4,848
Views
43
CrossRef citations to date
0
Altmetric
Research Paper

Intestinal epithelial HMGB1 inhibits bacterial infection via STAT3 regulation of autophagy

ORCID Icon, , ORCID Icon, ORCID Icon, , & ORCID Icon show all
Pages 1935-1953 | Received 22 Apr 2018, Accepted 01 Mar 2019, Published online: 09 Apr 2019

References

  • Lotze MT, Tracey KJ. High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal. Nat Rev Immunol. 2005;5(4):331–342.
  • Andersson U, Tracey KJ. HMGB1 is a therapeutic target for sterile inflammation and infection. Annu Rev Immunol. 2011;29:139–162.
  • Wang H, Bloom O, Zhang M, et al. HMG-1 as a late mediator of endotoxin lethality in mice. Science. 1999;285(5425):248–251.
  • Zhu X, Messer JS, Wang Y, et al. Cytosolic HMGB1 controls the cellular autophagy/apoptosis checkpoint during inflammation. J Clin Invest. 2015;125(3):1098–1110.
  • Mshvildadze M, Neu J. The infant intestinal microbiome: friend or foe? Early Hum Dev. 2010;86(Suppl 1):67–71.
  • Hooper LV. Do symbiotic bacteria subvert host immunity? Nat Rev Microbiol. 2009;7(5):367–374.
  • Hooper LV, Midtvedt T, Gordon JI. How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu Rev Nutr. 2002;22:283–307.
  • Bates JM, Akerlund J, Mittge E, et al. Intestinal alkaline phosphatase detoxifies lipopolysaccharide and prevents inflammation in zebrafish in response to the gut microbiota. Cell Host Microbe. 2007;2(6):371–382.
  • Santaolalla R, Abreu MT. Innate immunity in the small intestine. Curr Opin Gastroenterol. 2012;28(2):124–129.
  • Swamy M, Jamora C, Havran W, et al. Epithelial decision makers: in search of the ‘epimmunome‘. Nat Immunol. 2010;11(8):656–665.
  • Tang D, Kang R, Livesey KM, et al. Endogenous HMGB1 regulates autophagy. J Cell Biol. 2010;190(5):881–892.
  • Kang R, Livesey KM, Zeh HJ 3rd, et al. HMGB1 as an autophagy sensor in oxidative stress. Autophagy. 2011;7(8):904–906.
  • Fu XY. STAT3 in immune responses and inflammatory bowel diseases. Cell Res. 2006;16(2):214–219.
  • Yu H, Pardoll D, Jove R. STATs in cancer inflammation and immunity: a leading role for STAT3. Nat Rev Cancer. 2009;9(11):798–809.
  • Flanagan SE, Haapaniemi E, Russell MA, et al. Activating germline mutations in STAT3 cause early-onset multi-organ autoimmune disease. Nat Genet. 2014;46(8):812–814.
  • You L, Wang Z, Li H, et al. The role of STAT3 in autophagy. Autophagy. 2015;11(5):729–739.
  • Shen S, Niso-Santano M, Adjemian S, et al. Cytoplasmic STAT3 represses autophagy by inhibiting PKR activity. Mol Cell. 2012;48(5):667–680.
  • Wang YX, van Boxel-Dezaire AHH, Cheon H, et al. STAT3 activation in response to IL-6 is prolonged by the binding of IL-6 receptor to EGF receptor. Proc Natl Acad Sci U S A. 2013;110(42):16975–16980.
  • Niemand C, Nimmesgern A, Haan S, et al. Activation of STAT3 by IL-6 and IL-10 in primary human macrophages is differentially modulated by suppressor of cytokine signaling 3. J Iimmunol. 2003;170(6):3263–3272.
  • Kim HS, Kim DC, Kim HM, et al. STAT1 deficiency redirects IFN signalling toward suppression of TLR response through a feedback activation of STAT3. Sci Rep. 2015;5:13414.
  • Kong LY, Gelbard A, Wei J, et al. Inhibition of p-STAT3 enhances IFN-alpha efficacy against metastatic melanoma in a murine model. Clin Cancer Res off J Am Assoc Cancer Res. 2010;16(9):2550–2561.
  • Duan Y, Liao AP, Kuppireddi S, et al. Beta-Catenin activity negatively regulates bacteria-induced inflammation. Lab Invest. 2007;87(6):613–624.
  • Barthel M, Hapfelmeier S, Quintanilla-Martinez L, et al. Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infect Immun. 2003;71(5):2839–2858.
  • Muller S, Ronfani L, Bianchi ME. Regulated expression and subcellular localization of HMGB1, a chromatin protein with a cytokine function. J Intern Med. 2004;255(3):332–343.
  • Kalinina N, Agrotis A, Antropova Y, et al. Increased expression of the DNA-binding cytokine HMGB1 in human atherosclerotic lesions: role of activated macrophages and cytokines. Arterioscler Thromb Vasc Biol. 2004;24(12):2320–2325.
  • Saenz R, Futalan D, Leutenez L, et al. TLR4-dependent activation of dendritic cells by an HMGB1-derived peptide adjuvant. J Transl Med. 2014;12:211.
  • Van Beijnum JR, Buurman WA, Griffioen AW. Convergence and amplification of toll-like receptor (TLR) and receptor for advanced glycation end products (RAGE) signaling pathways via high mobility group B1 (HMGB1). Angiogenesis. 2008;11(1):91–99.
  • Zhang QC, Petrey D, Deng L, et al. Structure-based prediction of protein-protein interactions on a genome-wide scale. Nature. 2012;490(7421):556–560.
  • Zhang QC, Petrey D, Garzon JI, et al. PrePPI: a structure-informed database of protein-protein interactions. Nucleic Acids Res. 2013;41:828–833.
  • Sato T, Vries RG, Snippert HJ, et al. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature. 2009;459(7244):262–265.
  • Zhang YG, Wu S, Xia Y, et al. Salmonella-infected crypt-derived intestinal organoid culture system for host-bacterial interactions. Physiol Rep. 2014;2(9):e12147.
  • Engevik MA, Yacyshyn MB, Engevik KA, et al. Human Clostridium difficile infection: altered mucus production and composition. Am J Physiol Gastrointest Liver Physiol. 2015;308(6):510–524.
  • VanDussen KL, Marinshaw JM, Shaikh N, et al. Development of an enhanced human gastrointestinal epithelial culture system to facilitate patient-based assays. Gut. 2015;64(6):911–920.
  • Herfarth HH, Mohanty SP, Rath HC, et al. Interleukin 10 suppresses experimental chronic, granulomatous inflammation induced by bacterial cell wall polymers. Gut. 1996;39(6):836–845.
  • Du Toit A. Autophagy: STAT3 maintains order. Nat Rev Mol Cell Biol. 2012;13(12):754.
  • Yang H, Ochani M, Li J, et al. Reversing established sepsis with antagonists of endogenous high-mobility group box 1. Proc Natl Acad Sci U S A. 2004;101(1):296–301.
  • Xu YJ, Li L, Chen Y, et al. Role of HMGB1 in regulation of STAT3 expression in CD4(+) T cells from patients with aGVHD after allogeneic hematopoietic stem cell transplantation. Clin Immunol. 2015;161(2):278–283.
  • Wang G, Zhang J, Dui D, et al. High mobility group box 1 induces the activation of the Janus kinase 2 and signal transducer and activator of transcription 3 (JAK2/STAT3) signaling pathway in pancreatic acinar cells in rats, while AG490 and rapamycin inhibit their activation. Bosn J Basic Med Sci. 2016;16(4):307–312.
  • Lu R, Wu S, Zhang YG, et al. Salmonella protein AvrA activates the STAT3 signaling pathway in colon cancer. Neoplasia. 2016;18(5):307–316.
  • Lu R, Zhang YG, Sun J. STAT3 activation in infection and infection-associated cancer. Mol Cell Endocrinol. 2017;451:80–87.
  • Elschami M, Scherr M, Philippens B, et al. Reduction of STAT3 expression induces mitochondrial dysfunction and autophagy in cardiac HL-1 cells. Eur J Cell Biol. 2013;92(1):21–29.
  • Vitali R, Stronati L, Negroni A, et al. Fecal HMGB1 is a novel marker of intestinal mucosal inflammation in pediatric inflammatory bowel disease. Am J Gastroenterol. 2011;106(11):2029–2040.
  • Maeda S, Hikiba Y, Shibata W, et al. Essential roles of high-mobility group box 1 in the development of murine colitis and colitis-associated cancer. Biochem Biophys Res Commun. 2007;360(2):394–400.
  • Wu S, Zhang YG, Lu R, et al. Intestinal epithelial vitamin D receptor deletion leads to defective autophagy in colitis. Gut. 2015;64(7):1082–1094.
  • Sun J, Hobert ME, Rao AS, et al. Bacterial activation of beta-catenin signaling in human epithelia. Am J Physiol Gastrointest Liver Physiol. 2004;287(1):220–227.
  • Adachi M, Cui C, Dodge CT, et al. Targeting STAT3 inhibits growth and enhances radiosensitivity in head and neck squamous cell carcinoma. Oral Oncol. 2012;48(12):1220–1226.
  • Sun J, Hobert ME, Duan Y, et al. Crosstalk between NF-kappaB and beta-catenin pathways in bacterial-colonized intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol. 2005;289(1):129–137.
  • Lu R, Wu S, Liu X, et al. Chronic effects of a Salmonella type III secretion effector protein AvrA in vivo. PloS one. 2010;5(5):e10505.
  • Lu R, Voigt RM, Zhang Y, et al. Alcohol injury damages intestinal stem cells. Alcohol Clin Exp Res. 2017;41(4):727–734.
  • McCormick BA, Colgan SP, Delp-Archer C, et al. Salmonella typhimurium attachment to human intestinal epithelial monolayers: transcellular signalling to subepithelial neutrophils. J Cell Biol. 1993;123(4):895–907.
  • Wu S, Liao AP, Xia Y, et al. Vitamin D receptor negatively regulates bacterial-stimulated NF-kappaB activity in intestine. Am J Pathol. 2010;177(2):686–697.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.