Skip to main content
Log in

Distinct embryotoxic effects of lithium appeared in a new assessment model of the sea urchin: the whole embryo assay and the blastomere culture assay

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Early embryogenesis is one of the most sensitive and critical stages in animal development. Here we propose a new assessment model on the effect of pollutant to multicellular organism development. That is a comparison between the whole embryo assay and the blastomere culture assay. We examined the LiCl effect on the sea urchin early development in both of whole embryos and the culture of isolated blastomeres. The mesoderm and endoderm region were capable to differentiate into skeletogenic cells when they were isolated at 60-cell stage and cultured in vitro. The embryo developed to exogastrula by the vegetalizing effect of the same LiCl condition where ectodermal region changed their fate to endoderm, while the isolated blastomeres from the presumptive ectoderm region differentiated into skeletogenic cells in the culture with LiCl. The effect of LiCl to the sea urchin embryo and to the dissociated blastomere is a unique example where same cells response distinctly to the same agent depend on the condition around them. Present results show the importance of examining the process in cellular and tissue levels for the exact understanding on the morphological effect of chemicals and metals.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Aral H, Vecchio-Sadus A (2008) Toxicity of lithium to humans and the environment–a literature review. Ecotoxicol Environ Saf 70:349–356. doi:10.1016/j.ecoenv.2008.02.026

    Article  CAS  Google Scholar 

  • Duboc V, Röttinger E, Besnardeau L, Lepage T (2004) Nodal and BMP2/4 signaling organizes the oral-aboral axis of the sea urchin embryo. Dev Cell 6:397–410. doi:10.1016/S1534-5807(04)00056-5

    Article  CAS  Google Scholar 

  • Ettensohn CA, McClay DR (1988) Cell lineage conversion in the sea urchin embryo. Dev Biol 125:396–409

    Article  CAS  Google Scholar 

  • Ettensohn CA, Kitazawa C, Cheers MS, Leonard JD, Sharma T (2007) Gene regulatory networks and developmental plasticity in the early sea urchin embryo: alternative deployment of the skeletogenic gene regulatory network. Development 134:3077–3087. doi:10.1242/dev.009092

    Article  CAS  Google Scholar 

  • Fernández N, Cesar A, Salamanca MJ, DelValls TA (2006) Toxicological characterisation of the aqueous soluble phase of the Prestige fuel-oil using the sea-urchin embryo bioassay. Ecotoxicology 15:593–599. doi:10.1007/s10646-006-0096-y

    Article  Google Scholar 

  • Fukushi T (1962) The fate of isolated blastoderm cells of sea urchin blastulae and gastrulae into the blastocoel. Bull Mar Biol Stat Asamushi 11:21–30

    Google Scholar 

  • Hall TS (1942) The mode of action of lithium salts in amphibian development. J Exp Zool 89:1–30. doi:10.1002/jez.1400890102

    Article  CAS  Google Scholar 

  • Hamada M, Kiyomoto M (2003) Signals from primary mesenchyme cells regulate endoderm differentiation in the sea urchin embryo. Dev Growth Differ 45:339–350. doi:10.1046/j.1440-169X.2003.00702.x

    Article  Google Scholar 

  • Hardin JD, Cheng LY (1986) The mechanisms and mechanics of archenteron elongation during sea urchin gastrulation. Dev Biol 115:490–501. doi:10.1016/0012-1606(86)90269-1

    Article  Google Scholar 

  • Herbst C (1892) Experimentelle untersuchungen uber den einfluss der veranderten chemischen zusammensetzung des umgebenden MEDIUMS auf die entwicklung der tiere I. Teil. Versuche an seeigeleiern. Z Wiss Zool 55:446–518

    Google Scholar 

  • Hörstadius S (1973) Experimental embryology of echinoderms. Oxford Univ Press, London

    Google Scholar 

  • Kao KR, Masui Y, Elinson RP (1986) Lithium-induced respecification of pattern in Xenopus laevis embryos. Nature 322:371–373. doi:10.1038/322371a0

    Article  CAS  Google Scholar 

  • Khaner O, Wilt F (1990) The influence of cell interactions and tissue mass on differentiation of sea urchin mesomeres. Development 109:625–634

    CAS  Google Scholar 

  • Khaner O, Wilt F (1991) Interactions of different vegetal cells with mesomeres during early stages of sea urchin development. Development 112:881–890

    CAS  Google Scholar 

  • Kitamura K, Nishimura Y, Kubotera N, Higuchi Y, Yamaguchi M (2002) Transient activation of the micro1 homeobox gene family in the sea urchin (Hemicentrotus pulcherrimus) micromere. Dev Genes Evol 212:1–10. doi:10.1007/s00427-001-0202-3

    Article  CAS  Google Scholar 

  • Kiyomoto M, Tsukahara J (1991) Spicule formation-inducing substance in sea urchin embryo. Dev Growth Differ 33:443–450. doi:10.1111/j.1440-169X.1991.00443.x

    Article  Google Scholar 

  • Kiyomoto M, Kikuchi A, Unuma T, Yokota Y (2006) Effects of ethynylestradiol and bisphenol a on the development of sea urchin embryos and juveniles. Mar Biol 149:57–63. doi:10.1007/s00227-005-0208-x

    Article  CAS  Google Scholar 

  • Kiyomoto M, Kikuchi A, Morinaga S, Unuma T, Yokota Y (2008) Exogastrulation and interference with the expression of major yolk protein by estrogens administered to sea urchins. Cell Biol Toxicol 24:611–620. doi:10.1007/s10565-008-9073-y

    Article  CAS  Google Scholar 

  • Klein PS, Melton DA (1996) A molecular mechanism for the effect of lithium on development. Proc Natl Acad Sci USA 93:8455–8459

    Article  CAS  Google Scholar 

  • Kobayashi N (1991) Marine pollution bioassay by using sea urchin eggs in the Tanabe Bay, wakayama prefecture, Japan, 1970–1987. Mar Poll Bull 23:709–713. doi:10.1016/0025-326X(91)90765-K

    Article  Google Scholar 

  • Kobayashi N, Okamura H (2004) Effects of heavy metals on sea urchin embryo development 1. Tracing the cause by the effects. Chemosphere 55:1403–1412. doi:10.1016/j.chemosphere.2003.11.052

    Article  CAS  Google Scholar 

  • Kobayashi N, Okamura H (2005) Effects of heavy metals on sea urchin embryo development. Part 2. Interactive toxic effects of heavy metals in synthetic mine effluents. Chemosphere 61:1198–1203. doi:10.1016/j.chemosphere.2005.02.071

    Article  CAS  Google Scholar 

  • Kominami T, Takaichi M (1998) Unequal divisions at the third cleavage increase the number of primary mesenchyme cells in sea urchin embryos. Dev Growth Differ 40:545–553. doi:10.1046/j.1440-169X.1998.t01-3-00009.x

    Article  CAS  Google Scholar 

  • Komukai M, Iizuka Y, Yasumasu I (1989) Synthesis of protein enriched in Li +-induced vegetalized embryos of sea urchin during early development. Dev Growth Differ 31:371–378. doi:10.1111/j.1440-169X.1989.00371.x

    Article  CAS  Google Scholar 

  • Kszos LA, Stewart AJ (2003) Review of Lithium in the aquatic environment: distribution in the United States, toxicity and case example of groundwater contamination. Ecotoxicology 12:439–447. doi:10.1023/A:1026112507664

    Article  CAS  Google Scholar 

  • Livingston BT, Wilt FH (1989) Lithium evokes expression of vegetal-specific molecules in the animal blastomeres of sea urchin embryos. Proc Natl Acad Sci U S A 86:3669–3673

    Article  CAS  Google Scholar 

  • Livingston BT, Wilt FH (1990) Range and stability of cell fate determination in isolated sea urchin blastomeres. Development 108:403–410

    CAS  Google Scholar 

  • Logan CY, Miller JR, Ferkowiez MJ, McClay DR (1999) Nuclear beta-catenin is required to specify vegetal cell fates in the sea urchin embryo. Development 126:345–357

    CAS  Google Scholar 

  • Mwatibo JM, Green JD (1998) Estradiol disrupts sea urchin embryogenesis differently from methoxychlor. Bull Environ Contam Toxicol 61:577–582

    Article  CAS  Google Scholar 

  • Nocente-McGrath C, McIsaac R, Ernst SG (1991) Altered cell fate in LiCl-treated sea urchin embryos. Dev Biol 147:445–450. doi:10.1016/0012-1606(91)90302-J

    Article  CAS  Google Scholar 

  • Okazaki K (1975) Spicule formation by isolated micromeres of the sea urchin embryo. Am Zool 15:567–581

    Google Scholar 

  • Oliveri P, Carrick DM, Davidson EH (2002) A regulatory gene network that directs micromere specification in the sea urchin embryo. Dev Biol 246:209–228. doi:10.1006/dbio.2002.0627

    Article  CAS  Google Scholar 

  • Oliveri P, Davidson EH, McClay DR (2003) Activation of pmar1 controls specification of micromeres in the sea urchin embryo. Dev Biol 258:32–43. doi:10.1016/S0012-1606(03)00108-8

    Article  CAS  Google Scholar 

  • Phiel CJ, Klein PS (2001) Molecular targets of lithium action. Annu Rev Pharmacol Toxicol 41:789–813. doi:10.1146/annurev.pharmtox.41.1.789

    Article  CAS  Google Scholar 

  • Pillai MC, Vines CA, Wikramanayake AH, Cherr GN (2003) Polycyclic aromatic hydrocarbons disrupt axial development in sea urchin embryos through a b-catenin dependent pathway. Toxicology 186:93–108. doi:10.1016/S0300-483X(02)00695-9

    Article  CAS  Google Scholar 

  • Pinsino A, Matranga V, Trinchella F, Roccheri MC (2009) Sea urchin embryos as an in vivo model for the assessment of manganese toxicity: developmental and stress response effects. Ecotoxicology (in press). doi:10.1007/s10646-009-0432-0

  • Revilla-i-Domingo R, Oliveri P, Davidson EH (2007) A missing link in the sea urchin embryo gene regulatory network: hesC and the double-negative specification of micromeres. Proc Natl Acad Sci USA 104:12383–12388. doi:10.1073/pnas.0705324104

    Article  CAS  Google Scholar 

  • Salamanca MJ, Fernández N, Cesar A, Antón R, Lopez P, Delvalls A (2009) Improved sea-urchin embryo bioassay for in situ evaluation of dredged material. Ecotoxicology 18:1051–1057. doi:10.1007/s10646-009-0378-2

    Article  CAS  Google Scholar 

  • Shimizu K, Noro N, Matsuda R (1988) Micromere differentiation in the sea urchin embryo: expression of primary mesenchyme cell specific antigen during development. Dev Growth Differ 30:35–47. doi:10.1111/j.1440-169X.1988.00035.x

    Article  Google Scholar 

  • Shimizu-Nishikawa K, Katow H, Matsuda R (1990) Micromere differentiation in the sea urchin embryo; immunochemical characterization of primary mesenchyme cell-specific antigen and its biological roles. Dev Growth Differ 32:629–636. doi:10.1111/j.1440-169X.1990.00629.x

    Article  CAS  Google Scholar 

  • Stachel SE, Grunwald DJ, Myers PZ (1993) Lithium perturbation and goosecoid expression identify a dorsal specification pathway in the pregastrula zebrafish. Development 117:1261–1274

    CAS  Google Scholar 

  • Stephens L, Kitajima T, Wilt F (1989) Autonomous expression of tissue-specific genes in dissociated sea urchin embryos. Development 107:299–307

    CAS  Google Scholar 

  • Sweet HC, Gehring M, Ettensohn CA (2002) LvDelta is a mesoderm-inducing signal in the sea urchin embryo and can endow blastomeres with organizer-like properties. Development 129:1945–1955

    CAS  Google Scholar 

  • Sweet H, Amemiya S, Ransick A, Minokawa T, McClay DR, Wikramanayake A, Kuraishi R, Kiyomoto M, Nishida H, Henry J (2004) Blastomere isolation and transplantation. Methods Cell Biol 74:243–271

    Article  Google Scholar 

  • Wikramanayake AH, Huang L, Klein WH (1998) Catenin is essential for patterning the maternally specified animal-vegetal axi in the sea urchin embryo. Proc Natl Acad Sci USA 95:9343–9348

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Mr Mamoru Yamaguchi (Tateyama Marine Laboratory, Marine and Coastal Research Center, Ochanomizu University) for the animal collections and Dr Hideki Katow (Tohoku University) for providing PMC-specific antibody.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Masato Kiyomoto.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kiyomoto, M., Morinaga, S. & Ooi, N. Distinct embryotoxic effects of lithium appeared in a new assessment model of the sea urchin: the whole embryo assay and the blastomere culture assay. Ecotoxicology 19, 563–570 (2010). https://doi.org/10.1007/s10646-009-0452-9

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-009-0452-9

Keywords