Proteome of the early embryo-maternal dialogue in the cattle uterus

Journal of Proteome Research

Volumn 11, Issue 2, 2012, Pages 751-766

  Muñoz, Marta ^a   Corrales, Fernando J ^b   Caamaño, José N ^a   Díez, Carmen ^a   Trigal, Beatriz ^a   Mora, María I ^b   Martín, David ^a   Carrocera, Susana ^a   Gómez, Enrique ^a  

^a Área de Cultivos Hortofrutícolas y Forestales   (Spain)

^b UNIVERSITY OF NAVARRA   (Spain)

Author keywords

bovine; development; embryo; Interleukin 1Beta; NFkB; TNF; uterus

Indexed keywords

ALBUMIN; HEPATOMA DERIVED GROWTH FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INSULIN; INTERLEUKIN 1BETA; LACTOFERRIN; LIPOCORTIN 4; PEROXIREDOXIN; PROGESTERONE; PROTEOME; PURINE NUCLEOSIDE PHOSPHORYLASE; SYNAPTOTAGMIN; TUMOR NECROSIS FACTOR ALPHA; TWINFILIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ARTIFICIAL INSEMINATION; CATTLE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; FEMALE; GLYCOSYLATION; IMMUNOCYTOCHEMISTRY; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MOTHER FETUS RELATIONSHIP; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROGESTERONE BLOOD LEVEL; PROTEIN ANALYSIS; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; SIGNAL TRANSDUCTION; TWO DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS; UPREGULATION; UTERUS; UTERUS FLUID; WESTERN BLOTTING;

ANIMALS; BLASTOCYST; BLOTTING, WESTERN; BODY FLUIDS; CATTLE; CELL COUNT; CHROMATOGRAPHY, LIQUID; CLUSTER ANALYSIS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FEMALE; INTERLEUKIN-1BETA; MALE; NF-KAPPA B; PREGNANCY; PROTEOME; PROTEOMICS; REPRODUCIBILITY OF RESULTS; TANDEM MASS SPECTROMETRY; TUMOR NECROSIS FACTOR-ALPHA; UTERUS;

ANIMALIA; BOS; BOVINAE; MAMMALIA;

EID: 84856637803     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr200969a     Document Type: Article

References (108)

1. Schultz, G. A.; Heyner, S. Growth factors in preimplantation mammalian embryos Oxf. Rev. Reprod. Biol. 1993, 15, 43-81
2. Harlow, G. M.; Quinn, P. Development of preimplantation mouse embryos in vivo and in vitro Aust. J. Biol. Sci. 1982, 35 (2) 187-93
3. Farin, C. E.; Farmer, W. T.; Farin, P. W. Pregnancy recognition and abnormal offspring syndrome in cattle Reprod. Fertil. Dev. 2010, 22 (1) 75-87
4. Watkins, A. J.; Fleming, T. P. Blastocyst environment and its influence on offspring cardiovascular health: the heart of the matter J. Anat. 2009, 215 (1) 52-9
5. Havlicek, V.; Kuzmany, A.; Cseh, S.; Brem, G.; Besenfelder, U. The effect of long-term in vivo culture in bovine oviduct and uterus on the development and cryo-tolerance of in vitro produced bovine embryos Reprod. Domest. Anim. 2010, 45 (5) 832-7
6. Lonergan, P.; Pedersen, H. G.; Rizos, D.; Greve, T.; Thomsen, P. D.; Fair, T.; Evans, A.; Boland, M. P. Effect of the post-fertilization culture environment on the incidence of chromosome aberrations in bovine blastocysts Biol. Reprod. 2004, 71 (4) 1096-100
7. Rizos, D.; Ward, F.; Duffy, P.; Boland, M. P.; Lonergan, P. Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality Mol. Reprod. Dev. 2002, 61 (2) 234-48
8. Diskin, M. G.; Morris, D. G. Embryonic and early foetal losses in cattle and other ruminants Reprod. Domest. Anim. 2008, 43 (Suppl 2) 260-7
9. Inskeep, E. K.; Dailey, R. A. Embryonic death in cattle Vet. Clin. North Am. Food Anim. Pract. 2005, 21 (2) 437-61
10. Looney, C. R.; Nelson, J. S.; Schneider, H. J.; Forrest, D. W. Improving fertility in beef cow recipients Theriogenology 2006, 65 (1) 201-9
11. Wolf, E.; Arnold, G. J.; Bauersachs, S.; Beier, H. M.; Blum, H.; Einspanier, R.; Frohlich, T.; Herrler, A.; Hiendleder, S.; Kolle, S.; Prelle, K.; Reichenbach, H. D.; Stojkovic, M.; Wenigerkind, H.; Sinowatz, F. Embryo-maternal communication in bovine-strategies for deciphering a complex cross-talk Reprod. Domest. Anim. 2003, 38 (4) 276-89
12. Hunter, R. H. Modulation of gamete and embryonic microenvironments by oviduct glycoproteins Mol. Reprod. Dev. 1994, 39 (2) 176-81
13. Gardner, D. S.; Ozanne, S. E.; Sinclair, K. D. Effect of the early-life nutritional environment on fecundity and fertility of mammals Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2009, 364 (1534) 3419-27
14. Leese, H. J.; Hugentobler, S. A.; Gray, S. M.; Morris, D. G.; Sturmey, R. G.; Whitear, S. L.; Sreenan, J. M. Female reproductive tract fluids: composition, mechanism of formation and potential role in the developmental origins of health and disease Reprod. Fertil. Dev. 2008, 20 (1) 1-8
15. McMillen, I. C.; MacLaughlin, S. M.; Muhlhausler, B. S.; Gentili, S.; Duffield, J. L.; Morrison, J. L. Developmental origins of adult health and disease: the role of periconceptional and foetal nutrition Basic Clin. Pharmacol. Toxicol. 2008, 102 (2) 82-9
16. Han, H.; Hansen, T. R.; Berg, B.; Hess, B. W.; Ford, S. P. Maternal undernutrition induces differential cardiac gene expression in pulmonary hypertensive steers at high elevation Am. J. Physiol. Heart Circ. Physiol. 2008, 295 (1) H382-9
17. Martin, J. L.; Vonnahme, K. A.; Adams, D. C.; Lardy, G. P.; Funston, R. N. Effects of dam nutrition on growth and reproductive performance of heifer calves J. Anim. Sci. 2007, 85 (3) 841-7
18. Vonnahme, K. A.; Zhu, M. J.; Borowicz, P. P.; Geary, T. W.; Hess, B. W.; Reynolds, L. P.; Caton, J. S.; Means, W. J.; Ford, S. P. Effect of early gestational undernutrition on angiogenic factor expression and vascularity in the bovine placentome J. Anim. Sci. 2007, 85 (10) 2464-72
19. Berendt, F. J.; Frohlich, T.; Schmidt, S. E.; Reichenbach, H. D.; Wolf, E.; Arnold, G. J. Holistic differential analysis of embryo-induced alterations in the proteome of bovine endometrium in the preattachment period Proteomics 2005, 5 (10) 2551-60
20. Forde, N.; Carter, F.; Spencer, T. E.; Bazer, F. W.; Sandra, O.; Mansouri-Attia, N.; Okumu, L. A.; McGettigan, P. A.; Mehta, J. P.; McBride, R.; O'Gaora, P.; Roche, J. F.; Lonergan, P. Conceptus-induced changes in the endometrial transcriptome: how soon does the cow know she is pregnant? Biol. Reprod. 2011, 85 (1) 144-56
21. Beltman, M. E.; Forde, N.; Furney, P.; Carter, F.; Roche, J. F.; Lonergan, P.; Crowe, M. A. Characterisation of endometrial gene expression and metabolic parameters in beef heifers yielding viable or non-viable embryos on Day 7 after insemination Reprod. Fertil. Dev. 2010, 22 (6) 987-99
22. Koch, J. M.; Ramadoss, J.; Magness, R. R. Proteomic profile of uterine luminal fluid from early pregnant ewes J. Proteome Res. 2010, 9 (8) 3878-85
23. Gomez, E.; Rodriguez, A.; Munoz, M.; Caamano, J. N.; Carrocera, S.; Martin, D.; Facal, N.; Diez, C. Development and quality of bovine morulae cultured in serum-free medium with specific retinoid receptor agonists Reprod. Fertil. Dev. 2008, 20 (8) 884-91
24. Hidalgo, C. O.; Gomez, E.; Prieto, L.; Duque, P.; Goyache, F.; Fernandez, L.; Fernandez, I.; Facal, N.; Diez, C. Pregnancy rates and metabolic profiles in cattle treated with propylene glycol prior to embryo transfer Theriogenology 2004, 62 (3-4) 664-76
25. Thouas, G. A.; Korfiatis, N. A.; French, A. J.; Jones, G. M.; Trounson, A. O. Simplified technique for differential staining of inner cell mass and trophectoderm cells of mouse and bovine blastocysts Reprod. Biomed. Online 2001, 3 (1) 25-29
26. Gomez, E.; Rodriguez, A.; Munoz, M.; Caamano, J. N.; Hidalgo, C. O.; Moran, E.; Facal, N.; Diez, C. Serum free embryo culture medium improves in vitro survival of bovine blastocysts to vitrification Theriogenology 2008, 69 (8) 1013-21
27. Santamaria, E.; Avila, M. A.; Latasa, M. U.; Rubio, A.; Martin-Duce, A.; Lu, S. C.; Mato, J. M.; Corrales, F. J. Functional proteomics of nonalcoholic steatohepatitis: mitochondrial proteins as targets of S-adenosylmethionine Proc. Natl. Acad. Sci. U.S.A. 2003, 100 (6) 3065-70
28. Colinge, J.; Masselot, A.; Giron, M.; Dessingy, T.; Magnin, J. OLAV: Towards high-throughput tandem mass spectrometry data identification Proteomics 2003, 3 (8) 1454-63
29. Lee, R S. F.; Wheeler, T. T.; Peterson, A. J. Large-format, two-dimensional polyacrylamide gel electrophoresis of ovine periimplantation uterine luminal fluid proteins: identification of aldose reductase, cytoplasmic actin, and transferrin as conceptus-synthesized proteins Biol. Reprod. 1998, 59 (4) 743-52
30. Munoz, M.; Rodriguez, A.; De Frutos, C.; Caamano, J. N.; Diez, C.; Facal, N.; Gomez, E. Conventional pluripotency markers are unspecific for bovine embryonic-derived cell-lines Theriogenology 2008, 69 (9) 1159-64
31. Ledgard, A. M.; Lee, R. S.; Peterson, A. J. Bovine endometrial legumain and TIMP-2 regulation in response to presence of a conceptus Mol. Reprod. Dev. 2009, 76 (1) 65-74
32. Herzyk, D. J.; Berger, A. E.; Allen, J. N.; Wewers, M. D. Sandwich ELISA formats designed to detect 17 kDa IL-1 beta significantly underestimate 35 kDa IL-1 beta J. Immunol. Methods 1992, 148 (1-2) 243-54
33. Bermejo-Alvarez, P.; Rizos, D.; Lonergan, P.; Gutierrez-Adan, A. Transcriptional sexual dimorphism during preimplantation embryo development and its consequences for developmental competence and adult health and disease Reproduction 2011, 141 (5) 563-70
34. Ghosh, S.; May, M. J.; Kopp, E. B. NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses Annu. Rev. Immunol. 1998, 16, 225-60
35. Ali, S.; Mann, D. A. Signal transduction via the NF-kappaB pathway: a targeted treatment modality for infection, inflammation and repair Cell Biochem. Funct. 2004, 22 (2) 67-79
36. Herath, S.; Lilly, S. T.; Fischer, D. P.; Williams, E. J.; Dobson, H.; Bryant, C. E.; Sheldon, I. M. Bacterial lipopolysaccharide induces an endocrine switch from prostaglandin F2alpha to prostaglandin E2 in bovine endometrium Endocrinology 2009, 150 (4) 1912-20
37. Rodrigues, A.; Queiroz, D. B.; Honda, L.; Silva, E. J.; Hall, S. H.; Avellar, M. C. Activation of toll-like receptor 4 (TLR4) by in vivo and in vitro exposure of rat epididymis to lipopolysaccharide from Escherichia Coli Biol. Reprod. 2008, 79 (6) 1135-47
38. Ibeagha-Awemu, E. M.; Lee, J. W.; Ibeagha, A. E.; Bannerman, D. D.; Paape, M. J.; Zhao, X. Bacterial lipopolysaccharide induces increased expression of toll-like receptor (TLR) 4 and downstream TLR signaling molecules in bovine mammary epithelial cells Vet Res 2008, 39 (2) 11
39. Farnaud, S.; Evans, R. W. Lactoferrin - a multifunctional protein with antimicrobial properties Mol. Immunol. 2003, 40 (7) 395-405
40. Tsan, M. F.; Gao, B. Endogenous ligands of Toll-like receptors J. Leukoc. Biol. 2004, 76 (3) 514-9
41. Bauersachs, S.; Blum, H.; Mallok, S.; Wenigerkind, H.; Rief, S.; Prelle, K.; Wolf, E. Regulation of ipsilateral and contralateral bovine oviduct epithelial cell function in the postovulation period: a transcriptomics approach Biol. Reprod. 2003, 68 (4) 1170-7
42. Scotchie, J. G.; Fritz, M. A.; Mocanu, M.; Lessey, B. A.; Young, S. L. Proteomic analysis of the luteal endometrial secretome Reprod. Sci. 2009, 16 (9) 883-93
43. Sherry, B.; Jue, D. M.; Zentella, A.; Cerami, A. Characterization of high molecular weight glycosylated forms of murine tumor necrosis factor Biochem. Biophys. Res. Commun. 1990, 173 (3) 1072-8
44. Olszewski, M. B.; Groot, A. J.; Dastych, J.; Knol, E. F. TNF trafficking to human mast cell granules: mature chain-dependent endocytosis J. Immunol. 2007, 178 (9) 5701-9
45. Zolti, M.; Ben-Rafael, Z.; Meirom, R.; Shemesh, M.; Bider, D.; Mashiach, S.; Apte, R. N. Cytokine involvement in oocytes and early embryos Fertil. Steril. 1991, 56 (2) 265-72
46. Pampfer, S.; Wuu, Y. D.; Vanderheyden, I.; De Hertogh, R. Expression of tumor necrosis factor-alpha (TNF alpha) receptors and selective effect of TNF alpha on the inner cell mass in mouse blastocysts Endocrinology 1994, 134 (1) 206-12
47. Sharkey, A. M.; Dellow, K.; Blayney, M.; Macnamee, M.; Charnock-Jones, S.; Smith, S. K. Stage-specific expression of cytokine and receptor messenger ribonucleic acids in human preimplantation embryos Biol. Reprod. 1995, 53 (4) 974-81
48. Sheth, K. V.; Roca, G. L.; al-Sedairy, S. T.; Parhar, R. S.; Hamilton, C. J.; al-Abdul Jabbar, F. Prediction of successful embryo implantation by measuring interleukin-1-alpha and immunosuppressive factor(s) in preimplantation embryo culture fluid Fertil. Steril. 1991, 55 (5) 952-7
49. Takacs, P.; Kauma, S. The expression of interleukin-1 alpha, interleukin-1 beta, and interleukin-1 receptor type I mRNA during preimplantation mouse development J. Reprod. Immunol. 1996, 32 (1) 27-35
50. Kruessel, J. S.; Huang, H. Y.; Wen, Y.; Kloodt, A. R.; Bielfeld, P.; Polan, M. L. Different pattern of interleukin-1 beta-(IL-1 beta), interleukin-1 receptor antagonist- (IL-1ra) and interleukin-1 receptor type I- (IL-1R tI) mRNA-expression in single preimplantation mouse embryos at various developmental stages J. Reprod. Immunol. 1997, 34 (2) 103-20
51. Ross, J. W.; Malayer, J. R.; Ritchey, J. W.; Geisert, R. D. Characterization of the interleukin-1beta system during porcine trophoblastic elongation and early placental attachment Biol. Reprod. 2003, 69 (4) 1251-9
52. Barañao, R. I.; Piazza, A.; Rumi, L. S.; Polak de Fried, E. Interleukin-1 beta levels in human embryo culture supernatants and their predictive values for pregnancy Early Hum. Dev. 1997, 48 (1-2) 71-80
53. Okuda, K.; Sakumoto, R.; Okamoto, N.; Acosta, T. J.; Abe, H.; Okada, H.; Sinowatz, F.; Skarzynski, D. J. Cellular localization of genes and proteins for tumor necrosis factor-alpha (TNF), TNF receptor types I and II in bovine endometrium Mol. Cell. Endocrinol. 2010, 330 (1-2) 41-8
54. Grell, M.; Douni, E.; Wajant, H.; Lohden, M.; Clauss, M.; Maxeiner, B.; Georgopoulos, S.; Lesslauer, W.; Kollias, G.; Pfizenmaier, K.; Scheurich, P. The transmembrane form of tumor necrosis factor is the prime activating ligand of the 80 kDa tumor necrosis factor receptor Cell 1995, 83 (5) 793-802
55. Cobb, S. P.; Watson, E. D. Immunohistochemical study of immune cells in the bovine endometrium at different stages of the oestrous cycle Res. Vet. Sci. 1995, 59 (3) 238-41
56. Tartaglia, L. A.; Goeddel, D. V. Two TNF receptors Immunol. Today 1992, 13 (5) 151-3
57. Ihnatko, R.; Kubes, M. TNF signaling: early events and phosphorylation Gen. Physiol. Biophys. 2007, 26 (3) 159-67
58. Cavaillon, J. M.; Haeffner-Cavaillon, N. [Cytokines and inflammation] Rev. Prat. 1993, 43 (5) 547-52
59. de Hemptinne, V.; Rondas, D.; Toepoel, M.; Vancompernolle, K. Phosphorylation on Thr-106 and NO-modification of glyoxalase I suppress the TNF-induced transcriptional activity of NF-kappaB Mol. Cell. Biochem. 2009, 325 (1-2) 169-78
60. Sezen, D.; Bongiovanni, A. M.; Gelber, S.; Perni, U.; Hutson, J. M.; Skupski, D.; Witkin, S. S. Gelsolin down-regulates lipopolysaccharide-induced intraamniotic tumor necrosis factor-alpha production in the midtrimester of pregnancy Am. J. Obstet. Gynecol. 2009, 200 (2) 191 e1-4
61. Suzuki, K.; Hasegawa, T.; Sakamoto, C.; Zhou, Y. M.; Hato, F.; Hino, M.; Tatsumi, N.; Kitagawa, S. Cleavage of mitogen-activated protein kinases in human neutrophils undergoing apoptosis: role in decreased responsiveness to inflammatory cytokines J. Immunol. 2001, 166 (2) 1185-92
62. Li, J.; Yin, H. L.; Yuan, J. Flightless-I regulates proinflammatory caspases by selectively modulating intracellular localization and caspase activity J. Cell Biol. 2008, 181 (2) 321-33
63. Perrier, S.; Coussediere, C.; Dubost, J. J.; Albuisson, E.; Sauvezie, B. IL-1 receptor antagonist (IL-1RA) gene polymorphism in Sjogren's syndrome and rheumatoid arthritis Clin. Immunol. Immunopathol. 1998, 87 (3) 309-13
64. Solomon, A.; Dursun, D.; Liu, Z.; Xie, Y.; Macri, A.; Pflugfelder, S. C. Pro- and anti-inflammatory forms of interleukin-1 in the tear fluid and conjunctiva of patients with dry-eye disease Invest. Ophthalmol. Vis. Sci. 2001, 42 (10) 2283-92
65. Tabibzadeh, S.; Sun, X. Z. Cytokine expression in human endometrium throughout the menstrual cycle Hum. Reprod. 1992, 7 (9) 1214-21
66. Huang, H. Y.; Wen, Y.; Kruessel, J. S.; Raga, F.; Soong, Y. K.; Polan, M. L. Interleukin (IL)-1beta regulation of IL-1beta and IL-1 receptor antagonist expression in cultured human endometrial stromal cells J. Clin. Endocrinol. Metab. 2001, 86 (3) 1387-93
67. Simon, C.; Piquette, G. N.; Frances, A.; Polan, M. L. Localization of interleukin-1 type I receptor and interleukin-1 beta in human endometrium throughout the menstrual cycle J. Clin. Endocrinol. Metab. 1993, 77 (2) 549-55
68. Groebner, A. E.; Rubio-Aliaga, I.; Schulke, K.; Reichenbach, H. D.; Daniel, H.; Wolf, E.; Meyer, H. H.; Ulbrich, S. E. Increase of essential amino acids in the bovine uterine lumen during preimplantation development Reproduction 2011, 141 (5) 685-95
69. Eytan, O.; Elad, D. Analysis of intra-uterine fluid motion induced by uterine contractions Bull. Math Biol. 1999, 61 (2) 221-38
70. Velazquez, M. A.; Parrilla, I.; Van Soom, A.; Verberckmoes, S.; Kues, W.; Niemann, H. Sampling techniques for oviductal and uterine luminal fluid in cattle Theriogenology 2010, 73 (6) 758-67
71. Leung, S. T.; Derecka, K.; Mann, G. E.; Flint, A. P.; Wathes, D. C. Uterine lymphocyte distribution and interleukin expression during early pregnancy in cows J. Reprod. Fertil. 2000, 119 (1) 25-33
72. Oliveira, L. J.; Hansen, P. J. Deviations in populations of peripheral blood mononuclear cells and endometrial macrophages in the cow during pregnancy Reproduction 2008, 136 (4) 481-90
73. Ideta, A.; Hayama, K.; Nakamura, Y.; Sakurai, T.; Tsuchiya, K.; Tanaka, S.; Yamaguchi, T.; Fujiwara, H.; Imakawa, K.; Aoyagi, Y. Intrauterine administration of peripheral blood mononuclear cells enhances early development of the pre-implantation bovine embryo Mol. Reprod. Dev. 2010, 77 (11) 954-62
74. Casado-Vela, J.; Rodriguez-Suarez, E.; Iloro, I.; Ametzazurra, A.; Alkorta, N.; García-Velasco, J. A.; Matorral, R.; Prieto, B.; González, S.; Nagore, D.; Simón, L.; Elortza, F. Comprehensive proteomic analysis of human endometrial fluid aspirate J. Proteome Res. 2009, 8 (10) 4622-32
75. Ametzazurra, A.; Matorral, R.; García-Velasco, J. A.; Prieto, B.; Simón, L.; Martínez, A.; Nagore, D. Endometrial fluid is a specific and non-invasive biological sample for protein biomarker identification in endometriosis Hum. Reprod. 2009, 24 (4) 954-65
76. Hannan, N. J.; Stephens, A. N.; Rainczuk, A.; Hincks, C.; Rombauts, L. J.; Salamonsen, L. A. 2D-DiGE analysis of the human endometrial secretome reveals differences between receptive and nonreceptive states in fertile and infertile women J. Proteome Res. 2010, 9 (12) 6256-64
77. Kishima, Y.; Yamamoto, H.; Izumoto, Y.; Yoshida, K.; Enomoto, H.; Yamamoto, M.; Kuroda, T.; Ito, H.; Yoshizaki, K.; Nakamura, H. Hepatoma-derived growth factor stimulates cell growth after translocation to the nucleus by nuclear localization signals J. Biol. Chem. 2002, 277 (12) 10315-22
78. Tse, P. K.; Lee, Y. L.; Chow, W. N.; Luk, J. M.; Lee, K. F.; Yeung, W. S. Preimplantation embryos cooperate with oviductal cells to produce embryotrophic inactivated complement-3b Endocrinology 2008, 149 (3) 1268-76
79. Jang, H. H.; Kim, S. Y.; Park, S. K.; Jeon, H. S.; Lee, Y. M.; Jung, J. H.; Lee, S. Y.; Chae, H. B.; Jung, Y. J.; Lee, K. O.; Lim, C. O.; Chung, W. S.; Bahk, J. D.; Yun, D. J.; Cho, M. J.; Lee, S. Y. Phosphorylation and concomitant structural changes in human 2-Cys peroxiredoxin isotype I differentially regulate its peroxidase and molecular chaperone functions FEBS Lett. 2006, 580 (1) 351-5
80. Kang, S. W.; Chae, H. Z.; Seo, M. S.; Kim, K.; Baines, I. C.; Rhee, S. G. Mammalian peroxiredoxin isoforms can reduce hydrogen peroxide generated in response to growth factors and tumor necrosis factor-alpha J. Biol. Chem. 1998, 273 (11) 6297-302
81. Deroo, B. J.; Hewitt, S. C.; Peddada, S. D.; Korach, K. S. Estradiol regulates the thioredoxin antioxidant system in the mouse uterus Endocrinology 2004, 145 (12) 5485-92
82. Bing, Y. Z.; Hirao, Y.; Takenouchi, N.; Che, L. M.; Nakamura, H.; Yodoi, J.; Nagai, T. Effects of thioredoxin on the preimplantation development of bovine embryos Theriogenology 2003, 59 (3-4) 863-73
83. Ozawa, M.; Nagai, T.; Fahrudin, M.; Karja, N. W.; Kaneko, H.; Noguchi, J.; Ohnuma, K.; Kikuchi, K. Addition of glutathione or thioredoxin to culture medium reduces intracellular redox status of porcine IVM/IVF embryos, resulting in improved development to the blastocyst stage Mol. Reprod. Dev. 2006, 73 (8) 998-1007
84. Yang, S.; Luo, A.; Hao, X.; Lai, Z.; Ding, T.; Ma, X.; Mayinuer, M.; Shen, W.; Wang, X.; Lu, Y.; Ma, D.; Wang, S. Peroxiredoxin 2 Inhibits Granulosa Cell Apoptosis During Follicle Atresia Through the NFKB Pathway in Mice Biol. Reprod. 2011, 84 (6) 1182-9
85. Wu, W. X.; Derks, J. B.; Zhang, Q.; Nathanielsz, P. W. Changes in heat shock protein-90 and -70 messenger ribonucleic acid in uterine tissues of the ewe in relation to parturition and regulation by estradiol and progesterone Endocrinology 1996, 137 (12) 5685-93
86. Mangurten, A. B.; Brader, K. R.; Loos, B. M.; Lee, E.; Quiroga, A. I.; Bathori, J.; Lurain, J. R.; Laszlo, A.; Phillips, B. Hsp70 and Hsc70 are preferentially expressed in differentiated epithelial cells in normal human endometrium and ectocervix Cell Stress Chaperones 1997, 2 (3) 168-74
87. Tabibzadeh, S.; Broome, J. Heat shock proteins in human endometrium throughout the menstrual cycle Infect. Dis. Obstet. Gynecol. 1999, 7 (1-2) 5-9
88. Vydra, N.; Winiarski, B.; Rak-Raszewska, A.; Piglowski, W.; Mazurek, A.; Scieglinska, D.; Widlak, W. The expression pattern of the 70-kDa heat shock protein Hspa2 in mouse tissues Histochem. Cell Biol. 2009, 132 (3) 319-30
89. Khan, K. N.; Kitajima, M.; Imamura, T.; Hiraki, K.; Fujishita, A.; Sekine, I.; Ishimaru, T.; Masuzaki, H. Toll-like receptor 4-mediated growth of endometriosis by human heat-shock protein 70 Hum. Reprod. 2008, 23 (10) 2210-9
90. Chehna-Patel, N.; Warty, N.; Sachdeva, G.; Khole, V. Proteolytic tailoring of the heat shock protein 70 and its implications in the pathogenesis of endometriosis Fertil. Steril. 2011, 95 (5) 1560-7-e1-3
91. Shiokawa, S.; Sakai, K.; Akimoto, Y.; Suzuki, N.; Hanashi, H.; Nagamatsu, S.; Iwashita, M.; Nakamura, Y.; Hirano, H.; Yoshimura, Y. Function of the small guanosine triphosphate-binding protein RhoA in the process of implantation J. Clin. Endocrinol. Metab. 2000, 85 (12) 4742-9
92. Ponnampalam, A. P.; Rogers, P. A. Cyclic changes and hormonal regulation of annexin IV mRNA and protein in human endometrium Mol. Hum. Reprod. 2006, 12 (11) 661-9
93. Katoh, N. Detection of annexins I and IV in bronchoalveolar lavage fluids from calves inoculated with bovine herpes virus-1 J. Vet. Med. Sci. 2000, 62 (1) 37-41
94. Gotoh, M.; Takamoto, Y.; Kurosaka, K.; Masuda, J.; Ida, M.; Satoh, A.; Takayama, E.; Kojima-Aikawa, K.; Kobayashi, Y.; Matsumoto, I. Annexins I and IV inhibit Staphylococcus aureus attachment to human macrophages Immunol. Lett. 2005, 98 (2) 297-302
95. Roberts, R. M. Conceptus interferons and maternal recognition of pregnancy Biol. Reprod. 1989, 40 (3) 449-52
96. Spencer, T. E.; Sandra, O.; Wolf, E. Genes involved in conceptus-endometrial interactions in ruminants: insights from reductionism and thoughts on holistic approaches Reproduction 2008, 135 (2) 165-79
97. Martin, J. C.; Jasper, M. J.; Valbuena, D.; Meseguer, M.; Remohi, J.; Pellicer, A.; Simon, C. Increased adhesiveness in cultured endometrial-derived cells is related to the absence of moesin expression Biol. Reprod. 2000, 63 (5) 1370-6
98. Gray, C. A.; Abbey, C. A.; Beremand, P. D.; Choi, Y.; Farmer, J. L.; Adelson, D. L.; Thomas, T. L.; Bazer, F. W.; Spencer, T. E. Identification of endometrial genes regulated by early pregnancy, progesterone, and interferon tau in the ovine uterus Biol. Reprod. 2006, 74 (2) 383-94
99. Chen, Y.; Antoniou, E.; Liu, Z.; Hearne, L. B.; Roberts, R. M. A microarray analysis for genes regulated by interferon-tau in ovine luminal epithelial cells Reproduction 2007, 134 (1) 123-35
100. Bauersachs, S.; Ulbrich, S. E.; Gross, K.; Schmidt, S. E.; Meyer, H. H.; Wenigerkind, H.; Vermehren, M.; Sinowatz, F.; Blum, H.; Wolf, E. Embryo-induced transcriptome changes in bovine endometrium reveal species-specific and common molecular markers of uterine receptivity Reproduction 2006, 132 (2) 319-31
101. Roberts, R. M.; Chen, Y.; Ezashi, T.; Walker, A. M. Interferons and the maternal-conceptus dialog in mammals Semin. Cell Dev. Biol. 2008, 19 (2) 170-7
102. Ross, J. W.; Ashworth, M. D.; Mathew, D.; Reagan, P.; Ritchey, J. W.; Hayashi, K.; Spencer, T. E.; Lucy, M.; Geisert, R. D. Activation of the transcription factor, nuclear factor kappa-B, during the estrous cycle and early pregnancy in the pig Reprod. Biol. Endocrinol. 2010, 8, 39
103. Groebner, A. E.; Schulke, K.; Unterseer, S.; Reichenbach, H. D.; Reichenbach, M.; Buttner, M.; Wolf, E.; Meyer, H. H.; Ulbrich, S. E. Enhanced proapoptotic gene expression of XAF1, CASP8 and TNFSF10 in the bovine endometrium during early pregnancy is not correlated with augmented apoptosis Placenta 2010, 31 (3) 168-77
104. Ideta, A.; Nakamura, Y.; Tsuchiya, K.; Fujiwara, H.; Yamaguchi, T.; Imakawa, K. a.; Aoyagi, Y. Bovine embryo-maternal recognition may occur earlier in ai than in embryo transfer (ET) Reprod., Fertil. Dev. 2010, 23 (1) 162
105. Ulbrich, S. E.; Meyer, S. U.; Zitta, K.; Hiendleder, S.; Sinowatz, F.; Bauersachs, S.; Buttner, M.; Frohlich, T.; Arnold, G. J.; Reichenbach, H. D.; Wolf, E.; Meyer, H. H. Bovine endometrial metallopeptidases MMP14 and MMP2 and the metallopeptidase inhibitor TIMP2 participate in maternal preparation of pregnancy Mol. Cell. Endocrinol. 2011, 332 (1-2) 48-57
106. Dunne, L. D.; Diskin, M. G.; Sreenan, J. M. Embryo and foetal loss in beef heifers between day 14 of gestation and full term Anim. Reprod. Sci. 2000, 58 (1-2) 39-44
107. Walsh, S. W.; Williams, E. J.; Evans, A. C. A review of the causes of poor fertility in high milk producing dairy cows Anim. Reprod. Sci. 2011, 123 (3-4) 127-38
108. Lonergan, P.; Rizos, D.; Kanka, J.; Nemcova, L.; Mbaye, A. M.; Kingston, M.; Wade, M.; Duffy, P.; Boland, M. P. Temporal sensitivity of bovine embryos to culture environment after fertilization and the implications for blastocyst quality Reproduction 2003, 126 (3) 337-46