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Identification and expression analysis of a heat-shock protein 70 gene in Polycelis sp.

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Cell Stress and Chaperones Aims and scope

Abstract

Heat-shock protein 70 (HSP70) is ubiquitously found in a variety of organisms and plays an important role in cytoprotection, environmental monitoring, and disease resistance. In this study, the full-length complementary DNA (cDNA) of hsp70 from planarian Polycelis sp. was first cloned using rapid amplification of cDNA ends (RACE). The expression levels of Pyhsp70 were analyzed in the presence of various stressors by real-time PCR, and its temporal-spatial expression patterns were also examined in both intact and regenerative animals by whole-mount in situ hybridization. The results show that (1) the deduced amino acid sequence of Pyhsp70 includes three typical HSP70 family signature motifs and is highly conserved during evolution; (2) Pyhsp70 expression is induced by prolonged starvation, tissue damage, and ionic liquid but inhibited by high or low temperatures; and (3) Pyhsp70 mRNA is mainly expressed in the head peripheral region and in the regenerating blastema during regeneration. These results suggest that the highly expressed Pyhsp70 gene may contribute to enhance cytoprotection and tolerance against stress-induced molecular damage, and the migration of neoblasts to the wound, which might also be involved in the proliferation and differentiation of neoblasts. Our work provides basic data for the study of stress responses and regenerative mechanism in freshwater planarians.

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References

  • Aikawa M, Shimozawa A (1991) The multiple eyes of Polycelis. 1. Relation between the number of eyes and body length. Hydrobiologia 227:257–262

    Article  Google Scholar 

  • Akerfelt M, Morimoto RI, Sistonen L (2010) Heat shock factors: integrators of cell stress, development and lifespan. Nat Rev Mol Cell Biol 11:545–555

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Baguna J (2012) The planarian neoblast: the rambling history of its origin and some current black boxes. Int J Dev Biol 56:19–37

    Article  CAS  PubMed  Google Scholar 

  • Beaman GM, Dennison SR, Chatfield LK, Phoenix DA (2014) Reliability of HSP70 (HSPA) expression as a prognostic marker in glioma. Mol Cell Biochem 393:301–307

    Article  CAS  PubMed  Google Scholar 

  • Cardona A, Fernández J, Solana J, Romero R (2005) An in situ hybridization protocol for planarian embryos: monitoring myosin heavy chain gene expression. Dev Genes Evol 215:482–488

    Article  PubMed  Google Scholar 

  • Ciocca DR, Calderwood SK (2005) Heat shock proteins in cancer: diagnostic, prognostic, predictive, and treatment implications. Cells Stress Chaperones 10:86–103

    Article  CAS  Google Scholar 

  • Ciocca DR, Arrigo AP, Calderwood SK (2013) Heat shock proteins and heat shock factor 1 in carcinogenesis and tumor development: an update. Arch Toxicol 87:19–48

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Diller KR (2006) Stress protein expression kinetics. Annu Rev Biomed Eng 8:403–424

    Article  CAS  PubMed  Google Scholar 

  • Dong ZM, Shi CY, Zhang HX, Dou H, Cheng FF, Chen GW, Liu DZ (2014) The characteristics of Sox gene in Dugesia japonica. Gene 544:177–183

  • Dong ZM, Yuwen YQ, Wang QH, Chen GW, Liu DZ (2012) Eight genes expression patterns during visual system regeneration in Dugesia japonica. Gene Expr Patterns 12:1–6

    Article  CAS  PubMed  Google Scholar 

  • Evans CG, Chang L, Gestwicki JE (2010) Heat shock protein 70 (hsp70) as an emerging drug target. J Med Chem 53(12):4585–4602

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Freeman BC, Michels A, Song J, Kampinga HH, Morimoto RI (2000) Analysis of molecular chaperone activities using in vitro and in vivo approaches. Methods Mol Biol 99:393–419

    CAS  PubMed  Google Scholar 

  • Garrido C, Fromentin A, Bonnotte B, Favre N, Moutet M, Arrigo AP, Mehlen P, Solary E (1998) Heat shock protein 27 enhances the tumorigenicity of immunogenic rat colon carcinoma cells. Cancer Res 58:5495–5499

  • Gleixner AM, Pulugulla SH, Pant DB, Posimo JM, Crum TS, Leak RK (2014) Impact of aging on heat shock protein expression in the substantia nigra and striatum of the female rat. Cell Tissue Res 357:43–54

    Article  CAS  PubMed  Google Scholar 

  • Heikkila JJ (2010) Heat shock protein gene expression and function in amphibian model systems. Comp Biochem Physiol A Mol Integr Physiol 156:19–33

    Article  PubMed  Google Scholar 

  • Henderson B, Pockley AG (2010) Molecular chaperones and protein-folding catalysts as intercellular signaling regulators in immunity and inflammation. J Leukoc Biol 88(3):445–462

  • Jenei ZM, Gombos T, Förhécz Z, Pozsonyi Z, Karádi I, Jánoskuti L, Prohászka Z (2013) Elevated extracellular HSP70 (HSPA1A) level as an independent prognostic marker of mortality in patients with heart failure. Cell Stress Chaperones 18:809–813

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kalmar B, Greensmith L (2009) Induction of heat shock proteins for protection against oxidative stress. Adv Drug Deliv Rev 61:310–318

    Article  CAS  PubMed  Google Scholar 

  • Keskin S, Kayrak-Talay D, Akman U, Hortaçsu Ö (2007) A review of ionic liquids towards supercritical fluid applications. J Supercrit Fluids 43:150–180

    Article  CAS  Google Scholar 

  • Knakievicz T, Ferreira HB (2008) Evaluation of copper effects upon Girardia tigrina freshwater planarians based on a set of biomarkers. Chemosphere 71:419–428

    Article  CAS  PubMed  Google Scholar 

  • Kovalchin JT, Wang R, Wagh MS, Azoulay J, Sanders M (2006) In vivo delivery of heat shock protein 70 accelerates wound healing by up-regulating macrophage-mediated phagocytosis. Wound Repair Regen 14:129–137

    Article  PubMed  Google Scholar 

  • Landry TD, Brooks K, Poche D, Woolhiser M (2005) Acute toxicity profile of 1-butyl-3-methylimidazolium chloride. Bull Environ Contam Toxicol 74:559–565

    Article  CAS  PubMed  Google Scholar 

  • Lee SM, Chang WJ, Choi AR, Koo YM (2005) Influence of ionic liquids on the growth of Escherichia coli. Korean J Chem Eng 22(5):687–690

    Article  CAS  Google Scholar 

  • Li MH (2008) Effects of nonionic and ionic surfactants on survival, oxidative stress, and cholinesterase activity of planarian. Chemosphere 70:1796–1803

    Article  CAS  PubMed  Google Scholar 

  • Li XY, Luo YR, Yun MX, Wang J, Wang JJ (2010) Effects of 1-octyl-3-methylimidazolium bromide on the anti-oxidant system of earthworm. Chemosphere 78:853–858

    Article  CAS  PubMed  Google Scholar 

  • Liu CC, Jan YJ, Ko BS, Wu YM, Liang SM, Chen SC, Lee YM, Liu TA, Chang TC, Wang J, Shyue SK, Sung LY, Liou JY (2014) 14-3-3σ induces heat shock protein 70 expression in hepatocellular carcinoma. BMC Cancer 14:425

    Article  PubMed Central  PubMed  Google Scholar 

  • Ma KX, Chen GX, Lou H, Fei LN (2009) Cloning and expression analysis of hsp70 gene from freshwater planarian Dugesia japonica. Biologia 64:1018–1024

    Article  CAS  Google Scholar 

  • Mayer MP, Bukau B (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol Life Sci 62:670–684

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Moraga D, Meistertzheim AL, Tanguy-Royer S, Boutet I, Tanguy A, Donval A (2005) Stress response in Cu2+ and Cd2+ exposed oysters (Crassostrea gigas): an immunohistochemical approach. Comp Biochem Physiol C Toxicol Pharmacol 141:151–156

    Article  PubMed  Google Scholar 

  • Nadin SB, Sottile ML, Montt-Guevara MM, Gauna GV, Daguerre P, Leuzzi M, Gago FE, Ibarra J, Cuello-Carrión FD, Ciocca DR, Vargas-Roig LM (2014) Prognostic implication of HSPA (HSP70) in breast cancer patients treated with neoadjuvant anthracycline-based chemotherapy. Cell Stress Chaperones 19:493–505

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Navarro BS, Michiels NK, Köhler HR, D’Souza TG (2009) Differential expression of heat shock protein 70 in relation to stress type in the flatworm Schmidtea polychroa. Hydrobiologia 636:393–400

    Article  Google Scholar 

  • Newmark PA, Sánchez Alvarado A (2002) Not your father’s planarian: a classic model enters the era of functional genomics. Nat Rev Genet 3:210–219

    Article  CAS  PubMed  Google Scholar 

  • Ortega E, Hinchado MD, Martin-Cordero L, Asea A (2009) The effect of stress inducible extracellular Hsp72 on human neutrophil chemotaxis: a role during acute intense exercise. Stress 12:240–249

    Article  CAS  PubMed  Google Scholar 

  • Pearson JC, Lemons D, McGinnis W (2005) Modulating Hox gene functions during animal body patterning. Nat Rev Genet 6:893–904

    Article  CAS  PubMed  Google Scholar 

  • Ranke J, Mölter K, Stock F, Bottin-Weber U, Poczobutt J, Hoffmann J, Ondruschka B, Filser J, Jastorff B (2004) Biological effects of imidazolium ionic liquids with varying chain lengths in acute Vibrio fischeri and WST-1 cell viability assays. Ecotoxicol Environ Saf 58:396–404

    Article  CAS  PubMed  Google Scholar 

  • Reddien PW, Sánchez Alvarado A (2004) Fundamentals of planarian regeneration. Annu Rev Cell Dev Biol 20:725–757

    Article  CAS  PubMed  Google Scholar 

  • Rios-Arana JV, Gardea-Torresdey J, Webb R, Walsh EJ (2005) Heat shock protein 60 (HSP60) response of Plationus patulus (Rotifera: Monogononta) to combined exposures of arsenic and heavy metals. Hydrobiologia 546:577–585

    Article  CAS  Google Scholar 

  • Saló E (2006) The power of regeneration and the stem-cell kingdom: freshwater planarians (Platyhelminthes). Bioessays 28:546–559

    Article  PubMed  Google Scholar 

  • Salo E, Baguna J (2002) Regeneration in planarians and other worms: new findings, new tools, and new perspectives. J Exp Zool 292:528–539

    Article  CAS  PubMed  Google Scholar 

  • Sánchez Alvarado A (2000) Regeneration in the metazoans: why does it happen? Bioessays 22:578–590

    Article  PubMed  Google Scholar 

  • Sánchez Alvarado A (2006) Planarian regeneration: its end is its beginning. Cell 124:241–245

    Article  PubMed  Google Scholar 

  • Senf SM, Howard TM, Ahn B, Ferreira LF, Judge AR (2013) Loss of the inducible Hsp70 delays the inflammatory response to skeletal muscle injury and severely impairs muscle regeneration. PLoS One 8(4), e62687

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Seo J, Park TJ, Lee YM, Park H, Yoon YD, Lee JS (2006) Small heat shock protein 20 gene (Hsp20) of the intertidal copepod Tigriopus japonicus as a possible biomarker for exposure to endocrine disruptors. Bull Environ Contam Toxicol 76:566–572

    Article  CAS  PubMed  Google Scholar 

  • Shim JK, Jung DO, Park JW, Kim DW, Ha DM, Lee KY (2006) Molecular cloning of the heat-shock cognate 70 (Hsc70) gene from the two-spotted spider mite, Tetranychus urticae, and its expression in response to heat shock and starvation. Comp Biochem Physiol B 145:288–295

    Article  PubMed  Google Scholar 

  • Tashiro S (2009) Mechanism of liver regeneration after liver resection and portal vein embolization (ligation) is different? J Hepato-Biliary-Pancreat Surg 16:292–299

    Article  Google Scholar 

  • Ventura M, Canchaya C, Zhang Z, Fitzgerald GF, Van Sinderen D (2007) Molecular characterization of hsp20, encoding a small heat shock protein of Bifidobacterium breve UCC2003. Appl Environ Microbiol 73:4695–4703

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang RE (2011) Targeting heat shock proteins 70/90 and proteasome for cancer therapy. Curr Med Chem 18(27):4250–4264

    Article  CAS  PubMed  Google Scholar 

  • Yang JH, Mu YW, Dong SM, Jiang QC, Yang JX (2014) Changes in the expression of four heat shock proteins during the aging process in Brachionus calyciflorus (rotifera). Cell Stress Chaperones 19:33–52

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by grants from the National Natural Science Foundation of China (Nos. 31471965, 31170357, 30870368, 30670247, 30170119), the Ph.D. Programs Foundation of the Ministry of Education of China (No. 200804760003), the Outstanding Young Scientists Foundation of Henan Province (No. 0312001100), the Innovation Foundation of Henan Province (No. 2005126), the Basic and Advanced Technique Research Program of Technology Department of Henan Province (Nos. 122300410142, 142300410160), and the Doctoral Scientific Research Start-up Foundation of Henan Normal University (No. 521).

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Correspondence to Guangwen Chen.

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GenBank accession no. KP027180

Fangfang Cheng and Zimei Dong contributed equally to this work.

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Cheng, F., Dong, Z., Dong, Y. et al. Identification and expression analysis of a heat-shock protein 70 gene in Polycelis sp.. Cell Stress and Chaperones 20, 907–915 (2015). https://doi.org/10.1007/s12192-015-0608-x

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