Transcriptional profiling of cattle infected with Trypanosoma congolense highlights gene expression signatures underlying trypanotolerance and trypanosusceptibility
详细信息 查看全文
- 作者：Grace M O'Gorman (1)
Stephen DE Park (1)
Emmeline W Hill (1)
Kieran G Meade (2)
Paul M Coussens (3)
Morris Agaba (4)
Jan Naessens (4)
Stephen J Kemp (5)
David E MacHugh (1) (6) - 刊名：BMC Genomics
- 出版年：2009
- 出版时间：December 2009
- 年：2009
- 卷：10
- 期：1
- 全文大小：2174KB
- 参考文献：1. Darji A, Lucas R, Magez S, Torreele E, Palacios J, Sileghem M, Bajyana Songa E, Hamers R, De Baetselier P: Mechanisms underlying trypanosome-elicited immunosuppression. / Ann Soc Belg Med Trop 1992,72(Suppl 1):27-8.
2. Murray M, Dexter TM: Anaemia in bovine African trypanosomiasis. A review. / Acta Trop 1988,45(4):389-32.
3. Cattand P, Jannin J, Lucas P: Sleeping sickness surveillance: an essential step towards elimination. / Trop Med Int Health 2001,6(5):348-61. CrossRef
4. Naessens J: Bovine trypanotolerance: A natural ability to prevent severe anaemia and haemophagocytic syndrome? / Int J Parasitol 2006,36(5):521-28. CrossRef
5. Borst P, Cross GA: Molecular basis for trypanosome antigenic variation. / Cell 1982,29(2):291-03. CrossRef
6. Donelson JE: Antigenic variation and the African trypanosome genome. / Acta Trop 2003,85(3):391-04. CrossRef
7. Pays E: Regulation of antigen gene expression in Trypanosoma brucei. / Trends Parasitol 2005,21(11):517-20. CrossRef
8. Kristjanson PM, Swallow BM, Rowlands GJ, Kruska RL, de Leeuw PN: Measuring the costs of African trypanosomosis, the potential benefits of control and returns to research. / Agric Syst 1999, (59):79-8.
9. Murray M, Morrison WI, Whitelaw DD: Host susceptibility to African trypanosomiasis: trypanotolerance. / Adv Parasitol 1982, 21:1-8. CrossRef
10. Murray M, Trail JC, D'Ieteren GD: Trypanotolerance in cattle and prospects for the control of trypanosomiasis by selective breeding. / Rev Sci Tech 1990,9(2):369-86.
11. Naessens J, Teale AJ, Sileghem M: Identification of mechanisms of natural resistance to African trypanosomiasis in cattle. / Vet Immunol Immunopathol 2002,87(3-):187-94. CrossRef
12. Paling RW, Moloo SK, Scott JR, McOdimba FA, Logan-Henfrey LL, Murray M, Williams DJ: Susceptibility of N'Dama and Boran cattle to tsetse-transmitted primary and rechallenge infections with a homologous serodeme of Trypanosoma congolense. / Parasite Immunol 1991,13(4):413-25. CrossRef
13. Hill EW, O'Gorman GM, Agaba M, Gibson JP, Hanotte O, Kemp SJ, Naessens J, Coussens PM, MacHugh DE: Understanding bovine trypanosomiasis and trypanotolerance: the promise of functional genomics. / Vet Immunol Immunopathol 2005,105(3-):247-58. CrossRef
14. O'Gorman GM, Park SD, Hill EW, Meade KG, Mitchell LC, Agaba M, Gibson JP, Hanotte O, Naessens J, Kemp SJ, / et al.: Cytokine mRNA profiling of peripheral blood mononuclear cells from trypanotolerant and trypanosusceptible cattle infected with Trypanosoma congolense. / Physiol Genomics 2006,28(1):53-1. CrossRef
15. Barrett T, Troup DB, Wilhite SE, Ledoux P, Rudnev D, Evangelista C, Kim IF, Soboleva A, Tomashevsky M, Edgar R: NCBI GEO: mining tens of millions of expression profiles - database and tools update. / Nucleic Acids Res 2007, (35 Database):D760-65.
16. Lang T, Mansell A: The negative regulation of Toll-like receptor and associated pathways. / Immunol Cell Biol 2007,85(6):425-34. CrossRef
17. Dey R, Khan S, Pahari S, Srivastava N, Jadhav M, Saha B: Functional paradox in host-pathogen interaction dictates the fate of parasites. / Future Microbiol 2007, 2:425-37. CrossRef
18. Hanotte O, Ronin Y, Agaba M, Nilsson P, Gelhaus A, Horstmann R, Sugimoto Y, Kemp S, Gibson J, Korol A, / et al.: Mapping of quantitative trait loci controlling trypanotolerance in a cross of tolerant West African N'Dama and susceptible East African Boran cattle. / Proc Natl Acad Sci USA 2003,100(13):7443-448. CrossRef
19. Wang H, Frelin L, Pevsner J: Human syntaxin 7: a Pep12p/Vps6p homologue implicated in vesicle trafficking to lysosomes. / Gene 1997,199(1-):39-8. CrossRef
20. Wong SH, Xu Y, Zhang T, Hong W: Syntaxin 7, a novel syntaxin member associated with the early endosomal compartment. / J Biol Chem 1998,273(1):375-80. CrossRef
21. Castle A, Castle D: Ubiquitously expressed secretory carrier membrane proteins (SCAMPs) 1- mark different pathways and exhibit limited constitutive trafficking to and from the cell surface. / J Cell Sci 2005,118(Pt 16):3769-780. CrossRef
22. Fernandez-Chacon R, Achiriloaie M, Janz R, Albanesi JP, Sudhof TC: SCAMP1 function in endocytosis. / J Biol Chem 2000,275(17):12752-2756. CrossRef
23. Kouranti I, Sachse M, Arouche N, Goud B, Echard A: Rab35 regulates an endocytic recycling pathway essential for the terminal steps of cytokinesis. / Curr Biol 2006,16(17):1719-725. CrossRef
24. Reyes SL, Leon BF, Rozas VM, Gonzalez JP, Naves PR: BAFF: A regulatory cytokine of B lymphocytes involved in autoimmunity and lymphoid cancer. / Rev Med Chil 2006,134(9):1175-184.
25. Woodland RT, Schmidt MR, Thompson CB: BLyS and B cell homeostasis. / Semin Immunol 2006,18(5):318-26. CrossRef
26. Fearon DT, Carroll MC: Regulation of B lymphocyte responses to foreign and self-antigens by the CD19/CD21 complex. / Annu Rev Immunol 2000, 18:393-22. CrossRef
27. Smith KG, Fearon DT: Receptor modulators of B-cell receptor signalling - CD19/CD22. / Curr Top Microbiol Immunol 2000,245(1):195-12.
28. Devadas S, Das J, Liu C, Zhang L, Roberts AI, Pan Z, Moore PA, Das G, Shi Y: Granzyme B is critical for T cell receptor-induced cell death of type 2 helper T cells. / Immunity 2006,25(2):237-47. CrossRef
29. Wood P: Understanding immunology. / 2 Edition Harlow, England; New York: Pearson Prentice Hall 2006.
30. Pende D, Parolini S, Pessino A, Sivori S, Augugliaro R, Morelli L, Marcenaro E, Accame L, Malaspina A, Biassoni R, / et al.: Identification and molecular characterization of NKp30, a novel triggering receptor involved in natural cytotoxicity mediated by human natural killer cells. / J Exp Med 1999,190(10):1505-516. CrossRef
31. Moretta A, Bottino C, Vitale M, Pende D, Cantoni C, Mingari MC, Biassoni R, Moretta L: Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis. / Annu Rev Immunol 2001, 19:197-23. CrossRef
32. Delahaye NF, Barbier M, Fumoux F, Rihet P: Association analyses of NCR3 polymorphisms with P. falciparum mild malaria. / Microbes Infect 2007,9(2):160-66. CrossRef
33. Hirst M, Haliday E, Nakamura J, Lou L: Human GMP synthetase. Protein purification, cloning, and functional expression of cDNA. / J Biol Chem 1994,269(38):23830-3837.
34. Diener K, Wang XS, Chen C, Meyer CF, Keesler G, Zukowski M, Tan TH, Yao Z: Activation of the c-Jun N-terminal kinase pathway by a novel protein kinase related to human germinal center kinase. / Proc Natl Acad Sci USA 1997,94(18):9687-692. CrossRef
35. Katz P, Whalen G, Kehrl JH: Differential expression of a novel protein kinase in human B lymphocytes. Preferential localization in the germinal center. / J Biol Chem 1994,269(24):16802-6809.
36. Ramjaun AR, Angers A, Legendre-Guillemin V, Tong XK, McPherson PS: Endophilin regulates JNK activation through its interaction with the germinal center kinase-like kinase. / J Biol Chem 2001,276(31):28913-8919. CrossRef
37. Donovan A, Lima CA, Pinkus JL, Pinkus GS, Zon LI, Robine S, Andrews NC: The iron exporter ferroportin/Slc40a1 is essential for iron homeostasis. / Cell Metab 2005,1(3):191-00. CrossRef
38. Dunn LL, Rahmanto YS, Richardson DR: Iron uptake and metabolism in the new millennium. / Trends Cell Biol 2007,17(2):93-00. CrossRef
39. Jacobs HT, Turnbull DM: Nuclear genes and mitochondrial translation: a new class of genetic disease. / Trends Genet 2005,21(6):312-14. CrossRef
40. Taanman JW: The mitochondrial genome: structure, transcription, translation and replication. / Biochim Biophys Acta 1999,1410(2):103-23. CrossRef
41. Cartharius K, Frech K, Grote K, Klocke B, Haltmeier M, Klingenhoff A, Frisch M, Bayerlein M, Werner T: MatInspector and beyond: promoter analysis based on transcription factor binding sites. / Bioinformatics 2005,21(13):2933-942. CrossRef
42. Quandt K, Frech K, Karas H, Wingender E, Werner T: MatInd and MatInspector: new fast and versatile tools for detection of consensus matches in nucleotide sequence data. / Nucleic Acids Res 1995,23(23):4878-884. CrossRef
43. Geigy R, Kauffmann M: Sleeping sickness survey in the Serengeti area (Tanzania) 1971. I. Examination of large mammals for trypanosomes. / Acta Trop 1973,30(1):12-3.
44. Nantulya VM, Musoke AJ, Rurangirwa FR, Moloo SK: Resistance of cattle to tsetse-transmitted challenge with Trypanosoma brucei or Trypanosoma congolense after spontaneous recovery from syringe-passaged infections. / Infect Immun 1984,43(2):735-38.
45. Akol GW, Murray M: Early events following challenge of cattle with tsetse infected with Trypanosoma congolense : development of the local skin reaction. / Vet Rec 1982,110(13):295-02. CrossRef
46. Dwinger RH, Murray M, Moloo SK: Potential value of localized skin reactions (chancres) induced by Trypanosoma congolense transmitted by Glossina morsitans centralis for the analysis of metacyclic trypanosome populations. / Parasite Immunol 1987,9(3):353-62. CrossRef
47. Ulmer AJ, Scholz W, Ernst M, Brandt E, Flad HD: Isolation and subfractionation of human peripheral blood mononuclear cells (PBMC) by density gradient centrifugation on Percoll. / Immunobiology 1984,166(3):238-50.
48. Reimers M, Carey VJ: Bioconductor: an open source framework for bioinformatics and computational biology. / Methods Enzymol 2006, 411:119-34. CrossRef
49. Smyth GK: Linear models and empirical bayes methods for assessing differential expression in microarray experiments. / Stat Appl Genet Mol Biol 2004, 3:Article3.
50. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP: Exploration, normalization, and summaries of high density oligonucleotide array probe level data. / Biostatistics 2003,4(2):249-64. CrossRef
51. Yang YH, Dudoit S, Luu P, Lin DM, Peng V, Ngai J, Speed TP: Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. / Nucleic Acids Res 2002,30(4):e15. CrossRef
52. Benjamini Y, Hochberg Y: Controlling the false discovery rate - a practical and powerful approach to multiple testing. / J R Stat Soc Series B Stat Methodol 1995,57(1):289-00.
53. Falcon S, Gentleman R: Using GOstats to test gene lists for GO term association. / Bioinformatics 2007,23(2):257-58. CrossRef
54. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F: Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. / Genome Biol 2002,3(7):RESEARCH0034. CrossRef
55. Livak KJ, Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. / Methods 2001,25(4):402-08. CrossRef - 作者单位：Grace M O'Gorman (1)
Stephen DE Park (1)
Emmeline W Hill (1)
Kieran G Meade (2)
Paul M Coussens (3)
Morris Agaba (4)
Jan Naessens (4)
Stephen J Kemp (5)
David E MacHugh (1) (6)
1. Animal Genomics Laboratory, UCD School of Agriculture, Food Science and Veterinary Medicine, UCD College of Life Sciences, University College Dublin, Belfield, Dublin 4, Ireland
2. Comparative Immunology Group, School of Biochemistry and Immunology, Trinity College Dublin, Dublin 2, Ireland
3. Department of Animal Science and Center for Animal Functional Genomics, Michigan State University, 48824, East Lansing, Michigan, USA
4. International Livestock Research Institute, Box 30709, 00100, Nairobi, Kenya
5. School of Biological Sciences, University of Liverpool, L69 7ZD, Liverpool, UK
6. UCD Conway Institute of Biomolecular and Biomedical Research, University College Dublin, Dublin 4, Ireland
文摘
Background African animal trypanosomiasis (AAT) caused by tsetse fly-transmitted protozoa of the genus Trypanosoma is a major constraint on livestock and agricultural production in Africa and is among the top ten global cattle diseases impacting on the poor. Here we show that a functional genomics approach can be used to identify temporal changes in host peripheral blood mononuclear cell (PBMC) gene expression due to disease progression. We also show that major gene expression differences exist between cattle from trypanotolerant and trypanosusceptible breeds. Using bovine long oligonucleotide microarrays and real time quantitative reverse transcription PCR (qRT-PCR) validation we analysed PBMC gene expression in na?ve trypanotolerant and trypanosusceptible cattle experimentally challenged with Trypanosoma congolense across a 34-day infection time course. Results Trypanotolerant N'Dama cattle displayed a rapid and distinct transcriptional response to infection, with a ten-fold higher number of genes differentially expressed at day 14 post-infection compared to trypanosusceptible Boran cattle. These analyses identified coordinated temporal gene expression changes for both breeds in response to trypanosome infection. In addition, a panel of genes were identified that showed pronounced differences in gene expression between the two breeds, which may underlie the phenomena of trypanotolerance and trypanosusceptibility. Gene ontology (GO) analysis demonstrate that the products of these genes may contribute to increased mitochondrial mRNA translational efficiency, a more pronounced B cell response, an elevated activation status and a heightened response to stress in trypanotolerant cattle. Conclusion This study has revealed an extensive and diverse range of cellular processes that are altered temporally in response to trypanosome infection in African cattle. Results indicate that the trypanotolerant N'Dama cattle respond more rapidly and with a greater magnitude to infection compared to the trypanosusceptible Boran cattle. Specifically, a subset of the genes analyzed by real time qRT-PCR, which display significant breed differences, could collectively contribute to the trypanotolerance trait in N'Dama.