Rituximab Treatment Modulates the Release of Hydrogen Peroxide and the Production of Proinflammatory Cytokines by Monocyte at the Onset of Type 1 Diabetes

Author(s): Linda Hamouda, Maroua Miliani, Zeyneb Hadjidj, Rabia Messali, Mourad Aribi*.

Journal Name: Endocrine, Metabolic & Immune Disorders - Drug Targets
(Formerly Current Drug Targets - Immune, Endocrine & Metabolic Disorders)

Volume 19 , Issue 5 , 2019

Become EABM
Become Reviewer

Graphical Abstract:


Abstract:

Background: Monocytes are the main blood innate mononuclear phagocyte and one of the most important effector cells expressing Fcγ receptor, which is critical for the interaction with Fc domain of antibodies.

Objective: To evaluate the effect of Rituximab (RTX, a chimeric human anti-CD20 monoclonal antibody) on the functional activities of Monocytes (MOs) at the onset of human Type 1 Diabetes (T1D).

Methods: MOs were isolated from peripheral blood mononuclear cells (PBMCs) obtained from volunteer patients with recent-onset T1D and healthy control donors.

Results: The levels of the production of Interleukin 1β (IL-1β) and IL-6 were significantly increased in MOs from patients with T1D when compared to MOs from healthy controls (respectively, p < 0.01 and p < 0.05). Similarly, Interferon γ (IFN-γ), and intracellular free Calcium Ion (ifCa2+) levels were increased in T1D MOs than in control MOs, but the difference did not reach a significant level. Conversely, the production levels of IL-4 and catalase activity, as well as of both phagocytosis and killing capacities were decreased in MOs of T1D patients compared to MOs from healthy controls, but the difference was not significant for catalase activity and killing capacity (respectively, p < 0.01, p > 0.05, p < 0.01, and p > 0.05). Additionally, treatment with RTX significantly upregulated phagocytosis (p < 0.05), markedly downregulated the release of IL-1β (p < 0.01), ifCa2+, hydrogen peroxide (H2O2), and slightly downregulated the Nitric Oxide Synthase (NOS) activity, NOS activity-to-arginase activity ratio, the levels of Lactate Dehydrogenase (LDH)-based cytotoxicity, and the production of IL-6 and IFN-γ. Moreover, RTX treatment significantly upregulated the production of IL-4 (p < 0.05), IL-10 (p < 0.01) and the catalase activity (p < 0.05).

Conclusion: Our study has shown for the first time that RTX can reverse the abnormal functional activities of MOs as well as their production of proinflammatory cytokines at the onset of T1D. From a therapeutic point of view, RTX may potentially be suggested at the beginning of T1D to immunomodulate innate immunity and inflammatory conditions.

Keywords: Functional activities of monocyte, phagocytosis and killing capacities, proinflammatory and antiinflammatory/ regulatory cytokines, respiratory burst, rituximab, type 1 diabetes.

[1]
Herold, K.C.; Usmani-Brown, S.; Ghazi, T.; Lebastchi, J.; Beam, C.A.; Bellin, M.D.; Ledizet, M.; Sosenko, J.M.; Krischer, J.P.; Palmer, J.P. β cell death and dysfunction during type 1 diabetes development in at-risk individuals. J. Clin. Invest., 2015, 125(3), 1163-1173.
[2]
Rabinovitch, A.; Suarez-Pinzon, W.L. Roles of cytokines in the pathogenesis and therapy of type 1 diabetes. Cell Biochem. Biophys., 2007, 48(2-3), 159-163.
[3]
Yoon, J.W.; Jun, H.S. Autoimmune destruction of pancreatic beta cells. Am. J. Ther., 2005, 12(6), 580-591.
[4]
Bradshaw, E.M.; Raddassi, K.; Elyaman, W.; Orban, T.; Gottlieb, P.A.; Kent, S.C.; Hafler, D.A. Monocytes from patients with type 1 diabetes spontaneously secrete proinflammatory cytokines inducing Th17 cells. J. Immunol., 2009, 183(7), 4432-4439.
[5]
Bendtzen, K.; Mandrup-Poulsen, T.; Nerup, J.; Nielsen, J.H.; Dinarello, C.A.; Svenson, M. Cytotoxicity of human pi 7 interleukin-1 for pancreatic islets of langerhans. Science, 1986, 232(4757), 1545-1547.
[6]
Aribi, M.; Moulessehoul, S.; Kendouci-Tani, M.; Benabadji, A.B.; Hichami, A.; Khan, N.A. relationship between interleukin-1beta and lipids in type 1 diabetic patients. Med. Sci. Monit., 2007, 13(8), CR372-CR378.
[7]
Azar, S.T.; Tamim, H.; Beyhum, H.N.; Habbal, M.Z.; Almawi, W.Y. Type I (insulin-dependent) diabetes is a th1- and th2-mediated autoimmune disease. Clin. Diagn. Lab. Immunol., 1999, 6(3), 306-310.
[8]
Calabrese, L.H.; Rose-John, S. IL-6 biology: Implications for clinical targeting in rheumatic disease. Nat. Rev. Rheumatol., 2014, 10(12), 720-727.
[9]
Semnani, R.T.; Mahapatra, L.; Moore, V.; Sanprasert, V.; Nutman, T.B. Functional and phenotypic characteristics of alternative activation induced in human monocytes by interleukin-4 or the parasitic nematode brugia malayi. Infect. Immun., 2011, 79(10), 3957-3965.
[10]
Pescovitz, M.D.; Greenbaum, C.J.; Krause-Steinrauf, H.; Becker, D.J.; Gitelman, S.E.; Goland, R.; Gottlieb, P.A.; Marks, J.B.; McGee, P.F.; Moran, A.M.; Raskin, P.; Rodriguez, H. Rituximab, b-lymphocyte depletion, and preservation of beta-cell function. N. Engl. J. Med., 2009, 361(22), 2143-2152.
[11]
Johnson, P.; Glennie, M. The mechanisms of action of rituximab in the elimination of tumor cells. Semin. Oncol., 2003, 30(1), 3-8.
[12]
Carter, P. Improving the efficacy of antibody-based cancer therapies. Nat. Rev. Cancer, 2001, 1(2), 118-129.
[13]
Stern, M.; Herrmann, R. Overview of monoclonal antibodies in cancer therapy: Present and promise. Crit. Rev. Oncol. Hematol., 2005, 54(1), 11-29.
[14]
Uchida, J.; Hamaguchi, Y.; Oliver, J.A.; Ravetch, J.V.; Poe, J.C.; Haas, K.M.; Tedder, T.F. The innate mononuclear phagocyte network depletes b lymphocytes through fc receptor-dependent mechanisms during anti-cd20 antibody immunotherapy. J. Exp. Med., 2004, 199(12), 1659-1669.
[15]
Ravetch, J.V. Fc receptors. Curr. Opin. Immunol., 1997, 9(1), 121-125.
[16]
Richardson, A.; Fedoroff, S. Quantification of cells in culture. In: Protocols for Neural Cell Culture; Humana Press: Totowa, NJ, 1997; pp. 219-233.
[17]
Kitamura, N.; Nishinarita, S.; Takizawa, T.; Tomita, Y.; Horie, T. Cultured human monocytes secrete fibronectin in response to activation by proinflammatory cytokines. Clin. Exp. Immunol., 2000, 120(1), 66-70.
[18]
Laverny, G.; Penna, G.; Vetrano, S.; Correale, C.; Nebuloni, M.; Danese, S.; Adorini, L. Efficacy of a potent and safe vitamin d receptor agonist for the treatment of inflammatory bowel disease. Immunology Letters., 2010, 131(1), 49-58.
[19]
Beum, P.V.; Kennedy, A.D.; Williams, M.E.; Lindorfer, M.A.; Taylor, R.P. The shaving reaction: Rituximab/CD20 complexes are removed from mantle cell lymphoma and chronic lymphocytic leukemia cells by thp-1 monocytes. J. Immunol., 2006, 176(4), 2600-2609.
[20]
Rafiq, S.; Butchar, J.P.; Cheney, C.; Mo, X.; Trotta, R.; Caligiuri, M.; Jarjoura, D.; Tridandapani, S.; Muthusamy, N.; Byrd, J.C. Comparative assessment of clinically utilized cd20-directed antibodies in chronic lymphocytic leukemia cells reveals divergent nk cell, monocyte, and macrophage properties. J. Immunol., 2013, 190(6), 2702-2711.
[21]
Diem, K.; Magaret, A.; Klock, A.; Jin, L.; Zhu, J.; Corey, L. Image analysis for accurately counting cd4+ and cd8+ t cells in human tissue. J. Virol. Methods, 2015, 222, 117-121.
[22]
Safi, W.; Kuehnl, A.; Nüssler, A.; Eckstein, H.H.; Pelisek, J. differentiation of human cd14+ monocytes: An experimental investigation of the optimal culture medium and evidence of a lack of differentiation along the endothelial line. Exp. Mol. Med., 2016, 48e227
[23]
Nouari, W.; Ysmail-Dahlouk, L.; Aribi, M. Vitamin d3 enhances bactericidal activity of macrophage against Pseudomonas aeruginosa. Int. Immunopharmacol., 2016, 30, 94-101.
[24]
Aribi, M. Macrophage bactericidal assays. Methods Mol. Biol., 2018, 1784, 135-149.
[25]
Guevara, I.; Iwanejko, J.; Dembińska-Kieć, A.; Pankiewicz, J.; Wanat, A.; Anna, P.; Gołbek, I.; Bartuś, S.; Malczewska-Malec, M.; Szczudlik, A. Determination of nitrite/nitrate in human biological material by the simple griess reaction. Clinica. Chimica. Acta, 1998, 274(2), 177-188.
[26]
Rouzaut, A.; Subirá, M.L.; de Miguel, C.; Domingo-de-Miguel, E.; González, A.; Santiago, E.; López-Moratalla, N. Co-expression of inducible nitric oxide synthase and arginases in different human monocyte subsets. apoptosis regulated by endogenous NO. Biochim. Biophys. Acta, 1999, 1451(2), 319-333.
[27]
Gitelman, H.J. An improved automated procedure for the determination of calcium in biological specimens. Anal. Biochem., 1967, 18(3), 521-531.
[28]
Aebi, H. Catalase. In: Methods of Enzymatic Analysis; Elsevier, 1974; pp. 673-684.
[29]
Olsen, C.H. Statistics in infection and immunity revisited. Infect. Immun., 2014, 82(3), 916-920.
[30]
Pedersen, A.E.; Jungersen, M.B.; Pedersen, C.D. Monocytes mediate shaving of b-cell-bound anti-cd20 antibodies. Immunology, 2011, 133(2), 239-245.
[31]
Xia, C.Q.; Liu, Y.; Guan, Q. Clare- Salzler, M.J. Antibody-Based And Cellular Therapies Of Type 1 Diabetes. In: Type 1 Diabetes; Escher, A., Ed.; InTech, 2013.
[32]
Xu, X.; Shi, Y.; Cai, Y.; Zhang, Q.; Yang, F.; Chen, H.; Gu, Y.; Zhang, M.; Yu, L.; Yang, T. Inhibition of increased circulating Tfh cell by anti-cd20 monoclonal antibody in patients with type 1 diabetes. PLoS ONE, 2013, 8(11)e79858
[33]
Bour-Jordan, H.; Bluestone, J.A. B cell depletion: A novel therapy for autoimmune diabetes? J. Clin. Invest., 2007, 117(12), 3642-3645.
[34]
Xiu, Y.; Wong, C.P.; Bouaziz, J.D.; Hamaguchi, Y.; Wang, Y.; Pop, S.M.; Tisch, R.M.; Tedder, T.F. B lymphocyte depletion by cd20 monoclonal antibody prevents diabetes in nonobese diabetic mice despite isotype-specific differences in fcγr effector functions. J. IMMUNOL., 2008, 180(5), 2863-2875.
[35]
Thomas, H.E.; Darwiche, R.; Corbett, J.A.; Kay, T.W.H. Interleukin-1 plus -interferon-induced pancreatic -cell dysfunction is mediated by -cell nitric oxide production. Diabetes, 2002, 51(2), 311-316.
[36]
Reiling, N.; Ulmer, A.J.; Duchrow, M.; Ernst, M.; Flad, H.D.; Hauschildt, S. Nitric oxide synthase: MRNA expression of different isoforms in human monocytes/macrophages. Eur. J. Immunol., 1994, 24(8), 1941-1944.
[37]
Cunningham, J.M.; Mabley, J.G.; Green, I.C. Interleukin 1beta-mediated inhibition of arginase in RINm5F cells. Cytokine, 1997, 9(8), 570-576.
[38]
Elliott, T.G.; Cockcroft, J.R.; Groop, P.H.; Viberti, G.C.; Ritter, J.M. Inhibition of nitric oxide synthesis in forearm vasculature of insulin-dependent diabetic patients: Blunted vasoconstriction in patients with microalbuminuria. Clin. Sci., 1993, 85(6), 687-693.
[39]
Rath, M.; Müller, I.; Kropf, P.; Closs, E.I.; Munder, M. Metabolism via arginase or nitric oxide synthase: Two competing arginine pathways in macrophages. Front. Immunol., 2014, 5(532)
[40]
Zhai, Z.; Solco, A.; Wu, L.; Wurtele, E.S.; Kohut, M.L.; Murphy, P.A.; Cunnick, J.E. Echinacea increases arginase activity and has anti-inflammatory properties in raw 264.7 macrophage cells, indicative of alternative macrophage activation. J. Ethnopharmacol., 2009, 122(1), 76-85.
[41]
Sato, Y.; Hotta, N.; Sakamoto, N.; Matsuoka, S.; Ohishi, N.; Yagi, K. Lipid peroxide level in plasma of diabetic patients. Biochem. Med., 1979, 21(1), 104-107.
[42]
Giugliano, D.; Ceriello, A.; Paolisso, G. Oxidative stress and diabetic vascular complications. Diabetes Care, 1996, 19(3), 257-267.
[43]
Veal, E.A.; Day, A.M.; Morgan, B.A. Hydrogen peroxide sensing and signaling. Mol. Cell, 2007, 26(1), 1-14.
[44]
Curtsinger, J.M.; Schmidt, C.S.; Mondino, A.; Lins, D.C.; Kedl, R.M.; Jenkins, M.K.; Mescher, M.F. Inflammatory cytokines provide a third signal for activation of naive CD4+ and CD8+ T cells. J. Immunol., 1999, 162(6), 3256-3262.
[45]
Tse, H.M.; Milton, M.J.; Piganelli, J.D. Mechanistic analysis of the immunomodulatory effects of a catalytic antioxidant on antigen-presenting cells: Implication for their use in targeting oxidation-reduction reactions in innate immunity. Free Radic. Biol. Med., 2004, 36(2), 233-247.
[46]
Ysmail-Dahlouk, L.; Nouari, W.; Aribi, M. 1,25-Dihydroxyvitamin D3 down-modulates the production of proinflammatory cytokines and nitric oxide and enhances the phosphorylation of monocyte-expressed stat6 at the recent-onset type 1 diabetes. Immunol. Lett., 2016, 179, 122-130.
[47]
Benghalem, I.; Meziane, W.; Hadjidj, Z.; Ysmail-Dahlouk, L.; Belamri, A.; Mouhadjer, K.; Aribi, M. High-density lipoprotein immunomodulates the functional activities of macrophage and cytokines produced during ex vivo macrophage-CD4+ T cell crosstalk at the recent-onset human type 1 diabetes. Cytokine, 2017, 96, 59-70.
[48]
Bunbury, A.; Potolicchio, I.; Maitra, R.; Santambrogio, L. Functional analysis of monocyte mhc class ii compartments. FASEB J., 2008, 23(1), 164-171.
[49]
McLeish, K.R.; Dean, W.L.; Wellhausen, S.R.; Stelzer, G.T. Role of intracellular calcium in priming of human peripheral blood monocytes by bacterial lipopolysaccharide. Inflammation, 1989, 13(6), 681-692.
[50]
Wright, B.; Zeidman, I.; Greig, R.; Poste, G. Inhibition of macrophage activation by calcium channel blockers and calmodulin antagonists. Cell. Immunol., 1985, 95(1), 46-53.
[51]
Guest, C.B.; Deszo, E.L.; Hartman, M.E.; York, J.M.; Kelley, K.W.; Freund, G.G. Ca2+/calmodulin-dependent kinase kinase alpha is expressed by monocytic cells and regulates the activation profile. PLoS ONE, 2008, 3(2)e1606
[52]
Ainscough, J.S.; Gerberick, G.F.; Kimber, I.; Dearman, R.J. Interleukin-1β processing is dependent on a calcium-mediated interaction with calmodulin. J. Biol. Chem., 2015, 290(52), 31151-31161.
[53]
Ramadan, J.W.; Steiner, S.R.; O’Neill, C.M.; Nunemaker, C.S. The central role of calcium in the effects of cytokines on beta-cell function: Implications for type 1 and type 2 diabetes. Cell Calcium, 2011, 50(6), 481-490.
[54]
Walshe, C.A.; Beers, S.A.; French, R.R.; Chan, C.H.T.; Johnson, P.W.; Packham, G.K.; Glennie, M.J.; Cragg, M.S. Induction of cytosolic calcium flux by CD20 is dependent upon b cell antigen receptor signaling. J. Biol. Chem., 2008, 283(25), 16971-16984.
[55]
Janas, E.; Priest, R.; Wilde, J.I.; White, J.H.; Malhotra, R. Rituxan (anti-CD20 antibody)-induced translocation of CD20 into lipid rafts is crucial for calcium influx and apoptosis. Clin. Exp. Immunol., 2005, 139(3), 439-446.
[56]
Wassmann, S.; Wassmann, K.; Nickenig, G. Modulation of oxidant and antioxidant enzyme expression and function in vascular cells. Hypertension, 2004, 44(4), 381-386.
[57]
Voetman, A.A.; Roos, D. Endogenous catalase protects human blood phagocytes against oxidative damage by extracellularly generated hydrogen peroxide. Blood, 1980, 56(5), 846-852.
[58]
Zhu, H.; Jia, Z.; Zhang, L.; Yamamoto, M.; Misra, H.P.; Trush, M.A.; Li, Y. Antioxidants and phase 2 enzymes in macrophages: Regulation by NRF2 signaling and protection against oxidative and electrophilic stress. Exp. Biol. Med., 2008, 233(4), 463-474.
[59]
Park, Y.S.; Uddin, M.J.; Piao, L.; Hwang, I.; Lee, J.H.; Ha, H. Novel role of endogenous catalase in macrophage polarization in adipose tissue. https://www.hindawi.com/journals/mi/2016/ 8675905/abs/ (accessed Apr 20, 2018)
[60]
Gabbay, M.A.L.; Sato, M.N.; Duarte, A.J.S.; Dib, S.A. Serum titres of anti-glutamic acid decarboxylase-65 and anti-ia-2 autoantibodies are associated with different immunoregulatory milieu in newly diagnosed type 1 diabetes patients. Clin. Exp. Immunol., 2012, 168(1), 60-67.
[61]
Trinanes, J.; Salido, E.; Fernandez, J.; Rufino, M.; Gonzalez-Posada, J.M.; Torres, A.; Hernandez, D. Type 1 diabetes increases the expression of proinflammatory cytokines and adhesion molecules in the artery wall of candidate patients for kidney transplantation. Diabetes Care, 2012, 35(2), 427-433.
[62]
Sanda, S.; Bollyky, J.; Standifer, N.; Nepom, G.; Hamerman, J.A.; Greenbaum, C. Short-term IL-1beta blockade reduces monocyte CD11B integrin expression in an IL-8 dependent fashion in patients with type 1 diabetes. Clin. Immunol., 2010, 136(2), 170-173.
[63]
Rabinovitch, A.; Suarez-Pinzon, W.L. Cytokines and their roles in pancreatic islet beta-cell destruction and insulin-dependent diabetes mellitus. Biochem. Pharmacol., 1998, 55(8), 1139-1149.
[64]
Dunn, A.J. Mechanisms by which cytokines signal the brain. Int. Rev. Neurobiol., 2002, 52, 43-65.
[65]
Karlsson Faresjo, M.G.E.; Ernerudh, J.; Ludvigsson, J. Cytokine profile in children during the first 3 months after the diagnosis of type 1 diabetes. Scand. J. Immunol., 2004, 59(5), 517-526.
[66]
Atkinson, M.A.; Eisenbarth, G.S.; Michels, A.W. Type 1 diabetes. Lancet, 2014, 383(9911), 69-82.
[67]
Durinovic-Bello, I. Autoimmune diabetes: The role of t cells, mhc molecules and autoantigens. Autoimmunity, 1998, 27(3), 159-177.
[68]
Kristiansen, O.P.; Mandrup-Poulsen, T. Interleukin-6 and diabetes: The good, the bad, or the indifferent? Diabetes, 2005, 54(Suppl. 2), S114-S124.
[69]
Campbell, I.L.; Kay, T.W.; Oxbrow, L.; Harrison, L.C. Essential role for interferon-gamma and interleukin-6 in autoimmune insulin-dependent diabetes in nod/wehi mice. J. Clin. Invest., 1991, 87(2), 739-742.
[70]
Chen, Y.M.; Chen, H.H.; Lai, K.L.; Hung, W.T.; Lan, J.L.; Chen, D.Y. The effects of rituximab therapy on released interferon- levels in the quantiferon assay among ra patients with different status of mycobacterium tuberculosis infection. Rheumatology, 2013, 52(4), 697-704.
[71]
Barr, T.A.; Shen, P.; Brown, S.; Lampropoulou, V.; Roch, T.; Lawrie, S.; Fan, B.; O’Connor, R.A.; Anderton, S.M.; Bar-Or, A.; Fillatreau, S.; Gray, D. B cell depletion therapy ameliorates autoimmune disease through ablation of IL-6-producing b cells. J. Exp. Med., 2012, 209(5), 1001-1010.
[72]
Monson, N.L.; Cravens, P.; Hussain, R.; Harp, C.T.; Cummings, M.; de Pilar Martin, M.; Ben, L.H.; Do, J.; Lyons, J.A.; Lovette-Racke, A.; Stüve, O.; Shlomchik, M.; Eagar, T.N. Rituximab therapy reduces organ-specific t cell responses and ameliorates experimental autoimmune encephalomyelitis. PLoS ONE, 2011, 6(2)e17103
[73]
Russell, M.A.; Morgan, N.G. The impact of anti-inflammatory cytokines on the pancreatic β-cell. Islets, 2014, 6(3)e950547
[74]
Xiong, X.; Barreto, G.E.; Xu, L.; Ouyang, Y.B.; Xie, X.; Giffard, R.G. Increased brain injury and worsened neurological outcome in interleukin-4 knockout mice after transient focal cerebral ischemia. Stroke, 2011, 42(7), 2026-2032.
[75]
Colotta, F.; Re, F.; Muzio, M.; Bertini, R.; Polentarutti, N.; Sironi, M.; Giri, J.G.; Dower, S.K.; Sims, J.E.; Mantovani, A. Interleukin-1 type ii receptor: A decoy target for IL-1 that is regulated by IL-4. Science, 1993, 261(5120), 472-475.
[76]
Byrne, A.; Reen, D.J. Lipopolysaccharide induces rapid production of IL-10 by monocytes in the presence of apoptotic neutrophils. J. Immunol., 2002, 168(4), 1968-1977.
[77]
Oishi, S.; Takano, R.; Tamura, S.; Tani, S.; Iwaizumi, M.; Hamaya, Y.; Takagaki, K.; Nagata, T.; Seto, S.; Horii, T.; Osawa, S.; Furuta, T.; Miyajima, H.; Sugimoto, K. M2 polarization of murine peritoneal macrophages induces regulatory cytokine production and suppresses t-cell proliferation. Immunology, 2016, 149(3), 320-328.
[78]
Sabat, R.; Grütz, G.; Warszawska, K.; Kirsch, S.; Witte, E.; Wolk, K.; Geginat, J. Biology of interleukin-10. Cytokine Growth Factor Rev., 2010, 21(5), 331-344.
[79]
Cope, A.; Le Friec, G.; Cardone, J.; Kemper, C. The Th1 life cycle: molecular control of IFN-γ to IL-10 switching. Trends Immunol., 2011, 32(6), 278-286.
[80]
de Waal Malefyt, R.; Abrams, J.; Bennett, B.; Figdor, C.G.; de Vries, J.E. Interleukin 10(IL-10) inhibits cytokine synthesis by human monocytes: An autoregulatory role of IL-10 produced by monocytes. J. Exp. Med., 1991, 174(5), 1209-1220.
[81]
Oswald, I.P.; Wynn, T.A.; Sher, A.; James, S.L. Interleukin 10 inhibits macrophage microbicidal activity by blocking the endogenous production of tumor necrosis factor alpha required as a costimulatory factor for interferon gamma-induced activation. Proc. Natl. Acad. Sci. USA, 1992, 89(18), 8676-8680.
[82]
Shalev, I.; Schmelzle, M.; Robson, S.C.; Levy, G. Making sense of regulatory t cell suppressive function. Semin. Immunol., 2011, 23(4), 282-292.
[83]
Gallo, P.; Gonçalves, R.; Mosser, D.M. The influence of IgG density and macrophage Fc (Gamma) receptor cross-linking on phagocytosis and IL-10 production. Immunol. Lett., 2010, 133(2), 70-77.
[84]
Vogelpoel, L.T.C.; Baeten, D.L.P.; de Jong, E.C.; den Dunnen, J. Control of cytokine production by human Fc gamma receptors: Implications for pathogen defense and autoimmunity. Front. Immunol., 2015, 6, 79.
[85]
Boruchov, A.M.; Heller, G.; Veri, M.C.; Bonvini, E.; Ravetch, J.V.; Young, J.W. Activating and inhibitory IgG Fc receptors on human dcs mediate opposing functions. J. Clin. Invest., 2005, 115(10), 2914-2923.
[86]
Delamaire, M.; Maugendre, D.; Moreno, M.; Le Goff, M.C.; Allannic, H.; Genetet, B. Impaired leucocyte functions in diabetic patients. Diabet. Med., 1997, 14(1), 29-34.
[87]
Wilson, R.M.; Reeves, W.G. Neutrophil phagocytosis and killing in insulin-dependent diabetes. Clin. Exp. Immunol., 1986, 63(2), 478-484.
[88]
Geerlings, S.E.; Hoepelman, A.I. Immune dysfunction in patients with diabetes mellitus (dm). FEMS Immunol. Med. Microbiol., 1999, 26(3-4), 259-265.
[89]
Church, A.K.; VanDerMeid, K.R.; Baig, N.A.; Baran, A.M.; Witzig, T.E.; Nowakowski, G.S.; Zent, C.S. Anti-CD20 monoclonal antibody-dependent phagocytosis of chronic lymphocytic leukaemia cells by autologous macrophages. Clin. Exp. Immunol., 2016, 183(1), 90-101.
[90]
Chao, M.P.; Alizadeh, A.A.; Tang, C.; Myklebust, J.H.; Varghese, B.; Gill, S.; Jan, M.; Cha, A.C.; Chan, C.K.; Tan, B.T.; Park, C.Y.; Zhao, F.; Kohrt, H.E.; Malumbres, R.; Briones, J.; Gascoyne, R.D.; Lossos, I.S.; Levy, R.; Weissman, I.L.; Majeti, R. Anti-CD47 antibody synergizes with rituximab to promote phagocytosis and eradicate non-hodgkin lymphoma. Cell, 2010, 142(5), 699-713.
[91]
Burd, J.F.; Usategui-Gomez, M. A colorimetric assay for serum lactate dehydrogenase. Clin. Chim. Acta, 1973, 46(3), 223-227.
[92]
Smith, S.M.; Wunder, M.B.; Norris, D.A.; Shellman, Y.G. A simple protocol for using a ldh-based cytotoxicity assay to assess the effects of death and growth inhibition at the same time. PLoS ONE, 2011, 6(11)e26908


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 19
ISSUE: 5
Year: 2019
Page: [643 - 655]
Pages: 13
DOI: 10.2174/1871530319666190215153213
Price: $58

Article Metrics

PDF: 22
HTML: 2