Stress biology: Complexity and multifariousness in health and disease

doi:10.1016/j.cstres.2024.01.006

. 2024 Feb;29(1):143-157.

doi: 10.1016/j.cstres.2024.01.006. Epub 2024 Feb 3.

Stress biology: Complexity and multifariousness in health and disease

Matthias P Mayer¹, Laura Blair², Gregory L Blatch³, Thiago J Borges⁴, Ahmed Chadli⁵, Gabriela Chiosis⁶, Aurélie de Thonel⁷, Albena Dinkova-Kostova⁸, Heath Ecroyd⁹, Adrienne L Edkins¹⁰, Takanori Eguchi¹¹, Monika Fleshner¹², Kevin P Foley¹³, Sotirios Fragkostefanakis¹⁴, Jason Gestwicki¹⁵, Pierre Goloubinoff¹⁶, Jennifer A Heritz¹⁷, Christine M Heske¹⁸, Jonathan D Hibshman¹⁹, Jenny Joutsen²⁰, Wei Li²¹, Michael Lynes²², Marc L Mendillo²³, Nahid Mivechi²⁴, Fortunate Mokoena²⁵, Yuka Okusha²⁶, Veena Prahlad²⁷, Elizabeth Repasky²⁸, Sara Sannino²⁹, Federica Scalia³⁰, Reut Shalgi³¹, Lea Sistonen³², Emily Sontag³³, Patricija van Oosten-Hawle³⁴, Anniina Vihervaara³⁵, Anushka Wickramaratne³⁶, Shawn Xiang Yang Wang³⁷, Tawanda Zininga³⁸

Affiliations

¹ Center for Molecular Biology of Heidelberg University (ZMBH), DKFZ-ZMBH Alliance, Heidelberg, Germany. Electronic address: m.mayer@zmbh.uni-heidelberg.de.
² Department of Molecular Medicine, Morsani College of Medicine, University of South Florida, Tampa, FL 33612, USA.
³ Biomedical Research and Drug Discovery Research Group, Faculty of Health Sciences, Higher Colleges of Technology, Sharjah, United Arab Emirates; Biomedical Biotechnology Research Unit, Department of Biochemistry and Microbiology, Rhodes University, Grahamstown, South Africa.
⁴ Department of Surgery, Center for Transplantation Sciences, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02129, USA.
⁵ Georgia Cancer Center, Medical College of Georgia at Augusta University, Augusta, GA 30912, USA.
⁶ Department of Medicine, Division of Solid Tumors, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA; Chemical Biology Program, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA.
⁷ CNRS, UMR 7216, 75250 Paris Cedex 13, Paris, France; Univeristy of Paris Diderot, Sorbonne Paris Cité, Paris, France; Département Hospitalo-Universitaire DHU PROTECT, Paris, France.
⁸ Division of Cellular and Systems Medicine, Jacqui Wood Cancer Centre, School of Medicine, University of Dundee, Dundee, UK.
⁹ Molecular Horizons and School of Chemistry and Molecular Bioscience, University of Wollongong, Wollongong, New South Wales 2522, Australia.
¹⁰ Biomedical Biotechnology Research Unit (BioBRU), Department of Biochemistry and Microbiology, Rhodes University, Makhanda, South Africa.
¹¹ Department of Dental Pharmacology, Faculty of Medicine, Dentistry and Pharmaceutical Sciences, Okayama University, Okayama 700-8525, Japan.
¹² Department of Integrative Physiology, University of Colorado at Boulder, Boulder, CO 80309, USA.
¹³ Ranok Therapeutics, Waltham, MA 02451, USA.
¹⁴ Department of Biosciences, Molecular Cell Biology of Plants, Goethe University Frankfurt am Main, Frankfurt am Main 60438, Germany.
¹⁵ Institute for Neurodegenerative Diseases, University of California, San Francisco, CA 94158, USA.
¹⁶ Department of Plant Molecular Biology, Faculty of Biology and Medicine, University of Lausanne, Lausanne, Switzerland.
¹⁷ Department of Urology, SUNY Upstate Medical University, Syracuse, NY 13210, USA; Upstate Cancer Center, SUNY Upstate Medical University, Syracuse, NY 13210, USA; Department of Biochemistry and Molecular Biology, SUNY Upstate Medical University, Syracuse, NY 13210, USA.
¹⁸ Pediatric Oncology Branch, National Cancer Institute, National Institutes of Health, Bethesda, MD 20892, USA.
¹⁹ Biology Department, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA.
²⁰ Department of Pathology, Lapland Central Hospital, Lapland Wellbeing Services County, Rovaniemi, Finland.
²¹ Department of Dermatology and the Norris Comprehensive Cancer Center, University of Southern California Keck Medical Center, Los Angeles, CA 90033, USA.
²² Department of Molecular and Cell Biology, University of Connecticut, Storrs, CT 06269, USA.
²³ Department of Biochemistry and Molecular Genetics, Northwestern University Feinberg School of Medicine, Chicago, IL 60611, USA; Simpson Querrey Center for Epigenetics, Northwestern University Feinberg School of Medicine, Chicago, IL 60611, USA.
²⁴ Molecular Chaperone Biology, Medical College of Georgia, Georgia Cancer Center, Augusta University, Augusta, GA 30912, USA.
²⁵ Department of Biochemistry, North-West University, Mmabatho 2735, South Africa.
²⁶ Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA 02215, USA.
²⁷ Department of Cell Stress Biology, Roswell Park Comprehensive Cancer Center, Buffalo, NY 14203, USA.
²⁸ Department of Hematology and Oncology, Roswell Park Comprehensive Cancer Center, Buffalo, NY 14263, USA.
²⁹ Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA 15260, USA.
³⁰ Department of Biomedicine, Neuroscience and Advanced Diagnostics (BIND), University of Palermo, Palermo, Italy; Euro-Mediterranean Institute of Science and Technology (IEMEST), Palermo, Italy.
³¹ Department of Biochemistry, Rappaport Faculty of Medicine, Technion-Israel Institute of Technology, Haifa 31096, Israel.
³² Faculty of Science and Engineering, Cell Biology, Åbo Akademi University, Turku, Finland; Turku Bioscience Centre, University of Turku and Åbo Akademi University, Turku, Finland.
³³ Department of Biological Sciences, Marquette University, Milwaukee, WI 53233, USA.
³⁴ Department of Biological Sciences, University of North Carolina at Charlotte, Charlotte, NC 28223, USA.
³⁵ Department of Gene Technology, KTH Royal Institute of Technology, Science for Life Laboratory, Stockholm, Sweden.
³⁶ Laboratory of Molecular Biology, National Cancer Institute, National Institutes of Health, Bethesda, MD 20892, USA.
³⁷ Developmental Therapeutics Program, VCU Comprehensive Massey Cancer Center, VCU Institute of Molecular Medicine, Virginia Commonwealth University, School of Medicine, Richmond, VA 23298, USA.
³⁸ Department of Biochemistry, Stellenbosch University, Stellenbosch 7602, South Africa.

PMID: 38311120
PMCID: PMC10939078
DOI: 10.1016/j.cstres.2024.01.006

Stress biology: Complexity and multifariousness in health and disease

Matthias P Mayer et al. Cell Stress Chaperones. 2024 Feb.

. 2024 Feb;29(1):143-157.

doi: 10.1016/j.cstres.2024.01.006. Epub 2024 Feb 3.

Authors

Affiliations

¹ Center for Molecular Biology of Heidelberg University (ZMBH), DKFZ-ZMBH Alliance, Heidelberg, Germany. Electronic address: m.mayer@zmbh.uni-heidelberg.de.
² Department of Molecular Medicine, Morsani College of Medicine, University of South Florida, Tampa, FL 33612, USA.
³ Biomedical Research and Drug Discovery Research Group, Faculty of Health Sciences, Higher Colleges of Technology, Sharjah, United Arab Emirates; Biomedical Biotechnology Research Unit, Department of Biochemistry and Microbiology, Rhodes University, Grahamstown, South Africa.
⁴ Department of Surgery, Center for Transplantation Sciences, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02129, USA.
⁵ Georgia Cancer Center, Medical College of Georgia at Augusta University, Augusta, GA 30912, USA.
⁶ Department of Medicine, Division of Solid Tumors, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA; Chemical Biology Program, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA.
⁷ CNRS, UMR 7216, 75250 Paris Cedex 13, Paris, France; Univeristy of Paris Diderot, Sorbonne Paris Cité, Paris, France; Département Hospitalo-Universitaire DHU PROTECT, Paris, France.
⁸ Division of Cellular and Systems Medicine, Jacqui Wood Cancer Centre, School of Medicine, University of Dundee, Dundee, UK.
⁹ Molecular Horizons and School of Chemistry and Molecular Bioscience, University of Wollongong, Wollongong, New South Wales 2522, Australia.
¹⁰ Biomedical Biotechnology Research Unit (BioBRU), Department of Biochemistry and Microbiology, Rhodes University, Makhanda, South Africa.
¹¹ Department of Dental Pharmacology, Faculty of Medicine, Dentistry and Pharmaceutical Sciences, Okayama University, Okayama 700-8525, Japan.
¹² Department of Integrative Physiology, University of Colorado at Boulder, Boulder, CO 80309, USA.
¹³ Ranok Therapeutics, Waltham, MA 02451, USA.
¹⁴ Department of Biosciences, Molecular Cell Biology of Plants, Goethe University Frankfurt am Main, Frankfurt am Main 60438, Germany.
¹⁵ Institute for Neurodegenerative Diseases, University of California, San Francisco, CA 94158, USA.
¹⁶ Department of Plant Molecular Biology, Faculty of Biology and Medicine, University of Lausanne, Lausanne, Switzerland.
¹⁷ Department of Urology, SUNY Upstate Medical University, Syracuse, NY 13210, USA; Upstate Cancer Center, SUNY Upstate Medical University, Syracuse, NY 13210, USA; Department of Biochemistry and Molecular Biology, SUNY Upstate Medical University, Syracuse, NY 13210, USA.
¹⁸ Pediatric Oncology Branch, National Cancer Institute, National Institutes of Health, Bethesda, MD 20892, USA.
¹⁹ Biology Department, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA.
²⁰ Department of Pathology, Lapland Central Hospital, Lapland Wellbeing Services County, Rovaniemi, Finland.
²¹ Department of Dermatology and the Norris Comprehensive Cancer Center, University of Southern California Keck Medical Center, Los Angeles, CA 90033, USA.
²² Department of Molecular and Cell Biology, University of Connecticut, Storrs, CT 06269, USA.
²³ Department of Biochemistry and Molecular Genetics, Northwestern University Feinberg School of Medicine, Chicago, IL 60611, USA; Simpson Querrey Center for Epigenetics, Northwestern University Feinberg School of Medicine, Chicago, IL 60611, USA.
²⁴ Molecular Chaperone Biology, Medical College of Georgia, Georgia Cancer Center, Augusta University, Augusta, GA 30912, USA.
²⁵ Department of Biochemistry, North-West University, Mmabatho 2735, South Africa.
²⁶ Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA 02215, USA.
²⁷ Department of Cell Stress Biology, Roswell Park Comprehensive Cancer Center, Buffalo, NY 14203, USA.
²⁸ Department of Hematology and Oncology, Roswell Park Comprehensive Cancer Center, Buffalo, NY 14263, USA.
²⁹ Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA 15260, USA.
³⁰ Department of Biomedicine, Neuroscience and Advanced Diagnostics (BIND), University of Palermo, Palermo, Italy; Euro-Mediterranean Institute of Science and Technology (IEMEST), Palermo, Italy.
³¹ Department of Biochemistry, Rappaport Faculty of Medicine, Technion-Israel Institute of Technology, Haifa 31096, Israel.
³² Faculty of Science and Engineering, Cell Biology, Åbo Akademi University, Turku, Finland; Turku Bioscience Centre, University of Turku and Åbo Akademi University, Turku, Finland.
³³ Department of Biological Sciences, Marquette University, Milwaukee, WI 53233, USA.
³⁴ Department of Biological Sciences, University of North Carolina at Charlotte, Charlotte, NC 28223, USA.
³⁵ Department of Gene Technology, KTH Royal Institute of Technology, Science for Life Laboratory, Stockholm, Sweden.
³⁶ Laboratory of Molecular Biology, National Cancer Institute, National Institutes of Health, Bethesda, MD 20892, USA.
³⁷ Developmental Therapeutics Program, VCU Comprehensive Massey Cancer Center, VCU Institute of Molecular Medicine, Virginia Commonwealth University, School of Medicine, Richmond, VA 23298, USA.
³⁸ Department of Biochemistry, Stellenbosch University, Stellenbosch 7602, South Africa.

PMID: 38311120
PMCID: PMC10939078
DOI: 10.1016/j.cstres.2024.01.006

Abstract

Preserving and regulating cellular homeostasis in the light of changing environmental conditions or developmental processes is of pivotal importance for single cellular and multicellular organisms alike. To counteract an imbalance in cellular homeostasis transcriptional programs evolved, called the heat shock response, unfolded protein response, and integrated stress response, that act cell-autonomously in most cells but in multicellular organisms are subjected to cell-nonautonomous regulation. These transcriptional programs downregulate the expression of most genes but increase the expression of heat shock genes, including genes encoding molecular chaperones and proteases, proteins involved in the repair of stress-induced damage to macromolecules and cellular structures. Sixty-one years after the discovery of the heat shock response by Ferruccio Ritossa, many aspects of stress biology are still enigmatic. Recent progress in the understanding of stress responses and molecular chaperones was reported at the 12th International Symposium on Heat Shock Proteins in Biology, Medicine and the Environment in the Old Town Alexandria, VA, USA from 28th to 31st of October 2023.

Keywords: Heat shock proteins; Heat shock response; Heat shock transcription factors; Molecular chaperones; Protein folding diseases; Stress response.

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Figures

**Fig. 1**
Group photo of meeting attendees at the 12th International Symposium on Heat Shock Proteins in Biology, Medicine and the Environment inside the Hilton Old Town Alexandria, Alexandria, VA, USA.

**Fig. 2**
Matthias Mayer was honored as a CSSI Senior Fellow by CSSI founder Lawrence Hightower (left) and President Lea Sistonen (right).

See this image and copyright information in PMC

References

1. Ritossa F. A new puffing pattern induced by temperature shock and DNP in Drosophila (in English) Experientia. 1962;18:571–573. doi: 10.1007/BF02172188. - DOI
1. Vihervaara A., Mahat D.B., Guertin M.J., et al. Transcriptional response to stress is pre-wired by promoter and enhancer architecture (in English) Nat Commun. 2017;8:255. doi: 10.1038/s41467-017-00151-0. - DOI - PMC - PubMed
1. Mahat D.B., Salamanca H.H., Duarte F.M., Danko C.G., Lis J.T. Mammalian heat shock response and mechanisms underlying its genome-wide transcriptional regulation. Mol Cell. 2016;62:63–78. doi: 10.1016/j.molcel.2016.02.025. (in English) - DOI - PMC - PubMed
1. Rabindran S.K., Haroun R.I., Clos J., Wisniewski J., Wu C. Regulation of heat shock factor trimer formation: role of a conserved leucine zipper. Science. 1993;259:230–234. doi: 10.1126/science.8421783. (in English) - DOI - PubMed
1. Zuo J., Baler R., Dahl G., Voellmy R. Activation of the DNA-binding ability of human heat shock transcription factor 1 may involve the transition from an intramolecular to an intermolecular triple-stranded coiled-coil structure. Mol Cell Biol. 1994;14:7557–7568. doi: 10.1128/mcb.14.11.7557-7568.1994. (in English) - DOI - PMC - PubMed

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[1] Ritossa F. A new puffing pattern induced by temperature shock and DNP in Drosophila (in English) Experientia. 1962;18:571–573. doi: 10.1007/BF02172188. - DOI

[2] Ritossa F. A new puffing pattern induced by temperature shock and DNP in Drosophila (in English) Experientia. 1962;18:571–573. doi: 10.1007/BF02172188. - DOI

[3] Vihervaara A., Mahat D.B., Guertin M.J., et al. Transcriptional response to stress is pre-wired by promoter and enhancer architecture (in English) Nat Commun. 2017;8:255. doi: 10.1038/s41467-017-00151-0. - DOI - PMC - PubMed

[4] Vihervaara A., Mahat D.B., Guertin M.J., et al. Transcriptional response to stress is pre-wired by promoter and enhancer architecture (in English) Nat Commun. 2017;8:255. doi: 10.1038/s41467-017-00151-0. - DOI - PMC - PubMed

[5] Mahat D.B., Salamanca H.H., Duarte F.M., Danko C.G., Lis J.T. Mammalian heat shock response and mechanisms underlying its genome-wide transcriptional regulation. Mol Cell. 2016;62:63–78. doi: 10.1016/j.molcel.2016.02.025. (in English) - DOI - PMC - PubMed

[6] Mahat D.B., Salamanca H.H., Duarte F.M., Danko C.G., Lis J.T. Mammalian heat shock response and mechanisms underlying its genome-wide transcriptional regulation. Mol Cell. 2016;62:63–78. doi: 10.1016/j.molcel.2016.02.025. (in English) - DOI - PMC - PubMed

[7] Rabindran S.K., Haroun R.I., Clos J., Wisniewski J., Wu C. Regulation of heat shock factor trimer formation: role of a conserved leucine zipper. Science. 1993;259:230–234. doi: 10.1126/science.8421783. (in English) - DOI - PubMed

[8] Rabindran S.K., Haroun R.I., Clos J., Wisniewski J., Wu C. Regulation of heat shock factor trimer formation: role of a conserved leucine zipper. Science. 1993;259:230–234. doi: 10.1126/science.8421783. (in English) - DOI - PubMed

[9] Zuo J., Baler R., Dahl G., Voellmy R. Activation of the DNA-binding ability of human heat shock transcription factor 1 may involve the transition from an intramolecular to an intermolecular triple-stranded coiled-coil structure. Mol Cell Biol. 1994;14:7557–7568. doi: 10.1128/mcb.14.11.7557-7568.1994. (in English) - DOI - PMC - PubMed

[10] Zuo J., Baler R., Dahl G., Voellmy R. Activation of the DNA-binding ability of human heat shock transcription factor 1 may involve the transition from an intramolecular to an intermolecular triple-stranded coiled-coil structure. Mol Cell Biol. 1994;14:7557–7568. doi: 10.1128/mcb.14.11.7557-7568.1994. (in English) - DOI - PMC - PubMed

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Stress biology: Complexity and multifariousness in health and disease

Affiliations

Stress biology: Complexity and multifariousness in health and disease

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Abstract

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