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Asymmetric Localization and Distribution of Factors Determining Cell Fate During Early Development of Xenopus laevis

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Asymmetric Cell Division in Development, Differentiation and Cancer

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 61))

Abstract

Asymmetric division is a property of eukaryotic cells that is fundamental to the formation of higher life forms. Despite its importance, the mechanism behind it remains elusive. Asymmetry in the cell is induced by polarization of cell fate determinants that become unevenly distributed among progeny cells. So far dozens of determinants have been identified. Xenopus laevis is an ideal system to study asymmetric cell division during early development, because of the huge size of its oocytes and early-stage blastomeres. Here, we present the current knowledge about localization and distribution of cell fate determinants along the three body axes: animal–vegetal, dorsal–ventral, and left–right. Uneven distribution of cell fate determinants during early development specifies the formation of the embryonic body plan.

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References

  • Adams DS, Robinson KR, Fukumoto T, Yuan S, Albertson RC, Yelick P, Kuo L, McSweeney M, Levin M (2006) Early, H+-V+ATPase-dependent proton flux is necessary for consistent left-right patterning of non-mammalian vertebrates. Development 133:1657–1671

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Agius E, Oelgeschläger M, Wessely O, Kemp C, De Robertis EM (2000) Endodermal nodal-related signals and mesoderm induction in Xenopus. Development 127(6):1173–1178

    CAS  PubMed  PubMed Central  Google Scholar 

  • Blanpain C, Lowry WE, Geoghegan A, Polak L, Fuchs E (2004) Self-renewal, multipotency, and the existence of two cell populations within an epithelial stem cell niche. Cell 118:635–648

    Article  CAS  PubMed  Google Scholar 

  • Blum M, Schweickert A, Vick P, Wright CV, Danilchik MV (2014) Symmetry breakage in the vertebrate embryo: when does it happen and how does it work? Dev Biol 393:109–123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bubunenko M, Kress TL, Vempati UD, Mowry KL, King ML (2002) A consensus RNA signal that directs germ layer determinants to the vegetal cortex of Xenopus oocytes. Dev Biol 248:82–92

    Article  CAS  PubMed  Google Scholar 

  • Bunney TD, De Boer AH, Levin M (2003) Fusicoccin signaling reveals 14-3-3 protein function as a novel step in left-right patterning during amphibian embryogenesis. Development 130:4847–4858

    Article  CAS  PubMed  Google Scholar 

  • Cowan CR, Hyman AA (2004) Centrosomes direct cell polarity independently of microtubule assembly in C. elegans embryos. Nature 431(7004):92–96

    Article  CAS  PubMed  Google Scholar 

  • Cuykendall TN, Houston DW (2010) Identification of germ plasm-associated transcripts by microarray analysis of Xenopus vegetal cortex RNA. Dev Dyn 239:1838–1848

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Danilchik MV, Gerhadt JC (1987) Differentiation of the animal–vegetal axis in Xenopus laevis oocytes. I. Polarized intracellular translocation of platelets establishes the yolk gradient. Dev Biol 122:101–112

    Article  CAS  PubMed  Google Scholar 

  • Darras S, Maikawa Y, Elinson RP, Lemaire P (1997) Animal and vegetal pole cells of early Xenopus embryos respond differently to maternal dorsal determinants: implications for the patterning of the organiser. Development 124:4275–4286

    CAS  PubMed  Google Scholar 

  • De Domenico E, Owens ND, Grant IM, Gomes-Faria R, Gilchrist MJ (2015) Molecular asymmetry in the 8-cell stage Xenopus tropicalis embryo described by single blastomere transcript sequencing. Dev Biol 408(2):252–268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Denegre JM, Danilchik MV (1993) Deep cytoplasmic rearrangements in axis-respecified Xenopus embryos. Dev Biol 160:157–164

    Article  CAS  PubMed  Google Scholar 

  • Deshler JO, Highett J, Schnapp BJ (1997) Localization of Xenopus Vg1 mRNA by vera protein and the endoplasmatic reticulum. Science 276:1128–1131

    Article  CAS  PubMed  Google Scholar 

  • Dumont JN (1972) Oogenesis in Xenopus laevis (Daudin) I. Stages of oocyte development in laboratory maintained animals. J Morphol 136:153–179

    Article  CAS  PubMed  Google Scholar 

  • Etkin LD (1997) A new face from the endoplasmic reticulum: RNA localization. Science 276:1092–1093

    Article  CAS  PubMed  Google Scholar 

  • Etkin LD, Balcells S (1985) Transformed Xenopus embryos as a transient expression system to analyze gene expression at the midblastula transition. Dev Biol 108:173–178

    Article  CAS  PubMed  Google Scholar 

  • Flachsova M, Sindelka R, Kubista M (2013) Single blastomere expression profiling of Xenopus laevis embryos of 8 to 32-cells reveals developmental asymmetry. Sci Rep 3:2278

    Article  PubMed  PubMed Central  Google Scholar 

  • Fukumoto T, Kema IP, Levin M (2005a) Serotonin signaling is a very early step in patterning of the left-right axis in chick and frog embryos. Curr Biol 15:794–803

    Article  CAS  PubMed  Google Scholar 

  • Fukumoto T, Blakely R, Levin M (2005b) Serotonin transporter function is an early step in left-right patterning in chick and frog embryos. Dev Neurosci 27:349–363

    Article  CAS  PubMed  Google Scholar 

  • Gagnon JA, Kreiling JA, Powrie EA, Wood TR, Mowry KL (2013) Directional transport is mediated by a Dynein-dependent step in an RNA localization pathway. PLoS Biol 11(4):e1001551

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gautreau D, Cote CA, Mowry KL (1997) Two copies of a subelement from the Vg1 RNA localization sequence are sufficient to direct vegetal localization in Xenopus oocytes. Development 124:5013–5020

    CAS  PubMed  Google Scholar 

  • Gerhart J, Danilchik M, Doniach T, Roberts S, Rowning B, Stewart R (1989) Cortical rotation of the Xenopus egg: consequences for the anteroposterior pattern of embryonic dorsal development. Development 107:37–51

    PubMed  Google Scholar 

  • Gilbert SF (2010) Developmental biology, 9th edn. Sinauer Associates, Sunderland, MA

    Google Scholar 

  • Gönczy P, Rose LS (2005) Asymmetric cell division and axis formation in the embryo. In: WormBook (ed) The C. elegans research community. WormBook, Pasadena, CA. doi:10.1895/wormbook.1.30.1

    Google Scholar 

  • Gurdon JB (1968) Changes in somatic cell nuclei inserted into growing and maturing amphibian oocytes. J Embryol Exp Morphol 20:401–414

    CAS  PubMed  Google Scholar 

  • Heasman J (2006) Maternal determinants of embryonic cell fate. Semin Cell Dev Biol 17:93–98

    Article  CAS  PubMed  Google Scholar 

  • Heasman J, Quarmby J, Wylie CC (1984) The mitochondrial cloud of Xenopus ocytes: the source of germinal granule material. Dev Biol 105:458–469

    Article  CAS  PubMed  Google Scholar 

  • Heasman J, Kofron M, Wylie C (2000) Beta-catenin signaling activity dissected in the early Xenopus embryo: a novel antisense approach. Dev Biol 222:124–134

    Article  CAS  PubMed  Google Scholar 

  • Houston DW (2013) Regulation of cell polarity and RNA localization in vertebrate oocyte. Int Rev Cell Mol Biol 306:127–185

    Article  CAS  PubMed  Google Scholar 

  • Hyatt BA, Lohr JL, Yost HJ (1996) Initiation of vertebrate left-right axis formation by maternal Vg1. Nature 384:62–65

    Article  CAS  PubMed  Google Scholar 

  • Jullien J, Pasque V, Halley-Stott RP, Miyamoto K, Gurdon JB (2011) Mechanism of nuclear reprogramming by eggs and oocytes: a deterministic process? Nat Rev Mol Cell Biol 12:453–459

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • King ML, Messitt TJ, Mowry KL (2005) Putting RNAs in the right place at the right time: RNA localization in the frog oocyte. Biol Cell 97:19–33

    Article  CAS  PubMed  Google Scholar 

  • Kloc M, Etkin LD (1994) Delocalization of Vg1 mRNA from the vegetal cortex in Xenopus oocytes after destruction of Xlsirt RNA. Science 265:1101–1103

    Article  CAS  PubMed  Google Scholar 

  • Kloc M, Etkin LD (1995) Two distinct pathways for the localization of RNAs at the vegetal cortex in Xenopus oocytes. Development 121:287–297

    CAS  PubMed  Google Scholar 

  • Kloc M, Spohr G, Etkin LD (1993) Translocation of repetitive RNA sequences with the germ plasm in Xenopus oocytes. Science 262:1712–1714

    Article  CAS  PubMed  Google Scholar 

  • Kloc M, Larabell C, Etkin LD (1996) Elaboration of the messenger transport organizer pathway for localization of RNA to the vegetal cortex of Xenopus oocytes. Dev Biol. 180(1):119–30

    Google Scholar 

  • Kloc M, Larabell C, Chan AP, Etkin LD (1998) Contribution of METRO pathway localized molecules to the organization of the germ cell lineage. Mech Dev 75(1–2):81–93

    Article  CAS  PubMed  Google Scholar 

  • Kloc M, Bilinski S, Chan AP, Allen LH, Zearfoss NR, Etkin LD (2001) RNA localization and germ cell determination in Xenopus. Int Rev Cytol 203:63–91

    Article  CAS  PubMed  Google Scholar 

  • Kloc M, Dougherty MT, Bilinski S, Chan AP, Brey E, King ML, Patrick CW Jr, Etkin LD (2002) Three-dimensional ultrastructural analysis of RNA distribution within germinal granules of Xenopus. Dev Biol 241:79–93

    Article  CAS  PubMed  Google Scholar 

  • Kloc M, Bilinski S, Dougherty MT, Brey EM, Etkin LD (2004) Formation, architecture and polarity of female germline cyst in Xenopus. Dev Biol 266(1):43–61

    Article  CAS  PubMed  Google Scholar 

  • Knoblich JA (2008) Mechanisms of asymmetric stem cell division. Cell 132:583–597

    Article  CAS  PubMed  Google Scholar 

  • Knoblich JA (2010) Asymmetric cell division: recent developments and their implications for tumour biology. Nat Rev Mol Cell Biol 11:849–597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lane MC, Sheets MD (2006) Heading in a new direction: implications of the revised fate map for understanding Xenopus laevis development. Dev Biol 296(1):12–28

    Article  CAS  PubMed  Google Scholar 

  • Levin M, Thorlin T, Robinson KR, Nogi T, Mercola M (2002) Asymmetries in H+/K+-ATPase and cell membrane potentials comprise a very early step in left-right patterning. Cell 111:77–89

    Article  CAS  PubMed  Google Scholar 

  • Lewis RA, Kress TL, Cote CA, Gautreau D, Rokop ME, Mowry KL (2004) Conserved and clustered RNA recognition sequences are a critical feature of signals directing RNA localization in Xenopus oocytes. Mech Dev 121:101–109

    Article  CAS  PubMed  Google Scholar 

  • Lombard-Banek C, Moody SA, Nemes P (2016) Single-cell mass spectrometry for discovery proteomics: quantifying translational cell heterogeneity in the 16-cell frog (Xenopus) embryo. Angew Chem Int Ed Engl 55(7):2454–2458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marikawa Y, Li Y, Elinson RP (1997) Dorsal determinants in the Xenopus egg are firmly associated with the vegetal cortex and behave like activators of the Wnt pathway. Dev Biol 191:69–79

    Article  CAS  PubMed  Google Scholar 

  • Messitt TJ, Gagnon JA, Kreiling JA, Pratt CA, Yoon YJ, Mowry KL (2008) Multiple kinesin motors coordinate cytoplasmic RNA transport on a subpopulation of microtubules in Xenopus oocytes. Dev Cell 15(3):426–436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller JR, Rowning BA, Larabell CA, Yang-Snyder JA, Bates RL, Moon RT (1999) Establishment of the dorsal-ventral axis in Xenopus embryos coincides with dorsal enrichment of dishevelled that is dependent on cortical rotation. J Cell Biol 146:427–437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Newport J, Kirschner M (1982) A major developmental transition in early Xenopus embryos: I. characterization and timing of cellular changes at the midblastula stage. Cell 30:675–686

    Article  CAS  PubMed  Google Scholar 

  • Onjiko RM, Moody SA, Nemes P (2015) Single-cell mass spectrometry reveals small molecules that affect cell fates in the 16-cell embryo. Proc Natl Acad Sci USA 112(21):6545–6550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Onjiko RM, Morris SE, Moody SA, Nemes P (2016) Single-cell mass spectrometry with multi-solvent extraction identifies metabolic differences between left and right blastomeres in the 8-cell frog (Xenopus) embryo. Analyst 141(12):3648–3656

    Article  CAS  PubMed  Google Scholar 

  • Pandur PD, Sullivan SA, Moody SA (2002) Multiple maternal influences on dorsal-ventral fate of Xenopus animal blastomeres. Dev Dyn 225:581–587

    Article  CAS  PubMed  Google Scholar 

  • Pereira G, Yamashita YM (2011) Fly meets yeast: checking the correct orientation of cell division. Trends Cell Biol 21:526–533

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rowning BA, Wells J, Wu M, Gerhart JC, Moon RT, Larabell CA (1997) Microtubule-mediated transport of organelles and localization of beta-catenin to the future dorsal side of Xenopus eggs. Proc Natl Acad Sci USA 94:1224–1229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saiz N, Plusa B, Hadjantonakis AK (2015 Dec) Single cells get together: high-resolution approaches to study the dynamics of early mouse development. Semin Cell Dev Biol 47–48:92–100

    Article  PubMed  Google Scholar 

  • Schatten H, Sun QY (2010) The role of centrosomes in fertilization, cell division and establishment of asymmetry during embryo development. Semin Cell Dev Biol 21:174–184

    Article  PubMed  Google Scholar 

  • Schroeder MM, Gard DL (1992) Organization and regulation of cortical microtubules during the first cell cycle of Xenopus eggs. Development 114:699–709

    CAS  PubMed  Google Scholar 

  • Shahriyari L, Komarova NL (2013) Symmetric vs. asymmetric stem cell divisions: an adaptation against cancer? PLoS One 8:e76195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sidova M, Sindelka R, Castoldi M, Benes V, Kubista M (2015) Intracellular microRNA profiles form in the Xenopus laevis oocyte that may contribute to asymmetric cell division. Sci Rep 5:11157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sindelka R, Jonak J, Hands R, Bustin SA, Kubista M (2008) Intracellular expression profiles measured by real-time PCR tomography in the Xenopus laevis oocyte. Nucleic Acids Res 36:387–392

    Article  CAS  PubMed  Google Scholar 

  • Sindelka R, Sidova M, Svec D, Kubista M (2010) Spatial expression profiles in the Xenopus laevis oocytes measured with qPCR tomography. Methods 51(1):87–91

    Article  CAS  PubMed  Google Scholar 

  • Sive HL, Grainger MR and Harland MR (2000) Early development of Xenopus laevis—a laboratory manual. Cold Spring Harbor Laboratory Press, Chap 2, Fig. 2.1

    Google Scholar 

  • Skirkanich J, Luxardi G, Yang J, Kodjabachian L, Klein PS (2011) An essential role for transcription before the MBT in Xenopus laevis. Dev Biol 357(2):478–491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smits AH, Lindeboom RG, Perino M, van Heeringen SJ, Veenstra GJ, Vermeulen M (2014) Global absolute quantification reveals tight regulation of protein expression in single Xenopus eggs. Nucleic Acids Res 42:9880–9891

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Snedden DD, Bertke MM, Vernon D, Huber PW (2013) RNA localization in Xenopus oocytes uses a core group of trans-acting factors irrespective of destination. RNA 19:889–895

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun L, Bertke MM, Champion MM, Zhu G, Huber PW, Dovichi NJ (2014) Quantitative proteomics of Xenopus laevis embryos: expression kinetics of nearly 4000 proteins during early development. Sci Rep 4:4365

    PubMed  PubMed Central  Google Scholar 

  • Vandenberg LN, Levin M (2010) Far from solved: a perspective on what we know about early machanisms of left-right asymmetry. Dev Dyn 239:3131–3146

    Article  PubMed  Google Scholar 

  • Vincent JP, Gerhart JC (1987) Subcortical rotation in Xenopus eggs: an early step in embryonic axis specification. Dev Biol 123:526–539

    Article  CAS  PubMed  Google Scholar 

  • Vincent JP, Scharf SR, Gerhart JC (1987) Subcortical rotation in Xenopus eggs: a preliminary study of its machanochemical basis. Cell Motil Cytoskeleton 8:143–154

    Article  CAS  PubMed  Google Scholar 

  • Weaver C, Kimelman D (2004) Move it or lose it: axis specification in Xenopus. Development 131:3491–3499

    Article  CAS  PubMed  Google Scholar 

  • White JA, Heasman J (2008) Maternal control of pattern formation in Xenopus laevis. J Exp Zool B Mol Dev Evol 310:73–84

    Article  PubMed  Google Scholar 

  • Yisraeli JK, Sokol S, Melton DA (1990) A two-step model for the localization of maternal mRNA in Xenopus oocytes: involvement of microtubules and microfilaments in the translocation and anchoring of Vg1 mRNA. Development 108:289–298

    CAS  PubMed  Google Scholar 

  • Zearfoss NR, Chan AP, Kloc M, Allen LH, Etkin LD (2003) Identification of new Xlsirt family members in the Xenopus laevis oocyte. Mech Dev 120(4):503–509

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, King ML (1996) Xenopus VegT RNA is localized to the vegetal cortex during oogenesis and encodes a novel T-box transcription factor involved in mesodermal patterning. Development 122:4119–4129

    CAS  PubMed  Google Scholar 

  • Zhou Y, King ML (1996a) Localization of Xcat-2 RNA, a putative germ plasm component, to the mitochondrial cloud in Xenopus stage I oocyte. Development 122:2947–2953

    CAS  PubMed  Google Scholar 

  • Zhou Y, King ML (1996b) RNA transport to the vegetal cortex of Xenopus oocytes. Dev Biol 179:173–183

    Article  CAS  PubMed  Google Scholar 

  • Zhou Y, King ML (2004) Sending RNAs into the future: RNA localization and germ cell fate. IUBMB Life 56:19–27

    Article  CAS  PubMed  Google Scholar 

  • Kwon S, Abramson T, Munro TP, CM J, Kohrmann M, Schnapp BJ (2002) UUCAC- and vera-dependent localization of VegT TNA in Xenopus oocytes. Curr Biol 12:558–564

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This study was supported by Ministry of Youth, Education and Sports of the Czech Republic AV0Z50520701 and grant LH15074; BIOCEV CZ.1.05/1.1.00/02.0109 from the ERDF and by the Czech Science Foundation GA CR—GA16-07500S.

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Correspondence to Mikael Kubista .

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Sindelka, R., Sidova, M., Abaffy, P., Kubista, M. (2017). Asymmetric Localization and Distribution of Factors Determining Cell Fate During Early Development of Xenopus laevis . In: Tassan, JP., Kubiak, J. (eds) Asymmetric Cell Division in Development, Differentiation and Cancer. Results and Problems in Cell Differentiation, vol 61. Springer, Cham. https://doi.org/10.1007/978-3-319-53150-2_10

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