Equine embryology: An inventory of unanswered questions

Theriogenology

Volumn 68, Issue SUPPL. 1, 2007, Pages

  Betteridge, K J ^a  

^a UNIVERSITY OF GUELPH   (Canada)

Author keywords

Early pregnancy; Embryonic development; Horse

Indexed keywords

ANIMAL; ANIMAL MODEL; ARTICLE; BLASTOCYST; BREEDING; CELL COMMUNICATION; CYTOLOGY; EMBRYO DEVELOPMENT; ENDOMETRIUM; FEMALE; HORSE; NIDATION; OOCYTE; PHYSIOLOGY; PREGNANCY; PRENATAL DEVELOPMENT; REPRODUCTION; YOLK SAC;

ANIMALS; BLASTOCYST; CELL COMMUNICATION; EMBRYO IMPLANTATION; EMBRYONIC DEVELOPMENT; ENDOMETRIUM; FEMALE; HORSES; MODELS, ANIMAL; OOCYTES; PREGNANCY; PREGNANCY, ANIMAL; REPRODUCTION; YOLK SAC;

ANIMALIA; BOVIDAE; BOVINAE; EQUIDAE; SUIDAE;

EID: 34447648724     PISSN: 0093691X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.theriogenology.2007.04.037     Document Type: Article

References (99)

1. Hartman C.G. Physiological mechanisms concerned with conception - an inventory of unanswered questions. J Reprod Fertil 1 (1960) 283-293
2. Betteridge K.J. A commemoration of the fiftieth anniversary of the first recovery of a bovine embryo. Bovine Pract 15 (1980) 4-7
3. Tyndale-Biscoe H., and Renfree M. Reproductive Physiology of Marsupials (1987), Cambridge University Press, Cambridge p. 9
4. Nishihara H., Hasegawa M., and Okada N. Pegasoferae, an unexpected mammalian clade revealed by tracking ancient retroposon insertions. Proc Natl Acad Sci U S A 103 (2006) 9929-9934
5. Betteridge K.J. Comparative aspects of conceptus growth: a historical perspective. Reproduction 122 (2001) 11-19
6. Betteridge K.J. Embryo 'talk' in horses: its comparative relevance. Embryo Talk 1 (2006) 131-139
7. Galli C., Colleoni S., Duchi R., Lagutina I., and Lazzari G. Developmental competence of equine oocytes and embryos obtained by in vitro procedures ranging from in vitro maturation and ICSI to embryo culture, cryopreservation and somatic cell nuclear transfer. Anim Reprod Sci 98 (2007) 39-55
8. Ball B.A., Little T.V., Weber J.A., and Woods G.L. Survival of Day-4 embryos from young, normal mares and aged, subfertile mares after transfer to normal recipient mares. J Reprod Fertil 85 (1989) 187-194
9. Betteridge K.J. Comparative aspects of equine embryonic development. Anim Reprod Sci 60-61 (2001) 691-702
10. Enders A.C., Liu I.K.M., Bowers J., Lantz K.C., Schlafke S., and Suarez S. The ovulated ovum of the horse: cytology of non-fertilized ova to pronuclear stage ova. Biol Reprod 37 (1987) 453-466
11. Palmer E., Duchamp G., Bézard J., Magistrini M., King W.A., Bousquet D., et al. Non-surgical recovery of follicular fluid and oocytes of mares. J Reprod Fertil Suppl 35 (1987) 689-690 (abstr.)
12. Bézard J., Magistrini M., Duchamp G., and Palmer E. Chronology of equine fertilization and embryonic development in vivo and in vitro. Equine Vet J Suppl 8 (1989) 105-110
13. Grøndahl C., Grøndahl-Nielsen C., Eriksen T., Greve T., and Hyttel P. In vivo fertilization and initial embryogenesis in the mare. Equine Vet J Suppl 15 (1993) 79-83
14. Grøndahl C., Hyttel P., Grøndahl M.L., Eriksen T., Gotfredsen P., and Greve T. Structural and endocrine aspects of equine oocyte maturation in vivo. Mol Reprod Dev 42 (1995) 94-105
15. Grøndahl C., and Hyttel P. Nucleologenesis and ribonucleic acid synthesis in preimplantation equine embryos. Biol Reprod 55 (1996) 769-774
16. Antczak M., and Van Blerkom J. Oocyte influences on early development: the regulatory proteins leptin and STAT3 are polarized in mouse and human oocytes and differentially distributed within the cells of the preimplantation stage embryo. Mol Hum Reprod 3 (1997) 1067-1086
17. Fulka Jr. J., Kárníková L., and Moor R.M. Oocyte polarity: ICSI, cloning and related techniques. Hum Reprod 13 (1998) 3304-3305
18. Zernicka-Goetz M. Introduction. Semin Cell Dev Biol 15 (2004) 541
19. Hiiragi T., Alarcon V.B., Fujimori T., Louvet-Valée S., Maleszewski M., Maro B., et al. Where do we stand now? - Mouse early embryo patterning meeting in Freiburg, Germany (2005). Int J Dev Biol 50 (2006) 581-588
20. Albertini D.F., and Barrett S.L. The developmental origins of mammalian oocyte polarity. Semin Cell Dev Biol 15 (2004) 599-606
21. Planch C.E., Sanfins A., Rodriques P., and Albertini D. Cell polarity during folliculogenesis and oogenesis. Reprod Biomed Online 10 (2005) 478-484
22. Heng B.C., Cao T., Stojkovic M., and Vajta G. Mammalian oocyte polarity can be exploited for the automation of somatic cell nuclear transfer-in the development of a 'cloning biochip'. Med Hypotheses 67 (2006) 420-421
23. Brinsko S.P., Ball B.A., Miller P.G., Thomas P.G., and Ellington J.E. In vitro development of Day 2 embryos obtained from young, fertile mares and aged, subfertile mares. J Reprod Fertil 102 (1994) 371-378
24. Betteridge K.J., Eaglesome M.D., Mitchell D., Flood P.F., and Bériault R. Development of horse embryos up to twenty-two days after ovulation: observations on fresh specimens. J Anat 135 (1982) 191-209
25. Betteridge K.J. The structure and function of the equine capsule in relation to embryo manipulation and transfer. Equine Vet J Suppl 8 (1989) 92-100
26. Denker H.-W. Structural dynamics and function of early embryonic coats. Cells Tissues Organs 166 (2000) 180-207
27. Herrler A., and Beier H.M. Early embryonic coats: morphology, function, practical applications. Cells Tissues Organs 166 (2000) 233-246
28. Buhi W.F. Characterization and biological roles of oviduct-specific, oestrogen-dependent glycoprotein. Reproduction 123 (2002) 355-362
29. McCauley T.C., Buhi W.C., Wu G.M., Mao J., Caamano J.N., Didion B.A., et al. Oviduct-specific glycoprotein modulates sperm-zona binding and improves efficiency of porcine fertilization in vitro. Biol Reprod 69 (2003) 828-834
30. Fléchon J.-E., Kopecny V., Pivko J., Pavlok A., and Motlik J. Texture of the zona pellucida of the mature pig oocyte. The mammalian egg envelope revisited. Reprod Nutr Dev 44 (2004) 207-218
31. Familiari G., Relucenti M., Heyn R., Micara G., and Correr S. Three-dimensional structure of the zona pellucida at ovulation. Microsc Res Tech 69 (2006) 415-426
32. Betteridge K.J. Phylogeny, ontogeny and embryo transfer. Theriogenology 44 (1995) 1061-1098
33. Fléchon J.-E., Degrouard J., Kopecny V., Pivko J., Pavlok A., and Motlik J. The extracellular matrix of porcine mature oocytes: origin, composition and presumptive roles. Reprod Biol Endocrinol 1 (2003) 124
34. In: Betteridge K.J. (Ed). Embryo Transfer in Farm Animals: a Review of Techniques and Applications. Monograph No. 16 (1977), Canada Department of Agriculture, Ottawa
35. Barcroft L.C., Hay-Schmidt A., Caveney A., Gilfoyle E., Overstrom E.W., Hyttel P., et al. Trophectoderm differentiation in the bovine embryo: characterization of a polarized epithelium. J Reprod Fertil 114 (1998) 327-339
36. Wilson J.M., Caceci T., Potter G.D., and Kraemer D.C. Ultrastructure of cryopreserved horse embryos. J Reprod Fertil Suppl 35 (1987) 405-417
37. Bruyas J.-F., Bézard J., Lagneaux D., and Palmer E. Quantitative analysis of morphological modifications of day 6.5 horse embryos after cryopreservation: differential effects on inner cell mass and trophoblast cells. J Reprod Fertil 99 (1993) 15-23
38. Bruyas J.-F., Battut I., Pol J.-M., Botrel C., Fieni F., and Tainturier D. Quantitative analysis of morphological modifications of day 6.5 horse embryos after treatment with four cryoprotectants: differential effects on inner cell mass and trophoblast cells. Biol Reprod Monogr 1 (1995) 329-339
39. Tremoleda J.L., Stout T.A., Lagutina I., Lazzari G., Bevers M.M., Colenbrander B., et al. Effects of in vitro production on horse embryo morphology, cytoskeletal characteristics, and blastocyst capsule formation. Biol Reprod 69 (2003) 1895-1906
40. Malette B., Paquette Y., Merlen Y., and Bleau G. Oviductins possess chitinase- and mucin-like domains: a lead in the search for the biological function of these oviduct-specific ZP-associating glycoproteins. Mol Reprod Dev 41 (1995) 384-397
41. Kan F.W., and Esperanzate P.W. Surface mapping of binding of oviductin to the plasma membrane of golden hamster spermatozoa during in vitro capacitation and acrosome reaction. Mol Reprod Dev 73 (2006) 756-766
42. Ménézo Y., Elder K., and Viville S. Soluble HLA-G release by the human embryo: an interesting artefact?. Reprod Biomed Online 13 (2006) 763-764
43. Shao R, Weijdegård B, Fernandez-Rodriguez J, Egecioglu E, Andersson N, Thurin-Kjellberg A, et al. Ciliated epithelial-specific and regional-specific expression and regulation of the estrogen receptor beta2 in the fallopian tubes of immature rats. Am J Physiol Endocrinol Metab. 2007 Mar 20; [Epub ahead of print].
44. Squires E.L., McCue P.M., and Vanderwall D. The current status of equine embryo transfer. Theriogenology 51 (1999) 91-104
45. Stout T.A.E. Equine embryo transfer: review of developing potential. Equine Vet J 38 (2006) 467-478
46. Battut I., Colchen S., Fieni F., Tainturier D., and Bruyas J.-F. Success rates when attempting to nonsurgically collect equine embryos at 144, 156 or 168 h after ovulation. Equine Vet J Suppl 25 (1997) 60-62
47. th Int Symp Equine Emb Transf. Havemeyer Fdtn Monograph Series No. 3 (2001), R&W Publications, Newmarket 66-68
48. Betteridge K.J., and Fléchon J.-E. Anatomy and physiology of pre-attachment bovine embryos. Theriogenology 29 (1988) 155-187
49. Fléchon J.-E., Degrouard J., Fléchon B., Lefèvre F., and Traub O. Gap junction formation and connexion distribution in pig trophoblast before implantation. Placenta 25 (2004) 85-94
50. Enders A.C., Schlafke S., Lantz K.C., and Liu K.M. Endoderm cells of the equine yolk sac from Day 7 until formation of the definitive yolk sac placenta. Equine Vet J Suppl 15 (1993) 3-9
51. Stout T.A.E., Meadows S., and Allen W.R. Stage-specific formation of the equine blastocyst capsule is instrumental to hatching and to embryonic survival in vivo. Anim Reprod Sci 87 (2005) 269-281
52. Oriol J.G., Betteridge K.J., Clarke A.E., and Sharom F.J. Mucin-like glycoproteins in the equine embryonic capsule. Mol Reprod Dev 34 (1993) 255-265
53. Oriol J.G., Sharom F.J., and Betteridge K.J. Developmentally regulated changes in the glycoproteins of the equine embryonic capsule. J Reprod Fertil 99 (1993) 653-664
54. Albihn A., Waelchli R.O., Samper J., Oriol J.G., Croy B.A., and Betteridge K.J. Production of capsular material by equine trophoblast transplanted into immunodeficient mice. Reproduction 125 (2003) 855-863
55. Pollack G.H. Cells, Gels, and the Engines of Life: a New Unifying Approach to Cell Function (2001), Ebner and Sons, Seattle, WA, USA pp. 113-129
56. Ginther O.J. Reproductive Biology of the Mare: Basic and Applied Aspects. Second edn (1992), Equiservices Publishing, Cross Plains, WI, USA
57. Waelchli R.O., and Betteridge K.J. Osmolality of equine blastocyst fluid from Day 11 to Day 25 of pregnancy. Reprod Fertil Dev 8 (1996) 981-988
58. Watson A.J., Natale D.R., and Barcroft L.C. Molecular regulation of blastocyst formation. Anim Reprod Sci 82-83 (2004) 583-592
59. Crews LJ, Waelchli RO, Huang CX, Canny MJ, McCully ME, Betteridge KJ. Electrolyte distribution and yolk-sac morphology in frozen hydrated equine conceptuses during the second week of pregnancy (Under revision).
60. Waelchli R.O., Jaworski T., Ruddock W.D.J., and Betteridge K.J. Estimation of sodium and potassium concentrations in the uterine fluid of mares by microdialysis and ion chromatography. J Reprod Fertil Suppl 56 (2000) 327-332
61. Hochi S., Ogasawara M., Braun J., and Oguri N. Influence of relative embryonic volumes during glycerol equilibration on the survival of frozen-thawed equine blastocysts. J Reprod Dev 40 (1994) 243-249
62. Hochi S., Fujimoto T., and Oguri N. Large equine blastocysts are damaged by vitrification procedures. Reprod Fertil Dev 7 (1995) 113-117
63. Guillomot M., and Betteridge K.J. Permeability of the capsule of the equine embryo. Proc Soc Study Fertil Winter Meeting (1984) Abstr 58
64. Ginther O.J. Fixation and orientation of the early equine conceptus. Theriogenology 19 (1983) 613-623
65. Ginther O.J. Dynamic physical interactions between the equine conceptus and uterus. Equine Vet J Suppl 3 (1985) 41-47
66. McDowell K.J., Sharp D.C., Grubaugh W., Thatcher W.W., and Wilcox C.J. Restricted conceptus mobility results in failure of pregnancy maintenance in mare. Biol Reprod 39 (1988) 340-348
67. Stewart F., Charleston B., Crossett B., Barker P.J., and Allen W.R. A novel uterine protein that associates with the embryonic capsule in equids. J Reprod Fertil 105 (1995) 65-70
68. Müller-Schöttle F., Bogusz A., Grotzinger J., Herrler A., Krusche C.A., Beier-Hellwig K., et al. Full-length complementary DNA and the derived amino acid sequence of horse uteroglobin. Biol Reprod 66 (2002) 1723-1728
69. Herrler A., Stewart F., Crossett B., Pell J., Ellis P., Beier H., et al. Identification of proteins in the embryonic capsule. J Reprod Fertil Suppl 56 (2000) 601-606
70. Suire S., Stewart F., Beauchamp J., and Kennedy M.W. Uterocalin, a lipocalin provisioning the preattachment equine conceptus: fatty acid and retinol binding properties, and structural characterization. Biochem J 356 (2001) 369-376
71. Crossett B., Allen W.R., and Stewart F. A 19 kDa protein secreted by the endometrium of the mare is a novel member of the lipocalin family. Biochem J 320 Pt 1 (1996) 137-143
72. Crossett B., Suire S., Herrler A., Allen W.R., and Stewart F. Transfer of a uterine lipocalin from the endometrium of the mare to the developing equine conceptus. Biol Reprod 59 (1998) 483-490
73. Stewart F., Kennedy M.W., and Suire S. A novel uterine lipocalin supporting pregnancy in equids. Cell Mol Life Sci 57 (2000) 1373-1378
74. Quinn BA, Hayes MA, Waelchli RO, Kennedy MW, Betteridge KJ. Changes in major proteins in the embryonic capsule during immobilization (fixation) of the conceptus in the third week of pregnancy in the mare. Reproduction (in press).
75. Quinn B., Caswell D.E., Lillie B.N., Waelchli R.O., Betteridge K.J., and Hayes M.A. The GM2-activator protein is a major protein expressed by the encapsulated equine trophoblast. Anim Reprod Sci 94 (2006) 391-394
76. Herrler A., Pell J.M., Allen W.R., Beier H.M., and Stewart F. Horse conceptuses secrete insulin-like growth factor-binding protein 3. Biol Reprod 62 (2000) 1804-1811
77. Goff A.K., Leduc S., Poitras P., and Vaillancourt D. Steroid synthesis by equine conceptuses between days 7 and 14 and endometrial steroid metabolism. Domest Anim Endocrinol 10 (1993) 229-236
78. Raeside J.I., Christie H.L., Renaud R.L., Waelchli R.O., and Betteridge K.J. Estrogen metabolism in the equine conceptus and endometrium during early pregnancy in relation to estrogen concentrations in yolk-sac fluid. Biol Reprod 71 (2004) 1120-1127
79. Stout T.A.E., and Allen W.R. Prostaglandin E(2) and F(2 alpha) production by equine conceptuses and concentrations in conceptus fluids and uterine flushings recovered from early pregnant and dioestrous mares. Reproduction 123 (2002) 261-268
80. Marsan C., Goff A.K., Sirois J., and Betteridge K.J. Steroid secretion by different cell types of the horse conceptus. J Reprod Fertil Suppl 35 (1987) 363-369
81. King B.F., and Enders A.C. Comparative development of the mammalian yolk sac. In: Nogales F.F. (Ed). The Human Yolk Sac and Yolk Sac Tumors (1993), Springer-Verlag, Berlin 1-32
82. Jauniaux E., Poston L., and Burton G.J. Placental-related diseases of pregnancy: Involvement of oxidative stress and implications in human evolution. Hum Reprod Update 12 (2006) 747-755
83. Ruddock W.D.J., Crews L.J., Waelchli R.O., and Betteridge K.J. Fructose accumulation by the equine conceptus during the second to fourth weeks of gestation. Theriogenology 53 (2000) Abstr. 286
84. Chu J.W., Sharom F.J., Oriol J.G., Betteridge K.J., Cleaver B.D., and Sharp D.C. Biochemical changes in the equine capsule following prostaglandin-induced pregnancy failure. Mol Reprod Dev 46 (1997) 286-295
85. Arar S., Chan K.C., Quinn B.A., Waelchli R.O., Hayes M.A., Betteridge K.J., et al. Desialylation of core type 1 O-glycan in the equine embryonic capsule coincides with immobilization of the conceptus in the uterus. Carbohydr Res 342 (2007) 1110-1115
86. Silva L.A., and Ginther O.J. An early endometrial vascular indicator of completed orientation of the embryo and the role of dorsal endometrial encroachment in mares. Biol Reprod 74 (2006) 337-343
87. Morris L.H., and Allen W.R. Reproductive efficiency of intensively managed Thoroughbred mares in Newmarket. Equine Vet J 34 (2002) 51-60
88. Betteridge K.J., Waelchli R.O., Christie H.L., Raeside J.I., Quinn B.A., and Hayes M.A. Effects of luteolysis on conceptus development during the second and third weeks of pregnancy in the mare. Anim Reprod Sci 94 (2006) 383-386
89. Kastelic J.P., Adams G.P., and Ginther O.J. Role of progesterone in mobility, fixation, orientation and survival of the equine embryonic vesicle. Theriogenology 27 (1987) 655-662
90. Enders A.C., and Liu I.K. Lodgement of the equine blastocyst in the uterus from fixation through endometrial cup formation. J Reprod Fertil Suppl 44 (1991) 427-438
91. Denker H.-W., Betteridge K.J., and Sirois J. Shedding of the capsule and proteinase activity in the horse. J Reprod Fertil Suppl 35 (1987) 708 (Abstr)
92. Ewart J.C. Studies of the development of the horse. I. The development during the third week. Trans R Soc Edin 51 (1915) 287-329 + plates and figures
93. th Int Symp Equine Emb Transf. Havemeyer Fdn Monograph Series No. 14 (2005), R&W Publications, Newmarket 3-4
94. Fabra M., Raldua D., Bozzo M.G., Deen P.M., Lubzens E., and Cerda J. Yolk proteolysis and aquaporin-1o play essential roles to regulate fish oocyte hydration during meiosis resumption. Dev Biol 295 (2006) 250-262
95. Clarke H.G., Hope S.A., Byers S., and Rodgers R.J. Formation of ovarian follicular fluid may be due to the osmotic potential of large glycosaminoglycans and proteoglycans. Reproduction 132 (2006) 119-131
96. Wilson C.A., and Davies D.C. The control of sexual differentiation of the reproductive system and brain. Reproduction 133 (2007) 331-359
97. Hartman C.G. Research should spell fun. J Reprod Fertil Suppl 2 (1967) 1-10
98. Hartman C.G., Lewis W.H., Miller F.W., and Swett W.W. First findings of tubal ova in the cow, together with notes on oestrus. Anat Rec 48 (1931) 267-275
99. Flood P.F., Betteridge K.J., and Diocee M.S. Transmission electron microscopy of horse embryos 3-16 days after ovulation. J Reprod Fertil Suppl 32 (1982) 319-327