Abstract
This is a study on the ability of mouse embryos to compensate for a loss of cells and to develop with body parts of normal size and normal proportions during postimplantation development. Micro-manipulations were performed on 4-cell pre-implantation mouse embryos to reduce the number of cells by 25% (3/4 embryos) or 50% (2/4 embryos). Blastocysts developed from these embryos showed a preferential loss of inner cell mass population, and fewer of them formed viable embryos after implantation. The size of post-implantation 3/4 embryos was initially smaller than controls of the same gestational age, but compensatory growth, achieved by increasing cell numbers at above the normal rate and beyond the normal duration, took place between 6.5 and 11.5 days, resulting in a complete restoration of body size. During compensatory growth the 3/4 embryos rescheduled events of gastrulation and morphogenesis in keeping with cell number or body size appropriate for each developmental stage. The formation of the correct number of somites was accomplished by changing the rate of somite segmentation and by an adjustment of the size of individual somites and somitomeres proportional to the available amount of precursor tissues. Morphogenesis and pattern formation in embryos recovering from earlier cell losses are therefore regulated in accordance to tissue volume (or cell number) instead of chronological age or some intrinsic cellular clock.
Similar content being viewed by others
References
Abercrombie M (1946) Estimation of nuclear population from microtome sections. Anat Rec 94:239–247
Adamson ED (1987) Oncogenes in development. Development 99:449–472
Beddington RSP (1987) Isolation, culture and manipulation of post-implantation mouse embryos. In: Monk M (ed) Mammalian development. A practical approach. IRL Press, Oxford, pp 43–70
Brown NA, Fabro S (1981) Quantitation of rat embryonic development in vitro: a morphological scoring system. Teratology 24:65–78
Buehr M, McLaren A (1974) Size regulation in chimaeric mouse embryos. J Embryol Exp Morphol 31:229–234
Burgoyne PS, Tam PPL, Evans EP (1983) Retarded development of XO conceptuses during early pregnancy in the mouse. J Reprod Fertil 68:387–393
Cooke J (1988) A note on segmentation and the scale of pattern formation in insects and in vertebrates. Development 104 [Suppl]:245–248
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
Crossley PH, Little PFR (1991) A cluster of related zinc finger protein genes is deleted in the mouse embryonic lethal mutation tw18. Proc Natl Acad Sci USA 88:7923–7927
Henery CC, Bard JBL, Kaufman MH (1992) Tetraploidy in mice, embryonic cell number, and the grain of the developmental map. Dev Biol 152:233–241
Hills DJ, Strain AJ, Milner RDG (1987) Growth factors in embryogenesis. Oxford review of reproductive biology 9:399–455
Jacobson AG, Tam PPL (1982) Cephalic neurulation in the mouse embryo analyzed by SEM and morphometry. Anat Rec 203:375–396
Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. J Cell Biol 27:137A
Kaufman MH (1992) The atlas of mouse development. Academic Press, London
Kelley RO, Dekker RAF, Bluemink JG (1973) Ligand-mediated osmium binding: its application in coating biological specimens for scanning electron microscopy. J Ultrastruct Res 45:254–258
Lewis NE, Rossant J (1982) Mechanism of size regulation in mouse embryo aggregates. J Embryol Exp Morphol 72:169–181
Mercola M, Stiles CD (1988) Growth factor superfamilies and mammalian embryogenesis. Development 102:451–460
Poelmann RE (1980) Differential mitosis and degeneration patterns in relation to the alterations in the shape of the embryonic ectoderm of early post-implantation mouse embryos. J Embryol Exp Morphol 55:33–51
Rands GF (1986a) Size regulation in the mouse embryo I. The development of quadruple aggregates. J Embryol Exp Morphol 94:139–148
Rands GF (1986b) Size regulation in the mouse embryo II. The development of half embryos. J Embryol Exp Morphol 98:209–217
Rugh R (1968) The mouse. Its reproduction and development. Burgess, Minneapolis
Snow MHL (1977) Gastrulation in the mouse: growth and regionalization of the epiblast. J Embryol Exp Morphol 42:293–303
Snow MHL (1983) Restorative growth in mammalian embryos. In: Kalter H (ed) Issues and reviews in teratology. Vol I Plenum Press, New York, pp 251–284
Snow MHL (1986) Uncoordinated development of embryonic tissue following cytotoxic damage. In: Welsch F (ed) Approaches to elucidate a mechanism in teratogenesis. Hemisphere, Washington DC, pp 83–98
Snow MHL, Bennett D (1978) Gastrulation in the mouse: assessment of cell populations in the epiblast of tw18/tw18 embryos. J Embryol Exp Morphol 47:39–52
Snow MHL, Tam PPL (1979) Is compensatory growth a complicating factor in mouse teratology? Nature 279:555–557
Snow MHL, Tam PPL, McLaren A (1981) On the control and regulation of size and morphogenesis in mammalian embryos. In: Subtelny S, Abbott UK (eds) Levels of genetic control in development. Liss, New York, pp 201–217
Sturm K, Tam PPL (1993) Isolation and culture of whole postimplantation embryos and their germ layer derivatives. In: Wasserman P, DePamphilis M (eds) Methods in enzymology. A guide to techniques in mouse development. Academic Press (in press)
Tam PPL (1981) The control of somitogenesis in mouse embryos. J Embryol Exp Morphol 65 [Suppl]:103–128
Tam PPL (1986) A study on the pattern of prospective somites in the presomitic mesoderm of mouse embryos. J Embryol Exp Morphol 92:269–285
Tam PPL (1988) Post-implantation development of mitomycin-C treated mouse blastocysts. Teratology 37:205–212
Tam PPL (1990) Studying development in embryo fragments. In: Copp AJ, Cockroft DL (eds) Postimplantation mammalian development. IRL Press, Oxford, pp 317–338
Tam PPL, Meier S (1982) The establishment of a somitomeric pattern in the mesoderm of the gastrulating mouse embryo. Am J Anat 164:209–225
Tam PPL, Snow MHL (1981) Proliferation and migration of primordial germ cells during compensatory growth in mouse embryos. J Embryol Exp Morphol 64:133–147
Tam PPL, Meier S, Jacobson AG (1982) Differentiation of the metameric pattern in the embryonic axis of the mouse II. Somitomeric organization of the presomitic mesoderm. Differentiation 21:109–122
Tarkowski AK (1959) Experimental studies on regulation in the development of isolated blastomeres of mouse eggs. Acta Theriol 11:191–267
Theiler K (1972) The house mouse. Development and normal stages from fertilization to 4 weeks of age. Springer, Berlin Heidelberg New York
Tsunoda Y, McLaren A (1983) Effect of various procedures on the viability of mouse embryos containing half the normal number of blastomeres. J Reprod Fertil 69:315–322
Whittingham DG (1971) Culture of mouse ova. J Reprod Fertil 14 [Suppl]:7–21
Whittingham DG, Wales RG (1969) Storage of 2-cell mouse embryos in vitro. Aust J Biol Sci 22:1065–1068
Williams JPG (1981) Catch-up growth. J Embryol Exp Morphol 65 [Suppl]:89–101
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Power, M.A., Tam, P.P.L. Onset of gastrulation, morphogenesis and somitogenesis in mouse embryos displaying compensatory growth. Anat Embryol 187, 493–504 (1993). https://doi.org/10.1007/BF00174425
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00174425