OVO-like 1 regulates progenitor cell fate in human trophoblast development

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 45, 2015, Pages E6175-E6184

  Renaud, Stephen J ^a,b,c   Chakraborty, Damayanti ^a,b   Mason, Clifford W ^a   Karim Rumi, M A ^a,b   Vivian, Jay L ^a,b   Soares, Michael J ^a,b  

^a UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ASCL2 PROTEIN; CELL PROTEIN; INHIBITOR OF DIFFERENTIATION 1; MYC PROTEIN; TP63 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR OVO LIKE 1; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; OVOL1 PROTEIN, HUMAN; SMALL INTERFERING RNA;

CELL DIFFERENTIATION; CELL FATE; CELL MATURATION; CELL STIMULATION; CONFERENCE PAPER; CYTOTROPHOBLAST; FEMALE; GENE EXPRESSION; HORMONE SYNTHESIS; HUMAN; HUMAN CELL; PLACENTA; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; STEM CELL; SYNCYTIOTROPHOBLAST; ANALYSIS OF VARIANCE; ANIMAL; C57BL MOUSE; CHROMATIN IMMUNOPRECIPITATION; CYTOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; METABOLISM; MICROARRAY ANALYSIS; MOLECULAR GENETICS; MOUSE; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PREGNANCY; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; SPRAGUE DAWLEY RAT; TROPHOBLAST; WESTERN BLOTTING;

ANALYSIS OF VARIANCE; ANIMALS; BASE SEQUENCE; BLOTTING, WESTERN; CELL DIFFERENTIATION; CHROMATIN IMMUNOPRECIPITATION; DNA-BINDING PROTEINS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MICE; MICE, INBRED C57BL; MICROARRAY ANALYSIS; MOLECULAR SEQUENCE DATA; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; SEQUENCE ANALYSIS, RNA; STEM CELLS; TRANSCRIPTION FACTORS; TROPHOBLASTS;

EID: 84946781127     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1507397112     Document Type: Article

References (61)

1. Simpson RA, Mayhew TM, Barnes PR (1992) From 13 weeks to term, the trophoblast of human placenta grows by the continuous recruitment of new proliferative units: A study of nuclear number using the disector. Placenta 13(5):501-512.
2. Benirschke K, Burton GJ, Baergen RN (2012) Pathology of the Human Placenta (Springer, New York).
3. Ishihara N, et al. (2002) Increased apoptosis in the syncytiotrophoblast in human term placentas complicated by either preeclampsia or intrauterine growth retardation. Am J Obstet Gynecol 186(1):158-166.
4. Gauster M, Moser G, Orendi K, Huppertz B (2009) Factors involved in regulating trophoblast fusion: Potential role in the development of preeclampsia. Placenta 30(Suppl A):S49-54.
5. Fitzgerald B, et al. (2011) Villous trophoblast abnormalities in extremely preterm deliveries with elevated second trimester maternal serum hCG or inhibin-A. Placenta 32(4):339-345.
6. Tannetta DS, Dragovic RA, Gardiner C, Redman CW, Sargent IL (2013) Characterisation of syncytiotrophoblast vesicles in normal pregnancy and pre-eclampsia: Expression of Flt-1 and endoglin. PLoS One 8(2):e56754.
7. Knight M, Redman CW, Linton EA, Sargent IL (1998) Shedding of syncytiotrophoblast microvilli into the maternal circulation in pre-eclamptic pregnancies. Br J Obstet Gynaecol 105(6):632-640.
8. Huppertz B, Gauster M (2011) Trophoblast fusion. Adv Exp Med Biol 713:81-95.
9. Handwerger S (2010) New insights into the regulation of human cytotrophoblast cell differentiation. Mol Cell Endocrinol 323(1):94-104.
10. Loregger T, Pollheimer J, & Knofler M (2003) Regulatory transcription factors controlling function and differentiation of human trophoblast-A review. Placenta 24(Suppl A):S104-110.
11. Blaise S, de Parseval N, Bénit L, Heidmann T (2003) Genomewide screening for fusogenic human endogenous retrovirus envelopes identifies syncytin 2, a gene conserved on primate evolution. Proc Natl Acad Sci USA 100(22):13013-13018.
12. Mi S, et al. (2000) Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 403(6771):785-789.
13. Liang CY, et al. (2010) GCM1 regulation of the expression of syncytin 2 and its cognate receptor MFSD2A in human placenta. Biol Reprod 83(3):387-395.
14. Yu C, et al. (2002) GCMa regulates the syncytin-mediated trophoblastic fusion. J Biol Chem 277(51):50062-50068.
15. Johnson AD, Fitzsimmons D, Hagman J, Chamberlin HM (2001) EGL-38 Pax regulates the ovo-related gene lin-48 during Caenorhabditis elegans organ development. Development 128(15):2857-2865.
16. Payre F, Vincent A, Carreno S (1999) ovo/svb integrates Wingless and DER pathways to control epidermis differentiation. Nature 400(6741):271-275.
17. Dai X, et al. (1998) The ovo gene required for cuticle formation and oogenesis in flies is involved in hair formation and spermatogenesis in mice. Genes Dev 12(21): 3452-3463.
18. Li B, et al. (2005) Ovol1 regulates meiotic pachytene progression during spermatogenesis by repressing Id2 expression. Development 132(6):1463-1473.
19. Nair M, et al. (2006) Ovol1 regulates the growth arrest of embryonic epidermal progenitor cells and represses c-myc transcription. J Cell Biol 173(2):253-264.
20. Teng A, Nair M, Wells J, Segre JA, Dai X (2007) Strain-dependent perinatal lethality of Ovol1-deficient mice and identification of Ovol2 as a downstream target of Ovol1 in skin epidermis. Biochim Biophys Acta 1772(1):89-95.
21. Chidambaram A, et al. (1997) Characterization of a human homolog (OVOL1) of the Drosophila ovo gene, which maps to chromosome 11q13. Mamm Genome 8(12): 950-951.
22. Wice B, Menton D, Geuze H, Schwartz AL (1990) Modulators of cyclic AMP metabolism induce syncytiotrophoblast formation in vitro. Exp Cell Res 186(2):306-316.
23. Xu RH, et al. (2002) BMP4 initiates human embryonic stem cell differentiation to trophoblast. Nat Biotechnol 20(12):1261-1264.
24. Amita M, et al. (2013) Complete and unidirectional conversion of human embryonic stem cells to trophoblast by BMP4. Proc Natl Acad Sci USA 110(13):E1212-E1221.
25. Ezashi T, Telugu BP, Roberts RM (2012) Model systems for studying trophoblast differentiation from human pluripotent stem cells. Cell Tissue Res 349(3):809-824.
26. Li Y, et al. (2013) BMP4-directed trophoblast differentiation of human embryonic stem cells is mediated through a δNp63+ cytotrophoblast stem cell state. Development 140(19):3965-3976.
27. Nair M, Bilanchone V, Ortt K, Sinha S, Dai X (2007) Ovol1 represses its own transcription by competing with transcription activator c-Myb and by recruiting histone deacetylase activity. Nucleic Acids Res 35(5):1687-1697.
28. Tanaka M, Gertsenstein M, Rossant J, Nagy A (1997) Mash2 acts cell autonomously in mouse spongiotrophoblast development. Dev Biol 190(1):55-65.
29. Vargas A, et al. (2009) Syncytin-2 plays an important role in the fusion of human trophoblast cells. J Mol Biol 392(2):301-318.
30. Orendi K, Gauster M, Moser G, Meiri H, Huppertz B (2010) The choriocarcinoma cell line BeWo: Syncytial fusion and expression of syncytium-specific proteins. Reproduction 140(5):759-766.
31. Staab S, Steinmann-Zwicky M (1996) Female germ cells of Drosophila require zygotic ovo and otu product for survival in larvae and pupae respectively. Mech Dev 54(2): 205-210.
32. Delon I, Chanut-Delalande H, Payre F (2003) The Ovo/Shavenbaby transcription factor specifies actin remodelling during epidermal differentiation in Drosophila. Mech Dev 120(7):747-758.
33. Albrecht ED, Pepe GJ (1990) Placental steroid hormone biosynthesis in primate pregnancy. Endocr Rev 11(1):124-150.
34. Esnault C, Cornelis G, Heidmann O, Heidmann T (2013) Differential evolutionary fate of an ancestral primate endogenous retrovirus envelope gene, the EnvV syncytin, captured for a function in placentation. PLoS Genet 9(3):e1003400.
35. Watanabe K, et al. (2014) Mammary morphogenesis and regeneration require the inhibition of EMT at terminal end buds by Ovol2 transcriptional repressor. Dev Cell 29(1):59-74.
36. Diebold J, Arnholdt H, Lai MD, Löhrs U (1991) C-myc expression in early human placenta-A critical evaluation of its localization. Virchows Arch B Cell Pathol Incl Mol Pathol 61(1):65-73.
37. Xue WC, et al. (2005) Id helix-loop-helix proteins are differentially expressed in gestational trophoblastic disease. Histopathology 47(3):303-309.
38. Lee Y, et al. (2007) A unifying concept of trophoblastic differentiation and malignancy defined by biomarker expression. Hum Pathol 38(7):1003-1013.
39. Lasorella A, Uo T, Iavarone A (2001) Id proteins at the cross-road of development and cancer. Oncogene 20(58):8326-8333.
40. Waikel RL, Kawachi Y, Waikel PA, Wang XJ, Roop DR (2001) Deregulated expression of c-Myc depletes epidermal stem cells. Nat Genet 28(2):165-168.
41. Romano RA, et al. (2012) δNp63 knockout mice reveal its indispensable role as a master regulator of epithelial development and differentiation. Development 139(4): 772-782.
42. Li Y, Moretto-Zita M, Leon-Garcia S, Parast MM (2014) p63 inhibits extravillous trophoblast migration and maintains cells in a cytotrophoblast stem cell-like state. Am J Pathol 184(12):3332-3343.
43. Jiang B, Kamat A, Mendelson CR (2000) Hypoxia prevents induction of aromatase expression in human trophoblast cells in culture: Potential inhibitory role of the hypoxia-inducible transcription factor Mash-2 (mammalian achaete-scute homologous protein-2). Mol Endocrinol 14(10):1661-1673.
44. Jiang B, Mendelson CR (2003) USF1 and USF2 mediate inhibition of human trophoblast differentiation and CYP19 gene expression by Mash-2 and hypoxia. Mol Cell Biol 23(17):6117-6128.
45. Kumar P, Luo Y, Tudela C, Alexander JM, Mendelson CR (2013) The c-Myc-regulated microRNA-17 92 (miR-17 92) and miR-106a 363 clusters target hCYP19A1 and hGCM1 to inhibit human trophoblast differentiation. Mol Cell Biol 33(9):1782-1796.
46. Lee B, et al. (2014) Transcriptional mechanisms link epithelial plasticity to adhesion and differentiation of epidermal progenitor cells. Dev Cell 29(1):47-58.
47. Baczyk D, et al. (2009) Glial cell missing-1 transcription factor is required for the differentiation of the human trophoblast. Cell Death Differ 16(5):719-727.
48. Anson-Cartwright L, et al. (2000) The glial cells missing-1 protein is essential for branching morphogenesis in the chorioallantoic placenta. Nat Genet 25(3):311-314.
49. Baczyk D, et al. (2004) Complex patterns of GCM1 mRNA and protein in villous and extravillous trophoblast cells of the human placenta. Placenta 25(6):553-559.
50. Unezaki S, Horai R, Sudo K, Iwakura Y, Ito S (2007) Ovol2/Movo, a homologue of Drosophila ovo, is required for angiogenesis, heart formation and placental development in mice. Genes Cells 12(6):773-785.
51. Kumar A, et al. (2012) Molecular phylogeny of OVOL genes illustrates a conserved C2H2 zinc finger domain coupled by hypervariable unstructured regions. PLoS One 7(6):e39399.
52. Roca H, et al. (2013) Transcription factors OVOL1 and OVOL2 induce the mesenchymal to epithelial transition in human cancer. PLoS One 8(10):e76773.
53. Kliman HJ, Nestler JE, Sermasi E, Sanger JM, Strauss JF, 3rd (1986) Purification, characterization, and in vitro differentiation of cytotrophoblasts from human term placentae. Endocrinology 118(4):1567-1582.
54. Schulz LC, et al. (2008) Human embryonic stem cells as models for trophoblast differentiation. Placenta 29(Suppl A):S10-16.
55. Boulting GL, et al. (2011) A functionally characterized test set of human induced pluripotent stem cells. Nat Biotechnol 29(3):279-286.
56. Tanaka S, Kunath T, Hadjantonakis AK, Nagy A, Rossant J (1998) Promotion of trophoblast stem cell proliferation by FGF4. Science 282(5396):2072-2075.
57. Asanoma K, et al. (2011) FGF4-dependent stem cells derived from rat blastocysts differentiate along the trophoblast lineage. Dev Biol 351(1):110-119.
58. Huang W, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4(1):44-57.
59. Renaud SJ, Kubota K, Rumi MA, Soares MJ (2014) The FOS transcription factor family differentially controls trophoblast migration and invasion. J Biol Chem 289(8): 5025-5039.
60. Lee DS, Rumi MA, Konno T, Soares MJ (2009) In vivo genetic manipulation of the rat trophoblast cell lineage using lentiviral vector delivery. Genesis 47(7):433-439.
61. Oliver B, Perrimon N, Mahowald AP (1987) The ovo locus is required for sex-specific germ line maintenance in Drosophila. Genes Dev 1(9):913-923.