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Articles

Effects of magnesium deprivation on development and biomineralization in the sea urchin Arbacia lixula

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Pages 165-176 | Received 14 Jan 2019, Accepted 22 Apr 2019, Published online: 03 May 2019

References

  • Addadi L, Raz S, Weiner S. 2003. Taking advantage of disorder: amorphous calcium carbonate and its roles in biomineralization. Adv Mater. 15:959–970. doi:10.1002/adma.200300381
  • Albeck S, Aizenberg J, Addadi L, Weiner S. 1993. Interactions of various skeletal intracrystalline components with calcite crystals. J Am Chem Soc. 115:11691–11697.
  • Andersson AJ, Mackenzie FT, Bates NR. 2008. Life on the margin: implications of ocean acidification on Mg- calcite, high latitude and cold-water marine calcifiers. Mar Ecol Prog Ser. 373:265−273. doi:10.3354/meps07639
  • Anselmo HMR, Koerting L, Devito S, van Den Berg JHJ, Dubbeldam M, Kwadijk C, Murk AJ. 2011. Early life developmental effects of marine persistent organic pollutants on the sea urchin Psammechinus miliaris. Ecotox Environm Saf. 74:2182–2192. doi:10.1016/j.ecoenv.2011.07.037
  • Anstrom JA, Chin JE, Leaf DS, Parks AL, Raff RA. 1987. Localization and expression of msp130, a primary mesenchyme lineage-specific cell surface protein in the sea urchin embryo. Development. 101:255–265.
  • Arnone MI, Byrne M, Martinez P. 2015. Echinodermata. In: Wanninger A, editor. Evolutionary developmental biology of invertebrates 6 deuterostomia. New York: Springer; p. 1–58.
  • Beniash E, Aizenberg J, Addadi L, Weiner S. 1997. Amorphous calcium carbonate transforms into calcite during sea urchin larval spicule growth. Proc Roy Soc Lond Ser B. 264:461–465.
  • Borremans C, Hermans J, Baillon S, André L, Dubois P. 2009. Salinity effects on the Mg/Ca and Sr/Ca in starfish skeletons and the echinoderm relevance for paleoenvironmental reconstructions. Geology. 37(4):351–354. doi:10.1130/G25411A.
  • Byrne M. 2011. Impact of ocean warming and ocean acidification on marine invertebrate life history stages: vulnerabilities and potential for persistence in a changing ocean. Oceanogr Mar Biol Annu Rev. 49:1–42.
  • Byrne M, Lamare M, Winter D, Dworjanyn SA, Uthicke S. 2013. The stunting effect of a high CO2 ocean on calcification and development in sea urchin larvae, a synthesis from the tropics to the poles. Phil Trans R Soc B. 368:20120439.
  • Cavanaugh GM. 1956. Formulae and methods VI of the marine biological laboratory chemical room. Woods Hole (MA, USA): Marine Biological Laboratory.
  • Chave KE. 1954. Aspects of the biogeochemistry of magnesium. Calcareous marine organisms. J Geol. 62:266–283.
  • Chiarelli R, Martino C, Agnello M, Bosco L, Roccheri MC. 2016. Autophagy as a defense strategy against stress: focus on Paracentrotus lividus sea urchin embryos exposed to cadmium. Cell Stress Chaperones. 21(1):19–27. doi:10.1007/s12192-015-0639-3.
  • Costa C, Karakostis K, Zito F, Matranga V. 2012. Phylogenetic analysis and expression patterns of p16 and p19 in Paracentrotus lividus embryos. Dev Genes Evol. 222(4):245–251. doi:10.1007/s00427-012-0405-9.
  • Dubois P. 2014. The skeleton of postmetamorphic echinoderms in a changing world. Biol Bull. 226(3):223–236. doi:10.1086/BBLv226n3p223.
  • Ebert TA. 2013. Growth and survival of postsettlement sea urchins. In: Lawrence JM, editor. Sea urchins: biology and ecology, 3rd (Vol. 38). Amsterdam: Elsevier; p. 83–117.
  • Findlay HS, Wood H, Kendall MA, Spicer JI, Twitchett RJ, Widdicombe S. 2009. Calcification, a physiological process to be considered in the context of the whole organism. Biogeosci Discuss. 6:2267−2284.
  • Fitzer SC, Zhu W, Tanner KE, Phoenix VR, Kamenos NA, Cusack M. 2015. Ocean acidification alters the material properties of Mytilus edulis shells. J R Soc Interface. 12(103):pii: 20141227. doi:10.1098/rsif.2014.1227.
  • Fujino Y, Mitsunaga K, Yasumasu I. 1987. Development of sea urchin embryos in artificial sea water containing Br- in place of Cl-. Dev Growth Differ. 6:599–605.
  • Gibson AW, Burke RD. 1987. Migratory and invasive behavior of pigment cells in normal and animalized sea urchin embryos. Exp Cell Res. 173:546–557.
  • Guss KA, Ettensohn CA. 1997. Skeletal morphogenesis in the sea urchin embryo: regulation of primary mesenchyme gene expression and skeletal rod growth by ectoderm-derived cues. Development. 124:1899–1908.
  • Hasiuk FJ, Lohmann KC. 2010. Application of calcite Mg partitioning functions to the reconstruction of paleocean Mg/Ca. Geochim Cosmochim Acta. 74:6751–6763.
  • Herbst C. 1897. Über die zur Entwicklung der Seeigellarven notwendigen anorganischen Stoffe, ihre Rolle und ihre Vertretbarkeit. I. Arch EntwMech Org. 5:649–793.
  • Herbst C. 1904. Über die zur Entwicklung der Seeigellarven notwendigen anorganischen Stoffe, ihre Rolle und ihre Vertretbarkeit. III. Theil. Die Rolle der notwendigen anorganischen Stoffe. Arch EntwMech Org. 17:306–520.
  • Hermans J, André L, Navez J, Pernet P, Dubois P. 2011. Relative influences of solution composition and presence of intracrystalline proteins on magnesium incorporation in calcium carbonate minerals: insight into vital effects. J Geophys Res. 116:G01001. doi:10.1029/2010JG001487
  • Hermans J, Borremans C, Willenz P, André L, Dubois P. 2010. Temperature, salinity and growth rate dependences of Mg/Ca and Sr/Ca ratios of the skeleton of the sea urchin Paracentrotus lividus (Lamarck): an experimental approach. Mar Biol. 157:1293–1300. doi:10.1007/s00227-010-1409-5
  • Hetzinger S, Halfarc J, Kronzd A, Simond K, Adeye WH, Steneck RS. 2018. Reproducibility of Clathromorphum compactum coralline algal Mg/Ca ratios and comparison to high-resolution sea surface temperature data. Geochim Cosmochim Acta. 220:96–109. doi:10.1016/j.gca.2017.09.044
  • Hodor PG, Ettensohn CA. 1998. The dynamics and regulation of mesenchymal cell fusion in the sea urchin embryo. Dev Biol. 199:111–124.
  • Iglikowska A, Najorka J, Voronkov A, Chełchowski M, Kukliński P. 2017. Variability in magnesium content in Arctic echinoderm skeletons. Mar Environ Res. 129:207–218. doi:10.1016/j.marenvres.2017.06.002
  • Kanold JM, Lemloh ML, Schwendt P, Burghard Z, Baier J, Herbst F, Bill J, Marin F, Brümmer F. 2015. In vivo enrichment of magnesium ions modifies sea urchin spicule properties. Bioinspir Biomim Nan. 4(2):111–120. doi:10.1680/bbn.14.00023.
  • Karakostis K, Zanella-Cléon I, Immel F, Guichard N, Dru P, Lepage T, Plasseraud L, Matranga V, Marin F. 2016. A minimal molecular toolkit for mineral deposition? Biochemistry and proteomics of the test matrix of adult specimens of the sea urchin Paracentrotus lividus. J Proteomics. 136:133–144. doi:10.1016/j.jprot.2016.01.001
  • Leaf DS, Anstrom JA, Chin JE, Harkey MA. 1987. Antibodies to a fusion protein identify a cDNA clone encoding msp130, a primary mesenchyme-specific cell surface protein of the sea urchin embryo. Dev Biol. 121:29–40.
  • Lemloh ML, Burghard Z, Forien JP, Bill J, Brümmer F. 2013. Low Mg/Ca ratio alters material properties in sea urchin larvae skeleton. Bioinspir Biomim Nan. 2:28–34. doi:10.1680/bbn.12.00016
  • Livingston BT, Killian CE, Wilt F, Cameron A, Landrum MJ, Ermolaeva O, Sapojnikov V, Maglott DR, Buchanan AM, Ettensohn CA. 2006. A genome-wide analysis of biomineralization-related proteins in the sea urchin Strongylocentrotus purpuratus. Dev Biol. 300:335–348.
  • Loste E, Wilson RM, Seshadri R, Meldrum FC. 2003. The role of magnesium in stabilizing amorphous calcium carbonate and controlling calcite morphologies. J Cryst Growth. 254:206–218. doi:10.1016/S0022-0248(03)01153-9
  • Maisano M, Cappello T, Catanese E, Vitale V, Natalotto A, Giannetto A, Barreca D, Brunelli E, Mauceri A, Fasulo S. 2015. Developmental abnormalities and neurotoxicological effects of CuO NPs on the black sea urchin Arbacia lixula by embryotoxicity assay. Mar Environ Res. 111:121–127. doi:10.1016/j.marenvres.2015.05.010
  • Martino C, Bonaventura R, Byrne M, Roccheri MC, Matranga V. 2017a. Effects of exposure to gadolinium on the development of geographically and phylogenetically distant sea urchins species. Mar Environ Res. 128:98–106. doi:10.1016/j.marenvres.2016.06.001
  • Martino C, Chiarelli R, Bosco L, Roccheri MC. 2017b. Induction of skeletal abnormalities and autophagy in Paracentrotus lividus sea urchin embryos exposed to gadolinium. Mar Environ Res. 130:12–20. doi:10.1016/j.marenvres.2017.07.007
  • Martino C, Costa C, Roccheri MC, Koop D, Scudiero R, Byrne M. 2018. Gadolinium toxicity perturbs expression of skeletogenic genes, calcium uptake and larval development in phylogenetically distant sea urchin species. Aquat Toxicol. 194:57–66. doi:10.1016/j.aquatox.2017.11.004
  • Matranga V, Bonaventura R, Costa C, Karakostis K, Pinsino A, Russo R, Zito F. 2011. Echinoderms as blueprints for biocalcification: regulation of skeletogenic genes and matrices. Prog Mol Subcell Biol. 52:225–248. doi:10.1007/978-3-642-21230-7_8
  • Matranga V, Pinsino A, Bonaventura R, Costa C, Karakostis K, Martino C, Russo R, Zito F. 2013. Cellular and molecular bases of biomineralization in sea urchin embryos. Cah Biol Mar. 54:467–478.
  • Matranga V, Zito F, Costa C, Bonaventura R, Giarrusso R, Celi F. 2010. Embryonic development and skeletogenic gene expression affected by X-rays in the mediterranean sea urchin Paracentrotus lividus. Ecotoxicology. 19:530–537. doi:10.1007/s10646-009-0444-9
  • McIntyre DC, Lyons DC, Martik M, McClay DR. 2014. Branching out: origins of the sea urchin larval skeleton in development and evolution. Genesis. 52:173–185.
  • Morse JW, Andersson AJ, Mackenzie FT. 2006. Initial responses of carbonate-rich shelf sediments to rising atmospheric pCO2 and ‘ocean acidification’: role of high Mg-calcites. Geochim Cosmochim Acta. 70:5814−5830.
  • Okazaki K. 1962. Skeleton formation of sea urchin larvae. IV. Correlation in shape of spicule and matrix. Embryologia. 7:21–38.
  • Okazaki K. 1975. Spicule formation by isolated micromeres of the sea urchin embryo. Am Zool. 15:567–581.
  • Okazaki K, Inoue S. 1976. Crystal property of the larval sea urchin spicule. Dev Growth Differ. 18:413–434.
  • Oliveri P, Tu Q, Davidson EH. 2008. Global regulatory logic for specification of an embryonic cell lineage. Proc Natl Acad Sci USA. 105:5955–5962. doi:10.1073/pnas.0711220105
  • Pinsino A, Roccheri MC, Costa C, Matranga V. 2011. Manganese interferes with calcium, perturbs ERK signaling, and produces embryos with no skeleton. Toxicol Sci. 123:217–230. doi:10.1093/toxsci/kfr152
  • Raz S, Hamilton PC, Wilt FH, Weiner S, Addadi L. 2003. The transient phase of amorphous calcium carbonate in sea urchin larval spicules: the involvement of proteins and magnesium ions in its formation and stabilization. Adv Mater. 13:480–486. doi:10.1002/adfm.200304285
  • Ries JB. 2004. Effect of ambient Mg/Ca ratio on Mg fractionation in calcareous marine invertebrates: a record of the oceanic Mg/Ca ratio over the Phanerozoic. Geology. 32:981−984.
  • Romani A. 2014. Magnesium in health and disease. Berlin, Germany: Springer Science and Business Media Dordrecht.
  • Smith AM, Clark DE, Lamare MD, Winter DJ, Byrne M. 2016. Risk and resilience: variations in magnesium in echinoid skeletal calcite. Mar Ecol Prog Ser. 561:1–16. doi:10.3354/meps11908
  • Smith LC, Ghosh J, Buckley KM, Clow LA, Dheilly NM, Haug T, Henson JH, Li C, Lun CM, Majeske AJ, et al. 2010. Echinoderm immunity. Adv Exp Med Biol. 708:260–301.
  • Solek CM, Oliveri P, Loza-Coll M, Schrankel CS, Ho EC, Wang G, Rast JP. 2013. An ancient role for Gata-1/2/3 and Scl transcription factor homologs in the development of immunocytes. Dev Biol. 382:280–292. doi:10.1016/j.ydbio.2013.06.019
  • Stanley SM. 2006. Influence of seawater chemistry on biomineralization throughout phanerozoic time: paleontological and experimental evidence. Palaeogeogr Palaeoclimatol Palaeoecol. 232:214–236. doi:10.1016/j.palaeo.2005.12.010
  • Tellis M, Lauer MM, Nadella S, Bianchini A, Wood CM. 2013. Ionic status, calcium uptake, and Ca2+-ATPase activity during early development in the purple sea urchin (Strongylocentrotus purpuratus). Comp Biochem Physiol A Mol Integr Physiol. 166:272–277. doi:10.1016/j.cbpa.2013.05.028
  • Weber JN. 1969. The incorporation of magnesium into the skeletal calcites of echinoderms. Am J Sci. 267:537–566.
  • Weiner S, Levi-Kalisman Y, Raz S, Addadi L. 2003. Biologically formed amorphous calcium carbonate. Connect Tissue Res. 44(1):214–218.
  • Wilt FH. 2002. Biomineralization of the Spicules of Sea Urchin Embryos. Zool Sci. 19(3):253–261. doi:10.2108/zsj.19.253.
  • Wilt FH. 2005. Developmental biology meets materials science: morphogenesis of biomineralized structures. Dev Biol. 280:15–25. doi:10.1016/j.ydbio.2005.01.019
  • Zito F, Koop D, Byrne M, Matranga V. 2015. Carbonic anhydrase inhibition blocks skeletogenesis and echinochrome production in Paracentrotus lividus and Heliocidaris tuberculata embryos and larvae. Dev Growth Differ. 57(7):507–514. doi:10.1111/dgd.12229.
  • Zito F, Matranga V. 2009. Secondary mesenchyme cells as potential stem cells of the sea urchin embryo. In: Rinkevich B, Matranga V, editors. Stem cells in marine organisms. Netherlands: Springer; p. 187–213.

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