Proteomic profile of uterine luminal fluid from early pregnant ewes

Journal of Proteome Research

Volumn 9, Issue 8, 2010, Pages 3878-3885

  Koch, Jill M ^a   Ramadoss, Jayanth ^b   Magness, Ronald R ^b,c  

^a Perinatal Research Laboratories   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

early pregnancy; embryo; histotroph; proteomic profile; sheep; uterine luminal fluid

Indexed keywords

PLACENTA PROTEIN; PLACENTA PROTEIN PP9; PROTEIN; TRANSGELIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; EMBRYO DEVELOPMENT; EWE; FEMALE; FIRST TRIMESTER PREGNANCY; FLUSHING; GESTATIONAL AGE; GROWTH; IMMUNE SYSTEM; IMMUNOBLOTTING; IMMUNOREGULATION; LIQUID CHROMATOGRAPHY; LIQUID CHROMATOGRAPHY MASS SPECTROMETRY; MASS SPECTROMETRY; NONHUMAN; NUTRITION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEOMICS; UTERUS FLUID; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CHROMATOGRAPHY, ION EXCHANGE; CHROMATOGRAPHY, LIQUID; EMBRYO, MAMMALIAN; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; PREGNANCY; PROTEINS; PROTEOMICS; SHEEP; TANDEM MASS SPECTROMETRY; UTERUS; WISCONSIN;

OVIS ARIES;

EID: 77955454380     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr100096b     Document Type: Article

References (64)

1. Ashworth, C. J.; Bazer, F. W. Changes in ovine conceptus and endometrial function following asynchronous embryo transfer or administration of progesterone Biol. Reprod. 1989, 40 (2) 425-33
2. Roberts, R. M. Conceptus interferons and maternal recognition of pregnancy Biol. Reprod. 1989, 40 (3) 449-52
3. Bolet, G. Timing and extent of embryonic mortality in pigs, sheep and goats: Genetic variability. In Embryonic Mortality in Farm Animals; Sreenan, J. M., Ed.; Current topics in veterinary medicine and animal science, Vol. 34; M. Nijhoff: Dordrecht, the Netherlands, 1986; pp 12 - 43.
4. Dixon, A. B.; Knights, M.; Winkler, J. L.; Marsh, D. J.; Pate, J. L.; Wilson, M. E.; Dailey, R. A.; Seidel, G.; Inskeep, E. K. Patterns of late embryonic and fetal mortality and association with several factors in sheep J. Anim. Sci. 2007, 85 (5) 1274-84
5. Spencer, T. E.; Johnson, G. A.; Bazer, F. W.; Burghardt, R. C. Implantation mechanisms: Insights from the sheep Reproduction 2004, 128 (6) 657-68
6. Igwebuike, U. M. Trophoblast cells of ruminant placentas - A minireview Anim. Reprod. Sci. 2006, 93 (3-4) 185-98
7. Gao, H.; Wu, G.; Spencer, T. E.; Johnson, G. A.; Li, X.; Bazer, F. W. Select nutrients in the ovine uterine lumen. I. Amino acids, glucose, and ions in uterine lumenal flushings of cyclic and pregnant ewes Biol. Reprod. 2009, 80 (1) 86-93
8. Gao, H.; Wu, G.; Spencer, T. E.; Johnson, G. A.; Bazer, F. W. Select nutrients in the ovine uterine lumen. II. Glucose transporters in the uterus and peri-implantation conceptuses Biol. Reprod. 2009, 80 (1) 94-104
9. Godkin, J. D.; Bazer, F. W.; Moffatt, J.; Sessions, F.; Roberts, R. M. Purification and properties of a major, low molecular weight protein released by the trophoblast of sheep blastocysts at day 13-21 J. Reprod. Fertil. 1982, 65 (1) 141-50
10. Roberts, R. M. A novel group of interferons associated with the early ovine and bovine embryo J. Interferon Res. 1989, 9 (4) 373-8
11. Spencer, T. E.; Johnson, G. A.; Burghardt, R. C.; Bazer, F. W. Progesterone and placental hormone actions on the uterus: Insights from domestic animals Biol. Reprod. 2004, 71 (1) 2-10
12. Lee, R. S.; 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
13. Gibson, T. C.; Phernetton, T. M.; Wiltbank, M. C.; Magness, R. R. Development and use of an ovarian synchronization model to study the effects of endogenous estrogen and nitric oxide on uterine blood flow during ovarian cycles in sheep Biol. Reprod. 2004, 70 (6) 1886-94
14. Magness, R. R.; Shaw, C. E.; Phernetton, T. M.; Zheng, J.; Bird, I. M. Endothelial vasodilator production by uterine and systemic arteries. II. Pregnancy effects on NO synthase expression Am. J. Physiol. 1997, 272 (4 Pt 2) H1730-40
15. Martin, S. E.; Shabanowitz, J.; Hunt, D. F.; Marto, J. A. Subfemtomole MS and MS/MS peptide sequence analysis using nano-HPLC micro-ESI fourier transform ion cyclotron resonance mass spectrometry Anal. Chem. 2000, 72 (18) 4266-74
16. Ramadoss, J.; Liao, W. X.; Chen, D. B.; Magness, R. R., High-throughput caveolar proteomic signature profile for maternal binge alcohol consumption. Alcohol 2010, DOI: 10.1016/j.alcohol.2009.10.010.
17. Vanden Wymelenberg, A.; Gaskell, J.; Mozuch, M.; Sabat, G.; Ralph, J.; Skyba, O.; Mansfield, S. D.; Blanchette, R. A.; Martinez, D.; Grigoriev, I.; Kersten, P. J.; Cullen, D. Comparative transcriptome and secretome analysis of wood decay fungi Postia placenta and Phanerochaete chrysosporium Appl. Environ. Microbiol. 2010, 76 (11) 3599-610
18. Sun, S.; Meyer-Arendt, K.; Eichelberger, B.; Brown, R.; Yen, C. Y.; Old, W. M.; Pierce, K.; Cios, K. J.; Ahn, N. G.; Resing, K. A. Improved validation of peptide MS/MS assignments using spectral intensity prediction Mol. Cell. Proteomics 2007, 6 (1) 1-17
19. Wang, J.; Perez-Santiago, J.; Katz, J. E.; Mallick, P.; Bandeira, N. Peptide identification from mixture tandem mass spectra Mol. Cell. Proteomics 2010, 9, 1476-85
20. Lowenstein, J. M. Molecular phylogenetics Annu. Rev. Earth Planet Sci. 1986, 14, 71-83
21. Kijas, J. W.; Menzies, M.; Ingham, A. Sequence diversity and rates of molecular evolution between sheep and cattle genes Anim. Genet. 2006, 37 (2) 171-4
22. Keller, A.; Nesvizhskii, A. I.; Kolker, E.; Aebersold, R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search Anal. Chem. 2002, 74 (20) 5383-92
23. Nesvizhskii, A. I.; Keller, A.; Kolker, E.; Aebersold, R. A statistical model for identifying proteins by tandem mass spectrometry Anal. Chem. 2003, 75 (17) 4646-58
24. Stevenson, S. E.; Chu, Y.; Ozias-Akins, P.; Thelen, J. J. Validation of gel-free, label-free quantitative proteomics approaches: applications for seed allergen profiling J. Proteomics 2009, 72 (3) 555-66
25. Dasari, S.; Pereira, L.; Reddy, A. P.; Michaels, J. E.; Lu, X.; Jacob, T.; Thomas, A.; Rodland, M.; Roberts, C. T., Jr.; Gravett, M. G.; Nagalla, S. R. Comprehensive proteomic analysis of human cervical-vaginal fluid J. Proteome Res. 2007, 6 (4) 1258-68
26. Michaels, J. E.; Dasari, S.; Pereira, L.; Reddy, A. P.; Lapidus, J. A.; Lu, X.; Jacob, T.; Thomas, A.; Rodland, M.; Roberts, C. T., Jr.; Gravett, M. G.; Nagalla, S. R. Comprehensive proteomic analysis of the human amniotic fluid proteome: gestational age-dependent changes J. Proteome Res. 2007, 6 (4) 1277-85
27. Pereira, L.; Reddy, A. P.; Jacob, T.; Thomas, A.; Schneider, K. A.; Dasari, S.; Lapidus, J. A.; Lu, X.; Rodland, M.; Roberts, C. T., Jr.; Gravett, M. G.; Nagalla, S. R. Identification of novel protein biomarkers of preterm birth in human cervical-vaginal fluid J. Proteome Res. 2007, 6 (4) 1269-76
28. Zybailov, B.; Coleman, M. K.; Florens, L.; Washburn, M. P. Correlation of relative abundance ratios derived from peptide ion chromatograms and spectrum counting for quantitative proteomic analysis using stable isotope labeling Anal. Chem. 2005, 77 (19) 6218-24
29. Hearn, J. P. The embryo-maternal dialogue during early pregnancy in primates J. Reprod. Fertil. 1986, 76 (2) 809-19
30. Igwebuike, U. M. A review of uterine structural modifications that influence conceptus implantation and development in sheep and goats Anim. Reprod. Sci. 2009, 112 (1-2) 1-7
31. Riding, G. A.; Jones, A.; Holland, M. K.; Hill, J. R.; Lehnert, S. A. Proteomic analysis of bovine conceptus fluids during early pregnancy Proteomics 2008, 8 (1) 160-77
32. Ross, J. W.; Ashworth, M. D.; Stein, D. R.; Couture, O. P.; Tuggle, C. K.; Geisert, R. D. Identification of differential gene expression during porcine conceptus rapid trophoblastic elongation and attachment to uterine luminal epithelium Physiol. Genomics 2009, 36 (3) 140-8
33. Hu, J.; Spencer, T. E. Carbonic anhydrase regulate endometrial gland development in the neonatal uterus Biol. Reprod. 2005, 73 (1) 131-8
34. Camoretti-Mercado, B.; Forsythe, S. M.; LeBeau, M. M.; Espinosa, R., 3rd; Vieira, J. E.; Halayko, A. J.; Willadsen, S.; Kurtz, B.; Ober, C.; Evans, G. A.; Thweatt, R.; Shapiro, S.; Niu, Q.; Qin, Y.; Padrid, P. A.; Solway, J. Expression and cytogenetic localization of the human SM22 gene (TAGLN) Genomics 1998, 49 (3) 452-7
35. Kyama, C. M.; T'Jampens, D.; Mihalyi, A.; Simsa, P.; Debrock, S.; Waelkens, E.; Landuyt, B.; Meuleman, C.; Fulop, V.; Mwenda, J. M.; D'Hooghe, T. M. ProteinChip technology is a useful method in the pathogenesis and diagnosis of endometriosis: a preliminary study Fertil. Steril. 2006, 86 (1) 203-9
36. Inaba, N.; Renk, T.; Bohn, H. Immunohistochemical location of placental proteins (PP 8, 9, 10, 11, 12) in human term placentae Arch. Gynecol. 1980, 230 (2) 109-21
37. Huggett, A. S.; Nixon, D. A. Fructose as a component of the foetal blood in several mammalian species Nature 1961, 190, 1209
38. Sayegh, R.; Awwad, J. T.; Maxwell, C.; Lessey, B.; Isaacson, K. Alpha 2-macroglobulin production by the human endometrium J. Clin. Endocrinol. Metab. 1995, 80 (3) 1021-6
39. Sayegh, R. A.; Tao, X. J.; Leykin, L.; Isaacson, K. B. Endometrial alpha-2 macroglobulin; localization by in situ hybridization and effect on mouse embryo development in vitro J. Clin. Endocrinol. Metab. 1997, 82 (12) 4189-95
40. Fishelson, Z.; Attali, G.; Mevorach, D. Complement and apoptosis Mol. Immunol. 2001, 38 (2-3) 207-19
41. Girardi, G.; Bulla, R.; Salmon, J. E.; Tedesco, F. The complement system in the pathophysiology of pregnancy Mol. Immunol. 2006, 43 (1-2) 68-77
42. Roy, A. C.; Loke, D. F.; Saha, N.; Viegas, O. A.; Tay, J. S.; Ratnam, S. S. Interrelationships of serum paraoxonase, serum lipids and apolipoproteins in normal pregnancy. A longitudinal study Gynecol. Obstet. Invest. 1994, 38 (1) 10-3
43. Chappell, L. C.; Seed, P. T.; Briley, A. L.; Kelly, F. J.; Lee, R.; Hunt, B. J.; Parmar, K.; Bewley, S. J.; Shennan, A. H.; Steer, P. J.; Poston, L. Effect of antioxidants on the occurrence of pre-eclampsia in women at increased risk: A randomised trial Lancet 1999, 354 (9181) 810-6
44. Roberts, J. M.; Cooper, D. W. Pathogenesis and genetics of pre-eclampsia Lancet 2001, 357 (9249) 53-6
45. Palmer, J. L.; Abeles, R. H. The mechanism of action of S-adenosylhomocysteinase J. Biol. Chem. 1979, 254 (4) 1217-26
46. de la Calle, M.; Usandizaga, R.; Sancha, M.; Magdaleno, F.; Herranz, A.; Cabrillo, E. Homocysteine, folic acid and B-group vitamins in obstetrics and gynaecology Eur. J. Obstet. Gynecol. Reprod. Biol. 2003, 107 (2) 125-34
47. Schulz, L. C.; Bahr, J. M. Glucose-6-phosphate isomerase is necessary for embryo implantation in the domestic ferret Proc. Natl. Acad. Sci. U.S.A. 2003, 100 (14) 8561-6
48. Silliman, K.; Tall, A. R.; Kretchmer, N.; Forte, T. M. Unusual high-density lipoprotein subclass distribution during late pregnancy Metabolism 1993, 42 (12) 1592-9
49. Del Priore, G.; Chatterton, R. T., Jr.; Chandarana, A.; Silver, R. Comparison of maternal serum lipids before and during parturition Obstet. Gynecol. 1993, 82 (5) 837-40
50. Ndikum-Moffor, F. M.; Simmen, R. C.; Fields, P. A.; Katoh, N.; Oikawa, S.; Buhi, W. C.; Rollyson, M. K.; Chang, S. M.; Fields, M. J. Synthesis and messenger ribonucleic acid expression of apolipoproteins E and A-I by the bovine corpus luteum during the estrous cycle and pregnancy Biol. Reprod. 1997, 56 (3) 745-56
51. Rosing, U.; Samsioe, G.; Olund, A.; Johansson, B.; Kallner, A.; Serum levels of apolipoprotein, A.-I. A-II and HDL-cholesterol in second half of normal pregnancy and in pregnancy complicated by pre-eclampsia Horm. Metab. Res. 1989, 21 (7) 376-82
52. Thomas, T.; Macpherson, A.; Rogers, P. Ceruloplasmin gene expression in the rat uterus Biochim. Biophys. Acta 1995, 1261 (1) 77-82
53. Shaw, J. L.; Smith, C. R.; Diamandis, E. P. Proteomic analysis of human cervico-vaginal fluid J. Proteome Res. 2007, 6 (7) 2859-65
54. Casado-Vela, J.; Rodriguez-Suarez, E.; Iloro, I.; Ametzazurra, A.; Alkorta, N.; Garcia-Velasco, J. A.; Matorras, R.; Prieto, B.; Gonzalez, S.; Nagore, D.; Simon, L.; Elortza, F. Comprehensive proteomic analysis of human endometrial fluid aspirate J. Proteome Res. 2009, 8 (10) 4622-32
55. Ing, N. H.; Roberts, R. M. The major progesterone-modulated proteins secreted into the sheep uterus are members of the serpin superfamily of serine protease inhibitors J. Biol. Chem. 1989, 264 (6) 3372-9
56. Clawitter, J.; Trout, W. E.; Burke, M. G.; Araghi, S.; Roberts, R. M. A novel family of progesterone-induced, retinol-binding proteins from uterine secretions of the pig J. Biol. Chem. 1990, 265 (6) 3248-55
57. Stallings-Mann, M. L.; Burke, M. G.; Trout, W. E.; Roberts, R. M. Purification, characterization, and cDNA cloning of a Kunitz-type proteinase inhibitor secreted by the porcine uterus J. Biol. Chem. 1994, 269 (39) 24090-4
58. Imakawa, K.; Anthony, R. V.; Kazemi, M.; Marotti, K. R.; Polites, H. G.; Roberts, R. M. Interferon-like sequence of ovine trophoblast protein secreted by embryonic trophectoderm Nature 1987, 330 (6146) 377-9
59. Kayser, J. P.; Kim, J. G.; Cerny, R. L.; Vallet, J. L. Global characterization of porcine intrauterine proteins during early pregnancy Reproduction 2006, 131 (2) 379-88
60. Chae, J. I.; Cho, S. K.; Seo, J. W.; Yoon, T. S.; Lee, K. S.; Kim, J. H.; Lee, K. K.; Han, Y. M.; Yu, K. Proteomic analysis of the extraembryonic tissue from cloned porcine embryos Mol. Cell. Proteomics 2006, 5 (9) 1559-66
61. Pyo, J.; Hwang, S. I.; Oh, J.; Lee, S. J.; Kang, S. C.; Kim, J. S.; Lim, J. Characterization of a bovine pregnancy-associated protein using two-dimensional gel electrophoresis, N-terminal sequencing and mass spectrometry Proteomics 2003, 3 (12) 2420-7
62. 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
63. Kim, H. R.; Kang, J. K.; Yoon, J. T.; Seong, H. H.; Jung, J. K.; Lee, H. M.; Sik Park, C.; Jin, D. I. Protein profiles of bovine placenta derived from somatic cell nuclear transfer Proteomics 2005, 5 (16) 4264-73
64. Daikoku, T.; Tranguch, S.; Friedman, D. B.; Das, S. K.; Smith, D. F.; Dey, S. K. Proteomic analysis identifies immunophilin FK506 binding protein 4 (FKBP52) as a downstream target of Hoxa10 in the periimplantation mouse uterus Mol. Endocrinol. 2005, 19 (3) 683-97