Reproduction in Domestic Animals

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236 MA Hayes, BA Quinn, ND Keirstead, P Katavolos, RO Waelchli and KJ Betteridgecomparison, we used an experimental model of PGF 2a -induced luteolysis that leads to failure of fixation anddelayed loss of sialic acid from the embryonic capsule(Chu et al. 1997; Betteridge et al. 2006). These studiesfollow on from a previous demonstration that b 2 Massociated with the normal capsule is truncated to an8 kDa form (D9-b 2 M) around the time of fixation (Quinnet al. 2007). The present studies show that b 2 M exists asmultiple 10 kDa forms and one 8 kDa form that can beseparated by 2D-PAGE, and that luteolysis has only aminor influence on proteolysis or binding of b 2 M associatedwith the capsule.The most obvious luteolysis-associated alteration incapsule proteins was an increase in a 17 kDa secretoryphospholipase A2 (sPLA2) classified as type IIA on thebasis of amino acid and cDNA sequence homology of thecDNA sequence we obtained from pregnant endometrium.Previous reports have noted the presence of apartially characterized PLA2 in the normal pregnantuterus (Beier-Hellwig et al. 1995; Quinn et al. 2007) butits function there is unknown. PLA2s are a complexgroups of enzymes that cleave glycerophospholipids atthe sn-2 position and release a free fatty acid, most oftenarachidonic acid which is the cyclooxygenase substrateprecursor of various eicosanoids. PLA2s can thereby havediverse signalling roles that are especially important ininflammation and haemostasis, and in the regulation ofovarian function, pregnancy and parturition (Tithof et al.2007). Secretory PLA2-IIA has a high pI and binds toanionic phospholipid interface rather than phospholipidsin intact cell membranes (Beers et al. 2003; Birts et al.2007). Human sPLA2-IIA also has an ability to bind toheparin-sulphate proteoglycans (Birts et al. 2007). Whilethe functions of sPLA2-IIA are still unclear, the evidencesupports the view that they relate to its role as an innateimmune protein involved in the catabolism of cell debris(bacteria, apoptotic cells) in extracellular locations (Birtset al. 2007). Equine uterine sPLA2 characterized in ourstudies also has a high pI of 9.8, binds to the embryoniccapsule and increases when fixation has been blocked byadministration of PGF 2a . It is therefore plausible thatsPLA2 contributes to the imminent removal and degradationof the capsule or the conceptus.Uterocalin is a well characterized lipocalin secreted byendometrial glands in the luteal stage of the ovariancycle and in the early stages of normal pregnancy inequids (Stewart et al. 2000; Suire et al. 2001; Kennedy2005). Uterocalin is also a highly cationic protein(pI 9.4 similar to that of sPLA2) (Fig. 2) and thisproperty likely explains why it also binds to theembryonic capsule. Recent evidence suggests that uterocalinis involved in the transport of small lipophilic,mainly nutrient, substances across the glycan capsuleand into the yolk sac (Suire et al. 2001; Kennedy 2005;Quinn et al. 2007). Amounts in the uterine flush werelower after treatment with PGF 2a , consistent withprogesterone dependence (Suire et al. 2001). Theamounts present in the capsule were variable and bydays 16 and 18, some had been proteolytically convertedto smaller fragments of approximately 10 kDa (Fig. 2b).It appears likely that this alteration is part of the processof degradation of the capsule rather than a processrelevant to its function.Observations in the present study indicate that thereare at least two uteroglobin genes expressed in theequine uterus during early pregnancy. The form thatwas more consistent immunoreactively with equineuteroglobin (Mu¨ller-Scho¨ttle et al. 2002) was increasedsubstantially after luteolysis. Uteroglobin was firstidentified as a low molecular weight secreted uterineprotein in rabbits and is the founding member of thelarge secretoglobin superfamily of proteins that alsoincludes Clara cell secretory proteins (CCSP) (Beier2000; Mu¨ller-Scho¨ttle et al. 2002; Mukherjee et al.2007). These proteins are expressed in various tissues,mainly in the lung and uterus. Uteroglobin (secretoglobin1A1) is expressed in various mammals including thehorse (Mu¨ller-Scho¨ttle et al. 2002) and there are threeclosely similar genes in the horse genome, located onchromosome 12. Previous studies showed that theuteroglobin that is detected in immunoblots with anantibody to a peptide sequence of uteroglobin ⁄ secretoglobin1A1 is more abundant in the non-pregnant uterusthan during the fixation period of normal pregnancy(Quinn et al. 2007). Uteroglobin has a small lipophilicbinding pocket (von der Decken et al. 2005) and canbind prostaglandins such as PGF 2a (Mukherjee et al.2007) but the significance of these properties is unclear.Secretoglobins can bind various small lipophilic moleculesincluding retinoids and polychlorinated biphenyls(von der Decken et al. 2005; Mukherjee et al. 2007).CCSP has anti-inflammatory functions in the respiratorytract, where it might bind lipid mediators andsPLA2 (Mukherjee et al. 2007). Further studies arerequired to determine whether there is a relationshipbetween the increases in sPLA2 and uteroglobin inresponse to luteolysis.These studies have employed analytical methods witha level of sensitivity most suitable for demonstration ofchanges in the most abundant proteins. It is expectedthat there are also alterations in many cytokines andenzymes that are not apparent in these approaches.Moreover, it is still unclear whether the modifications inproteins and glycans that can be observed in the capsuleduring and after the period of fixation are functionallyimportant in interactions between the endometrium andconceptus. Some of these changes might be part of thenormal removal of the capsule. However, the increase insPLA2-type IIA in the capsule and a change in theexpression of uteroglobin genes might have a role in thepending demise of the conceptus in some circumstances.Alternatively, these changes might reflect the return tothe non-pregnant post-luteolysis condition.AcknowledgementsThis research was supported by the Natural Sciences and EngineeringResearch Council of Canada (NSERC); the Grayson Jockey ClubResearch Foundation Inc.; Equine Guelph; The E.P. Taylor researchFoundation; and the Ontario Ministry of Agriculture, Food and RuralAffairs (OMAFRA). Natalie Keirstead was supported by a Fellowshipfrom the Canadian Institutes of Health Research (CIHR). We thankDorothee Bienzle, Jeff Caswell, Gordon Kirby and John Lumsden foruse of analytical equipment funded by the Canadian Foundation forInnovation (CFI). We are grateful for technical advice of DavidHobson and Paul Huber in relation to DIGE methods, and for MSanalysis by Li Zhang at the Advanced Protein Technology Centre,Ó 2008 The Authors. Journal compilation Ó 2008 Blackwell Verlag
Proteins in Early Equine Conceptuses 237Hospital for Sick Children, Toronto, Ontario. The assistance of CaraLategan, Mandy Mulder and Garrett Jack and staff of the ArkellResearch Station is appreciated.ReferencesAlbihn A, Waelchli RO, Samper J, Oriol JG, Croy BA,Betteridge KJ, 2003: Production of capsular material byequine trophoblast transplanted into immunodeficient mice.Reproduction 125, 855–863.Arar S, Chan KH, Quinn BA, Waelchli RO, Hayes MA,Betteridge KJ, Monteiro MA, 2007: Desialylation of coretype 1 O-glycan in the equine embryonic capsule coincideswith immobilization of the conceptus in the uterus. CarbohydrRes 342, 1110–1115.Baker CB, Little TV, McDowell KJ, 1993: The live foaling rateper cycle in mares. Equine Vet J 15, 28–30.Ball BA, 1988: Embryonic loss in mares: incidence, possiblecauses and diagnostic considerations. Vet Clinics N AmEquine Pract 4, 263–290.Beers SA, Buckland AG, Giles N, Gelb MH, Wilton DC,2003: Effect of tryptophan insertions on the properties of thehuman group IIA phospholipase A2: mutagenesis producesan enzyme with characteristics similar to those of the humangroup V phospholipase A2. Biochemistry 42, 7326–7338.Beier HM, 2000: The discovery of uteroglobin and itssignificance for reproductive biology and endocrinology.Ann N Y Acad Sci 923, 9–24.Beier-Hellwig K, Kremer H, Bonn B, Lindner D, Beier HM,1995: Partial sequencing and identification of three proteinsfrom equine uterine secretion regulated by progesterone.Reprod Domest Anim 30, 295–298.Betteridge KJ, 2007: Equine embryology: an inventory ofunanswered questions. Theriogenology 68(Suppl 1), S9–S21.Betteridge KJ, Waelchli RO, Christie HL, Raeside JI, QuinnBA, Hayes MA, 2006: Effects of luteolysis on conceptusdevelopment during the second and third weeks of pregnancyin the mare. Anim Reprod Sci 91, 395–398.Birts CN, Barton CH, Wilton DC, 2007: A catalyticallyindependentphysiological function for human acute phaseprotein group IIA phospholipase A2: cellular uptake facilitatescell debris removal. J Biol Chem 283, 5034–5045.Bradford MM, 1976: A rapid and sensitive method for thequantitation of microgram quantities of protein utilizing theprinciple of protein-dye binding. Anal Biochem 72, 248–254.Brooks AS, Hammermueller J, DeLay JP, Hayes MA, 2003:Expression and secretion of ficolin beta by porcine neutrophils.Biochim Biophys Acta 1624, 36–45.Carnevale EM, Ramirez RJ, Squires EL, Alvarenga MA,Vanderwall DK, McCue PM, 2000: Factors affectingpregnancy rates and early embryonic death after equineembryo transfer. Theriogenology 54, 965–979.Chomczynski P, Sacchi N, 1987: Single-step method of RNAisolation by acid guanidinium thiocyanate-phenol-chloroformextraction. Anal Biochem 162, 156–159.Chu JW, Sharom FJ, Oriol JG, Betteridge KJ, Cleaver BD,Sharp DC, 1997: Biochemical changes in the equine capsulefollowing prostaglandin-induced pregnancy failure. MolReprod Dev 46, 286–295.Crossett B, Suire S, Herrler A, Allen WR, Stewart F, 1998:Transfer of a uterine lipocalin from the endometrium of themare to the developing equine conceptus. Biol Reprod 59,483–490.von der Decken V, Delbruck H, Herrler A, Beier HM, FischerR, Hoffmann KM, 2005: Recombinant bovine uteroglobinat 1.6 A resolution: a preliminary X-ray crystallographicanalysis. Acta Crystallogr F 61, 499–502.Ginther OJ, Bergfelt DR, Leith GS, Scraba ST, 1985:Embryonic loss in mares: incidence and ultrasonic morphology.Theriogenology 24, 73–86.Hobson DJ, Rupa P, Diaz GJ, Zhang H, Yang M, Mine Y,Turner PV, Kirby GM, 2007: Proteomic analysis ofovomucoid hypersensitivity in mice by two-dimensionaldifference gel electrophoresis (2D-DIGE). Food ChemToxicol 45, 2372–2380.Katavolos P2006: The role of Clara cells in the pathogenesis ofequine recurrent airway obstruction. PhD Thesis, Universityof Guelph.Kennedy MW, 2005: Uterocalin – provider of essential lipidsand amino acids to the pre-placentation equine conceptus.Havemeyer Found Monogr Ser 16, 53–56.Lillie BN, Hammermueller JD, Macinnes JI, Jacques M,Hayes MA, 2006: Porcine mannan-binding lectin A binds toActinobacillus suis and Haemophilus parasuis. Dev ComImmunol 30, 954–965.Morris LH, Allen WR, 2002: Reproductive efficiency ofintensively managed Thoroughbred mares in Newmarket.Equine Vet J 34, 51–60.Mukherjee AB, Zhang Z, Chilton BS, 2007: Uteroglobin: asteroid-inducible immunomodulatory protein that foundedthe secretoglobin superfamily. Endocr Rev 28, 707–725.Mu¨ller-Scho¨ttle F, Bogusz A, Grotzinger J, Herrler A,Krusche CA, Beier-Hellwig K, Beier HM, 2002: Full-lengthcomplementary DNA and the derived amino acid sequenceof horse uteroglobin. Biol Reprod 66, 1723–1728.Oriol JG, Betteridge KJ, Clarke AJ, Sharom FJ, 1993a:Mucin-like glycoproteins in the equine embryonic capsule.Mol Reprod Dev 34, 255–265.Oriol JG, Sharom FJ, Betteridge KJ, 1993b: Developmentallyregulated changes in the glycoproteins of the equineembryonic capsule. J Reprod Fertil 99, 653–664.Quinn BA, Caswell DE, Lillie BN, Waelchli RO, BetteridgeKJ, Hayes MA, 2006: The GM2-activator protein is a majorprotein expressed by the encapsulated equine trophoblast.Anim Reprod Sci 91, 391–394.Quinn BA, Hayes MA, Waelchli RO, Kennedy MW, BetteridgeKJ, 2007: Changes in major proteins in the embryonic capsuleduring immobilization (fixation) of the conceptus in the thirdweek of pregnancy in the mare. Reproduction 134, 161–170.Stewart F, Kennedy MW, Suire S, 2000: A novel uterinelipocalin supporting pregnancy in equids. Cell Mol Life Sci57, 1373–1378.Stout TA, Meadows S, Allen WR, 2005: Stage-specificformation of the equine blastocyst capsule is instrumentalto hatching and to embryonic survival in vivo. Anim ReprodSci 87, 269–281.Suire S, Stewart F, Beauchamp J, Kennedy MW, 2001:Uterocalin, a lipocalin provisioning the preattachmentequine conceptus: fatty acid and retinol binding properties,and structural characterization. Biochem J 356, 369–376.Tithof PK, Roberts MP, Guan W, Elgayyar M, Godkin JD,2007: Distinct phospholipase A2 enzymes regulate prostaglandinE2 and F2alpha production by bovine endometrialepithelial cells. Reprod Biol Endocrinol 5, 16.Waelchli RO, Betteridge KJ, 1996: Osmolality of equineblastocyst fluid from days 11 to 25 of pregnancy. ReprodFertil Dev 8, 981–988.Author’s address (for correspondence): MA Hayes, Department ofPathobiology, Ontario Veterinary College, University of Guelph,Guelph, Ontario, Canada N1G2W1. E-mail: ahayes@uoguelph.caConflict of interest: MA Hayes declares no conflict of interest; theremaining authors have not declared any conflict of interests.Ó 2008 The Authors. Journal compilation Ó 2008 Blackwell Verlag
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