Early life permethrin insecticide treatment leads to heart damage in adult rats

Early life environmental exposure to xenobiotics could represent a critical period for the onset of permanent alterations in the structure and function of different organs. Cardiovascular diseases can be related to various factors including environmental toxicants. The aim of the present study was to evaluate the effect of early life permethrin treatment (1/50 LD(50), from 6th to 21st day of life) on heart of adult rats. Increased DNA damage, decreased heart cell membrane fluidity, increased cholesterol content, protein and lipid oxidation were measured in heart cells from adult rats treated with permethrin during the neonatal period with respect to control rats. Moreover, the same group showed higher levels of cholesterol, IL-1β, IL-2, IFN-γ, rat-Rantes and IL-10 cytokines and decreased albumin content in plasma. Lower cholesterol levels and perturbation in the phospholipid lateral diffusion together with decreased GSH levels and increased GPx activity were measured in heart mitochondria of the treated group. Our findings support the evidence that the neonatal period has a critical role in the development of heart disease in adulthood. We hypothesize that the alterations observed in adult rats could depend on epigenetic changes that occurred during this period which influence gene expression throughout the rat's life, leading to alterations of certain parameters related to cardiac function.

[1]  S. Liu,et al.  Involvement of ceramide in inhibitory effect of IL-1 beta on L-type Ca2+ current in adult rat ventricular myocytes. , 1997, The American journal of physiology.

[2]  T. Ohe,et al.  Elevated levels of oxidative DNA damage in serum and myocardium of patients with heart failure. , 2006, Circulation Journal.

[3]  K. Matsumoto,et al.  Oxidized LDL-induced NF-kappa B activation and subsequent expression of proinflammatory genes are defective in monocyte-derived macrophages from CD36-deficient patients. , 2000, Arteriosclerosis, thrombosis, and vascular biology.

[4]  D. Barker.  Fetal and infant origins of adult disease , 2001, Monatsschrift Kinderheilkunde.

[5]  R. Gabbianelli,et al.  Different effects of Type I and Type II pyrethroids on erythrocyte plasma membrane properties and enzymatic activity in rats. , 2003, Toxicology.

[6]  Robert B. Gennis,et al.  Biomembranes: Molecular Structure and Function , 1988 .

[7]  Manoel Luis Costa,et al.  Membrane Cholesterol Depletion by Methyl-β-Cyclodextrin Enhances the Expression of Cardiac Differentiation Markers , 2010, Cells Tissues Organs.

[8]  Wayland J. Hayes,et al.  Pesticides studied in man , 1982 .

[9]  K. Nagata,et al.  Xanthine oxidase inhibition improves left ventricular dysfunction in dilated cardiomyopathic hamsters. , 2008, Journal of cardiac failure.

[10]  M. Takahashi,et al.  Estimation of lipid peroxidation of live cells using a fluorescent probe, diphenyl-1-pyrenylphosphine. , 2001, Free radical biology & medicine.

[11]  C. Relton,et al.  Epigenetics and child health: basic principles , 2010, Archives of Disease in Childhood.

[12]  A. Tall,et al.  Interleukin 8 Is Induced by Cholesterol Loading of Macrophages and Expressed by Macrophage Foam Cells in Human Atheroma (*) , 1996, The Journal of Biological Chemistry.

[13]  Madhur M. Gupta,et al.  Lipid peroxidation and glutathione peroxidase in ischemic heart disease , 2001, Indian Journal of Clinical Biochemistry.

[14]  S. Liu,et al.  G protein-mediated suppression of L-type Ca2+ current by interleukin-1 beta in cultured rat ventricular myocytes. , 1995, The American journal of physiology.

[15]  R. Gabbianelli,et al.  Lymphocyte DNA damage in rats exposed to pyrethroids: effect of supplementation with Vitamins E and C. , 2004, Toxicology.

[16]  D. Epps,et al.  Mitochondrial cholesterol content and membrane properties in porcine myocardial ischemia. , 1982, The American journal of physiology.

[17]  V. Mehra,et al.  Cytokines and cardiovascular disease , 2005, Journal of leukocyte biology.

[18]  Y. Barenholz,et al.  Fluidity parameters of lipid regions determined by fluorescence polarization. , 1978, Biochimica et biophysica acta.

[19]  Cinzia Nasuti,et al.  Dopaminergic system modulation, behavioral changes, and oxidative stress after neonatal administration of pyrethroids. , 2007, Toxicology.

[20]  M. Inoue,et al.  Effect of permethrin insecticide on rat polymorphonuclear neutrophils. , 2009, Chemico-biological interactions.

[21]  P. Nguyen,et al.  Perinatal undernutrition-induced obesity is independent of the developmental programming of feeding , 2009, Physiology & Behavior.

[22]  W. Valentine,et al.  Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. , 1967, The Journal of laboratory and clinical medicine.

[23]  Claudia Bolognesi,et al.  Genotoxicity of pesticides: a review of human biomonitoring studies. , 2003, Mutation research.

[24]  Q. Xia,et al.  Influence of interleukin-2 on Ca2+ handling in rat ventricular myocytes. , 2003, Journal of molecular and cellular cardiology.

[25]  I. Roberts‐Thomson,et al.  Glutathione concentrations and glutathione S‐transferase activity in human colonic neoplasms , 1994, Journal of gastroenterology and hepatology.

[26]  Michael Weis,et al.  Role of cytokines in cardiovascular diseases: a focus on endothelial responses to inflammation. , 2005, Clinical science.

[27]  Effects of early weaning on the circadian rhythm and behavioral satiety sequence in rats , 2011, Behavioural Processes.

[28]  J. A. Vale,et al.  Poisoning due to Pyrethroids , 2005, Toxicological reviews.

[29]  W. Bablok,et al.  A New Biometrical Procedure for Testing the Equality of Measurements from Two Different Analytical Methods. Application of linear regression procedures for method comparison studies in Clinical Chemistry, Part I , 1983, Journal of clinical chemistry and clinical biochemistry. Zeitschrift fur klinische Chemie und klinische Biochemie.

[30]  A. Collins,et al.  The nature and origin of DNA single-strand breaks determined with the comet assay. , 1998, Mutation research.

[31]  S. Verma,et al.  DNA damage repair and cardiovascular diseases. , 2010, The Canadian journal of cardiology.

[32]  R. Gabbianelli,et al.  Effect of permethrin plus antioxidants on locomotor activity and striatum in adolescent rats. , 2008, Toxicology.

[33]  I. Fridovich,et al.  The generation of superoxide radical during the autoxidation of hemoglobin. , 1971, The Journal of biological chemistry.

[34]  J. Novotný,et al.  G proteins, beta-adrenoreceptors and beta-adrenergic responsiveness in immature and adult rat ventricular myocardium: influence of neonatal hypo- and hyperthyroidism. , 1999, Journal of Molecular and Cellular Cardiology.

[35]  Hai-Tao He,et al.  Dynamics in the plasma membrane: how to combine fluidity and order , 2006, The EMBO journal.

[36]  R. Gabbianelli,et al.  Permethrin induces lymphocyte DNA lesions at both Endo III and Fpg sites and changes in monocyte respiratory burst in rats , 2009, Journal of applied toxicology : JAT.

[37]  P. Ferdinandy,et al.  Peroxynitrite is a major contributor to cytokine-induced myocardial contractile failure. , 2000, Circulation research.

[38]  Alexander Vaiserman,et al.  Early-life origin of adult disease: Evidence from natural experiments , 2011, Experimental Gerontology.

[39]  E Gratton,et al.  Quantitation of lipid phases in phospholipid vesicles by the generalized polarization of Laurdan fluorescence. , 1991, Biophysical journal.

[40]  J. Novotný,et al.  G Proteins,β-Adrenoreceptors andβ-Adrenergic Responsiveness in Immature and Adult Rat Ventricular Myocardium: Influence of Neonatal Hypo- and Hyperthyroidism , 1999 .

[41]  G. Lenaz,et al.  The primary role of glutathione against nuclear DNA damage of striatum induced by permethrin in rats , 2010, Neuroscience.

[42]  O. H. Lowry,et al.  Protein measurement with the Folin phenol reagent. , 1951, The Journal of biological chemistry.

[43]  B. Lentz,et al.  Membrane “fluidity” as detected by diphenylhexatriene probes , 1989 .

[44]  F. Cantalamessa.  Acute toxicity of two pyrethroids, permethrin, and cypermethrin in neonatal and adult rats , 2005, Archives of Toxicology.

[45]  E Gratton,et al.  Phase fluctuation in phospholipid membranes revealed by Laurdan fluorescence. , 1990, Biophysical journal.

[46]  A. Santroni,et al.  Extent of DNA damage in density-separated trout erythrocytes assessed by the 'comet' assay. , 1998, Mutation research.

[47]  R. Gabbianelli,et al.  Purine Bases Oxidation and Repair Following Permethrin Insecticide Treatment in Rat Heart Cells , 2010, Cardiovascular Toxicology.

[48]  R. Tice,et al.  A simple technique for quantitation of low levels of DNA damage in individual cells. , 1988, Experimental cell research.

[49]  V. Grant,et al.  Early maternal separation increases symptoms of activity-based anorexia in male and female rats. , 2009, Journal of experimental psychology. Animal behavior processes.

[50]  R. Gabbianelli,et al.  Cypermethrin-induced plasma membrane perturbation on erythrocytes from rats: reduction of fluidity in the hydrophobic core and in glutathione peroxidase activity. , 2002, Toxicology.

[51]  George Davey Smith,et al.  Epigenetic Epidemiology of Common Complex Disease: Prospects for Prediction, Prevention, and Treatment , 2010, PLoS medicine.

[52]  Y. Shukla,et al.  Mutagenic potential of cypermethrin in mouse dominant lethal assay. , 2002, Journal of environmental pathology, toxicology and oncology : official organ of the International Society for Environmental Toxicology and Cancer.

[53]  M. Villarini,et al.  Effect of different organotin compounds on DNA of gilthead sea bream (Sparus Aurata) erythrocytes assessed by the comet assay , 2002 .

[54]  S. Kritchevsky,et al.  Serum albumin concentration and heart failure risk The Health, Aging, and Body Composition Study. , 2010, American heart journal.