Lymphocyte phenotypes in wild-caught rats suggest potential mechanisms underlying increased immune sensitivity in post-industrial environments

Cellular and Molecular Immunology

Volumn 9, Issue 2, 2012, Pages 163-174

  Trama, Ashley M ^a   Holzknecht, Zoie E ^a   Thomas, Anitra D ^a   Su, Kuei Ying ^a   Lee, Sean M ^a   Foltz, Emily E ^a   Perkins, Sarah E ^b   Lin, Shu S ^a   Parker, William ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

allergy; autoimmunity; biome; hygiene; immune regulation

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; CELL ADHESION; CELL INTERACTION; CELL MATURATION; CELLULAR IMMUNITY; CONTROLLED STUDY; FEMALE; IMMUNE ADHERENCE; IMMUNOASSAY; IMMUNOPHENOTYPING; IMMUNOREACTIVITY; INTRACELLULAR SIGNALING; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE FUNCTION; MALE; NONHUMAN; PHENOTYPIC VARIATION; RAT; REGULATORY T LYMPHOCYTE; SENSITIVITY ANALYSIS; T LYMPHOCYTE SUBPOPULATION; UPREGULATION; WILD ANIMAL;

ANIMALS; ANIMALS, WILD; CELL ADHESION; CELL DIFFERENTIATION; CELL SEPARATION; COMPLEMENT ACTIVATION; FLOW CYTOMETRY; IMMUNIZATION; IMMUNOPHENOTYPING; INDUSTRY; RATS; RATS, INBRED STRAINS; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY;

RATTUS; RATTUS NORVEGICUS;

EID: 84863282038     PISSN: 16727681     EISSN: None     Source Type: Journal    
DOI: 10.1038/cmi.2011.61     Document Type: Article

References (73)

1. Borkow G, Leng Q, Weisman Z, Stein M, Galai N, Kalinkovich A et al. Chronic immune activation associated with intestinal helminth infections results in impaired signal transduction and anergy. J Clin Invest 2000; 106: 1053-1060.
2. Worldwide variation in prevalence of symptoms of asthma, allergic rhinoconjunctivitis, andatopic eczema: ISAAC. The International Study of Asthma and Allergies in Childhood (ISAAC) Steering Committee.[see comment]. Lancet 2005; 351: 1225-1232.
3. Onkamo P, Vaananen S, Karvonen M, Tuomilehto J. Worldwide increase in incidence of Type I diabetes-the analysis of the data on published incidence trends. Diabetologia 1999; 42: 1395-1403. (Pubitemid 30012309)
4. Black P. Why is the prevalence of allergy and autoimmunity increasing? Trends Immunol 2001; 22: 354-355. (Pubitemid 32673638)
5. Gergen PJ, Turkeltaub PC, Kovar MG. The prevalence of allergic skin test reactivity to eight common aeroallergens in the U.S. population: results from the second National Health and Nutrition Examination Survey. J Allergy Clin Immunol 1987; 80: 669-679. (Pubitemid 18025834)
6. Maizels RM, Bundy DA, Selkirk ME, Smith DF, Anderson RM. Immunological modulation and evasion by helminth parasites in human populations. Nature 1993; 365: 797-805. (Pubitemid 23341023)
7. Gale EA. A missing link in the hygiene hypothesis?[see comment]. Diabetologia 2002; 45: 588-594.
8. Yazdanbakhsh M, Kremsner PG, van Ree R. Allergy, parasites, and the hygiene hypothesis. Science 2002; 296: 490-494.
9. Holt PG. Parasites, atopy, and the hygiene hypothesis: resolution of a paradox?[see comment][comment]. Lancet 2000; 356: 1699-701.
10. de Borst MH, de Boer RA, Stolk RP, Slaets JP, Wolffenbuttel BH, Navis G. Vitamin D deficiency: universal risk factor for multifactorial diseases? Curr Drug Targets 2011; 12: 97-106.
11. Bilbo SD, Wray GA, Perkins SE, Parker W. Reconstitution of the human biome as the most reasonable solution for epidemics of allergic and autoimmune diseases. Med Hypotheses 2011; 77: 494-504.
12. Bickler SW, DeMaio A. Western diseases: current concepts and implications for pediatric surgery research and practice. Pediatr Surg Int 2008; 24: 251-255.
13. Capron A, Dombrowicz D, Capron M. Helminth infections and allergic diseases. Clin Rev Allergy Immunol 2004; 26: 25-34.
14. Wilson MS, Maizels RM. Regulation of allergy and autoimmunity in helminth infection. Clin Rev Allergy Immunol 2004; 24: 35-50. (Pubitemid 38333737)
15. Fumagalli M, Pozzoli U, Cagliani R, Comi GP, Riva S, Clerici M et al. Parasites represent a major selective force for interleukin genes and shape the genetic predisposition to autoimmune conditions. J Exp Med 2009; 206: 1395-1408.
16. Rook GA. Review series on helminths, immune modulation and the hygiene hypothesis: the broader implications of the hygiene hypothesis. Immunology 2009; 126: 3-11.
17. Correale J, Farez M. Association between parasite infection and immune responses in multiple sclerosis. Ann Neurol 2007; 61: 97-108. (Pubitemid 46363837)
18. Summers RW, Elliott DE, Qadir K, Urban JF Jr, Thompson R, Weinstock JV. Trichuris suis seems to be safe and possibly effective in the treatment of inflammatory bowel disease.[see comment]. Am J Gastroenterol 2003; 98: 2034-2041. (Pubitemid 37185802)
19. Imai S, Fujita K. Molecules of parasites as immunomodulatory drugs. Curr Top Med Chem 2004; 4: 539-552. (Pubitemid 38832737)
20. Hewitson JP, Grainger JR, Maizels RM. Helminth immunoregulation: the role of parasite secreted proteins in modulating host immunity. Mol Biochem Parasitol 2009; 167: 1-11.
21. Poinar G Jr, Boucot AJ. Evidence of intestinal parasites of dinosaurs. Parasitology 2006; 133: 245-249. (Pubitemid 44099912)
22. Hurtado AM, Frey MA, Hill K, Baker J. The role of helminths in human evolution. Implications for global health in the 21st century. In: Elton S, O'Higgins P (ed.) Medicine and Evolution: Current Applications, Future Prospects. New York: Taylor &Francis, 2008: 153-180.
23. Wilson MS, Maizels RM. Regulatory T cells induced by parasites and the modulation of allergic responses. Chem Immunol Allergy 2006; 90: 176-195. (Pubitemid 43265675)
24. Lesher A, Li B, Whitt P, Newton N, Devalapalli AP, Shieh K et al. Increased IL-4 production and attenuated proliferative and proinflammatory responses of splenocytes from wild-caught rats (Rattus norvegicus). Immunol Cell Biol 2006; 84: 374-382. (Pubitemid 43882843)
25. Devalapalli AP, Lesher A, Shieh K, Solow JS, Everett ML, Edala AS et al. Increased Levels of IgE and autoreactive, polyreactive IgG in wild rodents: implications for the hygiene hypothesis. Scand J Immunol 2006; 64: 125-136. (Pubitemid 44034316)
26. Hewitt JK, Fulker DW, Broadhurst PL. Genetics of escape avoidance conditioning in laboratory and wild populations of rats a biometrical approach. Behav Genet 1981; 11: 533-544. (Pubitemid 12164855)
27. Ashwood P, Wills S, van de Water J. The immune response in autism: a new frontier for autism research. J Leukoc Biol 2006; 80: 1-15. (Pubitemid 44841805)
28. Becker KG. Autism, asthma, inflammation, and the hygiene hypothesis. Med Hypotheses 2007; 69: 731-740. (Pubitemid 47260665)
29. Vargas DL, Nascimbene C, Krishnan C, Zimmerman AW, Pardo CA. Neuroglial activation and neuroinflammation in the brain of patients with autism. Ann Neurol 2005; 57: 67-81. (Pubitemid 40053317)
30. Miller RG. Simultaneous Statistical Inference. 2nd ed. New York: Springer-Verlag, 1981: 6-8.
31. Nolte-'t Hoen EN, Boot EP, Wagenaar-Hilbers JP, van Bilsen JH, Arkesteijn GJ, Storm G et al. Identification and monitoring of effector and regulatory T cells during experimental arthritis based on differential expression of CD25 and CD134. J Leukoc Biol 2008; 83: 112-121.
32. Abolins SR, Pocock MJ, Hafalla JC, Riley EM, Viney ME. Measures of immune function of wild mice, Mus musculus. Mol Ecol 2011; 20: 881-892.
33. Monteseirin J, Llamas E, Sanchez-Monteseirin H, Bonilla I, Camacho MJ, Conde J et al. IgE-mediated downregulation of L-selectin (CD62L) on lymphocytes from asthmatic patients. Allergy 2001; 56: 164-168. (Pubitemid 32115768)
34. Li O, Liu JQ, Zhang H, Zheng P, Liu Y, Bai XF. CD62L is required for the priming of encephalitogenic T cells but does not play a major role in the effector phase of experimental autoimmune encephalomyelitis. Scand J Immunol 2006; 64: 117-124. (Pubitemid 44034315)
35. Grewal IS, Foellmer HG, Grewal KD, Wang H, Lee WP, Tumas D et al. CD62L is required on effector cells for local interactions in the CNS to cause myelin damage in experimental allergic encephalomyelitis. Immunity 2001; 14: 291-302. (Pubitemid 32289293)
36. Meddows-Taylor S, Kuhn L, Meyers TM, Tiemessen CT. Altered expression of Lselectin (CD62L) on polymorphonuclear neutrophils of children vertically infected with human immunodeficiency virus type 1. J Clin Immunol 2001; 21: 286-292. (Pubitemid 32652601)
37. Schleiffenbaum B, Spertini O, Tedder TF. Soluble L-selectin is present in human plasma at high levels and retains functional activity. J Cell Biol 1992; 119: 229-238.
38. Hanna SM, Spiller OB, Linton SM, Mead RJ, Morgan BP. Rat T cells express neither CD55 nor CD59 and are dependent on Crry for protection from homologous complement. Eur J Immunol 2002; 32: 502-509. (Pubitemid 34173342)
39. Friese MA, Jones EY, Fugger L. MHC II molecules in inflammatory diseases: interplay of qualities and quantities. Trends Immunol 2005; 26: 559-561. (Pubitemid 41726441)
40. de Bara R, Kusuda M, Caspers-Velu L, Sanui H, Chan CC, Kuwabara T et al. Cryopexy enhances experimental autoimmune uveoretinitis (EAU) in rats. Invest Ophthalmol Vis Sci 1989; 30: 2165-2173. (Pubitemid 19259920)
41. Jimenez E, Sacedon R, Vicente A, Hernandez-Lopez C, Zapata AG, Varas A. Rat peripheral CD41CD81 T lymphocytes are partially immunocompetent thymusderived cells that undergo post-thymic maturation to become functionally mature CD41 T lymphocytes. J Immunol 2002; 168: 5005-5013. (Pubitemid 34495963)
42. Yang CP, Bell EB. Functional maturation of recent thymic emigrants in the periphery: development of alloreactivity correlates with the cyclic expression of CD45RC isoforms. Eur J Immunol 1992; 22: 2261-2269.
43. Acton RT, Morris RJ, Williams AF. Estimation of the amount and tissue distribution of rat Thy-1.1 antigen. Eur J Immunol 1974; 4: 598-602.
44. Takacs L, Osawa H, Toro I, Diamantstein T. Immunohistochemical localization of cells reacting with monoclonal antibodies directed against the interleukin-2 receptor of murine, rat and human origin. Clin Exp Immunol 1985; 59: 37-44. (Pubitemid 15197392)
45. Takacs L, Ruscetti FW, Kovacs EJ, Rocha B, Brocke S, Diamantstein T et al. Immature, double negative (CD42,CD82) rat thymocytes do not express IL-2 receptors. J Immunol 1988; 141: 3810-3818.
46. Deng J, Dekruyff RH, Freeman GJ, Umetsu DT, Levy S. Critical role of CD81 in cognate T-B cell interactions leading to Th2 responses. Int Immunol 2002; 14: 513-523. (Pubitemid 34521073)
47. Shoham T, Rajapaksa R, Boucheix C, Rubinstein E, Poe JC, Tedder TF et al. The tetraspanin CD81 regulates the expression of CD19 during B cell development in a postendoplasmic reticu lum compartment. J Immunol 2003; 171: 4062-4072. (Pubitemid 37238681)
48. Maecker HT, Do MS, Levy S. CD81 on B cells promotes interleukin 4 secretion and antibody production during T helper type 2 immune responses. Proc Natl Acad Sci USA 1998; 95: 2458-2462. (Pubitemid 28145963)
49. Nakagawa S, Arai Y, Mori H, Matsushita Y, Kubo T, Nakanishi T. Small interfering RNA targeting CD81 ameliorated arthritis in rats. Biochem Biophys Res Commun 2009; 388: 467-472.
50. Dijkstra S, Kooij G, Verbeek R, van der Pol SMA, Amor S, Geisert EE Jr et al. Targeting the tetraspanin CD81 blocks monocyte transmigration and ameliorates EAE. Neurobiol Dis 2008; 31: 413-421.
51. Maecker HT, Todd SC, Kim EC, Levy S. Differential expression of murine CD81 highlighted by new anti-mouse CD81 monoclonal antibodies. Hybridoma 2000; 19: 15-22. (Pubitemid 30184967)
52. Nagafuchi H, Shimoyama Y, Kashiwakura J, Takeno M, Sakane T, Suzuki N. Preferential expression of B7.2 (CD86), but not B7.1 (CD80), on B cells induced by CD40/CD40L interaction is essential for anti-DNA autoantibody production in patients with systemic lupus erythematosus. Clin Exp Rheumatol 2003; 21: 71-77. (Pubitemid 36267534)
53. Folzenlogen D, Hofer MF, Leung DY, Freed JH, Newell MK. Analysis of CD80 and CD86 expression on peripheral blood B lymphocytes reveals increased expression of CD86 in lupus patients. Clin Immunol Immunopathol 1997; 83: 199-204. (Pubitemid 27244306)
54. Podojil JR, Sanders VM. CD86 and beta2-adrenergic receptor stimulation regulate Bcell activity cooperatively. Trends Immunol 2005; 26: 180-185. (Pubitemid 41556854)
55. Kasprowicz DJ, Kohm AP, Berton MT, Chruscinski AJ, Sharpe A, Sanders VM. Stimulation of the B cell receptor, CD86 (B7-2), and the beta 2-adrenergic receptor intrinsically modulates the level of IgG1 and IgE produced per B cell. J Immunol 2000; 165: 680-690. (Pubitemid 30484733)
56. Webster JP, Macdonald DW. Parasites of wild brown rats (Rattus norvegicus) on UK farms. Parasitology 1995; 111: 247-255.
57. Easterbrook JD, Kaplan JB, Glass GE, Watson J, Klein SL. A survey of rodent-borne pathogens carried by wild-caught Norway rats: a potential threat to laboratory rodent colonies. Lab Anim 2008; 42: 92-98. (Pubitemid 351547531)
58. Ogilvie BM, Askenase PW, Rose E. Basophils and eosinophils in 3 strains of rats and in athymic nude rats following infection with the nematodes Nippostrongylus brasiliensis or Trichinella spiralis. Immunology 1980; 39: 385-90.
59. Baker DG. Natural pathogens of laboratory mice, rats, and rabbits and their effects on research. Clin Microbiol Rev 1998; 11: 231-266. (Pubitemid 28197353)
60. Perec-Matysiak A, Okulewicz A, Hildebrand J, Zalesny G. Helminth parasites of laboratory mice and rats. Wiad Parazytol 2006; 52: 99-102.
61. Matalka KZ. Neuroendocrine and cytokines-induced responses to minutes, hours, and days of mental stress. Neuroendocrinol Lett 2003; 24: 283-292. (Pubitemid 37368835)
62. Reiche EM, Nunes SO, Morimoto HK. Stress, depression, the immune system, and cancer. Lancet Oncol 2004; 5: 617-625. (Pubitemid 39303129)
63. Stojanovich L, Marisavljevich D. Stress as a trigger of autoimmune disease. Autoimmun Rev 2008; 7: 209-213.
64. Os'kina IN, Shikhevich SG, Karyagina AY, Gulevich RG. Humoral immune response in norway rats selected for behavior. Dokl Biol Sci 2001; 378: 277-279.
65. Lafferty KD. Microbiology. Interacting parasites. Science 2010; 330: 187-188.
66. Curry AJ, Else KJ, Jones F, Bancroft A, Grencis RK, Dunne DW. Evidence that cytokinemediated immune interactions induced by Schistosoma mansoni alter disease outcome in mice concurrently infected with Trichuris muris. J ExpMed 1995; 181: 769-774.
67. Graham AL. Ecological rules governing helminth-microparasite coinfection. Proc Natl Acad Sci USA 2008; 105: 566-570. (Pubitemid 351171748)
68. Wellicome SM, Kapahi P, Mason JC, Lebranchu Y, Yarwood H, Haskard DO. Detection of a circulating form of vascular cell adhesion molecule-1: raised levels in rheumatoid arthritis and systemic lupus erythematosus. Clin Exp Immunol 1993; 92: 412-418. (Pubitemid 23183748)
69. van Den Engel NK, Heidenthal E, Vinke A, Kolb H, Martin S. Circulating forms of intercellular adhesion molecule (ICAM)-1 in mice lacking membranous ICAM-1. Blood 2000; 95: 1350-1355. (Pubitemid 30099846)
70. Martin S, Rieckmann P, Melchers I, Wagner R, Bertrams J, Voskuyl AE et al. Circulating forms of ICAM-3 (cICAM-3). Elevated levels in autoimmune diseases and lack of association with cICAM-1. J Immunol 1995; 154: 19 51-1955.
71. Hamzaoui A, Hamzaoui K, Kahan A, Chabbou A. Levels of soluble VCAM-1, soluble ICAM-1 and soluble E-selectin in patients with tuberculous pleuritis. Mediat Inflamm 1996; 5: 276-279. (Pubitemid 26341999)
72. Koraka P, Murgue B, Deparis X, van Gorp EC, Setiati TE, Osterhaus AD et al. Elevation of soluble VCAM-1 plasma levels in children with acute dengue virus infection of varying severity. J Med Virol 2004; 72: 445-450. (Pubitemid 38133985)
73. Davis MM. A prescription for human immunology. Immunity 2008; 29: 835-838.