Abstract
Mouse chimaeras were produced by aggregating eight-cell embryos from two different F2 matings, abbreviated to AF2 and BF2 respectively: (C57BL/ OIa.AKR-Gpi-1s a, c/Ws female × BALB/c male)F2 and (C57BL/Ws female × CBA/Ca male)F2. Quantitative electrophoresis of glucose phosphate isomerase (GPI-1) was used to estimate the proportions of the two cell populations in different tissues of the 12\({\raise0.7ex\hbox{$1$} \!\mathord{\left/ {\vphantom {1 2}}\right.\kern-\nulldelimiterspace}\!\lower0.7ex\hbox{$2$}}\) day chimàeric conceptuses, with the % GPI-1A indicating the percentage of cells derived from the AF2 embryos. The % GPI-1A was found to be highly positively correlated within the primitive ectoderm lineage (between the fetus, amnion and yolk sac mesoderm) and within the primitive endoderm lineage (between the yolk sac endoderm and the parietal endoderm) but no correlation (either positive or negative) was seen between the two lineages. This confirms the results of a previous,study of chimaeras made between partially congenic strains and suggests the original conclusions have general validity. The % GPI-1A in the placenta was corrected for the expected contribution of maternal GPI-1, based on control experiments involving transfer of homozygous Gpi-1s b/Gpi-1s b embryos to the uteri of Gpi-1s a/Gpi-1s a pseudopregnant females. The corrected % GPI- lA in the placenta was positively correlated with that in each of the three primitive ectoderm derivatives. This suggests either (1) exchange of cells between the polar trophectoderm and the underlying part of the inner cell mass that forms the primitive ectoderm or (2) cells are incompletely mixed in the chimaeric blastocyst and patches of AF2 and BF2 cells straddle the boundary between the polar trophectoderm and the underlying primitive ectoderm. The second explanation does not imply the existence of shared developmental lineages between trophectoderm and primitive ectoderm in non-chimaeric embryos. Unlike that of any other tissue, the distribution of placental GPI-1A was U-shaped; in 17/28 placenta samples the proportion of the minor component was 10% or less. This suggests that the placental trophoblast is derived from a small number of coherenct clones of polar trophectoderm cells (either a small number of polar trophectoderm cells or a larger number if the two cell populations are not finely intermingled). Thus, although as a population the placentas of chimaeric conceptuses are balanced with respect to the % GPI-1A (mean close to 50%), individually most placentas are extremely unbalanced in their chimaeric composition (< 10% or > 90% GPI-IA). This non-random composition of the chimaeric placentas is in contrast to the widely held assumption that the distribution of cells in chimaeric conceptuses is normally random.
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References
Barsh GS, Lovett M, Epstein CJ (1990) Effects of the lethal yellow (Ay) mutation in mouse aggregation chimeras. Development 109:683–690
Bennett D (1978) Rescue of a lethal T/t locus genotype by chimaerism with normal embryos. Nature 272:539
Copp AJ (1978) Interaction between inner cell mass and trophectoderm of the mouse blastocyst. I. A study of cellular proliferation. J Embryol Exp Morphol 48:109–125
Copp AJ (1979) Interaction between inner cell mass and trophectoderm of the mouse blastocyst. II. The fate of the polar trophectoderm. J Embryol Exp Morphol 51:109–120
Cox DR, Smith SA, Epstein LB, Epstein CJ (1984) Mouse trisomy 16 as an animal model of human trisomy 21 (Down Syndrome) production of viable trisomy 16↔diploid mouse embryos. Dev Biol 101:416–424
Cruz YP, Pedersen RA (1985) Cell fate in the polar trophectoderm of mouse blastocysts as studied by microinjection of cell lineage tracers. Dev Biol 112:73–83
Epstein CJ, Smith SA, Cox DR (1984) Production and properties of mouse trisomy 15↔diploid chimeras. Dev Genet 4:159–165
Epstein CJ, Smith SA, Zamora T, Sawicki JA, Magnuson TR, Cox DR (1982) Production of viable adult trisomy 17↔diploid mouse chimeras. Proc Nat Acad Sci USA 79:4376–4380
Falconer DS, Avery PJ (1978) Variability of chimaeras and mosaics. J Embryol Exp Morphol 43:195–219
Fundle R, Howlett SK, Kothary R, Norris ML, Mills WE, Surani MA (1991) Developmental potential of parthenogenetic cells: role of genotype-specific modifiers. Development 108:941–946
Fundele R, Jägerbauer E-M, Kolbus U, Winking H, Gropp A (1985) Viability of trisomy 12 cells in mouse chimaeras. Roux's Arch Dev Biol 194:178–180
Fundele R, Norris ML, Barton SC, Fehlau M, Howlett SK, Mills WE, Surani MA (1990) Temporal and spatial selection against parthenogenetic cells during development of fetal chimeras. Development 108:203–211
Fundele R, Norris ML, Barton SC, Reik W, Surani MA (1989) Systematic elimination of parthenogenetic cells in mouse chimeras. Development 106:29–35
Gardner RL (1978) The relationship between cell lineage and differentiation in the early mouse embryo. In: Gehring WJ (ed) Results and problem in cell differentiation. Springer, Berlin Heidelberg, pp 205–241
Gardner RL, Papaioannou VE (1975) Differentiation in the trophectoderm and inner cell mass. In: Balls M, Wild AE (eds) The early development of mammals. Cambridge University Press, Cambridge, pp 107–132
Garner W, McLaren A (1974) Cell distribution in chimaeric mouse embryos before implantation. J Embryol Exp Morphol 32:495–503
Handyside AH (1978) Time of commitment of inside cells isolated from preimplantation mouse embryos. J Embryol Exp Morphol 45:37–53
Johnson MH, Maro B (1986) Time and space in the mouse early embryo: a cell biological approach to cell diversification. In: Rossant J, Pedersen RA (eds) Experimental approaches to mammalian embryonic development. Cambridge University Press, Cambridge, pp 35–65
Keighren M, West JD (1993) Analysis of cell ploidy in histological sections of mouse tissues by DNA-DNA in situ hybridisation with digoxigenin labelled probes. Histochem J 25:30–44
Kelly SJ (1979) Investigation into the degree of cell mixing that occurs between the 8-cell stage and the blastocyst stage of mouse development. J Exp Zool 207:121–130
Leask-Svajger B, Svajger A, Skreb N (1969) Separation of germ layers in presomite rat embryos. Experientia 25:1311–1312
McLaren A (1976) Mammalian chimaeras, Cambridge University Press, Cambridge
McLaren A, Buehr M (1990) Development of mouse germ cells in cultures of fetal gonads. Cell Differ Dev 31:185–195
McLaren A, Michic D (1956) Studies on the transfer of fertilized mouse eggs to uterine foster mothers. I. Factors affecting the implantation and survival of native and transferred eggs. J Exp Biol 33:394–416
Mintz B (1962) Formation of genotypically mosaic mouse embryos. Am Zool 2:432 [Abstr. 310]
Mintz B (1964) Formation of genetically mosaic mouse embryos, and early development of “lethal (t 12/t 12)-normal- mosaics. J Exp Zool 157:273–292
Mintz B, Gearhart JD, Guymont AG (1973) Phytohemagglutinin-mediated blastomere aggregation and development of allophenic mice. Dev Biol 31:195–199
Mullen RJ, Whitten WK (1971) Relationship of genotype and degree of chimerism in coat color to sex ratios and gametogenesis in chimeric mice. J Exp Zool 178:165–176
Nagy A, Páldi A, Dezso L, Varga L, Magyar A (1987) Prenatal fate of parthenogenetic cells in mouse aggregation chimaeras. Development 101:67–71
Nagy A, Sass M; Markkula M (1989) Systematic non-uniform distribution of parthenogenetic cells in adult mouse chimaeras. Development 106:321–324
Nicolson GL, Yanagamachi R, Yanagamachi H (1975) Ultrastructural localization of lectin binding sites of the zonae pellucidae and plasma membranes of mammalian eggs. J Cell Biol 66:263–274
Palmer SJ, Burgoyne PS (1991) The Mus musculus domesticus Tdy allele acts later than the Mus musculus musculus Tdy allele: a basis for XY sex-reversal in C57BL/6-YPOS mice. Development 113:709–714
Papaioannou VE, West JD (1981) Relationship between the parental origin of the X-chromosomes, embryonic cell lineage and X-chromosome expression in mice. Genet Res Camb 37:183–197
Pickering SJ, Maro B, Johnson MIL, Skepper JN (1988) The influence of cell contact on the division of mouse 8-cell blastomeres. Development 103:353–363
Pratt HPM (1987) Isolation, culture and manipulation of pre-implantation mouse embryos. In: Monk M (ed) Mammalian development: a practical approach. IRL Press, Oxford, pp 29–42
Quinn P, Barros C, Whittingham DG (1982) Preservation of hamster oocytes to assay the fertilizing capacity of human spermatozoa. J Repr Fert 66:161–168
Rossant J, Croy BA (1985) Genetic identification of the tissue of origin of cellular populations within the mouse placenta. J Embryol Exp Morphol 86:177–189
Spindle A (1982) Cell allocation in preimplantation mouse chimaeras. J Exp Zool 219:361–367
Surani MA, Barton SC, Howlett SK, Norris ML (1988) Influence of chromosomal determinants on development of androgenetic and parthenogenetic cells. Development 103:171–178
Surani MAH, Barton SC, Norris ML (1987) Influence of parental chromosomes on spatial specificity in adrogenetic↔parthenogenetic chimaeras in the mouse. Nature 326:395–397
Tarkowski AK (1961) Mouse chimaeras developed from fused eggs. Nature 190:857–860
Thomson JA, Seller D (1988) The developmental fate of androgenetic, parthenogenetic and gynogenetic cells in chimeric gastrulating mouse embryos. Gen Dev 2:1344–1351
Thomson JA, Solter D (1989) Chimeras between parthenogenetic or androgenetic blastomeres and normal embryos: allocation to the inner cell mass and trophectoderm. Dev Biol 131:580–583
West JD (1978) Analysis of clonal growth using chimaeras and mosaics. In: Johnson MH (ed) Development in mammals, vol 3. Elsevier/North Holland, Amsterdam New York Oxford, pp 413–460
West JD, Bücher Th, Linke IM, Dünnwald M (1984) Investigation of variability among mouse aggregation chimaeras and X-chromosome inactivation mosaics. J Embryol Exp Morphol 84:309–329
West JD, Green JF (1983) The transition from oocyte-coded to embryo-coded glucose phosphate isomerase in the early mouse embryo. J Embryol Exp Morphol 78:127–140
West JD, Leask R, Green JF (1986) Quantification of the transition from oocyte-coded to embryo-coded glucose phosphate isomerase in mouse embryos. J Embryol Exp Morphol 97:225–237
Whittingham DG (1971) Culture of mouse ova. J Reprod Fertil [Suppl] 14:7–21
Ziomek CA, Johnson MH (1982) The roles of phenotype and position in guiding the fate of 16-cell mouse blastomeres. Dev Biol 91:440–447
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James, R., Flockhart, J.H., Keighren, M. et al. Quantitative analysis of mid-gestation mouse aggregation chimaeras: non-random composition of the placenta. Roux's Arch Dev Biol 202, 296–305 (1993). https://doi.org/10.1007/BF00363218
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DOI: https://doi.org/10.1007/BF00363218