Functionally distinct T-helper cell phenotypes predict resistance to different types of parasites in a wild mammal
Abolins, S. et al. The comparative immunology of wild and laboratory mice, Mus musculus domesticus. Nat. Commun. 8, 14811. https://doi.org/10.1038/ncomms14811 (2017).ADS
Article
PubMed
PubMed Central
Google Scholar
Cox, F. E. G. Concomitant infections, parasites and immune responses. Parasitology 122, S23–S38. https://doi.org/10.1017/S003118200001698X (2001).Article
PubMed
Google Scholar
Seder, R. A., Darrah, P. A. & Roederer, M. T-cell quality in memory and protection: Implications for vaccine design. Nat. Rev. Immunol. 8, 247–258. https://doi.org/10.1038/nri2274 (2008).CAS
Article
PubMed
Google Scholar
Demas, G. E., Zysling, D. A., Beechler, B. R., Muehlenbein, M. P. & French, S. S. Beyond phytohaemagglutinin: Assessing vertebrate immune function across ecological contexts. J. Anim. Ecol. 80, 710–730. https://doi.org/10.1111/j.1365-2656.2011.01813.x (2011).Article
PubMed
Google Scholar
Pedersen, A. B. & Babayan, S. A. Wild immunology. Mol. Ecol. 20, 872–880. https://doi.org/10.1111/j.1365-294X.2010.04938.x (2011).CAS
Article
PubMed
Google Scholar
Abolins, S. et al. The ecology of immune state in a wild mammal, Mus musculus domesticus. PLoS Biol. 16, e2003538. https://doi.org/10.1371/journal.pbio.2003538 (2018).CAS
Article
PubMed
PubMed Central
Google Scholar
Ezenwa, V. O. Helminth–microparasite co-infection in wildlife: Lessons from ruminants, rodents and rabbits. Parasite Immunol. 38, 527–534. https://doi.org/10.1111/pim.12348 (2016).CAS
Article
PubMed
Google Scholar
Craig, B. H., Tempest, L. J., Pilkington, J. G. & Pemberton, J. M. Metazoan-protozoan parasite co-infections and host body weight in St Kilda Soay sheep. Parasitology 135, 433–441. https://doi.org/10.1017/S0031182008004137 (2008).CAS
Article
PubMed
Google Scholar
Graham, A. L. et al. Exposure to viral and bacterial pathogens among Soay sheep (Ovis aries) of the St Kilda archipelago. Epidemiol. Infect. 144, 1879–1888. https://doi.org/10.1017/S0950268816000017 (2016).CAS
Article
PubMed
Google Scholar
Murphy, K., Travers, P., Walport, M. & Janeway, C. Janeway’s Immunobiology (Garland Science, 2012).
Google Scholar
Parkin, J. & Cohen, B. An overview of the immune system. Lancet 357, 1777–1789. https://doi.org/10.1016/S0140-6736(00)04904-7 (2001).CAS
Article
PubMed
Google Scholar
Mosmann, T. R. & Coffman, R. L. TH1 and TH2 cells: Different patterns of lymphokine secretion lead to different functional properties. Annu. Rev. Immunol. 7, 145–173. https://doi.org/10.1146/annurev.iy.07.040189.001045 (1989).CAS
Article
PubMed
Google Scholar
Nakayamada, S., Takahashi, H., Kanno, Y. & O’Shea, J. J. Helper T cell diversity and plasticity. Curr. Opin. Immunol. 24, 297–302. https://doi.org/10.1016/j.coi.2012.01.014 (2012).CAS
Article
PubMed
PubMed Central
Google Scholar
Gerbe, F. et al. Intestinal epithelial tuft cells initiate type 2 mucosal immunity to helminth parasites. Nature 529, 226–230. https://doi.org/10.1038/nature16527 (2016).ADS
CAS
Article
PubMed
Google Scholar
Jain, A. & Pasare, C. Innate control of adaptive immunity: Beyond the three-signal paradigm. J. Immunol. (Baltimore, Md.: 1950) 198, 3791–3800. https://doi.org/10.4049/jimmunol.1602000 (2017).CAS
Article
Google Scholar
Schmitt, N. & Ueno, H. Regulation of human helper T cell subset differentiation by cytokines. Curr. Opin. Immunol. 34, 130–136. https://doi.org/10.1016/j.coi.2015.03.007 (2015).CAS
Article
PubMed
PubMed Central
Google Scholar
Abbas, A. K., Murphy, K. M. & Sher, A. Functional diversity of helper T lymphocytes. Nature 383, 787–793. https://doi.org/10.1038/383787a0 (1996).ADS
CAS
Article
PubMed
Google Scholar
Seder, R. A. & Paul, W. E. Acquisition of lymphokine-producing phenotype by CD4+ T cells. Annu. Rev. Immunol. 12, 635–673. https://doi.org/10.1146/annurev.iy.12.040194.003223 (1994).CAS
Article
PubMed
Google Scholar
Grencis, R. K. Immunity to helminths: Resistance, regulation, and susceptibility to gastrointestinal nematodes. Annu. Rev. Immunol. 33, 201–225. https://doi.org/10.1146/annurev-immunol-032713-120218 (2015).CAS
Article
PubMed
Google Scholar
O’Garra, A. & Robinson, D. In Advances in Immunology vol. 83 133–162 (Academic Press, 2004).Pereira, L. M. S., Gomes, S. T. M., Ishak, R. & Vallinoto, A. C. R. Regulatory T cell and forkhead box protein 3 as modulators of immune homeostasis. Front. Immunol. https://doi.org/10.3389/fimmu.2017.00605 (2017).Article
PubMed
PubMed Central
Google Scholar
Romagnani, S. T-cell subsets (Th1 versus Th2). Ann. Allergy Asthma Immunol. 85, 9–21. https://doi.org/10.1016/S1081-1206(10)62426-X (2000).CAS
Article
PubMed
Google Scholar
Sandquist, I. & Kolls, J. Update on regulation and effector functions of Th17 cells. F1000Res 7, 205–205. https://doi.org/10.12688/f1000research.13020.1 (2018).CAS
Article
PubMed
PubMed Central
Google Scholar
Stockinger, B. & Omenetti, S. The dichotomous nature of T helper 17 cells. Nat. Rev. Immunol. 17, 535–544. https://doi.org/10.1038/nri.2017.50 (2017).CAS
Article
PubMed
Google Scholar
Wilson, K., Fenton, A. & Tompkins, D. Wildlife Disease Ecology: Linking Theory to Data and Application (Cambridge University Press, 2019).Book
Google Scholar
Graham, A. L. Ecological rules governing helminth–microparasite coinfection. PNAS 105, 566–570. https://doi.org/10.1073/pnas.0707221105 (2008).ADS
CAS
Article
PubMed
PubMed Central
Google Scholar
Ezenwa, V. O., Etienne, R. S., Luikart, G., Beja-Pereira, A. & Jolles, A. E. Hidden consequences of living in a wormy world: Nematode-induced immune suppression facilitates tuberculosis invasion in African Buffalo. Am. Nat. 176, 613–624. https://doi.org/10.1086/656496 (2010).Article
PubMed
Google Scholar
Ezenwa, V. O. & Jolles, A. E. Opposite effects of anthelmintic treatment on microbial infection at individual versus population scales. Science 347, 175–177. https://doi.org/10.1126/science.1261714%JScience (2015).ADS
CAS
Article
PubMed
Google Scholar
Arriero, E. et al. From the animal house to the field: Are there consistent individual differences in immunological profile in wild populations of field voles (Microtus agrestis)?. PLoS One 12, e0183450. https://doi.org/10.1371/journal.pone.0183450 (2017).CAS
Article
PubMed
PubMed Central
Google Scholar
Jackson, J. A. et al. An immunological marker of tolerance to infection in wild rodents. PLoS Biol. 12, e1001901. https://doi.org/10.1371/journal.pbio.1001901 (2014).CAS
Article
PubMed
PubMed Central
Google Scholar
Beirne, C., Delahay, R. & Young, A. Sex differences in senescence: The role of intra-sexual competition in early adulthood. Proc. R. Soc. B. 282, 20151086. https://doi.org/10.1098/rspb.2015.1086 (2015).Article
PubMed
PubMed Central
Google Scholar
Young, S. et al. Relationships between immune gene expression and circulating cytokine levels in wild house mice. Ecol. Evol. 10, 13860–13871. https://doi.org/10.1002/ece3.6976 (2020).Article
PubMed
PubMed Central
Google Scholar
Turner, J. D. et al. Th2 cytokines are associated with reduced worm burdens in a human intestinal helminth infection. J. Infect. Dis. 188, 1768–1775. https://doi.org/10.1086/379370 (2003).CAS
Article
PubMed
Google Scholar
Craig, B. H., Pilkington, J. G., Kruuk, L. E. B. & Pemberton, J. M. Epidemiology of parasitic protozoan infections in Soay sheep (Ovis aries L.) on St Kilda. Parasitology 134, 9–21. https://doi.org/10.1017/S0031182006001144 (2006).Article
PubMed
Google Scholar
Maizels, R. M., Hewitson, J. P. & Smith, K. A. Susceptibility and immunity to helminth parasites. Curr. Opin. Immunol. 24, 459–466. https://doi.org/10.1016/j.coi.2012.06.003 (2012).CAS
Article
PubMed
PubMed Central
Google Scholar
Ozmen, O., Adanir, R. & Haligur, M. Immunohistochemical detection of the cytokine and chemokine expression in the gut of lambs and kids with coccidiosis. Small Rumin. Res. 105, 345–350. https://doi.org/10.1016/j.smallrumres.2011.11.010 (2012).Article
Google Scholar
Woolhouse, M. E. J. Patterns in parasite epidemiology: The peak shift. Parasitol. Today 14, 428–434. https://doi.org/10.1016/S0169-4758(98)01318-0 (1998).CAS
Article
PubMed
Google Scholar
Gibson, T. E. & Parfitt, J. W. The effect of age on the development by sheep of resistance to Trichostrongylus colubriformis. Res. Vet. Sci. 13, 529–535 (1972).CAS
Article
Google Scholar
Smith, W. D., Jackson, F., Jackson, E. & Williams, J. Age immunity to Ostertagia circumcincta: Comparison of the local immune responses of 4 1/2- and 10-month-old lambs. J. Comp. Pathol. 95, 235–245. https://doi.org/10.1016/0021-9975(85)90010-6 (1985).CAS
Article
PubMed
Google Scholar
Peters, A., Delhey, K., Nakagawa, S., Aulsebrook, A. & Verhulst, S. Immunosenescence in wild animals: Meta-analysis and outlook. Ecol. Lett. 22, 1709–1722. https://doi.org/10.1111/ele.13343 (2019).Article
PubMed
Google Scholar
Sparks, A. M. et al. Natural selection on antihelminth antibodies in a wild mammal population. Am. Nat. 192, 745–760. https://doi.org/10.1086/700115 (2018).Article
PubMed
Google Scholar
Froy, H. et al. Senescence in immunity against helminth parasites predicts adult mortality in a wild mammal. Science 365, 1296–1298. https://doi.org/10.1126/science.aaw5822%JScience (2019).ADS
CAS
Article
PubMed
Google Scholar
Nussey, D. H., Watt, K., Pilkington, J. G., Zamoyska, R. & McNeilly, T. N. Age-related variation in immunity in a wild mammal population. Aging Cell 11, 178–180. https://doi.org/10.1111/j.1474-9726.2011.00771.x (2012).CAS
Article
PubMed
Google Scholar
Watson, R. L. et al. Cellular and humoral immunity in a wild mammal: Variation with age & sex and association with overwinter survival. Ecol. Evol. 6, 8695–8705. https://doi.org/10.1002/ece3.2584 (2016).Article
PubMed
PubMed Central
Google Scholar
Pennock, N. D. et al. T cell responses: Naive to memory and everything in between. Adv. Physiol. Educ. 37, 273–283. https://doi.org/10.1152/advan.00066.2013 (2013).Article
PubMed
PubMed Central
Google Scholar
Chipeta, J. et al. CD4+and CD8+Cell cytokine profiles in neonates, older children, and adults: Increasing T helper type 1 and T cytotoxic type 1 cell populations with age. Cell. Immunol. 183, 149–156. https://doi.org/10.1006/cimm.1998.1244 (1998).CAS
Article
PubMed
Google Scholar
Sakata-Kaneko, S., Wakatsuki, Y., Matsunaga, Y., Usui, T. & Kita, T. Altered Th1/Th2 commitment in human CD4+ T cells with ageing. Clin. Exp. Immunol. 120, 267–273. https://doi.org/10.1046/j.1365-2249.2000.01224.x (2000).CAS
Article
PubMed
PubMed Central
Google Scholar
Duddy, M. E., Alter, A. & Bar-Or, A. Distinct profiles of human B cell effector cytokines: A role in immune regulation?. J. Immunol. (Baltimore, Md.: 1950) 172, 3422–3427. https://doi.org/10.4049/jimmunol.172.6.3422 (2004).CAS
Article
Google Scholar
Varma, T. K., Lin, C. Y., Toliver-Kinsky, T. E. & Sherwood, E. R. Endotoxin-induced gamma interferon production: Contributing cell types and key regulatory factors. Clin. Diagn. Lab. Immunol. 9, 530–543. https://doi.org/10.1128/CDLI.9.3.530-543.2002 (2002).CAS
Article
PubMed
PubMed Central
Google Scholar
McNeilly, T. N. et al. Suppression of ovine lymphocyte activation by Teladorsagia circumcincta larval excretory-secretory products. Vet. Res. 44, 70. https://doi.org/10.1186/1297-9716-44-70 (2013).CAS
Article
PubMed
PubMed Central
Google Scholar
Restif, O. & Amos, W. The evolution of sex-specific immune defences. Proc. R. Soc. B Biol. Sci. 277, 2247–2255. https://doi.org/10.1098/rspb.2010.0188 (2010).Article
Google Scholar
Hayward, A. D. et al. Heritable, heterogeneous, and costly resistance of sheep against nematodes and potential feedbacks to epidemiological dynamics. Am. Nat. 184, S58–S76. https://doi.org/10.1086/676929 (2014).Article
PubMed
Google Scholar
Sparks, A. M. et al. The genetic architecture of helminth-specific immune responses in a wild population of Soay sheep (Ovis aries). PLoS Genet. 15, e1008461. https://doi.org/10.1371/journal.pgen.1008461 (2019).CAS
Article
PubMed
PubMed Central
Google Scholar
Hayward, A. D., Wilson, A. J., Pilkington, J. G., Pemberton, J. M. & Kruuk, L. E. B. Ageing in a variable habitat: Environmental stress affects senescence in parasite resistance in St Kilda Soay sheep. Proc. R. Soc. B. 276, 3477–3485. https://doi.org/10.1098/rspb.2009.0906 (2009).Article
PubMed
PubMed Central
Google Scholar
Mosmann, T. R. & Sad, S. The expanding universe of T-cell subsets: Th1, Th2 and more. Immunol. Today 17, 138–146. https://doi.org/10.1016/0167-5699(96)80606-2 (1996).CAS
Article
PubMed
Google Scholar
Hassan, M., Hanrahan, J. P., Good, B., Mulcahy, G. & Sweeney, T. A differential interplay between the expression of Th1/Th2/Treg related cytokine genes in Teladorsagia circumcincta infected DRB1*1101 carrier lambs. Vet. Res. 42, 45. https://doi.org/10.1186/1297-9716-42-45 (2011).CAS
Article
PubMed
PubMed Central
Google Scholar
Noordwijk, A. J. V. & Jong, G. D. Acquisition and allocation of resources: Their influence on variation in life history tactics. Am. Nat. 128, 137–142. https://doi.org/10.1086/284547 (1986).Article
Google Scholar
Grainger, J. R. et al. Helminth secretions induce de novo T cell Foxp3 expression and regulatory function through the TGF-β pathway. J. Exp. Med. 207, 2331–2341. https://doi.org/10.1084/jem.20101074 (2010).CAS
Article
PubMed
PubMed Central
Google Scholar
Smith, K. A. et al. Low-level regulatory T-cell activity is essential for functional type-2 effector immunity to expel gastrointestinal helminths. Mucosal Immunol. 9, 428–443. https://doi.org/10.1038/mi.2015.73 (2016).CAS
Article
PubMed
Google Scholar
Beirne, C., Waring, L., McDonald, R. A., Delahay, R. & Young, A. Age-related declines in immune response in a wild mammal are unrelated to immune cell telomere length. Proc. R. Soc. B. 283, 20152949. https://doi.org/10.1098/rspb.2015.2949 (2016).CAS
Article
PubMed
PubMed Central
Google Scholar
Zaros, L. G. et al. Response of resistant and susceptible Brazilian Somalis crossbreed sheep naturally infected by Haemonchus contortus. Parasitol. Res. 113, 1155–1161. https://doi.org/10.1007/s00436-014-3753-8 (2014).CAS
Article
PubMed
Google Scholar
Gossner, A., Wilkie, H., Joshi, A. & Hopkins, J. Exploring the abomasal lymph node transcriptome for genes associated with resistance to the sheep nematode Teladorsagia circumcincta. Vet. Res. 44, 68. https://doi.org/10.1186/1297-9716-44-68 (2013).CAS
Article
PubMed
PubMed Central
Google Scholar
Wilkie, H., Gossner, A., Bishop, S. & Hopkins, J. Variations in T cell transcription factor sequence and expression associated with resistance to the sheep nematode Teladorsagia circumcincta. PLoS One 11, e0149644. https://doi.org/10.1371/journal.pone.0149644 (2016).CAS
Article
PubMed
PubMed Central
Google Scholar
Nussey, D. H., Coulson, T., Festa-Bianchet, M. & Gaillard, J.-M. Measuring senescence in wild animal populations: Towards a longitudinal approach. Funct. Ecol. 22, 393–406. https://doi.org/10.1111/j.1365-2435.2008.01408.x (2008).Article
Google Scholar
Seguel, M. et al. Immune stability predicts tuberculosis infection risk in a wild mammal. Proc. Biol. Sci. 286, 20191401. https://doi.org/10.1098/rspb.2019.1401 (2019).CAS
Article
PubMed
PubMed Central
Google Scholar
Pemberton, J. M. & Clutton-Brock, T. H. Soay Sheep: Dynamics and Selection in an Island Population (Cambridge University Press, 2004).
Google Scholar
Corripio-Miyar, Y. et al. Phenotypic and functional analysis of monocyte populations in cattle peripheral blood identifies a subset with high endocytic and allogeneic T-cell stimulatory capacity. Vet. Res. 46, 112. https://doi.org/10.1186/s13567-015-0246-4 (2015).CAS
Article
PubMed
PubMed Central
Google Scholar
Kwong, L. S. et al. Development of an ELISA for bovine IL-10. Vet. Immunol. Immunopathol. 85, 213–223. https://doi.org/10.1016/S0165-2427(02)00007-7 (2002).CAS
Article
PubMed
Google Scholar
Wattegedera, S. R. et al. Enhancing the toolbox to study IL-17A in cattle and sheep. Vet. Res. 48, 20–20. https://doi.org/10.1186/s13567-017-0426-5 (2017).CAS
Article
PubMed
PubMed Central
Google Scholar
Jackson, F. New technique for obtaining nematode ova from sheep faeces. Lab. Pract. 23, 65–66 (1974).ADS
CAS
PubMed
Google Scholar
R Development Core Team. R: A language and environment for statistical computing. Accessed Feb 2020. https://www.R-project.org/ (2019).
Venables, W. N. & Ripley, B. D. Random and Mixed Effects. In Modern Applied Statistics with S. Statistics and Computing. (2002).Package “corrplot”: visualization of a correlation matrix v. (Version 0.84) (2017).Jari Oksanen, F. et al. vegan: Community Ecology Package. R package version 2.5-6. Accessed Feb 2020. https://CRAN.R-project.org/package=vegan (2019). More