Alpha-B-crystallin induces an immune-regulatory and antiviral microglial response in preactive multiple sclerosis lesions

Journal of Neuropathology and Experimental Neurology

Volumn 72, Issue 10, 2013, Pages 970-979

  Bsibsi, Malika ^a   Holtman, Inge R ^b   Gerritsen, Wouter H ^c   Eggen, Bart J L ^b   Boddeke, Erik ^b   Van Der Valk, Paul ^c   Van Noort, Johannes M ^a   Amor, Sandra ^c,d  

^a Delta Crystallon BV   (Netherlands)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^c VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^d QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Alpha B crystallin; Microglia; Multiple sclerosis; Oligodendrocytes; Preactive MS lesions

Indexed keywords

CD14 ANTIGEN; CHEMOKINE; HEAT SHOCK PROTEIN ALPHA B CRYSTALLIN; INTERFERON; SMALL HEAT SHOCK PROTEIN; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 2; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; GENETIC TRANSCRIPTION; GENOME; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN TISSUE; IMMUNOREGULATION; MALE; MICROGLIA; MULTIPLE SCLEROSIS; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION;

AGED; AGED, 80 AND OVER; ALPHA-CRYSTALLIN B CHAIN; ANTIGENS, CD14; AXONS; BRAIN; FEMALE; HUMANS; MALE; MICROGLIA; MIDDLE AGED; MULTIPLE SCLEROSIS; NERVE FIBERS, MYELINATED; TOLL-LIKE RECEPTOR 1; TOLL-LIKE RECEPTOR 2;

EID: 84885031543     PISSN: 00223069     EISSN: 15546578     Source Type: Journal    
DOI: 10.1097/NEN.0b013e3182a776bf     Document Type: Article

References (51)

1. Filippi M, Rocca MA, Barkhof F, et al. Association between pathological and MRI findings in multiple sclerosis. Lancet Neurol 2012;11:349-60
2. Miller DH, Thompson AJ, Filippi M. Magnetic resonance studies of abnormalities in the normal appearing white matter and grey matter in multiple sclerosis. J Neurol 2003;250:1407-19 (Pubitemid 38121836)
3. Banati RB, Newcombe J, Gunn RN, et al. The peripheral benzodiazepine binding site in the brain in multiple sclerosis: Quantitative in vivo imaging of microglia as a measure of disease activity. Brain 2000;123: 2321-27
4. Moll NM, Rietsch AM, Thomas S, et al. Multiple sclerosis normal-appearing white matter: Pathology-imaging correlations. Ann Neurol 2011;70:764-73
5. Van der Valk P, Amor S. Preactive lesions in multiple sclerosis. Curr Opin Neurol 2009;22:207-13
6. Sanders V, Conrad AJ, TourtellotteWW. On classification of post-mortem multiple sclerosis plaques for neuroscientists. J Neuroimmunol 1993;46: 207-16 (Pubitemid 23284267)
7. Gay FW, Drye TJ, Dick GW, et al. The application of multifactorial cluster analysis in the staging of plaques in early multiple sclerosis. Identification and characterization of the primary demyelinating lesion. Brain 1997;120:1461-83
8. De Groot CJ, Bergers E, Kamphorst W, et al. Postmortem MRI-guided sampling of multiple sclerosis brain lesions: Increased yield of active demyelinating and (p)reactive lesions. Brain 2001;124:1635-45 (Pubitemid 32726776)
9. Barnett MH, Prineas JW. Relapsing and remitting multiple sclerosis: Pathology of the newly forming lesion. Ann Neurol 2004;55:458-68 (Pubitemid 38391962)
10. Marik C, Felts PA, Bauer J, et al. Lesion genesis in a subset of patients with multiple sclerosis: A role for innate immunity? Brain 2007;130: 2800-15 (Pubitemid 350033973)
11. Haider L, Fischer MT, Frischer JM, et al. Oxidative damage in multiple sclerosis lesions. Brain 2011;134:1914-24
12. Singh S, Metz I, Amor S, et al. Microglial nodules in early multiple sclerosis white matter are associated with degenerating axons. Acta Neuropathol 2013;125:595-608
13. Van Noort JM, BsibsiM, GerritsenWH, et al. Alpha B-crystallin is a target for adaptive immune responses and a trigger of innate responses in preactive multiple sclerosis lesions. J Neuropathol Exp Neurol 2010;69: 694-703
14. Van Noort JM, Bsibsi M, Nacken PJ, et al. Activation of an immune-regulatory macrophage response and inhibition of lung inflammation in a mouse model of COPD using heat-shock protein alpha B-crystallinYloaded PLGA microparticles. Biomaterials 2013;34:831-40
15. Bsibsi M, Ravid R, Gveric D, et al. Broad expression of Toll-like receptors in the human central nervous system. J Neuropathol Exp Neurol 2002;61:1013-21 (Pubitemid 35278723)
16. R Development Core Team. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing 2011.
17. Smyth GK. Limma: Linear models for microarray data. In: Bioinformatics and Computational Biology Solutions Using R and Bioconductor. Gentleman R, Carey V, Dudoit S, et al., eds. New York, NY: Springer, 2005:397-420
18. Ritchie ME, Silver J, Oshlack A, et al. A comparison of background correction methods for two-colour microarrays. Bioinformatics 2007;23: 2700-7 (Pubitemid 350048334)
19. Ritchie ME, Diyagama D, Neilson J, et al. Empirical array quality weights in the analysis of microarray data. BMC Bioinformatics 2006;7:261
20. Benjamini Y, Hochberg Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J Royal Statist Soc Series B 1995;57:289-300
21. Veenstra M, Ransohoff RM. Chemokine receptor CXCR2: Physiology regulator and neuroinflammation controller? J Neuroimmunol 2012;246:1-9
22. VanWeering HR, Boddeke HW, Vinet J, et al. CXCL10/CXCR3 signaling in glia cells differentially affects NMDA-induced cell death in CA and DG neurons of the mouse hippocampus. Hippocampus 2011;21:220-32
23. Olah M, Amor S, Brouwer N, et al. Identification of a microglia phenotype supportive of remyelination. Glia 2012;60:306-21
24. Sabat R, GrützG, Warszawska K, et al. Biology of interleukin-10. Cytokine Growth Factor Rev 2010;21:331-44
25. Fife BT, Pauken KE. The role of the PD-1 pathway in autoimmunity and peripheral tolerance. Ann N Y Acad Sci 2011;1217:45-59
26. Milner CM, Higman VA, Day AJ. TSG-6: A pluripotent inflammatory mediator? Biochem Soc Trans 2006;34:446-550
27. Ma A, Malynn BA. A20: Linking a complex regulator of ubiquitylation to immunity and human disease. Nat Rev Immunol. 2012;12:774-85
28. Verstrepen L, Carpentier I, Verhelst K, et al. ABINs: A20 binding inhibitors of NF-kappa B and apoptosis signaling. Biochem Pharmacol 2009;78:105-14
29. Cesario A, Rocca B, Rutella S. The interplay between indoleamine 2,3-dioxygenase 1 (IDO1) and cyclooxygenase (COX)-2 in chronic inflammation and cancer. Curr Med Chem 2011;18:2263-71
30. Cheyuo C, Yang WL, Wang P. The critical role of adrenomedullin and its binding protein, AMBP-1, in neuroprotection. Biol Chem 2012;393: 429-39
31. Varela-Nallar L, Parodi J, Faras GG, et al. Wnt-5a is a synaptogenic factor with neuroprotective properties against AA toxicity. Neurodegener Dis 2012;10:23-26
32. Maurer MH, Schäbitz WR, Schneider A. Old friends in new constellationsVThe hematopoietic growth factors G-CSF, GM-CSF, and EPO for the treatment of neurological diseases. Curr Med Chem 2008;15: 1407-11 (Pubitemid 351997791)
33. Niu J, Wang K, Graham S, et al. MCP-1-induced protein attenuates endotoxin-induced myocardial dysfunction by suppressing cardiac NF-1082;B activation via inhibition of I?B kinase activation. J Mol Cell Cardiol. 2011;51:177-86
34. Deban L, Russo RC, Sironi M, et al. Regulation of leukocyte recruitment by the long pentraxin PTX3. Nat Immunol 2010;11:328-34
35. Stark GR. How cells respond to interferons revisited: From early history to current complexity. Cytokine Growth Factor Rev 2007;18:419-23 (Pubitemid 47302834)
36. Waddell SJ, Popper SJ, Rubins KH, et al. Dissecting interferon-induced transcriptional programs in human peripheral blood cells. PLoS One 2010;5:e9753
37. Schoggins JW, Rice CM. Interferon-stimulated genes and their antiviral effector functions. Curr Opin Virol 2011;1:519-25
38. Lv M, Liu Y, Zhang J, et al. Roles of inflammation response in microglia cell through Toll-like receptors 2/interleukin-23/interleukin-17 pathway in cerebral ischemia/reperfusion injury. Neuroscience 2011;176:162-72
39. Van Horssen J, Singh S, van der Pol S, et al. Clusters of activated microglia in normal-appearing white matter show signs of innate immune activation. J Neuroinflammation 2012;9:156
40. Schönrock LM, Gawlowski G, Brück W. Interleukin-6 expression in human multiple sclerosis lesions. Neurosci Lett 2000;294:45-48
41. Gregory AP, Dendrou CA, Attfield KE, et al. TNF receptor 1 genetic risk mirrors outcome of anti-TNF therapy in multiple sclerosis. Nature 2012; 488:508-11
42. Mancini AD, Di Battista JA. The cardinal role of the phospholipase A(2)/cyclooxygenase-2/prostaglandin E synthase/prostaglandin E(2) (PCPP) axis in inflammostasis. Inflamm Res 2011;60:1083-92
43. Segal BM, Constantinescu CS, Raychaudhuri A, et al. Repeated subcutaneous injections of IL12/23 p40 neutralising antibody, ustekinumab, in patients with relapsing-remitting multiple sclerosis: A phase II, double-blind, placebo-controlled, randomised, dose-ranging study. Lancet Neurol 2008;7: 796-804
44. Vollmer TL, Wynn DR, Alam MS, et al. A phase 2, 24-week, randomized, placebo-controlled, double-blind study examining the efficacy and safety of an anti-interleukin-12 and-23 monoclonal antibody in patients with relapsing-remitting or secondary progressive multiple sclerosis. Mult Scler 2011;17:181-91
45. Masilamoni JG, Jesudason EP, Baben B, et al. Molecular chaperone alpha-crystallin prevents detrimental effects of neuroinflammation. Biochim Biophys Acta 2006;1762:284-93 (Pubitemid 43172843)
46. Ousman SS, Tomooka BH, van Noort JM, et al. Protective and therapeutic role for alphaB-crystallin in autoimmune demyelination. Nature 2007;448:474-79 (Pubitemid 47123511)
47. Arac A, Brownell SE, Rothbard JB, et al. Systemic augmentation of alphaB-crystallin provides therapeutic benefit twelve hours post-stroke onset via immune modulation. Proc Natl Acad Sci U S A 2011;108:13287-92
48. Klopstein A, Santos-Nogueira E, Francos-Quijorna I, et al. Beneficial effects of >B-crystallin in spinal cord contusion injury. J Neurosci 2012; 32:14478-88
49. Pangratz-Fuehrer S, Kaur K, Ousman SS, et al. Functional rescue of experimental ischemic optic neuropathy with >B-crystallin. Eye 2011;25: 809-17
50. Velotta JB, Kimura N, Chang SH, et al. >B-crystallin improves murine cardiac function and attenuates apoptosis in human endothelial cells exposed to ischemia-reperfusion. Ann Thorac Surg 2011;91:1907-13
51. Park H, Park S, Jeon H, et al. Alpha B-crystallin prevents the arrhythmogenic effects of particulate matter isolated from ambient air by attenuating oxidative stress. Toxicol Appl Pharmacol 2013;266:267-75