Trophoblast of domestic and companion animals: basic and applied clinical perspectives
Augustine Thomas Peter, Mohd Amin Beg, Ejaz Ahmad, Don Rick Bergfelt
Abstract
The trophoblast is the single most important functional structure of the placenta that mediates the attachment of the blastocyst to the endometrium. Trophoblast has the capability to proliferate in concert with the uterine epithelium to form the only site for nutrient and metabolic exchange between the fetus and dam throughout pregnancy. Trophoblast is made up of a remarkable versatile epithelium showing great capacity for invasion, cell fusion, hormone production, specific nutrient absorption, selective transport, active metabolism, and has the ability to resist maternal immunological attack. These functions are attributed to its inherent ability to synthesize many developmental factors or molecular regulators. While there is an abundance of publications available on the structural, functional, and clinical relevance of the placenta in various mammalian species, a comprehensive review on the comparative aspects of the trophoblast of domestic and companion animals is lacking. Besides, a timely description on the clinical perspective on the functional aspects of the trophoblast in relation to pregnancy diagnosis, placental insufficiency, pregnancy loss, and structural abnormalities of domestic and companion animals is necessary. A brief description on the basic chronology of events in each animal is followed by the applied clinical perspectives of trophoblast. Both the above aspects of trophoblasts of domestic and companion animals including the terminologies are summarized in tables to facilitate discussion.
Keywords
References
Abd-Elnaeim MM, Pfarrer C, Saber AS, AbouElmagd A, Jones CJ, Leiser R. 1999. Fetomaternal attachment and anchorage inthe early diffuse epitheliochorial placenta of the camel (Camelus dromedarius). Light, transmission, and scanning electron microscopic study. Cells Tissues Organs,164:141-154.
Al-Bassam MA, Thomson RG, O'Donnell L. 1981. Involution abnormalities in the postpartum 128-uterus of the bitch. Vet Pathol, 18:208-218.
Aleksic D, Blaschke L, Mißbach S, Hänske J, Weiß W, Handler J, Zimmermann W, Cabrera-Sharp V, Read JE, de Mestre AM, O'Riordan R, Moore T, Kammerer R. 2016. Convergent evolution of pregnancy-specific glycoproteins in human and horse. Reproduction, 152:171-184.
Allen WR, Wilsher S. 2009. A review of implantation and early placentation in the mare. Placenta, 30:1005- 1015.
Andersen A, Simpson M. 1973. Introduction. In: Andersen A. The Ovary and Reproductive Cycle of the Dog (Beagle). Los Altos, CA: Geron-X. pp. 11.
Andersen D. 1927. The rate of passage of the mammalian ovum through various portions of the fallopian tube. Am J Physiol, 82:557-569.
Anderson TD, Cheville NF. 1986. Ultrastructural morphometric analysis of Brucella abortus-infected trophoblasts in experimental placentitis. Bacterial replication occurs in rough endoplasmic reticulum. Am J Pathol, 124:226-237.
Anouassi A, Tibary A. 2013. Development of a large commercial camel embryo transfer program: 20 years of scientific research. Anim Reprod Sci, 136:211-221.
Antczak DF, de Mestre AM, Wilsher S, Allen WR. 2013. The equine endometrial cup reaction: a fetomaternal signal of significance. Annu Rev Anim Biosci, 1:419-442.
Assis Neto AC, Pereira FT, Santos TC, Ambrosio CE, Leiser R, Miglino MA. 2010. Morpho-physical recording of bovine conceptus (Bos indicus) and placenta from days 20 to 70 of pregnancy. Reprod Domest Anim, 45:760-772.
Attupuram NM, Kumaresan A, Narayanan K, Kumar H. 2016. Cellular and molecular mechanisms involved in placental separation in the bovine: a review. Mol Reprod Dev, 83:287-297.
Aurich C, Budik S. 2015. Early pregnancy in the horse revisited: does exception prove the rule? J Anim Sci Biotechnol, 6:50. doi: 10.1186/s40104-015-0048-6.
Bacon SJ, Ellis SA, Antczak DF. 2002. Control of expression of major histocompatibility complex genes in horse trophoblast. Biol Reprod, 66:1612-1620.
Bainbridge DR, Sargent IL, Ellis SA. 2001. Increased expression of major histocompatibility complex (MHC) class I transplantation antigens in bovine trophoblast cells before fusion with maternal cells. Reproduction, 122:907-913.
Barrau M, Abel, J, Torbit C, Tietz W. 1975. Development of the implantation chamber in the pregnant bitch. Am J Anat, 143:115-129.
Bazer FW, Song G, Kim J, Dunlap KA, Satterfield MC, Johnson GA, Burghardt RC, Wu G. 2012. Uterine biology in pigs and sheep. J Anim Sci Biotechnol. 3:23. doi: 10.1186/2049-1891-3-23.
Beceriklisoy HB, Walter I, Schäfer-Somi S, Miller I, Kanca H, Izgür 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.
Benedictus L, Koets Ad P, Rutten VPMG. 2015. The role of placental MHC class I expression in immuneassisted separation of the fetal membranes in cattle. J Reprod Immunol, 112:11-19.
Bergfelt DR, Peter AT, Beg MA. 2014. Relaxin: a hormonal aid to diagnose pregnancy status in wild mammalian species. Theriogenology, 82:1187-1198.
Betteridge KJ, Eaglesome MD, Mitchell D, Flood PF, Beriault R. 1982. Development of horse embryos up to twenty two days after ovulation: observations on fresh specimens. J Anat, 135:191-209.
Betteridge KJ. 2000. Comparative aspects of equine embryonic development. Anim Reprod Sci, 60/61:691- j702.
Bevilacqua E, Hoshida MS, Amarante-Paffaro A, Albieri-Borges A, Zago Gomes S. 2010. Trophoblast phagocytic program: roles in different placental systems. Int J Dev Biol, 54:495-505.
Bjorkman NH. 1968. Fine structure of cryptal and trophoblastic giant cells in the bovine placentome. J Ultrastruct Res, 24:249-258.
Brosnahan MM, Miller DC, Adams M, Antczak DF. 2012. IL-22 is expressed by the invasive trophoblast of the equine (Equus caballus) chorionic girdle. J Immunol, 188:4181-4187.
Cabrera-Sharp V, Read JE, Richardson S, Kowalski AA, Antczak DF, Cartwright JE, Mukherjee A, de Mestre AM. 2014. SMAD1/5 signaling in the early equine placenta regulates trophoblast differentiation and chorionic gonadotropin secretion. Endocrinology, 155:3054-3064.
Carter AM, Enders AC. 2004. Comparative aspects of trophoblast development and placentation. Reprod Biol Endocrinol, 2:46. doi:10.1186/1477-7827-2-46.
Carter AM, Enders AC. 2013. The evolution of epitheliochorial placentation. Annu Rev Anim Biosci, 1:443-467.
Carter AM, Mess AM. 2017. The evolution of fetal membranes and placentation in carnivores and ungulates (Ferungulata). Anim Reprod, 14:124-135.
Carvalho Neta AV, Stynen AP, Paixão TA, Miranda KL, Silva FL, Roux CM. Tsolis RM, Everts RE, Lewin HA, Adams LG, Carvalho AF, Lage AP, Santos RL. 2008. Modulation of the bovine trophoblastic innate immune response by Brucella abortus. Infect Immun, 76:1897-1907.
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 PW, Tsutsui T, Shille V. 2001. Embryo development, hormonal requirements and maternal responses during canine pregnancy. J Reprod Fertil, 57:169-179.
Corcoran CJ, Murphy EC. 1965. Rare bovine placental tumour--a case report. Vet Rec, 77:1234-1235.
Cross JC, Werb Z, Fisher SJ. 1994. Implantation and the placenta: key pieces of the development puzzle. Science, 266:1508-1518.
Croy BA, van den Heuvel MJ, Borzychowski AM, Tayade C. 2006. Uterine natural killer cells: a specialized differentiation regulated by ovarian hormones. Immunol Rev, 214:161-185.
Crump A, Donaldson WL, Miller J, Kydd JH, Allen WR, Antczak DF. 1987. Expression of major histocompatibility complex (MHC) antigens on horse trophoblast. J Reprod Fertil, 35:379-388.
Dantzer V. 1985. Electron microscopy of the initial stages of placentation in the pig. Anat Embryol, 172:281-293.
De Rensis F, López-Gatius F. 2014. Use of equine chorionic gonadotropin to control reproduction of the dairy cow. A review. Reprod Domest Anim, 49:177-182.
Diskin MG, Murphy JJ, Sreenan JM. 2006. Embryo survival in dairy cows managed under pastoral conditions. Anim Reprod Sci, 96:297-311.
Donaldson WL, Oriol JG, Pelkaus CL, Antczak DF. 1994. Paternal and maternal major histocompatibility complex class I antigens are expressed co-dominantly by equine trophoblast. Placenta, 15:123-135.
Dorniak P, Bazer FW, Spencer TE. 2013. Physiology and Endocrinology Symposium: Biological role of interferon tau in endometrial function and conceptus elongation. J Anim Sci, 91:1627-1638.
Eckersall PD, Harvey MJ, Ferguson JM, Renton JP, Nickson DA, Boyd JS. 1993. Acute phase proteins in canine pregnancy (Canis familiaris). J Reprod Fertil, 47:159-164.
Enders AC, Carter AM. 2006. Comparative placentation: some interesting modifications for histotrophic nutrition. A review. Placenta, 27(suppl. A):S11-16.
Erikson DW, Burghardt RC, Bayless KJ, Johnson GA. 2009. Secreted phosphoprotein 1 (SPP1, osteopontin) binds to integrin alpha v beta 6 on porcine trophectoderm cells and integrin alpha v beta 3 on uterine luminal epithelial cells, and promotes trophectoderm cell adhesion and migration. Biol Reprod, 81:814-825.
Evans J. Anderton D. 1992. Pregnancy diagnosis in the bitch: the development of a test based on the measurement of acute phase proteins in the blood. Ann Zootech, 41:397-405.
Gaviria MT, Hernandez A. 1994. Morphometry of implantation in sheep. I. Trophoblast attachment, modification of the uterine lining, conceptus size and embryo location. Theriogenology, 41:1139-1149.
Geisert RD, Zavy MT, Moffatt RJ, Blair RM, Yellin T. 1990. Embryonic steroids and the establishment of pregnancy in pigs. J Reprod Fertil, 40:293-305.
Geisert RD, Johnson GA, Burghardt RC. 2015. Implantation and establishment of pregnancy in the pig. In: Geisert RD, Bazer FW (Ed.). Regulation of Implantation and Establishment of Pregnancy in Mammals. NewYork, NY: Springer. pp. 137-163. (Adv Anat Embryol Cell Biol, 216).
Ginther OJ. 1985. Dynamic physical interactions between the equine embryo and uterus. Equine Vet J, 17(suppl. 3):41-47.
Gopal T, Leipold HW, Dennis SM. 1980. Hydatidiform moles in Holstein cattle. Vet Rec, 107:395-397.
Grazul-Bilska AT, Johnson ML, Borowicz PP, Baranko L, Redmer DA, Reynolds LP. 2013. Placental development during early pregnancy in sheep: Effects of embryo origin on fetal and placental growth and global methylation. Theriogenology, 79:94-102.
Green JA, Xie S, Szafranska B, Gan X, Szafranska B, Newman AG. McDowell K, Roberts RM. 1999. Identification of a new aspartic proteinase expressed by the outer chorionic cell layer of the equine placenta. Biol Reprod, 60:1069-1077.
Green JA, Xie S, Quan X, Bao B, Gan X, Mathialagan N. Beckers JF, Roberts RM. 2000. Pregnancy-associated bovine and ovine glycoproteins exhibit spatially and temporally distinct expression patterns during pregnancy. Biol Reprod, 62:1624-1631.
Gross TS, Williams WF. 1998. Bovine placental prostaglandin synthesis: principal cell synthesis as modulated by the binucleate cell. Biol Reprod, 38:1027- 1034.
Gullaba JM. 2013. Role of IL-8 and TIMP-2 on term canine trophoblast migration, invasion, and proliferation. Corvallis, OR: Oregon State University. Master Thesis.
Guillomot M. 1995. Cellular interactions during implantation in domestic ruminants. J Reprod Fertil, 49:39-51.
Günzel-Apel AR, Zabel S, Bunck CF, Dieleman SJ, Einspanier A, Hoppen HO. 2006. Concentrations of progesterone, prolactin and relaxin in the luteal phase and pregnancy in normal and short-cycling German Shepherd dogs. Theriogenology, 66:1431-1435.
Hall V, Hinrichs K, Lazzari G, Betts DH, Hyttel P. 2013. Early embryonic development, assisted reproductive technologies, and pluripotent stem cell biology in domestic mammals. Vet J, 197:128-142.
Henderson K, Stevens S, Bailey C, Hall G, Stewart J, Wards R. 1998. Comparison of the merits of measuring equine chorionic gonadotrophin (eCG) and blood and faecal concentrations of oestrone sulphate for determining the pregnancy status of miniature horses. Reprod Fertil Dev, 10:441-444.
Heuser CH. 1927. A study of the implantation of the ovum of the pig from the stage of the bilaminar blastocyst to the completion of the fetal membranes. Carnegie Contrib Embryol, 19:229-243.
Hill JA, Polgar K, Harlow BL, Anderson DJ. 1992. Evidence of embryo- and trophoblast-toxic cellular immune response(s) in women with recurrent spontaneous abortion. Am J Obstet Gynecol, 166:1044- 1052.
Holst PA, Phemister RD. 1971.The prenatal development of the dog: preimplantation events. Biol of Reprod, 5:194-206.
Hubrecht AAW. 1889. The placentation of Erinaceus Europaeus with remarks on the phylogeny of the placenta. Quart J Microsc Sci, 30:283-404.
Hunter RH. 1974. Chronological and cytological details of fertilization and early embryonic development in the domestic pig, Sus scrofa. Anat Rec, 178:169-185.
Huxtable CR, Duff BC, Bennett AM, Love DN, Butcher DR. 1979. Placental lesions in habitually aborting cats. Vet Pathol, 16:283-289.
Igwebuike UM. 2006. Trophoblast cells of ruminant placentas: a minireview. Anim Reprod Sci. 93:185-98.
Igwebuike UM. 2009. A review of uterine structural modifications that influence conceptus implantation and development in sheep and goats. Anim Reprod Sci. 112:1-7. doi: 10.1016/j.anireprosci.2008.
Jeffers MD, Grehan D, Gillan JE. 1994. Comparison of villous trophoblast proliferation rate in hydatidiform mole and non-molar abortion by assessment of proliferating cell nuclear antigen expression. Placenta, 15:551-556.
Johnston SD, Raksil S. 1987. Fetal loss in the dog and cat. Vet Clin North Am Small Anim Pract, 17:535-554.
Kehrer A. 1973. Chorionic development and structure of the placenta zonaria in the cat, dog and fox [in Germany]. Z Anat Entwicklungsgesch, 143:25-42.
King GJ, Atkinson BA, Robertson HA. 1980. Development of the bovine placentome from days 20 to 29 of gestation. J Reprod Fertil, 59:95-100.
Klein C, Scoggin KE, Ealy AD, Troedsson MH. 2010. Transcriptional profiling of equine endometrium during the time of maternal recognition of pregnancy. Biol Reprod, 83:102-113.
Klein C, Troedsson MH. 2011a. Maternal recognition of pregnancy in the horse: a mystery still to be solved. Reprod Fertil Dev, 23:952-963.
Klein C, Troedsson MH. 2011b. Transcriptional profiling of equine conceptuses reveals new aspects of embryo-maternal communication in the horse. Biol Reprod, 84:872-885.
Klisch K, Hecht W, Pfarrer C, Schuler G, Hoffman B, Leiser R. 1999. DNA content and ploidy level of bovine placentomal trophoblast giant cells. Placenta, 59:425-430.
Klisch K, Bevilacqua E, Olivera LV. 2005. Mitotic polyploidization in trophoblast giant cells of the alpaca. Cells Tissues Organs, 181:103-108.
Klonisch T, Mathias S, Cambridge G, HombachKlonisch S, Ryan PL, Allen WR. 1997. Placental localization of relaxin in the pregnant mare. Placenta, 18:121-128.
Klonisch T, Hombach-Klonisch S, Froehlich C, Kauffold J, Steger K, Huppertz B. 1999. Fischer B. Nucleic acid sequence of feline preprorelaxin and its localization within the feline placenta. Biol Reprod, 60:305-311.
Klonisch T, Kauffold J, Steger K, Bergmann M, Leiser R, Fischer B, Hombach- Klonisch S. 2001. Canine relaxin-like factor: unique molecular structure and differential expression within reproductive tissues of the dog. Biol Reprod, 64:442-450.
Kovacs WJ. Ojeda SR. 2012. Fertilization, implantation, and endocrinology of pregnancy. In: Kovacs WJ, Ojeda SR (Ed.). Textbook of Endocrine Physiology. New York, NY: Oxford University Press. pp. 264-291.
Kowalewski MP, Michel E, Gram A, Boos A, Guscetti F, Hoffmann B. Aslan S, Reichler I. 2011. Luteal and placental function in the bitch: spatiotemporal changes inprolactin receptor (PRLr) expression at dioestrus, pregnancy and normal and induced parturition. Reprod Biol Endocrinol, 9:109. doi:10.1186/1477-7827-9-109.
Kridli RT, Khalaj K, Bidarimath M, Tayade C. 2016. Placentation, maternal-fetal interface, and conceptus loss in swine. Theriogenology, 85:135-144.
Kuribayashi T, Shimada T, Matsumoto M, Kawato K, Honjyo T, Fukuyama M, Yamamoto Y, Yamamoto S. 2003. Determination of serum Creactive protein (CRP) in healthy beagle dogs of various ages and pregnant beagle dogs. Exp Anim, 52:387-390.
Kydd JH, Butcher GW, Antczak DF, Allen WR. 1991. Expression of major histocompatibility complex (MHC) class 1 molecules on early trophoblast. J Reprod Fertil, 44:463-477.
Kuribayashi T, Shimada T, Matsumoto M, Kawato K, Honjyo T, Fukuyama M, Leiser R, Koob B. 1993. Development and characteristics of placentation in a carnivore, the domestic cat. J Exp Zool, 266:642-656.
Leiser R, Kaufmann P. 1994. Placental structure: in a comparative aspect. Exp Clin Endocrinol, 102:122-134.
Maher JK, Tresnan DB, Deacon S, Hannah L, Antczak DF. 1996. Analysis of MHC class I expression in equine trophoblast cells using in situ hybridization. Placenta, 17:351-359.
Majewska M, Panasiewicz G, Klisch K, Olivera LV, Mamani JM, Abd-Elnaeim MM. Szafranska B. 2009. Pregnancy-associated glycoprotein (PAG) family: transcripts and gene amplicons in camelids. Reprod Biol, 9:127-150.
McNaughton AP, Murray RD. 2009. Structure and function of the bovine fetomaternal unit in relation to the causes of retained fetal membranes. Vet Rec, 165:615-622.
Meinecke B, Kuiper H, Drögemüller C, Leeb T, Meinecke-Tillmann S. 2003. A mola hydatidosa coexistent with a foetus in a bovine freemartin pregnancy. Placenta, 24:107-112.
Miglino MA, Ambrósio CE, dos Santos Martins D, Wenceslau CV, Pfarrer C, Leiser R. 2006. The carnivore pregnancy: the development of the embryo and fetal membranes. Theriogenology, 66:1699-1702.
Mordak R, Stewart PA. 2015. Periparturient stress and immune suppression as a potential cause of retained placenta in highly productive dairy cows: examples of prevention. Acta Vet Scand, 57:84. doi:10.1186/s13028- 015-0175-2
Morris FJ, Kerr SM, Laven RA, Collett MG. 2008. Large hydatidiform mole: an unusual finding in a calving cow. N Z Vet J, 56:243-246. doi: 10.1080/00480169.2008.36841.
Nakano H, Shimada A, Imai K, Takezawa T, Takahashi T, Hashizume K. 2002. Bovine trophoblastic cell differentiation on collagen substrata: formation of binucleate cells expressing placental lactogen. Cell Tissue Res, 307:225-235.
Noronha LE, Antczak DF. 2010. Maternal immune responses to trophoblast: the contribution of the horse to pregnancy immunology. Am J Reprod Immunol, 64:231- 244.
Olio RL, Lobo LM, Pereira MA, Santos AC, Viana DC, Favaron PO, Miglino MA. 2014. Accessory placental structures: a review. Open J Anim Sci, 4:305- 312. http://dx.doi.org/10.4236/ojas.2014.45039.
Orfanou DC, Ververidis HN, Pourlis A, Fragkou IA, Kokoli AN, Boscos CM, Taitzoglou IA, Tzora A, Nerou CM, Athanasiou L, Fthenakis GC. 2009. Postpartum involution of the canine uterus - gross anatomical and histological features. Reprod Domest Anim, 44:152-155.
Oriol JG, Sharom FJ, Betteridge KJ. 1993. Developmentally regulated changes in the glycoproteins of the equine embryonic capsule. J Reprod Fertil, 99:653-664.
Peippo J, Machaty Z, Peter A. 2011. Terminologies for the pre-attachment bovine embryo. Theriogenology, 76:1373-1379.
Peter AT. 2013. Bovine placenta: a review on morphology, components, and defects from terminology and clinical perspectives. Theriogenology, 80:693-705.
Peter AT. 2015. Retained fetal membranes. In: Hopper RM (Ed.). Bovine Reproduction. Hoboken, NJ: Wiley Blackwell. pp. 431-439.
Raheem KA. 2017. An insight into maternal recognition of pregnancy in mammalian species. J Saudi Soc Agric Sci, 16:1-6. doi:10.1016/j.jssas.2015.01.002.
Ranilla MJ, Sulon J, Carro MD, Mantecón AR, Beckers JF. 1994. Plasmatic profiles of pregnancy-associated glycoprotein and progesterone levels during gestation in Churra and Merino sheep. Theriogenology, 42:537-545.
Rapacz-Leonard A, Dąbrowska M, Janowski T. 2014. Major histocompatibility complex I mediates immunological tolerance of the trophoblast during pregnancy and may mediate rejection during parturition. Mediators Inflamm, 2014: 579279. doi:10.1155/2014/579279.
Reberg S, Peter AT, Blevins W. 1992. Subinvolution of placental sites in dogs. Compend Contin Educ Pract Vet, 4:789-796.
Reimers TJ, Ullmann MB, Hansel W. 1985. Progesterone and prostanoid production by bovine binucleate trophoblastic cells. Biol Reprod, 33:1227- 1236.
Reynaud K, Fontbonne A, Marseloo N, Viaris de Lesegno C, Saint-Dizier M, Chastant-Maillard S. 2006. In vivo canine oocyte maturation, fertilization and early embryogenesis. A review. Theriogenology, 66:1685-1693.
Roberts RM. 1989. Conceptus interferons and maternal recognition of pregnancy. Biol Reprod, 40:449-452.
Roberts RM, Cross JC, Leaman DW. 1992. Interferons as hormones of pregnancy. Endocr Rev, 13:432-452.
Roberts SJ. 1971. Veterinary Obstetrics and Genital Diseases (Theriogenology). Woodstock, VT: Published by the author.
Robertson R, Allen H, Bokelman D. 1979. Aspirin: teratogenic evaluation in the dog. Teratology, 20:313- 320.
Ross JW, Malayer JR, Ritchey JW, Geisert RD. 2003. Characterization of the interleukin-1beta system during porcine trophoblastic elongation and early placental attachment. Biol Reprod, 69:1251-1259.
Sahlfeld L, Hazzard T, Kutzler M. 2012. Cellular characteristics of cultured canine trophoblasts. Reprod Domest Anim, 47:161-164.
Samuel CA, Allen WR, Steven DH. 1974. Studies on the equine placenta. I. Development of the microcotyledons. J Reprod Fertil, 4:441-445.
Schuler G, Ozalp GR, Hoffmann B, Harada N, Browne P, Conley AJ. 2006. Reciprocal expression of 17alpha-hydroxylase-C17,20-lyase and aromatase cytochrome P450 during bovine trophoblast differentiation: a two-cell system drives placental oestrogen synthesis. Reproduction, 131:669-679.
Schuler G, Greven H, Kowalewski MP, Döring B, Ozalp GR, Hoffmann B. 2008. Placental steroids in cattle: hormones, placental growth factors or byproducts of trophoblast giant cell differentiation? Exp Clin Endocrinol Diabetes, 116:429-436.
Skidmore JA, Wooding FB, Allen WR. 1996. Implantation and early placentation in the onehumped camel (Camelus dromedarius). Placenta, 17:253-262.
Smith T. 1919. A characteristic localization of Bacillus abortus in the bovine fetal membranes. J Exp Med, 29:451-456.
Soares MJ. 2004. The prolactin and growth hormone families: pregnancy-specific hormones/cytokines at the maternal-fetal interface. Reprod Biol Endocrinol, 2:51. doi: 10.1186/1477-7827-2-51.
Sontas HB, Stelletta C, Milani C, Mollo A, Romagnoli S. 2015. Full recovery of subinvolution of placental sites in an American Staffordshire terrier bitch. J Small Anim Pract, 52:42-45.
Sousa NM, Garbayo JM, Figueiredo JR, Sulon J, Gonçalves PBD, Beckers JF. 1999. Pregnancyassociated glycoprotein and progesterone profiles during pregnancy and postpartum in native goats from the north-east of Brazil. Small Rumin Res, 32:137-147.
Sousa NM, Ayad A, Beckers JF, Gajewski Z. 2006. Pregnancy-associated glycoproteins (PAG) as pregnancy markers in the ruminants. J Physiol Pharmacol, 57:153-171.
Sousa NM, Beckers JF, Gajewski Z. 2008. Current trends in follow-up of trophoblastic function in ruminant species. J Physiol Pharmacol, 59:65-74.
Staun-Ram E, Shalev E. 2005. Human trophoblast function during the implantation process. Reprod Biol Endocrin, 3:56. doi:10.1186/1477-7827-3-56.
Steven DH. 1982. Placentation in the mare. J Reprod Fertil, 31:41-55.
Stout TA, Meadows S, Allen WR. 2005. Stagespecific formation of the equine blastocyst capsule is instrumental to hatching and to embryonic survival in vivo. Anim Reprod Sci, 87:269-281.
Szafrañska B, Panasiewicz G. 2002. The placental expression of the porcine pregnancy-associated glycoprotein (pPAG) gene family examined in situ and in vitro. Anim Reprod Sci, 72:95-113.
Tibary A. 2001. Fertilization, embryo and fetal development in camelids. In: Proceedings of the Annual Conference of the Society for Theriogenology, 2001, Vancouver, BC, Canada. Montgomery, AL: Society for Theriogenology. pp. 387-396.
Tsutsui T, Amano T, Shimizu T, Murao I, Stabenfeldt GH. 1989. Evidence for transuterine migration of embryos in the domestic cat. Nihon Juigaku Zasshi, 51:613-617.
Tsutsui T, Stewart DR. 1991. Determination of the source of relaxin immunoreactivity during pregnancy in the dog. J Vet Med Sci, 53:1025-1029.
Tsutsui T, Stabenfeldt GH. 1993. Biology of ovarian cycles, pregnancy and pseudopregnancy in the domestic cat. J Reprod Fertil, 47:29-35.
Ulutas PA, Musal B, Kiral F, Bildik A. 2009. Acute phase protein levels in pregnancy and oestrus cycle in bitches. Res Vet Sci, 86:373-376.
Van Mourik M., Macklon N. Heijnen C. 2009. Embryonic implantation: cytokines, adhesion molecules, and immune cells in establishing an implantation environment. J Leukocyte Biol, 85:4-19.
Waelchli RO, Bettreridge KJ. 2013. Morphology of twin and triplet equine conceptuses during weeks 3 and 4 of pregnancy. Reprod Fertil Dev, 25:762-774.
Weber JA, Freeman DA, Vanderwall DK, Woods GL. 1991. Prostaglandin E2 hastens oviductal transport of equine embryos. Biol Reprod, 45:544-546.
Whitlock BK, Maxwell HS. 2008. Pregnancyassociated glycoproteins and pregnancy wastage in cattle. Theriogenology, 70:550-559.
Wilsher S, Allen WR. 2011. Intrauterine administration of plant oils inhibits luteolysis in the mare. Equine Vet J, 43:99-105.
Wooding FB, Wathes DC. 1980. Binucleate cell migration in the bovine placentome. J Reprod Fertil, 59:425-430.
Wooding FB, Staples LD, Peacock MA. 1982. Structure of trophoblast papillae on the sheep conceptus at implantation. J Anat, 134:507-516.
Wooding FB, Beckers JF. 1987. Trinucleate cells and the ultrastructural localisation of bovine placental lactogen. Cell Tissue Res, 247:667-673.
Wooding FB. 1992. Current topic: the synepitheliochorial placenta of ruminants: binucleate cell fusions and hormone production. Placenta, 13:101- 113.
Wooding FB, Hobbs T, Morgan G, Heap RB, Flint APF. 1993. Cellular dynamics of growth in sheep and goat synepitheliochorial placentomes: an autoradiographic study. J Reprod Fertil, 98:275-283.
Wooding FB, Ozturk M, Skidmore JA, Allen WR. 2003. Developmental changes in localization of steroid synthesis enzymes in camelid placenta. Reproduction, 26:239-247.
Wooding FB, Roberts RM, Green JA. 2005. Light and electron microscope immunocytochemical studies of the distribution of pregnancy associated glycoproteins (PAGs) throughout pregnancy in the cow: possible functional implications. Placenta, 26:807-827.
Wooding P, Burton G. 2008. Comparative placentation: Structures, Functions and Evolution. Heidelberg: Springer. 301 pp.
Yamashita K, Fujinaga T, Miyamoto T, Hagio M, Izumisawa Y, Kotani T. 1994. Canine acute phase response: relationship between serum cytokine activity and acute phase protein in dogs. J Vet Med Sci, 56:487- 492.
Zoli AP, Demez P, Beckers JF, Reznik M, Beckers A. 1992. Light and electron microscopic immunolocalization of bovine pregnancyassociated glycoprotein in the bovine placentome. Biol Reprod, 46:623-629.
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