Importance of temperature on immuno-metabolic regulation and cancer progression.
cancer immunometabolism
energy balance
fat metabolism
gut microbiota
temperature
Journal
The FEBS journal
ISSN: 1742-4658
Titre abrégé: FEBS J
Pays: England
ID NLM: 101229646
Informations de publication
Date de publication:
24 Sep 2022
24 Sep 2022
Historique:
revised:
01
09
2022
received:
23
06
2022
accepted:
20
09
2022
pubmed:
25
9
2022
medline:
25
9
2022
entrez:
24
9
2022
Statut:
aheadofprint
Résumé
Cancer immunotherapies emerge as promising strategies for restricting tumour growth. The tumour microenvironment (TME) has a major impact on the anti-tumour immune response and on the efficacy of the immunotherapies. Recent studies have linked changes in the ambient temperature with particular immuno-metabolic reprogramming and anti-cancer immune response in laboratory animals. Here, we describe the energetic balance of the organism during change in temperature, and link this to the immune alterations that could be of relevance for cancer, as well as for other human diseases. We highlight the contribution of the gut microbiota in modifying this interaction. We describe the overall metabolic response and underlying mechanisms of tumourigenesis in mouse models at varying ambient temperatures and shed light on their potential importance in developing therapeutics against cancer.
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Clayton Foundation for Biomedical Research
Organisme : H2020 European Research Council
ID : 815962
Organisme : Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
ID : 310030_205042
Informations de copyright
© 2022 Federation of European Biochemical Societies.
Références
Li XY, Wenes M, Romero P, Huang SCC, Fendt SM, Ho PC. Navigating metabolic pathways to enhance antitumour immunity and immunotherapy. Nat Rev Clin Oncol. 2019;16:425-41.
Wang HP, Franco F, Ho PC. Metabolic regulation of Tregs in cancer: opportunities for immunotherapy. Trends Cancer. 2017;3:583-92.
Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer. 2010;127:2893-917.
Singh GK, Jemal A. Socioeconomic and racial/ethnic disparities in cancer mortality, incidence, and survival in the United States, 1950-2014: over six decades of changing patterns and widening inequalities. J Environ Public Health. 2017;2017:2819372.
Chondronikola M, Volpi E, Borsheim E, Porter C, Saraf MK, Annamalai P, et al. Brown adipose tissue activation is linked to distinct systemic effects on lipid metabolism in humans. Cell Metab. 2016;23:1200-6.
van der Lans AAJJ, Hoeks J, Brans B, Vijgen GHEJ, Visser MGW, Vosselman MJ, et al. Cold acclimation recruits human brown fat and increases nonshivering thermogenesis. J Clin Investig. 2013;123:3395-403.
Walden TB, Hansen IR, Timmons JA, Cannon B, Nedergaard J. Recruited vs. nonrecruited molecular signatures of brown, "brite," and white adipose tissues. Am J Physiol Endocrinol Metab. 2012;302:E19-31.
Galon J, Bruni D. Approaches to treat immune hot, altered and cold tumours with combination immunotherapies. Nat Rev Drug Discov. 2019;18:197-218.
Duan QQ, Zhang HL, Zheng JN, Zhang LJ. Turning cold into hot: firing up the tumor microenvironment. Trends Cancer. 2020;6:605-18.
Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71:209-49.
Sharma A, Sharma T, Panwar MS, Sharma D, Bundel R, Hamilton RT, et al. Colder environments are associated with a greater cancer incidence in the female population of the United States. Tumour Biol. 2017;39:1010428317724784.
Shah VH. Response to: Grant re: Shah, Rieger, and pan, precipitation and climate zone explains the geographical disparity in the invasive cancer incidence rates in the United States (from: Grant W, environ. Eng. Sci. 2020 [Epub ahead of print]; DOI: 10.1089/ees.2019.0508) “the primary determinant of the geographical disparity in the invasive cancer incidence rates in the United States is solar UVB dose”. Environ Eng Sci. 2020;37:231-1.
Sundaresan G, Suthanthirarajan N, Namasivayam A. Certain immunological parameters in subacute cold stress. Indian J Physiol Pharmacol. 1990;34:57-60.
Jansky L, Pospisilova D, Honzova S, Ulicny B, Sramek P, Zeman V, et al. Immune system of cold-exposed and cold-adapted humans. Eur J Appl Physiol Occup Physiol. 1996;72:445-50.
Kokolus KM, Capitano ML, Lee CT, Eng JW, Waight JD, Hylander BL, et al. Baseline tumor growth and immune control in laboratory mice are significantly influenced by subthermoneutral housing temperature. Proc Natl Acad Sci USA. 2013;110:20176-81.
Sears CL, Pardoll DM. The intestinal microbiome influences checkpoint blockade. Nat Med. 2018;24:254-5.
Lee KA, Thomas AM, Bolte LA, Bjork JR, de Ruijter LK, Armanini F, et al. Cross-cohort gut microbiome associations with immune checkpoint inhibitor response in advanced melanoma. Nat Med. 2022;28:535-44.
Gesta S, Tseng YH, Kahn CR. Developmental origin of fat: tracking obesity to its source. Cell. 2007;131:242-56.
Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science. 2009;324:1029-33.
Richard AJ, White U, Elks CM, Stephens JM. Adipose tissue: physiology to metabolic dysfunction. In: Feingold KR, Anawalt B, Boyce A, Chrousos G, de Herder WW, Dhatariya K, et al., editors. Endotext. South Dartmouth, MA: MDText.com, Inc.; 2020. p. 2000-.
Rosen ED, Spiegelman BM. What we talk about when we talk about fat. Cell. 2014;156:20-44.
Aquila H, Link TA, Klingenberg M. The uncoupling protein from Brown fat mitochondria is related to the mitochondrial Adp Atp carrier - analysis of sequence homologies and of folding of the protein in the membrane. EMBO J. 1985;4:2369-76.
Chan M, Lim YC, Yang J, Namwanje M, Liu LH, Qiang L. Identification of a natural beige adipose depot in mice. J Biol Chem. 2019;294:6751-61.
Oreskovich SM, Ong FJ, Ahmed BA, Konyer NB, Blondin DP, Gunn E, et al. MRI reveals human Brown adipose tissue is rapidly activated in response to cold. J Endocr Soc. 2019;3:2374-84.
Vosselman MJ, Hoeks J, Brans B, Pallubinsky H, Nascimento EBM, van der Lans AAJJ, et al. Low brown adipose tissue activity in endurance-trained compared with lean sedentary men. Int J Obesity. 2015;39:1696-702.
Richard JE, Lopez-Ferreras L, Chanclon B, Eerola K, Micallef P, Skibicka KP, et al. CNS beta3-adrenergic receptor activation regulates feeding behavior, white fat browning, and body weight. Am J Physiol Endocrinol Metab. 2017;313:E344-58.
Suarez-Zamorano N, Fabbiano S, Chevalier C, Stojanovic O, Colin DJ, Stevanovic A, et al. Microbiota depletion promotes browning of white adipose tissue and reduces obesity. Nat Med. 2015;21:1497-501.
Warner A, Kjellstedt A, Carreras A, Bottcher G, Peng XR, Seale P, et al. Activation of beta(3)-adrenoceptors increases in vivo free fatty acid uptake and utilization in brown but not white fat depots in high-fat-fed rats. Am J Physiol Endocrinol Metab. 2016;311:E901-10.
Bartelt A, Bruns OT, Reimer R, Hohenberg H, Ittrich H, Peldschus K, et al. Brown adipose tissue activity controls triglyceride clearance. Nat Med. 2011;17:200-U93.
Iwen KA, Backhaus J, Cassens M, Waltl M, Hedesan OC, Merkel M, et al. Cold-induced Brown adipose tissue activity alters plasma fatty acids and improves glucose metabolism in men. J Clin Endocrinol Metab. 2017;102:4226-34.
McNeill B, Morton NM, Stimson RH. Substrate utilization by Brown adipose tissue: what's hot and What's not? Front Endocrinol. 2020;11:571659.
Skop V, Guo J, Liu N, Xiao C, Hall KD, Gavrilova O, et al. Mouse thermoregulation: introducing the concept of the thermoneutral point. Cell Rep. 2020;31:107501.
McKie GL, Medak KD, Knuth CM, Shamshoum H, Townsend LK, Peppier WT, et al. Housing temperature affects the acute and chronic metabolic adaptations to exercise in mice. J Physiol. 2019;597:4581-600.
Cui X, Nguyen NL, Zarebidaki E, Cao Q, Li F, Zha L, et al. Thermoneutrality decreases thermogenic program and promotes adiposity in high-fat diet-fed mice. Physiol Rep. 2016;4:e12799.
Ganeshan K, Chawla A. Warming the mouse to model human diseases. Nat Rev Endocrinol. 2017;13:458-65.
Feldmann HM, Golozoubova V, Cannon B, Nedergaard J. UCP1 ablation induces obesity and abolishes diet-induced thermogenesis in mice exempt from thermal stress by living at thermoneutrality. Cell Metab. 2009;9:203-9.
Weir G, Ramage LE, Akyol M, Rhodes JK, Kyle CJ, Fletcher AM, et al. Substantial metabolic activity of human Brown adipose tissue during warm conditions and cold-induced lipolysis of local triglycerides. Cell Metab. 2018;27:1348-1355.e4.
Rosenwald M, Perdikari A, Rulicke T, Wolfrum C. Bi-directional interconversion of brite and white adipocytes. Nat Cell Biol. 2013;15:659-67.
Roh HC, Tsai LTY, Shao M, Tenen D, Shen Y, Kumari M, et al. Warming induces significant reprogramming of beige, but not brown, adipocyte cellular identity. Cell Metab. 2018;27:1121-1137 e5.
Buck MD, Sowell RT, Kaech SM, Pearce EL. Metabolic instruction of immunity. Cell. 2017;169:570-86.
Stearns SC. The evolution of life histories. Oxford: Oxford University Press; 1992.
Wang A, Medzhitov R. Counting calories: the cost of inflammation. Cell. 2019;177:223-4.
Okin D, Medzhitov R. Evolution of inflammatory diseases. Curr Biol. 2012;22:R733-40.
Spiljar M, Steinbach K, Rigo D, Suarez-Zamorano N, Wagner I, Hadadi N, et al. Cold exposure protects from neuroinflammation through immunologic reprogramming. Cell Metab. 2021;33:2231-2246.e8.
Hadadi N, Spiljar M, Steinbach K, Colakoglu M, Chevalier C, Salinas G, et al. Comparative multi-tissue profiling reveals extensive tissue-specificity in transcriptome reprogramming during thermal adaptation. Elife. 2022;11:e78556.
Foxman EF, Storer JA, Fitzgerald ME, Wasik BR, Hou L, Zhao HY, et al. Temperature-dependent innate defense against the common cold virus limits viral replication at warm temperature in mouse airway cells. Proc Natl Acad Sci USA. 2015;112:827-32.
Jaakkola K, Saukkoriipi A, Jokelainen J, Juvonen R, Kauppila J, Vainio O, et al. Decline in temperature and humidity increases the occurrence of influenza in cold climate. Environ Health. 2014;13:22.
Williams JW, Elvington A, Ivanov S, Kessler S, Luehmann H, Baba O, et al. Thermoneutrality but not UCP1 deficiency suppresses monocyte mobilization into blood. Circ Res. 2017;121(6):662-76.
Jurankova E, Jezova D, Vigas M. Central stimulation of hormone release and the proliferative response of lymphocytes in humans. Mol Chem Neuropathol. 1995;25:213-23.
Castellani JW, IK MB, Rhind SG. Cold exposure: human immune responses and intracellular cytokine expression. Med Sci Sports Exerc. 2002;34:2013-20.
Ullevig SL, Umeda M, Chung E, Sesatty AL, Samsuhadi KE, Fogt DL. Effects of acute cold exposure on plasma inflammatory and lipid biomarkers related to cardiovascular disease risk. J Integr Cardiol. 2018;4(6):1-7.
Becker M, Serr I, Salb VK, Ott VB, Mengel L, Bluher M, et al. Short-term cold exposure supports human Treg induction in vivo. Mol Metab. 2019;28:73-82.
Man K, Kallies A, Vasanthakumar A. Resident and migratory adipose immune cells control systemic metabolism and thermogenesis. Cell Mol Immunol. 2022;19:421-31.
Lee MW, Odegaard JI, Mukundan L, Qiu Y, Molofsky AB, Nussbaum JC, et al. Activated type 2 innate lymphoid cells regulate beige fat biogenesis. Cell. 2015;160:74-87.
Fabbiano S, Suárez-Zamorano N, Rigo DE, Veyrat-Durebex C, Stevanovic Dokic A, Colin DJJ, et al. Caloric restriction leads to Browning of White adipose tissue through type 2 immune signaling. Cell Metab. 2016;24:434-46.
Suárez-Zamorano N, Fabbiano S, Chevalier C, Stojanović O, Colin DJ, Stevanović A, et al. Microbiota depletion promotes browning of white adipose tissue and reduces obesity. Nat Med. 2015;21:1497-501.
Nguyen KD, Qiu YF, Cui XJ, Goh YPS, Mwangi J, David T, et al. Alternatively activated macrophages produce catecholamines to sustain adaptive thermogenesis. Nature. 2011;480:104-U272.
Nussbaum JC, Van Dyken SJ, von Moltke J, Cheng LE, Mohapatra A, Molofsky AB, et al. Type 2 innate lymphoid cells control eosinophil homeostasis. Nature. 2013;502:245-8.
Van Dyken SJ, Locksley RM. Interleukin-4-and Interleukin-13-mediated alternatively activated macrophages: roles in homeostasis and disease. Annu Rev Immunol. 2013;31:317-43.
Luan B, Yoon YS, Le Lay J, Kaestner KH, Hedrick S, Montminy M. CREB pathway links PGE2 signaling with macrophage polarization. Proc Natl Acad Sci USA. 2015;112:15642-7.
Chung KJ, Chatzigeorgiou A, Economopoulou M, Garcia-Martin R, Alexaki VI, Mitroulis I, et al. A self-sustained loop of inflammation-driven inhibition of beige adipogenesis in obesity. Nat Immunol. 2017;18:654-64.
Camell CD, Sander J, Spadaro O, Lee A, Nguyen KY, Wing A, et al. Inflammasome-driven catecholamine catabolism in macrophages blunts lipolysis during ageing. Nature. 2017;550:119-23.
Pirzgalska RM, Seixas E, Seidman JS, Link VM, Sanchez NM, Mahu I, et al. Sympathetic neuron-associated macrophages contribute to obesity by importing and metabolizing norepinephrine. Nat Med. 2017;23:1309-18.
Jiang H, Ding X, Cao Y, Wang H, Zeng W. Dense intra-adipose sympathetic arborizations are essential for cold-induced Beiging of mouse White adipose tissue. Cell Metab. 2017;26:686-692.e3.
Bond LM, Burhans MS, Ntambi JM. Uncoupling protein-1 deficiency promotes brown adipose tissue inflammation and ER stress. Plos One. 2018;13:e0205726.
Brenner IK, Castellani JW, Gabaree C, Young AJ, Zamecnik J, Shephard RJ, et al. Immune changes in humans during cold exposure: effects of prior heating and exercise. J Appl Physiol (1985). 1999;87:699-710.
Hennig J, Laschefski U, Becker H, Rammsayer T, Netter P. Immune cell and cortisol responses to physically and pharmacologically induced lowering of body core temperature. Neuropsychobiology. 1993;28:82-6.
Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S. Functions of natural killer cells. Nat Immunol. 2008;9:503-10.
Nagai M, Iriki MC. Changes in immune activities by heat stress. In: Kosaka M, Suguhara T, Schmidt KL, Simon E, editors. Thermotherapy for neoplasia, inflammation and pain. Tokyo, Japan: Springer; 2001. p. 266-70.
Zhang HG, Mehta K, Cohen P, Guha C. Hyperthermia on immune regulation: a temperature's story. Cancer Lett. 2008;271:191-204.
Schell SR, Wessels FJ, Abouhamze A, Moldawer LL, Copeland EM 3rd. Pro- and antiinflammatory cytokine production after radiofrequency ablation of unresectable hepatic tumors. J Am Coll Surg. 2002;195:774-81.
Xu ZY, You WJ, Zhou YB, Chen WT, Wang YZ, Shan TZ. Cold-induced lipid dynamics and transcriptional programs in white adipose tissue. BMC Biol. 2019;17:74.
Wang ZC, Ning TL, Song AY, Rutter J, Wang QA, Jiang L. Chronic cold exposure enhances glucose oxidation in brown adipose tissue. EMBO Rep. 2020;21:e50085.
Lopezsoriano FJ, Alemany M. Effect of cold-temperature exposure and acclimation on amino-acid Pool changes and enzyme-activities of rat Brown adipose-tissue. Biochim Biophys Acta. 1987;925:265-71.
Ikeda K, Kang Q, Yoneshiro T, Camporez JP, Maki H, Homma M, et al. UCP1-independent signaling involving SERCA2b-mediated calcium cycling regulates beige fat thermogenesis and systemic glucose homeostasis. Nat Med. 2017;23:1454-65.
Flachs P, Adamcova K, Zouhar P, Marques C, Janovska P, Viegas I, et al. Induction of lipogenesis in white fat during cold exposure in mice: link to lean phenotype. Int J Obesity. 2017;41:372-80.
Kazak L, Chouchani ET, Jedrychowski MP, Erickson BK, Shinoda K, Cohen P, et al. A creatine-driven substrate cycle enhances energy expenditure and thermogenesis in beige fat. Cell. 2015;163:643-55.
Ikeda K, Kang QQ, Yoneshiro T, Camporez JP, Maki H, Homma M, et al. UCP1-independent signaling involving SERCA2b-mediated calcium cycling regulates beige fat thermogenesis and systemic glucose homeostasis. Nat Med. 2017;23:1454-+.
Ferrante AW Jr. The immune cells in adipose tissue. Diabetes Obes Metab. 2013;15(Suppl 3):34-8.
Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW. Obesity is associated with macrophage accumulation in adipose tissue. J Clin Investig. 2003;112:1796-808.
Lumeng CN, DelProposto JB, Westcott DJ, Saltiel AR. Phenotypic switching of adipose tissue macrophages with obesity is generated by spatiotemporal differences in macrophage subtypes. Diabetes. 2008;57:3239-46.
Kosteli A, Sugaru E, Haemmerle G, Martin JF, Lei J, Zechner R, et al. Weight loss and lipolysis promote a dynamic immune response in murine adipose tissue. J Clin Invest. 2010;120:3466-79.
Rausch ME, Weisberg S, Vardhana P, Tortoriello DV. Obesity in C57BL/6J mice is characterized by adipose tissue hypoxia and cytotoxic T-cell infiltration. Int J Obes (Lond). 2008;32:451-63.
Clavel T, Desmarchelier C, Haller D, Gerard P, Rohn S, Lepage P, et al. Intestinal microbiota in metabolic diseases: from bacterial community structure and functions to species of pathophysiological relevance. Gut Microbes. 2014;5:544-51.
Camarillo-Guerrero LF, Almeida A, Rangel-Pineros G, Finn RD, Lawley TD. Massive expansion of human gut bacteriophage diversity. Cell. 2021;184:1098-1109 e9.
Simmonds P, Adams MJ, Benko M, Breitbart M, Brister JR, Carstens EB, et al. Consensus statement: virus taxonomy in the age of metagenomics. Nat Rev Microbiol. 2017;15:161-8.
Perez JC. Fungi of the human gut microbiota: roles and significance. Int J Med Microbiol. 2021;311:151490.
Kong HH, Segre JA. Cultivating fungal research. Science. 2020;368:365-6.
Fiers WD, Gao IH, Iliev ID. Gut mycobiota under scrutiny: fungal symbionts or environmental transients? Curr Opin Microbiol. 2019;50:79-86.
Sivan A, Corrales L, Hubert N, Williams JB, Aquino-Michaels K, Earley ZM, et al. Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy. Science. 2015;350:1084-9.
Tanoue T, Morita S, Plichta DR, Skelly AN, Suda W, Sugiura Y, et al. A defined commensal consortium elicits CD8 T cells and anti-cancer immunity. Nature. 2019;565:600-5.
Chevalier C, Stojanovic O, Colin DJ, Suarez-Zamorano N, Tarallo V, Veyrat-Durebex C, et al. Gut microbiota orchestrates energy homeostasis during cold. Cell. 2015;163:1360-74.
Qu Q, Li H, Bai L, Zhang SW, Sun JQ, Lv WJ, et al. Effects of heat stress on gut microbiome in rats. Indian J Microbiol. 2021;61:338-47.
Gomez de Aguero M, Ganal-Vonarburg SC, Fuhrer T, Rupp S, Uchimura Y, Li H, et al. The maternal microbiota drives early postnatal innate immune development. Science. 2016;351:1296-302.
Keating C, Hughes D, Mahony T, Cysneiros D, Ijaz UZ, Smith CJ, et al. Cold adaptation and replicable microbial community development during long-term low-temperature anaerobic digestion treatment of synthetic sewage. FEMS Microbiol Ecol. 2018;94:fiy095.
Backhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, et al. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci USA. 2004;101:15718-23.
Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444:1027-31.
Ridaura VK, Faith JJ, Rey FE, Cheng J, Duncan AE, Kau AL, et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science. 2013;341:1241214.
Chevalier C, Stojanovic O, Colin DJ, Suarez-Zamorano N, Tarallo V, Veyrat-Durebex C, et al. Gut microbiota orchestrates energy homeostasis during cold. Cell. 2015;163:1360-74.
Zietak M, Kovatcheva-Datchary P, Markiewicz LH, Stahlman M, Kozak LP, Backhed F. Altered microbiota contributes to reduced diet-induced obesity upon cold exposure. Cell Metab. 2016;23:1216-23.
Worthmann A, John C, Ruhlemann MC, Baguhl M, Heinsen FA, Schaltenberg N, et al. Cold-induced conversion of cholesterol to bile acids in mice shapes the gut microbiome and promotes adaptive thermogenesis. Nat Med. 2017;23:839-49.
Zhang XY, Sukhchuluun G, Bo TB, Chi QS, Yang JJ, Chen B, et al. Huddling remodels gut microbiota to reduce energy requirements in a small mammal species during cold exposure. Microbiome. 2018;6:103.
Lambert GP, Gisolfi CV, Berg DJ, Moseley PL, Oberley LW, Kregel KC. Selected contribution: hyperthermia-induced intestinal permeability and the role of oxidative and nitrosative stress. J Appl Physiol (1985). 2002;92:1750-61. discussion 1749.
Moseley PL, Gapen C, Wallen ES, Walter ME, Peterson MW. Thermal stress induces epithelial permeability. Am J Physiol. 1994;267:C425-34.
Lambert GP. Role of gastrointestinal permeability in exertional heatstroke. Exerc Sport Sci Rev. 2004;32:185-90.
Cani PD, Delzenne NM. Gut microflora as a target for energy and metabolic homeostasis. Curr Opin Clin Nutr. 2007;10:729-34.
Koch F, Thom U, Albrecht E, Weikard R, Nolte W, Kuhla B, et al. Heat stress directly impairs gut integrity and recruits distinct immune cell populations into the bovine intestine. Proc Natl Acad Sci USA. 2019;116:10333-8.
Fabbiano S, Suarez-Zamorano N, Chevalier C, Lazarevic V, Kieser S, Rigo D, et al. Functional gut microbiota remodeling contributes to the caloric restriction-induced metabolic improvements. Cell Metab. 2018;28:907-921.e7.
Cao Y, Liu Y, Dong Q, Wang T, Niu C. Alterations in the gut microbiome and metabolic profile in rats acclimated to high environmental temperature. J Microbial Biotechnol. 2022;15:276-88.
Yi J, He G, Yang J, Luo Z, Yang X, Luo X. Heat acclimation regulates the autophagy-lysosome function to protect against heat stroke-induced brain injury in mice. Cell Physiol Biochem. 2017;41:101-14.
Wen C, Li S, Wang J, Zhu Y, Zong X, Wang Y, et al. Heat stress alters the intestinal microbiota and metabolomic profiles in mice. Front Microbiol. 2021;12:706772.
Chevalier C, Kieser S, Colakoglu M, Hadadi N, Brun J, Rigo D, et al. Warmth prevents bone loss through the gut microbiota. Cell Metab. 2020;32:575-590.e7.
Hesterberg RS, Cleveland JL, Epling-Burnette PK. Role of polyamines in immune cell functions. Med Sci (Basel). 2018;6:22.
Hussain T, Wang J, Murtaza G, Metwally E, Yang H, Kalhoro MS, et al. The role of polyphenols in regulation of heat shock proteins and gut microbiota in weaning stress. Oxid Med Cell Longev. 2021;2021:6676444.
Liu HY, Gu F, Zhu CP, Yuan L, Zhu CY, Zhu MA, et al. Epithelial heat shock proteins mediate the protective effects of Limosilactobacillus reuteri in dextran sulfate sodium-induced colitis. Front Immunol. 2022;13:865982.
Arnal ME, Lalles JP. Gut epithelial inducible heat-shock proteins and their modulation by diet and the microbiota. Nutr Rev. 2016;74:181-97.
Kieser S, Zdobnov EM, Trajkovski M. Comprehensive mouse microbiota genome catalog reveals major difference to its human counterpart. PLoS Comput Biol. 2022;18:e1009947.
Park JC, Im SH. Of men in mice: the development and application of a humanized gnotobiotic mouse model for microbiome therapeutics. Exp Mol Med. 2020;52:1383-96.
Nagpal R, Wang S, Solberg Woods LC, Seshie O, Chung ST, Shively CA, et al. Comparative microbiome signatures and short-chain fatty acids in mouse, rat, non-human primate, and human feces. Front Microbiol. 2018;9:2897.
Samuel BS, Gordon JI. A humanized gnotobiotic mouse model of host-archaeal-bacterial mutualism. Proc Natl Acad Sci USA. 2006;103:10011-6.
Hart J. Association between air temperature and cancer death rates in Florida: an ecological study. Dose Response. 2015;13:dose-response.14-024.Hart.
Maebayashi T, Ishibashi N, Aizawa T, Sakaguchi M, Sato T, Kawamori J, et al. Treatment outcomes of concurrent hyperthermia and chemoradiotherapy for pancreatic cancer: insights into the significance of hyperthermia treatment. Oncol Lett. 2017;13:4959-64.
Lee SY, Fiorentini G, Szasz AM, Szigeti G, Szasz A, Minnaar CA. Quo Vadis oncological hyperthermia (2020)? Front Oncol. 2020;10:1690.
Koppenol WH, Bounds PL, Dang CV. Otto Warburg's contributions to current concepts of cancer metabolism. Nat Rev Cancer. 2011;11:325-37.
Cao Y. Adipocyte and lipid metabolism in cancer drug resistance. J Clin Invest. 2019;129:3006-17.
Iwamoto H, Abe M, Yang Y, Cui D, Seki T, Nakamura M, et al. Cancer lipid metabolism confers antiangiogenic drug resistance. Cell Metab. 2018;28:104-117 e5.
Pace L, Nicolai E, Basso L, Garbino N, Soricelli A, Salvatore M. Brown adipose tissue in breast cancer evaluated by [(18)F] FDG-PET/CT. Mol Imaging Biol. 2020;22:1111-5.
Fujii T, Nishiki E, Endo M, Tokuda S, Nakazawa Y, Kurozumi S, et al. Implication of atypical supraclavicular F18-fluorodeoxyglucose uptake in patients with breast cancer: relationship between brown adipose tissue and TILs, PD-L1. Eur J Cancer. 2020;138:S94-4.
Bos SA, Gill CM, Martinez-Salazar EL, Torriani M, Bredella MA. Preliminary investigation of brown adipose tissue assessed by PET/CT and cancer activity. Skeletal Radiol. 2019;48:413-9.
Cao Q, Hersl J, La H, Smith M, Jenkins J, Goloubeva O, et al. A pilot study of FDG PET/CT detects a link between brown adipose tissue and breast cancer. BMC Cancer. 2014;14:126.
Ogawa Y, Abe K, Sakoda A, Onizuka H, Sakai S. FDG-PET and CT findings of activated brown adipose tissue in a patient with paraganglioma. Eur J Radiol Open. 2018;5:126-30.
Wang GX, Zhao XY, Lin JD. The brown fat secretome: metabolic functions beyond thermogenesis. Trends Endocrinol Metab. 2015;26:231-7.
Lee EJ, Chung TW, Kim KJ, Bae B, Kim BS, Kim S, et al. Macrophage stimulated by low ambient temperature hasten tumor growth via glutamine production. Biomedicine. 2020;8:381.
Shore AM, Karamitri A, Kemp P, Speakman JR, Graham NS, Lomax MA. Cold-induced changes in gene expression in brown adipose tissue, white adipose tissue and liver. PLoS One. 2013;8:e68933.
Puigserver P, Wu Z, Park CW, Graves R, Wright M, Spiegelman BM. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell. 1998;92:829-39.
Grommes C, Landreth GE, Heneka MT. Antineoplastic effects of peroxisome proliferator-activated receptor gamma agonists. Lancet Oncol. 2004;5:419-29.
Bhalla K, Hwang BJ, Dewi RE, Ou L, Twaddel W, Fang HB, et al. PGC1alpha promotes tumor growth by inducing gene expression programs supporting lipogenesis. Cancer Res. 2011;71:6888-98.
Bandyopadhayaya S, Ford B, Mandal CC. Cold-hearted: a case for cold stress in cancer risk. J Therm Biol. 2020;91:102608.
Seki T, Yang Y, Sun X, Lim S, Xie S, Guo Z, et al. Brown-fat-mediated tumour suppression by cold-altered global metabolism. Nature. 2022;608:421-8.
Fan Y, Pedersen O. Gut microbiota in human metabolic health and disease. Nat Rev Microbiol. 2021;19:55-71.
Viaud S, Saccheri F, Mignot G, Yamazaki T, Daillere R, Hannani D, et al. The intestinal microbiota modulates the anticancer immune effects of cyclophosphamide. Science. 2013;342:971-6.
Iida N, Dzutsev A, Stewart CA, Smith L, Bouladoux N, Weingarten RA, et al. Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science. 2013;342:967-70.
Vetizou M, Pitt JM, Daillere R, Lepage P, Waldschmitt N, Flament C, et al. Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science. 2015;350:1079-84.
Luu M, Riester Z, Baldrich A, Reichardt N, Yuille S, Busetti A, et al. Microbial short-chain fatty acids modulate CD8(+) T cell responses and improve adoptive immunotherapy for cancer. Nat Commun. 2021;12:4077.
He Y, Fu L, Li Y, Wang W, Gong M, Zhang J, et al. Gut microbial metabolites facilitate anticancer therapy efficacy by modulating cytotoxic CD8(+) T cell immunity. Cell Metab. 2021;33:988-1000 e7.
Hylander BL, Repasky EA. Thermoneutrality, mice, and cancer: a heated opinion. Trends Cancer. 2016;2:166-75.
Ganeshan K, Chawla A. Warming the mouse to model human diseases. Nat Rev Endocrinol. 2017;13:458-65.
Villarroya F, Cereijo R, Villarroya J, Gavalda-Navarro A, Giralt M. Toward an understanding of how immune cells control Brown and Beige Adipobiology. Cell Metab. 2018;27:954-61.
Goto T, Naknukool S, Yoshitake R, Hanafusa Y, Tokiwa S, Li Y, et al. Proinflammatory cytokine interleukin-1beta suppresses cold-induced thermogenesis in adipocytes. Cytokine. 2016;77:107-14.
Sakamoto T, Nitta T, Maruno K, Yeh YS, Kuwata H, Tomita K, et al. Macrophage infiltration into obese adipose tissues suppresses the induction of UCP1 level in mice. Am J Physiol Endocrinol Metab. 2016;310:E676-87.
Medrikova D, Sijmonsma TP, Sowodniok K, Richards DM, Delacher M, Sticht C, et al. Brown adipose tissue harbors a distinct sub-population of regulatory T cells. PLoS One. 2015;10:e0118534.
Schoeler M, Caesar R. Dietary lipids, gut microbiota and lipid metabolism. Rev Endocr Metab Disord. 2019;20:461-72.
Jia XK, Xu W, Zhang L, Li XY, Wang RR, Wu SS. Impact of gut microbiota and microbiota-related metabolites on hyperlipidemia. Front Cell Infect Microbiol. 2021;11:634780.
Wu HJ, Wu E. The role of gut microbiota in immune homeostasis and autoimmunity. Gut Microbes. 2012;3:4-14.
Gordon CJ. The mouse thermoregulatory system: its impact on translating biomedical data to humans. Physiol Behav. 2017;179:55-66.
Ruiz de Azua I, Mancini G, Srivastava RK, Rey AA, Cardinal P, Tedesco L, et al. Adipocyte cannabinoid receptor CB1 regulates energy homeostasis and alternatively activated macrophages. J Clin Invest. 2017;127:4148-62.
Giles DA, Ramkhelawon B, Donelan EM, Stankiewicz TE, Hutchison SB, Mukherjee R, et al. Modulation of ambient temperature promotes inflammation and initiates atherosclerosis in wild type C57BL/6 mice. Mol Metab. 2016;5:1121-30.
Pilch W, Pokora I, Szygula Z, Palka T, Pilch P, Cison T, et al. Effect of a single finnish sauna session on white blood cell profile and cortisol levels in athletes and non-athletes. J Hum Kinet. 2013;39:127-35.