Characterization of the placental transcriptome through mid to late gestation in the mare
Autoři:
Shavahn C. Loux aff001; Pouya Dini aff001; Hossam El-Sheikh Ali aff001; Theodore Kalbfleisch aff001; Barry A. Ball aff001
Působiště autorů:
Maxwell H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, KY, United States of America
aff001; Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium
aff002; Theriogenology Department, Faculty of Veterinary Medicine, University of Mansoura, Mansoura City, Egypt
aff003
Vyšlo v časopise:
PLoS ONE 14(11)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0224497
Souhrn
The placenta is a dynamic organ which undergoes extensive remodeling throughout pregnancy to support, protect and nourish the developing fetus. Despite the importance of the placenta, very little is known about its gene expression beyond very early pregnancy and post-partum. Therefore, we utilized RNA-sequencing to characterize the transcriptome from the fetal (chorioallantois) and maternal (endometrium) components of the placenta from mares throughout gestation (4, 6, 10, 11 m). Within the endometrium, 47% of genes changed throughout pregnancy, while in the chorioallantois, 29% of genes underwent significant changes in expression. Further bioinformatic analyses of both differentially expressed genes and highly expressed genes help reveal similarities and differences between tissues. Overall, the tissues were more similar than different, with ~ 95% of genes expressed in both tissues, and high similarities between the most highly expressed genes (9/20 conserved), as well as marked similarities between the PANTHER pathways identified. The most highly expressed genes fell under a few broad categories, including endocrine and immune-related transcripts, iron-binding proteins, extracellular matrix proteins, transport proteins and antioxidants. Serine protease inhibitors were particularly abundant, including SERPINA3, 6 and 14, as well as SPINK7 and 9. This paper also demonstrates the ability to effectively separate maternal and fetal components of the placenta, with only a minimal amount of chorioallantoic contamination in the endometrium (~8%). This aspect of equine placentation is a boon for better understanding gestational physiology and allows the horse to be used in areas where a separation of fetal and maternal tissues is essential. Overall, these data represent the first large-scale characterization of placental gene expression in any species and include time points from multiple mid- to late-gestational stages, helping further our understanding of gestational physiology.
Klíčová slova:
endometrium – Placenta – Gene expression – Pregnancy – Immune response – Immune system proteins – Horses – Extracellular matrix proteins
Zdroje
1. Mikheev AM, Nabekura T, Kaddoumi A, Bammler TK, Govindarajan R, Hebert MF, et al. Profiling gene expression in human placentae of different gestational ages: an OPRU Network and UW SCOR Study. Reproductive sciences (Thousand Oaks, Calif). 2008;15(9):866–77. Epub 2008/12/04. doi: 10.1177/1933719108322425 19050320; PubMed Central PMCID: PMC2702165.
2. Winn VD, Haimov-Kochman R, Paquet AC, Yang YJ, Madhusudhan MS, Gormley M, et al. Gene expression profiling of the human maternal-fetal interface reveals dramatic changes between midgestation and term. Endocrinology. 2007;148(3):1059–79. Epub 2006/12/16. doi: 10.1210/en.2006-0683 17170095.
3. Tanaka TS, Jaradat SA, Lim MK, Kargul GJ, Wang X, Grahovac MJ, et al. Genome-wide expression profiling of mid-gestation placenta and embryo using a 15,000 mouse developmental cDNA microarray. Proceedings of the National Academy of Sciences of the United States of America. 2000;97(16):9127–32. Epub 2000/08/02. doi: 10.1073/pnas.97.16.9127 10922068; PubMed Central PMCID: PMC16833.
4. Zhang W, Zhong L, Wang J, Han J. Distinct MicroRNA Expression Signatures of Porcine Induced Pluripotent Stem Cells under Mouse and Human ESC Culture Conditions. PloS one. 2016;11(7):e0158655. Epub 2016/07/08. doi: 10.1371/journal.pone.0158655 27384321; PubMed Central PMCID: PMC4934789.
5. Majewska M, Lipka A, Paukszto L, Jastrzebski JP, Myszczynski K, Gowkielewicz M, et al. Transcriptome profile of the human placenta. Functional & integrative genomics. 2017;17(5):551–63. Epub 2017/03/03. doi: 10.1007/s10142-017-0555-y 28251419; PubMed Central PMCID: PMC5561170.
6. Klein C. Novel equine conceptus?endometrial interactions on Day 16 of pregnancy based on RNA sequencing. Reproduction, fertility, and development. 2015. Epub 2015/05/06. doi: 10.1071/rd14489 25940503.
7. Scaravaggi I, Borel N, Romer R, Imboden I, Ulbrich SE, Zeng S, et al. Cell type-specific endometrial transcriptome changes during initial recognition of pregnancy in the mare. Reproduction, fertility, and development. 2018. Epub 2018/09/27. doi: 10.1071/rd18144 30253121.
8. Merkl M, Ulbrich SE, Otzdorff C, Herbach N, Wanke R, Wolf E, et al. Microarray analysis of equine endometrium at days 8 and 12 of pregnancy. Biology of reproduction. 2010;83(5):874–86. Epub 2010/07/16. doi: 10.1095/biolreprod.110.085233 20631402.
9. Smits K, De Coninck DI, Van Nieuwerburgh F, Govaere J, Van Poucke M, Peelman L, et al. The Equine Embryo Influences Immune-Related Gene Expression in the Oviduct. Biology of reproduction. 2016;94(2):36. Epub 2016/01/08. doi: 10.1095/biolreprod.115.136432 26740593.
10. Iqbal K, Chitwood JL, Meyers-Brown GA, Roser JF, Ross PJ. RNA-seq transcriptome profiling of equine inner cell mass and trophectoderm. Biology of reproduction. 2014;90(3):61. Epub 2014/01/31. doi: 10.1095/biolreprod.113.113928 24478389; PubMed Central PMCID: PMC4435230.
11. Reinholt BM, Bradley JS, Jacobs RD, Ealy AD, Johnson SE. Tissue organization alters gene expression in equine induced trophectoderm cells. General and comparative endocrinology. 2017;247:174–82. Epub 2017/02/06. doi: 10.1016/j.ygcen.2017.01.030 28161437.
12. Read JE, Cabrera-Sharp V, Offord V, Mirczuk SM, Allen SP, Fowkes RC, et al. Dynamic changes in gene expression and signalling during trophoblast development in the horse. Reproduction (Cambridge, England). 2018;156(4):313–30. Epub 2018/10/12. doi: 10.1530/rep-18-0270 30306765; PubMed Central PMCID: PMC6170800.
13. Wang X, Miller DC, Harman R, Antczak DF, Clark AG. Paternally expressed genes predominate in the placenta. Proceedings of the National Academy of Sciences of the United States of America. 2013;110(26):10705–10. Epub 2013/06/12. doi: 10.1073/pnas.1308998110 23754418; PubMed Central PMCID: PMC3696791.
14. Wang X, Miller DC, Clark AG, Antczak DF. Random X inactivation in the mule and horse placenta. Genome research. 2012;22(10):1855–63. Epub 2012/05/31. doi: 10.1101/gr.138487.112 22645258; PubMed Central PMCID: PMC3460181.
15. Brosnahan MM, Miller DC, Adams M, Antczak DF. IL-22 is expressed by the invasive trophoblast of the equine (Equus caballus) chorionic girdle. Journal of immunology (Baltimore, Md: 1950). 2012;188(9):4181–7. Epub 2012/04/12. doi: 10.4049/jimmunol.1103509 22490443; PubMed Central PMCID: PMC3746837.
16. Dini P, Daels P, Loux SC, Esteller-Vico A, Carossino M, Scoggin KE, et al. Kinetics of the chromosome 14 microRNA cluster ortholog and its potential role during placental development in the pregnant mare. BMC genomics. 2018;19(1):954. Epub 2018/12/24. doi: 10.1186/s12864-018-5341-2 30572819.
17. Canisso IF, Ball BA, Esteller-Vico A, Williams NM, Squires EL, Troedsson MH. Changes in maternal androgens and oestrogens in mares with experimentally induced ascending placentitis. Equine veterinary journal. 2016. Epub 2016/01/06. doi: 10.1111/evj.12556 26729310.
18. Legacki EL, Scholtz EL, Ball BA, Stanley SD, Berger T, Conley AJ. The dynamic steroid landscape of equine pregnancy mapped by mass spectrometry. Reproduction (Cambridge, England). 2016;151(4):421–30. Epub 2016/01/28. doi: 10.1530/rep-15-0547 26814209.
19. Vincze B, Gaspardy A, Kulcsar M, Baska F, Balint A, Hegedus GT, et al. Equine alpha-fetoprotein levels in Lipizzaner mares with normal pregnancies and with pregnancy loss. Theriogenology. 2015;84(9):1581–6. Epub 2015/09/12. doi: 10.1016/j.theriogenology.2015.08.006 26359849.
20. Canisso IF, Ball BA, Scoggin KE, Squires EL, Williams NM, Troedsson MH. Alpha-fetoprotein is present in the fetal fluids and is increased in plasma of mares with experimentally induced ascending placentitis. Animal reproduction science. 2015;154:48–55. Epub 2015/01/21. doi: 10.1016/j.anireprosci.2014.12.019 25599591.
21. Canisso IF, Ball BA, Cray C, Williams NM, Scoggin KE, Davolli GM, et al. Serum Amyloid A and Haptoglobin Concentrations are Increased in Plasma of Mares with Ascending Placentitis in the Absence of Changes in Peripheral Leukocyte Counts or Fibrinogen Concentration. American journal of reproductive immunology (New York, NY: 1989). 2014;72(4):376–85. Epub 2014/06/12. doi: 10.1111/aji.12278 24916762.
22. Loux SC, Scoggin KE, Bruemmer JE, Canisso IF, Troedsson MH, Squires EL, et al. Evaluation of circulating miRNAs during late pregnancy in the mare. PloS one. 2017;12(4):e0175045. Epub 2017/04/08. doi: 10.1371/journal.pone.0175045 28388652; PubMed Central PMCID: PMC5384662.
23. Bujold E, Romero R, Kusanovic JP, Erez O, Gotsch F, Chaiworapongsa T, et al. Proteomic profiling of amniotic fluid in preterm labor using two-dimensional liquid separation and mass spectrometry. The journal of maternal-fetal & neonatal medicine: the official journal of the European Association of Perinatal Medicine, the Federation of Asia and Oceania Perinatal Societies, the International Society of Perinatal Obstet. 2008;21(10):697–713. Epub 2008/11/18. doi: 10.1080/14767050802053289 19012186; PubMed Central PMCID: PMC3163445.
24. Romero R, Chaemsaithong P, Chaiyasit N, Docheva N, Dong Z, Kim CJ, et al. CXCL10 and IL-6: Markers of two different forms of intra-amniotic inflammation in preterm labor. American journal of reproductive immunology (New York, NY: 1989). 2017;78(1). Epub 2017/05/26. doi: 10.1111/aji.12685 28544362.
25. Romero R, Espinoza J, Rogers WT, Moser A, Nien JK, Kusanovic JP, et al. Proteomic analysis of amniotic fluid to identify women with preterm labor and intra-amniotic inflammation/infection: the use of a novel computational method to analyze mass spectrometric profiling. The journal of maternal-fetal & neonatal medicine: the official journal of the European Association of Perinatal Medicine, the Federation of Asia and Oceania Perinatal Societies, the International Society of Perinatal Obstet. 2008;21(6):367–88. Epub 2008/06/24. doi: 10.1080/14767050802045848 18570116; PubMed Central PMCID: PMC2570775.
26. Loux SC, Ball BA. The proteome of fetal fluids in mares with experimentally-induced placentitis. Placenta. 2018;64:71–8. doi: 10.1016/j.placenta.2018.03.004 29626984
27. Mitchell D. Detection of foetal circulation in the mare and cow by Doppler ultra-sound. The Veterinary record. 1973;93(13):365–8. Epub 1973/09/29. doi: 10.1136/vr.93.13.365 4772215.
28. Silver M, Comline RS. Fetal and placental O2 consumption and the uptake of different metabolites in the ruminant and horse during late gestation. Advances in experimental medicine and biology. 1976;75:731–6. Epub 1976/01/01. doi: 10.1007/978-1-4684-3273-2_85 1015452.
29. Rossdale P, Silver M, Comline RS, Hall LW, Nathanielsz PW. Plasma cortisol in the foal during the late fetal and early neonatal period. Research in veterinary science. 1973;15(3):395–7. Epub 1973/11/01. 4792023.
30. Allen WR, Hamilton DW, Moor RM. The origin of equine endometrial cups. II. Invasion of the endometrium by trophoblast. The Anatomical record. 1973;177(4):485–501. Epub 1973/12/01. doi: 10.1002/ar.1091770403 4762726.
31. Holtan DW, Nett TM, Estergreen VL. Plasma progestagens in pregnant mares. Journal of reproduction and fertility Supplement. 1975;(23):419–24. Epub 1975/10/01. 1060818.
32. Legacki EL, Ball BA, Corbin CJ, Loux SC, Scoggin KE, Stanley SD, et al. Equine fetal adrenal, gonadal and placental steroidogenesis. Reproduction (Cambridge, England). 2017;154(4):445–54. Epub 2017/09/08. doi: 10.1530/rep-17-0239 28878092.
33. Arthur GH. The fetal fluids of domestic animals. Journal of reproduction and fertility Supplement. 1969;9:Suppl 9:45–52. Epub 1969/06/01. 4917717.
34. Samuel CA, Allen WR, Steven DH. Ultrastructural development of the equine placenta. Journal of reproduction and fertility Supplement. 1975;(23):575–8. Epub 1975/10/01. 1060847.
35. Douglas RH, Ginther OJ. Development of the equine fetus and placenta. Journal of reproduction and fertility Supplement. 1975;(23):503–5. Epub 1975/10/01. 1060832.
36. Samuel CA, Allen WR, Steven DH. Studies on the equine placenta II. Ultrastructure of the placental barrier. Journal of reproduction and fertility. 1976;48(2):257–64. Epub 1976/11/01. doi: 10.1530/jrf.0.0480257 1033277.
37. Allen WR, Wilsher S. A review of implantation and early placentation in the mare. Placenta. 2009;30(12):1005–15. Epub 2009/10/24. doi: 10.1016/j.placenta.2009.09.007 19850339.
38. Steven DH. Placentation in the mare. Journal of reproduction and fertility Supplement. 1982;31:41–55. Epub 1982/11/01. 6762433.
39. Kalbfleisch TS, Rice ES, DePriest MS Jr., Walenz BP, Hestand MS, Vermeesch JR, et al. Improved reference genome for the domestic horse increases assembly contiguity and composition. Communications biology. 2018;1:197. Epub 2018/11/21. doi: 10.1038/s42003-018-0199-z 30456315; PubMed Central PMCID: PMC6240028 adviser of Dovetail Genomics, LLC. The other authors declare no competing interests.
40. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29(1):15–21. Epub 10/25. doi: 10.1093/bioinformatics/bts635 23104886.
41. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature biotechnology. 2010;28(5):511–5. Epub 2010/05/04. doi: 10.1038/nbt.1621 20436464; PubMed Central PMCID: PMC3146043.
42. Langfelder P, Horvath S. WGCNA: an R package for weighted correlation network analysis. BMC bioinformatics. 2008;9:559. Epub 2008/12/31. doi: 10.1186/1471-2105-9-559 19114008; PubMed Central PMCID: PMC2631488.
43. Mi H, Muruganujan A, Casagrande JT, Thomas PD. Large-scale gene function analysis with the PANTHER classification system. Nature protocols. 2013;8(8):1551–66. Epub 2013/07/23. doi: 10.1038/nprot.2013.092 23868073.
44. Bulmer JN, Morrison L, Longfellow M, Ritson A, Pace D. Granulated lymphocytes in human endometrium: histochemical and immunohistochemical studies. Human reproduction (Oxford, England). 1991;6(6):791–8. Epub 1991/07/01. doi: 10.1093/oxfordjournals.humrep.a137430 1757516.
45. Grunig G, Triplett L, Canady LK, Allen WR, Antczak DF. The maternal leucocyte response to the endometrial cups in horses is correlated with the developmental stages of the invasive trophoblast cells. Placenta. 1995;16(6):539–59. Epub 1995/09/01. doi: 10.1016/s0143-4004(05)80005-0 8570575.
46. Allen WR. Immunological aspects of the endometrial cup reaction and the effect of xenogeneic pregnancy in horses and donkeys. Journal of reproduction and fertility Supplement. 1982;31:57–94. Epub 1982/11/01. 6962845.
47. Antczak DF, de Mestre AM, Wilsher S, Allen WR. The equine endometrial cup reaction: a fetomaternal signal of significance. Annual review of animal biosciences. 2013;1:419–42. Epub 2013/01/01. doi: 10.1146/annurev-animal-031412-103703 25387026; PubMed Central PMCID: PMC4641323.
48. Conley AJ. Review of the reproductive endocrinology of the pregnant and parturient mare. Theriogenology. 2016;86(1):355–65. Epub 2016/05/10. doi: 10.1016/j.theriogenology.2016.04.049 27156685.
49. Allen WR, Gower S, Wilsher S. Localisation of epidermal growth factor (EGF), its specific receptor (EGF-R) and aromatase at the materno-fetal interface during placentation in the pregnant mare. Placenta. 2017;50:53–9. Epub 2017/02/06. doi: 10.1016/j.placenta.2016.12.024 28161062.
50. Marshall DE, Dumasia MC, Wooding P, Gower DB, Houghton E. Studies into aromatase activity associated with fetal allantochorionic and maternal endometrial tissues of equine placenta. Identification of metabolites by gas chromatography mass spectrometry. The Journal of steroid biochemistry and molecular biology. 1996;59(3–4):281–96. Epub 1996/11/01. doi: 10.1016/s0960-0760(96)00115-x 9010320.
51. Klein C. Early pregnancy in the mare: old concepts revisited. Domestic animal endocrinology. 2016;56 Suppl:S212–7. Epub 2016/06/28. doi: 10.1016/j.domaniend.2016.03.006 27345319.
52. Knox RV, Zhang Z, Day BN, Anthony RV. Identification of relaxin gene expression and protein localization in the uterine endometrium during early pregnancy in the pig. Endocrinology. 1994;135(6):2517–25. Epub 1994/12/01. doi: 10.1210/endo.135.6.7988439 7988439.
53. Klein C. The role of relaxin in mare reproductive physiology: A comparative review with other species. Theriogenology. 2016;86(1):451–6. Epub 2016/05/10. doi: 10.1016/j.theriogenology.2016.04.061 27158127.
54. Almeida J, Conley AJ, Mathewson L, Ball BA. Expression of steroidogenic enzymes during equine testicular development. Reproduction (Cambridge, England). 2011;141(6):841–8. Epub 2011/02/09. doi: 10.1530/rep-10-0499 21300693.
55. Kisielewska K, Rytelewska E, Gudelska M, Kiezun M, Dobrzyn K, Szeszko K, et al. The effect of orexin B on steroidogenic acute regulatory protein, P450 side-chain cleavage enzyme, and 3beta-hydroxysteroid dehydrogenase gene expression, and progesterone and androstenedione secretion by the porcine uterus during early pregnancy and the estrous cycle. Journal of animal science. 2019;97(2):851–64. Epub 2018/12/07. doi: 10.1093/jas/sky458 30508170; PubMed Central PMCID: PMC6358223.
56. Yamanouchi K, Hirasawa K, Hasegawa T, Ikeda A, Chang KT, Matsuyama S, et al. Equine inhibin/activin beta A-subunit mRNA is expressed in the endometrial gland, but not in the trophoblast, during pregnancy. Molecular reproduction and development. 1997;47(4):363–9. Epub 1997/08/01. doi: 10.1002/(SICI)1098-2795(199708)47:4<363::AID-MRD2>3.0.CO;2-I 9211420.
57. Mitchell MD, Peiris HN, Kobayashi M, Koh YQ, Duncombe G, Illanes SE, et al. Placental exosomes in normal and complicated pregnancy. American journal of obstetrics and gynecology. 2015;213(4 Suppl):S173–81. Epub 2015/10/03. doi: 10.1016/j.ajog.2015.07.001 26428497.
58. Salomon C, Rice GE. Role of Exosomes in Placental Homeostasis and Pregnancy Disorders. Progress in molecular biology and translational science. 2017;145:163–79. Epub 2017/01/24. doi: 10.1016/bs.pmbts.2016.12.006 28110750.
59. Tong M, Chamley LW. Placental extracellular vesicles and feto-maternal communication. Cold Spring Harbor perspectives in medicine. 2015;5(3):a023028. Epub 2015/01/31. doi: 10.1101/cshperspect.a023028 25635060; PubMed Central PMCID: PMC4355256.
60. Brattsand M, Stefansson K, Hubiche T, Nilsson SK, Egelrud T. SPINK9: a selective, skin-specific Kazal-type serine protease inhibitor. The Journal of investigative dermatology. 2009;129(7):1656–65. Epub 2009/02/06. doi: 10.1038/jid.2008.448 19194479.
61. Wu Z, Wu Y, Fischer J, Bartels J, Schroder JM, Meyer-Hoffert U. Skin-Derived SPINK9 Kills Escherichia coli. The Journal of investigative dermatology. 2019;139(5):1135–42. Epub 2018/11/24. doi: 10.1016/j.jid.2018.11.004 30468739.
62. Loux SC, Scoggin KE, Troedsson MH, Squires EL, Ball BA. Characterization of the cervical mucus plug in mares. Reproduction (Cambridge, England). 2017;153(2):197–210. Epub 2016/11/16. doi: 10.1530/rep-16-0396 27845690.
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