7,993
Views
30
CrossRef citations to date
0
Altmetric
Articles

Temperature as a modulator of the gut microbiome: what are the implications and opportunities for thermal medicine?

&
Pages 83-89 | Received 07 May 2019, Accepted 26 Jun 2019, Published online: 03 Dec 2019

References

  • van der Zee J, van Rhoon GC. Cervical cancer: radiotherapy and hyperthermia. Int J Hyperthermia. 2006;22:229–234.
  • Issels RD, Lindner LH, Verweij J, et al. Effect of neoadjuvant chemotherapy plus regional hyperthermia on long-term outcomes among patients with localized high-risk soft tissue sarcoma: the EORTC 62961-ESHO 95 randomized clinical trial. JAMA Oncol. 2018;4:483–492.
  • Mauri G, Nicosia L, Xu Z, et al. Focused ultrasound: tumour ablation and its potential to enhance immunological therapy to cancer. Br Inst Radiol. 2018;91:20170641.
  • Jones EL, Oleson JR, Prosnitz LR, et al. Randomized trial of hyperthermia and radiation for superficial tumors. J Clin Oncol. 2005;23:3079–3085.
  • Pavlov MJ, Ceranic MS, Latincic SM, et al. Cytoreductive surgery and hyperthermic intraperitoneal chemotherapy for the treatment of advanced epithelial and recurrent ovarian carcinoma: a single center experience. Int J Hyperthermia. 2018;34:564–569.
  • Bull JM, Scott GL, Strebel FR, et al. Fever-range whole-body thermal therapy combined with cisplatin, gemcitabine, and daily interferon-alpha: a description of a phase I-II protocol. Int J Hyperthermia. 2008;24:649–662.
  • Lee CT, Kokolus KM, Leigh ND, et al. Defining immunological impact and therapeutic benefit of mild heating in a murine model of arthritis. PLoS One. 2015;10:e0120327.
  • Janssen CW, Lowry CA, Mehl MR, et al. Whole-body hyperthermia for the treatment of major depressive disorder: a randomized clinical trial. JAMA Psychiatry. 2016;73:789–795.
  • Fontaine SS, Novarro AJ, Kohl KD. Environmental temperature alters the digestive performance and gut microbiota of a terrestrial amphibian. J Exp Biol. 2018;221:187559.
  • Sohail MU, Hume ME, Byrd JA, et al. Molecular analysis of the caecal and tracheal microbiome of heat-stressed broilers supplemented with prebiotic and probiotic. Avian Pathol. 2015;44:67–74.
  • Thapa S, Zhang Y, Allen MS. Effects of temperature on bacterial microbiome composition in Ixodes scapularis ticks. Microbiologyopen. 2019;8:e00719.
  • Minich JJ, Morris MM, Brown M, et al. Elevated temperature drives kelp microbiome dysbiosis, while elevated carbon dioxide induces water microbiome disruption. PLoS One. 2018;13:e0192772.
  • Hooper LV, Littman DR, Macpherson AJ. Interactions between the microbiota and the immune system. Science. 2012;336:1268–1273.
  • Demaria S, Ng B, Devitt ML, et al. Ionizing radiation inhibition of distant untreated tumors (abscopal effect) is immune mediated. Int J Radiat Oncol Biol Phys. 2004;58:862–870.
  • Sharp HJ, Wansley EK, Garnett CT, et al. Synergistic antitumor activity of immune strategies combined with radiation. Front Biosci. 2007;12:4900–4910.
  • Shiao SL, Coussens LM. The tumor-immune microenvironment and response to radiation therapy. J Mammary Gland Biol Neoplasia. 2010;15:411–421.
  • Demaria S, Formenti SC. Role of T lymphocytes in tumor response to radiotherapy. Front Oncol. 2012;2:95.
  • Ludgate CM. Optimizing cancer treatments to induce an acute immune response: radiation abscopal effects, PAMPs, and DAMPs. Clin Cancer Res. 2012;18:4522–4525.
  • Zeng J, Harris TJ, Lim M, et al. Immune modulation and stereotactic radiation: improving local and abscopal responses. Biomed Res Int. 2013;2013:1.
  • Zitvogel L, Galluzzi L, Smyth MJ, et al. Mechanism of action of conventional and targeted anticancer therapies: reinstating immunosurveillance. Immunity. 2013;39:74–88.
  • Gerber SA, Lim JY, Connolly KA, et al. Radio-responsive tumors exhibit greater intratumoral immune activity than nonresponsive tumors. Int J Cancer. 2014;134:2383–2392.
  • Apetoh L, Ghiringhelli F, Tesniere A, et al. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med. 2007;13:1050–1059.
  • Mattarollo SR, Loi S, Duret H, et al. Pivotal role of innate and adaptive immunity in anthracycline chemotherapy of established tumors. Cancer Res. 2011;71:4809–4820.
  • Bracci L, Schiavoni G, Sistigu A, et al. Immune-based mechanisms of cytotoxic chemotherapy: implications for the design of novel and rationale-based combined treatments against cancer. Cell Death Differ. 2014;21:15–25.
  • de Biasi AR, Villena-Vargas J, Adusumilli PS. Cisplatin-induced antitumor immunomodulation: a review of preclinical and clinical evidence. Clin Cancer Res. 2014;20:5384–5391.
  • Emens LA, Middleton G. The interplay of immunotherapy and chemotherapy: harnessing potential synergies. Cancer Immunol Res. 2015;3:436–443.
  • Galluzzi L, Buque A, Kepp O, et al. Immunological effects of conventional chemotherapy and targeted anticancer agents. Cancer Cell. 2015;28:690–714.
  • Zitvogel L, Kepp O, Kroemer G. Immune parameters affecting the efficacy of chemotherapeutic regimens. Nat Rev Clin Oncol. 2011;8:151–160.
  • Galluzzi L, Chan TA, Kroemer G, et al. The hallmarks of successful anticancer immunotherapy. Sci Transl Med. 2018;10:eaat7807.
  • Viaud S, Saccheri F, Mignot G, et al. The intestinal microbiota modulates the anticancer immune effects of cyclophosphamide. Science. 2013;342:971–976.
  • Iida N, Dzutsev A, Stewart CA, et al. Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science. 2013;342:967–970.
  • Chen L, Tai WC, Brar MS, et al. Tumor grafting induces changes of gut microbiota in athymic nude mice in the presence and absence of medicinal Gynostemma saponins. PLoS One. 2015;10:e0126807.
  • Al-Qadami G, Van Sebille Y, Le H, et al. Gut microbiota: implications for radiotherapy response and radiotherapy-induced mucositis. Expert Rev Gastroenterol Hepatol. 2019;13:485–496.
  • Vetizou M, Pitt JM, Daillere R, et al. Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science. 2015;350:1079–1084.
  • Gopalakrishnan V, Spencer CN, Nezi L, et al. Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients. Science. 2018;359:97–103.
  • Matson V, Fessler J, Bao R, et al. The commensal microbiome is associated with anti-PD-1 efficacy in metastatic melanoma patients. Science. 2018;359:104–108.
  • Routy B, Le Chatelier E, Derosa L, et al. Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors. Science. 2018;359:91–97.
  • McQuade JL, Daniel CR, Helmink BA, et al. Modulating the microbiome to improve therapeutic response in cancer. Lancet Oncol. 2019;20:e77–e91.
  • Fessler JL, Gajewski TF. The microbiota: a new variable impacting cancer treatment outcomes. Clin Cancer Res. 2017;23:3229–3231.
  • Fessler J, Matson V, Gajewski TF. Exploring the emerging role of the microbiome in cancer immunotherapy. J Immunother Cancer. 2019;7:108.
  • Ley RE, Turnbaugh PJ, Klein S, et al. Microbial ecology: human gut microbes associated with obesity. Nature. 2006;444:1022–1023.
  • Turnbaugh PJ, Ley RE, Mahowald MA, et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444:1027–1031.
  • National Research Council (US) Committee for the Update of the Guide for the Care and Use of Laboratory Animals. Guide for the cared and use of laboratory animals. 8th ed. Washington, DC: The National Academies Press; 2012.
  • Schmidt E, Mykytczuk N, Schulte-Hostedde AI. Effects of the captive and wild environment on diversity of the gut microbiome of deer mice (Peromyscus maniculatus). ISME J. 2019;13:1293–1305.
  • Ma BW, Bokulich NA, Castillo PA, et al. Routine habitat change: a source of unrecognized transient alteration of intestinal microbiota in laboratory mice. PLoS One. 2012;7:e47416.
  • Franklin CL, Ericsson AC. Microbiota and reproducibility of rodent models. Lab Anim (NY). 2017;46:114–122.
  • Hufeldt MR, Nielsen DS, Vogensen FK, et al. Variation in the gut microbiota of laboratory mice is related to both genetic and environmental factors. Comp Med. 2010;60:336–347.
  • Servick K. Of mice and microbes. Science. 2016;353:741–743.
  • McCoy KD, Geuking MB, Ronchi F. Gut microbiome standardization in control and experimental mice. Curr Protoc Immunol. 2017;117:23.21.21–23.21.13.
  • Parker KD, Albeke SE, Gigley JP, et al. Microbiome composition in both wild-type and disease model mice is heavily influenced by mouse facility. Front Microbiol. 2018;9:1598.
  • Villarino NF, LeCleir GR, Denny JE, et al. Composition of the gut microbiota modulates the severity of malaria. Proc Natl Acad Sci USA. 2016;113:2235–2240.
  • Bidot WA, Ericsson AC, Franklin CL. Effects of water decontamination methods and bedding material on the gut microbiota. PLoS One. 2018;13:e0198305.
  • Cui B, Su D, Li W, et al. Effects of chronic noise exposure on the microbiome-gut-brain axis in senescence-accelerated prone mice: implications for Alzheimer's disease. J Neuroinflammation. 2018;15:190.
  • Wu G, Tang W, He Y, et al. Light exposure influences the diurnal oscillation of gut microbiota in mice. Biochem Biophys Res Commun. 2018;501:16–23.
  • Turner PV. The role of the gut microbiota on animal model reproducibility. Anim Model Exp Med. 2018;1:109–115.
  • Ghaly S, Kaakoush NO, Lloyd F, et al. Ultraviolet irradiation of skin alters the faecal microbiome independently of vitamin D in mice. Nutrients 2018;10:1069.
  • Deaver JA, Eum SY, Toborek M. Circadian disruption changes gut microbiome taxa and functional gene composition. Front Microbiol. 2018;9:737.
  • Antoch MP, Kondratov RV, Takahashi JS. Circadian clock genes as modulators of sensitivity to genotoxic stress. Cell Cycle 2005;4:901–907.
  • Jenkins SV, Vang KB, Gies A, et al. Sample storage conditions induce post-collection biases in microbiome profiles. BMC Microbiol. 2018;18:227.
  • Song SJ, Amir A, Metcalf JL, et al. Preservation methods differ in fecal microbiome stability, affecting suitability for field studies. mSystems. 2016;1:e00021–16.
  • Nicholls HT, Krisko TI, LeClair KB, et al. Regulation of adaptive thermogenesis by the gut microbiome. FASEB J. 2016;30:854–852.
  • Giles DA, Moreno-Fernandez ME, Stankiewicz TE, et al. Thermoneutral housing exacerbates nonalcoholic fatty liver disease in mice and allows for sex-independent disease modeling. Nat Med. 2017;23:829–838.
  • Worthmann A, John C, Ruhlemann MC, et al. Cold-induced conversion of cholesterol to bile acids in mice shapes the gut microbiome and promotes adaptive thermogenesis. Nat Med. 2017;23:839–849.
  • Thapa S, Zhang Y, Allen MS. Effects of temperature on bacterial microbiome composition in Ixodes scapularis ticks. Microbiologyopen. 2018;8:e00719.
  • Brothers CJ, Van Der Pol WJ, Morrow CD, et al. Ocean warming alters predicted microbiome functionality in a common sea urchin. Proc Biol Sci. 2018;285:20180340.
  • Kokou F, Sasson G, Nitzan T, et al. Host genetic selection for cold tolerance shapes microbiome composition and modulates its response to temperature. Elife. 2018;7:e36398.
  • eLife. Tropical fish adapt to cold temperatures in coordination with their microbiome. ScienceDaily [Internet]. [cited 2018 Nov 20]. Available from: https://www.sciencedaily.com/releases/2018/11/181120125843.htm
  • Zhang XY, Sukhchuluun G, Bo TB, et al. Huddling remodels gut microbiota to reduce energy requirements in a small mammal species during cold exposure. Microbiome. 2018;6:103.
  • Qi H, Wang P, Liu C, et al. Involvement of HIF-1alpha in MLCK-dependent endothelial barrier dysfunction in hypoxia. Cell Physiol Biochem. 2011;27:251–262.
  • Yamagata K, Tagami M, Takenaga F, et al. Hypoxia-induced changes in tight junction permeability of brain capillary endothelial cells are associated with IL-1beta and nitric oxide. Neurobiol Dis. 2004;17:491–499.
  • Lambert GP. Stress-induced gastrointestinal barrier dysfunction and its inflammatory effects. J Anim Sci. 2009;87:E101–E108.
  • Pearce SC, Mani V, Boddicker RL, et al. Heat stress reduces intestinal barrier integrity and favors intestinal glucose transport in growing pigs. PLoS One. 2013;8:e70215.
  • Dokladny K, Zuhl MN, Moseley PL. Intestinal epithelial barrier function and tight junction proteins with heat and exercise. J Appl Physiol (1985). 2016;120:692–701.
  • Costa KA, Soares AD, Wanner SP, et al. L-arginine supplementation prevents increases in intestinal permeability and bacterial translocation in male Swiss mice subjected to physical exercise under environmental heat stress. J Nutr. 2014;144:218–223.
  • Bouchama A, Parhar RS, el-Yazigi A, et al. Endotoxemia and release of tumor necrosis factor and interleukin 1 alpha in acute heatstroke. J Appl Physiol. 1991;70:2640–2644.
  • Appenheimer MM, Girard RA, Chen Q, et al. Conservation of IL-6 trans-signaling mechanisms controlling L-selectin adhesion by fever-range thermal stress. Eur J Immunol. 2007;37:2856–2867.
  • Sakaguchi Y, Makino M, Kaneko T, et al. Therapeutic efficacy of long duration-low temperature whole body hyperthermia when combined with tumor necrosis factor and carboplatin in rats. Cancer Res. 1994;54:2223–2227.
  • Juang T, Stauffer PR, Craciunescu OA, et al. Thermal dosimetry characteristics of deep regional heating of non-muscle invasive bladder cancer. Int J Hyperthermia. 2014;30:176–183.
  • Sapareto SA, Dewey WC. Thermal dose determination in cancer therapy. Int J Radiat Oncol Biol Phys. 1984;10:787–800.
  • Lee SY, Kim JH, Han YH, et al. The effect of modulated electro-hyperthermia on temperature and blood flow in human cervical carcinoma. Int J Hyperthermia. 2018;34:953–960.