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

Biology of Reproduction

Volumn 80, Issue 2, 2009, Pages 227-234

  De Mestre, Amanda M ^a,b   Miller, Donald ^a   Roberson, Mark S ^a   Liford, Jenny ^a   Chizmar, Lisay C ^a   McLaughlin, Kristin E ^a   Antczak, Douglas F ^a  

^a Department of Obstetrics Gynecology   (United States)

^b ROYAL VETERINARY COLLEGE   (United Kingdom)

Author keywords

CDX2; Chorionic girdle; Chorionic gonadotropin; Conceptus; Differentiation; DLX3; Endometrial cups; EOMES; Equine chorionic gonadotropin; GCM1; HAND1; Horse; Transcription factors; Trophoblast

Indexed keywords

CHORIONIC GONADOTROPIN BETA SUBUNIT; EOMESODERMIN; MESSENGER RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CDX2; TRANSCRIPTION FACTOR DLX3; TRANSCRIPTION FACTOR DLX5; TRANSCRIPTION FACTOR GCM 1; TRANSCRIPTION FACTOR HAND1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CELL DIFFERENTIATION; CELL FUNCTION; CELL STRUCTURE; CHORION; CONTROLLED STUDY; FETUS DEVELOPMENT; FIRST TRIMESTER PREGNANCY; GENE EXPRESSION; HORSE; NONHUMAN; PLACENTA FUNCTION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SYNCYTIOTROPHOBLAST; TROPHOBLAST;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; FEMALE; FETUS; GESTATIONAL AGE; HORSES; MODELS, BIOLOGICAL; NEUROPEPTIDES; PREGNANCY; PREGNANCY, ANIMAL; TRANSCRIPTION FACTORS; TROPHOBLASTS; UP-REGULATION;

EQUIDAE;

EID: 59949097595     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.108.070920     Document Type: Article

References (51)

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; 24:123-130.
2. 2.Loregger T, Pollheimer J, Knofler M. Regulatory transcription factors controlling function and differentiation of human trophoblast: a review. Placenta 2003; 24(suppl A):S104-S110.
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; 404:95-99.
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; 25:553-559.
5. Nait-Oumesmar B, Copperman AB, Lazzarini RA. Placental expression and chromosomal localization of the human Gcm 1 gene. J Histochem Cytochem 2000; 48:915-922.
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; 25:311-314.
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; 20:530-541.
8. Chawengsaksophak K, James R, Hammond VE, Kontgen F, Beck F. Homeosis and intestinal tumours in Cdx2 mutant mice. Nature 1997; 386: 84-87.
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; 96:162-167.
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; 25:146-157.
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; 114:744-754.
12. Knofler 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; 224:77-86.
13. Riley P, Anson-Cartwright L, Cross JC. The Hand1 bHLH transcription factor is essential for placentation and cardiac morphogenesis. Nat Genet 1998; 18:271-275.
14. Allen WR, Stewart F. Equine placentation. Reprod Fertil Dev 2001; 13: 623-634.
15. Billington WD. The immunological problem of pregnancy: 50 years with the hope of progress: a tribute to Peter Medawar. J Reprod Immunol 2003; 60:1-11.
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; 69: 915-924.
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; 17:351-359.
18. Handwerger S, Aronow B. Dynamic changes in gene expression during human trophoblast differentiation. Recent Prog Horm Res 2003; 58:263-281.
19. Allen WR, Moor RM. The origin of the equine endometrial cups, I: production of PMSG by fetal trophoblast cells. J Reprod Fertil 1972; 29: 313-316.
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; 52:69-78.
21. Enders AC, Liu IK. Trophoblast-uterine interactions during equine chorionic girdle cell maturation, migration, and transformation. Am J Anat 1991; 192:366-381.
22. Enders AC, Liu IKM. Lodgement of the equine blastocyst in the uterus from fixation through endometrial cup formation. J Reprod Fertil Suppl 1991; 44:427-438.
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; 29:158-169.
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; 22:749-767.
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; 64:753-763.
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; 35:371-378.
29. Antczak DF, Bright SM, Remick LH, Bauman BE. Lymphocyte alloantigens of the horse, I: serologic and genetic studies. Tissue Antigens 1982; 20:172-187.
30. Some sequence data for this paper were retrieved from the Horse Genome Resource Database NCBI: National Library of Medicine, Bethesda, Maryland. World Wide Web (URL: http://www.ncbi.nlm.nih.gov/projects/genome/guide/horse/). (June, 2006).
31. Rozen S, Skaletsky HJ. Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds.), Bioinformatic Methods and Protocols: Methods in Molecular Biology. Totowa, NJ: Humana Press; 2000:365-386.
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; 278:50377-50385.
33. Meller M, Vadachkoria S, Luthy DA, Williams MA. Evaluation ofhousekeeping genes in placental comparative expression studies. Placenta 2005; 26:601-607.
34. Stewart F, Thomson JA, Leigh SE, Warwick JM. Nucleotide (cDNA) sequence encoding the horse gonadotrophin alpha-subunit. J Endocrinol 1987; 115:341-346.
35. Matsui T, Sugino H, Miura M, Bousfield GR, Ward DN, Titani K, Mizuochi T. Beta-subunits of equine chorionic gonadotropin and luteinizing hormone with an identical amino acid sequence have different asparagine-linked oligosaccharide chains. Biochem Biophys Res Commun 1991; 174:940-945.
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; 288:448-460.
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; 73:559-567.
38. Hashemolhosseini S, Wegner M. Impacts of a new transcription factor family: mammalian GCM proteins in health and disease. J Cell Biol 2004; 166:765-768.
39. Chen CP, Chen CY, Yang YC, Su TH, Chen H. Decreased placental GCM1 (glial cells missing) gene expression in pre-eclampsia. Placenta 2004; 25:413-121.
40. Cross JC, Nakano H, Natale DR, Simmons DG, Watson ED. Branching morphogenesis during development of placental villi. Differentiation 2006; 74:393-401.
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; 277:50062-50068.
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 Tantigen. J Endocrinol 2001; 171:45-55.
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; 93:14912-14916.
44. Cohen SX, Moulin M, Hashemolhosseini S, Kilian K, Wegner M, Muller 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; 22:1835-1845.
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; 94:4739-4744.
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; 274:32279-32286.
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; 132:205-211.
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; 38:370-376.
49. Cross JC. How to make a placenta: mechanisms of trophoblast cell differentiation in mice: a review. Placenta 2005; 26(suppl A):S3-S9.
50. Beck F, Erler T, Russell A, James R. Expression of Cdx-2 in the mouseembryo and placenta: possible role in patterning of the extra-embryonic membranes. Dev Dyn 1995; 204:219-227.
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; 23: 1514-1525.