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Monocytes Activate Eosinophils for Enhanced Helminthotoxicity And

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Monocytes Activate Eosinophils for Enhanced Helminthotoxicity And © ELSEVIER Ann. Inst. PasteurlImmunol. Paris 1987 1987, 138, 97-116 MONOCYTES ACTIVATE EOSINOPHILS FOR ENHANCED HELMINTHOTOXICITY AND INCREASED GENERATION OF LEUKOTRIENE C4 by P. Eisas (1), T.H. Lee (2), H.L. Lenzi (3), and A.J. Dessein (1) (1) Centre d'Immunologie INSERM-CNRS de Marseille-Luminy, Case 906, 13288 Marseille Cedex 9 (France) (2) Guy's Hospital, London SEI 9RT (UK), and (3) Depto de Patologia, Fiocruz, Rio de Janeiro (Brazil) SUMMARY Recent observations have shown that eosinophils are activated in certain clinical conditions and that activation may enhance the role of eosinophils in immune protection against helminth parasites and in the pathogenesis of certain diseases associated with high eosinophilia. Our laboratory has attempted to identify the immunological mechanisms causing such an activation. The data summarized here show that eosinophils can be activated in vitro with supernatants of resting or stimulated monocytes. The supernatants enhance eosinophil helminthotoxicity by increasing cell degranulation; they also enhance the generation of leukotrienes in eosinophils by exerting a per• missive effect on an early step of arachidonic acid metabolism. Biochemical analysis of the enhancing activities suggests that they are car• ried by a unique molecule or a unique set of molecules whose biochemical and functional properties are different from those of previously described monokines such as IL-l, IFN-o:,~, CSF and TNF. Studies on individuals with chronic schistosomiasis suggest that such regulatory interactions between eosinophils and macrophages may take place in the hepatic granulomatous reactions in patients with hepatosplenic schistosomiasis. KEY-WORDS: Monocyte, Eosinophilia, Leukotriene, Allergy, Helmin• thotoxicity; Immunoregulation, Schistosomiasis. Received November 24, 1986. 98 P. ELSAS AND COLL. Introduction. The eosinophil leukocyte is located in the connective tissues under the epithelial layer of the skin, bronchi, gastrointestinal tract and the wall of the uterus [1]. In healthy individuals, only a small number of eosinophils, estimated at 11400 of the total eosinophil pool of the organism, circulate in the blood, where they remain for a short (3 to 8 h) period before entering the tissues. Most infections cause an increase in neutrophil number without increasing blood and tissue eosinophilia. Some bacterial infections cause eosinopenia (reviewed in [2]). Blood and tissue eosinophilia are markedly augmented in individuals with allergic diseases or with helminth infections [3]. In certain of these subjects, eosinophiIs represent up to 90 010 of the blood white cells and may be observed in large numbers in certain organs, i.e. in the bronchi of certain individuals undergoing allergic crisis or in parasitized tissue [2, 4]. The association between atopic diseases, helminthiasis and high eosinophilia have suggested that eosinophils take part in the regulation of allergic reac• tions, in particular in hypersensitivity type I reactions and in immune protec• tion against helminth parasites [2]. Eosinophils secrete a variety of mediators which might affect the development of the inflammation. The most impor• tant of these mediators are probably the 5-lipoxygenase metabolites of arachidonic acid: 5-hydroxyeicosatetraenoic acid (5-HETE) and leukotriene C4 (LTC4) [5-9]. 5-HETE is a potent chemotactic factor for neutrophils, LTC4 is a smooth muscle constrictor and a vasospastic and venopermeabili• ty factor [10-12]; LTC4, with its cysteinylglycyl and cysteinyl analogues LTD4 and LTE4, constitutes the activity previously termed slow-reacting substance of anaphylaxis [13]. A critical role of eosinophils in protective immunity against parasites is suggested by numerous studies: eosinophils are strongly helminthotoxic in vitro [14] and can be found attached and degranulating on disintegrated helminth larvae in tissues of immune-infected hosts [15]. Several eosinophil degranulation products such as the major basic protein (MBP), eosinophil cationic protein (ECP) and eosinophil peroxidase are highly toxic for the parasite, either because they dismember parasite tegument [16] or because they generate oxygen radicals [17]. AA arachidonic acid. HPLC high-performance liquid chroma• Ab antibody. tography. ADCC antibody-dependent cellular cytotoxicity. IFN interferon. C complement. IL-l interleukin-l. CSF colony-stimulating factor. LT leukotriene. EAF eosinophil-activating factor. MBP major basic protein. ECEF eosinophil cytotoxicity-enhancing MEM minimal essential medium. factor. MK monokine. ECP eosinophil cationic protein. NDGA nordihydroguaiaretic acid. EPO eosinophil peroxidase. PBMC peripheral blood mononuclear cell. HES hypereosinophilic syndrome. RP-HPLC reverse phase HPLC. HETE 5-hydroxyeicosatetraenoic acid. TNF tumour necrosis factor. MONOCYTES, EOSINOPHILS, HELMINTHS AND LTC4 99 Since eosinophils appear to be a major component of the host's response to helminth infections, factors modulating their helminthotoxic capacity have received much attention. Lymphokines secreted by cells from Schistosoma mansoni egg granulomas [18] and mast-cell-derived mediators, such as the eosinophil-chemotactic factor of anaphylaxis [19, 20, 21], were shown to poten• tiate the helminthotoxicity of eosinophils in vitro. Early reports have shown that eosinophils, in certain hypereosinophilic states such as in the hypereosinophilic syndrome (HES) or in tropical eosinophilia, appear sometimes degranulated and vacuolated [22, 23]. The proteins, normally stored in eosinophil granules, were detected in abnormal quantities in the blood of certain of these patients [24]. Since these substances are toxic for mammalian cells, it has been suggested that abnormal degranula• tion of the eosinophils in hypereosinophilic states may cause or aggravate organ damage associated with certain hypereosinophilia. More recently, eosinophils have also been implicated in the pathogenesis of certain asthmatic conditions. The mechanism(s) causing degranulation of eosinophils in hypereosino• philia is unknown. However, recent observations suggest that it may result from the activation of the cells: eosinophils from individuals with eosinophilia from various aetiological origins exhibit enhanced helminthotoxicity [25], low surface charge, augmented metabolism and high lysosomal enzymatic activities [26]. Finally, eosinophils from hypereosinophilic subjects could be fractionated on density gradients into two fractions, eosinophils in the less dense fraction demonstrated enhanced helminthotoxicity and altered oxidative metabolism, and they may represent an activated cell population [27]. The association between eosinophilia and eosinophil activation has sug• gested that eosinopoietic factors may have the dual function of stimulating stem cells and activating mature blood eosinophils. This hypothesis has received some support from the demonstration that semi-purified colony-stimulating factor (CFS-ex) of placental origin markedly enhanced the helminthotoxicity of blood eosinophils, probably by enhancing cell degranulation [28]. These observations have been recently confirmed and extended in experiments per• formed with cloned recombinant CSF-ex. During the course of the CSF studies, we observed that supernatants of resting PBMC also markedly enhanced eosinophil cytotoxicity. Further analysis of this phenomenon showed that it was caused by a monokine which exerts profound regulatory effects on several eosinophil functions. These studies and their possible biological implications are discussed here. Resting human blood mononuclear cells produce, in culture, factors which enhance ADCC by human blood eosinophils. Human peripheral blood mononuclear cells (PBMC) purified by centrifuga• tion of heparinized blood on «Ficoll Hypaque» were cultured (2 x 106 cells/ml) in serum-free defined medium; the supernatants were collected 24 h 100 P. ELSAS AND COLL. later and added to human eosinophils (5 III of conditioned medium for 106 eosinophils) which had been purified (> 85 0,10 pure; contaminating cells were neutrophils) from the blood of individuals with 2 to 15 % eosinophilia. After a short incubation period (5 to 60 min) in the conditioned medium, eosinophils were tested in an ADCC reaction on S. mansoni larvae in the presence of heat-inactivated human antischistosomular antibodies. At low Ab concen• trations, control medium-treated eosinophils only adhered in small numbers to the larvae (fig. 1) and killed a small fraction (2 to 10 %) of schistosomula (fig. 2). In contrast, eosinophils treated with the conditioned media adhered in large numbers to schistosomula and demonstrated high helminthotoxicity (40 to 80 %). PBMC supernatants were not toxic for the larvae, as assessed by microscopic examination and maturation of worms when injected in A B o o o e " FIG. 1. - Enhancement oj eosinophil adherence to Ab-coated schistosomula by blood mononuclear eel/-conditioned medium. Eosinophils purified on metrizamide gradients were incubated for 30 min with a 1/5 dilution of control medium (A) or mononuclear cell-conditioned medium (B) and added to Ab• coated schistosomula. Pictures were taken 90 min later. The conditioned medium was prepared by culturing 2 x 106 human blood mononuclear cells/ml of serum-free medium for 24 h. MONOCYTES, EOSINOPHILS, HELMINTHS AND LTC4 101 mice [29, 30]. The factor(s) causing enhancement of eosinophil cytotoxicity was termed ECEF (eosinophil cytotoxicity-enhancing factor). Control eosinophils neither adhered to nor killed schistosomula in the
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