Characterization of the small heat shock protein Hsp27 gene in Chironomus riparius (Diptera) and its expression profile in response to temperature changes and xenobiotic exposures

Cell Stress and Chaperones

Volumn 19, Issue 4, 2014, Pages 529-540

  Martínez Paz, Pedro ^a   Morales, Mónica ^a   Martín, Raquel ^a   Martínez Guitarte, José Luis ^a   Morcillo, Gloria ^a  

^a UNIVERSIDAD NACIONAL DE EDUCACIÓN A DISTANCIA   (Spain)

Author keywords

4 Nonylphenol (NP); Bisphenol A (BPA); Cadmium; Cold heat shock; Tributyltin (TBT); Triclosan (TCS)

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; ALPHA CRYSTALLIN; BIOLOGICAL MARKER; CADMIUM; ENDOCRINE DISRUPTOR; HEAT SHOCK PROTEIN 27; MESSENGER RNA; NONYLPHENOL; SMALL HEAT SHOCK PROTEIN; TRIBUTYLTIN; TRICLOSAN; XENOBIOTIC AGENT; INSECT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHIRONOMUS RIPARIUS; COLD SHOCK RESPONSE; COLD STRESS; CONTROLLED STUDY; DIPTERA; DROSOPHILA MELANOGASTER; ECOTOXICOLOGY; FLUORESCENCE IN SITU HYBRIDIZATION; GENE; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENE MAPPING; GENE OVEREXPRESSION; HEAT SHOCK; HSC70 GENE; HSP27 GENE; HSP40 GENE; HSP90 GENE; MEDITERRANEAN FRUIT FLY; NONHUMAN; NUCLEOTIDE SEQUENCE; POLLUTANT; POLYTENE CHROMOSOME; PRIORITY JOURNAL; PROTEIN DOMAIN; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SARCOPHAGA; TEMPERATURE; UPREGULATION; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; CHIRONOMIDAE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGICAL STRESS; PHYSIOLOGY; SEQUENCE ALIGNMENT;

ALPHA-CRYSTALLINS; AMINO ACID SEQUENCE; ANIMALS; CHIRONOMIDAE; GENE EXPRESSION REGULATION; HSP27 HEAT-SHOCK PROTEINS; INSECT PROTEINS; MOLECULAR SEQUENCE DATA; SEQUENCE ALIGNMENT; STRESS, PHYSIOLOGICAL; TEMPERATURE; XENOBIOTICS;

EID: 84904093442     PISSN: 13558145     EISSN: 14661268     Source Type: Journal    
DOI: 10.1007/s12192-013-0479-y     Document Type: Article

References (83)

1. Antizar-Ladislao B (2008) Environmental levels, toxicity and human exposure to tributyltin (TBT)-contaminated marine environment. A review. Environ Int 34:292-308
2. Arrigo AP (1998) Small stress proteins: chaperones that act as regulators of intracellular redox state and programmed cell death. Biol Chem 379:19-26
3. Bierkens J, Maes J, Vander Plaetse F (1998) Dose-dependent induction of heat shock protein 70 synthesis in Raphidocelis subcapitata following exposure to different classes of environmental pollutants. Environ Pollut 101:91-97 (Pubitemid 28431995)
4. Bonham RT, Fine MR, Pollock FM, Shelden EA (2003) Hsp27, Hsp70 and metallothionein in MDCK and LLC-PK1 renal epithelial cells: effects of prolonged exposure to cadmium. Toxicol Appl Pharmacol 191:63-73 (Pubitemid 36959964)
5. Bruey JM, Ducasse C, Bonniaud P, Ravagnan L, Susin SA, Diaz-Latoud C, Gurbuxani S, Arrigo AP, Kroemer G, Solary E, Garrido C (2000) Hsp27 negatively regulates cell death by interacting with cytochrome C. Nat Cell Biol 2:645-652
6. Chen CP, Denlinger DL, Lee RE (1987) Cold-shock injury and rapid cold hardening in the flesh fly Sarcophaga crassipalpis. Physiol Zool 60:297-304
7. Clark MS, Worland MR (2008) How insects survive the cold: molecular mechanisms. J Comp Physiol B-Biochem Syst Environ Physiol 178:917-933
8. Colinet H, Lee SF, Hoffmann A (2010) Temporal expression of heat shock genes during cold stress and recovery fromchill coma in adult Drosophila melanogaster. FEBS J 277:174-185
9. Cousins IT, Staples CA, Klecka GM, Mackay D (2002) A multimedia assessment of the environmental fate of bisphenol A. Hum Ecol Risk Assess 8:1107-1135 (Pubitemid 41445941)
10. de Jong WW, Leunissen JA, Voorter CE (1993) Evolution of the alpha-crystallin/small heat-shock protein family.Mol Biol Evol 10:103-126 (Pubitemid 23040227)
11. Denlinger DL, Rinehart JP, Yocum GD (2001) Stress proteins: a role in insect diapause? In: Denlinger DL, Giebultowicz J, Saunders DS (eds) Insect timing: Circadian rhythmicity to seasonality. Elsevier, Amsterdam, pp 155-171
12. EPA (US) (1996) Chironomid sediment toxicity test, ecological effects test guidelines. EPA 712-C-96-313; 2nd ed. EPA 600/R-99/064, Washington DC, USA
13. Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243-282 (Pubitemid 29143171)
14. Franck E, Madsen O, van Rheede T, Ricard G, Huynen MA, de Jong WW (2004) Evolutionary diversity of vertebrate small heat shock proteins. J Mol Evol 59:792-805 (Pubitemid 40100875)
15. Fu X, Li W, Mao Q, Chang Z (2003) Disulfide bonds convert small heat shock protein Hsp16.3 from a chaperone to a non-chaperone: implications for evolution of cysteine in molecular chaperones. Biochem Biophys Res Commun 308:627-635 (Pubitemid 36945539)
16. Gkouvitsas T, Kontogiannatos D, Kourti A (2008) Differential expression of two small Hsps during diapause in the corn stalk borer Sesamia nonagrioides (Lef.). J Insect Physiol 54:1503-1510
17. Gopalakrishnan Nair PM, Park SY, Lee SW, Choi J (2011) Differential expression of ribosomal protein gene, gonadotrophin relasing hormone gene and Balbiani ring protein gene in silver nanoparticles exposed Chironomus riparius. Aquat Toxicol 101:31-37
18. Goto SG, Kimura MT (2004) Heat-shock-responsive genes are not involved in the adult diapause of Drosophila triauraria. Gene 326:117-122 (Pubitemid 38068492)
19. Gupta SC, Shrama A, Mishra M, Mishra RK, Chowdhuri DK (2010) Heat shock proteins in toxicology: how close and how far? Life Sci 86:377-384
20. Hao X, Zhang S, Timakov B, Zhang P (2007) The Hsp27 gene is not required for Drosophila development but its activity is associated with starvation resistance. Cell Stress Chaperones 12:364-372
21. Hartl FU, Hayer-Hartl M (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295:1852-1858 (Pubitemid 34214115)
22. Hatakeyama S (1988) Chronic effects of Cu on reproduction of Polypedilum nubifer (Chironomidae) through water and food. Ecotoxicol Environ Saf 16:1-10
23. Hinther A, Bromba CM, Wulff JE, Helbing CC (2011) Effects of triclocarban, triclosan, and methyl triclosan on thyroid hormone action and stress in frog and mammalian culture systems. Environ Sci Technol 45:5395-5402
24. Hoffmann AA, Parsons PA (1991) Evolutionary genetics and environmental stress. Oxford University Press, New York
25. Hoffmann AA, Sørensen JG, Loeschcke V (2003) Adaptation of Drosophila to temperature extremes: bringing together quantitative and molecular approaches. J Therm Biol 28:175-216 (Pubitemid 36383351)
26. Huang LH, Kang L (2007) Cloning and interspecific altered expression of heat shock protein genes in two leafminer species in response to thermal stress. Insect Mol Biol 16:491-500
27. Huang LH, Wang CZ, Kang L (2009) Cloning and expression of five heat shock protein genes in relation to cold hardening and development in the leafminer, Liriomyza sativae. J Insect Physiol 55:279-285
28. Karouna-Renier NK, Rao KR (2009) An inducible HSP70 gene from the midge Chironomus dilutus: characterization and transcription profile under environmental stress. Insect Mol Biol 18:87-96
29. Karouna-Renier NK, Zehr JP (2003) Short-term exposures to chronically toxic copper concentrations induce HSP70 proteins in the midge larvae (Chironomus tentans) . Sci Total Environ 312:267-272 (Pubitemid 36836216)
30. Kokolakis G, Tatari M, Zacharopoulou A, Mintzas AC (2008) The hsp27 gene of the Mediterranean fruit fly, Ceratitis capitata: structural characterization, regulation and developmental expression. Insect Mol Biol 17:699-710
31. Lee SB, Choi J (2006) Multilevel evaluation of nonylphenol toxicity in fourth-instar larvae of Chironomus riparius (Diptera, Chironomidae). Environ Toxicol Chem 25:3006-3014
32. Lee RE, Chen CP, Denlinger DL (1987) A rapid cold-hardening process in insects. Science 238:1415-1417
33. Li AQ, Popova-Butler A, Dean DH, Denlinger DL (2007) Proteomics of the flesh fly brain reveals an abundance of upregulated heat shock proteins during pupal diapause. J Insect Physiol 53:385-391 (Pubitemid 46498096)
34. Lindquist S (1980) Varying patterns of protein synthesis in Drosophila during heat shock: implications for regulation. Dev Biol 77:463-479
35. Liu Z, Xi D, Kang M, Guo X, Xu B (2012) Molecular cloning and characterization of Hsp27.6: the first reported small heat shock protein from Apis cerana cerana. Cell Stress Chaperones 17:539-551
36. Martinez EA, Moore BC, Schaumloffel J, Dasgupta N (2003) Morphological abnormalities in Chironomus tentans exposed to cadmium and copper-spiked sediments. Ecotoxicol Environ Saf 55:204-212 (Pubitemid 36555406)
37. Martínez-Guitarte JL, Planelló R, Morcillo G (2007) Characterization and expression during development and under environmental stress of the genes encoding ribosomal proteins L11 and L13 in Chironomus riparius. Comp Biochem Physiol B Biochem Mol Biol 147:590-596 (Pubitemid 46929094)
38. Martínez-Paz P, Morales M, Martínez-Guitarte JL, Morcillo G (2012) Characterization of a cytochrome P450 gene (CYP4G) and modulation under different exposures to xenobiotics (tributyltin, nonylphenol, bisphenol A) in Chironomus riparius aquatic larvae. Comp Biochem Physiol C-Toxicol Pharmacol 155:333-343
39. Michailova P, Petrova N, Ilkova J, Bovero S, Brunetti S, White K, Sella G (2006) Genotoxic effect of copper on salivary gland polytene chromosomes of Chironomus riparius Meigen 1804 (Diptera, Chironomidae). Environ Pollut 144:647-654 (Pubitemid 44363116)
40. Morales M, Planelló R, Martínez-Paz P, Herrero O, Cortés E, Martínez-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
41. Morales M, Martínez-Paz P, Ozáez I, Martínez- Guitarte JL, Morcillo G (2013) DNA damage and transcriptional changes induced by tributyltin (TBT) after short in vivo exposures of Chironomus riparius (Diptera) larvae. Comp Biochem Physiol C-Toxicol Pharmacol 158:57-63
42. Morcillo G, Barettino D, Carmona MJ, Carretero T, Díez JL (1988) Telomeric-DNA sequences differentially activated by heat-shock in two chironomus subspecies. Chromosoma 96:139-144
43. Morrow G, Battistini S, Zhang P, Tanguay RM (2004) Decreased lifespan in the absence of expression of the mitochondrial small heat shock protein Hsp22 in Drosophila. J Biol Chem 279:43382-43385 (Pubitemid 39390636)
44. Nolen EAA, Morimoto RI (2002) Chaperoning signaling pathways: molecular chaperones as stress-sensing heat shock proteins. J Cell Sci 115:2809-2816
45. OECD. Organisation for Economic Co-operation and Development (2001) Guideline for testing of chemicals, sediment-water chironomid toxicity test using spiked sediment. 218 pp
46. Ozáez I, Martinez-Guitarte JL, Morcillo G (2013) Effects of in vivo exposure to UV filters (4-MBC, OMC, BP-3, 4-HB, OC, OD-PABA) on endocrine signaling genes in the insect Chironomus riparius. Sci Total Environ 456-457:120-126
47. Park K, Kwak IS (2008) Characterization of heat shock protein 40 and 90 in Chironomus riparius larvae: effects of di(2-ethylhexyl) phthalate exposure on gene expressions and mouthpart deformities. Chemosphere 74:89-95
48. Park K, Kwak IS (2009) Alcohol dehydrogenase gene expression in Chironomus riparius exposed to di(2-ethylhexyl) phthalate. Comp Biochem Comp Biochem Physiol C-Toxicol Pharmaco 150361-367
49. Park K, Kwak IS (2010) Molecular effects of endocrine-disrupting chemicals on the Chironomus riparius estrogen-related receptor gene. Chemosphere 79:934-941
50. Parsell DA, Lindquist S (1993) The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu Rev Genet 27:437-496 (Pubitemid 24011359)
51. Planelló R, Martínez-Guitarte JL, Morcillo G (2007) Ribosomal genes as early targets of cadmium-induced toxicity in Chironomus riparius larvae. Sci Total Environ 373:113-121 (Pubitemid 46107634)
52. Planelló R, Martínez-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
53. Planelló R, Martínez-Guitarte JL, Morcillo G (2010) Effect of acute exposure to cadmium on the expression of heat-shock and hormone-nuclear receptor genes in the aquatic midge Chironomus riparius. Sci Total Environ 408:1598-1603
54. Planelló R, Herrrero O, Martínez-Guitarte JL, Morcillo G (2011) Comparative effects of butyl benzyl phthalate (BBP) and di-2-ethylhexyl phthalate (DEHP) on the aquatic larvae of Chironomus riparius based on gene expression assays related to the endocrine system, the stress response and ribosomes. Aquat Toxicol 105:62-70
55. Qin W, Neal SJ, Robertson RM, Westwood JT, Walker VK (2005) Cold hardening and transcriptional change in Drosophila melanogaster. Insect Mol Biol 14:607-613 (Pubitemid 44914743)
56. Raut SA, Angus RA (2010) Triclosan has endocrine-disrupting effects in male western mosquitofish Gambusia affinis. Environ Toxicol Chem 29:1287-1291
57. Reineke A (2005) Identification and expression of a small heat shock protein in two lines of the endoparasitic wasp Venturia canescens. Comp Biochem Physiol A-Mol Integr Physiol 141:60-69
58. Rinehart JP, Li A, Yocum GD, Robich RM, Hayward SA, Denlinger DL (2007) Up-regulation of heat shock proteins is essential for cold survival during insect diapause. Proc Natl Acad Sci U S A 104:11130-11137 (Pubitemid 47175106)
59. Robich RM, Rinehart JP, Kitchen LJ, Denlinger DL (2007) Diapause-specific gene expression in the northern house mosquito, Culex pipiens L., identified by suppressive subtractive hybridization. J Insect Physiol 53:235-245 (Pubitemid 46349109)
60. Sakano D, Li B, Xia Q, Yamamoto K, Banno Y, Fujii H, Aso Y (2006) Genes encoding small heat shock proteins of the silkworm, Bombyx mori. Biosci Biotechnol Biochem 70:2443-2450 (Pubitemid 44656410)
61. Silver JT, Noble EG (2012) Regulation of survival gene hsp70. Cell Stress Chaperones 17:1-9
62. Sinclair BJ, Gibbs AG, Roberts SP (2007) Gene transcription during exposure to, and recovery from, cold and desiccation stress in Drosophila melanogaster. Insect Mol Biol 16:435-443 (Pubitemid 47094272)
63. Snell TW, Brogdon SE, Morgan MB (2003) Gene expression profiling in ecotoxicology. Ecotoxicology 12:475-483 (Pubitemid 37485480)
64. Soares A, Guieysse B, Fefferson B, Cartmell E, Lester JN (2008) Nonylphenol in the environment: a critical review on occurrence, fate, toxicity and treatment in wastewaters. Environ Int 34:1033-1049
65. Sonoda S, Ashfaq M, Tsumuki H (2006) Cloning and nucleotide sequencing of three heat shock protein genes (hsp90, hsc70 and hsp19.5) from the Diamondback moth, Plutella xylostella (L.) and their expression in relation to developmental stage and temperature. Arch Insect Biochem Physiol 62:80-90 (Pubitemid 43987537)
66. Sonoda S, Ashfaq M, Tsumuki H (2007) A comparison of heat shock protein genes from cultured cells of the Cabbage armyworm, Mamestra brassicae, in response to heavy metals. Arch Insect Biochem Physiol 65:210-222 (Pubitemid 47242719)
67. Sorensen JG, Kristensen TN, Loeschcke V (2003) The evolutionary and ecological role of heat shock proteins. Ecol Lett 6:1025-1037 (Pubitemid 37365491)
68. Southgate R, Ayme A, Voellmy R (1983) Nucleotide sequence analysis of the Drosophila small heat shock gene cluster at locus 67B. J Mol Biol 165:35-57 (Pubitemid 13122845)
69. Sun Y, MacRae TH (2005) Small heat shock proteins:molecular structure and chaperone function. Cell Mol Life Sci 62:2460-2476 (Pubitemid 41801099)
70. Tachibana S, Numata H, Goto SG (2005) Gene expression of heat-shock proteins (Hsp23, Hsp70 and Hsp90) during and after larval diapause in the blow fly Lucilia sericata. J Insect Physiol 51:641-647 (Pubitemid 40886408)
71. Tammariello SP, Rinehart JP, Denlinger DL (1999) Desiccation elicits heat shock protein transcription in the flesh fly, Sarcophaga crassipalpis, but does not enhance tolerance to high or low temperatures. J Insect Physiol 45:933-938 (Pubitemid 29379004)
72. Tsvetkova NM, Horváth I, Török Z, Wolkers WF, Balogi Z, Shigapova N, Crowe LM, Tablin F, Vierling E, Crowe JH, Vigh L (2002) Small heat-shock proteins regulate membrane lipid polymorphism. Proc Natl Acad Sci U S A 99:13504-13509 (Pubitemid 35215411)
73. Vazquez J, Pauli D, Tissieres A (1993) Transcriptional regulation in Drosophila during heat shock: a nuclear run-on analysis. Chromosoma 102:233-248 (Pubitemid 23094986)
74. Veldhoen N, Skirrow RC, Osachoff H, Wigmore H, Clapson DJ, Gunderson MP, Van Aggelen G, Helbing CC (2006) The bactericidal agent triclosan modulates thyroid hormone-associated gene expression and disrupts postembryonic anuran development. Aquat Toxicol 80:217-227 (Pubitemid 44768034)
75. Wang HD, Kazemi-Esfarjani P, Benzer S (2004) Multiple-stress analysis for isolation of Drosophila longevity genes. Proc Natl Acad Sci U S A 101:12610-12615 (Pubitemid 39122072)
76. Wang HS, Wang XH, Zhou CS, Huang LH, Zhang SF, Guo W, Kang L (2007) cDNA cloning of heat shock proteins and their expression in the two phases of the migratory locust. Insect Mol Biol 16:207-219 (Pubitemid 46376343)
77. Wang F, Feng M, Xu P, Xiao H, Niu P, Yang X, Bai Y, Peng Y, Yao P, Tan H, Tanguay RM, Wu T (2009) The level of Hsp27 in limphocytes is negatively associated with a higher risk of lung cancer. Cell Stress Chaperones 14:245-251
78. Waters ER, Aevermann BD, Sanders-Reed Z (2008) Comparative analysis of the small heat shock proteins in three angiosperm genomes. Cell Stress Chaperones 13:127-142
79. Williams K, Green A, Pascoe DW, Gower DE (1987) Effects of cadmium on oviposition and egg viability in Chironomus riparius (Diptera: Chironomidae). Bull Environ Contam Toxicol 38:86-90 (Pubitemid 17001600)
80. Xu P, Xiao J, Liu L, Li T, Huang D (2010) Molecular cloning and characterization of four heat shock protein genes from Macrocentrus cingulum (Hymenoptera: Braconidae). Mol Biol Rep 37:2265-2272
81. Yang QL, Yao CL, Wang ZY (2012) Acute temperature and cadmium stress response characterization of small heat shock protein 27 in large yellow croaker, Larimichthys crocea. Comp Biochem Physiol C-Toxicol Pharmacol 155:190-197
82. Yocum GD, Joplin KH, Denlinger DL (1998) Upregulation of a 23 kDa small heat shock protein transcript during pupal diapause in the flesh fly, Sarcophaga crassipalpis. Insect Biochem Mol Biol 28:677-682 (Pubitemid 28424075)
83. Yoshimi T, Minowa K, Karouna-Renier NK, Watanabe C, Sugaya Y, Miura T (2002) Activation of a stress-induced gene by insecticides in the midge, Chironomus yoshimatsui. J Biochem Mol Toxicol 16:10-17 (Pubitemid 34211258)