Genetic susceptibility to S. aureus mastitis in sheep: Differential expression of mammary epithelial cells in response to live bacteria or supernatant

Physiological Genomics

Volumn 44, Issue 7, 2012, Pages 403-416

  Bonnefont, Cécile M D ^a,b,c   Rainard, Pascal ^d,e   Cunha, Patricia ^d,e   Gilbert, Florence B ^d,e   Toufeer, Mehdi ^a,b   Aurel, Marie Rose ^f   Rupp, Rachel ^c   Foucras, Gilles ^a,b  

^a CNRS   (France)

^b IHAP   (France)

^c CEMAGREF   (France)

^d UR1282   (France)

^e UNIVERSITÉ DE TOURS   (France)

^f Unité Expérimentale   (France)

Author keywords

Genetic predisposition; Mammary epithelial cell; Mastitis; Microarray; Staphylococcus aureus

Indexed keywords

INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 8; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BREAST EPITHELIUM; CELL COUNT; CELL SELECTION; DISEASE PREDISPOSITION; EWE; GENE EXPRESSION; GENETIC SUSCEPTIBILITY; IMMUNE RESPONSE; INFLAMMATION; MASTITIS; MICROARRAY ANALYSIS; MONONUCLEAR CELL; NEUTROPHIL; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; STAPHYLOCOCCUS AUREUS; STIMULATION; SUPERNATANT; UPREGULATION;

ANIMALS; CLUSTER ANALYSIS; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORKS; GENETIC PREDISPOSITION TO DISEASE; MAMMARY GLANDS, ANIMAL; MASTITIS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SHEEP; STAPHYLOCOCCUS AUREUS; SUBCELLULAR FRACTIONS;

ANIMALIA; BACTERIA (MICROORGANISMS); OVIS ARIES; STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS;

EID: 84859527849     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00155.2011     Document Type: Article

References (61)

1. Aderem A, Ulevitch RJ. Toll-like receptors in the induction of the innate immune response. Nature 406: 782-787, 2000.
2. Van Amersfoort ES, Van Berkel TJC, Kuiper J. Receptors, mediators, and mechanisms involved in bacterial sepsis and septic shock. Clin Microbiol Rev 16: 379-414, 2003.
3. Barber MR, Pantschenko AG, Hinckley LS, Yang TJ. Inducible and constitutive in vitro neutrophil chemokine expression by mammary epithelial and myoepithelial cells. Clin Diagn Lab Immunol 6: 791-798, 1999.
4. Barkema HW, Green MJ, Bradley AJ, Zadoks RN. Invited review: the role of contagious disease in udder health. J Dairy Sci 92: 4717-4729, 2009.
5. Bayles KW, Wesson CA, Liou LE, Fox LK, Bohach GA, Trumble WR. Intracellular Staphylococcus aureus escapes the endosome and induces apoptosis in epithelial cells. Infect Immun 66: 336-342, 1998.
6. Bergonier D, de Crémoux R, Rupp R, Lagriffoul G, Berthelot X. Mastitis of dairy small ruminants. Vet Res 34: 689-716, 2003.
7. Boldrick JC, Alizadeh AA, Diehn M, Dudoit S, Liu CL, Belcher CE, Botstein D, Staudt LM, Brown PO, Relman DA. Stereotyped and specific gene expression programs in human innate immune responses to bacteria. Proc Natl Acad Sci USA 99: 972-977, 2002.
8. Bonnefont C, Toufeer M, Caubet C, Foulon E, Tasca C, Aurel MR, Bergonier D, Boullier S, Robert-Granie C, Foucras G, Rupp R. Transcriptomic analysis of milk somatic cells in mastitis resistant and susceptible sheep upon challenge with Staphylococcus epidermidis and Staphylococcus aureus. BMC Genomics 12: 208-223, 2011.
9. Bossers K, Ylstra B, Brakenhoff RH, Smeets SJ, Verhaagen J, van de Wiel MA. Intensity-based analysis of dual-color gene expression data as an alternative to ratio-based analysis to enhance reproducibility. BMC Genomics 11: 112-124, 2010.
10. Bottero V, Imbert V, Frelin C, Formento JL, Peyron JF. Monitoring NF-kappa B transactivation potential via real-time PCR quantification of I kappa B-alpha gene expression. Mol Diagn 7: 187-194, 2003.
11. Boudjellab N, Chan-Tang HS, Zhao X. Bovine interleukin-1 expression by cultured mammary epithelial cells (MAC-T) and its involvement in the release of MAC-T derived interleukin-8. Comp Physiol Biochem 127: 191-199, 2000.
12. Bougarn S, Cunha P, Gilbert FB, Meurens F, Rainard P. Technical note: Validation of candidate reference genes for normalization of quantitative PCR in bovine mammary epithelial cells responding to inflammatory stimuli. J Dairy Sci 94: 2425-2430, 2011.
13. Bougarn S, Cunha P, Harmache A, Fromageau A, Gilbert FB, Rainard P. Muramyl dipeptide synergizes with Staphylococcus aureus lipoteichoic acid to recruit neutrophils in the mammary gland and to stimulate mammary epithelial cells. Clin Vaccine Immunol 17: 1797-1809, 2010.
14. Brand B, Hartmann A, Repsilber D, Griesbeck-Zilch B, Wellnitz O, Kuhn C, Ponsuksili S, Meyer HH, Schwerin M. Comparative expression profiling of E. coli and S. aureus inoculated primary mammary gland cells sampled from cows with different genetic predispositions for somatic cell score. Genet Sel Evol 43: 24-40, 2011.
15. Calvinho LF, Almeida RA, Oliver SP. Influence of bacterial factors on proliferation of bovine mammary epithelial cells. Rev Argent Microbiol 33: 28-35, 2001.
16. Casel P, Moreews F, Lagarrigue S, Klopp C. sigReannot: an oligo-set re-annotation pipeline based on similarities with the Ensembl transcripts and Unigene clusters. BMC Proc 3: S3, 2009.
17. Van Damme J, Wuyts A, Froyen G, Van Coillie E, Struyf S, Billiau A, Proost P, Wang J, Opdenakker G. Granulocyte chemotactic protein-2 and related CXC chemokines: from gene regulation to receptor usage. J Leukoc Biol 62: 563-569, 1997.
18. Davies G, Genini S, Bishop SC, Giuffra E. An assessment of opportunities to dissect host genetic variation in resistance to infectious diseases in livestock. Animal 3: 415-436, 2009.
19. Fournier B, Philpott DJ. Recognition of Staphylococcus aureus by the innate immune system. Clin Microbiol Rev 18: 521-540, 2005.
20. de la Fuente R, Díez RM, Domínguez-Bernal G, Orden JA, Martínez-Pulgarín S. Restoring catalase activity in Staphylococcus aureus subsp. anaerobius leads to loss of pathogenicity for lambs. Vet Res 41: 41-52, 2010.
21. Gilot P, Lina G, Cochard T, Poutrel B. Analysis of the genetic variability of genes encoding the RNA III-activating components Agr and TRAP in a population of Staphylococcus aureus strains isolated from cows with mastitis. J Clin Microbiol 40: 4060-4067, 2002.
22. Griesbeck-Zilch B, Meyer HHD, Kuhn CH, Schwerin M, Wellnitz O. Staphylococcus aureus and Escherichia coli cause deviating expression profiles of cytokines and lactoferrin messenger ribonucleic acid in mammary epithelial cells. J Dairy Sci 91: 2215-2224, 2008.
23. Griesbeck-Zilch B, Osman M, Kuhn C, Schwerin M, Bruckmaier RH, Pfaffl MW, Hammerle-Fickinger A, Meyer HHD, Wellnitz O. Analysis of key molecules of the innate immune system in mammary epithelial cells isolated from marker-assisted and conventionally selected cattle. J Dairy Sci 92: 4621-4633, 2009.
24. 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 by IL-1A or tumor necrosis factor alpha. Infection Immunity 79: 695-707, 2011.
25. Günther J, Koczan D, Yang W, Nurnberg G, Repsilber D, Schuberth HJ, Park Z, Maqbool N, Molenaar A, Seyfert HM. Assessment of the immune capacity of mammary epithelial cells: comparison with mammary tissue after challenge with Escherichia coli. Vet Res 40: 31-44, 2009.
26. Holland DB, Bojar RA, Farrar MD, Holland KT. Differential innate immune responses of a living skin equivalent model colonized by Staphylococcus epidermidis or Staphylococcus aureus. FEMS Microbiol Lett 290: 149-155, 2009.
27. Korhonen H, Marnila P, Gill HS. Milk immunoglobulins and complement factors. Br J Nutr 84: 75-80, 2000.
28. Kühn C, Reinhardt F, Schwerin M. Marker assisted selection of heifers improved milk somatic cell count compared to selection on conventional pedigree breeding values. Arch Tierz Dummerstorf 51: 23-32, 2008.
29. Lahouassa H, Moussay E, Rainard P, Riollet C. Differential cytokine and chemokine responses of bovine mammary epithelial cells to Staphylococcus aureus and Escherichia coli. Cytokine 38: 12-21, 2007.
30. Lutzow YC, 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 4: 18-41, 2008.
31. Lutzow SYC, Gray C, Vuocolo T, Donaldson L, Broadway M, Tellam R. Lipopolysaccharide and lipoteichoic acid induce different innate immune responses in bovine mammary epithelial cells. Cytokine 31: 72-86, 2005.
32. Martinez-Pulgarin S, Dominguez-Bernal G, Orden JA, de la Fuente R. Simultaneous lack of catalase and beta-toxin in Staphylococcus aureus leads to increased intracellular survival in macrophages and epithelial cells and to attenuated virulence in murine and ovine models. Microbiology 155: 1505-1515, 2009.
33. Matthews KR, Almeida RA, Oliver SP. Bovine mammary epithelial cell invasion by Streptococcus uberis. Infect Immun 62: 5641-5646, 1994.
34. Moreilhon C, Gras D, Hologne C, Bajolet O, Cottrez F, Magnone V, Merten M, Groux H, Puchelle E, Barbry P. Live Staphylococcus aureus and bacterial soluble factors induce different transcriptional responses in human airway cells. Physiol Genomics 20: 244-255, 2005.
35. Paape MJ, Bannerman DD, Zhao X, Lee JW. The bovine neutrophil: structure and function in blood and milk. Vet Res 34: 597-627, 2003.
36. Paape MJ, Mehrzad J, Zhao X, Detilleux J, Burvenich C. Defense of the bovine mammary gland by polymorphonuclear neutrophil leukocytes. J Mammary Gland Biol 7: 109-121, 2002.
37. Pareek R, Wellnitz O, Van Dorp R, Burton J, Kerr D. Immunorelevant gene expression in LPS-challenged bovine mammary epithelial cells. J Appl Genet 46: 171-177, 2005.
38. Pawitan Y, Michiels S, Koscielny S, Gusnanto A, Ploner A. False discovery rate, sensitivity and sample size for microarray studies. Bioinformatics 21: 3017-3024, 2005.
39. Pisoni G, Moroni P, Genini S, Stella A, Boettcher PJ, Cremonesi P, Scaccabarozzi L, Giuffra E, Castiglioni B. Differentially expressed genes associated with Staphylococcus aureus mastitis in dairy goats. Vet Immunol Immunopathol 135: 208-217, 2010.
40. Rainard P, Corrales JC, Barrio MB, Cochard T, Poutrel B. Leucotoxic activities of Staphylococcus aureus strains isolated from cows, ewes, and goats with mastitis: importance of LukM/LukF=-PV leukotoxin. Clin Diagn Lab Immunol 10: 272-277, 2003.
41. Rainard P, Fromageau A, Cunha P, Gilbert FB. Staphylococcus aureus lipoteichoic acid triggers inflammation in the lactating bovine mammary gland. Vet Res 39: 52-64, 2008.
42. Rainard P, Riollet C, Berthon P, Cunha P, Fromageau A, Rossignol C, Gilbert FB. The chemokine CXCL3 is responsible for the constitutive chemotactic activity of bovine milk for neutrophils. Mol Immunol 45: 4020-4027, 2008.
43. Rainard P, Riollet C. Mobilization of neutrophils and defense of the bovine mammary gland. Reprod Nutr Dev 43: 439-457, 2003.
44. Rescigno M, Lopatin U, Chieppa M. Interactions among dendritic cells, macrophages, and epithelial cells in the gut: implications for immune tolerance. Curr Opin Immunol 20: 669-675, 2008.
45. Riollet C, Rainard P, Poutrel B. Cell subpopulations and cytokine expression in cow milk in response to chronic Staphylococcus aureus infection. J Dairy Sci 84: 1077-1084, 2001.
46. Rozen S, Skaletsky H. Primer3 on the www for general users and for biologist programmers. Meth Mol Biol 132: 365-386, 2000.
47. Rupp R, Bergonier D, Dion S, Hygonenq MC, Aurel MR, Robert-Granié C, Foucras G. Response to somatic cell count-based selection for mastitis resistance in a divergent selection experiment sheep. J Dairy Sci 92: 1203-1219, 2009.
48. da Silva MCA, Zahm JM, Gras D, Bajolet O, Abely M, Hinnrasky J, Milliot M, de Assis MC, Hologne C, Bonnet N, Merten M, Plotkowski MC, Puchelle E. Dynamic interaction between airway epithelial cells and Staphylococcus aureus. Am J Physiol Lung Cell Mol Physiol 287: L543-L551, 2004.
49. Smyth GK. Limma: linear models for microarray data. In: Bioinformatics and Computational Biology Solutions using R and Bioconductor, edited by Gentleman R, Carey VJ, Huber W, Irizarry RA, Dudoit S. New York: Springer, 2005, p. 397-444.
50. Sordillo LM. Factors affecting mammary gland immunity and mastitis susceptibility. Livest Prod Sci 98: 89-99, 2005.
51. Sutra L, Poutrel B. Virulence factors involved in the pathogenesis of bovine intramammary infections due to Staphylococcus aureus. J Med Microbiol 40: 79-89, 1994.
52. 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 92: 117-129, 2009.
53. Tao WJ, Mallard B. Differentially expressed genes associated with Staphylococcus aureus mastitis of Canadian Holstein cows. Vet Immunol Immunopathol 120: 201-211, 2007.
54. Toufeer M, Bonnefont CMD, Foulon E, Caubet C, Tasca C, Aurel MR, Robert-Granié C, Rupp R, Foucras G. Gene expression profiling of dendritic cells reveals important mechanisms associated with predisposition to staphylococcus infections. PLoS One 6: e22147-e22160, 2011.
55. 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 3: RESEARCH0034.1-0034.11, 2002.
56. Veldkamp KE, VanKessel KPM, Verhoef J, VanStrijp JAG. Staphylococcal culture supernates stimulate human phagocytes. Inflammation 21: 541-551, 1997.
57. Vetillard J, Drouet M, Neildez-Nguyen TM, Mestries JC, Mathieu J, Thierry D, Herodin F. Interleukine-8 acts as a strong peripheral blood granulocyte-recruiting agent rather than as a hematopoietic progenitor cell-mobilizing factor. J Hematother Stem Cell Res 8: 365-379, 1999.
58. Weber A, Weber AT, McDonald TL, Larson MA. Staphylococcus aureus lipotechoic acid induces differential expression of bovine serum amyloid A3 (SAA3) by mammary epithelial cells: Implications for early diagnosis of mastitis. Vet Immunol Immunopathol 109: 79-83, 2006.
59. Wells SJ, Ott SL, Seitzinger AH. Key health issues for dairy cattle-new and old. J Dairy Sci 81: 3029-3035, 1998.
60. 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 (S. aureus) and E coli, but S. aureus fails to both activate NF-kappaB in mammary epithelial cells and to quickly induce TNFalpha and interleukin-8 (CXCL8) expression in the udder. Mol Immunol 45: 1385-1397, 2008.
61. Zoumpopoulou G, Tsakalidou E, Dewulf J, Pot B, Grangette C. Differential crosstalk between epithelial cells, dendritic cells and bacteria in a co-culture model. Intl J Food Microbiol 131: 40-51, 2009.