Inhibition of glyceraldehyde-3-phosphate dehydrogenase activity by antibodies present in the cerebrospinal fluid of patients with multiple sclerosis

Journal of Immunology

Volumn 185, Issue 3, 2010, Pages 1968-1975

  Kölln, Johanna ^a   Zhang, Yiping ^a   Thai, Gaby ^a   Demetriou, Michael ^a   Hermanowicz, Neal ^a   Duquette, Pierre ^b   Van Den Noort, Stanley ^a   Qin, Yufen ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b NOTRE DAME HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYME ANTIBODY; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE ANTIBODY; IMMUNOGLOBULIN G; TRIOSEPHOSPHATE ISOMERASE; TRIOSEPHOSPHATE ISOMERASE ANTIBODY; UNCLASSIFIED DRUG; AUTOANTIBODY;

ADULT; ARTICLE; CEREBROSPINAL FLUID; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; HUMAN; MALE; MULTIPLE SCLEROSIS; NEUROLOGIC DISEASE; PRIORITY JOURNAL; PROTEIN PURIFICATION; ANIMAL; BIOSYNTHESIS; COMPARATIVE STUDY; DEGENERATIVE DISEASE; DOWN REGULATION; DRUG ANTAGONISM; ENZYME ACTIVATION; ENZYMOLOGY; IMMUNOLOGY; METABOLISM; MIDDLE AGED; PHYSIOLOGY; RABBIT; UPREGULATION;

ADULT; ANIMALS; AUTOANTIBODIES; DOWN-REGULATION; ENZYME ACTIVATION; FEMALE; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASES; HUMANS; IMMUNOGLOBULIN G; MALE; MIDDLE AGED; MULTIPLE SCLEROSIS; NEURODEGENERATIVE DISEASES; RABBITS; TRIOSE-PHOSPHATE ISOMERASE; UP-REGULATION;

EID: 77956409953     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0904083     Document Type: Article

References (66)

1. Hafler, D. A., A. Compston, S. Sawcer, E. S. Lander, M. J. Daly, P. L. De Jager, P. I. de Bakker, S. B. Gabriel, D. B. Mirel, A. J. Ivinson, et al; International Multiple Sclerosis Genetics Consortium. 2007. Risk alleles for multiple sclerosis identified by a genomewide study. N. Engl. J. Med. 357: 851-862.
2. Oksenberg, J. R., S. E. Baranzini, S. Sawcer, and S. L. Hauser. 2008. The genetics of multiple sclerosis: SNPs to pathways to pathogenesis. Nat. Rev. Genet. 9: 516-526.
3. Compston, A., and A. Coles. 2008. Multiple sclerosis. Lancet 372: 1502-1517.
4. Poser, C. 1978. Multiple Sclerosis: An Analysis of 812 Cases by Means of Electronic Data Progressing. Springer, Berlin.
5. Dutta, R., and B. D. Trapp. 2007. Pathogenesis of axonal and neuronal damage in multiple sclerosis. Neurology 68:S22-31; discussion S43-54.
6. Fu, L., P. M. Matthews, N. De Stefano, K. J. Worsley, S. Narayanan, G. S. Francis, J. P. Antel, C. Wolfson, and D. L. Arnold. 1998. Imaging axonal damage of normal-appearing white matter in multiple sclerosis. Brain 121: 103-113.
7. Kolln, J., H. M. Ren, R. R. Da, Y. Zhang, E. Spillner, M. Olek, N. Hermanowicz, L. G. Hilgenberg, M. A. Smith, S. van den Noort, and Y. Qin. 2006. Triosephosphate isomerase- and glyceraldehyde-3-phosphate dehydrogenase-reactive autoantibodies in the cerebrospinal fluid of patients with multiple sclerosis. J. Immunol. 177: 5652-5658. (Pubitemid 44527641)
8. Sirover, M. A. 1999. New insights into an old protein: the functional diversity of mammalian glyceraldehyde-3-phosphate dehydrogenase. Biochim. Biophys. Acta 1432: 159-184.
9. Kliman, H. J., and T. L. Steck. 1980. Association of glyceraldehyde-3- phosphate dehydrogenase with the human red cell membrane. A kinetic analysis. J. Biol. Chem. 255: 6314-6321.
10. Tsai, I. H., S. N. Murthy, and T. L. Steck. 1982. Effect of red cell membrane binding on the catalytic activity of glyceraldehyde-3-phosphate dehydrogenase. J. Biol. Chem. 257: 1438-1442.
11. Jeffery, C. J. 1999. Moonlighting proteins. Trends Biochem. Sci. 24: 8-11.
12. Kumagai, H., and H. Sakai. 1983. A porcine brain protein (35 K protein) which bundles microtubules and its identification as glyceraldehyde 3-phosphate dehydrogenase. J Biochem 93: 1259-1269.
13. Durrieu, C., F. Bernier-Valentin, and B. Rousset. 1987. Microtubules bind glyceraldehyde 3-phosphate dehydrogenase and modulate its enzyme activity and quaternary structure. Arch. Biochem. Biophys. 252: 32-40.
14. Muronetz, V. I., Z. X. Wang, T. J. Keith, H. R. Knull, and D. K. Srivastava. 1994. Binding constants and stoichiometries of glyceraldehyde 3-phosphate dehydrogenase- tubulin complexes. Arch. Biochem. Biophys. 313: 253-260.
15. Schekman, R., and L. Orci. 1996. Coat proteins and vesicle budding. Science 271: 1526-1533.
16. Nagy, E., and W. F. Rigby. 1995. Glyceraldehyde-3-phosphate dehydrogenase selectively binds AU-rich RNA in the NAD(+)-binding region (Rossmann fold). J. Biol. Chem. 270: 2755-2763.
17. Dastoor, Z., and J. L. Dreyer. 2001. Potential role of nuclear translocation of glyceraldehyde-3-phosphate dehydrogenase in apoptosis and oxidative stress. J. Cell Sci. 114: 1643-1653.
18. Burke, D. 1983. Demyelination in optic neuritis and its effects on the visual evoked potential. Aust. J. Ophthalmol. 11: 341-345.
19. Makhina, T., G. Loers, C. Schulze, B. Ueberle, M. Schachner, and R. Kleene. 2009. Extracellular GAPDH binds to L1 and enhances neurite outgrowth. Mol. Cell. Neurosci. 41: 206-218.
20. Li, Y., P. Nowotny, P. Holmans, S. Smemo, J. S. Kauwe, A. L. Hinrichs, K. Tacey, L. Doil, R. van Luchene, V. Garcia, et al. 2004. Association of late-onset Alzheimer's disease with genetic variation in multiple members of the GAPD gene family. Proc. Natl. Acad. Sci. USA 101: 15688-15693.
21. Hara, M. R., N. Agrawal, S. F. Kim, M. B. Cascio, M. Fujimuro, Y. Ozeki, M. Takahashi, J. H. Cheah, S. K. Tankou, L. D. Hester, et al. 2005. S-nitrosylated GAPDH initiates apoptotic cell death by nuclear translocation following Siah1 binding. Nat. Cell Biol. 7: 665-674.
22. Zhang, Y., R.-R. Da, and W.-Z. Guo, H. M. RenHilgenberg, L. G., R. A. Sobel, W. W. Tourtellotte, M. A. Smith, and M. K. Olek, S. Gupta et al. 2005. Axon reactive B cells clonally expanded in the cerebrospinal fluid of patients with multiple sclerosis. J. Clin. Immunol. 25: 254-264.
23. Zhang, Y., R. R. Da, L. G. Hilgenberg, W. W. Tourtellotte, R. A. Sobel, M. A. Smith, M. Olek, R. Nagra, G. Sudhir, S. van den Noort, and Y. Qin. 2005. Clonal expansion of IgA-positive plasma cells and axon-reactive antibodies in MS lesions. J. Neuroimmunol. 167: 120-130. (Pubitemid 41244805)
24. Blume, K. G., J. C. Kaplan, G. W. Lohr, B. Ramot, and W. N. Valentine, and International Committee for Standardization in Haematology. 1977. Recommended methods for red-cell enzyme analysis. Br. J. Haematol. 35: 331-340.
25. Owens, G. P., H. Kraus, M. P. Burgoon, T. Smith-Jensen, M. E. Devlin, and D. H. Gilden. 1998. Restricted use of VH4 germline segments in an acute multiple sclerosis brain. Ann. Neurol. 43: 236-243.
26. Qin, Y. F., P. Duquette, Y. P. Zhang, P. Talbot, R. Poole, and J. Antel. 1998. Clonal expansion and somatic hypermutation of V(H) genes of B cells from cerebrospinal fluid in multiple sclerosis. J. Clin. Invest. 102: 1045-1050.
27. Baranzini, S. E., M. C. Jeong, C. Butunoi, R. S. Murray, C. C. A. Bernard, and J. R. Oksenberg. 1999. B cell repertoire diversity and clonal expansion in multiple sclerosis brain lesions. J. Immunol. 163: 5133-5144.
28. Colombo, M., M. Dono, P. Gazzola, S. Roncella, A. Valetto, N. Chiorazzi, G. L. Mancardi, and M. Ferrarini. 2000. Accumulation of clonally related B lymphocytes in the cerebrospinal fluid of multiple sclerosis patients. J. Immunol. 164: 2782-2789. (Pubitemid 30115513)
29. Haubold, K., G. P. Owens, P. Kaur, A. M. Ritchie, D. H. Gilden, and J. L. Bennett. 2004. B-lymphocyte and plasma cell clonal expansion in monosymptomatic optic neuritis cerebrospinal fluid. Ann. Neurol. 56: 97-107.
30. Obermeier, B., R. Mentele, J. Malotka, J. Kellermann, T. Kümpfel, H. Wekerle, F. Lottspeich, R. Hohlfeld, and K. Dornmair. 2008. Matching of oligoclonal immunoglobulin transcriptomes and proteomes of cerebrospinal fluid in multiple sclerosis. Nat. Med. 14: 688-693.
31. Qin, Y., and P. Duquette. 2003. B-cell immunity in MS. Int. MS J. 10: 110-120.
32. Shan, D., O. W. Press, T. T. Tsu, M. S. Hayden, and J. A. Ledbetter. 1999. Characterization of scFv-Ig constructs generated from the anti-CD20 mAb 1F5 using linker peptides of varying lengths. J. Immunol. 162: 6589-6595.
33. de Inés, C., B. Cochlovius, S. Schmidt, S. Kipriyanov, H. J. Rode, and M. Little. 1999. Apoptosis of a human melanoma cell line specifically induced by membrane- bound single-chain antibodies. J. Immunol. 163: 3948-3956.
34. Owens, G. P., J. L. Bennett, H. Lassmann, K. C. O'Connor, A. M. Ritchie, A. Shearer, C. Lam, X. Yu, M. Birlea, C. DuPree, et al. 2009. Antibodies produced by clonally expanded plasma cells in multiple sclerosis cerebrospinal fluid. Ann. Neurol. 65: 639-649.
35. Rokitansky. 1846. Handbuch der pathologischen anatornic. Bei Braumuller & Seidel.
36. Charcot. 1846. Lectures on diseases of the nervous system. Bei Braumuller & Seidel, ed. The New Sydenham Society, London.
37. Putnam, T. 1936. Studies in multiple sclerosis. Arch. Neurol. Psychiatry 35: 1289-1308.
38. Greenfield, J., and L. King. 1936. Observations on the histopathology of the cerebral lesions in disseminated sclerosis. Brain 59: 445-458.
39. Davie, C. A., G. J. Barker, S. Webb, P. S. Tofts, A. J. Thompson, A. E. Harding, W. I. McDonald, and D. H. Miller. 1995. Persistent functional deficit in multiple sclerosis and autosomal dominant cerebellar ataxia is associated with axon loss. Brain 118: 1583-1592.
40. Losseff, N. A., S. L. Webb, J. I. O'Riordan, R. Page, L. Wang, G. J. Barker, P. S. Tofts, W. I. McDonald, D. H. Miller, and A. J. Thompson. 1996. Spinal cord atrophy and disability in multiple sclerosis. A new reproducible and sensitive MRI method with potential to monitor disease progression. Brain 119: 701-708.
41. Arnold, D. L., G. T. Riess, P. M. Matthews, G. S. Francis, D. L. Collins, C. Wolfson, and J. P. Antel. 1994. Use of proton magnetic resonance spectroscopy for monitoring disease progression in multiple sclerosis. Ann. Neurol. 36: 76-82.
42. De Stefano, N., P. M. Matthews, J. P. Antel, M. Preul, G. Francis, and D. L. Arnold. 1995. Chemical pathology of acute demyelinating lesions and its correlation with disability. Ann. Neurol. 38: 901-909.
43. Sheline, C. T., and D. W. Choi. 1998. Neuronal death in cultured murine cortical cells is induced by inhibition of GAPDH and triosephosphate isomerase. Neurobiol. Dis. 5: 47-54.
44. Nakazawa, M., T. Uehara, and Y. Nomura. 1997. Koningic acid (a potent glyceraldehyde-3-phosphate dehydrogenase inhibitor)-induced fragmentation and condensation of DNA in NG108-15 cells. J. Neurochem. 68: 2493-2499. (Pubitemid 27218171)
45. Vécsei, L., and E. Pál. 1993. [Current data on the pathogenesis of neurodegenerative diseases and some muscular disorders: therapeutic prospectives]. Orv. Hetil. 134: 1683-1687.
46. Senatorov, V. V., V. Charles, P. H. Reddy, D. A. Tagle, and D. M. Chuang. 2003. Overexpression and nuclear accumulation of glyceraldehyde-3-phosphate dehydrogenase in a transgenic mouse model of Huntington's disease. Mol. Cell. Neurosci. 22: 285-297.
47. Tsuchiya, K., H. Tajima, T. Kuwae, T. Takeshima, T. Nakano, M. Tanaka, K. Sunaga, Y. Fukuhara, K. Nakashima, E. Ohama, et al. 2005. Pro-apoptotic protein glyceraldehyde-3-phosphate dehydrogenase promotes the formation of Lewy body-like inclusions. Eur. J. Neurosci. 21: 317-326.
48. Mazzola, J. L., and M. A. Sirover. 2003. Subcellular alteration of glyceraldehyde-3-phosphate dehydrogenase in Alzheimer's disease fibroblasts. J. Neurosci. Res. 71: 279-285.
49. Du, X., T. Matsumura, D. Edelstein, L. Rossetti, Z. Zsengellér, C. Szabo, and M. Brownlee. 2003. Inhibition of GAPDH activity by poly(ADP-ribose) polymerase activates three major pathways of hyperglycemic damage in endothelial cells. J. Clin. Invest. 112: 1049-1057.
50. Perl, A., and K. Banki. 2000. Genetic and metabolic control of the mitochondrial transmembrane potential and reactive oxygen intermediate production in HIV disease. Antioxid. Redox Signal. 2: 551-573.
51. Smith, K. J., and H. Lassmann. 2002. The role of nitric oxide in multiple sclerosis. Lancet Neurol. 1: 232-241. (Pubitemid 37159185)
52. Dutta, R., J. McDonough, X. Yin, J. Peterson, A. Chang, T. Torres, T. Gudz, W. B. Macklin, D. A. Lewis, R. J. Fox, et al. 2006. Mitochondrial dysfunction as a cause of axonal degeneration in multiple sclerosis patients. Ann. Neurol. 59: 478-489.
53. Chard, D. T., C. M. Griffin, G. J. Parker, R. Kapoor, A. J. Thompson, and D. H. Miller. 2002. Brain atrophy in clinically early relapsing-remitting multiple sclerosis. Brain 125: 327-337.
54. Takasaki, Y., K. Kaneda, M. Matsushita, H. Yamada, M. Nawata, R. Matsudaira, M. Asano, R. Mineki, N. Shindo, and H. Hashimoto. 2004. Glyceraldehyde 3-phosphate dehydrogenase is a novel autoantigen leading autoimmune responses to proliferating cell nuclear antigen multiprotein complexes in lupus patients. Int. Immunol. 16: 1295-1304.
55. Goudot-Crozel, V., D. Caillol, M. Djabali, and A. J. Dessein. 1989. The major parasite surface antigen associated with human resistance to schistosomiasis is a 37-kD glyceraldehyde-3P-dehydrogenase. J. Exp. Med. 170: 2065-2080.
56. Pancholi, V., and V. A. Fischetti. 1993. Glyceraldehyde-3-phosphate dehydrogenase on the surface of group A streptococci is also an ADP-ribosylating enzyme. Proc. Natl. Acad. Sci. USA 90: 8154-8158.
57. Rosinha, G. M., A. Myioshi, V. Azevedo, G. A. Splitter, and S. C. Oliveira. 2002. Molecular and immunological characterisation of recombinant Brucella abortus glyceraldehyde-3-phosphate-dehydrogenase, a T- and B-cell reactive protein that induces partial protection when co-administered with an interleukin-12-expressing plasmid in a DNA vaccine formulation. J. Med. Microbiol. 51: 661-671.
58. Sawcer, S., M. Maranian, E. Setakis, V. Curwen, E. Akesson, A. Hensiek, F. Coraddu, R. Roxburgh, D. Sawcer, J. Gray, et al. 2002. A whole genome screen for linkage disequilibrium in multiple sclerosis confirms disease associations with regions previously linked to susceptibility. Brain 125: 1337-1347. (Pubitemid 34587142)
59. Ebers, G. C., A. D. Sadovnick, N. J. Risch; Canadian Collaborative Study Group. 1995. A genetic basis for familial aggregation in multiple sclerosis. Nature 377: 150-151.
60. Bachmann, S., and J. Kesselring. 1998. Multiple sclerosis and infectious childhood diseases. Neuroepidemiology 17: 154-160. (Pubitemid 28275872)
61. Anderson, A. C., D. E. Anderson, L. Bregoli, W. D. Hastings, N. Kassam, C. Lei, R. Chandwaskar, J. Karman, E. W. Su, M. Hirashima, et al. 2007. Promotion of tissue inflammation by the immune receptor Tim-3 expressed on innate immune cells. Science 318: 1141-1143.
62. Chabas, D., S. E. Baranzini, D. Mitchell, C. C. Bernard, S. R. Rittling, D. T. Denhardt, R. A. Sobel, C. Lock, M. Karpuj, R. Pedotti, et al. 2001. The influence of the proinflammatory cytokine, osteopontin, on autoimmune demyelinating disease. Science 294: 1731-1735.
63. Horikawa, Y., T. Tsubaki, and M. Nakajima. 1973. Rubella antibody in multiple sclerosis. Lancet 1: 996-997.
64. Catalano, L. W., Jr. 1972. Herpesvirus hominis antibody in multiple sclerosis and amyotrophic lateral sclerosis. Neurology 22: 473-478.
65. Giovannoni, G., G. R. Cutter, J. Lunemann, R. Martin, C. Münz, S. Sriram, I. Steiner, M. R. Hammerschlag, and C. A. Gaydos. 2006. Infectious causes of multiple sclerosis. Lancet Neurol. 5: 887-894.
66. Uchibori, A., M. Sakuta, S. Kusunoki, and A. Chiba. 2005. Autoantibodies in postinfectious acute cerebellar ataxia. Neurology 65: 1114-1116. (Pubitemid 41429644)