Effects of Escherichia coli- and Staphylococcus aureus-induced mastitis in lactating cows

REPRODUCTION

RESEARCH

EffectsofEscherichiacoli-andStaphylococcusaureus-inducedmastitisinlactatingcowsonoocytedevelopmentalcompetence

SAsaf,GLeitner1,OFurman,YLavon,DKalo,DWolfensonandZRoth

DepartmentofAnimalSciences,FacultyofAgriculture,FoodandEnvironment,theHebrewUniversity,Rehovot76100,Israeland1MastitisLaboratory,TheVeterinaryInstitute,BetDagan50250,Israel

CorrespondenceshouldbeaddressedtoZRoth;Email:roth@agri.huji.ac.il

Abstract

Mastitisisassociatedwithdecreasedfertilityindairycows.Inthecurrentstudy,wecreatedanexperimentalmodeltosimulateshort-termmastitisbyasingleintramammaryadministrationofGram-negativeendotoxinofEscherichiacoliorigin(GK),orGram-positivetoxinofStaphylococcusaureusorigin(GC),toexaminetheeffectofmastitisonoocytedevelopmentalcompetence.HealthyHolsteincowsweresynchronized,andfollicular uid(FF)ofcowstreatedwithGCorGKandofuninfectedcows(controls)wasaspiratedfromthepreovulatoryfolliclesbytransvaginalultrasoundprocedure.TheaspiratedFFwasusedasmaturationmediumforinvitro

embryoproduction.ThedistributionofmaturedoocytesintodifferentcorticalgranuleclassesandmeioticstageswasaffectedbyGKadministration(P!0.05)butnotbyGCadministration.Theproportionofoocytesthatcleavedtotwo-andfour-cellstageembryos(44hpostfertilization)waslowerinbothGCandGKgroupsthanincontrols(P!0.05).Blastocystformationrate(7–8dayspostfertilization)waslowerintheGKgroup(P!0.05)andnumericallylowerintheGCgroupcomparedwiththeiruninfectedcounterparts.The

totalcellnumberinblastocystsdidnotdifferamonggroups;however,theapoptoticindexwashigherintheGCgroup(P!0.05),butnotintheGKgroup,relativetocontrols.ExaminingmRNArelativeabundanceinoocytesandearlyembryosrevealedmastitis-inducedalterationsinPTGS2(COX2),POU5F1,andHSF1butnotinSLC2A1(GLUT1)orGDF9.ResultsindicateadifferentialdisruptiveeffectofmastitisinducedbyGKandGConoocytedevelopmentalcompetenceinassociationwithalterationsinmaternalgeneexpression.

Reproduction(2014)14733–43

Introduction

Mastitisisoneofthemajordiseasesaffectingdairycattleworldwide.Itcauseslargeeconomiclossestothedairyindustry,duetobothlossofmilkproductionandlowmilkquality.Mastitisalsohasdeleteriouseffectsonreproductiveperformance.Forinstance,thetimefromparturitionto rstinseminationislongerandthenumberofservicesforconceptionislargerinmastiticcows(Schricketal.2001,Maizonetal.2004,Lavonetal.2011a).Otherepidemiologicalstudieshavedemonstratedthatconceptionrates(Loef eretal.1999,Santosetal.2004)andpregnancyrates(Harmanetal.1996)arelowerinmastiticvshealthycows.

Oocytedevelopmentalcompetenceisacquiredinaprogressivemannerthroughoutfolliculardevelopmentandincludesavarietyofmolecularandcellularmodi cationsthatarerequiredfortheoocytetocompletemeiosis,successfulfertilization,maternalzygotetransition,andfurtherpre-andpostimplantationdevelopment(Coticchioetal.2004).Theovarianfollicular uid(FF)inwhichtheoocyteisenclosedanddevelopedisofplasmaorigin(Edwards1974).Thus,itisreasonabletoassumethatelevationofbiomoleculesin

q2014SocietyforReproductionandFertilityISSN1470–1626(paper)1741–7899(online)

theplasmauponphysiologicaland/orpathologicalimpairments,suchasmastitis,mightaffectFFcompo-sitionandthefollicle-enclosedoocyte.Insupportofthis,Nakajimaetal.(1997)reportedthepresenceoftumornecrosisfactora(TNFa)andinterleukin6(IL6)inthemilkandserumofcowswithnaturallyoccurringcoliformmastitis.Blumetal.(2000)reportedanincreaseinTNFaandNOx(nitriteandnitrate)inthemilkandplasmauponEscherichiacoli-inducedmastitis.Hisaedaetal.(2001)detectedinterferon-gandTNFainserumandwheysamplesfromnaturallyoccurringcoliformmastitis.Supplementationoflipopolysaccharide(LPS),prostaglandinF2a(PGF2a),nitricoxide(NO)generator,orsodiumnitroprussidetothematurationorculturemediumdeleteriouslyaffectedthedevelopmentalcom-petenceofbovineoocytes(Sotoetal.2003a).ExposingbovineembryostoTNFaincreasedtheproportionofapoptoticblastomeresinthedevelopedblastocyst(Sotoetal.2003b).Inaddition,TNFadecreasesthenumberofcellsintheinnercellmassinmouseembryosandlowersembryonicsurvival(Pampferetal.1994,Wuuetal.1999).Nevertheless,theconcentrationofin ammatorymediatorsintheFFofthepreovulatoryfolliclehasneverbeenexamined.Here,wehypothesizedthat

DOI:10.1530/REP-13-0383

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