Gene Expression Profiling of The Budding Yeast S. Cerevisiae Upon Exporsure to The Pesticide Atrazine


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Atrazine (ATR; 2-chloro-4-ethylamino-6-isopropylamino-s-triazine), a chlorinated triazine, has been one of the most heavily used herbicides in the world. It is used to control a variety of broadleaf weeds and grasses and as a result of its widespread use and moderate persistence, it has been identified as a principal contaminant of surface waters [1]. It can be present at several parts per million in agricultural runoff and can reach 40 parts per billion (ppb) in precipitation [2]. Atrazine inhibits photosynthesis of most plants by inhibiting electron transfer at the reducing site of chloroplast complex II [3]. Its mode of action involves competition for binding to the QB protein (32-kDa protein) with plastoquinone in photosystem II [4, 5].

Human exposure to atrazine has been confirmed in several studies and, for example, it is estimated that around 60% of the U.S. population is exposed to atrazine [6]. Epidemiologic studies have linked environmental and/or occupational ATR exposure to increased mortality [7] and to non-Hodgkin’s lymphoma [8]. The understanding of the role of ATR in such processes is fairly limited. However, in experimental models several data point towards hormonal and reproductive system effects of ATR. In rodents reported effects include reduction of testosterone levels [9], a disruption of regular ovarian cycles, and the induction of pseudopregnacies [10]. ATR has also been shown to affect the sexual development of frog larvae exposed to it at very low concentrations (0.1 ppb) and to decrease the testosterone levels in sexually mature frog males when exposed to 25 ppb of atrazine [2]. Very recently it has been shown that sustained exposure of male rats to low level of ATR can cause neurotoxicity in the dopaminergic systems of the brain [11] that are critical for the mediation of movement as well as cognition, thus suggesting
that ATR may be an environmental risk factor that contributes to neurodegenerative diseases associated with these systems, such as Parkinson’s disease and schizophrenia.

Atrazine has been banned in the EU following the report of it causing sexual differentiation in frog at 0.1 ppb [2] (Commission Decision of 10 March 2004 concerning the non-inclusion of atrazine in Annex I to Council directive 91/414/EEC and the withdrawal of authorization for plant protection products containing this active substance. OJ, L78, 53-55).

In this report we describe the results of the measurement and the analysis of gene expression profiling of the budding yeast Saccharomyces cerevisiae exposed to low concentrations of atrazine. Gene expression is a sensitive indicator of toxicant exposure, disease state, and cellular metabolism and thus it represents a unique way of characterizing how cells and organisms adapt to changes in the external environment [12]. The measurement of gene expression levels, upon exposure to a chemical, can be used both to provide information about the mechanism of action of toxicants, and also to form a sort of “genetic signature” from the pattern of gene expression changes it causes both in vitro [13, 14] or in vivo [15].

DNA microarray technology has been extensively applied to the analyses of natural and anthropogenic factors in yeast for which whole genome chips have been available for a few years [16-18]. Causton and colleagues [17] analyzed how the whole genome of yeast is remodeled in response to environmental stressors such as temperature, pH, oxidation, and nutrients. The stress response was dependent on the level of the stress and showed an additive effect for multiple stressors. The same approach has been used to characterize the alteration of gene expression in yeast
induced by the pesticide thiuram [19].

The goal of this study was to analyze the effect of atrazine exposure at low concentrations on a eukaryotic organism with the objective to identify potential biomarkers of atrazine exposure at environmentally relevant concentrations. The
budding yeast Saccharomyces cerevisiae is an excellent model to study stressassociated gene expression response [20]. This is due to the possibility of monitoring the transcriptional activity of the whole genome in a single experiment combined with relatively simple culturing procedures. For example this organism as been successfully used to develop a test to detect chronic toxicity effects of exposure to heavy metals as a diagnostic tool within aquatic biota [21].

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