High production of CXCL13 in blood and brain during persistent infection with the relapsing fever spirochete Borrelia turicatae

Journal of Neuropathology and Experimental Neurology

Volumn 66, Issue 3, 2007, Pages 208-217

  Gelderblom, Harald ^a,b,c   Londoño, Diana ^a   Bai, Yunhong ^a   Cabral, Erik S ^b   Quandt, Jacqueline ^c   Hornung, Ron ^d   Martin, Roland ^c   Marques, Adriana ^b   Cadavid, Diego ^a,e  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^d SAIC FREDERICK INC   (United States)

^e MSB H506 ^*  (United States)

Author keywords

B cells; Borrelia; CXCL13; Interleukin 10; Neuroborreliosis; Relapsing fever; T cells

Indexed keywords

CXCL1 CHEMOKINE; CXCL13 CHEMOKINE; RECOMBINANT INTERLEUKIN 10; UNCLASSIFIED DRUG; ALPHA CHEMOKINE; CXCL13 PROTEIN, MOUSE; INTERLEUKIN 10; MESSENGER RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; BACTEREMIA; BORRELIA; BORRELIA INFECTION; BORRELIA TURICATAE; BRAIN INFECTION; BRAIN INJURY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE SEVERITY; FEMALE; GLIOSIS; HEART; LEPTOMENINX; MACROPHAGE ACTIVATION; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PARENCHYMA; PRIORITY JOURNAL; SINGLE DRUG DOSE; SPIROCHETE; T LYMPHOCYTE; UPREGULATION; ANIMAL; BIOSYNTHESIS; BRAIN; C57BL MOUSE; CLASSIFICATION; DNA MICROARRAY; DRUG EFFECT; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION REGULATION; METABOLISM; METHODOLOGY; MICROBIOLOGY; NONPARAMETRIC TEST; PATHOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; B-LYMPHOCYTES; BORRELIA; BORRELIA INFECTIONS; BRAIN; CHEMOKINES, CXC; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION REGULATION, BACTERIAL; HEART; INTERLEUKIN-10; MICE; MICE, INBRED C57BL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RELAPSING FEVER; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; STATISTICS, NONPARAMETRIC;

EID: 34247127789     PISSN: 00223069     EISSN: None     Source Type: Journal    
DOI: 10.1097/01.jnen.0000248556.30209.6d     Document Type: Article

References (33)

1. Cadavid D, Barbour AG. Neuroborreliosis during relapsing fever: Review of the clinical manifestations, pathology, and treatment of infections in humans and experimental animals. Clin Infect Dis 1998;26:151-64
2. Hinnebusch BJ, Barbour AG, Restrepo BI, Schwan TG. Population structure of the relapsing fever spirochete Borrelia hermsii as indicated by polymorphism of two multigene families that encode immunogenic outer surface lipoproteins. Infect Immun 1998;66:432-40
3. Cadavid D, Sondey M, Garcia E, Lawson CL. Residual brain infection in relapsing fever borreliosis. J Infect Dis 2006;193:1451-58
4. Newman K Jr, Johnson RC. T-cell-independent elimination of Borrelia turicatae. Infect Immun 1984;45:572-76
5. Cadavid D, Thomas DD, Crawley R, Barbour AG. Variability of a bacterial surface protein and disease expression in a possible mouse model of systemic Lyme borreliosis. J Exp Med 1994;179:631-42
6. Cadavid D, Pennington PM, Kerentseva TA, Bergstrom S, Barbour AG. Immunologic and genetic analyses of VmpA of a neurotropic strain of Borrelia turicatae. Infect Immun 1997;65:3352-60
7. Cadavid D, Pachner AR, Estanislao L, Patalapati R, Barbour AG. Isogenic serotypes of Borrelia turicatae show different localization in the brain and skin of mice. Infect Immun 2001;69:3389-97
8. Bosma MJ, Carroll AM. The SCID mouse mutant: Definition, characterization, and potential uses. Annu Rev Immunol 1991;9:323-50
9. Gelderblom H, Schmidt J, Londono D, et al. Role of interleukin 10 during persistent infection with Borrelia turicatae. Am J Pathol 2007;170:251-62
10. Pennington PM, Cadavid D, Barbour AG. Characterization of VspB of Borrelia turicatae, a major outer membrane protein expressed in blood and tissues of mice. Infect Immun 1999;67:4637-45
11. Cadavid D, Bundoc V, Barbour AG. Experimental infection of the mouse brain by a relapsing fever Borrelia species: A molecular analysis. J Infect Dis 1993;168:143-51
12. Barbour AG, Tessier SL, Stoenner HG. Variable major proteins of Borrellia hermsii. J Exp Med 1982;156:1312-24
13. Bai Y, Narayan K, Dail D, et al. Spinal cord involvement in the nonhuman primate model of Lyme disease. Lab Invest 2004;84:160-72
14. Hosack DA, Dennis G Jr, Sherman BT, Lane HC, Lempicki RA. Identifying biological themes within lists of genes with EASE. Genome Biol 2003;4:R70
15. Londoño D, Bai Y, Zuckert W, Cadavid D. Cardiac apoptosis in severe relapsing fever borreliosis. Infect Immun 2005;73:7669-76
16. Perry VH, Hume DA, Gordon S. Immunohistochemical localization of macrophages and microglia in the adult and developing mouse brain. Neuroscience 1985;15:313-26
17. Sethi N, Sondey M, Bai Y, Kim K, Cadavid D. Interaction of a neurotropic strain of Borrelia turicatae with the cerebral microcirculation system. Infect Immunity 2006;74:6408-18
18. Alugupalli KR, Gerstein RM, Chen J, Szomolanyi-Tsuda E, Woodland RT, Leong JM. The resolution of relapsing fever borreliosis requires IgM and is concurrent with expansion of B1b lymphocytes. J Immunol 2003;170:3819-27
19. Ruddle NH. Lymphoid neo-organogenesis: Lymphotoxin's role in inflammation and development. Immunol Res 1999;19:119-25
20. Amft N, Curnow SJ, Scheel-Toellner D, et al. Ectopic expression of the B cell-attracting chemokine BCA-1 (CXCL13) on endothelial cells and within lymphoid follicles contributes to the establishment of germinal center-like structures in Sjögren_s syndrome. Arthritis Rheum 2001;44:2633-41
21. Pachner AR, Dail D, Narayan K, Dutta K, Cadavid D. Increased expression of B-lymphocyte chemoattractant, but not pro-inflammatory cytokines, in muscle tissue in rhesus chronic Lyme borreliosis. Cytokine 2002;19:297-307
22. Cadavid D, Bai Y, Hodzic E, Narayan K, Barthold SW, Pachner AR. Cardiac involvement in non-human primates infected with the Lyme disease spirochete Borrelia burgdorferi. Lab Invest 2004;84:1439-50
23. Cadavid D. The mammalian host response to Borrelia infection. Wien Klin Wochenschr 2006;118:653-58.
24. Narayan K, Dail D, Li L, et al. The nervous system as ectopic germinal center: Production of CXCL13 and IgG in infected tissues in Lyme neuroborreliosis. Ann Neurol 2005;57:813-23
25. Rupprecht T, Pfister HW, Angele B, Kastenbauer S, Wilske B, Koedel U. The chemokine CXCL13 (BLC): A putative diagnostic marker for neuroborreliosis. Neurology 2005;65:448-50
26. Muellegger R, Means T, Lee M, Glickstein L, Lulster A, Steere A. High mRNA levels of the IFN-γ-inducible Th1-type chemokines, CXCL10 and CXCL9, in the lesional skin of patients with erythema migrans or acrodermatitis chronica atrophicans and of the B cell active chemokine, CXCL13, in borrelial lymphocytoma. Papers from the 10th International Conference on Lyme Borreliosis and Other Tick-Borne Diseases, Vienna, Austria, 2005
27. Shirato K, Kimura T, Mizutani T, Kariwa H, Takashima I. Different chemokine expression in lethal and non-lethal murine West Nile virus infection. J Med Virol 2004;74:507-13
28. Segal BM, Logigian EL. Sublime diagnosis of Lyme neuroborreliosis. Neurology 2005;65:351-52
29. Krumbholz M, Theil D, Cepok S, et al. Chemokines in multiple sclerosis: CXCL12 and CXCL13 up-regulation is differentially linked to CNS immune cell recruitment. Brain 2006;129:200-11
30. Gebbia JA, Monco JC, Degen JL, Bugge TH, Benach JL. The plasminogen activation system enhances brain and heart invasion in murine relapsing fever borreliosis. J Clin Invest 1999;103:81-87
31. Kloss CU, Bohatschek M, Kreutzberg GW, Raivich G. Effect of lipopolysaccharide on the morphology and integrin immunoreactivity of ramified microglia in the mouse brain and in cell culture. Exp Neurol 2001;168:32-46
32. + T-lymphocytes in vitro. Cell Immunol 2000;201:124-31
33. Larsson C, Andersson M, Pelkonen J, Guo BP, Nordstrand A, Bergstrom S. Persistent brain infection and disease reactivation in relapsing fever borreliosis. Microbes Infect 2006;8:2213-19