FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / BMC Genomics / Deep sequencing of the uterine immune response to bacteria d...
BMC genomics2015; 16; 934; doi: 10.1186/s12864-015-2139-3

Deep sequencing of the uterine immune response to bacteria during the equine oestrous cycle.

Abstract: The steroid hormone environment in healthy horses seems to have a significant impact on the efficiency of their uterine immune response. The objective of this study was to characterize the changes in gene expression in the equine endometrium in response to the introduction of bacterial pathogens and the influence of steroid hormone concentrations on this expression. Methods: Endometrial biopsies were collected from five horses before and 3 h after the inoculation of Escherichia coli once in oestrus (follicle >35 mm in diameter) and once in dioestrus (5 days after ovulation) and analysed using high-throughput RNA sequencing techniques (RNA-Seq). Results: Comparison between time points revealed that 2422 genes were expressed at significantly higher levels and 2191 genes at significantly lower levels 3 h post inoculation in oestrus in comparison to pre-inoculation levels. In dioestrus, the expression of 1476 genes was up-regulated and 383 genes were down-regulated post inoculation. Many immune related genes were found to be up-regulated after the introduction of E. coli. These include pathogen recognition receptors, particularly toll-like receptors TLR2 and 4 and NOD-like receptor NLRC5. In addition, several interleukins including IL1B, IL6, IL8 and IL1ra were significantly up-regulated. Genes for chemokines, including CCL 2, CXCL 6, 9, 10, 11 and 16 and those for antimicrobial peptides, including secretory phospholipase sPLA 2, lipocalin 2, lysozyme and equine β-defensin 1, as well as the gene for tissue inhibitor for metalloproteinases TIMP-1 were also up-regulated post inoculation. Conclusions: The results of this study emphasize the complexity of an effective uterine immune response during acute endometritis and the tight balance between pro- and anti-inflammatory factors required for efficient elimination of bacteria. It is one of the first high-throughput analyses of the uterine inflammatory response in any species and several new potential targets for treatment of inflammatory diseases of the equine uterus have been identified.
Get Full Text
Publication Date: 2015-11-14 PubMed ID: 26572250PubMed Central: PMC4647707DOI: 10.1186/s12864-015-2139-3Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article
  • Research Support
  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research study focused on identifying the changes in gene expression in a horse’s uterus when exposed to bacterial pathogens, and how the presence of different concentrations of steroid hormones influences this gene expression.

Methodology

  • The research team conducted endometrial biopsies on five horses both pre and post-inoculation with Escherichia coli, also known as E. coli. This occurred once during oestrus (when the horse’s follicle was larger than 35mm in diameter) and once during dioestrus (which was five days after ovulation).
  • The researchers used high-throughput RNA sequencing techniques (RNA-Seq) to assess the gene expression changes that occurred following the introduction of bacterial pathogens.

Results

  • The study found that in oestrus, 2422 genes were expressed at significantly higher levels and 2191 genes at significantly lower levels 3 hours after the inoculation with E.coli, when compared to the pre-inoculation levels.
  • During dioestrus, 1476 genes showed increased expression post-inoculation, while the expression of 383 genes was down-regulated.
  • Several immune-related genes, including TLR2 and 4, NOD-like receptor NLRC5 and a variety of interleukins, became more active after exposure to E.coli.
  • Genes associated with chemokines and antimicrobial peptides, including secretory phospholipase sPLA 2, lipocalin 2, lysozyme and equine β-defensin 1, as well as the gene for the tissue inhibitor TIMP-1, were also more active post inoculation.

Conclusions

  • The findings highlight the complexity of the uterine immune response in the face of acute endometritis and the delicate balance required between pro- and anti-inflammatory factors for efficient bacterial elimination.
  • This study is pioneering in its high-throughput examination of the uterine inflammatory response across species, and it has helped identify new potential targets in the treatment of inflammatory diseases of the equine uterus.

Cite This Article

APA
Marth CD, Young ND, Glenton LY, Noden DM, Browning GF, Krekeler N. (2015). Deep sequencing of the uterine immune response to bacteria during the equine oestrous cycle. BMC Genomics, 16, 934. https://doi.org/10.1186/s12864-015-2139-3

Publication

BMC genomics
ISSN: 1471-2164
NlmUniqueID: 100965258
Country: England
Language: English
Volume: 16
Pages: 934
PII: 934

Researcher Affiliations

Marth, Christina D
  • Asia-Pacific Centre for Animal Health, Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, 250 Princes Highway, Werribee, VIC, 3030, Australia. christina.marth@unimelb.edu.au.
Young, Neil D
  • Asia-Pacific Centre for Animal Health, Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, 250 Princes Highway, Werribee, VIC, 3030, Australia. nyoung@unimelb.edu.au.
Glenton, Lisa Y
  • Asia-Pacific Centre for Animal Health, Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, 250 Princes Highway, Werribee, VIC, 3030, Australia. l.glenton@student.unimelb.edu.au.
Noden, Drew M
  • Department of Biomedical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY, 14853-6401, USA. drewnoden@gmail.com.
Browning, Glenn F
  • Asia-Pacific Centre for Animal Health, Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, 250 Princes Highway, Werribee, VIC, 3030, Australia. glenfb@unimelb.edu.au.
Krekeler, Natali
  • Asia-Pacific Centre for Animal Health, Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, 250 Princes Highway, Werribee, VIC, 3030, Australia. krekeler@unimelb.edu.au.

MeSH Terms

  • Animals
  • Antimicrobial Cationic Peptides / genetics
  • Antimicrobial Cationic Peptides / metabolism
  • Chemokines / genetics
  • Chemokines / metabolism
  • Cytokines / genetics
  • Cytokines / metabolism
  • Endometritis / immunology
  • Endometritis / microbiology
  • Endometritis / veterinary
  • Endometrium / immunology
  • Endometrium / metabolism
  • Escherichia coli Infections / immunology
  • Escherichia coli Infections / veterinary
  • Estrous Cycle / genetics
  • Female
  • Gene Expression
  • Gonadal Steroid Hormones
  • High-Throughput Nucleotide Sequencing
  • Horse Diseases / genetics
  • Horse Diseases / immunology
  • Horse Diseases / microbiology
  • Horses
  • Matrix Metalloproteinases / genetics
  • Matrix Metalloproteinases / metabolism

References

This article includes 103 references
  1. Traub-Dargatz JL, Salman MD, Voss JL. Medical problems of adult horses, as ranked by equine practitioners.. J Am Vet Med Assoc 1991 May 15;198(10):1745-7.
    pubmed: 2071472
  2. Zent WW, Troedsson MHT, Xue J-L. Postbreeding Uterine Fluid Accumulation in a Normal Population of Thoroughbred Mares: A Field Study. Proceedings of the Annual Convention of the American Association of Equine Practitioners 1998; p. 64.
  3. Riddle WT, LeBlanc MM, Stromberg AJ. Relationships between uterine culture, cytology and pregnancy rates in a Thoroughbred practice.. Theriogenology 2007 Aug;68(3):395-402.
    pubmed: 17583785doi: 10.1016/j.theriogenology.2007.05.050google scholar: lookup
  4. Troedsson MH, Loset K, Alghamdi AM, Dahms B, Crabo BG. Interaction between equine semen and the endometrium: the inflammatory response to semen.. Anim Reprod Sci 2001 Dec 3;68(3-4):273-8.
    pubmed: 11744271doi: 10.1016/s0378-4320(01)00164-6google scholar: lookup
  5. Watson ED. Post-breeding endometritis in the mare.. Anim Reprod Sci 2000 Jul 2;60-61:221-32.
    pubmed: 10844197doi: 10.1016/s0378-4320(00)00110-xgoogle scholar: lookup
  6. England GC, Burgess CM, Freeman SL. Perturbed sperm-epithelial interaction in bitches with mating-induced endometritis.. Vet J 2012 Dec;194(3):314-8.
    pubmed: 22721627doi: 10.1016/j.tvjl.2012.04.031google scholar: lookup
  7. Troedsson MHT. Therapeutic considerations for mating-induced endometritis. Pferdeheilkunde 1997;13(5):516–20.
  8. Troedsson MH, Liu IK. Uterine clearance of non-antigenic markers (51Cr) in response to a bacterial challenge in mares potentially susceptible and resistant to chronic uterine infections.. J Reprod Fertil Suppl 1991;44:283-8.
    pubmed: 1795272
  9. Collins S. A study of the incidence of cervical and uterine infection in Thoroughbred mares in Ireland. Vet Rec 1964;66:673–6.
  10. Bain AM. The rôle of infection in infertility in the thoroughbred mare.. Vet Rec 1966 Jan 29;78(5):168-73.
    pubmed: 5948366doi: 10.1136/vr.78.5.168google scholar: lookup
  11. Albihn A, Båverud V, Magnusson U. Uterine microbiology and antimicrobial susceptibility in isolated bacteria from mares with fertility problems.. Acta Vet Scand 2003;44(3-4):121-9.
    pmc: PMC1831563pubmed: 15074625doi: 10.1186/1751-0147-44-121google scholar: lookup
  12. Gilbert RO, Shin ST, Guard CL, Erb HN, Frajblat M. Prevalence of endometritis and its effects on reproductive performance of dairy cows.. Theriogenology 2005 Dec;64(9):1879-88.
    pubmed: 15961149doi: 10.1016/j.theriogenology.2005.04.022google scholar: lookup
  13. Waller CM, Bilkei G, Cameron RD. Effect of periparturient diseases accompanied by excessive vulval discharge and weaning to mating interval on sow reproductive performance.. Aust Vet J 2002 Sep;80(9):545-9.
    pubmed: 12398316doi: 10.1111/j.1751-0813.2002.tb11033.xgoogle scholar: lookup
  14. Fontaine E, Levy X, Grellet A, Luc A, Bernex F, Boulouis HJ, Fontbonne A. Diagnosis of endometritis in the bitch: a new approach.. Reprod Domest Anim 2009 Jul;44 Suppl 2:196-9.
    pubmed: 19754567doi: 10.1111/j.1439-0531.2009.01376.xgoogle scholar: lookup
  15. Mir F, Fontaine E, Albaric O, Greer M, Vannier F, Schlafer DH, Fontbonne A. Findings in uterine biopsies obtained by laparotomy from bitches with unexplained infertility or pregnancy loss: an observational study.. Theriogenology 2013 Jan 15;79(2):312-22.
    pubmed: 23178080doi: 10.1016/j.theriogenology.2012.09.005google scholar: lookup
  16. Newton ER, Prihoda TJ, Gibbs RS. A clinical and microbiologic analysis of risk factors for puerperal endometritis.. Obstet Gynecol 1990 Mar;75(3 Pt 1):402-6.
    pubmed: 2406660
  17. Senger PL. Spermatozoa in the Female Tract - Transport, Capacitation and Fertilization. In: Senger PL, editor. Pathways to Pregnancy and Parturition 3ed. Redmond, OR: Current Conceptions; 2012. pp. 266–83.
  18. Evans MJ, Hamer JM, Gason LM, Graham CS, Asbury AC, Irvine CH. Clearance of bacteria and non-antigenic markers following intra-uterine inoculation into maiden mares: Effect of steroid hormone environment.. Theriogenology 1986 Jul;26(1):37-50.
    pubmed: 16726168doi: 10.1016/0093-691x(86)90110-xgoogle scholar: lookup
  19. Ramadan AA, Johnson GL 3rd, Lewis GS. Regulation of uterine immune function during the estrous cycle and in response to infectious bacteria in sheep.. J Anim Sci 1997 Jun;75(6):1621-32.
    pubmed: 9250526doi: 10.2527/1997.7561621xgoogle scholar: lookup
  20. de Winter PJJ, Verdonck M, de Kruif A, Devriese LA, Haesebrouck F. Endometritis and vaginal discharge in the sow. Anim Reprod Sci 1992;28(1–4):51–8.
  21. Nishikawa Y, Baba T, Imori T. Effect of the estrous cycle on uterine infection induced by Escherichia coli.. Infect Immun 1984 Feb;43(2):678-83.
    pmc: PMC264353pubmed: 6363298doi: 10.1128/iai.43.2.678-683.1984google scholar: lookup
  22. Arora N, Sandford J, Browning GF, Sandy JR, Wright PJ. A model for cystic endometrial hyperplasia/pyometra complex in the bitch.. Theriogenology 2006 Oct;66(6-7):1530-6.
    pubmed: 16620926doi: 10.1016/j.theriogenology.2006.02.019google scholar: lookup
  23. Tsumagari S, Ishinazaka T, Kamata H, Ohba S, Tanaka S, Ishii M, Memon MA. Induction of canine pyometra by inoculation of Escherichia coli into the uterus and its relationship to reproductive features.. Anim Reprod Sci 2005 Jul;87(3-4):301-8.
    pubmed: 15911179doi: 10.1016/j.anireprosci.2004.11.006google scholar: lookup
  24. Christoffersen M, Woodward E, Bojesen AM, Jacobsen S, Petersen MR, Troedsson MH, Lehn-Jensen H. Inflammatory responses to induced infectious endometritis in mares resistant or susceptible to persistent endometritis.. BMC Vet Res 2012 Mar 29;8:41.
    pmc: PMC3368729pubmed: 22458733doi: 10.1186/1746-6148-8-41google scholar: lookup
  25. Nash DM, Sheldon IM, Herath S, Lane EA. Markers of the uterine innate immune response of the mare.. Anim Reprod Sci 2010 May;119(1-2):31-9.
    pubmed: 20022187doi: 10.1016/j.anireprosci.2009.11.008google scholar: lookup
  26. Christoffersen M, Woodward EM, Bojesen AM, Petersen MR, Squires EL, Lehn-Jensen H, Troedsson MH. Effect of immunomodulatory therapy on the endometrial inflammatory response to induced infectious endometritis in susceptible mares.. Theriogenology 2012 Sep 15;78(5):991-1004.
    pubmed: 22819284doi: 10.1016/j.theriogenology.2012.04.016google scholar: lookup
  27. An H, Yu Y, Zhang M, Xu H, Qi R, Yan X, Liu S, Wang W, Guo Z, Guo J, Qin Z, Cao X. Involvement of ERK, p38 and NF-kappaB signal transduction in regulation of TLR2, TLR4 and TLR9 gene expression induced by lipopolysaccharide in mouse dendritic cells.. Immunology 2002 May;106(1):38-45.
    pmc: PMC1782697pubmed: 11972630doi: 10.1046/j.1365-2567.2002.01401.xgoogle scholar: lookup
  28. Chen C, Zibiao H, Ming Z, Shiyi C, Ruixia L, Jie W, SongJia L. Expression pattern of Toll-like receptors (TLRs) in different organs and effects of lipopolysaccharide on the expression of TLR 2 and 4 in reproductive organs of female rabbit.. Dev Comp Immunol 2014 Oct;46(2):341-8.
    pubmed: 24858029doi: 10.1016/j.dci.2014.05.008google scholar: lookup
  29. Silva E, Leitão S, Henriques S, Kowalewski MP, Hoffmann B, Ferreira-Dias G, da Costa LL, Mateus L. Gene transcription of TLR2, TLR4, LPS ligands and prostaglandin synthesis enzymes are up-regulated in canine uteri with cystic endometrial hyperplasia-pyometra complex.. J Reprod Immunol 2010 Jan;84(1):66-74.
    pubmed: 19945173doi: 10.1016/j.jri.2009.10.004google scholar: lookup
  30. Swangchan-Uthai T, Lavender CR, Cheng Z, Fouladi-Nashta AA, Wathes DC. Time course of defense mechanisms in bovine endometrium in response to lipopolysaccharide.. Biol Reprod 2012 Jun;87(6):135.
    pubmed: 23077171doi: 10.1095/biolreprod.112.102376google scholar: lookup
  31. Mariathasan S, Weiss DS, Newton K, McBride J, O'Rourke K, Roose-Girma M, Lee WP, Weinrauch Y, Monack DM, Dixit VM. Cryopyrin activates the inflammasome in response to toxins and ATP.. Nature 2006 Mar 9;440(7081):228-32.
    pubmed: 16407890doi: 10.1038/nature04515google scholar: lookup
  32. Barbé F, Douglas T, Saleh M. Advances in Nod-like receptors (NLR) biology.. Cytokine Growth Factor Rev 2014 Dec;25(6):681-97.
    pubmed: 25070125doi: 10.1016/j.cytogfr.2014.07.001google scholar: lookup
  33. Schroder K, Tschopp J. The inflammasomes.. Cell 2010 Mar 19;140(6):821-32.
    pubmed: 20303873doi: 10.1016/j.cell.2010.01.040google scholar: lookup
  34. Benko S, Magalhaes JG, Philpott DJ, Girardin SE. NLRC5 limits the activation of inflammatory pathways.. J Immunol 2010 Aug 1;185(3):1681-91.
    pubmed: 20610642doi: 10.4049/jimmunol.0903900google scholar: lookup
  35. Cui J, Zhu L, Xia X, Wang HY, Legras X, Hong J, Ji J, Shen P, Zheng S, Chen ZJ, Wang RF. NLRC5 negatively regulates the NF-kappaB and type I interferon signaling pathways.. Cell 2010 Apr 30;141(3):483-96.
    pmc: PMC3150216pubmed: 20434986doi: 10.1016/j.cell.2010.03.040google scholar: lookup
  36. Christoffersen M, Baagoe CD, Jacobsen S, Bojesen AM, Petersen MR, Lehn-Jensen H. Evaluation of the systemic acute phase response and endometrial gene expression of serum amyloid A and pro- and anti-inflammatory cytokines in mares with experimentally induced endometritis.. Vet Immunol Immunopathol 2010 Nov 15;138(1-2):95-105.
    pubmed: 20728224doi: 10.1016/j.vetimm.2010.07.011google scholar: lookup
  37. Ghasemi F, Gonzalez-Cano P, Griebel PJ, Palmer C. Proinflammatory cytokine gene expression in endometrial cytobrush samples harvested from cows with and without subclinical endometritis.. Theriogenology 2012 Oct 15;78(7):1538-47.
    pubmed: 22925636doi: 10.1016/j.theriogenology.2012.06.022google scholar: lookup
  38. Di Pietro C, Cicinelli E, Guglielmino MR, Ragusa M, Farina M, Palumbo MA, Cianci A. Altered transcriptional regulation of cytokines, growth factors, and apoptotic proteins in the endometrium of infertile women with chronic endometritis.. Am J Reprod Immunol 2013 May;69(5):509-17.
    pubmed: 23351011doi: 10.1111/aji.12076google scholar: lookup
  39. Nevalainen TJ, Graham GG, Scott KF. Antibacterial actions of secreted phospholipases A2. Review.. Biochim Biophys Acta 2008 Jan-Feb;1781(1-2):1-9.
    pubmed: 18177747doi: 10.1016/j.bbalip.2007.12.001google scholar: lookup
  40. Linde A, Ross CR, Davis EG, Dib L, Blecha F, Melgarejo T. Innate immunity and host defense peptides in veterinary medicine.. J Vet Intern Med 2008 Mar-Apr;22(2):247-65.
    pubmed: 18312280doi: 10.1111/j.1939-1676.2007.0038.xgoogle scholar: lookup
  41. Tomee JF, Koëter GH, Hiemstra PS, Kauffman HF. Secretory leukoprotease inhibitor: a native antimicrobial protein presenting a new therapeutic option?. Thorax 1998 Feb;53(2):114-6.
    pmc: PMC1758711pubmed: 9624296doi: 10.1136/thx.53.2.114google scholar: lookup
  42. Couto MA, Harwig SS, Cullor JS, Hughes JP, Lehrer RI. eNAP-2, a novel cysteine-rich bactericidal peptide from equine leukocytes.. Infect Immun 1992 Dec;60(12):5042-7.
    pmc: PMC258275pubmed: 1452336doi: 10.1128/iai.60.12.5042-5047.1992google scholar: lookup
  43. Couto MA, Harwig SS, Lehrer RI. Selective inhibition of microbial serine proteases by eNAP-2, an antimicrobial peptide from equine neutrophils.. Infect Immun 1993 Jul;61(7):2991-4.
    pmc: PMC280950pubmed: 8514405doi: 10.1128/iai.61.7.2991-2994.1993google scholar: lookup
  44. Flo TH, Smith KD, Sato S, Rodriguez DJ, Holmes MA, Strong RK, Akira S, Aderem A. Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron.. Nature 2004 Dec 16;432(7019):917-21.
    pubmed: 15531878doi: 10.1038/nature03104google scholar: lookup
  45. Farnaud S, Evans RW. Lactoferrin--a multifunctional protein with antimicrobial properties.. Mol Immunol 2003 Nov;40(7):395-405.
    pubmed: 14568385doi: 10.1016/s0161-5890(03)00152-4google scholar: lookup
  46. Roberts RM, Raub TJ, Bazer FW. Role of uteroferrin in transplacental iron transport in the pig.. Fed Proc 1986 Sep;45(10):2513-8.
    pubmed: 3527760
  47. Wooding FB, Morgan G, Fowden AL, Allen WR. Separate sites and mechanisms for placental transport of calcium, iron and glucose in the equine placenta.. Placenta 2000 Sep;21(7):635-45.
    pubmed: 10985966doi: 10.1053/plac.2000.0550google scholar: lookup
  48. Khokha R, Murthy A, Weiss A. Metalloproteinases and their natural inhibitors in inflammation and immunity.. Nat Rev Immunol 2013 Sep;13(9):649-65.
    pubmed: 23969736doi: 10.1038/nri3499google scholar: lookup
  49. Parks WC, Wilson CL, López-Boado YS. Matrix metalloproteinases as modulators of inflammation and innate immunity.. Nat Rev Immunol 2004 Aug;4(8):617-29.
    pubmed: 15286728doi: 10.1038/nri1418google scholar: lookup
  50. Szabo KA, Ablin RJ, Singh G. Matrix metalloproteinases and the immune response. Clin Appl Immunol Rev 2004;4(5):295–319.
  51. Oddsdottir C, Riley SC, Leask R, Edwards DR, Watson ED. Activities of matrix metalloproteinases-9 and-2 in uterine fluid during induced equine endometritis. Pferdeheilkunde 2008;24(1):70–3.
  52. Hagman R, Rönnberg E, Pejler G. Canine uterine bacterial infection induces upregulation of proteolysis-related genes and downregulation of homeobox and zinc finger factors.. PLoS One 2009 Nov 26;4(11):e8039.
    pmc: PMC2777310pubmed: 19956711doi: 10.1371/journal.pone.0008039google scholar: lookup
  53. Marth CD, Young ND, Glenton LY, Noden DM, Browning GF, Krekeler N. Effect of ovarian hormones on the healthy equine uterus: a global gene expression analysis.. Reprod Fertil Dev 2015 May 20;.
    doi: 10.1071/RD14513pubmed: 25989818google scholar: lookup
  54. Tan YF, Li FX, Piao YS, Sun XY, Wang YL. Global gene profiling analysis of mouse uterus during the oestrous cycle.. Reproduction 2003 Aug;126(2):171-82.
    pubmed: 12887274doi: 10.1530/rep.0.1260171google scholar: lookup
  55. Mitko K, Ulbrich SE, Wenigerkind H, Sinowatz F, Blum H, Wolf E, Bauersachs S. Dynamic changes in messenger RNA profiles of bovine endometrium during the oestrous cycle.. Reproduction 2008 Feb;135(2):225-40.
    pubmed: 18239051doi: 10.1530/rep-07-0415google scholar: lookup
  56. Talbi S, Hamilton AE, Vo KC, Tulac S, Overgaard MT, Dosiou C, Le Shay N, Nezhat CN, Kempson R, Lessey BA, Nayak NR, Giudice LC. Molecular phenotyping of human endometrium distinguishes menstrual cycle phases and underlying biological processes in normo-ovulatory women.. Endocrinology 2006 Mar;147(3):1097-121.
    pubmed: 16306079doi: 10.1210/en.2005-1076google scholar: lookup
  57. Bauersachs S, Ulbrich SE, Gross K, Schmidt SE, Meyer HH, Einspanier R, Wenigerkind H, Vermehren M, Blum H, Sinowatz F, Wolf E. Gene expression profiling of bovine endometrium during the oestrous cycle: detection of molecular pathways involved in functional changes.. J Mol Endocrinol 2005 Jun;34(3):889-908.
    pubmed: 15956356doi: 10.1677/jme.1.01799google scholar: lookup
  58. Borthwick JM, Charnock-Jones DS, Tom BD, Hull ML, Teirney R, Phillips SC, Smith SK. Determination of the transcript profile of human endometrium.. Mol Hum Reprod 2003 Jan;9(1):19-33.
    pubmed: 12529417doi: 10.1093/molehr/gag004google scholar: lookup
  59. Kotilainen T, Huhtinen M, Katila T. Sperm-induced leukocytosis in the equine uterus.. Theriogenology 1994 Feb 2;41(3):629-36.
    pubmed: 16727418doi: 10.1016/0093-691x(94)90173-ggoogle scholar: lookup
  60. McKinnon AO, McCue PM. Uterine Abnormalities. In: McKinnon AO, Squires EL, Vaala WE, Dickson VD, editors. Equine Reproduction. 2. Oxford: Wiley-Blackwell; 2011. pp. 2137–61.
  61. McCue PM, Scoggin CF, Lindholm AR. Estrus. In: McKinnon AO, Squires EL, Vaala WE, Dickson VD, editors. Equine Reproduction. 2. Oxford: Wiley-Blackwell; 2011. pp. 1716–27.
  62. Samper JC, Pycock JF. The Normal Uterus in Estrus. In: Samper JC, Pycock JF, McKinnon AO, editors. Current Therapy in Equine Reproduction. St. Louis, Missouri, US: Saunders Elsevier; 2007. pp. 32–5.
  63. Lohse M, Bolger AM, Nagel A, Fernie AR, Lunn JE, Stitt M, Usadel B. RobiNA: a user-friendly, integrated software solution for RNA-Seq-based transcriptomics.. Nucleic Acids Res 2012 Jul;40(Web Server issue):W622-7.
    pmc: PMC3394330pubmed: 22684630doi: 10.1093/nar/gks540google scholar: lookup
  64. Kinsella RJ, Kähäri A, Haider S, Zamora J, Proctor G, Spudich G, Almeida-King J, Staines D, Derwent P, Kerhornou A, Kersey P, Flicek P. Ensembl BioMarts: a hub for data retrieval across taxonomic space.. Database (Oxford) 2011;2011:bar030.
    pmc: PMC3170168pubmed: 21785142doi: 10.1093/database/bar030google scholar: lookup
  65. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2.. Nat Methods 2012 Mar 4;9(4):357-9.
    pmc: PMC3322381pubmed: 22388286doi: 10.1038/nmeth.1923google scholar: lookup
  66. Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome.. BMC Bioinformatics 2011 Aug 4;12:323.
    pmc: PMC3163565pubmed: 21816040doi: 10.1186/1471-2105-12-323google scholar: lookup
  67. Robinson MD, Oshlack A. A scaling normalization method for differential expression analysis of RNA-seq data.. Genome Biol 2010;11(3):R25.
    pmc: PMC2864565pubmed: 20196867doi: 10.1186/gb-2010-11-3-r25google scholar: lookup
  68. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc Ser B (Stat Method) 1995;57:289–300.
  69. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data.. Bioinformatics 2010 Jan 1;26(1):139-40.
    pmc: PMC2796818pubmed: 19910308doi: 10.1093/bioinformatics/btp616google scholar: lookup
  70. Young MD, Wakefield MJ, Smyth GK, Oshlack A. Gene ontology analysis for RNA-seq: accounting for selection bias.. Genome Biol 2010;11(2):R14.
    pmc: PMC2872874pubmed: 20132535doi: 10.1186/gb-2010-11-2-r14google scholar: lookup
  71. Carlson M, Falcon S, Pages H, Li N. GO.db: A set of annotation maps describing the entire Gene Ontology. bioconductor.org 2.8.0. Japan: The Institue of Statistical Mathematics; 2007.
  72. Kanehisa M, Goto S. KEGG: kyoto encyclopedia of genes and genomes.. Nucleic Acids Res 2000 Jan 1;28(1):27-30.
    pmc: PMC102409pubmed: 10592173doi: 10.1093/nar/28.1.27google scholar: lookup
  73. Marth CD, Young ND, Glenton LY, Noden DM, Browning GF, Krekeler N. Effect of ovarian hormones on the healthy equine uterus: a global gene expression analysis.. Reprod Fertil Dev 2015 May 20;.
    pubmed: 25989818doi: 10.1071/rd14513google scholar: lookup
  74. Vels L, Røntved CM, Bjerring M, Ingvartsen KL. Cytokine and acute phase protein gene expression in repeated liver biopsies of dairy cows with a lipopolysaccharide-induced mastitis.. J Dairy Sci 2009 Mar;92(3):922-34.
    pubmed: 19233785doi: 10.3168/jds.2008-1209google scholar: lookup
  75. Tizard IR. Innate Immunity: The Recognition of Invaders. In: Tizard IR, editor. Veterinary Immunology : an Introduction. 8. Philadelphia, PA: Saunders; 2008. pp. 11–20.
  76. Hoshino K, Takeuchi O, Kawai T, Sanjo H, Ogawa T, Takeda Y, Takeda K, Akira S. Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product.. J Immunol 1999 Apr 1;162(7):3749-52.
    pubmed: 10201887
  77. Chow JC, Young DW, Golenbock DT, Christ WJ, Gusovsky F. Toll-like receptor-4 mediates lipopolysaccharide-induced signal transduction.. J Biol Chem 1999 Apr 16;274(16):10689-92.
    pubmed: 10196138doi: 10.1074/jbc.274.16.10689google scholar: lookup
  78. Shao CY, Wang H, Meng X, Zhu JQ, Wu YQ, Li JJ. Characterization of the innate immune response in goats after intrauterine infusion of E. coli using histopathological, cytologic and molecular analyses.. Theriogenology 2012 Aug;78(3):593-604.
    pubmed: 22541320doi: 10.1016/j.theriogenology.2012.03.005google scholar: lookup
  79. Eaton SR T, Card C. Toll-like receptor-2 and −4 in the equine endometrium during physiologic post-breeding endometritis. Anim Reprod Sci 2010;121(1/2):96–7.
  80. Woodward EM, Christoffersen M, Campos J, Betancourt A, Horohov D, Scoggin KE, Squires EL, Troedsson MH. Endometrial inflammatory markers of the early immune response in mares susceptible or resistant to persistent breeding-induced endometritis.. Reproduction 2013 Mar 1;145(3):289-96.
    pubmed: 23580950doi: 10.1530/rep-12-0452google scholar: lookup
  81. Arend WP, Welgus HG, Thompson RC, Eisenberg SP. Biological properties of recombinant human monocyte-derived interleukin 1 receptor antagonist.. J Clin Invest 1990 May;85(5):1694-7.
    pmc: PMC296623pubmed: 2139669doi: 10.1172/jci114622google scholar: lookup
  82. Hannan NJ, Salamonsen LA. Role of chemokines in the endometrium and in embryo implantation.. Curr Opin Obstet Gynecol 2007 Jun;19(3):266-72.
    pubmed: 17495644doi: 10.1097/gco.0b013e328133885fgoogle scholar: lookup
  83. Gangur V, Birmingham NP, Thanesvorakul S. Chemokines in health and disease.. Vet Immunol Immunopathol 2002 Jul;86(3-4):127-36.
    pubmed: 12007879doi: 10.1016/s0165-2427(02)00018-1google scholar: lookup
  84. Colditz IG, Zwahlen RD, Baggiolini M. Neutrophil accumulation and plasma leakage induced in vivo by neutrophil-activating peptide-1.. J Leukoc Biol 1990 Aug;48(2):129-37.
    pubmed: 2196320doi: 10.1002/jlb.48.2.129google scholar: lookup
  85. Cole AM, Ganz T, Liese AM, Burdick MD, Liu L, Strieter RM. Cutting edge: IFN-inducible ELR- CXC chemokines display defensin-like antimicrobial activity.. J Immunol 2001 Jul 15;167(2):623-7.
    pubmed: 11441062doi: 10.4049/jimmunol.167.2.623google scholar: lookup
  86. Conti P, Boucher W, Letourneau R, Feliciani C, Reale M, Barbacane RC, Vlagopoulos P, Bruneau G, Thibault J, Theoharides TC. Monocyte chemotactic protein-1 provokes mast cell aggregation and [3H]5HT release.. Immunology 1995 Nov;86(3):434-40.
    pmc: PMC1383948pubmed: 8550082
  87. Gijsbers K, Gouwy M, Struyf S, Wuyts A, Proost P, Opdenakker G, Penninckx F, Ectors N, Geboes K, Van Damme J. GCP-2/CXCL6 synergizes with other endothelial cell-derived chemokines in neutrophil mobilization and is associated with angiogenesis in gastrointestinal tumors.. Exp Cell Res 2005 Feb 15;303(2):331-42.
    pubmed: 15652347doi: 10.1016/j.yexcr.2004.09.027google scholar: lookup
  88. Liao F, Rabin RL, Yannelli JR, Koniaris LG, Vanguri P, Farber JM. Human Mig chemokine: biochemical and functional characterization.. J Exp Med 1995 Nov 1;182(5):1301-14.
    pmc: PMC2192190pubmed: 7595201doi: 10.1084/jem.182.5.1301google scholar: lookup
  89. Taub DD, Lloyd AR, Conlon K, Wang JM, Ortaldo JR, Harada A, Matsushima K, Kelvin DJ, Oppenheim JJ. Recombinant human interferon-inducible protein 10 is a chemoattractant for human monocytes and T lymphocytes and promotes T cell adhesion to endothelial cells.. J Exp Med 1993 Jun 1;177(6):1809-14.
    pmc: PMC2191047pubmed: 8496693doi: 10.1084/jem.177.6.1809google scholar: lookup
  90. Conti P, DiGioacchino M. MCP-1 and RANTES are mediators of acute and chronic inflammation.. Allergy Asthma Proc 2001 May-Jun;22(3):133-7.
    pubmed: 11424873doi: 10.2500/108854101778148737google scholar: lookup
  91. Daly C, Rollins BJ. Monocyte chemoattractant protein-1 (CCL2) in inflammatory disease and adaptive immunity: therapeutic opportunities and controversies.. Microcirculation 2003 Jun;10(3-4):247-57.
    pubmed: 12851642doi: 10.1038/sj.mn.7800190google scholar: lookup
  92. Cole KE, Strick CA, Paradis TJ, Ogborne KT, Loetscher M, Gladue RP, Lin W, Boyd JG, Moser B, Wood DE, Sahagan BG, Neote K. Interferon-inducible T cell alpha chemoattractant (I-TAC): a novel non-ELR CXC chemokine with potent activity on activated T cells through selective high affinity binding to CXCR3.. J Exp Med 1998 Jun 15;187(12):2009-21.
    pmc: PMC2212354pubmed: 9625760doi: 10.1084/jem.187.12.2009google scholar: lookup
  93. Yang D, Chen Q, Hoover DM, Staley P, Tucker KD, Lubkowski J, Oppenheim JJ. Many chemokines including CCL20/MIP-3alpha display antimicrobial activity.. J Leukoc Biol 2003 Sep;74(3):448-55.
    pubmed: 12949249doi: 10.1189/jlb.0103024google scholar: lookup
  94. Pycock JF, Allen WE. Inflammatory components in uterine fluid from mares with experimentally induced bacterial endometritis.. Equine Vet J 1990 Nov;22(6):422-5.
    pubmed: 2269266doi: 10.1111/j.2042-3306.1990.tb04309.xgoogle scholar: lookup
  95. Hayes M, Quinn B, Lillie B, Côté O, Bienzle D, Waelchli R. Changes in various endometrial proteins during cloprostenol-induced failure of early pregnancy in mares. Anim Reprod Sci 2012;9:723–41.
  96. Bruhn O, Grötzinger J, Cascorbi I, Jung S. Antimicrobial peptides and proteins of the horse--insights into a well-armed organism.. Vet Res 2011 Sep 2;42(1):98.
    pmc: PMC3179947pubmed: 21888650doi: 10.1186/1297-9716-42-98google scholar: lookup
  97. Kolm G, Klein D, Knapp E, Watanabe K, Walter I. Lactoferrin expression in the horse endometrium: relevance in persisting mating-induced endometritis.. Vet Immunol Immunopathol 2006 Nov 15;114(1-2):159-67.
    pubmed: 16973221doi: 10.1016/j.vetimm.2006.08.005google scholar: lookup
  98. Suire S, Stewart F, Beauchamp J, Kennedy MW. Uterocalin, a lipocalin provisioning the preattachment equine conceptus: fatty acid and retinol binding properties, and structural characterization.. Biochem J 2001 Jun 1;356(Pt 2):369-76.
    pmc: PMC1221847pubmed: 11368763doi: 10.1042/0264-6021:3560369google scholar: lookup
  99. Van den Steen PE, Proost P, Wuyts A, Van Damme J, Opdenakker G. Neutrophil gelatinase B potentiates interleukin-8 tenfold by aminoterminal processing, whereas it degrades CTAP-III, PF-4, and GRO-alpha and leaves RANTES and MCP-2 intact.. Blood 2000 Oct 15;96(8):2673-81.
    pubmed: 11023497
  100. Van Den Steen PE, Wuyts A, Husson SJ, Proost P, Van Damme J, Opdenakker G. Gelatinase B/MMP-9 and neutrophil collagenase/MMP-8 process the chemokines human GCP-2/CXCL6, ENA-78/CXCL5 and mouse GCP-2/LIX and modulate their physiological activities.. Eur J Biochem 2003 Sep;270(18):3739-49.
    pubmed: 12950257doi: 10.1046/j.1432-1033.2003.03760.xgoogle scholar: lookup
  101. Tester AM, Cox JH, Connor AR, Starr AE, Dean RA, Puente XS, López-Otín C, Overall CM. LPS responsiveness and neutrophil chemotaxis in vivo require PMN MMP-8 activity.. PLoS One 2007 Mar 21;2(3):e312.
    pmc: PMC1819564pubmed: 17375198doi: 10.1371/journal.pone.0000312google scholar: lookup
  102. Li Q, Park PW, Wilson CL, Parks WC. Matrilysin shedding of syndecan-1 regulates chemokine mobilization and transepithelial efflux of neutrophils in acute lung injury.. Cell 2002 Nov 27;111(5):635-46.
    pubmed: 12464176doi: 10.1016/s0092-8674(02)01079-6google scholar: lookup
  103. McQuibban GA, Gong JH, Wong JP, Wallace JL, Clark-Lewis I, Overall CM. Matrix metalloproteinase processing of monocyte chemoattractant proteins generates CC chemokine receptor antagonists with anti-inflammatory properties in vivo.. Blood 2002 Aug 15;100(4):1160-7.
    pubmed: 12149192

Citations

This article has been cited 10 times.
  1. Jacobsen S, Mortensen CD, Høj EA, Vinther AM, Berg LC, Adler DMT, Verwilghen D, van Galen G. Neutrophil Gelatinase-Associated Lipocalin in Synovial Fluid from Horses with and without Septic Arthritis.. Animals (Basel) 2022 Dec 21;13(1).
    doi: 10.3390/ani13010029pubmed: 36611638google scholar: lookup
  2. Ibrahim S, Hedia M, Taqi MO, Derbala MK, Mahmoud KGM, Ahmed Y, Sosa AS, Saber YHA, Hasanain MH, Nawito MF, Seidel GE. Extracellular vesicles in low volume uterine lavage and serum: novel and promising biomarker for endometritis in Arabian mares.. BMC Vet Res 2022 Jan 18;18(1):42.
    doi: 10.1186/s12917-022-03137-3pubmed: 35042518google scholar: lookup
  3. Weber KS, Wagener K, Blanco M, Bauersachs S, Bollwein H. A comparative analysis of the intrauterine transcriptome in fertile and subfertile mares using cytobrush sampling.. BMC Genomics 2021 May 22;22(1):377.
    doi: 10.1186/s12864-021-07701-3pubmed: 34022808google scholar: lookup
  4. Segabinazzi LGTM, Canisso IF, Podico G, Cunha LL, Novello G, Rosser MF, Loux SC, Lima FS, Alvarenga MA. Intrauterine Blood Plasma Platelet-Therapy Mitigates Persistent Breeding-Induced Endometritis, Reduces Uterine Infections, and Improves Embryo Recovery in Mares.. Antibiotics (Basel) 2021 Apr 23;10(5).
    doi: 10.3390/antibiotics10050490pubmed: 33922743google scholar: lookup
  5. Wonfor RE, Creevey CJ, Natoli M, Hegarty M, Nash DM, Rose MT. Interaction of preimplantation factor with the global bovine endometrial transcriptome.. PLoS One 2020;15(12):e0242874.
    doi: 10.1371/journal.pone.0242874pubmed: 33284816google scholar: lookup
  6. Canisso IF, Segabinazzi LGTM, Fedorka CE. Persistent Breeding-Induced Endometritis in Mares - a Multifaceted Challenge: From Clinical Aspects to Immunopathogenesis and Pathobiology.. Int J Mol Sci 2020 Feb 20;21(4).
    doi: 10.3390/ijms21041432pubmed: 32093296google scholar: lookup
  7. Van Cleemput J, Poelaert KCK, Laval K, Vanderheijden N, Dhaenens M, Daled S, Boyen F, Pasmans F, Nauwynck HJ. An Alphaherpesvirus Exploits Antimicrobial β-Defensins To Initiate Respiratory Tract Infection.. J Virol 2020 Mar 31;94(8).
    doi: 10.1128/JVI.01676-19pubmed: 31996426google scholar: lookup
  8. Kharayat NS, Sharma G C, Kumar GR, Bisht D, Chaudhary G, Singh SK, Das GK, Garg AK, Kumar H, Krishnaswamy N. Differential expression of endometrial toll-like receptors (TLRs) and antimicrobial peptides (AMPs) in the buffalo (Bubalus bubalis) with endometritis.. Vet Res Commun 2019 Nov;43(4):261-269.
    doi: 10.1007/s11259-019-09761-zpubmed: 31407222google scholar: lookup
  9. Narra HP, Sahni A, Khanipov K, Fofanov Y, Sahni SK. Global Transcriptomic Profiling of Pulmonary Gene Expression in an Experimental Murine Model of Rickettsia conorii Infection.. Genes (Basel) 2019 Mar 8;10(3).
    doi: 10.3390/genes10030204pubmed: 30857242google scholar: lookup
  10. Marth CD, Firestone SM, Glenton LY, Browning GF, Young ND, Krekeler N. Oestrous cycle-dependent equine uterine immune response to induced infectious endometritis.. Vet Res 2016 Nov 8;47(1):110.
    doi: 10.1186/s13567-016-0398-xpubmed: 27825391google scholar: lookup
Subscribe to our newsletter
Join 99,344 horse owners like you who receive our email updates on horse health and nutrition.