Negative energy balance alters global gene expression and immune responses in the uterus of postpartum dairy cows

Physiological Genomics

Volumn 39, Issue 1, 2009, Pages 1-13

  Wathes, D Claire ^a   Cheng, Zhangrui ^a   Chowdhury, Waliul ^a   Fenwick, Mark A ^a,d   Fitzpatrick, Richard ^b,e   Morris, Dermot G ^b   Patton, Joe ^c   Murphy, John J ^c  

^a ROYAL VETERINARY COLLEGE   (United Kingdom)

^b Animal Production Research Centre   (Ireland)

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

^d HAMMERSMITH HOSPITAL   (United Kingdom)

^e Boston Scientific Galway   (Ireland)

Author keywords

Antimicrobial peptides; Bovine; Endometrium; Innate immune system; Microarray

Indexed keywords

3 HYDROXYBUTYRIC ACID; CALGRANULIN; CHEMOKINE; CYTOKINE; MATRIX METALLOPROTEINASE; RNA;

ANIMAL EXPERIMENT; ARTICLE; CONNECTIVE TISSUE DISEASE; CONTROL GROUP; CONTROLLED STUDY; DAIRY CATTLE; DISEASE SEVERITY; ENDOMETRITIS; ENDOMETRIUM; ENERGY BALANCE; FATTY ACID BLOOD LEVEL; FERTILITY; GENE CONTROL; GENE EXPRESSION; HEMATOLOGY; IMMUNE RESPONSE; INFLAMMATION; LACTATION; LEUKOCYTE COUNT; LYMPHOCYTE COUNT; MICROBIAL CONTAMINATION; MILK; NONHUMAN; PRIORITY JOURNAL; PUERPERIUM; SLAUGHTERHOUSE; UPREGULATION; UTERUS;

ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; CATTLE; DAIRYING; DINOPROST; ENDOMETRIUM; ENERGY METABOLISM; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; HORMONES; INSULIN-LIKE GROWTH FACTOR I; POLYMERASE CHAIN REACTION; POSTPARTUM PERIOD; SERUM AMYLOID A PROTEIN; UTERUS;

BOVINAE;

EID: 70349130410     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00064.2009     Document Type: Article

References (77)

1. Bauman DE, Currie WB. Partitioning of nutrients during pregnancy and lactation: a review of mechanisms involving homeostasis and homeorhesis. J Dairy Sci 63: 1514-1529, 1980.
2. Bell AW. Regulation of organic nutrient metabolism during transition from late pregnancy to early lactation. J Anim Sci 73: 2804-2819, 1995.
3. Bernabucci U, Ronchi B, Lacetera N, Nardone A. Influence of body condition score on relationships between metabolic status and oxidative stress in periparturient dairy cows. J Dairy Sci 88: 2017-2026, 2005. (Pubitemid 41431184)
4. Bondurant RH. Inflammation in the bovine female reproductive tract. J Anim Sci 77, Suppl 2: 101-110, 1999.
5. Borsberry S, Dobson H. Periparturient diseases and their effect on reproductive performance in five dairy herds. Vet Rec 124: 17-219, 1989.
6. Butler WR. Energy balance relationships with follicular development, ovulation and fertility in postpartum dairy cows. Livest Prod Sci 83: 211-221, 2003.
7. Cai TQ, Weston PG, Lund LA, Brodie B, McKenna DJ, Wagner WC. Association between neutrophil functions and periparturient disorders in cows. Am J Vet Res 55: 934-943, 1994.
8. Cole AM. Innate host defence of human vaginal and cervical mucosae. Curr Top Microbiol Immunol 306: 199-230, 2006.
9. Cole AM, Cole AL. Antimicrobial polypeptides are key anti-HIV-1 effector molecules of cervicovaginal host defense. Am J Reprod Immunol 59: 27-34, 2008.
10. Cormican P, Meade KG, Cahalane S, Narciandi F, Chapwanya A, Lloyd AT, O'Farrelly C. Evolution, expression and effectiveness in a cluster of novel bovine beta-defensins. Immunogenetics 60: 147-156, 2008.
11. Dejkhamron P, Thimmarayappa J, Kotlyarevska K, Sun J, Lu C, Bonkowski EL, Denson LA, Menon RK. Lipopolysaccharide (LPS) directly suppresses growth hormone receptor (GHR) expression through MyD88-dependent and -independent Toll-like receptor-4/MD2 complex signaling pathways. Mol Cell Endocrinol 274: 35-42, 2007. (Pubitemid 47126683)
12. Diamond G, Kaiser V, Rhodes J, Russell JP, Bevins CL. Transcriptional regulation of beta-defensin gene expression in tracheal epithelial cells. Infect Immun 68: 113-119, 2000. (Pubitemid 30016685)
13. Donofrio G, Herath S, Sartori C, Cavirani S, Flammini CF, Sheldon IM. Bovine herpesvirus 4 is tropic for bovine endometrial cells and modulates endocrine function. Reproduction 134: 183-197, 2007. (Pubitemid 47244850)
14. Drackley JK. Biology of dairy cows during the transition period: the final frontier? J Dairy Sci 82: 2259-2273, 1999.
15. Drobny EC, Abramson EC, Baumann G. Insulin receptors in acute infection: a study of factors conferring insulin resistance. J Clin Endocrinol Metab 58: 710-716, 1984. (Pubitemid 14137267)
16. Dunbar ME, Wysolmerski JJ. Parathyroid hormone-related protein: a developmental regulatory molecule necessary for mammary gland development. J Mammary Gland Biol Neoplasia 4: 21-23, 1999.
17. Fenwick MA, Fitzpatrick R, Kenny DA, Diskin MG, Patton J, Murphy JJ, Wathes DC. Interrelationships between negative EB (NEB) and IGF regulation in liver of lactating dairy cows. Domest Anim Endocrinol 34: 31-44, 2008. (Pubitemid 350087613)
18. Foldi J, Kulcsar M, Pecsi A, Huyghe B, de Sa C, Lohuis JA, Cox P, Huszenicza G. Bacterial complications of postpartum uterine involution in cattle. Anim Reprod Sci 96: 265-281, 2006. (Pubitemid 44584596)
19. Fourichon C, Seegers H, Malher X. Effects of disease on reproduction in the dairy cow. A meta-analysis. Theriogenology 53: 1729-1759, 1999.
20. Froy O, Hananel A, Chapnik N, Madar Z. Differential effect of insulin treatment on decreased levels of beta-defensins and Toll-like receptors in diabetic rats. Mol Immunol 44: 796-802, 2007. (Pubitemid 44415013)
21. Gier HT, Marion GB. Uterus of the cow after parturition: involutional changes. Am J Vet Res 29: 83-96, 1968.
22. Gilbert RO, Shin ST, Guard CL, Erb HN, Frajblat M. Prevalence of endometritis and its effects on reproductive performance of dairy cows. Theriogenology 64: 1879-1888, 2005.
23. Gray CA, Stewart D M, Johnson GA, Spencer TE. Postpartum uterine involution in sheep: histoarchitecture and changes in endometrial gene expression. Reproduction 125: 185-198, 2003.
24. Hammon DS, Evjen IM, Dhiman TR, Goff JP, Walters JL. Neutrophil function and energy status in Holstein cows with uterine health disorders. Vet Immunol Immunopathol 113: 21-29, 2006.
25. Harada A, Sekido N, Akahoshi T, Wada T, Mukaida N, Matsushima K. Essential involvement of interleukin-8 (IL-8) in acute inflammation. J Leukoc Biol 56: 559-564, 1994. (Pubitemid 24348812)
26. Hay JE. Liver disease in pregnancy. Hepatology 47: 1067-1076, 2008.
27. Hu X, Chavravarty SD, Ivashiv LB. Regulation of interferon and Toll-like receptor signaling during macrophage activation by opposing feedforward and feedback inhibition mechanisms. Immunologic Rev 226: 41-56, 2008.
28. Iles KE, Forman HJ. Macrophage signaling and respiratory burst. Immunologic Res 26: 95-105, 2002.
29. Jarrige J. INRAtion V2.7: Microsoft computer program of ration formulation for ruminant livestock. In: Logiciel de Rationnement des Ruminants, edited by Agabriel J, Champciaux P, Espinasse C. Dijon, France: CNERTA, 1989.
30. Kagnoff MF. Microbial-epithelial cell crosstalk during inflammation: the host response. Ann NY Acad Sci 1072: 313-320, 2006. (Pubitemid 44448464)
31. Kang KW, Lee SJ, Kim SG. Molecular mechanism of nrf2 activation by oxidative stress. Antioxid Redox Signal 7: 1164-1173, 2005.
32. Kehrli ME, Burton JL, Nonnecke BJ, Lee EK. Effects of stress on leukocyte trafficking and immune responses: implications for vaccination. Adv Vet Med 41: 61-81, 1999.
33. King AE, Critchley HO, Kelly RW. Innate immune defences in the human endometrium. Reprod Biol Endocrinol 1: 116, 2003.
34. Kirwan JP, Varastehpour A, Jing M, Presley L, Shao J, Friedman JE, Catalano PM. Reversal of insulin resistance postpartum is linked to enhanced skeletal muscle insulin signaling. J Clin Endocrinol Metab 89: 4678-4684, 2004. (Pubitemid 39244488)
35. Kü bler D, Gosenca D, Wind M, Heid H, Friedberg I, Jahnen-Dechent W, Lehmann WD. Proteolytic processing by matrix metalloproteinases and phosphorylation by protein kinase CK2 of fetuin-A, the major globulin of fetal calf serum. Biochimie 89: 410-418, 2007.
36. Lacetera N, Franci O, Scalia D, Bernabucci U, Ronchi B, Nardone A. Effects of nonesterified fatty acids and beta-hydroxybutyrate on functions of mononuclear cells obtained from ewes. Am J Vet Res 63: 414-418, 2002.
37. Lacetera N, Scalia D, Bernabucci U, Ronchi B, Pirazzi D, Nardone A. Lymphocyte functions in overconditioned cows around parturition. J Dairy Sci 88: 2010-2016, 2005. (Pubitemid 41431183)
38. Leite-Browning ML, McCawley LJ, Choi OH, Matrisian LM, Ochieng J. Interactions of alpha2-HS-glycoprotein (fetuin) with MMP-3 and murine squamous cell carcinoma cells. Int J Oncol 21: 965-971, 2002.
39. Leslie KE. The events of normal and abnormal postpartum endocrinology and uterine involution in dairy cows: a review. Can Vet J 24: 67-71, 1983.
40. Lewis GS. Uterine health and disorders. J Dairy Sci 80: 984-994, 1997.
41. Llewellyn S, Fitzpatrick R, Kenny DA, Patton J, Wathes DC. Endometrial expression of the insulin-like growth factor system during uterine involution in the postpartum dairy cow. Domest Anim Endocrinol 34: 391-402, 2008.
42. Loor JJ, Dann HM, Guretzky NA, Everts RE, Oliveira R, Green CA, Litherland NB, Rodriguez-Zas SL, Lewin HA, Drackley JK. Plane of nutrition prepartum alters hepatic gene expression and function in dairy cows as assessed by longitudinal transcript and metabolic profiling. Physiol Genomics 27: 29-41, 2005. (Pubitemid 44511823)
43. Mallard BA, Dekkers JC, Ireland MJ, Leslie KE, Sharif S, Vankampen CL, Wagter L, Wilkie BN. Alteration in immune responsiveness during the peripartum period and its ramification on dairy cow and calf health. J Dairy Sci 81: 585-595, 1998. (Pubitemid 128444859)
44. Maruyama S, Hirayama C, Yamamoto S, Koda M, Udagawa A, Kadowaki Y, Inoue M, Sagayama A, Umeki K. Red blood cell status in alcoholic and non-alcoholic liver disease. J Lab Clin Med 138: 332-337, 2001. (Pubitemid 33066155)
45. Mateus L, Lopes da Costa L, Bernardo F, Robalo Silva J. Influence of puerperal uterine infection on uterine involution and postpartum ovarian activity in dairy cows. Reprod Domest Anim 37: 31-35, 2002. (Pubitemid 34220183)
46. Mathews ST, Chellam N, Srinivas PR, Cintron VJ, Leon MA, Goustin AS, Grunberger G. Alpha2-HSG, a specific inhibitor of insulin receptor autophosphorylation, interacts with the insulin receptor. Mol Cell Endocrinol 164: 87-98, 2000. (Pubitemid 30665503)
47. McCarthy SD, Morris DG, Diskin MG, Kenny D, Patton J, Murphy JJ, Fenwick M, Wathes DC, Fitzpatrick R. Negative energy balance alters hepatic gene expression and key biological processes in dairy cows during the early post partum period. In: Proc Irish Agr Res Forum [http://www.agresearchforum.com/ publicationsarf/2007/page%20030.pdf].
48. Minuto F, Palermo C, Arvigo M, Barreca AM. The IGF system and bone. J Endocrinol Invest 28, Suppl: 8-10, 2005.
49. Mørk G, Schjerven H, Mangschau L, Søyland E, Brandtzaeg P. Proinflammatory cytokines upregulate expression of calprotectin (L1 protein, MRP-8/MRP-14) in cultured human keratinocytes. Br J Dermatol 149: 484-491, 2003. (Pubitemid 37287605)
50. Naschberger E, Werner T, Vicente AB, Guenzi E, Topolt K, Leubert R, Lubeseder-Martellato C, Nelson PJ, Sturzl M. Nuclear factor-κB motif and interferon-α stimulated response element co-operate in the activation of guanylate-binding protein-1 expression by inflammatory cytokines in endothelial cells. Biochem J 379: 409-420, 2004. (Pubitemid 38570114)
51. Opsomer G, Gröhn YT, Hertl J, Coryn M, Deluyker H, de Kruif A. Risk factors for post partum ovarian dysfunction in high producing dairy cows in Belgium: a field study. Theriogenology 53: 841-857, 2000. (Pubitemid 30151403)
52. Park SJ, Yoon WG, Song JS, Jung HS, Kim CJ, Oh SY, Yoon BH, Jung G, Kim HJ, Nirasawa T. Proteome analysis of human amnion and amniotic fluid by two-dimensional electrophoresis and matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Proteomics 6: 349-363, 2006. (Pubitemid 43142958)
53. Patton J, Kenny DA, Mee JF, O'Mara FP, Wathes DC, Cook M, Murphy JJ. Effect of milking frequency and diet on milk production, energy balance, and reproduction in dairy cows. J Dairy Sci 89: 1478-1487, 2006. (Pubitemid 44365836)
54. Rahimi F, Hsu K, Endoh Y, Geczy CL. FGF-2, IL-1beta and TGF-beta regulate fibroblast expression of S100A8. FEBS J 272: 2811-2827, 2005.
55. Ray S, Lukyanov P, Ochieng J. Members of the cystatin superfamily interact with MMP-9 and protect it from autolytic degradation without affecting its gelatinolytic activities. Biochim Biophys Acta 1652: 91-102, 2003. (Pubitemid 38224413)
56. Robinson RS, Pushpakumara PG, Cheng Z, Peters AR, Abayasekara DR, Wathes DC. Effects of dietary polyunsaturated fatty acids on ovarian and uterine function in lactating dairy cows. Reproduction 124: 119-131, 2002. (Pubitemid 34785373)
57. Roche JF. The effect of nutritional management of the dairy cow on reproductive efficiency. Anim Reprod Sci 96: 282-296, 2006.
58. Roosen S, Exner K, Paul S, Schröder JM, Kalm E, Looft C. Bovine beta-defensins: identification and characterization of novel bovine betadefensin genes and their expression in mammary gland tissue. Mamm Genome 15: 834-842, 2004. (Pubitemid 40012696)
59. Ross KF, Herzberg MC. Calprotectin expression by gingival epithelial cells. Infect Immun 69: 3248-3254, 2001. (Pubitemid 32332223)
60. Rowson LE, Lamming GE, Fry RM. Influence of ovarian hormones on uterine infection. Nature 171: 749-750, 1953.
61. Rü etschi U, Rosén A, Karlsson G, Zetterberg H, Rymo L, Hagberg H, Jacobsson B. Proteomic analysis using protein chips to detect biomarkers in cervical and amniotic fluid in women with intra-amniotic inflammation. J Proteome Res 4: 2236-2242, 2005.
62. Rutledge RG, Cote C. Mathematics of quantitative kinetic PCR and the application of standard curves. Nucleic Acids Res 31: e93, 2003.
63. Salamonsen LA, Zhang J, Brasted M. Leukocyte networks and human endometrial remodelling. J Reprod Immunol 57: 95-108, 2002. (Pubitemid 35245742)
64. Sheldon IM. The postpartum uterus. Vet Clin Food Anim 20: 569-591, 2004.
65. Sheldon IM, Dobson H. Postpartum uterine health in cattle. Anim Reprod Sci 82-83: 295-306, 2004.
66. Sheldon IM, Lewis GS, Leblanc S, Gilbert RO. Defining postpartum uterine disease in cattle. Theriogenology 65: 1516-1530, 2006.
67. Singh J, Murray RD, Mshelia G, Woldehiwet Z. The immune status of the bovine uterus during the peripartum period. Vet J 175: 301-309, 2008. (Pubitemid 351343652)
68. Sivan E, Chen X, Homko CJ, Reece EA, Boden G. Longitudinal study of carbohydrate metabolism in healthy obese pregnant women. Diabetes Care 20: 1470-1475, 1997. (Pubitemid 27366828)
69. Stefan N, Hennige AM, Staiger H, Machann J, Schick F, Krober SM, Machicao F, Fritsche A, Haring HU. Alpha2-Heremans-Schmid glycoprotein/ fetuin-A is associated with insulin resistance and fat accumulation in the liver in humans. Diabetes Care 29: 853-857, 2006. (Pubitemid 44115306)
70. Taylor VJ, Cheng Z, Pushpakumara PG, Beever DE, Wathes DC. Relationships between the plasma concentrations of insulin-like growth factor-I in dairy cows and their fertility and milk yield. Vet Rec 155: 583-588, 2004. (Pubitemid 39517552)
71. Urieli-Shoval S, Linke RP, Matzner Y. Expression and function of serum amyloid A, a major acute-phase protein, in normal and disease states. Curr Opin Hematol 7: 64-69, 2000. (Pubitemid 30007690)
72. Wang X, Jiang J, Warram J, Baumann G, Gan Y, Menon RK, Denson LA, Zinn KR, Frank SJ. Endotoxin-induced proteolytic reduction in hepatic growth hormone receptor: a novel mechanism for GH insensitivity. Mol Endocrinol 22: 1427-1437, 2008. (Pubitemid 351787002)
73. Wathes DC, Cheng Z, Bourne N, Taylor VJ, Coffey MP, Brotherstone S. Differences between primiparous and multiparous dairy cows in the inter-relationships between metabolic traits, milk yield and body condition score in the periparturient period. Domest Anim Endocrinol 33: 203-225, 2007. (Pubitemid 47018291)
74. White MF. Regulating insulin signaling and beta-cell function through IRS proteins. Can J Physiol Pharmacol 84: 725-737, 2006. (Pubitemid 44897893)
75. Young IR, Rice GE, Palliser HK, Ayhan M, Dellios NL, Hirst JJ. Identification of bactenecin-1 in cervicovaginal fluid by two-dimensional electrophoresis in an ovine model of preterm labour. Proteomics 7: 281-288, 2007. (Pubitemid 46184090)
76. Zasloff M. Antimicrobial peptides, innate immunity, and the normally sterile urinary tract. J Am Soc Nephrol 18: 2810-2816, 2007. (Pubitemid 350058386)
77. Zerbe H, Schneider N, Leibold W, Wensing T, Kruip TA, Schuberth HJ. Altered functional and immunophenotypical properties of neutrophilic granulocytes in postpartum cows associated with fatty liver. Theriogenology 54: 771-786, 2000. (Pubitemid 30848283)