Origin and characteristics of glycogen cells in the developing murine placenta

Developmental Dynamics

Volumn 235, Issue 12, 2006, Pages 3280-3294

  Coan, P M ^a   Conroy, N ^a   Burton, G J ^a   Ferguson Smith, A C ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Genomic imprinting; Glycogen cells; Invasion; Junctional zone; Migration; Mouse; Placenta; Stereology; Trophoblast

Indexed keywords

CONNEXIN 31; DECORIN; GELATINASE B; GLUCAGON; GLYCOGEN; SOMATOMEDIN B; SOMATOMEDIN B RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL INVASION; CELL JUNCTION; CELL MIGRATION; CELL POPULATION; CELL SIZE; CELL TYPE; CELL VOLUME; DECIDUA; GENE EXPRESSION REGULATION; GENOME IMPRINTING; GROWTH REGULATION; MOUSE; NONHUMAN; PLACENTA DEVELOPMENT; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; STEREOLOGY; TROPHOBLAST;

ANIMALS; CELL COUNT; CELL MOVEMENT; CELL SIZE; CONNEXINS; CYCLIN-DEPENDENT KINASE INHIBITOR P57; EXTRACELLULAR MATRIX PROTEINS; FEMALE; GESTATIONAL AGE; GLUCAGON; GLYCOGEN; IMMUNOHISTOCHEMISTRY; KI-67 ANTIGEN; MALE; MATRIX METALLOPROTEINASE 9; MICE; MICE, INBRED C57BL; PLACENTA; PREGNANCY; PROTEOGLYCANS; RECEPTOR, IGF TYPE 2;

MURINAE;

EID: 33845360672     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.20981     Document Type: Article

References (81)

1. Adamson SL, Yong L, 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. Ain R, Canham LN, Soares MJ. 2003. Gestation stage-dependent intrauterine trophoblast cell invasion in the rat and mouse: novel endocrine phenotype and regulation. Dev Biol 260:176-190.
3. Baker J, Liu J-P, Efstratiadis A. 1993. Role of insulin-like growth factors in embryonic and postnatal growth. Cell 75:73-82.
4. Bany BM, Harvey MB, Schultz GA. 2000. Expression of matrix metalloproteinases 2 and 9 in the mouse uterus during implantation and oil-induced decidualization. J Reprod Fertil 120:125-134.
5. Barash V, Shafrir E. 1990. Mobilization of placental glycogen in diabetic rats. Placenta 11:515-521.
6. Behrendtsen O, Alexander C, Werb Z. 1992. Metalloproteinases mediate extracellular matrix degradation by cells from mouse blastocyst outgrowths. Development 114:447-456.
7. Bouillot S, Rampon C, Tillet E, Huber P. 2006. Tracing the glycogen cells with protocadherin 12 during mouse placenta development. Placenta 27:882-888.
8. Coan PM, Ferguson-Smith AC, Burton GJ. 2004. Developmental dynamics of the definitive mouse placenta assessed by stereology. Biol Reprod 70:1806-1813.
9. Coan PM, Ferguson-Smith AC, Burton GJ. 2005. Ultrastructural changes in the interhaemal membrane and junctional zone of the murine chorioallantoic placenta across gestation. J Anat 207:783-796.
10. Constancia M, Hemberger M, Hughes J, Dean W, Ferguson-Smith A, Fundele R, Stewart F, Kelsey G, Fowden A, Sibley C, Reik W. 2002. Placental-specific IGF-II is a major modulator of placental and fetal growth. Nature 417:945-948.
11. Cross J. 2005. How to make a placenta: mechanisms of trophoblast cell differentiation in mice - a review. Placenta 26: S3-S9.
12. Croy A. 1999. Hasn't the time come to replace the term metrial gland? J Reprod Immunol 42:127-129.
13. Croy BA, Ashkar AA, Minhas K, Greenwood JD. 2000. Can murine uterine natural killer cells give insights into the pathogenesis of preeclampsia? J Soc Gynecol Invest 7:12-20.
14. Dahl E, Winterhager E, Reuß B, Butterweck A, Willecke K. 1996. Expression of the gap junction proteins connexin31 and connexin43 correlates with communication compartments in extraembryonic tissues and in the gastrulating mouse embryo, respectively. J Cell Sci 109:191-197.
15. Davies J, Glasser SR. 1968. Histologica and fine structural observations on the placenta of the rat. Acta Anat 69:542-608.
16. de Lange Davies C, Melder RJ, Munn LL, Mouta-Carreira C, Jain RK, Boucher Y. 2001. Decorin inhibits endothelial migration and tube-like structure formation: role of thrombospondin-1. Microvasc Res 62:26-42.
17. Duchrow M, Schlueter C, Wohlenberg C, Flad HD, Gerdes J. 1996. Molecular characterisation of the gene locus of the human cell proliferation-associated nuclear protein defined by monoclonal antibody Ki-67. Cell Prolif 29:1-12.
18. Frank D, Fortino W, Clark L, Musalo R, Wang W, Saxena A, Li C-M, Reik W, Ludwig T, Tycko B. 2002. Placental overgrowth in mice lacking imprinted gene Ipl. Proc Natl Acad Sci U S A 99:7490-7495.
19. Georgiades P, Watkins M, Burton GJ, Ferguson-Smith A. 2001. Roles for genomic imprinting and the zygote genome in placental development. Proc Natl Acad Sci USA 98:4522-4527.
20. Georgiades P, Ferguson-Smith A, Burton GJ. 2002. Comparative developmental anatomy of the murine and human placenta. Placenta 23:3-19.
21. Gerdes J, Schwab U, Lemke H, Stein H. 1983. Production of a mouse monoclonal antibody reactive with a human nuclear antigen associated with cell proliferation. Int J Cancer 31:13-20.
22. Gerdes J, Li L, Schlueter C, Duchrow M, Wohlenberg C, Gerlach C, Stahmer I, Kloth S, Brandt E, Flad HD. 1991. immunobiochemical and molecular biologic characterisation of the cell proliferation-associated nuclear antigen that is defined by monoclonal antibody Ki-67. Am J Pathol 138:867-873.
23. Guillemot F, Caspary T, Tilghman SM, Copeland NG, Gilbert DJ, Jenkins NA, Anderson DJ, Joyner AL, Rossant J, Nagy A. 1995. Genomic imprinting of Mash2, a mouse gene required for trophoblast development. Nat Genet 3:235-242.
24. Gundersen H. 1988. The nucleator. J Microsc 151:3-21.
25. Gundersen H, Jensen E. 1985. Stereological estimate of volume weighted mean volume of arbitrary particles observed on random sections. J Microsc 138:127-142.
26. Hattori N, Davies TC, Anson-Cartwright L, Cross JC. 2000. Periodic expression of the cyclin-dependent kinase inhibitor p57 (Kip2) in trophoblast giant cells defines a G2-like gap phase of the endocycle. Mol Biol Cell 11:1037-1047.
27. He Y, Smith SK, Day KA, Clark DE, Licence DR, Charnock-Jones DS. 1999. Alternative splicing of vascular endothelial growth factor (VBGF)-R1 (FLT-1) pre-mRNA is important for the regulation of VEGF activity. Mol Endocrinol 13:537-545.
28. Howard CV, Reed M. 1998. Unbiased stereology: three-dimensional measurements in microscopy. New York: Springer-Verlag.
29. Iozzo RV. 1998. Matrix proteoglycans: from molecular design to cellular function. Annu Rev Biochem 67:609-652.
30. Jensen EB, Gundersen HJG. 1989. Fundamental stereological formulae based on isotropically oriented probes through fixed points with applications to particle analysis. J Microsc 153:249-267.
31. Kibschull M, Magin TM, Traub O, Winterhager E. 2005. Cx31 and Cx43 double-deficient mice reveal independent functions in murine placental and skin development. Dev Dyn 233:853-863.
32. Kinsella MG, Fischer JW, Mason DP, Wight TN. 2000. Retrovirally mediated expression of decorin by macrovascular endothelial cells. Effects on cellular migration and fibronectin fibrillogenesis in vitro. J Biol Chem 275:13924-13932.
33. Kirchhausen T. 2002. Single-handed recognition of a sorting traffic motif by the GGA proteins. Nat Struct Biol 9:241-244.
34. Lau MM, Stewart CE, Liu Z, Bhatt H, Rotwein P, Stewart CL. 1994. Loss of the imprinted IGF2/cation-independent mannose 6-phosphate receptor results in fetal overgrowth and perinatal lethality. Genes Dev 8:2953-2963.
35. Lescisin KR, Varmuza S, Rossant J. 1988. Isolation and characterisation of a novel trophoblast-specific cDNA in the mouse. Genes Dev 2:1639-1646.
36. Li Y, Behringer RR. 1998. Esx-1 is an X-chromosome-imprinted regulator of placental development and fetal growth. Nat Genet 20:309-311.
37. Liu J-P, Baker J, Perkins AS, Robertson EJ, Efstratiadis A. 1993. Mice carrying null mutations of the genes encoding insulin-like growth factor (Igf1) and type I IGF receptor (Igf1r). Cell 75:59-72.
38. Lodish H, Baltimore D, Berk A, Zipursky SL, Matsudaira P, Darnell J. 1998. Molecular cell biology. New York: Scientific American Books, Inc.
39. Lopez MF, Dikkes P, Zurakowski D, Villa-Komaroff L. 1996. Insulin-like growth factor II affects the appearance and glycogen content of glycogen cells in the murine placenta. Endocrinology 137:2100-2108.
40. Louvi A, Accili D, Efstratiadis A. 1997. Growth-promoting interaction of IGF-II with the insulin receptor during mouse embryonic development. Dev Biol 189:33-48.
41. Ludwig T, Eggenschwiler J, Fisher P, D'Ercole A, Davenport M, Efstratiadis A. 1996. Mouse mutants lacking the type 2 IGF receptor (IGF2R) are rescued from perinatal lethality in Igf2 and Igf1r null backgrounds. Dev Biol 177:517-535.
42. Lysiak JJ, Hunt J, Pringle GA, Lala PK. 1995. Localization of transforming growth factor β and its natural inhibitor decorin in the human placenta and decidua throughout gestation. Placenta 16:221-231.
43. Ma GT, Solovena V, Tzeng S-J, Lowe LA, Pfendler KC, Iannaccone PM, Kuehn MR, Linzer DIH. 2001. Nodal regulates trophoblast differentiation and placental development. Dev Biol 236:124-135.
44. Malassiné A, Frendo JL, Evain-Brion D. 2003. A comparison of placental development and endocrine functions between the human and mouse model. Hum Reprod Update 9:531-539.
45. Mann CA, Hempstock J, Charnock-Jones DS, Ferguson-Smith AC, Burton GJ. 2003. Oxidative stress and apoptosis in the labyrinth of the normal mouse placenta increase with gestational age. Placenta 24:A.21.
46. CIP1 Cdk inhibitor family, is a candidate tumor suppressor gene. Genes Dev 6:650-662.
47. Mayhew T, Huppertz B, Kaufmann P, Kingdom C. 2003. The 'reference trap' revisited: examples of the dangers in using ratios to describe fetoplacental angiogenesis and trophoblast turnover. Placenta 24:1-7.
48. McKinnon T, Chakraborty C, Gleeson LM, Chidiac P, Lala PK. 2001. Stimulation of human extravillous trophoblast migration by IGF-II is mediated by IGF type 2 receptor involving inhibitory G protein(s) and phosphorylation of MAPK. J Endocrinol Metab 86:3665-3674.
49. Milstone DS, Redline RW, O'Donnell PE, Davis VM, Stavrakis G. 2000. E-selectin expression and function in a unique placental trophoblast population at the fetal-maternal interface: regulation by a trophoblast-restricted transcriptional mechanism conserved between humans and mice. Dev Dyn 219:63-76.
50. Mizuno Y, Sotomaru Y, Katsuzawa Y, Kono T, Meguro M, Oshimura M, Kawai J, Tomaru Y, Kiyosawa H, Nikaido I, Amanuma H, Hayashizaki Y, Okazaki Y. 2002. Asb4, Ata3, and Dcn are novel imprinted genes identified by high-throughput screening using RIKEN cDNA microarray. Biochem Biophys Res Commun 290:1499-1505.
51. Moscatello DK, Santra M, Mann DM, McQuillan DJ, Wong AJ, Iozzo RV. 1998. Decorin suppresses tumor cell growth by activating the epidermal growth factor receptor. J Clin Invest 101:406-412.
52. Xic1, a Cdk inhibitor, promotes the determination of glial cells in Xenopus retina. Cell 99:499-510.
53. Patel S, Santra M, McQuillan DJ, Iozzo RV, Thomas AP. 1998. Decorin activates the epidermal growth factor receptor and elevates cytosolic Ca21 in A431 carcinoma cells. J Biol Chem 273:3121-3124.
54. Pijnenborg R, Robertson WB, Brosens I, Dixon G. 1981. Review article: trophoblast invasion and the establishment of haemochorial placentation in man and laboratory animals. Placenta 2:71-92.
55. Plum A, Winterhager E, Pesch J, Lauterman J, Hallas G, Rosentreter B, Traub O, Herberhold C, Willecke K. 2001. Connexin31-deficiency in mice causes transient placental dysmorphogenesis but does not impair hearing and skin differentiation. Dev Biol 231:334-347.
56. Rampon C, Prandini M-H, Boullot S, Pointu H, Tillet E, Frank R, Vernet M, Huber P. 2005. Protocadherin 12 (VE-cadherin 2) is expressed in endothelial, trophoblast, and mesangial cells. Exp Cell Res 302:48-60.
57. Redline RW, Chernicky CL, Tan H-Q, Ilan J, Ilan J. 1993. Differential expression of insulin-like growth factor-II in specific regions of the late (post 9.5) murine placenta. Mol Reprod Dev 36:121-129.
58. Reuss B, Hellmann P, Dahl E, Traub O, Butterweck A, Grummer R, Winterhager E. 1996. Connexins and E-cadherin are differentially expressed during trophoblast invasion and placenta differentiation in the rat. Dev Dyn 205:172-182.
59. Rodriguez TA, Sparrow DB, Scott AN, Withington SL, Preis JI, Michalicek J, Clements M, Tsang TE, Sioda T, Beddington RSP, Dunwoodie SL. 2004. Cited1 is required in trophoblasts for placental development and for embryo growth and survival. Mol Cell Biol 24:228-244.
60. Rossant J, Cross JC. 2001. Placental development: lessons from mouse mutants. Nat Rev Genet 2:538-548.
61. Roth I, Fisher S. 1999. IL-10 is an autocrine inhibitor of human placental cytotrophoblast MMP-9 production and invasion. Dev Biol 205:194-204.
62. Senior P, Byrne S, Brammar W, Beck F. 1990. Expression of the IGF-II/mannose-6-phosphate receptor mRNA and protein in the developing rat. Development 109:67-73.
63. Soares MJ. 2004. The prolactin and growth hormone families: pregnancy-specific hormones/cytokines at the maternal-fetal interface. Reprod Biol Endocrinol 2:51-66.
64. Soares MJ, Linzer DIH. 2001. Rodent prolactin family and pregnancy. Norwell, MA: Kluwer Academic Publishers.
65. Solberg H, Rinkenberger J, Dano K, Werb Z, Lund LR. 2003. A functional overlap of plasminogen and MMPs regulates vascularization during placental development. Development 130:4439-4450.
66. Stander M, Naumann U, Wick W, Welle M. 1999. Transforming growth factor-β and p-21: multiple molecular targets of decorin-mediated suppression of neoplastic growth. Cell Tissue Res 296:221-227.
67. Stryer L. 1996. Biochemistry. New York: WH Freeman and Co.
68. Kip2 regulates the proper development of labyrinthine and spongiotrophoblasts. Mol Hum Reprod 6:1019-1025.
69. Tanaka M, Gersenstein M, Rossant J, Nagy A. 1997. Mash2 acts cell autonomously in mouse spongiotrophoblast development. Dev Biol 190:55-65.
70. Tanaka S, Oda M, Toyoshima Y, Wakayama T, Tanaka M, Yoshida N, Hattori N, Ohgane J, Yanagimachi R, Shiota K. 2001. Placentamegaly in cloned mouse concepti caused by expansion of the spongiotrophoblast layer. Biol Reprod 65:1813-1821.
71. Teesalu T, Grassi F, Guttinger M. 1998. Expression pattern of the epithelial v-like antigen (Eva) transcript suggests a possible role in placental morphogenesis. Dev Genet 23:317-323.
72. Van den Steen P, Dubois B, Nelissen I, Rudd P, Dwek R, Opdenakker G. 2002. Biochemistry and molecular biology of gelatinase B or matrix metalloproteinase-9 (MMP-9). Crit Rev Biochem Mol Biol 37:375-536.
73. von Figura K, Haslik A. 1986. Lysosomal enzymes and their receptors. Annu Rev Biochem 55:167-193.
74. Waddell BJ, Hisheh S, Dharmarajam AM, Burton PJ. 2000. Apoptosis in rat placenta is zone-dependent and stimulated by glucocorticoids. Biol Reprod 63:1913-1917.
75. Westbury J, Watkins M, Ferguson-Smith AC, Smith J. 2001. Dynamic temporal and spatial regulation of the cdk inhibitor p57(kip2) during embryo morphogenesis. Mech Dev 109:83-89.
76. Xu G, Guimond M-J, Charkraborty C, Lala PK. 2002. Control of proliferation, migration and invasiveness of human extravillous trophoblast by decorin, a decidual product. Biol Reprod 67:681-689.
77. Yamaguchi Y, Mann DM, Ruoslahti E. 1990. Negative regulation of transforming growth factor-β by the proteoglycan decorin. Nature 346:281-284.
78. Kip2 results in increased apoptosis an delayed differentiation during mouse development. Genes Dev 11:973-983.
79. Yang Z-Z, Tschopp O, Hemmings-Mieszczak M, Feng J, Brodbeck D, Perentes E, Hemmings BA. 2003. Protein kinase Ba/Akt1 regulates placental development and fetal growth. J Biol Chem 278:32124-32131.
80. Kip2 regulates actin dynamics by binding and translocating LIM-kinase 1 to the nucleus. J Biol Chem 278:52919-52923.
81. KIP2 indicates a role in Beckwith-Wiedemann syndrome. Nature 387:151-158.