Immunology in wild nonmodel rodents: An ecological context for studies of health and disease

Parasite Immunology

Volumn 37, Issue 5, 2015, Pages 220-232

  Jackson, J A ^a  

^a ABERYSTWYTH UNIVERSITY   (United Kingdom)

Author keywords

Disease; Immunoepidemiology; Immunoregulation; PRR; Rodent; Th 2

Indexed keywords

NUCLEIC ACID; PROTEIN;

DISEASE SURVEILLANCE; DISEASE TRANSMISSION; ENVIRONMENTAL FACTOR; GENE; GENE EXPRESSION PROFILING; GENE LOCUS; HOMEOSTASIS; HOST PATHOGEN INTERACTION; IMMUNE RESPONSE; IMMUNITY; IMMUNOPATHOLOGY; IMMUNOREGULATION; INFECTION; INFLAMMATION; INNATE IMMUNITY; MACROPARASITE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVERSE ENGINEERING; REVIEW; RISK FACTOR; RODENT; WILD ANIMAL; ANIMAL; DOMESTIC ANIMAL; GENOTYPE ENVIRONMENT INTERACTION; IMMUNOLOGY; PARASITOLOGY; PROCEDURES; VETERINARY;

ANIMALIA; RODENTIA;

ANIMALS; ANIMALS, DOMESTIC; ANIMALS, WILD; GENE EXPRESSION PROFILING; GENE-ENVIRONMENT INTERACTION; INFECTION; RODENTIA;

EID: 84928312905     PISSN: 01419838     EISSN: 13653024     Source Type: Journal    
DOI: 10.1111/pim.12180     Document Type: Review

References (98)

1. Jackson JA, Begon M, Birtles R, et al. The analysis of immunological profiles in wild animals: a case study on immunodynamics in the field vole, Microtus agrestis. Mol Ecol 2011; 20: 893-909.
2. 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.
3. Williams TD, Turan N, Diab AM, et al. Towards a system level understanding of non-model organisms sampled from the environment: a network biology approach. PLoS Comput Biol 2011; 7: e1002126.
4. Pedersen AB & Babayan SA. Wild immunology. Mol Ecol 2011; 20: 872-880.
5. Friberg IM, Bradley JE & Jackson JA. Macroparasites, innate immunity and immunoregulation: developing natural models. Trends Parasitol 2010; 26: 540-549.
6. Bradley JE & Jackson JA. Measuring immune system variation to help understand host-pathogen community dynamics. Parasitology 2008; 135: 807-823.
7. Rook GA. Regulation of the immune system by biodiversity from the natural environment: an ecosystem service essential to health. Proc Natl Acad Sci USA 2013; 110: 18360-18367.
8. Coussens LM & Werb Z. Inflammation and cancer. Nature 2002; 420: 860-867.
9. Canivell S & Gomis R. Diagnosis and classification of autoimmune diabetes mellitus. Autoimmun Rev 2014; 13: 403-407.
10. Legatzki A, Rosler B & von Mutius E. Microbiome diversity and asthma and allergy risk. Curr Allergy Asthma Rep 2014; 14: 466.
11. Kannarkat GT, Boss JM & Tansey MG. The role of innate and adaptive immunity in Parkinson's disease. J Parkinsons Dis 2013; 3: 493-514.
12. Ellwardt E & Zipp F. Molecular mechanisms linking neuroinflammation and neurodegeneration in MS. Exp Neurol 2014; 262PA: 8-17.
13. Rook GA, Raison CL & Lowry CA. Microbiota, immunoregulatory old friends and psychiatric disorders. Adv Exp Med Biol 2014; 817: 319-356.
14. Rook GA. Hygiene hypothesis and autoimmune diseases. Clin Rev Allergy Immunol 2012; 42: 5-15.
15. Turner AK & Paterson S. Wild rodents as a model to discover genes and pathways underlying natural variation in infectious disease susceptibility. Parasite Immunol 2013; 35: 386-395.
16. Brock PM, Murdock CC & Martin LB. The history of ecoimmunology and its integration with disease ecology. Integr Comp Biol 2014; 54: 353-362.
17. Jackson JA, Friberg IM, Little S & Bradley JE. Review series on helminths, immune modulation and the hygiene hypothesis: immunity against helminths and immunological phenomena in modern human populations: coevolutionary legacies? Immunology 2009; 126: 18-27.
18. Chia R, Achilli F, Festing MFW & Fisher EMC. The origins and uses of mouse outbred stocks. Nat Genet 2005; 37: 1181-1186.
19. Babay BEC, Louzir H, KebaÃ-er C, Boubaker S, Dellagi K & Cazenave P-A. Inbred strains derived from feral mice reveal new pathogenic mechanisms of experimental Leishmaniasis due to Leishmania major. Infect Immun 2004; 72: 4603-4611.
20. Harper J. Wild-derived mouse stocks: an underappreciated tool for aging research. Age (Dordr) 2008; 30: 135-145.
21. Gabriel SE, Brigman KN, Koller BH, Boucher RC & Stutts MJ. Cystic fibrosis heterozygote resistance to cholera toxin in the cystic fibrosis mouse model. Science 1994; 266: 107-109.
22. Pasvol G, Weatherall DJ & Wilson RJ. Cellular mechanism for the protective effect of haemoglobin S against P. falciparum malaria. Nature 1978; 274: 701-703.
23. Willcocks LC, Carr EJ, Niederer HA, et al. A defunctioning polymorphism in FCGR2B is associated with protection against malaria but susceptibility to systemic lupus erythematosus. Proc Natl Acad Sci USA 2010; 107: 7881-7885.
24. Woolf LI. The heterozygote advantage in phenylketonuria. Am J Hum Genet 1986; 38: 773-775.
25. Lee JC, Espeli M, Anderson CA, et al. Human SNP links differential outcomes in inflammatory and infectious disease to a FOXO3-regulated pathway. Cell 2013; 155: 57-69.
26. Fumagalli M, Sironi M, Pozzoli U, Ferrer-Admetlla A, Pattini L & Nielsen R. Signatures of environmental genetic adaptation pinpoint pathogens as the main selective pressure through human evolution. PLoS Genet 2011; 7: e1002355.
27. Forni D, Cagliani R, Tresoldi C, et al. An evolutionary analysis of antigen processing and presentation across different timescales reveals pervasive selection. PLoS Genet 2014; 10: e1004189.
28. Leffler EM, Gao Z, Pfeifer S, et al. Multiple instances of ancient balancing selection shared between humans and chimpanzees. Science 2013; 339: 1578-1582.
29. Morger J, Bajnok J, Boyce K, et al. Naturally occurring Toll-like receptor 11 (TLR11) and Toll-like receptor 12 (TLR12) polymorphisms are not associated with Toxoplasma gondii infection in wild wood mice. Infect Genet Evol 2014; 26: 180-184.
30. Tschirren B, Andersson M, Scherman K, Westerdahl H, Mittl PR & Raberg L. Polymorphisms at the innate immune receptor TLR2 are associated with Borrelia infection in a wild rodent population. Proc Biol Sci 2013; 280: 20130364.
31. Tschirren B, Raberg L & Westerdahl H. Signatures of selection acting on the innate immunity gene Toll-like receptor 2 (TLR2) during the evolutionary history of rodents. J Evol Biol 2011; 24: 1232-1240.
32. Turner AK, Begon M, Jackson JA, Bradley JE & Paterson S. Genetic diversity in cytokines associated with immune variation and resistance to multiple pathogens in a natural rodent population. PLoS Genet 2011; 7: e1002343.
33. Turner AK, Begon M, Jackson JA & Paterson S. Evidence for selection at cytokine loci in a natural population of field voles (Microtus agrestis). Mol Ecol 2012; 21: 1632-1646.
34. Graham AL, Shuker DM, Pollitt LC, Auld S, Wilson AJ & Little TJ. Fitness consequences of immune responses: strengthening the empirical framework for ecoimmunology. Funct Ecol 2011; 25: 5-17.
35. Meerburg BG, Singleton GR & Kijlstra A. Rodent-borne diseases and their risks for public health. Crit Rev Microbiol 2009; 35: 221-270.
36. Davis S, Calvet E & Leirs H. Fluctuating rodent populations and risk to humans from rodent-borne zoonoses. Vector Borne Zoonotic Dis 2005; 5: 305-314.
37. Lloyd-Smith JO, Schreiber SJ, Kopp PE & Getz WM. Superspreading and the effect of individual variation on disease emergence. Nature 2005; 438: 355-359.
38. Graham AL, Cattadori IM, Lloyd-Smith JO, Ferrari MJ & Bjornstad ON. Transmission consequences of coinfection: cytokines writ large? Trends Parasitol 2007; 23: 284-291.
39. Turner AK, Beldomenico PM, Bown K, et al. Host-parasite biology in the real world: the field voles of Kielder. Parasitology 2014; 141: 997-1017.
40. Demas GE & Nelson RJ. Photoperiod, ambient temperature, and food availability interact to affect reproductive and immune function in adult male deer mice (Peromyscus maniculatus). J Biol Rhythms 1998; 13: 253-262.
41. Martin LB, Weil ZM & Nelson RJ. Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs. Philos Trans R Soc Lond B Biol Sci 2008; 363: 321-339.
42. Nelson RJ & Demas GE. Seasonal changes in immune function. Q Rev Biol 1996; 71: 511-548.
43. Martin LB, Coon CA, Liebl AL & Schrey AW. Surveillance for microbes and range expansion in house sparrows. Proc Biol Sci 2013; 281: 20132690.
44. White TA, Perkins SE, Heckel G & Searle JB. Adaptive evolution during an ongoing range expansion: the invasive bank vole (Myodes glareolus) in Ireland. Mol Ecol 2013; 22: 2971-2985.
45. Wang LF, Walker PJ & Poon LL. Mass extinctions, biodiversity and mitochondrial function: are bats 'special' as reservoirs for emerging viruses? Curr Opin Virol 2011; 1: 649-657.
46. Martin LB 2nd, Weil ZM & Nelson RJ. Immune defense and reproductive pace of life in Peromyscus mice. Ecology 2007; 88: 2516-2528.
47. Guivier E, Galan M, Henttonen H, Cosson JF & Charbonnel N. Landscape features and helminth co-infection shape bank vole immunoheterogeneity, with consequences for Puumala virus epidemiology. Heredity (Edinb) 2014; 112: 274-281.
48. Bidaisee S & Macpherson CN. Zoonoses and one health: a review of the literature. J Parasitol Res 2014; 2014: 874345.
49. Friberg IM, Lowe A, Ralli C, Bradley JE & Jackson JA. Temporal anomalies in immunological gene expression in a time series of wild mice: signature of an epidemic? PLoS One 2011; 6: e20070.
50. Ueno K, Ishii A & Ito K. ELM: enhanced lowest common ancestor based method for detecting a pathogenic virus from a large sequence dataset. BMC Bioinformatics 2014; 15: 254.
51. Liu S, Vijayendran D & Bonning BC. Next generation sequencing technologies for insect virus discovery. Viruses 2011; 3: 1849-1869.
52. Zhou P, Cowled C, Todd S, et al. Type III IFNs in pteropid bats: differential expression patterns provide evidence for distinct roles in antiviral immunity. J Immunol 2011; 186: 3138-3147.
53. Shi Z & Hu Z. A review of studies on animal reservoirs of the SARS coronavirus. Virus Res 2008; 133: 74-87.
54. Kan B, Wang M, Jing H, et al. Molecular evolution analysis and geographic investigation of severe acute respiratory syndrome coronavirus-like virus in palm civets at an animal market and on farms. J Virol 2005; 79: 11892-11900.
55. Lin CY, Roberts GW, Kift-Morgan A, Donovan KL, Topley N & Eberl M. Pathogen-specific local immune fingerprints diagnose bacterial infection in peritoneal dialysis patients. J Am Soc Nephrol 2013; 24: 2002-2009.
56. Jackson JA, Hall AJ, Friberg IM, et al. An immunological marker of tolerance to infection in wild rodents. PLoS Biol 2014; 12: e1001901.
57. Sheldon BC & Verhulst S. Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 1996; 11: 317-321.
58. Rajabi-Maham H, Orth A & Bonhomme F. Phylogeography and postglacial expansion of Mus musculus domesticus inferred from mitochondrial DNA coalescent, from Iran to Europe. Mol Ecol 2008; 17: 627-641.
59. Behnke J & Harris PD. Heligmosomoides bakeri: a new name for an old worm? Trends Parasitol 2010; 26: 524-529.
60. White TA & Perkins SE. The ecoimmunology of invasive species. Funct Ecol 2012; 26: 1313-1323.
61. Grabherr MG, Haas BJ, Yassour M, et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 2011; 29: 644-652.
62. Eberhardt AT, Costa SA, Marini MR, et al. Parasitism and physiological trade-offs in stressed capybaras. PLoS One 2013; 8: 12.
63. Racca AL, Eberhardt AT, Moreno PG, Baldi C & Beldomenico PM. Differences in natural antibody titres comparing free-ranging guanacos (Lama guanicoe) and capybaras (Hydrochoerus hydrochaeris). Vet J 2014; 199: 308-309.
64. Schwensow N, Axtner J & Sommer S. Are associations of immune gene expression, body condition and parasite burden detectable in nature? A case study in an endemic rodent from the Brazilian Atlantic Forest. Infect Genet Evol 2011; 11: 23-30.
65. Pradet-Balade B, Boulmé F, Beug H, Müllner EW & Garcia-Sanz JA. Translation control: bridging the gap between genomics and proteomics? Trends Biochem Sci 2001; 26: 225-229.
66. Payne SH. The utility of protein and mRNA correlation. Trends Biochem Sci 2015; 40: 1-3.
67. Oko L, Aduddell-Swope B, Willis D, et al. Profiling helper T cell subset gene expression in deer mice. BMC Immunol 2006; 7: 18.
68. Jackson JA, Friberg IM, Bolch L, et al. Immunomodulatory parasites and toll-like receptor-mediated tumour necrosis factor alpha responsiveness in wild mammals. BMC Biol 2009; 7: 16.
69. Schountz T & Prescott J. Hantavirus immunology of rodent reservoirs: current status and future directions. Viruses 2014; 6: 1317-1335.
70. Johnston PR & Rolff J. Immune- and wound-dependent differential gene expression in an ancient insect. Dev Comp Immunol 2013; 40: 320-324.
71. Lenz TL, Eizaguirre C, Rotter B, Kalbe M & Milinski M. Exploring local immunological adaptation of two stickleback ecotypes by experimental infection and transcriptome-wide digital gene expression analysis. Mol Ecol 2013; 22: 774-786.
72. McLoughlin KE, Nalpas NC, Rue-Albrecht K, et al. RNA-seq transcriptional profiling of peripheral blood leukocytes from cattle infected with Mycobacterium bovis. Front Immunol 2014; 5: 396.
73. Day E, Dear PH & McCaughan F. Digital PCR strategies in the development and analysis of molecular biomarkers for personalized medicine. Methods 2013; 59: 101-107.
74. Forreryd A, Johansson H, Albrekt AS & Lindstedt M. Evaluation of high throughput gene expression platforms using a genomic biomarker signature for prediction of skin sensitization. BMC Genom 2014; 15: 17.
75. Villaverde AF & Banga JR. Reverse engineering and identification in systems biology: strategies, perspectives and challenges. J R Soc Interface 2014; 11: 20130505.
76. Molloy MJ, Bouladoux N & Belkaid Y. Intestinal microbiota: shaping local and systemic immune responses. Semin Immunol 2012; 24: 58-66.
77. Hooper LV, Littman DR & Macpherson AJ. Interactions between the microbiota and the immune System. Science 2012; 336: 1268-1273.
78. Hanski I, von Hertzen L, Fyhrquist N, et al. Environmental biodiversity, human microbiota, and allergy are interrelated. Proc Natl Acad Sci USA 2012; 109: 8334-8339.
79. Sayi A, Kohler E, Toller IM, et al. TLR-2-activated B cells suppress Helicobacter-induced preneoplastic gastric immunopathology by inducing T regulatory-1 cells. J Immunol 2011; 186: 878-890.
80. Vijay-Kumar M, Aitken JD, Carvalho FA, et al. Metabolic syndrome and altered gut microbiota in mice lacking toll-like receptor 5. Science 2010; 328: 228-231.
81. Medzhitov R. TLR-mediated innate immune recognition. Semin Immunol 2007; 19: 1-2.
82. Friberg IM, Little S, Ralli C, et al. Macroparasites at peripheral sites of infection are major and dynamic modifiers of systemic antimicrobial pattern recognition responses. Mol Ecol 2013; 22: 2810-2826.
83. Maizels RM, Hewitson JP & Gause WC. Heligmosomoides polygyrus: one species still. Trends Parasitol 2011; 27: 100-101.
84. Reynolds LA, Harcus Y, Smith KA, et al. MyD88 signaling inhibits protective immunity to the gastrointestinal helminth parasite Heligmosomoides polygyrus. J Immunol 2014; 193: 2984-2993.
85. Helmby H & Grencis RK. Essential role for TLR4 and MyD88 in the development of chronic intestinal nematode infection. Eur J Immunol 2003; 33: 2974-2979.
86. Behnke JM, Mugambi JM, Clifford S, et al. Genetic variation in resistance to repeated infections with Heligmosomoides polygyrus bakeri, in inbred mouse strains selected for the mouse genome project. Parasite Immunol 2006; 28: 85-94.
87. + regulatory T Cells control innate immune reactivity after injury. J Immunol 2005; 174: 2957-2963.
88. Segura M, Su Z, Piccirillo C & Stevenson MM. Impairment of dendritic cell function by excretory-secretory products: a potential mechanism for nematode-induced immunosuppression. Eur J Immunol 2007; 37: 1887-1904.
89. Mueller T, Terada T, Rosenberg IM, Shibolet O & Podolsky DK. Th2 cytokines down-regulate TLR expression and function in human intestinal epithelial cells. J Immunol 2006; 176: 5805-5814.
90. Guivier E, Galan M, Salvador AR, et al. Tnf-alpha expression and promoter sequences reflect the balance of tolerance/resistance to Puumala hantavirus infection in European bank vole populations. Infect Genet Evol 2010; 10: 1208-1217.
91. Axtner J & Sommer S. Heligmosomoides polygyrus infection is associated with lower MHC class II gene expression in Apodemus flavicollis: indication for immune suppression? Infect Genet Evol 2011; 11: 2063-2071.
92. Schountz T, Shaw TI, Glenn TC, Feldmann H & Prescott J. Expression profiling of lymph node cells from deer mice infected with Andes virus. BMC Immunol 2013; 14: 18.
93. Boppana VD, Thangamani S, Adler AJ & Wikel SK. SAAG-4 is a novel mosquito salivary protein that programmes host CD4(+) T cells to express IL-4. Parasite Immunol 2009; 31: 287-295.
94. Boppana VD, Thangamani S, Alarcon-Chaidez FJ, Adler AJ & Wikel SK. Blood feeding by the Rocky Mountain spotted fever vector, Dermacentor andersoni, induces interleukin-4 expression by cognate antigen responding CD4(+) T cells. Parasit Vectors 2009; 2: 9.
95. Gause WC, Urban JF & Stadecker MJ. The immune response to parasitic helminths: insights from murine models. Trends Immunol 2003; 24: 269-277.
96. Ho IC, Tai TS & Pai SY. GATA3 and the T-cell lineage: essential functions before and after T-helper-2-cell differentiation. Nat Rev Immunol 2009; 9: 125-135.
97. Allen JE & Wynn TA. Evolution of Th2 immunity: a rapid repair response to tissue destructive pathogens. PLoS Pathog 2011; 7: 4.
98. Raberg L, Graham AL & Read AF. Decomposing health: tolerance and resistance to parasites in animals. Philos Trans R Soc Lond B Biol Sci 2009; 364: 37-49.