Proteomic analysis of uterine fluid during the pre-implantation period of pregnancy in cattle

Reproduction

Volumn 147, Issue 5, 2014, Pages 575-587

  Forde, Niamh ^a   McGettigan, Paul A ^a   Mehta, Jai P ^a   O'Hara, Lydia ^a   Mamo, Solomon ^a   Bazer, Fuller W ^b   Spencer, Thomas E ^c   Lonergan, Pat ^a  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

^b TEXAS A AND M UNIVERSITY   (United States)

^c WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE REDUCTASE; ALDOA PROTEIN; CATB PROTEIN; CATD PROTEIN; CATG PROTEIN; CATHEPSIN B; CATHEPSIN D; CO3 PROTEIN; COMPLEMENT COMPONENT C3; CST6 PROTEIN; CYSTATIN M; FRUCTOSE BISPHOSPHATE ALDOLASE; GANGLIOSIDE GD 1B; GD12 PROTEIN; GD18 PROTEIN; GDA PROTEIN; GELS PROTEIN; GUANINE DEAMINASE; HEAT SHOCK COGNATE PROTEIN 70; HEAT SHOCK COGNATE PROTEIN 90A1; IDHC PROTEIN; ISOCITRATE DEHYDROGENASE; ISOCITRATE DEHYDROGENASE 1; PNPH PROTEIN; PURINE NUCLEOSIDE PHOSPHORYLASE; SERPINA31 PROTEIN; TERA PROTEIN; TISSUE INHIBITOR OF METALLOPROTEINASE 2; UNCLASSIFIED DRUG; UNINDEXED DRUG; VCN PROTEIN; HEAT SHOCK PROTEIN; PLACENTA PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BLASTOCYST; ENDOMETRIUM; EXPERIMENTAL CATTLE; FEMALE; GENE EXPRESSION; GENE ONTOLOGY; LIQUID CHROMATOGRAPHY; NONHUMAN; NUCLEOTIDE SEQUENCE; PREGNANCY; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; PROTEOMICS; RNA SEQUENCE; TANDEM MASS SPECTROMETRY; UTERINE LUMINAL FLUID; UTERUS FLUID; ZONA PELLUCIDA; ANIMAL; BOVINAE; BREEDING; EMBRYO DEVELOPMENT; GENE EXPRESSION REGULATION; PHYSIOLOGY; UTERUS;

ANIMALS; CATTLE; EMBRYONIC DEVELOPMENT; ENDOMETRIUM; FEMALE; FRUCTOSE-BISPHOSPHATE ALDOLASE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEAT-SHOCK PROTEINS; PREGNANCY; PREGNANCY PROTEINS; PREGNANCY, ANIMAL; PROTEOMICS; UTERUS;

EID: 84898974818     PISSN: 14701626     EISSN: 17417899     Source Type: Journal    
DOI: 10.1530/REP-13-0010     Document Type: Article

References (62)

1. Afonso S, Romagnano L & Babiarz B 1997 The expression and function of cystatin C and cathepsin B and cathepsin L during mouse embryo implantation and placentation. Development 124 3415-3425. (Pubitemid 27440456)
2. el-Banna AA & Hafez ES 1970 Egg transport in beef cattle. Journal of Animal Science 30 430-432.
3. Baston-Buest DM, Schanz A, Buest S, Fischer JC, Kruessel JS & Hess AP 2010 The embryo's cystatin C and F expression functions as a protective mechanism against the maternal proteinase cathepsin S in mice. Reproduction 139 741-748. (doi:10.1530/REP-09-0381)
4. Bauersachs S, Ulbrich SE, Gross K, Schmidt SE, Meyer HH, Einspanier R, Wenigerkind H, Vermehren M, Blum H, Sinowatz F et al. 2005 Gene expression profiling of bovine endometrium during the oestrous cycle: detection ofmolecular pathways involved in functional changes. Journal of Molecular Endocrinology 34 889-908. (doi:10.1677/jme.1.01799) (Pubitemid 40903609)
5. Bauersachs S, Ulbrich SE, Reichenbach HD, Reichenbach M, Buttner M, Meyer HH, Spencer TE, Minten M, Sax G, Winter G et al. 2012 Comparison of the effects of early pregnancy with human interferon, a2 (IFNA2), on gene expression in bovine endometrium. Biology of Reproduction 86 46. (doi:10.1095/biolreprod.111. 094771)
6. Bazer FW, Spencer TE, Johnson GA, Burghardt RC & Wu G 2009 Comparative aspects of implantation. Reproduction 138 195-209. (doi:10.1530/REP-09-0158)
7. Bazer FW, Wu G, Spencer TE, Johnson GA, Burghardt RC & Bayless K 2010 Novel pathways for implantation and establishment and maintenance of pregnancy in mammals. Molecular Human Reproduction 16 135-152. (doi:10.1093/molehr/gap095)
8. Berendt FJ, Frohlich T, Schmidt SE, Reichenbach HD, Wolf E & Arnold GJ 2005 Holistic differential analysis of embryo-induced alterations in the proteome of bovine endometrium in the preattachment period. Proteomics 5 2551-2560. (doi:10.1002/pmic.200401242) (Pubitemid 40966482)
9. Betteridge KJ, Eaglesome MD, Randall GC & Mitchell D 1980 Collection, description and transfer of embryos from cattle 10-16 days after oestrus. Journal of Reproduction and Fertility 59 205-216. (doi:10.1530/jrf.0. 0590205) (Pubitemid 10088033)
10. Brandao DO, Maddox-Hyttel P, Lovendahl P, Rumpf R, Stringfellow D & Callesen H 2004 Post hatching development: a novel system for extended in vitro culture of bovine embryos. Biology of Reproduction 71 2048-2055. (doi:10.1095/biolreprod.103.025916) (Pubitemid 39586953)
11. Cagnone GL, Dufort I, Vigneault C & Sirard MA 2012 Differential gene expression profile in bovine blastocysts resulting from hyperglycemia exposure during early cleavage stages. Biology of Reproduction 86 50. (doi:10.1095/biolreprod.111.094391)
12. Carter F, Forde N, Duffy P, Wade M, Fair T, Crowe MA, Evans AC, Kenny DA, Roche JF & Lonergan P 2008 Effect of increasing progesterone concentration from day 3 of pregnancy on subsequent embryo survival and development in beef heifers. Reproduction, Fertility, and Development 20 368-375. (doi:10.1071/RD07204) (Pubitemid 351363828)
13. Clemente M, de La Fuente J, Fair T, Al Naib A, Gutierrez-Adan A, Roche JF, Rizos D & Lonergan P 2009 Progesterone and conceptus elongation in cattle: a direct effect on the embryo or an indirect effect via the endometrium? Reproduction 138 507-517 (doi:10.1530/REP-09-0152)
14. Costello LM, O'Boyle P, Godkin JD, Diskin MG, Hynes AC & Morris DG 2010 Retinol-binding protein (RBP), retinol and b-carotene in the bovine uterus and plasma during the oestrous cycle and the relationship between systemic progesterone and RBP on day 7. Reproduction, Fertility, and Development 22 1198-1205. (doi:10.1071/RD10034)
15. Dorniak P, Bazer FW & Spencer TE 2011a Prostaglandins regulate conceptus elongation and mediate effects of interferon tau on the ovine uterine endometrium. Biology of Reproduction 84 1119-1127. (doi:10.1095/biolreprod.110. 089979)
16. Dorniak P, Welsh TH Jr, Bazer FW & Spencer TE 2011b Endometrial HSD11B1 and cortisol regeneration in the ovine uterus: effects of pregnancy, interferon tau, and prostaglandins. Biology of Reproduction 86 124. (doi:10.1095/biolreprod.111.097063)
17. Farin CE, Imakawa K, Hansen TR, McDonnell JJ, Murphy CN, Farin PW & Roberts RM 1990 Expression of trophoblastic interferon genes in sheep and cattle. Biology of Reproduction 43 210-218. (doi:10.1095/ biolreprod43.2.210) (Pubitemid 20242410)
18. Faulkner S, Elia G, Mullen MP, O'Boyle P, Dunn MJ & Morris D 2012 A comparison of the bovine uterine and plasma proteome using iTRAQ proteomics. Proteomics 12 2014-2023. (doi:10.1002/pmic.201100609)
19. Forde N, Carter F, Fair T, Crowe MA, Evans AC, Spencer TE, Bazer FW, McBride R, Boland MP, O'Gaora P et al. 2009 Progesterone-regulated changes in endometrial gene expression contribute to advanced conceptus development in cattle. Biology of Reproduction 81 784-794. (doi:10.1095/biolreprod.108.074336)
20. Forde N, Spencer TE, Bazer FW, Song G, Roche JF & Lonergan P 2010 Effect of pregnancy and progesterone concentration on expression of genes encoding for transporters or secreted proteins in the bovine endometrium. Physiological Genomics 41 53-62. (doi:10.1152/physiolgenomics. 00162.2009)
21. Forde N, Beltman ME, Duffy GB, Duffy P, Mehta JP, O'Gaora P, Roche JF, Lonergan P & Crowe MA 2011a Changes in the endometrial transcriptome during the bovine estrous cycle: effect of low circulating progesterone and consequences for conceptus elongation. Biology of Reproduction 84 266-278. (doi:10.1095/biolreprod.110.085910)
22. Forde N, Carter F, Spencer TE, Bazer FW, Sandra O, Mansouri-Attia N, Okumu LA, McGettigan PA, Mehta JP, McBride R et al. 2011b Conceptus-induced changes in the endometrial transcriptome: how soon does the cow know she is pregnant? Biology of Reproduction 85 144-156 (doi:10.1095/biolreprod.110.090019)
23. Forde N, Duffy GB, McGettigan PA, Browne JA, Mehta JP, Kelly AK, Mansouri-Attia N, Sandra O, Loftus BJ, CroweMA et al. 2012a Evidence for an early endometrial response to pregnancy in cattle: both dependent upon and independent of interferon tau. Physiological Genomics 44 799-810. (doi:10.1152/physiolgenomics.00067.2012)
24. Forde N, Mehta JP, MintenM, Crowe MA, Roche JF, Spencer TE & Lonergan P 2012b Effects of lowprogesterone on the endometrial transcriptome in cattle. Biology of Reproduction 87 124. (doi:10.1095/biolreprod.112.103424)
25. Gao H, Wu G, Spencer TE, Johnson GA, Li X & Bazer FW 2009 Select nutrients in the ovine uterine lumen. I. Amino acids, glucose, and ions in uterine lumenal flushings of cyclic and pregnant ewes. Biology of Reproduction 80 86-93. (doi:10.1095/biolreprod.108.071597)
26. Garrett JE, Geisert RD, Zavy MT & Morgan GL 1988 Evidence for maternal regulation of early conceptus growth and development in beef cattle. Journal of Reproduction and Fertility 84 437-446. (doi:10.1530/jrf.0. 0840437) (Pubitemid 18268059)
27. Gray CA, Burghardt RC, Johnson GA, Bazer FW & Spencer TE 2002 Evidence that absence of endometrial gland secretions in uterine gland knockout ewes compromises conceptus survival and elongation. Reproduction 124 289-300. (doi:10.1530/rep.0.1240289)
28. Gray CA, Adelson DL, Bazer FW, Burghardt RC, Meeusen EN & Spencer TE 2004 Discovery and characterization of an epithelial-specific galectin in the endometrium that forms crystals in the trophectoderm. PNAS 101 7982-7987. (doi:10.1073/pnas.0402669101) (Pubitemid 38698040)
29. Guillomot M, Flechon JE & Wintenberger-Torres S 1981 Conceptus attachment in the ewe: an ultrastructural study. Placenta 2 169-182. (doi:10.1016/S0143-4004(81)80021-5)
30. Hackett AJ, Durnford R, Mapletoft RJ & Marcus GJ 1993 Location and status of embryos in the genital tract of superovulated cows 4 to 6 days after insemination. Theriogenology 40 1147-1153. (doi:10.1016/0093- 691X(93)90285-D)
31. Hosokawa M, Kashiwaya K, Eguchi H, Ohigashi H, Ishikawa O, Furihata M, Shinomura Y, ImaiK, Nakamura Y&NakagawaH2008Over-expression of cysteine proteinase inhibitor cystatin 6 promotes pancreatic cancer growth. Cancer Science 99 1626-1632. (doi:10.1111/j.1349-7006.2008.00869.x)
32. Hugentobler SA, Sreenan JM, Humpherson PG, Leese HJ, Diskin MG & Morris DG 2010 Effects of changes in the concentration of systemic progesterone on ions, amino acids and energy substrates in cattle oviduct and uterine fluid and blood. Reproduction, Fertility, and Development 22 684-694. (doi:10.1071/RD09129)
33. Ko E, Park SE, Cho EY, Kim Y, Hwang JA, Lee YS, Nam SJ, Bang S, Park J & Kim DH 2010 Cystatin M loss is associated with the losses of estrogen receptor, progesterone receptor, and HER4 in invasive breast cancer. Breast Cancer Research 12 R100. (doi:10.1186/bcr2783)
34. Krisher RL & Prather RS 2012 A role for the Warburg effect in preimplantation embryo development: metabolic modification to support rapid cell proliferation. Molecular Reproduction and Development 79 311-320. (doi:10.1002/mrd.22037)
35. Ledgard AM, Lee RS & Peterson AJ 2009 Bovine endometrial legumain and TIMP-2 regulation in response to presence of a conceptus. Molecular Reproduction and Development 76 65-74. (doi:10.1002/mrd.20931)
36. Ledgard AM, Berg MC, McMillan MH, Smolenski G & Peterson AJ 2012 Effect of asynchronous transfer on bovine embryonic development and relationship with early cycle uterine proteome profiles. Reproduction, Fertility, and Development 24 962-972. (doi:10.1071/RD11225)
37. Lewis SK, Farmer JL, Burghardt RC, Newton GR, Johnson GA, Adelson DL, Bazer FW & Spencer TE 2007 Galectin 15 (LGALS15): a gene uniquely expressed in the uteri of sheep and goats that functions in trophoblast attachment. Biology of Reproduction 77 1027-1036. (doi:10.1095/ biolreprod.107.063594) (Pubitemid 350197980)
38. Loureiro B, Block J, Favoreto MG, Carambula S, Pennington KA, Ealy AD & Hansen PJ 2011 Consequences of conceptus exposure to colonystimulating factor 2 on survival, elongation, interferon-tau secretion, and gene expression. Reproduction 141 617-624. (doi:10.1530/REP-10-0511)
39. Mamo S, Mehta JP, McGettigan P, Fair T, Spencer TE, Bazer FW& Lonergan P 2011 RNA sequencing reveals novel gene clusters in bovine conceptuses associatedwithmaternal recognitionofpregnancyandimplantation.Biology of Reproduction 85 1143-1151 (doi:10.1095/biolreprod.111.092643)
40. Mansouri-Attia N, Aubert J, Reinaud JP, Giraud-Delville C, Taghouti G, Galio L, Everts RE, Degrelle S, Richard C, Hue I et al. 2009 Gene expression profiles of bovine caruncular and intercaruncular endometrium at implantation. Physiological Genomics 39 14-27. (doi:10.1152/ physiolgenomics.90404.2008)
41. Mullen MP, Elia G, Hilliard M, Parr MH, Diskin MG, Evans AC & CroweMA 2012a Proteomic characterization of histotroph during the preimplantation phase of the estrous cycle in cattle. Journal of Proteome Research 11 3004-3018. (doi:10.1021/pr300144q)
42. Mullen MP, Forde N, Parr MH, Diskin MG, Morris DG, Nally JE, Evans AC & Crowe MA 2012b Alterations in systemic concentrations of progesterone during the early luteal phase affect RBP4 expression in the bovine uterus. Reproduction, Fertility, and Development 24 715-722. (doi:10.1071/RD11246)
43. Munoz M, Corrales FJ, Caamano JN, Diez C, Trigal B, Mora MI, Martin D, Carrocera S & Gomez E 2012 Proteome of the early embryo-maternal dialogue in the cattle uterus. Journal of Proteome Research 11 751-766. (doi:10.1021/pr200969a)
44. Northey DL & French LR 1980 Effect of embryo removal and intrauterine infusion of embryonic homogenates on the lifespan of the bovine corpus luteum. Journal of Animal Science 50 298-302.
45. Redel BK, Brown AN, Spate LD, Whitworth KM, Green JA & Prather RS 2012 Glycolysis in preimplantation development is partially controlled by the Warburg effect. Molecular Reproduction and Development 79 262-271. (doi:10.1002/mrd.22017)
46. Robinson MD, McCarthy DJ & Smyth GK 2010 edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26 139-140. (doi:10.1093/bioinformatics/btp616)
47. Satterfield MC, Bazer FW & Spencer TE 2006 Progesterone regulation of preimplantation conceptus growth and galectin 15 (LGALS15) in the ovine uterus. Biology of Reproduction 75 289-296. (doi:10.1095/ biolreprod.106.052944) (Pubitemid 44107199)
48. Satterfield MC, Song G, Kochan KJ, Riggs PK, Simmons RM, Elsik CG, Adelson DL, Bazer FW, Zhou H & Spencer TE 2009 Discovery of candidate genes and pathways in the endometrium regulating ovine blastocyst growth and conceptus elongation. Physiological Genomics 39 85-99. (doi:10.1152/physiolgenomics. 00001.2009)
49. Simmons RM, Erikson DW, Kim J, Burghardt RC, Bazer FW, Johnson GA & Spencer TE 2009 Insulin-like growth factor binding protein one in the ruminant uterus: potential endometrial marker and regulator of conceptus elongation. Endocrinology 150 4295-4305. (doi:10.1210/en.2009-0060)
50. Song G, Spencer TE & Bazer FW 2005 Cathepsins in the ovine uterus: regulation by pregnancy, progesterone, and interferon tau. Endocrinology 146 4825-4833. (doi:10.1210/en.2005-0768) (Pubitemid 41446620)
51. Song G, Spencer TE & Bazer FW 2006 Progesterone and interferon-tau regulate cystatin C in the endometrium. Endocrinology 147 3478-3483. (doi:10.1210/en.2006-0122) (Pubitemid 43901139)
52. Song G, Bazer FW & Spencer TE 2007 Differential expression of cathepsins and cystatin C in ovine uteroplacental tissues. Placenta 28 1091-1098. (doi:10.1016/j.placenta.2007.04.004) (Pubitemid 47355235)
53. Song G, Satterfield MC, Kim J, Bazer FW & Spencer TE 2008 Gastrinreleasing peptide (GRP) in the ovine uterus: regulation by interferon tau and progesterone. Biology of Reproduction 79 376-386. (doi:10.1095/ biolreprod.108.068403)
54. Song G, Bailey DW, Dunlap KA, Burghardt RC, Spencer TE, Bazer FW & Johnson GA 2010 Cathepsin B, cathepsin L, and cystatin C in the porcine uterus and placenta: potential roles in endometrial/placental remodeling and in fluid-phase transport of proteins secreted by uterine epithelia across placental areolae. Biology of Reproduction 82 854-864. (doi:10.1095/biolreprod.109. 080929)
55. Spencer TE & Gray CA 2006 Sheep uterine gland knockout (UGKO) model. Methods in Molecular Medicine 121 85-94.
56. Spencer TE, SandraO&Wolf E 2008 Genes involved in conceptus-endometrial interactions in ruminants: insights fromreductionismand thoughts on holistic approaches. Reproduction 135 165-179. (doi:10.1530/REP-07- 0327) (Pubitemid 351267387)
57. Spencer TE, Forde N, Dorniak P, Hansen TR, Romero JJ & Lonergan P 2013 Conceptus-derived prostaglandins regulate gene expression in the endometrium prior to pregnancy recognition in ruminants. Reproduction 146 377-387. (doi:10.1530/REP-13-0165)
58. Vajta G, Alexopoulos NI & Callesen H 2004 Rapid growth and elongation of bovine blastocysts in vitro in a three-dimensional gel system. Theriogenology 62 1253-1263. (doi:10.1016/j.theriogenology. 2004.01.007) (Pubitemid 39123704)
59. Vander Heiden MG, Cantley LC & Thompson CB 2009 Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324 1029-1033. (doi:10.1126/science.1160809)
60. Vejlsted M, Du Y, Vajta G & Maddox-Hyttel P 2006 Post-hatching development of the porcine and bovine embryo-defining criteria for expected development in vivo and in vitro. Theriogenology 65 153-165. (Pubitemid 41688339)
61. Vigneswaran N, Wu J & Zacharias W 2003 Upregulation of cystatin M during the progression of oropharyngeal squamous cell carcinoma from primary tumor to metastasis. Oral Oncology 39 559-568. (doi:10.1016/ S1368-8375(03)00038-1) (Pubitemid 36694479)
62. Vigneswaran N, Wu J, Nagaraj N, James R, Zeeuwen P & ZachariasW2006 Silencing of cystatin M in metastatic oral cancer cell line MDA- 686Ln by siRNA increases cysteine proteinases and legumain activities, cell proliferation and in vitro invasion. Life Sciences 78 898-907. (doi:10.1016/j.lfs.2005.05.096) (Pubitemid 43082316)