Abstract
During the past decade we have witnessed great progress in the understanding of cellular, molecular, and epigenetic aspects of preimplantation mouse development. However, some of the issues, especially those regarding the nature and regulation of mouse development, are still unresolved and controversial and raise heated discussion among mammalian embryologists. This chapter presents different standpoints and various research approaches aimed at examining the fate and potency of cells (blastomeres) of mouse preimplantation embryo. In dealing with this subject, it is important to recognize the difference between the fate of blastomere and the prospective potency of blastomere, with the first being its contribution to distinct tissues during normal development, and the second being a full range of its developmental capabilities, which can be unveiled only by experimental perturbation of the embryo. Studies of the developmental potential and the fate of blastomeres are of the utmost importance as they may lead to future clinical application in reproductive and regenerative medicine.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
AlarcĂłn VB, Marikawa Y (2003) Deviation of the blastocyst axis from the first cleavage plane does not affect the quality of mouse postimplantation development. Biol Reprod 69:1208â1212
AlarcĂłn VB, Marikawa Y (2005) Unbiased contribution of the first two blastomeres to mouse blastocyst development. Mol Reprod Dev 72:354â361
AlarcĂłn VB, Marikawa Y (2008) Spatial alignment of the mouse blastocyst axis across the first cleavage plane is caused by mechanical constraint rather than developmental bias among blastomeres. Mol Reprod Dev 75:1143â1153
Chazaud C, Yamanaka Y, Pawson T, Rossant J (2006) Early lineage segregation between epiblast and primitive endoderm in mouse blastocysts through the Grb2-MAPK pathway. Dev Cell 10:615â624
Chroscicka A, Komorowski S, Maleszewski M (2004) Both blastomeres of the mouse 2-cell embryo contribute to the embryonic portion of the blastocyst. Mol Reprod Dev 68:308â312
Chung Y, Klimanskaya I, Becker S, Marh J, Lu SJ, Johnson J, Meisner L, Lanza R (2005) Embryonic and extraembryonic stem cell lines derived from single mouse blastomeres. Nature 439:216â219
Davies TJ, Gardner RL (2002) The plane of first cleavage is not related to the distribution of sperm components in the mouse. Hum Reprod 17:2368â2379
Dietrich JE, Hiiragi T (2007) Stochastic patterning in the mouse pre-implantation embryo. Development 134:4219â4231
Dziadek M (1979) Cell differentiation in isolated inner cell masses of mouse blastocysts in vitro: onset of specific gene expression. J Embryol Exp Morphol 53:367â379
Fleming TP, Warren PD, Chisholm JC, Johnson MH (1984) Trophectodermal processes regulate the expression of totipotency within the inner cell mass of the mouse expanding blastocyst. J Embryol Exp Morphol 84:63â90
Fujimori T, Kurotaki Y, Miyazaki J, Nabeshima Y (2003) Analysis of cell lineage in two- and four-cell mouse embryos. Development 130:5113â5122
Gardner RL (1985) Regeneration of endoderm from primitive ectoderm in the mouse embryo: fact or artifact. J Embryol Exp Morphol 88:303â326
Gardner RL (1997) The early blastocyst is bilaterally symmetrical and its axis of symmetry is aligned with the animal-vegetal axis of the zygote in the mouse. Development 124:289â301
Gardner RL (2001) Specification of embryonic axes begins before cleavage in normal mouse development. Development 128:839â847
Gardner RL, Davies TJ (2003) Is the plane of first cleavage related to the point of sperm entry in the mouse? Reprod Biomed Online 6:157â160
Gardner RL, Johnson MH (1972) An investigation of inner cell mass and trophoblast tissues following their isolation from the mouse blastocyst. J Embryol Exp Morphol 28:279â312
Gardner R, Rossant J (1979) Investigation of the fate of 4,5 day post-coitum mouse inner cell mass by blastocyst injection. J Embryol Exp Morphol 52:141â152
Geens M, Mateizel I, Sermon K, De Rycke M, Spits C, Cauffman G, Devroey P, Tournaye H, Liebaers I, Van de Velde H (2009) Human embryonic stem cell lines derived from single blastomeres of two 4-cell stage embryos. Hum Reprod 24:2709â2717
GonzĂĄlez S, Ibåñez E, SantalĂł J (2011) Influence of early fate decisions at the two-cell stage on the derivation of mouse embryonic stem cell lines. Stem Cell Res 7:54â65
Gray D, Plusa B, Piotrowska K, Na J, Tom B, Glover DM, Zernicka-Goetz M (2004) First cleavage of the mouse embryo responds to change in egg shape at fertilization. Curr Biol 14:397â405
Guo G, Huss M, Tong GQ, Wang C, Sun LL, Clarke ND, Robson P (2010) Resolution of cell fate decisions revealed by single-cell gene expression analysis from zygote to blastocyst. Dev Cell 18:675â685
Handyside AH (1978) Time of commitment of inside cells isolated from preimplantation mouse embryos. J Embryol Exp Morphol 45:37â53
Handyside AH, Barton SC (1977) Evaluation of the technique of immunosurgery for the isolation of inner cell masses from mouse blastocysts. J Embryol Exp Morphol 37:217â226
Hansis C, Grifo JA, Tang Y, Krey LC (2002) Assessment of beta-HCG, beta-LH mRNA and ploidy in individual human blastomeres. Reprod Biomed Online 5:156â161
Hansis C, Grifo JA, Krey LC (2004) Candidate lineage marker genes in human preimplantation embryos. Reprod Biomed Online 8:577â583
Hardy K, Martin KL, Leese HJ, Winston RM, Handyside AH (1990) Human preimplantation development in vitro is not adversely affected by biopsy at the 8-cell stage. Hum Reprod 5:708â714
Hiiragi T, Solter D (2004) First cleavage plane of the mouse egg is not predetermined but defined by the topology of the two apposing pronuclei. Nature 430:360â364
Hiiragi T, Alarcon VB, Fujimori T, Louvet-Vallee S, Maleszewski M, Marikawa Y, Maro B, Solter D (2006) Where do we stand now? Mouse early embryo patterning meeting in Freiburg, Germany. Int J Dev Biol 50:581â586
Hogan B, Tilly R (1978a) In vitro development of inner cell masses isolated immunosurgically from mouse blastocysts. II. Inner cell masses from 3,5- to 4,0-day p.c. blastocysts. J Embryol Exp Morphol 45:107â21
Hogan B, Tilly R (1978b) In vitro development of inner cell masses isolated immunosurgically from mouse blastocysts. I. Inner cell masses from 3,5-day p.c. blastocysts incubated for 24h before immunosurgery. J Embryol Exp Morphol 45:93â105
Handyside AH, Kontogianni EH, Hardy K, Winston RM (1990) Pregnancies from biopsied human preimplantation embryos sexed by Y-specific DNA amplification. Nature 344:768â770
James RM, Klerkx AHEM, Keighren M, Flockhart JH, West JD (1995) Restricted distribution of tetraploid cells in mouse tetraploidâ<==>âdiploid chimaeras. Dev Biol 167:213â226
Jedrusik A, Parfitt DE, Guo G, Skamagki M, Grabarek JB, Johnson MH, Robson P, Zernicka-Goetz M (2008) Role of Cdx2 and cell polarity in cell allocation and specification of trophectoderm and inner cell mass in the mouse embryo. Genes Dev 22:2692â2706
Johnson MH, Ziomek CA (1981) The foundation of two distinct cell lineages within the mouse morula. Cell 24:71â80
Johnson WH, Loskutoff NM, Plante Y, Betteridge KJ (1995) Production of four identical calves by the separation of blastomeres from an in vitro derived four-cell embryo. Vet Rec 137:15â16
Kelly SJ (1975) Studies of the potency of the early cleavage blastomeres of the mouse. In: Balls M, Wild AE (eds) The early development of mammals. Cambridge University Press, Cambridge, pp 97â105
Kelly SJ (1977) Studies of the developmental potential of 4- and 8-cell stage mouse blastomeres. J Exp Zool 200:365â376
Klimanskaya I, Chung Y, Becker S, Lu SJ, Lanza R (2007) Derivation of human embryonic stem cells from single blastomeres. Nat Protoc 2:1963â1972
Kubiak JZ, Tarkowski AK (1985) Electrofusion of mouse blastomeres. Exp Cell Res 157:561â566
Kurimoto K, Kabuta Y, Ohinata Y, Ono Y, Uno KD, Hamada RG, Ueda HR, Saitou M (2006) An improved single-cell cDNA amplification method for efficient high-density oligonucleotide microarray analysis. Nucleic Acids Res 34:e42
Kurotaki Y, Hatta K, Nakao K, Nabeshima Y, Fujimori T (2007) Blastocyst axis is specified independently of early cell lineage but aligns with the ZP shape. Science 316:719â723
Louvet-Vallee S, Dard N, Santa-Maria A, Aghion J, Maro B (2001) A major posttranslational modification of ezrin takes place during epithelial differentiation in the early mouse embryo. Dev Biol 231:190â200
Louvet-VallĂ©e S, Vinot S, Maro B (2005) Mitotic spindles and cleavage planes are oriented randomly in the two-cell mouse embryo. Curr Biol 15:464â469
Markert CL, Petters RM (1978) Manufactured hexaparental mice show that adults are derived from three embryonic cells. Science 202:56â58
MacKay GE, West JD (2005) Fate of tetraploid cells in 4nâ2n chimeric mouse blastocysts. Mech Dev 122:1266â1281
McGrath J, Solter D (1984) Completion of mouse embryogenesis requires both the maternal and paternal genomes. Cell 37:179â183
McLaren A (1976) Mammalian chimaeras. Cambridge University Press, Cambridge, London, New York, Melbourne
Mintz B (1962) Formation of genotypically mosaic mouse embryos. Am Zool 2:432
Mintz B (1964) Formation of genetically mosaic mouse embryos and early development of âlethal (t 12/t 12)-normalâ mosaics. J Exp Zool 157:273â292
Meilhac SM, Adams RJ, Morris SA, Danckaert A, Le-Garrec JF, Zernicka-Goetz M (2009) Active cell movements coupled to positional induction are involved in lineage segregation in the mouse. Dev Biol 331:210â221
Moore NW, Adams CE, Rowson LEA (1968) Developmental potential of single blastomeres of the rabbit egg. J Reprod Fertil 17:527â531
Morris SA, Teo RT, Li H, Robson P, Glover DM, Zernicka-Goetz M (2010) Origin and formation of the first two distinct cell types of the inner cell mass in the mouse embryo. Proc Natl Acad Sci USA 107:6364â6369
Motosugi N, Bauer T, Polanski Z, Solter D, Hiiragi T (2005) Polarity of the mouse embryo is established at blastocyst and is not prepatterned. Genes Dev 19:1081â1092
Mullen RJ, Whitten WK, Carter SC (1970) Studies on chimeric mice and half-embryos. In: Annual report of the Jackson Laboratory. Bar harbor, Maine, pp 67â68
Nichols J, Gardner RL (1984) Heterogeneous differentiation of external cells in individual isolated early mouse inner cell masses in culture. J Embryol Exp Morphol 80:225â240
OzdzeĆski W, Szczesny E, Tarkowski AK (1997) Postimplantation development of mouse blastocysts with two separate inner cell masses. Anat Embryol (Berl) 195:467â471
Pedersen RA, Spindle AI, Wiley LM (1977) Regeneration of endoderm by ectoderm isolated from mouse blastocysts. Nature 270:453â457
Pierce GB, Arechaga J, Muro C, Wells RS (1988) Differentiation of ICM cells into trophectoderm. Am J Pathol 132:356â364
Pinyopummin A, Takahashi Y, Hishinuma M, Kanagawa H (1994) Development of single blastomeres from 4-cell stage embryos after aggregation with parthenogenones in mice. Jpn J Vet Res 42:119â126
Piotrowska K, Zernicka-Goetz M (2001) Role for sperm in spatial patterning of the early mouse embryo. Nature 409:517â521
Piotrowska K, Wianny F, Pedersen RA, Zernicka-Goetz M (2001) Blastomeres arising from the first cleavage division have distinguishable fates in normal mouse development. Development 128:3739â3748
Piotrowska-Nitsche K, Perea-Gomez A, Haraguchi S, Zernicka-Goetz M (2005) Four-cell stage mouse blastomeres have different developmental properties. Development 132:479â490
Plachta N, Bollenbach T, Pease S, Fraser SE, Pantazis P (2011) Oct4 kinetics predict cell lineage patterning in the early mammalian embryo. Nat Cell Biol 13:117â123
Plusa B, Grabarek JB, Piotrowska K, Glover DM, Zernicka-Goetz M (2002a) Site of the previous meiotic division defines cleavage orientation in the mouse embryo. Nat Cell Biol 4:811â815
Plusa B, Piotrowska K, Zernicka-Goetz M (2002b) Sperm entry position provides a surface marker for the first cleavage plane of the mouse zygote. Genesis 32:193â198
Plusa B, Hadjantonakis AK, Gray D, Piotrowska-Nitsche K, Jedrusik A, Papaioannou VE, Glover DM, Zernicka-Goetz M (2005) The first cleavage of the mouse zygote predicts the blastocyst axis. Nature 434:391â395
Plusa B, Piliszek A, Frankenberg S, Artus J, Hadjantonakis AK (2008) Distinct sequential cell behaviours direct primitive endoderm formation in the mouse blastocyst. Development 135:3081â3091
Ralston A, Rossant J (2008) Cdx2 acts downstream of cell polarization to cell-autonomously promote trophectoderm fate in the early mouse embryo. Dev Biol 313:614â629
Randle BJ (1982) Cosegregation of monoclonal antibody reactivity and cell behaviour in the mouse preimplantation embryo. J Embryol Exp Morphol 70:261â278
Rossant J (1975a) Investigation of the determinative state of the mouse inner cell mass. II. The fate of isolated inner cell masses transferred to the oviduct. J Embryol Exp Morphol 33:991â1001
Rossant J (1975b) Investigation of the determinative state of the mouse inner cell mass. I. Aggregation of isolated inner cell masses with morulae. J Embryol Exp Morphol 33:979â990
Rossant J (1976) Postimplantation development of blastomeres isolated from 4- and 8-cell mouse eggs. J Embryol Exp Morphol 36:283â290
Rossant J, Lis WT (1979) Potential of isolated mouse inner cell masses to form trophectoderm derivatives in vivo. Dev Biol 70:255â261
Rossant J, Vijh KM (1980) Ability of outside cells from preimplantation mouse embryos to form inner cell mass derivatives. Dev Biol 76:475â482
Seidel F (1952) Die entwicklugspotenzen einen isolierten blastomere des zweizellen-stadiums im saugetierei. Naturwissenschaften 39:355â356
Seidel F (1960) Die entwicklungsfahigkeiten isolierter furchungszellen aus dem ei des kaninchens Oryctolagus cuniculus. Roux Arch Entw Mech 152:43â130
Solter D, Knowles BB (1975) Immunosurgery of mouse blastocyst. Proc Natl Acad Sci USA 72:5099â5102
Spindle AI (1978) Trophoblast regeneration by inner cell masses isolated from cultured mouse embryos. J Exp Zool 203:483â489
Staessen C, Platteau P, Van Assche E, Michiels A, Tournaye H, Camus M, Devroey P, Liebaers I, Van Steirteghem A (2004) Comparison of blastocyst transfer with or without preimplantation genetic diagnosis for aneuploidy screening in couples with advanced maternal age: a prospective randomized controlled trial. Hum Reprod 19:2849â2858
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 132:2093â2102
Surani MAH, Handyside AH (1983) Reassortment of cells according to position in mouse morulae. J Exp Zool 225:505â511
Surani MA, Barton SC, Norris ML (1984) Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis. Nature 308:548â550
Suwinska A, Czolowska R, Ozdzenski W, Tarkowski AK (2008) Blastomeres of the mouse embryo lose totipotency after the fifth cleavage division: expression of Cdx2 and Oct4 and developmental potential of inner and outer blastomeres of 16- and 32-cell embryos. Dev Biol 322:133â44
Szczepanska K, Stanczuk L, Maleszewski M (2011) Isolated mouse inner cell mass is unable to reconstruct trophectoderm. Differentiation 82:1â8
Tarkowski AK (1959a) Experiments on the development of isolated blastomeres of mouse eggs. Nature 184:1286â1287
Tarkowski AK (1959b) Experimental studies on regulation in the development of isolated blastomeres of mouse eggs. Acta Theriol 3:191â267
Tarkowski AK (1961) Mouse chimaeras developed from fused eggs. Nature 190:857â860
Tarkowski AK (1998) Mouse chimaeras revisited: recollections and reflections. Int J Dev Biol 42:903â908
Tarkowski AK (1963) Studies on mouse chimeras developed from eggs fused in vitro. Natl Cancer Inst Monogr 11:51â71
Tarkowski AK, Witkowska A, Nowicka J (1970) Experimental partheonogenesis in the mouse. Nature 226:162â165
Tarkowski AK, Wojewodzka M (1982) A method for obtaining chimaeric mouse blastocysts with two separate inner cell masses: a preliminary report. J Embryol Exp Morphol 71:215â221
Tarkowski AK, Wroblewska J (1967) Development of blastomeres of mouse eggs isolated at the 4- and 8-cell stage. J Embryol Exp Morphol 18:155â180
Tarkowski AK, Witkowska A, Opas J (1977) Development of cytochalasin B-induced tetraploid and diploid/tetraploid mosaic mouse embryos. J Embryol Exp Morphol 41:47â64
Tarkowski AK, Ozdzenski W, CzoĆowska R (2001a) Mouse singletons and twins developed from isolated diploid blastomeres supported with tetraploid blastomeres. Int J Dev Biol 45:591â596
Tarkowski AK, Ozdzenski W, CzoĆowska R (2001b) How many blastomeres of the 4-cell embryo contribute cells to the mouse body? Int J Dev Biol 45:811â816
Tarkowski AK, Ozdzenski W, Czolowska R (2005a) Identical triplets and twins developed from isolated blastomeres of 8- and 16-cell mouse embryos supported with tetraploid blastomeres. Int J Dev Biol 49:825â832
Tarkowski AK, Jagiello K, Czolowska R, Ozdzenski W (2005b) Mouse chimaeras developed from electrofused blastocysts: new evidence for developmental plasticity of the inner cell mass. Int J Dev Biol 49:909â914
Tarkowski AK, Suwinska A, Czolowska R, OzdzeĆski W (2010) Individual blastomeres of 16- and 32-cell mouse embryos are able to develop into foetuses and mice. Dev Biol 348:190â198
Torres-Padilla ME, Parfitt DE, Kouzarides T, Zernicka-Goetz M (2007) Histone arginine methylation regulates pluripotency in the early mouse embryo. Nature 445:214â218
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 69:315â322
Tsunoda Y, Yasui T, Okubo Y, Nakamura K, Sugie T (1987) Development of one or two blastomeres from eight-cell mouse embryos to term in the presence of parthenogenetic eggs. Theriogenology 28:615â623
Wakayama S, Hikichi T, Suetsugu R, Sakaide Y, Bui H, Mizutani E, Wakayama T (2007) Efficient establishment of mouse embryonic stem cell lines from single blastomeres and polar bodies. Stem Cells 25:986â993
Willadsen SM (1981) The developmental capacity of blastomeres from 4- and 8- cell sheep embryos. J Embryol Exp Morphol 65:165â172
Waksmundzka M, Wisniewska A, Maleszewski M (2006) Allocation of cells in mouse blastocyst is not determined by the order of cleavage of the first two blastomeres. Biol Reprod 75:582â587
Van de Velde H, Cauffman G, Tournaye H, Devroey P, Liebaers I (2008) The four blastomeres of a 4-cell stage human embryo are able to develop individually into blastocysts with inner cell mass and trophectoderm. Hum Reprod 23:1742â1747
Ziomek CA, Johnson MH (1982) The roles of phenotype and position in guiding the fate of 16-cell mouse blastomeres. Dev Biol 91:440â447
Ziomek CA, Johnson MH, Handyside AH (1982) The developmental potential of mouse 16-cell blastomeres. J Exp Zool 221:345â355
Acknowledgments
I would like to dedicate this work to Professor A.K. Tarkowski, my mentor, as an expression of respect for his work and scientific achievements. I am grateful to Professor A.K. Tarkowski, Professor M. Kloc, Dr. J. Kubiak, and Professor M. Maleszewski for critical reading and valuable suggestions. During the preparation of this work Aneta Suwinska was supported by the grant in the framework of PARENT-BRIDGE Programme from the Foundation for Polish Science POMOST/2010-1/9 and a grant from Polish Ministry of Science and Higher Education N N301 311637.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2012 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
SuwiĆska, A. (2012). Preimplantation Mouse Embryo: Developmental Fate and Potency of Blastomeres. In: Kubiak, J. (eds) Mouse Development. Results and Problems in Cell Differentiation, vol 55. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-30406-4_8
Download citation
DOI: https://doi.org/10.1007/978-3-642-30406-4_8
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-30405-7
Online ISBN: 978-3-642-30406-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)