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Immunomodulatory Effects of the Tityus Serrulatus Venom on Murine Macrophage Functions in Vitro

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Immunomodulatory Effects of the Tityus Serrulatus Venom on Murine Macrophage Functions in Vitro Mediators of Inflammation • 2005:1 (2005) 39–49 • PII: S0962935104409272 • DOI: 10.1155/MI.2005.39 RESEARCH COMMUNICATION Immunomodulatory Effects of the Tityus serrulatus Venom on Murine Macrophage Functions in Vitro Vera L. Petricevich1, 2 and Ivo Lebrun3 1Facultad de Medicina de la Universidad Autonoma del Estado de Morelos, 62210 Cuernavaca, Mexico 2Immunochemistry Laboratory, Butantan Institute, 055503-900 Sao˜ Paulo, Brazil 3Biochemistry and Biophysics Laboratory, Butantan Institute, 055503-900 Sao˜ Paulo, Brazil Received 27 September 2004; accepted 29 October 2004 Tityus serrulatus scorpion venom (TSV) consists of a very complex mixture of molecules and demonstrates significant immunomod- ulatory activities capable of stimulating immune functions in vivo. The purpose of this study was to compare the crude TSV with fractionated toxins extracted from this venom in order to determine which toxin(s) presented immunomodulatory effects on peri- toneal macrophages. TSV was fractionated using gel filtration chromatography resulting in 5 heterogeneous fractions. The effects of these different fractions were analysed in vitro using detection by means of cytokines, oxygen intermediate metabolites (H2O2), and nitric oxide (NO) in supernatants of peritoneal macrophages. Several functional bioassays were employed: tumor necrosis factor (TNF) activity was assayed by measuring its cytotoxic activity in L929 cells, and other cytokines were assayed by enzyme-linked immunosorbent assay, whereas NO levels were detected by Griess colorimetric reactions in culture supernatant of macrophages exposedtodifferent fractions. In vitro studies revealed that all fractions studied here presented an increment in H2O2, NO, and cytokines levels. The more pronounced increments were observed in macrophage cultures exposed to fraction FII which demon- strated that (a) the highest levels of IL-1α,IL-β, and TNF were observed after 12 hours and that (b) the maximum levels of IFN-γ and NO were observed after 72 hours. Taken together, these data indicate that fractions have a differential immunomodulating effect on macrophage secretion, and that FII is a potent activator of TNF production of macrophages. INTRODUCTION among humans [2, 3]. The most thoroughly studied as- pects consist of the isolation, chemical, and physiological Scorpion venoms consist of a complex of several tox- characterization of these toxic peptides [4, 5, 6]. ins that exhibit a wide range of biological properties and Victims of envenoming by a scorpion suffer a va- actions, as well as chemical compositions, toxicity, and riety of pathologies, involving mainly both sympathetic pharmacokinetic and pharmacodynamic characteristics. (tachycardia, hypertension, sweating, and mydriasis) and Tityus serrulatus is considered one of the most dan- parasympathetic (bradycardia, hypotension, secretions, gerous species to humans in Brazil and is responsible for and miosis) stimulation as well as central manifestations many clinical cases of envenomation in the southern re- such as irritability, hyperthermia, vomiting, tremor, and gion of this country. This venom is capable of exerting convulsion. Experimental studies have shown that the avarietyofeffects on excitable tissues, due to its role in injection of whole venom and purified toxins from the the peripheral nervous system where it enhances the re- venom Tserrulatuscan cause profuse salivation [7], in- lease of neurotransmitters [1]. The information presented creased gastric [8] and pancreatic secretion [9], acute gas- here deals with biological, chemical, and immunological tric mucosal [10] and pancreatic [1, 9] injuries, as wells aspects of different toxins and offers a comparison and as disorders in intestinal motility [1]. In order to address an assessment of these, as observed in the symptoms pre- these issues, basic information needs to be obtained from sented in mice from the most dangerous species of Brazil- representative experiments on animal models using ade- ian scorpions: Tserrulatus.Thisspeciesisfoundinanim- quate venom samples as it is necessary to apply inflam- mense geographical area of the country and represents an matory inducers. Previous studies have shown that dif- important public health problem causing fatal accidents ferential susceptibility to venom depends on the strain of mice used [11, 12]. It is well established that the predom- inant lethal action of scorpion venom exerts a variety of Correspondence and reprint requests to Vera L. Petricevich, effects on excitable tissues. In the case of snake venoms, it Facultad de Medicina de la Universidad Autonoma del Estado is well known that levels of lethality and toxicity exhibit de Morelos, 62210 Cuernavaca, Mexico; [email protected] enormous variety according to the age, sex, nutritional © 2005 Hindawi Publishing Corporation 40 V. L. Petricevich and I. Lebrun 2005:1 (2005) state, and geographic regions where the animals were cap- sciences Pharmingen (Calif), and recombinant TNF was tured [13]. To minimise the experimental bias, BALB/c purchased from Boehringer Mannheim (Mannheim, Ger- mice and a mixture of Tserrulatusvenom obtained from many). 40 adult specimens, all from the same geographic region, were used throughout all experiments. Scorpion venom Macrophages have been shown to be involved Tserrulatusscorpions were provided by the in different homeostatic mechanisms and pathological Artropodes Laboratory, Butantan Institute (SP, Brazil). events, and may be engaged in complex interactions. The venom was obtained by electrostimulation using Macrophages are involved in several areas of body func- the method previously described [20]. Fifty mg of crude tion, such as phagocytosis, enzyme liberation, free radical dried venom was solubilized in ammonium acetate buffer, generation, and as mediators of inflammatory processes. pH 4.7, and centrifuged at 1 5000 Xg for 30 minutes, here Cytokine release by macrophages has shown that excessive named TSV(—), without glycoproteins, and fraction G or insufficient production may significantly contribute to was named the nontoxic fraction. Soluble venom from T the pathophysiology of a range of diseases [14, 15, 16, 17]. serrulatus was applied to a Sephadex G-50 Superfine and Generally, the treatment of macrophages with lead re- eluted with 20 mM ammonium acetate buffer, pH 4.7. sults in the disregulation of the production of inflamma- The fractions were collected using an automatic collector tory cytokines, tumor necrosis factor (TNF), interleukin- (Pharmacia-LKB Frac-100). Fractions were pooled ac- 1 (IL-1), and IL-6, and preferential production of the cording to the absorbance profile at 280 nm and assayed TH1 type of cytokines interferon-gamma (IFN-γ)andIL- for toxicity. The five fractions obtained here are named as 2. In the case of crude scorpion venom, the treatment fractions FI, FII, FIII, FIV, and FV which correspond to of macrophages results in the production of inflamma- 18.6%, 31.4%, 21.3%, 24.4%, and 4.3%, respectively. tory cytokines [18]. It is widely acknowledged that in cy- tokines, a diverse group of proteins are important for the Animals regulation of inflammatory responses as well as in the generation of immunity to pathogens. Interaction with BALB/c female mice (18–20 g), obtained from the Bu- venom causes the secretion of a variety of cytokines by tantan Institute, were used throughout the study to test macrophages. However a detailed description of the in- the lethality of the venom and its components. Different duction of these cytokines by venoms is still unclear even fractions containing 50 µg of protein diluted in the ap- though various studies regarding cytokine induction by propriate buffers were assayed by intraperitoneal (IP) in- these toxins as well as by infection have been reported jection. Intoxicated animals usually showed the following [18, 19]. symptoms: tremor, salivation, diarrhoea, and death. Mice TSV is involved in immunomodulation, although the were maintained and used according to animal welfare in- mechanism for this activity has not been fully elucidated. ternational recommendations of the International Society This study was designed to determine the most impor- on Toxicology, 1992 [21]. tant toxin obtained from venom which causes the im- munomodulatory activity. Here for the first time we de- Stimulation of mice peritoneal macrophages ff scribed in detail the e ect of purified fractions extracted Groups of mice from BALB/c were sacrificed and from TSV on the production of cytokines and nitric ox- their cells were harvested by peritoneal lavage [22]. The ide (NO) production and on macrophage activation. Im- peritoneal cavity was injected with 5 mL of cold RPMI- ff munomodulatory e ects induced by these fractions on 1640. The fluid-distended peritoneal cavity was massaged, NO production and macrophage activation were com- and the cells were collected and washed three times by pared with those obtained from the cells stimulated with centrifugation at 290 Xg for 5 minutes. The cells were γ IFN- . seeded in 96-well microtiter plates at a concentration of 1 × 106 cells/mL and cultured in RPMI-1640 medium MATERIALS AND METHODS supplemented with 10% FCS. After incubation at 37◦C for 2 hours in humidified 5% CO2, the plates were then Chemicals, reagents, and buffers washed twice with RPMI-1640 medium to remove non- Actinomycin D, orthophenyldiamine (OPD), and ni- adherent cells and the adherent cells were referred to as tric oxide (NO) were purchased from Sigma (St. Louis, macrophages. More than 95% of the cells was identified Mo),
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