Potential of a unique antibody gene signature to predict conversion to clinically definite multiple sclerosis

Journal of Neuroimmunology

Volumn 213, Issue 1-2, 2009, Pages 123-130

  Cameron, Elizabeth M ^a   Spencer, Sade ^a   Lazarini, Jonathan ^a   Harp, Christopher T ^a   Ward, E Sally ^b   Burgoon, Mark ^c   Owens, Gregory P ^c   Racke, Michael K ^d   Bennett, Jeffrey L ^c   Frohman, Elliot M ^a   Monson, Nancy L ^a,b  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c UNIVERSITY OF COLORADO   (United States)

^d THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

Author keywords

Antibodies; B lymphocytes; Gene rearrangement; Multiple sclerosis; Mutational signature

Indexed keywords

B LYMPHOCYTE ANTIBODY;

ACCURACY; ARTICLE; B LYMPHOCYTE; CEREBROSPINAL FLUID ANALYSIS; CLINICAL ARTICLE; CODON; COHORT ANALYSIS; CONTROLLED STUDY; GENE FREQUENCY; GENE MUTATION; HUMAN; MULTIPLE SCLEROSIS; PATHOGENESIS; PREDICTION; PREVALENCE; PRIORITY JOURNAL;

AMINO ACID SEQUENCE; ANTIBODIES; AUTOANTIBODIES; B-LYMPHOCYTES; BIOLOGICAL MARKERS; DATABASES, GENETIC; DIAGNOSTIC TECHNIQUES, NEUROLOGICAL; DISEASE PROGRESSION; GENES; GENETIC MARKERS; HUMANS; IMMUNOGLOBULINS; MOLECULAR BIOLOGY; MULTIPLE SCLEROSIS; MUTATION; PROTEOME; SEQUENCE ALIGNMENT;

EID: 68049083540     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2009.05.014     Document Type: Article

References (59)

1. Achiron A. Winning combination: the additive/synergistic benefits of IVIg in corticosteroid refractory optic neuritis. Eur. J. Neurol. 15 (2008) 1145
2. Antel J., and Bar-Or A. Roles of immunoglobulins and B cells in multiple sclerosis: from pathogenesis to treatment. J. Neuroimmunol. 180 (2006) 3-8
3. Baranzini S.E., Jeong M.C., Butunoi C., Murray R.S., Bernard C.C., and Oksenberg J.R. B cell repertoire diversity and clonal expansion in multiple sclerosis brain lesions. J. Immunol. 163 (1999) 5133-5144
4. Barkhof F., Filippi M., Miller D.H., Scheltens P., Campi A., Polman C.H., Comi G., Ader H.J., Losseff N., and Valk J. Comparison of MRI criteria at first presentation to predict conversion to clinically definite multiple sclerosis. Brain 120 Pt 11 (1997) 2059-2069
5. Beck R.W., Trobe J.D., Moke P.S., Gal R.L., Xing D., Bhatti M.T., Brodsky M.C., Buckley E.G., Chrousos G.A., Corbett J., Eggenberger E., Goodwin J.A., Katz B., Kaufman D.I., Keltner J.L., Kupersmith M.J., Miller N.R., Nazarian S., Orengo-Nania S., Savino P.J., Shults W.T., Smith C.H., and Wall M. High- and low-risk profiles for the development of multiple sclerosis within 10 years after optic neuritis: experience of the optic neuritis treatment trial. Arch. Ophthalmol. 121 (2003) 944-949
6. Bennett J.L., Haubold K., Ritchie A.M., Edwards S.J., Burgoon M., Shearer A.J., Gilden D.H., and Owens G.P. CSF IgG heavy-chain bias in patients at the time of a clinically isolated syndrome. J. Neuroimmunol. 199 (2008) 126-132
7. Brex P.A., Ciccarelli O., O'Riordan J.I., Sailer M., Thompson A.J., and Miller D.H. A longitudinal study of abnormalities on MRI and disability from multiple sclerosis. N. Engl. J. Med. 346 (2002) 158-164
8. Brezinschek H.P., Brezinschek R.I., and Lipsky P.E. Analysis of the heavy chain repertoire of human peripheral B cells using single-cell polymerase chain reaction. J. Immunol. 155 (1995) 190-202
9. Brezinschek H.P., Foster S.J., Brezinschek R.I., Dorner T., Domiati-Saad R., and Lipsky P.E. Analysis of the human VH gene repertoire. Differential effects of selection and somatic hypermutation on human peripheral CD5(+)/IgM+ and CD5(-)/IgM+ B cells. J. Clin. Invest. 99 (1997) 2488-2501
10. Brezinschek H.P., Foster S.J., Dorner T., Brezinschek R.I., and Lipsky P.E. Pairing of variable heavy and variable kappa chains in individual naive and memory B cells. J. Immunol. 160 (1998) 4762-4767
11. Cole S.R., Beck R.W., Moke P.S., Kaufman D.I., and Tourtellotte W.W. The predictive value of CSF oligoclonal banding for MS 5 years after optic neuritis. Optic Neuritis Study Group. Neurology 51 (1998) 885-887
12. Colombo M., Dono M., Gazzola P., Roncella S., Valetto A., Chiorazzi N., Mancardi G.L., and Ferrarini M. Accumulation of clonally related B lymphocytes in the cerebrospinal fluid of multiple sclerosis patients. J. Immunol. 164 (2000) 2782-2789
13. Cook G.P., and Tomlinson I.M. The human immunoglobulin VH repertoire. Immunol. Today 16 (1995) 237-242
14. Dalton C.M., Brex P.A., Miszkiel K.A., Hickman S.J., MacManus D.G., Plant G.T., Thompson A.J., and Miller D.H. Application of the new McDonald criteria to patients with clinically isolated syndromes suggestive of multiple sclerosis. Ann. Neurol. 52 (2002) 47-53
15. Dorner T., Brezinschek H.P., Brezinschek R.I., Foster S.J., Domiati-Saad R., and Lipsky P.E. Analysis of the frequency and pattern of somatic mutations within nonproductively rearranged human variable heavy chain genes. J. Immunol. 158 (1997) 2779-2789
16. Dorner T., Brezinschek H.P., Foster S.J., Brezinschek R.I., Farner N.L., and Lipsky P.E. Comparable impact of mutational and selective influences in shaping the expressed repertoire of peripheral IgM+/CD5- and IgM+/CD5+ B cells. Eur. J. Immunol. 28 (1998) 657-668
17. Dorner T., Brezinschek H.P., Foster S.J., Brezinschek R.I., Farner N.L., and Lipsky P.E. Delineation of selective influences shaping the mutated expressed human Ig heavy chain repertoire. J. Immunol. 160 (1998) 2831-2841
18. Dorner T., Foster S.J., Farner N.L., and Lipsky P.E. Somatic hypermutation of human immunoglobulin heavy chain genes: targeting of RGYW motifs on both DNA strands. Eur. J. Immunol. 28 (1998) 3384-3396
19. Duddy M., and Bar-Or A. B-cells in multiple sclerosis. Int. MS. J. 13 (2006) 84-90
20. Farner N.L., Dorner T., and Lipsky P.E. Molecular mechanisms and selection influence the generation of the human V lambda J lambda repertoire. J. Immunol. 162 (1999) 2137-2145
21. Franciotta D., Salvetti M., Lolli F., Serafini B., and Aloisi F. B cells and multiple sclerosis. Lancet. Neurol. 7 (2008) 852-858
22. Freedman M.S., Thompson E.J., Deisenhammer F., Giovannoni G., Grimsley G., Keir G., Ohman S., Racke M.K., Sharief M., Sindic C.J., Sellebjerg F., and Tourtellotte W.W. Recommended standard of cerebrospinal fluid analysis in the diagnosis of multiple sclerosis: a consensus statement. Arch. Neurol. 62 (2005) 865-870
23. Frohman E.M., Goodin D.S., Calabresi P.A., Corboy J.R., Coyle P.K., Filippi M., Frank J.A., Galetta S.L., Grossman R.I., Hawker K., Kachuck N.J., Levin M.C., Phillips J.T., Racke M.K., Rivera V.M., and Stuart W.H. The utility of MRI in suspected MS: report of the Therapeutics and Technology Assessment Subcommittee of the American Academy of Neurology. Neurology 61 (2003) 602-611
24. Frohman E.M., Racke M.K., and Raine C.S. Multiple sclerosis-the plaque and its pathogenesis. N. Engl. J. Med. 354 (2006) 942-955
25. Guddat L.W., Herron J.N., and Edmundson A.B. Three-dimensional structure of a human immunoglobulin with a hinge deletion. Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 4271-4275
26. Hansen A., Dorner T., and Lipsky P.E. Use of immunoglobulin variable-region genes by normal subjects and patients with systemic lupus erythematosus. Int. Arch. Allergy. Immunol. 123 (2000) 36-45
27. Harp C., Lee J., Lambracht-Washington D., Cameron E., Olsen G., Frohman E., Racke M., and Monson N. Cerebrospinal fluid B cells from multiple sclerosis patients are subject to normal germinal center selection. J. Neuroimmunol. 183 (2007) 189-199
28. 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., and Smith C.H. B-cell depletion with rituximab in relapsing-remitting multiple sclerosis. N. Engl. J. Med. 358 (2008) 676-688
29. Huang C., Stewart A.K., Schwartz R.S., and Stollar B.D. Immunoglobulin heavy chain gene expression in peripheral blood B lymphocytes. J. Clin. Invest. 89 (1992) 1331-1343
30. Kabat E.A., Glusman M., and Knaub V. Quantitative estimation of the albumin and gamma globulin in normal and pathologic cerebrospinal fluid by immunochemical methods. Am. J. Med. 4 (1948) 653-662
31. Kabat E.A., Wu T.T., Bilofsky H., Reid-Miller M., and Perry H. Sequences of proteins of immunological interest. United States Department of Health and Human Services, Washington, D.C (1983)
32. Kolln J., Ren H.M., Da R.R., Zhang Y., Spillner E., Olek M., Hermanowicz N., Hilgenberg L.G., Smith M.A., van den Noort S., and Qin Y. Triosephosphate isomerase- and glyceraldehyde-3-phosphate dehydrogenase-reactive autoantibodies in the cerebrospinal fluid of patients with multiple sclerosis. J. Immunol. 177 (2006) 5652-5658
33. Korteweg T., Tintore M., Uitdehaag B., Rovira A., Frederiksen J., Miller D., Fernando K., Filippi M., Agosta F., Rocca M., Fazekas F., Enzinger C., Matthews P., Parry A., Polman C., Montalban X., and Barkhof F. MRI criteria for dissemination in space in patients with clinically isolated syndromes: a multicentre follow-up study. Lancet. Neurol. 5 (2006) 221-227
34. Kraj P., Rao S.P., Glas A.M., Hardy R.R., Milner E.C., and Silberstein L.E. The human heavy chain Ig V region gene repertoire is biased at all stages of B cell ontogeny, including early pre-B cells. J. Immunol. 158 (1997) 5824-5832
35. Lambracht-Washington D., O'Connor K.C., Cameron E.M., Jowdry A., Ward E.S., Frohman E., Racke M.K., and Monson N.L. Antigen specificity of clonally expanded and receptor edited cerebrospinal fluid B cells from patients with relapsing remitting MS. J. Neuroimmunol. 186 (2007) 164-176
36. Leussink V.I., Lehmann H.C., Meyer zu Horste G., Hartung H.P., Stuve O., and Kieseier B.C. Rituximab induces clinical stabilization in a patient with fulminant multiple sclerosis not responding to natalizumab. Evidence for disease heterogeneity. J. Neurol. 255 (2008) 1436-1438
37. Martin Mdel P., and Monson N.L. Potential role of humoral immunity in the pathogenesis of multiple sclerosis (MS) and experimental autoimmune encephalomyelitis (EAE). Front. Biosci. 12 (2007) 2735-2749
38. McDonald W.I., Compston A., Edan G., Goodkin D., Hartung H.P., Lublin F.D., McFarland H.F., Paty D.W., Polman C.H., Reingold S.C., Sandberg-Wollheim M., Sibley W., Thompson A., van den Noort S., Weinshenker B.Y., and Wolinsky J.S. Recommended diagnostic criteria for multiple sclerosis: guidelines from the International Panel on the diagnosis of multiple sclerosis. Ann. Neurol. 50 (2001) 121-127
39. McLaughlin K.A., and Wucherpfennig K.W. B cells and autoantibodies in the pathogenesis of multiple sclerosis and related inflammatory demyelinating diseases. Adv. Immunol. 98 (2008) 121-149
40. Monson N.L., Dorner T., and Lipsky P.E. Targeting and selection of mutations in human V lambda rearrangements. Eur. J. Immunol. 30 (2000) 1597-1605
41. Monson N.L., Brezinschek H.P., Brezinschek R.I., Mobley A., Vaughan G.K., Frohman E.M., Racke M.K., and Lipsky P.E. Receptor revision and atypical mutational characteristics in clonally expanded B cells from the cerebrospinal fluid of recently diagnosed multiple sclerosis patients. J. Neuroimmunol. 158 (2005) 170-181
42. O'Riordan J.I., Thompson A.J., Kingsley D.P., MacManus D.G., Kendall B.E., Rudge P., McDonald W.I., and Miller D.H. The prognostic value of brain MRI in clinically isolated syndromes of the CNS. A 10-year follow-up. Brain 121 Pt 3 (1998) 495-503
43. Owens G.P., Kraus H., Burgoon M.P., Smith-Jensen T., Devlin M.E., and Gilden D.H. Restricted use of VH4 germline segments in an acute multiple sclerosis brain. Ann. Neurol. 43 (1998) 236-243
44. Owens G.P., Ritchie A.M., Burgoon M.P., Williamson R.A., Corboy J.R., and Gilden D.H. Single-cell repertoire analysis demonstrates that clonal expansion is a prominent feature of the B cell response in multiple sclerosis cerebrospinal fluid. J. Immunol. 171 (2003) 2725-2733
45. Owens G.P., Bennett J.L., Gilden D.H., and Burgoon M.P. The B cell response in multiple sclerosis. Neurol. Res. 28 (2006) 236-244
46. Owens G.P., Winges K.M., Ritchie A.M., Edwards S., Burgoon M.P., Lehnhoff L., Nielsen K., Corboy J., Gilden D.H., and Bennett J.L. VH4 gene segments dominate the intrathecal humoral immune response in multiple sclerosis. J. Immunol. 179 (2007) 6343-6351
47. Paolino E., Fainardi E., Ruppi P., Tola M.R., Govoni V., Casetta I., Monetti V.C., Granieri E., and Carreras M. A prospective study on the predictive value of CSF oligoclonal bands and MRI in acute isolated neurological syndromes for subsequent progression to multiple sclerosis. J. Neurol. Neurosurg. Psychiatry. 60 (1996) 572-575
48. Polman C.H., Reingold S.C., Edan G., Filippi M., Hartung H.P., Kappos L., Lublin F.D., Metz L.M., McFarland H.F., O'Connor P.W., Sandberg-Wollheim M., Thompson A.J., Weinshenker B.G., and Wolinsky J.S. Diagnostic criteria for multiple sclerosis: 2005 revisions to the "McDonald Criteria". Ann. Neurol. 58 (2005) 840-846
49. Qin Y., Duquette P., Zhang Y., Talbot P., Poole R., and Antel J. Clonal expansion and somatic hypermutation of V(H) genes of B cells from cerebrospinal fluid in multiple sclerosis. J. Clin. Invest. 102 (1998) 1045-1050
50. Ritchie A.M., Gilden D.H., Williamson R.A., Burgoon M.P., Yu X., Helm K., Corboy J.R., and Owens G.P. Comparative analysis of the CD19+ and CD138+ cell antibody repertoires in the cerebrospinal fluid of patients with multiple sclerosis. J. Immunol. 173 (2004) 649-656
51. Siritho S., and Freedman M.S. The prognostic significance of cerebrospinal fluid in multiple sclerosis. J. Neurol. Sci. 279 (2009) 21-25
52. Soderstrom M., Ya-Ping J., Hillert J., and Link H. Optic neuritis: prognosis for multiple sclerosis from MRI, CSF, and HLA findings. Neurology 50 (1998) 708-714
53. Stuve O., Cepok S., Elias B., Saleh A., Hartung H.P., Hemmer B., and Kieseier B.C. Clinical stabilization and effective B-lymphocyte depletion in the cerebrospinal fluid and peripheral blood of a patient with fulminant relapsing-remitting multiple sclerosis. Arch. Neurol. 62 (2005) 1620-1623
54. Stuve O., Bennett J.L., Hemmer B., Wiendl H., Racke M.K., Bar-Or A., Hu W., Zivadinov R., Weber M.S., Zamvil S.S., Pacheco M.F., Menge T., Hartung H.P., Kieseier B.C., and Frohman E.M. Pharmacological treatment of early multiple sclerosis. Drugs 68 (2008) 73-83
55. Tian C., Luskin G.K., Dischert K.M., Higginbotham J.N., Shepherd B.E., and Crowe Jr. J.E. Evidence for preferential Ig gene usage and differential TdT and exonuclease activities in human naive and memory B cells. Mol. Immunol. 44 (2007) 2173-2183
56. Tintore M., Rovira A., Martinez M.J., Rio J., Diaz-Villoslada P., Brieva L., Borras C., Grive E., Capellades J., and Montalban X. Isolated demyelinating syndromes: comparison of different MR imaging criteria to predict conversion to clinically definite multiple sclerosis. AJNR. Am. J. Neuroradiol. 21 (2000) 702-706
57. Tselis A., Perumal J., Caon C., Hreha S., Ching W., Din M., Van Stavern G., and Khan O. Treatment of corticosteroid refractory optic neuritis in multiple sclerosis patients with intravenous immunoglobulin. Eur. J. Neurol. 15 (2008) 1163-1167
58. Wardemann H., Yurasov S., Schaefer A., Young J.W., Meffre E., and Nussenzweig M.C. Predominant autoantibody production by early human B cell precursors. Science 301 (2003) 1374-1377
59. Yurasov S., Wardemann H., Hammersen J., Tsuiji M., Meffre E., Pascual V., and Nussenzweig M.C. Defective B cell tolerance checkpoints in systemic lupus erythematosus. J. Exp. Med. 201 (2005) 703-711