Exposure to ultraviolet radiation causes proteomic changes in embryos of the purple sea urchin, Strongylocentrotus purpuratus

Journal of Experimental Marine Biology and Ecology

Volumn 397, Issue 2, 2011, Pages 106-120

  Campanale, Joseph P ^a   Tomanek, Lars ^a   Adams, Nikki L ^a  

^a CALIFORNIA POLYTECHNIC STATE UNIVERSITY   (United States)

Author keywords

Proteome response; Sea urchin embryo; Two dimensional gel electrophoresis (2D GE); Ultraviolet radiation; UVR

Indexed keywords

COASTAL WATER; DESORPTION; ECHINODERM; ELECTROKINESIS; EMBRYO; EXPERIMENTAL STUDY; FERTILIZATION (REPRODUCTION); GENE EXPRESSION; MASS SPECTROMETRY; PROTEIN; PROTEOMICS; ULTRAVIOLET RADIATION;

ECHINOIDEA; STRONGYLOCENTROTUS; STRONGYLOCENTROTUS PURPURATUS;

EID: 78650406860     PISSN: 00220981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jembe.2010.11.022     Document Type: Article

References (114)

1. Adams N.L., Foltz K.R. A molecular approach to understanding UV-induced mitotic delay in sea urchin embryos. Proceedings from the North American Echinoderm Conference 2001. Gulf of Mexico Sciences 2002, 19:165.
2. Adams N.L., Shick J.M. Mycosporine-like amino acids provide protection against ultraviolet radiation in eggs of the green sea urchin Strongylocentrotus droebachiensis. Photochem. Photobiol. 1996, 64:149-158.
3. Adams N.L., Shick J.M. Mycosporine-like amino acids prevent UVB-induced abnormalities during early development of the green sea urchin Strongylocentrotus droebachiensis. Mar. Biol. 2001, 138:267-280.
4. Adams N., Shick J.M., Dunlap W. Selective accumulation of mycosporine-like amino acids in ovaries of green sea urchin, Strongylocentrotus droebachiensis, is not affected by ultraviolet radiation. Mar. Biol. 2001, 138:284-294.
5. Agueli C., Geraci F., Giudice G., Chimenti L., Cascino D., Sconzo G. A constitutive 70 kDa heat-shock protein is localized on the fibers of spindles and asters at metaphase in an ATP-dependent manner: a new chaperone role is proposed. Biochem. J. 2001, 360:413-419.
6. Anderson S., Hoffman J., Wild G., Bosch I., Karentz D. Cytogenetic, cellular, and developmental responses in Antarctic sea urchins (Starchiness neumayeri) following laboratory ultraviolet-B and ambient solar radiation exposures. Antarct. J. 1993, 28:115-116.
7. Anderson S., Zepp R., Machula J., Santavy D., Hansen L., Mueller E. Indicators of UV exposure in corals and their relevance to global climate change and coral bleaching. Hum. Ecol. Risk Assess. 2001, 7:1271-1282.
8. Athar M., Kim A.L., Ahmad N., Mukhtar H., Gautier J., Bickers D.R. Mechanism of ultraviolet B-induced cell cycle arrest in G2/M phase in immortalized skin keratinocytes with defective p53. Biochem. Bioph. Res. Co. 2000, 277:107-111.
9. Bancroft B.A., Baker N.J., Blaustein A.R. Effects of UVB on marine and freshwater organisms: a synthesis through meta-analysis. Ecol. Lett. 2007, 10:332-345.
10. Belenguer P., Caizergues-Ferrer M., Labbé J.C., Dorée M., Amalric F. Mitosis-specific phosphorylation of nucleolin by p34cdc2 protein kinase. Mol. Cell. Biol. 1990, 10:3607-3618.
11. Berth M., Moser F.M., Kolbe M., Bernhardt J. The state of the art in the analysis of two dimensional gel electrophoresis images. Appl. Microbiol. Biotechnol. 2007, 76:1223-1243.
12. Bonaventura R., Poma V., Costa C., Matranga V. UVB radiation prevents skeleton growth and stimulates expression of stress markers in sea urchin embryos. Biochem. Bioph. Res. Co. 2005, 328:150-157.
13. Bonaventura R., Poma V., Russo R., Zito F., Matranga V. Effects of UV-B radiation on development and hsp70 expression in sea urchin cleavage embryos. Mar. Biol. 2006, 149:79-86.
14. Bradham C.A., Foltz K.R., Beane W.S., Arnone M.I., Rizzo F., Coffman J.A., Mushegan A., Goel M., Morales J., Geneviere A., Laparz F., Robertson A.J., Kelkar H., Loza-Coll M., Townley I.K., Raish M., Roux M.M., Lepage T., Gache C., McClay D.R., Manning G. The sea urchin kinome: a first look. Dev. Biol. 2006, 300:180-193.
15. Caldwell M.M., Björn L.O., Bornman J.F., Kulandiavelu G., Teramura A.H., Tevini M. Effects of increased solar ultraviolet radiation on terrestrial ecosystems. J. Photoch. Photobio. B. 1998, 46:40-52.
16. Cullen J., Neale P. Ultraviolet radiation, ozone depletion, and marine photosynthesis. Photosynth. Res. 1994, 39:303-320.
17. Dunaway S., Liu H., Walworth N. Interaction of 14-3-3 protein with Chk1 affects localization and checkpoint function. Journal of Cell Science. 2004, 118:39-50.
18. Epel D., Hemela K., Shick M., Patton C. Development in the floating world: defenses of eggs and embryos against damage from UV-radiation. Am. Zool. 1999, 39:271-278.
19. Ferl R.J., Manak M.S., Reyes M.F. The 14-3-3s. Genome Biol. 2002, 3:3010.1-3010.7.
20. Fernandez-Guerra A., Aze A., Morales J., Mulner-Lorillon O., Cosson B., Cormier P., Bradham C., Adams N.L., Robertson A.J., Marzluff W.F., Coffman J.A., Genevière A.M. The genomic repertoire for cell cycle control and DNA metabolism in S. purpuratus. Dev. Biol. 2006, 300:238-251.
21. Fu H., Subramanian R.R., Masters S.C. 14-3-3 Proteins: structure, function, and regulation. Annu. Rev. Pharmacol. 2000, 40:617-647.
22. Gabrielli B.G., Clark J.M., McCormack A.K., Ellem K.A.O. Ultraviolet light-induced G2 phase cell cycle checkpoint blocks cdc25-dependent progression into mitosis. Oncogene. 1997, 15:749-758.
23. Geraci F., Agueli C., Giudice G., Sconzo G. Localization of HSP70, Cdc2, and cyclin B in sea urchin oocytes in non-stressed conditions. Biochem. Bioph. Res. Co. 2003, 310:748-753.
24. Giese A. Studies on ultraviolet radiation action upon animal cells. Photophysiology, vol II 1964, 203-245. Academic, New York. A. Giese (Ed.).
25. Giles N., Forrest A., Gabrielli B. 14-3-3 acts as an intramolecular bridge to regulate cdc25B localization and activity. J. Biol. Chem. 2003, 278:28580-28587.
26. Glickman M.H., Ciechanover A. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol. Rev. 2002, 82:373-428.
27. Glockzin S., Ogi F.X., Hengstermann A., Scheffner M., Blattner C. Involvement of the DNA repair protein hHR23 in p53 degradation. Mol. Cell Biol. 2003, 23:8960-8969.
28. Goel M., Mushegian A. Intermediary metabolism in sea urchin: the first inferences from the genome sequence. Dev. Biol. 2006, 300:282-292.
29. Goldstone J.V., Hamdoun A., Cole B.J., Howard-Ashby M., Nebert D.W., Scally M., Dean M., Epel D., Hahn M.E., Stegean J.J. The chemical defensome: environmental sensing and response genes in the Strongylocentrotus purpuratus genome. Dev. Biol. 2006, 300:366-384.
30. Goschke, G.A., 2005. The presence and activity of Chk1 in the UV-induced cellular response in the purple sea urchin, Strongylocentrotus purpuratus. M.S. Thesis, California Polytechnic State University, San Luis Obispo.
31. Green D.R., Reed J.C. Mitochondria and apoptosis. Science 1998, 281:1309-1312.
32. Häder D., Kumar H., Smith R., Worrest R. Effects of solar UV radiation on aquatic ecosystems and interactions with climate change. Photochem. Photobiol. Sci. 2007, 6:267-285.
33. Hamdoun A., Epel D. Embryo stability and vulnerability in an always changing world. Proc. Natl. Acad. Sci. 2007, 104:1745-1750.
34. Hamer B., Pavičić Hamer D., Müller W.E.G., Batel R. Stress-70 proteins in marine mussel Mytilus galloprovincialis as biomarkers of environmental pollution: a field study. Environ. Int. 2004, 30:873-882.
35. Helmbrecht K., Zeise E., Rensing L. Chaperones in cell cycle regulation and mitogenic signal transduction: a review. Cell Prolif. 2000, 33:341-365.
36. Hoegh-Guldberg O., Hughes L., McIntyre S., Lindenmayer D.B., Pamesan C., Possingham H.P., Thomas C.D. Assisted colonization and rapid climate change. Science. 2008, 321:345-346.
37. Hollósy F. Effects of ultraviolet radiation on plant cells. Micron. 2002, 33:179-197.
38. Howard-Ashby M., Materna S.C., Brown T., Tu Q., Oliveri P., Cameron R.A., Davidson E.H. High regulatory gene use in sea urchin embryogenesis: implications for bliaterian development and evolution. Dev. Biol. 2006, 300:27-34.
39. Imlay J., Linn S. DNA damage and oxygen radical toxicity. Science. 1988, 240:1302-1309.
40. Iordanov M.S., Pribnow D., Magun J.L., Dinh T.H., Pearson J.A., Magun B.E. Ultraviolet radiation triggers the ribotoxic stress response in mammalian cells. J. Biol. Chem. 1998, 273:15794-15803.
41. Isley N.M., Lamare C.Marchall, Barker M. Expression of the DNA repair enzyme, Photolyase, in developmental tissues and larvae, and in response to ambient UV-R in the Antarctic sea urchin Sterchinuc neumayeri. Photochem. Photobiol. 2009, 85:1168-1172.
42. Jackson G.A., Strathmann R.R. Larval mortality from offshore mixing as a link between precompetent and competent periods of development. Am. Nat. 1981, 118:16-26.
43. Jo S.H., Son M.K., Koh H.J., Lee S.M., Song I.H., Kim Y.O., Lee Y.S., Jeong K.S., Kim W.B., Park J.W., Song B.J., Huhe T.L. Control of mitochondrial redox balance and cellular defense against oxidative damage by mitochondrial NADP+-dependent isocitrate dehydrogenase. J. Biol. Chem. 2001, 276:16168-16176.
44. Kawahara H., Phillipova R., Yokosawa H., Patel R., Tanaka K., Whitaker M. Inhibiting proteasome activity causes overreplication of DNA and blocks entry into mitosis in sea urchin embryos. J Cell Sci. 2000, 113:2659-2670.
45. Kerr J., McElroy C. Evidence for large upward trends of ultraviolet radiation linked to ozone depletion. Science. 1993, 262:1032-1034.
46. Kil I.S., Park J.W. Regulation of mitochondrial NADP+-dependent isocitrate dehydrogenase activity by glutathionylation. J. Biol. Chem. 2005, 280:10846-10854.
47. Kültz D. Molecular and evolutionary basis of the cellular stress response. Annu. Rev. Physiol. 2005, 67:225-257.
48. Lamare M.D., Hoffman J. Natural variation of carotenoids in the eggs and gonads of the echinoid genus, Strongylocentrotus: implications for their role in ultraviolet radiation photoprotection. J. Exp. Mar. Biol. Ecol. 2004, 312:215-233.
49. Lamare M.D., Barker M.F., Lesser M.P., Marshall C.J. DNA photorepair in echinoid embryos: effects of temperature on repair rate in Antarctic and non-Antarctic species. J. Exp. Biol. 2006, 209:5017-5028.
50. Lamare M.D., Barker M.F., Lesser M.P. In situ rates of DNA damage and abnormal development in Antarctic and non-Antarctic sea urchin embryos. Aquatic Biology 2007, 1:21-32.
51. Lesser M.P. Depth-dependent effects of ultraviolet radiation on survivorship, oxidative stress and DNA damage in sea urchin (Strongylocentrotus droebachiensis) embryos from the Gulf of Maine. Photochem Photobiol. 2010, 8:382-388.
52. Lesser M., Kruse V., Barry T. Exposure to ultraviolet radiation causes apoptosis in developing sea urchin embryos. J. Exp. Biol. 2003, 206:4097-4103.
53. Lesser M.P., Barry T.M., Lamare M.D., Barker M.F. Biological weighting functions for DNA damage in sea urchin embryos exposed to ultraviolet radiation. J. Exp. Mar. Biol. Ecol. 2006, 328:10-21.
54. Leustek T., Dalie B., Amir-Shapira D., Brot N., Weissbach H. A member of the Hsp70 family is localized in mitochondria and resembles Escherichia coli DnaK. Proc. Natl. Acad. Sci. 1989, 86:7805-7808.
55. Lin D., Lechleiter J.D. Mitochondrial targeted cyclophilin D protects cells from cell death by peptidyl prolyl isomerization. J. Biol. Chem. 2002, 277:31134-31141.
56. Lister K.N., Lamare M.D., Burritt D.J. Oxidative damage in response to natural levels of UV-B radiation in larvae of the tropical sea urchin Tripneustes gratilla. Photochem. Photobio. 2010, 86:1091-1098.
57. Liu Q., Guntuku S., Cui X., Matsuoka S., Cortez D., et al. Chk1 is an essential kinase that is regulated by Atr and required for the G2/M DNA damage checkpoint. Genes and Development. 2000, 14:1448-1459.
58. Livingston B.T., Killian C.E., Wilt F., Cameron A., Landrum M.J., Ermolaeva O., Sapojnikov V., Maglott D.R., Buchanan A.M., Ettensohn C.A. A genome-wide analysis of biomineralization-related proteins in the sea urchin Strongylocentrotus purpuratus. Dev. Biol. 2006, 300:335-348.
59. Madronich S., Mckenzie R., Bjorn L., Caldwell M. Changes in biologically active ultraviolet radiation reaching the Earth's surface. Environmental Effects of Ozone Depletion: 1998 Assessment 1998, 5-19. United Nations, New York, Environment programme report. J. van der Leun, X. Tang, M. Tevini (Eds.).
60. Marchler-Bauer A., Anderson J.B., Chitsaz F., Derbyshire M.K., DeWeese-Scott C., Fong J.H., Geer L.Y., Geer R.C., Gonzales N.R., Gwadz M., He S., Hurwitz D.I., Jackson J.D., Ke Z., Lanczycki C.J., Leibert C.A., Liu C., Lu F., Lu S., Marchler G.H., Mullokandov M., Song J.S., Tasneem A., Thanki N., Yamashita R.A., Zhang D., Zhang N., Bryant S.H. CDD: specific functional annotation with the conserved domain database. Nucleic Acids Res. 2009, 37:D205-D210.
61. McKenzie R., Bijorn L., Bais A., Ilyasd M. Changes in biologically active ultraviolet radiation reaching the Earth's surface. Photochem. Photobiol. Sci. 2003, 2:5-15.
62. McKenzie R.L., Aucamp P.J., Bais A.F., Björn L.O., Ilyasd M. Changes in biologically-active ultraviolet radiation reaching the Earth's surface. Photochem. Photobiol. Sci. 2007, 6:218-231.
63. Morgan S.G., Christy J.H. Survival of marine larvae under the countervailing selective pressures of photodamage and predation. Limnol. Oceanogr. 1996, 41:498-504.
64. Parker S.H., Parker T.A., George K.S., Wu S. The roles of translation initiation regulation in ultraviolet light-induced apoptosis. Mol. Cell Biochem. 2006, 293:173-181.
65. Pavey S., Russell T., Gabrielli B. G2 phase cell cycle arrest in human skin following UV irradiation. Oncogene. 2001, 20:6103-6110.
66. Peak M., Peak J. Hydroxyl radical quenching agents protect against DNA breakage caused by both 365-nm and gamma radiation. Photochem. Photobiol. 1990, 51:649-652.
67. Pechenik, J.A., 1987. Environmental influences on larval survival and development. In: Giese, A. C., Pearse, J. S., Pearse, V. B. (eds.) Reproduction of marine invertebrates, Vol. IX. Blackwell Scientific Publications and Boxwood Press, Cambridge, 511-608.
68. Perkins D.N., Pappin D.J.C., Creasy D.M., Cottrell J.S. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis. 1999, 20:3551-3567.
69. Pesando D., Huitorel P., Dolcini V., Angelini C., Guidetti P., Falugi C. Biological targets of neurotoxic pesticides analyzed by alteration of developmental events in the Mediterranean sea urchin, Paracentrotus lividus. Mar. Environ. Res. 2003, 55:39-57.
70. Pourzand C., Tyrell R.M. Apoptosis, the role of oxidative stress and the example of solar UV radiation. Photochem. Photobiol. 1999, 70:380-390.
71. Przeslawski R. Combined effects of solar radiation and desiccation on the mortality and development of encapsulated embryos of rocky shore gastropods. Mar. Ecol. Prog. Ser. 2005, 298:169-177.
72. Rao B., Hindgardner R. Analysis of DNA synthesis and x-ray-induced mitotic delay in sea urchins. Radiat. Res. 1965, 26:534-537.
73. Rhind N., Russell P. Chk1 and Cds1: linchpins of the DNA damage and replication checkpoint pathways. Journal of Cell Science. 2000, 113:3889-3896.
74. Robinson D.N., Spudich J.A. Towards a molecular understanding of cytokinesis. Trends Cell Biol. 2000, 10:228-237.
75. Roux M.M., Radeke M., Goel M., Mushegian A., Foltz K.R. 2DE identification of proteins exhibiting turnover and phosphorylation dynamics during sea urchin egg activation. Dev. Biol. 2008, 313:630-647.
76. Russo R., Bonaventura R., Zito F., Schroder H., Muller I., Muller W., Matranga V. Stress to cadmium monitored by metallothionein gene induction in Paracentrotus lividus embryos. Cell Stress Chaperon. 2003, 8:232-241.
77. Rustad R. Changes in the sensitivity to ultraviolet-induced mitotic delay during the cell division cycle of the sea urchin egg. Exp. Cell Res. 1960, 21:596-602.
78. Rustad R. Radiation responses during the mitotic cycle of the sea urchin egg. Developmental aspects of the cell cycle 1971, 127-159. Academic, New York. I. Cameron, G. Padilla, A. Zimmerman (Eds.).
79. Saeed A.I., Sharov V., White J., Li J., Liang W., Bhagabati N., Braisted J., Klapa M., Currier T., Thiagarajan M., Sturn A., Snuffin M., Rezantsev A., Popov D., Ryltsov A., Kostukovich E., Borisovsky I., Liu Z., Vinsavich A., Trush V., Quackenbush J. TM4: a free, open-source system for microarray data management and analysis. Biotechniques. 2003, 34:374-378.
80. Samanta M.P., Tongprasit W., Istrail S., Cameron R.A., Tu Q., Davidson E.H., Stolc V. The transcriptome of the sea urchin embryo. Science. 2006, 314:960-962.
81. Sconzo G., Amore G., Capra G., Giudice G., Cascino D., Ghersi G. Identification and characterization of a constitutive HSP75 in sea urchin embryos. Biochem. Bioph. Res. Co. 1997, 234:24-29.
82. Sconzo G., Palla F., Agueli C., Spinelli G., Giudice G., Cascino D., Geraci F. Constitutive hsp70 is essential to mitosis during early cleavage of Paracentrotus lividus embryos: the blockage of constitutive hsp70 impairs mitosis. Biochem. Bioph. Res. Co. 1999, 260:143-149.
83. Setlow R. The wavelengths in sunlight effective in producing skin cancer. A theoretical analysis. Proc. Natl. Acad. Sci. USA 1974, 71:3363-3366.
84. Shapiro B.M. The control of oxidant stress at fertilization. Science. 1991, 252:533-536.
85. Shick J.M., Romaine-Loud S., Ferrier-Pages C., Gattuso J.-P. Ultraviolet-B radiation stimulates shikimate pathway-dependent accumulation of mycosporine-like amino acids in the coral Stylophora pistillata despite decreases in its population of symbiotic dinoflagellates. Limnol. Oceanogr. 1999, 44:1667-1682.
86. Smith R.C., Baker K.S. Penetration of UV-B and biologically effective dose-rates in natural waters. Photochem. Photobio. 1979, 29:311-323.
87. Smith R., Prezlin B., Baker K., Bidigare R., Boucher N., Coley T., Karentz D., MacIntyre S., Matlick H., Menzies D., Ondrusek M., Wan Z., Water K. Ozone depletion: ultraviolet radiation and phytoplankton biology in natural waters. Science. 1992, 255:252-259.
88. Sodergren E., Weinstock G.M., Davidson E.H., Cameron R.A., Gibbs R.A., Angerer R.C., Angerer L.M., Arnone M.I., Burgess D.R., Burke R.D., Coffman J.A., Dean M., Elphick M.R., Ettensohn C.A., Foltz K.R., Hamdoun A., Hynes R.O., Klein W.H., Marzluff W., McClay D.R., Morris R.L., Mushegian A., Rast J.P., Smith L.C., Thorndyke M.C., Vacquier V.D., Wessel G.M., Wray G., Zhang L., Elsik C.G., Ermolaeva O., Hlavina W., Hofmann G., Kitts P., Landrum M.J., Mackey A.J., Maglott D., Panopoulou G., Poustka A.J., Pruitt K., Sapojnikov V., Song X., Souvorov A., Solovyev V., Wei Z., Whittaker C.A., Worley K., Durbin K.J., Shen Y., Fedrigo O., Garfield D., Haygood R., Primus A., Satija R., Severson T., Gonzalez-Garay M.L., Jackson A.R., Milosavljevic A., Tong M., Killian C.E., Livingston B.T., Wilt F.H., Adams N., Belle R., Carbonneau S., Cheung R., Cormier P., Cosson B., Croce J., Fernandez-Guerra A., Geneviere A.M., Goel M., Kelkar H., Morales J., Mulner-Lorillon O., Robertson A.J., Goldstone J.V., Cole B., Epel D., Gold B., Hahn M.E., Howard-Ashby M., Scally M., Stegeman J.J., Allgood E.L., Cool J., Judkins K.M., McCafferty S.S., Musante A.M., Obar R.A., Rawson A.P., Rossetti B.J., Gibbons I.R., Hoffman M.P., Leone A., Istrail S., Materna S.C., Samanta M.P., Stolc V., Tongprasit W., Tu Q., Bergeron K.F., Brandhorst B.P., Whittle J., Berney K., Bottjer D.J., Calestani C., Peterson K., Chow E., Yuan Q.A., Elhaik E., Graur D., Reese J.T., Bosdet I., Heesun S., Marra M.A., Schein J., Anderson M.K., Brockton V., Buckley K.M., Cohen A.H., Fugmann S.D., Hibino T., Loza-Coll M., Majeske A.J., Messier C., Nair S.V., Pancer Z., Terwilliger D.P., Agca C., Arboleda E., Chen N., Churcher A.M., Hallbook F., Humphrey G.W., Idris M.M., Kiyama T., Liang S., Mellott D., Mu X., Murray G., Olinski R.P., Raible F., Rowe M., Taylor J.S., Tessmar-Raible K., Wang D., Wilson K.H., Yaguchi S., Gaasterland T., Galindo B.E., Gunaratne H.J., Juliano C., Kinukawa M., Moy G.W., Neill A.T., Nomura M., Raisch M., Reade A., Roux M.M., Song J.L., Su Y.H., Townley I.K., Voronina E., Wong J.L., Amore G., Branno M., Brown E.R., Cavalieri V., Duboc V., Duloquin L., Flytzanis C., Gache C., Lapraz F., Lepage T., Locascio A., Martinez P., Matassi G., Matranga V., Range R., Rizzo F., Rottinger E., Beane W., Bradham C., Byrum C., Glenn T., Hussain S., Manning G., Miranda E., Thomason R., Walton K., Wikramanayke A., Wu S.Y., Xu R., Brown C.T., Chen L., Gray R.F., Lee P.Y., Nam J., Oliveri P., Smith J., Muzny D., Bell S., Chacko J., Cree A., Curry S., Davis C., Dinh H., Dugan-Rocha S., Fowler J., Gill R., Hamilton C., Hernandez J., Hines S., Hume J., Jackson L., Jolivet A., Kovar C., Lee S., Lewis L., Miner G., Morgan M., Nazareth L.V., Okwuonu G., Parker D., Pu L.L., Thorn R., Wright R. The genome of the sea urchin Strongylocentrotus purpuratus. Science 2006, 314:941-952.
89. Stitzel M.L., Seydoux G. Regulation of the oocyte-to-zygote transition. Science. 2007, 316:407-408.
90. Strathmann R.R., Staver J.M., Hoffman J.R. Risk and the evolution of cell-cycle durations of embryos. Evolution. 2002, 56:708-720.
91. Sumegi M., Hunyadi-Gulyas E., Medzihradszky K.F., Udvardy A. 26S proteasome subunits are O-linked N-acetylglucosamine-modified in Drosophila melanogaster. Biochem. Biophys. Res. Commun. 2003, 312:1284-1289.
92. Sun H.Q., Yamamoto M., Mejullano M., Yin H.L. Gelsolin, a multifunctional actin regulatory protein. J. Biol. Chem. 1999, 274:33179-33182.
93. Takagi M., Absalon M.J., McLure K.G., Kastan M.B. Regulation of p53 translation and induction after DNA damage by ribosomal protein and nucleolin. Cell. 2005, 123:49-63.
94. Tatusov R.L., Fedorova N.D., Jackson J.D., Jacobs A.R., Kiryutin B., Koonin E.V., Krylov D.M., Mazumder R., Mekhedov S.L., Nikolskaya A.N., Rao B.S., Smirnov S., Sverdlov A.V., Vasudevan S., Wolf Y.I., Yin J.J., Natale D.A. The COG database: and updated version includes eukaryotes. BMC. Bioinfo. 2003, 4:41.
95. Tedetti M., Sempere R. Percentage of ultraviolet radiation in the marine environment. A review. Photochem. Photobiol. 2006, 82:389-397.
96. Tevini M. Molecular biological effects of ultraviolet radiation. UV-B Radiation and Ozone Depletion: Effects on Humans, Animals, Plants, Microorganisms, and Materials 1993, 1-16. Lewis Publishers, Baca Raton, FL. M. Tevini (Ed.).
97. Tomanek L. Two-dimensional gel analysis of the heat-shock response in marine snails (genus Tegula): interspecific variation in protein expression and acclimation ability. J. Exp. Biol. 2005, 208:3133-3143.
98. Tomanek L. Variation in the heat shock response and its implication for predicting the effects of global climate change on species biogeographical distribution ranges and metabolic costs. J. Exp. Biol. 2010, 213:971-979.
99. Tomanek L. Environmental proteomics: changes in the proteome of marine organisms in response to environmental stress, pollutants, infection, symbiosis and development. Annu. Rev. Marine Sci. 2011, (available online).
100. Tomanek L., Zuzow M.J. The proteomic response of the mussel congeners Mytilus galloprovincialis and M. trossulus to acute heat stress: implications for thermal tolerance limits and metabolic costs of thermal stress. J. Exp. Biol. 2010, 213:3559-3574.
101. Tyrrell L. UV-A (320-380nm) Radiation as an oxidative stress. Oxidative Stress: Oxidants and Antioxidants 1991, 57-83. Academic Press, San Diego, CA. H. Sies (Ed.).
102. United Nations Environment Programme, Environmental Effects Assessment Panel Environmental effects of ozone depletion and its interactions with climate change: progress report, 2004. Photochem. Photobiol. Sci. 2005, 22:177-184.
103. United Nations Environment Programme, Environmental Effects Assessment Panel Environmental effects of ozone depletion and its interactions with climate change: progress report, 2005. Photochem. Photobiol. Sci. 2006, 5:13-24.
104. Vega Thurber R., Epel D. Apoptosis in early development of the sea urchin, Strongylocentrotus purpuratus. Dev. Biol. 2007, 303:336-346.
105. Verma R., Chen S., Feldman S., Schieltz D., Yates J., Dohmen J., Deshaies R.J. Proteasomal proteomics: identification of nucleotide-sensitive proteasome-interacting proteins by mass spectrometric analysis of affinity-purified proteasomes. Mol. Biol. Cell. 2000, 11:3425-3439.
106. Veselská R., Janisch R. The effects of UV irradiation on changes in cytoskeleton and viability of mouse fibroblasts L929 cell line. Scripta Medica. 2000, 73:393-408.
107. Williamson C., Schulze P., Hargreaves B., Seva J. The impact of short-term exposure to UV-B radiation on zooplankton communities in north temperate lakes. J. Plankton Res. 1994, 16:205-218.
108. Wong J., Créton R., Wessel G. The oxidative burst at fertilization is dependent upon activation of the dual oxidase Udx1. Dev. Cell. 2004, 7:801-814.
109. World Meteorological Organization Scientific assessment of ozone depletion 2006-summary. Global Ozone Research Monitoring Project-Report 50 2007.
110. Zamansky G.B., Chou I.N. Environmental wavelengths of ultraviolet light induce cytoskeletal damage. J. Invest. Dermatol. 1987, 89:606.
111. Zeitz L., Ferguson R., Garfinkel A. Radiation-induced effects on DNA synthesis in developing sea urchin eggs. Rad. Res. 1968, 34:200-208.
112. Zepp R.G., Callaghan T.V., Erickson D.J. Interactive effects of ozone depletion and climate change on biogeochemical cycles. Photochem. Photobiol. Sci. 2003, 2:51-61.
113. Zhang F., Su K., Yang X., Bowe D.B., Paterson A.J., Kudlow J.E. O-GlcNAc modification is an endogenous inhibitor of the proteasome. Cell. 2003, 115:715-725.
114. Zhang F., Hu Y., Huang P., Toleman C.A., Paterson A.J., Kudlow J.E. Proteasome function is regulated by cyclic AMP-dependent protein kinase through phosphorylation of RPT6. J. Biol. Chem. 2007, 282:22460-22471.