Letter | Published:

Asymmetric inheritance of centrosomally localized mRNAs during embryonic cleavages

Abstract

During development, different cell fates are generated by cell–cell interactions or by the asymmetric distribution of patterning molecules. Asymmetric inheritance is known to occur either through directed transport along actin microfilaments into one daughter cell1,2 or through capture of determinants by a region of the cortex inherited by one daughter3,4,5. Here we report a third mechanism of asymmetric inheritance in a mollusc embryo. Different messenger RNAs associate with centrosomes in different cells and are subsequently distributed asymmetrically during division. The segregated mRNAs are diffusely distributed in the cytoplasm and then localize, in a microtubule-dependent manner, to the pericentriolar matrix. During division, they dissociate from the core mitotic centrosome and move by means of actin filaments to the presumptive animal daughter cell cortex. In experimental cells with two interphase centrosomes, mRNAs accumulate on the correct centrosome, indicating that differences between centrosomes control mRNA targeting. Blocking the accumulation of mRNAs on the centrosome shows that this event is required for subsequent cortical localization. These events produce a complex pattern of mRNA localization, in which different messages distinguish groups of cells with the same birth order rank and similar developmental potentials.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1

    Takizawa, P. A., Sil, A., Swedlow, J. R., Herskowitz, I. & Vale, R. D. Actin-dependent localization of an RNA encoding a cell-fate determinant in yeast. Nature 389, 90–93 (1997)

  2. 2

    Long, R. M. et al. Mating type switching in yeast controlled by asymmetric localization of ASH1 mRNA. Science 277, 383–387 (1997)

  3. 3

    Spana, E. P. & Doe, C. Q. The Prospero transcription factor is asymmetrically localized to the cell cortex during neuroblast mitosis in Drosophila. Development 121, 3187–3195 (1995)

  4. 4

    Boyd, L., Guo, S., Levitan, D., Stinchcomb, D. T. & Kemphues, K. J. PAR-2 is asymmetrically distributed and promotes association of P granules and PAR-1 with the cortex in C. elegans embryos. Development 122, 3075–3084 (1996)

  5. 5

    Lu, B. W., Ackerman, L., Jan, L. Y. & Jan, Y. N. Modes of protein movement that lead to the asymmetric localization of partner of numb during Drosophila neuroblast division. Mol. Cell 4, 883–891 (1999)

  6. 6

    Crampton, H. E. Experimental studies on gastropod development. Roux's Arch. EntwMech. Org. 3, 1–19 (1896)

  7. 7

    Clement, A. C. Experimental studies on germinal localization in Ilyanassa. I. The role of the polar lobe in determination of the cleavage pattern and its influence in later development. J. Exp. Zool. 132, 427–446 (1952)

  8. 8

    Wilson, E. B. Experimental studies in germinal localization. II Experiments on the cleavage-mosaic in patella and dentalium. J. Exp. Zool. 1, 197–268 (1904)

  9. 9

    Clement, A. C. Development of Ilyanassa following the removal of the D macromere at successive cleavage stages. J. Exp. Zool. 149, 193–216 (1962)

  10. 10

    Macdonald, P. M., Ingham, P. & Struhl, G. Isolation, structure, and expression of even-skipped—a 2nd pair-rule gene of Drosophila containing a homeo box. Cell 47, 721–734 (1986)

  11. 11

    Wharton, K. A., Ray, R. P. & Gelbart, W. M. An activity gradient of Decapentaplegic is necessary for the specification of dorsal pattern elements in the Drosophila embryo. Development 117, 807–822 (1993)

  12. 12

    Holley, S. A. et al. A conserved system for dorsal–ventral patterning in insects and vertebrates involving Sog and Chordin. Nature 376, 249–253 (1995)

  13. 13

    Shimell, M. J., Ferguson, E. L., Childs, S. R. & Oconnor, M. B. The Drosophila dorsal–ventral patterning gene Tolloid is related to human bone morphogenetic protein-1. Cell 67, 469–481 (1991)

  14. 14

    Clement, A. C. Cell determination and organogenesis in molluscan development—reappraisal based on deletion experiments in Ilyanassa. Am. Zool. 16, 447–453 (1976)

  15. 15

    Render, J. Cell fate maps in the Ilyanassa obsoleta embryo beyond the third division. Dev. Biol. 189, 301–310 (1997)

  16. 16

    Sweet, H. C. Specification of first quartet micromeres in Ilyanassa involves inherited factors and position with respect to the inducing D macromere. Development 125, 4033–4044 (1998)

  17. 17

    Yoshida, S., Marikawa, Y. & Satoh, N. posterior end mark, a novel maternal gene encoding a localized factor in the ascidian embryo. Development 122, 2005–2012 (1996)

  18. 18

    Nishikata, T., Hibino, T. & Nishida, H. 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 (1999)

  19. 19

    Mello, C. C. et al. The PIE-1 protein and germline specification in C. elegans embryos. Nature 382, 710–712 (1996)

  20. 20

    Reese, K. J., Dunn, M. A., Waddle, J. A. & Seydoux, G. Asymmetric segregation of PIE-1 in C. elegans is mediated by two complementary mechanisms that act through separate PIE-1 protein domains. Mol. Cell 6, 445–455 (2000)

  21. 21

    Wu, X. Y. & Palazzo, R. E. Differential regulation of maternal vs. paternal centrosomes. Proc. Natl Acad. Sci. USA 96, 1397–1402 (1999)

  22. 22

    Bonaccorsi, S., Giansanti, M. G. & Gatti, M. Spindle assembly in Drosophila neuroblasts and ganglion mother cells. Nature Cell Biol. 2, 54–56 (2000)

  23. 23

    Piel, M., Meyer, P., Khodjakov, A., Rieder, C. L. & Bornens, M. The respective contributions of the mother and daughter centrioles to centrosome activity and behavior in vertebrate cells. J. Cell Biol. 149, 317–329 (2000)

  24. 24

    Conklin, E. G. Karyokinesis and cytokinesis in the maturation, fertilization and cleavage of Crepidula and other gasteropoda. J. Acad. Nat. Sci. Philadelphia Ser. 2 12, 1–21 (1902)

  25. 25

    Goto, S. & Hayashi, S. Cell migration within the embryonic limb primordium of Drosophila as revealed by a novel fluorescence method to visualize mRNA and protein. Dev. Genes Evol. 207, 194–198 (1997)

  26. 26

    Sanders, M. A. & Salisbury, J. L. Centrin plays an essential role in microtubule severing during flagellar excision in Chlamydomonas reinhardtii. J. Cell Biol. 124, 795–805 (1994)

  27. 27

    Paoletti, A., Moudjou, M., Paintrand, M., Salisbury, J. L. & Bornens, M. Most of centrin in animal cells is not centrosome-associated and centrosomal centrin is confined to the distal lumen of centrioles. J. Cell Sci. 109, 3089–3102 (1996)

  28. 28

    Lambert, J. D. & Nagy, L. M. MAPK signaling by the D quadrant embryonic organizer of the mollusc Ilyanassa obsoleta. Development 128, 45–56 (2001)

Download references

Acknowledgements

We thank J. Cooley, D. Bentley and J. Wandelt for technical help; J. Salisbury and G. Hermann for antibodies; D. Brower, C. Gregorio and G. Von Dassow for critically reading the manuscript; and R. Palazzo, M. Goulding, G. Lambert, E. Wilk and M. Gibson for technical advice and discussions. This work was supported by an National Science Foundation (NSF) Graduate Research Fellowship and an NSF Doctoral Dissertation Improvement Grant to J.D.L., and a grant from the NSF to L.M.N.

Author information

Correspondence to Lisa M. Nagy.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Rights and permissions

Reprints and Permissions

About this article

Further reading

Figure 1: Diagram of Ilyanassa cleavage and patterns of centrosomally localized mRNA.
Figure 2: Localization of mRNAs to the centrosome and mRNA dynamics during cleavage.
Figure 3: Cytoskeletal basis of mRNA localization.
Figure 4: mRNAs are localized to specific subsets of cells during cleavage, and mRNAs are specifically targeted to particular centrosomes.

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.