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Develpmental changes at the materno-embryonic interface in early pregnancy of the alpaca, Lamos pacos

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Abstract

This study analyses the manner in which trophoblast cells adhere to uterine epithelium and the subsequent interactions that contribute to the establishment of epitheliochorial placentation in the alpaca Lama pacos. Specimens at the luteal and follicular phases and at 22, 26, 30 and 45 days of pregnancy (op) were processed for morphological studies. On day 15 op, the blastocysts are completely free within the uterine lumen, with implantation starting around day 20. On days 22 and 26 of gestation, the trophoblast is apposed to the epithelial surface of the uterus, with areas of contact and adhesion by means of complex interdigitation. Implantation sites occur prevalently in the left uterine horn, but an expanded trophoblast also occupies large extensions of the right horn, where the maternofetal interaction shows peculiar areas of apposition. As development continues, attachment areas become more extensive. On days 30 and 45, many secretory granules can be seen in the uterine epithelium, while giant multinucleate cells appear interposed between the remaining trophoblast cells, showing intense alkaline phosphatase activity, deposits containing iron and PAS-positive granules. Placental lactogen hormone is not present within the cytoplasm of the binucleate or multinucleate trophoblast cells. By day 30 of gestation, the trophoblast layer is lined by an extraembryonic connective tissue that by day 45 is well vascularized, thus indicating the starting point of placental formation. Fetal and maternal capillaries indent the epithelium and the trophoblast, narrowing the specialized areas of exchange, which occur along the entire maternofetal interface, characterizing the diffuse nature of this placenta.

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References

  • Aba M, Bravo P, Forsberg G, Kindahl H (1997) Endocrine changes during early pregnancy in the alpaca. Anim Reprod Sci 47:273–279

    Article  CAS  PubMed  Google Scholar 

  • Abd-Elnaeim MM, Pfarrer C, Saber AS, Abou-Elmagd A, Jones C, Leiser R (1999) Fetomaternal attachment and anchorage in the early diffuse epitheliochorial placenta of the camel (Camelus dromedarius). Cell Tissue Organ 164:141–154

    Article  CAS  Google Scholar 

  • Adams CL, Moir CE, Shiach P (1989) Plasma progesterone concentrations in pregnant and non-pregnant llamas (Lama glama). J Vet Rec 16:618–620

    Google Scholar 

  • Adams G, Sumar J, Ginther O (1991) Form and function of the corpus luteum in llamas. Anim Reprod Sci 24:127–138

    Google Scholar 

  • Bancroft J, Stevens A (1996) Theory and practice of histological techniques. Churchill Livingstone, New York

  • Basu S, Kindahl H (1987) Development of a continuous blood collection technique and a detailed study of prostaglandins F2α release during luteolysis and early pregnancy in heifers. J Vet Med Series A 34:487–500

    CAS  Google Scholar 

  • Bielanska-Osuchowska Z, Kunska A (1995) A new approach to the areolar structures in the pig placenta: histochemistry and development of mucous areolae. Folia Histochem Cytobiol 33:95–101

    CAS  PubMed  Google Scholar 

  • Björkman N (1973) Fine structure of the fetal-maternal area of exchange in the epitheliochorial and endotheliochorial types of placentation. Acta Anat 86:1–22

    Google Scholar 

  • Bowen J, Burghardt R (2000) Cellular mechanisms of implantation in domestic farm animals. Semin Cell Dev Biol 11:93–104

    Google Scholar 

  • Bravo W, Sumar J (1989) Laparoscopic examination of the ovarian activity in alpacas. Anim Reprod Sci 21:271–281

    Google Scholar 

  • Bravo W, Stanfeldt G, Fowler M, Lasley B (1993) Ovarian and endocrine patterns associated with reproductive abnormalities in llamas and alpacas. JAVMA 202:268–272

    CAS  Google Scholar 

  • Bravo W, Stewart D, Lasley B, Fowler M (1996) Hormonal indicators of pregnancy in llamas and alpacas. JAVMA 208:2027–2030

    CAS  Google Scholar 

  • Dantzer V (1985) Electron microscopy of the initial stages of placentation in the pig. Anat Embryol 172:281–293

    CAS  PubMed  Google Scholar 

  • Duello T, Byatt J, Bremel R (1986) Immunohistochemical localization of placental lactogen in binucleate cells of bovine placentomes. Endocrinology 119:1351–1355

    Google Scholar 

  • Elwishy A (1987) Reproduction in the female dromedary (Camelus dromedarius): a review. Anim Reprod Sci 15:273–297

    Google Scholar 

  • Fernandez-Baca S (1993) Manipulation of reproductive functions in male and female new world camelids. Anim Reprod Sci 33:307–323

    Google Scholar 

  • Fernandez-Baca S, Madden D, Novoa C (1970) Effect of different mating stimuli on induction of ovulation in the alpaca. J Reprod Fertil 22:261–267

    CAS  PubMed  Google Scholar 

  • Fernandez-Baca S, Hansel W, Saatman R, Sumar J, Novoa C (1979) Differential luteolytic effects of right and left uterine horns in the alpaca. Biol Reprod 20:586–595

    CAS  PubMed  Google Scholar 

  • Fowler M (1989) Medicine and surgery of South American Camelids: llama, alpaca, vicuña, guanaco. Iowa State University Press, Iowa

    Google Scholar 

  • Fowler ME, Olander HJ (1990) Fetal membranes and ancillary structures of llamas (Lama glama). Am J Vet Res 51:1495–1500

    CAS  PubMed  Google Scholar 

  • Friess A, Sinowatz F, Skolek-Winnisch R (1980) The placenta of the pig. I. Fine structural changes of the placental barrier during pregnancy. Anat Embryol 158:179–191

    CAS  PubMed  Google Scholar 

  • Gorokhovskii N, Shmidt G, Shagaeva V, Baptidanova I (1975) Giant cells in the placenta of the bactrian camel in the fetal period of development. Arkh Anat Gistol Embriol 69:41–46

    CAS  PubMed  Google Scholar 

  • Gray C, Taylor K, Ramsey W, Hill J, Bazer F, Bartol F, Spencer T (2001) Endometrial gland are required for preimplantation conceptus elongation and survival. Biol Reprod 64:1608–1613

    CAS  PubMed  Google Scholar 

  • Guillomot M (1995) Cellular interactions during implantation in domestic ruminant. J Reprod Fertil [Suppl] 49:39–51

    Google Scholar 

  • Guillomot M, Flechon J, Wintenber-Torres S (1981) Conceptus attachment in the ewe: an ultra-structural study. Placenta 2:169–182

    CAS  PubMed  Google Scholar 

  • Guillomot M, Guay P (1982) Ultrastructural features of the cell surfaces of uterine and trophoblastic epithelia during embryo attachment in the cow. Anat Rec 204:315–322

    CAS  PubMed  Google Scholar 

  • Hunt J, Petroff M, Burnett T (2000) Uterine leukocytes: Key players in pregnancy. Semin Cell Dev Biol 11:127–137

    Google Scholar 

  • Johnson G, Burghardt R, Spencer T, Newton G, Ott T (1999) Ovine Osteopontin: II. Osteopontin and αvβ3 integrin expression in the uterus and conceptus during the periimplantation period. Biol Reprod 61:892–899

    CAS  PubMed  Google Scholar 

  • Johnson L (1989) Llama reproduction. Vet Clinic North Am Food Anim Pract 5:159–182

    CAS  Google Scholar 

  • Jones CJP, Dantzer V, Stoddart RW (1995) Changes in glycan distribution within the porcine interhaemal barrier during gestation. Cell Tissue Res 279:551–564

    Article  CAS  PubMed  Google Scholar 

  • Jones CJP, Dantzer V, Leiser R, Krebs C, Stoddart RW (1997) Localisation of glycans in the placenta: a comparative study of epitheliochorial, endotheliochorial and haemomonochorial placentation. Microsci Res Tech 38:100–114

    Article  CAS  Google Scholar 

  • Jones CJP, Abd-Elnaeim M, Bevilacqua E, Oliveira LV, Leiser R (2002) Comparison of uteroplacental glycosylation in the camel (Camelus dromedarius) and alpaca (Lama pacos). Reproduction 123:115–126

    CAS  PubMed  Google Scholar 

  • Keys JL, King GJ (1990) Microscopic examination of porcine conceptus-maternal interface between days 10 and 19 of pregnancy. Am J Anat 188:221–238

    CAS  PubMed  Google Scholar 

  • Kimber S (2000) Cell biology of implantation and placentation. Introduction. Semin Cell Dev Biol 11:61–65

    Google Scholar 

  • Mossman H (1987) Vertebrate fetal membranes. Comparative ontogeny and morphology; evolution; phylogenetic significance; basic functions; research opportunities. Rutgers University Press, New Jersey

  • Novoa C (1970) Reproduction in camelidae. J Reprod Fertil 22:3–20

    CAS  PubMed  Google Scholar 

  • Olivera LV (1998) Implantação embrionária em alpacas. Msc Thesis, Depto Histologia e Embriologia, ICB-I, University of São Paulo

  • Raub T, Bazer F, Roberts R (1985) Localization of the iron transport glycoprotein, uteroferrin, in the porcine endometrium and placenta by using immunocolloidal gold. Anat Embryol 171:253–258

    CAS  PubMed  Google Scholar 

  • Samuel CA, Allen WR, Steven DH (1974) Studies on the equine placenta. J. Reprod Fertil 41:441–445

    CAS  Google Scholar 

  • San Martin M, Copaira M, Zuniga J, Rodriguez R, Bustinza G, Acosta L (1968) Aspects of reproduction in the alpaca. J Reprod Fertil 16:395–399

    PubMed  Google Scholar 

  • Sinowatz F, Friess A (1983) Uterine glands of the pig during pregnancy. An ultrastructural and cytochemical study. Anat Embryol 166:121–134

    CAS  PubMed  Google Scholar 

  • Skidmore JA, Allen WR, Heap R (1994) Oestrogen synthesis by the peri-implantation conceptus of the one-humped camel (Camelus dromedarius). J Reprod Fertil 101:363–367

    CAS  PubMed  Google Scholar 

  • Skidmore JA, Wooding FBP, Allen WR (1996) Implantation and early placentation in the one-humped camel (Camelus dromedarius). Placenta 17:253–262

    CAS  PubMed  Google Scholar 

  • Steven DH, Burton GJ, Sumar J, Nathanielsz PW (1980) Ultrastructural observations on the placenta of the alpaca (Lama pacos). Placenta 1:21–32

    CAS  PubMed  Google Scholar 

  • Sumar J (1988) Removal of the ovaries or ablation of the corpus luteum and its effect on the maintenance of gestation in the alpaca and llama. Acta Vet Scand 83:133–141

    CAS  PubMed  Google Scholar 

  • Sumar J (2000) Llamas and alpacas. In: Hafez B, Hafez E (eds) Reproduction in farm animals. Lippincott Williams Wilkins, Pennsylvania, pp 218–236

  • Sumar J, Fredriksson G, Alarcon V, Kindahl H, Edqvist L (1988) Levels of 15 keto-13, 14-dihydro-PGFG2 a progesterone and oestradiol-17b after induced ovulations in llamas and alpacas. Acta Vet Scand 29:339–346

    CAS  PubMed  Google Scholar 

  • Van Lennep E (1961) The histology of the placenta of the one-humped camel (Camelus dromedarius L.) during the first half of pregnancy. Acta morph Neerl Scand 4:180–193

    Google Scholar 

  • Van Lennep E (1963) The placenta of the one-humped camel (Camelus dromedarius L) during the second half of gestation. Acta Morph Neerl Scand 5:373–379

    Google Scholar 

  • Wango EO, Wooding FBP, Heap RB (1990) The role of trophoblastic binucleate cells in implantation in the goat: a morphological study. J Anat 171:241–257

    CAS  PubMed  Google Scholar 

  • Wathes C, Wooding FBP (1980) An electron microscopic study of implantation in the cow. Am J Anat 159:285–306

    CAS  PubMed  Google Scholar 

  • Wooding FBP (1992) Current topic: the synepitheliochorial placenta of ruminants: binucleate cell fusions and hormone production. Placenta 13:101–113

    CAS  PubMed  Google Scholar 

  • Wooding FBP, Beckers JF (1987) Trinucleate cells and the ultrastructural localisation of bovine placental lactogen. Cell Tissue Res 247:667–673

    CAS  PubMed  Google Scholar 

  • Wooding FBP, Flint APF (1994) Placentation. In: Lamminig GE (ed) Marshall’s physiology of reproduction. Chapman Hall, London, pp 233–429

  • Wooding FBP, Wathes C (1980) Binucleate cell migration in the bovine placentome. J Reprod Fertil 59:425–430

    CAS  PubMed  Google Scholar 

  • Wooding FBP, Morgan G, Forsyth IA, Butcher G, Hutchings A, Billingsley SA, Gluckman PD (1992) Light and electron microscopic studies of cellular localization of oPL with monoclonal and polyclonal antibodies. J Histochem Cytochem 40:1001–1009

    CAS  PubMed  Google Scholar 

  • Wooding FBP, Morgan G, Monaghan S, Hamon M, Heap RB (1996) Functional specialization in the ruminant placenta: Evidence for two populations of fetal binucleate cells of different selective synthetic capacity. Placenta 17:75–86

    CAS  PubMed  Google Scholar 

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Acknowledgements

This study was supported by grants from FAPESP 95/1880/4. Mr. Gaspar F. Lima, Edson R. Oliveira, Wilson R. Azevedo and Gerson B. Silva are acknowledged for their technical assistance, Msc. Guido Pérez for helping us to get and collect the samples. The authors would like to specially thank Dr. Carolyn Jones for her continuing interest, support and values advice in the preparation of the manuscript. We also thank all personnel of the La Raya Research Center and Institute of Camelids South American-IIPC, Puno-Peru.

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Authors and Affiliations

  1. Faculty of Medicine Veterinary and Zootechnology, National University Altiplano, Puno, 291, Casilla, Peru

    L. V. M. Olivera

  2. Department of Morphology, University of Santo Amaro, São Paulo, Brazil

    D. A. Zago

  3. Academic Unit of Obstetrics and Gynaecology, School of Medicine of the University of Manchester, St Mary’s Hospital, Whitworth Park, Manchester, UK

    C. J. P. Jones

  4. Department of Histology and Embryology, Institute of Biomedical Sciences, University of São Paulo, Av. Prof. Lineu Prestes, 1524, 05508-900 São Paulo, SP, Brazil

    L. V. M. Olivera, D. A. Zago & E. Bevilacqua

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  1. L. V. M. Olivera
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  4. E. Bevilacqua
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Correspondence to E. Bevilacqua.

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Olivera, L.V.M., Zago, D.A., Jones, C.J.P. et al. Develpmental changes at the materno-embryonic interface in early pregnancy of the alpaca, Lamos pacos . Anat Embryol 207, 317–331 (2003). https://doi.org/10.1007/s00429-003-0346-1

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