FREE SHIPPING over $40
OVER 10000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Biology of reproduction2008; 80(2); 227-234; doi: 10.1095/biolreprod.108.070920

Glial cells missing homologue 1 is induced in differentiating equine chorionic girdle trophoblast cells.

Abstract: The objective of this study was to identify transcription factors associated with differentiation of the chorionic girdle, the invasive form of equine trophoblast. The expression patterns of five transcription factors were determined on a panel of conceptus tissues from early horse pregnancy. Tissues from Days 15 through 46 were tested. Eomesodermin (EOMES), glial cells missing homologue 1 (GCM1), heart and neural crest derivatives expressed transcript 1 (HAND1), caudal type homeobox 2 (CDX2), and distal-less homeobox 3 (DLX3) were detected in horse trophoblast, but the expression patterns for these genes varied. EOMES had the most restricted distribution, while DLX3 CDX2, and HAND1 were widely expressed. GCM1 seemed to increase in the developing chorionic girdle, and this was confirmed by quantitative RT-PCR assays. GCM1 expression preceded a striking increase in expression of equine chorionic gonadotropin beta (CGB) in the chorionic girdle, and binding sites for GCM1 were discovered in the promoter region of the CGB gene. GCM1, CGB, and CGA mRNA were expressed preferentially in binucleate cells as opposed to uninucleate cells of the chorionic girdle. Based on these findings, it is likely that GCM1 has a role in differentiation and function of the invasive trophoblast of the equine chorionic girdle and endometrial cups. The equine binucleate chorionic girdle (CG) secreting trophoblast shares molecular, morphological, and functional characteristics with human syncytiotrophoblast and represents a model for studies of human placental function.
Get Full Text
Publication Date: 2008-10-29 PubMed ID: 18971425PubMed Central: PMC2804814DOI: 10.1095/biolreprod.108.070920Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article
  • Research Support
  • N.I.H.
  • Extramural
  • Research Support
  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research investigates the role of the transcription factor ‘glial cells missing homologue 1’ in the development of equine placental structures, specifically the chorionic girdle. The study identified this factor as a likely player in the differentiation of specific cells in the placenta and a key component in the regulation of pathology relevant to human placental function.

Transcription Factors and Trophoblast Differentiation

  • The aim was to recognize transcription factors tied to the differentiation of the chorionic girdle – an invasive form of the equine (horse) trophoblast, or cells forming the outer layer of a blastocyst (early-stage embryo).
  • The team investigated the expression of five transcription factors: Eomesodermin (EOMES), glial cells missing homologue 1 (GCM1), heart and neural crest derivatives expressed transcript 1 (HAND1), caudal type homeobox 2 (CDX2), and distal-less homeobox 3 (DLX3).
  • These factors were detected, but exhibited variable expression patterns. For instance, EOMES had a very limited distribution while DLX3, CDX2, and HAND1 showed widespread expression.

Role of GCM1 in Chorionic Girdle Development

  • GCM1 in particular, was noticed to increase in the chorionic girdle as it developed. Further testing with quantitative RT-PCR assays confirmed this observation.
  • Importantly, increases in GCM1 expression were followed by surges in the expression of equine chorionic gonadotropin beta (CGB), indicating a possible connection between these events.
  • The researchers found binding sites for GCM1 within the promoter region of the CGB gene, further supporting the concept of a direct regulatory relationship between these entities.

GCM1 and Cell Differentiation

  • GCM1, along with CGB and CGA mRNA, was shown to be preferentially expressed in binucleate (two-nuclei) cells versus uninucleate (single-nucleus) cells in the chorionic girdle.
  • From these findings, the research posits that GCM1 likely plays a crucial role in the differentiation of these invasive trophoblasts and eventually in the creation of the equine chorionic girdle and endometrial cups.

Implications for Human Placental Studies

  • The equine chorionic girdle provides a useful model for studying human placental function due to shared characteristics in molecular structure, morphology, and functionality with human syncytiotrophoblasts.
  • This perception of GCM1’s role in equine cell differentiation is consequential as it could pave the way for better understanding of human placental development and related pathologies.

Cite This Article

APA
de Mestre AM, Miller D, Roberson MS, Liford J, Chizmar LC, McLaughlin KE, Antczak DF. (2008). Glial cells missing homologue 1 is induced in differentiating equine chorionic girdle trophoblast cells. Biol Reprod, 80(2), 227-234. https://doi.org/10.1095/biolreprod.108.070920

Publication

Biology of reproduction
ISSN: 0006-3363
NlmUniqueID: 0207224
Country: United States
Language: English
Volume: 80
Issue: 2
Pages: 227-234

Researcher Affiliations

de Mestre, Amanda M
  • Baker Institute for Animal Health and Department of Biomedical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, New York 14853, USA. ademestre@rvc.ac.uk
Miller, Donald
    Roberson, Mark S
      Liford, Jenny
        Chizmar, Lisay C
          McLaughlin, Kristin E
            Antczak, Douglas F

              MeSH Terms

              • Animals
              • Cell Differentiation / genetics
              • Cells, Cultured
              • Female
              • Fetus / metabolism
              • Gestational Age
              • Horses / genetics
              • Horses / physiology
              • Models, Biological
              • Neuropeptides / genetics
              • Neuropeptides / metabolism
              • Pregnancy
              • Pregnancy, Animal
              • Transcription Factors / genetics
              • Transcription Factors / metabolism
              • Trophoblasts / metabolism
              • Trophoblasts / physiology
              • Up-Regulation

              Grant Funding

              • R01 HD049545 / NICHD NIH HHS
              • R01-HD049545 / NICHD NIH HHS

              References

              This article includes 51 references
              1. Cross JC, Baczyk D, Dobric N, Hemberger M, Hughes M, Simmons DG, Yamamoto H, Kingdom JC. Genes, development and evolution of the placenta.. Placenta 2003 Feb-Mar;24(2-3):123-30.
                pubmed: 12596737doi: 10.1053/plac.2002.0887google scholar: lookup
              2. Loregger T, Pollheimer J, Knöfler M. Regulatory transcription factors controlling function and differentiation of human trophoblast--a review.. Placenta 2003 Apr;24 Suppl A:S104-10.
                pubmed: 12842421doi: 10.1053/plac.2002.0929google scholar: lookup
              3. Russ AP, Wattler S, Colledge WH, Aparicio SA, Carlton MB, Pearce JJ, Barton SC, Surani MA, Ryan K, Nehls MC, Wilson V, Evans MJ. Eomesodermin is required for mouse trophoblast development and mesoderm formation.. Nature 2000 Mar 2;404(6773):95-9.
                pubmed: 10716450doi: 10.1038/35003601google scholar: lookup
              4. Baczyk D, Satkunaratnam A, Nait-Oumesmar B, Huppertz B, Cross JC, Kingdom JC. Complex patterns of GCM1 mRNA and protein in villous and extravillous trophoblast cells of the human placenta.. Placenta 2004 Jul;25(6):553-9.
                pubmed: 15135239doi: 10.1016/j.placenta.2003.12.004google scholar: lookup
              5. Nait-Oumesmar B, Copperman AB, Lazzarini RA. Placental expression and chromosomal localization of the human Gcm 1 gene.. J Histochem Cytochem 2000 Jul;48(7):915-22.
                pubmed: 10858268doi: 10.1177/002215540004800704google scholar: lookup
              6. Anson-Cartwright L, Dawson K, Holmyard D, Fisher SJ, Lazzarini RA, Cross JC. The glial cells missing-1 protein is essential for branching morphogenesis in the chorioallantoic placenta.. Nat Genet 2000 Jul;25(3):311-4.
                pubmed: 10888880doi: 10.1038/77076google scholar: lookup
              7. Scott IC, Anson-Cartwright L, Riley P, Reda D, Cross JC. The HAND1 basic helix-loop-helix transcription factor regulates trophoblast differentiation via multiple mechanisms.. Mol Cell Biol 2000 Jan;20(2):530-41.
                pmc: PMC85124pubmed: 10611232doi: 10.1128/mcb.20.2.530-541.2000google scholar: lookup
              8. Chawengsaksophak K, James R, Hammond VE, Köntgen F, Beck F. Homeosis and intestinal tumours in Cdx2 mutant mice.. Nature 1997 Mar 6;386(6620):84-7.
                pubmed: 9052785doi: 10.1038/386084a0google scholar: lookup
              9. Morasso MI, Grinberg A, Robinson G, Sargent TD, Mahon KA. Placental failure in mice lacking the homeobox gene Dlx3.. Proc Natl Acad Sci U S A 1999 Jan 5;96(1):162-7.
                pmc: PMC15110pubmed: 9874789doi: 10.1073/pnas.96.1.162google scholar: lookup
              10. Janatpour MJ, Utset MF, Cross JC, Rossant J, Dong J, Israel MA, Fisher SJ. A repertoire of differentially expressed transcription factors that offers insight into mechanisms of human cytotrophoblast differentiation.. Dev Genet 1999;25(2):146-57.
                pubmed: 10440849doi: 10.1002/(sici)1520-6408(1999)25:2<146::aid-dvg9>3.0.co;2-kgoogle scholar: lookup
              11. Red-Horse K, Zhou Y, Genbacev O, Prakobphol A, Foulk R, McMaster M, Fisher SJ. Trophoblast differentiation during embryo implantation and formation of the maternal-fetal interface.. J Clin Invest 2004 Sep;114(6):744-54.
                pmc: PMC516273pubmed: 15372095doi: 10.1172/jci22991google scholar: lookup
              12. Knöfler M, Meinhardt G, Vasicek R, Husslein P, Egarter C. Molecular cloning of the human Hand1 gene/cDNA and its tissue-restricted expression in cytotrophoblastic cells and heart.. Gene 1998 Dec 11;224(1-2):77-86.
                pubmed: 9931445doi: 10.1016/s0378-1119(98)00511-3google scholar: lookup
              13. Riley P, Anson-Cartwright L, Cross JC. The Hand1 bHLH transcription factor is essential for placentation and cardiac morphogenesis.. Nat Genet 1998 Mar;18(3):271-5.
                pubmed: 9500551doi: 10.1038/ng0398-271google scholar: lookup
              14. Allen WR, Stewart F. Equine placentation.. Reprod Fertil Dev 2001;13(7-8):623-34.
                pubmed: 11999314doi: 10.1071/rd01063google scholar: lookup
              15. Billington WD. The immunological problem of pregnancy: 50 years with the hope of progress. A tribute to Peter Medawar.. J Reprod Immunol 2003 Oct;60(1):1-11.
                pubmed: 14568673doi: 10.1016/s0165-0378(03)00083-4google scholar: lookup
              16. Holtz R, Choi JC, Petroff MG, Piskurich JF, Murphy SP. Class II transactivator (CIITA) promoter methylation does not correlate with silencing of CIITA transcription in trophoblasts.. Biol Reprod 2003 Sep;69(3):915-24.
                pubmed: 12748124doi: 10.1095/biolreprod.103.017103google scholar: lookup
              17. Maher JK, Tresnan DB, Deacon S, Hannah L, Antczak DF. Analysis of MHC class I expression in equine trophoblast cells using in situ hybridization.. Placenta 1996 Jul-Aug;17(5-6):351-9.
                pubmed: 8829219doi: 10.1016/s0143-4004(96)90060-0google scholar: lookup
              18. Handwerger S, Aronow B. Dynamic changes in gene expression during human trophoblast differentiation.. Recent Prog Horm Res 2003;58:263-81.
                pubmed: 12795423doi: 10.1210/rp.58.1.263google scholar: lookup
              19. Allen WR, Moor RM. The origin of the equine endometrial cups. I. Production of PMSG by fetal trophoblast cells.. J Reprod Fertil 1972 May;29(2):313-6.
                pubmed: 5023705doi: 10.1530/jrf.0.0290313google scholar: lookup
              20. Donaldson WL, Oriol JG, Plavin A, Antczak DF. Developmental regulation of class I major histocompatibility complex antigen expression by equine trophoblastic cells.. Differentiation 1992 Dec;52(1):69-78.
                pubmed: 1286777doi: 10.1111/j.1432-0436.1992.tb00501.xgoogle scholar: lookup
              21. Enders AC, Liu IK. Trophoblast-uterine interactions during equine chorionic girdle cell maturation, migration, and transformation.. Am J Anat 1991 Dec;192(4):366-81.
                pubmed: 1781447doi: 10.1002/aja.1001920405google scholar: lookup
              22. Enders AC, Liu IK. Lodgement of the equine blastocyst in the uterus from fixation through endometrial cup formation.. J Reprod Fertil Suppl 1991;44:427-38.
                pubmed: 1795287
              23. de Mestre AM, Bacon SJ, Costa CC, Leadbeater JC, Noronha LE, Stewart F, Antczak DF. Modeling trophoblast differentiation using equine chorionic girdle vesicles.. Placenta 2008 Feb;29(2):158-69.
                pubmed: 18054076doi: 10.1016/j.placenta.2007.10.005google scholar: lookup
              24. Wooding FB, Morgan G, Fowden AL, Allen WR. A structural and immunological study of chorionic gonadotrophin production by equine trophoblast girdle and cup cells.. Placenta 2001 Sep-Oct;22(8-9):749-67.
                pubmed: 11597196doi: 10.1053/plac.2001.0707google scholar: lookup
              25. Stewart F, Lennard SN, Allen WR. Mechanisms controlling formation of the equine chorionic girdle. Biol Reprod Mono 1995; 1: 151 159.
              26. Stout SS, Stewart F, Allen WR. The role of allantoic mesenchyme in the formation of the equine chorionic girdle. Theriogenology 2002; 58: 813 815.
              27. Adams AP, Antczak DF. Ectopic transplantation of equine invasive trophoblast.. Biol Reprod 2001 Mar;64(3):753-63.
                pubmed: 11207188doi: 10.1095/biolreprod64.3.753google scholar: lookup
              28. Antczak DF, Oriol JG, Donaldson WL, Poleman C, Stenzler L, Volsen SG, Allen WR. Differentiation molecules of the equine trophoblast.. J Reprod Fertil Suppl 1987;35:371-8.
                pubmed: 3479591
              29. Antczak DF, Bright SM, Remick LH, Bauman BE. Lymphocyte alloantigens of the horse. I. Serologic and genetic studies.. Tissue Antigens 1982 Sep;20(3):172-87.
                pubmed: 6182639doi: 10.1111/j.1399-0039.1982.tb00343.xgoogle scholar: lookup
              30. ntttttSome sequence data for this paper were retrieved from the Horse Genome Resource Database NCBI:ntttttNational Library of Medicine,ntttttBethesda, Maryland.ntttttWorld Wide Web (URL: http://www.ncbi.nlm.nih.gov/projects/genome/guide/horse/). (June, 2006).ntttt
              31. Rozen S, Skaletsky H. Primer3 on the WWW for general users and for biologist programmers.. Methods Mol Biol 2000;132:365-86.
                pubmed: 10547847doi: 10.1385/1-59259-192-2:365google scholar: lookup
              32. de Mestre AM, Khachigian LM, Santiago FS, Staykova MA, Hulett MD. Regulation of inducible heparanase gene transcription in activated T cells by early growth response 1.. J Biol Chem 2003 Dec 12;278(50):50377-85.
                pubmed: 14522979doi: 10.1074/jbc.m310154200google scholar: lookup
              33. Meller M, Vadachkoria S, Luthy DA, Williams MA. Evaluation of housekeeping genes in placental comparative expression studies.. Placenta 2005 Sep-Oct;26(8-9):601-7.
                pubmed: 16085039doi: 10.1016/j.placenta.2004.09.009google scholar: lookup
              34. Stewart F, Thomson JA, Leigh SE, Warwick JM. Nucleotide (cDNA) sequence encoding the horse gonadotrophin alpha-subunit.. J Endocrinol 1987 Nov;115(2):341-6.
                pubmed: 3437252doi: 10.1677/joe.0.1150341google scholar: lookup
              35. Matsui T, Sugino H, Miura M, Bousfield GR, Ward DN, Titani K, Mizuochi T. Beta-subunits of equine chorionic gonadotropin and lutenizing hormone with an identical amino acid sequence have different asparagine-linked oligosaccharide chains.. Biochem Biophys Res Commun 1991 Jan 31;174(2):940-5.
                pubmed: 1704232doi: 10.1016/0006-291x(91)91509-bgoogle scholar: lookup
              36. Degrelle SA, Campion E, Cabau C, Piumi F, Reinaud P, Richard C, Renard JP, Hue I. Molecular evidence for a critical period in mural trophoblast development in bovine blastocysts.. Dev Biol 2005 Dec 15;288(2):448-60.
                pubmed: 16289134doi: 10.1016/j.ydbio.2005.09.043google scholar: lookup
              37. Imakawa K, Kim MS, Matsuda-Minehata F, Ishida S, Iizuka M, Suzuki M, Chang KT, Echternkamp SE, Christenson RK. Regulation of the ovine interferon-tau gene by a blastocyst-specific transcription factor, Cdx2.. Mol Reprod Dev 2006 May;73(5):559-67.
                pubmed: 16489630doi: 10.1002/mrd.20457google scholar: lookup
              38. Hashemolhosseini S, Wegner M. Impacts of a new transcription factor family: mammalian GCM proteins in health and disease.. J Cell Biol 2004 Sep 13;166(6):765-8.
                pmc: PMC2172107pubmed: 15353544doi: 10.1083/jcb.200406097google scholar: lookup
              39. Chen CP, Chen CY, Yang YC, Su TH, Chen H. Decreased placental GCM1 (glial cells missing) gene expression in pre-eclampsia.. Placenta 2004 May;25(5):413-21.
                pubmed: 15081636doi: 10.1016/j.placenta.2003.10.014google scholar: lookup
              40. Cross JC, Nakano H, Natale DR, Simmons DG, Watson ED. Branching morphogenesis during development of placental villi.. Differentiation 2006 Sep;74(7):393-401.
                pubmed: 16916377doi: 10.1111/j.1432-0436.2006.00103.xgoogle scholar: lookup
              41. Yu C, Shen K, Lin M, Chen P, Lin C, Chang GD, Chen H. GCMa regulates the syncytin-mediated trophoblastic fusion.. J Biol Chem 2002 Dec 20;277(51):50062-8.
                pubmed: 12397062doi: 10.1074/jbc.m209316200google scholar: lookup
              42. Thway TM, Clay CM, Maher JK, Reed DK, McDowell KJ, Antczak DF, Eckert RL, Nilson JH, Wolfe MW. Immortalization of equine trophoblast cell lines of chorionic girdle cell lineage by simian virus-40 large T antigen.. J Endocrinol 2001 Oct;171(1):45-55.
                pubmed: 11572789doi: 10.1677/joe.0.1710045google scholar: lookup
              43. Akiyama Y, Hosoya T, Poole AM, Hotta Y. The gcm-motif: a novel DNA-binding motif conserved in Drosophila and mammals.. Proc Natl Acad Sci U S A 1996 Dec 10;93(25):14912-6.
                pmc: PMC26236pubmed: 8962155doi: 10.1073/pnas.93.25.14912google scholar: lookup
              44. Cohen SX, Moulin M, Hashemolhosseini S, Kilian K, Wegner M, Müller CW. Structure of the GCM domain-DNA complex: a DNA-binding domain with a novel fold and mode of target site recognition.. EMBO J 2003 Apr 15;22(8):1835-45.
                pmc: PMC154474pubmed: 12682016doi: 10.1093/emboj/cdg182google scholar: lookup
              45. Schreiber J, Sock E, Wegner M. The regulator of early gliogenesis glial cells missing is a transcription factor with a novel type of DNA-binding domain.. Proc Natl Acad Sci U S A 1997 Apr 29;94(9):4739-44.
                pmc: PMC20794pubmed: 9114061doi: 10.1073/pnas.94.9.4739google scholar: lookup
              46. Yamada K, Ogawa H, Honda S, Harada N, Okazaki T. A GCM motif protein is involved in placenta-specific expression of human aromatase gene.. J Biol Chem 1999 Nov 5;274(45):32279-86.
                pubmed: 10542267doi: 10.1074/jbc.274.45.32279google scholar: lookup
              47. Couture L, Lemonnier JP, Troalen F, Roser JF, Bousfield GR, Bellet D, Bidart JM. Immunochemical studies of equine chorionic gonadotropin (eCG), eCG alpha, and eCG beta.. Endocrinology 1993 Jan;132(1):205-11.
                pubmed: 7678214doi: 10.1210/endo.132.1.7678214google scholar: lookup
              48. Madersbacher S, Klieber R, Mann K, Marth C, Tabarelli M, Wick G, Berger P. Free alpha-subunit, free beta-subunit of human chorionic gonadotropin (hCG), and intact hCG in sera of healthy individuals and testicular cancer patients.. Clin Chem 1992 Mar;38(3):370-6.
                pubmed: 1372196
              49. Cross JC. How to make a placenta: mechanisms of trophoblast cell differentiation in mice--a review.. Placenta 2005 Apr;26 Suppl A:S3-9.
                pubmed: 15837063doi: 10.1016/j.placenta.2005.01.015google scholar: lookup
              50. Beck F, Erler T, Russell A, James R. Expression of Cdx-2 in the mouse embryo and placenta: possible role in patterning of the extra-embryonic membranes.. Dev Dyn 1995 Nov;204(3):219-27.
                pubmed: 8573715doi: 10.1002/aja.1002040302google scholar: lookup
              51. Adjaye J, Huntriss J, Herwig R, BenKahla A, Brink TC, Wierling C, Hultschig C, Groth D, Yaspo ML, Picton HM, Gosden RG, Lehrach H. Primary differentiation in the human blastocyst: comparative molecular portraits of inner cell mass and trophectoderm cells.. Stem Cells 2005 Nov-Dec;23(10):1514-25.
                pubmed: 16081659doi: 10.1634/stemcells.2005-0113google scholar: lookup

              Citations

              This article has been cited 13 times.
              1. Antczak DF, Allen WRT. Placentation in Equids. Adv Anat Embryol Cell Biol 2021;234:91-128.
                doi: 10.1007/978-3-030-77360-1_6pubmed: 34694479google scholar: lookup
              2. Lee JK, Oh SJ, Park H, Shin OS. Recent Updates on Research Models and Tools to Study Virus-Host Interactions at the Placenta. Viruses 2019 Dec 18;12(1).
                doi: 10.3390/v12010005pubmed: 31861492google scholar: lookup
              3. Pillai VV, Siqueira LG, Das M, Kei TG, Tu LN, Herren AW, Phinney BS, Cheong SH, Hansen PJ, Selvaraj V. Physiological profile of undifferentiated bovine blastocyst-derived trophoblasts. Biol Open 2019 May 1;8(5).
                doi: 10.1242/bio.037937pubmed: 30952696google scholar: lookup
              4. Read JE, Cabrera-Sharp V, Offord V, Mirczuk SM, Allen SP, Fowkes RC, de Mestre AM. Dynamic changes in gene expression and signalling during trophoblast development in the horse. Reproduction 2018 Oct 1;156(4):313–330.
                doi: 10.1530/REP-18-0270pubmed: 30306765google scholar: lookup
              5. Read JE, Cabrera-Sharp V, Offord V, Mirczuk SM, Allen SP, Fowkes RC, de Mestre AM. Dynamic changes in gene expression and signalling during trophoblast development in the horse. Reproduction 2018 Oct 1;156(4):313-330.
                doi: 10.1530/REP-18-0270pubmed: 29991567google scholar: lookup
              6. Read JE, Cabrera-Sharp V, Kitscha P, Cartwright JE, King PJ, Fowkes RC, de Mestre AM. Glial Cells Missing 1 Regulates Equine Chorionic Gonadotrophin Beta Subunit via Binding to the Proximal Promoter. Front Endocrinol (Lausanne) 2018;9:195.
                doi: 10.3389/fendo.2018.00195pubmed: 29755409google scholar: lookup
              7. Tachibana Y, Sakurai T, Bai H, Shiota K, Nambo Y, Nagaoka K, Imakawa K. RNA-seq analysis of equine conceptus transcripts during embryo fixation and capsule disappearance. PLoS One 2014;9(12):e114414.
                doi: 10.1371/journal.pone.0114414pubmed: 25514169google scholar: lookup
              8. Antczak DF, de Mestre AM, Wilsher S, Allen WR. The equine endometrial cup reaction: a fetomaternal signal of significance. Annu Rev Anim Biosci 2013 Jan;1:419-42.
                doi: 10.1146/annurev-animal-031412-103703pubmed: 25387026google scholar: lookup
              9. Cabrera-Sharp V, Read JE, Richardson S, Kowalski AA, Antczak DF, Cartwright JE, Mukherjee A, de Mestre AM. SMAD1/5 signaling in the early equine placenta regulates trophoblast differentiation and chorionic gonadotropin secretion. Endocrinology 2014 Aug;155(8):3054-64.
                doi: 10.1210/en.2013-2116pubmed: 24848867google scholar: lookup
              10. Noronha LE, Huggler KE, de Mestre AM, Miller DC, Antczak DF. Molecular evidence for natural killer-like cells in equine endometrial cups. Placenta 2012 May;33(5):379-86.
                doi: 10.1016/j.placenta.2012.01.018pubmed: 22357194google scholar: lookup
              11. Wilson ML, Brueggmann D, Desmond DH, Mandeville JE, Goodwin TM, Ingles SA. A fetal variant in the GCM1 gene is associated with pregnancy induced hypertension in a predominantly hispanic population. Int J Mol Epidemiol Genet 2011 Aug 30;2(3):196-206.
                pubmed: 21915358
              12. de Mestre AM, Hanlon D, Adams AP, Runcan E, Leadbeater JC, Erb HN, Costa CC, Miller D, Allen WR, Antczak DF. Functions of ectopically transplanted invasive horse trophoblast. Reproduction 2011 Jun;141(6):849-56.
                doi: 10.1530/REP-10-0462pubmed: 21389079google scholar: lookup
              13. Sievers J, Distl O. Genomic Patterns of Homozygosity and Genetic Diversity in the Rhenish German Draught Horse. Genes (Basel) 2025 Mar 11;16(3).
                doi: 10.3390/genes16030327pubmed: 40149478google scholar: lookup
              Subscribe to our newsletter
              Join 99,824 horse owners like you who receive our email updates on horse health and nutrition.