Aeromonas hydrophila inhibits autophagy triggering cytosolic translocation of mtDNA which activates the pro-apoptotic caspase-1/IL-1β-nitric oxide axis in headkidney macrophages

References

• Janda JM, Abbott SL. The genus Aeromonas: taxonomy, pathogenicity, and infection. Clin Microbiol Rev. 2010 Jan 1;23:35–73. Pmid:20065325.
   PubMed Web of Science ®Google Scholar
• Galindo CL, Fadl AA, Sha J, et al. Microarray analysis of Aeromonas hydrophila cytotoxic enterotoxin-treated murine primary macrophages. Infect Immun. 2004 Sep 1;72:5439–5445. Pmid:15322042.
   PubMed Web of Science ®Google Scholar
• Banerjee C, Singh A, Das TK, et al. Ameliorating ER-stress attenuates Aeromonas hydrophila-induced mitochondrial dysfunctioning and caspase mediated HKM apoptosis in Clarias batrachus. Sci Rep. 2014 Jul 25;4(1):1–3. Pmid: 25059203.
   Google Scholar
• Van Nhieu GT, Clair C, Grompone G, et al. Calcium signalling during cell interactions with bacterial pathogens. Biol Cell. 2004 Feb;96(1):93–101. Pmid:15093131.
   PubMed Web of Science ®Google Scholar
• Malhotra JD, Kaufman RJ. ER stress and its functional link to mitochondria: role in cell survival and death. Cold Spring Harb Perspect Biol. 2011 Sep 1;3:a004424. Pmid:21813400.
   PubMed Web of Science ®Google Scholar
• Tabas I, Ron D. Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat Cell Biol. 2011 Mar;13(3):184–190. Pmid:21364565.
   PubMed Web of Science ®Google Scholar
• Afrazi A, Branca MF, Sodhi CP, et al. Toll-like receptor 4-mediated endoplasmic reticulum stress in intestinal crypts induces necrotizing enterocolitis. J Biol Chem. 2014Apr4;289(14):9584–9599. Pmid:24519940.
   PubMed Web of Science ®Google Scholar
• Orrenius S, Zhivotovsky B, Nicotera P. Regulation of cell death: the calcium–apoptosis link. Nat Rev Mol Cell Biol. 2003 Jul;4(7):552–565. Pmid:12838338.
   PubMed Web of Science ®Google Scholar
• Rutkowski DT, Arnold SM, Miller CN, et al. Adaptation to ER stress is mediated by differential stabilities of pro-survival and pro-apoptotic mRNAs and proteins. PLoS Biol. 2006 Nov 7;4(11):e374. Pmid:17090218.
   PubMed Web of Science ®Google Scholar
• Hetz C. The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Pmid:22251901. Nat Rev Mol Cell Biol. 2012 Feb;13(2):89–102.
   PubMed Web of Science ®Google Scholar
• Szegezdi E, Logue SE, Gorman AM, et al. Mediators of endoplasmic reticulum stress‐induced apoptosis. EMBO Rep. 2006 Sep;7(9):880–885. Pmid:16953201.
   PubMed Web of Science ®Google Scholar
• Ibarra C, Estrada M, Carrasco L, et al. Insulin-like growth factor-1 induces an inositol 1, 4, 5-trisphosphate-dependent increase in nuclear and cytosolic calcium in cultured rat cardiac myocytes. J Biol Chem. 2004 Feb 27;279(9):7554–7565. Pmid:14660553.
   PubMed Web of Science ®Google Scholar
• Chun J, Prince A. Activation of Ca2+-dependent signaling by TLR2. J Immunol. 2006 Jul 15;177:1330–1337. Pmid:16818794.
   PubMed Web of Science ®Google Scholar
• Shelly A, Banerjee C, Saurav GK, et al. Aeromonas hydrophila-induced alterations in cytosolic calcium activate pro-apoptotic cPKC-MEK1/2-tnfα axis in infected head kidney macrophages of Clarias gariepinus. Dev Comp Immunol. 2017 Nov 1;76:392–402. Pmid: 28713009.
   PubMed Web of Science ®Google Scholar
• Clapham DE. Calcium signaling. Cell. 2007 Dec 14;131:1047–1058. Pmid:18083096.
   PubMed Web of Science ®Google Scholar
• Berridge MJ, Bootman MD, Roderick HL. Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol. 2003 Jul;4(7):517–529. Pmid:12838335.
   PubMed Web of Science ®Google Scholar
• Hajnóczky G, Csordás G, Das S, et al. Mitochondrial calcium signalling and cell death: approaches for assessing the role of mitochondrial Ca2+ uptake in apoptosis. Cell Calcium. 2006 Nov 1;40(5–6)553–560. Pmid:17074387.
   PubMed Web of Science ®Google Scholar
• Pinton P, Giorgi C, Siviero R, et al. Calcium and apoptosis: ER-mitochondria Ca 2+ transfer in the control of apoptosis. Oncogene. 2008 Oct;27(50):6407–6418. Pmid:18955969.
   PubMed Web of Science ®Google Scholar
• Banerjee C, Khatri P, Raman R, et al. Role of calmodulin-calmodulin kinase II, camp/protein kinase A and ERK 1/2 on Aeromonas hydrophila-induced apoptosis of head kidney macrophages. PLoS Pathog. 2014 Apr 24;10:e1004018. Pmid:24763432.
   PubMed Web of Science ®Google Scholar
• Rousset S, Emre Y, Join-Lambert O, et al. The uncoupling protein 2 modulates the cytokine balance in innate immunity. Cytokine. 2006 Aug 1;35:135–142. Pmid:16971137.
   PubMed Web of Science ®Google Scholar
• West AP, Shadel GS, Ghosh S. Mitochondria in innate immune responses. Nat Rev Immunol. 2011 Jun;11(6):389–402. Pmid:21597473.
   PubMed Web of Science ®Google Scholar
• Brookes PS, Yoon Y, Robotham JL, et al. Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am J Physiol Cell Physiol. 2004 Oct;287(4):C817–33. Pmid:15355853.
   PubMed Web of Science ®Google Scholar
• Zhang K, Kaufman RJ. From endoplasmic-reticulum stress to the inflammatory response. Nature. 2008 Jul;454(7203):455–462. Pmid:18650916.
   PubMed Web of Science ®Google Scholar
• Tiku V, Tan MW, Dikic I. Mitochondrial functions in infection and immunity. Trends Cell Biol. 2020 Apr 1;30:263–275. Pmid:32200805.
   PubMed Web of Science ®Google Scholar
• Kausar S, Yang L, Abbas MN, et al. Mitochondrial DNA: a key regulator of anti-microbial innate immunity. Genes (Basel). 2020 Jan;111:86. Pmid:31940818.
   PubMed Web of Science ®Google Scholar
• West AP, Shadel GS. Mitochondrial DNA in innate immune responses and inflammatory pathology. Nat Rev Immunol. 2017 Jun;17(6):363. Pmid:28393922.
   PubMed Web of Science ®Google Scholar
• Nakahira K, Haspel JA, Rathinam VA, et al. Autophagy proteins regulate innate immune response by inhibiting NALP3 inflammasome-mediated mitochondrial DNA release. Nat Immunol. 2011 Mar;123:222–230. Pmid:21151103.
   PubMed Web of Science ®Google Scholar
• Bronner DN, O’Riordan MX. A near death experience: shigella manipulates host death machinery to silence innate immunity. EMBO J. 2014 Oct 1;33:2137–2139. Pmid:25180233.
   PubMed Web of Science ®Google Scholar
• Twig G, Hyde B, Shirihai OS. Mitochondrial fusion, fission and autophagy as a quality control axis: the bioenergetic view. Biochim Biophys Acta Bioenerg. 2008 Sep 1;1777:1092–1097. Pmid:18519024.
   PubMed Web of Science ®Google Scholar
• Schroder K, Tschopp J. The inflammasomes. Cell. 2010 Mar 19;140:821–832. Pmid:20303873.
   PubMed Web of Science ®Google Scholar
• López-Castejón G, Sepulcre MP, Mulero I, et al. Molecular and functional characterization of gilthead seabream Sparus aurata caspase-1: the first identification of an inflammatory caspase in fish.Mol Immunol. 2008 Jan 1;45:49–57. Pmid:17610954.
   PubMed Web of Science ®Google Scholar
• Vojtech LN, Scharping N, Woodson JC, et al.Roles of inflammatory caspases during processing of zebrafish interleukin-1β in Francisella noatunensis infection. Infect Immun. 2012 Aug 1;80:2878–2885. Pmid:22689811.
   PubMed Web of Science ®Google Scholar
• Reis MI, Do Vale A, Pereira PJ, et al. Caspase-1 and IL-1β processing in a teleost fish. PLoS One. 2012 Nov 30;7:e50450. Pmid:23336286.
   PubMed Web of Science ®Google Scholar
• Rojas V, Camus‐Guerra H, Guzmán F, et al. Pro‐inflammatory caspase‐1 activation during the immune response in cells from rainbow trout Oncorhynchus mykiss (Walbaum 1792) challenged with pathogen‐associated molecular patterns. J Fish Dis. 2015 Nov;38(11):993–1003. Pmid:25477241.
   PubMed Web of Science ®Google Scholar
• Pancer Z, Cooper MD. The evolution of adaptive immunity. Annu Rev Immunol. 2006 Apr 23;24:497–518. Pmid:16551257.
   PubMed Web of Science ®Google Scholar
• Pan P, Zhang Q, Liu W, et al. Dengue virus infection activates interleukin-1β to induce tissue injury and vascular leakage. Front Microbiol. 2019 Nov 22;10:2637. Pmid:31824450.
   PubMed Web of Science ®Google Scholar
• Krishnan N, Robertson BD, Thwaites G. Pathways of IL-1β secretion by macrophages infected with clinical Mycobacterium tuberculosis strains. Tuberculosis. 2013 Sep 1;93:538–547. Pmid:23849220.
   PubMedGoogle Scholar
• Gov L, Karimzadeh A, Ueno N, et al. Human innate immunity to Toxoplasma gondii is mediated by host caspase-1 and ASC and parasite GRA15. mBio. 2013 Aug 30;4(4). Pmid:23839215.
   PubMed Web of Science ®Google Scholar
• Scapigliati G, Buonocore F, Bird S, et al. Phylogeny of cytokines: molecular cloning and expression analysis of sea bass Dicentrarchus labrax interleukin-1β. Fish Shellfish Immunol. 2001 Nov 1;11(8)711–726. Pmid:11759041.
   PubMed Web of Science ®Google Scholar
• Pelegrın P, Chaves-Pozo E, Mulero V, et al. Production and mechanism of secretion of interleukin-1β from the marine fish gilthead seabream. Dev Comp Immunol. 2004 Mar 1;28:229–237. Pmid:14642889.
   PubMed Web of Science ®Google Scholar
• Wang Y, Wang Q, Baoprasertkul P, et al. Genomic organization, gene duplication, and expression analysis of interleukin-1β in channel catfish (Ictalurus punctatus). Mol Immunol. 2006 Apr 1;43:1653–1664. Pmid:16280165.
   PubMed Web of Science ®Google Scholar
• Seppola M, Larsen AN, Steiro K, et al. Characterisation and expression analysis of the interleukin genes, IL-1β, IL-8 and IL-10, in Atlantic cod (Gadus morhua L.). Mol Immunol. 2008Feb1;45:887–897. Pmid:17875325.
   PubMed Web of Science ®Google Scholar
• Bird S, Wang T, Zou J, et al. The first cytokine sequence within cartilaginous fish: IL-1β in the small spotted catshark (Scyliorhinus canicula). J Immunol. 2002 Apr 1;168:3329–3340. Pmid:11907090.
   PubMed Web of Science ®Google Scholar
• Ogryzko NV, Renshaw SA, Wilson HL. The IL-1 family in fish: swimming through the muddy waters of inflammasome evolution.Dev Comp Immunol. 2014 Sep 1;46:53–62. Pmid:24690566.
   PubMed Web of Science ®Google Scholar
• Gräb J, Rybniker J. The expanding role of p38 mitogen-activated protein kinase in programmed host cell death. Microbiol Insights. 2019 Jul;12:1178636119864594. Pmid:31384128.
   Google Scholar
• Dhanasekaran DN, Reddy EP. JNK signaling in apoptosis. Oncogene. 2008 Oct 20;27(48):6245–6251. Pmid: 18931691.
   PubMed Web of Science ®Google Scholar
• Dunn JD, Alvarez LA, Zhang X, et al. Reactive oxygen species and mitochondria: a nexus of cellular homeostasis. Redox Biol. 2015 Dec 1;6:472–485. Pmid: 26432659.
   PubMed Web of Science ®Google Scholar
• Stocks CJ, Schembri MA, Sweet MJ, et al.For when bacterial infections persist: toll‐like receptor‐inducible direct antimicrobial pathways in macrophages. J Leukoc Biol. 2018 Jan 2;103:35–51. Pmid: 29345056.
   PubMed Web of Science ®Google Scholar
• Ahmad T, Aggarwal K, Pattnaik B, et al. Computational classification of mitochondrial shapes reflects stress and redox state. Cell Death Dis. 2013 Jan 17;4(1)e461–e. Pmid: 23328668.
   PubMedGoogle Scholar
• Ligon LA, Steward O. Role of microtubules and actin filaments in the movement of mitochondria in the axons and dendrites of cultured hippocampal neurons.J Comp Neurol.2000 Nov 20;427:351–361. Pmid:11054698.
   PubMed Web of Science ®Google Scholar
• Rizzuto R, Pozzan T. Microdomains of intracellular Ca2+: molecular determinants and functional consequences. Physiol Rev. 2006 Jan;86(1):369–408. Pmid: 16371601.
   PubMed Web of Science ®Google Scholar
• Kim KH, Park JY, Jung HJ, et al.Identification and biological activities of a new antiangiogenic small molecule that suppresses mitochondrial reactive oxygen species. Biochem Biophys Res Commun. 2011 Jan 7;404:541–545. Pmid: 21144820.
   PubMed Web of Science ®Google Scholar
• Han C, Li Q, Xu J, et al. Characterization of Clarias gariepinus mitochondrial genome sequence and a comparative analysis with other catfishes. Biologia. 2015 Sep;70(9):1245–1253.
   Web of Science ®Google Scholar
• Kumar M, Kumar J, Sharma S, et al. TLR22-mediated activation of TNF-α-caspase-1/IL-1β inflammatory axis leads to apoptosis of Aeromonas hydrophila-infected macrophages. Mol Immunol. 2021 Sep 1;137:114–123. Pmid: 34242920.
   PubMed Web of Science ®Google Scholar
• Medel-Matus JS, Álvarez-Croda DM, Martínez-Quiroz J, et al. IL-1β increases necrotic neuronal cell death in the developing rat hippocampus after status epilepticus by activating type I IL-1 receptor (IL-1RI). Int J Dev Neurosci. 2014 Nov 1;38:232–240. Pmid:25449684.
   PubMed Web of Science ®Google Scholar
• Shen J, Xu S, Zhou H, et al. IL-1β induces apoptosis and autophagy via mitochondria pathway in human degenerative nucleus pulposus cells. Sci Rep. 2017 Jan 25;7(1):1–2. Pmid: 28120948.
   PubMedGoogle Scholar
• Zaitsev SV, Appelskog IB, Kapelioukh IL, et al. Imidazoline compounds protect against interleukin 1beta-induced beta-cell apoptosis. Diabetes. 2001 Feb 1;50(suppl 1):S70. Pmid:11272206.
   PubMedGoogle Scholar
• Størling J, Binzer J, Andersson AK, et al. Nitric oxide contributes to cytokine-induced apoptosis in pancreatic beta cells via potentiation of JNK activity and inhibition of Akt. Diabetologia. 2005 Oct;4810:2039–2050. Pmid: 16132952.
   PubMed Web of Science ®Google Scholar
• Magnadóttir B. Innate immunity of fish (overview). Fish Shellfish Immunol. 2006 Feb 1;20:137–151. Pmid:15950491.
   PubMed Web of Science ®Google Scholar
• Wiles TJ, Dhakal BK, Eto DS, et al. Inactivation of host Akt/protein kinase B signaling by bacterial pore-forming toxins. Pmid:18234841. Mol Biol Cell. 2008 Apr;19(4):1427–1438.
   PubMed Web of Science ®Google Scholar
• de Frias M, Iglesias-Serret D, Cosialls AM, et al. Akt inhibitors induce apoptosis in chronic lymphocytic leukemia cells. Haematologica. 2009 Dec;9412:1698–1707. Pmid:19815839.
   PubMed Web of Science ®Google Scholar
• Hu H, Tian M, Ding C, et al. The C/EBP homologous protein (CHOP) transcription factor functions in endoplasmic reticulum stress-induced apoptosis and microbial infection. Front Immunol. 2019 Jan 4;9:3083. Pmid:30662442.
   PubMed Web of Science ®Google Scholar
• Li Y, Jiang W, Niu Q, et al. eIF2α-CHOP-BCl-2/JNK and IRE1α-XBP1/JNK signaling promote apoptosis and inflammation and support the proliferation of Newcastle disease virus. Cell Death Dis. 2019 Nov 26;10(12)1–5. Pmid:31767828.
   Google Scholar
• Delierneux C, Kouba S, Shanmughapriya S, et al. Mitochondrial calcium regulation of redox signaling in cancer.Cells. 2020 Feb 12;9:432. Pmid:32059571.
   PubMed Web of Science ®Google Scholar
• Hayashi-Nishino M, Fujita N, Noda T, et al. A subdomain of the endoplasmic reticulum forms a cradle for autophagosome formation. Nat Cell Biol. 2009 Dec;11(12):1433–1437. Pmid:19898463.
   PubMed Web of Science ®Google Scholar
• Pinegin B, Vorobjeva N, Pashenkov M, et al. The role of mitochondrial ROS in antibacterial immunity. J Cell Physiol. 2018 May;233(5):3745–3754. Pmid:28771715.
   PubMed Web of Science ®Google Scholar
• Wang J, Toan S, Zhou H. New insights into the role of mitochondria in cardiac microvascular ischemia/reperfusion injury. Pmid:32246225. Angiogenesis. 2020 Aug;23(3):299–314.
   PubMed Web of Science ®Google Scholar
• Marchi S, Pinton P. Alterations of calcium homeostasis in cancer cells. Curr Opin Pharmacol. 2016 Aug 1;29:1–6. Pmid:27043073.
   PubMed Web of Science ®Google Scholar
• Missiroli S, Patergnani S, Caroccia N, et al. Mitochondria-associated membranes (MAMs) and inflammation. Cell Death Dis. 2018 Feb 28;9(3)1–4. Pmid:29491386.
   PubMedGoogle Scholar
• Scheibye-Knudsen M, Fang EF, Croteau DL, et al.Protecting the mitochondrial powerhouse.Trends Cell Biol.2015 Mar 1;25:158–170. Pmid:25499735.
   PubMed Web of Science ®Google Scholar
• West AP, Khoury-Hanold W, Staron M, et al. Mitochondrial DNA stress primes the antiviral innate immune response. Nature. 2015 Apr 23;520(7548):553–557. Pmid:25642965.
   PubMed Web of Science ®Google Scholar
• Kanneganti TD, Kundu M, Green DR. Innate immune recognition of mtDNA—an undercover signal?Cell Metab. 2015 Jun 2;21:793–794. Pmid:26039443.
   PubMed Web of Science ®Google Scholar
• Boyapati RK, Tamborska A, Dorward DA, et al. Advances in the understanding of mitochondrial DNA as a pathogenic factor in inflammatory diseases. F1000Res. 2017 Feb 20;6:169. Pmid:28299196.
   PubMedGoogle Scholar
• Glick D, Barth S, Macleod KF. Autophagy: cellular and molecular mechanisms. J Pathol. 2010 May;221(1):3–12. Pmid:20225336.
   PubMed Web of Science ®Google Scholar
• Zhu H, Toan S, Mui D, et al. Mitochondrial quality surveillance as a therapeutic target in myocardial infarction. Acta Physiol. 2021 Mar;231(3):e13590. Pmid:33270362.
   PubMed Web of Science ®Google Scholar
• Deretic V. Autophagy: an emerging immunological paradigm.J Immunol. 2012 Jul 1;189:15–20. Pmid:22723639.
   PubMed Web of Science ®Google Scholar
• Sorbara MT, Girardin SE. Mitochondrial ROS fuel the inflammasome. Cell Res. 2011 Apr;21(4):558–560. Pmid:21283134.
   PubMed Web of Science ®Google Scholar
• Zhou H, Zhu P, Wang J, et al. DNA-PKcs promotes alcohol-related liver disease by activating Drp1-related mitochondrial fission and repressing FUNDC1-required mitophagy. Signal Transduct Target Ther. 2019 Dec 6;4:56. Pmid: 31839999.
   PubMed Web of Science ®Google Scholar
• Naik E, Dixit VM. Mitochondrial reactive oxygen species drive proinflammatory cytokine production. J Exp Med. 2011 Mar 14;208:417–420. Pmid:21357740.
   PubMed Web of Science ®Google Scholar
• McCoy AJ, Koizumi Y, Higa N, et al.Differential regulation of caspase-1 activation via NLRP3/NLRC4 inflammasomes mediated by aerolysin and type III secretion system during Aeromonas veronii infection.J Immunol. 2010 Dec 1;185:7077–7084. Pmid:21037094.
   PubMed Web of Science ®Google Scholar
• Fernandes-Alnemri T, Yu JW, Juliana C, et al. The AIM2 inflammasome is critical for innate immunity to Francisella tularensis. Nat Immunol. 2010 May;115:385–393. Pmid:20351693.
   PubMed Web of Science ®Google Scholar
• Rathinam VA, Jiang Z, Waggoner SN, et al. The AIM2 inflammasome is essential for host defense against cytosolic bacteria and DNA viruses. Nat Immunol. 2010 May;115:395–402. Pmid:20351692.
   PubMed Web of Science ®Google Scholar
• Pereira CA, Carlos D, Ferreira NS, et al. Mitochondrial DNA promotes NLRP3 inflammasome activation and contributes to endothelial dysfunction and inflammation in type 1 diabetes. Front Physiol. 2020 Jan 17;10:1557. Pmid:32009974.
   PubMed Web of Science ®Google Scholar
• Franchi L, Eigenbrod T, Muñoz-Planillo R, et al. The inflammasome: a caspase-1-activation platform that regulates immune responses and disease pathogenesis. Nat Immunol. 2009 Mar;10(3):241–247. Pmid:19221555.
   PubMed Web of Science ®Google Scholar
• Wang J, Zhu P, Li R, et al. Fundc1-dependent mitophagy is obligatory to ischemic preconditioning-conferred renoprotection in ischemic AKI via suppression of Drp1-mediated mitochondrial fission. Redox Biol. 2020 Feb;30:101415. Pmid: 31901590.
   PubMed Web of Science ®Google Scholar