Abstract
Although similar at the molecular and cellular levels, endocrine mechanisms governing reproductive function in the domestic dog (Canis familiaris) differ markedly at the regulatory level from those known in other domestic animal species. Some of the events, e.g., the lack of luteolysis in the absence of pregnancy, resulting in similar luteal function and, therefore, hormonal profiles in early pregnant and nonpregnant animals, are species-specific. Consequently, no early gestation marker has so far been identified for the dog. Following implantation, relaxin of fetal placental origin can be detected and used for pregnancy diagnosis. Characterized by the lack of an active luteolytic principle from intra- or extra-luteal sources, the canine reproductive cycle appears to represent a “basic” form of mammalian reproductive function with apparently reduced opportunities for facilitating fecundity and hastening reproduction. Nevertheless, in the dog some kind of mechanism for synchronization between blastocyst development and uterine preparation for pregnancy must have evolved in order to support gestation. Driven by this assumption, studies including our recent investigations have been initiated aimed at characterizing some of the embryo-mediated effects of the preimplantation embryo on the canine uterus. Moreover, the lack of a uterine luteolysin and consequently the absence of a need to develop an antiluteolytic strategy make the dog an interesting model for investigating early evolutionary mechanisms involved in the preparation for implantation and ensuring embryo survival. These mechanisms result in an inverse relationship between the duration of pregnancy and of the nonpregnant cycle in the dog, compared with all other domestic animal species.
Dedicated to the memory of Professor Patrick W. Concannon, PhD, a pioneer in the sciences of small animal reproduction
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References
Amoroso EC (1952) Placentation. In: Parkes AS (ed) Marshall’s physiology of reproduction. Longmans Green, London, pp 127–316
Archbald LF, Baker BA, Clooney LL, Godke RA (1980) A surgical method for collecting canine embryos after induction of estrus and ovulation with exogenous gonadotropins. Vet Med Small Anim Clin 75:228–238
Barak Y, Nelson MC, Ong ES et al (1999) PPAR gamma is required for placental, cardiac, and adipose tissue development. Mol Cell 4:585–595
Bazer FW (1989) Establishment of pregnancy in sheep and pigs. Reprod Fetil Dev 1:237–242
Bazer FW, Thatcher WW (1977) Theory of maternal recognition of pregnancy in swine based on estrogen controlled endocrine versus exocrine secretion of prostaglandin F2alpha by the uterine endometrium. Prostaglandins 14:397–400
Bazer FW, Thatcher WW, Hansen PJ, Mirando MA, Ott TL, Plante C (1991) Physiological mechanisms of pregnancy recognition in ruminants. J Reprod Fertil Suppl 43:39–47
Beceriklisoy HB, Walter I, Schafer-Somi S, Miller I, Kanca H, Izgur H, Aslan S (2007) Matrix metalloproteinase (MMP)-2 and MMP-9 activity in the canine uterus before and during placentation. Reprod Domest Anim 42:654–659. doi:10.1111/j.1439-0531.2006.00838.x
Bethea CL, Cronin MJ, Haluska GJ, Novy MJ (1989) The effect of relaxin infusion on prolactin and growth hormone secretion in monkeys. J Clin Endocrinol Metab 69:956–962. doi:10.1210/jcem-69-5-956
Bischoff TLW (1845) Entwicklungsgeschichte des Hunde-Eies. (Eng.: The development of the canine oocyte.). Braunschweig, Druck und Verlag von Friedrich Veweg und Sohn. http://digi.ub.uni-heidelberg.de/diglit/bischoff1845
Brar AK, Frank GR, Kessler CA, Cedars MI, Handwerger S (1997) Progesterone-dependent decidualization of the human endometrium is mediated by cAMP. Endocrine 6:301–307. doi:10.1007/BF02820507
Buhi WC, Thatcher MJ, Shille VM, Alvarez IM, Lannon AP, Johnson J (1992) Synthesis of uterine endometrial proteins during early diestrus in the cyclic and pregnant dog, and after estrogen and progesterone treatment. Biol Reprod 47:326–336
Buhi WC, Shille VM, Thatcher MJ, Alvarez IM, Qiu YX (1993) Identification and immunolocalization of proteins synthesized by dog endometrium and membranes. J Reprod Fertil Suppl 47:141–157
Buhi WC, Alvarez IM, Shille VM, Thatcher MJ, Harney JP, Cotton M (1995) Purification and characterization of a uterine retinol-binding protein in the bitch. Bioch J 311(Pt2):407–415
Bukowska D, Kempisty B, Jackowska M, Wozna M, Antosik P, Piotrowska H, Jaskowski JM (2011) Analysis of integrins and vascular endothelial growth factor isoforms mRNA expression in the canine uterus during perimplantation period. Pol J Vet Sci 14:253–258
Bysted BV, Dieleman SJ, Hyttel P, Greve T (2001) Embryonic developmental stages in relation to the LH peak in dogs. J Reprod Fertil Suppl 57:181–186
Concannon PW (2009) Endocrinologic control of normal canine ovarian function. Reprod Domest Anim Suppl 2:3–15. doi:10.1111/j.1439-0531.2009.01414.x
Concannon PW (2011) Reproductive cycles of the domestic bitch. Anim Reprod Sci 124:200–210. doi:10.1016/j.anireprosci.2010.08.028
Concannon PW (2012) Research challenges in endocrine aspects of canine ovarian cycles. Reprod Domest Anim Suppl 6:6–12. doi:10.1111/rda.12121
Concannon PW, Butler WR, Hansel W, Knight PJ, Hamilton JM (1978) Parturition and lactation in the bitch: serum progesterone, cortisol and prolactin. Biol Reprod 19:1113–1118
Concannon PW, McCann JP, Temple M (1989) Biology and endocrinology of ovulation, pregnancy and parturition in the dog. J Reprod Fertil Suppl 39:3–25
Concannon PW, Gimpel T, Newton L, Castracane VD (1996) Postimplantation increase in plasma fibrinogen concentration with increase in relaxin concentration in pregnant dogs. Am J Vet Res 57:1382–1385
Concannon P, Tsutsui T, Shille V (2001) Embryo development, hormonal requirements and maternal responses during canine pregnancy. J Reprod Fertil Suppl 57:169–179
Dorniak P, Spencer TE (2013) Biological roles of progesterone, prostaglandins, and interferon tau in endometrial function and conceptus elongation in ruminants. Anim Reprod 10:239–251
Eckersall PD, Harvey MJ, Ferguson JM, Renton JP, Nickson DA, Boyd JS (1993) Acute phase proteins in canine pregnancy (Canis familiaris). J Reprod Fertil Suppl 47:159–164
England G, Pacey AA (1998) Transportation and interaction of dog spermatozoa within the repoductive tract of the bitch; comparative aspects. In Linde-Forsberg C (ed) Advances in canine reproduction, Centre for Reproductive Biology Report 3, Uppsala, pp 57–84
Evans JM, Anderton DJ (1992) Pregnancy diagnosis in the bich: the development of test based on the measurement of acute phase proteins in the blood. Annales de Zootechnie 41:397–405
Gram A, Buchler U, Boos A, Hoffmann B, Kowalewski MP (2013) Biosynthesis and degradation of canine placental prostaglandins: prepartum changes in expression and function of prostaglandin F2alpha-synthase (PGFS, AKR1C3) and 15-hydroxyprostaglandin dehydrogenase (HPGD). Biol Reprod 89:2. doi:10.1095/biolreprod.113.109918
Gram A, Boos A, Kowalewski MP (2014a) Uterine and placental expression of canine oxytocin receptor during pregnancy and normal and induced parturition. Reprod Domest Anim Suppl 2:41–49. doi:10.1111/rda.12295
Gram A, Fox B, Buchler U, Boos A, Hoffmann B, Kowalewski MP (2014b) Canine placental prostaglandin E2 synthase: expression, localization, and biological functions in providing substrates for prepartum PGF2alpha synthesis. Biol Reprod 91:154. doi:10.1095/biolreprod.114.122929
Gridelet V, Tsampalas M, Berndt S et al (2013) Evidence for cross-talk between the LH receptor and LH during implantation in mice. Reprod Fertil Dev 25:511–522. doi:10.1071/RD11241
Guo B, Tian Z, Han BC, Zhang XM, Yang ZM, Yue ZP (2009) Expression and hormonal regulation of Hoxa10 in canine uterus during the peri-implantation period. Reprod Domest Anim 44:638–642. doi:10.1111/j.1439-0531.2007.01037.x
Hatoya S, Torii R, Kondo Y et al (2006) Isolation and characterization of embryonic stem-like cells from canine blastocysts. Mol Reprod Dev 73:298–305. doi:10.1002/mrd.20392
Hoffmann B, Hoveler R, Hasan SH, Failing K (1992) Ovarian and pituitary function in dogs after hysterectomy. J Reprod Fertil 96:837–845
Hoffmann B, Hoveler R, Nohr B, Hasan SH (1994) Investigations on hormonal changes around parturition in the dog and the occurrence of pregnancy-specific non conjugated oestrogens. Exp Clin Endocrinol 102:185–189. doi:10.1055/s-0029-1211280
Hoffmann B, Busges F, Baumgartner W (2004a) Immunohistochemical detection of CD4-, CD8- and MHC II-expressing immune cells and endoglin in the canine corpus luteum at different stages of dioestrus. Reprod Domest Anim 39:391–395. doi:10.1111/j.1439-0531.2004.00520.x
Hoffmann B, Busges F, Engel E, Kowalewski MP, Papa P (2004b) Regulation of corpus luteum-function in the bitch. Reprod Domest Anim 39:232–240. doi:10.1111/j.1439-0531.2004.00508.x
Holst PA, Phemister RD (1971) The prenatal development of the dog: preimplantation events. Biol Reprod 5:194–206
Iesaka T, Sato T, Igarashi M (1975) Role of prostaglandin F2alpha in ovulation. Endocrinol Jpn 22:279–285
Irwin JC, de las Fuentes L, Giudice LC (1994) Growth factors and decidualization in vitro. Ann N Y Acad Sci 734:7–18
Jabbour HN, Critchley HO, Boddy SC (1998) Expression of functional prolactin receptors in nonpregnant human endometrium: janus kinase-2, signal transducer and activator of transcription-1 (STAT1), and STAT5 proteins are phosphorylated after stimulation with prolactin. J Clin Endocrinol Metab 83:2545–2553. doi:10.1210/jcem.83.7.4989
Janowski T, Fingerhut J, Kowalewski MP et al (2014) In vivo investigations on luteotropic activity of prostaglandins during early diestrus in nonpregnant bitches. Theriogenology 82:915–920. doi:10.1016/j.theriogenology.2014.07.005
Kautz E, Gram A, Aslan S et al (2014) Expression of genes involved in the embryo-maternal interaction in the early-pregnant canine uterus. Reproduction 147:703–717. doi:10.1530/REP-13-0648
Kehrer A (1973) Zur Entwicklung und Ausbildung des Chorions der Placenta zonaria bei Katze, Hund und Fuchs. Z Anat Entwicklungsgesch 143:24–42
Kennedy TG, Doktorcik PE (1988) Effects of analogues of prostaglandin E2 and F2 alpha on the decidual cell reaction in the rat. Prostaglandins 35:207–219
Klonisch T, Hombach-Klonisch S, Froehlich C, Kauffold J, Steger K, Steinetz BG, Fischer B (1999) Canine preprorelaxin: nucleic acid sequence and localization within the canine placenta. Biol Rreprod 60:551–557
Komar CM (2005) Peroxisome proliferator-activated receptors (PPARs) and ovarian function-implications for regulating steroidogenesis, differentiation, and tissue remodeling. Reprod Biol Endocrinol 3:41. doi:10.1186/1477-7827-3-41
Kowalewski MP (2012) Endocrine and molecular control of luteal and placental function in dogs: a review. Reprod Domest Anim Suppl 6:19–24. doi:10.1111/rda.12036
Kowalewski MP (2014) Luteal regression vs. prepartum luteolysis: regulatory mechanisms governing canine corpus luteum function. Reprod Biol 14:89–102. doi:10.1016/j.repbio.2013.11.004
Kowalewski MP, Hoffmann B (2008) Molecular cloning and expression of StAR protein in the canine corpus luteum during dioestrus. Exp Clin Endocrinol Diabetes 116:158–161. doi:10.1055/s-2007-992121
Kowalewski MP, Mason JI, Howie AF, Morley SD, Schuler G, Hoffmann B (2006a) Characterization of the canine 3beta-hydroxysteroid dehydrogenase and its expression in the corpus luteum during diestrus. J Steroid Biochem Mol Biol 101:254–262. doi:10.1016/j.jsbmb.2006.06.029
Kowalewski MP, Schuler G, Taubert A, Engel E, Hoffmann B (2006b) Expression of cyclooxygenase 1 and 2 in the canine corpus luteum during diestrus. Theriogenology 66:1423–1430. doi:10.1016/j.theriogenology.2006.01.039
Kowalewski MP, Mutembei HM, Hoffmann B (2008a) Canine prostaglandin E2 synthase (PGES) and its receptors (EP2 and EP4): expression in the corpus luteum during dioestrus. Anim Reprod Sci 109:319–329. doi:10.1016/j.anireprosci.2007.11.023
Kowalewski MP, Mutembei HM, Hoffmann B (2008b) Canine prostaglandin F2alpha receptor (FP) and prostaglandin F2alpha synthase (PGFS): molecular cloning and expression in the corpus luteum. Anim Reprod Sci 107:161–175. doi:10.1016/j.anireprosci.2007.06.026
Kowalewski MP, Beceriklisoy HB, Aslan S, Agaoglu AR, Hoffmann B (2009) Time related changes in luteal prostaglandin synthesis and steroidogenic capacity during pregnancy, normal and antiprogestin induced luteolysis in the bitch. Anim Rreprod Sci 116:129–138. doi:10.1016/j.anireprosci.2008.12.011
Kowalewski MP, Beceriklisoy HB, Pfarrer C, Aslan S, Kindahl H, Kucukaslan I, Hoffmann B (2010) Canine placenta: a source of prepartal prostaglandins during normal and antiprogestin-induced parturition. Reproduction 139:655–664. doi:10.1530/REP-09-0140
Kowalewski MP, Meyer A, Hoffmann B, Aslan S, Boos A (2011a) Expression and functional implications of peroxisome proliferator-activated receptor gamma (PPARgamma) in canine reproductive tissues during normal pregnancy and parturition and at antiprogestin induced abortion. Theriogenology 75:877–886. doi:10.1016/j.theriogenology.2010.10.030
Kowalewski MP, Michel E, Gram A et al (2011b) Luteal and placental function in the bitch: spatio-temporal changes in prolactin receptor (PRLr) expression at dioestrus, pregnancy and normal and induced parturition. Reprod Biol Endocrinol 9:109. doi:10.1186/1477-7827-9-109
Kowalewski MP, Fox B, Gram A, Boos A, Reichler I (2013) Prostaglandin E2 functions as a luteotrophic factor in the dog. Reproduction 145:213–226. doi:10.1530/REP-12-0419
Kowalewski MP, Ihle S, Siemieniuch MJ et al (2014a) Formation of the early canine CL and the role of prostaglandin E2 (PGE2) in regulation of its function: An in vivo approach. Theriogenology doi: 86(6):1038–1047. doi:10.1016/j.theriogenology.2014.12.006
Kowalewski MP, Kautz E, Hogger E, Hoffmann B, Boos A (2014b) Interplacental uterine expression of genes involved in prostaglandin synthesis during canine pregnancy and at induced prepartum luteolysis/abortion. Reprod Biol Endocrinol 12:46. doi:10.1186/1477-7827-12-46
Lessey BA, Castelbaum AJ, Sawin SW, Sun J (1995) Integrins as markers of uterine receptivity in women with primary unexplained infertility. Fertil Steril 63:535–542
Li Y, Huang C, Klindt J, Anderson LL (1993) Stimulation of prolactin secretion in the pig: central effects of relaxin and the antiprogesterone RU 486. Endocrinology 133:1205–1212. doi:10.1210/endo.133.3.8365362
Liu WM, Pang RT, Cheong AW, Ng EH, Lao K, Lee KF, Yeung WS (2012) Involvement of microRNA lethal-7a in the regulation of embryo implantation in mice. PLoS One 7:e37039. doi:10.1371/journal.pone.0037039
Lonergan P (2011) Influence of progesterone on oocyte quality and embryo development in cows. Theriogenology 76:1594–1601. doi:10.1016/j.theriogenology.2011.06.012
Luz MR, Cesario MD, Binelli M, Lopes MD (2006) Canine corpus luteum regression: apoptosis and caspase-3 activity. Theriogenology 66:1448–1453. doi:10.1016/j.theriogenology.2006.02.025
Mann GE, Lamming GE (2001) Relationship between maternal endocrine environment, early embryo development and inhibition of the luteolytic mechanism in cows. Reproduction 121:175–180
Nishiyama T, Tsumagari S, Ito M, Kimura J, Watanabe G, Taya K, Takeishi M (1999) Immunohistochemical study of steroidogenic enzymes in the ovary and placenta during pregnancy in the dog. Anat Histol Embryol 28:125–129
Nohr B, Hoffmann B, Steinetz BE (1993) Investigation of the endocrine control of parturition in the dog by application of an antigestagen. J Reprod Fertil Suppl 47:542–543
Okkens AC, Kooistra HS (2006) Anoestrus in the dog: a fascinating story. Reprod Domest Anim = Zuchthygiene 41:291–296. doi:10.1111/j.1439-0531.2006.00702.x
Onclin K, Murphy B, Verstegen JP (2002) Comparisons of estradiol, LH and FSH patterns in pregnant and nonpregnant beagle bitches. Theriogenology 57:1957–1972
Pacey AA, Freeman SL, England GC (2000) Contact of dog spermatozoa with homologous uterine tube epithelium prolongs flagellar activity in relation to the stage of the estrous cycle. Theriogenology 54:109–118 doi:10.1016/S0093-691X(00)00329-0
Papa PC, Hoffmann B (2011) The corpus luteum of the dog: source and target of steroid hormones? Reprod Domest Anim 46:750–756. doi:10.1111/j.1439-0531.2010.01749.x
Papa P, Sousa LM, Silva Rdos S et al (2014) Glucose transporter 1 expression accompanies hypoxia sensing in the cyclic canine corpus luteum. Reproduction 147:81–89. doi:10.1530/REP-13-0398
Parhar RS, Yagel S, Lala PK (1989) PGE2-mediated immunosuppression by first trimester human decidual cells blocks activation of maternal leukocytes in the decidua with potential anti-trophoblast activity. Cell Immunol 120:61–74
Patel FA, Clifton VL, Chwalisz K, Challis JR (1999) Steroid regulation of prostaglandin dehydrogenase activity and expression in human term placenta and chorio-decidua in relation to labor. J Clin Endocrinol Metab 84:291–299. doi:10.1210/jcem.84.1.5399
Prigent-Tessier A, Tessier C, Hirosawa-Takamori M, Boyer C, Ferguson-Gottschall S, Gibori G (1999) Rat decidual prolactin. Identification, molecular cloning, and characterization. J Biol Chem 274:37982–37989
Ramathal CY, Bagchi IC, Taylor RN, Bagchi MK (2010) Endometrial decidualization: of mice and men. Semin Reprod Med 28:17–26. doi:10.1055/s-0029-1242989
Renton JP, Boyd JS, Eckersall PD, Ferguson JM, Harvey MJ, Mullaney J, Perry B (1991) Ovulation, fertilization and early embryonic development in the bitch (Canis familiaris). J Reprod Fertil 93:221–231
Rijsselaere T, England G, Freeman S, Maes D, Van Soom A (2014) Current knowledge on the transport and fate of spermatozoa in the reproductive tract of the bitch. Reprod Domest Anim Suppl 2:2–7. doi:10.1111/rda.12299
Schafer-Somi S, Ali Aksoy O, Patzl M et al (2005) The activity of matrix metalloproteinase-2 and −9 in serum of pregnant and non-pregnant bitches. Reprod Domest Anim 40:46–50. doi:10.1111/j.1439-0531.2004.00552.x
Schafer-Somi S, Beceriklisoy HB, Budik S et al (2008) Expression of genes in the canine pre-implantation uterus and embryo: implications for an active role of the embryo before and during invasion. Reprod Domest Anim 43:656–663. doi:10.1111/j.1439-0531.2007.00966.x
Schafer-Somi S, Beceriklisoy HB, Walter I et al (2009a) Expression of MHC-I and -II in uterine tissue from early pregnant bitches. Reprod Domest Anim Supp 2:103–108. doi:10.1111/j.1439-0531.2009.01444.x
Schafer-Somi S, Klein D, Beceriklisoy HB et al (2009b) Uterine progesterone receptor and leukaemia inhibitory factor mRNA expression in canine pregnancy. Reprod Domest Suppl 2:109–114. doi:10.1111/j.1439-0531.2009.01390.x
Schafer-Somi S, Sabitzer S, Klein D et al (2012) Is apoptosis a regulatory mechanism during early canine pregnancy? Reprod Domest Anim Suppl 6:169–172. doi:10.1111/rda.12063
Schafer-Somi S, Sabitzer S, Klein D et al (2013) Vascular endothelial (VEGF) and epithelial growth factor (EGF) as well as platelet-activating factor (PAF) and receptors are expressed in the early pregnant canine uterus. Reprod Domest Anim 48:20–26. doi:10.1111/j.1439-0531.2012.02019.x
Schaiff WT, Carlson MG, Smith SD, Levy R, Nelson DM, Sadovsky Y (2000) Peroxisome proliferator-activated receptor-gamma modulates differentiation of human trophoblast in a ligand-specific manner. J Clin Endocrinol Metab 85:3874–3881. doi:10.1210/jcem.85.10.6885
Shimizu T, Tsutsui T, Murao I, Orima H (1990) Incidence for transuterine migration of embryos in the dog. Nihon juigaku zasshi (The Japanese Journal of Veterinary Science) 52:1273–1275
Short RV (1969) Implantation and the maternal recognition of pregnancy. In: Wolstenholme GEW, O’Connor M (eds) Ciba foundation symposium on foetal autonomy. Churchill, London, pp 2–26
Spencer TE, Bazer FW (2004) Conceptus signals for establishment and maintenance of pregnancy. Reprod Biol Endocrinol 2:49. doi:10.1186/1477-7827-2-49
Starkey MP, Scase TJ, Mellersh CS, Murphy S (2005) Dogs really are man’s best friend–canine genomics has applications in veterinary and human medicine! Brief Funct Genomic Proteomic 4:112–128
Stefanoska I, Jovanovic Krivokuca M, Vasilijic S, Cujic D, Vicovac L (2013) Prolactin stimulates cell migration and invasion by human trophoblast in vitro. Placenta 34:775–783. doi:10.1016/j.placenta.2013.06.305
Steinetz BG, Goldsmith LT, Harvey HJ, Lust G (1989) Serum relaxin and progesterone concentrations in pregnant, pseudopregnant, and ovariectomized, progestin-treated pregnant bitches: detection of relaxin as a marker of pregnancy. Am J Ves Res 50:68–71
Tsafriri A, Lindner HR, Zor U, Lamprecht SA (1972) Physiological role of prostaglandins in the induction of ovulation. Prostaglandins 2:1–10
Tseng L, Mazella J (1999) Prolactin and its receptor in human endometrium. Sem Reprod Endocrinol 17:23–27. doi:10.1055/s-2007-1016208
Tsutsui T, Shimizu T, Hori T, Kawakami E (2002) Factors affecting transuterine migration of canine embryos. J Vet Med Sci 64:1117–1121
Vermeirsch H, Simoens P, Hellemans A, Coryn M, Lauwers H (2000) Immunohistochemical detection of progesterone receptors in the canine uterus and their relation to sex steroid hormone levels. Theriogenology 53:773–788 doi:10.1016/S0093-691X(99)00273-3
Wang Q, Fujii H, Knipp GT (2002) Expression of PPAR and RXR isoforms in the developing rat and human term placentas. Placenta 23:661–671
Yu J, Wu J, Bagchi IC, Bagchi MK, Sidell N, Taylor RN (2011) Disruption of gap junctions reduces biomarkers of decidualization and angiogenesis and increases inflammatory mediators in human endometrial stromal cell cultures. Mol Cell Endocrinol 344:25–34. doi:10.1016/j.mce.2011.04.011
Zhang S, Lin H, Kong S, Wang S, Wang H, Armant DR (2013) Physiological and molecular determinants of embryo implantation. Mol Aspects Med 34:939–980. doi:10.1016/j.mam.2012.12.011
Ziecik AJ, Waclawik A, Kaczmarek MM, Blitek A, Jalali BM, Andronowska A (2011) Mechanisms for the establishment of pregnancy in the pig. Reprod Domest Anim Suppl 3:31–41. doi:10.1111/j.1439-0531.2011.01843.x
Acknowledgments
The work was supported in part by funds from the Swiss National Science Foundation (SNSF) research grant number 408 31003A_140947. The authors would like to thank Jeanne Peter and Oxana Kaunova-Christ from the Department of Scientific Communication of the Vetsuisse Faculty, University of Zurich, for their help with preparing schematic figures and to Dr. Barry Bavister for careful editing of the manuscript. The technical expertise and contributions of Elisabeth Högger and Stefanie Ihle are gratefully appreciated. The authors thank Prof. Bernd Hoffmann, from Justus-Liebig University Giessen, Giessen, Germany, and Prof. Alois Boos, from the University of Zurich, for critical reading of the manuscript and their helpful comments.
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Kowalewski, M.P., Gram, A., Kautz, E., Graubner, F.R. (2015). The Dog: Nonconformist, Not Only in Maternal Recognition Signaling. In: Geisert, R., Bazer, F. (eds) Regulation of Implantation and Establishment of Pregnancy in Mammals. Advances in Anatomy, Embryology and Cell Biology, vol 216. Springer, Cham. https://doi.org/10.1007/978-3-319-15856-3_11
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