Role of inflammation and apoptosis in multiple sclerosis: Comparative analysis between the periphery and the central nervous system

Journal of Neuroimmunology

Volumn 287, Issue , 2015, Pages 80-87

  Macchi, Beatrice ^a   Marino Merlo, Francesca ^b   Nocentini, Ugo ^a,c   Pisani, Valerio ^c   Cuzzocrea, Salvatore ^b   Grelli, Sandro ^a   Mastino, Antonio ^b,d  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b UNIVERSITY OF MESSINA   (Italy)

^c IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^d INSTITUTE OF TRANSLATIONAL PHARMACOLOGY   (Italy)

Author keywords

Apoptosis; Inflammation; Multiple sclerosis; Targeted therapy

Indexed keywords

BETA INTERFERON; CYTOKINE;

APOPTOSIS; AUTOIMMUNITY; BLOOD BRAIN BARRIER; BRAIN DAMAGE; CELL LOSS; CENTRAL NERVOUS SYSTEM DISEASE; COMPARATIVE STUDY; DISEASE ACTIVITY; DISEASE COURSE; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; HUMAN; IMMUNOPATHOGENESIS; MULTIPLE SCLEROSIS; MYELIN SHEATH; NERVE CELL DEGENERATION; NERVE INJURY; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; OLIGODENDROGLIA; PERIPHERAL NEUROPATHY; PRIORITY JOURNAL; REVIEW; CENTRAL NERVOUS SYSTEM; COMPLICATION; INFLAMMATION; PATHOLOGY; PATHOPHYSIOLOGY; PERIPHERAL NERVOUS SYSTEM; PHYSIOLOGY;

APOPTOSIS; CENTRAL NERVOUS SYSTEM; HUMANS; INFLAMMATION; MULTIPLE SCLEROSIS; PERIPHERAL NERVOUS SYSTEM;

EID: 84943234695     PISSN: 01655728     EISSN: 18728421     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2015.08.016     Document Type: Review

References (75)

1. Babij R., Perumal J.S. Comparative efficacy of alemtuzumab and established treatment in the management of multiple sclerosis. Neuropsychiatr. Dis. Treat. 2015, 11:1221-1229.
2. Barnett M.H., Prineas J.W. Relapsing and remitting multiple sclerosis: pathology of the newly forming lesion. Ann. Neurol. 2004, 55:458-468.
3. Beynon V., Quintana F.J., Weiner H.L. Activated human CD4+CD45RO+ memory T-cells indirectly inhibit NLRP3 inflammasome activation through downregulation of P2X7R signalling. PLoS One 2012, 7:e39576.
4. Calabrese V., Scapagnini G., Ravagna A., Bella R., Foresti R., Bates T.E., Giuffrida Stella A.M., Pennisi G. Nitric oxide synthase is present in the cerebrospinal fluid of patients with active multiple sclerosis and is associated with increases in cerebrospinal fluid protein nitrotyrosine and S-nitrosothiols and with changes in glutathione levels. J. Neurosci. Res. 2002, 70:580-587.
5. Caprariello A.V., Mangla S., Miller R.H., Selkirk S.M. Apoptosis of oligodendrocytes in the central nervous system results in rapid focal demyelination. Ann. Neurol. 2012, 72:395-405.
6. Carbone F., De Rosa V., Carrieri P.B., Montella S., Bruzzese D., Porcellini A., Procaccini C., La Cava A., Matarese G. Regulatory T cell proliferative potential is impaired in human autoimmune disease. Nat. Med. 2014, 20:69-74.
7. Castillo-Trivino T., Braithwaite D., Bacchetti P., Waubant E. Rituximab in relapsing and progressive forms of multiple sclerosis: a systematic review. PLoS One 2013, 8:e66308.
8. Cencioni M.T., Santini S., Ruocco G., Borsellino G., De Bardi M., Grasso M.G., Ruggieri S., Gasperini C., Centonze D., Barila D., Battistini L., Volpe E. FAS-ligand regulates differential activation-induced cell death of human T-helper 1 and 17 cells in healthy donors and multiple sclerosis patients. Cell Death Dis. 2015, 6:e1741.
9. Choi S.R., Howell O.W., Carassiti D., Magliozzi R., Gveric D., Muraro P.A., Nicholas R., Roncaroli F., Reynolds R. Meningeal inflammation plays a role in the pathology of primary progressive multiple sclerosis. Brain 2012, 135:2925-2937.
10. Comi C., Leone M., Bonissoni S., DeFranco S., Bottarel F., Mezzatesta C., Chiocchetti A., Perla F., Monaco F., Dianzani U. Defective T cell Fas function in patients with multiple sclerosis. Neurology 2000, 55:921-927.
11. Corcione A., Casazza S., Ferretti E., Giunti D., Zappia E., Pistorio A., Gambini C., Mancardi G.L., Uccelli A., Pistoia V. Recapitulation of B cell differentiation in the central nervous system of patients with multiple sclerosis. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:11064-11069.
12. Curtin F., Hartung H.P. Novel therapeutic options for multiple sclerosis. Expert. Rev. Clin. Pharmacol. 2014, 7:91-104.
13. de Jong B.A., Huizinga T.W., Bollen E.L., Uitdehaag B.M., Bosma G.P., van Buchem M.A., Remarque E.J., Burgmans A.C., Kalkers N.F., Polman C.H., Westendorp R.G. Production of IL-1beta and IL-1Ra as risk factors for susceptibility and progression of relapse-onset multiple sclerosis. J. Neuroimmunol. 2002, 126:172-179.
14. Du C., Liu C., Kang J., Zhao G., Ye Z., Huang S., Li Z., Wu Z., Pei G. MicroRNA miR-326 regulates TH-17 differentiation and is associated with the pathogenesis of multiple sclerosis. Nat. Immunol. 2009, 10:1252-1259.
15. Duddy M., Niino M., Adatia F., Hebert S., Freedman M., Atkins H., Kim H.J., Bar-Or A. Distinct effector cytokine profiles of memory and naive human B cell subsets and implication in multiple sclerosis. J. Immunol. 2007, 178:6092-6099.
16. Durelli L., Conti L., Clerico M., Boselli D., Contessa G., Ripellino P., Ferrero B., Eid P., Novelli F. T-helper 17 cells expand in multiple sclerosis and are inhibited by interferon-beta. Ann. Neurol. 2009, 65:499-509.
17. Fischer M.T., Sharma R., Lim J.L., Haider L., Frischer J.M., Drexhage J., Mahad D., Bradl M., van Horssen J., Lassmann H. NADPH oxidase expression in active multiple sclerosis lesions in relation to oxidative tissue damage and mitochondrial injury. Brain 2012, 135:886-899.
18. Frisullo G., Angelucci F., Caggiula M., Nociti V., Iorio R., Patanella A.K., Sancricca C., Mirabella M., Tonali P.A., Batocchi A.P. pSTAT1, pSTAT3, and T-bet expression in peripheral blood mononuclear cells from relapsing-remitting multiple sclerosis patients correlates with disease activity. J. Neurosci. Res. 2006, 84:1027-1036.
19. Guo H., Callaway J.B., Ting J.P. Inflammasomes: mechanism of action, role in disease, and therapeutics. Nat. Med. 2015, 21:677-687.
20. Gurevich M., Achiron A. The switch between relapse and remission in multiple sclerosis: continuous inflammatory response balanced by Th1 suppression and neurotrophic factors. J. Neuroimmunol. 2012, 252:83-88.
21. Hagman S., Kolasa M., Basnyat P., Helminen M., Kahonen M., Dastidar P., Lehtimaki T., Elovaara I. Analysis of apoptosis-related genes in patients with clinically isolated syndrome and their association with conversion to multiple sclerosis. J. Neuroimmunol. 2015, 280:43-48.
22. Haider L., Fischer M.T., Frischer J.M., Bauer J., Hoeftberger R., Botond G., Esterbauer H., Binder C.J., Witztum J.L., Lassmann H. Oxidative damage in multiple sclerosis lesions. Brain 2011, 134:1914-1924.
23. Hauser S.L., Waubant E., Arnold D.L., Vollmer T., Antel J., Fox R.J., Bar-Or A., Panzara M., Sarkar N., Agarwal S., Langer-Gould A., Smith C.H. B-cell depletion with rituximab in relapsing-remitting multiple sclerosis. N. Engl. J. Med. 2008, 358:676-688.
24. Hebb A.L., Moore C.S., Bhan V., Campbell T., Fisk J.D., Robertson H.A., Thorne M., Lacasse E., Holcik M., Gillard J., Crocker S.J., Robertson G.S. Expression of the inhibitor of apoptosis protein family in multiple sclerosis reveals a potential immunomodulatory role during autoimmune mediated demyelination. Mult. Scler. 2008, 14:577-594.
25. Henderson A.P., Barnett M.H., Parratt J.D., Prineas J.W. Multiple sclerosis: distribution of inflammatory cells in newly forming lesions. Ann. Neurol. 2009, 66:739-753.
26. Hilliard B., Wilmen A., Seidel C., Liu T.S., Goke R., Chen Y. Roles of TNF-related apoptosis-inducing ligand in experimental autoimmune encephalomyelitis. J. Immunol. 2001, 166:1314-1319.
27. Jamshidian A., Shaygannejad V., Pourazar A., Zarkesh-Esfahani S.H., Gharagozloo M. Biased Treg/Th17 balance away from regulatory toward inflammatory phenotype in relapsed multiple sclerosis and its correlation with severity of symptoms. J. Neuroimmunol. 2013, 262:106-112.
28. Johnson B.H., Bonafede M.M., Watson C. Platform therapy compared with natalizumab for multiple sclerosis: relapse rates and time to relapse among propensity score-matched US patients. CNS Drugs 2015, 29:503-510.
29. Julia E., Edo M.C., Horga A., Montalban X., Comabella M. Differential susceptibility to apoptosis of CD4+T cells expressing CCR5 and CXCR3 in patients with MS. Clin. Immunol. 2009, 133:364-374.
30. Kay E., Scotland R.S., Whiteford J.R. Toll-like receptors: role in inflammation and therapeutic potential. Biofactors 2014, 40:284-294.
31. Knippenberg S., Peelen E., Smolders J., Thewissen M., Menheere P., Cohen Tervaert J.W., Hupperts R., Damoiseaux J. Reduction in IL-10 producing B cells (Breg) in multiple sclerosis is accompanied by a reduced naive/memory Breg ratio during a relapse but not in remission. J. Neuroimmunol. 2011, 239:80-86.
32. Kutzelnigg A., Lucchinetti C.F., Stadelmann C., Bruck W., Rauschka H., Bergmann M., Schmidbauer M., Parisi J.E., Lassmann H. Cortical demyelination and diffuse white matter injury in multiple sclerosis. Brain 2005, 128:2705-2712.
33. Libbey J.E., Cusick M.F., Fujinami R.S. Role of pathogens in multiple sclerosis. Int. Rev. Immunol. 2014, 33:266-283.
34. Lin W., Lin Y., Li J., Fenstermaker A.G., Way S.W., Clayton B., Jamison S., Harding H.P., Ron D., Popko B. Oligodendrocyte-specific activation of PERK signaling protects mice against experimental autoimmune encephalomyelitis. J. Neurosci. 2013, 33:5980-5991.
35. Lisak R.P., Benjamins J.A., Nedelkoska L., Barger J.L., Ragheb S., Fan B., Ouamara N., Johnson T.A., Rajasekharan S., Bar-Or A. Secretory products of multiple sclerosis B cells are cytotoxic to oligodendroglia in vitro. J. Neuroimmunol. 2012, 246:85-95.
36. Liu, T., Ji, R.R., 2014. Toll-Like Receptors and Itch. Itch: Mechanisms and Treatment. 2014 by Taylor & Francis Group, LLC.: Boca Raton FL.
37. Lopez-Gomez C., Fernandez O., Antonio Garcia-Leon J., Jesus Pinto-Medel M., Oliver-Martos B., Ortega-Pinazo J., Suardiaz M., Garcia-Trujillo L., Guijarro-Castro C., Benito-Leon J., Prat I., Varade J., Alvarez-Lafuente R., Urcelay E., Leyva L. TRAIL/TRAIL receptor system and susceptibility to multiple sclerosis. PLoS One 2011, 6.
38. Louveau A., Smirnov I., Keyes T.J., Eccles J.D., Rouhani S.J., Peske J.D., Derecki N.C., Castle D., Mandell J.W., Lee K.S., Harris T.H., Kipnis J. Structural and functional features of central nervous system lymphatic vessels. Nature 2015, 523:337-341.
39. Lucchinetti C., Bruck W., Parisi J., Scheithauer B., Rodriguez M., Lassmann H. Heterogeneity of multiple sclerosis lesions: implications for the pathogenesis of demyelination. Ann. Neurol. 2000, 47:707-717.
40. Macchi B., Matteucci C., Nocentini U., Caltagirone C., Mastino A. Impaired apoptosis in mitogen-stimulated lymphocytes of patients with multiple sclerosis. Neuroreport 1999, 10:399-402.
41. Macchi B., Matteucci C., Nocentini U., Tacconi S., Pagnini V., Mastino A., Caltagirone C. Defective Fas ligand productions in lymphocytes from MS patients. Neuroreport 2001, 12:4113-4116.
42. Mahad D., Ziabreva I., Lassmann H., Turnbull D. Mitochondrial defects in acute multiple sclerosis lesions. Brain 2008, 131:1722-1735.
43. Mandel I., Paperna T., Miller A. Aberrant expression of the apoptosis-related proteins BAK and MCL1 in T cells in multiple sclerosis. J. Neuroimmunol. 2012, 244:51-56.
44. Masters S.L. Specific inflammasomes in complex diseases. Clin. Immunol. 2013, 147:223-228.
45. Mc Guire C., Volckaert T., Wolke U., Sze M., de Rycke R., Waisman A., Prinz M., Beyaert R., Pasparakis M., van Loo G. Oligodendrocyte-specific FADD deletion protects mice from autoimmune-mediated demyelination. J. Immunol. 2010, 185:7646-7653.
46. Metz I., Weigand S.D., Popescu B.F., Frischer J.M., Parisi J.E., Guo Y., Lassmann H., Bruck W., Lucchinetti C.F. Pathologic heterogeneity persists in early active multiple sclerosis lesions. Ann. Neurol. 2014, 75:728-738.
47. Mifsud E.J., Tan A.C., Jackson D.C. TLR agonists as modulators of the innate immune response and their potential as agents against infectious disease. Front. Immunol. 2014, 5:79.
48. Moore C.S., Hebb A.L., Robertson G.S. Inhibitor of apoptosis protein (IAP) profiling in experimental autoimmune encephalomyelitis (EAE) implicates increased XIAP in T lymphocytes. J. Neuroimmunol. 2008, 193:94-105.
49. Moreno M., Negrotto L., Rio J., Moubarak R., Martin I., Bustamante M.F., Comella J.X., Vidal-Jordana A., Perez-Boza J., Montalban X., Comabella M. Activation-induced cell death in T lymphocytes from multiple sclerosis patients. J. Neuroimmunol. 2014, 272:51-55.
50. Moreno M., Saenz-Cuesta M., Castillo J., Canto E., Negrotto L., Vidal-Jordana A., Montalban X., Comabella M. Circulating levels of soluble apoptosis-related molecules in patients with multiple sclerosis. J. Neuroimmunol. 2013, 263:152-154.
51. Papini A.M., Konig E. Novel diagnostic tools and solutions for multiple sclerosis treatment: a patent review (2009-2014). Expert Opin. Ther. Pat. 2015, 25:873-884.
52. Peelen E., Damoiseaux J., Muris A.H., Knippenberg S., Smolders J., Hupperts R., Thewissen M. Increased inflammasome related gene expression profile in PBMC may facilitate T helper 17 cell induction in multiple sclerosis. Mol. Immunol. 2015, 63:521-529.
53. Pennisi G., Cornelius C., Cavallaro M.M., Salinaro A.T., Cambria M.T., Pennisi M., Bella R., Milone P., Ventimiglia B., Migliore M.R., Di Renzo L., De Lorenzo A., Calabrese V. Redox regulation of cellular stress response in multiple sclerosis. Biochem. Pharmacol. 2011, 82:1490-1499.
54. Piccio L., Naismith R.T., Trinkaus K., Klein R.S., Parks B.J., Lyons J.A., Cross A.H. Changes in B- and T-lymphocyte and chemokine levels with rituximab treatment in multiple sclerosis. Arch. Neurol. 2010, 67:707-714.
55. Racke M.K., Yang Y., Lovett-Racke A.E. Is T-bet a potential therapeutic target in multiple sclerosis?. J. Interf. Cytokine Res. 2014, 34:623-632.
56. Reuss R., Mistarz M., Mirau A., Kraus J., Bodeker R.H., Oschmann P. FADD is upregulated in relapsing remitting multiple sclerosis. Neuroimmunomodulation 2014, 21:221-225.
57. Rinta S., Kuusisto H., Raunio M., Paalavuo R., Levula M., Lehtimaki T., Elovaara I. Apoptosis-related molecules in blood in multiple sclerosis. J. Neuroimmunol. 2008, 205:135-141.
58. Saresella M., Gatti A., Tortorella P., Marventano I., Piancone F., La Rosa F., Caputo D., Rovaris M., Biasin M., Clerici M. Toll-like receptor 3 differently modulates inflammation in progressive or benign multiple sclerosis. Clin. Immunol. 2014, 150:109-120.
59. Schirmer L., Rothhammer V., Hemmer B., Korn T. Enriched CD161high CCR6+ gammadelta T cells in the cerebrospinal fluid of patients with multiple sclerosis. JAMA Neurol. 2013, 70:345-351.
60. Semra Y.K., Seidi O.A., Sharief M.K. Overexpression of the apoptosis inhibitor FLIP in T cells correlates with disease activity in multiple sclerosis. J. Neuroimmunol. 2001, 113:268-274.
61. Sharief M.K., Douglas M., Noori M., Semra Y.K. The expression of pro- and anti-apoptosis Bcl-2 family proteins in lymphocytes from patients with multiple sclerosis. J. Neuroimmunol. 2002, 125:155-162.
62. Simpson S., Taylor B.V., van der Mei I. The role of epidemiology in MS research: Past successes, current challenges and future potential. Mult. Scler. 2015, 21:969-977.
63. Szabo S.J., Sullivan B.M., Stemmann C., Satoskar A.R., Sleckman B.P., Glimcher L.H. Distinct effects of T-bet in TH1 lineage commitment and IFN-gamma production in CD4 and CD8 T cells. Science 2002, 295:338-342.
64. Tzartos J.S., Friese M.A., Craner M.J., Palace J., Newcombe J., Esiri M.M., Fugger L. Interleukin-17 production in central nervous system-infiltrating T cells and glial cells is associated with active disease in multiple sclerosis. Am. J. Pathol. 2008, 172:146-155.
65. van der Valk P., De Groot C.J. Staging of multiple sclerosis (MS) lesions: pathology of the time frame of MS. Neuropathol. Appl. Neurobiol. 2000, 26:2-10.
66. van Horssen J., Singh S., van der Pol S., Kipp M., Lim J.L., Peferoen L., Gerritsen W., Kooi E.J., Witte M.E., Geurts J.J., de Vries H.E., Peferoen-Baert R., van den Elsen P.J., van der Valk P., Amor S. Clusters of activated microglia in normal-appearing white matter show signs of innate immune activation. J. Neuroinflammation 2012, 9:156.
67. van Noort J.M., Baker D., Amor S. Mechanisms in the development of multiple sclerosis lesions: reconciling autoimmune and neurodegenerative factors. CNS Neurol. Disord. Drug Targets 2012, 11:556-569.
68. Venken K., Hellings N., Hensen K., Rummens J.L., Stinissen P. Memory CD4+CD127high T cells from patients with multiple sclerosis produce IL-17 in response to myelin antigens. J. Neuroimmunol. 2010, 226:185-191.
69. Veto S., Acs P., Bauer J., Lassmann H., Berente Z., Setalo G., Borgulya G., Sumegi B., Komoly S., Gallyas F., Illes Z. Inhibiting poly(ADP-ribose) polymerase: a potential therapy against oligodendrocyte death. Brain 2010, 133:822-834.
70. von Budingen H.C., Kuo T.C., Sirota M., van Belle C.J., Apeltsin L., Glanville J., Cree B.A., Gourraud P.A., Schwartzburg A., Huerta G., Telman D., Sundar P.D., Casey T., Cox D.R., Hauser S.L. B cell exchange across the blood-brain barrier in multiple sclerosis. J. Clin. Invest. 2012, 122:4533-4543.
71. Waiczies S., Weber A., Lunemann J.D., Aktas O., Zschenderlein R., Zipp F. Elevated Bcl-X-L levels correlate with T cell survival in multiple sclerosis. J. Neuroimmunol. 2002, 126:213-220.
72. Weller R.O., Galea I., Carare R.O., Minagar A. Pathophysiology of the lymphatic drainage of the central nervous system: implications for pathogenesis and therapy of multiple sclerosis. Pathophysiology 2010, 17:295-306.
73. Wucherpfennig K.W., Newcombe J., Li H., Keddy C., Cuzner M.L., Hafler D.A. Gamma delta T-cell receptor repertoire in acute multiple sclerosis lesions. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:4588-4592.
74. Yang L., Kress B.T., Weber H.J., Thiyagarajan M., Wang B., Deane R., Benveniste H., Iliff J.J., Nedergaard M. Evaluating glymphatic pathway function utilizing clinically relevant intrathecal infusion of CSF tracer. J. Transl. Med. 2013, 11:107.
75. Yeo Y.A., Martinez Gomez J.M., Croxford J.L., Gasser S., Ling E.A., Schwarz H. CD137 ligand activated microglia induces oligodendrocyte apoptosis via reactive oxygen species. J. Neuroinflammation 2012, 9:173.