Transcriptomic analysis of the stress response to weaning at housing in bovine leukocytes using RNA-seq technology

BMC Genomics

Volumn 13, Issue 1, 2012, Pages

  O'Loughlin, Aran ^a,b   Lynn, David J ^a   McGee, Mark ^a   Doyle, Sean ^b   McCabe, Matthew ^a   Earley, Bernadette ^a  

^a ANIMAL AND GRASSLAND RESEARCH AND INNOVATION CENTRE   (Ireland)

^b NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CXCL2 CHEMOKINE; CXCL7 CHEMOKINE; EOTAXIN 2; EPITHELIAL DERIVED NEUTROPHIL ACTIVATING FACTOR 78; G PROTEIN COUPLED RECEPTOR; HAPTOGLOBIN; HYDROCORTISONE; INTERLEUKIN 8; MONOCYTE CHEMOTACTIC PROTEIN 1; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ALTERNATIVE RNA SPLICING; ANIMAL CELL; ARTICLE; CALF (BOVINE); CONTROLLED STUDY; EXON; GENE; GENE EXPRESSION; GPCR GENE; HOMEOSTASIS; HYDROCORTISONE BLOOD LEVEL; IMMUNE RESPONSE; INNATE IMMUNITY; LEUKOCYTE COUNT; LYMPHOCYTE; MALE; MEMBRANE TRANSPORT; NONHUMAN; NUCLEOTIDE SEQUENCE; RGS GENE; RNA ANALYSIS; RNA SEQUENCE; STRESS; THROMBOCYTE COUNT; UPREGULATION; WEANING;

ALTERNATIVE SPLICING; ANIMALS; BINDING SITES; BLOOD PLATELETS; BODY TEMPERATURE; CATTLE; COMPUTATIONAL BIOLOGY; CYTOKINES; EXONS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HAPTOGLOBINS; HOUSING, ANIMAL; HYDROCORTISONE; LEUKOCYTES; LYMPHOCYTES; MALE; NEUTROPHILS; RNA; SEQUENCE ANALYSIS, RNA; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS; TRANSCRIPTOME; WEANING;

BOVINAE;

EID: 84862249840     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-13-250     Document Type: Article

References (77)

1. Veissier I, Le Neindre P. Weaning in calves: its effects on social organization. Appl Anim Behav Sci 1989, 24(1):43-54.
2. Price EO, Harris JE, Borgwardt RE, Sween ML, Connor JM. Fenceline contact of beef calves with their dams at weaning reduces the negative effects of separation on behavior and growth rate. J Anim Sci 2003, 81(1):116-121.
3. Haley DB, Bailey DW, Stookey JM. The effects of weaning beef calves in two stages on their behavior and growth rate. J Anim Sci 2005, 83(9):2205-2214.
4. Enríquez DH, Ungerfeld R, Quintans G, Guidoni AL, Hötzel MJ. The effects of alternative weaning methods on behaviour in beef calves. Livest Sci 2010, 128(1-3):20-27.
5. Hickey MC, Drennan M, Earley B. The effect of abrupt weaning of suckler calves on the plasma concentrations of cortisol, catecholamines, leukocytes, acute-phase proteins and in vitro interferon-gamma production. J Anim Sci 2003, 81(11):2847-2855.
6. Blanco M, Casasús I, Palacio J. Effect of age at weaning on the physiological stress response and temperament of two beef cattle breeds. Animal 2009, 3(01):108-117. 10.1017/S1751731108002978, 22444177.
7. Arthington JD, Spears JW, Miller DC. The effect of early weaning on feedlot performance and measures of stress in beef calves. J Anim Sci 2005, 83(4):933-939.
8. Arthington JD, Qiu X, Cooke RF, Vendramini JMB, Araujo DB, Chase CC, Coleman SW. Effects of preshipping management on measures of stress and performance of beef steers during feedlot receiving. J Anim Sci 2008, 86(8):2016-2023. 10.2527/jas.2008-0968, 18407994.
9. Lynch EM, Earley B, McGee M, Doyle S. Effect of post-weaning management practices on physiological and immunological responses of weaned beef calves. Irish Journal of Agricultural and Food Research (In review) 2011, 50:161-174.
10. O'Loughlin A, McGee M, Waters S, Doyle S, Earley B. Examination of the bovine leukocyte environment using immunogenetic biomarkers to assess immunocompetence following exposure to weaning stress. BMC Vet Res 2011, 7(1):45. 10.1186/1746-6148-7-45, 3177877, 21834971.
11. Enriquez D, Hotzel M, Ungerfeld R. Minimising the stress of weaning of beef calves: a review. Acta Vet Scand 2011, 53(1):28. 10.1186/1751-0147-53-28, 3108315, 21569479.
12. Mackenzie AM, Drennan M, Rowan TG, Dixon JB, Carter SD. Effect of transportation and weaning on humoral immune responses of calves. Res Vet Sci 1997, 63(3):227-230. 10.1016/S0034-5288(97)90025-4, 9491448.
13. Ensminger M, Perry R. Beef Cattle Science 1997, 727. Interstate Publishers, Inc, Part B Danville, IL, Seventh Edition.
14. Carroll JA, Forsberg NE. Influence of Stress and Nutrition on Cattle Immunity. Veterinary ClinNorth Am: Food Animal Practice 2007, 23(1):105-149.
15. Carroll JA, Arthington JD, Chase CC. Early weaning alters the acute-phase reaction to an endotoxin challenge in beef calves. J Anim Sci 2009, 87(12):4167-4172. 10.2527/jas.2009-2016, 19717781.
16. Babcock AH, Renter DG, White BJ, Dubnicka SR, Scott HM. Temporal distributions of respiratory disease events within cohorts of feedlot cattle and associations with cattle health and performance indices. Preventive Veterinary Med 2010, 97(3-4):198-219.
17. Broom D. A History of Animal Welfare Science. Acta Biotheor 2011, 59(2):121-137. 10.1007/s10441-011-9123-3, 21347723.
18. Hubbard C, Scott K. Do farmers and scientists differ in their understanding and assessment of farm animal welfare?. Anim Welf 2011, 20:79-87.
19. Lynch EM, Earley B, McGee M, Doyle S. Effect of abrupt weaning at housing on leukocyte distribution, functional activity of neutrophils, and acute phase protein response of beef calves. BMC Vet Res 2010, 6(1):39. 10.1186/1746-6148-6-39, 2917424, 20649947.
20. Marioni JC, Mason CE, Mane SM, Stephens M, Gilad Y. RNA-seq: An assessment of technical reproducibility and comparison with gene expression arrays. Genome Res 2008, 18(9):1509-1517. 10.1101/gr.079558.108, 2527709, 18550803.
21. Huang W, Khatib H. Comparison of transcriptomic landscapes of bovine embryos using RNA-Seq. BMC Genomics 2010, 11(1):711. 10.1186/1471-2164-11-711, 3019235, 21167046.
22. Rinaldi M, Li RW, Capuco AV. Mastitis associated transcriptomic disruptions in cattle. Vet Immunol Immunopathol 2010, 138(4):267-279. 10.1016/j.vetimm.2010.10.005, 21040982.
23. Langmead B, Trapnell C, Pop M, Salzberg S. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009, 10(3):R25. 10.1186/gb-2009-10-3-r25, 2690996, 19261174.
24. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010, 26(1):139-140. 10.1093/bioinformatics/btp616, 2796818, 19910308.
25. Robinson M, Oshlack A. A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol 2010, 11(3):R25. 10.1186/gb-2010-11-3-r25, 2864565, 20196867.
26. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Royal Statistical Soc Series B (Methodol) 1995, 57(1):289-300.
27. Oshlack A, Wakefield M. Transcript length bias in RNA-seq data confounds systems biology. Biol Direct 2009, 4(1):14. 10.1186/1745-6150-4-14, 2678084, 19371405.
28. Gene ontology: tool for the unification of biology. Nat Genet 2000, 25(1):25-29. 10.1038/75556, 3037419, 10802651.
29. Young M, Wakefield M, Smyth G, Oshlack A. Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 2010, 11(2):R14. 10.1186/gb-2010-11-2-r14, 2872874, 20132535.
30. Lynn D, Winsor G, Chan C, Richard N, Laird M, Barsky A, Gardy J, Roche F, Chan T, Shah N, et al. InnateDB: facilitating systems-level analyses of the mammalian innate immune response. Mol Syst Biol 2008, 4:218. 2564732, 18766178.
31. Ho Sui SJ, Mortimer JR, Arenillas DJ, Brumm J, Walsh CJ, Kennedy BP, Wasserman WW. oPOSSUM: identification of over-represented transcription factor binding sites in co-expressed genes. Nucleic Acids Res 2005, 33(10):3154-3164. 10.1093/nar/gki624, 1142402, 15933209.
32. Sultan M, Schulz MH, Richard H, Magen A, Klingenhoff A, Scherf M, Seifert M, Borodina T, Soldatov A, Parkhomchuk D, et al. A Global View of Gene Activity and Alternative Splicing by Deep Sequencing of the Human Transcriptome. Science 2008, 321(5891):956-960. 10.1126/science.1160342, 18599741.
33. Klostermeier U, Barann M, Wittig M, Hasler R, Franke A, Gavrilova O, Kreck B, Sina C, Schilhabel M, Schreiber S, et al. A tissue-specific landscape of sense/antisense transcription in the mouse intestine. BMC Genomics 2011, 12(1):305. 10.1186/1471-2164-12-305, 3125268, 21663663.
34. Cole SW. Social regulation of leukocyte homeostasis: The role of glucocorticoid sensitivity. Brain Behav Immun 2008, 22(7):1049-1055. 10.1016/j.bbi.2008.02.006, 3004947, 18394861.
35. Chang L-C, Madsen SA, Toelboell T, Weber PSD, Burton JL. Effects of glucocorticoids on Fas gene expression in bovine blood neutrophils. J Endocrinol 2004, 183(3):569-583. 10.1677/joe.1.05822, 15590983.
36. Weber PSD, Madsen-Bouterse SA, Rosa GJM, Sipkovsky S, Ren X, Almeida PE, Kruska R, Halgren RG, Barrick JL, Burton JL. Analysis of the bovine neutrophil transcriptome during glucocorticoid treatment. Physiol Genomics 2006, 28(1):97-112. 10.1152/physiolgenomics.00094.2006, 16912069.
37. Paape MJ, Bannerman DD, Zhao X, Lee J-W. The bovine neutrophil: Structure and function in blood and milk. Vet Res 2003, 34(5):597-627.
38. Jones ML, Allison RW. Evaluation of the Ruminant Complete Blood Cell Count. Veterinary Clin North Am: Food Animal Practice 2007, 23(3):377-402.
39. Anderson BH, Watson DL, Colditz IG. The Effect of Dexamethasone on Some Immunological Parameters in Cattle. Vet Res Commun 1999, 23(7):399-413. 10.1023/A:1006365324335, 10598072.
40. Madsen-Bouterse SA, Rosa GJM, Burton JL. Glucocorticoid Modulation of Bcl-2 Family Members A1 and Bak during Delayed Spontaneous Apoptosis of Bovine Blood Neutrophils. Endocrinology 2006, 147(8):3826-3834. 10.1210/en.2006-0142, 16675521.
41. Buckham Sporer KR, Burton JL, Earley B, Crowe MA. Transportation stress in young bulls alters expression of neutrophil genes important for the regulation of apoptosis, tissue remodeling, margination, and anti-bacterial function. Veterinary Immunol Immunopathol 2007, 118(1-2):19-29.
42. Sapolsky RM, Romero LM, Munck AU. How Do Glucocorticoids Influence Stress Responses? Integrating Permissive, Suppressive, Stimulatory, and Preparative Actions. Endocr Rev 2000, 21(1):55-89. 10.1210/er.21.1.55, 10696570.
43. Droste SK, de Groote L, Atkinson HC, Lightman SL, Reul JMHM, Linthorst ACE. Corticosterone Levels in the Brain Show a Distinct Ultradian Rhythm but a Delayed Response to Forced Swim Stress. Endocrinology 2008, 149(7):3244-3253. 10.1210/en.2008-0103, 18356272.
44. Weber PSD, Toelboell T, Chang L-C, Tirrell JD, Saama PM, Smith GW, Burton JL. Mechanisms of glucocorticoid-induced down-regulation of neutrophil L-selectin in cattle: evidence for effects at the gene-expression level and primarily on blood neutrophils. J Leukoc Biol 2004, 75(5):815-827.
45. Burton JL, Madsen SA, Chang L-C, Weber PSD, Buckham KR, van Dorp R, Hickey M-C, Earley B. Gene expression signatures in neutrophils exposed to glucocorticoids: A new paradigm to help explain "neutrophil dysfunction" in parturient dairy cows. Vet Immunol Immunopathol 2005, 105(3-4):197-219.
46. Pang WY, Earley B, Sweeney T, Pirani S, Gath V, Crowe MA. Effects of banding or burdizzo castration of bulls on neutrophil phagocytosis and respiratory burst, CD62-L expression, and serum interleukin-8 concentration. J Anim Sci 2009, 87(10):3187-3195. 10.2527/jas.2009-1905, 19617515.
47. Diacovo TG, Catalina MD, Siegelman MH, Andrian U. Circulating Activated Platelets Reconstitute Lymphocyte Homing and Immunity in L-selectin-Deficient Mice. J Exp Med 1998, 187(2):197-204. 10.1084/jem.187.2.197, 2212105, 9432977.
48. He L, Vasiliou K, Nebert DW. Analysis and update of the human solute carrier (SLC) gene superfamily. Hum Genomics 2009, 3(2):195-206. 2752037, 19164095.
49. Elenkov IJ, Iezzoni DG, Daly A, Harris AG, Chrousos GP. Cytokine Dysregulation, Inflammation and Well-Being. Neuroimmunomodulation 2005, 12(5):255-269. 10.1159/000087104, 16166805.
50. Mantovani A, Bonecchi R, Locati M. Tuning inflammation and immunity by chemokine sequestration: decoys and more. Nat Rev Immunol 2006, 6(12):907-918. 10.1038/nri1964, 17124512.
51. Cardona AE, Li M, Liu L, Savarin C, Ransohoff RM. Chemokines in and out of the central nervous system: much more than chemotaxis and inflammation. J Leukoc Biol 2008, 84(3):587-594. 10.1189/jlb.1107763, 2516908, 18467654.
52. Cascieri MA, Springer MS. The chemokine/chemokine-receptor family: potential and progress for therapeutic intervention. Curr Opin Chem Biol 2000, 4(4):420-427. 10.1016/S1367-5931(00)00113-7, 10959770.
53. Hirao Y, Kanda T, Aso Y, Mitsuhashi M, Kobayashi I. Interleukin-8-An Early Marker for Bacterial Infection. Lab Medicine 2000, 31(1):39-44.
54. Craig A, Mai J, Cai S, Jeyaseelan S. Neutrophil Recruitment to the Lungs during Bacterial Pneumonia. Infect Immun 2009, 77(2):568-575. 10.1128/IAI.00832-08, 2632043, 19015252.
55. Henn V, Slupsky JR, Grafe M, Anagnostopoulos I, Forster R, Muller-Berghaus G, Kroczek RA. CD40 ligand on activated platelets triggers an inflammatory reaction of endothelial cells. Nature 1998, 391(6667):591-594. 10.1038/35393, 9468137.
56. Badolato R, Sozzani S, Lukacs NW, Schaller M. Lymphocyte trafficking and chemokine receptors during pulmonary disease. Lymphocyte Trafficking in Health and Disease 2006, 115-131. Birkhäuser, Basel, Switzerland, Parnham MJ, 3.
57. Rostene W, Kitabgi P, Parsadaniantz SM. Chemokines: a new class of neuromodulator?. Nat Rev Neurosci 2007, 8(11):895-903. 10.1038/nrn2255, 17948033.
58. Oo YH, Adams DH. The role of chemokines in the recruitment of lymphocytes to the liver. J Autoimmun 2010, 34(1):45-54. 10.1016/j.jaut.2009.07.011, 19744827.
59. Neubig RR, Siderovski DP. Regulators of G-Protein signalling as new central nervous system drug targets. Nat Rev Drug Discov 2002, 1(3):187-197. 10.1038/nrd747, 12120503.
60. Verhamme P, Hoylaerts M. Hemostasis and inflammation: two of a kind?. Thromb J 2009, 7(1):15. 10.1186/1477-9560-7-15, 2784434, 19922636.
61. von Hundelshausen P, Weber C. Platelets as Immune Cells: Bridging Inflammation and Cardiovascular Disease. Circ Res 2007, 100(1):27-40. 10.1161/01.RES.0000252802.25497.b7, 17204662.
62. Gleissner CA, von Hundelshausen P, Ley K. Platelet Chemokines in Vascular Disease. Arterioscler Thromb Vasc Biol 2008, 28(11):1920-1927. 10.1161/ATVBAHA.108.169417, 2657037, 18723831.
63. Smyth SS, McEver RP, Weyrich AS, Morrell CN, Hoffman MR, Arepally GM, French PA, Dauerman HL, Becker RC. For The Platelet Colloquium P: Platelet functions beyond hemostasis. J Thromb Haemost 2009, 7(11):1759-1766. 10.1111/j.1538-7836.2009.03586.x, 19691483.
64. Yeaman M. Platelets in defense against bacterial pathogens. Cellular Mol Life Sci 2010, 67(4):525-544.
65. Crowley DJ, Kanakaris NK, Giannoudis PV. Debridement and wound closure of open fractures: The impact of the time factor on infection rates. Injury 2007, 38(8):879-889. 10.1016/j.injury.2007.01.012, 17532320.
66. Oikarinen A, Haapasaari KM, Sutinen M, Tasanen K. The molecular basis of glucocorticoid-induced skin atrophy: topical glucocorticoid apparently decreases both collagen synthesis and the corresponding collagen mRNA level in human skin in vivo. Br J Dermatol 1998, 139(6):1106-1110. 10.1046/j.1365-2133.1998.02646.x, 9990383.
67. Cutroneo KR, Sterling KM. How do glucocorticoids compare to oligo decoys as inhibitors of collagen synthesis and potential toxicity of these therapeutics?. J Cell Biochem 2004, 92(1):6-15. 10.1002/jcb.20030, 15095399.
68. Kahan V, Andersen ML, Tomimori J, Tufik S. Stress, immunity and skin collagen integrity: Evidence from animal models and clinical conditions. Brain Behav Immun 2009, 23(8):1089-1095. 10.1016/j.bbi.2009.06.002, 19523511.
69. Barreiro O, De La Fuente H, Mittelbrunn M, Sánchez-Madrid F. Functional insights on the polarized redistribution of leukocyte integrins and their ligands during leukocyte migration and immune interactions. Immunol Rev 2007, 218(1):147-164. 10.1111/j.1600-065X.2007.00529.x, 17624951.
70. Volger OL, Fledderus JO, Kisters N, Fontijn RD, Moerland PD, Kuiper J, van Berkel TJ, Bijnens A-PJJ, Daemen MJAP, Pannekoek H, et al. Distinctive Expression of Chemokines and Transforming Growth Factor-β Signaling in Human Arterial Endothelium during Atherosclerosis. Am J Pathol 2007, 171(1):326-337. 10.2353/ajpath.2007.061196, 1941599, 17591977.
71. Kumpers P, Lukasz A, David S, Horn R, Hafer C, Faulhaber-Walter R, Fliser D, Haller H, Kielstein J. Excess circulating angiopoietin-2 is a strong predictor of mortality in critically ill medical patients. Crit Care 2008, 12(6):R147. 10.1186/cc7130, 2646310, 19025590.
72. Giuliano J, Wheeler D. Excess circulating angiopoietin-2 levels in sepsis: harbinger of death in the intensive care unit?. Crit Care 2009, 13(1):114. 10.1186/cc7685, 2688109, 19226440.
73. Brandt E, Petersen F, Ludwig A, Ehlert JE, Bock L, Flad HD. The beta-thromboglobulins and platelet factor 4: blood platelet-derived CXC chemokines with divergent roles in early neutrophil regulation. J Leukoc Biol 2000, 67(4):471-478.
74. Wågsäter D, Zhu C, Björck HM, Eriksson P. Effects of PDGF-C and PDGF-D on monocyte migration and MMP-2 and MMP-9 expression. Atherosclerosis 2009, 202(2):415-423. 10.1016/j.atherosclerosis.2008.04.050, 18573494.
75. Sorrells SF, Sapolsky RM. An inflammatory review of glucocorticoid actions in the CNS. Brain Behav Immun 2007, 21(3):259-272. 10.1016/j.bbi.2006.11.006, 1997278, 17194565.
76. Dhabhar FS. Enhancing versus Suppressive Effects of Stress on Immune Function: Implications for Immunoprotection versus Immunopathology. Allergy Asthma Clin Immunol 2008, 4(1):2-11. 10.1186/1710-1492-4-1-2, 2869337, 20525121.
77. Eruslanov EB, Lyadova IV, Kondratieva TK, Majorov KB, Scheglov IV, Orlova MO, Apt AS. Neutrophil Responses to Mycobacterium tuberculosis Infection in Genetically Susceptible and Resistant Mice. Infect Immun 2005, 73(3):1744-1753. 10.1128/IAI.73.3.1744-1753.2005, 1064912, 15731075.