Blimp1/Prdm1 governs terminal differentiation of endovascular trophoblast giant cells and defines multipotent progenitors in the developing placenta

Genes and Development

Volumn 26, Issue 18, 2012, Pages 2063-2074

  Mould, Arne ^a   Morgan, Marc A J ^a   Li, Li ^a   Bikoff, Elizabeth K ^a   Robertson, Elizabeth J ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Blimp1 prdm1; Endovascular trophoblast giant cells; Placenta; Spiral artery; Trophoblast stem cells

Indexed keywords

B LYMPHOCYTE INDUCED MATURATION PROTEIN 1; BETA GALACTOSIDASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTERY; ARTICLE; BLIMP1 GENE; CELL DIFFERENTIATION; CELL INVASION; CELL LINEAGE; CELL POPULATION; CELL PROLIFERATION; CONTROLLED STUDY; DIPLOIDY; EMBRYO; FEMALE; GENE; GENE EXPRESSION; GENE FUNCTION; GIANT CELL; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LOSS OF FUNCTION MUTATION; MALE; MORPHOGENESIS; MOUSE; MULTIPOTENT STEM CELL; NONHUMAN; PLACENTA DEVELOPMENT; PRDM1 GENE; PRIORITY JOURNAL; SPIRAL ARTERY; SPONGIOTROPHOBLAST; TRANSCRIPTION REGULATION; TROPHOBLAST;

ANIMALS; CELL DIFFERENTIATION; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GIANT CELLS; MICE; PLACENTA; PREGNANCY; STEM CELLS; TRANSCRIPTION FACTORS; TROPHOBLASTS;

EID: 84866519031     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.199828.112     Document Type: Article

References (61)

1. Adamson SL, Lu Y, Whiteley KJ, Holmyard D, Hemberger M, Pfarrer C, Cross JC. 2002. Interactions between trophoblast cells and the maternal and fetal circulation in the mouse placenta. Dev Biol 250: 358-373.
2. Ancelin K, Lange UC, Hajkova P, Schneider R, Bannister AJ, Kouzarides T, Surani MA. 2006. Blimp1 associates with Prmt5 and directs histone arginine methylation in mouse germ cells. Nat Cell Biol 8: 623-630.
3. Anson-Cartwright L, Dawson K, Holmyard D, Fisher SJ, Lazzarini RA, Cross JC. 2000. The glial cells missing-1 protein is essential for branching morphogenesis in the chorioallantoic placenta. Nat Genet 25: 311-314.
4. Arnold SA, Sugnaseelan J, Groszer M, Srinivas S, Robertson EJ. 2009. Generation and analysis of a mouse line harboring GFP in the Eomes/Tbr2 locus. Genesis 47: 775-781.
5. Balbin M, Fueyo A, Knauper V, Lopez JM, Alvarez J, Sanchez LM, Quesada V, Bordallo J, Murphy G, Lopez-Otin C. 2001. Identification and enymatic characterization of two diverging murine counterparts of human intersitial collagenase (MMP-1) expressed at sites of embryonic implantation. J Biol Chem 276: 10253-10262.
6. Ben-Haim N, Lu C, Guzman-Ayala M, Pescatore L, Mesnard D, Bischofberger M, Naef F, Robertson EJ, Constam DB. 2006. The nodal precursor acting via activin receptors induces mesoderm by maintaining a source of its convertases and BMP4. Dev Cell 11: 313-323.
7. Bikoff EK, Morgan MA, Robertson EJ. 2009. An expanding job description for Blimp-1/PRDM1. Curr Opin Genet Dev 19: 1-7.
8. Bissonauth V, Roy S, Gravel M, Guillemette S, Charron J. 2006. Requirement for Map2k1 (Mek1) in extra-embryonic ectoderm during placentation. Development 133: 3429-3440.
9. Bouillot S, Rampon C, Tillet E, Huber P. 2006. Tracing the gylcogen cells with protocadherin 12 during mouse placenta development. Placenta 27: 882-888.
10. Brown LJ, Alawoki M, Crawford ME, Reida T, Sears A, Torma T, Albig AR. 2010. Lipocalin-7 is a matricellular regulator of angiogenesis. PLoS ONE 5: e13905. doi: 10.1371/journal.pone.0013905.
11. Constam DB, Robertson EJ. 2000. SPC4/PACE4 regulates a TGF b signalling network during axis formation. Genes Dev 14: 1146-1155.
12. Crotty S, Johnston RJ, Schoenberger SP. 2010. Effectors and memories: Bcl-6 and Blimp-1 in T and B lymphocyte differentiation. Nat Immunol 11: 114-120.
13. Doody GM, Care MA, Burgoyne NJ, Bradford JR, Bota M, Bonifer C, Westhead DR, Tooze RM. 2010. An extended set of PRDM1/BLIMP1 target genes links binding motif type to dynamic repression. Nucleic Acids Res 38: 5336-5350.
14. Geng Y, Yu Q, Sicinska E, Das M, Schneider JE, Bhattacharya S, Rideout WM, Bronson RT, Gardner H, Sicinski P. 2003. Cyclin E ablation in the mouse. Cell 114: 431-443.
15. Gonzalez MA, Tachibana KE, Adams DJ, van der Weyden L, Hemberger M, Coleman N, Bradley A, Laskey RA. 2006. Geminin is essential to prevent endoreduplication and to form pluripotent cells during mammalian development. Genes Dev 20: 1880-1884.
16. Guillemot F, Nagy A, Auerbach A, Rossant J, Joyner AL. 1994. Essential role of Mash-2 in extraembryonic development. Nature 371: 333-336.
17. Guzman-Ayala M, Ben-Haim N, Beck S, Constam DB. 2004. Nodal protein processing and fibroblast growth factor 4 synergize to maintain a trophoblast stem cell microenvironment. Proc Natl Acad Sci 101: 15656-15660.
18. Harper J, Mould A, Andrews RM, Bikoff E, Robertson EJ. 2011. The transcriptional repressor Blimp1/Prdm1 regulates postnatal reprogramming of intestinal enterocytes. Proc Natl Acad Sci 108: 10585-10590.
19. Hemberger M, Himmelbauer H, Ruschmann J, Zeitz C, Fundele R. 2000. cDNA subtraction cloning reveals novel genes whose temporal and spatial expression indicates association with trophoblast invasion. Dev Biol 222: 158-169.
20. Hemberger M, Nozaki T, Masutani M, Cross JC. 2003. Differential expression of angiogenic and vasodilatory factors by invasive trophoblast giant cells depending on depth of invasion. Dev Dyn 227: 185-191.
21. Horsley V, O'Carroll DO, Tooze R, Ohinata Y, Saitou M, Obukhanych T, Nussenzweig M, Tarakhovsky A, Fuchs E. 2006. Blimp1 defines a progenitor population that governs cellular input to the sebaceous gland. Cell 126: 597-609.
22. Hu D, Cross JC. 2010. Development and function of trophoblast giant cells in the rodent placenta. Int J Dev Biol 54: 341-354.
23. Hu D, Cross JC. 2011. Ablation of Tpbpa-positive trophoblast precursors leads to defects in maternal spiral artery remodeling in the mouse placenta. Dev Biol 358: 231-239.
24. Huang DW, Sherman BT, Lempicki RA. 2009. Systematic and integrative analysis of large gene lists using DAVID Bioinformatics Resources. Nat Protoc 4: 44-57.
25. Kallies A, Nutt SL. 2007. Terminal differentiation of lymphocytes depends on Blimp-1. Curr Opin Immunol 19: 156-162.
26. Kallies A, Hasbold J, Tarlinton DM, Dietricch W, Corocoran LM, Hodgkin PD, Nutt SL. 2004. Plasma cell ontogeny defined by quantitative changes in blimp-1 expression. J Exp Med 200: 967-977.
27. Kallies A, Carotta S, Huntington ND, Bernard NJ, Tarlinton DM, Smyth MJ, Nutt SL. 2011. A role for Blimp1 in the transcriptional network controlling natural killer cell maturation. Blood 117: 1869-1879.
28. Ma GT, Soloveva V, Tzeng SJ, Lowe LA, Pfendler KC, Iannoccone PM, Kuehn MR, Linzer DIH. 2001. Nodal regulates trophoblast differentiation and placental development. Dev Biol 236: 124-135.
29. Magnusdottir E, Kalachikov S, Mizukoshi K, Savitsky D, Ishida-Yamamoto A, Panteleyev AA, Calame K. 2007. Epidermal terminal differentiation depends on B lymphocyte-induced maturation protein-1. Proc Natl Acad Sci 104: 14988-14993.
30. Manzur M, Ganss R. 2009. Regulator of G protein signalling 5: A new player in vascular remodelling. Trends Cardiovasc Med 19: 26-30.
31. Martins G, Calame K. 2008. Regulation and functions of Blimp-1 in T and B lymphocytes. Annu Rev Immunol 26: 133-169.
32. Moffett A, Loke C. 2006. Immunology of placentation in eutherian mammals. Nat Rev Immunol 6: 584-594.
33. Morgan MA, Magnusdottir E, Kuo TC, Tunyaplin C, Harper J, Arnold SJ, Calame K, Robertson EJ, Bikoff EK. 2009. Blimp-1/Prdm1 alternative promoter usage during mouse development and plasma cell differentiation. Mol Cell Biol 29: 5813-5827.
34. Navankasattusas S, Whitehead KJ, Suli A, Sorensen LK, Lim AH, Zhao J, Park KW, Wythe JD, Thomas KR, Chien CB, et al. 2008. The netrin receptor UNC5B promotes angiogenesis in specific vascular beds. Development 135: 659-667.
35. Nagy A, Gertsenstein M, Vintersten K, Behringer R. 2003. Manipulating the mouse embryo: A laboratory manual. Cold Spring Harbor Lab Press, Cold Spring Harbor, NY.
36. Niwa H, Toyooka Y, Shimosato D, Strumpf D, Takahashi K, Yagi R, Rossant J. 2005. Interaction between Oct3/4 and Cdx2 determines trophectoderm differentiation. Cell 123: 917-929.
37. Nutt SL, Fairfax KA, Kallies A. 2007. BLIMP1 guides the fate of effector B and T cells. Nat Rev Immunol 7: 923-927.
38. Ohinata Y, Payer B, O'Carroll D, Ancelin K, Ono Y, Sano M, Barton SC, Obukhanych T, Nussenzweig M, Tarakhovsky A, et al. 2005. Blimp1 is a critical determinant of the germ cell lineage in mice. Nature 436: 207-213.
39. Paria BC, Ma W, Tan J, Raja S, Das SK, Dey SK, Hogan BLM. 2001. Cellular and molecular responses of the uterus to embryo implantation can be elicited by locally applied growth factors. Proc Natl Acad Sci 98: 1047-1052.
40. Parisi T, Beck AR, Rougier N, McNeil T, Lucian L, Werb Z, Amati B. 2003. Cyclins E1 and E2 are required for endoreplication in placental trophoblast giant cells. EMBO J 22: 4794-4803.
41. Riley P, Anson-Cartwright L, Cross JC. 1998. The Hand1 bHLH transcription factor is essential for placentation and cardiac morphogenesis. Nat Genet 18: 271-275.
42. Robertson EJ, Charatsi I, Joyner CJ, Koonce CH, Morgan M, Islam A, Paterson C, Lejsek E, Arnold SJ, Kallies A, et al. 2007. Blimp1 regulates development of the posterior forelimb, caudal pharyngeal arches, heart and sensory vibrissae in mice. Development 134: 4335-4345.
43. Russ AP, Wattler S, Colledge WH, Aparicio SA, Carlton MB, Pearce JJ, Barton SC, Surani MA, Ryan K, Nehls MC, et al. 2000. Eomesodermin is required for mouse trophoblast development and mesoderm formation. Nature 404: 95-99.
44. Scott IC, Anson-Cartwright L, Riley P, Reda D, Cross JC. 2000. The Hand1 basic helix-loop-helix transcription factor regulates trophoblast differentiation via multiple mechanisms. Mol Cell Biol 20: 530-541.
45. Screen M, Dean W, Cross JC, Hemberger M. 2008. Cathepsin proteases have distinct roles in trophoblast function and vascular remodelling. Development 135: 3311-3320.
46. Shalaby F, Rossant J, Yamaguchi TP, Gertsenstein M, Wu XF, Breitman ML, Schuh AC. 1995. Failure of blood-island formation and vasculagenesis in Flk-1-deficient mice. Nature 376: 62-66.
47. Shimshek DR, Kim J, Hübner MR, Spergel DJ, Buchholz F, Casanova E, Stewart AF, Seeburg PH, Sprengel R. 2002. Codon-improved Cre recombinase (iCre) expression in the mouse. Genesis 34: 208-214.
48. Simmons DG, Cross JC. 2005. Determinants of trophoblast lineage and cell subtype specification in the mouse placenta. Dev Biol 284: 12-24.
49. Simmons DG, Fortier AL, Cross JC. 2007. Diverse subtypes and developmental origins of trophoblast giant cells in the mouse placenta. Dev Biol 304: 567-578.
50. Simmons DG, Natale DRC, Begay V, Hughes M, Leutz A, Cross JC. 2008a. Early patterning of the chorion leads to the trilaminar trophoblast cell structure in the placental labyrinth. Development 135: 2083-2091.
51. Simmons DG, Rawn S, Davies A, Hughes M, Cross JC. 2008b. Spatial and temporal expression of the 23 murine prolactin/placental lactogen-related genes is not associated with their position in the locus. BMC Genomics 9: 352-372.
52. Smith MA, Maurin M, Cho HI, Becknell B, Freud AG, Yu J, Wei S, Djeu J, Celis E, Caligiuri MA, et al. 2010. PRDM1/Blimp1 controls effector cytokine production in human NK cells. J Immunol 185: 6058-6067.
53. Soriano P. 1999. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 21: 70-71.
54. Strumpf D, Mao CA, Yamanaka Y, Ralston A, Chawengsaksophak K, Beck F, Rossant J. 2005. Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst. Development 132: 2093-2102.
55. Tanaka M, Gertsenstein M, Rossant J, Nagy A. 1997. Mash2 acts cell autonomously in mouse spongiotrophoblast development. Dev Biol 190: 55-65.
56. Tanaka S, Kunath T, Hadjantonakis AK, Nagy A, Rossant J. 1998. Promotion of trophoblast stem cell proliferation by FGF2. Science 282: 2072-2075.
57. Tesser RB, Scherholz PLA, do Nascimento L, Katz SG. 2010. Trophoblast glycogen cells differentiate early in the mouse ectoplacental cone: Putative role during placentation. Histochem Cell Biol 134: 83-92.
58. Vincent SD, Dunn NR, Sciammas R, Shapiro-Shalef M, Davis MM, Calame K, Bikoff EK, Robertson EJ. 2005. The zinc finger transcriptional repressor Blimp1/Prdm1 is dispensable for early axis formation but is required for specification of primordial germ cells in the mouse. Development 132: 1315-1325.
59. Watson ED, Cross JC. 2005. Development of structures and transport functions in the mouse placenta. Physiology (Bethesda) 20: 180-193.
60. Welch RM. 2009. Blimp hovers over Tcell immunity. Immunity 31: 178-180.
61. Winn VD, Haimov-Kochman R, Paquet AC, Yang YJ, Madhusudhan MS, Gormley M, Feng KT, Bernlohr DA, McDonagh S, Pereira L, et al. 2007. Gene expression profiling of the human maternal-fetal interface reveals dramatic changes between midgestation and term. Endocrinology 148: 1059-1079.