Abstract
Sepsis, which is a highly heterogeneous syndrome, can result in death as a consequence of a systemic inflammatory response syndrome. The activation and regulation of the immune system play a key role in the initiation, development and prognosis of sepsis. Due to the different periods of sepsis when the objects investigated were incorporated, clinical trials often exhibit negative or even contrary results. Thus, in this review we aim to sort out the current knowledge in how immune cells play a role during sepsis.
Keywords: Sepsis, innate immunity, adaptive immunity, inflammation, protein, immune system.
Graphical Abstract
[1]
Singer, M.; Deutschman, C.S.; Seymour, C.W.; Shankar-Hari, M.; Annane, D.; Bauer, M.; Bellomo, R.; Bernard, G.R.; Chiche, J.D.; Coopersmith, C.M.; Hotchkiss, R.S.; Levy, M.M.; Marshall, J.C.; Martin, G.S.; Opal, S.M.; Rubenfeld, G.D.; van der Poll, T.; Vincent, J.L.; Angus, D.C. The third international consensus definitions for sepsis and septic shock (Sepsis-3). JAMA, 2016, 315(8), 801-810.
[2]
Delano, M.J.; Ward, P.A. The immune system’s role in sepsis progression, resolution, and long-term outcome. Immunol. Rev., 2016, 274(1), 330-353.
[3]
Goodwin, A.J.; Rice, D.A.; Simpson, K.N.; Ford, D.W. Frequency, cost, and risk factors of readmissions among severe sepsis survivors. Crit. Care Med., 2015, 43(4), 738-746.
[4]
Xu, P.B.; Lou, J.S.; Ren, Y.; Miao, C.H.; Deng, X.M. Gene expression profiling reveals the defining features of monocytes from septic patients with compensatory anti-inflammatory response syndrome. J. Infect., 2012, 65(5), 380-391.
[5]
Unsinger, J.; Kazama, H.; McDonough, J.S.; Hotchkiss, R.S.; Ferguson, T.A. Differential lymphopenia-induced homeostatic proliferation for CD4+ and CD8+ T cells following septic injury. J. Leukoc. Biol., 2009, 85(3), 382-390.
[6]
Benjamim, C.F.; Hogaboam, C.M.; Kunkel, S.L. The chronic consequences of severe sepsis. J. Leukoc. Biol., 2004, 75(3), 408-412.
[7]
Benjamim, C.F.; Ferreira, S.H.; Cunha, F.Q. Role of nitric oxide in the failure of neutrophil migration in sepsis. J. Infect. Dis., 2000, 182(1), 214-223.
[8]
Alves-Filho, J.C.; Freitas, A.; Souto, F.O.; Spiller, F.; Paula-Neto, H.; Silva, J.S.; Gazzinelli, R.T.; Teixeira, M.M.; Ferreira, S.H.; Cunha, F.Q. Regulation of chemokine receptor by Toll-like receptor 2 is critical to neutrophil migration and resistance to polymicrobial sepsis. Proc. Natl. Acad. Sci. USA, 2009, 106(10), 4018-4023.
[9]
Deering, R.P.; Orange, J.S. Development of a clinical assay to evaluate toll-like receptor function. Clin. Vaccine Immunol., 2006, 13(1), 68-76.
[10]
Sakai, K.; Suzuki, H.; Oda, H.; Akaike, T.; Azuma, Y.; Murakami, T.; Sugi, K.; Ito, T.; Ichinose, H.; Koyasu, S.; Shirai, M. Phosphoinositide 3-kinase in nitric oxide synthesis in macrophage: Critical dimerization of inducible nitric-oxide synthase. J. Biol. Chem., 2006, 281(26), 17736-17742.
[11]
Dal Secco, D.; Moreira, A.P.; Freitas, A.; Silva, J.S.; Rossi, M.A.; Ferreira, S.H.; Cunha, F.Q. Nitric oxide inhibits neutrophil migration by a mechanism dependent on ICAM-1: Role of soluble guanylate cyclase. Nitric Oxide Biol. Chem., 2006, 15(1), 77-86.
[12]
Evron, T.; Daigle, T.L.; Caron, M.G. GRK2: Multiple roles beyond G protein-coupled receptor desensitization. Trends Pharmacol. Sci., 2012, 33(3), 154-164.
[13]
Khandaker, M.H.; Xu, L.; Rahimpour, R.; Mitchell, G.; DeVries, M.E.; Pickering, J.G.; Singhal, S.K.; Feldman, R.D.; Kelvin, D.J. CXCR1 and CXCR2 are rapidly down-modulated by bacterial endotoxin
through a unique agonist-independent, tyrosine kinasedependent
mechanism. J. Immunol., (Baltimore, Md.: 1950), 1998, 161(4), 1930-1938.
[14]
Benjamim, C.F.; Silva, J.S.; Fortes, Z.B.; Oliveira, M.A.; Ferreira, S.H.; Cunha, F.Q. Inhibition of leukocyte rolling by nitric oxide during sepsis leads to reduced migration of active microbicidal neutrophils. Infect. Immun., 2002, 70(7), 3602-3610.
[15]
Paula-Neto, H.A.; Alves-Filho, J.C.; Souto, F.O.; Spiller, F.; Amendola, R.S.; Freitas, A.; Cunha, F.Q.; Barja-Fidalgo, C. Inhibition of guanylyl cyclase restores neutrophil migration and maintains bactericidal activity increasing survival in sepsis. Shock (Augusta, Ga.), 2011, 35(1), 17-27.
[16]
Arraes, S.M.; Freitas, M.S.; da Silva, S.V.; de Paula Neto, H.A.; Alves-Filho, J.C.; Auxiliadora Martins, M.; Basile-Filho, A.; Tavares-Murta, B.M.; Barja-Fidalgo, C.; Cunha, F.Q. Impaired neutrophil chemotaxis in sepsis associates with GRK expression and inhibition of actin assembly and tyrosine phosphorylation. Blood, 2006, 108(9), 2906-2913.
[17]
Tavares-Murta, B.M.; Zaparoli, M.; Ferreira, R.B.; Silva-Vergara, M.L.; Oliveira, C.H.; Murta, E.F.; Ferreira, S.H.; Cunha, F.Q. Failure of neutrophil chemotactic function in septic patients. Crit. Care Med., 2002, 30(5), 1056-1061.
[18]
O'Brien, A.D.; Rosenstreich, D.L.; Scher, I.; Campbell, G.H.; MacDermott, R.P.; Formal, S.B. Genetic control of susceptibility to
Salmonella typhimurium in mice: Role of the LPS gene. J. Immunol.,
(Baltimore, Md. : 1950), 1980, 124(1), 20-24.
[19]
Alves-Filho, J.C.; de Freitas, A.; Russo, M.; Cunha, F.Q. Toll-like receptor 4 signaling leads to neutrophil migration impairment in polymicrobial sepsis. Crit. Care Med., 2006, 34(2), 461-470.
[20]
Opal, S.M.; Laterre, P.F.; Francois, B.; LaRosa, S.P.; Angus, D.C.; Mira, J.P.; Wittebole, X.; Dugernier, T.; Perrotin, D.; Tidswell, M.; Jauregui, L.; Krell, K.; Pachl, J.; Takahashi, T.; Peckelsen, C.; Cordasco, E.; Chang, C.S.; Oeyen, S.; Aikawa, N.; Maruyama, T.; Schein, R.; Kalil, A.C.; Van Nuffelen, M.; Lynn, M.; Rossignol, D.P.; Gogate, J.; Roberts, M.B.; Wheeler, J.L.; Vincent, J.L. Effect of eritoran, an antagonist of MD2-TLR4, on mortality in patients with severe sepsis: The ACCESS randomized trial. JAMA, 2013, 309(11), 1154-1162.
[21]
Klesius, P.H.; Chambers, W.H.; Schultz, R.D. Effect of bacterial lipopolysaccharide on bovine polymorphonuclear neutrophil migration in vitro. Vet. Immunol. Immunopathol., 1984, 7(3-4), 239-244.
[22]
Rios-Santos, F.; Alves-Filho, J.C.; Souto, F.O.; Spiller, F.; Freitas, A.; Lotufo, C.M.; Soares, M.B.; Dos Santos, R.R.; Teixeira, M.M.; Cunha, F.Q. Down-regulation of CXCR2 on neutrophils in severe sepsis is mediated by inducible nitric oxide synthase-derived nitric oxide. Am. J. Respir. Crit. Care Med., 2007, 175(5), 490-497.
[23]
Alves-Filho, J.C.; Sonego, F.; Souto, F.O.; Freitas, A.; Verri, W.A., Jr; Auxiliadora-Martins, M.; Basile-Filho, A.; McKenzie, A.N.; Xu, D.; Cunha, F.Q.; Liew, F.Y. Interleukin-33 attenuates sepsis by enhancing neutrophil influx to the site of infection. Nat. Med., 2010, 16(6), 708-712.
[24]
Cummings, C.J.; Martin, T.R.; Frevert, C.W.; Quan, J.M.; Wong, V.A.; Mongovin, S.M.; Hagen, T.R.; Steinberg, K.P.; Goodman, R.B. Expression and function of the chemokine receptors CXCR1 and CXCR2 in sepsis. J. Immunol., (Baltimore, Md. : 1950),, 1999, 162(4), 2341-2346.
[25]
Drifte, G.; Dunn-Siegrist, I.; Tissieres, P.; Pugin, J. Innate immune functions of immature neutrophils in patients with sepsis and severe systemic inflammatory response syndrome. Crit. Care Med., 2013, 41(3), 820-832.
[26]
Ostuni, R.; Natoli, G.; Cassatella, M.A.; Tamassia, N. Epigenetic regulation of neutrophil development and function. Semin. Immunol., 2016, 28(2), 83-93.
[28]
Branzk, N.; Lubojemska, A.; Hardison, S.E.; Wang, Q.; Gutierrez, M.G.; Brown, G.D.; Papayannopoulos, V. Neutrophils sense microbe size and selectively release neutrophil extracellular traps in response to large pathogens. Nat. Immunol., 2014, 15(11), 1017-1025.
[29]
Anzilotti, C.; Pratesi, F.; Tommasi, C.; Migliorini, P. Peptidylarginine deiminase 4 and citrullination in health and disease. Autoimmun. Rev., 2010, 9(3), 158-160.
[30]
Ma, A.C.; Kubes, P. Platelets, neutrophils, and neutrophil extracellular traps (NETs) in sepsis. J. Thromb. Haemost., 2008, 6(3), 415-420.
[32]
Hakkim, A.; Fuchs, T.A.; Martinez, N.E.; Hess, S.; Prinz, H.; Zychlinsky, A.; Waldmann, H. Activation of the Raf-MEK-ERK pathway is required for neutrophil extracellular trap formation. Nat. Chem. Biol., 2011, 7(2), 75-77.
[33]
Metzler, K.D.; Goosmann, C.; Lubojemska, A.; Zychlinsky, A.; Papayannopoulos, V. A myeloperoxidase-containing complex regulates neutrophil elastase release and actin dynamics during NETosis. Cell Reports, 2014, 8(3), 883-896.
[34]
Sollberger, G.; Tilley, D.O.; Zychlinsky, A. Neutrophil extracellular traps: The biology of chromatin externalization. Dev. Cell, 2018, 44(5), 542-553.
[35]
Desai, J.; Mulay, S.R.; Nakazawa, D.; Anders, H.J. Matters of life and death. How neutrophils die or survive along NET release and is “NETosis” = necroptosis? Cell. Mol. Life Sci., 2016, 73(11-12), 2211-2219.
[36]
Kenny, E.F.; Herzig, A.; Kruger, R.; Muth, A.; Mondal, S.; Thompson, P.R.; Brinkmann, V.; Bernuth, H.V.; Zychlinsky, A. Diverse stimuli engage different neutrophil extracellular trap pathways. eLife, 2017, 6, e24437.
[37]
Sollberger, G.; Amulic, B.; Zychlinsky, A. Neutrophil extracellular trap formation is independent of de novo gene expression. PLoS One, 2016, 11(6), e0157454.
[38]
Park, S.Y.; Shrestha, S.; Youn, Y.J.; Kim, J.K.; Kim, S.Y.; Kim, H.J.; Park, S.H.; Ahn, W.G.; Kim, S.; Lee, M.G.; Jung, K.S.; Park, Y.B.; Mo, E.K.; Ko, Y.; Lee, S.Y.; Koh, Y.; Park, M.J.; Song, D.K.; Hong, C.W. Autophagy primes neutrophils for neutrophil extracellular trap formation during sepsis. Am. J. Respir. Crit. Care Med., 2017, 196(5), 577-589.
[39]
Meng, W.; Paunel-Gorgulu, A.; Flohe, S.; Hoffmann, A.; Witte, I.; MacKenzie, C.; Baldus, S.E.; Windolf, J.; Logters, T.T. Depletion of neutrophil extracellular traps in vivo results in hypersusceptibility to polymicrobial sepsis in mice. Crit. Care (London, England), 2012, 16(4), R137.
[40]
Saffarzadeh, M.; Juenemann, C.; Queisser, M.A.; Lochnit, G.; Barreto, G.; Galuska, S.P.; Lohmeyer, J.; Preissner, K.T. Neutrophil extracellular traps directly induce epithelial and endothelial cell death: A predominant role of histones. PLoS One, 2012, 7(2), e32366.
[41]
Weber, C. Liver: Neutrophil extracellular traps mediate bacterial liver damage. Nat. Rev. Gastroenterol. Hepatol., 2015, 12(5), 251.
[42]
Xu, J.; Zhang, X.; Pelayo, R.; Monestier, M.; Ammollo, C.T.; Semeraro, F.; Taylor, F.B.; Esmon, N.L.; Lupu, F.; Esmon, C.T. Extracellular histones are major mediators of death in sepsis. Nat. Med., 2009, 15(11), 1318-1321.
[43]
Czaikoski, P.G.; Mota, J.M.; Nascimento, D.C.; Sonego, F.; Castanheira, F.V.; Melo, P.H.; Scortegagna, G.T.; Silva, R.L.; Barroso-Sousa, R.; Souto, F.O.; Pazin-Filho, A.; Figueiredo, F.; Alves-Filho, J.C.; Cunha, F.Q. Neutrophil extracellular traps induce organ damage during experimental and clinical sepsis. PLoS One, 2016, 11(2), e0148142.
[44]
Storisteanu, D.M.; Pocock, J.M.; Cowburn, A.S.; Juss, J.K.; Nadesalingam, A.; Nizet, V.; Chilvers, E.R. Evasion of neutrophil extracellular traps by respiratory pathogens. Am. J. Respir. Cell Mol. Biol., 2017, 56(4), 423-431.
[45]
Yoo, S.; Ha, S.J. Generation of tolerogenic dendritic cells and their therapeutic applications. Immune Netw., 2016, 16(1), 52-60.
[46]
Steinman, R.M.; Banchereau, J. Taking dendritic cells into medicine. Nature, 2007, 449(7161), 419-426.
[47]
Steinman, R.M.; Hawiger, D.; Nussenzweig, M.C. Tolerogenic dendritic cells. Annu. Rev. Immunol., 2003, 21, 685-711.
[48]
Moore, K.W.; de Waal Malefyt, R.; Coffman, R.L.; O’Garra, A. Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol., 2001, 19, 683-765.
[49]
Wakkach, A.; Fournier, N.; Brun, V.; Breittmayer, J.P.; Cottrez, F.; Groux, H. Characterization of dendritic cells that induce tolerance and T regulatory 1 cell differentiation in vivo. Immunity, 2003, 18(5), 605-617.
[50]
Domogalla, M.P.; Rostan, P.V.; Raker, V.K.; Steinbrink, K. Tolerance through education: How tolerogenic dendritic cells shape immunity. Front. Immunol., 2017, 8, 1764.
[52]
Yamazaki, S.; Iyoda, T.; Tarbell, K.; Olson, K.; Velinzon, K.; Inaba, K.; Steinman, R.M. Direct expansion of functional CD25+ CD4+ regulatory T cells by antigen-processing dendritic cells. J. Exp. Med., 2003, 198(2), 235-247.
[53]
Amodio, G.; Renna, M.; Paladino, S.; Venturi, C.; Tacchetti, C.; Moltedo, O.; Franceschelli, S.; Mallardo, M.; Bonatti, S.; Remondelli, P. Endoplasmic reticulum stress reduces the export from the ER and alters the architecture of post-ER compartments. Int. J. Biochem. Cell Biol., 2009, 41(12), 2511-2521.
[54]
Zhu, X.M.; Yao, F.H.; Yao, Y.M.; Dong, N.; Yu, Y.; Sheng, Z.Y. Endoplasmic reticulum stress and its regulator XBP-1 contributes to dendritic cell maturation and activation induced by high mobility group box-1 protein. Int. J. Biochem. Cell Biol., 2012, 44(7), 1097-1105.
[55]
Bravo, R.; Gutierrez, T.; Paredes, F.; Gatica, D.; Rodriguez, A.E.; Pedrozo, Z.; Chiong, M.; Parra, V.; Quest, A.F.; Rothermel, B.A.; Lavandero, S. Endoplasmic reticulum: ER stress regulates mitochondrial bioenergetics. Int. J. Biochem. Cell Biol., 2012, 44(1), 16-20.
[56]
Benjamim, C.F.; Hogaboam, C.M.; Lukacs, N.W.; Kunkel, S.L. Septic mice are susceptible to pulmonary aspergillosis. Am. J. Pathol., 2003, 163(6), 2605-2617.
[57]
Benjamim, C.F.; Lundy, S.K.; Lukacs, N.W.; Hogaboam, C.M.; Kunkel, S.L. Reversal of long-term sepsis-induced immunosuppression by dendritic cells. Blood, 2005, 105(9), 3588-3595.
[58]
Zhang, L.T.; Yao, Y.M.; Yao, F.H.; Huang, L.F.; Dong, N.; Yu, Y.; Sheng, Z.Y. Association between high-mobility group box-1 protein release and immune function of dendritic cells in thermal injury. J. Interferon Cytokine Res., 2010, 30(7), 487-495.
[59]
Zhu, X.M.; Yao, Y.M.; Liang, H.P.; Xu, S.; Dong, N.; Yu, Y.; Sheng, Z.Y. The effect of high mobility group box-1 protein on splenic dendritic cell maturation in rats. J. Interferon Cytokine Res., 2009, 29(10), 677-686.
[60]
Blanco, P.; Palucka, A.K.; Pascual, V.; Banchereau, J. Dendritic cells and cytokines in human inflammatory and autoimmune diseases. Cytokine Growth Factor Rev., 2008, 19(1), 41-52.
[61]
Coombes, J.L.; Siddiqui, K.R.; Arancibia-Carcamo, C.V.; Hall, J.; Sun, C.M.; Belkaid, Y.; Powrie, F. A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism. J. Exp. Med., 2007, 204(8), 1757-1764.
[62]
Mucida, D.; Park, Y.; Kim, G.; Turovskaya, O.; Scott, I.; Kronenberg, M.; Cheroutre, H. Reciprocal TH17 and regulatory T cell differentiation
mediated by retinoic acid. Science. (New York, N.Y.),, 2007, 317(5835), 256-260.
[63]
Sun, C.M.; Hall, J.A.; Blank, R.B.; Bouladoux, N.; Oukka, M.; Mora, J.R.; Belkaid, Y. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J. Exp. Med., 2007, 204(8), 1775-1785.
[64]
Mora, J.R.; Iwata, M.; Eksteen, B.; Song, S.Y.; Junt, T.; Senman, B.; Otipoby, K.L.; Yokota, A.; Takeuchi, H.; Ricciardi-Castagnoli, P.; Rajewsky, K.; Adams, D.H.; von Andrian, U.H. Generation of gut-homing IgA-secreting B cells by intestinal dendritic cells. gut-homing IgA-secreting B cells by intestinal dendritic cells Science, (New York, N.Y.),, 2006, 314(5802), 1157-1160.
[65]
Iwata, M.; Hirakiyama, A.; Eshima, Y.; Kagechika, H.; Kato, C.; Song, S.Y. Retinoic acid imprints gut-homing specificity on T cells. Immunity, 2004, 21(4), 527-538.
[66]
Laudanski, K. Adoptive transfer of naive dendritic cells in resolving post-sepsis long-term immunosuppression. Med. Hypotheses, 2012, 79(4), 478-480.
[67]
Roquilly, A.; Broquet, A.; Jacqueline, C.; Gautreau, L.; Segain, J.P.; de Coppet, P.; Caillon, J.; Altare, F.; Josien, R.; Asehnoune, K. Toll-like receptor-4 agonist in post-haemorrhage pneumonia: role of dendritic and natural killer cells. Eur. Respir. J., 2013, 42(5), 1365-1378.
[68]
Hotchkiss, R.S.; Tinsley, K.W.; Swanson, P.E.; Grayson, M.H.; Osborne, D.F.; Wagner, T.H.; Cobb, J.P.; Coopersmith, C. Karl,
I.E. Depletion of dendritic cells, but not macrophages, in patients
with sepsis. J. Immunol., (Baltimore, Md.: 1950),, 2002, 168(5), 2493-2500.
[69]
Gautier, E.L.; Huby, T.; Saint-Charles, F.; Ouzilleau, B.; Chapman, M.J.; Lesnik, P. Enhanced dendritic cell survival attenuates
lipopolysaccharide-induced immunosuppression and increases resistance
to lethal endotoxic shock. J. Immunol., (Baltimore, Md 1950), 2008, 180(10), 6941-6946.
[70]
Grimaldi, D.; Louis, S.; Pene, F.; Sirgo, G.; Rousseau, C.; Claessens, Y.E.; Vimeux, L.; Cariou, A.; Mira, J.P.; Hosmalin, A.; Chiche, J.D. Profound and persistent decrease of circulating dendritic cells is associated with ICU-acquired infection in patients with septic shock. Intensive Care Med., 2011, 37(9), 1438-1446.
[71]
Bohannon, J.; Cui, W.; Sherwood, E.; Toliver-Kinsky, T. Dendritic
cell modification of neutrophil responses to infection after burn injury. J. Immunol., (Baltimore, Md.: 1950),, 2010, 185(5), 2847-
2853.
[72]
Toliver-Kinsky, T.E.; Cui, W.; Murphey, E.D.; Lin, C.; Sherwood, E.R. Enhancement of dendritic cell production by fms-like tyrosine
kinase-3 ligand increases the resistance of mice to a burn wound infection. J. Immunol., (Baltimore, Md.: 1950),, 2005, 174(1), 404-
410.
[73]
Toliver-Kinsky, T.E.; Lin, C.Y.; Herndon, D.N.; Sherwood, E.R. Stimulation of hematopoiesis by the Fms-like tyrosine kinase 3 ligand restores bacterial induction of Th1 cytokines in thermally injured mice. Infect. Immun., 2003, 71(6), 3058-3067.
[74]
Na, Y.R.; Je, S.; Seok, S.H. Metabolic features of macrophages in inflammatory diseases and cancer. Cancer Lett., 2018, 413, 46-58.
[75]
Cazalis, M.A.; Friggeri, A.; Cave, L.; Demaret, J.; Barbalat, V.; Cerrato, E.; Lepape, A.; Pachot, A.; Monneret, G.; Venet, F. Decreased
HLA-DR antigen-associated invariant chain (CD74)
mRNA expression predicts mortality after septic shock. Crit. Care,
(London, England),, 2013, 17(6), R287.
[76]
Cheron, A.; Floccard, B.; Allaouchiche, B.; Guignant, C.; Poitevin, F.; Malcus, C.; Crozon, J.; Faure, A.; Guillaume, C.; Marcotte, G.; Vulliez, A.; Monneuse, O.; Monneret, G. Lack of recovery in
monocyte human leukocyte antigen-DR expression is independently
associated with the development of sepsis after major trauma. Crit. Care, (London, England),, 2010, 14(6), R208.
[77]
Landelle, C.; Lepape, A.; Voirin, N.; Tognet, E.; Venet, F.; Bohe, J.; Vanhems, P.; Monneret, G. Low monocyte human leukocyte antigen-DR is independently associated with nosocomial infections after septic shock. Intensive Care Med., 2010, 36(11), 1859-1866.
[78]
Muthu, K.; He, L.K.; Melstrom, K.; Szilagyi, A.; Gamelli, R.L.; Shankar, R. Perturbed bone marrow monocyte development following burn injury and sepsis promote hyporesponsive monocytes. J. Burn Care Res., 2008, 29(1), 12-21.
[79]
Saeed, S.; Quintin, J.; Kerstens, H.H.; Rao, N.A.; Aghajanirefah, A.; Matarese, F.; Cheng, S.C.; Ratter, J.; Berentsen, K.; van der Ent, M.A.; Sharifi, N.; Janssen-Megens, E.M.; Ter Huurne, M.; Mandoli, A.; van Schaik, T.; Ng, A.; Burden, F.; Downes, K.; Frontini, M.; Kumar, V.; Giamarellos-Bourboulis, E.J.; Ouwehand, W.H.; van der Meer, J.W.; Joosten, L.A.; Wijmenga, C.; Martens, J.H.; Xavier, R.J.; Logie, C.; Netea, M.G.; Stunnenberg, H.G. Epigenetic
programming of monocyte-to-macrophage differentiation
and trained innate immunity. Science, (New York, N.Y.),, 2014, 345(6204), 1251086.
[80]
Kockara, A.; Kayatas, M. Renal cell apoptosis and new treatment options in sepsis-induced acute kidney injury. Ren. Fail., 2013, 35(2), 291-294.
[81]
Lotze, M.T.; Tracey, K.J. High-mobility group box 1 protein (HMGB1): Nuclear weapon in the immune arsenal. Nat. Rev. Immunol., 2005, 5(4), 331-342.
[82]
Zhu, X.M.; Yao, Y.M.; Liang, H.P.; Liu, F.; Dong, N.; Yu, Y.; Sheng, Z.Y. Effect of high mobility group box-1 protein on apoptosis of peritoneal macrophages. Arch. Biochem. Biophys., 2009, 492(1-2), 54-61.
[83]
Le Tulzo, Y.; Pangault, C.; Gacouin, A.; Guilloux, V.; Tribut, O.; Amiot, L.; Tattevin, P.; Thomas, R.; Fauchet, R.; Drenou, B. Early
circulating lymphocyte apoptosis in human septic shock is associated
with poor outcome. Shock, (Augusta, Ga.),, 2002, 18(6), 487-
494.
[84]
Menzel, C.L.; Sun, Q.; Loughran, P.A.; Pape, H.C.; Billiar, T.R.; Scott, M.J. Caspase-1 is hepatoprotective during trauma and hemorrhagic
shock by reducing liver injury and inflammation. Mol.
Med., (Cambridge, Mass.),, 2011, 17(9-10), 1031-1038.
[85]
Osuka, A.; Hanschen, M.; Stoecklein, V.; Lederer, J.A. A protective
role for inflammasome activation following injury. Shock,
(Augusta, Ga.),, 2012, 37(1), 47-55.
[86]
Jorgensen, I.; Miao, E.A. Pyroptotic cell death defends against intracellular pathogens. Immunol. Rev., 2015, 265(1), 130-142.
[87]
Miao, E.A.; Leaf, I.A.; Treuting, P.M.; Mao, D.P.; Dors, M.; Sarkar, A.; Warren, S.E.; Wewers, M.D.; Aderem, A. Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria. Nat. Immunol., 2010, 11(12), 1136-1142.
[88]
Talmadge, J.E.; Gabrilovich, D.I. History of myeloid-derived suppressor cells. Nat. Rev. Cancer, 2013, 13(10), 739-752.
[89]
Ostrand-Rosenberg, S.; Sinha, P. Myeloid-derived suppressor cells:
Linking inflammation and cancer. J. Immunol., (Baltimore, Md.:
1950), 2009, 182(8), 4499-4506.
[90]
Brandau, S.; Trellakis, S.; Bruderek, K.; Schmaltz, D.; Steller, G.; Elian, M.; Suttmann, H.; Schenck, M.; Welling, J.; Zabel, P.; Lang, S. Myeloid-derived suppressor cells in the peripheral blood of cancer patients contain a subset of immature neutrophils with impaired migratory properties. J. Leukoc. Biol., 2011, 89(2), 311-317.
[91]
Ochoa, A.C.; Zea, A.H.; Hernandez, C.; Rodriguez, P.C. Arginase, prostaglandins, and myeloid-derived suppressor cells in renal cell carcinoma. Clin. Cancer Res., 2007, 13(2 Pt 2), 721s-726s.
[92]
Chikamatsu, K.; Sakakura, K.; Toyoda, M.; Takahashi, K.; Yamamoto, T.; Masuyama, K. Immunosuppressive activity of CD14+ HLA-DR- cells in squamous cell carcinoma of the head and neck. Cancer Sci., 2012, 103(6), 976-983.
[93]
Gilbert, K.M.; Thoman, M.; Bauche, K.; Pham, T.; Weigle, W.O. Transforming growth factor-beta 1 induces antigen-specific unresponsiveness in naive T cells. Immunol. Invest., 1997, 26(4), 459-472.
[94]
Wan, Y.Y.; Flavell, R.A. TGF-beta and regulatory T cell in immunity and autoimmunity. J. Clin. Immunol., 2008, 28(6), 647-659.
[95]
Knapp, S.; Thalhammer, F.; Locker, G.J.; Laczika, K.; Hollenstein, U.; Frass, M.; Winkler, S.; Stoiser, B.; Wilfing, A.; Burgmann, H. Prognostic value of MIP-1 alpha, TGF-beta 2, sELAM-1, and sVCAM-1 in patients with gram-positive sepsis. Clin. Immunol. Immunopathol., 1998, 87(2), 139-144.
[96]
Marie, C.; Cavaillon, J.M.; Losser, M.R. Elevated levels of circulating transforming growth factor-beta 1 in patients with the sepsis syndrome. Ann. Intern. Med., 1996, 125(6), 520-521.
[97]
Ochando, J.C.; Chen, S.H. Myeloid-derived suppressor cells in transplantation and cancer. Immunol. Res., 2012, 54(1-3), 275-285.
[98]
Corzo, C.A.; Cotter, M.J.; Cheng, P.; Cheng, F.; Kusmartsev, S.; Sotomayor, E.; Padhya, T.; McCaffrey, T.V.; McCaffrey, J.C.; Gabrilovich, D.I. Mechanism regulating reactive oxygen species in
tumor-induced myeloid-derived suppressor cells. J. Immunol., (Baltimore,
Md.: 1950),, 2009, 182(9), 5693-5701.
[99]
Yang, R.; Cai, Z.; Zhang, Y.; Yutzy, W.H.; Roby, K.F.; Roden, R.B. CD80 in immune suppression by mouse ovarian carcinoma-associated Gr-1+CD11b+ myeloid cells. Cancer Res., 2006, 66(13), 6807-6815.
[100]
Gabrilovich, D.I.; Nagaraj, S. Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol., 2009, 9(3), 162-174.
[101]
Delano, M.J.; Scumpia, P.O.; Weinstein, J.S.; Coco, D.; Nagaraj, S.; Kelly-Scumpia, K.M.; O’Malley, K.A.; Wynn, J.L.; Antonenko, S.; Al-Quran, S.Z.; Swan, R.; Chung, C.S.; Atkinson, M.A.; Ramphal, R.; Gabrilovich, D.I.; Reeves, W.H.; Ayala, A.; Phillips, J.; Laface, D.; Heyworth, P.G.; Clare-Salzler, M.; Moldawer, L.L. MyD88-dependent expansion of an immature GR-1(+)CD11b(+) population induces T cell suppression and Th2 polarization in sepsis. J. Exp. Med., 2007, 204(6), 1463-1474.
[102]
Sinha, P.; Clements, V.K.; Bunt, S.K.; Albelda, S.M.; Ostrand-Rosenberg, S. Cross-talk between myeloid-derived suppressor cells
and macrophages subverts tumor immunity toward a type 2 response. J. Immunol., (Baltimore, Md.: 1950),, 2007, 179(2), 977-
983.
[103]
Delano, M.J.; Thayer, T.; Gabrilovich, S.; Kelly-Scumpia, K.M.; Winfield, R.D.; Scumpia, P.O.; Cuenca, A.G.; Warner, E.; Wallet, S.M.; Wallet, M.A.; O'Malley, K.A.; Ramphal, R.; Clare-Salzer, M.; Efron, P.A.; Mathews, C.E.; Moldawer, L.L. Sepsis induces
early alterations in innate immunity that impact mortality to secondary
infection. J. Immunol., (Baltimore,
Md.: 1950),, 2011, 186(1), 195-202.
[104]
Noel, G.; Wang, Q.; Osterburg, A.; Schwemberger, S.; James, L.; Haar, L.; Giacalone, N.; Thomas, I.; Ogle, C. A ribonucleotide reductase
inhibitor reverses burn-induced inflammatory defects. Shock, (Augusta, Ga.),, 2010, 34(5), 535-544.
[105]
Sander, L.E.; Sackett, S.D.; Dierssen, U.; Beraza, N.; Linke, R.P.; Muller, M.; Blander, J.M.; Tacke, F.; Trautwein, C. Hepatic acute-phase proteins control innate immune responses during infection by promoting myeloid-derived suppressor cell function. J. Exp. Med., 2010, 207(7), 1453-1464.
[106]
Brudecki, L.; Ferguson, D.A.; McCall, C.E.; El Gazzar, M. Myeloid-derived suppressor cells evolve during sepsis and can enhance or attenuate the systemic inflammatory response. Infect. Immun., 2012, 80(6), 2026-2034.
[107]
Derive, M.; Bouazza, Y.; Alauzet, C.; Gibot, S. Myeloid-derived suppressor cells control microbial sepsis. Intensive Care Med., 2012, 38(6), 1040-1049.
[108]
Kusmartsev, S.; Cheng, F.; Yu, B.; Nefedova, Y.; Sotomayor, E.; Lush, R.; Gabrilovich, D. All-trans-retinoic acid eliminates immature myeloid cells from tumor-bearing mice and improves the effect of vaccination. Cancer Res., 2003, 63(15), 4441-4449.
[109]
Serafini, P.; Meckel, K.; Kelso, M.; Noonan, K.; Califano, J.; Koch, W.; Dolcetti, L.; Bronte, V.; Borrello, I. Phosphodiesterase-5 inhibition augments endogenous antitumor immunity by reducing myeloid-derived suppressor cell function. J. Exp. Med., 2006, 203(12), 2691-2702.
[110]
De Santo, C.; Serafini, P.; Marigo, I.; Dolcetti, L.; Bolla, M.; Del Soldato, P.; Melani, C.; Guiducci, C.; Colombo, M.P.; Iezzi, M.; Musiani, P.; Zanovello, P.; Bronte, V. Nitroaspirin corrects immune dysfunction in tumor-bearing hosts and promotes tumor eradication by cancer vaccination. Proc. Natl. Acad. Sci. USA, 2005, 102(11), 4185-4190.
[111]
Zheng, Y.; Xu, M.; Li, X.; Jia, J.; Fan, K.; Lai, G. Cimetidine suppresses lung tumor growth in mice through proapoptosis of myeloid-derived suppressor cells. Mol. Immunol., 2013, 54(1), 74-83.
[112]
Hotchkiss, R.S.; Tinsley, K.W.; Swanson, P.E.; Schmieg, R.E., Jr; Hui, J.J.; Chang, K.C.; Osborne, D.F.; Freeman, B.D.; Cobb, J.P.; Buchman, T.G. Karl, I.E. Sepsis-induced apoptosis causes progressive
profound depletion of B and CD4+ T lymphocytes in humans. J. Immunol., (Baltimore, Md.: 1950),, 2001, 166(11), 6952-
6963.
[113]
Cavaillon, J.M.; Annane, D. Compartmentalization of the inflammatory response in sepsis and SIRS. J. Endotoxin Res., 2006, 12(3), 151-170.
[114]
Wesche-Soldato, D.E.; Chung, C.S.; Gregory, S.H.; Salazar-Mather, T.P.; Ayala, C.A.; Ayala, A. CD8+ T cells promote inflammation and apoptosis in the liver after sepsis: Role of Fas-FasL. Am. J. Pathol., 2007, 171(1), 87-96.
[115]
Arens, C.; Bajwa, S.A.; Koch, C.; Siegler, B.H.; Schneck, E.; Hecker, A.; Weiterer, S.; Lichtenstern, C.; Weigand, M.A.; Uhle, F. Sepsis-induced long-term immune paralysis--results of a descriptive,
explorative study. Crit. Care, (London, England),, 2016, 20, 93.
[116]
Carson, W.F.; Cavassani, K.A.; Dou, Y.; Kunkel, S.L. Epigenetic regulation of immune cell functions during post-septic immunosuppression. Epigenetics, 2011, 6(3), 273-283.
[117]
Condotta, S.A.; Khan, S.H.; Rai, D.; Griffith, T.S.; Badovinac, V.P. Polymicrobial sepsis increases susceptibility to chronic viral infection
and exacerbates CD8+ T cell exhaustion. J. Immunol., (Baltimore,
Md.: 1950),, 2015, 195(1), 116-125.
[118]
Wherry, E.J.; Kurachi, M. Molecular and cellular insights into T cell exhaustion. Nat. Rev. Immunol., 2015, 15(8), 486-499.
[119]
Patil, N.K.; Guo, Y.; Luan, L.; Sherwood, E.R. Targeting immune cell checkpoints during sepsis. Int. J. Mol. Sci., 2017, 18(11), 2413.
[120]
Zhang, Y.; Li, J.; Lou, J.; Zhou, Y.; Bo, L.; Zhu, J.; Zhu, K.; Wan, X.; Cai, Z.; Deng, X. Upregulation of programmed death-1 on T
cells and programmed death ligand-1 on monocytes in septic shock
patients. Crit. Care, (London, England),, 2011, 15(1), R70.
[121]
Fife, B.T.; Pauken, K.E.; Eagar, T.N.; Obu, T.; Wu, J.; Tang, Q.; Azuma, M.; Krummel, M.F.; Bluestone, J.A. Interactions between PD-1 and PD-L1 promote tolerance by blocking the TCR-induced stop signal. Nat. Immunol., 2009, 10(11), 1185-1192.
[122]
Francisco, L.M.; Sage, P.T.; Sharpe, A.H. The PD-1 pathway in tolerance and autoimmunity. Immunol. Rev., 2010, 236, 219-242.
[123]
Bardhan, K.; Anagnostou, T.; Boussiotis, V.A. The PD1:PD-L1/2 pathway from discovery to clinical implementation. Front. Immunol., 2016, 7, 550.
[124]
Krummel, M.F.; Allison, J.P. Pillars article: CD28 and CTLA-4
have opposing effects on the response of T cells to stimulation. J.
Immunol., (Baltimore, Md.: 1950),, 2011, 187(7), 3459-3465.
[125]
Walunas, T.L.; Lenschow, D.J.; Bakker, C.Y.; Linsley, P.S.; Freeman, G.J.; Green, J.M.; Thompson, C.B.; Bluestone, J.A. Pillars article:
CTLA-4 can function as a negative regulator of T cell activation. J. Immunol., (Baltimore, Md.: 1950),, 2011, 187(7), 3466-
3474.
[126]
Inoue, S.; Bo, L.; Bian, J.; Unsinger, J.; Chang, K.; Hotchkiss, R.S. Dose-dependent effect of anti-CTLA-4 on survival in sepsis. Shock,
(Augusta, Ga.),, 2011, 36(1), 38-44.
[127]
Zhang, Y.; Yao, Y.M.; Huang, L.F.; Dong, N.; Yu, Y.; Sheng, Z.Y. The potential effect and mechanism of high-mobility group box 1 protein on regulatory T cell-mediated immunosuppression. J. Interferon Cytokine Res., 2011, 31(2), 249-257.
[128]
O’Sullivan, S.T.; Lederer, J.A.; Horgan, A.F.; Chin, D.H.; Mannick, J.A.; Rodrick, M.L. Major injury leads to predominance of the T helper-2 lymphocyte phenotype and diminished interleukin-12 production associated with decreased resistance to infection. Ann. Surg., 1995, 222(4), 482-490 discussion 490-492.
[129]
Smeekens, S.P.; Ng, A.; Kumar, V.; Johnson, M.D.; Plantinga, T.S.; van Diemen, C.; Arts, P.; Verwiel, E.T.; Gresnigt, M.S.; Fransen, K.; van Sommeren, S.; Oosting, M.; Cheng, S.C.; Joosten, L.A.; Hoischen, A.; Kullberg, B.J.; Scott, W.K.; Perfect, J.R.; van der Meer, J.W.; Wijmenga, C.; Netea, M.G.; Xavier, R.J. Functional genomics identifies type I interferon pathway as central for host defense against Candida albicans. Nat. Commun., 2013, 4, 1342.
[130]
Schaller, M.; Ito, T.; Allen, R.M.; Kroetz, D.; Kittan, N.; Ptaschinski, C.; Cavassani, K.; Carson, W.F.; Godessart, N.; Grembecka, J.; Cierpicki, T.; Dou, Y.; Kunkel, S.L. Epigenetic regulation of IL-12-dependent T cell proliferation. J. Leukoc. Biol., 2015, 98(4), 601-613.
[131]
Carson, W.F.; Cavassani, K.A.; Ito, T.; Schaller, M.; Ishii, M.; Dou, Y.; Kunkel, S.L. Impaired CD4+ T-cell proliferation and effector function correlates with repressive histone methylation events in a mouse model of severe sepsis. Eur. J. Immunol., 2010, 40(4), 998-1010.
[132]
Mack, V.E.; McCarter, M.D.; Naama, H.A.; Calvano, S.E.; Daly, J.M. Dominance of T-helper 2-type cytokines after severe injury. Arch. Surg., (Chicago, Ill.: 1960),, 1996, 131(12), 1303-1308; discussion
1308-1309.
[133]
T O'Sullivan, S.; Lederer, J.; Horgan, A.; Chin, D.; Mannick, J.;
Rodrick, M. Major injury leads to predominance of the T helper-2
lymphocyte phenotype and diminished interleukin-12 production
associated with decreased resistance to infection. Ann. Surg., 1995, 222(4), 482-490; discussion 490.
[134]
Mukherjee, S.; Allen, R.M.; Lukacs, N.W.; Kunkel, S.L.; Carson, W.F. STAT3-mediated IL-17 production by postseptic T cells ex acerbates viral immunopathology of the lung. Shock, (Augusta,
Ga.),, 2012, 38(5), 515-523.
[135]
Hanschen, M.; Tajima, G.; O’Leary, F.; Hoang, K.; Ikeda, K.; Lederer, J.A. Phospho-flow cytometry based analysis of differences in T cell receptor signaling between regulatory T cells and CD4+ T cells. J. Immunol. Methods, 2012, 376(1-2), 1-12.
[136]
Williams, L.M.; Rudensky, A.Y. Maintenance of the Foxp3-dependent developmental program in mature regulatory T cells requires continued expression of Foxp3. Nat. Immunol., 2007, 8(3), 277-284.
[137]
Wan, Y.Y.; Flavell, R.A. Regulatory T-cell functions are subverted and converted owing to attenuated Foxp3 expression. Nature, 2007, 445(7129), 766-770.
[138]
Brunkow, M.E.; Jeffery, E.W.; Hjerrild, K.A.; Paeper, B.; Clark, L.B.; Yasayko, S.A.; Wilkinson, J.E.; Galas, D.; Ziegler, S.F.; Ramsdell, F. Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse. Nat. Genet., 2001, 27(1), 68-73.
[139]
Buckner, J.H. Mechanisms of impaired regulation by CD4(+)CD25(+)FOXP3(+) regulatory T cells in human autoimmune diseases. Nat. Rev. Immunol., 2010, 10(12), 849-859.
[140]
Bluestone, J.A.; Abbas, A.K. Natural versus adaptive regulatory T cells. Nat. Rev. Immunol., 2003, 3(3), 253-257.
[141]
Yao, Y.M.; Huang, L.F. The potential role of regulatory T cells in postburn sepsis. Zhonghua Shao Shang Za Zhi Chin. J. Burns, 2011, 27(2), 81-83.
[142]
Peters, N.; Sacks, D. Immune privilege in sites of chronic infection: Leishmania and regulatory T cells. Immunol. Rev., 2006, 213, 159-179.
[143]
Vignali, D.A.; Collison, L.W.; Workman, C.J. How regulatory T cells work. Nat. Rev. Immunol., 2008, 8(7), 523-532.
[144]
Venet, F.; Chung, C.S.; Kherouf, H.; Geeraert, A.; Malcus, C.; Poitevin, F.; Bohe, J.; Lepape, A.; Ayala, A.; Monneret, G. Increased circulating regulatory T cells (CD4(+)CD25 (+)CD127 (-)) contribute to lymphocyte anergy in septic shock patients. Intensive Care Med., 2009, 35(4), 678-686.
[145]
Cavassani, K.A.; Carson, W.F.; Moreira, A.P.; Wen, H.; Schaller, M.A.; Ishii, M.; Lindell, D.M.; Dou, Y.; Lukacs, N.W.; Keshamouni, V.G.; Hogaboam, C.M.; Kunkel, S.L. The post sepsis-induced expansion and enhanced function of regulatory T cells create an environment to potentiate tumor growth. Blood, 2010, 115(22), 4403-4411.
[146]
Delano, M.J.; Ward, P.A. Sepsis-induced immune dysfunction: Can immune therapies reduce mortality? J. Clin. Invest., 2016, 126(1), 23-31.
[147]
Hotchkiss, R.S.; Monneret, G.; Payen, D. Sepsis-induced immunosuppression: from cellular dysfunctions to immunotherapy. Nat. Rev. Immunol., 2013, 13(12), 862-874.
[148]
Holtmeier, W.; Kabelitz, D. gammadelta T cells link innate and adaptive immune responses. Chem. Immunol. Allergy, 2005, 86, 151-183.
[149]
Andreu-Ballester, J.C.; Tormo-Calandin, C.; Garcia-Ballesteros, C.; Perez-Griera, J.; Amigo, V.; Almela-Quilis, A.; Ruiz del Castillo, J.; Penarroja-Otero, C.; Ballester, F. Association of gammadelta T cells with disease severity and mortality in septic patients. Clin. Vaccine Immunol., 2013, 20(5), 738-746.
[150]
Tomasello, E.; Bedoui, S. Intestinal innate immune cells in gut homeostasis and immunosurveillance. Immunol. Cell Biol., 2013, 91(3), 201-203.
[151]
Hu, C.K.; Venet, F.; Heffernan, D.S.; Wang, Y.L.; Horner, B.; Huang, X.; Chung, C.S.; Gregory, S.H.; Ayala, A. The role of hepatic
invariant NKT cells in systemic/local inflammation and mortality
during polymicrobial septic shock. J. Immunol., (Baltimore,
Md.: 1950),, 2009, 182(4), 2467-2475.
[152]
Godfrey, D.I.; MacDonald, H.R.; Kronenberg, M.; Smyth, M.J.; Van Kaer, L. NKT cells: What’s in a name? Nat. Rev. Immunol., 2004, 4(3), 231-237.
[153]
Parekh, V.V.; Wilson, M.T.; Olivares-Villagomez, D.; Singh, A.K.; Wu, L.; Wang, C.R.; Joyce, S.; Van Kaer, L. Glycolipid antigen induces long-term natural killer T cell anergy in mice. J. Clin. Invest., 2005, 115(9), 2572-2583.
[154]
Chuang, K.I.; Leung, B.; Hsu, N.; Harris, H.W. Heparin protects against septic mortality via apoE-antagonism. Am. J. Surg., 2011, 202(3), 325-335.
[155]
Mauri, C.; Bosma, A. Immune regulatory function of B cells. Annu. Rev. Immunol., 2012, 30, 221-241.
[156]
Gustave, C.A.; Gossez, M.; Demaret, J.; Rimmele, T.; Lepape, A.; Malcus, C.; Poitevin-Later, F.; Jallades, L.; Textoris, J.; Monneret, G.; Venet, F. Septic shock shapes B cell response toward an exhausted-
like/immunoregulatory profile in patients. J. Immunol.,
(Baltimore, Md.: 1950),, 2018, 200(7), 2418-2425.
[157]
Maecker, H.T.; McCoy, J.P.; Nussenblatt, R. Standardizing immunophenotyping for the human immunology project. Nat. Rev. Immunol., 2012, 12(3), 191-200.
[158]
Zan, H.; Casali, P. Epigenetics of peripheral B-cell differentiation and the antibody response. Front. Immunol., 2015, 6, 631.
[159]
Wang, R.X.; Yu, C.R.; Dambuza, I.M.; Mahdi, R.M.; Dolinska, M.B.; Sergeev, Y.V.; Wingfield, P.T.; Kim, S.H.; Egwuagu, C.E. Interleukin-35 induces regulatory B cells that suppress autoimmune disease. Nat. Med., 2014, 20(6), 633-641.
[160]
Peng, B.; Ming, Y.; Yang, C. Regulatory B cells: The cutting edge of immune tolerance in kidney transplantation. Cell Death Dis., 2018, 9(2), 109.
[161]
Moir, S.; Fauci, A.S. B-cell exhaustion in HIV infection: The role of immune activation. Curr. Opin. HIV AIDS, 2014, 9(5), 472-477.
[162]
Kardava, L.; Moir, S.; Wang, W.; Ho, J.; Buckner, C.M.; Posada, J.G.; O’Shea, M.A.; Roby, G.; Chen, J.; Sohn, H.W.; Chun, T.W.; Pierce, S.K.; Fauci, A.S. Attenuation of HIV-associated human B cell exhaustion by siRNA downregulation of inhibitory receptors. J. Clin. Invest., 2011, 121(7), 2614-2624.
[163]
Monroe, J.G. Ligand-independent tonic signaling in B-cell receptor function. Curr. Opin. Immunol., 2004, 16(3), 288-295.
[164]
Monserrat, J.; de Pablo, R.; Diaz-Martin, D.; Rodriguez-Zapata, M.; de la Hera, A.; Prieto, A.; Alvarez-Mon, M. Early alterations of B cells in patients with septic shock. Crit. Care (London, England),, 2013, 17(3), R105.
[165]
Weber, G.F.; Chousterman, B.G.; He, S.; Fenn, A.M.; Nairz, M.; Anzai, A.; Brenner, T.; Uhle, F.; Iwamoto, Y.; Robbins, C.S.; Noiret, L.; Maier, S.L.; Zonnchen, T.; Rahbari, N.N.; Scholch, S.; Klotzsche-von Ameln, A.; Chavakis, T.; Weitz, J.; Hofer, S.; Weigand, M.A.; Nahrendorf, M.; Weissleder, R.; Swirski, F.K. Interleukin-
3 amplifies acute inflammation and is a potential therapeutic
target in sepsis. Science, (New York, N.Y.),, 2015, 347(6227), 1260-1265.
[166]
Rauch, P.J.; Chudnovskiy, A.; Robbins, C.S.; Weber, G.F.; Etzrodt, M.; Hilgendorf, I.; Tiglao, E.; Figueiredo, J.L.; Iwamoto, Y.; Theurl, I.; Gorbatov, R.; Waring, M.T.; Chicoine, A.T.; Mouded, M.; Pittet, M.J.; Nahrendorf, M.; Weissleder, R.; Swirski, F.K. Innate
response activator B cells protect against microbial sepsis. Science,
(New York, N.Y.),, 2012, 335(6068), 597-601.
[167]
Serafini, N.; Vosshenrich, C.A.; Di Santo, J.P. Transcriptional regulation of innate lymphoid cell fate. Nat. Rev. Immunol., 2015, 15(7), 415-428.
[168]
Honda, K.; Littman, D.R. The microbiota in adaptive immune homeostasis and disease. Nature, 2016, 535(7610), 75-84.
[169]
Colonna, M. Innate lymphoid cells: Diversity, plasticity, and unique functions in immunity. Immunity, 2018, 48(6), 1104-1117.
[170]
Bar-Ephraim, Y.E.; Mebius, R.E. Innate lymphoid cells in secondary lymphoid organs. Immunol. Rev., 2016, 271(1), 185-199.
[171]
Wang, S.; Xia, P.; Chen, Y.; Qu, Y.; Xiong, Z.; Ye, B.; Du, Y.; Tian, Y.; Yin, Z.; Xu, Z.; Fan, Z. Regulatory innate lymphoid cells control innate intestinal inflammation. Cell, 2017, 171(1), 201-216.e18.
[172]
Finfer, S.; Chittock, D.R.; Su, S.Y.; Blair, D.; Foster, D.; Dhingra, V.; Bellomo, R.; Cook, D.; Dodek, P.; Henderson, W.R.; Hebert, P.C.; Heritier, S.; Heyland, D.K.; McArthur, C.; McDonald, E.; Mitchell, I.; Myburgh, J.A.; Norton, R.; Potter, J.; Robinson, B.G.; Ronco, J.J. Intensive versus conventional glucose control in critically ill patients. N. Engl. J. Med., 2009, 360(13), 1283-1297.
[173]
Sprung, C.L.; Annane, D.; Keh, D.; Moreno, R.; Singer, M.; Freivogel, K.; Weiss, Y.G.; Benbenishty, J.; Kalenka, A.; Forst, H.; Laterre, P.F.; Reinhart, K.; Cuthbertson, B.H.; Payen, D.; Briegel, J. Hydrocortisone therapy for patients with septic shock. N. Engl. J. Med., 2008, 358(2), 111-124.
[174]
Marshall, J.C. Why have clinical trials in sepsis failed? Trends Mol. Med., 2014, 20(4), 195-203.
[175]
Tse, M.T. Trial watch: Sepsis study failure highlights need for trial design rethink. Nat. Rev. Drug Discov., 2013, 12(5), 334.
[176]
Pearce, E.L.; Pearce, E.J. Metabolic pathways in immune cell activation and quiescence. Immunity, 2013, 38(4), 633-643.
[177]
Cheng, S.C.; Scicluna, B.P.; Arts, R.J.; Gresnigt, M.S.; Lachmandas, E.; Giamarellos-Bourboulis, E.J.; Kox, M.; Manjeri, G.R.; Wagenaars, J.A.; Cremer, O.L.; Leentjens, J.; van der Meer, A.J.; van de Veerdonk, F.L.; Bonten, M.J.; Schultz, M.J.; Willems, P.H.; Pickkers, P.; Joosten, L.A.; van der Poll, T.; Netea, M.G. Broad defects in the energy metabolism of leukocytes underlie immunoparalysis in sepsis. Nat. Immunol., 2016, 17(4), 406-413.
[178]
van Vught, L.A.; Klein Klouwenberg, P.M.; Spitoni, C.; Scicluna, B.P.; Wiewel, M.A.; Horn, J.; Schultz, M.J.; Nurnberg, P.; Bonten, M.J.; Cremer, O.L.; van der Poll, T. Incidence, risk factors, and attributable mortality of secondary infections in the intensive care unit after admission for sepsis. JAMA, 2016, 315(14), 1469-1479.
[179]
De Santa, F.; Narang, V.; Yap, Z.H.; Tusi, B.K.; Burgold, T.; Austenaa, L.; Bucci, G.; Caganova, M.; Notarbartolo, S.; Casola, S.; Testa, G.; Sung, W.K.; Wei, C.L.; Natoli, G. Jmjd3 contributes to the control of gene expression in LPS-activated macrophages. EMBO J., 2009, 28(21), 3341-3352.
[180]
Ishii, M.; Wen, H.; Corsa, C.A.; Liu, T.; Coelho, A.L.; Allen, R.M.; Carson, W.F.; Cavassani, K.A.; Li, X.; Lukacs, N.W.; Hogaboam, C.M.; Dou, Y.; Kunkel, S.L. Epigenetic regulation of the alternatively activated macrophage phenotype. Blood, 2009, 114(15), 3244-3254.
[181]
Unsinger, J.; McGlynn, M.; Kasten, K.R.; Hoekzema, A.S.; Watanabe, E.; Muenzer, J.T.; McDonough, J.S.; Tschoep, J.; Ferguson, T.A.; McDunn, J.E.; Morre, M.; Hildeman, D.A.; Caldwell, C.C.; Hotchkiss, R.S. IL-7 promotes T cell viability, trafficking, and
functionality and improves survival in sepsis. J. Immunol., (Baltimore,
Md.: 1950),, 2010, 184(7), 3768-3779.
Related Journals
Protein & Peptide Letters
Related Books
Frontiers in Protein and Peptide Sciences
Article Metrics
100
9