133
Views
12
CrossRef citations to date
0
Altmetric
Original Research

A Comparison Between 1 Day versus 7 Days of Sepsis in Mice with the Experiments on LPS-Activated Macrophages Support the Use of Intravenous Immunoglobulin for Sepsis Attenuation

, , , , &
Pages 7243-7263 | Published online: 22 Dec 2021

References

  • Singer M, Deutschman CS, Seymour CW, et al. The third international consensus definitions for sepsis and septic shock (Sepsis-3). JAMA. 2016;315(8):801–810. doi:10.1001/jama.2016.0287
  • Dang CP, Issara-Amphorn J, Charoensappakit A, et al. BAM15, a mitochondrial uncoupling agent, attenuates inflammation in the LPS injection mouse model: an adjunctive anti-inflammation on macrophages and hepatocytes. J Innate Immun. 2021;13(6):359–375. doi:10.1159/000516348
  • Dang CP, Leelahavanichkul A. Over-expression of miR-223 induces M2 macrophage through glycolysis alteration and attenuates LPS-induced sepsis mouse model, the cell-based therapy in sepsis. PLoS One. 2020;15(7):e0236038. doi:10.1371/journal.pone.0236038
  • Nedeva C, Menassa J, Puthalakath H. Sepsis: inflammation is a necessary evil. Front Cell Dev Biol. 2019;7:108. doi:10.3389/fcell.2019.00108
  • Drewry AM, Ablordeppey EA, Murray ET, et al. Monocyte function and clinical outcomes in febrile and afebrile patients with severe sepsis. Shock. 2018;50(4):381–387. doi:10.1097/SHK.0000000000001083
  • Murray PJ. Macrophage Polarization. Annu Rev Physiol. 2017;79(1):541–566. doi:10.1146/annurev-physiol-022516-034339
  • Taratummarat S, Sangphech N, Vu CTB, et al. Gold nanoparticles attenuates bacterial sepsis in cecal ligation and puncture mouse model through the induction of M2 macrophage polarization. BMC Microbiol. 2018;18(1):85. doi:10.1186/s12866-018-1227-3
  • Hotchkiss RS, Opal SM. Activating immunity to fight a foe — a new path. N Eng J Med. 2020;382(13):1270–1272. doi:10.1056/NEJMcibr1917242
  • Hamidzadeh K, Christensen SM, Dalby E, Chandrasekaran P, Mosser DM. Macrophages and the recovery from acute and chronic inflammation. Annu Rev Physiol. 2017;79(1):567–592. doi:10.1146/annurev-physiol-022516-034348
  • Palm NW, Medzhitov R. Not so fast: adaptive suppression of innate immunity. Nat Med. 2007;13(10):1142–1144. doi:10.1038/nm1007-1142b
  • Shanker A. Adaptive control of innate immunity. Immunol Lett. 2010;131(2):107–112. doi:10.1016/j.imlet.2010.04.002
  • Sae-Khow K, Charoensappakit A, Visitchanakun P, et al. Pathogen-associated molecules from gut translocation enhance severity of cecal ligation and puncture sepsis in iron-overload β-thalassemia mice. J Inflamm Res. 2020;13:719–735. doi:10.2147/JIR.S273329
  • Panpetch W, Sawaswong V, Chanchaem P, et al. Candida administration worsens cecal ligation and puncture-induced sepsis in obese mice through gut dysbiosis enhanced systemic inflammation, impact of pathogen-associated molecules from gut translocation and saturated fatty acid. Front Immunol. 2020;11:561652. doi:10.3389/fimmu.2020.561652
  • Issara-Amphorn J, Chancharoenthana W, Visitchanakun P, Leelahavanichkul A. Syk inhibitor attenuates polymicrobial sepsis in fcgriib-deficient lupus mouse model, the impact of lupus characteristics in sepsis. J Innate Immun. 2020;12(6):461–479. doi:10.1159/000509111
  • Visitchanakun P, Tangtanatakul P, Trithiphen O, et al. Plasma miR-370-3P as a biomarker of sepsis-associated encephalopathy, the transcriptomic profiling analysis of microRNA-arrays from mouse brains. Shock. 2020;54:3. doi:10.1097/SHK.0000000000001473
  • Surawut S, Makjaroen J, Thim-uam A, et al. Increased susceptibility against Cryptococcus neoformans of lupus mouse models (pristane-induction and FcGRIIb deficiency) is associated with activated macrophage, regardless of genetic background. J Microbiol. 2019;57(1):45–53. doi:10.1007/s12275-019-8311-8
  • Thim-uam A, Surawut S, Issara-Amphorn J, et al. Leaky-gut enhanced lupus progression in the Fc gamma receptor-IIb deficient and pristane-induced mouse models of lupus. Sci Rep. 2020;10(1):777. doi:10.1038/s41598-019-57275-0
  • Visitchanakun P, Saisorn W, Wongphoom J, et al. Gut leakage enhances sepsis susceptibility in iron-overloaded β-thalassemia mice through macrophage hyperinflammatory responses. Am J Physiol Gastrointestinal Liver Physiol. 2020;318(5):G966–G979. doi:10.1152/ajpgi.00337.2019
  • Leelahavanichkul A, Yasuda H, Doi K, et al. Methyl-2-acetamidoacrylate, an ethyl pyruvate analog, decreases sepsis-induced acute kidney injury in mice. Am J Physiol Renal Physiol. 2008;295(6):F1825–F1835. doi:10.1152/ajprenal.90442.2008
  • Jaroonwitchawan T, Visitchanakun P, Dang PC, Ritprajak P, Palaga T, Leelahavanichkul A. Dysregulation of Lipid Metabolism in Macrophages Is Responsible for Severe Endotoxin Tolerance in FcgRIIB-Deficient Lupus Mice. Front Immunol. 2020;11:959. doi:10.3389/fimmu.2020.00959
  • Yang D, Elner SG, Bian Z-M, Till GO, Petty HR, Elner VM. Pro-inflammatory cytokines increase reactive oxygen species through mitochondria and NADPH oxidase in cultured RPE cells. Exp Eye Res. 2007;85(4):462–472. doi:10.1016/j.exer.2007.06.013
  • Hsu H-Y, Wen M-H. Lipopolysaccharide-mediated reactive oxygen species and signal transduction in the regulation of interleukin-1 gene expression. J Biol Chem. 2002;277(25):22131–22139. doi:10.1074/jbc.M111883200
  • Bhunyakarnjanarat T, Udompornpitak K, Saisorn W, et al. Prominent indomethacin-induced enteropathy in fcgriib deficient lupus mice: an impact of macrophage responses and immune deposition in gut. Int J Mol Sci. 2021;22(3):1377. doi:10.3390/ijms22031377
  • Saisorn W, Saithong S, Phuengmaung P, et al. Acute kidney injury induced lupus exacerbation through the enhanced neutrophil extracellular traps (and apoptosis) in Fcgr2b deficient lupus mice with renal ischemia reperfusion injury. Front Immunol. 2021;12:2336. doi:10.3389/fimmu.2021.669162
  • Boes M, Prodeus AP, Schmidt T, Carroll MC, Chen J, Critical A. Role of natural immunoglobulin M in immediate defense against systemic bacterial infection. J Exp Med. 1998;188(12):2381–2386. doi:10.1084/jem.188.12.2381
  • Bournazos S, Ravetch JV. Fcγ receptor function and the design of vaccination strategies. Immunity. 2017;47(2):224–233. doi:10.1016/j.immuni.2017.07.009
  • Kozicky LK, Zhao ZY, Menzies SC, et al. Intravenous immunoglobulin skews macrophages to an anti-inflammatory, IL-10-producing activation state. J Leukoc Biol. 2015;98(6):983–994. doi:10.1189/jlb.3VMA0315-078R
  • Akyol GY, Manaenko A, Akyol O, et al. IVIG activates FcγRIIB-SHIP1-PIP3 pathway to stabilize mast cells and suppress inflammation after ICH in mice. Sci Rep. 2017;7(1):15583. doi:10.1038/s41598-017-15455-w
  • Voigt A, Rahnefeld A, Kloetzel P, Krüger E. Cytokine-induced oxidative stress in cardiac inflammation and heart failure—how the ubiquitin proteasome system targets this vicious cycle. Front Physiol. 2013;4(42). doi:10.3389/fphys.2013.00042
  • Mittal M, Siddiqui MR, Tran K, Reddy SP, Malik AB. Reactive oxygen species in inflammation and tissue injury. Antioxid Redox Signal. 2014;20(7):1126–1167. doi:10.1089/ars.2012.5149
  • Alejandria MM, Lansang MAD, Dans LF, Mantaring Iii JB. Intravenous immunoglobulin for treating sepsis, severe sepsis and septic shock. Cochrane Database Sys Rev. 2013;(9). doi:10.1002/14651858.CD001090.pub2.
  • Yang Y, Yu X, Zhang F, Xia Y. Evaluation of the effect of intravenous immunoglobulin dosing on mortality in patients with sepsis: a network meta-analysis. Clin Ther. 2019;41(9):1823–1838.e1824. doi:10.1016/j.clinthera.2019.06.010
  • Ozcan PE, Senturk E, Orhun G, et al. Effects of intravenous immunoglobulin therapy on behavior deficits and functions in sepsis model. Ann Intensive Care. 2015;5(1):62. doi:10.1186/s13613-015-0062-z
  • Esen F, Orhun G, Ozcan PE, et al. Neuroprotective effects of intravenous immunoglobulin are mediated through inhibition of complement activation and apoptosis in a rat model of sepsis. Intensive Care Med Exp. 2017;5(1):1. doi:10.1186/s40635-016-0114-1
  • St-Amour I, Bousquet M, Paré I, et al. Impact of intravenous immunoglobulin on the dopaminergic system and immune response in the acute MPTP mouse model of Parkinson’s disease. J Neuroinflammation. 2012;9(1):234. doi:10.1186/1742-2094-9-234
  • Puli L, Pomeshchik Y, Olas K, Malm T, Koistinaho J, Tanila H. Effects of human intravenous immunoglobulin on amyloid pathology and neuroinflammation in a mouse model of Alzheimer’s disease. J Neuroinflammation. 2012;9(1):105. doi:10.1186/1742-2094-9-105
  • Magga J, Puli L, Pihlaja R, et al. Human intravenous immunoglobulin provides protection against Aβ toxicity by multiple mechanisms in a mouse model of Alzheimer’s disease. J Neuroinflammation. 2010;7(1):90. doi:10.1186/1742-2094-7-90
  • Leontyev D, Katsman Y, Branch DR. Mouse background and IVIG dosage are critical in establishing the role of inhibitory Fcγ receptor for the amelioration of experimental ITP. Blood. 2012;119(22):5261–5264. doi:10.1182/blood-2012-03-415695
  • Thomson C, Wang Y, Jackson L, et al. Pandemic H1N1 influenza infection and vaccination in humans induces cross-protective antibodies that target the hemagglutinin stem. Front Immunol. 2012;3:87. doi:10.3389/fimmu.2012.00087
  • Leelahavanichkul A, Worasilchai N, Wannalerdsakun S, et al. Gastrointestinal leakage detected by serum (1→3)-β-D-glucan in mouse models and a pilot study in patients with sepsis. Shock. 2016;46(5):506–518. doi:10.1097/SHK.0000000000000645
  • Issara-Amphorn J, Dang CP, Saisorn W, Limbutara K, Leelahavanichkul A. Candida administration in bilateral nephrectomy mice elevates serum (1→3)-β-D-glucan that enhances systemic inflammation through energy augmentation in macrophages. Int J Mol Sci. 2021;22(9):5031. doi:10.3390/ijms22095031
  • Munshi HG, Montgomery RB. Severe neutropenia: a diagnostic approach. West J Med. 2000;172(4):248–252. doi:10.1136/ewjm.172.4.248
  • Cao C, Yu M, Chai Y. Pathological alteration and therapeutic implications of sepsis-induced immune cell apoptosis. Cell Death Dis. 2019;10(10):782. doi:10.1038/s41419-019-2015-1
  • Stebegg M, Kumar SD, Silva-Cayetano A, Fonseca VR, Linterman MA, Graca L. Regulation of the germinal center response. Front Immunol. 2018;9:2469. doi:10.3389/fimmu.2018.02469
  • Kotas ME, Matthay MA. Mesenchymal stromal cells and macrophages in sepsis: new insights. Eur Respir J. 2018;51(4):1800510. doi:10.1183/13993003.00510-2018
  • Qiu P, Liu Y, Zhang J. Review: the role and mechanisms of macrophage autophagy in sepsis. Inflammation. 2019;42(1):6–19. doi:10.1007/s10753-018-0890-8
  • Mallat J, Leone S, Cascella M, Fiore M. Should endotoxin be a research priority in Gram-negative sepsis and septic shock? Expert Rev Clin Pharmacol. 2019;12(8):697–699. doi:10.1080/17512433.2019.1627871
  • Amornphimoltham P, Yuen PST, Star RA, Leelahavanichkul A. Gut leakage of fungal-derived inflammatory mediators: part of a gut-liver-kidney axis in bacterial sepsis. Dig Dis Sci. 2019;64(9):2416–2428. doi:10.1007/s10620-019-05581-y
  • Ptak W, Paliwal V, Bryniarski K. Aggregated immunoglobulin protects immune T cells from suppression: dependence on isotype, Fc portion, and macrophage FcγR. Scand J Immunol. 1998;47(2):136–145. doi:10.1046/j.1365-3083.1998.00264.x
  • Ben Mkaddem S, Benhamou M, Monteiro RC. Understanding Fc receptor involvement in inflammatory diseases: from mechanisms to new therapeutic tools. Front Immunol. 2019;10:811. doi:10.3389/fimmu.2019.00811
  • Morgan MJ, Liu Z-G. Crosstalk of reactive oxygen species and NF-κB signaling. Cell Res. 2011;21(1):103–115. doi:10.1038/cr.2010.178
  • Lingappan K. NF-κB in oxidative stress. Curr Opin Toxicol. 2018;7:81–86. doi:10.1016/j.cotox.2017.11.002
  • Herb M, Schramm M. Functions of ROS in macrophages and antimicrobial immunity. Antioxidants. 2021;10(2):313. doi:10.3390/antiox10020313
  • Fang FC. Antimicrobial actions of reactive oxygen species. mBio. 2011;2(5). doi:10.1128/mBio.00141-11
  • Meng T-C, Fukada T, Tonks NK. Reversible oxidation and inactivation of protein tyrosine phosphatases in vivo. Mol Cell. 2002;9(2):387–399. doi:10.1016/S1097-2765(02)00445-8
  • Victor MV, Juan VE, Antonio H-M, Milagros R. Oxidative stress and mitochondrial dysfunction in sepsis: a potential therapy with mitochondria-targeted antioxidants. Infect Disorders Drug Targets. 2009;9(4):376–389. doi:10.2174/187152609788922519
  • Quinlan CL, Orr AL, Perevoshchikova IV, Treberg JR, Ackrell BA, Brand MD. Mitochondrial complex II can generate reactive oxygen species at high rates in both the forward and reverse reactions. J Biol Chem. 2012;287(32):27255–27264. doi:10.1074/jbc.M112.374629
  • Acín-Pérez R, Carrascoso I, Baixauli F, et al. ROS-triggered phosphorylation of complex ii by Fgr kinase regulates cellular adaptation to fuel use. Cell Metab. 2014;19(6):1020–1033. doi:10.1016/j.cmet.2014.04.015
  • Ruttkay-Nedecky B, Nejdl L, Gumulec J, et al. The role of metallothionein in oxidative stress. Int J Mol Sci. 2013;14(3). doi:10.3390/ijms14036044.
  • Song J, Park DW, Moon S, et al. Diagnostic and prognostic value of interleukin-6, pentraxin 3, and procalcitonin levels among sepsis and septic shock patients: a prospective controlled study according to the Sepsis-3 definitions. BMC Infect Dis. 2019;19(1):968. doi:10.1186/s12879-019-4618-7
  • Venet F, Monneret G. Advances in the understanding and treatment of sepsis-induced immunosuppression. Nat Rev Nephrol. 2018;14(2):121–137. doi:10.1038/nrneph.2017.165
  • Chen R, Zhou L. PD-1 signaling pathway in sepsis: does it have a future? Clin Immunol. 2021;229:108742. doi:10.1016/j.clim.2021.108742
  • Vu CTB, Thammahong A, Leelahavanichkul A, Ritprajak P. Alteration of macrophage immune phenotype in a murine sepsis model is associated with susceptibility to secondary fungal infection. Asian Pac J Allergy Immunol. 2019. doi:10.12932/AP-170519-0565
  • Ondee T, Jaroonwitchawan T, Pisitkun T, et al. Decreased protein kinase C-β Type II associated with the prominent endotoxin exhaustion in the macrophage of FcGRIIb−/− Lupus prone mice is revealed by phosphoproteomic analysis. Int J Mol Sci. 2019;20(6):1354. doi:10.3390/ijms20061354
  • Martin MD, Badovinac VP, Griffith TS. CD4 T cell responses and the sepsis-induced immunoparalysis state. Front Immunol. 2020;11:1364. doi:10.3389/fimmu.2020.01364
  • Wu -D-D, Li T, Ji X-Y. Dendritic cells in sepsis: pathological alterations and therapeutic implications. J Immunol Res. 2017;2017:3591248. doi:10.1155/2017/3591248
  • Bouras M, Asehnoune K, Roquilly A. Contribution of dendritic cell responses to sepsis-induced immunosuppression and to susceptibility to secondary pneumonia. Front Immunol. 2018;9(2590):548. doi:10.3389/fimmu.2018.02590