Cell Stress and Chaperones

, 15:83 | Cite as

Identification of a novel inducible cytosolic Hsp70 gene in Chinese shrimp Fenneropenaeus chinensis and comparison of its expression with the cognate Hsc70 under different stresses

Original Paper

Abstract

The heat shock protein 70 (Hsp70) family is widely expressed in eukaryotic cells as the major chaperone protein. In this study, the full-length complementary DNA (cDNA) of a novel inducible cytosolic Hsp70 family member (FcHsp70) was cloned from Fenneropenaeus chinensis. FcHsp70 full-length cDNA consists of 2,511 bp with a 1,890-bp open reading frame encoding 629 amino acids. Three Hsp70 protein family signatures, IDLGTTYS, IIDLGGGTFDVSIL, and IVLVGGSTRIPKVQK, were found in the predicted FcHsp70 amino acid sequence. Phylogenetic analysis showed that FcHsp70 was categorized together with the inducible HSP70s reported in other crustaceans. Compared to the previously identified cognate Hsp70 (FcHsc70) in F. chinensis, the expression of FcHsp70 showed quite different expression profiles when the shrimp were subjected to different stresses including heat shock and heavy metal treatments. Under heat shock treatment, the expression of FcHsp70 showed much higher up-regulation than FcHsc70. Copper treatment also induced higher up-regulation of FcHsp70 than FcHsc70. Cadmium treatment did not induce the expression of FcHsp70, but caused down-regulation of FcHsc70. The different expression profiles of FcHsp70 and FcHsc70 in shrimp may indicate their different reactions to different stresses. Therefore, Hsp70 or Hsc70 could be developed as a biomarker to indicate different stresses in shrimp.

Keywords

Heat shock proteins Hsp70 Heat shock Heavy metal Stress Fenneropenaeus chinensis 

Notes

Acknowledgments

This work was supported by the National High-Tech Research and Development Program of China (863 program) 2006AA09Z424 and 2006AA10A402 and the Major State Basic Research Development Program of China (973 program) 2006CB101804.

References

  1. Asea A, Rehli M, Kabingu E et al (2002) Novel signal transduction pathway utilized by extracellular HSP70 role of Toll-like receptor (TLR) 2 and TLR4. J Biol Chem 277(17):15028–15034. doi: 10.1074/jbc.M200497200 CrossRefPubMedGoogle Scholar
  2. Boone AN, Vijayan MM (2002) Constitutive heat shock protein 70 (HSC70) expression in rainbow trout hepatocytes: effect of heat shock and heavy metal exposure. Comp Biochem Physiol C Toxicol Pharmacol 132(2):223–233. doi: 10.1016/S1532-0456(02)00066-2 CrossRefPubMedGoogle Scholar
  3. Boorstein WR, Craig EA (1990) Regulation of a yeast HSP70 gene by a cAMP responsive transcriptional control element. EMBO J 9(8):2543–2553PubMedGoogle Scholar
  4. Boutet I, Tanguy A, Rousseau S, Auffret M, Moraga D (2003) Molecular identification and expression of heat shock cognate 70 (hsc70) and heat shock protein 70 (hsp70) genes in the Pacific oyster Crassostrea gigas. Cell Stress Chaperones 8(1):76–85. doi: 10.1379/1466-1268(2003)8<76:MIAEOH>2.0.CO;2 CrossRefPubMedGoogle Scholar
  5. Bukau B, Horwich AL, Cycles H (1998) The Hsp70 and Hsp60 review chaperone machines. Cell 92:351–366. doi: 10.1016/S0092-8674(00)80928-9 CrossRefPubMedGoogle Scholar
  6. Calabrese A, MacInnes JR, Nelson DA, Miller JE (1977) Survival and growth of bivalve larvae under heavy-metal stress. Mar Biol 41(2):179–184. doi: 10.1007/BF00394024 CrossRefGoogle Scholar
  7. Cellura C, Toubiana M, Parrinello N, Roch P (2006) HSP70 gene expression in Mytilus galloprovincialis hemocytes is triggered by moderate heat shock and Vibrio anguillarum, but not by V. splendidus or Micrococcus lysodeikticus. Dev Comp Immunol 30(11):984–997. doi: 10.1016/j.dci.2005.12.009 CrossRefPubMedGoogle Scholar
  8. Chuang KH, Ho SH, Song YL (2007) Cloning and expression analysis of heat shock cognate 70 gene promoter in tiger shrimp (Penaeus monodon). Gene 405(1–2):10–18. doi: 10.1016/j.gene.2007.08.016 CrossRefPubMedGoogle Scholar
  9. Clayton ME, Steinmann R, Fent K (2000) Different expression patterns of heat shock proteins hsp 60 and hsp 70 in zebra mussels (Dreissena polymorpha) exposed to copper and tributyltin. Aquat Toxicol 47(3–4):213–226. doi: 10.1016/S0166-445X(99)00022-3 CrossRefGoogle Scholar
  10. Daugaard M, Rohde M, Jaattela M (2007) The heat shock protein 70 family: highly homologous proteins with overlapping and distinct functions. FEBS Lett 581(19):3702–3710. doi: 10.1016/j.febslet.2007.05.039 CrossRefPubMedGoogle Scholar
  11. Demand J, Luders J, Hohfeld J (1998) The carboxy-terminal domain of Hsc70 provides binding sites for a distinct set of chaperone cofactors. Mol Cell Biol 18(4):2023–2028PubMedGoogle Scholar
  12. Ellis J (1987) Proteins as molecular chaperones. Nature 328(6129):378–379. doi: 10.1038/328378a0 CrossRefPubMedGoogle Scholar
  13. Farcy E, Serpentini A, Fievet B, Lebel JM (2007) Identification of cDNAs encoding HSP70 and HSP90 in the abalone Haliotis tuberculata: transcriptional induction in response to thermal stress in hemocyte primary culture. Comp Biochem Physiol B Biochem Mol Biol 146(4):540–550. doi: 10.1016/j.cbpb.2006.12.006 CrossRefPubMedGoogle Scholar
  14. Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282. doi: 10.1146/annurev.physiol.61.1.243 CrossRefPubMedGoogle Scholar
  15. Flaherty KM, DeLuca-Flaherty C, McKay DB (1990) Three-dimensional structure of the ATPase fragment of a 70K heat-shock cognate protein. Nature 346(6285):623–628. doi: 10.1038/346623a0 CrossRefPubMedGoogle Scholar
  16. Flemming CA, Trevors JT (1989) Copper toxicity and chemistry in the environment: a review. Water Air Soil Pollut 44(1):143–158. doi: 10.1007/BF00228784 CrossRefGoogle Scholar
  17. Franzellitti S, Fabbri E (2005) Differential HSP70 gene expression in the Mediterranean mussel exposed to various stressors. Biochem Biophys Res Commun 336(4):1157–1163. doi: 10.1016/j.bbrc.2005.08.244 CrossRefPubMedGoogle Scholar
  18. Gething MJ, Sambrook J (1992) Protein folding in the cell. Nature 355(6355):33–45. doi: 10.1038/355033a0 CrossRefPubMedGoogle Scholar
  19. Guhathakurta H, Kaviraj A (2000) Heavy metal concentration in water, sediment, shrimp (Penaeus monodon) and mullet (Liza parsia) in some brackish water ponds of Sunderban, India. Mar Pollut Bull 40(11):914–920. doi: 10.1016/S0025-326X(00)00028-X CrossRefGoogle Scholar
  20. Jiang J, Prasad K, Lafer EM, Sousa R (2005) Structural basis of interdomain communication in the Hsc70 chaperone. Mol Cell 20(4):513–524. doi: 10.1016/j.molcel.2005.09.028 CrossRefPubMedGoogle Scholar
  21. Jiao C, Wang Z, Li F, Zhang C, Xiang J (2004) Cloning, sequencing and expression analysis of cDNA encoding a constitutive heat shock protein 70 (HSC70) in Fenneropenaeus chinensis. Chin Sci Bull 49(22):2385–2393. doi: 10.1360/982004-120 CrossRefGoogle Scholar
  22. Johnson BD, Schumacher RJ, Ross ED, Toft DO (1998) Hop modulates hsp70/hsp90 interactions in protein folding. J Biol Chem 273(6):3679–3686. doi: 10.1074/jbc.273.6.3679 CrossRefPubMedGoogle Scholar
  23. Kappes B, Suetterlin BW, Hofer-Warbinek R, Humar R, Franklin RM (1993) Two major phosphoproteins of Plasmodium falciparum are heat shock proteins. Mol Biochem Parasitol 59(1):83–94. doi: 10.1016/0166-6851(93)90009-M CrossRefPubMedGoogle Scholar
  24. Karouna-Renier NK, Zehr JP (2003) Short-term exposures to chronically toxic copper concentrations induce HSP70 proteins in midge larvae (Chironomus tentans). Sci Total Environ 312(1–3):267–272. doi: 10.1016/S0048-9697(03)00254-7 CrossRefPubMedGoogle Scholar
  25. Li FH, Luan W, Zhang CS, Zhang JQ, Wang B, Xie YS, Li SH, Xiang JH (2009) Cloning of cytoplasmic heat shock protein 90 (FcHSP90) from Fenneropenaeus chinensis and its expression response to heat shock and hypoxia. Cell Stress Chaperones 14:161–172. doi: 10.1007/s12192-008-0069-6 CrossRefPubMedGoogle Scholar
  26. Lindquist S (1986) The heat-shock response. Ann Rev Biochem 55(1):1151–1191. doi: 10.1146/annurev.bi.55.070186.005443 CrossRefPubMedGoogle Scholar
  27. Liu J, Yang WJ, Zhu XJ, Karouna-Renier NK, Rao RK (2004) Molecular cloning and expression of two HSP70 genes in the prawn, Macrobrachium rosenbergii. Cell Stress Chaperones 9(3):313–323. doi: 10.1379/CSC-40R.1 CrossRefPubMedGoogle Scholar
  28. Lo WY, Liu KF, Liao IC, Song YL (2004) Cloning and molecular characterization of heat shock cognate 70 from tiger shrimp (Penaeus monodon). Cell Stress Chaperones 9(4):332–343. doi: 10.1379/CSC-47R.1 CrossRefPubMedGoogle Scholar
  29. Luan W, Li F, Zhang J, Wang B, Xiang J (2007) Cloning and expression of glucose regulated protein 78 (GRP78) in Fenneropenaeus chinensis. Mol Biol Rep 36(2):289–298. doi: 10.1007/s11033-007-9178-z CrossRefPubMedGoogle Scholar
  30. Mayer MP, Schröder H, Rüdiger S, Paal K, Laufen T, Bukau B (2000) Multistep mechanism of substrate binding determines chaperone activity of Hsp70. Nat Struct Biol 7:586–593. doi: 10.1038/76819 CrossRefPubMedGoogle Scholar
  31. McCarty JS, Walker GC (1991) DnaK as a thermometer: threonine-199 is site of autophosphorylation and is critical for ATPase activity. Proc Natl Acad Sci U S A 88(21):9513–9517. doi: 10.1073/pnas.88.21.9513 CrossRefPubMedGoogle Scholar
  32. Miller EK, Raese JD, Morrison-Bogorad M (1991) Expression of heat shock protein 70 and heat shock cognate 70 messenger RNAs in rat cortex and cerebellum after heat shock or amphetamine treatment. J Neurochem 56(6):2060–2071. doi: 10.1111/j.1471-4159.1991.tb03467.x CrossRefPubMedGoogle Scholar
  33. Moksnes PO, Lindahl U, Haux C (1995) Metallothionein as a bioindicator of heavy metal exposure in the tropical shrimp, Penaeus vannamei: a study of dose-dependent induction. Mar Environ Res 39(1–4):143–146. doi: 10.1016/0141-1136(94)00057-V CrossRefGoogle Scholar
  34. Murata M, Gong P, Suzuki K, Koizumi S (1999) Differential metal response and regulation of human heavy metal-inducible genes. J Cell Physiol 180(1):105–113. doi: 10.1002/(SICI)1097-4652(199907)180:1<105::AID-JCP12>3.0.CO;2-5 CrossRefPubMedGoogle Scholar
  35. Nadeau D, Corneau S, Plante I, Morrow G, Tanguay RM (2001) Evaluation for Hsp70 as a biomarker of effect of pollutants on the earthworm Lumbricus terrestris. Cell Stress Chaperones 6(2):153–163. doi: 10.1379/1466-1268(2001)006<0153:EFHAAB>2.0.CO;2 CrossRefPubMedGoogle Scholar
  36. Pelham HR (1989) Heat shock and the sorting of luminal ER proteins. EMBO J 8(11):3171PubMedGoogle Scholar
  37. Piano A, Franzellitti S, Tinti F, Fabbri E (2005) Sequencing and expression pattern of inducible heat shock gene products in the European flat oyster, Ostrea edulis. Gene 361:119–126. doi: 10.1016/j.gene.2005.06.034 CrossRefPubMedGoogle Scholar
  38. Rainbow PS, White SL (1989) Comparative strategies of heavy metal accumulation by crustaceans: zinc, copper and cadmium in a decapod, an amphipod and a barnacle. Hydrobiologia 174(3):245–262. doi: 10.1007/BF00008164 CrossRefGoogle Scholar
  39. Ramya TNC, Surolia N, Surolia A (2006) 15-Deoxyspergualin modulates Plasmodium falciparum heat shock protein function. Biochem Biophys Res Commun 348(2):585–592. doi: 10.1016/j.bbrc.2006.07.082 CrossRefPubMedGoogle Scholar
  40. Rinehart JP, Yocum GD, Denlinger DL (2000) Developmental upregulation of inducible hsp70 transcripts, but not the cognate form, during pupal diapause in the flesh fly, Sarcophaga crassipalpis. Insect Biochem Mol Biol 30(6):515–521. doi: 10.1016/S0965-1748(00)00021-7 CrossRefPubMedGoogle Scholar
  41. Robbins J, Dilworth SM, Laskey RA, Dingwall C (1991) Two interdependent basic domains in nucleoplasmin nuclear targeting sequence: identification of a class of bipartite nuclear targeting sequence. Cell 64(3):615–623. doi: 10.1016/0092-8674(91)90245-T CrossRefPubMedGoogle Scholar
  42. Sadiq M, Zaidi TH (1982) Heavy metal concentrations in shrimp, crab, and sediment obtained from Ad-Dammam sewage outfall area. Bull Environ Contam Toxicol 29(3):313–319. doi: 10.1007/BF01706234 CrossRefPubMedGoogle Scholar
  43. Sanders BM (1993) Stress proteins in aquatic organisms: an environmental perspective. Crit Rev Toxicol 23(1):49–75. doi: 10.3109/10408449309104074 CrossRefPubMedGoogle Scholar
  44. Sherman MY, Goldberg AL (1993) Heat shock of escherichia coli increases binding of dnaK (the hsp70 Homolog) to polypeptides by promoting its phosphorylation. Proc Natl Acad Sci U S A 90(18):8648–8652. doi: 10.1073/pnas.90.18.8648 CrossRefPubMedGoogle Scholar
  45. Shonhai A, Boshoff A, Blatch GL (2005) Plasmodium falciparum heat shock protein 70 is able to suppress the thermosensitivity of an Escherichia coli DnaK mutant strain. Mol Genet Genomics 274(1):70–78. doi: 10.1007/s00438-005-1150-9 CrossRefPubMedGoogle Scholar
  46. Song L, Wu L, Ni D, Chang Y, Xu W, Xing K (2006) The cDNA cloning and mRNA expression of heat shock protein 70 gene in the haemocytes of bay scallop (Argopecten irradians, Lamarck 1819) responding to bacteria challenge and naphthalin stress. Fish Shellfish Immunol 21(4):335–345. doi: 10.1016/j.fsi.2005.12.011 CrossRefPubMedGoogle Scholar
  47. Spurgeon DJ, Hopkin SP, Jones DT (1994) Effects of cadmium, copper, lead and zinc on growth, reproduction and survival of the earthworm Eisenia fetida (Savigny): assessing the environmental impact of point-source metal contamination in terrestrial ecosystems. Environ Pollut 84(2):123–130. doi: 10.1016/0269-7491(94)90094-9 CrossRefPubMedGoogle Scholar
  48. Stohs SJ, Bagchi D (1995) Oxidative mechanisms in the toxicity of metal ions. Free Radic Biol Med 18(2):321–336. doi: 10.1016/0891-5849(94)00159-H CrossRefPubMedGoogle Scholar
  49. Suh WC, Burkholder WF, Lu CZ, Zhao X, Gottesman ME, Gross CA (1998) Interaction of the Hsp70 molecular chaperone, DnaK, with its cochaperone DnaJ. Proc Natl Acad Sci U S A 95:15223–15228. doi: 10.1073/pnas.95.26.15223 CrossRefPubMedGoogle Scholar
  50. Szabo A, Langer T, Schroder H, Flanagan J, Bukau B, Hartl FU (1994) The ATP hydrolysis-dependent reaction cycle of the Escherichia coli Hsp70 system-DnaK, DnaJ, and GrpE. Proc Natl Acad Sci U S A 91(22):10345–10349. doi: 10.1073/pnas.91.22.10345 CrossRefPubMedGoogle Scholar
  51. Terasawa K, Minami M, Minami Y (2005) Constantly updated knowledge of Hsp90. J Biochem 137(4):443–447. doi: 10.1093/jb/mvi056 CrossRefPubMedGoogle Scholar
  52. Thériault JR, Mambula SS, Sawamura T, Stevenson MA, Calderwood SK (2005) Extracellular HSP70 binding to surface receptors present on antigen presenting cells and endothelial/epithelial cells. FEBS Lett 579(9):1951–1960. doi: 10.1016/j.febslet.2005.02.046 CrossRefPubMedGoogle Scholar
  53. Tsan MF, Gao B (2004) Heat shock protein and innate immunity. Cell Mol Immunol 1(4):274–279PubMedGoogle Scholar
  54. Vilaboa NE (1995) cAMP increasing agents prevent the stimulation of heat-shock protein 70 (HSP70) gene expression by cadmium chloride in human myeloid cell lines. J Cell Sci 108:2877–2883PubMedGoogle Scholar
  55. Vogel M, Bukau B, Mayer MP (2006) Allosteric regulation of Hsp70 chaperones by a proline switch. Mol Cell 21(3):359–367. doi: 10.1016/j.molcel.2005.12.017 CrossRefPubMedGoogle Scholar
  56. Wang TF, Chang JH, Wang C (1993) Identification of the peptide binding domain of hsc70. 18-Kilodalton fragment located immediately after ATPase domain is sufficient for high affinity binding. J Biol Chem 268(35):26049–26051PubMedGoogle Scholar
  57. Wu B, Hunt C, Morimoto R (1985) Structure and expression of the human gene encoding major heat shock protein HSP70. Mol Cell Biol 5(2):330–341PubMedGoogle Scholar
  58. Zhu X, Zhao X, Burkholder WF, Gragerov A, Ogata CM, Gottesman ME, Hendrickson WA (1996) Structural analysis of substrate binding by the molecular chaperone DnaK. Science 272(5268):1606–1614. doi: 10.1126/science.272.5268.1606 CrossRefPubMedGoogle Scholar

Copyright information

© Cell Stress Society International 2009

Authors and Affiliations

  1. 1.Institute of OceanologyChinese Academy of SciencesQingdaoPeople’s Republic of China
  2. 2.Graduate UniversityChinese Academy of SciencesBeijingPeople’s Republic of China
  3. 3.CSIRO Livestock IndustriesQueensland Bioscience PrecinctSt LuciaAustralia

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