Differential transcription of heat shock protein 90 (HSP90) in the dinoflagellate Prorocentrum minimum by copper and endocrine-disrupting chemicals

Ecotoxicology

Volumn 21, Issue 5, 2012, Pages 1448-1457

  Guo, Ruoyu ^a   Ki, Jang Seu ^a  

^a Sangmyung University   (South Korea)

Author keywords

Environmental stress; Gene expression; HSP90; Prorocentrum minimum; Toxic

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; AMINO ACID; COPPER; ENDOCRINE DISRUPTOR; HEAT SHOCK PROTEIN 90; METAL; POLYCHLORINATED BIPHENYL; POLYPEPTIDE;

COPPER; DINOFLAGELLATE; DOSE-RESPONSE RELATIONSHIP; ENDOCRINE DISRUPTOR; GENE EXPRESSION; PROTEIN; SURVIVAL; TEMPERATURE TOLERANCE;

ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DINOFLAGELLATE; GENE; GENE EXPRESSION; GENETIC CODE; GENETIC CONSERVATION; GENETIC TRANSCRIPTION; GENOTOXICITY; HEAT SHOCK PROTEIN 90 GENE; HSP90 GENE; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PRIORITY JOURNAL; PROROCENTRUM MINIMUM; REAL TIME POLYMERASE CHAIN REACTION; TEMPERATURE STRESS; THERMAL EXPOSURE; UPREGULATION;

AMINO ACID SEQUENCE; COPPER; DINOFLAGELLIDA; ENDOCRINE DISRUPTORS; GENE EXPRESSION; HSP90 HEAT-SHOCK PROTEINS; MOLECULAR SEQUENCE DATA; OPEN READING FRAMES; PHYLOGENY; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS;

ALGAE; DINOPHYCEAE; PROROCENTRUM MINIMUM;

EID: 84865031665     PISSN: 09639292     EISSN: 15733017     Source Type: Journal    
DOI: 10.1007/s10646-012-0898-z     Document Type: Article

References (47)

1. Aluru N, Jorgensen EH,Maule AG, VijayanMM(2004) PCB disruption of the hypothalamus-pituitary-interrenal axis involves brain glucocorti coid receptor downregulation in anadromousArctic charr.AmJ Physiol Regul Integr Comp Physiol 287:787-793
2. Coteur G, Danis B, Fowler SW, Teyssié JL, Dubois P, Warnau M (2001) Effects of PCBs on reactive oxygen species (ROS) production by the immune cells of Paracentrotus lividus (Echinodermata). Mar Pollut Bull 42:667-672
3. Crevel G, Bates H, Huikeshoven H, Cotterill S (2001) The Drosophila Dpit47 protein is a nuclear Hsp90 co-chaperone that interacts with DNA polymerase alpha. J Cell Sci 114:2015-2025
4. Efeoǧlu B (2009) Heat shock proteins and heat shock response in plants. GUJ Sci 22:67-75
5. Fast NM, Xue L, Bingham S, Keeling PJ (2002) Re-examining alveolate evolution using multiple protein molecular phylogenies. J Eukaryot Microbiol 49:30-37
6. Fukuda Y, Endoh H (2008) Phylogenetic analyses of the dinoflagellate Noctiluca scintillans based on b-tubulin and Hsp90 genes. Eur J Protistol 44:27-33
7. Fukuda A, Ishii Y, Tasaki K, Matsusue K, Ishida T, Oguri K (1999) Induction of molecular chaperones HSP70 and HSP90 in rat liver cytosol by a highly toxic coplanar PCB. Fukuoka Igaku Zasshi 90:259-271
8. Gaetke LM, Chow CK (2003) Copper toxicity, oxidative stress, and antioxidant nutrients. Toxicology 189:147-163
9. Gao Q, Song L, Ni D, Wu L, Zhang H, Chang Y (2007) cDNA cloning and mRNA expression of heat shock protein 90 gene in the haemocytes of Zhikong scallop Chlamys farreri. Comp Biochem Physiol B Biochem Mol Biol 147:704-715
10. Guo R, Ki J-S (2011a) Evaluation and validation of internal control genes for studying gene expression in the dinoflagellate Prorocentrum minimum using real-time PCR. Eur J Protistol. doi: 10.1016/j.ejop.2011.11.001
11. Guo R, Ki J-S (2011b) Spliced leader sequences detected from EST data of the dinoflagellates, Cochlodinium polykrikoides and Prorocentrum minimum. Algae 26:229-235
12. Gupta SC, Sharma A, Mishra M, Mishra RK, Chowdhuri DK (2010) Heat shock proteins in toxicology: how close and how far? Life Sci 86:377-384
13. Hackett JD, Bhattacharya D (2006) The genomes of dinoflagellates. In: KatzLA,BhattacharyaD(eds)Genomics and evolution ofmicrobial eukaryotes. Oxford University Press, New York, pp 48-63
14. Hackett JD, Anderson DM, Erdner DL, Bhattacharya D (2004) Dinoflagellates: a remarkable evolutionary experiment. Am J Bot 91:1523-1534
15. Hao H, Naomoto Y, Bao X, Watanabe N, Sakurama K, Noma K, Motoki T, Tomono Y, Fukazawa T, Shirakawa Y, Yamatsuji T, Matsuoka J, Takaoka M (2010) HSP90 and its inhibitors. Oncol Rep 23:1483-1492
16. Hoppenrath M, Leander BS (2010) Dinoflagellate phylogeny as inferred from heat shock protein 90 and ribosomal gene sequences. PLoS ONE 5:e13220. doi:10.1371/journal.pone.0013220
17. Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ (1998) Multiple sequence alignment with Clustal X. Trends Biochem Sci 23:403-405
18. Jönsson ME, Gao K, Olsson JA, Goldstone JV, Brandt I (2010) Induction patterns of new CYP1 genes in environmentally exposed rainbow trout. Aquat Toxicol 98:311-321
19. Kim B-E, Nevit T, Thiele DJ (2008) Mechanisms for copper acquisition distribution and regulation. Nat Chem Biol 4: 176-185
20. Kovacic P (2010) How safe is bisphenol A? fundamentals of toxicity: metabolism, electron transfer and oxidative stress. Med Hypotheses 75:1-4
21. Leander BS, Keeling PJ (2004) Early evolutionary history of dinoflagellates and apicomplexans (Alveolata) as inferred from Hsp90 and actin phylogenies. J Phycol 40:341-350
22. Levy G, Lutz I, Krüger A, Kloas W (2004) Bisphenol A induces feminization in Xenopus laevis tadpoles. Environ Res 94: 102-111
23. Li R, Chen G-Z, Tam NFY, Luan T-G, Shin PKS, Cheung SG, Liu Y (2009) Toxicity of bisphenol A and its bioaccumulation and removal by a marine microalga Stephanodiscus hantzschii. Ecotox Environ Safe 72:321-328
24. Lin S, Zhang H, Jiao N (2006) Potential utility of mitochondrial cytochrome b and its mRNA editing in resolving closely related dinoflagellates: a case study of Prorocentrum (Dinophyceae). J Phycol 42:646-654
25. Liu H, Chen H, Jing J, Ma X (2011) Cloning and characterization of the HSP90 beta gene from Tanichthys albonubes Lin (Cyprinidae): effect of copper and cadmium exposure. Fish Physiol Biochem. doi:10.1007/s10695-011-9556-2
26. Mensink BJWG, Smit CE, Montforts MHMM (2008) Manual for summarising and evaluating environmental aspects of plant protection products. RIVM report 601712004/2008. National Institute for Public Health and the Environment, RIVM, Bilthoven, The Netherlands
27. Millán de Kuhn R, Streb C, Breiter R, Richter P, Neesse T, Häder DP (2006) Screening for unicellular algae as possible bioassay organisms for monitoring marine water samples. Water Res 40: 2695-2703
28. Morales M, Planelló R, Mart́nez-Paz P, Herrero O, Cortés E, Mart́nez-Guitarte JL, Morcillo G (2011) Characterization of Hsp70 gene in Chironomus riparius: expression in response to endocrine disrupting pollutants as a marker of ecotoxicological stress. Comp Biochem Physiol C Toxicol Pharmacol 153:150-158
29. Mukhopadhyay I, Nazir A, Saxena DK, Chowdhuri DK (2003) Heat shock response: hsp70 in environmental monitoring. J Biochem Mol Toxicol 17:249-254
30. Organization for Economic Co-operation and Development (OECD) (2006) Freshwater alga and cyanobacteria, growth inhibition test. Guideline no. 201 (adopted 23 Mar. 2006). OECD guidelines for testing of chemicals, OECD, Paris
31. Papaconstantinou AD, Goering PL, Umbreit TH, Brown KM (2003) Regulation of uterine hsp90a, hsp72 and HSF-1 transcription in B6C3F1 mice by b-estradiol and bisphenol A: involvement of the estrogen receptor and protein kinase C. Toxicol Lett 144: 257-270
32. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45
33. Planelló R, Mart́nez-Guitarte JL, Morcillo G (2008) The endocrine disruptor bisphenol A increases the expression of HSP70 and ecdysone receptor genes in the aquatic larvae of Chironomus riparius. Chemosphere 71:1870-1876
34. Prodromou C, Pearl LH (2003) Structure and functional relationships of Hsp90. Curr Cancer Drug Targets 3:301-323
35. Rhee J-S, Raisuddin S, Lee K-W, Seo J-S, Ki J-S, Kim I-C, Park HG, Lee J-S (2009) Heat shock protein (Hsp) gene responses of the intertidal copepod Tigriopus japonicus to environmental toxicants. Comp Biochem Physiol C Toxicol Pharmacol 149: 104-112
36. Rosic NN, Pernice M, Dove S, Dunn S, Hoegh-Guldberg O (2011) Gene expression profiles of cytosolic heat shock proteins Hsp70 and Hsp90 from symbiotic dinoflagellates in response to thermal stress: possible implications for coral bleaching. Cell Stress Chaperon 16:69-80
37. Sano J, Kato KH (2009) Localization and copy number of the proteincoding genes actin, alpha-tubulin, and HSP90 in the nucleus of a primitive dinoflagellate, Oxyrrhis marina. Zoolog Sci 26: 745-753
38. Shalchian-Tabrizi K, Minge MA, Cavalier-Smith T, Nedreklepp JM, Klaveness D, Jakobsen KS (2006) Combined heat shock protein 90 and ribosomal RNA sequence phylogeny supports multiple replacements of dinoflagellate plastids. J Eukaryot Microbiol 53:217-224
39. Sørensen JG, Kristensen TN, Loeschcke V (2003) The evolutionary and ecological role of heat shock proteins. Ecol Lett 6: 1025-1037
40. Stephanou A, Latchman DS (2011) Transcriptional modulation of heat-shock protein gene expression. Biochem Res Int. doi: 10.1155/2011/238601
41. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731-2739
42. Venn AA, Quinn J, Jones R, Bodnar A (2009) P-glycoprotein (multixenobiotic resistance) and heat shock protein gene expression in the reef coral Montastraea franksi in response to environmental toxicants. Aquat Toxicol 93:188-195
43. Vijayan MM, Aluru N, Maule AG, Jørgensen EH (2006) Fasting augments PCB impact on liver metabolism in anadromous Arctic char. Toxicol Sci 91:431-439
44. Welch WJ, Feramisco JR (1982) Purification of the major mammalian heat shock proteins. J Biol Chem 257:14949-14959
45. Zhang J, Hou Y, Miranda L, Campbell D, Sturm NR, Gaasterland T, Lin S (2007) Spliced leader RNA trans-splicing in dinoflagellates. Proc Natl Acad Sci USA 104:4618-4623
46. Zhang H, Campbell DA, Sturm NR, Lin S (2009) Dinoflagellate spliced leader RNA genes display a variety of sequences and genomic arrangements. Mol Biol Evol 26:1757-1771
47. Zhang H, Campbell DA, Sturm NR, Dungan CF, Lin S (2011) Spliced leader RNAs, mitochondrial gene frameshifts and multi-protein phylogeny expand support for the genus Perkinsus as a unique group of alveolates. PLoS ONE 6:e19933