Intracellular Thermometry Uncovers Spontaneous Thermogenesis and Associated Thermal Signaling

Overview

Journal Commun Biol

Specialty Biology

Date 2021 Dec 10

PMID 34887517

Citations 16

Authors

Kohki Okabe

Seiichi Uchiyama

Affiliations

Soon will be listed here.

Abstract

Conventional thermal biology has elucidated the physiological function of temperature homeostasis through spontaneous thermogenesis and responses to variations in environmental temperature in organisms. In addition to research on individual physiological phenomena, the molecular mechanisms of fever and physiological events such as temperature-dependent sex determination have been intensively addressed. Thermosensitive biomacromolecules such as heat shock proteins (HSPs) and transient receptor potential (TRP) channels were systematically identified, and their sophisticated functions were clarified. Complementarily, recent progress in intracellular thermometry has opened new research fields in thermal biology. High-resolution intracellular temperature mapping has uncovered thermogenic organelles, and the thermogenic functions of brown adipocytes were ascertained by the combination of intracellular thermometry and classic molecular biology. In addition, intracellular thermometry has introduced a new concept, "thermal signaling", in which temperature variation within biological cells acts as a signal in a cascade of intriguing biological events.

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References

Oo S, Oo H, Takayama H, Ishii K, Takeshita Y, Goto H . Selenoprotein P-mediated reductive stress impairs cold-induced thermogenesis in brown fat. Cell Rep. 2022; 38(13):110566. DOI: 10.1016/j.celrep.2022.110566. View

Kedersha N, Gupta M, Li W, Miller I, Anderson P . RNA-binding proteins TIA-1 and TIAR link the phosphorylation of eIF-2 alpha to the assembly of mammalian stress granules. J Cell Biol. 1999; 147(7):1431-42. PMC: 2174242. DOI: 10.1083/jcb.147.7.1431. View

Patel D, Franklin K . Temperature-regulation of plant architecture. Plant Signal Behav. 2009; 4(7):577-9. PMC: 2710546. DOI: 10.4161/psb.4.7.8849. View

Kato H, Okabe K, Miyake M, Hattori K, Fukaya T, Tanimoto K . ER-resident sensor PERK is essential for mitochondrial thermogenesis in brown adipose tissue. Life Sci Alliance. 2020; 3(3). PMC: 7010021. DOI: 10.26508/lsa.201900576. View

Preussner M, Goldammer G, Neumann A, Haltenhof T, Rautenstrauch P, Muller-McNicoll M . Body Temperature Cycles Control Rhythmic Alternative Splicing in Mammals. Mol Cell. 2017; 67(3):433-446.e4. DOI: 10.1016/j.molcel.2017.06.006. View

Castillo K, Diaz-Franulic I, Canan J, Gonzalez-Nilo F, Latorre R . Thermally activated TRP channels: molecular sensors for temperature detection. Phys Biol. 2017; 15(2):021001. DOI: 10.1088/1478-3975/aa9a6f. View

Wang F, Han Y, Gu N . Cell Temperature Measurement for Biometabolism Monitoring. ACS Sens. 2020; 6(2):290-302. DOI: 10.1021/acssensors.0c01837. View

Childs C . Body temperature and clinical thermometry. Handb Clin Neurol. 2018; 157:467-482. DOI: 10.1016/B978-0-444-64074-1.00029-X. View

Chapman C, Liu Y, Sonek G, Tromberg B . The use of exogenous fluorescent probes for temperature measurements in single living cells. Photochem Photobiol. 1995; 62(3):416-25. DOI: 10.1111/j.1751-1097.1995.tb02362.x. View

10.

Baffou G, Rigneault H, Marguet D, Jullien L . A critique of methods for temperature imaging in single cells. Nat Methods. 2014; 11(9):899-901. DOI: 10.1038/nmeth.3073. View

11.

Wu Y, Alam M, Balasubramanian P, Ermakova A, Fischer S, Barth H . Nanodiamond Theranostic for Light-Controlled Intracellular Heating and Nanoscale Temperature Sensing. Nano Lett. 2021; 21(9):3780-3788. PMC: 8289278. DOI: 10.1021/acs.nanolett.1c00043. View

12.

Zhou J, Del Rosal B, Jaque D, Uchiyama S, Jin D . Advances and challenges for fluorescence nanothermometry. Nat Methods. 2020; 17(10):967-980. DOI: 10.1038/s41592-020-0957-y. View

13.

Tatsumi T, Sampei M, Saito K, Honda Y, Okazaki Y, Arata N . Age-Dependent and Seasonal Changes in Menstrual Cycle Length and Body Temperature Based on Big Data. Obstet Gynecol. 2020; 136(4):666-674. PMC: 7505142. DOI: 10.1097/AOG.0000000000003910. View

14.

Hirsch S, Sundaramoorthy S, Davies T, Zhuravlev Y, Waters J, Shirasu-Hiza M . FLIRT: fast local infrared thermogenetics for subcellular control of protein function. Nat Methods. 2018; 15(11):921-923. PMC: 6295154. DOI: 10.1038/s41592-018-0168-y. View

15.

Kriszt R, Arai S, Itoh H, Lee M, Goralczyk A, Ang X . Optical visualisation of thermogenesis in stimulated single-cell brown adipocytes. Sci Rep. 2017; 7(1):1383. PMC: 5431191. DOI: 10.1038/s41598-017-00291-9. View

16.

Yang J, Yang H, Lin L . Quantum dot nano thermometers reveal heterogeneous local thermogenesis in living cells. ACS Nano. 2011; 5(6):5067-71. DOI: 10.1021/nn201142f. View

17.

Okabe K, Sakaguchi R, Shi B, Kiyonaka S . Intracellular thermometry with fluorescent sensors for thermal biology. Pflugers Arch. 2018; 470(5):717-731. PMC: 5942359. DOI: 10.1007/s00424-018-2113-4. View

18.

Kimura H, Nagoshi T, Yoshii A, Kashiwagi Y, Tanaka Y, Ito K . The thermogenic actions of natriuretic peptide in brown adipocytes: The direct measurement of the intracellular temperature using a fluorescent thermoprobe. Sci Rep. 2017; 7(1):12978. PMC: 5636787. DOI: 10.1038/s41598-017-13563-1. View

19.

Choi J, Zhou H, Landig R, Wu H, Yu X, Von Stetina S . Probing and manipulating embryogenesis via nanoscale thermometry and temperature control. Proc Natl Acad Sci U S A. 2020; 117(26):14636-14641. PMC: 7334529. DOI: 10.1073/pnas.1922730117. View

20.

Tsuji T, Ikado K, Koizumi H, Uchiyama S, Kajimoto K . Difference in intracellular temperature rise between matured and precursor brown adipocytes in response to uncoupler and β-adrenergic agonist stimuli. Sci Rep. 2017; 7(1):12889. PMC: 5635136. DOI: 10.1038/s41598-017-12634-7. View