Equine oviduct explant culture: A basic model to decipher embryo-maternal communication

Reproduction, Fertility and Development

Volumn 26, Issue 7, 2014, Pages 954-966

  Nelis, Hilde ^a   D'Herde, Katharina ^b   Goossens, Karen ^a   Vandenberghe, Lynn ^a   Leemans, Bart ^a   Forier, Katrien ^a   Smits, Katrien ^a   Braeckmans, Kevin ^a   Peelman, Luc ^a   Van Soom, Ann ^a  

^a GHENT UNIVERSITY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

Author keywords

dark cell degeneration; horse

Indexed keywords

GLUCOSE; LACTIC ACID; MICRORNA; PROTEOME; TRANSCRIPTOME;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DEGENERATION; CELL DIFFERENTIATION; CELL HYPOXIA; CELL MEMBRANE; CELL NUCLEUS; COLUMNAR EPITHELIUM; CONTROLLED STUDY; EMBRYO; EMBRYO MATERNAL COMMUNICATION; EMBRYO RESEARCH; EPITHELIUM CELL; EQUIDAE; EXPLANT; FEMALE; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; GLUT1 GENE; HIF1A GENE; IN VITRO STUDY; LAMINA PROPRIA; MARKER GENE; MICROSCOPY; NONHUMAN; NUCLEOLUS; NUCLEOTIDE SEQUENCE; OVIDUCT; PAI1 GENE; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSMISSION ELECTRON MICROSCOPY; UPA GENE; UPREGULATION; VEGFA GENE; ANIMAL; ANIMAL EMBRYO; BIOLOGICAL MODEL; CULTURE TECHNIQUE; CYTOLOGY; EMBRYOLOGY; GENETICS; HORSE; METABOLISM; MUCOSA; PHYSIOLOGY; PROCEDURES; STROMA CELL; TIME; TUNEL ASSAY; ULTRASTRUCTURE; UTERINE TUBE; VETERINARY;

ANIMALS; APOPTOSIS; CELL CULTURE TECHNIQUES; CELL HYPOXIA; EMBRYO, MAMMALIAN; EPITHELIAL CELLS; FALLOPIAN TUBES; FEMALE; GENE EXPRESSION; GLUCOSE; HORSES; IN SITU NICK-END LABELING; LACTIC ACID; MICROSCOPY, ELECTRON, TRANSMISSION; MODELS, BIOLOGICAL; MUCOUS MEMBRANE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STROMAL CELLS; TIME FACTORS; TRANSCRIPTOME;

EID: 84906238320     PISSN: 10313613     EISSN: 14485990     Source Type: Journal    
DOI: 10.1071/RD13089     Document Type: Article

References (80)

1. Abe, H., and Hoshi, H. (1997). Bovine oviductal epithelial cells: their cell culture and applications in studies for reproductive biology. Cytotechnology 23, 171-183. doi:10.1023/A:1007929826186
2. Ball, B. A., and Miller, P. G. (1992). Survival of equine embryos co-cultured with equine oviductal epithelium from the 4-cell to 8-cell to the blastocyst stage after transfer to synchronous recipient mares. Theriogenology 37(5), 979-991. doi:10.1016/0093-691X(92)90097-B
3. Ball, B. A., Altschul, M., and Ellington, J. E. (1991). In vitro development of Day-2 equine embryos co-cultured with oviductal explants or trophoblastic vesicles. Theriogenology 35(3), 669-682. doi:10.1016/0093- 691X(91)90462-M
4. Ball, B. A., Brinsko, S. P., Thomas, P. G. A., Miller, P. G., and Ellington, J. E. (1993). Development to blastocysts of one-cell to 2-cell equine embryos after co-culture with uterine tubal epithelial cells. Am. J. Vet. Res. 54(7), 1139-1144.
5. Barenberg, P., Strahlendorf, H., and Strahlendorf, J. (2001). Hypoxia induces an excitotoxic-type of dark-cell degeneration in cerebellar Purkinje neurons. Neurosci. Res. 40(3), 245-254. doi:10.1016/S0168- 0102(01)00234-6
6. Bavister,B.D. (1995).Culture of preimplantationembryos: facts and artefacts. Hum. Reprod. Update 1(2), 91-148. doi:10.1093/HUMUPD/1.2.91
7. Blasi, F. (1997). uPA, uPAR, PAI-I: key intersection of proteolytic, adhesive and chemotactic highways? Immunol. Today 18, 415-417. doi:10.1016/ S0167-5699(97)01121-3
8. Bogaert, L., Van Poucke, M., De Baere, C., Peelman, L., Gasthuys, F., and Martens, A. (2006). Selection of a set of reliable reference genes for quantitative real-time PCR in normal equine skin and in equine sarcoids. BMC Biotechnol. 6, 24. doi:10.1186/1472-6750-6-24
9. Brinsko, S. P., Ball, B. A., Miller, P. G., Thomas, P. G. A., and Ellington, J. E. (1994). In vitro development of Day-2 embryos obtained from young, fertile mares and aged, subfertile mares. J. Reprod. Fertil. 102(2), 371-378. doi:10.1530/JRF.0.1020371
10. Buhi, W. C. (2002). Characterization and biological roles of oviductspecific, oestrogen-dependent glycoprotein. Reproduction 123(3), 355-362. doi:10.1530/REP.0.1230355
11. Buhi, W. C., Alvarez, I. M., and Kouba, A. J. (2000). Secreted proteins of the oviduct. Cells Tissues Organs 166(2), 165-179. doi:10.1159/000016731
12. Bustin, S.A., Benes, V., Garson, J.A., Hellemans, J., Huggett, J.,Kubista,M., Mueller, R., Nolan, T., Pfaffl, M. W., Shipley, G. L., Vandesompele, J., and Wittwer, C. T. (2009). The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 55, 611-622. doi:10.1373/CLINCHEM.2008.112797
13. Campbell, D. L., Douglas, L. W., and Ramge, J. C. (1979). Cannulation of the equine oviduct and chemical analysis of oviduct fluid. Theriogenology 12, 47-59. doi:10.1016/0093-691X(79)90009-8
14. Cappelli, K., Felicetti, M., Capomaccio, S., Spinsanti, G., Silvestrelli, M., and Supplizi, A. V. (2008). Exercise-induced stress in horses: selection of the most-stable reference genes for quantitative RT-PCR normalization. BMC Mol. Biol. 9, 49. doi:10.1186/1471-2199-9-49
15. Carmeliet, P., Mackman, N., Moons, L., Luther, T., Gressens, P., VanVlaenderen, I., Demunck, H., Kasper, M., Breier, G., Evrard, P., Muller, M., Risau, W., Edgington, T., and Collen, D. (1996). Role of tissue factor in embryonic blood-vessel development. Nature 383(6595), 73-75. doi:10.1038/383073A0
16. Chi, J. T., Wang, Z., Nuyten, D. S. A., Rodriguez, E. H., Schaner, M. E., Salim,A.,Wang, Y., Kristensen, G. B.,Helland,A., Borresen-Dale,A. L., Giaccia, A., Longaker,M. T., Hastie, T., Yang, G. P., van de Vijver, M. J., and Brown, P. O. (2006). Gene-expression programs in response to hypoxia: cell-type specificity and prognostic significance in human cancers. PLoS Med. 3, e47. doi:10.1371/JOURNAL.PMED.0030047
17. Choi, Y. H., Roasa, L. M., Love, C. C., Varner, D. D., Brinsko, S., and Hinrichs, K. (2004). Blastocyst formation rates in vivo and in vitro of in vitro-matured equine oocytes fertilized by intracytoplasmic sperm injection. Biol. Reprod. 70(5), 1231-1238. doi:10.1095/BIOLREPROD. 103.023903
18. Choi, Y. H., Love, C. C., Varner, D. D., and Hinrichs, K. (2006). Equine blastocyst development after intracytoplasmic injection of sperm subjected to two freeze-thaw cycles. Theriogenology 65(4), 808-819. doi:10.1016/J. THERIOGENOLOGY.2005.04.035
19. Cox, C. I., and Leese, H. J. (1997). Retention of functional characteristics by bovine oviduct and uterine epithelia in vitro. Anim. Reprod. Sci. 46, 169-178. doi:10.1016/S0378-4320(96)01621-1
20. De Pauw, I.M., Van Soom, A., Laevens, H.,Verberckmoes, S., and de Kruif, A. (2002). Sperm binding to epithelial oviduct explants in bulls with different non-return rates investigated with a new in vitro model. Biol. Reprod. 67(4), 1073-1079. doi:10.1095/BIOLREPROD67.4.1073
21. DePauw, I.M. C.,VanSoom,A.,Maes, D.,Verberckmoes, S., anddeKruif, A. (2003). Effect of sperm coating on the survival and penetrating ability of in vitro-stored bovine spermatozoa. Theriogenology 59(5-6), 1109-1122. doi:10.1016/S0093-691X(02)01186-X
22. Dobrinski, I., Jacob, J. R., Tennant, B. C., and Ball, B. A. (1999). Generation of an equine oviductal epithelial cell line for the study of sperm-oviduct interactions. Theriogenology 52, 875-885. doi:10.1016/S0093-691X (99)00179-X
23. Eyestone, W. H., and First, N. L. (1989). Co-culture of early cattle embryos to the blastocyst stage with oviductal tissue or in conditioned medium. J. Reprod. Fertil. 85(2), 715-720. doi:10.1530/JRF.0.0850715
24. Eyestone, W. H., Jones, J. M., and First, N. L. (1991). Some factors affecting the efficacy of oviduct tissue-conditioned medium for the culture of early bovine embryos. J. Reprod. Fertil. 92(1), 59-64. doi:10.1530/JRF. 0.0920059
25. Fan, X., Heijnen, C. J., van der Kooij, M. A., Groenendaal, F., and van Bel, F. (2009). The role and regulation of hypoxia-inducible factor-1 alpha expression in brain development and neonatal hypoxic-ischemic brain injury. Brain Res. Brain Res. Rev. 62(1), 99-108. doi:10.1016/J.BRAIN RESREV.2009.09.006
26. Faul, F., Erdfelder, E., Lang, A.-G., and Buchner, A. (2007). G*Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav. Res. Methods 39(2), 175-191.
27. Ferrara, N., Carver-Moore, K., Chen, H., Dowd, M., Lu, L., O'Shea, K. S., Powell-Braxton, L., Hillan, K. J., and Moore, M. W. (1996). Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 380, 439-442. doi:10.1038/380439A0
28. Fischer, B., and Bavister, B. D. (1993). Oxygen tension in the oviduct and uterus of Rhesus monkeys, hamsters and rabbits. J. Reprod. Fertil. 99(2), 673-679. doi:10.1530/JRF.0.0990673
29. Gabler, C., Einspanier, A., Schams, D., and Einspanier, R. (1999). Expression of vascular endothelial growth factor (VEGF) and its corresponding receptors (flt-1 and flk-1) in the bovine oviduct. Mol. Reprod. Dev. 53, 376-383. doi:10.1002/(SICI)1098-2795(199908) 53:4,376::AID-MRD2.3.0.CO;2-Z
30. Gabler, C., Killian, G. J., and Einspanier, R. (2001). Differential expression of extracellular matrix components in the bovine oviduct during the oestrous cycle. Reproduction 122, 121-130. doi:10.1530/REP.0. 1220121
31. Garner, D. L., Johnson, L. A., Yue, S. T., Roth, B. L., and Haugland, R. P. (1994). Dual DNA staining assessment of bovine sperm viability using Sybr-14 and propidium iodide. J. Androl. 15(6), 620-629.
32. Gjørret, J. O., Fabian, D., Avery, B., and Maddox-Hyttel, P. (2007). Active caspase-3 and ultrastructural evidence of apoptosis in spontaneous and induced cell death in bovine in vitro-produced pre-implantation embryos. Mol. Reprod. Dev. 74, 961-971. doi:10.1002/MRD.20714
33. Goossens, J. F., Foulon,C.,Villard,A. L., Puy, J.Y.,Lefebvre, I., Perigaud,C., Vaccher, C., and Bonte, J. P. (2005). Column selection and method development for the separation of nucleoside phosphotriester diastereoisomers, new potential anti-viral drugs. Application to cellular extract analysis. Biomed. Chromatogr. 19, 415-425. doi:10.1002/BMC.500
34. Hahn, T., Barth, S., Weiss, U., Mosgoeller, W., and Desoye, G. (1998). Sustained hyperglycaemia in vitro down-regulates the GLUT1 glucose transport system of cultured human term placental trophoblast: a mechanism to protect fetal development? FASEB J. 12, 1221-1231.
35. Hardy, K., and Spanos, S. (2002). Growth factor expression and function in the human and mouse preimplantation embryo. J. Endocrinol. 172(2), 221-236. doi:10.1677/JOE.0.1720221
36. Hardy, K., Wright, C., Rice, S., Tachataki, M., Roberts, R., Morgan, D., Spanos, S., and Taylor, D. (2002). Future developments in assisted reproduction in humans. Reproduction 123(2), 171-183. doi:10.1530/ REP.0.1230171
37. Hinrichs, K. (2010). In vitro production of equine embryos: state of the art. Reprod. Domest. Anim. 45, 3-8. doi:10.1111/J.1439-0531.2010. 01624.X
38. Hinrichs, K., and Choi, Y.-H. (2005). Assisted reproductive techniques in the horse. Clinical techniques in equine practice 4, 210-218. doi:10.1053/J.CTEP.2005.07.002
39. Holm, P., Walker, S. K., and Seamark, R. F. (1996). Embryo viability, duration of gestation and birth weight in sheep after transfer of in vitromatured and in vitro-fertilized zygotes cultured in vitro or in vivo. J. Reprod. Fertil. 107(2), 175-181. doi:10.1530/JRF.0.1070175
40. Kouba, A. J., Burkhardt, B. R., Alvarez, I. M., Goodenow, M. M., and Buhi, W. C. (2000). Oviductal plasminogen activator inhibitor-1 (PAI-1): mRNA, protein and hormonal regulation during the oestrous cycle and early pregnancy in the pig. Mol. Reprod. Dev. 56, 378-386. doi:10.1002/ 1098-2795(200007)56:3,378: :AID-MRD8.3.0.CO;2-B
41. Krysko, D. V., Vanden Berghe, T., D'Herde, K., and Vandenabeele, P. (2008). Apoptosis and necrosis: detection, discrimination and phagocytosis. Methods 44, 205-221. doi:10.1016/J.YMETH.2007.12.001
42. Leclerc, E., Sakai, Y., and Fujii, T. (2003). Cell culture in 3-dimensional microfluidic structure of PDMS (polydimethylsiloxane). Biomed. Microdevices 5, 109-114. doi:10.1023/A:1024583026925
43. Leese, H. J., Alexiou, M., Comer, M. T., Lamb, V. K., and Thompson, J. G. (1995). Assessment of embryo nutritional requirements and role of co-culture techniques. Adv. Rep. End. 7, 11-23.
44. Leist, M., and Jaattela, M. (2001). Four deaths and a funeral: from caspases to alternative mechanisms. Nat. Rev. Mol. Cell Biol. 2, 589-598. doi:10.1038/35085008
45. Lenth, R. V. (2007). Statistical power calculations. J. Anim. Sci. 85(13 suppl), E24-E29. doi:10.2527/JAS.2006-449
46. Liao, H., Hyman, M. C., Lawrence, D. A., and Pinsky, D. J. (2007). Molecular regulation of the PAI-1 gene by hypoxia: contributions of Egr-1, HIF-1 alpha and C/EBP alpha. FASEB J. 21(3), 935-949. doi:10.1096/FJ.06-6285COM
47. Lonergan, P., Sharif, H., Monaghan, P., Wahid, H., Gallagher, M., and Gordon, I. (1991). Factors affecting embryo yield following maturation, fertilization and culture in vitro of bovine oocytes. Isr. J. Agric. Res. 30(1), 78.
48. Luo, H. L., Kimura, K., Aoki, M., and Hirako, M. (2002). Vascular endothelial growth factor (VEGF) promotes the early development of bovine embryo in the presence of cumulus cells. J. Vet. Med. Sci. 64, 967-971. doi:10.1292/JVMS.64.967
49. Menck, M.C., Guyader-Joly, C., Peynot, N., Le Bourhis, D., Lobo, R. B., Renard, J. P., and Heyman, Y. (1997). Beneficial effects of Vero cells for developing IVF bovine eggs in two different co-culture systems. Reprod. Nutr. Dev. 37(2), 141-150. doi:10.1051/RND:19970202
50. Merkl, M., Ulbrich, S. E., Otzdorff, C., Herbach, N., Wanke, R., Wolf, E., Handler, J., and Bauersachs, S. (2010). Microarray analysis of equine endometrium at Days 8 and 12 of pregnancy. Biol. Reprod. 83(5), 874-886. doi:10.1095/BIOLREPROD.110.085233
51. Misener, S., Krawetz, S., Rozen, S., and Skaletsky, H. (1999). Primer3 on the WWW for general users and for biologist programmers. In 'Bioinformatics Methods and Protocols.' (Eds S. Misener and S. Krawetz). pp. 365-386. (Humana Press: Merelbeke, Belgium)
52. Mishra, S., Lei, Z. M., and Rao, C. V. (2003). A novel role of luteinizing hormone in the embryo development in co-cultures. Biol. Reprod. 68, 1455-1462. doi:10.1095/BIOLREPROD.102.011874
53. Namura, S., Zhu, J. M., Fink, K., Endres, M., Srinivasan, A., Tomaselli, K. J., Yuan, J. Y., and Moskowitz, M. A. (1998). Activation and cleavage of caspase-3 in apoptosis induced by experimental cerebral ischemia. J. Neurosci. 18, 3659-3668.
54. Nelis, H. M., Goossens, K., Leemans, B., Peelman, L., and Van Soom, A. (2012). Steroid-regulatedmRNAexpression in oviduct epithelial cells in the mare. Reprod. Fertil. Dev. 25(1), Abstract 220.
55. Nelis, H. M., Vanden Bussche, J., Goossens, K., Vanhaecke, L., Vandenberghe, L., Leemans, B., Peelman, L., and Van Soom, A. (2013). Postovulatory concentrations of progesterone and b-oestradiol in the equine oviduct are upregulating mRNA expression of PAI1, CSF and MMP1 both in vivo and in an explant model in vitro. In 'Proceedings of the 1st general meeting of COST action FA1201, Epiconcept: Epigenetics and Periconception environment, Antalya, Turkey, 24-25 April 2013. (Eds A. Van Soom, A. Fazeli, M. Kuran). P. 56. (Faculty of Agriculture, Ondokuz Mayis University: Samsun.)
56. Pierson, R. A., and Ginther, O. J. (1985). Ultrasonic evaluation of the corpus luteum of the mare. Theriogenology 23, 795-806. doi:10.1016/0093- 691X(85)90155-4
57. Raleigh, J. A., Calkins-Adams, D. P., Rinker, L. H., Ballenger, C. A., Weissler, M. C., Fowler, W. C., Novotny, D. B., and Varia, M. A. (1998). Hypoxia and vascular endothelial growth factor expression in human squamous cell carcinomas using pimonidazole as a hypoxia marker. Cancer Res. 58, 3765-3768.
58. Reischl, J., Prelle, K., Schol, H., Neumuller, C., Einspanier, R., Sinowatz, F., and Wolf, E. (1999). Factors affecting proliferation and dedifferentiation of primary bovine oviduct epithelial cells in vitro. Cell Tissue Res. 296, 371-383. doi:10.1007/S004410051297
59. Roach, H. I., and Clarke, N. M. P. (2000). Physiological cell death of chondrocytes in vivo is not confined to apoptosis-new observations on the mammalian growth plate. J. Bone Joint Surg. Br. 82, 601-613. doi:10.1302/0301-620X.82B4.9846
60. Rottmayer, R., Ulbrich, S. E., Kolle, S., Prelle, K., Neumueller, C., Sinowatz, F., Meyer, H. H. D., Wolf, E., and Hiendleder, S. (2006). A bovine oviduct epithelial cell suspension culture system suitable for studying embryo-maternal interactions: morphological and functional characterization. Reproduction 132, 637-648. doi:10.1530/REP.1. 01136
61. Shweiki, D., Itin, A., Soffer, D., and Keshet, E. (1992). Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 359, 843-845. doi:10.1038/359843A0
62. Smits, K. G. K., Van Soom, A., Govaere, J., Hoogewijs, M., Vanhaesebrouck, E., Galli, C., Colleoni, S., Vandesompele, J., and Peelman, L. (2009). Selection of reference genes for quantitative realtime PCR in equine in vivo and fresh and frozen-thawed in vitro blastocysts. BMC Res. Notes 2, 246. doi:10.1186/1756-0500-2-246
63. Smits, K., Goossens, K., Van Soom, A., Govaere, J., Hoogewijs, M., and Peelman, L. J. (2011). In vivo-derived horse blastocysts show transcriptional upregulation of developmentally important genes compared with in vitro-produced horse blastocysts. Reprod. Fertil. Dev. 23, 364-375. doi:10.1071/RD10124
64. Smits, K., Govaere, J., Hoogewijs, M., Piepers, S., and Van Soom, A. (2012). A pilot comparison of laser-assisted vs piezo drill ICSI for the in vitro production of horse embryos. Reprod. Domest. Anim. 47(1), e1-e3. doi:10.1111/J.1439-0531.2011.01814.X
65. Stadelmann, C., and Lassmann, H. (2000). Detection of apoptosis in tissue sections. Cell Tissue Res. 301, 19-31. doi:10.1007/S004410000203
66. Tadokoro, C., Yoshimoto, Y., Sakata, M., Imai, T., Yamaguchi, M., Kurachi, H., Oka, Y., Maeda, T., and Miyake, A. (1995). Expression and localization of glucose-transporter-1 (Glut1) in the rat oviduct-A possible supplier of glucose to embryo during early embryonic development. Biochem. Biophys. Res. Commun. 214, 1211-1218. doi:10.1006/BBRC.1995.2415
67. Thibodeaux, J.K.,Myers,M.W.,Goodeaux, L. L.,Menezo,Y.,Roussel, J.D., Broussard, J. R., and Godke, R. A. (1992a). Evaluating an in vitro culture system of bovine uterine and oviduct epithelial cells for subsequent embryo co-culture. Reprod. Fertil. Dev. 4, 573-583. doi:10.1071/ RD9920573
68. Thomas, P. G. A., Ignotz, G. G., Ball, B. A., Miller, P. G., Brinsko, S. P., and Currie, B. (1995). Isolation, culture and characterization of equine oviduct epithelial cells in vitro. Mol. Reprod. Dev. 41, 468-478. doi:10.1002/MRD.1080410409
69. Ulbrich, S. E., Kettler, A., and Einspanier, R. (2003). Expression and localization of oestrogen receptor alpha, oestrogen receptor beta and progesterone receptor in the bovine oviduct in vivo and in vitro. J. Steroid Biochem. Mol. Biol. 84, 279-289. doi:10.1016/S0960-0760(03)00039-6
70. Ulbrich, S. E., Groebner, A. E., and Bauersachs, S. (2013). Transcriptional profiling to address molecular determinants of endometrial receptivity-lessons from studies in livestock species. Methods 59(1), 108-115. doi:10.1016/J.YMETH.2012.10.013
71. Vandaele, L., Mateusen, B., Maes, D. G. D., de Kruif, A., and van Soom, A. (2007). Temporal detection of caspase-3 and-7 in bovine in vitroproduced embryos of different developmental capacity. Reproduction 133, 709-718. doi:10.1530/REP-06-0109
72. Vander Heiden, M. G., Cantley, L. C., and Thompson, C. B. (2009). Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324, 1029-1033. doi:10.1126/SCIENCE.1160809
73. Van Soom, A., Van Vlaenderen, I., Mahmoudzadeh, A. R., Deluyker, H., and de Kruif, A. (1992). Compaction rate of in vitro-fertilized bovine embryos related to the interval from insemination to first cleavage. Theriogenology 38(5), 905-919. doi:10.1016/0093-691X(92)90165-N
74. Walter, I. (1995a). Culture of bovine oviduct epithelial cells (BOEC). Anat. Rec. 243, 347-356. doi:10.1002/AR.1092430309
75. Wijayagunawardane, M. P. B., Kodithuwakku, S. P., Yamamoto, D., and Miyamoto, A. (2005). Vascular endothelial growth factor system in the cow oviduct: a possible involvement in the regulation of oviductal motility and embryo transport. Mol. Reprod. Dev. 72, 511-520. doi:10.1002/MRD.20379
76. Wrenzycki, C., Herrmann, D., Lemme, E., Korsawe, K., Carnwath, J. W., and Niemann, H. (1998). Transcriptional level of developmentally important genes in bovine preimplantation embryos generated in vitro. Theriogenology 49, 191 [Abstract]. doi:10.1016/S0093-691X(98) 90544-1
77. Wrenzycki, C., Herrmann, D., Keskintepe, L., Martins, A., Sirisathien, S., Brackett, B., and Niemann, H. (2001). Effects of culture system and protein supplementation on mRNA expression in pre-implantation bovine embryos. Hum. Reprod. 16(5), 893-901. doi:10.1093/HUM REP/16.5.893
78. Wydooghe, E., Vandaele, L., Beek, J., Favoreel, H., Heindryckx, B., De Sutter, P., and Van Soom, A. (2011). Differential apoptotic staining of mammalian blastocysts based on double immunofluorescent CDX2 and active caspase-3 staining. Anal. Biochem. 416, 228-230. doi:10.1016/ J.AB.2011.05.033
79. Yuan, Y. Q., Van Soom, A., Coopman, F. O. J., Mintiens, K., Boerjan, M. L., Van Zeveren, A., de Kruif, A., and Peelman, L. J. (2003). Influence of oxygen tension on apoptosis and hatching in bovine embryos cultured in vitro. Theriogenology 59(7), 1585-1596. doi:10.1016/S0093-691X (02)01204-9
80. Zuker, M. (2003). Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31, 3406-3415. doi:10.1093/NAR/ GKG595