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Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE (Open Access)

Influence of pathogenic bacteria species present in the postpartum bovine uterus on proteome profiles

A. M. Ledgard A B , G. A. Smolenski A , H. Henderson A and R. S.-F. Lee A
+ Author Affiliations
- Author Affiliations

A AgResearch, Ruakura Research Centre, East Street, Hamilton 3240, New Zealand.

B Corresponding author. Email: anita.ledgard@agresearch.co.nz

Reproduction, Fertility and Development 27(2) 395-406 https://doi.org/10.1071/RD13144
Submitted: 9 May 2013  Accepted: 31 October 2013   Published: 12 December 2013

Journal Compilation © CSIRO Publishing 2015 Open Access CC BY-NC-ND

Abstract

In the first 2–3 weeks after parturition >90% of dairy cows will have some form of uterine infection. Uterine contamination with pathogens, such as Trueperella (formerly Arcanobacterium) pyogenes increases the risk of developing more severe endometritis, which can reduce conception rates. In this study, we compared the uterine proteome of cows infected with Trueperella pyogenes with that of uninfected cows, using 2D gel electrophoresis, and identified annexins A1 and A2 (ANXA1 and ANXA2), apolipoprotein A-1, calprotectin (S100A9), cathelicidin, enolase 1 (ENO1), peptidoglycan recognition protein 1 (PGLYRP1), phosphoglycerate mutase 1 (PGAM1), serine dehydratase (SDS) and serine protease inhibitors (SERPIN) B1, B3 and B4 proteins as differing in abundance in endometritis. Subsequently, levels of ten of these proteins were monitored in uterine samples collected from a herd of lactating, dairy cows at 15 and 42 days post-partum (DPP). The levels were compared with the cytology scores of the samples and the bacterial species isolated from the uterus. Cathelicidin, PGLYRP1, SERPINB1 and S100A9 levels at 15DPP showed strong positive correlations (r = 0.78, 0.80, 0.79, and 0.68 respectively; P < 0.001) with % of polymorphonuclear neutrophils (PMN). When compared with other bacterial pathogens identified, Streptococcus agalactiae and Truperella pyogenes induced increased expression of the indicator proteins, suggesting that these organisms may adversely affect the subsequent ability of the cow to conceive. Interestingly, there was no difference in the proportion of cows pregnant at 6 and 17 weeks after start of mating between the cows with high or low %PMN.

Additional keywords: Arcanobacterium pyogenes, endometritis, postpartum, pregnancy, Streptococcus agalactiae, uterine.


References

Asselin, E., Lacroix, D., and Fortier, M. A. (1997). IFN-tau increases PGE2 production and COX-2 gene expression in the bovine endometrium in vitro. Mol. Cell. Endocrinol. 132, 117–126.
IFN-tau increases PGE2 production and COX-2 gene expression in the bovine endometrium in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXlslCjt78%3D&md5=2699d0d53cd89f7afb77a1ee976a3403CAS | 1:CAS:528:DyaK2sXlslCjt78%3D&md5=2699d0d53cd89f7afb77a1ee976a3403CAS | 9324053PubMed |

Bergey, D. H. (1994). ‘Bergey’s Manual of Determinative Bacteriology’. 9th edn. (Eds J. G. Holt, N. R. Krieg, P. H. Sneath, J. T. Staley and S. T. Williams.) (Lippincott Williams & Wilkins: Philadelphia.)

Beveridge, J. D., Gordon, B. M., Brewer, D., Clark, M. E., and Caswell, J. L. (2008). Altered protein expression in neutrophils of calves treated with dexamethasone. Can. J. Vet. Res. 72, 249–252.
| 1:CAS:528:DC%2BD1cXmvFSjsrk%3D&md5=c6cc50b279c8db007d175e49ce3cd75eCAS | 18505188PubMed |

Billington, S. J., Jost, B. H., Cuevas, W. A., Bright, K. R., and Songer, J. G. (1997). The Arcanobacterium (Actinomyces) pyogenes haemolysin, pyolysin, is a novel member of the thiol-activated cytolysin family. J. Bacteriol. 179, 6100–6106.
| 1:CAS:528:DyaK2sXmsFCisLs%3D&md5=7651c23515ee8f616c076b033399e72fCAS | 9324258PubMed |

Bondurant, R. H. (1999). Inflammation in the bovine female reproductive tract. J. Anim. Sci. 77, 101–110.
| 1:CAS:528:DyaK1MXlvFWhtbc%3D&md5=18ceb3d26f07450bf21ceb07f40e6417CAS | 15526785PubMed |

Bos, C. L., Richel, D. J., Ritsema, T., Peppelenbosch, M. P., and Versteeg, H. H. (2004). Prostanoids and prostanoid receptors in signal transduction. Int. J. Biochem. Cell Biol. 36, 1187–1205.
Prostanoids and prostanoid receptors in signal transduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjsVWnsLc%3D&md5=42d440c368ad6be5980b94dbb5528a11CAS | 15109566PubMed |

Cole, A. M. (2006). Innate host defence of human vaginal and cervical mucosae. Curr. Top. Microbiol. Immunol. 306, 199–230.
Innate host defence of human vaginal and cervical mucosae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xos1ymur0%3D&md5=a5865419c628dc8038426be0d8b5ff99CAS | 16909923PubMed |

Domínguez, F., Garrido-Gómez, T., López, J. A., Camafeita, E., Quiñonero, A., Pellicer, A., and Simón, C. (2009). Proteomic analysis of the human receptive versus non-receptive endometrium using differential in-gel electrophoresis and MALDI-MS unveils stathmin 1 and annexin A2 as differentially regulated. Hum. Reprod. 24, 2607–2617.
Proteomic analysis of the human receptive versus non-receptive endometrium using differential in-gel electrophoresis and MALDI-MS unveils stathmin 1 and annexin A2 as differentially regulated.Crossref | GoogleScholarGoogle Scholar | 19556289PubMed |

Dziarski, R., and Gupta, D. (2010). Review: mammalian peptidoglycan recognition proteins (PGRPs) in innate immunity. Innate Immun. 16, 168–174.
Review: mammalian peptidoglycan recognition proteins (PGRPs) in innate immunity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpt1Cnsb0%3D&md5=7db835c8e3406de84a5f33d0d246ae40CAS | 20418257PubMed |

Foell, D., Frosch, M., Sorg, C., and Roth, J. (2004). Phagocyte-specific calcium-binding S100 proteins as clinical laboratory markers of inflammation. Clin. Chim. Acta 344, 37–51.
Phagocyte-specific calcium-binding S100 proteins as clinical laboratory markers of inflammation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXktVOnsrg%3D&md5=55beb46790f3152e663acbefaa66c84dCAS | 15149869PubMed |

Fontán, P. A., Pancholi, V., Nociari, M. M., and Fischetti, V. A. (2000). Antibodies to streptococcal surface enolase react with human alpha-enolase: implications in poststreptococcal sequelae. J. Infect. Dis. 182, 1712–1721.
Antibodies to streptococcal surface enolase react with human alpha-enolase: implications in poststreptococcal sequelae.Crossref | GoogleScholarGoogle Scholar | 11069244PubMed |

Fothergill-Gilmore, L. A., and Watson, H. C. (1989). The phosphoglycerate mutase. Adv. Enzymol. Relat.Areas Mol. Bio. 62, 227–313.
| 1:CAS:528:DyaL1MXlt12nsb4%3D&md5=1aa634a95ca36e6f93aa36d492817c3fCAS |

Fourichon, C., Seegers, H., and Malher, X. (2000). Effect of disease on reproduction in the dairy cow: a meta-analysis. Theriogenology 53, 1729–1759.
Effect of disease on reproduction in the dairy cow: a meta-analysis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3cvpsFensQ%3D%3D&md5=41c23c9e6d5a8251d11fec42c771f5e2CAS | 10968418PubMed |

Gabler, C., Drillich, M., Fischer, C., Holder, C., Heuwieser, W., and Einspanier, R. (2009). Endometrial expression of selected transcripts involved in prostaglandin synthesis in cows with endometritis. Theriogenology 71, 993–1004.
Endometrial expression of selected transcripts involved in prostaglandin synthesis in cows with endometritis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXivVWltb4%3D&md5=a3b70f40d099814d4e18fac701671999CAS | 19162311PubMed |

Gatto, M., Iaccarino, L., Ghirardello, A., Bassi, N., Pontisso, P., Punzi, L., Shoenfeld, Y., and Doria, A. (2013). Serpins, immunity and autoimmunity: old molecules, new functions. Clin. Rev. Allergy Immunol. 45, 267–280.
Serpins, immunity and autoimmunity: old molecules, new functions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsVymurbL&md5=fd1b84e4ce1880c4b74d96f100c2421aCAS | 23325331PubMed |

Gautam, G., Nakao, T., Koike, K., Long, S. T., Yusuf, M., Ranasinghe, R. M., and Hayashi, A. (2010). Spontaneous recovery or persistence of postpartum endometritis and risk factors for its persistence in Holstein cows. Theriogenology 73, 168–179.
Spontaneous recovery or persistence of postpartum endometritis and risk factors for its persistence in Holstein cows.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1MfhslGruw%3D%3D&md5=b03fb44216799f2b357c5bb9b952cf8bCAS | 19837450PubMed |

Gebhardt, C., Németh, J., Angel, P., and Hess, J. (2006). S100A8 and S100A9 in inflammation and cancer. Biochem. Pharmacol. 72, 1622–1631.
S100A8 and S100A9 in inflammation and cancer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFOjt77F&md5=a8af9bcc144ee8903b6c126f970ef983CAS | 16846592PubMed |

Green, M. P., Ledgard, A. M., Beaumont, S. E., Berg, M. C., McNatty, K. P., Peterson, A. J., and Back, P. J. (2011). Long-term alteration of follicular steroid concentrations in relation to subclinical endometritis in postpartum dairy cows. J. Anim. Sci. 89, 3551–3560.
Long-term alteration of follicular steroid concentrations in relation to subclinical endometritis in postpartum dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVSqsr3F&md5=895eff854620e4adf20210ea53dc1857CAS | 1:CAS:528:DC%2BC3MXhsVSqsr3F&md5=895eff854620e4adf20210ea53dc1857CAS | 21666004PubMed |

Griffin, J. F. T., Hartigan, P. J., and Nunn, W. R. (1974). Non-specific uterine infection and bovine fertility. I. Infection patterns and endometritis during the first seven weeks post-partum. Theriogenology 1, 91–106.
Non-specific uterine infection and bovine fertility. I. Infection patterns and endometritis during the first seven weeks post-partum.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE28%2Fms1ynsA%3D%3D&md5=3d1aa10c744529759fb7d5420f442a36CAS |

Hughes, M. J., Moore, J. C., Lane, J. D., Wilson, R., Pribul, P. K., Younes, Z. N., Dobson, R. J., Everest, P., Reason, A. J., Redfern, J. M., Greer, F. M., Paxton, T., Panico, M., Morris, H. R., Feldman, R. G., and Santangelo, J. D. (2002). Identification of major outer surface proteins of Streptococcus agalactiae. Infect. Immun. 70, 1254–1259.
Identification of major outer surface proteins of Streptococcus agalactiae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhsFSls7o%3D&md5=f560f08f74f7a52b916b637e9627427dCAS | 11854208PubMed |

Hutchinson, J. L., Rajagopal, S. P., Sales, K. J., and Jabbour, H. N. (2011). Molecular regulators of resolution of inflammation: potential therapeutic targets in the reproductive system. Reproduction 142, 15–28.
Molecular regulators of resolution of inflammation: potential therapeutic targets in the reproductive system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFSqu7%2FK&md5=e347c7678a13d9d814395b996a62b6b4CAS | 21490125PubMed |

Kasimanickam, R., Duffield, T. F., Foster, R. A., Gartley, C. J., Leslie, K. E., Walton, J. S., and Johnson, W. H. (2005). A comparison of the cytobrush and uterine lavage techniques to evaluate endometrial cytology in clinically normal postpartum dairy cows. Can. Vet. J. 46, 255–259.
| 15884649PubMed |

Keefe, G. P. (1997). Streptococcus agalactiae mastitis: a review Can. Vet. J. 38, 429–437.
| 1:STN:280:DyaK2szmtlynsg%3D%3D&md5=1ef335415ca4423a2f23312467dd06feCAS | 9220132PubMed |

Kudo, I., Murakami, M., Hara, S., and Inoue, K. (1993). Mammalian non-pancreatic phospholipases A2. Biochim. Biophys. Acta 1170, 217–231.
Mammalian non-pancreatic phospholipases A2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXjtF2k&md5=0ca6bed3b72fb65108241486a9ae5e54CAS | 1:CAS:528:DyaK2cXjtF2k&md5=0ca6bed3b72fb65108241486a9ae5e54CAS | 8218339PubMed |

LeBlanc, S. J. (2008). Postpartum uterine disease and dairy-herd reproductive performance: a review. Vet. J. 176, 102–114.
Postpartum uterine disease and dairy-herd reproductive performance: a review.Crossref | GoogleScholarGoogle Scholar | 18328749PubMed |

LeBlanc, S. J., Osawa, T., and Dubuc, J. (2011). Reproductive tract defence and disease in postpartum dairy cows. Theriogenology 76, 1610–1618.
Reproductive tract defence and disease in postpartum dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVanurzF&md5=d6ed029da7c68070dbd11a21d0209231CAS | 1:CAS:528:DC%2BC3MXhsVanurzF&md5=d6ed029da7c68070dbd11a21d0209231CAS | 21890187PubMed |

Ledgard, A. M., Meier, S., and Peterson, A. J. (2011). Evaluation of the uterine environment early in pregnancy establishment to characterise cows with a potentially superior ability to support conceptus survival. Reprod. Fertil. Dev. 23, 737–747.
Evaluation of the uterine environment early in pregnancy establishment to characterise cows with a potentially superior ability to support conceptus survival.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MjhsVCktA%3D%3D&md5=33611b737d285d6fecbae7e4b5a5b2cbCAS | 1:STN:280:DC%2BC3MjhsVCktA%3D%3D&md5=33611b737d285d6fecbae7e4b5a5b2cbCAS | 21791175PubMed |

Ledgard, A. M., Berg, M. C., McMillan, W. H., Smolenski, G., and Peterson, A. J. (2012). Effect of asynchronous transfer on bovine embryonic development and relationship with early cycle uterine proteome profiles. Reprod. Fertil. Dev. 24, 962–972.
Effect of asynchronous transfer on bovine embryonic development and relationship with early cycle uterine proteome profiles.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38bisl2rtg%3D%3D&md5=1eadccc146d53205a835ebf29f18567dCAS | 1:STN:280:DC%2BC38bisl2rtg%3D%3D&md5=1eadccc146d53205a835ebf29f18567dCAS | 22935157PubMed |

Lewis, G. S. (1997). Uterine health and disorders. J. Dairy Sci. 80, 984–994.
Uterine health and disorders.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjsVOksbs%3D&md5=113f77a7e26b867dfc6b4df63068f9c1CAS | 1:CAS:528:DyaK2sXjsVOksbs%3D&md5=113f77a7e26b867dfc6b4df63068f9c1CAS | 9178140PubMed |

Li, C. Y., Lang, J. H., Liu, H. Y., and Zhou, H. M. (2008). Expression of annexin-1 in patients with endometriosis. Chin. Med. J. (Engl.) 121, 927–931.
| 1:CAS:528:DC%2BD1cXnslGqtrY%3D&md5=857711311ed09220b9b3a95508bcba41CAS |
| 1:CAS:528:DC%2BD1cXnslGqtrY%3D&md5=857711311ed09220b9b3a95508bcba41CAS | 18706208PubMed |

Mateus, L., da Costa, L. L., Bernardo, F., and Silva, J. R. (2002). Influence of puerperal uterine infection on uterine involution and postpartum ovarian activity in dairy cows. Reprod. Domest. Anim. 37, 31–35.
Influence of puerperal uterine infection on uterine involution and postpartum ovarian activity in dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD387ltVGhtw%3D%3D&md5=f627510169bd194c9d1c0e2de13921a1CAS | 11882243PubMed |

McDougall, S., Macaulay, R., and Compton, C. (2007). Association between endometritis diagnosis using a novel intravaginal device and reproductive performance in dairy cattle. Anim. Reprod. Sci. 99, 9–23.
Association between endometritis diagnosis using a novel intravaginal device and reproductive performance in dairy cattle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2s7it12msg%3D%3D&md5=ec694d042d62b0b07269e3bff3d1f8a0CAS | 16630700PubMed |

McDougall, S., Hussien, H., Aberdein, D., Buckle, K., Roche, J. R., Burke, C. R., Mitchell, M. D., and Meier, S. (2011). Relationships between cytology, bacteriology and vaginal discharge scores and reproductive performance in dairy cows. Theriogenology 76, 229–240.
Relationships between cytology, bacteriology and vaginal discharge scores and reproductive performance in dairy cows.Crossref | GoogleScholarGoogle Scholar | 21601918PubMed |

Miller, A. N., Williams, E. J., Sibley, K., Herath, S., Lane, E. A., Fishwick, J., Nash, D. M., Rycroft, A. N., Dobson, H., Bryant, C. E., and Sheldon, I. M. (2007). The effects of Arcanobacterium pyogenes on endometrial function in vitro, and on uterine and ovarian function in vivo. Theriogenology 68, 972–980.
The effects of Arcanobacterium pyogenes on endometrial function in vitro, and on uterine and ovarian function in vivo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVOgsb7E&md5=074ea222e709748b1d266bab6728057fCAS | 17825901PubMed |

Paape, M., Mehrzad, J., Zhao, X., Detilleux, J., and Burvenich, C. (2002). Defence of the bovine mammary gland by polymorphonuclear neutrophil leukocytes. J. Mammary Gland Biol. Neoplasia 7, 109–121.
Defence of the bovine mammary gland by polymorphonuclear neutrophil leukocytes.Crossref | GoogleScholarGoogle Scholar | 12463734PubMed |

Pancholi, V. (2001). Multifunctional alpha-enolase: its role in diseases. Cell. Mol. Life Sci. 58, 902–920.
Multifunctional alpha-enolase: its role in diseases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlvFSmsrY%3D&md5=04ae1248af98766a08bc0165fe8180edCAS | 1:CAS:528:DC%2BD3MXlvFSmsrY%3D&md5=04ae1248af98766a08bc0165fe8180edCAS | 11497239PubMed |

Parent, J., and Fortier, M. A. (2005). Expression and contribution of three different isoforms of prostaglandin E synthase in the bovine endometrium. Biol. Reprod. 73, 36–44.
Expression and contribution of three different isoforms of prostaglandin E synthase in the bovine endometrium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXls1Srtrs%3D&md5=7c7ef6888af91daf74baeeabac9721d0CAS | 1:CAS:528:DC%2BD2MXls1Srtrs%3D&md5=7c7ef6888af91daf74baeeabac9721d0CAS | 15744024PubMed |

Parente, L., and Solito, E. (2004). Annexin 1: more than an anti-phospholipase protein. Inflamm. Res. 53, 125–132.
Annexin 1: more than an anti-phospholipase protein.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjvVyht7k%3D&md5=6c0ae5a2d45c62afb85f906d8af09195CAS | 1:CAS:528:DC%2BD2cXjvVyht7k%3D&md5=6c0ae5a2d45c62afb85f906d8af09195CAS | 15060718PubMed |

Perretti, M., and D’Acquisto, F. (2009). Annexin A1 and glucocorticoids as effectors of the resolution of inflammation. Nat. Rev. Immunol. 9, 62–70.
Annexin A1 and glucocorticoids as effectors of the resolution of inflammation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFartbzP&md5=791089b728a2b49b44f8ee19dea982b9CAS | 19104500PubMed |

Petzl, W., Zerbe, H., Günther, J., Yang, W., Seyfert, H. M., Nürnberg, G., and Schuberth, H. J. (2008). Escherichia coli, but not Staphylococcus aureus triggers an early increased expression of factors contributing to the innate immune defence in the udder of the cow. Vet. Res. 39, 18.
Escherichia coli, but not Staphylococcus aureus triggers an early increased expression of factors contributing to the innate immune defence in the udder of the cow.Crossref | GoogleScholarGoogle Scholar | 18258172PubMed |

Plöntzke, J., Madoz, L. V., De la Sota, R. L., Drillich, M., and Heuwiesera, W. (2010). Subclinical endometritis and its impact on reproductive performance in grazing dairy cattle in Argentina. Anim. Reprod. Sci. 122, 52–57.
Subclinical endometritis and its impact on reproductive performance in grazing dairy cattle in Argentina.Crossref | GoogleScholarGoogle Scholar | 20727691PubMed |

Raynal, P., and Pollard, H. B. (1994). Annexins: the problem of assessing the biological role for a gene family of multifunctional calcium- and phospholipid-binding proteins. Biochim. Biophys. Acta 1197, 63–93.
Annexins: the problem of assessing the biological role for a gene family of multifunctional calcium- and phospholipid-binding proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXivFahsro%3D&md5=7279eb1b3b000b69612e16bdf6697e75CAS | 8155692PubMed |

Santos, T. M., and Bicalho, R. C. (2012). Diversity and succession of bacterial communities in the uterine fluid of postpartum metritic, endometritic and healthy dairy cows. PLoS ONE 7, e53048.
Diversity and succession of bacterial communities in the uterine fluid of postpartum metritic, endometritic and healthy dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXotVahsw%3D%3D&md5=eb2441531d547e12e4111f6588b09a5bCAS | 23300859PubMed |

Schukken, Y. H., Günther, J., Fitzpatrick, J., Fontaine, M. C., Goetze, L., Holst, O., Leigh, J., Petzl, W., Schuberth, H. J., Sipka, A., Smith, D. G., Quesnell, R., Watts, J., Yancey, R., Zerbe, H., Gurjar, A., Zadoks, R. N., and Seyfert, H. M. (2011). Host-response patterns of intramammary infections in dairy cows. Vet. Immunol. Immunopathol. 144, 270–289.
Host-response patterns of intramammary infections in dairy cows.Crossref | GoogleScholarGoogle Scholar | 21955443PubMed |

Sheldon, I. M., and Dobson, H. (2004). Postpartum uterine health in cattle. Anim. Reprod. Sci. 82–83, 295–306.
Postpartum uterine health in cattle.Crossref | GoogleScholarGoogle Scholar | 15271461PubMed |

Sheldon, I. M., Lewis, G. S., LeBlanc, S., and Gilbert, R. O. (2006). Defining postpartum uterine disease in cattle. Theriogenology 65, 1516–1530.
Defining postpartum uterine disease in cattle.Crossref | GoogleScholarGoogle Scholar | 16226305PubMed |

Sheldon, I. M., Cronin, J., Goetze, L., Donofrio, G., and Schuberth, H. J. (2009). Defining postpartum uterine disease and the mechanisms of infection and immunity in the female reproductive tract in cattle. Biol. Reprod. 81, 1025–1032.
Defining postpartum uterine disease and the mechanisms of infection and immunity in the female reproductive tract in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsV2lt7vP&md5=1eb97bfdce6227dfbb27d396ccc1f21eCAS | 19439727PubMed |

Smolenski, G. A., Wieliczko, R. J., Pryor, S. M., Broadhurst, M. K., Wheeler, T. T., and Haigh, B. J. (2011). The abundance of milk cathelicidin proteins during bovine mastitis. Vet. Immunol. Immunopathol. 143, 125–130.
The abundance of milk cathelicidin proteins during bovine mastitis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpvFymurg%3D&md5=82390d763309ab1f2f06aae76005f2e8CAS | 21774993PubMed |

Snell, K. (1984). Enzymes of serine metabolism in normal, developing and neoplastic rat tissues. Adv. Enzyme Regul. 22, 325–400.
Enzymes of serine metabolism in normal, developing and neoplastic rat tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXkt1WgtLw%3D&md5=0cc8eb9c221340df4c3e3446b363c7a3CAS | 1:CAS:528:DyaL2cXkt1WgtLw%3D&md5=0cc8eb9c221340df4c3e3446b363c7a3CAS | 6089514PubMed |

Spellerberg, B. (2000). Pathogenesis of neonatal Streptoccoccus agalactiae infections. Microbes Infect. 2, 1733–1742.
Pathogenesis of neonatal Streptoccoccus agalactiae infections.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M7itFantQ%3D%3D&md5=1a07b84b1c4b46497356d404407243dfCAS | 11137046PubMed |

Subramaniam, R., Dassanayake, R. P., Norimine, J., Brown, W. C., Knowles, D. P., and Srikumaran, S. (2010). Molecular cloning, characterisation and in vitro expression of SERPIN B1 of bighorn sheep (Ovis canadensis) and domestic sheep (Ovis aries) and comparison with that of other species. Vet. Immunol. Immunopathol. 137, 327–331.
Molecular cloning, characterisation and in vitro expression of SERPIN B1 of bighorn sheep (Ovis canadensis) and domestic sheep (Ovis aries) and comparison with that of other species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFWqu73E&md5=80fe2fced109463c190cbacc69fd7c70CAS | 1:CAS:528:DC%2BC3cXhtFWqu73E&md5=80fe2fced109463c190cbacc69fd7c70CAS | 20591503PubMed |

Swangchan-Uthai, T., Chen, Q., Kirton, S. E., Fenwick, M. A., Cheng, Z., Patton, J., Fouladi-Nashta, A. A., and Wathes, D. C. (2013). Influence of energy balance on the antimicrobial peptides S100A8 and S100A9 in the endometrium of the post-partum dairy cow. Reproduction 145, 527–539.
Influence of energy balance on the antimicrobial peptides S100A8 and S100A9 in the endometrium of the post-partum dairy cow.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXpsVejsb0%3D&md5=cb47252e08b5cd939c696aa985bc2e0eCAS | 23533291PubMed |

Tomasinsig, L., and Zanetti, M. (2005). The cathelicidins – structure, function and evolution. Curr. Protein Pept. Sci. 6, 23–34.
The cathelicidins – structure, function and evolution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhsVWqtLg%3D&md5=39b2430430dd0b63c0e5f75500dff937CAS | 15638766PubMed |

Walter, M., Berg, H., Leidenberger, F. A., Schweppe, K.-W., and Northemann, W. (1995). Autoreactive epitopes within the human a-enolase and their recognition by sera from patients with endometriosis. J. Autoimmun. 8, 931–945.
Autoreactive epitopes within the human a-enolase and their recognition by sera from patients with endometriosis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK28vit1Squw%3D%3D&md5=f42c995a33255fb38a9b1ebaed0fcc09CAS | 8824716PubMed |

Wang, M., Liu, L. H., Wang, S., Li, X., Lu, X., Gupta, D., and Dziarski, R. (2007). Human peptidoglycan recognition proteins require zinc to kill both gram-positive and gram-negative bacteria and are synergistic with antibacterial peptides. J. Immunol. 178, 3116–3125.
| 1:CAS:528:DC%2BD2sXhvFSit78%3D&md5=19430cbc0545e103b449d136d3eff958CAS |
| 1:CAS:528:DC%2BD2sXhvFSit78%3D&md5=19430cbc0545e103b449d136d3eff958CAS | 17312159PubMed |

Williams, E. J., Fischer, D. P., Pfeiffer, D. U., England, G. C., Noakes, D. E., Dobson, H., and Sheldon, I. M. (2005). Clinical evaluation of postpartum vaginal mucus reflects uterine bacterial infection and the immune response in cattle. Theriogenology 63, 102–117.
Clinical evaluation of postpartum vaginal mucus reflects uterine bacterial infection and the immune response in cattle.Crossref | GoogleScholarGoogle Scholar | 15589277PubMed |

Yassin, A. F., Hupfer, H., Siering, C., and Schumann, P. (2011). Comparative chemotaxonomic and phylogenetic studies on the genus Arcanobacterium Collins et al. 1982 emend. Lehnen et al. 2006: proposal for Trueperella gen. nov. and emended description of the genus Arcanobacterium. Int. J. Syst. Evol. Microbiol. 61, 1265–1274.
Comparative chemotaxonomic and phylogenetic studies on the genus Arcanobacterium Collins et al. 1982 emend. Lehnen et al. 2006: proposal for Trueperella gen. nov. and emended description of the genus Arcanobacterium.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MrnvVemtg%3D%3D&md5=268fb34755e86d0620c8e661c81d1390CAS | 1:STN:280:DC%2BC3MrnvVemtg%3D%3D&md5=268fb34755e86d0620c8e661c81d1390CAS | 20622055PubMed |