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Differential expression of endometrial toll-like receptors (TLRs) and antimicrobial peptides (AMPs) in the buffalo (Bubalus bubalis) with endometritis

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Abstract

Toll like receptors (TLRs) and β-defensins expressed in the endometrium are part of the innate uterine defense mechanism (UDM). In the present study, transcriptional profile of TLRs (1–3, 6–8, 10, and) and β-defensins such as lingual antimicrobial peptide (LAP), tracheal antimicrobial peptide (TAP) and bovine neutrophil beta-defensin 4 (BNBD4) were studied. Bubaline genitalia were collected from abattoir and the endometrium was categorized into one of the following seven groups (n = 7/group) based on cyclicity and endometritis: follicular non-endometritis (FNE), luteal non-endometritis (LNE), follicular cytological endometritis (FCE), luteal cytological endometritis (LCE), follicular purulent endometritis (FPE), luteal purulent endometritis (LPE) and acyclic non-endometritis (ANE). Cytological endometritis (CE) was diagnosed by uterine cytology while purulent endometritis (PE) was diagnosed by the presence of purulent or mucopurulent exudate in the uterine lumen. Real time PCR was performed and the relative fold change was analysed. TLR1 and BNBD4 transcripts were not found in the buffalo endometrium. Of all the innate immune genes studied, upregulation of TLR and β-defensins was mostly contributed by the inflammatory status of endometrium. Further, there was a prominent upregulation of TAP in buffaloes with endometritis. However, no association could be found between the inflammatory status of the endometrium and phase of estrous cycle with respect to the expression of TLRs and β-defensins.

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References

  • Afrazi A, Sodhi CP, Good M, Jia H, Siggers R, Yazji I, Ma C, Neal MD, Prindle T, Grant ZS, Branca MF, Ozolek J, Chang EB, Hackam DJ (2012) Intracellular heat shock protein-70 negatively regulates TLR4 signaling in the newborn intestinal epithelium. J Immunol 188(9):4543–4557

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ajevar G, Muthu S, Sarkar M, Kumar H, Das GK, Krishnaswamy N (2014) Trnascriptional profile of endometrial TLR4 and 5 genes during the estrous cycle and uterine infection in the buffalo. Vet Res Commun 38:171–176

    PubMed  Google Scholar 

  • Alva-Murillo N, Ochoa-Zarzosa A, Lopez-Meza J (2012) Short chain fatty acids (propionic and hexanoic) decrease Staphylococcus aureus internalization into bovine mammary epithelial cells and modulate antimicrobial peptide expression. Vet Microbiol 155(2-4):324–331

    CAS  PubMed  Google Scholar 

  • Azawi OI (2008) Postpartum uterine infection in cattle: a review. Anim Reprod Sci 105:187–208

    CAS  PubMed  Google Scholar 

  • Azawi OI, Omran SN, Hadad JJ (2008) A study of endometritis causing repeat breeding of cycling Iraqi Buffalo cows. Reprod Domest Anim 43(6):735–743

    CAS  PubMed  Google Scholar 

  • Bera BC, Chaudhury P, Bhattacharya D, Bera AK, Das SK (2007) Cloning, sequencing and expression of cDNA of bovine neutrophil beta-defensin from water buffalo (Bubalus bubalis). Int J Immunogenet 34(3):173–179

    CAS  PubMed  Google Scholar 

  • Berghuis L, Abdelaziz KT, Bierworth J, Wyer L, Jacob G, Karrow NA, Sharif S, Clark ME, Jeff L (2014) Comparison of innate immune agonists for induction of tracheal antimicrobial peptide gene expression in tracheal epithelial cells of cattle. Vet Res 45(1):105

    PubMed  PubMed Central  Google Scholar 

  • Borges AM, Healey GD, Sheldon IM (2012) Explants of intact endometrium to model bovine innate immunity and inflammation ex vivo. Am J Reprod Immunol 67:526–539

    CAS  PubMed  Google Scholar 

  • Chapwanya A, Meade KG, Doherty ML, Callanan JJ, Mee JF, O'Farrelly C (2009) Histopathological and molecular evaluation of Holstein-Friesian cows postpartum: toward an improved understanding of uterine innate immunity. Theriogenology 71:1396–1407

    CAS  PubMed  Google Scholar 

  • Chapwanya A, Meade KG, Foley C, Narciandi F, Evans AC, Doherty ML, Callanan JJ, O'Farrelly C (2012) The postpartum endometrial inflammatory response: a normal physiological event with potential implications for bovine fertility. Reprod Fertil Dev 24(8):1028–1039

    CAS  PubMed  Google Scholar 

  • Chapwanya A, Meade KG, Doherty ML, Callanan JJ, O’Farrelly C (2013) Endometrial epithelial cells are potent producers of tracheal antimicrobial peptide and serum amyloid A3 gene expression in response to E. coli stimulation. Vet Immunol Immunopathol 151(1–2):157–162

    CAS  PubMed  Google Scholar 

  • Cohen RO, Colodner R, Ziv G, Keness J (1996) Isolation and antimicrobial susceptibility of obligate anaerobic bacteria recovered from the uterus of dairy postparturent endometritis. Zentralbl Veterinarmed B 43:193–199

    CAS  PubMed  Google Scholar 

  • Cormican P, Meade KG, Cahalane S, Narciandi F, Chapwanya A, Lloyd AT, O'Farrelly C (2008) Evolution, expression and effectivness in a cluster of novel bovine beta-defensins. Immunogenetics 60:147–156

    CAS  PubMed  Google Scholar 

  • Davies D, Meade KG, Herath S, Eckersall PD, Gonzalez D, White JO, Conlan RS, O'Farrelly C, Sheldon IM (2008) Toll-like receptor and antimicrobial peptide expression in the bovine endometrium. Reprod Biol Endocrinol 6:1–12

    Google Scholar 

  • Esposito G, Irons PC, Webb EC, Chapwanya A (2014) Interactions between negative energy balance, metabolic diseases, uterine health and immune response in transition dairy cows. Anim Reprod Sci 144(3-4):60–71

    CAS  PubMed  Google Scholar 

  • Frew L, Stock SJ (2011) Antimicrobial peptides and pregnancy. Reproduction 141:725–735

    CAS  PubMed  Google Scholar 

  • Ganz T (2003) The role of antimicrobial peptides in innate immunity. Integr Comp Biol 43:300–304

    CAS  PubMed  Google Scholar 

  • Gier HT, Marion GB (1968) Uterus of the cow after parturition: involutional changes. Am J Vet 29(1):83–96

    CAS  Google Scholar 

  • Gilbert RO, Shin ST, Guard CL, Erb HN, Frajblat M (2005) Prevalence of endometritis and its effect on reproductive performance of dairy cows. Theriogenology 64:1879–1888

    PubMed  Google Scholar 

  • Griffin JFT, Hartigan PJ, Nunn WR (1974) Non-specific uterine infection and bovine fertility: I infection patterns and endometritis during the first seven weeks post-partum. Theriogenology 1:91–106

    CAS  PubMed  Google Scholar 

  • Herath S, Dobson H, Bryant CE, Sheldon IM (2006) Use of the cow as a large animal model of uterine infection and immunity. J Reprod Immunol 69:13–22

    CAS  PubMed  Google Scholar 

  • Herath S, Lilly ST, Fischer DP, Williams EJ, Dobson H, Bryant CE, Sheldon IM (2009) Bacterial lipopolysaccharide induces an endocrine switch from prostaglandin F2alpha to prostaglandin E2 in bovine endometrium. Endocrinology 150:1912–1920

    CAS  PubMed  Google Scholar 

  • Ireland JJ, Murphee RL, Coulson PB (1980) Accuracy of predicting stages of bovine estrous cycle by gross appearance of the corpus luteum. J Dairy Sci 63:155–160

    CAS  PubMed  Google Scholar 

  • Joseph D, More T (2011) Molecular characterization of lingual antimicrobial peptide in the female reproductive tract of Buffalo. Vet World 4(3):120–123

    Google Scholar 

  • Kannaki TR, Shanmugam M, Verma PC (2011) Toll-like receptors and their role in animal reproduction. Anim Reprod Sci 125:1–12

    CAS  PubMed  Google Scholar 

  • Kawai T, Akira S (2010) The role of pattern-recognition receptors in innate immunity: update on toll-like receptors. Nat Immunol 11:373–384

    CAS  PubMed  Google Scholar 

  • King AE, Critchley HO, Kelly RW (2003) Innate immune defences in the human endometrium. Reprod Biol Endocrinol 1:116

    PubMed  PubMed Central  Google Scholar 

  • Lewis GS (2003) Steroidal regulation of uterine resistance to bacterial infection in livestock. Reprod Biol Endocrinol 1:117

    PubMed  PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real time quantitative PCR and the 2(−Delta delta C(T)) method. Methods 25:4028

    Google Scholar 

  • Loyi T, Kumar H, Nandi S, Mathapati BS, Patra MK, Pattnaik B (2012) Differential expression of pro-inflammatory cytokines in endometrial tissue of buffaloes with clinical and sub-clinical endometritis. Res Vet Sci 90:336–340

    Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • Martinon F, Mayor A, Tschopp J (2009) The inflammasomes: guardians of the body. Annu Rev Immunol 27:229–265

    CAS  PubMed  Google Scholar 

  • McGuire K, Jones M, Werling D, Williams JL, Glass EJ, Jann O (2005) Radiation hybrid mapping of all 10 characterized bovine toll-like receptors. Anim Genet 37:47–50

    Google Scholar 

  • Raman SRP, Bawa SJS (1977) Incidence of pre and postpartum reproductive disorders in buffaloes. Haryana Veterinarian 16:99–101

    Google Scholar 

  • Rao AV, Sreemannarayana O (1982) Clinical analysis of reproductive failure among female buffaloes (Bubalus bubalis) under village management in Andhra Pradesh. Theriogenology 18(4):403–411

    CAS  PubMed  Google Scholar 

  • Ruder CA, Sasser RG, Williams RJ, Ely JK, Bull RC, Butler JE (1981) Uterine infections in the postpartum cow: II. Possible synergistic effect of fusobacterium necrophorum and Corynebacterium pyogenes. Theriogenology 15:573–580

    Google Scholar 

  • Ruiz-González I, Minten M, Wang X, Dunlap KA, Bazer FW (2015) Involvement of TLR7 and TLR8 in conceptus development and establishment of pregnancy in sheep. Reproduction 149(4):305–316

    PubMed  Google Scholar 

  • Schneider JJ, Unholzer A, Schaller M, Schäfer-Korting M, Korting HC (2005) Human defensins. J Mol Med 83:587–595

    CAS  PubMed  Google Scholar 

  • Selsted ME, Ouellette AJ (2005) Mammalian defensins in the antimicrobial immune response. Nat Immunol 6(6):551–557

    CAS  PubMed  Google Scholar 

  • Sheldon IM (2004) The postpartum uterus. Vet Clin Food Anim 20:569–591

    Google Scholar 

  • Sheldon IM, Bromfield JJ (2011) Innate immunity in the human endometrium and ovary. Am J Reprod Immunol 66(1):63–71

    PubMed  Google Scholar 

  • Sheldon IM, Dobson H (2004) Postpartum uterine health in cattle. Anim Reprod Sci 82–83:295–306

    PubMed  Google Scholar 

  • Sheldon IM, Noakes DE, Rycroft AN, Pfeiffer DU, Dobson H (2002) Influence of uterine bacterial contamination after parturition on ovarian dominant follicle selection and follicle growth and function in cattle. Reproduction 123:837–845

    CAS  PubMed  Google Scholar 

  • Sheldon IM, Lewis GS, LeBlanc S, Gilbert RO (2006) Defining postpartum uterine disease in cattle. Theriogenology 65:1516–1530

    PubMed  Google Scholar 

  • Sheldon IM, Cronin J, Goetze L, Donofrio G, Schuberth HJ (2009) Defining postpartum uterine disease and the mechanisms of infection and immunity in the female reproductive tract in cattle. Biol Reprod 81:1025–1032

    CAS  PubMed  PubMed Central  Google Scholar 

  • Siemieniuch MJ, Szostek AZ, Gajos K, Kozdrowski R, Nowak M, Okuda K, (2016) Type of Inflammation Differentially Affects Expression of Interleukin 1β and 6 Tumor necrosis factor-α and toll–like receptors in subclinical endometritis in mares. PLoS One 11(5):1–17

    Google Scholar 

  • Silva E, Leitão S, Henriques S, Kowalewski MP, Hoffmann B, Ferreira-Dias G, da Costa LL, Mateus L (2010) 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 84(1):66–74

    CAS  PubMed  Google Scholar 

  • Turner ML, Cronin JG, Healey GD, Sheldon IM (2014) Epithelial and stromal cells of bovine endometrium have roles in innate immunity and initiate inflammatory responses to bacterial lipopeptides in vitro via toll-like receptors TLR2, TLR1, and TLR6. Endocrinology 155:1453–1465

    PubMed  PubMed Central  Google Scholar 

  • Vahanan MB, Raj GD, Pawar RMC, Gopinath VP, Raja A, Thangavelu A (2008) Expression profile of toll like receptor in a range of water buffalo tissues (Bubalus bubalis). Vet Immun Immunopathol 126:149–155

    CAS  Google Scholar 

  • Wang Z, Wang G (2004) APD: the antimicrobial peptide database. Nucleic Acids Res 32:590–592

    Google Scholar 

  • Williams EJ, Fischer DP, England GCW, Dobson H, Pfeiffer DU, Sheldon IM (2005) Clinical evaluation of postpartum vaginal mucus reflects uterine bacterial infection and the inflammatory response to endometritis in cattle. Theriogenology 63(1):102–117

    PubMed  Google Scholar 

  • Wira CR, Grant-Tschudy KS, Crane-Godreau MA (2005) Epithelial cells in the female reproductive tract: a central role as sentinels of immune protection. Am J Reprod Immunol 53:65–76

    CAS  PubMed  Google Scholar 

  • Zeng Y, Adegoke EO, Wang X, Lin X, Wang H, Wang C, Zhang G (2017) Expression of β-defensins in bovine oviduct and uterus during follicular and luteal phases. Comp Clin Pathol 26:749–756

    CAS  Google Scholar 

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Correspondence to Narayanan Krishnaswamy.

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Kharayat, N.S., Sharma G, C., Kumar, G.R. et al. Differential expression of endometrial toll-like receptors (TLRs) and antimicrobial peptides (AMPs) in the buffalo (Bubalus bubalis) with endometritis. Vet Res Commun 43, 261–269 (2019). https://doi.org/10.1007/s11259-019-09761-z

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