Human autoantibodies to amphiphysin induce defective presynaptic vesicle dynamics and composition

Brain

Volumn 139, Issue 2, 2016, Pages 365-379

  Werner, Christian ^a,b   Pauli, Martin ^b   Doose, Sören ^b   Weishaupt, Andreas ^b   Haselmann, Holger ^a,b   Grünewald, Benedikt ^a,b   Sauer, Markus ^b   Heckmann, Manfred ^b   Toyka, Klaus V ^b   Asan, Esther ^b   Sommer, Claudia ^b   Geis, Christian ^a,b  

^a JENA UNIVERSITY HOSPITAL   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

amphiphysin; autoantibody; clathrin mediated endocytosis; dSTORM super resolution microscopy; stiff person syndrome

Indexed keywords

AMPHIPHYSIN; AUTOANTIBODY; BREFELDIN A; CLATHRIN; ENDOPHILIN; IMMUNOGLOBULIN G; NEUROTRANSMITTER; SYNAPTOBREVIN; SYNAPTOBREVIN 2; SYNAPTOBREVIN 7; UNCLASSIFIED DRUG; NERVE PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNE DISEASE; CELL MEMBRANE; CENTRAL NERVOUS SYSTEM DISEASE; DISORIENTATION; ELECTRON MICROSCOPY; ENDOCYTOSIS; ENDOSOME; EXOCYTOSIS; FEMALE; GABAERGIC TRANSMISSION; HUMAN; INTERNEURON; MOUSE; NERVE CELL; NERVE ENDING; NEUROTRANSMISSION; NONHUMAN; PALLIATIVE THERAPY; PRIORITY JOURNAL; RAT; SPINAL CORD; SYNAPSE; SYNAPSE VESICLE; SYNAPTOSOME; ANIMAL; BLOOD; C57BL MOUSE; CELL CULTURE; DRUG EFFECTS; INTRASPINAL DRUG ADMINISTRATION; LEWIS RAT; METABOLISM; PREGNANCY; STIFF-PERSON SYNDROME; ULTRASTRUCTURE;

ANIMALS; AUTOANTIBODIES; CELLS, CULTURED; FEMALE; HUMANS; INJECTIONS, SPINAL; MICE; MICE, INBRED C57BL; NERVE TISSUE PROTEINS; NEURONS; PREGNANCY; PRESYNAPTIC TERMINALS; RATS; RATS, INBRED LEW; STIFF-PERSON SYNDROME; SYNAPTIC VESICLES;

EID: 84959917178     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awv324     Document Type: Article

References (56)

1. Andreska T, Aufmkolk S, Sauer M, Blum R. High abundance of BDNF within glutamatergic presynapses of cultured hippocampal neurons. Front Cell Neurosci 2014; 8: 107
2. Arkhipov A, Yin Y, Schulten K. Membrane-bending mechanism of amphiphysin N-BAR domains. Biophys J 2009; 97: 2727-35
3. Boucrot E, Ferreira AP, Almeida-Souza L, Debard S, Vallis Y, Howard G, et al. Endophilin marks and controls a clathrin-independent endocytic pathway. Nature 2015; 517: 460-5
4. Dalakas MC. Stiff person syndrome: advances in pathogenesis and therapeutic interventions. Curr Treat Options Neurol 2009; 11: 102-10
5. Dani A, Huang B, Bergan J, Dulac C, Zhuang X. Superresolution imaging of chemical synapses in the brain. Neuron 2010; 68: 843-56
6. David C, Solimena M, De Camilli P. Autoimmunity in stiff-Man syndrome with breast cancer is targeted to the C-terminal region of human amphiphysin, a protein similar to the yeast proteins, Rvs167 and Rvs161. FEBS Lett 1994; 351: 73-9
7. De Camilli P, Thomas A, Cofiell R, Folli F, Lichte B, Piccolo G, et al. The synaptic vesicle-associated protein amphiphysin is the 128-kD autoantigen of Stiff-Man syndrome with breast cancer. J Exp Med 1993; 178: 2219-23
8. De Jesus-Cortes HJ, Nogueras-Ortiz CJ, Gearing M, Arnold SE, Vega IE. Amphiphysin-1 protein level changes associated with taumediated neurodegeneration. Neuroreport 2012; 23: 942-6
9. Di Paolo G, Sankaranarayanan S, Wenk MR, Daniell L, Perucco E, Caldarone BJ, et al. Decreased synaptic vesicle recycling efficiency and cognitive deficits in amphiphysin 1 knockout. Neuron 2002; 33: 789-804
10. Dong Y, Gou Y, Li Y, Liu Y, Bai J. Synaptojanin cooperates in vivo with endophilin through an unexpected mechanism. Elife 2015; 4
11. Ehmann N, van de Linde S, Alon A, Ljaschenko D, Keung XZ, Holm T, et al. Quantitative super-resolution imaging of Bruchpilot distinguishes active zone states. Nat Commun 2014; 5: 4650
12. Esbjorner EK, Chan F, Rees E, Erdelyi M, Luheshi LM, Bertoncini CW, et al. Direct observations of amyloid beta self-assembly in live cells provide insights into differences in the kinetics of Abeta(1-40) and Abeta(1-42) aggregation. Chem Biol 2014; 21: 732-42
13. Evergren E, Marcucci M, Tomilin N, Low P, Slepnev V, Andersson F, et al. Amphiphysin is a component of clathrin coats formed during synaptic vesicle recycling at the lamprey giant synapse. Traffic 2004; 5: 514-28
14. Faundez V, Horng JT, Kelly RB. A function for the AP3 coat complex in synaptic vesicle formation from endosomes. Cell 1998; 93: 423-32
15. Ferguson SM, Brasnjo G, Hayashi M, Wolfel M, Collesi C, Giovedi S, et al. A selective activity-dependent requirement for dynamin 1 in synaptic vesicle endocytosis. Science 2007; 316: 570-4
16. Geis C, Grunewald B, Weishaupt A, Wultsch T, Toyka KV, Reif A, et al. Human IgG directed against amphiphysin induces anxiety behavior in a rat model after intrathecal passive transfer. J Neural Transm 2012; 119: 981-5
17. Geis C, Weishaupt A, Hallermann S, Grunewald B, Wessig C, Wultsch T, et al. Stiff person syndrome-associated autoantibodies to amphiphysin mediate reduced GABAergic inhibition. Brain 2010; 133: 3166-80
18. Gleichman AJ, Spruce LA, Dalmau J, Seeholzer SH, Lynch DR. Anti-NMDA receptor encephalitis antibody binding is dependent on amino acid identity of a small region within the GluN1 amino terminal domain. J Neurosci 2012; 32: 11082-94
19. Grabs D, Slepnev VI, Songyang Z, David C, Lynch M, Cantley LC, et al. The SH3 domain of amphiphysin binds the proline-rich domain of dynamin at a single site that defines a new SH3 binding consensus sequence. J Biol Chem 1997; 272: 13419-25
20. Hua Z, Leal-Ortiz S, Foss SM, Waites CL, Garner CC, Voglmaier SM, et al. v-SNARE composition distinguishes synaptic vesicle pools. Neuron 2011; 71: 474-87
21. Irani SR, Gelfand JM, Al-Diwani A, Vincent A. Cell-surface central nervous system autoantibodies: clinical relevance and emerging paradigms. Ann Neurol 2014; 76: 168-84
22. Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG. Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol 2010; 8: e1000412
23. Kim SH, Ryan TA. A distributed set of interactions controls mu2 functionality in the role of AP-2 as a sorting adaptor in synaptic vesicle endocytosis. J Biol Chem 2009; 284: 32803-12
24. Kittelmann M, Liewald JF, Hegermann J, Schultheis C, Brauner M, Steuer Costa W, et al. In vivo synaptic recovery following optogenetic hyperstimulation. Proc Natl Acad Sci USA 2013; 110: E3007-16
25. Koo SJ, Markovic S, Puchkov D, Mahrenholz CC, Beceren-Braun F, Maritzen T, et al. SNARE motif-mediated sorting of synaptobrevin by the endocytic adaptors clathrin assembly lymphoid myeloid leukemia (CALM) and AP180 at synapses. Proc Natl Acad Sci USA 2011; 108: 13540-5
26. Lai M, Hughes EG, Peng X, Zhou L, Gleichman AJ, Shu H, et al. AMPA receptor antibodies in limbic encephalitis alter synaptic receptor location. Ann Neurol 2009; 65: 424-34
27. Leypoldt F, Armangue T, Dalmau J. Autoimmune encephalopathies. Ann N Y Acad Sci 2015; 1338: 94-114
28. Lichte B, Veh RW, Meyer HE, Kilimann MW. Amphiphysin, a novel protein associated with synaptic vesicles. EMBO J 1992; 11: 2521-30
29. Llobet A, Gallop JL, Burden JJ, Camdere G, Chandra P, Vallis Y, et al. Endophilin drives the fast mode of vesicle retrieval in a ribbon synapse. J Neurosci 2011; 31: 8512-9
30. Macia E, Ehrlich M, Massol R, Boucrot E, Brunner C, Kirchhausen T. Dynasore, a cell-permeable inhibitor of dynamin. Dev Cell 2006; 10: 839-50
31. Meinck HM, Faber L, Morgenthaler N, Seissler J, Maile S, Butler M, et al. Antibodies against glutamic acid decarboxylase: prevalence in neurological diseases. J Neurol Neurosurg Psychiatry 2001; 71: 100-3
32. Micheva KD, Ramjaun AR, Kay BK, McPherson PS. SH3 domaindependent interactions of endophilin with amphiphysin. FEBS Lett 1997; 414: 308-12
33. Milosevic I, Giovedi S, Lou X, Raimondi A, Collesi C, Shen H, et al. Recruitment of endophilin to clathrin-coated pit necks is required for efficient vesicle uncoating after fission. Neuron 2011; 72: 587-601
34. Murinson BB. Stiff-person syndrome. Neurologist 2004; 10: 131-7
35. Raimondi A, Ferguson SM, Lou X, Armbruster M, Paradise S, Giovedi S, et al. Overlapping role of dynamin isoforms in synaptic vesicle endocytosis. Neuron 2011; 70: 1100-14
36. Ranson RN, Santer RM, Watson AH. The relationship between serotonin, dopamine beta hydroxylase and GABA immunoreactive inputs and spinal preganglionic neurones projecting to the major pelvic ganglion of Wistar rats. Neuroscience 2006; 141: 1935-49
37. Reynolds ES. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 1963; 17: 208-12
38. Sandbrink F, Syed NA, Fujii MD, Dalakas MC, Floeter MK. Motor cortex excitability in stiff-person syndrome. Brain 2000; 123 (Pt 11): 2231-9
39. Shetty A, Sytnyk V, Leshchyns'ka I, Puchkov D, Haucke V, Schachner M. The neural cell adhesion molecule promotes maturation of the presynaptic endocytotic machinery by switching synaptic vesicle recycling from adaptor protein 3 (AP-3)-to AP-2-dependent mechanisms. J Neurosci 2013; 33: 16828-45
40. Shupliakov O, Low P, Grabs D, Gad H, Chen H, David C, et al. Synaptic vesicle endocytosis impaired by disruption of dynamin-SH3 domain interactions. Science 1997; 276: 259-63
41. Soda K, Balkin DM, Ferguson SM, Paradise S, Milosevic I, Giovedi S, et al. Role of dynamin, synaptojanin, and endophilin in podocyte foot processes. J Clin Invest 2012; 122: 4401-11
42. Sommer C, Weishaupt A, Brinkhoff J, Biko L, Wessig C, Gold R, et al. Paraneoplastic stiff-person syndrome: passive transfer to rats by means of IgG antibodies to amphiphysin. Lancet 2005; 365: 1406-11
43. Somogyi J. Differences in ratios of GABA, glycine and glutamate immunoreactivities in nerve terminals on rat hindlimb motoneurons: a possible source of post-synaptic variability. Brain Res Bull 2002; 59: 151-61
44. Takamori S, Holt M, Stenius K, Lemke EA, Gronborg M, Riedel D, et al. Molecular anatomy of a trafficking organelle. Cell 2006; 127: 831-46
45. Takei K, Mundigl O, Daniell L, De Camilli P. The synaptic vesicle cycle: a single vesicle budding step involving clathrin and dynamin. J Cell Biol 1996; 133: 1237-50
46. Trempe JF, Chen CX, Grenier K, Camacho EM, Kozlov G, McPherson PS, et al. SH3 domains from a subset of BAR proteins define a Ubl-binding domain and implicate parkin in synaptic ubiquitination. Mol Cell 2009; 36: 1034-47
47. Vasconcelos OM, Dalakas MC. Stiff-person Syndrome. Curr Treat Options Neurol 2003; 5: 79-90
48. Voglmaier SM, Edwards RH. Do different endocytic pathways make different synaptic vesicles? Curr Opin Neurobiol 2007; 17: 374-80
49. Voglmaier SM, Kam K, Yang H, Fortin DL, Hua Z, Nicoll RA, et al. Distinct endocytic pathways control the rate and extent of synaptic vesicle protein recycling. Neuron 2006; 51: 71-84
50. von Kleist L, Stahlschmidt W, Bulut H, Gromova K, Puchkov D, Robertson MJ, et al. Role of the clathrin terminal domain in regulating coated pit dynamics revealed by small molecule inhibition. Cell 2011; 146: 471-84
51. Watanabe S, Rost BR, Camacho-Perez M, Davis MW, Sohl-Kielczynski B, Rosenmund C, et al. Ultrafast endocytosis at mouse hippocampal synapses. Nature 2013; 504: 242-7
52. Watson AH, Bazzaz AA. GABA and glycine-like immunoreactivity at axoaxonic synapses on 1a muscle afferent terminals in the spinal cord of the rat. J Comp Neurol 2001; 433: 335-48
53. Weinberg RJ, van Eyck SL. A tetramethylbenzidine/tungstate reaction for horseradish peroxidase histochemistry. J Histochem Cytochem 1991; 39: 1143-8
54. Werner C, Haselmann H, Weishaupt A, Toyka KV, Sommer C, Geis C. Stiff person-syndrome IgG affects presynaptic GABAergic release mechanisms. J Neural Transm 2015; 122: 357-62
55. Wessig C, Klein R, Schneider MF, Toyka KV, Naumann M, Sommer C. Neuropathology and binding studies in anti-amphiphysinassociated stiff-person syndrome. Neurology 2003; 61: 195-8
56. Wolter S, Loschberger A, Holm T, Aufmkolk S, Dabauvalle MC, van de Linde S, et al. rapidSTORM: accurate, fast open-source software for localization microscopy. Nat Methods 2012; 9: 1040-1.