Hsp70 and Hsp90 are differentially expressed in crayfish muscle and neurons after heat stress

References

• Espina S, Diazherrera F, Buckler L. Preferred and avoided temperatures in the crayfish Procambarus clarkii (Decapoda, Cambaridae). J Therm Biol. 1993;18(1):35–39.
   Web of Science ®Google Scholar
• Fanjul-Moles ML, Bosques-Tistler T, Prieto-Sagredo J, Castanon- Cervantes O, Fernandez-Rivera-Rio L. Effect of variation in photoperiod and light intensity on oxygen consumption, lactate concentration and behavior in crayfish Procambarus clarkii and Procambarus digueti. Comp Biochem Physiol A Mol Integr Physiol. 1998;119(1):263–269.
   PubMed Web of Science ®Google Scholar
• Powell ML, Watts SA. Effect of temperature acclimation on metabolism and hemocyanin binding affinities in two crayfish, Procambarus clarkii and Procambarus zonangulus. Comp Biochem Physiol A Mol Integr Physiol. 2006;144(2):211–217.
   Web of Science ®Google Scholar
• Gherardi F, Holdich DM. Crustacean Issues 11. Crayfish in Europe as Alien Species. Rotterdam, The Netherlands: AA Balkema; 1999.
   Google Scholar
• Khalil MT, Sleem SH. Can the crayfish eradicate schistosomiasis in Egypt and Africa? J Am Sci. 2011;7(7):457–462.
   Google Scholar
• Mkoji GM, Hofkin BV, Kuris AM, et al. Impact of the crayfish Pro- cambarus clarkii on Schistosoma haematobium transmission in Kenya. Am JTrop MedHyg. 1999;61(5):751–759.
   Web of Science ®Google Scholar
• Hofkin BV Mkoji GM, Koech DK, Loker ES. Control of schistosome- transmitting snails in Kenya by the North American crayfish Procam- barus clarkii. Am J Trop Med Hyg. 1991;45(3):339–344.
   Web of Science ®Google Scholar
• Steinmann P, Keiser J, Bos R, Tanner M, Utzinger J. Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infect Dis. 2006;6(7):411–425.
   PubMed Web of Science ®Google Scholar
• Lindquist S, Craig EA. The heat-shock proteins. Annu Rev Genet. 1988;22:631–677.
   PubMed Web of Science ®Google Scholar
• Welch WJ, Feramisco JR. Purification of the major mammalian heat shock proteins. J Biol Chem. 1982;257(24):14949–14959.
   Web of Science ®Google Scholar
• Jolly C, Morimoto RI. Role of the heat shock response and molecular chaperones in oncogenesis and cell death. J Natl Cancer Inst. 2000;92(19):1564–1572.
   PubMedGoogle Scholar
• Gething MJ, Sambrook J. Protein folding in the cell. Nature. 1992;355(6355):33–45.
   PubMed Web of Science ®Google Scholar
• Hartl FU, Martin J, Neupert W. Protein folding in the cell: the role of molecular chaperones Hsp70 and Hsp60. Annu Rev Biophys Biomol Struct. 1992;21:293–322.
   PubMedGoogle Scholar
• Peterson NS, Moller G, Mitchell HK. Genetic mapping of the coding regions for three heat-shock proteins in Drosophila melanogaster. Genetics. 1979;92(3):891–902.
   Web of Science ®Google Scholar
• Borges JC, Ramos CH. Protein folding assisted by chaperones. Protein PeptLett. 2005;12(3):257–261.
   Google Scholar
• Walter S, Buchner J. Molecular chaperones - cellular machines for protein folding. Angew Chem Int Ed Engl. 2002;41(7):1098–1113.
   PubMed Web of Science ®Google Scholar
• Luders J, Demand J, Hohfeld J. The ubiquitin-related BAG-1 provides a link between the molecular chaperones Hsc70/Hsp70 and the proteasome. J Biol Chem. 2000;275(7):4613–4617.
   PubMed Web of Science ®Google Scholar
• Mayer MP, Bukau B. Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol Life Sci. 2005;62(6):670–684.
   PubMed Web of Science ®Google Scholar
• Wegele H, Muller L, Buchner J. Hsp70 and Hsp90 — a relay team for protein folding. Rev Physiol Biochem Pharmacol. 2004;151:1–44.
   PubMed Web of Science ®Google Scholar
• Csermely P, Schnaider T, Soti C, Prohaszka Z, Nardai G. The 90-kDa molecular chaperone family: structure, function, and clinical applications. A comprehensive review. Pharmacol Ther. 1998;79(2):129–168.
   PubMed Web of Science ®Google Scholar
• Kimmins S, MacRae TH. Maturation of steroid receptors: an example of functional cooperation among molecular chaperones and their associated proteins. Cell Stress Chaperones. 2000;5(2):76–86.
   Web of Science ®Google Scholar
• Pratt WB. The role of the hsp90-based chaperone system in signal transduction by nuclear receptors and receptors signaling via MAP kinase. Annu Rev Pharmacol Toxicol. 1997;37:297–326.
   PubMed Web of Science ®Google Scholar
• Pratt WB, Toft DO. Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr Rev. 1997;18(3):306–360.
   PubMed Web of Science ®Google Scholar
• Buchner J. Hsp90 and Co — a holding for folding. Trends Biochem Sci. 1999;24(4):136–141.
   Web of Science ®Google Scholar
• Picard D. Heat-shock protein 90, a chaperone for folding and regulation. Cell Mol Life Sci. 2002;59(10):1640–1648.
   PubMed Web of Science ®Google Scholar
• Calderwood SK, Khaleque MA, Sawyer DB, Ciocca DR. Heat shock proteins in cancer: chaperones of tumorigenesis. Trends Biochem Sci. 2006;31(3):164–172.
   PubMed Web of Science ®Google Scholar
• Keppler BR, Grady AT, Jarstfer MB. The biochemical role of the heat shock protein 90 chaperone complex in establishing human telomerase activity. J Biol Chem. 2006;281(29):19840–19848.
   Web of Science ®Google Scholar
• Rutherford SL, Zuker CS. Protein folding and the regulation of signaling pathways. Cell. 1994;79(7):1129–1132.
   Web of Science ®Google Scholar
• Walsh D, Li Z, Wu Y, Nagata K. Heat shock and the role of the heat shock proteins during neural plate induction in early mammalian CNS and brain development. Cell Mol Life Sci. 1997;53(2):198–211.
   Web of Science ®Google Scholar
• Sidera K, Samiotaki M, Yfanti E, Panayotou G, Patsavoudi E. Involvement of cell surface Hsp90 in cell migration reveals a novel role in the developing nervous system. J Biol Chem. 2004;279(44):45379–45388.
   Web of Science ®Google Scholar
• Auluck PK, Chan HY, Trojanowski JQ, Lee VM, Bonini NM. Chaperone suppression of alpha-synuclein toxicity in a Drosophila model for Parkinson’s disease. Science. 2002;295(5556):865–868.
   PubMed Web of Science ®Google Scholar
• Chan HY, Warrick JM, Gray-Board GL, Paulson HL, Bonini NM. Mechanisms of chaperone suppression of polyglutamine disease: selectivity, synergy and modulation of protein solubility in Drosophila. Hum Mol Genet. 2000;9(19):2811–2820.
   PubMed Web of Science ®Google Scholar
• Cummings CJ, Sun Y, Opal P, et al. Over-expression of inducible Hsp70 chaperone suppresses neuropathology and improves motor function in SCA1 mice. Hum Mol Genet. 2001;10(14):1511–1518.
   Web of Science ®Google Scholar
• Fernandez-Funez P, Nino-Rosales ML, de Gouyon B, et al. Identification of genes that modify ataxin-1-induced neurodegeneration. Nature. 2000;408(6808):101–106.
   PubMed Web of Science ®Google Scholar
• Kazemi-Esfarjani P, Benzer S. Genetic suppression of polyglutamine toxicity in Drosophila. Science. 2000;287(5459):1837–1840.
   PubMed Web of Science ®Google Scholar
• Warrick JM, Chan HY, Gray-Board GL, Chai Y, Paulson HL, Bonini NM. Suppression of polyglutamine-mediated neurodegeneration in Drosophila by the molecular chaperone Hsp70. Nat Genet. 1999;23(4):425–428.
   PubMed Web of Science ®Google Scholar
• Magrane J, Smith RC, Walsh K, Querfurth HW Heat shock protein 70 participates in the neuroprotective response to intracellularly expressed beta-amyloid in neurons. J Neurosci. 2004;24(7):1700–1706.
   PubMed Web of Science ®Google Scholar
• Wang L, Xie C, Greggio E, et al. The chaperone activity of heat shock protein 90 is critical for maintaining the stability of leucine-rich repeat kinase 2. J Neurosci. 2008;28(13):3384–3391.
   PubMed Web of Science ®Google Scholar
• Waza M, Adachi H, Katsuno M, et al. 17-AAG, an Hsp90 inhibitor, ameliorates polyglutamine-mediated motor neuron degeneration. Nat Med. 2005;11(10):1088–1095.
   PubMed Web of Science ®Google Scholar
• Chang ES. Stressed-out lobsters: crustacean hyperglycemic hormone and stress proteins. Integr Comp Biol. 2005;45(1):43–50.
   Web of Science ®Google Scholar
• Rochelle JM, Grossfeld RM, Bunting DL, Tytell M, Dwyer BE, Xue ZY. Stress protein synthesis by crayfish CNS tissue in vitro. Neurochem Res. 1991;16(5):533–542.
   Web of Science ®Google Scholar
• Zhang X-Y, Zhang M-Z, Zheng C-J, Liua J, Hu H-J. Identification of two hsp90 genes from the marine crab, Portunus trituberculatus and their specific expression profiles under different environmental conditions. Comp Biochem Physiol C Toxicol Pharmacol. 2009;150(4):465–473.
   Web of Science ®Google Scholar
• Fang DA, Wang Q, He L, Wang J, Wang Y. Characterization of heat shock protein 70 in the red claw crayfish (Cherax quadricarinatus): evidence for its role in regulating spermatogenesis. Gene. 2012;492(1):138–147.
   Web of Science ®Google Scholar
• Spees JL, Chang SA, Snyder MJ, Chang ES. Thermal acclimation and stress in the American lobster, Homarus americanus: equivalent temperature shifts elicit unique gene expression patterns for molecular chaperones and polyubiquitin. Cell Stress Chaperones. 2002;7(1):97–106.
   Web of Science ®Google Scholar
• Bittner GD. Long term survival of severed distal axonal stumps in vertebrates and invertebrates. Am Zool. 1988;28:1165–1179.
   Google Scholar
• Bittner GD. Long-term survival of anucleate axons and its implications for nerve regeneration. Trends Neurosci. 1991;14(5):188–193.
   Web of Science ®Google Scholar
• Xue ZY, Grossfeld RM. Stress protein synthesis and accumulation after traumatic injury of crayfish CNS. Neurochem Res. 1993;18(2):209–218.
   Web of Science ®Google Scholar
• Zeng Y, Lu CP. Identification of differentially expressed genes in haemocytes of the crayfish (Procambarus clarkii) infected with white spot syndrome virus by suppression subtractive hybridization and cDNA microarrays. Fish Shellfish Immunol. 2009;26(4):646–650.
   Web of Science ®Google Scholar
• Chucholl C. Disjunct distribution pattern of Procambarus clarkii (Crustacea, Decapoda, Astacida, Cambaridae) in an artificial lake system in Southwestern Germany. Aquatic Invasions. 2011;6(1):109–113.
   Web of Science ®Google Scholar
• Huner JV Kowalczuk JG, Avault JW Jr. Calcium and magnesium levels in the intermolt(C4) carapaces of three species of freshwater crawfish (Cambaridae: decapoda). Comp Biochem Physiol A Comp Physiol. 1976;55(2a):183–185.
   Google Scholar
• Wu R, Sun L, Lei M, Xie ST. [Molecular identification and expression of heat shock cognate 70 (HSC70) in the Pacific white shrimp Litopenaeus vannamei]. Mol Biol (Mosk). 2008;42(2):265—274. Russian.
   Web of Science ®Google Scholar
• Ginzinger DG. Gene quantification using real-time quantitative PCR: an emerging technology hits the mainstream. ExpHematol. 2002;30(6):503–512.
   PubMed Web of Science ®Google Scholar
• Bustin SA, Beaulieu JF, Huggett J, et al. MIQE precis: practical implementation of minimum standard guidelines for fluorescence-based quantitative real-time PCR experiments. BMC Mol Biol. 2010;11:74.
   PubMed Web of Science ®Google Scholar
• Nolan T, Hands RE, Bustin SA. Quantification of mRNA using real-time RT-PCR. Nat Protoc. 2006;1(3):1559–1582.
   PubMed Web of Science ®Google Scholar
• Zhang Y. I-TASSER server for protein 3D structure prediction. BMC Bioinformatics. 2008;9:40.
   PubMed Web of Science ®Google Scholar
• Zhang Y. I-TASSER: fully automated protein structure prediction in CASP8. Proteins. 2009;77 Suppl 9:100–113.
   Google Scholar
• Gupta RS. Phylogenetic analysis of the 90 kD heat shock family of protein sequences and an examination of the relationship among animals, plants, and fungi species. Mol Biol Evol. 1995;12(6):1063–1073.
   Web of Science ®Google Scholar
• Stebbins CE, Russo AA, Schneider C, Rosen N, Hartl FU, Pavletich NP Crystal structure of an Hsp90-geldanamycin complex: targeting of a protein chaperone by an antitumor agent. Cell. 1997;89(2):239–250.
   PubMed Web of Science ®Google Scholar
• Young JC, Obermann WM, Hartl FU. Specific binding of tetratricopep- tide repeat proteins to the C-terminal 12-kDa domain of hsp90. J Biol Chem. 1998;273(29):18007–18010.
   Web of Science ®Google Scholar
• Mailhos C, Howard MK, Latchman DS. Heat shock proteins hsp90 and hsp70 protect neuronal cells from thermal stress but not from programmed cell death. J Neurochem. 1994;63(5):1787–1795.
   Web of Science ®Google Scholar
• Sanders BM. Stress proteins in aquatic organisms: an environmental perspective. Crit Rev Toxicol. 1993;23(1):49–75.
   PubMed Web of Science ®Google Scholar
• Pratt WB, Toft DO. Regulation of signaling protein function and trafficking by the Hsp90/Hsp70-based chaperone machinery. Exp Biol Med (Maywood). 2003;228(2):111–133.
   PubMed Web of Science ®Google Scholar
• Prodromou C, Roe SM, O’Brien R, Ladbury JE, Piper PW, Pearl LH. Identification and structural characterization of the ATP/ADP-binding site in the Hsp90 molecular chaperone. Cell. 1997;90(1):65–75.
   PubMed Web of Science ®Google Scholar
• Fontana J, Fulton D, Chen Y, et al. Domain mapping studies reveal that the M domain of hsp90 serves as a molecular scaffold to regulate Akt-dependent phosphorylation of endothelial nitric oxide synthase and NO release. Circ Res. 002;90(8):866–873.
   Web of Science ®Google Scholar
• Brunt SA, Silver JC. Molecular cloning and characterization of two different cDNAs encoding the molecular chaperone Hsp90 in the oomycete Achlya ambisexualis. Fungal Genet Biol. 2004;41(2):239–252.
   Web of Science ®Google Scholar
• Grenert JP, Sullivan WP, Fadden P, et al. The amino-terminal domain of heat shock protein 90 (hsp90) that binds geldanamycin is an ATP/ ADP switch domain that regulates hsp90 conformation. J Biol Chem. 1997;272(38):23843–23850.
   PubMed Web of Science ®Google Scholar
• Obermann WM, Sondermann H, Russo AA, Pavletich NP, Hartl FU. In vivo function of Hsp90 is dependent on ATP binding and ATP hydrolysis. J Cell Biol. 1998;143(4):901–910.
   PubMed Web of Science ®Google Scholar
• Bergerat A, de Massy B, Gadelle D, Varoutas PC, Nicolas A, Forterre P An atypical topoisomerase II from Archaea with implications for meiotic recombination. Nature. 1997;386(6623):414–417.
   PubMed Web of Science ®Google Scholar
• Johnson JL, Toft DO. A novel chaperone complex for steroid receptors involving heat shock proteins, immunophilins, and p23. J Biol Chem. 1994;269(40):24989–24993.
   PubMed Web of Science ®Google Scholar
• Johnson JL, Toft DO. Binding of p23 and hsp90 during assembly with the progesterone receptor. Mol Endocrinol. 1995;9(6):670–678.
   Google Scholar
• Prodromou C, Pearl LH. Structure and functional relationships of Hsp90. Curr Cancer Drug Targets. 2003;3(5):301–323.
   PubMed Web of Science ®Google Scholar
• Robbins J, Dilworth SM, Laskey RA, Dingwall C. Two interdependent basic domains in nucleoplasmin nuclear targeting sequence: identification of a class of bipartite nuclear targeting sequence. Cell. 1991;64(3):615–623.
   PubMed Web of Science ®Google Scholar
• Li P, Zha J, Zhang Z, et al. Molecular cloning, mRNA expression, and characterization of Hsp90 gene from Chinese mitten crab Eriocheir japonica sinensis. Comp Biochem Physiol B Biochem Mol Biol. 2009;153(3):229–235.
   Web of Science ®Google Scholar
• Khan VR, Brown IR. The effect of hyperthermia on the induction of cell death in brain, testis, and thymus of the adult and developing rat. Cell Stress Chaperones. 2002;7(1):73–90.
   Web of Science ®Google Scholar
• Batulan Z, Shinder GA, Minotti S, et al. High threshold for induction of the stress response in motor neurons is associated with failure to activate HSF1. J Neurosci. 2003;23(13):5789–5798.
   Web of Science ®Google Scholar
• Brown IR, Rush SJ. Cellular localization of the heat shock transcription factors HSF1 and HSF2 in the rat brain during postnatal development and following hyperthermia. Brain Res. 1999;821(2):333–340.
   Web of Science ®Google Scholar
• Maroni P, Bendinelli P, Tiberio L, Rovetta F, Piccoletti R, Schiaffonati L. In vivo heat-shock response in the brain: signalling pathway and transcription factor activation. Brain Res Mol Brain Res. 2003;119(1):90–99.
   Google Scholar
• Kaarniranta K, Oksala N, Karjalainen HM, et al. Neuronal cells show regulatory differences in the hsp70 gene response. Mol Brain Res. 2002;101(1—2):136–140.
   Google Scholar
• Manzerra P, Brown IR. Expression of heat shock genes (hsp70) in the rabbit spinal cord: localization of constitutive and hyperthermia- inducible mRNA species. J Neurosci Res. 1992;31(4):606–615.
   Web of Science ®Google Scholar
• Manzerra P, Brown IR. The neuronal stress response: nuclear translocation of heat shock proteins as an indicator of hyperthermic stress. Exp Cell Res. 1996;229(1):35–47.
   Web of Science ®Google Scholar
• Taylor DM, De Koninck P, Minotti S, Durham HD. Manipulation of protein kinases reveals different mechanisms for upregulation of heat shock proteins in motor neurons and non-neuronal cells. Mol Cell Neurosci. 2007;34(1):20–33.
   Web of Science ®Google Scholar
• Sarge KD, Murphy SP, Morimoto RI. Activation of heat shock gene transcription by heat shock factor 1 involves oligomerization, acquisition of DNA-binding activity, and nuclear localization and can occur in the absence of stress. Mol Cell Biol. 1993;13(3):1392–1407.
   PubMed Web of Science ®Google Scholar
• Sorger PK, Lewis MJ, Pelham HR. Heat shock factor is regulated differently in yeast and HeLa cells. Nature. 1987;329(6134):81–84.
   PubMed Web of Science ®Google Scholar
• Sorger PK, Pelham HR. Yeast heat shock factor is an essential DNA-binding protein that exhibits temperature-dependent phosphorylation. Cell. 1988;54(6):855–864.
   PubMed Web of Science ®Google Scholar
• Batulan Z, Taylor DM, Aarons RJ, et al. Induction of multiple heat shock proteins and neuroprotection in a primary culture model of familial amyotrophic lateral sclerosis. NeurobiolDis. 2006;24(2):213–225.
   Google Scholar