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In Vitro Effects of Chlorpyrifos, Parathion, Methyl Parathion and Their Oxons on Cardiac Muscarinic Receptor Binding in Neonatal and Adult Rats

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In Vitro Effects of Chlorpyrifos, Parathion, Methyl Parathion and Their Oxons on Cardiac Muscarinic Receptor Binding in Neonatal and Adult Rats Toxicology 170 (2002) 1–10 www.elsevier.com/locate/toxicol In vitro effects of chlorpyrifos, parathion, methyl parathion and their oxons on cardiac muscarinic receptor binding in neonatal and adult rats Marcia D. Howard a, Carey N. Pope b,* a Department of Toxicology, College of Pharmacy, The Uni6ersity of Louisiana at Monroe, Monroe, LA 71209, USA b Department of Physiological Sciences, College of Veterinary Medicine, 264 McElroy Hall, Oklahoma State Uni6ersity, Stillwater, OK 74078, USA Received 7 June 2001; received in revised form 8 August 2001; accepted 15 August 2001 Abstract Organophosphorus insecticides elicit toxicity by inhibiting acetylcholinesterase. Young animals are generally more sensitive than adults to these toxicants. A number of studies reported that some organophosphorus agents also bind directly to muscarinic receptors, in particular the m2 subtype, in tissues from adult rats. As both the density and agonist affinity states of cardiac muscarinic receptors (primarily m2) have been reported to change in an age-related manner, we evaluated the relative in vitro sensitivity of cardiac muscarinic receptors in tissues from neonatal (7–11 days of age) and adult (90 days of age) rats to selected organophosphorus compounds (chlorpyrifos, parathion, methyl parathion and their oxygen analogs or oxons). The effects of the cholinergic agonist carbachol (100 pM–5 mM) or an organophosphorus toxicant (50 pM–10 mM) on muscarinic receptor binding were determined using the 3 3 nonselective muscarinic ligand [ H]quinuclidinyl benzilate or the m2-preferential ligand [ H]oxotremorine-M acetate. Carbachol displaced [3H]oxotremorine labeling in adult and neonatal membranes in a relatively similar manner 3 (IC50 =7–20 nM). The oxons all displaced [ H]oxotremorine binding in a concentration-dependent manner, with chlorpyrifos oxon being the most potent (IC50: neonates, 15 nM; adults, 7 nM) and efficacious (maximum displacement: neonates, 42%; adults, 56%). Interestingly, methyl parathion was an extremely potent displacer of 3 [ H]oxotremorine binding in adult tissues (IC50 =0.5 nM, maximum displacement=37%) but had no effect in neonatal tissues. The displacement of [3H]oxotremorine binding by chlorpyrifos oxon (10 mM) was still apparent after washing the tissues, suggesting the oxon irreversibly blocked agonist binding to the receptor while interaction with MePS appeared reversible. As effective concentrations of the oxons were relatively similar to their anticholinesterase potencies, these findings suggest that direct interaction with cardiac muscarinic receptors by some organophosphorus agents may occur at relevant exposure levels and contribute to cardiac toxicity. © 2002 Elsevier Science Ireland Ltd. All rights reserved. Keywords: Organophosphates; Cardiac; Age-related; Insecticides; Mechanism; Acetylcholinesterase inhibition * Corresponding author. Tel.: +1-405-744-6257; fax: +1-405-744-0462. E-mail address: [email protected] (C.N. Pope). 0300-483X/02/$ - see front matter © 2002 Elsevier Science Ireland Ltd. All rights reserved. PII: S0300-483X(01)00498-X 2 M.D. Howard, C.N. Pope / Toxicology 170 (2002) 1–10 1. Introduction of muscle contraction. While m2 receptors are thought to be the primary subtype of muscarinic Pesticides are unique contaminants in that they receptors in the heart, all subtypes (m1 –m5) have are intentionally released into the environment to been recently identified in human heart (Wang et elicit toxicity in certain ‘pest’ species. Unfortu- al., 2001). nately, a lack of selectivity often leads to prob- The OP insecticides examined in this study are lems of toxicity in humans and other non-target phosphorothioate compounds that must be con- species. Organophosphorus (OP) pesticides are verted by cytochrome P450 enzymes to their re- the major chemical class of insecticides used in the spective oxons to elicit cholinergic toxicity world today (Aspelin, 1994; Bardin et al, 1994). (Sultatos, 1994). While all OP insecticides are Coye et al. (1987) reported that OP insecticides thought to act through a common mechanism were the most frequently involved pesticides in initiated by inhibition of AChE, differential ex- non-occupational poisonings in the state of Cali- pression of toxicity following similar changes in fornia. Organophosphorus poisonings continue to acetylcholinesterase activity have been reported be a major cause of morbidity and mortality in (Chaudhuri et al., 1993; Pope et al., 1995; Liu and third world countries (Peter and Cherian, 2000). Pope, 1998). Differential effects in the presence of The primary mode of action for OP pesticides is similar changes in acetylcholinesterase activity initiated through inhibition of acetylcholinesterase could be the result of direct or indirect actions at (AChE, E.C. 3.1.1.7), the enzyme responsible for macromolecular targets other than AChE (Bakry degrading the neurotransmitter acetylcholine et al., 1988; Silveira et al., 1990; Jett et al., 1991; (Saunders and Harper, 1994; Brown and Taylor, Ward et al., 1993; Huff et al., 1994; Huff and 1996; Pope, 1999). Excessive acetylcholine (ACh) Abou-Donia, 1995; Ward and Mundy, 1996; accumulation due to enzyme inhibition results in Pope, 1999). Several studies suggest that some overstimulation of cholinergic receptors and signs OPs can bind directly to the m2 muscarinic recep- of cholinergic toxicity such as salivation, lacrima- tor and function as an agonist (Bakry et al., 1988; tion, urination and defecation (SLUD), bradycar- Silveira et al., 1990; Huff et al., 1994; Ward and dia, miosis, nausea, and respiratory dysfunction Mundy, 1996; Van Den Beukel et al., 1997). As (Ecobiochon, 1996). Cholinergic receptors can be the heart expresses predominately m2 receptors, divided into nicotinic (nAChR) and muscarinic this organ system could be particularly sensitive (mAChR) subclasses. Five muscarinic receptor to such direct actions of some OP agents (Kellar subtypes, referred to as m1 –m5, have been iden- et al., 1985; Sharma et al., 1997). In contrast to tified through molecular cloning (Brown and Tay- brain, where muscarinic receptor density increases lor, 1996) and four muscarinic receptor subtypes during postnatal maturation, cardiac muscarinic have been pharmacologically identified using receptor density declines with maturation. In ad- [3H]ACh binding (Alberts et al., 1994). dition, age-related differences in the ability of Muscarinic receptors belong to the largest su- cardiac muscarinic receptors to convert from high perfamily of cell-surface receptors, i.e. those to low affinity states have been reported (Baker et linked to G proteins: m1,m3 and m5 subtypes are al. 1985; McMahon, 1989) generally coupled to stimulation of phospholipase Generally, young animals are more sensitive Candm2 and m4 subtypes are linked to inhibition than adults to acute OP insecticide toxicity of adenylyl cyclase (Alberts et al., 1994; Brown (Brodeur and DuBois, 1963; Benke and Murphy, and Taylor, 1996). The G-protein coupled mus- 1975; Pope et al., 1991; Atterberry et al., 1997; carinic receptors contain seven hydrophobic seg- Zheng et al., 2000). The possibility of higher ments, 20–30 amino acids long, spanning the sensitivity in children to some pesticides in part phospholipid bilayer (Peralta et al., 1987; Bonner, led to the enactment of the US Food Quality 1989; Alberts et al., 1994). Muscarinic receptors in Protection Act (FQPA), requiring an additional the heart are intimately involved in cardiac func- safety factor in the risk assessment process and an tion, dynamically regulating force and frequency explicit determination that tolerances were safe M.D. Howard, C.N. Pope / Toxicology 170 (2002) 1–10 3 for children (FQPA, 1996). Immature animals are tained on 12-h light:12-h dark cycle and were fed more sensitive to the acute toxicity of chlorpyrifos food and water ad libitum. (CPF), parathion (PS) and methyl parathion (MePS) (Benke and Murphy, 1975; Pope et al., 2.3. Tissue collection, membrane preparation and 1991; Moser et al., 1998). We evaluated possible biochemical assay age-related differences in direct interaction be- tween CPF, PS, MePS and their oxons (CPFO, Following decapitation, hearts were quickly ex- PO and MePO, respectively) and cardiac mus- cised and rinsed in 10 mM Tris buffer, pH 7.4 carinic receptors. Our findings suggest that car- (25 °C) containing 1 mM EDTA (McMahon, diac muscarinic receptors may be particularly 1989). After removal of connective tissue and sensitive to low levels of some OP toxicants, and blood vessels, both atria and ventricles were that these direct interactions between receptors minced and frozen at −70 °C until time of assay. and OP agents could contribute to age-related Cardiac membranes were prepared according to and OP-selective toxicity. the method of Silveira et al. (1990). Briefly, hearts were rinsed in ice-cold saline, blotted dry and homogenized (1:15 in 5 mM Hepes, pH 7.4) four 2. Materials and methods times for 30 s (25 000 rpm, Polytron, Brinkmann Instruments, Westbury, NY), with a 1-min pause 2.1. Chemicals between homogenizations. Homogenized tissues were then centrifuged for 10 min at 1000×g All OP toxicants were purchased from Chem (4 °C) and the resulting supernatant was subse- Service (West Chester, PA; ]97% purity). quently centrifuged for 45 min at 40 000×g.The 3 [ H]oxotremorine-M acetate (specific activity P2 pellet was resuspended with 10 strokes using a 85.8–86.4 Ci/mmol; OXO), and [3H]quinuclidinyl Dounce homogenizer and membranes were used benzilate (specific activity
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