Chilo suppressalis heat shock proteins are regulated by heat shock factor 1 during heat stress.
Chilo suppressalis
heat shock element
heat shock factor 1
heat shock protein
temperature
Journal
Insect molecular biology
ISSN: 1365-2583
Titre abrégé: Insect Mol Biol
Pays: England
ID NLM: 9303579
Informations de publication
Date de publication:
02 2023
02 2023
Historique:
received:
26
04
2022
accepted:
21
10
2022
pubmed:
25
10
2022
medline:
18
1
2023
entrez:
24
10
2022
Statut:
ppublish
Résumé
Heat shock factor 1 (HSF1) functions to maintain cellular and organismal homeostasis by regulating the expression of target genes, including those encoding heat shock proteins (HSPs). In the present study, the gene encoding HSF1 was cloned from the rice pest Chilo suppressalis, and designated Cshsf1. The deduced protein product, CsHSF1, contained conserved domains typical of the HSF1 family, including a DNA-binding domain, two hydrophobic heptad repeat domains, and a C-terminal transactivation domain. Real-time quantitative PCR showed that Cshsf1 was highly expressed in hemocytes. Expression analysis in different developmental stages of C. suppressalis revealed that Cshsf1 was most highly expressed in male adults. RNAi-mediated silencing of Cshsf1 expression reduced C. suppressalis survival at high temperatures. To investigate the regulatory interactions between Cshsf1 and Cshsps, the promoters and expression patterns of 18 identified Cshsps in C. suppressalis were analysed; four types of heat shock elements (HSEs) were identified in promoter regions including canonical, tail-tail, head-head, and step/gap. The expression of Cshsp19.0, Cshsp21.7B, Cshsp60, Cshsp70 and Cshsp90 was positively regulated by Cshsf1; however, Cshsp22.8, Cshsp702, Cshsp705 and Cshsp706 gene expression was not altered. This study provides a foundation for future studies of HSF1 in insects during thermal stress.
Substances chimiques
Heat-Shock Proteins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
69-78Informations de copyright
© 2022 Royal Entomological Society.
Références
Åkerfelt, M., Morimoto, R.I. & Sistonen, L. (2010) Heat shock factors: integrators of cell stress, development and lifespan. Nature Reviews Molecular Cell Biology, 11, 545-555.
Ali, H., Alqarni, A.S., Owayss, A.A., Hassan, A.M. & Smith, B.H. (2017) Osmotic concentration in three races of honey bee, Apis mellifera L. under environmental conditions of arid zone. Saudi Journal of Biological Sciences, 24, 1081-1085.
Anckar, J. & Sistonen, L. (2011) Regulation of HSF1 function in the heat stress response: implications in aging and disease. Annual Review of Biochemistry, 80, 1089-1115.
Bale, J.S., Masters, G.J., Hodkinson, I.D., Awmack, C., Bezemer, T.M. & Brown, V.K. (2002) Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Global Change Biology, 8, 1-16.
Barna, J., Csermely, P. & Vellai, T. (2018) Roles of heat shock factor 1 beyond the heat shock response. Cellular and Molecular Life Sciences, 75, 2897-2916.
Bustin, S.A., Benes, V., Garson, J.A., Hellemans, J., Huggett, J., Kubista, M. et al. (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry, 55, 611-622.
Castro-Mondragon, J.A., Riudavets-Puig, R., Rauluseviciute, I., Lemma, R.B., Turchi, L., Blanc-Mathieu, R. et al. (2022) JASPAR 2022: the 9th release of the open-access database of transcription factor binding profiles. Nucleic Acids Research, 50, D165-D173.
Chang, Y.W., Wang, Y.C., Zhang, X.X., Iqbal, J., Lu, M.X. & Du, Y.Z. (2021) Transcriptional regulation of small heat shock protein genes by heat shock factor 1 (HSF1) in Liriomyza trifolii under heat stress. Cell Stress & Chaperones, 26, 835-843.
Chatterjee, S. & Burns, T.F. (2017) Targeting heat shock proteins in cancer: a promising therapeutic approach. International Journal of Molecular Sciences, 18, 1978.
Chen, W., Geng, S.L., Song, Z., Li, Y.J., Wang, H. & Cao, J.Y. (2018) Alternative splicing and expression analysis of HSF1 in diapause pupal brains in the cotton bollworm, Helicoverpa armigera. Pest Management Science, 75, 1258-1269.
Chiang, W.C., Ching, T.T., Lee, H.C., Mousigian, C. & Hsu, A.L. (2012) HSF-1 regulators DDL-1/2 link insulin-like signaling to heat-shock responses and modulation of longevity. Cell, 148, 322-334.
Collier, R.J., Collier, J.L., Rhoads, R.P. & Baumgard, L.H. (2008) Invited review: genes involved in the bovine heat stress response. Journal of Dairy Science, 91, 445-454.
Dixon, A.F.G. & Kundu, R. (1997) Trade-off between reproduction and length of adult life in males and mating females of aphids. European Journal of Entomology, 94, 105-109.
Dong, C.L., Zhu, F., Lu, M.X. & Du, Y.Z. (2021) Characterization and functional analysis of Cshsp19.0 encoding a small heat shock protein in Chilo suppressalis (Walker). International Journal of Biological Macromolecules, 188, 924-931.
Fujikake, N., Nagai, Y., Popiel, H.A., Kano, H., Yamaguchi, M. & Toda, T. (2005) Alternative splicing regulates the transcriptional activity of drosophila heat shock transcription factor in response to heat/cold stress. FEBS Letters, 579, 3842-3848.
Gao, P., Lu, M.X., Pan, D.D. & Du, Y.Z. (2019) Characterization of an inducible HSP70 gene in Chilo suppressalis and expression in response to environmental and biological stress. Cell Stress & Chaperones, 25, 65-72.
Graveley, B.R. (2001) Alternative splicing: increasing diversity in the proteomic world. Trends in Genetics, 17, 100-107.
Han, L.Z., Li, S.B., Liu, P.L., Peng, Y.F. & Hou, M.L. (2012) New artificial diet for continuous rearing of Chilo suppressalis (Lepidoptera: Crambidae). Annals of the Entomological Society of America, 105, 253-258.
Harada, E. & Goto, S.G. (2017) Upregulation of heat-shock proteins in larvae, but not adults, of the flesh fly during hot summer days. Cell Stress & Chaperones, 22, 823-831.
Hassan, F., Nawaz, A., Rehman, M.S., Ali, M.A., Dilshad, S.M.R. & Yang, C. (2019) Prospects of HSP70 as a genetic marker for thermo-tolerance and immuno-modulation in animals under climate change scenario. Animal Nutrition, 5, 340-350.
Hightower, L.E. (1991) Heat shock, stress proteins, chaperones, and proteotoxicity. Cell, 66, 191-197.
Hsu, A.L. (2003) Regulation of aging and age-related disease by DAF-16 and heat-shock factor. Science, 300, 1142-1145.
Hu, J., Chen, B. & Li, Z. (2014) Thermal plasticity is related to the hardening response of heat shock protein expression in two Bactrocera fruit flies. Journal of Insect Physiology, 67, 105-113.
Huang, L.H., Wang, H.S. & Kang, L. (2008) Different evolutionary lineages of large and small heat shock proteins in eukaryotes. Cell Research, 18, 1074-1076.
Jedlicka, P., Mortin, M.A. & Wu, C. (1997) Multiple functions of drosophila heat shock transcription factorin vivo. The EMBO Journal, 16, 2452-2462.
Jin, J., Li, Y., Zhou, Z., Zhang, H., Guo, J. & Wan, F. (2020) Heat shock factor is involved in regulating the transcriptional expression of two potential Hsps (AhHsp70 and AhsHsp21) and its role in heat shock response of Agasicles hygrophila. Frontiers in Physiology, 11, 562204.
Johnston, J.A., Ward, C.L. & Kopito, R.R. (1998) Aggresomes: a cellular response to misfolded proteins. The Journal of Cell Biology, 143, 1883-1898.
Kihara, F., Niimi, T., Yamashita, O. & Yaginuma, T. (2011) Heat shock factor binds to heat shock elements upstream of heat shock protein 70a and Samui genes to confer transcriptional activity in Bombyx mori diapause eggs exposed to 5°C. Insect Biochemistry and Molecular Biology, 41, 843-851.
Kim, H., Bartley, G.E., Young, S.A., Seo, K.H. & Yokoyama, W. (2013) Altered hepatic gene expression profiles associated with improved fatty liver, insulin resistance, and intestinal permeability after Hydroxypropyl methylcellulose (HPMC) supplementation in diet-induced obese mice. Journal of Agricultural and Food Chemistry, 61, 6404-6411.
Kim, Y.K., Weber, M.B., Anderson, W.W. & Gowaty, P.A. (2010) Preference status does not indicate intrinsic quality differences in Drosophila pseudoobscura. Integrative Zoology, 5, 198-207.
Knorr, D.Y., Hartung, D., Schneider, K., Hintz, L. & Heinrich, R. (2021) Locust Hemolymph conveys erythropoietin-like Cytoprotection via activation of the cytokine receptor CRLF3. Frontiers in Physiology, 12, 648245.
Kovács, D., Sigmond, T., Hotzi, B., Bohár, B., Fazekas, D., Deák, V. et al. (2019) HSF1Base: a comprehensive database of HSF1 (heat shock factor 1) target genes. International Journal of Molecular Sciences, 20, 5815.
Kroeger, P.E. & Morimoto, R.I. (1994) Selection of new HSF1 and HSF2 DNA-binding sites reveals difference in trimer cooperativity. Molecular and Cellular Biology, 14, 7592-7603.
Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870-1874.
Liu, G., Ozoe, F., Furuta, K. & Ozoe, Y. (2015) 4,5-substituted 3-Isoxazolols with insecticidal activity act as competitive antagonists of housefly GABA receptors. Journal of Agricultural and Food Chemistry, 63, 6304-6312.
Lu, M.X., Cao, S.S., Liu, Z.X., Wang, X. & Du, Y.Z. (2014) Heat tolerance of developmental and seasonal stages of Chilo suppressalis. Entomologia Experimentalis et Applicata, 152, 91-99.
Lu, M.X., Hua, J., Cui, Y.D. & Du, Y.Z. (2013) Five small heat shock protein genes from Chilo suppressalis: characteristics of gene, genomic organization, structural analysis, and transcription profiles. Cell Stress & Chaperones, 19, 91-104.
Lu, M.X., Liu, Z.X., Cui, Y.D. & Du, Y.Z. (2014) Expression patterns of three heat shock proteins in Chilo suppressalis (Lepidoptera: Pyralidae). Annals of the Entomological Society of America, 107, 667-673.
Lu, M.X., Liu, Z.X., Wang, X. & Du, Y.Z. (2012) Seasonal cold tolerance of Chilo suppressalis (Lepidoptera: Pyralidae). Annals of the Entomological Society of America, 105, 479-483.
Lu, Z., Zhu, P., Gurr, G.M., Zheng, X., Chen, G. & Heong, K.L. (2014) Rice Pest management by ecological engineering: a pioneering attempt in China. Rice Planthoppers, pp. 161-178. London: Springer-Verlag London ltd.
Ma, W.H., Zhao, X.X., Yin, C.L., Jiang, F., Du, X.Y., Chen, T.Y. et al. (2020) A chromosome-level genome assembly reveals the genetic basis of cold tolerance in a notorious rice insect pest, Chilo suppressalis. Molecular Ecology Resources, 20, 268-282.
Maheshwari, M., Bhutani, S., Das, A., Mukherjee, R., Sharma, A., Kino, Y. et al. (2013) Dexamethasone induces heat shock response and slows down disease progression in mouse and fly models of Huntington's disease. Human Molecular Genetics, 23, 2737-2751.
Marchler-Bauer, A., Derbyshire, M.K., Gonzales, N.R., Lu, S., Chitsaz, F., Geer, L.Y. et al. (2014) CDD: NCBI's conserved domain database. Nucleic Acids Research, 43, D222-D226.
Mayer, M.P. & Bukau, B. (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cellular and Molecular Life Sciences, 62, 670-684.
Michalak, P., Minkov, I., Helin, A., Lerman, D.N., Bettencourt, B.R., Feder, M.E. et al. (2001) Genetic evidence for adaptation-driven incipient speciation of Drosophila melanogaster along a microclimatic contrast in “evolution canyon,” Israel. Proceedings of the National Academy of Sciences, 98, 13195-13200.
Morimoto, R.I. (1998) Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes & Development, 12, 3788-3796.
Newton, E.M., Knauf, U., Green, M. & Kingston, R.E. (1996) The regulatory domain of human heat shock factor 1 is sufficient to sense heat stress. Molecular and Cellular Biology, 16, 839-846.
Nolan, T., Hands, R.E. & Bustin, S.A. (2006) Quantification of mRNA using real-time RT-PCR. Nature Protocols, 1, 1559-1582.
Qiang, C.K., Du, Y.Z., Yu, L.Y., Cui, Y.D. & Zhou, B.Y. (2010) Cloning and expression of heat shock protein 90 gene from the Diapausing larvae of the Rice stem borer, Chilo Suppressalis (Lepidoptera: Pyralidae) exposed to temperature stress. Research Journal of Biotechnology, 5, 68-75.
Rabindran, S.K., Haroun, R.I., Clos, J., Wisniewski, J. & Wu, C. (1993) Regulation of heat shock factor trimer formation: role of a conserved leucine zipper. Science, 259, 230-234.
Ray, J., Munn, P.R., Vihervaara, A., Lewis, J.J., Ozer, A., Danko, C.G. et al. (2019) Chromatin conformation remains stable upon extensive transcriptional changes driven by heat shock. Proceedings of the National Academy of Sciences, 116, 201901244.
Sakurai, H. & Enoki, Y. (2010) Novel aspects of heat shock factors: DNA recognition, chromatin modulation and gene expression. FEBS Journal, 277, 4140-4149.
Schmittgen, T.D. & Livak, K.J. (2008) Analyzing real-time PCR data by the comparative CT method. Nature Protocols, 3, 1101-1108.
Song, J., Lu, M.X. & Du, Y.Z. (2020) Molecular cloning and expression patterns of two small heat shock proteins from Chilo suppressalis (Walker). Journal of Integrative Agriculture, 19, 1522-1529.
Stamm, S., Ben-Ari, S., Rafalska, I., Tang, Y., Zhang, Z., Toiber, D. et al. (2005) Function of alternative splicing. Gene, 344, 1-20.
Tian, Z., Wang, S., Bai, B., Gao, B. & Liu, J. (2020) Effects of temperature on survival, development, and reproduction of Aphis glycines (Hemiptera: Aphididae) autumnal morphs. Florida Entomologist, 103, 236-242.
Tokumoto, S., Miyata, Y., Deviatiiarov, R., Yamada, T.G., Hiki, Y., Kozlova, O. et al. (2021) Genome-wide role of HSF1 in transcriptional regulation of desiccation tolerance in the Anhydrobiotic cell line, Pv11. International Journal of Molecular Sciences, 22, 5798.
Tran, S.E.F., Meinander, A., Holmström, T.H., Rivero-Müller, A., Heiskanen, K.M., Linnau, E.K. et al. (2003) Heat stress downregulates FLIP and sensitizes cells to Fas receptor-mediated apoptosis. Cell Death and Differentiation, 10, 1137-1147.
Veri, A.O., Miao, Z., Shapiro, R.S., Tebbji, F., O'Meara, T.R., Kim, S.H. et al. (2018) Tuning Hsf1 levels drives distinct fungal morphogenetic programs with depletion impairing Hsp90 function and overexpression expanding the target space. PLoS Genetics, 14, e1007270.
Volovik, Y., Maman, M., Dubnikov, T., Bejerano-Sagie, M., Joyce, D., Kapernick, E.A. et al. (2012) Temporal requirements of heat shock factor-1 for longevity assurance. Aging Cell, 11, 491-499.
Vujanac, M., Fenaroli, A. & Zimarino, V. (2005) Constitutive nuclear import and stress-regulated nucleocytoplasmic shuttling of mammalian heat-shock factor 1. Traffic, 6, 214-229.
Wiederrecht, G., Seto, D. & Parker, C.S. (1988) Isolation of the gene encoding the S. cerevisiae heat shock transcription factor. Cell, 6, 841-853.
Wu, C. (1995) Heat shock transcription factors: structure and regulation. Annual Review of Cell and Developmental Biology, 11, 441-469.
Xia, W., Voellmy, R. & Spector, N.L. (2000) Sensitization of tumor cells to Fas killing through overexpression of heat-shock transcription factor 1. Journal of Cellular Physiology, 183, 425-431.
Xiao, H., Perisic, O. & Lis, J.T. (1991) Cooperative binding of drosophila heat shock factor to arrays of a conserved 5 bp unit. Cell, 64, 585-593.
Xu, J., Lu, M.X., Cui, Y.D. & Du, Y.Z. (2017) Selection and evaluation of reference genes for expression analysis using qRT-PCR in Chilo suppressalis (Lepidoptera: Pyralidae). Journal of Economic Entomology, 110, 683-691.
Zhang, G., Storey, J.M. & Storey, K.B. (2011) Chaperone proteins and winter survival by a freeze tolerant insect. Journal of Insect Physiology, 57, 1115-1122.
Zhang, G., Storey, J.M. & Storey, K.B. (2018) Elevated chaperone proteins are a feature of winter freeze avoidance by larvae of the goldenrod gall moth, Epiblema scudderiana. Journal of Insect Physiology, 106, 106-113.
Zhang, Y.W., Wang, F., Wu, F., Wang, Y.H., Wang, X., Gui, Y.H. et al. (2020) Tnni1b-ecr183-d2, an 87 bp cardiac enhancer of zebrafish. PeerJ, 8, e10289.
Zhang, Y.B., Zhang, G.F., Liu, W.X. & Wan, F.H. (2019) Variable temperatures across different stages have novel effects on behavioral response and population viability in a host-feeding parasitoid. Scientific Reports, 9, 2202.
Zhao, X., Li, Q., Meng, Q., Yue, C. & Xu, C. (2017) Identification and expression of cysteine sulfinate decarboxylase, possible regulation of taurine biosynthesis in Crassostrea gigas in response to low salinity. Scientific Reports, 7, 5505.
Zhong, M., Orosz, A. & Wu, C. (1998) Direct sensing of heat and oxidation by drosophila heat shock transcription factor. Molecular Cell, 2, 101-108.
Zhu, G., Xue, M., Luo, Y., Ji, G., Liu, F., Zhao, H. et al. (2017) Effects of short-term heat shock and physiological responses to heat stress in two Bradysia adults, Bradysia odoriphaga and Bradysia difformis. Scientific Reports, 7, 13381.