin immunoreactivity in the monkey and human brain of control subjects and patients with Parkinson's disease. J. Comp. Neurol. 419, 175-192.
32. Najim al-Din A. S., Wriekat A., Mubaidin A., Dasouki M., and, Hiari M,. (1994) Pallido-pyramidal degeneration, supranuclear upgaze paresis and dementia: Kufor-Rakeb syndrome. Acta Neurol. Scand. 89, 347-352.
33. Olanow C. W., Stocchi F., and, Lang A. E., (2011) Parkinson's Disease: Non-Motor and Non-Dopaminergic Features. Wiley-Blackwell, Chichester, West Sussex, UK.
34. Perrot R., and, Eyer J., (2009) Neuronal intermediate filaments and neurodegenerative disorders. Brain Res. Bull. 80, 282-295.
35. Pollanen M. S., Bergeron C., and, Weyer L., (1992) Detergent-insoluble cortical Lewy body fibrils share epitopes with neurofilament and tau. J. Neurochem. 58, 1953-1956.
36. Ray S. K., and, Banik N. L., (2003) Calpain and its involvement in the pathophysiology of CNS injuries and diseases: therapeutic potential of calpain inhibitors for prevention of neurodegeneration. Curr. Drug Targets CNS Neurol. Disord. 2, 173-189.
37. Reynolds A. D., Banerjee R., Liu J., Gendelman H. E., and, Mosley R. L., (2007) Neuroprotective activities of CD4+ CD25+ regulatory T cells in an animal model of Parkinson's disease. J. Leukoc. Biol. 82, 1083-1094.
38. Rosell A., and, Lo E. H., (2008) Multiphasic roles for matrix metalloproteinases after stroke. Curr. Opin. Pharmacol. 8, 82-89.
39. Rosenberg G. A., (2009) Matrix metalloproteinases and their multiple roles in neurodegenerative diseases. Lancet Neurol. 8, 205-216.
40. Roy A., Ghosh A., Jana A., Liu X., Brahmachari S., Gendelman H. E., and, Pahan K., (2012) Sodium phenylbutyrate controls neuroinflammatory and antioxidant activities and protects dopaminergic neurons in mouse models of Parkinson's disease. PLoS ONE 7, e38113.
41. Sage J. I., Kortis H. I., and, Sommer W., (1990) Evidence for the role of spinal cord systems in Parkinson's disease-associated pain. Clin. Neuropharmacol. 13, 171-174.
42. Samantaray S., Knaryan V. H., Guyton M. K., Matzelle D. D., Ray S. K., and, Banik N. L., (2007) The parkinsonian neurotoxin rotenone activates calpain and caspase-3 leading to motoneuron degeneration in spinal cord of Lewis rats. Neuroscience 146, 741-755.
43. Samantaray S., Knaryan V. H., Butler J. T., Ray S. K., and, Banik N. L., (2008a) Spinal cord degeneration in C57BL/6N mice following induction of experimental parkinsonism with MPTP. J. Neurochem. 104, 1309-1320.
44. Samantaray S., Ray S. K., and, Banik N. L., (2008b) Calpain as a potential therapeutic target in Parkinson's disease. CNS Neurol. Disord. Drug Targets 7, 305-312.
45. Samantaray S., Knaryan V. H., Le Gal C., Ray S. K., and, Banik N. L., (2011) Calpain inhibition protected spinal cord motoneurons against 1-methyl-4-phenylpyridinium ion and rotenone. Neuroscience 192, 263-274.
46. Sandyk R., and, Lacono R. P., (1987) Spinal dopamine mechanisms and primary sensory symptoms in Parkinson's disease. Int. J. Neurosci. 32, 927-931.
47. Sanfilipo M. P., Benedict R. H., Weinstock-Guttman B., and, Bakshi R., (2006) Gray and white matter brain atrophy and neuropsychological impairment in multiple sclerosis. Neurology 66, 685-692.
48. Shea T. B., Chan W. K., Kushkuley J., and, Lee S., (2009) Organizational dynamics, functions, and pathobiological dysfunctions of neurofilaments. Results Probl. Cell Differ. 48, 29-45.
49. Shields D. C., and, Banik N. L., (1998) Upregulation of calpain activity and expression in experimental allergic encephalomyelitis: a putative role for calpain in demyelination. Brain Res. 794, 68-74.
50. Shields D. C., Schaecher K. E., Saido T. C., and, Banik N. L., (1999) A putative mechanism of demyelination in multiple sclerosis by a proteolytic enzyme, calpain. Proc. Natl Acad. Sci. USA 96, 11486-11491.
51. Siderowf A., and, Lang A. E., (2012) Premotor Parkinson's disease: concepts and definitions. Mov. Disord. 27, 608-616.
52. Smith J. A., Das A., Ray S. K., and, Banik N. L., (2012) Role of pro-inflammatory cytokines released from microglia in neurodegenerative diseases. Brain Res. Bull. 87, 10-20.
53. Sternberger L. A., and, Sternberger N. H., (1983) Monoclonal antibodies distinguish phosphorylated and nonphosphorylated forms of neurofilaments in situ. Proc. Natl Acad. Sci. USA 80, 6126-6130.
54. Szaro B. G., and, Strong M. J., (2010) Post-transcriptional control of neurofilaments: New roles in development, regeneration and neurodegenerative disease. Trends Neurosci. 33, 27-37.
55. Teismann P., Tieu K., Choi D. K., Wu D. C., Naini A., Hunot S., Vila M., Jackson-Lewis V., and, Przedborski S., (2003) Cyclooxygenase-2 is instrumental in Parkinson's disease neurodegeneration. Proc. Natl Acad. Sci. USA 100, 5473-5478.
56. Trojanowski J. Q., Ishihara T., Higuchi M., Yoshiyama Y., Hong M., Zhang B., Forman M. S., Zhukareva V., and, Lee V. M., (2002) Amyotrophic lateral sclerosis/parkinsonism dementia complex: transgenic mice provide insights into mechanisms underlying a common tauopathy in an ethnic minority on Guam. Exp. Neurol. 176, 1-11.
57. Vijitruth R., Liu M., Choi D. Y., Nguyen X. V., Hunter R. L., and, Bing G., (2006) Cyclooxygenase-2 mediates microglial activation and secondary dopaminergic cell death in the mouse MPTP model of Parkinson's disease. J. Neuroinflammation 3, 6.
58. Vivacqua G., Casini A., Vaccaro R., Salvi E. P., Pasquali L., Fornai F., Yu S., and, D'Este L., (2011) Spinal cord and parkinsonism: neuromorphological evidences in humans and experimental studies. J. Chem. Neuroanat. 42, 327-340.
59. Vivacqua G., Biagioni F., Yu S., Casini A., Bucci D., D'Este L., and, Fornai F., (2012) Loss of spinal motor neurons and alteration of alpha-synuclein immunostaining in MPTP induced Parkinsonism in mice. J. Chem. Neuroanat. 44, 76-85.
60. Wakabayashi K., and, Takahashi H., (1997) The intermediolateral nucleus and Clarke's column in Parkinson's disease. Acta Neuropathol. 94, 287-289.
61. Wang T., Zhang W., Pei Z., Block M., Wilson B., Reece J. M., Miller D. S., and, Hong J. S., (2006) Reactive microgliosis participates in MPP+-induced dopaminergic neurodegeneration: role of 67 kDa laminin receptor. FASEB J. 20, 906-915.
62. Weil-Fugazza J., and, Godefroy F., (1993) Dorsal and ventral dopaminergic innervation of the spinal cord: functional implications. Brain Res. Bull. 30, 319-324.
63. Wilkin G. P., and, Knott C., (1999) Glia: a curtain raiser. Adv. Neurol. 80, 3-7.
64. Yasuda Y., Shinagawa R., Yamada M., Mori T., Tateishi N., and, Fujita S., (2007) Long-lasting reactive changes observed in microglia in the striatal and substantia nigral of mice after 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Brain Res. 1138, 196-202.
65. Yoshikawa K., Nakata Y., Yamada K., and, Nakagawa M., (2004) Early pathological changes in the parkinsonian brain demonstrated by diffusion tensor MRI. J. Neurol. Neurosurg. Psychiatry 75, 481-484.
66. Zhu Q., Couillard-Despres S., and, Julien J. P., (1997) Delayed maturation of regenerating myelinated axons in mice lacking neurofilaments. Exp. Neurol. 148, 299-316.