Insights into small Heat Shock Proteins: Drivers of environmental stress tolerance in selected animal species

Jamada Bwambale, Justus Aisu, Muziri Mugwanya, DOI: 10.46793/BiolNyss.16.1.5B

Abstract


Insects, nematodes, and aquatic animals face several biotic and abiotic stressors that can significantly affect their fitness – specifically damaging their cellular protein function. As a result, they have evolved sophisticated stress-responsive mechanisms. Certain endogenous proteins, the small Heat Shock Proteins (sHSPs), are proposed to maintain the stability and function of proteins under stress. Since the identification of the first sHSPs, an increasing number of sHSPs, mainly due to the new robust sequencing tools, continue to be identified and reported to play a critical role in the response of organisms to stress. This review explores and summarizes the contributions of the sHSPs implicated in the stress response of different animal species in unique environments. Understanding their function is crucial for advancing our knowledge of how different animal species adapt to harsh environments while maintaining cellular homeostasis.


Keywords


abiotic stress, biotic stress, aquatic animals, cell damage, insects, nematodes, resistance

Full Text:

PDF

References


Abdullah, M. (1961). Behavioral effects of temperature on insects. The Ohio Journal of Science, 61, 212-219.

Adhikari, B. N., Wall, D. H., & Adams, B. J. (2010). Effect of slow desiccation and freezing on gene transcription and stress survival of an Antarctic nematode. Journal of Experimental Biology, 213(11), 1803–1812. https://doi.org/10.1242/jeb.032268

Albrecht, F. O., Verdier, M., & Blackith, R. E. (1959). Maternal Control of Ovariole Number in the Progeny of the Migratory Locust. Nature, 184(4680), 103–104. https://doi.org/10.1038/184103a0

Arockiaraj, J., Vanaraja, P., Easwvaran, S., Singh, A., Othman, R. Y., & Bhassu, S. (2012). Gene expression and functional studies of small heat shock protein 37 (MrHSP37) from Macrobrachium rosenbergii challenged with infectious hypodermal and hematopoietic necrosis virus (IHHNV). Molecular Biology Reports, 39(6), 6671–6682. https://doi.org/10.1007/s11033-012-1473-7

Atungulu, E., Tanaka, H., Fujita, K., Yamamoto, K., Sakata, M., Sato, E., Hara, M., Yamashita, T., & Suzuki, K. (2006). A Double Chaperone Function of the sHsp Genes against Heat-Based Environmental Adversity in the Soil-Dwelling Leaf Beetles. Journal of Insect Biotechnology and Sericology, 75, 15–22. https://api.semanticscholar.org/CorpusID:82542287

Baglan, H., Lazzari, C. R., & Guerrieri, F. J. (2018). Glyphosate impairs learning in Aedes aegypti mosquito larvae at field-realistic doses. The Journal of Experimental Biology, 221(Pt 20), jeb187518. https://doi.org/10.1242/jeb.187518

Balakumaran, M., Chidambaranathan, P., Tej Kumar, J. P. J. P., Sirohi, A., Kumar Jain, P., Gaikwad, K., Iyyappan, Y., Rao, A. R., Sahu, S., Dahuja, A., & Mohan, S. (2022). Deciphering the mechanism of anhydrobiosis in the entomopathogenic nematode Heterorhabditis indica through comparative transcriptomics. PLoS ONE, 17(10 October). https://doi.org/10.1371/journal.pone.0275342

Balali-Mood, M., Naseri, K., Tahergorabi, Z., Khazdair, M. R., & Sadeghi, M. (2021). Toxic Mechanisms of Five Heavy Metals: Mercury, Lead, Chromium, Cadmium, and Arsenic. Frontiers in Pharmacology, 12(April), 1–19. https://doi.org/10.3389/fphar.2021.643972

Bale, J. S., Masters, G. J., Hodkinson, I. D., Awmack, C., Bezemer, T. M., Brown, V. K., Butterfield, J., Buse, A., Coulson, J. C., Farrar, J., Good, J. E. G., Harrington, R., Hartley, S., Jones, T. H., Lindroth, R. L., Press, M. C., Symrnioudis, I., Watt, A. D., & Whittaker, J. B. (2002). Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Global Change Biology, 8(1), 1–16. https://doi.org/10.1046/j.1365-2486.2002.00451.x

Basha, E., O’Neill, H., & Vierling, E. (2012). Small heat shock proteins and α-crystallins: dynamic proteins with flexible functions. Trends in Biochemical Sciences, 37(3), 106–117. https://doi.org/10.1016/j.tibs.2011.11.005

Basson, C. H., & Terblanche, J. S. (2010). Metabolic responses of Glossina pallidipes (Diptera: Glossinidae) puparia exposed to oxygen and temperature variation: Implications for population dynamics and subterranean life. Journal of Insect Physiology, 56(12), 1789–1797. https://doi.org/10.1016/j.jinsphys.2010.07.010

Bildik, A. E., Ekren, G. S. A., Akdeniz, G., & Kiral, F. K. (2019). Effect of environmental temperature on heat shock proteins (HSP30, HSP70, HSP90) and IGF-I mRNA expression in Sparus aurata. Iranian Journal of Fisheries Sciences, 18, 1014–1024. https://api.semanticscholar.org/CorpusID:190881931

Brunquell, J., Morris, S., Lu, Y., Cheng, F., & Westerheide, S. D. (2016). The genome-wide role of HSF-1 in the regulation of gene expression in Caenorhabditis elegans. BMC Genomics, 17(1), 559. https://doi.org/10.1186/s12864-016-2837-5

Cadet, J., Sage, E., & Douki, T. (2005). Ultraviolet radiation-mediated damage to cellular DNA. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, 571(1–2), 3–17. https://doi.org/10.1016/j.mrfmmm.2004.09.012

Chapuis, M.-P., Simpson, S. J., Blondin, L., & Sword, G. A. (2011). Taxa-specific heat shock proteins are over-expressed with crowding in the Australian plague locust. Journal of Insect Physiology, 57(11), 1562–1567. https://doi.org/10.1016/j.jinsphys.2011.08.011

Chen, W., Zhang, M., Luo, X., Zhang, Z., & Hu, X. (2022). Molecular characterization of heat shock protein 20 (hsp20) in goldfish (Carassius auratus) and expression analysis in response to environmental stresses. Aquaculture Reports, 24, 101106. https://doi.org/10.1016/j.aqrep.2022.101106

Chen, X., & Zhang, Y. (2015). Identification of multiple small heat-shock protein genes in Plutella xylostella (L.) and their expression profiles in response to abiotic stresses. Cell Stress and Chaperones, 20(1), 23–35. https://doi.org/10.1007/s12192-014-0522-7

Cheng, S., Lin, R., Wang, L., Qiu, Q., Qu, M., Ren, X., Zong, F., Jiang, H., & Yu, C. (2018). Comparative susceptibility of thirteen selected pesticides to three different insect egg parasitoid Trichogramma species. Ecotoxicology and Environmental Safety, 166, 86–91. https://doi.org/10.1016/j.ecoenv.2018.09.050

Chu, J., Jiang, D., Yan, M., Li, Y., Wang, J., Wu, F., & Sheng, S. (2020). Identifications, Characteristics, and Expression Patterns of Small Heat Shock Protein Genes in a Major Mulberry Pest, Glyphodes pyloalis (Lepidoptera: Pyralidae). Journal of Insect Science, 20(3). https://doi.org/10.1093/jisesa/ieaa029

Colinet, H., Lee, S. F., & Hoffmann, A. (2010a). Knocking down expression of Hsp22 and Hsp23 by RNA interference affects recovery from chill coma in Drosophila melanogaster. Journal of Experimental Biology, 213(24), 4146–4150. https://doi.org/10.1242/jeb.051003

Colinet, H., Lee, S. F., & Hoffmann, A. (2010b). Temporal expression of heat shock genes during cold stress and recovery from chill coma in adult Drosophila melanogaster. The FEBS Journal, 277(1), 174–185. https://doi.org/10.1111/j.1742-4658.2009.07470.x

Colinet, H., Sinclair, B. J., Vernon, P., & Renault, D. (2015). Insects in Fluctuating Thermal Environments. Annual Review of Entomology, 60(1), 123–140. https://doi.org/10.1146/annurev-ento-010814-021017

Currie, S. (2000). The effects of heat shock and acclimation temperature on hsp70 and hsp30 mRNA expression in rainbow trout: in vivo and in vitro comparisons. Journal of Fish Biology, 56(2), 398–408. https://doi.org/10.1006/jfbi.1999.1166

Dahlgaard, J., Loeschcke, V., Michalak, P., & Justesen, J. (1998). Induced thermotolerance and associated expression of the heat‐shock protein Hsp70 in adult Drosophila melanogaster. Functional Ecology, 12(5), 786–793. https://doi.org/10.1046/j.1365-2435.1998.00246.x

Das, S., Kar, I., & Patra, A. K. (2023). Cadmium induced bioaccumulation, histopathology, gene regulation in fish and its amelioration – A review. Journal of Trace Elements in Medicine and Biology, 79(November 2021), 127202. https://doi.org/10.1016/j.jtemb.2023.127202

D’Ávila, V. A., Barbosa, W. F., Guedes, R. N. C., & Cutler, G. C. (2018). Effects of Spinosad, Imidacloprid, and Lambda-cyhalothrin on Survival, Parasitism, and Reproduction of the Aphid Parasitoid Aphidius colemani. Journal of Economic Entomology, 111(3), 1096–1103. https://doi.org/10.1093/jee/toy055

Denlinger, D. L., Rinehart, J. P., & Yocum, G. D. (2001). Stress proteins. In Insect Timing: Circadian Rhythmicity to Seasonality (pp. 155–171).

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. https://doi.org/10.1016/j.ijbiomac.2021.07.186

Eisenhardt, B. D. (2013). Small heat shock proteins: Recent developments. Biomolecular Concepts, 4(6), 583–595. https://doi.org/10.1515/bmc-2013-0028

Erkut, C., Vasilj, A., Boland, S., Habermann, B., Shevchenko, A., & Kurzchalia, T. V. (2013). Molecular strategies of the Caenorhabditis elegans dauer larva to survive extreme desiccation. PLoS ONE, 8(12). https://doi.org/10.1371/journal.pone.0082473

Ezemaduka, A. N., Wang, Y., & Li, X. (2017). Expression of CeHSP17 Protein in Response to Heat Shock and Heavy Metal Ions. Journal of Nematology, 49(3).

Feder, M. E., & Hofmann, G. E. (1999). Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annual Review of Physiology, 61, 243–282. https://doi.org/10.1146/annurev.physiol.61.1.243

Flis, Ł., Malewski, T., & Dobosz, R. (2024). Temperature Effects on Expression Levels of hsp Genes in Eggs and Second-Stage Juveniles of Meloidogyne hapla Chitwood, 1949. International Journal of Molecular Sciences, 25(9). https://doi.org/10.3390/ijms25094867

Fonseca, F., Pénicaud, C., Tymczyszyn, E. E., Gómez-Zavaglia, A., & Passot, S. (2019). Factors influencing the membrane fluidity and the impact on production of lactic acid bacteria starters. In Applied Microbiology and Biotechnology (Vol. 103, Issue 17, pp. 6867–6883). Springer Verlag. https://doi.org/10.1007/s00253-019-10002-1

Gaur, V. K., Sharma, P., Sirohi, R., Awasthi, M. K., Dussap, C. G., & Pandey, A. (2020). Assessing the impact of industrial waste on environment and mitigation strategies: A comprehensive review. Journal of Hazardous Materials, 398(April), 123019. https://doi.org/10.1016/j.jhazmat.2020.123019

Georgiadou, E. C., Kowalska, E., Patla, K., Kulbat, K., Smolińska, B., Leszczyńska, J., & Fotopoulos, V. (2018). Influence of Heavy Metals (Ni, Cu, and Zn) on Nitro-Oxidative Stress Responses, Proteome Regulation and Allergen Production in Basil (Ocimum basilicum L.) Plants. Frontiers in Plant Science, 9. https://doi.org/10.3389/fpls.2018.00862

Gething, M.-J., & Sambrook, J. (1992). Protein folding in the cell. Nature, 355(6355), 33–45. https://doi.org/10.1038/355033a0

Gilbert, N., & Raworth, D. A. (1996). FORUM: INSECTS AND TEMPERATURE—A GENERAL THEORY. The Canadian Entomologist, 128(1), 1–13. https://doi.org/10.4039/Ent1281-1

Gkouvitsas, T., Kontogiannatos, D., & Kourti, A. (2008). Differential expression of two small Hsps during diapause in the corn stalk borer Sesamia nonagrioides (Lef.). Journal of Insect Physiology, 54(12), 1503–1510. https://doi.org/10.1016/j.jinsphys.2008.08.009

González‐Tokman, D., Córdoba‐Aguilar, A., Dáttilo, W., Lira‐Noriega, A., Sánchez‐Guillén, R. A., & Villalobos, F. (2020). Insect responses to heat: physiological mechanisms, evolution and ecological implications in a warming world. Biological Reviews, 95(3), 802–821. https://doi.org/10.1111/brv.12588

Guillén, L., Pascacio-Villafán, C., Osorio-Paz, I., Ortega-Casas, R., Enciso-Ortíz, E., Altúzar-Molina, A., Velázquez, O., & Aluja, M. (2022). Coping with global warming: Adult thermal thresholds in four pestiferous Anastrepha species determined under experimental laboratory conditions and development/survival times of immatures and adults under natural field conditions. Frontiers in Physiology, 13. https://doi.org/10.3389/fphys.2022.991923

Häder, D.-P., Banaszak, A. T., Villafañe, V. E., Narvarte, M. A., González, R. A., & Helbling, E. W. (2020). Anthropogenic pollution of aquatic ecosystems: Emerging problems with global implications. Science of The Total Environment, 713, 136586. https://doi.org/10.1016/j.scitotenv.2020.136586

Hadley, N. F. (1994). Water Relations of Terrestrial Arthropods. https://api.semanticscholar.org/CorpusID:83962304

Hansen, J. M., Go, Y.-M., & Jones, D. P. (2006). Nuclear and mitochondrial compartmentation of oxidative stress and redox signaling. Annual Review of Pharmacology and Toxicology, 46, 215–234. https://doi.org/10.1146/annurev.pharmtox.46.120604.141122

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(4), 364. https://doi.org/10.1379/CSC-308.1

Hartwig, A., Asmuss, M., Blessing, H., Hoffmann, S., Jahnke, G., Khandelwal, S., Pelzer, A., & Bürkle, A. (2002). Interference by toxic metal ions with zinc-dependent proteins involved in maintaining genomic stability. Food and Chemical Toxicology: An International Journal Published for the British Industrial Biological Research Association, 40(8), 1179–1184. https://doi.org/10.1016/s0278-6915(02)00043-1

Hibshman, J. D., Carra, S., & Goldstein, B. (2023). Tardigrade small heat shock proteins can limit desiccation-induced protein aggregation. Communications Biology, 6(1), 121. https://doi.org/10.1038/s42003-023-04512-y

Hoback, W. W., & Stanley, D. W. (2001). Insects in hypoxia. Journal of Insect Physiology, 47(6), 533–542. https://doi.org/10.1016/s0022-1910(00)00153-0

Hong, M., Kwon, J. Y., Shim, J., & Lee, J. (2004). Differential hypoxia response of hsp-16 genes in the nematode. Journal of Molecular Biology, 344(2), 369–381. https://doi.org/10.1016/j.jmb.2004.09.077

Horikawa, M., Fukuyama, M., Antebi, A., & Mizunuma, M. (2024). Regulatory mechanism of cold-inducible diapause in Caenorhabditis elegans. Nature Communications, 15(1). https://doi.org/10.1038/s41467-024-50111-8

Huang, L.-H., Chen, B., & Kang, L. (2007). Impact of mild temperature hardening on thermotolerance, fecundity, and Hsp gene expression in Liriomyza huidobrensis. Journal of Insect Physiology, 53(12), 1199–1205. https://doi.org/10.1016/j.jinsphys.2007.06.011

Huang, L.-H., Wang, C.-Z., & Kang, L. (2009). Cloning and expression of five heat shock protein genes in relation to cold hardening and development in the leafminer, Liriomyza sativa. Journal of Insect Physiology, 55(3), 279–285. https://doi.org/10.1016/j.jinsphys.2008.12.004

Huang, P., Kang, S., Chen, W., Hsu, T., Lo, C., Liu, K., & Chen, L. (2008). Identification of the small heat shock protein, HSP21, of shrimp Penaeus monodon and the gene expression of HSP21 is inactivated after white spot syndrome virus (WSSV) infection. Fish & Shellfish Immunology, 25(3), 250–257. https://doi.org/10.1016/j.fsi.2008.06.002

Huang, Y., Zhang, Y., Niu, X., Sun, Y., Wang, H., Guo, X., Xu, B., & Wang, C. (2023). AccsHSP21.7 enhances the antioxidant capacity of Apis cerana cerana. Journal of the Science of Food and Agriculture, 103(11), 5401–5411. https://doi.org/10.1002/jsfa.12614

Jaishankar, M., Tseten, T., Anbalagan, N., Mathew, B. B., & Beeregowda, K. N. (2014). Toxicity, mechanism and health effects of some heavy metals. Interdisciplinary Toxicology, 7(2), 60–72. https://doi.org/10.2478/intox-2014-0009

Jecock, R. M., & Devaney, E. (1992). Expression of small heat shock proteins by the third-stage larva of Brugia pahangi. In Molecular and Biochemical Parasitology (Vol. 56).

Jomova, K., Raptova, R., Alomar, S. Y., Alwasel, S. H., Nepovimova, E., Kuca, K., & Valko, M. (2023). Reactive oxygen species, toxicity, oxidative stress, and antioxidants: chronic diseases and aging. In Archives of Toxicology, 97(10), 2499–2574. Springer Science and Business Media Deutschland GmbH. https://doi.org/10.1007/s00204-023-03562-9

Jomova, K., & Valko, M. (2011). Advances in metal-induced oxidative stress and human disease. Toxicology, 283(2–3), 65–87. https://doi.org/10.1016/j.tox.2011.03.001

Kannan, K., & Jain, S. (2000). Oxidative stress and apoptosis. Pathophysiology: The Official Journal of the International Society for Pathophysiology, 7(3), 153–163. https://doi.org/10.1016/s0928-4680(00)00053-5

Katoh, K., Misawa, K., Kuma, K.-I., & Miyata, T. (n.d.). MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform.

Katoh, K., & Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution, 30(4), 772–780. https://doi.org/10.1093/molbev/mst010

Kayastha, P., Wieczorkiewicz, F., Pujol, M., Robinson, A., Michalak, M., Kaczmarek, Ł., & Poprawa, I. (2024). Elevated external temperature affects cell ultrastructure and heat shock proteins (HSPs) in Paramacrobiotus experimentalis Kaczmarek, Mioduchowska, Poprawa, & Roszkowska, 2020. Scientific Reports, 14(1). https://doi.org/10.1038/s41598-024-55295-z

Khan, Z., Elahi, A., Bukhari, D. A., & Rehman, A. (2022). Cadmium sources, toxicity, resistance and removal by microorganisms—A potential strategy for cadmium eradication. Journal of Saudi Chemical Society, 26(6), 101569. https://doi.org/10.1016/j.jscs.2022.101569

Kim, B. M., Rhee, J. S., Jeong, C. B., Seo, J. S., Park, G. S., Lee, Y. M., & Lee, J. S. (2014). Heavy metals induce oxidative stress and trigger oxidative stress-mediated heat shock protein (HSP) modulation in the intertidal copepod Tigriopus japonicus. Comparative Biochemistry and Physiology Part C: Toxicology and Pharmacology, 166, 65–74. https://doi.org/10.1016/j.cbpc.2014.07.005

King, A. M., & MacRae, T. H. (2015). Insect heat shock proteins during stress and diapause. Annual Review of Entomology, 60(1), 59–75. https://doi.org/10.1146/annurev-ento-011613-162107

Kyriakou, E., Taouktsi, E., & Syntichaki, P. (2022). The thermal stress coping network of the nematode Caenorhabditis elegans. International Journal of Molecular Sciences, 23(23). https://doi.org/10.3390/ijms232314907

Lee, J., & Lee, J. (2013). Hypoxia-inducible factor-1 (HIF-1)-independent hypoxia response of the small heat shock protein hsp-16.1 gene regulated by chromatin-remodeling factors in the nematode Caenorhabditis elegans. Journal of Biological Chemistry, 288(3), 1582–1589. https://doi.org/10.1074/jbc.M112.401554

Li, C., Wang, L., Ning, X., Chen, A., Zhang, L., Qin, S., Wu, H., & Zhao, J. (2010). Identification of two small heat shock proteins with different response profiles to cadmium and pathogen stresses in Venerupis philippinarum. Cell Stress and Chaperones, 15(6), 897–904. https://doi.org/10.1007/s12192-010-0198-6

Li, H., Liu, S., He, C., Gao, X., & Yuan, X. (2013). Identification of a small HSP gene from hard clam Meretrix meretrix and its potential as an environmental stress biomarker. Aquatic Biology, 18(3), 243–252. https://doi.org/10.3354/ab00503

Li, J., Moghaddam, S. H. H., Du, X., Zhong, B.-X., & Chen, Y.-Y. (2012). Comparative analysis on the expression of inducible HSPs in the silkworm, Bombyx mori. Molecular Biology Reports, 39(4), 3915–3923. https://doi.org/10.1007/s11033-011-1170-y

Li, M., Tang, T., Yuan, F., Zhang, Y., Li, F., & Liu, F. (2022). Protective effects of small heat shock proteins in Daphnia magna against heavy metal exposure. Science of The Total Environment, 848, 157565. https://doi.org/10.1016/j.scitotenv.2022.157565

Li, M., Wei, X. M., Li, J., Wei, S. M., Zhang, J. L., Chen, G. H., & Zhang, X. M. (2023). Effect of short-term exposure to high temperatures on the reproductive behavior and physiological enzyme activities in the fruit fly Zeugodacus tau (Walker). Frontiers in Physiology, 14, 1036397. https://doi.org/10.3389/FPHYS.2023.1036397/BIBTEX

Liang, P., & MacRae, T. H. (1999). The synthesis of a small heat shock/α-crystallin protein in Artemia and its relationship to stress tolerance during development. Developmental Biology, 207(2), 445–456. https://doi.org/10.1006/dbio.1998.9138

Liu, G., Roy, J., & Johnson, E. A. (2006). Identification and function of hypoxia-response genes in Drosophila melanogaster. Physiological Genomics, 25(1), 134–141. https://doi.org/10.1152/physiolgenomics.00262.2005

Liu, X., Shi, H., Liu, Z., Kang, Y., Wang, J., & Huang, J. (2019). Effect of heat stress on heat shock protein 30 (Hsp30) mRNA expression in rainbow trout (Oncorhynchus mykiss). https://api.semanticscholar.org/CorpusID:201724315

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 and Chaperones, 17(5), 539–551. https://doi.org/10.1007/S12192-012-0330-X

Lopez-Martinez, G., Elnitsky, M. A., Benoit, J. B., Lee, R. E., & Denlinger, D. L. (2008). High resistance to oxidative damage in the Antarctic midge Belgica antarctica, and developmentally linked expression of genes encoding superoxide dismutase, catalase and heat shock proteins. Insect Biochemistry and Molecular Biology, 38(8), 796–804. https://doi.org/10.1016/j.ibmb.2008.05.006

Mahanty, A., Purohit, G. K., Yadav, R. P., Mohanty, S., & Mohanty, B. P. (2017). Hsp90 and Hsp47 appear to play an important role in minnow Puntius sophore for surviving in the hot spring run-off aquatic ecosystem. Fish Physiology and Biochemistry, 43(1), 89–102. https://doi.org/10.1007/s10695-016-0270-y

Martelli, F., Zhongyuan, Z., Wang, J., Wong, C.-O., Karagas, N. E., Roessner, U., Rupasinghe, T., Venkatachalam, K., Perry, T., Bellen, H. J., & Batterham, P. (2020). Low doses of the neonicotinoid insecticide imidacloprid induce ROS triggering neurological and metabolic impairments in Drosophila. Proceedings of the National Academy of Sciences of the United States of America, 117(41), 25840–25850. https://doi.org/10.1073/pnas.2011828117

Martín-Folgar, R., & Martínez-Guitarte, J.-L. (2017). Cadmium alters the expression of small heat shock protein genes in the aquatic midge Chironomus riparius. Chemosphere, 169, 485–492. https://doi.org/10.1016/j.chemosphere.2016.11.067

Meng, J.-Y., Zhang, C.-Y., Zhu, F., Wang, X.-P., & Lei, C.-L. (2009). Ultraviolet light-induced oxidative stress: Effects on antioxidant response of Helicoverpa armigera adults. Journal of Insect Physiology, 55(6), 588–592. https://doi.org/10.1016/j.jinsphys.2009.03.003

Meyer-Rochow, V. B., Kashiwagi, T., & Eguchi, E. (2002). Selective photoreceptor damage in four species of insects induced by experimental exposures to UV-irradiation. Micron, 33(1), 23–31. https://doi.org/10.1016/S0968-4328(00)00073-1

Michaud, M. R., Teets, N. M., Peyton, J. T., Blobner, B. M., & Denlinger, D. L. (2011). Heat shock response to hypoxia and its attenuation during recovery in the flesh fly, Sarcophaga crassipalpis. Journal of Insect Physiology, 57(1), 203–210. https://doi.org/10.1016/j.jinsphys.2010.11.007

Miernyk, J. A. (1999). Protein folding in the plant cell. Plant Physiology, 121(3), 695–703. https://doi.org/10.1104/pp.121.3.695

Moiseenko, T. I., & Gashkina, N. A. (2020). Distribution and bioaccumulation of heavy metals (Hg, Cd, and Pb) in fish: Influence of the aquatic environment and climate. Environmental Research Letters, 15(11). https://doi.org/10.1088/1748-9326/abbf7c

Morales, M., Planelló, R., Martínez-Paz, P., Herrero, O., Cortés, E., Martínez-Guitarte, J. L., & Morcillo, G. (2011). Characterization of Hsp70 gene in Chironomus riparius: Expression in response to endocrine-disrupting pollutants as a marker of ecotoxicological stress. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 153(1), 150–158. https://doi.org/10.1016/j.cbpc.2010.10.003

Morris, A. M., & Aquilina, J. A. (2010). Evidence for specific subunit distribution and interactions in the quaternary structure of α-crystallin. Proteins: Structure, Function, and Bioinformatics, 78(11), 2546–2553. https://doi.org/10.1002/prot.22766

Morrow, G., Battistini, S., Zhang, P., & Tanguay, R. M. (2004). Decreased lifespan in the absence of expression of the mitochondrial small heat shock protein Hsp22 in Drosophila. The Journal of Biological Chemistry, 279(42), 43382–43385. https://doi.org/10.1074/jbc.C400357200

Mugwanya, M., Dawood, M. A. O., Kimera, F., & Sewilam, H. (2022). Anthropogenic temperature fluctuations and their effect on aquaculture: A comprehensive review. Aquaculture and Fisheries, 7(3), 223–243. https://doi.org/10.1016/j.aaf.2021.12.005

Muthusamy, S. K., Dalal, M., Chinnusamy, V., & Bansal, K. C. (2017). Genome-wide identification and analysis of biotic and abiotic stress regulation of small heat shock protein (HSP20) family genes in bread wheat. Journal of Plant Physiology, 211, 100–113. https://doi.org/10.1016/j.jplph.2017.01.004

Nooten, S. S., Korten, H., Schmitt, T., & Kárpáti, Z. (2024). The heat is on: reduced detection of floral scents after heatwaves in bumblebees. Proceedings of the Royal Society B: Biological Sciences, 291(2029), 20240352. https://doi.org/10.1098/rspb.2024.0352

Otaka, M., Odashima, M., & Watanabe, S. (2006). Role of heat shock proteins (molecular chaperones) in intestinal mucosal protection. Biochemical and Biophysical Research Communications, 348(1), 1–5. https://doi.org/10.1016/j.bbrc.2006.07.028

Parsell, D. A., & Lindquist, S. (1993). The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annual Review of Genetics, 27, 437–496. https://doi.org/10.1146/annurev.ge.27.120193.002253

Peter, E., Candido, M. (2002). The Small Heat Shock Proteins of the Nematode Caenorhabditis elegans: Structure, Regulation and Biology. In: Arrigo, AP., Müller, W.E.G. (eds) Small Stress Proteins. Progress in Molecular and Subcellular Biology, vol 28. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-56348-5_4

Qiu, Z., Bossier, P., Wang, X., Bojikova-Fournier, S., & MacRae, T. H. (2006). Diversity, structure, and expression of the gene for p26, a small heat shock protein from Artemia. Genomics, 88(2), 230–240. https://doi.org/10.1016/j.ygeno.2006.02.008

Rajak, P., & Roy, S. (2018). Heat Shock Proteins and Pesticide Stress. In A. A. A. Asea & P. Kaur (Eds.), Regulation of Heat Shock Protein Responses (Vol. 13, pp. 27–40). Springer International Publishing. http://link.springer.com/10.1007/978-3-319-74715-6_2

Reichmann, D., Voth, W., & Jakob, U. (2018). Maintaining a Healthy Proteome during Oxidative Stress. Molecular Cell, 69(2), 203–213. https://doi.org/10.1016/j.molcel.2017.12.021

Rinehart, J. P., Denlinger, D. L., & Rivers, D. B. (2002). Upregulation of transcripts encoding select heat shock proteins in the flesh fly Sarcophaga crassipalpis in response to venom from the ectoparasitoid wasp Nasonia vitripennis. Journal of Invertebrate Pathology, 79(1), 62–63. https://doi.org/10.1016/S0022-2011(02)00002-2

Rinehart, J. P., Li, A., Yocum, G. D., Robich, R. M., Hayward, S. A. L., & Denlinger, D. L. (2007). Up-regulation of heat shock proteins is essential for cold survival during insect diapause. Proceedings of the National Academy of Sciences, 104(27), 11130–11137. https://doi.org/10.1073/pnas.0703538104

Russnak, R. H., Peter, E., & Candido, M. (1983). Nucleic Acids Research: Cloning and analysis of cDNA sequences coding for two 16 kilodalton heat shock proteins (hsps) in Caenorhabditis elegans: homology with the small hsps of Drosophila.

Sadura, I., & Janeczko, A. (2024). Are Heat Shock Proteins Important in Low-Temperature-Stressed Plants? A Minireview. Agronomy, 14(6). https://doi.org/10.3390/agronomy14061296

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. Bioscience, Biotechnology, and Biochemistry, 70(10), 2443–2450. https://doi.org/10.1271/bbb.60176

Samanta, S., Barman, M., Chakraborty, S., Banerjee, A., & Tarafdar, J. (2021). Involvement of small heat shock proteins (sHsps) in developmental stages of fall armyworm, Spodoptera frugiperda, and its expression pattern under abiotic stress condition. Heliyon, 7(4), e06906. https://doi.org/10.1016/j.heliyon.2021.e06906

Sampayo, J. N., Olsen, A., & Lithgow, G. J. (2003). Oxidative stress in Caenorhabditis elegans: protective effects of superoxide dismutase/catalase mimetics. Aging Cell, 2(6), 319–326. https://doi.org/10.1046/j.1474-9728.2003.00063.x

Sánchez-Bayo, F., & Wyckhuys, K. A. G. (2019). Worldwide decline of the entomofauna: A review of its drivers. Biological Conservation, 232, 8–27. https://doi.org/10.1016/j.biocon.2019.01.020

Sang, W., Ma, W.-H., Qiu, L., Zhu, Z.-H., & Lei, C.-L. (2012). The involvement of heat shock protein and cytochrome P450 genes in response to UV-A exposure in the beetle Tribolium castaneum. Journal of Insect Physiology, 58(6), 830–836. https://doi.org/10.1016/j.jinsphys.2012.03.007

Shan, Y., Yan, S., Hong, X., Zha, J., & Qin, J. (2020). Effect of imidacloprid on the behavior, antioxidant system, multixenobiotic resistance, and histopathology of Asian freshwater clams (Corbicula fluminea). Aquatic Toxicology, 218, 105333. https://doi.org/10.1016/j.aquatox.2019.105333

Shashikumar, S., & Rajini, P. S. (2010). Cypermethrin elicited responses in heat shock protein and feeding in Caenorhabditis elegans. Ecotoxicology and Environmental Safety, 73(5), 1057–1062. https://doi.org/10.1016/j.ecoenv.2010.02.003

Shekhar, M. S., Kiruthika, J., & Ponniah, A. G. (2013). Identification and expression analysis of differentially expressed genes from shrimp (Penaeus monodon) in response to low salinity stress. Fish & Shellfish Immunology, 35(6), 1957–1968. https://doi.org/10.1016/j.fsi.2013.09.038

Shim, J.-K., Ha, D.-M., Nho, S.-K., Song, K.-S., & Lee, K.-Y. (2008). Upregulation of heat shock protein genes by envenomation of ectoparasitoid Bracon hebetor in larval host of Indian meal moth Plodia interpunctella. Journal of Invertebrate Pathology, 97(3), 306–309. https://doi.org/10.1016/j.jip.2007.10.001

Somensi, N., Brum, P. O., de Miranda Ramos, V., Gasparotto, J., Zanotto-Filho, A., Rostirolla, D. C., da Silva Morrone, M., Moreira, J. C. F., & Pens Gelain, D. (2017). Extracellular HSP70 Activates ERK1/2, NF-kB and Pro-Inflammatory Gene Transcription Through Binding with RAGE in A549 Human Lung Cancer Cells. Cellular Physiology and Biochemistry: International Journal of Experimental Cellular Physiology, Biochemistry, and Pharmacology, 42(6), 2507–2522. https://doi.org/10.1159/000480213

Sonone, S. S., Jadhav, S., Sankhla, M. S., & Kumar, R. (2021). Water Contamination by Heavy Metals and their Toxic Effect on Aquaculture and Human Health through Food Chain. Letters in Applied NanoBioScience, 10(2), 2148–2166. https://doi.org/10.33263/LIANBS102.21482166

Sørensen, J. G., Kristensen, T. N., & Loeschcke, V. (2003). The evolutionary and ecological role of heat shock proteins. Ecology Letters, 6(11), 1025–1037. https://doi.org/10.1046/j.1461-0248.2003.00528.x

Strayer, A., Wu, Z., Christen, Y., Link, C. D., & Luo, Y. (2003). Expression of the small heat‐shock protein Hsp‐16‐2 in Caenorhabditis elegans is suppressed by Ginkgo biloba extract EGb 761. The FASEB Journal, 17(15), 2305–2307. https://doi.org/10.1096/fj.03-0376fje

Sun, W., Montagu, M. Van, & Verbruggen, N. (2002). Small heat shock proteins and stress tolerance. Plant Physiology and Biochemistry, 1577(8), 1–9.

Sun, Y., & MacRae, T. H. (2005). Small heat shock proteins: Molecular structure and chaperone function. Cellular and Molecular Life Sciences, 62(21), 2460–2476. https://doi.org/10.1007/s00018-005-5190-4

Tamás, L., Mistrík, I., & Zelinová, V. (2017). Heavy metal-induced reactive oxygen species and cell death in barley root tip. Environmental and Experimental Botany, 140(May), 34–40. https://doi.org/10.1016/j.envexpbot.2017.05.016

Tamás, M. J., Sharma, S. K., Ibstedt, S., Jacobson, T., & Christen, P. (2014). Heavy metals and metalloids as a cause for protein misfolding and aggregation. Biomolecules, 4(1), 252–267. https://doi.org/10.3390/biom4010252

Thorne, M. A. S., Kagoshima, H., Clark, M. S., Marshall, C. J., & Wharton, D. A. (2014). Molecular analysis of the cold-tolerant Antarctic nematode, Panagrolaimus davidi. PLoS ONE, 9(8). https://doi.org/10.1371/journal.pone.0104526

Tian, L., Wang, X., Wang, X., Lei, C., & Zhu, F. (2018). Starvation-, thermal-, and heavy metal-associated expression of four small heat shock protein genes in Musca domestica. Gene, 642, 268–276. https://doi.org/10.1016/j.gene.2017.11.041

Tissières, A., Mitchell, H. K., & Tracy, U. M. (1974). Protein synthesis in salivary glands of Drosophila melanogaster: relation to chromosome puffs. Journal of Molecular Biology, 84(3), 389–398. https://doi.org/10.1016/0022-2836(74)90447-1

Tsvetkova, N. M., Horváth, I., Török, Z., Wolkers, W. F., Balogi, Z., Shigapova, N., Crowe, L. M., Tablin, F., Vierling, E., Crowe, J. H., & Vigh, L. (2002). Small heat-shock proteins regulate membrane lipid polymorphism. Proceedings of the National Academy of Sciences of the United States of America, 99(21), 13504–13509. https://doi.org/10.1073/pnas.192468399

Tyson, T., O’Mahony Zamora, G., Wong, S., Skelton, M., Daly, B., Jones, J. T., Mulvihill, E. D., Elsworth, B., Phillips, M., Blaxter, M., & Burnell, A. M. (2012). A molecular analysis of desiccation tolerance mechanisms in the anhydrobiotic nematode Panagrolaimus superbus using expressed sequenced tags. BMC Research Notes, 5. https://doi.org/10.1186/1756-0500-5-68

van Klink, R., Bowler, D. E., Gongalsky, K. B., Swengel, A. B., Gentile, A., & Chase, J. M. (2020). Meta-analysis reveals declines in terrestrial but increases in freshwater insect abundances. Science (New York, N.Y.), 368(6489), 417–420. https://doi.org/10.1126/science.aax9931

Viitasalo, M., & Bonsdorff, E. (2022). Global climate change and the Baltic Sea ecosystem: direct and indirect effects on species, communities and ecosystem functioning. Earth System Dynamics, 13(2), 711–747. https://doi.org/10.5194/esd-13-711-2022

Villeneuve, T. S., Ma, X., Sun, Y., Oulton, M. M., Oliver, A. E., & MacRae, T. H. (2006). Inhibition of apoptosis by p26: implications for small heat shock protein function during Artemia development. Cell Stress & Chaperones, 11(1), 71. https://doi.org/10.1379/CSC-154R.1

Walsh, B. S., Parratt, S. R., Mannion, N. L. M., Snook, R. R., Bretman, A., & Price, T. A. R. (2021). Plastic responses of survival and fertility following heat stress in pupal and adult Drosophila virilis. Ecology and Evolution, 11(24), 18238–18247. https://doi.org/10.1002/ece3.8418

Wang, F., Li, D., Chen, Q., & Ma, L. (2016). Genome-wide survey and characterization of the small heat shock protein gene family in Bursaphelenchus xylophilus. Gene, 579(2), 153–161. https://doi.org/10.1016/j.gene.2015.12.047

Wang, H., Li, K., Zhu, J.-Y., Fang, Q., Ye, G.-Y., Wang, H., Li, K., & Zhu, J.-Y. (2012). Cloning and expression pattern of heat shock protein genes from the endoparasitoid wasp, Pteromalus puparum, in response to environmental stresses. Archives of Insect Biochemistry and Physiology, 79(4–5), 247–263. https://doi.org/10.1002/arch.21013

Wang, H.‐S., Wang, X.‐H., Zhou, C.‐S., Huang, L.‐H., Zhang, S.‐F., Guo, W., & Kang, L. (2007). cDNA cloning of heat shock proteins and their expression in the two phases of the migratory locust. Insect Molecular Biology, 16(2), 207–219. https://doi.org/10.1111/j.1365-2583.2006.00715.x

Wang, X. X., Geng, S. L., Zhang, X. S., & Xu, W. H. (2020). P-S6K is associated with insect diapause via the ROS/AKT/S6K/CREB/HIF-1 pathway in the cotton bollworm, Helicoverpa armigera. Insect Biochemistry and Molecular Biology, 120. https://doi.org/10.1016/J.IBMB.2019.103262

Willsie, J. K., & Clegg, J. S. (2001). Nuclear p26, a small heat shock/α-crystallin protein, and its relationship to stress resistance in Artemia franciscana embryos. Journal of Experimental Biology, 204(13), 2339–2350. https://doi.org/10.1242/jeb.204.13.2339

Willsie, J. K., & Clegg, J. S. (2002). Small heat shock protein p26 associates with nuclear lamins and HSP70 in nuclei and nuclear matrix fractions from stressed cells. Journal of Cellular Biochemistry, 84(3), 601–614. https://doi.org/10.1002/jcb.10040

Xie, J., Hu, X.-X., Zhai, M.-F., Yu, X.-J., Song, X.-W., Gao, S.-S., Wu, W., & Li, B. (2019). Characterization and functional analysis of hsp18.3 gene in the red flour beetle, Tribolium castaneum. Insect Science, 26(2), 263–273. https://doi.org/10.1111/1744-7917.12543

Xie, J., Xiong, W., Hu, X., Gu, S., Zhang, S., Gao, S., Song, X., Bi, J., & Li, B. (2018). Characterization and functional analysis of hsp21.8b: An orthologous small heat shock protein gene in Tribolium castaneum. Journal of Applied Entomology, 142(7), 654–666. https://doi.org/10.1111/jen.12519

Yang, C.-L., Meng, J.-Y., Zhou, L., Yao, M.-S., & Zhang, C.-Y. (2021). Identification of five small heat shock protein genes in Spodoptera frugiperda and expression analysis in response to different environmental stressors. Cell Stress and Chaperones, 26(3), 527–539. https://doi.org/10.1007/s12192-021-01198-1

Yang, Q.-L., Yao, C.-L., & Wang, Z.-Y. (2012). Acute temperature and cadmium stress response characterization of small heat shock protein 27 in large yellow croaker, Larimichthys crocea. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 155(2), 190–197. https://doi.org/10.1016/j.cbpc.2011.08.003

Younis, A. E., Geisinger, F., Ajonina-Ekoti, I., Soblik, H., Steen, H., Mitreva, M., Erttmann, K. D., Perbandt, M., Liebau, E., & Brattig, N. W. (2011). Stage-specific excretory-secretory small heat shock proteins from the parasitic nematode Strongyloides ratti - Putative links to host’s intestinal mucosal defense system. FEBS Journal, 278(18), 3319–3336. https://doi.org/10.1111/j.1742-4658.2011.08248.x

Yu, L.-M., Zhang, W.-H., Han, X.-X., Li, Y.-Y., Lu, Y., Pan, J., Mao, J.-Q., Zhu, L.-Y., Deng, J.-J., Huang, W., & Liu, Y.-H. (2019). Hypoxia-Induced ROS Contribute to Myoblast Pyroptosis during Obstructive Sleep Apnea via the NF-κB/HIF-1α Signaling Pathway. Oxidative Medicine and Cellular Longevity, 2019, 1–19. https://doi.org/10.1155/2019/4596368

Yuan, F., Yang, Z., Tang, T., Xie, S., & Liu, F. (2019). A 28.6-kD small heat shock protein (MnHSP28.6) protects Macrobrachium nipponense against heavy metal toxicity and oxidative stress by virtue of its anti-aggregation activity. Fish & Shellfish Immunology, 95, 635–643. https://doi.org/10.1016/j.fsi.2019.10.053

Yuan, J.-W., Song, H.-X., Chang, Y.-W., Yang, F., Xie, H.-F., Gong, W.-R., & Du, Y.-Z. (2022). Identification, expression analysis and functional verification of two genes encoding small heat shock proteins in the western flower thrips, Frankliniella occidentalis (Pergande). International Journal of Biological Macromolecules, 211, 74–84. https://doi.org/10.1016/j.ijbiomac.2022.05.056

Zarei, S., Ghafouri, H., Vahdatiraad, L., & Heidari, B. (2024). The influence of HSP inducers on salinity stress in sterlet sturgeon (Acipenser ruthenus): In vitro study on HSP expression, immune responses, and antioxidant capacity. Cell Stress and Chaperones, 29(4), 552–566. https://doi.org/10.1016/j.cstres.2024.06.004

Zevian, S. C., & Yanowitz, J. L. (2014). Methodological considerations for heat shock of the nematode Caenorhabditis elegans. Methods, 68(3), 450–457. https://doi.org/10.1016/j.ymeth.2014.04.015

Zhang, A., Lu, Y., Li, C., Zhang, P., Su, X., Li, Y., Wang, C., & Li, T. (2013). A small heat shock protein (sHSP) from Sinonovacula constricta against heavy metals stresses. Fish & Shellfish Immunology, 34(6), 1605–1610. https://doi.org/10.1016/j.fsi.2013.03.005

Zhang, G., Storey, J. M., & Storey, K. B. (2011). Chaperone proteins and winter survival by a freeze-tolerant insect. Journal of Insect Physiology, 57(8), 1115–1122. https://doi.org/10.1016/j.jinsphys.2011.02.016

Zhang, Y., Liu, Y., Guo, X., Li, Y., Gao, H., Guo, X., & Xu, B. (2014). sHsp22.6, an intronless small heat shock protein gene, is involved in stress defense and development in Apis cerana cerana. Insect Biochemistry and Molecular Biology, 53, 1–12. https://doi.org/10.1016/j.ibmb.2014.06.007

Zhang, Y., Liu, Y., Zhang, J., Guo, Y., & Ma, E. (2015). Molecular Cloning and mRNA Expression of Heat Shock Protein Genes and Their Response to Cadmium Stress in the Grasshopper Oxya chinensis. PLOS ONE, 10(7), e0131244. https://doi.org/10.1371/journal.pone.0131244

Zhu, J.-Y., Wu, G.-X., Ye, G.-Y., & Hu, C. (2013). Heat shock protein genes (hsp20, hsp75 and hsp90) from Pieris rapae: molecular cloning and transcription in response to parasitization by Pteromalus puparum. Insect Science, 20(2), 183–193. https://doi.org/10.1111/j.1744-7917.2011.01494.x


Refbacks

  • There are currently no refbacks.