The functional importance of sequence versus expression variability of MHC alleles in parasite resistance

Genetica

Volumn 140, Issue 10-12, 2012, Pages 407-420

  Axtner, Jan ^a,b   Sommer, Simone ^a  

^a LEIBNIZ INSTITUTE FOR ZOO AND WILDLIFE RESEARCH   (Germany)

^b Research Institute Havelhoehe (FIH)   (Germany)

Author keywords

Apodemus flavicollis; Gastrointestinal helminths; Gene expression; Immune genes; Rodent; Sequence variability

Indexed keywords

ANIMALIA; APODEMUS FLAVICOLLIS; CESTODA; MUS; OXYURIDA; OXYUROIDEA; RODENTIA; SYPHACIA STROMA; VERMES;

EID: 84873414552     PISSN: 00166707     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10709-012-9689-y     Document Type: Article

References (98)

1. Anderson RC (2000) Nematode parasites of vertebrates: their development and transmission, 2nd edn. Introduction. CABI, Wallingford, pp 1-16.
2. Axtner J, Sommer S (2007) Gene duplication, allelic diversity, selection processes and adaptive value of MHC class II DRB genes of the bank vole, Clethrionomys glareolus. Immunogenetics 59: 417-426.
3. Axtner J, Sommer S (2009) Validation of internal reference genes for quantitative real-time PCR in a non-model organism, the yellow-necked mouse, Apodemus flavicollis. BMC Res Notes 2: 264.
4. Axtner J, Sommer S (2011) Heligmosomoides polygyrus infection is associated with lower MHC class II gene expression in Apodemus flavicollis: indication for immune suppression? Infect Gene Evol 11: 2063-2071.
5. Bansemir AD, Sukhdeo MV (1994) The food resource of adult Heligmosomoides polygyrus in the small intestine. J Parasitol 80: 24-28.
6. Baumgart M, Moos V, Schuhbauer D, Müller B (1998) Differential expression of major histocompatibility complex class II genes on murine macrophages associated with T cell cytokine profile and protective/suppressive effects. Proc Natl Acad Sci USA 95: 6936-6940.
7. Bernatchez L, Landry C (2003) MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years. J Evol Biol 16: 363-377.
8. Bowen L, Aldrige B, Beckmen K, Gelatt T, Rea L, Burek K, Pitcher K, Stott J (2006) Differential expression of immune response genes in Steller sea lions (Eumetopias jubatus): an indicator of ecosystem health? EcoHealth 3: 109-113.
9. Bowen L, Riva F, Mohr C, Aldrige B, Schwartz J, Miles AK, Stott JL (2007) Differential gene expression induced by exposure of captive mink to fuel oil: a model for the sea otter. EcoHealth 4: 298-309.
10. Brown SA, Rosenthal KL (1997) Self-assessment colour review of small mammals. Manson Publishing, London.
11. Brown JH, Jardetzky TS, Gorga JC, Stern LJ, Urban RG, Strominger JL, Wiley DC (1993) Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature 364: 33-39.
12. Bulut Z, McCormick C, Bos D, DeWoody J (2008) Polymorphism of alternative splicing of major histocompatibility complex transcripts in wild tiger salamanders. J Mol Evol 67: 68-75.
13. Buonocore F, Randelli E, Casani D, Costantini S, Facchiano A, Scapigliati G, Stet RJM (2007) Molecular cloning, differential expression and 3D structural analysis of the MHC class-II ß chain from sea bass (Dicentrarchus labrax L.). Fish Shellfish Immunol 23: 853-866.
14. Charbonnel N, Pemberton J (2005) A long-term genetic survey of an ungulate population reveals balancing selection acting on MHC through spatial and temporal fluctuations in selection. Heredity 95: 377-388.
15. Crawley MJ (2007) The R book. Wiley, Chichester.
16. Deter J, Bryja J, Chaval Y, Galan M, Henttonen H, Laakkonen J, Voutilainen L, Vapalathi O, Vaheri A, Salvador A, Morand S, Cosson J-F, Charbonnel N (2008) Association between the DQA MHC class II gene and Puumala virus infection in Myodes glareolus, the bank vole. Infect Gene Evol 8: 450-458.
17. Díaz S, Giovambattista G, Peral-García P (2005) Polymorphisms of the upstream regulatory region of the major histocompatibility complex DRB genes in domestic horses. Intl J Immunogenet 32: 91-98.
18. Doherty PC, Zinkernagel RM (1975) Enhanced immunological surveillance in mice heterozygous at the H-2 gene complex. Nature 256: 50-52.
19. Edwards SE, Hedrick PW (1998) Evolution and ecology of MHC molecules: from genomics to sexual selection. Trends Ecol Evol 13: 305-311.
20. Eizaguirre C, Lenz TL, Kalbe M, Milinski M (2012) Rapid and adaptive evolution of MHC genes under parasite selection in experimental vertebrate populations. Nat Commun 3: 621.
21. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3. 5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10: 564-567.
22. Ferrari N, Cattadori IM, Nespereira J, Rizzoli A, Hudson PJ (2004) The role of host sex in parasite dynamics: field experiments on the yellow-necked mouse Apodemus flavicollis. Ecol Lett 7: 88-94.
23. Ferrari N, Cattadori IM, Rizzoli A, Hudson PJ (2009) Heligmosomoides polygyrus reduces infestation of Ixodes ricinus in free-living yellow-necked mice, Apodemus flavicollis. Parasitology 136: 305-316.
24. Fremont DH, Hendrickson WA, Marrack P, Kappler J (1996) Structures of an MHC class II molecule with covalently bound single peptides. Science 272: 1001-1004.
25. Froeschke G, Sommer S (2005) MHC class II DRB variability and parasite load in the striped mouse (Rhabdomys pumilio) in the Southern Kalahari. Mol Biol Evol 22: 1254-1259.
26. Froeschke G, Sommer S (2012) Insights into the complex associations between MHC class II DRB polymorphism and multiple gastrointestinal parasite iInfestations in the striped mouse. PLoS ONE 7: e31820.
27. Froeschke G, Harf R, Sommer S, Matthee S (2010) Effects of precipitation on parasite burden along a natural climatic gradient in southern Africa-implications for possible shifts in infestation patterns due to global changes. Oikos 119: 1029-1039.
28. Gardiola J, Maffei A (1993) Control of MHC class II gene expression in autoimmune, infectious, and neoplastic diseases. Crit Rev Immunol 13: 247-268.
29. Handunnetthi L, Ramagopalan SV, Ebers GC, Knight JC (2010) Regulation of major histocompatibility complex class II gene expression, genetic variation and disease. Genes Immun 11: 99-112.
30. Hedrick PW, Thomson G, Klitz W (1987) Evolutionary genetics and HLA: another classic example. Biol J Linn Soc Lond 31: 311-331.
31. Heldt C, Listing J, Sözeri O, Bläsing F, Frischbutter S, Müller B (2003) Differential expression of HLA class II genes associated with disease susceptibility and progression in rheumatoid arthritis. Arthritis Rheum 48: 2779-2787.
32. Herkel J, Jagemann B, Wiegard C, Lazaro JFG, Lueth S, Kanzler S, Blessing M, Schmitt E, Lohse AW (2003) MHC class II-expressing hepatocytes function as antigen-presenting cells and activate specific CD4 T lymphocyutes. Hepatology 37: 1079-1085.
33. Hill AVS, Allsopp CEM, Kwiatkowski D, Anstey NM, Twumasi P, Rowe PA, Bennett S, Brewster D, McMichael AJ, Greenwood BM (1991) Common West African HLA antigens are associated with protection from severe malaria. Nature 352: 595-600.
34. Huggett J, Dheda K, Bustin S, Zumla A (2005) Real-time RT-PCR normalisation; strategies and considerations. Genes Immun 6: 279-284.
35. Hughes AL, Nei M (1988) Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335: 167-170.
36. Hughes AL, Nei M (1989) Nucleotide substitution at major histocompatibility complex class II loci: evidence for overdominant selection. Proc Natl Acad Sci USA 86: 958-962.
37. Hughes AL, Yeager M (1998) Natural selection at major histocompatibility complex loci of vertebrates. Annu Rev Genet 32: 415-435.
38. Hughes AL, Hughes MK, Howell CY, Nei M, Howard JC, Higgs P (1994) Natural selection at the class II major histocompatibility complex loci of mammals. Philos Trans R Soc Lond B Biol Sci 346: 359-367.
39. Jüdes V (1979) Untersuchungen zur Ökologie der Waldmaus (Apodemus sylvaticus Linné, 1758) und der Gelbhalsmaus (Apodemus flavicollis Melchior, 1834) im Raum Kiel (Schleswig-Holstein). Mamm Biol 44: 81-95.
40. Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic, New York.
41. Klein J (1987) Origin of major histocompatibility complex polymorphism: the trans-species hypothesis. Hum Immunol 19: 155-162.
42. Klein J, Sato A, Nagl S, O'hUigín C (1998) Molecular trans-species polymorphism. Annu Rev Ecol Syst 29: 1-21.
43. Klimpel S, Förster M, Schmahl G (2007) Parasites of two abundant sympatric rodent species in relation to host phylogeny and ecology. Parasitol Res 100: 867-875.
44. Kloch A, Babik W, Bajer A, Sinski E, Radwan J (2010) Effects of MHC-DRB genotype and allele number on the load of gut parasites in the bank vole Myodes glareolus. Mol Ecol 19: 255-265.
45. Lareau LF, Green RE, Bhatnagar RS, Brenner SE (2004) The evolving roles of alternative splicing. Curr Opin in Struct Biol 14: 273-282.
46. Laurens V, Chapusot C, del Rosario Ordonez M, Bentrari F, Padros MR, Tournefier A (2001) Axolotl MHC class II β chain: predominance of one allele and alternative splicing of the β1 domain. Eur J Immunol 31: 506-515.
47. LeibundGut-Landmann S, Waldburger J-M, Krawczyk M, Otten LA, Suter T, Fontana A, Acha-Orbea H, Reith W (2004) Mini-review: specificity and expression of CIITA, the master regulator of MHC class II genes. Eur J Immunol 34: 1513-1525.
48. Lenz TL (2011) Computional prediction of MHC II-antigen binding supports divergent allele advantage and explains trans-species polymorphism. Evolution 65: 2380-2390.
49. Lenz TL, Wells K, Pfeiffer M, Sommer S (2009) Diverse MHC IIB allele repertoire increases parasite resistance and body condition in the long-tailed giant rat (Leopoldamys sabanus). BMC Evol Biol 9: 269.
50. Loisel DA, Rockman MV, Wray GA, Altmann J, Alberts SC (2006) Ancient polymorphism and functional variation in the primate MHC-DQA1 5′ cis-regulatory region. Proc Natl Acad Sci USA 103: 16331-16336.
51. Lüder CGK, Lang C, Giraldo-Velasquez M, Algner M, Gerdes J, Gross U (2003) Toxoplasma gondii inhibits MHC class II expression in neural antigen-presenting cells by down-regulating the class II transactivator CIITA. J Neuroimmunol 134: 12-24.
52. Martinsohn JT, Sousa AB, Guethlein LA, Howard JC (1999) The gene conversion hypothesis of MHC evolution: a review. Immunogenetics 50: 168-200.
53. McClelland EE, Penn DJ, Potts WK (2003) Major histocompatibility complex heterozygote superiority during coinfection. Infect Immun 71: 2079-2086.
54. McFarland BJ, Katz JF, Sant AJ, Beeson C (2005) Energetics and cooperativity of the hydrogen bonding and anchor interactions that bind peptides to MHC class II protein. J Mol Biol 350: 170-183.
55. Meyer-Lucht Y, Sommer S (2005) MHC diversity and the association to nematode parasitism in the yellow-necked mouse (Apodemus flavicollis). Mol Ecol 14: 2233-2243.
56. Meyer-Lucht Y, Sommer S (2009) Number of MHC alleles is related to parasite loads in natural populations of yellow necked mice, Apodemus flavicollis. Evol Ecol Res 11: 1085-1097.
57. Meyer-Lucht Y, Otten C, Püttker T, Sommer S (2008) Selection, diversity and evolutionary patterns of the MHC class II DAB in free-ranging Neotropical marsupials. BMC Genet 9: 39.
58. Mitchison NA, Roes J (2002) Patterned variation in murine MHC promoters. Proc Natl Acad Sci USA 99: 10561-10566.
59. Morley M, Molony CM, Weber TM, Devlin JL, Ewens KG, Spielman RS, Cheung VG (2004) Genetic analysis of genome-wide variation in human gene expression. Nature 430: 743-747.
60. Musolf K, Meyer-Lucht Y, Sommer S (2004) Evolution of MHC-DRB class II polymorphism in the genus Apodemus and a comparison of DRB sequences within the family Muridae (Mammalia: Rodentia). Immunogenetics 56: 420-426.
61. Nei M (2005) Selectionism and neutralism in molecular evolution. Mol Biol Evol 22: 2318-2342.
62. Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3: 418-426.
63. Nei M, Rooney AP (2005) Concerted and birth-and-death evolution of multigene families. Annu Rev Genet 39: 121-152.
64. Nei M, Gu X, Sitnikova T (1997) Evolution by the birth-and-death process in multigene families of the vertebrate immune system. Proc Natl Acad Sci USA 94: 7799-7806.
65. Nemeth E, Baird AW, O'Farrelly C (2009) Microanatomy of the liver immune system. Semin Immunopathol 31: 333-343.
66. Noss EH, Harding CV, Boom WH (2000) Mycobacterium tuberculosis inhibits MHC class II antigen processing in murine bone marrow macrophages. Cell Immunol 201: 63-74.
67. Oleksiak MF, Churchill GA, Crawford DL (2002) Variation in gene expression within and among natural populations. Nature Genet 32: 261-266.
68. Ouborg NJ, Vriezen WH (2007) An ecologist's guide to ecogenomics. J Ecol 95: 8-16.
69. Pai RK, Convery M, Hamilton TA, Boom WH, Harding CV (2003) Inhibition of IFN-γ-induced class II transactivator expression by a 19-kDa lipoprotein from Mycobacterium tuberculosis: a potential mechanism for immune evasion. J Immunol 171: 175-184.
70. Parham P, Otha T (1996) Population biology of antigen presentation by MHC class I molecules. Science 272: 67-74.
71. Penn DJ, Potts WK (1999) The evolution of mating preferences and major histocompatibility complex genes. Am Nat. 153: 145-164.
72. Piertney SB, Oliver MK (2006) The evolutionary ecology of the major histocompatibility complex. Heredity 96: 7-21.
73. Racanelli V, Rehermann B (2006) The liver as an immunological organ. Hepatology 43: 54-62.
74. Ramakers C, Ruijter JM, Lekanne Deprez RH, Moorman AFM (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339: 62-66.
75. Reiczigel J, Rózsa L (2005) Quantitative parasitology 3. 0. Budapest. Distributed by the authors.
76. Reiczigel J, Abonyi-Tóth Z, Singer J (2008) An exact confidence set for two binomial proportions and exact unconditional confidence intervals for the difference and ratio of proportions. Comput Stat Data Anal 52: 5046-5053.
77. Rózsa L, Reiczigel J, Majoros G (2010) Quantifying parasites in samples of hosts. J Parasitol 86: 228-232.
78. Ruijter JM, Ramakers C, Hoogaars WMH, Karlen Y, Bakker O, van den Hoff MJB, Moorman AFM (2009) Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res 37: e45.
79. Schad J, Dechmann D, Voigt C, Sommer S (2012) Evidence for the 'good genes' theory: association of parasitism and reproductive state with immune gene constitution in the bat, Noctilio albiventris. PLoS ONE 7(5): e37101.
80. Schwensow N, Dausmann KH, Eberle M, Fietz J, Sommer S (2010) Functional associations of similar MHC alleles and shared parasite species in two sympatric lemurs. Infect Gene Evol 10: 662-668.
81. Schwensow N, Axtner J, Sommer S (2011) 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 Gene Evol 11: 23-30.
82. Seivwreight LJ, Redpath SM, Mougeot F, Watt L, Hudson PJ (2004) Faecal egg counts provide a reliable measure of Trichostrongylus tenuis intensities in free-living red grouse Lagopus lagopus scoticus. J Helminthol 78: 69-76.
83. Selmi C, Mackay IR, Gershwin ME (2007) The immunological milieu of the liver. Semin Liver Dis 27: 129-139.
84. Slade RW, McCallum HI (1992) Overdominant vs. frequency-dependent selection at MHC loci. Genetics 132: 861-862.
85. Sommer S (2005) The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Front Zool 2: 16.
86. Spurgin LG, Richardson DS (2010) How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proc Biol Sci 277: 979-988.
87. Takahata N, Nei M (1990) Allelic genealogy under overdominant and frequency-dependent selection and polymorphism of major histocompatibility complex loci. Genetics 124: 967-978.
88. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4. 0. Mol Biol Evol 24: 1596-1599.
89. Thellin O, Zorzi W, Lakaye B, De Borman B, Coumans B, Hennen G, Grisar T, Igout A, Heinen E (1999) Housekeeping genes as internal standards: use and limits. J Biotechnol 75: 291-295.
90. Tiegs G, Lohse AW (2009) Immune tolerance: what is unique about the liver. J Autoimmun 34: 1-6.
91. Ting JP-Y, Trowsdale J (2002) Genetic control of MHC class II expression. Cell 109: S21-S33.
92. Vandesompele J, De Preter K, Pattyn F, Poppe B, van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: 7.
93. Wegner KM, Kalbe M, Rauch G, Kurtz J, Schaschl H, Reusch TBH (2006) Genetic variation in MHC class II expression and interactions with MHC sequence polymorphism in three-spined sticklebacks. Mol Ecol 15: 1153-1164.
94. Westerdahl H (2004) No evidence of an MHC-based female mating preference in great reed warblers. Mol Ecol 13: 2465-2470.
95. Willems E, Leyns L, Vandesompele J (2008) Standardization of real-time PCR gene expression data from independent biological replicates. Anal Biochem 379: 127-129.
96. Wojciechowski W, DeSanctis J, Skamene E, Radzioch D (1999) Attenuation of MHC class II expression in macrophages infected with Mycobacterium bovis bacillus Calmette-Guerin involves class II transactivator and depends on the Nramp1 gene. J Immunol 163: 2688-2696.
97. Yang Z (2007) PAML 4: a program package for phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586-1591.
98. Zhong G, Fan T, Liu L (1999) Chlamydia inhibits interferon γ-inducible major histocompatibility complex class II expression by degradation of upstream stimulatory factor 1. J Exp Med 189: 1931-1938.