Intense Inflammation and Nerve Damage in Early Multiple Sclerosis Subsides at Older Age: A Reflection by Cerebrospinal Fluid Biomarkers

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Khademi, Mohsen ^a   Dring, Ann M ^b   Gilthorpe, Jonathan D ^b   Wuolikainen, Anna ^b   Al Nimer, Faiez ^a,c   Harris, Robert A ^a   Andersson, Magnus ^c   Brundin, Lou ^a,c   Piehl, Fredrik ^a,c   Olsson, Tomas ^a,c   Svenningsson, Anders ^b  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UMEÅ UNIVERSITY   (Sweden)

^c KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; CXCL13 CHEMOKINE; GELATINASE B; NEUROFILAMENT LIGHT CHAIN; OSTEOPONTIN; PROTEIN VARIANT; UNCLASSIFIED DRUG;

ADOLESCENT; ADULT; AGE DISTRIBUTION; AGED; ARTICLE; CEREBROSPINAL FLUID ANALYSIS; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE CLASSIFICATION; DISEASE MARKER; DISEASE SEVERITY; EARLY DIAGNOSIS; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMAN; MAJOR CLINICAL STUDY; MALE; MULTIPLE SCLEROSIS; NERVE INJURY; NERVOUS SYSTEM INFLAMMATION; NEUROPATHOLOGY; PATIENT ASSESSMENT; PROTEIN DETERMINATION;

AGED; BIOLOGICAL MARKERS; CASE-CONTROL STUDIES; CENTRAL NERVOUS SYSTEM; DEMOGRAPHY; HUMANS; INFLAMMATION; LEAST-SQUARES ANALYSIS; MODELS, BIOLOGICAL; MULTIPLE SCLEROSIS; MULTIPLE SCLEROSIS, RELAPSING-REMITTING; PRINCIPAL COMPONENT ANALYSIS;

EID: 84877107261     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0063172     Document Type: Article

References (59)

1. Compston A, Coles A, (2002) Multiple sclerosis. Lancet 359: 1221-1231.
2. Compston A, Coles A, (2008) Multiple sclerosis. Lancet 372: 1502-1517.
3. Kipp M, van der Valk P, Amor S, (2012) Pathology of multiple sclerosis. CNS neurol disord drug targets 11: 506-517.
4. Kremenchutzky M, Cottrell D, Rice G, Hader W, Baskerville J, et al. (1999) The natural history of multiple sclerosis: a geographically based study. 7. Progressive-relapsing and relapsing-progressive multiple sclerosis: a re-evaluation. Brain 122: 1941-1950.
5. Kornek B, Lassmann H, (1999) Axonal pathology in multiple sclerosis. A historical note. Brain Pathol 9: 651-656.
6. Ferguson B, Matyszak MK, Esiri MM, Perry VH, (1997) Axonal damage in acute multiple sclerosis lesions. Brain 120: 393-399.
7. Trapp BD, Nave KA, (2008) Multiple sclerosis: an immune or neurodegenerative disorder? Annu Rev Neurosci 31: 247-269.
8. Bruck W, Porada P, Poser S, Rieckmann P, Hanefeld F, et al. (1995) Monocyte/macrophage differentiation in early multiple sclerosis lesions. Ann Neurol 38: 788-796.
9. Tektonidou MG, Ward MM, (2011) Validation of new biomarkers in systemic autoimmune diseases. Nat Rev Rheumatol 7: 708-717.
10. Harris VK, Sadiq SA, (2009) Disease biomarkers in multiple sclerosis: potential for use in therapeutic decision making. Mol Diagn Ther 13: 225-244.
11. Kieseier BC, Seifert T, Giovannoni G, Hartung HP, (1999) Matrix metalloproteinases in inflammatory demyelination: targets for treatment. Neurology 53: 20-25.
12. Gijbels K, Masure S, Carton H, Opdenakker G, (1992) Gelatinase in the cerebrospinal fluid of patients with multiple sclerosis and other inflammatory neurological disorders. J Neuroimmunol 41: 29-34.
13. Leppert D, Ford J, Stabler G, Grygar C, Lienert C, et al. (1998) Matrix metalloproteinase-9 (gelatinase B) is selectively elevated in CSF during relapses and stable phases of multiple sclerosis. Brain 121: 2327-2334.
14. Ram M, Sherer Y, Shoenfeld Y, (2006) Matrix metalloproteinase-9 and autoimmune diseases. J Clin Immunol 26: 299-307.
15. Khademi M, Bornsen L, Rafatnia F, Andersson M, Brundin L, et al. (2009) The effects of natalizumab on inflammatory mediators in multiple sclerosis: prospects for treatment-sensitive biomarkers. Eur J Neurol 16: 528-536.
16. Ransohoff RM, Kivisakk P, Kidd G, (2003) Three or more routes for leukocyte migration into the central nervous system. Nat Rev Immunol 3: 569-581.
17. Sorensen TL, Roed H, Sellebjerg F, (2002) Chemokine receptor expression on B cells and effect of interferon-beta in multiple sclerosis. J Neuroimmunol 122: 125-131.
18. Krumbholz M, Theil D, Cepok S, Hemmer B, Kivisakk P, et al. (2006) Chemokines in multiple sclerosis: CXCL12 and CXCL13 up-regulation is differentially linked to CNS immune cell recruitment. Brain 129: 200-211.
19. Kuenz B, Lutterotti A, Ehling R, Gneiss C, Haemmerle M, et al. (2008) Cerebrospinal fluid B cells correlate with early brain inflammation in multiple sclerosis. PloS one 3: e2559.
20. Bielekova B, Komori M, Xu Q, Reich DS, Wu T, (2012) Cerebrospinal Fluid IL-12p40, CXCL13 and IL-8 as a Combinatorial Biomarker of Active Intrathecal Inflammation. PloS one 7: e48370.
21. Brettschneider J, Czerwoniak A, Senel M, Fang L, Kassubek J, et al. (2010) The chemokine CXCL13 is a prognostic marker in clinically isolated syndrome (CIS). PloS one 5: e11986.
22. Khademi M, Kockum I, Andersson ML, Iacobaeus E, Brundin L, et al. (2011) Cerebrospinal fluid CXCL13 in multiple sclerosis: a suggestive prognostic marker for the disease course. Mult Scler 17: 335-343.
23. Sellebjerg F, Bornsen L, Khademi M, Krakauer M, Olsson T, et al. (2009) Increased cerebrospinal fluid concentrations of the chemokine CXCL13 in active MS. Neurology 73: 2003-2010.
24. Mazzali M, Kipari T, Ophascharoensuk V, Wesson JA, Johnson R, et al. (2002) Osteopontin-a molecule for all seasons. QJM 95: 3-13.
25. Wang KX, Denhardt DT, (2008) Osteopontin: role in immune regulation and stress responses. Cytokine Growth Factor Rev 19: 333-345.
26. Chabas D, Baranzini SE, Mitchell D, Bernard CC, Rittling SR, et al. (2001) The influence of the proinflammatory cytokine, osteopontin, on autoimmune demyelinating disease. Science 294: 1731-1735.
27. Bornsen L, Khademi M, Olsson T, Sorensen PS, Sellebjerg F, (2011) Osteopontin concentrations are increased in cerebrospinal fluid during attacks of multiple sclerosis. Mult Scler 17: 32-42.
28. Lycke JN, Karlsson JE, Andersen O, Rosengren LE, (1998) Neurofilament protein in cerebrospinal fluid: a potential marker of activity in multiple sclerosis. J Neurol NeurosurgPsychiatry 64: 402-404.
29. Norgren N, Sundstrom P, Svenningsson A, Rosengren L, Stigbrand T, et al. (2004) Neurofilament and glial fibrillary acidic protein in multiple sclerosis. Neurology 63: 1586-1590.
30. Salzer J, Svenningsson A, Sundstrom P, (2010) Neurofilament light as a prognostic marker in multiple sclerosis. Mult Scler 16: 287-292.
31. Gunnarsson M, Malmestrom C, Axelsson M, Sundstrom P, Dahle C, et al. (2011) Axonal damage in relapsing multiple sclerosis is markedly reduced by natalizumab. Ann Neurol 69: 83-89.
32. Trojano M, Liguori M, Bosco Zimatore G, Bugarini R, Avolio C, et al. (2002) Age-related disability in multiple sclerosis. Ann Neurol 51: 475-480.
33. Buchanan RJ, Chakravorty BJ, Tyry T, Hatcher W, Vollmer T, (2009) Age-related comparisons of people with multiple sclerosis: demographic, disease, and treatment characteristics. NeuroRehabilitation 25: 271-278.
34. Deryck O, Ketelaer P, Dubois B, (2006) Clinical characteristics and long term prognosis in early onset multiple sclerosis. J Neurol 253: 720-723.
35. Tremlett H, Paty D, Devonshire V, (2006) Disability progression in multiple sclerosis is slower than previously reported. Neurology 66: 172-177.
36. McDonald WI, Compston A, Edan G, Goodkin D, Hartung HP, et al. (2001) Recommended diagnostic criteria for multiple sclerosis: guidelines from the International Panel on the diagnosis of multiple sclerosis. Ann Neurol 50: 121-127.
37. Iacobaeus E, Ryschkewitsch C, Gravell M, Khademi M, Wallstrom E, et al. (2009) Analysis of cerebrospinal fluid and cerebrospinal fluid cells from patients with multiple sclerosis for detection of JC virus DNA. Mult Scler 15: 28-35.
38. Wold S, Esbensen K, Geladi P, (1987) Principal Component Analysis. Chemometrics and Intelligent Laboratory Systems 2: 37-52.
39. Trygg J, Wold S, (2002) Orthogonal projections to latent structures (O-PLS). J Chemometrics 16: 119-128.
40. De Stefano N, Narayanan S, Francis GS, Arnaoutelis R, Tartaglia MC, et al. (2001) Evidence of axonal damage in the early stages of multiple sclerosis and its relevance to disability. Arch Neurol 58: 65-70.
41. Ratchford JN, Saidha S, Sotirchos ES, Oh JA, Seigo MA, et al. (2013) Active MS is associated with accelerated retinal ganglion cell/inner plexiform layer thinning. Neurology 80: 47-54.
42. Confavreux C, Vukusic S, (2006) Natural history of multiple sclerosis: a unifying concept. Brain 129: 606-616.
43. Meinl E, Krumbholz M, Derfuss T, Junker A, Hohlfeld R (2008) Compartmentalization of inflammation in the CNS: A major mechanism driving progressive multiple sclerosis. J Neurol Sci.
44. Wolinsky JS, Narayana PA, O'Connor P, Coyle PK, Ford C, et al. (2007) Glatiramer acetate in primary progressive multiple sclerosis: results of a multinational, multicenter, double-blind, placebo-controlled trial. Ann Neurol 61: 14-24.
45. Panitch H, Miller A, Paty D, Weinshenker B, (2004) Interferon beta-1b in secondary progressive MS: results from a 3-year controlled study. Neurology 63: 1788-1795.
46. Clinical Trial of Recombinant Interferon-beta-1a in MS (SPECTRIMS) Study Group (2004) Randomized controlled trial of interferon- beta-1a in secondary progressive MS: Clinical results. Neurology 63: 1768-1768.
47. Hawker K, O'Connor P, Freedman MS, Calabresi PA, Antel J, et al. (2009) Rituximab in patients with primary progressive multiple sclerosis: results of a randomized double-blind placebo-controlled multicenter trial. Ann Neurol 66: 460-471.
48. Romme Christensen J, Bornsen L, Khademi M, Olsson T, Jensen PE, et al. (2012) CSF inflammation and axonal damage are increased and correlate in progressive multiple sclerosis. Multiple sclerosis (Epub ahead of print).
49. Miller RA, (1991) Aging and immune function. Int Rev Cytol 124: 187-215.
50. Franceschi C, Bonafe M, Valensin S, (2000) Human immunosenescence: the prevailing of innate immunity, the failing of clonotypic immunity, and the filling of immunological space. Vaccine 18: 1717-1720.
51. Linton PJ, Li SP, Zhang Y, Bautista B, Huynh Q, et al. (2005) Intrinsic versus environmental influences on T-cell responses in aging. Immunol Rev 205: 207-219.
52. Sellebjerg F, Sorensen TL, (2003) Chemokines and matrix metalloproteinase-9 in leukocyte recruitment to the central nervous system. Brain Res Bull 61: 347-355.
53. Tortorella C, Bellacosa A, Paolicelli D, Fuiani A, Di Monte E, et al. (2005) Age-related gadolinium-enhancement of MRI brain lesions in multiple sclerosis. J Neurol Sci 239: 95-99.
54. Koch M, Mostert J, Heersema D, De Keyser J, (2007) Progression in multiple sclerosis: further evidence of an age dependent process. J Neurol Sci 255: 35-41.
55. Tremlett H, Zhao Y, Joseph J, Devonshire V, (2008) Relapses in multiple sclerosis are age- and time-dependent. J Neurol Neurosurg Psychiatry 79: 1368-1374.
56. Tutuncu M, Tang J, Zeid NA, Kale N, Crusan DJ, et al. (2012) Onset of progressive phase is an age-dependent clinical milestone in multiple sclerosis. Mult Scle (Epub ahead of print).
57. Confavreux C, Vukusic S, (2006) Age at disability milestones in multiple sclerosis. Brain 129: 595-605.
58. Frischer JM, Bramow S, Dal-Bianco A, Lucchinetti CF, Rauschka H, et al. (2009) The relation between inflammation and neurodegeneration in multiple sclerosis brains. Brain 132: 1175-1189.
59. Danilov AI, Andersson M, Bavand N, Wiklund NP, Olsson T, et al. (2003) Nitric oxide metabolite determinations reveal continuous inflammation in multiple sclerosis. J Neuroimmunol 136: 112-118.