Abstract
The pattern of the earliest cell divisions in a vertebrate embryo lays the groundwork for later developmental events such as gastrulation, organogenesis, and overall body plan establishment. Understanding these early cleavage patterns and the mechanisms that create them is thus crucial for the study of vertebrate development. This chapter describes the early cleavage stages for species representing ray-finned fish, amphibians, birds, reptiles, mammals, and proto-vertebrate ascidians and summarizes current understanding of the mechanisms that govern these patterns. The nearly universal influence of cell shape on orientation and positioning of spindles and cleavage furrows and the mechanisms that mediate this influence are discussed. We discuss in particular models of aster and spindle centering and orientation in large embryonic blastomeres that rely on asymmetric internal pulling forces generated by the cleavage furrow for the previous cell cycle. Also explored are mechanisms that integrate cell division given the limited supply of cellular building blocks in the egg and several-fold changes of cell size during early development, as well as cytoskeletal specializations specific to early blastomeres including processes leading to blastomere cohesion. Finally, we discuss evolutionary conclusions beginning to emerge from the contemporary analysis of the phylogenetic distributions of cleavage patterns. In sum, this chapter seeks to summarize our current understanding of vertebrate early embryonic cleavage patterns and their control and evolution.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Aimar C (1997) Formation of new plasma membrane during the first cleavage cycle in the egg of Xenopus laevis: an immunocytological study. Dev Growth Differ 39:693–704
Ajduk A, Zernicka-Goetz M (2015) Polarity and cell division orientation in the cleavage embryo: from worm to human. Mol Hum Reprod. Epub ahead of print
Amodeo AA, Jukam D, Straight AF, Skotheim JM (2015) Histone titration against the genome sets the DNA-to-cytoplasm threshold for the Xenopus midblastula transition. Proc Natl Acad Sci U S A 112:E1086–E1095
Azzarello A, Hoest T, Mikkelsen AL (2012) The impact of pronuclei morphology and dynamicity on live birth outcome after time-lapse. Hum Reprod 27:2649–2657
Ballard WW (1986a) Morphogenetic movements and a provisional fate map of development in the holostean fish, Amia calva. J Exp Zool 238:355–372
Ballard WW (1986b) Stages and rates of normal development in the holostean fish, Amia calva. J Exp Zool 238:337–354
Basile N, Nogales Mdel C, Bronet F, Florensa M, Riqueiros M, Rodrigo L, García-Velasco J, Meseguer M (2014) Increasing the probability of selecting chromosomally normal embryos by time-lapse morphokinetics analysis. Fertil Steril 101:699–704
Batten BE, Albertini DF, Ducibella T (1987) Patterns of organelle distribution in mouse embryos during preimplantation development. Am J Anat 178:204–213
Bjerkness M (1986) Physical theory of the orientation of astral mitotic spindles. Science 234:1413–1416
Black SD, Vincent J-P (1988) The first cleavage plane and the embryonic axis are determined by separate mechanisms in Xenopus laevis. II. Experimental dissociation by lateral compression of the egg. Dev Biol 128:65–71
Bluemink JG (1970) The first cleavage of the amphibian egg. An electron microscope study of the onset of cytokinesis in the egg of Ambystoma mexicanum. J Ultrastruct Res 32:142–166
Bluemink JG, deLaat SW (1973) New membrane formation during cytokinesis in normal and cytochalasin B-treated eggs of Xenopus laevis: I. Electron microscope observations. J Cell Biol 59:89–108
Boucaut JC, Darribere T, Boulekbache H, Thiery JP (1984) Prevention of gastrulation but not neurulation by antibodies to fibronectin in amphibian embryos. Nature 307:364–367
Brachet A (1910) Experimental polyspermy as a means of analysis of fecundation. Arch Entwiklungsmech Org 30:261–303
Buchholz DR, Singamsetty S, Karadge U, Williamson S, Langer CE, Elinson RP (2007) Nutritional endoderm in a direct developing frog: a potential parallel to the evolution of the amniote egg. Dev Dyn 236:1259–1272
Bukarov A, Nadezhdina E, Slepchenko B, Rodionov V (2003) Centrosome positioning in interphase cells. J Cell Biol 162:963–969
Burbank KS, Mitchison TJ, Fisher DS (2007) Slide-and-cluster models for spindle assembly. Curr Biol 17:1373–1383
Burruel V, Klooster K, Barker CM, Pera RR, Meyers S (2014) Abnormal early cleavage events predict early embryo demise: sperm oxidative stress and early abnormal cleavage. Sci Rep 4:6598
Byers TJ, Armstrong PB (1986) Membrane protein redistribution during Xenopus first cleavage. J Cell Biol 102:2176–2184
Cai S, Weaver LN, Ems-McClung SC, Walczak CE (2009) Kinesin-14 family proteins HSET/XCTK2 control spindle length by cross-linking and sliding microtubules. Mol Biol Cell 20:1348–1359
Campbell A, Fishel S, Bowman N, Duffy S, Sedler M, Hickman CF (2013) Modelling a risk classification of aneuploidy in human embryos using non-invasive morphokinetics. Reprod Biomed Online 26:477–485
Cao LG, Wang YL (1996) Signals from the spindle midzone are required for the stimulation of cytokinesis in cultured epithelial cells. Mol Biol Cell 7:225–232
Chamayou S, Patrizio P, Storaci G, Tomaselli V, Alecci C, Ragolia C, Crescenzo C, Guglielmino A (2013) The use of morphokinetic parameters to select all embryos with full capacity to implant. J Assist Reprod Genet 30:703–710
Chambers EL (1939) The movement of the egg nucleus in relation to the sperm aster in the echinoderm egg. J Exp Biol 16:409–424
Chavez SL, Loweke KE, Han JH, Moussavi F, Colls P, Munne S, Behr B, Reijo Pera RA (2012) Dynamic blastomere behaviour reflects human embryo ploidy by the four-cell stage. Nat Commun 3:1251
Chavez SL, McElroy SL, Bossert NL, De Jonge CJ, Rodriguez MV, Leong DE, Behr B, Westphal LM, Reijo Pera RA (2014) Comparison of epigenetic mediator expression and function in mouse and human embryonic blastomeres. Hum Mol Genet 23:4970–4984
Chow JF, Yeung WS, Lau EY, Lee VC, Ng EH, Ho PC (2014) Array comparative genomic hybridization analyses of all blastomeres of a cohort of embryos from young IVF patients revealed significant contribution of mitotic errors to embryo mosaicism at the cleavage stage. Reprod Biol Endocrinol 12:105
Cockburn K, Rossant J (2010) Making the blastocyst: lessons from the mouse. J Clin Invest 120:995–1003
Collart C, Allen GE, Bradshaw CR, Smith J, Zegerman CP (2013) Titration of four replication factors is essential for the Xenopus laevis midblastula transition. Science 341:893–896
Collazo A (1996) Evolutionary correlations between early development and life history in plethodontid salamanders and teleost fishes. Am Zool 36:116–131
Collazo A, Bolker JA, Keller R (1994) A phylogenetic perspective on teleost gastrulation. Am Nat 144:133–152
Conklin EG (1905) The organization and cell lineage of the ascidian egg. J Acad Nat Sci Phil 13:1–119
Courtois A, Schuh M, Ellenberg J, Hiiragi T (2012) The transition from meiotic to mitotic spindle assembly is gradual during early mammalian development. J Cell Biol 198:357–370
Cruz M, Galdea B, Garrido N, Pedersen KS, Martínez M, Pérez-Cano I, Muñoz M, Meseguer M (2011) Embryo quality, blastocyst and ongoing pregnancy rates in oocyte donation patients whose embryos were monitored by time-lapse imaging. J Assist Reprod Genet 28:569–573
Cruz M, Garrido N, Herrero J, Pérez-Cano I, Muñoz M, Meseguer M (2012) Timing of cell division in human cleavage-stage embryos is linked with blastocyst formation and quality. Reprod Biomed Online 25:371–381
Da Silva-Buttkus P, Jayasooriya GS, Mora JM, Mobberley M, Ryder TA, Baithun M, Stark J, Franks S, Hardy K (2008) Effect of cell shape and packing density on granulosa cell proliferation and formation of multiple layers during early follicle development in the ovary. J Cell Sci 121:3890–3900
Dal Canto M, Coticchio G, Mignini Renzini M, De Ponti E, Novara PV, Brambillasca F, Comi R, Fadini R (2012) Cleavage kinetics analysis of human embryos predicts development to blastocyst and implantation. Reprod Biomed Online 25:474–480
Danilchik M, Williams M, Brown E (2013) Blastocoel-spanning filopodia in cleavage-stage Xenopus laevis: potential roles in morphogen distribution and detection. Dev Biol 382:70–81
Danilchik MV, Brown EE (2008) Membrane dynamics of cleavage furrow closure in Xenopus laevis. Dev Dyn 237:565–579
Danilchik MV, Funk WC, Brown EE, Larkin K (1998) Requirement for microtubules in new membrane formation during cytokinesis of Xenopus embryos. Dev Biol 194:47–60
Davidson LA, Dzamba BD, Keller R, DeSimone DW (2008) Live imaging of cell protrusive activity, and extracellular matrix assembly and remodeling during morphogenesis in the frog, Xenopus laevis. Dev Dyn 237:2684–2692
Davidson LA, Keller R, DeSimone DW (2004) Assembly and remodeling of the fibrillar fibronectin extracellular matrix during gastrulation and neurulation in Xenopus laevis. Dev Dyn 231:888–895
Decker M, Jaensch S, Pozniakovsky A, Zinke A, O'Connell KF, Zachariae W, Myers E, Hyman AA (2011) Limiting amounts of centrosome material set centrosome size in C. elegans embryos. Curr Biol 21:1259–1267
Delattre M, Gönczy P (2004) The arithmetic of centrosome biogenesis. J Cell Sci 117:1619–1629
Dobson AT, Raja R, Abeyta MJ, Taylor T, Shen S, Haqq C, Pera RA (2004) The unique transcriptome through day 3 of human preimplantation development. Hum Mol Genet 13:1461–1470
Dogterom M, Kerssemakers JW, Romet-Lemmone G, Janson ME (2005) Force generation by dynamic microtubules. Curr Opin Cell Biol 17:67–74
Ducibella T, Anderson E (1975) Cell shape and membrane changes in the eight-cell mouse embryo: prerequisites for morphogenesis of the blastocyst. Dev Biol 47:45–58
Dumont S, Mitchinson TJ (2009) Force and length in the mitotic spindle. Curr Biol 19:R749–R761
Edwards RG, Purdy JM, Steptoe PC, Walters DE (1981) The growth of human preimplantation embryos in vitro. Am J Obstet Gynecol 141:408–416
Elinson RP (1975) Site of sperm entry and a cortical contraction associated with egg activation in the frog Rana pipiens. Dev Biol 47:257–268
Elinson RP (2009) Nutritional endoderm: a way to breach the holoblastic-meroblastic barrier in tetrapods. J Exp Zool Part B Mol Dev Evol 312B:526–532
Eno C, Pelegri F (2013) Gradual recruitment and selective clearing generate germ plasm aggregates in the zebrafish embryo. Bioarchitecture 3:125–132
Eno C, Pelegri F (2016) Germ cell determinant transmission, segregation and function in the zebrafish embryo. In: Carreira RP (ed) Insights from animal reproduction. InTech, Rijeka, Croatia, pp 115–142
Eno C, Solanki B, Pelegri F (2016) aura (mid1ip1l) regulates the cytoskeleton at the zebrafish egg-to-embryo transition. Development 143:1585–1599
Fankhauser G (1932) Cytological studies on egg fragments of the salamander triton: II. The history of the supernumerary sperm nuclei in normal fertilization and cleavage of fragments containing the egg nucleus. J Exp Zool 62:185–235
Feng B, Schwarz H, Jesuthasan S (2002) Furrow-specific endocytosis during cytokinesis of zebrafish blastomeres. Exp Cell Res 279:14–20
Fesenko I, Kurth T, Sheth B, Fleming TP, Citi S, Hausen P (2000) Tight junction biogenesis in the early Xenopus embryo. Mech Dev 96:51–65
Field CM, Groen CA, Nguyen PA, Mitchison TJ (2015) Spindle-to-cortex communication in cleaving, polyspermic Xenopus eggs. Mol Biol Cell 26:3628–3640
Fierro-González JC, White MD, Silva JCR, Plachta N (2013) Cadherin-dependent filopodia control preimplantation embryo compaction. Nat Cell Biol 15:1424–1433
Flach G, Johnson MH, Braude PR, Taylor RA, Bolton VN (1982) The transition from maternal to embryonic control in the 2-cell mouse embryo. EMBO J 1:681–686
Fleming TP, Hay M, Javed Q, Citi S (1993) Localisation of tight junction protein cingulin is temporally and spatially regulated during early mouse development. Development 117:1135–1144
Fleming TP, Papenbrock T, Fesenko I, Hausen P, Sheth B (2000) Assembly of tight junctions during early vertebrate development. Semin Cell Dev Biol 11:291–299
Gaglio T, Dionne MA, Compton DA (1997) Mitotic spindle poles are organized by structural and motor proteins in addition to centrosomes. J Cell Biol 1997:1055–1066
Galán A, Montaner D, Póo ME, Valbuena D, Ruiz V, Aguilar C, Dopazo J, Simón C (2010) Functional genomics of 5- to 8-cell stage human embryos by blastomere single-cell cDNA analysis. PLoS One 5:e13615
Gardner RL (2002) Experimental analysis of second cleavage in the mouse. Hum Reprod 17:3178–3189
Gilbert SF (2000) Early mammalian development. Sinauer Associates, Sunderland, MA
Glotzer M (2001) Animal cell cytokinesis. Annu Rev Cell Dev Biol 17:351–386
Good MC, Vahey MD, Skandarajah A, Fletcher DA, Heald R (2013) Cytoplasmic volume modulates spindle size during embryogenesis. Science 342:856–860
Greenan G, Brangwynne CP, Jaensch S, Gharakhani J, Jülicher F, Hyman AA (2010) Centrosome size sets mitotic spindle length in Caenorhabditis elegans embryos. Curr Biol 20:353–358
Grill SW, Howard J, Schaffer E, Stelzer EH, Hyman AA (2003) The distribution of active force generators controls mitotic spindle position. Science 301:518–521
Grill SW, Hyman AA (2005) Spindle positioning by cortical pulling forces. Dev Cell 8:461–465
Gulyas BJ (1975) A reexamination of cleavage patterns in eutherian mammalian eggs: rotation of blastomere pairs during second cleavage in the rabbit. J Exp Zool 193:235–248
Hamaguchi MS, Hiramoto Y (1986) Analysis of the role of astral rays in pronuclear migration in sand dollar eggs by the colcemid-UV method. Dev Growth Differ 28:143–156
Hamatani T, Carter MG, Sharov AA, Ko MSH (2004) Dynamics of global gene expression changes during mouse preimplantation development. Dev Cell 6:117–131
Han Y-C, Pralong-Zamofing D, Ackermann U, Geering K (1991) Modulation of Na, K-ATPase expression during early development of Xenopus laevis. Dev Biol 145:174–181
Harrison RH, Kuo HC, Scriven PN, Handyside AH, Ogilvie CM (2000) Lack of cell cycle checkpoints in human cleavage stage embryos revealed by a clonal pattern of chromosomal mosaicism analysed by sequential multicolour FISH. Zygote 8:217–224
Hart NH, Becker KA, Wolenski JS (1992) The sperm entry site during fertilization of the zebrafish egg: localization of actin. Mol Reprod Dev 32:217–228
Hart NH, Donovan M (1983) Fine structure of the chorion and site of sperm entry in the egg of Brachydanio. J Exp Zool 227:277–296
Hashimoto S, Kato N, Saeki K, Morimoto Y (2012) Selection of high-potential embryos by culture in poly(dimethylsiloxane) microwells and time-lapse imaging. Fertil Steril 97:332–337
Hazel J, Krutkramelis K, Mooney P, Tomschik M, Gerow K, Oakey J, Gatlin JC (2013) Changes in cytoplasmic volume are sufficient to drive spindle scaling. Science 342:853–856
Heald R, Tournebize R, Blank T, Sandaltzopoulos R, Becker P, Hyman A, Karsenti E (1996) Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopus. Nature 382:420–425
Heald R, Tournebize R, Habermann A, Karsenti E, Hyman A (1997) Spindle assembly in Xenopus extracts: respective roles of centrosomes and microtubule self-organization. J Cell Biol 138:615–628
Heasman J, Crawford A, Goldstone K, Garner-Hamrick P, Gumbiner B, McCrea P, Kintner C, Noro CY, Wylie C (1994a) Overexpression of cadherins and underexpression of ß-catenin inhibit dorsal mesoderm induction in early Xenopus embryos. Cell 79:791–803
Heasman J, Ginsberg D, Geiger B, Goldstone K, Pratt T, Yoshida-Noro C, Wylie CC (1994b) A functional test for maternally inherited cadherin in Xenopus shows its importance in cell adhesion at the blastula stage. Development 120:49–57
Hertwig O (1893) Ueber den Werth der ersten Furchungszellen fuer die Organbildung des Embryo: Experimentelle studien am Frosch- und Tritonei. Arch mikr Anat xlii:662–807
Hibino T, Nishikata T, Nishida H (1998) Centrosome-attracting body: a novel structure closely related to unequal cleavages in the ascidian embryo. Dev Growth Differ 40:85–95
Hill TL, Kirschner MW (1982) Subunit treadmilling of microtubules or actin in the presence of cellular barriers: possible conversion of chemical free energy into mechanical work. Proc Natl Acad Sci U S A 79:490–494
Hlinka D, Kalatová B, Dolinská S, Rutarová J, Rezacová J, Lazarovská S, Dudás M (2012) Time-lapse cleavage rating predicts human embryo viability. Physiol Res 61:513–525
Hoh JH, Heinz WF, Werbin JL (2013) Spatial information dynamics during early zebrafish development. Dev Biol 377:126–137
Houliston E, Maro B (1989) Posttranslational modification of distinct microtubule subpopulations during cell polarization and differentiation in the mouse preimplantation embryo. J Cell Biol 108:543–551
Iseto T, Nishida H (1999) Ultrastructural studies on the centrosome-attracting body: electron-dense matrix and its role in unequal cleavages in ascidian embryos. Dev Growth Differ 41:601–609
Ishihara K, Nguyen PA, Groen AC, Field CM, Mitchison TJ (2014) Microtubule nucleation remote from centrosomes may explain how asters span large cells. Proc Natl Acad Sci U S A 111:17715–17722
Jesuthasan S (1998) Furrow-associated microtubule arrays are required for the cohesion of zebrafish blastomeres following cytokinesis. J Cell Sci 111:3695–3703
Johnson DS, Gemelos G, Baner J, Ryan A, Cinnioglu C, Banjevic M, Ross R, Alper M, Barrett B, Frederick JM, Potter D, Behr B, Rabinowitz M (2010) Preclinical validation of a microarray method for full molecular karyotyping of blastomeres in a 24-h protocol. Hum Reprod 25:1066–1075
Johnson MH, Maro B (1984) The distribution of cytoplasmic actin in mouse 8-cell blastomeres. J Embryol Exp Morphol 82:97–117
Johnson MH, Ziomek CA (1981a) The foundation of two distinct cell lineages within the mouse morula. Cell 24:71–80
Johnson MH, Ziomek CA (1981b) Induction of polarity in mouse 8-cell blastomeres: specificity, geometry, and stability. J Cell Biol 91:303–308
Just EE (1919) The fertilization reaction in Echinarachnius parma. Biol Bull 36:1–10
Kalt MR (1971a) The relationship between cleavage and blastocoel formation in Xenopus laevis: I. Light microscopic observations. J Embryol Exp Morphol 26:37-49
Kalt MR (1971b) The relationship between cleavage and blastocoel formation in Xenopus laevis: II. Electron microscopic observations. J Embryol Exp Morphol 26:51–66
Keller RE (1986) The cellular basis of amphibian gastrulation. In: Browder LW (ed) Developmental biology, a comprehensive synthesis, vol 2, The cellular basis of morphogenesis. Plenum Publishing Corporation, New York
Kidder GM, McLachlin JR (1985) Timing of transcription and protein synthesis underlying morphogenesis in preimplantation mouse embryos. Dev Biol 112:265–275
Kimmel C, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development in the zebrafish. Dev Dyn 203:253–310
Kimura K, Kimura A (2011) Intracellular organelles mediate cytoplasmic pulling force for centrosome centration in the Caenorhabditis elegans early embryo. Proc Natl Acad Sci U S A 108:137–142
Ko MS, Kitchen JR, Wang X, Threat TA, Wang X, Hasegawa A, Sun, Grahovac MJ, Kargul GJ, Lim MK, Cui Y, Sano Y, Tanaka T, Liang Y, Mason S, Paonessa PD, Sauls AD, DePalma GE, Sharara R, Rowe LB, Eppig JJ, Morrell C, Doi H (2000) Large-scale cDNA analysis reveals phased gene expression patterns during preimplantation mouse development. Development 127:1737–1749
Kotak S, Gönczy P (2013) Mechanisms of spindle positioning: cortical force generators in the limelight. Curr Opin Cell Biol 25:741–748
Koyama H, Suzuki H, Yang X, Jiang S, Foote HR (1994) Analysis of polarity of bovine and rabbit embryos by scanning electron microscopy. Biol Reprod 50:163–170
Kühl M, Wedlich D (1996) Xenopus cadherins: sorting out types and functions in embryogenesis. Dev Dyn 207:121–134
Kunda P, Baum B (2009) The actin cytoskeleton in spindle assembly and positioning. Trends Cell Biol 19:174–179
Landry DW, Zucker HA, Sauer MV, Reznik M, Wiebe L (2006) Hypocellularity and absence of compaction as criteria for embryonic death. Regen Med 1:367–371
Lázaro-Diéguez F, Ispolatov I, Müsch A (2015) Cell shape impacts on the positioning of the mitotic spindle with respect to the substratum. Mol Biol Cell 26:1286–1295
Lee G, Hynes R, Kirschner M (1984) Temporal and spatial regulation of fibronectin in early Xenopus development. Cell 36:729–740
Lee HC, Choi HJ, Park TS, Lee SI, Kim YM, Rengaraj D, Nagai H, Sheng G, Lin JM, Han JY (2013) Cleavage events and sperm dynamics in chick intrauterine embryos. PLoS One 8:e80631
Lessman CA (2012) Centrosomes in the zebrafish (Danio rerio): a review including the related basal body. Cilia 1:9
Levy JB, Johnson MH, Goodall H, Maro B (1986) The timing of compaction: control of a major developmental transition in mouse early embryogenesis. J Embryol Exp Morphol 95:213–237
Lindeman RE, Pelegri F (2012) Localized products of futile cycle/lrmp promote centrosome-nucleus attachment in the zebrafish zygote. Curr Biol 22:843–851
Liu Y, Chapple V, Feenan K, Roberts P, Matson P (2015) Clinical significance of intercellular contact at the four-cell stage of human embryos, and the use of abnormal cleavage patterns to identify embryos with low implantation potential: a time-lapse study. Fertil Steril 103:1485–1491
Liu Y, Chapple V, Roberts P, Matson P (2014) Prevalence, consequence, and significance of reverse cleavage by human embryos viewed with the use of the Embryoscope time-lapse video system. Fertil Steril 102(1295–1300):e1292
Lohka MJ, Maller JL (1985) Induction of nuclear envelope breakdown, chromosome condensation, and spindle formation in cell-free extracts. J Cell Biol 101:518–523
Long WL, Ballard WW (2001) Normal embryonic stages of the longnose gar, Lepisosteus osseus. BMC Dev Biol 1:6
Longo D, Peirce SM, Skalak TC, Davidson L, Marsden M, Dzamba B, DeSimone DW (2004) Multicellular computer simulation of morphogenesis: blastocoel roof thinning and matrix assembly in Xenopus laevis. Dev Biol 271:210–222
Los FJ, Van Opstal D, van den Berg C (2004) The development of cytogenetically normal, abnormal and mosaic embryos: a theoretical model. Hum Reprod Update 10:79–94
Lundin K, Bergh C, Hardarson T (2001) Early embryo cleavage is a strong indicator of embryo quality in human IVF. Hum Reprod 16:2652–2657
Luxenburg C, Pasolli HA, Williams SE, Fuchs E (2011) Developmental roles for Srf, cortical cytoskeleton and cell shape in epidermal spindle orientation. Nat Cell Biol 13:203–214
Mabuchi I, Tsukita S, Tsukita S, Sawai T (1988) Cleavage furrow isolated from newt eggs: contraction, organization of the actin filaments and protein components of the furrow. Proc Natl Acad Sci U S A 85:5966–5970
Manandhar G, Sutovsky P, Joshi HC, Stearns T, Schatten G (1998) Centrosome reduction during mouse spermiogenesis. Dev Biol 203:424–434
Martineau SN, Andreassen PR, Margolis RL (1995) Delay of HeLa cell cleavage into interphase using dihydrocytochalasin B: retention of a postmitotic spindle and telophase disc correlates with synchronous cleavage recovery. J Cell Biol 131:191–205
Matsubara Y, Sakai A, Kuroiwa A, Suzuki T (2014) Efficient embryonic culture method for the Japanese striped snake, Elaphe quadrivirgata, and its early developmental stages. Dev Growth Differ 56:573–582
McNally FJ (2013) Mechanisms of spindle positioning. J Cell Biol 200:131–140
Merzdorf CS, Chen YH, Goodenough DA (1998) Formation of functional tight junctions in Xenopus embryos. Dev Biol 195:187–203
Meseguer M, Herrero J, Tejera A, Hilligsøe KM, Ramsing NB, Remohí J (2011) The use of morphokinetics as a predictor of embryo implantation. Hum Reprod 26:2658–2671
Meseguer M, Rubio I, Cruz M, Basile N, Marcos J, Requena A (2012) Embryo incubation and selection in a time-lapse monitoring system improves pregnancy outcome compared with a standard incubator: a retrospective cohort study. Fertil Steril 98:1481–1489
Minc N, Burgess D, Chang F (2011) Influence of cell geometry on division-plane positioning. Cell 144:414–426
Mishima M (2016) Centralspindlin in Rappaport’s cleavage signaling. Semin Cell Dev Biol 53:45–56
Mitchison TJ, Nguyen PA, Coughlin M, Groen AC (2013) Self-organization of stabilized microtubules by both spindle and midzone mechanisms in Xenopus egg cytosol. Mol Biol Cell 24:1559–1573
Muller HAJ, Hausen P (1995) Epithelial cell polarity in early Xenopus development. Dev Dyn 202:405–420
Mulnard J, Huygens R (1978) Ultrastructural localization of non-specific alkaline phosphatase during cleavage and blastocyst formation in the mouse. J Embryol Exp Morphol 44:121–131
Nagai H, Sezaki M, Kakigushi K, Nakaya Y, Chul Lee H, Ladher R, Sasanami T, Han JH, Yonemura S, Sheng G (2015) Cellular analysis of cleavage-stage chick embryos reveals hidden conservation in vertebrate early development. Development 142:1279–1286
Nair S, Marlow F, Abrams E, Kapp L, Mullins M, Pelegri F (2013) The chromosomal passenger protein Birc5b organizes microfilaments and germ plasm in the zebrafish embryo. PLoS Genet 9:e1003448
Natale DR, Watson AJ (2002) Rac-1 and IQGAP are potential regulators of E-cadherin-catenin interactions during murine preimplantation development. Mech Dev 119(Suppl 1):S21–S26
Navara CS, First NL, Schatten G (1994) Microtubule organization in the cow during fertilization, polyspermy, parthenogenesis, and nuclear transfer: the role of the sperm aster. Dev Biol 1:29–40
Needleman DJ, Groen AC, Ohi R, Maresca T, Mirny L, Mitchison TJ (2010) Fast microtubule dynamics in meiotic spindles measured by single molecule imaging: evidence that the spindle environment does not stabilize microtubules. Mol Biol Cell 21:323–333
Negishi T, Takada T, Kawai N, Nishida H (2007) Localized PEM mRNA and protein are involved in cleavage-plane orientation and unequal cell divisions in ascidians. Curr Biol 17:1014–1025
Newport J, Kirschner M (1982a) A major developmental transition in early Xenopus embryos: II. Control of the onset of transcription. Cell 30:687–696
Newport J, Kirschner M (1982b) A major developmental transition in early Xenopus embryos: I. Characterization and timing of cellular changes at the midblastula stage. Cell 30:675–686
Ng E, Claman P, Léveillé MC, Tanphaichitr N, Compitak K, Suwajanakorn S, Wells G (1995) Sex ratio of babies is unchanged after transfer of fast- versus slow-cleaving embryos. J Assist Reprod Genet 12:566–568
Nguyen PA, Groen AC, Loose M, Ishihara K, Wühr M, Field CM, Mitchison TJ (2014) Spatial organization of cytokinesis signaling reconstituted in a cell-free system. Science 346:244–247
Niakan KK, Eggan K (2013) Analysis of human embryos from zygote to blastocyst reveals distinct gene expression patterns relative to the mouse. Dev Biol 375:54–64
Nieuwkoop PD, Faber J (1967) Normal table of Xenopus laevis. North Holland, Amsterdam
Nikas G, Ao A, Winston RM, Handyside AH (1996) Compaction and surface polarity in the human embryo in vitro. Biol Reprod 55:32–37
Nishida H (1987) Cell lineage analysis in ascidian embryos by intracellular injection of a tracer enzyme: III. Up to the tissue restricted stage. Dev Biol 121:526–541
Nishida H (1994) Localization of determinants for formation of the anterior-posterior axis in eggs of the ascidian Halocynthia roretzi. Dev Biol 120:3093–3104
Nishida H (1996) Vegetal egg cytoplasm promotes gastrulation and is responsible for specification of vegetal blastomeres in embryos of the ascidian Halocynthia roretzi. Dev Biol 122:1271–1279
Nishida H (2002) Specification of developmental fates in ascidian embryos: molecular approach to maternal determinants and signaling molecules. Int Rev Cytol 217:227–276
Nishida H, Satoh N (1983) Cell lineage analysis in ascidian embryos by intracellular injection of a tracer enzyme: I. Up to the eight-cell stage. Dev Biol 99:382–394
Nishikata T, Hibino T, Nishida H (1999) The centrosome-attracting body, microtubule system, and posterior egg cytoplasm are involved in positioning of cleavage planes in the ascidian embryo. Dev Biol 209:72–85
O'Farrell PH, Stumpff J, Su TT (2004) Embryonic cleavage cycles: how is a mouse like a fly. Curr Biol 14:R35–R45
Ohsugi M, Hwang SY, Butz S, Knowles BB, Solter D, Kemler R (1996) Expression and cell membrane localization of catenins during mouse preimplantation development. Dev Dyn 206:391–402
Olivier N, Luengo-Oroz MA, Duloquin L, Faure E, Savy T, Veilleux I, Solinas X, Débarre D, Bourgine P, Santos A, Peyriéras N, Beaurepaire E (2010) Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy. Science 329:967–971
Pauken CM, Capco DG (1999) Regulation of cell adhesion during embryonic compaction of mammalian embryos: roles for PKC and beta-catenin. Mol Reprod Dev 54:135–144
Peippo J, Bredbacka P (1995) Sex-related growth rate differences in mouse preimplantation embryos in vivo and in vitro. Mol Reprod Dev 40:56–61
Pergament E, Fiddler M, Cho N, Johnson D, Holmgren WJ (1994) Sexual differentiation and preimplantation cell growth. Hum Reprod 9:1730–1732
Peshkin L, Wühr M, Pearl E, Haas W, Freeman RMJ, Gerhart JC, Klein AM, Horb M, Gygi SP, Kirschner MW (2015) On the relationship of protein and mRNA dynamics in vertebrate embryonic development. Dev Cell 35:383–394
Petropoulos S, Edsgärd D, Reinius B, Deng Q, Panula SP, Codeluppi S, Plaza Reyes A, Linnarsson S, Sandberg R, Lanner F (2016) Single-cell RNA-Seq reveals lineage and X chromosome dynamics in human preimplantation embryos. Cell 165:1012–1026
Pflüger E (1884) Uber die Einwirkung der Schwerkraft und anderer Bedingungen auf die Richtung der Zelltheilung. Arch Physiol 34:607–616
Piotrowska-Nitsche K, Perea-Gomez A, Haraguchi S, Zernicka-Goetz M (2005) Four-cell stage mouse blastomeres have different developmental properties. Development 132:479–490
Piotrowska-Nitsche K, Zernicka-Goetz M (2005) Spatial arrangement of individual 4-cell stage blastomeres and the order in which they are generated correlate with blastocyst pattern in the mouse embryo. Mech Dev 122:487–500
Pribenszky C, Losonczi E, Molnár M, Lang Z, Mátyás S, Rajczy K, Molnár K, Kovács P, Nagy P, Conceicao J, Vajta G (2010) Prediction of in-vitro developmental competence of early cleavage-stage mouse embryos with compact time-lapse equipment. Reprod Biomed Online 20:371–379
Prodon F, Dru P, Roegiers F, Sardet C (2005) Polarity of the ascidian egg cortex and relocalization of cER and mRNAs in the early embryo. J Cell Sci 118:2393–2404
Rappaport R (1961) Experiments concerning the cleavage stimulus in sand dollar eggs. J Exp Zool 148:81–89
Rappaport R (1996) Cytokinesis in animal cells. Cambridge University Press, Cambridge
Rappaport R, Rappaport BN (1974) Establishment of cleavage furrows by the mitotic spindle. J Exp Zool 189:189–196
Reber SB, Baumbart J, Widlund PO, Pozniakovsky A, Howard J, Hyman AA, Jülicher F (2013) ZMAP215 activity sets spindle length by controlling the total mass of spindle microtubules. Nat Cell Biol 15:1116–1122
Reeve WJ, Kelly FP (1983) Nuclear position in the cells of the mouse early embryo. Embryol Exp Morphol 75:117–139
Reima I, Lehtonen E, Virtanen I, Flechon JE (1993) The cytoskeleton and associated proteins during cleavage, compaction and blastocyst differentiation in the pig. Differentiation 54:35–45
Reinsch S, Karsenti E (1997) Movement of nuclei along microtubules in Xenopus egg extracts. Curr Biol 3:211–214
Roberts SJ, Leaf DS, Moore HP, Gerhart JC (1992) The establishment of polarized membrane traffic in Xenopus laevis embryos. J Cell Biol 118:1359–1369
Roegiers F, Djediat C, Dumollard R, Roubiere C, Sardet C (1999) Phases of cytoplasmic and cortical reorganizations of the ascidian zygote between fertilization and first division. Development 126:3101–3117
Roegiers F, McDougall A, Sardet C (1995) The sperm entry point defines the orientation of the calcium-induced contraction wave that directs the first phase of cytoplasmic reorganization in the ascidian egg. Development 121:3457–3466
Rose L, Gönczy P (2014) Polarity establishment, asymmetric division and segregation of fate determinants in early C. elegans embryos. WormBook 30:1–43
Roux W (1903) Ueber die Ursachen der Bestimmung der Hauptrichttingen des Embryo in Froschei. Anat Anz 23:5–91, 113–150, 101–193
Rubio I, Kuhlmann R, Agerholm I, Kirk J, Herrero J, Escribá MJ, Bellver F, Meseguer M (2012) Limited implantation success of direct-cleaved human zygotes: a time-lapse study. Fertil Steril 98:1458–1463
Sanders EJ, Singal PK (1975) Furrow formation in Xenopus embryos. Involvement of the golgi body as revealed by ultrastructural localization of thiamine pyrophosphatase activity. Exp Cell Res 93:219–224
Sardet C, Dru P, Prodon F (2006) Maternal determinants and mRNAs in the cortex of ascidian oocytes, zygotes and embryos. Biol Cell 97:35–49
Sardet C, Nishida H, Prodon F, Sawada K (2003) Maternal mRNAs of PEM and macho 1, the ascidian muscle determinant, associate and move with a rough endoplasmic reticulum network in the egg cortex. Development 130:5839–5849
Sawai T (1974) Furrow formation on a piece of cortex transplanted to the cleavage of the newt egg. J Cell Sci 15:259–267
Sawai T (1980) On propagation of cortical factor and cytoplasmic factor participating in cleavage furrow formation of the newts egg. Dev Growth Differ 22:437–444
Sawai T, Yomota A (1990) Cleavage plane determination in amphibian eggs. Ann N Y Acad Sci 582:40–49
Sawin KE, Mitchison TJ (1991) Mitotic spindle assembly by two different pathways in vitro. J Cell Biol 112:925–940
Schatten G (1994) The centrosome and its mode of inheritance: the reduction of the centrosome during gametogenesis and its restoration during fertilization. Dev Biol 165:299–335
Schatten H (2012) The cell biology of fertilization. Academic, San Diego
Schuh M, Ellenberg J (2007) Self-organization of MTOCs replaces centrosome function during acentrosomal spindle assembly in live mouse oocytes. Cell 130:484–498
Schweisguth F (2015) Asymmetric cell division in the Drosophila bristle lineage: from polarization of sensory organ precursor cells to Notch-mediated binary fate decision. Wiley Interdiscip Rev Dev Biol 4:299–309
Selman K, Wallace RA, Sarka A, Qi X (1993) Stages of oocyte development in the zebrafish, Brachydanio rerio. J Morphol 218:203–224
Servetnick M, Schulte-Merker S, Hausen P (1990) Cell surface proteins during early Xenopus development: analysis of cell surface proteins and total glycoproteins provides evidence for a maternal glycoprotein pool. Roux’s Arch Dev Biol 198:433–442
Sheng G (2014) Day-1 chick development. Dev Dyn 243:357–367
Sheth B, Fesenko I, Collins JE, Moran B, Wild AE, Anderson JM, Fleming TP (1997) Tight junction assembly during mouse blastocyst formation is regulated by late expression of ZO-1 alpha+ isoform. Development 124:2027–2037
Sheth B, Fontaine JJ, Ponza E, McCallum A, Page A, Citi S, Louvard D, Zahraoui A, Fleming TP (2000) Differentiation of the epithelial apical junctional complex during mouse preimplantation development: a role for rab13 in the early maturation of the tight junction. Mech Dev 97:93–104
Shirae-Kurabayashi M, Nishikata T, Takamura K, Tanaka KJ, Nakamoto C, Nakamura A (2006) Dynamic redistribution of vasa homolog and exclusion of somatic cell determinants during germ cell specification in Ciona intestinalis. Development 133:2683–2693
Skiadas CC, Jackson KV, Racowsky C (2006) Early compaction on day 3 may be associated with increased implantation potential. Fertil Steril 86:1386–1391
Slack C, Warner AE (1973) Intracellular and intercellular potentials in the early amphibian embryo. J Physiol 232:313–330
Sousa-Nunes R, Somers WG (2013) Mechanisms of asymmetric progenitor divisions in the Drosophila central nervous system. Adv Exp Med Biol 786:79–102
Stensen MH, Tanbo TG, Storeng R, Abyholm T, Fedorcsak P (2015) Fragmentation of human cleavage-stage embryos is related to the progression through meiotic and mitotic cell cycles. Fertil Steril 103:374–381
Steptoe PC, Edwards RG, Purdy JM (1971) Human blastocysts grown in culture. Nature 229:132–133
Straight AF, Field CM (2000) Microtubules, membranes and cytokinesis. Curr Biol 10:R760–R770
Strauss B, Adams RJ, Papalopulu N (2006) A default mechanism of spindle orientation based on cell shape is sufficient to generate cell fate diversity in polarised Xenopus blastomeres. Development 133:3883–3893
Su K-C, Bement WM, Petronczki M, von Dassow G (2014) An astral simulacrum of the central spindle accounts for normal, spindle-less, and anucleate cytokinesis in echinoderm embryos. Mol Biol Cell 25:4049–4062
Sugimura S, Akai T, Hashiyada Y, Somfai T, Inaba Y, Hirayama M, Yamanouchi T, Matsuda H, Kobayashi S, Aikawa Y, Ohtake M, Kobayashi E, Konishi K, Imai K (2012) Promising system for selecting healthy in vitro-fertilized embryos in cattle. PLoS One 7:e36627
Sutherland AE, Speed TP, Calarco PG (1990) Inner cell allocation in the mouse morula: the role of oriented division during fourth cleavage. Dev Biol 137:13–25
Symerly C, Wu GJ, Zoran S, Ord T, Rawlins R, Jones J, Navara C, Gerrity M, Rinehart J, Binor Z, Asch R, Schatten G (1995) The paternal inheritance of the centrosome, the cell's microtubule-organizing center, in humans, and the implications for infertility. Nat Med 1:47–52
Takeuchi M, Takahashi M, Okabe M, Aizawa S (2009) Germ layer patterning in bichir and lamprey; an insight into its evolution in vertebrates. Dev Biol 332:90–102
Theusch EV, Brown KJ, Pelegri F (2006) Separate pathways of RNA recruitment lead to the compartmentalization of the zebrafish germ plasm. Dev Biol 292:129–141
Tran PT, Marsh L, Doye V, Inoue S, Chang F (2001) A mechanism for nuclear positioning in fission yeast based on microtubule pushing. J Cell Biol 153:397–411
Uochi T, Takahashi S, Ninomiya H, Fukui A, Asashima M (1997) The Na+, K+-ATPase (alpha) subunit requires gastrulation in the Xenopus embryo. Dev Growth Differ 39:571–580
Urven LE, Yabe T, Pelegri F (2006) A role for non-muscle myosin II function in furrow maturation in the early zebrafish embryo. J Cell Sci 119:4342–4352
Van Soom A, Boerjan ML, Bols PE, Vanroose G, Lein A, Doryn M, de Kruif A (1997) Timing of compaction and inner cell allocation in bovine embryos produced in vivo after superovulation. Biol Reprod 57:1041–1049
Vanneste E, Voet T, Le Caignec C, Ampe M, Konings P, Melotte C, Debrock S, Amyere M, Vikkula M, Schuit F, Fryns JP, Verbeke G, D'Hooghe T, Moreau Y, Vermeesch JR (2009) Chromosome instability is common in human cleavage-stage embryos. Nat Med 15:577–583
Vassena R, Boué S, González-Roca E, Aran B, Auer H, Veiga A, Izpisua Belmonte JC (2011) Waves of early transcriptional activation and pluripotency program initiation during human preimplantation development. Development 138:3699–3709
Vestweber D, Gossler A, Boller K, Kemler R (1987) Expression and distribution of cell adhesion molecule uvomorulin in mouse preimplantation embryos. Dev Biol 124:451–456
Walczak CE, Vernos I, Mitchison TJ, Karsenti E, Heald R (1998) A model for the proposed roles of different microtubule-based motor proteins in establishing spindle bipolarity. Curr Biol 8:903–913
Wang QT, Piotrowska K, Ciemerych MA, Milenkovic L, Scott MP, Davis RW, Zernicka-Goetz M (2004) A genome-wide study of gene activity reveals developmental signaling pathways in the preimplantation mouse embryo. Dev Cell 6:133–144
Weinerman R, Feng R, Ord TS, Schultz RM, Bartolomei MS, Coutifaris C, Mainigi M (2016) Morphokinetic evaluation of embryo development in a mouse model: functional and molecular correlates. Biol Reprod 94:64
Williams SE, Fuchs E (2013) Oriented divisions, fate decisions. Curr Opin Cell Biol 25:749–758
Winning RS, Scales JB, Sargent TD (1996) Disruption of cell adhesion in Xenopus embryos by Pagliaccio, an Eph-class receptor tyrosine kinase. Dev Biol 179:309–319
Wise PAD, Vickaryous MK, Russell AP (2009) An embryonic staging table for in ovo development of Eublepharis macularius, the leopard gecko. Anat Rec (Hoboken) 292:1198–1212
Wong CC, Loewke KE, Bossert NL, Behr B, De Jonge CJ, Baer TM, Reijo Pera RA (2010) Non-invasive imaging of human embryos before embryonic genome activation predicts development to the blastocyst stage. Nat Biotechnol 28:1115–1121
Woolley DM, Fawcett DW (1973) The degeneration and disappearance of the centrioles during the development of the rat spermatozoon. Anat Rec 177:289–301
Wühr M, Chen Y, Dumont S, Groen AC, Needleman DJ, Salic A, Mitchinson TJ (2008) Evidence for an upper limit to mitotic spindle length. Curr Biol 18:1256–1261
Wühr M, Dumont S, Groen AC, Needleman DJ, Mitchison TJ (2009) How does a millimeter-sized cell find its center? Cell Cycle 8:1115–1121
Wühr M, Tan ES, Parker SK, Detrich HWI, Mitchinson TJ (2010) A model for cleavage plane determination in early amphibian and fish embryos. Curr Biol 20:2040–2045
Wylie C (2000) Germ cells. Curr Opin Genet Dev 10:410–413
Xiong F, Ma W, Hisckock TW, Mosaliganti KR, Tentner AR, Brakke KA, Rannou N, Gelas A, Souhait, Swinbume IA, Obholzer MSG (2014) Interplay of cell shape and division orientation promotes robust morphogenesis of developing epithelia. Cell 159:415–427
Xu KP, Yadav BR, King WA, Betteridge KJ (1992) Sex-related differences in developmental rates of bovine embryos produced and cultured in vitro. Mol Reprod Dev 31:249–252
Yabe T, Ge X, Lindeman R, Nair S, Runke G, Mullins M, Pelegri F (2009) The maternal-effect gene cellular island encodes Aurora B kinase and is essential for furrow formation in the early zebrafish embryo. PLoS Genet 5:e1000518
Yang Z, Zhang J, Salem SA, Liu X, Kuang Y, Salem RD, Liu J (2014) Selection of competent blastocysts for transfer by combining time-lapse monitoring and array CGH testing for patients undergoing preimplantation genetic screening: a prospective study with sibling oocytes. BMC Med Genomics 7:38
Zeng F, Baldwin DA, Schultz RM (2004) Transcript profiling during preimplantation mouse development. Dev Biol 272:483–496
Zhang P, Zucchelli M, Bruce S, Hambiliki F, Stavreus-Evers A, Levkov L, Skottman H, Kerselä E, Kere J, Hovatta O (2009) Transcriptome profiling of human pre-implantation development. PLoS One 4:e7844
Ziomek CA, Johnson MH (1980) Cell surface interaction induces polarization of mouse 8-cell blastomeres at compaction. Cell 21:935–942
Zotin AI (1964) The mechanism of cleavage in amphibian and sturgeon eggs. J Embryol Exp Morphol 12:247–262
Acknowledgments
D.H. was supported by NIH grant TG 2 T32 GM007133-40 and NSF grant 1144752-IGERT, as well as the Graduate School and the College of Life Science and Agriculture at U. Wisconsin, Madison, and thanks Danielle Grotjahn for the help and discussions with related work. S.C. gratefully acknowledges the National Centers for Translational Research in Reproduction and Infertility (NCTRI)/NICHD (P50 HD071836), Howard and Georgeanna Jones Foundation for Reproductive Medicine, Medical Research Foundation of Oregon, and the Collins Medical Trust for funding. Research in the laboratory of M.D. is supported by the National Science Foundation (IOS-1557527). M.W. was supported by the Charles A. King Trust Postdoctoral Fellowship Program, Bank of America, N.A., Co-Trustee. Research in the laboratory of F.P. is supported by NIH grant RO1 GM065303.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer International Publishing Switzerland
About this chapter
Cite this chapter
Hasley, A., Chavez, S., Danilchik, M., Wühr, M., Pelegri, F. (2017). Vertebrate Embryonic Cleavage Pattern Determination. In: Pelegri, F., Danilchik, M., Sutherland, A. (eds) Vertebrate Development. Advances in Experimental Medicine and Biology, vol 953. Springer, Cham. https://doi.org/10.1007/978-3-319-46095-6_4
Download citation
DOI: https://doi.org/10.1007/978-3-319-46095-6_4
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-46093-2
Online ISBN: 978-3-319-46095-6
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)