Effects of Escherichia coli- and Staphylococcus aureus-induced mastitis in lactating cows(13)

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SAsafandothers

AControl

G+

G–

1.5e

gna1.0hc dlo0.5F0

B3.5e

3.0gn2.5ah2.0c d1.5loF1.00.50

Figure7Effectofinducedmastitisongeneexpression.MIIstage

oocyteswerecollectedattheendof22-hmaturation(A)andfour-cellstageembryoswerecollected42hpostfertilization(B).PresentedarerelativetranscriptlevelsofPTGS2,HSF1,POU5F1,GDF9,and

SLC2A1.Quanti cationrelativetoYWHAZispresentedasmeansGS.E.M.;differentlettersindicatetreatmenteffectwithinaspeci cgene,P!0.05.Theexaminationincluded100oocytesand50embryospergroupfrom vedifferentruns.

meiosisandreachedtheMIIstage(i.e.nuclearmaturation)waslowerintheGKgroup.Similarly,theproportionofoocytesde nedaccordingtotheircorticalgranuledistributionasclassI(i.e.cytoplasmicmatu-ration)wasalsoaffectedintheGKgroupcomparedwiththecontrolgroup.Ontheotherhand,GCmastitisdidnotaffecteithernuclearorcytoplasmicmaturationbutloweredthecleavagerate.These ndingssuggestthatdifferentmechanismsforeachtypeoftoxin,resultingindifferentialeffectsonoocytematuration,couldberelatedtothedegreeofthein ammatoryresponse,rgerinthemastiticgroupinducedbyGKtoxinthaninthatinducedbyGCtoxin.

Withrespecttooocytedevelopmentalcompetence,maturationinFFobtainedfrombothmastiticgroups(inducedbyGKandGC)reducedtheproportionofoocytesthatfertilizedandcleavedtotwo-andfour-cellstageembryos.Moreover,bothtypesofbacteriadeleteriouslyaffectedtheproportionofembryosthatdevelopedtotheblastocyststage,withaprominenteffectintheGKmastiticgroup.BecauseinthecurrentstudyoocyteswerematuredinFFaspiratedfrommastiticcows,thedeleteriouseffectonoocytedevelopmentalcompetenceshouldbeconsideredadirecteffectonthepreovulatoryenclosedoocytethatiscarriedovertotheblastocyststage.Suchalterationsmightexplain,inpart,thereducedfertilityinmastiticcows(Lavonetal.2011b).Anepidemiologicalstudy(Lavonetal.2011b)showedalong-termeffectofE.coli-inducedmastitisonconceptionrate.Inparticular,apastclinicaleventoccurringupto10dayspriortoAIsigni cantlyreducedtheprobabilityofconception.Furthermore,wehave

Reproduction(2014)14733–43

recentlyshownthatE.colimastitisoccurringduringa90-dayperiodpriortoperformingIVM/IVFdisruptstheovarianpoolofGVstageoocytes,resultinginadecreaseinblastocystformationrate(Rothetal.2013).Takentogether,the ndingssupporttheviewthatnotonlythedevelopingembryobutalsotheoocyteishighlysusceptibletopathogenic(mastitis)stress.

Giventheprominenteffectonoocytematurationandthelong-lastingeffectonembryonicdevelopment,onemightexpectthatblastocystsdevelopedfromoocytesmaturedinFFaspiratedfrommastiticcowswillbeofinferiorquality.However,the ndingsarecomplexandnotentirelyclear.Whilethetotalcellcountfortheblastocystsdidnotdifferbetweengroups,theapoptoticcellcountwashigherintheGCbutnotintheGKgrouprelativetocontrols.Modestapoptosisisessentialforembryonicsurvival(Paula-Lopes&Hansen2002),whereasahighlevelofapoptoticblastomeresmightdecreasetheinnercellmass,reduceembryonicsurvival,andincreaseembryonicdeath(Pampferetal.1994,Wuuetal.1999).Thisphenomenonhasbeenwelldocumen-tedforpreimplantationembryosexposedtothermalstress(Paula-Lopes&Hansen2002).Nevertheless,inthecurrentstudy,neitheroocytesnorembryoswereexposedtohyperthermiaandthetransienthyperthermiadevelopedinvivointheGKtreatedcowshasnothingtodowithoocytesmaturedinGKFF.Ontheotherhand,astheoocyteswerematuredinFF,itispossiblethatimmune-activatedfactorspassviathecirculationintotheFFandinturnimpairoocytedevelopmentalcompetence.Supportingthisassumptionarereportsthatmastitisimpairstheconcentrationsofin ammationmediatorssuchasIL6,TNFa,andNOinmilkandblood(Nakajimaetal.1997,Blumetal.2000,Hisaedaetal.2001).Althoughnotexaminedinthecurrentstudy,anincreaseinin ammationmediatorsmightalsobeexpressedintheFF.Previousstudieshavereportedanincreaseinthein ammatorycomponentintheplasmawithin6–12hofmastitisinduction(Mehrzadetal.2007).Inthecurrentstudy,maturationinFFaspirated6hafterinductionofmastitisimpairedoocytedevelop-mentalcompetence,whichmightsupportthisassump-tion.Itisalsopossiblethatmastitisinducedchangesinthehypothalamus–pituitary–ovarianaxismightaffectsteroidconcentrationinthepreovulatoryfollicle(Lavonetal.2011b),whichinturnmightaffecttheoocytemicroenvironment.

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