Blood γδ T cells, Campylobacter jejuni, and GM1 titers in Guillain–Barré syndrome
Corresponding Author
Stephen N. Scelsa MD
Department of Neurology, Beth Israel Medical Center, New York, New York, USA
Albert Einstein College of Medicine, Bronx, New York, USA
Beth Israel Medical Center, Phillips Ambulatory Care Center, 10 Union Square, Suite 2Q, New York, New York 10003Search for more papers by this authorViolette Ghali MD
Department of Immunology, Beth Israel Medical Center, New York, New York, USA
Search for more papers by this authorSteven Herskovitz MD
Department of Neurology, Montefiore Medical Center, Bronx, New York, USA
Search for more papers by this authorPhyllis Bieri MD
Department of Neurology, Montefiore Medical Center, Bronx, New York, USA
Search for more papers by this authorDeborah L. Shank MS
Department of Immunology, Beth Israel Medical Center, New York, New York, USA
Search for more papers by this authorDaniel D. J. MacGowan MD
Department of Neurology, Beth Israel Medical Center, New York, New York, USA
Albert Einstein College of Medicine, Bronx, New York, USA
Search for more papers by this authorSally Liau MS
Department of Immunology, Beth Israel Medical Center, New York, New York, USA
Search for more papers by this authorCorresponding Author
Stephen N. Scelsa MD
Department of Neurology, Beth Israel Medical Center, New York, New York, USA
Albert Einstein College of Medicine, Bronx, New York, USA
Beth Israel Medical Center, Phillips Ambulatory Care Center, 10 Union Square, Suite 2Q, New York, New York 10003Search for more papers by this authorViolette Ghali MD
Department of Immunology, Beth Israel Medical Center, New York, New York, USA
Search for more papers by this authorSteven Herskovitz MD
Department of Neurology, Montefiore Medical Center, Bronx, New York, USA
Search for more papers by this authorPhyllis Bieri MD
Department of Neurology, Montefiore Medical Center, Bronx, New York, USA
Search for more papers by this authorDeborah L. Shank MS
Department of Immunology, Beth Israel Medical Center, New York, New York, USA
Search for more papers by this authorDaniel D. J. MacGowan MD
Department of Neurology, Beth Israel Medical Center, New York, New York, USA
Albert Einstein College of Medicine, Bronx, New York, USA
Search for more papers by this authorSally Liau MS
Department of Immunology, Beth Israel Medical Center, New York, New York, USA
Search for more papers by this authorAbstract
The γδ T cells participate in microbial defense, are prevalent in intestinal epithelia, and are activated in autoimmune diseases. We studied whether peripheral blood γδ cells and γδ subsets are increased in Guillain–Barré syndrome (GBS) and whether elevations are associated with Campylobacter jejuni infection or GM1 elevations. In 20 GBS patients, we performed serial flow cytometry studies of blood γδ, Vδ1, and Vδ2 cells (±CD8+), C jejuni, and ganglioside titers. There was no significant difference in median γδ T-cell percentages between GBS patients and controls at onset and at convalescence. However, 5 patients had marked Vδ1/CD8+ elevations. Elevated Vδ1 or Vδ1/CD8+ cells occurred in 3 of 6 patients with C jejuni or GM1 titer elevations. A minority of GBS patients have elevations of Vδ1/CD8+ cells, possibly associated with elevated C jejuni or GM1 titers. The γδ T cells may have a cytotoxic (or suppressor) role in the disease. Muscle Nerve 30: 423–432, 2004
REFERENCES
- 1 Albers JW, Donofrio PD, McGonagle TK. Sequential electrodiagnostic abnormalities in acute inflammatory demyelinating polyradiculoneuropathy. Muscle Nerve 1985; 8: 528–539.
- 2 Andreu JL, Trujillo A, Alonso JM, Mulero J, Martinez-A C. Selective expansion of T-cells bearing γδ receptor and expressing an unusual repertoire in the synovial membrane of patients with rheumatoid arthritis. Arthritis Rheum 1991; 7: 808–814.
- 3 Ang CW, Noordzij PG, de Klerk MA, Endtz HP, van Doorn PA, Laman JD. Ganglioside mimicry of Campylobacter jejuni lipopolysaccharides determines antiganglioside specificity in rabbits. Infect Immun 2002; 70: 5081–5085.
- 4 Asbury AK, Cornblath DR. Assessment of current diagnostic criteria for Guillain–Barré syndrome. Ann Neurol 1990; 27(Suppl): S21–S24.
- 5 Aspinall GO, McDonald AG, Pang H, Kurjanczyk LA, Penner JL. Lipopolysaccharides of Campylobacter jejuni serotype O:19: structures of core oligosaccharide regions from the serostrain and two bacterial isolates from patients with the Guillain–Barré syndrome. Biochemistry 1994; 33: 241–249.
- 6 Battistini L, Selmaj K, Kowal C, Ohmen J, Modlin RL, Raine CS, Brosnan CF. Multiple sclerosis: limited diversity of the V 2-J 3 T-cell receptor in chronic active lesions. Ann Neurol 1995; 37: 198–203.
- 7 Bauer S, Groh V, Wu J, Steinle A, Phillips JH, Lanier LL, Spies T. Activation of NK cells and T-cells by NKG2D, a receptor for stress inducible MICA. Science 1999; 285: 727–729.
- 8 Ben-Smith A, Gaston JSH, Barber PC, Winer JB. Isolation and characterisation of T lymphocytes from sural nerve biopsies in patients with Guillain–Barré syndrome and chronic inflammatory demyelinating polyneuropathy. J Neurol Neurosurg Psychiatry 1996; 61: 362–368.
- 9 Ben-Smith A, Goodall JC, Gaston JSH, Winer JB. Stimulation of peripheral blood lymphocytes with Campylobacter jejuni generates a gamma delta T-cell response in patients with Guillain–Barré syndrome. Clin Exp Immunol 1997; 109: 121–126.
- 10 Borsellino G, Poccia F, Placido R, Tramonti D, Mancino G, Luchetti S, Galgani S, Bonetti B, Bach S, Cipriani B, Brosnan CF, Battistini L. Phenotypic and functional properties of gamma delta T-cells from patients with Guillain–Barré syndrome. J Neuroimmunol 2000; 102: 199–207.
- 11 Bucy RP, Chen CH, Cooper MD. Tissue localization and CD8 accessory molecule expression of T γδ cells in humans. J Immunol 1989; 142: 3045–3049.
- 12 Chien Y, Jores R. T-cells with B-cell–like recognition properties. Curr Biol 1995; 5: 1116–1118.
- 13 Cooper JC, Ben-Smith A, Savage COS, Winer JB. Unusual T-cell receptor phenotype V gene usage of gamma delta T-cells in a line derived from the peripheral nerve of a patient with Guillain–Barré syndrome. J Neurol Neurosurg Psychiatry 2000; 69: 522–524.
- 14 Fujihashi K, Taguchi T, Aicher WK, McGhee JR, Bluestone JA, Eldridge JH, Kiyono H. Immunoregulatory functions for murine intraepithelial lymphocytes: γδ T-cell receptor-positive (TCR+) T-cells abrogate oral tolerance, while αβ TCR+ T-cells provide B cell help. J Exp Med 1992; 175: 695–707.
- 15 Fujioka T, Purev E, Kremlev SG, Ventura ES, Rostami A. Flow cytometric analysis of infiltrating cells in peripheral nerves in experimental allergic neuritis. J Neuroimmunol 2000; 108: 181–191.
- 16 Gao YL, Rajan AJ, Raine CS, Brosnan CF. Gamma delta T-cells express activation markers in the central nervous system of mice with chronic-relapsing experimental autoimmune encephalomyelitis. J Autoimmun 2001; 17: 261–271.
- 17 Guillain–Barré syndrome study group. Plasmapheresis and acute Guillain–Barré syndrome. Neurology 1985; 35: 1096–1104.
- 18 Hadden RD, Gregson NA, Gold R, Willison HJ, Hughes RA. Guillain–Barré syndrome serum and anti-Campylobacter antibody do not exacerbate experimental autoimmune neuritis. J Neuroimmunol 2001; 119: 306–316.
- 19 Hadden RD, Karch H, Hartung HP, Zielasek J, Weissbrich B, Schubert J, Weishaupt A, Cornblath DR, Swan AV, Hughes RA, Toyka KV, Plasma Exchange/Sandoglobulin Guillain–Barré Syndrome Trial Group. Preceding infections, immune factors, and outcome in Guillain–Barré syndrome. Neurology 2001; 56: 758–765.
- 20 Hamzaoui K, Hamzaoui A, Hentati F, Kahan A, Ayed K, Chabbou A, Ben Hamida M, Hamza M. Phenotype and functional profile of T-cells expressing γδ receptor from patients with active Behcet's disease. J Rheumatol 1994; 21: 2301–2306.
- 21 Hara T, Mizuno Y, Takaki K, Takada H, Akeda H, Aoki T, Nagata M, Ueda K, Matsuzaki G, Yoshikai Y. Predominant activation and expansion of V 9-bearing γδ T-cells in vivo as well as in vitro in salmonella infection. J Clin Invest 1992; 90: 204–210.
- 22 Hayday A, Geng L. Gamma delta T-cells regulate autoimmunity. Curr Opin Immunol 1997; 9: 884–889.
- 23 Ho TW, Mishu B, Li CY, Gao CY, Cornblath DR, Griffin JW, Asbury AK, Blaser MJ, McKhann GM. Guillain–Barré syndrome in northern China: relationship to Campylobacter jejuni infection and anti-glycolipid antibodies. Brain 1995; 118: 597–605.
- 24 Hohlfeld R, Engel AG. The role of gamma-delta T lymphocytes in inflammatory muscle disease. Chem Immunol 1992; 53: 75–85.
- 25 Hohfeld R, Engel AG, Ii K, Harper MC. Polymyositis mediated by T lymphocytes that express the gamma-delta receptor. N Engl J Med 1991; 324: 877–881.
- 26 Holoshitz J, Konig F, Coligan JE, De Bruyn J, Strober S. Isolation of CD4- CD8- mycobacteria–reactive T lymphocyte clones from rheumatoid arthritis synovial fluid. Nature 1989; 339: 226–229.
- 27 Hughes RA, Hadden RD, Gregson NA, Smith KJ. Pathogenesis of Guillain–Barré syndrome. J Neuroimmunol 1999; 100: 74–97.
- 28
Hughes RAC,
Newsom-Davis JM,
Perkin GD,
Pierce JM.
Controlled trial of prednisolone in acute polyneuropathy.
Lancet
1978;
7:
750–753.
10.1016/S0140-6736(78)92644-2 Google Scholar
- 29 Kabelitz D. Human Gamma Delta T-cells. Int Arch Allergy Immunol 1993; 102: 1–9.
- 30 Kabelitz D, Bender A, Schonelmaier S, Schoel B, Kaufman SHE. A large fraction of human peripheral blood γδ+ T-cells is activated by mycobacterium tuberculosis but not by its 65-kD heat shock protein. J Exp Med 1990; 171: 667–679.
- 31 Kaufman SHE. Gamma delta and other unconventional T lymphocytes: what do they see and what do they do? Proc Natl Acad Sci USA 1996; 93: 2272–2279.
- 32 Kleyweg RP, van der Meche FGA, Schmitz PIM. Interobserver agreement in the assessment of muscle strength and functional abilities in Guillain–Barré syndrome. Muscle Nerve 1991; 14: 1103–1109.
- 33 Kornberg AJ, Pestronk A, Bieser K, Ho TW, McKhann GM, Wu HS, Jiang Z. The clinical correlates of high titer IgG anti-GM1 antibodies. Ann Neurol 1994; 35: 234–237.
- 34 Kornblatt AN, Barrett T, Morris GK, Tosh FE. Epidemiologic and laboratory investigation of an outbreak of Campylobacter enteritis associated with raw milk. Am J Epidemiol 1985; 122: 884–889.
- 35 Li CY, Xue P, Tian WQ, Liu RC, Yang C. Experimental Campylobacter jejuni infection in the chicken: an animal model of axonal Guillain–Barré syndrome. J Neurol Neursurg Psych 1996; 61: 279-284.
- 36 Mishu B, Ilyas AA, Koski CL, Vriesendorp F, Cook SD, Mithen F, Blaser MJ. Serologic evidence of previous campylobacter jejuni infection in patients with the Guillain–Barré syndrome. Ann Intern Med 1993; 118: 947–953.
- 37 Morita CT, Beckman EM, Bukowski JF, Tanaka Y, Band H, Bloom BR, Golan DE, Brenner MB. Direct presentation of nonpeptide prenyl pyrophosphate antigens to human gamma delta T-cells. Immunity 1995; 3: 495–507.
- 38 Munk ME, Gatrill A, Kaufman SHE. Target cell lysis and IL-2 secretion by γδ T lymphocytes after activation with bacteria. J Immunol 1990; 145: 2435–2439.
- 39 Nachamkin I, Enberg J, Gutacker M, Meinersman RJ, Li CY, Arzate P, Teeple E, Fussing V, Ho TW, Asbury AK, Griffin JW, McKhann GM, Piffaretti JC. Molecular population genetic analysis of Campylobacter jejuni HS:19 associated with Guillain–Barré syndrome and gastroenteritis. J Infect Dis 2001; 184: 221–226.
- 40 Oomes PG, Jacobs BC, Hazenberg MPH, Bänffer JRJ, van der Meché FGA. Anti-GM1 IgG antibodies and campylobacter bacteria in Guillain–Barré syndrome: evidence of molecular mimicry. Ann Neurol 1995; 38: 170–175.
- 41 Poggi A, Zocchi MR, Costa P, Ferrero E, Borsellino G, Placido R, Galgani S, Salvetti, Gasperini C, Ristori G, Brosnan CF, Battistini L. IL-12-mediated NKRP1A up-regulation and consequent enhancement of endothelial transmigration of Vδ2+ TCR+ T lymphocytes from healthy donors and multiple sclerosis patients. J Immunol 1999; 162: 4349–4354.
- 42 Rajan AJ, Gao Y-L, Raine CS, Brosnan CF. A pathogenic role for gamma delta T-cells in relapsing–remitting experimental allergic encephalomyelitis in the SJL mouse. J Immunol 1996; 157: 941–949.
- 43 Rees JH, Gregson NA, Hughes RAC. Anti-ganglioside GM1 antibodies in Guillain–Barré syndrome and their relationship to Campylobacter jejuni infection. Ann Neurol 1995; 38: 809–816.
- 44 Rees JH, Soudain SE, Gregson NA, Hughes RAC. Campylobacter jejuni infection and Guillain–Barré syndrome. N Engl J Med 1995; 333: 1374–1379.
- 45 Roura-Mir IC, Alcalde L, Vargas F, Tolosa E, Obiols G, Foz M, Jaraquemada D, Pujol-Borrell R. Gamma delta lymphocytes in endocrine autoimmunity: evidence of expansion in Graves' disease but not in type 1 diabetes. Clin Exp Immunol 1993; 92: 288–295.
- 46 Roussilhon C, Agrapart M, Ballet JJ, Bensusan A. T lymphocytes bearing the γδ T-cell receptor in patients with acute Plasmodium falciparum malaria. J Infect Dis 1990; 162: 283–285.
- 47 Stinissen P, Vandevyver C, Medaer R, Vandegaer L, Nies J, Tuyls L, Hafler DA, Raus J, Zhang J. Increased frequency of γδ T-cells in cerebrospinal fluid and peripheral blood of patients with multiple sclerosis. Reactivity, cytotoxicity, and T-cell receptor V gene rearrangements. J Immunol 1995; 154: 4883–4894.
- 48 Wen L, Hayday AC. Gamma delta T-cell help in responses to pathogens and in the development of systemic autoimmunity. Immunol Res 1997; 16: 229–241.
- 49 Willison HJ, Yuki N. Peripheral neuropathies and anti-glycolipid antibodies. Brain 2002; 125: 2591–2625.
- 50 Yuki N, Taki T, Inagaki F, Kasama T, Takahashi M, Saito K, Handa S, Miyatake T. A bacterium lipopolysaccharide that elicits Guillain–Barré syndrome has a GM1 ganglioside-like structure. J Exp Med 1993; 178: 1771–1775.