Exogenous Hsp70 delays senescence and improves cognitive function in aging mice
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Significance: The compromised ability of neurons to express Heat Shock Protein 70 (Hsp70) correlates with aging-related neurodegeneration. In this study, middle-aged and old mice were treated chronically until death with human Hsp70 delivered intranasally and were investigated after 5 or 9 mo of Hsp70 treatment for their cognitive ability and synaptic density. Hsp70 treatment extended mean and maximum lifespan, improved learning and memory in old animals, increased curiosity, decreased anxiety, and helped maintain synaptic structures that degrade with age. These results provide evidence that intranasal administration of Hsp70 could have significant therapeutic potential in preserving brain tissue and memory for middle-age and old individuals and could be applied either as unique self-contained treatment or in combination with other pharmacological therapies.
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There are 4 core genes significantly downregulated in astrocytes in all brain regions, 2 of which are heat shock proteins.
“There are 4 core genes significantly downregulated in astrocytes in all brain regions, 2 of which are heat shock proteins (Figure 2G), protective molecular chaperones that prevent protein damage (Bobkova et al., 2015).”
From The aging astrocyte transcriptome from multiple regions of the mouse brain. (2018) · cites this paper as Bobkova et al., 2015
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Guide for the Care and Use of Laboratory Animals: Eighth Edition
(2011) · doi:10.17226/12910 · Cited by 16,199 · see citing works
Developments of a water-maze procedure for studying spatial learning in the rat
Morris, R. (1984) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(84)90007-4 · Cited by 7,180 · see citing works
Guide for the care and use of laboratory animals
(1997) · Choice Reviews Online · doi:10.5860/choice.34-3310 · Cited by 2,930 · see citing works
Hsp70 chaperones: Cellular functions and molecular mechanism
Mayer, M. P., & Bukau, B. (2005) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-004-4464-6 · Cited by 2,857 · see citing works
Prevalence of Dementia in the United States: The Aging, Demographics, and Memory Study
Plassman, B. L., Langa, K. M., Fisher, G. G., Heeringa, S. G., Weir, D. R., Ofstedal, M. B., Burke, J. R., Hurd, M. D., Potter, G. G., Rodgers, W. L., et al. (2007) · Neuroepidemiology · doi:10.1159/000109998 · Cited by 1,932 · see citing works
Molecular Chaperone Functions in Protein Folding and Proteostasis
Kim, Y., Hipp, M. S., Bracher, A., Hayer-Hartl, M. K., & Hartl, F. U. (2013) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-060208-092442 · Cited by 1,468 · see citing works
XBP-1 Is a Cell-Nonautonomous Regulator of Stress Resistance and Longevity
Taylor, R. C., & Dillin, A. G. (2013) · Cell · doi:10.1016/j.cell.2013.05.042 · Cited by 570 · see citing works
Synapse Formation and Function Is Modulated by the Amyloid Precursor Protein
Priller, C., Bauer, T., Mitteregger, G., Krebs, B., Kretzschmar, H. A., & Herms, J. W. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.1450-06.2006 · Cited by 548 · see citing works
Hsp70 stabilizes lysosomes and reverts Niemann–Pick disease-associated lysosomal pathology
Kirkegaard, T., Roth, A. G., Petersen, N. H. T., Mahalka, A. K., Olsen, O. D., Moilanen, I., Zylicz, A., Knudsen, J., Sandhoff, K., Arenz, C., et al. (2010) · Nature · doi:10.1038/nature08710 · Cited by 519 · see citing works
Lee, S., Hwang, A. B., & Kenyon, C. J. (2010) · Current Biology · doi:10.1016/j.cub.2010.10.057 · Cited by 495 · see citing works
Ferrington, D. A., & Gregerson, D. S. (2012) · Progress in molecular biology and translational science · doi:10.1016/b978-0-12-397863-9.00003-1 · Cited by 416 · see citing works
The Heat Shock Response: Systems Biology of Proteotoxic Stress in Aging and DiseasePreprint
Morimoto, R. (2011) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2012.76.010637 · Cited by 407 · see citing works
MHC Class I: An Unexpected Role in Neuronal Plasticity
Shatz, C. J. (2009) · Neuron · doi:10.1016/j.neuron.2009.09.044 · Cited by 369 · see citing works
Synaptophysin: leading actor or walk‐on role in synaptic vesicle exocytosis?
Valtorta, F., Pennuto, M., Bonanomi, D., & Benfenati, F. (2004) · BioEssays · doi:10.1002/bies.20012 · Cited by 346 · see citing works
Calderwood, S. K., Murshid, A., & Prince, T. L. (2009) · Gerontology · doi:10.1159/000225957 · Cited by 343 · see citing works
Lipofuscin and Aging: A Matter of Toxic Waste
Gray, D. A., & Woulfe, J. (2005) · Science of Aging Knowledge Environment · doi:10.1126/sageke.2005.5.re1 · Cited by 279 · see citing works
Proteostasis and the Aging Proteome in Health and Disease
Morimoto, R. I., & Cuervo, A. M. (2014) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/glu049 · Cited by 277 · see citing works
Guillaume, B., Chapiro, J., Stroobant, V., Colau, D., Holle, B. V., Parvizi, G. K., Bousquet, M., Théate, I., Parmentier, N., & den Eynde, B. J. V. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1009778107 · Cited by 218 · see citing works
Regulation of Organismal Proteostasis by Transcellular Chaperone Signaling
van Oosten‐Hawle, P., Porter, R. S., & Morimoto, R. I. (2013) · Cell · doi:10.1016/j.cell.2013.05.015 · Cited by 197 · see citing works
Degradation of Damaged Proteins
Pickering, A. M., & Davies, K. J. A. (2012) · Progress in molecular biology and translational science · doi:10.1016/b978-0-12-397863-9.00006-7 · Cited by 173 · see citing works
Heat shock proteins in neurodegenerative disorders and aging
Leak, R. K. (2014) · Journal of Cell Communication and Signaling · doi:10.1007/s12079-014-0243-9 · Cited by 170 · see citing works
Regulation of survival gene hsp70
Silver, J. T., & Noble, E. G. (2011) · Cell Stress and Chaperones · doi:10.1007/s12192-011-0290-6 · Cited by 149 · see citing works
Neuronal circuitry regulates the response of Caenorhabditis elegans to misfolded proteins
Prahlad, V., & Morimoto, R. I. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1106557108 · Cited by 143 · see citing works
Landis, G. N., Shen, J., & Tower, J. (2012) · Aging · doi:10.18632/aging.100499 · Cited by 142 · see citing works
Therapeutic effect of exogenous hsp70 in mouse models of Alzheimer’s disease
Bobkova, N. V., Garbuz, D. G., Nesterova, I., Medvinskaya, N., Samokhin, A., Alexandrova, I., Yashin, V., Karpov, V., Kukharsky, M. S., Ninkina, N. N., et al. (2013) · Journal of Alzheimer's Disease · doi:10.3233/jad-130779 · Cited by 138 · see citing works
Self-citationIntegrating the stress response: lessons for neurodegenerative diseases from C. elegans
Prahlad, V., & Morimoto, R. I. (2008) · Trends in Cell Biology · doi:10.1016/j.tcb.2008.11.002 · Cited by 134 · see citing works
Antioxidant protection: A promising therapeutic intervention in neurodegenerative disease
Ghosh, N., Ghosh, R. B., & Mandal, S. C. (2011) · Free Radical Research · doi:10.3109/10715762.2011.574290 · Cited by 116 · see citing works
Fonager, J., Beedholm, R., Clark, B. F. C., & Rattan, S. I. S. (2002) · Experimental Gerontology · doi:10.1016/s0531-5565(02)00128-6 · Cited by 114 · see citing works
Proteasomal activity in brain differs between species and brain regions and changes with age.
Zeng, B.-Y., Medhurst, A. D., Jackson, M., Rose, S., & Jenner, P. (2005) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2005.01.008 · Cited by 113 · see citing works
Stress proteins in aging and life span
Murshid, A., Eguchi, T., & Calderwood, S. K. (2013) · International Journal of Hyperthermia · doi:10.3109/02656736.2013.798873 · Cited by 111 · see citing works
Nonlinear changes in cognition with age and their neuropsychologic correlates.
Albert, M., Fh, D., & Naeser, M. A. (1987) · PubMed · Cited by 102 · see citing works
Cooperation of heat shock protein 90 and p23 in aryl hydrocarbon receptor signaling
Cox, M., & Miller, C. A. (2004) · Cell stress & chaperones (Print) · doi:10.1379/1466-1268(2004)009 · Cited by 90 · see citing works
Lifespan of mice and primates correlates with immunoproteasome expression
Pickering, A. M., Lehr, M., & Miller, R. A. (2015) · Journal of Clinical Investigation · doi:10.1172/jci80514 · Cited by 81 · see citing works
Accumulation of modified proteins and aggregate formation in aging
Nowotny, K., Jung, T., Grune, T., & Höhn, A. (2014) · Experimental Gerontology · doi:10.1016/j.exger.2014.05.016 · Cited by 79 · see citing works
Administration of Hsp70 in vivo inhibits motor and sensory neuron degeneration
Tidwell, J. L., Houenou, L. J., & Tytell, M. (2004) · Cell Stress and Chaperones · doi:10.1379/csc-9r.1 · Cited by 79 · see citing works
Hydra, the everlasting embryo, confronts aging
Martínez, D. E., & Bridge, D. M. (2012) · The International Journal of Developmental Biology · doi:10.1387/ijdb.113461dm · Cited by 71 · see citing works
Zanker, D. J., Waithman, J. C., Yewdell, J. W., & Chen, W. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1300802 · Cited by 71 · see citing works
Higher levels of heat shock proteins in longer-lived mammals and birds
Salway, K. D., Gallagher, E. J., Page, M. M., & Stuart, J. A. (2011) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2011.06.002 · Cited by 70 · see citing works
Hsp70 Chaperone as a Survival Factor in Cell Pathology
Guzhova, I. V., & Margulis, B. A. (2006) · International review of cytology · doi:10.1016/s0074-7696(06)54003-3 · Cited by 67 · see citing works
Ekimova, I. V., Nitsinskaya, L. E., Romanova, I. V., Pastukhov, Y. F., Margulis, B. A., & Guzhova, I. V. (2010) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2010.06989.x · Cited by 67 · see citing works
Rozhkova, E., Yurinskaya, M. M., Zatsepina, O. G., Garbuz, D. G., Карпов, В. Л., Surkov, S. A., Murashev, A. N., Ostrov, V. F., Margulis, B. A., Евгеньев, М. Б., et al. (2010) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.05375.x · Cited by 66 · see citing works
Self-citationThe induction of heat shock proteins as a potential strategy to treat neurodegenerative disorders
Klettner, A. (2004) · Drug News & Perspectives · doi:10.1358/dnp.2004.17.5.829033 · Cited by 58 · see citing works
Protective Effect of Heat Shock Proteins in the Nervous System
Latchman, D. S. (2004) · Current Neurovascular Research · doi:10.2174/1567202043480206 · Cited by 56 · see citing works
Genetics of human longevity with emphasis on the relevance of HSP70 as candidate genes
Singh, R. (2007) · Frontiers in bioscience · doi:10.2741/2405 · Cited by 54 · see citing works
Винокуров, М. Г., Ostrov, V. F., Yurinskaya, M. M., Garbuz, D. G., Murashev, A. N., Antonova, O. Y., & Евгеньев, М. Б. (2011) · Cell Stress and Chaperones · doi:10.1007/s12192-011-0288-0 · Cited by 53 · see citing works
Self-citationKustanova, G. A., Murashev, A. N., Карпов, В. Л., Margulis, B. A., Guzhova, I. V., Прохоренко, И. Р., Grachev, S. V., & Evgen’ev, M. B. (2006) · Cell Stress and Chaperones · doi:10.1379/csc-195r.1 · Cited by 52 · see citing works
Self-citationSarup, P. M., Sørensen, P. B., & Loeschcke, V. (2013) · Experimental Gerontology · doi:10.1016/j.exger.2013.11.017 · Cited by 51 · see citing works
Haley, G. E., Kohama, S. G., Urbanski, H. F., & Raber, J. (2010) · AGE · doi:10.1007/s11357-010-9137-9 · Cited by 51 · see citing works
The evaluation of autofluorescence emission spectra derived from neuronal lipopigment
Dowson, J. H. (1982) · Journal of Microscopy · doi:10.1111/j.1365-2818.1982.tb04628.x · Cited by 48 · see citing works
Heat‐Shock Protein 70 Genes and Human Longevity
Singh, R., Kølvraa, S., Bross, P., Christensen, K., Gregersen, N., Tan, Q., Jensen, U. B., Eiberg, H., & Rattan, S. I. S. (2006) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1354.040 · Cited by 46 · see citing works
Developmental Sculpting of Intracortical Circuits by MHC Class I H2-Db and H2-Kb
Steinmetz, J. D., Sapp, R. W., Brott, B. K., Lee, H., Miyamichi, K., Luo, L., Cheng, S., Djurisic, M. R., & Shatz, C. J. (2014) · Cerebral Cortex · doi:10.1093/cercor/bhu243 · Cited by 39 · see citing works
Zheng, H., Nagaraja, G. M., Kaur, P., Asea, E. E., & Asea, A. A. A. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.024612 · Cited by 37 · see citing works
Relationship between heat shock protein 70 expression and life span in Daphnia
Schumpert, C. A., Handy, I., Dudycha, J. L., & Patel, R. C. (2014) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2014.04.001 · Cited by 34 · see citing works
The Fate of Exogenous Human HSP70 Introduced into Animal Cells by Different Means
Yurinskaya, M. M., Zatsepina, O. G., Винокуров, М. Г., Бобкова, Н. В., Garbuz, D. G., Morozov, A., Kulikova, D. A., Mitkevich, V. A., Makarov, A. А., Funikov, S. Y., et al. (2015) · Current Drug Delivery · doi:10.2174/1567201812666150724094207 · Cited by 32 · see citing works
Self-citationHsp72, inflammation, and aging: causes, consequences, and perspectives
Ortega, E., Bote, E., Besedovsky, H. O., & del Rey, A. (2012) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2012.06619.x · Cited by 26 · see citing works
A neuronal aging pattern unique to humans and common chimpanzees
Gilissen, E., Leroy, K., Yilmaz, Z., Kövari, E., Bouras, C., Boom, A., Poncelet, L., ERWIN, J. M., Sherwood, C. C., Hof, P. R., et al. (2014) · Brain Structure and Function · doi:10.1007/s00429-014-0931-5 · Cited by 25 · see citing works
Ng’oma, E., Reichwald, K., Dorn, A., Wittig, M., Balschun, T. C., Franke, A., Platzer, M., & Cellerino, A. (2014) · Aging · doi:10.18632/aging.100660 · Cited by 19 · see citing works
Proteasomes in the brain of β2-microglobulin knockout mice
Lyupina, Y. V., Bogatyrev, M. E., Orlova, A. S., Marjukhnich, E. V., Kazansky, D. B., & Sharova, N. P. (2013) · Biochemistry (Moscow) · doi:10.1134/s0006297913100064 · Cited by 11 · see citing works
Li, J., Niu, W., Qi, Y., Wufuer, M., Zhu, P., Muhuyati, Cheng, Z., & Qiu, C. (2009) · Translational research · doi:10.1016/j.trsl.2009.08.002 · Cited by 9 · see citing works
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López-Otín, C., Blasco, M. A., Partridge, L., Serrano, M., & Kroemer, G. (2023) · Cell · doi:10.1016/j.cell.2022.11.001 · Cited by 6,549 · see citing works
The aging astrocyte transcriptome from multiple regions of the mouse brain.
Boisvert, M. M., Erikson, G. A., Shokhirev, M. N., & Allen, N. J. (2018) · Cell Reports · doi:10.1016/j.celrep.2017.12.039 · Cited by 702 · see citing works
Miao, J., Liu, J., Niu, J., Zhang, Y., Shen, W., Luo, C., Liu, Y., Li, C., Li, H., Yang, P., et al. (2019) · Aging Cell · doi:10.1111/acel.13004 · Cited by 279 · see citing works
Wnt9a Promotes Renal Fibrosis by Accelerating Cellular Senescence in Tubular Epithelial Cells
Luo, C., Zhou, S., Zhou, Z., Liu, Y., Yang, L., Liu, J., Zhang, Y., Li, H., Liu, Y., Hou, F. F., et al. (2018) · Journal of the American Society of Nephrology · doi:10.1681/asn.2017050574 · Cited by 277 · see citing works
Singh, M. K., Shin, Y., Ju, S., Han, S., Choe, W., Yoon, K., Kim, S. S., & Kang, I. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25084209 · Cited by 231 · see citing works
Amyloid assembly and disassembly
Chuang, E., Hori, A. M., Hesketh, C. D., & Shorter, J. (2018) · Journal of Cell Science · doi:10.1242/jcs.189928 · Cited by 182 · see citing works
Proteostasis collapse is a driver of cell aging and death
Santra, M., Dill, K. A., & de Graff, A. M. R. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1906592116 · Cited by 175 · see citing works
Heat-Shock Proteins in Neuroinflammation
Dukay, B., Csoboz, B., & Tóth, M. E. (2019) · Frontiers in Pharmacology · doi:10.3389/fphar.2019.00920 · Cited by 132 · see citing works
Proteasomes and Several Aspects of Their Heterogeneity Relevant to Cancer
Morozov, A. V., & Карпов, В. Л. (2019) · Frontiers in Oncology · doi:10.3389/fonc.2019.00761 · Cited by 111 · see citing works
Self-citationAutophagy: Multiple Mechanisms to Protect Skin from Ultraviolet Radiation-Driven Photoaging
Wang, M., Pourzand, C., Lei, X., & Zhong, J. L. (2019) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2019/8135985 · Cited by 102 · see citing works
Cell non-autonomous regulation of health and longevity
Miller, H. A., Kitto, E. S., Pletcher, S. D., & Leiser, S. F. (2020) · eLife · doi:10.7554/elife.62659 · Cited by 97 · see citing works
Sex‐specific aging in animals: Perspective and future directions
Bronikowski, A., Meisel, R., Biga, P. R., Walters, J., Mank, J., Larschan, E. N., Wilkinson, G., Valenzuela, N., Conard, A., de Magalhães, J. D., et al. (2022) · Aging Cell · doi:10.1111/acel.13542 · Cited by 78 · see citing works
Zatsepina, O. G., Evgen’ev, M. B., & Garbuz, D. G. (2021) · Cells · doi:10.3390/cells10071638 · Cited by 79 · see citing works
Self-citationVitamin D3 regulates apoptosis and proliferation in the testis of D-galactose-induced aged rat model
Jeremy, M., Gurusubramanian, G., & Roy, V. K. (2019) · Scientific Reports · doi:10.1038/s41598-019-50679-y · Cited by 74 · see citing works
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Ya, J., & Bayraktutan, U. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241411538 · Cited by 57 · see citing works
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McLaughlin, T., Falkowski, M., Park, J. W., Keegan, S., Elliott, M. H., Wang, J. J., & Zhang, S. X. (2018) · Molecular Neurodegeneration · doi:10.1186/s13024-018-0250-z · Cited by 56 · see citing works
Engineering therapeutic protein disaggregases
Shorter, J. (2016) · Molecular Biology of the Cell · doi:10.1091/mbc.e15-10-0693 · Cited by 52 · see citing works
Evgen’ev, M. B., Krasnov, G. S., Nesterova, I. V., Garbuz, D. G., Карпов, В. Л., Morozov, A. V., Snezhkina, A. V., Samokhin, A. N., Sergeev, A., Куликов, А. М., et al. (2017) · Journal of Alzheimer s Disease · doi:10.3233/jad-170398 · Cited by 45 · see citing works
Self-citationExtracellular heat shock proteins in neurodegenerative diseases: New perspectives
Lyon, M. S., & Milligan, C. (2019) · Neuroscience Letters · doi:10.1016/j.neulet.2019.134462 · Cited by 45 · see citing works
Age-associated changes in microglia and astrocytes ameliorate blood-brain barrier dysfunction
Pan, J., Ma, N., Zhong, J., Yu, B., Wan, J., & Zhang, W. (2021) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2021.08.030 · Cited by 42 · see citing works
Leite, J. S. M., Cruzat, V. F., Krause, M. D. S., & de Bittencourt, P. I. H. (2016) · Nutrire · doi:10.1186/s41110-016-0021-y · Cited by 40 · see citing works
Morozov, A. V., Astakhova, T. M., Garbuz, D. G., Krasnov, G. S., Bobkova, N. V., Zatsepina, O. G., Карпов, В. Л., & Evgen’ev, M. B. (2017) · Cell Stress and Chaperones · doi:10.1007/s12192-017-0792-y · Cited by 39 · see citing works
Self-citationSirtuin-1 attenuates cadmium-induced renal cell senescence through p53 deacetylation
Chou, X., Li, X., Min, Z., Ding, F., Ma, K., Shen, Y. L., Sun, D., & Wu, Q. (2022) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2022.114098 · Cited by 36 · see citing works
Zhang, S., Liu, W., Wang, P., Hu, B., Lv, X., Chen, S., Wang, B., & Shao, Z. (2021) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-021-04052-1 · Cited by 34 · see citing works
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Jagaraj, C. J., Shadfar, S., Kashani, S. A., Saravanabavan, S., Farzana, F., & Atkin, J. D. (2024) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-024-05164-9 · Cited by 33 · see citing works
Proteostasis and ageing: insights from long‐lived mutant mice
Sands, W. A., Page, M. M., & Selman, C. (2017) · The Journal of Physiology · doi:10.1113/jp274334 · Cited by 32 · see citing works
Evgen’ev, M. B., Bobkova, N. V., Krasnov, G. S., Garbuz, D. G., Funikov, S. Y., Kudryavtseva, A. V., Куликов, А. М., Samokhin, A. N., Maltsev, A. V., & Nesterova, I. V. (2019) · Journal of Alzheimer s Disease · doi:10.3233/jad-180987 · Cited by 32 · see citing works
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Self-citationSolarz, A., Majcher‐Maślanka, I., Kryst, J., & Chocyk, A. (2021) · Neuroscience · doi:10.1016/j.neuroscience.2021.02.026 · Cited by 27 · see citing works
Hsp70 affects memory formation and behaviorally relevant gene expression in Drosophila melanogaster
Zatsepina, O. G., Nikitina, E. A., Shilova, V. Y., Chuvakova, L. N., Sorokina, S. Y., Vorontsova, Y. E., Tokmacheva, E. V., Funikov, S. Y., Rezvykh, A. P., & Evgen’ev, M. B. (2021) · Cell Stress and Chaperones · doi:10.1007/s12192-021-01203-7 · Cited by 29 · see citing works
Self-citationRecombinant HSP70 and mild heat shock stimulate growth of aged mesenchymal stem cells
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Self-citationGenetic and epigenetic alterations in aging and rejuvenation of human
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Acuña-Catalán, D., Shah, S., Wehrfritz, C., Nomura, M., Acevedo, A., Olmos, C., Quiroz, G., Huerta, H., Bons, J., Ampuero, E., et al. (2024) · Cell Reports Medicine · doi:10.1016/j.xcrm.2024.101593 · Cited by 27 · see citing works
The development of modified human Hsp70 (HSPA1A) and its production in the milk of transgenic mice
Gurskiy, Y. G., Garbuz, D. G., Soshnikova, N. V., Краснов, А. Н., Deykin, A. V., Lazarev, V. F., Sverchinsky, D. V., Margulis, B. A., Zatsepina, O. G., Карпов, В. Л., et al. (2016) · Cell Stress and Chaperones · doi:10.1007/s12192-016-0729-x · Cited by 24 · see citing works
Self-citationHegde, A. N., Duke, L. M., Timm, L. E., & Nobles, H. (2023) · Sub-cellular biochemistry/Subcellular biochemistry · doi:10.1007/978-3-031-21410-3_5 · Cited by 23 · see citing works
Kawasaki, F., Koonce, N. L., Guo, L., Fatima, S., Qiu, C., Moon, M. T., Zheng, Y., & Ordway, R. W. (2016) · Disease Models & Mechanisms · doi:10.1242/dmm.026385 · Cited by 23 · see citing works
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Kang, Z., Lin, Y., Su, C., Li, S., Xie, W., & Wu, X. (2023) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2023.110791 · Cited by 22 · see citing works
Chaperones vs. oxidative stress in the pathobiology of ischemic stroke
Soldatov, V. O., Venediktov, A. A., Белых, А. Е., Piavchenko, G. A., Naimzada, M. D., Ogneva, N., Kartashkina, N. L., & Bushueva, O. Y. (2024) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2024.1513084 · Cited by 22 · see citing works
Heat shock proteins and cellular senescence in humans: A systematic review
Hebishy, M., Shintouo, C. M., Dufait, I., Debacq‐Chainiaux, F., Bautmans, I., & Njemini, R. (2023) · Archives of Gerontology and Geriatrics · doi:10.1016/j.archger.2023.105057 · Cited by 20 · see citing works
Trajectories of cardiovascular ageing—from molecular mechanisms to clinical implementation
Ministrini, S., Wenzl, F. A., Lüscher, T. F., & Camici, G. G. (2024) · Cardiovascular Research · doi:10.1093/cvr/cvae178 · Cited by 21 · see citing works
Cell-surface HSP70 associates with thrombomodulin in endothelial cells
Araujo, T. L. S., Venturini, G., Moretti, A. I. S., Tanaka, L. Y., Pereira, A. C., & Laurindo, F. R. M. (2019) · Cell Stress and Chaperones · doi:10.1007/s12192-018-00964-y · Cited by 19 · see citing works
The Role of Hsp70 in Adaptation to Adverse Conditions and Its Possible Medical Application
Evgen’ev, M. B., Onikienko, S. B., Chuvakova, L. N., Garbuz, D. G., & Zatsepina, O. G. (2023) · Frontiers in Bioscience-Landmark · doi:10.31083/j.fbl2802025 · Cited by 19 · see citing works
Self-citationLozupone, M., Dibello, V., Sardone, R., Castellana, F., Zupo, R., Lampignano, L., Bortone, I., Stallone, R., Altamura, M., Bellomo, A., et al. (2023) · Expert Opinion on Drug Discovery · doi:10.1080/17460441.2023.2200245 · Cited by 18 · see citing works
Evaluating cytotoxicity of methyl benzoate in vitro
Bunch, H., Park, J., Choe, H., Mostafiz, M. M., Kim, J., & Lee, K. (2020) · Heliyon · doi:10.1016/j.heliyon.2020.e03351 · Cited by 17 · see citing works
Neuroregeneration: Regulation in Neurodegenerative Diseases and Aging
Бобкова, Н. В., Полтавцева, Р. А., Leonov, S. V., & Sukhikh, G. T. (2020) · Biochemistry (Moscow) · doi:10.1134/s0006297920140060 · Cited by 17 · see citing works
Proteostasis defects: Medicinal challenges of imperfect aging & neurodegeneration
Kumar, P., Choudhary, A., Kinger, S., Jagtap, Y. A., Dubey, A. R., Gutti, R. K., Chitkara, D., Suresh, A. K., & Mishra, A. (2023) · Translational Medicine of Aging · doi:10.1016/j.tma.2023.09.001 · Cited by 16 · see citing works
Hsp70 and gama-Semino protein as possible prognostic marker of prostate cancer
Mishra, M. K. (2018) · Frontiers in bioscience · doi:10.2741/4684 · Cited by 16 · see citing works
Wang, M., Chen, X., Zheng, Z., Yu, S.-J., Zhou, B., Liu, Y., Liu, D.-H., Chen, Y.-M., & Qian, X. (2019) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-019-03627-3 · Cited by 15 · see citing works
Ribeiro, C. T., Peixoto, D. O., Santos¹, L. F. D. S., Girardi, C. S., Brum, P. O., Kessler, F. G. C., Somensi, N., Behrens, L. M. P., Bittencourt, R. R., Soares, L. S., et al. (2021) · Brain Behavior & Immunity - Health · doi:10.1016/j.bbih.2021.100253 · Cited by 16 · see citing works
Encapsulated Hsp70 decreases endotoxin-induced production of ROS and TNFα in human phagocytes
Yurinskaya, M. M., Kochetkova, O. Y., Shabarchina, L. I., O.Yu., A., Сусликов, А. В., Евгеньев, М. Б., & Vinokurov, M. G. (2016) · Cell Stress and Chaperones · doi:10.1007/s12192-016-0743-z · Cited by 16 · see citing works
Kwon, H. J., Kim, W., Jung, H. Y., Kang, M. S., Kim, J. W., Hahn, K. R., Yoo, D. Y., Yoon, Y. S., Hwang, I. K., & Kim, D. W. (2019) · Laboratory Animal Research · doi:10.1186/s42826-019-0020-2 · Cited by 15 · see citing works
From Small Peptides to Large Proteins against Alzheimer’sDisease
Picone, P., Sanfilippo, T., Vasto, S., Baldassano, S., Guggino, R., Nuzzo, D., Bulone, D., Biagio, P. L. S., Muscolino, E., Monastero, R., et al. (2022) · Biomolecules · doi:10.3390/biom12101344 · Cited by 15 · see citing works
Liu, Q.-X., Zhang, W., Wang, J., Hou, W., & Wang, Y. (2017) · Journal of Ginseng Research · doi:10.1016/j.jgr.2017.04.006 · Cited by 15 · see citing works
Liu, S., Mou, J., Zhu, X., Liu, J., Du, C., Zhu, Z., Tan, J., Cheng, S., Qiu, X., Huang, W. Y., et al. (2025) · ACS Nano · doi:10.1021/acsnano.5c12590 · Cited by 14 · see citing works
Yang, J. H., Zhang, H., Sun, S., Wang, X., Guan, Y., Mi, Q.-L., Zeng, W., Xiang, H., Zhu, H., Zou, X. G., et al. (2020) · Cell Stress and Chaperones · doi:10.1007/s12192-020-01068-2 · Cited by 14 · see citing works
Alfalfa-derived HSP70 administered intranasally improves insulin sensitivity in mice
Tytell, M., Davis, A., Giles, J. M., Snider, L. C., Xiao, R., Dozier, S., Presley, T. D., & Kavanagh, K. (2017) · Cell Stress and Chaperones · doi:10.1007/s12192-017-0835-4 · Cited by 14 · see citing works
Aging, cancer, and autophagy: connections and therapeutic perspectives
Zapatería, B., & Arias, E. (2025) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2024.1516789 · Cited by 12 · see citing works
Beresewicz, M. (2022) · Neurochemistry International · doi:10.1016/j.neuint.2022.105455 · Cited by 12 · see citing works
Proteomic profiling of senescent human diploid fibroblasts treated with gamma-tocotrienol
Tan, J. K., Jaafar, F., & Makpol, S. (2018) · BMC Complementary and Alternative Medicine · doi:10.1186/s12906-018-2383-6 · Cited by 12 · see citing works
Preexposure to heat stress attenuates sepsis-associated inflammation and cognitive decline in rats
Jiang, S., Bai, L., Zhang, X., Zhou, X., & Liu, Y. (2022) · Neuroscience Letters · doi:10.1016/j.neulet.2022.136647 · Cited by 11 · see citing works
Whole-body pulsed EMF stimulation improves cognitive and psychomotor activity in senescent rats
Téglás, T., Dörnyei, G., Bretz, K., & Nyakas, C. J. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.04.036 · Cited by 11 · see citing works
Jeremy, M., Gurusubramanian, G., & Roy, V. K. (2019) · Molecular Reproduction and Development · doi:10.1002/mrd.23280 · Cited by 11 · see citing works
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Bhatia, T. N., Clark, R. N., Needham, P. G., Miner, K. M., Jamenis, A. S., Eckhoff, E. A., Abraham, N., Hu, X., Wipf, P., Luk, K. C., et al. (2021) · Neurotherapeutics · doi:10.1007/s13311-021-01114-6 · Cited by 10 · see citing works
Duan, Y., Xiang, Y., Chu, J., Lin, X., He, M., Zhang, C., Sun, S., & Ling, H. (2022) · The Tohoku Journal of Experimental Medicine · doi:10.1620/tjem.2022.j108 · Cited by 9 · see citing works
Xie, Y., Huang, J., & Chen, Y. (2022) · Brain and Behavior · doi:10.1002/brb3.2861 · Cited by 9 · see citing works
Vinokurov, A. Y., Palalov, A. A., Kritskaya, K. A., Demyanenko, S. V., Garbuz, D. G., Evgen’ev, M. B., Esteras, N., & Abramov, A. Y. (2024) · Molecular Neurobiology · doi:10.1007/s12035-024-04077-9 · Cited by 9 · see citing works
Self-citationLee, J., Han, M., Wang, K., Butler, L. R., & Sinclair, D. A. (2026) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2026.101442 · Cited by 7 · see citing works
Bakar, Z. H. A., Damanhuri, H. A., Makpol, S., Aizat, W. M., Sani, N. F. A., Hamzah, A. I. Z. A., Aripin, K. N. N., Rani, M. D. M., Noh, N. A., Razali, R., et al. (2018) · Journal of Alzheimer s Disease · doi:10.3233/jad-180511 · Cited by 8 · see citing works
Tian, F., Li, W., Lyu, Y., Zhang, P., Mu, J., Pei, Q.-L., & Zheng, J. (2019) · NeuroToxicology · doi:10.1016/j.neuro.2019.11.003 · Cited by 7 · see citing works
Heat shock proteins: a history of study in Russia
Евгеньев, М. Б. (2021) · Cell Stress and Chaperones · doi:10.1007/s12192-021-01219-z · Cited by 7 · see citing works
Morphofunctional features in mice treated by low and high Hsp70 doses
Piavchenko, G. A., Venediktov, A. A., Александрович, К. Е., & Kuznetsov, S. L. (2023) · Sechenov Medical Journal · doi:10.47093/2218-7332.2023.918.13 · Cited by 7 · see citing works
Tarbox, H. E., Branch, A., & Fried, S. D. (2025) · Science Advances · doi:10.1126/sciadv.adt3778 · Cited by 6 · see citing works
Khalaf, N. B. (2026) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2026.1711422 · Cited by 6 · see citing works
Nakajima, T., Maruhashi, T., Morimatsu, T., & Mukai, Y. (2019) · FEBS Letters · doi:10.1002/1873-3468.13707 · Cited by 6 · see citing works
A short-lived fish with long-lasting effects: hallmarks of aging in Nothobranchius furzeri
Savel, O., Lehmann, J., Poyraz, Y. K., & Page, M. M. (2026) · Frontiers in Aging · doi:10.3389/fragi.2025.1741819 · Cited by 6 · see citing works
Morozov, A. V., Yurinskaya, M. M., Mitkevich, V. A., Garbuz, D. G., Преображенская, О. В., Винокуров, М. Г., Evgen’ev, M. B., Карпов, В. Л., & Makarov, A. А. (2017) · Molecular Biology · doi:10.1134/s0026893316060133 · Cited by 5 · see citing works
Self-citationExogenous Hsp70 attenuates nitroglycerin-induced migraine-like symptoms in mice
Wu, F., Huang, Y., Wei, G., Huang, Z., Shi, C., Lin, W., & Liao, J. (2021) · Journal of Neurophysiology · doi:10.1152/jn.00314.2021 · Cited by 5 · see citing works
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Alway, S. E. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-810422-4.00026-9 · Cited by 6 · see citing works
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Choudhary, A., Kumar, P., Jagtap, Y. A., Kinger, S., Jha, H. C., Gutti, R. K., Sharma, V., Prajapati, V. K., & Mishra, A. (2025) · Brain Network Disorders · doi:10.1016/j.bnd.2025.05.001 · Cited by 4 · see citing works
Proteomic aging clocks in epidemiological studies: advances, applications and prospects
Xiao, H., Lau, C. E., Dehghan, A., & Robinson, O. (2026) · Nature Aging · doi:10.1038/s43587-026-01118-x · Cited by 4 · see citing works
Chen, Y., Xie, Y., & Ni, H. (2022) · Experimental Brain Research · doi:10.1007/s00221-022-06490-9 · Cited by 4 · see citing works
Voinsky, I., Goldenberg, O., Israel‐Elgali, I., Volkov, H., Puzianowska‐Kuźnicka, M., Shomron, N., & Gurwitz, D. (2024) · Drug Development Research · doi:10.1002/ddr.70011 · Cited by 4 · see citing works
A familial natural short sleep mutation in dec2 extends healthspan and lifespan in Drosophila
Pandey, P., Wall, P. K., Lopez, S. R., Zunica, E. R. M., Dubuisson, O. S., Dantas, W. S., Davuluri, G., Taylor, A. L., Wall, T. K., Juge, H. J., et al. (2025) · iScience · doi:10.1016/j.isci.2025.113388 · Cited by 4 · see citing works
The unfolded protein response in progeria arteries originates from non-endothelial cell types
Silva, R. A., Sarigol, F., Karagöz, G. E., Osmanagic‐Myers, S., & Foisner, R. (2025) · Life Science Alliance · doi:10.26508/lsa.202503485 · Cited by 3 · see citing works
APOE and Alzheimer's disease: Pathologic clues from transgenic Drosophila melanogaster
Haddadi, M., Haghi, M., Rezaei, N., Kiani, Z., Akkülah, T., & Çelik, A. (2024) · Archives of Gerontology and Geriatrics · doi:10.1016/j.archger.2024.105420 · Cited by 3 · see citing works
Garbuz, D. G., Sverchinsky, D. V., Davletshin, A. I., Margulis, B. A., Mitkevich, V. A., Куликов, А. М., & Evgen’ev, M. B. (2019) · Cell Stress and Chaperones · doi:10.1007/s12192-019-01038-3 · Cited by 3 · see citing works
Self-citationIntranasal Administration of Hsp70: Molecular and Therapeutic Consequences
Evgen’ev, M. B., Garbuz, D. G., Morozov, A. V., & Bobkova, N. V. (2018) · Heat shock proteins · doi:10.1007/978-3-319-89551-2_16 · Cited by 3 · see citing works
Self-citationBobkova, N. V., Chuvakova, L. N., Kononova, S. V., Kovalev, V. I., Sukhikh, G. T., Zatsepina, O. G., Rezvykh, A. P., & Евгеньев, М. Б. (2025) · Molecular Neurobiology · doi:10.1007/s12035-025-05135-6 · Cited by 2 · see citing works
Self-citationThe APOE Gene Cluster in Normal Aging
Florczak‐Wyspianska, J., Hurła, M., Pikor, D., Poszwa, J., Korczowska-Łącka, I., Szymanowicz, O., Pluto-Prądzyńska, A., Goutor, U., Wiszniewska, M., Kozubski, W. P., et al. (2025) · Journal of Integrative Neuroscience · doi:10.31083/jin36401 · Cited by 2 · see citing works
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Panchal, K., Kumar, A., & Tiwari, A. K. (2018) · Heat shock proteins · doi:10.1007/978-3-319-89551-2_1 · Cited by 2 · see citing works
Heat Shock Proteins in Neural Signaling: Implications in Health and Disease
Mishra, P. S., & Singh, A. P. (2019) · Heat shock proteins · doi:10.1007/978-3-030-03952-3_22 · Cited by 2 · see citing works
Heat Shock Proteins, a Key Modulator of Neuroinflammation in Alzheimer’s Disease
Panchal, K., Bhatt, V., Raval, M., & Tiwari, A. K. (2020) · Heat shock proteins · doi:10.1007/7515_2020_12 · Cited by 2 · see citing works
Barny, L. A., Garcia, S. K., Houcek, A., Uzay, B., Kim, M., Kavalali, E. T., & Plate, L. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.08.11.669714 · Cited by 2 · see citing works
RNA and protein degradation in the aging process
Lin, J., Qiu, Y., Ye, C., Zhang, Y., Zeng, Z., Yao, B., Hu, Y., & Zhao, L. (2025) · Cellular Signalling · doi:10.1016/j.cellsig.2025.112166 · Cited by 1 · see citing works
Cocciolone, L., Souparnika, A., Uvarova, V., Kessler, K., & van Oosten‐Hawle, P. (2025) · Cell Stress and Chaperones · doi:10.1016/j.cstres.2025.100127 · Cited by 1 · see citing works
Barny, L. A., Garcia, S. K., Houcek, A., Uzay, B., Kim, M., Kavalali, E. T., & Plate, L. (2026) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2521663123 · Cited by 2 · see citing works
Linking mitochondrial dysfunction to sarcopenia
Alway, S. E. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-822146-4.00004-1 · Cited by 1 · see citing works
Полтавцева, Р. А., Bobkova, N. V., Zhdanova, D. Y., Svirshchevskaya, E. V., & Sukhikh, G. T. (2021) · Biochemistry (Moscow) Supplement Series A Membrane and Cell Biology · doi:10.1134/s1990747821050068 · Cited by 1 · see citing works
Self-citationRezvykh, A. P., Юринская, М. М., Винокуров, М. Г., Krasnov, G. S., Mitkevich, V. A., Makarov, A. А., Evgen’ev, M. B., & Zatsepina, O. G. (2018) · Molecular Biology · doi:10.1134/s0026898418060150 · Cited by 1 · see citing works
Self-citation
- Authors
- Bobkova, N. V., Evgen’ev, M., Garbuz, D. G., Kulikov, A. M., Morozov, A., Samokhin, A., Velmeshev, D., Medvinskaya, N., Nesterova, I., Pollock, A., & Nudler, E.
- Affiliations
- Russian Academy of Sciences (RU)
- Institute of Cell Biophysics, Russian Academy of Sciences, Pushchino, Moscow, 142290, Russia;
- Engelhardt Institute of Molecular Biology (RU)
- Institute of Developmental Biology, Moscow, 124319, Russia;
- Engelhardt Institute of Molecular Biology, Russian Academy of Sciences, Moscow, 119991, Russia;
- Howard Hughes Medical Institute (US)
- Corresponding author
- Nudler, Evgeny
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2015-12-14
- Volume
- 112
- Issue
- 52
- Pages
- 16006-16011
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC4702952
- OpenAlex
- W2270421926
- Cited by
- 118
- References
- 59
- Citations by year
- 2026: 8 · 2025: 17 · 2024: 11 · 2023: 10 · 2022: 8 · 2021: 12 · 2020: 7 · 2019: 17 · 2018: 16 · 2017: 6 · 2016: 6
- FWCI
- 4.05
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Howard Hughes Medical Institute (NA)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Heat shock proteins research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Antioxidants, Aging, Portulaca oleracea
- Keywords
- HSP70, intranasal administration, aging, lifespan extension, cognitive function, learning and memory, neurodegeneration, synaptophysin, lipofuscin accumulation, proteasome activity, synaptic integrity, neuroprotection
- MeSH terms
- Aging, Animals, Brain, Cognition, Exploratory Behavior, Humans, Lipofuscin, Longevity, Male, Memory, Mice, Inbred Strains, Microscopy, Fluorescence, Motor Activity, Recombinant Proteins, Blotting, Western, Synaptophysin, Maze Learning, HSP70 Heat-Shock Proteins, Protein Subunits, Proteasome Endopeptidase Complex
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