Manganese interferes with calcium, perturbs ERK signaling, and produces embryos with no skeleton

Toxicological Sciences

Volumn 123, Issue 1, 2011, Pages 217-230

  Pinsino, Annalisa ^a,b   Roccheri, Maria Carmela ^a   Costa, Caterina ^b   Matranga, Valeria ^b  

^a UNIVERSITY OF PALERMO   (Italy)

^b CNR   (Italy)

Author keywords

Aquatic toxicology; Biomineralization; Development; Embryo; Metals

Indexed keywords

CALCIUM; MANGANESE; MITOGEN ACTIVATED PROTEIN KINASE;

ARTICLE; ATOMIC ABSORPTION SPECTROMETRY; BIOMINERALIZATION; BONE DEVELOPMENT; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO; EMBRYOTOXICITY; FERTILIZATION; GENE EXPRESSION; GERM LAYER; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE MICROSCOPY; MICROSCOPY; NONHUMAN; SEA URCHIN;

ABNORMALITIES, DRUG-INDUCED; ANIMALS; BONE AND BONES; CALCIUM; EMBRYO CULTURE TECHNIQUES; EMBRYO, NONMAMMALIAN; FLUORESCEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IN SITU HYBRIDIZATION; MANGANESE COMPOUNDS; MAP KINASE SIGNALING SYSTEM; PHOSPHORYLATION; RNA, MESSENGER; SEA URCHINS; TERATOGENS; TOXICITY TESTS;

ECHINOIDEA; PARACENTROTUS LIVIDUS; VERTEBRATA;

EID: 80052470789     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfr152     Document Type: Article

References (82)

1. Abramowitz, J., and Suki, W. N. (1996). Ca-ATPase and bone cell mineralization. Miner. Electrolyte Metab. 22, 336-344.
2. 2+), and calmodulin. Cell. Signal. 14, 649-654.
3. Angerer, R. C., and Angerer, L. M. (2007). Sea Urchin Embryo: Specification of Cell Fate. Available at: http://www.els.net. Accessed June 27, 2011.
4. Anstrom, J. A., Chin, J. E., Leaf, D. S., Parks, A. L., and Raff, R. A. (1987). Localization and expression of msp130, a primary mesenchyme lineage-specific cell surface protein in the sea urchin embryo. Development. 101, 255-265.
5. Armstrong, N., Hardin, J., and McClay, D. R. (1993). Cell-cell interactions regulate skeleton formation in the sea urchin embryo. Development. 119, 833-840.
6. Benson, S. C., Benson, N. C., and Wilt, F. (1986). The organic matrix of the skeletal spicule of sea urchin embryos. J. Cell Biol. 102, 1878-1886.
7. Bonaventura, R., Poma, V., Costa, C., and Matranga, V. (2005). UVB radiation prevents skeleton growth and stimulates the expression of stress markers in sea urchin embryos. Biochem. Biophys. Res. Commun. 328, 150-157.
8. Brini, M., and Carafoli, E. (2009). Calcium pumps in health and disease. Physiol. Rev. 89, 1341-1378.
9. Cameron, R. A., Britten, R. J., and Davidson, E. H. (1993). The embryonic ciliated band of the sea urchin, Strongylocentrotus purpuratus derives from both oral and aboral ectoderm. Dev. Biol. 160, 369-376.
10. Campos, L. S., Decker, L., Taylor, V., and Skarnes, W. (2006). Notch, epidermal growth factor receptor, and β1-integrin pathways are coordinated in neural stem cells. J. Biol. Chem. 281, 5300-5309.
11. Chung, S. E., Park, H., Chang, N., Oh, S., Cheong, H., Ha, E., Kim, B., Ha, M., Kim, Y., and Hong, Y. (2011). Effect of in utero exposure to manganese on the neurodevelopment of the infant. Epidemiology. 22, S70.
12. Colomina, M. T., Domingo, J. L., Llobet, J. M., and Corbella, J. (1996). Effect of day of exposure on the developmental toxicity of manganese in mice. Vet. Hum. Toxicol. 38, 7-9.
13. Corson, L. B., Yamanaka, Y., Lai, K. M., and Rossant, J. (2003). Spatial and temporal patterns of ERK signaling during mouse embryogenesis. Development. 130, 4527-4537.
14. Croce, J. C., and McClay, D. R. (2010). Dynamics of Delta/Notch signaling on endomesoderm segregation in the sea urchin embryo. Development. 137, 83-91.
15. Culotta, V. C., Yang, M., and Hall, M. D. (2005). Manganese transport and trafficking: lessons learned from Saccharomyces cerevisiae. Eukaryot. Cell. 4, 1159-1165.
16. Davidson, E. H., Cameron, R. A., and Ransick, A. (1998). Specification of cell fate in the sea urchin embryo: summary and some proposed mechanisms. Development. 125, 3269-3290.
17. Decker, G. L., Morrill, J. B., and Lennarz, W. J. (1987). Characterization of sea urchin primary mesenchyme cells and spicules during biomineralization in vitro. Development. 101, 297-312.
18. Doyle, D., and Kapron, C. M. (2002). Inhibition of cell differentiation by manganese chloride in micromass cultures of mouse embryonic limb bud cells. Toxicol. In Vitro 16, 101-106.
19. Du, S. J., Frenkel, V., Kindschi, G., and Zohar, Y. (2001). Visualizing normal and defective bone development in zebrafish embryos using the fluorescent chromophore calcein. Dev. Biol. 238, 239-246.
20. Dubois, P., and Chen, C. (1989). Calcification in echinoderms. In Echinoderm Studies (M. Jangoux and J. M. Lawrence, Eds.), Vol. 3, pp. 109-178. AA Balkema, Rotterdam, The Netherlands.
21. Ducibella, T., Schultz, R. M., and Ozil, J. P. (2006). Role of calcium signals in early development. Semin. Cell Dev. Biol. 17, 324-332.
22. Duloquin, L., Lhomond, G., and Gache, C. (2007). Localized VEGF signaling from ectoderm to mesenchyme cells controls morphogenesis of the sea urchin embryo skeleton. Development. 134, 2293-2302.
23. Ettensohn, C. A. (2009). Lessons from a gene regulatory network: echinoderm skeletogenesis provides insights into evolution, plasticity and morphogenesis. Development. 136, 11-21.
24. Ettensohn, C. A., and Malinda, K. M. (1993). Size regulation and morphogenesis: a cellular analysis of skeletogenesis in the sea urchin embryo. Development. 119, 155-167.
25. Faddy, H. M., Smart, C. E., Xu, R., Lee, G. Y., Kenny, P. A., Feng, M., Rao, R., Brown, M. A., Bissell, M. J., Roberts-Thomson, S. J., et al. (2008). Localization of plasma membrane and secretory calcium pumps in the mammary gland. Biochem. Biophys. Res. Commun. 369, 977-978.
26. Fernandez-Serra, M., Consales, C., Livigni, A., and Arnone, M. I. (2004). Role of the ERK mediated signaling pathway in mesenchyme formation and differentiation in the sea urchin embryo. Dev. Biol. 268, 384-402.
27. Gabay, L., Seger, R., and Shilo, B. Z. (1997). MAP kinase in situ activation atlas during Drosophila embryogenesis. Development. 124, 3535-3541.
28. Giordano, G., Pizzurro, D., VanDeMark, K., Guazzetti, M., and Costa, L. G. (2009). Manganese inhibits the ability of astrocytes to promote neuronal differentiation. Toxicol. Appl. Pharmacol. 240, 226-235.
29. 2+ ATPase. Biochem. Biophys. Res. Commun. 339, 443-449.
30. 2+-ATPase in sea urchin spermatozoa. FEBS Lett. 580, 3900-3904.
31. Gunaratne, H. J., and Vacquier, V. D. (2007). Sequence, annotation and developmental expression of the sea urchin Ca2+-ATPase family. Gene. 397, 67-75.
32. Guo, X. E., Takai, E., Jiang, X., Xu, Q., Whitesides, G. M., Yardley, J. T., Hung, C. T., Chow, E. M., Hantschel, T., and Costa, K. D. (2006). Intracellular calcium waves in bone cell networks under single cell nanoindentation. Mol. Cell. Biomech. 3, 95-107.
33. Guss, K. A., and Ettensohn, C. A. (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.
34. Hardin, J., Coffman, J. A., Black, S. D., and McClay, D. R. (1992). Commitment along the dorsoventral axis of the sea urchin embryo is altered in response to NiCl2. Development. 116, 671-685.
35. Hoenderop, J. G. J., Nilius, B., and Bindels, R. J. M. (2005). Calcium absorption across epithelia. Physiol. Rev. 85, 373-422.
36. Killian, C. E., and Wilt, F. H. (1996). Characterization of the proteins comprising the integral matrix of Strongylocentrotus purpuratus embryonic spicules. J. Biol. Chem. 271, 9150-9159.
37. Killian, C. E., and Wilt, F. H. (2008). Molecular aspects of biomineralization of the echinoderm endoskeleton. Chem. Rev. 108, 4463-4474.
38. Kiyomoto, M., Zito, F., Costa, C., Poma, V., Sciarrino, S., and Matranga, V. (2007). Skeletogenesis by transfated secondary mesenchyme cells is dependent on extracellular matrix-ectoderm interactions in Paracentrotus lividus sea urchin embryos. Dev. Growth Differ. 49, 731-741.
39. Kumano, M., Carroll, D. J., Denu, J. M., and Foltz, K. R. (2001). Calcium-mediated inactivation of the MAP kinase pathway in sea urchin eggs at fertilization. Dev. Biol. 236, 244-257.
40. Kupzig, S., Walker, S. A., and Cullen, P. J. (2005). The frequencies of calcium oscillations are optimized for efficient calcium-mediated activation of Ras and the ERK/MAPK cascade. Proc. Natl. Acad. Sci. U. S. A. 102, 7577-7582.
41. Livingston, B. T., Killian, C. E., Wilt, F., Cameron, A., Landrum, M. J., Ermolaeva, O., Sapojnikov, V., Maglott, D. R., Buchanan, A. M., and Ettensohn, C. A. (2006). A genome-wide analysis of biomineralization related proteins in the sea urchin Strongylocentrotus purpuratus. Dev. Biol. 300, 335-348.
42. Livingston, B. T., and Wilt, F. H. (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.
43. Livingston, B. T., and Wilt, F. H. (1990). Determination of cell fate in sea urchin embryos. Bioessays. 12, 115-119.
44. Logan, C. Y., Miller, J. R., Ferkowicz, M. J., and McClay, D. R. (1999). Nuclear beta-catenin is required to specify vegetal cell fates in the sea urchin embryo. Development. 126, 345-357.
45. Matranga, V., Zito, F., Costa, C., Bonaventura, R., Giarrusso, S., and Celi, F. (2010). Embryonic development and skeletogenic gene expression affected by X-rays in the Mediterranean sea urchin Paracentrotus lividus. Ecotoxicology 19, 530-537.
46. Nakano, E., Okazaki, K., and Iwamatsu, T. (1963). Accumulation of radioactive calcium in larvae of the sea urchin Pseudocentrotus depressus. Biol. Bull. 125, 125-132.
47. Okazaki, K., and Inoue, S. (1976). Crystal property of the larval sea urchin spicule. Dev. Growth Differ. 18, 413-434.
48. cyt signal in the mouse. Dev. Biol. 282, 39-54.
49. Perl, D. P., and Olanow, C. W. (2007). The neuropathology of manganese-induced parkinsonism. J. Neuropathol. Exp. Neurol. 66, 675-682.
50. Pinsino, A., Matranga, V., Trinchella, F., and Roccheri, M. C. (2010). Sea urchin embryos as an in vivo model for the assessment of manganese toxicity: developmental and stress response effects. Ecotoxicology. 19, 555-562.
51. Poustka, A. J., Kühn, A., Groth, D., Weise, V., Yaguchi, S., Burke, R. D., Herwig, R., Lehrach, H., and Panopoulou, G. (2007). A global view of gene expression in lithium and zinc treated sea urchin embryos: new components of gene regulatory networks. Genome Biol. 8, R85.
52. Ramachandran, R. K., Govindarajan, V., Seid, C. A., Patil, S., and Tomlinson, C. R. (1995). Role for platelet-derived growth factor-like and epidermal growth factorlike signaling pathways in gastrulation and spiculogenesis in the Lytechinus sea urchin embryo. Dev. Dyn. 204, 77-88.
53. Roccheri, M. C., Agnello, M., Bonaventura, R., and Matranga, V. (2004). Cadmium induces the expression of specific stress proteins in sea urchin embryos. Biochem. Biophys. Res. Commun. 321, 80-87.
54. Roepke, T. A., Snyder, M. J., and Cherr, G. N. (2005). Estradiol and endocrine disrupting compounds adversely affect development of sea urchin embryos at environmentally relevant concentrations. Aquat. Toxicol. 71, 155-173.
55. Röttinger, E., Besnardeau, L., and Lepage, T. (2004). A Raf/MEK/ERK signalling pathway is required for development of the sea urchin embryo micromere lineage through phosphorylation of the transcription factor Ets. Development. 131, 1075-1087.
56. Röttinger, E., Saudemont, A., Duboc, V., Besnardeau, L., McClay, D., and Lepage, T. (2008). FGF signals guide migration of mesenchymal cells, control skeletal morphogenesis [corrected] and regulate gastrulation during sea urchin development. Development. 135, 353-365.
57. Roux, M. M., Townley, I. K., Raisch, M., Reade, A., Bradham, C., Humphreys, G., Gunaratne, H. J., Killian, C. E., Moy, G., Su, Y. H., et al. (2006). A functional genomic and proteomic perspective of sea urchin calcium signaling and egg activation. Dev. Biol. 300, 416-433.
58. Russo, R., Bonaventura, R., Zito, F., Schroeder, H. C., Müller, I., Müller, W. E. G., and Matranga, V. (2003). Stress to cadmium monitored by metallothionein gene induction in Paracentrotus lividus embryos. Cell Stress Chaperones. 8, 232-241.
59. Sanchez, D. J., Domingo, J. L., Llobet, J. M., and Keen, C. L. (1993). Maternal and developmental toxicity of manganese in the mouse. Toxicol. Lett. 69, 45-52.
60. Santamaria, A. B. (2008). Manganese exposure, essentiality and toxicity. Indian J. Med. Res. 128, 484-500.
61. Santella, L., Lim, D., and Moccia, F. (2004). Calcium and fertilization: the beginning of life. Trends Biochem. Sci. 29, 400-408.
62. Slusarski, D. C., and Pelegri, F. (2007). Calcium signaling in vertebrate patterning and morphogenesis. Dev. Biol. 307, 1-13.
63. Smith, J., and Davidson, E. H. (2008). Gene regulatory network subcircuit controlling a dynamic spatial pattern of signaling in the sea urchin embryo. Proc. Natl. Acad. Sci. U. S. A. 105, 20089-20094.
64. Timourian, H. (1968). The effect of zinc on sea urchin morphogenesis. J. Exp. Zool. 169, 121-132.
65. 2+ pumps in the golgi apparatus. Biochim. Biophys. Acta 1742, 103-112.
66. Vangheluwe, P., Sepulveda, M. R., Missiaen, L., Raeymaekers, L., Wuytack, F., and Vanoevelen, J. (2009). Intracellular Ca2+- and Mn2+-transport ATPases. Chem. Rev. 109, 4733-4759.
67. 2+ ions. J. Biol. Chem. 280, 22800-22808.
68. Vigeh, M., Yokoyama, K., Ramezanzadeh, F., Dahaghin, M., Fakhriazad, E., Seyedaghamiri, Z., and Araki, S. (2008). Blood manganese concentrations and intrauterine growth restriction. Reprod. Toxicol. 25, 219-223.
69. 2+ oscillations. EMBO J. 23, 1749-1760.
70. Wessel, G. M., and McClay, D. R. (1985). Sequential expression of germlayer specific molecules in the sea urchin embryo. Dev. Biol. 111, 451-463.
71. Whitaker, M. (2006). Calcium at fertilization and in early development. Physiol. Rev. 86, 25-88.
72. Wilt, F. H. (2002). Biomineralization of the spicules of sea urchin embryos. Zool. Sci. 19, 253-261.
73. Wilt, F. H. (2005). Developmental biology meets materials science: morphogenesis of biomineralized structures. Dev. Biol. 280, 15-25.
74. Wilt, F. H., Killian, C. E., Hamilton, P., and Croker, L. (2008). The dynamics of secretion during sea urchin embryonic skeleton formation. Exp. Cell Res. 314, 1744-1752.
75. Wood, R. J. (2009). Manganese and birth outcome. Nutr. Rev. 67, 416-420.
76. 2+ store. Pflugers Arch. 446, 148-153.
77. Yaguchi, S., Yaguchi, J., Angerer, R. C., Angerer, L. M., and Burke, R. D. (2010). TGFβ signaling positions the ciliary band and patterns neurons in the sea urchin embryo. Dev. Biol. 347, 71-81.
78. 2+ in specification of vegetal cell fate in early sea urchin embryos. J. Exp. Biol. 204, 823-834.
79. Zito, F., Costa, C., Sciarrino, S., Poma, V., Russo, R., Angerer, L. M., and Matranga, V. (2003). Expression of univin, a TGF-beta growth factor, requires ectoderm-ECM interaction and promotes skeletal growth in the sea urchin embryo. Dev. Biol. 264, 217-227.
80. Zito, F., and Matranga, V. (2009). Secondary mesenchyme cells as potential stem cells of the sea urchin embryo. In Stem Cells in Marine Organisms (B. Rinkevic and V. Matranga, Eds.), pp. 187-213. Springer, Dordrecht, The Netherlands.
81. Zito, F., Tesoro, V., McClay, D. R., Nakano, E., and Matranga, V. (1998). Ectoderm cell-ECM interaction is essential for sea urchin embryo skeletogenesis. Dev. Biol. 96, 184-192.
82. Zota, A. R., Ettinger, A. S., Bouchard, M., Amarasiriwardena, C. J., Schwartz, J., Hu, H., and Wright, R. O. (2009). Maternal blood manganese levels and infant birth weight. Epidemiology. 20, 367-373.