Escherichia coli- and Staphylococcus aureus-induced mastitis differentially modulate transcriptional responses in neighbouring uninfected bovine mammary gland quarters

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Jensen, Kirsty ^a   Günther, Juliane ^b   Talbot, Richard ^a   Petzl, Wolfram ^c   Zerbe, Holm ^c   Schuberth, Hans Joachim ^d   Seyfert, Hans Martin ^b   Glass, Elizabeth J ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b LEIBNIZ INSTITUTE FOR FARM ANIMAL BIOLOGY FBN   (Germany)

^c UNIVERSITY OF MUNICH   (Germany)

^d UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

Author keywords

Bovine; Escherichia coli; Mastitis; Microarray; Staphylococcus aureus

Indexed keywords

TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BOVINE MASTITIS; CONTROLLED STUDY; COW; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTION; FEMALE; GENE EXPRESSION; GENE IDENTIFICATION; IMMUNOREGULATION; MAMMARY GLAND; MICROARRAY ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION; TRANSCRIPTION REGULATION; TRANSFORMING GROWTH FACTOR BETA1 GENE; UNINDEXED SEQUENCE;

ANIMALS; CATTLE; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; FEMALE; GENE EXPRESSION REGULATION; MAMMARY GLANDS, ANIMAL; MASTITIS, BOVINE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; TIME FACTORS; TRANSCRIPTION, GENETIC;

ANIMALIA; BOS; BOVINAE; ESCHERICHIA COLI; STAPHYLOCOCCUS AUREUS;

EID: 84872177827     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-36     Document Type: Article

References (60)

1. Viguier C, Arora S, Gilmartin N, Welbeck K, O'Kennedy R. Mastitis detection: current trends and future perspectives. Trends Biotech 2009, 27:486-493.
2. Schukken YH, Günther J, Fitzpatrick J, Fontaine MC, Goetze L, Holst O, Leigh J, Petzl W, Schuberth HJ, Sipka A, Smith DGE, Quesnell R, Watts J, Yancey R, Zerbe H, Gurjar A, Zadoks RN, Seyfert HM. Host-response patterns of intramammary infections in dairy cows. Vet Immunol Immunopath 2011, 144:270-289.
3. Rinaldi M, Li RW, Bannerman DD, Daniels KM, Evock-Clover C, Silva MVB, Paape MJ, Van Ryssen B, Burvenich C, Capuco AV. A sentinel function for teat tissues in dairy cows: dominant innate immune response elements define early response to E. coli mastitis. Funct Integr Genomics 2010, 10:21-38.
4. Buitenhuis B, Røntved CM, Edwards SM, Ingvartsen KL, Sørensen P. In depth analysis of genes and pathways of the mammary gland involved in the pathogenesis of bovine Escherichia coli-mastitis. BMC Genomics 2011, 12:130.
5. Moyes KM, Drackley JK, Morin DE, Bionaz M, Rodriguez-Zas SL, Everts RE, Lewin HA, Loor JJ. Gene network and pathway analysis of bovine mammary tissue challenged with Streptococcus uberis reveals induction of cell proliferation and inhibition of PPARγ signalling as potential mechanism for the negative relationships between immune response and lipid metabolism. BMC Genomics 2009, 10:542.
6. Swanson KM, Stelwagen K, Dobson J, Henderson HV, Davis SR, Farr VC, Singh K. Transcriptome profiling of Streptococcus uberis-induced mastitis reveals fundamental differences between immune gene expression in the mammary gland and in a primary cell culture model. J Dairy Sci 2009, 92:117-129.
7. Lutzow YCS, Donaldson L, Gray CP, Vuocolo T, Pearson RD, Reverter A, Byrne KA, Sheehy PA, Windon R, Tellam RL. Identification of immune genes and proteins involved in the response of bovine mammary tissue to Staphylococcus aureus infection. BMC Vet Res 2008, 4:18.
8. Genini S, Badaoui B, Sclep G, Bishop SC, Waddington D, van der Pinard LMH, Klopp C, Cabau C, Seyfert HM, Petzl W, Jensen K, Glass EJ, de Greeff A, Smith HE, Smits MA, Olsaker I, Boman GM, Pisoni G, Moroni P, Castiglioni B, Cremonesi P, Del Corvo M, Foulon E, Foucras G, Rupp R, Giuffra E. Strengthening insights into host reponses to mastitis infection in ruminants by combining heterogeneous microarray data sources. BMC Genomics 2011, 12:225.
9. Loor JJ, Moyes KM, Bionaz M. Functional adaptations of the transcriptome to mastitis-causing pathogens: the mammary gland and beyond. J Mammary Gland Biol Neoplasia 2011, 16:305-322.
10. Petzl W, Zerbe H, Günther J, Yang W, Seyfert H-M, Nürnberg G, Schuberth HJ. Escherichia coli, but not Staphylococcus aureus, triggers an early increased expression of factors contributing to the innate immune defense in the udder of the cow. Vet Res 2008, 39:18.
11. Chang CC, Winter AJ, Norcross NL. Immune response in the bovine mammary gland after intestinal, local and systemic immunization. Infect Immun 1981, 31:650-659.
12. Mehrzad J, Dosogne H, Meyer E, Burvenich C. Local and systemic effects of endotoxin mastitis on the chemiluminescence of milk and blood neutrophils in dairy cows. Vet Res 2001, 32:131-144.
13. Bannerman DD, Paape MJ, Lee JW, Zhao X, Hope JC, Rainard P. Escherichia coli and Staphylococcus aureus elicit differential innate immune responses following intramammary infection. Clin Diagn Lab Immunol 2004, 11:463-472.
14. Schmitz S, Pfaffl MW, Meyer HHD, Bruckmaier RM. Short-term changes of mRNA expression of various inflammatory factors and milk proteins in mammary tissue during LPS-induced mastitis. Domest Anim Endocrin 2004, 26:111-126.
15. Silva LFP, Liesman JS, Etchbarne BE, Nielsen MSW, VandeHaar MJ. Intramammary infusion of IGF-1 increases bromodeoxyuridine labelling in mammary epithelial cells of prepubertal heifers. J Dairy Sci 2005, 88:2771-2773.
16. Grönlund U, Johannisson A, Waller KP. Changes in blood and milk lymphocyte sub-populations during acute and chronic phases of Staphylococcus aureus induced bovine mastitis. Res Vet Sci 2006, 80:147-154.
17. Mitterhuemer S, Petzl W, Krebs S, Mehne D, Klanner A, Wolf E, Zerbe H, Blum H. Escherichia coli infection induces distinct local and systemic transcriptome responses in the mammary gland. BMC Genomics 2010, 11:138.
18. Donaldson L, Vuocolo T, Gray C, Strandberg Y, Reverter A, McWilliam S, Wang Y, Byrne K, Tellam R. Construction and validation of a bovine innate immune microarray. BMC Genomics 2005, 6:135.
19. Dennis G, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA. DAVID: database for annotation, visualization and integrated discovery. Genome Biol 2003, 4:P3.
20. Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009, 4:44-57.
21. Günther J, Esch K, Poschadel N, Petzl W, Zerbe H, Mitterhuemer S, Blum H, Seyfert HM. Comparative kinetics of Escherichia coli- and Staphylococcus aureus-specific activation of key immune pathways in mammary epithelial cells demonstrates that S. aureus elicits a delayed response dominated by interleukin-6 (IL-6) but not IL-1A or tumor necrosis factor alpha. Infect Immun 2011, 79:695-707.
22. Rainard P, Riollet C. Innate immunity of the bovine mammary gland. Vet Res 2006, 37:369-400.
23. Whelehan CJ, Meade KG, Eckersall PD, Young FJ, O'Farrelly CO. Experimental Staphylococcus aureus infection of the mammary gland induces region-specific changes in innate immune gene expression. Vet Immunol Immunopathol 2011, 140:181-189.
24. Burvenich C, Van Merris V, Mehrzad J, Diez-Fraile A, Duchateau L. Severity of E. coli mastitis is mainly determined by cow factors. Vet Res 2003, 34:521-564.
25. Bansal BK, Hamann J, Grabowski NT, Singh KB. Variation in the composition of selected milk fraction samples from healthy and mastitic quarters and its significance for mastitis diagnosis. J Dairy Res 2005, 72:144-152.
26. Hamann J, Schröder A, Merle R. Differential cell count and interdependence of udder quarters. Mastitis in dairy production: current knowledge and future solutions 2005, 190-195. The Netherlands: Wageningen Academic Publishers, Hogeveen H.
27. Merle R, Schröder A, Hamann J. Cell function in the bovine mammary gland: a preliminary study on interdependence of healthy and infected udder quarters. J Dairy Res 2007, 74:174-179.
28. Riollet C, Rainard P, Poutrel B. Cell subpopulations and cytokine expression in cow milk in response to chronic Staphylococcus aureus infection. J Dairy Sci 2001, 84:1077-1084.
29. Suojala L, Orro T, Järvinen H, Saatsi J, Pyörälä S. Acute phase response in two consecutive experimentally induced E. coli intramammary infections in dairy cows. Acta Vet Scand 2008, 50:18.
30. Petzl W, Günther J, Pfister T, Sauter-Louis C, Goetze L, von Aulock S, Hafner-Marx A, Schuberth H-J, Seyfert H-M, Zerbe H. Lipopolysaccharide pretreatment of the udder protects against experimental Escherichia coli mastitis. Innate Immun 2012, 18:467-477.
31. Günther J, Petzl W, Zerbe H, Schuberth H-J, Koczan D, Goetze L, Seyfert H-M. Lipopolysaccharide priming enhances expression of effectors of immune defence while decreasing expression of pro-inflammatory cytokines in mammary epithelia cells from cows. BMC Genomics 2012, 13:17.
32. Yang W, Zerbe H, Petzl W, Brunner RM, Gunther J, Draing C, von Aulock S, Schuberth HJ, Seyfert HM. Bovine TLR2 and TLR4 properly transduce signals from Staphylococcus aureus and E. coli, but S. aureus fails to both activate NF-κB in mammary epithelial cells and to quickly induce TNFα and interleukin-8 (CXCL8) expression in the udder. Mol Immunol 2008, 45:1385-1397.
33. Li MO, Wan YY, Sanjabi S, Robertson AKL, Flavell RA. Transforming growth factor-β regulation of immune responses. Annu Rev Immunol 2006, 24:99-146.
34. Jonker JW, Merino G, Musters S, van Herwaarden AE, Bolscher E, Wagenaar E, Mesman E, Dale TC, Schinkel AH. The breast cancer resistance protein BCRP (ABCG2) concentrates drugs and carcinogenic xenotoxins into milk. Nat Med 2005, 11:127-129.
35. Mani O, Sorensen MT, Sejrsen K, Bruckmaier RM, Albrecht C. Differential expression and localization of lipid transporters in the bovine mammary gland during the pregnancy-lactation cycle. J Dairy Sci 2009, 92:3744-3756.
36. van Herwaarden AE, Wagenaar E, Merino G, Jonker JW, Rosing H, Beijnen JH, Schinkel AH. Multidrug transporter ABCG2/breast cancer resistance protein secretes riboflavin (vitamin B2) into milk. Mol Cell Biol 2007, 27:1247-1253.
37. Cohen-Zinder M, Seroussi E, Larkin DM, Loor JJ, Loor JJ, van der Everts WA, Lee J-H, Drackley JK, Band MR, Hernandez AG, Shani M, Lewin HA, Weller JI, Ron M. Identification of a missense mutation in the bovine ABCG2 gene with a major effect on the QTL on chromosome 6 affecting milk yield and composition in Holstein cattle. Genome Res 2005, 15:936-944.
38. Weikard R, Widmann P, Buitkamp J, Emmerling R, Kuehn C. Revisiting the quantitative trait loci for milk production traits on BTA6. Anim Genet 2011, 43:318-323.
39. Vanselow J, Yang W, Herrmann J, Zerbe H, Schuberth H-J, Petzl W, Tomek W, Seyfert H-M. DNA-remethylation around a STAT5-binding enhancer in the αS1-casein promoter is associated with abrupt shutdown of αS1-casein synthesis during acute mastitis. J Mol Endocrinol 2006, 37:463-477.
40. Baughman G, Wiederrecht GJ, Campbell NF, Martin MM, Bourgeois S. FKBP51, a novel T-cell-specific immunophilin capable of calcineurin inhibition. Mol Cell Biol 1995, 15:4395-4402.
41. Denny WB, Valentine DL, Reynolds PD, Smith DF, Scammell JG. Squirrel monkey immunophilin FKBP51 is a potent inhibitor of glucocorticoid receptor binding. Endocrinology 2000, 141:4107-4113.
42. Park J, Kim M, Na G, Jeon I, Kwon Y, Kim J, Youn H, Koo Y. Glucocorticoids modulate NF-κB-dependent gene expression by up-regulating FKBP51 expression in Newcastle disease virus-infected chickens. Mol Cell Endo 2007, 278:7-17.
43. Bouwmeester T, Bauch A, Ruffner H, Angrand P-O, Bergamini G, Croughton K, Cruciat C, Eberhard D, Gagneur J, Ghidelli S, Hopf C, Huhse B, Mangano R, Michon AM, Schirle M, Schleg J, Schwab M, Stein MA, Bauer A, Casari G, Drewes G, Gavin AC, Jackson DB, Joberty G, Naubauer G, Rick J, Kuster B, Superti-Furga G. A physical and functional map of the human TNF-α/NF-κB signal transduction pathway. Nat Cell Biol 2004, 6:97-105.
44. Jiang L, Sørensen P, Røntved C, Vels L, Ingvartsen KL. Gene expression profiling of liver from dairy cows treated intra-mammary with lipopolysaccharide. BMC Genomics 2008, 9:443.
45. Matzinger P. Tolerance, danger, and the extended family. Annu Rev Immunol 1994, 12:991-1045.
46. Manson J, Thiemermann C, Brohi K. Trauma alarmins as activators of damage-induced inflammation. Brit J Surg 2012, 99(Suppl 1):12-20.
47. Fontana MF, Vance RE. Two signal models in innate immunity. Immunol Rev 2011, 243:26-39.
48. Kimura K, Harp JA, Goff JP, Olsen SC. Lymphocytes from one side of the bovine mammary gland migrate to the contra lateral gland and lymph node tissue. Vet Immunol Immunopathol 2005, 108:409-415.
49. Chirgwin JM, Przybyla AE, MacDonald RJ, Rutter WJ. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 1979, 18:5294-5299.
50. Smyth GK. Bioinformatics and Computational Biology Solutions using R and Bioconductor. Bioinformatics and Computational Biology Solutions using R and Bioconductor 2005, 397-420. New York: Springer, Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W.
51. Jaffrézic F, de Koning DJ, Boettcher PJ, Bonnet A, Buitenhuis B, Closset R, Déjean A, Delmas C, Detilleux JC, Dovč P, Duval M, Foulley J-L, Hedegaard J, Hornshøj H, Hulsegge I, Janss L, Jensen K, Jiang L, Lavrič M, Lê Cao K-A, Lund MS, Malinverni R, Marot G, Nie H, Petzl W, Pool MH, Robert-Granié C, San Cristobal M, van Schothorst EM, Schuberth H-J, et al. Analysis of the real EADGENE dataset: comparison of methods and guidelines for data normalisation and selection of differentially expressed genes. Genet Sel Evol 2007, 39:633-650.
52. Jensen K, Talbot R, Paxton E, Waddington D, Glass EJ. Development and validation of a bovine macrophage specific cDNA microarray. BMC Genomics 2006, 7:224.
53. Baird D, Johnstone P, Wilson T. Normalization of microarray data using a spatial mixed model analysis which includes splines. Bioinformatics 2004, 20:3196-3205.
54. Smyth GK, Speed TP. Normalization of cDNA microarray data. Methods 2003, 31:265-273.
55. Smyth GK. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004, 3:3.
56. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B 1995, 57:289-300.
57. Rozen S, Skaletsky HJ. Primer3 on the WWW for general users and for biologist programmers. Bioinformatics Methods and Protocols: Methods in Molecular Biology 2000, 365-386. Totowa: Humana Press, Krawetz S, Misener S.
58. Jensen K, Paxton E, Waddington D, Talbot R, Darghouth M, Glass EJ. Differences in the transcriptional responses induced by Theileria annulata infection in bovine monocytes derived from resistant and susceptible cattle breeds. Int J Parasitol 2008, 38:313-325.
59. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001, 29:e45.
60. Goldammer T, Zerbe H, Molenaar A, Schuberth HJ, Brunner RM, Kata SR, Seyfert HM. Mastitis increases mammary mRNA abundance of beta-defensin 5, toll-like-receptor 2 (TLR2), and TLR4 but not TLR9 in cattle. Clin Diagn Lab Immunol 2004, 11:174-185.