Multiple innate antibacterial immune defense elements are correlated in diverse ungulate species
Autoři:
Brian S. Dugovich aff001; Lucie L. Crane aff002; Benji B. Alcantar aff002; Brianna R. Beechler aff002; Brian P. Dolan aff002; Anna E. Jolles aff002
Působiště autorů:
Department of Integrative Biology, Oregon State University, Corvallis, OR, United States of America
aff001; Department of Biomedical Sciences, Oregon State University, Corvallis, OR, United States of America
aff002; Wildlife Safari, Winston, OR, United States of America
aff003
Vyšlo v časopise:
PLoS ONE 14(11)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0225579
Souhrn
In this study, we aimed to evaluate to what extent different assays of innate immunity reveal similar patterns of variation across ungulate species. We compared several measures of innate antibacterial immune function across seven different ungulate species using blood samples obtained from captive animals maintained in a zoological park. We measured mRNA expression of two receptors involved in innate pathogen detection, toll-like receptors 2 and 5 (TLR2 and 5), the bactericidal capacity of plasma, as well as the number of neutrophils and lymphocytes. Species examined included aoudad (Ammotragus lervia), American bison (Bison bison bison), yak (Bos grunniens), Roosevelt elk (Cervus canadensis roosevelti), fallow deer (Dama dama), sika deer (Cervus nippon), and Damara zebra (Equus quagga burchellii). Innate immunity varied among ungulate species. However, we detected strong, positive correlations between the different measures of innate immunity–specifically, TLR2 and TLR5 were correlated, and the neutrophil to lymphocyte ratio was positively associated with TLR2, TLR5, and bacterial killing ability. Our results suggest that ecoimmunological study results may be quite robust to the choice of assays, at least for antibacterial innate immunity; and that, despite the complexity of the immune system, important sources of variation in immunity in natural populations may be discoverable with comparatively simple tools.
Klíčová slova:
Immune response – Blood plasma – White blood cells – Polymerase chain reaction – Lymphocytes – Antibacterials – Neutrophils – Toll-like receptors
Zdroje
1. Medzhitov R, Janeway CA. Innate immunity: Impact on the adaptive immune response. Curr Opin Immunol. 1997;9: 4–9. doi: 10.1016/s0952-7915(97)80152-5 9039775
2. Gabay C, Kushner I. Mechanisms of disease: Acute-phase proteins and other systemic responses to inflammation. N Engl J Med. 1999;340: 448–454. doi: 10.1056/NEJM199902113400607 9971870
3. Kawai T, Akira S. The roles of TLRs, RLRs and NLRs in pathogen recognition. Int Immunol. 2009;21: 317–337. doi: 10.1093/intimm/dxp017 19246554
4. Brubaker SW, Bonham KS, Zanoni I, Kagan JC. Innate Immune Pattern Recognition: A Cell Biological Perspective. Annual Review of Immunology Vol 33. 2015;33: 257–290. doi: 10.1146/annurev-immunol-032414-112240 25581309
5. Silva MT, Correia-Neves M. Neutrophils and macrophages: the main partners of phagocyte cell systems. Front Immunol. 2012;3. doi: 10.3389/fimmu.2012.00174 22783254
6. Demas GE, Zysling DA, Beechler BR, Muehlenbein MP, French SS. Beyond phytohaemagglutinin: assessing vertebrate immune function across ecological contexts. J Anim Ecol. 2011;80: 710–730. doi: 10.1111/j.1365-2656.2011.01813.x 21401591
7. Downs CJ, Stewart KM. A primer in ecoimmunology and immunology for wildlife research and management. Calif Fish Game. 2014;100: 371–395.
8. de Oliviera Nascimento L, Massari P, Wetzler L. The Role of TLR2 in Infection and Immunity. Front Immunol. 2012;3. doi: 10.3389/fimmu.2012.00079 22566960
9. Yoon SI, Kurnasov O, Natarajan V, Hong MS, Gudkov AV, Osterman AL, et al. Structural Basis of TLR5-Flagellin Recognition and Signaling. Science. 2012;335: 859–864. doi: 10.1126/science.1215584 22344444
10. Guthrie GJK, Charles KA, Roxburgh CSD, Horgan PG, McMillan DC, Clarke SJ. The systemic inflammation-based neutrophil-lymphocyte ratio: Experience in patients with cancer. Critical Reviews in Oncology Hematology. 2013;88: 218–230.
11. Davis AK, Maney DL, Maerz JC. The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists. Funct Ecol. 2008;22: 760–772.
12. Fowler ME, Miller RE. Zoo and wild animal medicine. 5th ed. St. Louis, Mo.: St. Louis, Mo.: Saunders; 2003.
13. Beechler BR, Broughton H, Bell A, Ezenwa VO, Jolles AE. Innate Immunity in Free-Ranging African Buffalo (Syncerus caffer): Associations with Parasite Infection and White Blood Cell Counts. Physiol Biochem Zool. 2012;85: 255–264. doi: 10.1086/665276 22494981
14. Liebl AL, Martin LB. Simple quantification of blood and plasma antimicrobial capacity using spectrophotometry. Funct Ecol. 2009;23: 1091–1096.
15. Matson KD, Tieleman BI, Klasing KC. Capture stress and the bactericidal competence of blood and plasma in five species of tropical birds. Physiol Biochem Zool. 2006;79: 556–564. doi: 10.1086/501057 16691521
16. Dugovich BS, Peel MJ, Palmer AL, Zielke RA, Sikora AE, Beechler BR, et al. Detection of bacterial-reactive natural IgM antibodies in desert bighorn sheep populations. PLoS One. 2017;12: 15.
17. Levy O. Antimicrobial proteins and peptides of blood: templates for novel antimicrobial agents. Blood. 2000;96: 2664–2672. 11023496
18. Yang D, Biragyn A, Hoover DM, Lubkowski J, Oppenheim JJ. Multiple roles of antimicrobial defensins, cathelicidins, and eosinophil-derived neurotoxin in host defense. Annu Rev Immunol. 2004;22: 181–215. doi: 10.1146/annurev.immunol.22.012703.104603 15032578
19. Jolles AE, Beechler BR, Dolan BP. Beyond mice and men: environmental change, immunity and infections in wild ungulates. Parasite Immunol. 2015;37: 255–266. doi: 10.1111/pim.12153 25354672
20. Jolles AE, Ezenwa VO. Ungulates as model systems for the study of disease processes in natural populations. J Mammal. 2015;96: 4–15.
21. Martin C, Pastoret P-P, Brochier B, Humblet M-F, Saegerman C. A survey of the transmission of infectious diseases/infections between wild and domestic ungulates in Europe. Vet Res. 2011;42: 70. doi: 10.1186/1297-9716-42-70 21635726
22. Cases-Diaz E, Marco I, Lopez-Olvera JR, Mentaberre G, Serrano E, Lavin S. Effect of Acepromazine and Haloperidol in Male Iberian Ibex (Capra pyrenaica) Captured by Box-Trap. J Wildl Dis. 2012;48: 763–767. doi: 10.7589/0090-3558-48.3.763 22740543
23. Marco I, Lavin S. Effect of the method of capture on the haematology and blood chemistry of red deer (Cervus elaphus). Res Vet Sci. 1999;66: 81–84. doi: 10.1053/rvsc.1998.0248 10208884
24. Strobel S, Becker NI, Encarnacao JA. No short-term effect of handling and capture stress on immune responses of bats assessed by bacterial killing assay. Mamm Biol. 2015;80: 312–315.
25. Tieleman BI, Williams JB, Ricklefs RE, Klasing KC. Constitutive innate immunity is a component of the pace-of-life syndrome in tropical birds. Proceedings of the Royal Society B-Biological Sciences. 2005;272: 1715–1720.
26. French SS, Neuman-Lee LA. Improved ex vivo method for microbiocidal activity across vertebrate species. Biol Open. bio.biologists.org; 2012;1: 482–487. doi: 10.1242/bio.2012919 23213440
27. Gervasi SS, Hunt EG, Lowry M, Blaustein AR. Temporal patterns in immunity, infection load and disease susceptibility: understanding the drivers of host responses in the amphibian-chytrid fungus system. Funct Ecol. 2014;28: 569–578.
28. Dolan BP, Fisher KM, Colvin ME, Benda SE, Peterson JT, Kent ML, et al. Innate and adaptive immune responses in migrating spring-run adult chinook salmon, Oncorhynchus tshawytscha. Fish Shellfish Immunol. 2016;48: 136–144. doi: 10.1016/j.fsi.2015.11.015 26581919
29. Oksanen J, Kindt R, Legendre P, O’Hara B. The vegan package. researchgate.net. Available: https://www.researchgate.net/profile/Gavin_Simpson/publication/228339454_The_vegan_Package/links/0912f50be86bc29a7f000000/The-vegan-Package.pdf
30. Bates D, Mächler M, Bolker B, Walker S. Fitting Linear Mixed-Effects Models Using lme4. Journal of Statistical Software, Articles. 2015;67: 1–48.
31. Jaeger BC, Edwards LJ, Das K, Sen PK. An R-2 statistic for fixed effects in the generalized linear mixed model. J Appl Stat. Taylor & Francis; 2017;44: 1086–1105.
32. Koller B, Kappler M, Latzin P, Gaggar A, Schreiner M, Takyar S, et al. TLR expression on neutrophils at the pulmonary site of infection: TLR1/TLR2-mediated up-regulation of TLR5 expression in cystic fibrosis lung disease. Mian Yi Xue Za Zhi. 2008;181: 2753–2763.
33. Harada K, Isse K, Nakanuma Y. Interferon gamma accelerates NF-kappa B activation of biliary epithelial cells induced by toll-like receptor and ligand interaction. J Clin Pathol. 2006;59: 184–190. doi: 10.1136/jcp.2004.023507 16443736
34. Homma T, Kato A, Hashimoto N, Batchelor J, Yoshikawa M, Imai S, et al. Corticosteroid and cytokines synergistically enhance toll-like receptor 2 expression in respiratory epithelial cells. Am J Respir Cell Mol Biol. 2004;31: 463–469. doi: 10.1165/rcmb.2004-0161OC 15242847
35. Bernardino ALF, Myers TA, Alvarez X, Hasegawa A, Philipp MT. Toll-like receptors: Insights into their possible role in the pathogenesis of Lyme neuroborreliosis. Infect Immun. 2008;76: 4385–4395. doi: 10.1128/IAI.00394-08 18694963
36. Cabral ES, Gelderblom H, Hornung RL, Munson PJ, Martin R, Marques AR. Borrelia burgdorferi lipoprotein-mediated TLR2 stimulation causes the down-regulation of TLR5 in human monocytes. J Infect Dis. 2006;193: 849–859. doi: 10.1086/500467 16479520
37. Young HS, Dirzo R, Helgen KM, McCauley DJ, Nunn CL, Snyder P, et al. Large wildlife removal drives immune defence increases in rodents. Funct Ecol. 2016;30: 799–807.
38. Mak TW, Saunders ME, Jett BD. Primer to the Immune Response. Elsevier Science; 2013.
39. Maeda S. Veterinary Immunology: An Introduction—by Ian R. Tizard. Vet Dermatol. 2009;20: 144–144.
40. Roland L, Drillich M, Iwersen M. Hematology as a diagnostic tool in bovine medicine. J Vet Diagn Invest. 2014;26: 592–598. doi: 10.1177/1040638714546490 25121728
41. Martin LB II, Weil ZM, Nelson RJ. Refining approaches and diversifying directions in ecoimmunology. Integr Comp Biol. 2006;46: 1030–1039. doi: 10.1093/icb/icl039 21672805
42. Prall SP, Muehlenbein MP. Testosterone and Immune Function in Primates: A Brief Summary with Methodological Considerations. Int J Primatol. 2014;35: 805–824.
43. Viney M, Riley EM. The Immunology of Wild Rodents: Current Status and Future Prospects. Front Immunol. 2017 Nov 14;8:1481. doi: 10.3389/fimmu.2017.01481 29184549
44. Fair PA, Schaefer AM, Houser DS, Bossart GD, Romano TA, Champagne CD, et al. The environment as a driver of immune and endocrine responses in dolphins (Tursiops truncatus). PLoS One. 2017 May 3;12(5):e0176202. doi: 10.1371/journal.pone.0176202 28467830
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