Белки теплового шока в нормальной физиологии насекомых

Авторы

  • Татьяна Геннадьевна Зачепило Институт физиологии им. И. П. Павлова РАН; Российский государственный педагогический университет им. А. И. Герцена https://orcid.org/0000-0001-6350-7050
  • Алиса Кирилловна Прибышина Институт физиологии им. И. П. Павлова РАН

DOI:

https://doi.org/10.33910/2687-1270-2022-3-2-221-232

Ключевые слова:

насекомые, белки теплового шока, шапероны, развитие, старение, нервная система, диапауза

Аннотация

Белки теплового шока являются молекулярными шаперонами, отвечают за правильную укладку белков и обеспечивают поддержание клеточного гомеостаза. Длительное время считалось, что белки теплового шока необходимы для развития клеточного ответа на тепловой шок, действие химических веществ, высушивание, гипоксию и другие стрессоры. Однако в последнее время появляется все больше фактов участия белков теплового шока в нормальной физиологии млекопитающих и насекомых. Данный обзор посвящен участию белков теплового шока в процессах развития, старения, в функционировании мышечной, зрительной и нервной систем у насекомых, а также в протекании диапаузы. У насекомых важную роль в этих процессах играют малые белки теплового шока. Повышение уровня экспрессии малых белков теплового шока способствует увеличению продолжительности жизни у мутантов дрозофилы. Активность белков теплового шока из семейства Hsp70 у насекомых связана с развитием и работой зрительной и центральной нервной системы, в частности, условно-рефлекторной деятельности у дрозофилы. Во время диапаузы осуществляется активация тех или иных белков теплового шока в зависимости от филогенетического положения, особенностей развития и экологии насекомого.

Библиографические ссылки

Bakthisaran, R., Tangirala, R., Rao, Ch. M. (2015) Small heat shock proteins: Role in cellular functions and pathology. Biochimica et Biophysica Acta (ВВА)—Proteins and Proteomics, vol. 1854, no. 4, pp. 291–319. https://doi.org/10.1016/j.bbapap.2014.12.019 (In English)

Chen, B., Kayukawa, T., Monteiro, A., Ishikawa, Y. (2005) The expression of the HSP90 gene in response to winter and summer diapauses and thermal-stress in the onion maggot, Delia antiqua. Insect Molecular Biology, vol. 14, no. 6, pp. 697–702. https://doi.org/10.1111/j.1365-2583.2005.00602.x (In English)

Chen, B., Kayukawa, T., Monteiro, A., Ishikawa, Y. (2006) Cloning and characterization of the HSP70 gene, and its expression in response to diapauses and thermal stress in the onion maggot, Delia antiqua. Journal of Biochemistry and Molecular Biology, vol. 39, no. 6, pp. 749–758. https://doi.org/10.5483/bmbrep.2006.39.6.749 (In English)

Das, N., Levine, R. L., Orr, W. C., Sohal, R. S. (2001) Selectivity of protein oxidative damage during aging in Drosophila melanogaster. Biochemical Journal, vol. 360, no. 1, pp. 209–216. https://doi.org/10.1042/0264-6021:3600209 (In English)

Fleming, J. E., Walton, J. K., Dubitski, R., Bensch, K. G. (1988) Aging results in an unusual expression of Drosophila heat shock proteins. Proceedings of the National Academy of Sciences USA, vol. 85, no. 11, pp. 4099–4103. https://doi.org/10.1073/pnas.85.11.4099 (In English)

Fremdt, H., Amendt, J., Zehner, R. (2014) Diapause-specific gene expression in Calliphora vicina (Diptera: Calliphoridae)—a useful diagnostic tool for forensic entomology. The International Journal of Legal Medicine, vol. 128, no. 6, pp. 1001–1011. https://doi.org/10.1007/s00414-013-0920-x (In English)

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, vol. 54, no. 12, pp. 1503–1510. https://doi.org/10.1016/j.jinsphys.2008.08.009 (In English)

Gkouvitsas, T., Kontogiannatos, D., Kourti, A. (2009a) Cognate Hsp70 gene is induced during deep larval diapause in the moth Sesamia nonagrioides. Insect Molecular Biology, vol. 18, no. 2, pp. 253–264. https://doi.org/10.1111/j.1365-2583.2009.00866.x (In English)

Gkouvitsas, T., Kontogiannatos, D., Kourti, A. (2009b) Expression of the Hsp 83 gene in response to diapause and thermal stress in the moth Sesamia nonagrioides. Insect Molecular Biology, vol. 8, no. 6, pp. 759–768. https://doi.org/10.1111/j.1365-2583.2009.00922.x (In English)

Jabłońska, J., Dubińska-Magiera, M., Jagla, T. et al. (2018) Drosophila Hsp67Bc hot-spot variants alter muscle structure and function. Cellular and Molecular Life Sciences, vol. 75, no. 23, pp. 4341–4356. https://doi.org/10.1007/s00018-018-2875-z (In English)

Jagla, T., Dubińska-Magiera, M., Poovathumkadavil, P. et al. (2018) Developmental expression and functions of the small heat shock proteins in Drosophila. International Journal of Molecular Sciences, vol. 19, no. 11, article 3441. https://doi.org/10.3390/ijms19113441 (In English)

Kankare, M., Salminen, T., Laiho, A. et al. (2010) Changes in gene expression linked with adult reproductive diapause in a northern malt fly species: A candidate gene microarray study. BMC Ecology and Evolution, vol. 10, article 3. https://doi.org/10.1186/1472-6785-10-3 (In English)

Kayukawa, T., Chen, B., Miyazaki, S. et al. (2005) Expression of mRNA for the t-complex polypeptide-1, a subunit of chaperonin CCT, is upregulated in association with increased cold hardiness in Delia antiqua. Cell Stress and Chaperones, vol. 10, no. 3, pp. 204–210. https://doi.org/10.1379%2FCSC-106R.1 (In English)

Khazaeli, A. A., Tatar, M., Pletcher, S. D., Curtsinger, J. W. (1997) Heat-induced longevity extension in Drosophila. I. Heat treatment, mortality, and thermotolerance. The Journals of Gerontology: Series A: Biological Sciences and Medical Sciences, vol. 52, no. 1, pp. B48–52. https://doi.org/10.1093/gerona/52a.1.b48 (In English)

King, A. M., MacRae, T. H. (2015) Insect heat shock proteins during stress and diapause. Annual Review of Entomology, vol. 7, no. 60, pp. 59–75. https://doi.org/10.1146/annurev-ento-011613-162107 (In English)

King, V., Tower, J. (1999) Aging-specific expression of Drosophila Hsp22. Developmental Biology, vol. 207, no. 1, pp. 107–118. https://doi.org/10.1006/dbio.1998.9147 (In English)

Kumar, A., Tiwari, A. K. (2018) Molecular chaperone Hsp70 and its constitutively active form Hsc70 play an indispensable role during eye development of Drosophila melanogaster. Molecular Neurobiology, vol. 55, no. 5, pp. 4345–4361. https://doi.org/10.1007/s12035-017-0650-z (In English)

Kurzik-Dumke, U., Lohman, E. (1995) Sequence of the new Drosophila melanogaster small heat-shock-related gene, lethal(2) essential for life [l(2)efl], at locus 59F4,5. Gene, vol. 154, no. 2, pp. 171–175. https://doi.org/10.1016/0378-1119(94)00827-F (In English)

Le Bourg, E., Valenti, P., Lucchetta, P., Payre, F. (2001) Effects of mild heat shocks at young age on aging and longevity in Drosophila melanogaster. Biogerontology, vol. 2, no. 3, pp. 155–164. https://doi.org/10.1023/a:1011561107055 (In English)

Lee, Y.-K., Manalo, D., Liu, A. Y.-C. (1996) Heat shock response. Biological Signals, vol. 5, no. 3, pp. 180–191. https://doi.org/10.1159/000109187 (In English)

Leemans, R, Egger, B, Loop, T. et al. (2000) Quantitative transcript imaging in normal and heat-shocked Drosophila embryos by using high-density oligonucleotide arrays. Proceedings of the National Academy of Sciences, vol. 97, no. 22, pp. 12138–12143. https://doi.org/10.1073/pnas.210066997 (In English)

Macario, A. J. L., Macario, E. C. (2002) Sick chaperones and ageing: A perspective. Ageing Research Reviews, vol. 1, no. 2, pp. 295–311. https://doi.org/10.1016/s1568-1637(01)00005-8 (In English)

Marin, R., Valet, J. P., Tanguay, R. M. (1993) Hsp23 and Hsp26 exhibit distinct spatial and temporal patterns of constitutive expression in Drosophila adults. Development Genetics, vol. 14, no. 1, pp. 69–77. https://doi.org/10.1002/dvg.1020140109 (In English)

Mason, P. J., Hall, L. M. C., Gausz, J. (1984) The expression of heat shock genes during normal development in Drosophila melanogaster (heat shock/abundant transcripts/developmental regulation). Molecular and General Genetics, vol. 194, no. 1–2, pp. 73–78. https://doi.org/10.1007/BF00383500 (In English)

Michaud, S., Marin, R., Westwood, J. T., Tanguay, R. M. (1997) Cell-specific expression and heat-shock induction of Hsps during spermatogenesis in Drosophila melanogaster. Journal of Cell Science, vol. 110, no. 17, pp. 1989–1997. https://doi.org/10.1242/jcs.110.17.1989 (In English)

Michaud, S., Tanguay, R. M. (2003) Expression of the Hsp23 chaperone during Drosophila embryogenesis: Association to distinct neural and glial lineages. BMC Developmental Biology, vol. 3, article 9. https://doi.org/10.1186/1471-213x-3-9 (In English)

Minois, N. (2000) Longevity and aging: Beneficial effects of exposure to mild stress. Biogerontology, vol. 1, no. 1, pp. 15–29. https://doi.org/10.1023/a:1010085823990 (In English)

Moribe, Y., Oka, K., Niimi, T. et al. (2010) Expression of heat shock protein 70a mRNA in Bombyx mori diapause eggs. Journal of Insect Physiology, vol. 56, no. 9, pp. 1246–1252. https://doi.org/10.1016/j.jinsphys.2010.03.023 (In English)

Morrow, G., Tanguay, R. M. (2003) Heat shock proteins and aging in Drosophila melanogaster. Seminars in Cell and Developmental Biology, vol. 14, no. 5, pp. 291–299. https://doi.org/10.1016/j.semcdb.2003.09.023 (In English)

Niedzwiecki, A., Kongpachith, A. M., Fleming, J. E. (1991) Aging affects expression of 70-kDa heat shock proteins in Drosophila. The Journal of Biological Chemistry, vol. 266, no. 14, pp. 9332–9338. https://doi.org/10.1016/S0021-9258(18)31590-4 (In English)

Pauli, D., Arrigo, A. P., Vazquez, J. et al. (1989) Expression of the small heat shock genes during Drosophila development: Comparison of the accumulation of hsp23 and hsp27 mRNAs and polypeptides. Genome, vol. 31, no. 2, pp. 671–676. https://doi.org/10.1139/g89-123 (In English)

Pauli, D., Tonka, C. H. (1987) A Drosophila heat shock gene from locus 67B is expressed during embryogenesis and pupation. Journal of Molecular Biology, vol. 198, no. 2, pp. 235–240. https://doi.org/10.1016/0022-2836(87)90309-3 (In English)

Pauli, D., Tonka, C.-H., Ayme-Southgate, A. (1988) An unusual split Drosophila heat shock gene expressed during embryogenesis. Journal of Molecular Biology, vol. 200, no. 1, pp. 47–53. https://doi.org/10.1016/0022-2836(88)90332-4 (In English)

Quan, G., Duan, J., Fick, W. et al. (2018) Expression profiles of 14 small heat shock protein (sHSP) transcripts during larval diapause and under thermal stress in the spruce budworm, Choristoneura fumiferana (L.). Cell Stress Chaperones, vol. 23, no. 6, pp. 1247–1256. https://doi.org/10.1007%2Fs12192-018-0931-0 (In English)

Raut, S., Mallik, B., Parichha, A. et al. (2017) RNAi-mediated reverse genetic screen identified Drosophila chaperones regulating eye and neuromuscular junction morphology. G3. Genes. Genomes. Genetics, vol. 7, no. 7, pp. 2023–2038. https://doi.org/10.1534/g3.117.041632 (In English)

Reynolds, J. A., Hand, S. C. (2009) Embryonic diapause highlighted by differential expression of mRNAs for ecdysteroidogenesis, transcription and lipid sparing in the cricket Allonemobius socius. The Journal of Experimental Biology, vol. 212, no. 13, pp. 2075–2084. https://doi.org/10.1242%2Fjeb.027367 (In English)

Rinehart, J. P., Li, A., Yocum, G. D. et al. (2007) Up-regulation of heat shock proteins is essential for cold survival during insect diapause. Proceedings of the National Academy of Sciences, vol. 104, no. 27, pp. 11130–11137. https://doi.org/10.1073/pnas.0703538104 (In English)

Santana, E., de los Reyes, T., Casas-Tintó, S. (2020) Small heat shock proteins determine synapse number and neuronal activity during development. PLOS One, vol. 15, no. 5, article e0233231. https://doi.org/10.1371/journal.pone.0233231 (In English)

Sasibhushan, S., Ponnuvel, K. M., Vijayaprakash, N. B. (2012) Diapause specific gene expression in the eggs of multivoltine silkworm Bombyx mori, identified by suppressive subtractive hybridization. Comparative Biochemistry & Physiology, vol. 161, no. 4, pp. 371–379. https://doi.org/10.1016/j.cbpb.2012.01.002 (In English)

Sasibhushan, S., Rao, C. G. P., Ponnuvel, K. M. (2013) Genome wide microarray based expression profiles during early embryogenesis in diapause induced and non-diapause eggs of polyvoltine silkworm Bombyx mori. Genomics, vol. 102, no. 4, pp. 379–387. https://doi.org/10.1016/j.ygeno.2013.07.007 (In English)

Simon, A. F., Shih, C., Mack, A., Benzer, S. (2003) Steroid control of longevity in Drosophila melanogaster. Science, vol. 299, no. 5611, pp. 1407–1410. https://doi.org/10.1126/science.1080539 (In English)

Sonoda, S., Fukumoto, K., Izumi, Y. et al. (2006) Cloning of heat shock protein genes (hsp90 and hsc70) and their expression during larval diapause and cold tolerance acquisition in the rice stem borer, Chilo suppressalis Walker. Archives of Insect Biochemistry and Physiology, vol. 63, no. 1, pp. 36–47. https://doi.org/10.1002/arch.20138 (In English)

Sorensen, J. G., Loeshcke, V. (2001) Larval crowding in Drosophila melanogaster induces Hsp70 expression, and leads to increased adult longevity and adult thermal stress resistance. Journal of Insect Physiology, vol. 47, no. 11, pp. 1301–1307. https://doi.org/10.1016/s0022-1910(01)00119-6 (In English)

Tachibana, S. I., Numata, H., Goto, S. G. (2005) Gene expression of heat-shock proteins (Hsp23, Hsp70 and Hsp90) during and after larval diapause in the blow fly Lucilia sericata. Journal of Insect Physiology, vol. 51, no. 6, pp. 641–647. https://doi.org/10.1016/j.jinsphys.2004.11.012 (In English)

Tatar, M., Bartke, A., Antebi, A. (2003) The endocrine regulation of aging by insulin-like signals. Science, vol. 299, no. 5611, pp. 1346–1351. https://doi.org/10.1126/science.1081447 (In English)

Tatar, M., Khazaeli, A. A., Curtsinger, J. W. (1997) Chaperoning extended life. Nature, vol. 390, no. 6655, article 30. https://doi.org/10.1038/36237 (In English)

Teixeira, L. A. F., Polavarapu, S. (2005) Expression of heat shock protein 70 after heat stress during pupal diapause in Rhagoletis mendax (Diptera: Tephritidae). Annals of the Entomological Society of America, vol. 98, no. 6, pp. 966–972. https://doi.org/10.1603/0013-8746(2005)098[0966:EOHSPA]2.0.CO;2 (In English)

Thomas, S. R., Lengyel, J. A. (1986) Ecdysteroid-regulated heat-shock gene expression during Drosophila melanogaster development. Developmental Biology, vol. 115, no. 2, pp. 434–438. https://doi.org/10.1016/0012-1606(86)90263-0 (In English)

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, vol. 84, no 3, pp. 389–398. https://doi.org/10.1016/0022-2836(74)90447-1 (In English)

Tower, J. (2011) Heat shock proteins and Drosophila aging. Experimental Gerontology, vol. 46, no. 5, pp. 355–362. https://doi.org/10.1016/j.exger.2010.09.002 (In English)

Tungjitwitayakul, J., Tatun, N., Singtripop, T., Sakurai, S. (2008) Characteristic expression of three heat shock-responsive genes during larval diapause in the bamboo borer Omphisa fuscidentalis. Zoological Science, vol. 25, no. 3, pp. 321–333. https://doi.org/10.2108/zsj.25.321 (In English)

Verbeke, P., Fonager, J., Clark, B. F. C., Rattan, S. I. S. (2001) Heat-shock response and ageing: Mechanisms and applications. Cell Biology International, vol. 25, no. 9, pp. 845–857. https://doi.org/10.1006/cbir.2001.0789 (In English)

Wheeler, J. C., King, V., Tower, J. (1999) Sequence requirements for upregulated expression of Drosophila hsp70 transgenes during aging. Neurobiology of Aging, vol. 20, no. 5, pp. 545–553. https://doi.org/10.1016/s0197-4580(99)00088-3 (In English)

Wójtowicz, I., Jabłońska, J., Zmojdzian, M. et al. (2015) Drosophila small heat shock protein CryAB ensures structural integrity of developing muscles, and proper muscle and heart performance. Development, vol. 142, no. 5, pp. 994–1005. https://doi.org/10.1242/dev.115352 (In English)

Wu, Y. K., Zou, C., Fu, D. M. et al. (2018) Molecular characterization of three Hsp90 from Pieris and expression patterns in response to cold and thermal stress in summer and winter diapause of Pieris melete. Journal of Insect Science, vol. 25, no. 2, pp. 273–283. https://doi.org/10.1111/1744-7917.12414 (In English)

Xiao, Ch., Hull, D., Qiu, Sh. et al. (2019) Expression of heat shock protein 70 is insufficient to extend Drosophila melanogaster longevity. G3. Genes. Genomes. Genetics, vol. 9, no. 12, pp. 4197–4207. https://doi.org/10.1534/g3.119.400782 (In English)

Yan, L. J., Sohal, R. S. (1998) Mitochondrial adenine nucleotide translocase is modified oxidatively during aging. Proceedings of the National Academy of Sciences, vol. 95, no. 22, pp. 12896–12901. https://doi.org/10.1073/pnas.95.22.12896 (In English)

Yocum, G. D. (2001) Differential expression of two HSP70 transcripts in response to cold shock, thermoperiod, and adult diapause in the Colorado potato beetle. Journal of Insect Physiology, vol. 47, no. 10, pp. 1139–1145. https://doi.org/10.1016/S0022-1910(01)00095-6 (In English)

Zatsepina, O. G., Nikitina, E. A., Shilova, V. Y. et al. (2021) Hsp70 affects memory formation and behaviorally relevant gene expression in Drosophila melanogaster. Cell Stress and Chaperones, vol. 26, no. 3, pp. 575–594. https://doi.org/10.1007/s12192-021-01203-7 (In English)

Zimmerman, J. L., Petri, W., Meselson, M. (1983) Accumulation of a specific subset of D. melanogaster heat shock mRNAs in normal development without heat shock. Cell, vol. 32, no. 4, pp. 1161–1170. https://doi.org/10.1016/0092-8674(83)90299-4 (In English)

Zoo, S., Meadows, S., Sharp, L. et al. (2000) Genome-wide study of aging and oxidative stress response in Drosophila melanogaster. Proceedings of the National Academy of Sciences, vol. 97, no. 25, pp. 13726–13731. https://doi.org/10.1073/pnas.260496697 (In English)

Загрузки

Опубликован

30.08.2022

Выпуск

Раздел

Обзоры