35
Maternal mRNAs and Cell Lineages
Last, embryonic development is being described with
ever-increasing biological detail at multiple levels of analysis. The abundant protein and nucleic acids in each embryo
and the ability to easily monitor cellular and intracellular
behaviors make Xenopus an ideal organism in which to integrate many of these levels into a complex multi-scale model
of development. Given the current trend towards the development of sophisticated statistical and machine-learning
computational tools to explore and work with vast amounts
of data, a “systems biology” approach to rapidly enabling
accurate modeling of complex spatio-temporal interactions
of biological molecules, genes, and cell behavior into gene
regulatory networks is ideally suited to Xenopus embryos.
With its rich history and abundant experimental advantages across many scales of organization, the early Xenopus
embryo holds promise for rigorously providing a united
view of cellular (and subcellular) morphogenesis and the
molecular structure of genetic information, with the cell as a
(proper) frame of reference. Such an effort may well occupy
the next 200 years.
ACKNOWLEDGMENTS
The author would like to thank Maurine Neiman for critical
reading and editing of the manuscript, Malgorzata Kloc for
discussion on structural RNAs, and the University of Iowa
for support.
REFERENCES
Abu-Remaileh, M., Gerson, A., Farago, M., Nathan, G., Alkalay,
I., Rousso, S.Z., Gur, M., Fainsod, A., Bergman, Y., 2010.
Oct-3/4 regulates stem cell identity and cell fate decisions
by modulating Wnt/β-catenin signalling. EMBO J 29,
3236–3248.
Afouda, B.A., Nakamura, Y., Shaw, S., Charney, R.M., Paraiso,
K.D., Blitz, I.L., Cho, K.W.Y., Hoppler, S., 2020. Foxh1/
Nodal def nes context-specif c direct maternal Wnt/β-catenin
target gene regulation in early development. Iscience 23,
101314.
Agius, E., Wessely, O., Kemp, C., Robertis, E.M.D., 2000.
Endodermal nodal-related signals and mesoderm induction
in Xenopus. Development 127, 1173–1183.
Aguero, T., Jin, Z., Chorghade, S., Kalsotra, A., King, M.L.,
Yang, J., 2017. Maternal dead-end 1 promotes translation of
nanos1 through binding the eIF3 complex. Development 144,
dev.152611.
Aguero, T., Jin, Z., Owens, D., Malhotra, A., Newman, K., Yang,
J., King, M.L., 2018. Combined functions of two RRMs in
Dead-end1 mimic helicase activity to promote nanos1 translation in the germline. Mol Reprod Dev 85, 896–908.
Amerongen, R.V., Nawijn, M.C., Lambooij, J.-P., Proost, N.,
Jonkers, J., Berns, A., 2010. Frat oncoproteins act at the
crossroad of canonical and noncanonical Wnt-signaling
pathways. Oncogene 29, 93–104.
Ancel, P., Vintemberger, P., 1948. Recherches sur le déterminisme
de la symétrie bilatérale dans l’œuf des amphibiens. Bull.
Biol. Fr. Belg. Suppl 31, 1–182.
André, J., Rouiller, C., 1956. L’ultrastructure de la membrane
nucléaire des ovocytes del l’araignée (Tegenaria domestica
Clark). In: Proc. European Conf. Electron Microscopy. New
York: Stokholm Acad. Press. pp. 162–164.
Aslan, Y., Tadjuidje, E., Zorn, A.M., Cha, S.-W., 2017. Higheffciency non-mosaic CRISPR-mediated knock-in and indel
mutation in F0 Xenopus. Development 144, 2852–2858.
Baer, K. von, 1834. Die Metamorphose des Eies der Batrachier vor
der Erscheinung des Embryo und Folgerungen aus ihr für die
Theorie der Erzeugung. Archiv für Anatomie, Physiologie
und wissenschaftliche Medizin 481–509.
Bates, T.J.D., Vonica, A., Heasman, J., Brivanlou, A.H., Bell, E.,
2013. Coco regulates dorsoventral specifcation of germ
layers via inhibition of TGFβ signalling. Development 140,
4177–4181.
Beams, H.W., Kessel, R.G., 1974. The problem of germ cell determinants. Int Rev Cytol 39, 413–479.
Belenkaya, T.Y., Han, C., Standley, H.J., Lin, Xinda, Houston,
D.W., Heasman, J., Lin, Xinhua, 2002. Pygopus encodes
a nuclear protein essential for wingless/Wnt signaling.
Development 129, 4089–4101.
Berekelya, L.A., Mikryukov, A.A., Luchinskaya, N.N., Ponomarev,
M.B., Woodland, H.R., Belyavsky, A.V., 2007. The protein
encoded by the germ plasm RNA germes associates with
dynein light chains and functions in Xenopus germline
development. Differentiation 75, 546–558.
Berekelya, L.A., Ponomarev, M., Luchinskaya, N., Belyavsky, A.,
2003. Xenopus germes encodes a novel germ plasm-associated
transcript. Gene Expression Patterns: GEP 3, 521–524.
Betley, J.N., Frith, M.C., Graber, J.H., Choo, S., Deshler, J.O.,
2002. A ubiquitous and conserved signal for RNA localization in chordates. Current Biology 12, 1756–1761.
Bilic, J., Huang, Y.-L., Davidson, G., Zimmermann, T., Cruciat,
C.-M., Bienz, M., Niehrs, C., 2007. Wnt induces LRP6
signalosomes and promotes dishevelled-dependent LRP6
phosphorylation. Science 316, 1619–1622.
Birsoy, B., Berg, L., Williams, P.H., Smith, J.C., Wylie, C.C.,
Christian, J.L., Heasman, J., 2005. XPACE4 is a localized
pro-protein convertase required for mesoderm induction and
the cleavage of specif c TGFβ proteins in Xenopus development. Development 132, 591–602.
Birsoy, B., Kofron, M., Schaible, K., Wylie, C.C., Heasman, J.,
2006. Vg 1 is an essential signaling molecule in Xenopus
development. Development 133, 15–20.
Blythe, S.A., Cha, S.-W., Tadjuidje, E., Heasman, J., Klein, P.S.,
2010. Beta-catenin primes organizer gene expression by
recruiting a histone H3 arginine 8 methyltransferase, Prmt2.
Developmental Cell 19, 220–231.
Boke, E., Ruer, M., Wühr, M., Coughlin, M., Lemaitre, R., Gygi,
S.P., Alberti, S., Drechsel, D., Hyman, A.A., Mitchison, T.J.,
2016. Amyloid-like self-assembly of a cellular compartment.
Cell 166, 637–650.
Bontems, F., Stein, A., Marlow, F., Lyautey, J., Gupta, T., Mullins,
M.C., Dosch, R., 2009. Bucky ball organizes germ plasm
assembly in zebraf sh. Current Biology 19, 414–422.
Boterenbrood, E.C., Nieuwkoop, P.D., 1973. The formation of the
mesoderm in urodelean amphibians. Wilhelm Roux’ Archiv
für Entwicklungsmechanik der Organismen 173, 319–332.
Bounoure, L., 1934. Recherches sur la lignée germinale chez la
grenouille rousse aux premiers stades du développment. Ann
Sci Nat 17, 67–248.
Bounoure, L., 1931. Sur l’existence d’un déterminant germinal
dans l’oeuf indivis de la Grenouille rousse. CR Acad Sci
Paris 193, 402.
Bounoure, L., Aubry, R., Huck, M.L., 1954. Nouvelles recherches
experimentales sur les origines de la lignee reproductrice
Maternal mRNAs and Cell Lineages
Last, embryonic development is being described with
ever-increasing biological detail at multiple levels of analysis. The abundant protein and nucleic acids in each embryo
and the ability to easily monitor cellular and intracellular
behaviors make Xenopus an ideal organism in which to integrate many of these levels into a complex multi-scale model
of development. Given the current trend towards the development of sophisticated statistical and machine-learning
computational tools to explore and work with vast amounts
of data, a “systems biology” approach to rapidly enabling
accurate modeling of complex spatio-temporal interactions
of biological molecules, genes, and cell behavior into gene
regulatory networks is ideally suited to Xenopus embryos.
With its rich history and abundant experimental advantages across many scales of organization, the early Xenopus
embryo holds promise for rigorously providing a united
view of cellular (and subcellular) morphogenesis and the
molecular structure of genetic information, with the cell as a
(proper) frame of reference. Such an effort may well occupy
the next 200 years.
ACKNOWLEDGMENTS
The author would like to thank Maurine Neiman for critical
reading and editing of the manuscript, Malgorzata Kloc for
discussion on structural RNAs, and the University of Iowa
for support.
REFERENCES
Abu-Remaileh, M., Gerson, A., Farago, M., Nathan, G., Alkalay,
I., Rousso, S.Z., Gur, M., Fainsod, A., Bergman, Y., 2010.
Oct-3/4 regulates stem cell identity and cell fate decisions
by modulating Wnt/β-catenin signalling. EMBO J 29,
3236–3248.
Afouda, B.A., Nakamura, Y., Shaw, S., Charney, R.M., Paraiso,
K.D., Blitz, I.L., Cho, K.W.Y., Hoppler, S., 2020. Foxh1/
Nodal def nes context-specif c direct maternal Wnt/β-catenin
target gene regulation in early development. Iscience 23,
101314.
Agius, E., Wessely, O., Kemp, C., Robertis, E.M.D., 2000.
Endodermal nodal-related signals and mesoderm induction
in Xenopus. Development 127, 1173–1183.
Aguero, T., Jin, Z., Chorghade, S., Kalsotra, A., King, M.L.,
Yang, J., 2017. Maternal dead-end 1 promotes translation of
nanos1 through binding the eIF3 complex. Development 144,
dev.152611.
Aguero, T., Jin, Z., Owens, D., Malhotra, A., Newman, K., Yang,
J., King, M.L., 2018. Combined functions of two RRMs in
Dead-end1 mimic helicase activity to promote nanos1 translation in the germline. Mol Reprod Dev 85, 896–908.
Amerongen, R.V., Nawijn, M.C., Lambooij, J.-P., Proost, N.,
Jonkers, J., Berns, A., 2010. Frat oncoproteins act at the
crossroad of canonical and noncanonical Wnt-signaling
pathways. Oncogene 29, 93–104.
Ancel, P., Vintemberger, P., 1948. Recherches sur le déterminisme
de la symétrie bilatérale dans l’œuf des amphibiens. Bull.
Biol. Fr. Belg. Suppl 31, 1–182.
André, J., Rouiller, C., 1956. L’ultrastructure de la membrane
nucléaire des ovocytes del l’araignée (Tegenaria domestica
Clark). In: Proc. European Conf. Electron Microscopy. New
York: Stokholm Acad. Press. pp. 162–164.
Aslan, Y., Tadjuidje, E., Zorn, A.M., Cha, S.-W., 2017. Higheffciency non-mosaic CRISPR-mediated knock-in and indel
mutation in F0 Xenopus. Development 144, 2852–2858.
Baer, K. von, 1834. Die Metamorphose des Eies der Batrachier vor
der Erscheinung des Embryo und Folgerungen aus ihr für die
Theorie der Erzeugung. Archiv für Anatomie, Physiologie
und wissenschaftliche Medizin 481–509.
Bates, T.J.D., Vonica, A., Heasman, J., Brivanlou, A.H., Bell, E.,
2013. Coco regulates dorsoventral specifcation of germ
layers via inhibition of TGFβ signalling. Development 140,
4177–4181.
Beams, H.W., Kessel, R.G., 1974. The problem of germ cell determinants. Int Rev Cytol 39, 413–479.
Belenkaya, T.Y., Han, C., Standley, H.J., Lin, Xinda, Houston,
D.W., Heasman, J., Lin, Xinhua, 2002. Pygopus encodes
a nuclear protein essential for wingless/Wnt signaling.
Development 129, 4089–4101.
Berekelya, L.A., Mikryukov, A.A., Luchinskaya, N.N., Ponomarev,
M.B., Woodland, H.R., Belyavsky, A.V., 2007. The protein
encoded by the germ plasm RNA germes associates with
dynein light chains and functions in Xenopus germline
development. Differentiation 75, 546–558.
Berekelya, L.A., Ponomarev, M., Luchinskaya, N., Belyavsky, A.,
2003. Xenopus germes encodes a novel germ plasm-associated
transcript. Gene Expression Patterns: GEP 3, 521–524.
Betley, J.N., Frith, M.C., Graber, J.H., Choo, S., Deshler, J.O.,
2002. A ubiquitous and conserved signal for RNA localization in chordates. Current Biology 12, 1756–1761.
Bilic, J., Huang, Y.-L., Davidson, G., Zimmermann, T., Cruciat,
C.-M., Bienz, M., Niehrs, C., 2007. Wnt induces LRP6
signalosomes and promotes dishevelled-dependent LRP6
phosphorylation. Science 316, 1619–1622.
Birsoy, B., Berg, L., Williams, P.H., Smith, J.C., Wylie, C.C.,
Christian, J.L., Heasman, J., 2005. XPACE4 is a localized
pro-protein convertase required for mesoderm induction and
the cleavage of specif c TGFβ proteins in Xenopus development. Development 132, 591–602.
Birsoy, B., Kofron, M., Schaible, K., Wylie, C.C., Heasman, J.,
2006. Vg 1 is an essential signaling molecule in Xenopus
development. Development 133, 15–20.
Blythe, S.A., Cha, S.-W., Tadjuidje, E., Heasman, J., Klein, P.S.,
2010. Beta-catenin primes organizer gene expression by
recruiting a histone H3 arginine 8 methyltransferase, Prmt2.
Developmental Cell 19, 220–231.
Boke, E., Ruer, M., Wühr, M., Coughlin, M., Lemaitre, R., Gygi,
S.P., Alberti, S., Drechsel, D., Hyman, A.A., Mitchison, T.J.,
2016. Amyloid-like self-assembly of a cellular compartment.
Cell 166, 637–650.
Bontems, F., Stein, A., Marlow, F., Lyautey, J., Gupta, T., Mullins,
M.C., Dosch, R., 2009. Bucky ball organizes germ plasm
assembly in zebraf sh. Current Biology 19, 414–422.
Boterenbrood, E.C., Nieuwkoop, P.D., 1973. The formation of the
mesoderm in urodelean amphibians. Wilhelm Roux’ Archiv
für Entwicklungsmechanik der Organismen 173, 319–332.
Bounoure, L., 1934. Recherches sur la lignée germinale chez la
grenouille rousse aux premiers stades du développment. Ann
Sci Nat 17, 67–248.
Bounoure, L., 1931. Sur l’existence d’un déterminant germinal
dans l’oeuf indivis de la Grenouille rousse. CR Acad Sci
Paris 193, 402.
Bounoure, L., Aubry, R., Huck, M.L., 1954. Nouvelles recherches
experimentales sur les origines de la lignee reproductrice