دورية أكاديمية
DAMPs Released From Injured Renal Tubular Epithelial Cells Activate Innate Immune Signals in Healthy Renal Tubular Epithelial Cells.
العنوان: | DAMPs Released From Injured Renal Tubular Epithelial Cells Activate Innate Immune Signals in Healthy Renal Tubular Epithelial Cells. |
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المؤلفون: | DeWolf SE; Department of Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA.; Department of Pulmonary and Critical Care Medicine, University of California San Diego, San Diego, CA., Kasimsetty SG; Department of Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA., Hawkes AA; Department of Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA., Stocks LM; LifeSharing Organ Procurement Organization, San Diego, CA., Kurian SM; Division of Cell and Organ Transplantion, Scripps Clinic and Green Hospital, La Jolla, CA., McKay DB; Department of Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA.; Division of Cell and Organ Transplantion, Scripps Clinic and Green Hospital, La Jolla, CA. |
المصدر: | Transplantation [Transplantation] 2022 Aug 01; Vol. 106 (8), pp. 1589-1599. Date of Electronic Publication: 2021 Dec 23. |
نوع المنشور: | Journal Article; Research Support, N.I.H., Extramural |
اللغة: | English |
بيانات الدورية: | Publisher: Lippincott Williams & Wilkins Country of Publication: United States NLM ID: 0132144 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1534-6080 (Electronic) Linking ISSN: 00411337 NLM ISO Abbreviation: Transplantation Subsets: MEDLINE |
أسماء مطبوعة: | Publication: Hagerstown, MD : Lippincott Williams & Wilkins Original Publication: Baltimore, Williams & Wilkins. |
مواضيع طبية MeSH: | Acute Kidney Injury* , Reperfusion Injury*/metabolism, Alarmins ; Epithelial Cells/metabolism ; Humans ; Immunity, Innate ; Kidney/metabolism |
مستخلص: | Background: Renal ischemia-reperfusion injury (IRI) predictably causes acute kidney injury after shock and major cardiovascular procedures in all kidneys procured for transplantation. The earliest events of IRI are triggered by molecules released from injured cells, damage-associated molecular patterns (DAMPs), that bind pattern recognition receptors (PRRs) constitutively expressed on many cells within the kidney. Activation of PRR signaling leads to production of proinflammatory molecules, which incite a cascade of inflammatory events leading to acute kidney injury. Renal tubular epithelial cells (RTECs) are particularly susceptible to ischemic injury, and proximal RTEC injury is pathognomonic of renal IRI. To better understand how injured RTECs contribute to the cycle of deleterious inflammation in the setting of renal IRI, this study asked whether DAMPs released from injured RTECs induced PRR signals in healthy RTECs. Methods: Human RTECs were necrosed ex vivo to release intracellular DAMPs and resulting necrotic supernatant used to stimulate healthy RTECs, T lymphocytes, and monocytes. Results: DAMPs released from necrosed RTECs upregulated PRRs known to be associated with renal IRI and activated mitogen-activated protein kinase signaling pathways. Proinflammatory cytokines were upregulated in response to necrotic supernatant, and this upregulation was abrogated by MEK-1 inhibition. The RTEC-derived DAMPs were also potent inducers of T-cell activation/proliferation and monocyte migration. Conclusions: This is the first study to our knowledge to show that endogenous DAMPs released from injured RTECs directly activate PRR signaling in healthy RTECs. These findings provide new insights directed to therapeutics for renal IRI. Competing Interests: The authors declare no conflicts of interest. (Copyright © 2021 Wolters Kluwer Health, Inc. All rights reserved.) |
References: | Chertow GM, Burdick E, Honour M, et al. Acute kidney injury, mortality, length of stay, and costs in hospitalized patients. J Am Soc Nephrol. 2005;16:3365–3370. Thakar CV, Christianson A, Freyberg R, et al. Incidence and outcomes of acute kidney injury in intensive care units: a Veterans Administration study. Crit Care Med. 2009;37:2552–2558. Coca SG, Singanamala S, Parikh CR. Chronic kidney disease after acute kidney injury: a systematic review and meta-analysis. Kidney Int. 2012;81:442–448. Matzinger P. Tolerance, danger, and the extended family. Annu Rev Immunol. 1994;12:991–1045. Pradeu T, Cooper EL. The danger theory: 20 years later. Front Immunol. 2012;3:287. Jang HR, Rabb H. Immune cells in experimental acute kidney injury. Nat Rev Nephrol. 2015;11:88–101. Dai H, Thomson AW, Rogers NM. Dendritic cells as sensors, mediators, and regulators of ischemic injury. Front Immunol. 2019;10:2418. Bonventre JV, Yang L. Cellular pathophysiology of ischemic acute kidney injury. J Clin Invest. 2011;121:4210–4221. Rosin DL, Okusa MD. Dangers within: DAMP responses to damage and cell death in kidney disease. J Am Soc Nephrol. 2011;22:416–425. Mulay SR, Kumar SV, Lech M, et al. How kidney cell death induces renal necroinflammation. Semin Nephrol. 2016;36:162–173. Anders H-J. Toll-like receptors and danger signaling in kidney injury. J Am Soc Nephrol. 2010;21:1270–1274. Anders H-J. Of inflammasomes and alarmins: IL-1β and IL-1α in kidney disease. J Am Soc Nephrol. 2016;27:2564–2575. Anders H-J, Schaefer L. Beyond tissue injury-damage-associated molecular patterns, toll-like receptors, and inflammasomes also drive regeneration and fibrosis. J Am Soc Nephrol. 2014;25:1387–1400. Jain S, Plenter R, Nydam T, et al. Injury pathways that lead to AKI in a mouse kidney transplant model. Transplantation. 2020;104:1832–1841. Altemeier WA, Liles WC, Villagra-Garcia A, et al. Ischemia-reperfusion lung injury is attenuated in MyD88-deficient mice. PLoS One. 2013;8:e77123. Faubel S, Ljubanovic D, Reznikov L, et al. Caspase-1-deficient mice are protected against cisplatin-induced apoptosis and acute tubular necrosis. Kidney Int. 2004;66:2202–2213. Ferhat M, Robin A, Giraud S, et al. Endogenous IL-33 contributes to kidney ischemia-reperfusion injury as an alarmin. J Am Soc Nephrol. 2018;29:1272–1288. Kim H-J, Lee DW, Ravichandran K, et al. NLRP3 inflammasome knockout mice are protected against ischemic but not cisplatin-induced acute kidney injury. J Pharmacol Exp Ther. 2013;346:465–472. Leemans JC, Stokman G, Claessen N, et al. Renal-associated TLR2 mediates ischemia/reperfusion injury in the kidney. J Clin Invest. 2005;115:2894–2903. Mkaddem SB, Werts C, Goujon J-M, et al. Heat shock protein gp96 interacts with protein phosphatase 5 and controls toll-like receptor 2 (TLR2)-mediated activation of extracellular signal-regulated kinase (ERK) ½ in post-hypoxic kidney cells. J Biol Chem. 2009;284:12541–12549. Pulskens WP, Teske GJ, Butter LM, et al. Toll-like receptor-4 coordinates the innate immune response of the kidney to renal ischemia/reperfusion injury. PLoS One. 2008;3:e3596. Shigeoka AA, Kambo A, Mathison JC, et al. Nod1 and nod2 are expressed in human and murine renal tubular epithelial cells and participate in renal ischemia reperfusion injury. J Immunol. 2010;184:2297–2304. Shigeoka AA, Mueller JL, Kambo A, et al. An inflammasome-independent role for epithelial-expressed Nlrp3 in renal ischemia-reperfusion injury. J Immunol. 2010;185:6277–6285. Iyer SS, He Q, Janczy JR, et al. Mitochondrial cardiolipin is required for Nlrp3 inflammasome activation. Immunity. 2013;39:311–323. Iyer SS, Pulskens WP, Sadler JJ, et al. Necrotic cells trigger a sterile inflammatory response through the Nlrp3 inflammasome. Proc Natl Acad Sci U S A. 2009;106:20388–20393. Kayagaki N, Warming S, Lamkanfi M, et al. Non-canonical inflammasome activation targets caspase-11. Nature. 2011;479:117–121. Li M, Carpio DF, Zheng Y, et al. An essential role of the NF-kappa B/toll-like receptor pathway in induction of inflammatory and tissue-repair gene expression by necrotic cells. J Immunol. 2001;166:7128–7135. Mariathasan S, Weiss DS, Newton K, et al. Cryopyrin activates the inflammasome in response to toxins and ATP. Nature. 2006;440:228–232. Nakahira K, Haspel JA, Rathinam VA, et al. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat Immunol. 2011;12:222–230. Rovere-Querini P, Capobianco A, Scaffidi P, et al. HMGB1 is an endogenous immune adjuvant released by necrotic cells. EMBO Rep. 2004;5:825–830. Shimada K, Crother TR, Karlin J, et al. Oxidized mitochondrial DNA activates the NLRP3 inflammasome during apoptosis. Immunity. 2012;36:401–414. Allam R, Scherbaum CR, Darisipudi MN, et al. Histones from dying renal cells aggravate kidney injury via TLR2 and TLR4. J Am Soc Nephrol. 2012;23:1375–1388. Azroyan A, Cortez-Retamozo V, Bouley R, et al. Renal intercalated cells sense and mediate inflammation via the P2Y14 receptor. PLoS One. 2015;10:e0121419. Kawai C, Kotani H, Miyao M, et al. Circulating extracellular histones are clinically relevant mediators of multiple organ injury. Am J Pathol. 2016;186:829–843. Rabadi M, Kim M, Li H, et al. ATP induces PAD4 in renal proximal tubule cells via P2X7 receptor activation to exacerbate ischemic AKI. Am J Physiol Renal Physiol. 2018;314:F293–F305. Rabadi MM, Ghaly T, Goligorksy MS, et al. HMGB1 in renal ischemic injury. Am J Physiol Renal Physiol. 2012;303:F873–F885. Wu H, Ma J, Wang P, et al. HMGB1 contributes to kidney ischemia reperfusion injury. J Am Soc Nephrol. 2010;21:1878–1890. Yamasaki K, Muto J, Taylor KR, et al. NLRP3/cryopyrin is necessary for interleukin-1beta (IL-1beta) release in response to hyaluronan, an endogenous trigger of inflammation in response to injury. J Biol Chem. 2009;284:12762–12771. Zhou R, Tardivel A, Thorens B, et al. Thioredoxin-interacting protein links oxidative stress to inflammasome activation. Nat Immunol. 2010;11:136–140. Liu N, Wang H, Han G, et al. Alleviation of apoptosis of bone marrow-derived mesenchymal stem cells in the acute injured kidney by heme oxygenase-1 gene modification. Int J Biochem Cell Biol. 2015;69:85–94. Repetto G, del Peso A, Zurita JL. Neutral red uptake assay for the estimation of cell viability/cytotoxicity. Nat Protoc. 2008;3:1125–1131. Mogensen TH. Pathogen recognition and inflammatory signaling in innate immune defenses. Clin Microbiol Rev. 2009;22:240–273. Anjum R, Blenis J. The RSK family of kinases: emerging roles in cellular signalling. Nat Rev Mol Cell Biol. 2008;9:747–758. Bogoyevitch MA, Kobe B. Uses for JNK: the many and varied substrates of the c-Jun N-terminal kinases. Microbiol Mol Biol Rev. 2006;70:1061–1095. Kinsey GR, Li L, Okusa MD. Inflammation in acute kidney injury. Nephron Exp Nephrol. 2008;109:e102–e107. DeWolf SE, Shigeoka AA, Scheinok A, et al. Expression of TLR2, NOD1, and NOD2 and the NLRP3 inflammasome in renal tubular epithelial cells of male versus female mice. Nephron. 2017;137:68–76. Kasimsetty SG, DeWolf SE, Shigeoka AA, et al. Regulation of TLR2 and NLRP3 in primary murine renal tubular epithelial cells. Nephron Clin Pract. 2014;127:119–123. Linkermann A, Stockwell BR, Krautwald S, et al. Regulated cell death and inflammation: an auto-amplification loop causes organ failure. Nat Rev Immunol. 2014;14:759–767. Nakagawa S, Omura T, Yonezawa A, et al. Extracellular nucleotides from dying cells act as molecular signals to promote wound repair in renal tubular injury. Am J Physiol Renal Physiol. 2014;307:F1404–F1411. Sarhan M, Land WG, Tonnus W, et al. Origin and consequences of necroinflammation. Physiol Rev. 2018;98:727–780. Reddy M, Eirikis E, Davis C, et al. Comparative analysis of lymphocyte activation marker expression and cytokine secretion profile in stimulated human peripheral blood mononuclear cell cultures: an in vitro model to monitor cellular immune function. J Immunol Methods. 2004;293:127–142. Puré E, Cuff CA. A crucial role for CD44 in inflammation. Trends Mol Med. 2001;7:213–221. Chen GY, Nuñez G. Sterile inflammation: sensing and reacting to damage. Nat Rev Immunol. 2010;10:826–837. Anders HJ, Muruve DA. The inflammasomes in kidney disease. J Am Soc Nephrol. 2011;22:1007–1018. Jordan SC, Ammerman N, Choi J, et al. Interleukin-6: an important mediator of allograft injury. Transplantation. 2020;104:2497–2506. Shankar AS, Hoorn EJ, Gribnau J, et al. Current state of renal regenerative therapies. Transplantation. 2019;103:250–261. Vénéreau E, Ceriotti C, Bianchi ME. DAMPs from cell death to new life. Front Immunol. 2015;6:422. Tingle SJ, Sewpaul A, Bates L, et al. Dual microRNA blockade increases expression of antioxidant protective proteins: implications for ischemia-reperfusion injury. Transplantation. 2020;104:1853–1861. |
معلومات مُعتمدة: | R01 DK113162 United States DK NIDDK NIH HHS; R01 DK128547 United States DK NIDDK NIH HHS; R21 AI154471 United States AI NIAID NIH HHS |
المشرفين على المادة: | 0 (Alarmins) |
تواريخ الأحداث: | Date Created: 20211226 Date Completed: 20220728 Latest Revision: 20231002 |
رمز التحديث: | 20240628 |
مُعرف محوري في PubMed: | PMC9218002 |
DOI: | 10.1097/TP.0000000000004038 |
PMID: | 34954736 |
قاعدة البيانات: | MEDLINE |
تدمد: | 1534-6080 |
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DOI: | 10.1097/TP.0000000000004038 |