Autonomous Cell Fate Specification: Overview

Abstract

Autonomous cell fate specification is a form of embryonic specification in which a developing cell is able to differentiate (become a cell carrying out a specialised function) without receiving external signals. This property is enabled by cytoplasmic determinants (cytoplasmic regulatory factors necessary for specification) that are deposited in different regions of the ovum during oogenesis. These cytoplasmic determinants are partitioned into individual cells during embryonic cleavage, and thus endow these cells with the ability to form specific cell types. If an autonomously specified cell is removed from the embryo during early development and cultured in isolation, that cell will produce the descendants that it would have normally produced in the undisturbed embryo. Frequently, the embryo from which the cell was removed lacks the structures normally made by the missing cell. Autonomous cell fate specification is often used during patterning of invertebrate embryos such as ctenophores, annelids, molluscs, echinoderms and tunicates.

Key Concepts:

  • The cytoplasm of animal eggs is heterogeneous in composition due to the asymmetric deposition of key regulatory factors termed cytoplasmic determinants.

  • In general, cytoplasmic determinants are asymmetrically distributed along the primordial axis of the ovum termed the animal–vegetal axis.

  • Most cytoplasmic determinants are maternal (produced under the control of the mother's genome) ribonucleic acids (RNAs).

  • Cytoplasmic determinants provide the necessary information for specifying embryonic cell fates.

  • When inheritance of cytoplasmic determinants by a cell is sufficient for that cell to undergo its final differentiation, it is said to undergo autonomous cell fate specification.

  • Autonomous cell fate specification is mostly seen in invertebrate embryos, but no embryo depends exclusively on this method of cell fate specification.

Keywords: autonomous; specification; cytoplasmic determinants; cell fate; embryology; invertebrates

Figure 1.

Fate maps of the sea urchin Strongylocentrotus purpuratus at (a) the 16‐cell stage and (b) the 32‐cell stage. (c) Structures of the early pluteus. (d) Specification of micromeres in the sea urchin during normal development, in isolated micromeres and in embryos where nuclear accumulation of β‐catenin is blocked.

Figure 2.

(a) Ooplasmic segregation in the tunicate Styela partita. (b) The eight‐cell stage. (c) Normal fates of isolated cell pairs from an eight‐cell stage embryo.

Figure 3.

Polar lobe formation in Ilyanassa obsoleta during cleavage (a)–(i). Note that in each case the polar lobe contents are segregated to the D cell. Later in development, the 4d cell will form most of the mesoderm in this gastropod. The trefoil stage mentioned in the article is shown in (c) and (d). (j) Structures found in the veliger larva of Ilyanassa.

Figure 4.

(a) Lineage map of germ cell formation in the nematode C. elegans. Inset shows location of the primordial germ cells in the newly hatched larva. (b) Distribution of the protein PIE‐1 (pharyngeal and intestinal excess; shown in purple) at different stages of development. At the two‐cell stage, moderate concentrations of PIE‐1 are found in both the cytoplasm and nucleus of P1. By the four‐cell stage, PIE‐1 is more concentrated in the nucleus of the P2 cell than in the cytoplasm, and by the 8‐ to 12‐cell stage high concentrations of PIE‐1 are localised to the nucleus of P3. Ant., anterior; post., posterior.

Figure 5.

Early development of the ctenophore Mnemiopsis leidyi, and experimental analysis of cell fate specification (a)–(d). (a) The site of polar body release in the zygote marks the oral pole of the embryo. (b) The lateral view of the eight‐cell stage embryo where the E and M lineages are generated. (c) The lateral view of the 16‐cell stage embryo showing the e1 and m1 micromeres and the 1E and 1M macromeres. (d) Lateral view of the mid‐gastrula stage embryo showing the migration of the ectodermal cells (blue) via epiboly towards the oral pole. Large macromeres (yellow) give rise to the endoderm and the oral micromeres (red) that give rise to the mesoderm are produced at the oral pole of the embryo. Blastomere isolation and deletion studies of the early ctenophore embryo (f)–(j). (f) Each isolated E macromere of the eight‐cell stage embryo gives rise to a partial larva with two ctene rows. (g) Isolated M macromeres of the eight‐cell stage embryo gives rise to a partial larva with no ctene rows. (h) Isolation of 1E and 2M blastomeres together results in larvae with two ctene rows and (i) isolation of 2E and 1M blastomeres together gives rise to larvae with four ctene rows. (j) Deleting two adjacent e1 micromeres at the 16‐cell stage results in the loss of both ctene rows and the endodermal canals on the side from which the micromeres are deleted. Also, the tentacle on that side is highly reduced.

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References

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Further Reading

Davidson EH (1990) How embryos work: a comparative view of diverse modes of cell fate specification. Development 108: 365–389.

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Kalthoff K (2001b) Experimental and genetic analysis of Caenorhabditis elegans development. In: Analysis of Biological Development, 2nd edn, pp. 666–690. New York: McGraw‐Hill.

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Byrum, Christine A, Wijesena, Naveen M, and Wikramanayake, Athula H(Aug 2012) Autonomous Cell Fate Specification: Overview. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0001148.pub3]