A natural human IgM that binds to gangliosides is therapeutic in murine models of amyotrophic lateral sclerosis

DMM Disease Models and Mechanisms

Volumn 8, Issue 8, 2015, Pages 831-842

  Xu, Xiaohua ^a   Denic, Aleksandar ^a   Jordan, Luke R ^b   Wittenberg, Nathan J ^b   Warrington, Arthur E ^a   Wootla, Bharath ^a   Papke, Louisa M ^a   Zoecklein, Laurie J ^a   Yoo, Daehan ^b   Shaver, Jonah ^b   Oh, Sang Hyun ^b   Pease, Larry R ^a   Rodriguez, Moses ^a  

^a MAYO CLINIC   (United States)

^b University of Minnesota   (United States)

Author keywords

ALS; Amyotrophic lateral sclerosis; Axon growth; Gangliosides; GD1a; GT1b; Neurite extension; Neuroprotection; SOD1; SPR; Supported lipid bilayers; Surface plasmon resonance

Indexed keywords

ALPHA TUBULIN; GANGLIOSIDE GD 1A; GANGLIOSIDE GT 1B; IMMUNOGLOBULIN M; RECOMBINANT HUMAN IMMUNOGLOBULIN M 12; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; EPITOPE; GANGLIOSIDE; GANGLIOSIDE, GD1A; LIPID BILAYER; PROTEIN BINDING; SUPEROXIDE DISMUTASE; TRISIALOGANGLIOSIDE GT1; TUBULIN;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DEMYELINATION; DRUG USE; FEMALE; HUMAN; MALE; MICROTUBULE; MOUSE; MSOD1 MOUSE; NEURITE; NONHUMAN; PRIORITY JOURNAL; SINGLE DRUG DOSE; SPINAL CORD NERVE CELL; SPINAL CORD VENTRAL HORN; SURFACE PLASMON RESONANCE; THIN LAYER CHROMATOGRAPHY; WEIGHT REDUCTION; ANIMAL; CELL LINE; CHEMISTRY; DISEASE COURSE; DISEASE MODEL; DOSE RESPONSE; IMMUNOLOGY; LIPID BILAYER; METABOLISM; MOLECULAR MODEL; PATHOLOGY; SOLUBILITY; SPINAL CORD; SURVIVAL ANALYSIS; TRANSGENIC MOUSE;

MURINAE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; CELL LINE; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; DOSE-RESPONSE RELATIONSHIP, IMMUNOLOGIC; EPITOPES; GANGLIOSIDES; HUMANS; IMMUNOGLOBULIN M; LIPID BILAYERS; MICE; MICE, TRANSGENIC; MICROTUBULES; MODELS, MOLECULAR; NEURITES; PROTEIN BINDING; RECOMBINANT PROTEINS; SOLUBILITY; SPINAL CORD; SUPEROXIDE DISMUTASE; SURFACE PLASMON RESONANCE; SURVIVAL ANALYSIS; TUBULIN;

EID: 84939552007     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.020727     Document Type: Article

References (66)

1. Advokat, C. and Gulati, A. (1991). Spinal transection reduces both spinal antinociception and CNS concentration of systemically administered morphine in rats. Brain Res. 555, 251-258.
2. Axelrod, D. , Koppel, D. E. , Schlessinger, J. , Elson, E. and Webb, W. W. (1976). Mobility measurement by analysis of fluorescence photobleaching recovery kinetics. Biophys. J. 16, 1055-1069.
3. Banks, W. A. , Ortiz, L. , Plotkin, S. R. and Kastin, A. J. (1991). Human interleukin (IL) 1 alpha, murine IL-1 alpha and murine IL-1 beta are transported from blood to brain in the mouse by a shared saturable mechanism. J. Pharmacol. Exp. Ther. 259, 988-996.
4. Banks, W. A. , Terrell, B. , Farr, S. A. , Robinson, S. M. , Nonaka, N. and Morley, J. E. (2002). Passage of amyloid beta protein antibody across the blood-brain barrier in a mouse model of Alzheimer's disease. Peptides 23, 2223-2226.
5. Banks, W. A. , Farr, S. A. , Morley, J. E. , Wolf, K. M. , Geylis, V. and Steinitz, M. (2007). Anti-amyloid beta protein antibody passage across the blood-brain barrier in the SAMP8 mouse model of Alzheimer's disease: An age-related selective uptake with reversal of learning impairment. Exp. Neurol. 206, 248-256.
6. Bosco, D. A. , Morfini, G. , Karabacak, N. M. , Song, Y. , Gros-Louis, F. , Pasinelli, P. , Goolsby, H. , Fontaine, B. A. , Lemay, N. , McKenna-Yasek, D. et al. (2010). Wild-type and mutant SOD1 share an aberrant conformation and a common pathogenic pathway in ALS. Nat. Neurosci. 13, 1396-1403.
7. Brolo, A. G. , Gordon, R. , Leathem, B. and Kavanagh, K. L. (2004). Surface plasmon sensor based on the enhanced light transmission through arrays of nanoholes in gold films. Langmuir 20, 4813-4815.
8. Bruijn, L. I. , Miller, T. M. and Cleveland, D. W. (2004). Unraveling themechanisms involved in motor neuron degeneration in ALS. Annu. Rev. Neurosci. 27, 723-749.
9. Cantù, L. , Del Favero, E. , Sonnino, S. and Prinetti, A. (2011). Gangliosides and the multiscale modulation of membrane structure. Chem. Phys. Lipids 164, 796-810.
10. Ciric, B. , VanKeulen, V. , Rodriguez, M. , Kyle, R. A. , Gertz, M. A. and Pease, L. R. (2001). Clonal evolution in Waldenstrom macroglobulinemia highlights functional role of B-cell receptor. Blood 97, 321-323.
11. Cluskey, S. and Ramsden, D. B. (2001). Mechanisms of neurodegeneration in amyotrophic lateral sclerosis. Mol. Pathol. 54, 386-392.
12. Cooper, M. A. and Williams, D. H. (1999). Kinetic analysis of antibody-antigen interactions at a supported lipid monolayer. Anal. Biochem. 276, 36-47.
13. Crothers, D. M. and Metzger, H. (1972). The influence of polyvalency on the binding properties of antibodies. Immunochemistry 9, 341-357.
14. Dahlin, A. , Zäch, M. , Rindzevicius, T. , Käll, M. , Sutherland, D. S. and Höök, F. (2005). Localized surface plasmon resonance sensing of lipid-membranemediated biorecognition events. J. Am. Chem. Soc. 127, 5043-5048.
15. Denic, A. , Macura, S. I. , Warrington, A. E. , Pirko, I. , Grossardt, B. R. , Pease, L. R. and Rodriguez, M. (2011). A single dose of neuron-binding human monoclonal antibody improves spontaneous activity in a murine model of demyelination. PLoS ONE 6, e26001.
16. Fujitani, M. , Kawai, H. , Proia, R. L. , Kashiwagi, A. , Yasuda, H. and Yamashita, T. (2005). Binding of soluble myelin-associated glycoprotein to specific gangliosides induces the association of p75NTR to lipid rafts and signal transduction. J. Neurochem. 94, 15-21.
17. Gill, D. M. and King, C. A. (1975). The mechanism of action of cholera toxin in pigeon erythrocyte lysates. J. Biol. Chem. 250, 6424-6432.
18. Gold, M. , Pul, R. , Bach, J.-P. , Stangel, M. and Dodel, R. (2012). Pathogenic and physiological autoantibodies in the central nervous system. Immunol. Rev. 248, 68-86.
19. Gros-Louis, F. , Soucy, G. , Lariviere, R. and Julien, J. P. (2010). Intracerebroventricular infusion of monoclonal antibody or its derived Fab fragment against misfolded forms of SOD1 mutant delays mortality in a mouse model of ALS. J. Neurochem. 113, 1188-1199.
20. Gurney, M. E. , Fleck, T. J. , Himes, C. S. and Hall, E. D. (1998). Riluzole preserves motor function in a transgenic model of familial amyotrophic lateral sclerosis. Neurology 50, 62-66.
21. Hunter, S. F. , Leavitt, J. A. and Rodriguez, M. (1997). Direct observation of myelination in vivo in the mature human central nervous system. A model for the behaviour of oligodendrocyte progenitors and their progeny. Brain 120, 2071-2082.
22. Im, H. , Wittenberg, N. J. , Lesuffleur, A. , Lindquist, N. C. and Oh, S.-H. (2010). Membrane protein biosensing with plasmonic nanopore arrays and porespanning lipid membranes. Chem. Sci. 1, 688-696.
23. Im, H. , Lee, S. H. , Wittenberg, N. J. , Johnson, T. W. , Lindquist, N. C. , Nagpal, P. , Norris, D. J. and Oh, S.-H. (2011). Template-stripped smooth Ag nanohole arrays with silica shells for surface plasmon resonance biosensing. ACS Nano 5, 6244-6253.
24. Im, H. , Wittenberg, N. J. , Lindquist, N. C. and Oh, S.-H. (2012). Atomic layer deposition (ALD): A versatile technique for plasmonics and nanobiotechnology. J. Mater. Res. 27, 663-671.
25. Iwamori, M. , Ohta, Y. , Uchida, Y. and Tsukada, Y. (1997). Arthrobacter ureafaciens sialidase isoenzymes, L, M1 and M2, cleave fucosyl GM1. Glycoconj. J. 14, 67-73.
26. Jagust, W. (2013). Vulnerable neural systems and the borderland of brain aging and neurodegeneration. Neuron 77, 219-234.
27. Jönsson, P. , Jonsson, M. P. , Tegenfeldt, J. O. and Höök, F. (2008). A method improving the accuracy of fluorescence recovery after photobleaching analysis. Biophys. J. 95, 5334-5348.
28. Koval, E. D. , Shaner, C. , Zhang, P. , du Maine, X. , Fischer, K. , Tay, J. , Chau, B. N. , Wu, G. F. and Miller, T. M. (2013). Method for widespread microRNA-155 inhibition prolongs survival in ALS-model mice. Hum. Mol. Genet. 22, 4127-4135.
29. Kozlowski, G. P. , Sterzl, I. and Nilaver, G. (1992). Localization patterns for immunoglobulins and albumins in the brain suggest diverse mechanisms for their transport across the blood-brain barrier (BBB). Prog. Brain Res. 91, 149-154.
30. Kuziemko, G. M. , Stroh, M. and Stevens, R. C. (1996). Cholera toxin binding affinity and specificity for gangliosides determined by surface plasmon resonance. Biochemistry 35, 6375-6384.
31. Lincecum, J. M. , Vieira, F. G. , Wang, M. Z. , Thompson, K. , De Zutter, G. S. , Kidd, J. , Moreno, A. , Sanchez, R. , Carrion, I. J. , Levine, B. A. et al. (2010). From transcriptome analysis to therapeutic anti-CD40L treatment in the SOD1 model of amyotrophic lateral sclerosis. Nat. Genet. 42, 392-399.
32. Loberto, N. , Prioni, S. , Prinetti, A. , Ottico, E. , Chigorno, V. , Karagogeos, D. and Sonnino, S. (2003). The adhesion protein TAG-1 has a ganglioside environment in the sphingolipid-enriched membrane domains of neuronal cells in culture. J. Neurochem. 85, 224-233.
33. Ludolph, A. G. , Udvardi, P. T. , Schaz, U. , Henes, C. , Adolph, O. , Weigt, H. U. , Fegert, J. M. , Boeckers, T. M. and Föhr, K. J. (2010). Atomoxetine acts as an NMDA receptor blocker in clinically relevant concentrations. Br. J. Pharmacol. 160, 283-291.
34. Lutz, H. U. , Binder, C. J. and Kaveri, S. (2009). Naturally occurring auto-antibodies in homeostasis and disease. Trends Immunol. 30, 43-51.
35. McGoldrick, P. , Joyce, P. I. , Fisher, E. M. C. and Greensmith, L. (2013). Rodent models of amyotrophic lateral sclerosis. Biochim. Biophys. Acta 1832, 1421-1436.
36. Mitsunaga, Y. , Ciric, B. , Van Keulen, V. , Warrington, A. E. , Paz Soldan, M. M. , Bieber, A. J. , Rodriguez, M. and Pease, L. R. (2002). Direct evidence that a human antibody derived from patient serum can promote myelin repair in a mouse model of chronic-progressive demyelinating disease. FASEB J. 16, 1325-1327.
37. Morrison, B. M. and Morrison, J. H. (1999). Amyotrophic lateral sclerosis associated with mutations in superoxide dismutase: A putative mechanism of degeneration. Brain Res. Brain Res. Rev. 29, 121-135.
38. Morrison, B. M. , Janssen, W. G. , Gordon, J. W. and Morrison, J. H. (1998). Time course of neuropathology in the spinal cord of G86R superoxide dismutase transgenic mice. J. Comp. Neurol. 391, 64-77.
39. Nagpal, P. , Lindquist, N. C. , Oh, S.-H. and Norris, D. J. (2009). Ultrasmooth patterned metals for plasmonics and metamaterials. Science 325, 594-597.
40. Nguyen, T. , Mehta, N. R. , Conant, K. , Kim, K.-J. , Jones, M. , Calabresi, P. A. , Melli, G. , Hoke, A. , Schnaar, R. L. , Ming, G.-L. et al. (2009). Axonal protective effects of the myelin-associated glycoprotein. J. Neurosci. 29, 630-637.
41. Palestini, P. , Pitto, M. , Tedeschi, G. , Ferraretto, A. , Parenti, M. , Brunner, J. and Masserini, M. (2000). Tubulin anchoring to glycolipid-enriched, detergentresistant domains of the neuronal plasma membrane. J. Biol. Chem. 275, 9978-9985.
42. Pan, B. , Fromholt, S. E. , Hess, E. J. , Crawford, T. O. , Griffin, J. W. , Sheikh, K. A. and Schnaar, R. L. (2005). Myelin-associated glycoprotein and complementary axonal ligands, gangliosides, mediate axon stability in the CNS and PNS: Neuropathology and behavioral deficits in single-and double-null mice. Exp. Neurol. 195, 208-217.
43. Pepinsky, R. B. , Shao, Z. , Ji, B. , Wang, Q. , Meng, G. , Walus, L. , Lee, X. , Hu, Y. , Graff, C. , Garber, E. et al. (2011). Exposure levels of anti-LINGO-1 Li81 antibody in the central nervous system and dose-efficacy relationships in rat spinal cord remyelination models after systemic administration. J. Pharmacol. Exp. Ther. 339, 519-529.
44. Pirko, I. , Ciric, B. , Gamez, J. , Bieber, A. J. , Warrington, A. E. , Johnson, A. J. , Hanson, D. P. , Pease, L. R. , Macura, S. I. and Rodriguez, M. (2004). A human antibody that promotes remyelination enters the CNS and decreases lesion load as detected by T2-weighted spinal cord MRI in a virus-induced murine model of MS. FASEB J. 18, 1577-1579.
45. Reiber, H. and Peter, J. B. (2001). Cerebrospinal fluid analysis: Disease-related data patterns and evaluation programs. J. Neurol. Sci. 184, 101-122.
46. Ripps, M. E. , Huntley, G. W. , Hof, P. R. , Morrison, J. H. and Gordon, J. W. (1995). Transgenic mice expressing an altered murine superoxide dismutase gene provide an animal model of amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. USA 92, 689-693.
47. Rodriguez, M. , Warrington, A. E. and Pease, L. R. (2009). Invited article: Human natural autoantibodies in the treatment of neurologic disease. Neurology 72, 1269-1276.
48. Saito, M. , Kitamura, H. and Sugiyama, K. (2001). The specificity of monoclonal antibody A2B5 to c-series gangliosides. J. Neurochem. 78, 64-74.
49. Schnaar, R. L. and Lopez, P. H. H. (2009). Myelin-associated glycoprotein and its axonal receptors. J. Neurosci. Res. 87, 3267-3276.
50. Scott, S. , Kranz, J. E. , Cole, J. , Lincecum, J. M. , Thompson, K. , Kelly, N. , Bostrom, A. , Theodoss, J. , Al-Nakhala, B. M. , Vieira, F. G. et al. (2008). Design, power, and interpretation of studies in the standard murine model of ALS. Amyotroph. Lateral Scler. 9, 4-15.
51. Sheikh, K. A. , Sun, J. , Liu, Y. , Kawai, H. , Crawford, T. O. , Proia, R. L. , Griffin, J. W. and Schnaar, R. L. (1999). Mice lacking complex gangliosides develop Wallerian degeneration and myelination defects. Proc. Natl. Acad. Sci. USA 96, 7532-7537.
52. Sonnino, S. , Mauri, L. , Ciampa, M. G. and Prinetti, A. (2013). Gangliosides as regulators of cell signaling: Ganglioside-protein interactions or ganglioside-driven membrane organization? J. Neurochem. 124, 432-435.
53. Sreedharan, J. and Brown, R. H. , Jr. , (2013). Amyotrophic lateral sclerosis: Problems and prospects. Ann. Neurol. 74, 309-316.
54. Stewart, A. , Sandercock, J. , Bryan, S. , Hyde, C. , Barton, P. M. , Fry-Smith, A. and Burls, A. (2001). The clinical effectiveness and cost-effectiveness of riluzole for motor neurone disease: A rapid and systematic review. Health Technol. Assess. 5, 1-97.
55. Tamm, L. K. and McConnell, H. M. (1985). Supported phospholipid bilayers. Biophys. J. 47, 105-113.
56. Tu, P. H. , Raju, P. , Robinson, K. A. , Gurney, M. E. , Trojanowski, J. Q. and Lee, V. M. (1996). Transgenic mice carrying a human mutant superoxide dismutase transgene develop neuronal cytoskeletal pathology resembling human amyotrophic lateral sclerosis lesions. Proc. Natl. Acad. Sci. USA 93, 3155-3160.
57. Turner, B. J. and Talbot, K. (2008). Transgenics, toxicity and therapeutics in rodent models of mutant SOD1-mediated familial ALS. Prog. Neurobiol. 85, 94-134.
58. Vinson, M. , Rausch, O. , Maycox, P. R. , Prinjha, R. K. , Chapman, D. , Morrow, R. , Harper, A. J. , Dingwall, C. , Walsh, F. S. , Burbidge, S. A. et al. (2003). Lipid rafts mediate the interaction between myelin-associated glycoprotein (MAG) on myelin and MAG-receptors on neurons. Mol. Cell. Neurosci. 22, 344-352.
59. Vyas, A. A. , Patel, H. V. , Fromholt, S. E. , Heffer-Lauc, M. , Vyas, K. A. , Dang, J. , Schachner, M. and Schnaar, R. L. (2002). Gangliosides are functional nerve cell ligands for myelin-associated glycoprotein (MAG), an inhibitor of nerve regeneration. Proc. Natl. Acad. Sci. USA 99, 8412-8417.
60. Warrington, A. E. , Asakura, K. , Bieber, A. J. , Ciric, B. , Van Keulen, V. , Kaveri, S. V. , Kyle, R. A. , Pease, L. R. and Rodriguez, M. (2000). Human monoclonal antibodies reactive to oligodendrocytes promote remyelination in a model of multiple sclerosis. Proc. Natl. Acad. Sci. USA 97, 6820-6825.
61. Warrington, A. E. , Bieber, A. J. , Van Keulen, V. , Ciric, B. , Pease, L. R. and Rodriguez, M. (2004). Neuron-binding human monoclonal antibodies support central nervous system neurite extension. J. Neuropathol. Exp. Neurol. 63, 461-473.
62. Wittenberg, N. J. , Im, H. , Xu, X. , Wootla, B. , Watzlawik, J. , Warrington, A. E. , Rodriguez, M. and Oh, S.-H. (2012). High-affinity binding of remyelinating natural autoantibodies to myelin-mimicking lipid bilayers revealed by nanohole surface plasmon resonance. Anal. Chem. 84, 6031-6039.
63. Wright, B. R. , Warrington, A. E. , Edberg, D. D. and Rodriguez, M. (2009). Cellular mechanisms of central nervous system repair by natural autoreactive monoclonal antibodies. Arch. Neurol. 66, 1456-1459.
64. Xu, X. , Warrington, A. E. , Bieber, A. J. and Rodriguez, M. (2011a). Enhancing CNS repair in neurological disease: Challenges arising from neurodegeneration and rewiring of the network. CNS Drugs 25, 555-573.
65. Xu, X. , Warrington, A. E. , Wright, B. R. , Bieber, A. J. , Van Keulen, V. , Pease, L. R. and Rodriguez, M. (2011b). A human IgM signals axon outgrowth: Coupling lipid raft to microtubules. J. Neurochem. 119, 100-112.
66. Yang, T. , Jung, S.-Y. , Mao, H. and Cremer, P. S. (2001). Fabrication of phospholipid bilayer-coated microchannels for on-chip immunoassays. Anal. Chem. 73, 165-169.