全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用:99美元

查看量下载量

相关文章

更多...
PLOS ONE  2012 

Anxiogenic Effects of Developmental Bisphenol A Exposure Are Associated with Gene Expression Changes in the Juvenile Rat Amygdala and Mitigated by Soy

DOI: 10.1371/journal.pone.0043890

Full-Text   Cite this paper   Add to My Lib

Abstract:

Early life exposure to Bisphenol A (BPA), a component of polycarbonate plastics and epoxy resins, alters sociosexual behavior in numerous species including humans. The present study focused on the ontogeny of these behavioral effects beginning in adolescence and assessed the underlying molecular changes in the amygdala. We also explored the mitigating potential of a soy-rich diet on these endpoints. Wistar rats were exposed to BPA via drinking water (1 mg/L) from gestation through puberty, and reared on a soy-based or soy-free diet. A group exposed to ethinyl estradiol (50 μg/L) and a soy-free diet was used as a positive estrogenic control. Animals were tested as juveniles or adults for anxiety-like and exploratory behavior. Assessment of serum BPA and genistein (GEN), a soy phytoestrogen, confirmed that internal dose was within a human-relevant range. BPA induced anxiogenic behavior in juveniles and loss of sexual dimorphisms in adult exploratory behavior, but only in the animals reared on the soy-free diet. Expression analysis revealed a suite of genes, including a subset known to mediate sociosexual behavior, associated with BPA-induced juvenile anxiety. Notably, expression of estrogen receptor beta (Esr2) and two melanocortin receptors (Mc3r, Mc4r) were downregulated. Collectively, these results show that behavioral impacts of BPA can manifest during adolescence, but wane in adulthood, and may be mitigated by diet. These data also reveal that, because ERβ and melanocortin receptors are crucial to their function, oxytocin/vasopressin signaling pathways, which have previously been linked to human affective disorders, may underlie these behavioral outcomes.

References

[1]  Frye C, Bo E, Calamandrei G, Calza L, Dessi-Fulgheri F, et al. (2011) Endocrine Disrupters: A Review of Some Sources, Effects, and Mechanisms of Actions on Behavior and Neuroendocrine Systems. J Neuroendocrinol 24(1): 144–159.
[2]  Wolstenholme JT, Rissman EF, Connelly JJ (2011) The role of Bisphenol A in shaping the brain, epigenome and behavior. Horm Behav 59: 296–305.
[3]  Nakagami A, Negishi T, Kawasaki K, Imai N, Nishida Y, et al. (2009) Alterations in male infant behaviors towards its mother by prenatal exposure to bisphenol A in cynomolgus monkeys (Macaca fascicularis) during early suckling period. Psychoneuroendocrinology 34: 1189–1197.
[4]  Braun JM, Kalkbrenner AE, Calafat AM, Yolton K, Ye X, et al. (2011) Impact of early-life bisphenol a exposure on behavior and executive function in children. Pediatrics 128: 873–882.
[5]  Braun JM, Yolton K, Dietrich KN, Hornung R, Ye X, et al. (2009) Prenatal bisphenol A exposure and early childhood behavior. Environ Health Perspect 117: 1945–1952.
[6]  Kessler RC, Chiu WT, Demler O, Merikangas KR, Walters EE (2005) Prevalence, severity, and comorbidity of 12-month DSM-IV disorders in the National Comorbidity Survey Replication. Arch Gen Psychiatry 62: 617–627.
[7]  Aguiar A, Eubig PA, Schantz SL (2010) Attention deficit/hyperactivity disorder: a focused overview for children's environmental health researchers. Environ Health Perspect 118: 1646–1653.
[8]  Cooper JE, Kendig EL, Belcher SM (2011) Assessment of bisphenol A released from reusable plastic, aluminium and stainless steel water bottles. Chemosphere 85(6):943–947.
[9]  Liao C, Kannan K (2011) Widespread occurrence of bisphenol A in paper and paper products: implications for human exposure. Environ Sci Technol 45: 9372–9379.
[10]  Lakind JS, Naiman DQ (2010) Daily intake of bisphenol A and potential sources of exposure: 2005–2006 National Health and Nutrition Examination Survey. J Expo Sci Environ Epidemiol 21(3):272–279.
[11]  Calafat AM, Ye X, Wong LY, Reidy JA, Needham LL (2008) Exposure of the U.S. population to bisphenol A and 4-tertiary-octylphenol: 2003–2004. Environ Health Perspect 116: 39–44.
[12]  Vandenberg LN, Maffini MV, Sonnenschein C, Rubin BS, Soto AM (2009) Bisphenol-A and the great divide: a review of controversies in the field of endocrine disruption. Endocr Rev 30: 75–95.
[13]  Patisaul HB, Bateman HL (2008) Neonatal exposure to endocrine active compounds or an ERbeta agonist increases adult anxiety and aggression in gonadally intact male rats. Horm Behav 53(4):580–588.
[14]  Pelayo S, Oliveira E, Thienpont B, Babin PJ, Raldua D, et al. (2012) Triiodothyronine-induced changes in the zebrafish transcriptome during the eleutheroembryonic stage: Implications for bisphenol A developmental toxicity. Aquat Toxicol 110–111: 114–122.
[15]  Jones DC, Miller GW (2008) The effects of environmental neurotoxicants on the dopaminergic system: A possible role in drug addiction. Biochem Pharmacol 76: 569–581.
[16]  Dolinoy DC, Huang D, Jirtle RL (2007) Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development. Proc Natl Acad Sci U S A 104: 13056–13061.
[17]  McCarrison R (1933) The goitrogenic action of soya-bean and ground-nut. Indian J Med Res 21: 179–181.
[18]  Bennetts HW, Underwood EJ, Shier FL (1946) A specific breeding problem of sheep on subterranean clover pastures in Western Australia. Aust Vet J 22: 2.
[19]  Patisaul HB, Jefferson W (2010) The pros and cons of phytoestrogens. Front Neuroendocrinol 31(4):400–419.
[20]  Kuiper GG, Lemmen JG, Carlsson B, Corton JC, Safe SH, et al. (1998) Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 139: 4252–4263.
[21]  Dixon RA, Ferreira D (2002) Genistein. Phytochemistry 60: 205–211.
[22]  Messina MJ, Persky V, Setchell KD, Barnes S (1994) Soy intake and cancer risk: a review of the in vitro and in vivo data. Nutr Cancer 21: 113–131.
[23]  Zhang Y, Chen H (2011) Genistein, an epigenome modifier during cancer prevention. Epigenetics 6: 888–891.
[24]  Muhlhauser A, Susiarjo M, Rubio C, Griswold J, Gorence G, et al. (2009) Bisphenol A effects on the growing mouse oocyte are influenced by diet. Biol Reprod 80: 1066–1071.
[25]  Cederroth CR, Zimmermann C, Beny JL, Schaad O, Combepine C, et al. (2010) Potential detrimental effects of a phytoestrogen-rich diet on male fertility in mice. Molecular and Cellular Endocrinology 321: 152–160.
[26]  Patisaul HB, Jefferson W (2010) The pros and cons of phytoestrogens. Frontiers in neuroendocrinology 31: 400–419.
[27]  Sullivan AW, Hamilton P, Patisaul HB (2011) Neonatal agonism of ERbeta impairs male reproductive behavior and attractiveness. Hormones and behavior 60: 185–194.
[28]  Lund TD, Lephart ED (2001) Dietary soy phytoestrogens produce anxiolytic effects in the elevated plus-maze. Brain Research 913: 180–184.
[29]  Lephart ED, Setchell KD, Handa RJ, Lund TD (2004) Behavioral effects of endocrine-disrupting substances: phytoestrogens. ILAR journal/National Research Council, Institute of Laboratory Animal Resources 45: 443–454.
[30]  Patisaul HB, Blum A, Luskin JR, Wilson ME (2005) Dietary soy supplements produce opposite effects on anxiety in intact male and female rats in the elevated plus-maze. Behav Neurosci 119: 587–594.
[31]  Millan MJ (2003) The neurobiology and control of anxious states. Prog Neurobiol 70: 83–244.
[32]  Brown NM, Setchell KD (2001) Animal models impacted by phytoestrogens in commercial chow: implications for pathways influenced by hormones. Laboratory investigation; a journal of technical methods and pathology 81: 735–747.
[33]  Thigpen JE, Setchell KD, Ahlmark KB, Locklear J, Spahr T, et al. (1999) Phytoestrogen content of purified, open- and closed-formula laboratory animal diets. Laboratory animal science 49: 530–536.
[34]  Brown NM, Setchell KD (2001) Animal models impacted by phytoestrogens in commercial chow: implications for pathways influenced by hormones. Lab Invest 81: 735–747.
[35]  Cooper S, Latendresse JR, Doerge DR, Twaddle NC, Fu X, et al. (2006) Dietary modulation of p-nonylphenol-induced polycystic kidneys in male Sprague-Dawley rats. Toxicol Sci 91: 631–642.
[36]  Miyawaki J, Sakayama K, Kato H, Yamamoto H, Masuno H (2007) Perinatal and postnatal exposure to bisphenol a increases adipose tissue mass and serum cholesterol level in mice. J Atheroscler Thromb 14: 245–252.
[37]  Fujimoto T, Kubo K, Aou S (2006) Prenatal exposure to bisphenol A impairs sexual differentiation of exploratory behavior and increases depression-like behavior in rats. Brain Res 1068: 49–55.
[38]  Kabuto H, Amakawa M, Shishibori T (2004) Exposure to bisphenol A during embryonic/fetal life and infancy increases oxidative injury and causes underdevelopment of the brain and testis in mice. Life Sci 74: 2931–2940.
[39]  Coughlin JL, Winnik B, Buckley B (2011) Measurement of bisphenol A, bisphenol A ss-D-glucuronide, genistein, and genistein 4′-ss-D-glucuronide via SPE and HPLC-MS/MS. Analytical and bioanalytical chemistry 401: 995–1002.
[40]  Patisaul HB, Burke KT, Hinkle RE, Adewale HB, Shea D (2009) Systemic administration of diarylpropionitrile (DPN) or phytoestrogens does not affect anxiety-related behaviors in gonadally intact male rats. Hormones and Behavior 55: 319–328.
[41]  Marcondes FK, Miguel KJ, Melo LL, Spadari-Bratfisch RC (2001) Estrous cycle influences the response of female rats in the elevated plus-maze test. Physiology & Behavior 74: 435–440.
[42]  Becker JB, Arnold AP, Berkley KJ, Blaustein JD, Eckel LA, et al. (2005) Strategies and methods for research on sex differences in brain and behavior. Endocrinology 146: 1650–1673.
[43]  Jakubowski M, Blum M, Roberts JL (1991) Postnatal development of gonadotropin-releasing hormone and cyclophilin gene expression in the female and male rat brain. Endocrinology 128: 2702–2708.
[44]  Walker DM, Juenger TE, Gore AC (2009) Developmental profiles of neuroendocrine gene expression in the preoptic area of male rats. Endocrinology 150: 2308–2316.
[45]  Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.
[46]  Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(?Delta Delta C(T)) Method. Methods 25: 402–408.
[47]  Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3: 1101–1108.
[48]  Vandenberg LN, Hauser R, Marcus M, Olea N, Welshons WV (2007) Human exposure to bisphenol A (BPA). Reprod Toxicol 24: 139–177.
[49]  Doerge DR, Vanlandingham M, Twaddle NC, Delclos KB (2010) Lactational Transfer of Bisphenol a in Sprague-Dawley Rats. Toxicol Lett 199(3):372–376.
[50]  Doerge DR, Twaddle NC, Churchwell MI, Newbold RR, Delclos KB (2006) Lactational transfer of the soy isoflavone, genistein, in Sprague-Dawley rats consuming dietary genistein. Reprod Toxicol 21: 307–312.
[51]  Hascoet M, Bourin M, Dhonnchadha BA (2001) The mouse light-dark paradigm: a review. Prog Neuropsychopharmacol Biol Psychiatry 25: 141–166.
[52]  Pellow S, Chopin P, File SE, Briley M (1985) Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods 14: 149–167.
[53]  Benjamini Y, Hochberg Y (2000) On the adaptive control of the false discovery rate in multiple testing with independent statistics. Journal of Educational and Behavioral Statistics 25: 60–83.
[54]  Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B (Methodological) 57: 289–300.
[55]  Imhof JT, Coelho ZM, Schmitt ML, Morato GS, Carobrez AP (1993) Influence of gender and age on performance of rats in the elevated plus maze apparatus. Behav Brain Res 56: 177–180.
[56]  Johnston AL, File SE (1991) Sex differences in animal tests of anxiety. Physiol Behav 49: 245–250.
[57]  Marcondes FK, Miguel KJ, Melo LL, Spadari-Bratfisch RC (2001) Estrous cycle influences the response of female rats in the elevated plus-maze test. Physiol Behav 74: 435–440.
[58]  Cox KH, Gatewood JD, Howeth C, Rissman EF (2010) Gestational exposure to bisphenol A and cross-fostering affect behaviors in juvenile mice. Horm Behav 58(5): 754–761.
[59]  Jasarevic E, Sieli PT, Twellman EE, Welsh TH Jr, Schachtman TR, et al. (2011) From the Cover: Disruption of adult expression of sexually selected traits by developmental exposure to bisphenol A. Proceedings of the National Academy of Sciences of the United States of America 108: 11715–11720.
[60]  Gioiosa L, Fissore E, Ghirardelli G, Parmigiani S, Palanza P (2007) Developmental exposure to low-dose estrogenic endocrine disruptors alters sex differences in exploration and emotional responses in mice. Hormones and Behavior 52: 307–316.
[61]  Palanza P, Gioiosa L, vom Saal FS, Parmigiani S (2008) Effects of developmental exposure to bisphenol A on brain and behavior in mice. Environmental research 108: 150–157.
[62]  Bouwknecht JA, Paylor R (2002) Behavioral and physiological mouse assays for anxiety: a survey in nine mouse strains. Behav Brain Res 136: 489–501.
[63]  Bonthuis PJ, Cox KH, Searcy BT, Kumar P, Tobet S, et al. (2010) Of mice and rats: key species variations in the sexual differentiation of brain and behavior. Frontiers in neuroendocrinology 31: 341–358.
[64]  Kalinichev M, Easterling KW, Plotsky PM, Holtzman SG (2002) Long-lasting changes in stress-induced corticosterone response and anxiety-like behaviors as a consequence of neonatal maternal separation in Long-Evans rats. Pharmacol Biochem Behav 73: 131–140.
[65]  Richter CA, Birnbaum LS, Farabollini F, Newbold RR, Rubin BS, et al. (2007) In vivo effects of bisphenol A in laboratory rodent studies. Reproductive toxicology 24: 199–224.
[66]  Crews D, Gillette R, Scarpino SV, Manikkam M, Savenkova MI, et al. (2012) Epigenetic transgenerational inheritance of altered stress responses. Proc Natl Acad Sci U S A 109: 9143–9148.
[67]  Choleris E, Ogawa S, Kavaliers M, Gustafsson JA, Korach KS, et al. (2006) Involvement of estrogen receptor alpha, beta and oxytocin in social discrimination: A detailed behavioral analysis with knockout female mice. Genes Brain Behav 5: 528–539.
[68]  Sabatier N, Caquineau C, Dayanithi G, Bull P, Douglas AJ, et al. (2003) Alpha-melanocyte-stimulating hormone stimulates oxytocin release from the dendrites of hypothalamic neurons while inhibiting oxytocin release from their terminals in the neurohypophysis. J Neurosci 23: 10351–10358.
[69]  Lund TD, Rovis T, Chung WC, Handa RJ (2005) Novel actions of estrogen receptor-beta on anxiety-related behaviors. Endocrinology 146: 797–807.
[70]  Meyer-Lindenberg A, Domes G, Kirsch P, Heinrichs M (2011) Oxytocin and vasopressin in the human brain: social neuropeptides for translational medicine. Nat Rev Neurosci 12: 524–538.
[71]  Gabor CS, Phan A, Clipperton-Allen AE, Kavaliers M, Choleris E (2012) Interplay of oxytocin, vasopressin, and sex hormones in the regulation of social recognition. Behav Neurosci 126: 97–109.
[72]  Osterlund MK, Witt MR, Gustafsson JA (2005) Estrogen action in mood and neurodegenerative disorders: estrogenic compounds with selective properties-the next generation of therapeutics. Endocrine 28: 235–242.
[73]  Patisaul HB, Scordalakes EM, Young LJ, Rissman EF (2003) Oxytocin, but not oxytocin receptor, is regulated by oestrogen receptor beta in the female mouse hypothalamus. J Neuroendocrinol 15: 787–793.
[74]  Nomura M, McKenna E, Korach K, Pfaff D, Ogawa S (2002) Estrogen receptor-b regulates transcript levels for oxytocin and arginine vasopressin in the hypothalamic paraventricular nucleus of male mice. Molecular Brain Research 109: 84–94.
[75]  Donaldson ZR, Young LJ (2008) Oxytocin, vasopressin, and the neurogenetics of sociality. Science 322: 900–904.
[76]  McCarthy MM, Altemus M (1997) Central nervous system actions of oxytocin and modulation of behavior in humans. Mol Med Today 3: 269–275.
[77]  Wolstenholme JT, Edwards M, Shetty SR, Gatewood JD, Taylor JA, et al. (2012) Gestational Exposure to Bisphenol A Produces Transgenerational Changes in Behaviors and Gene Expression. Endocrinology 153(8):3828–3838.
[78]  Bielsky IF, Hu SB, Szegda KL, Westphal H, Young LJ (2004) Profound impairment in social recognition and reduction in anxiety-like behavior in vasopressin V1a receptor knockout mice. Neuropsychopharmacology 29: 483–493.
[79]  Guastella AJ, Einfeld SL, Gray KM, Rinehart NJ, Tonge BJ, et al. (2010) Intranasal oxytocin improves emotion recognition for youth with autism spectrum disorders. Biol Psychiatry 67: 692–694.
[80]  Kim J, Semaan SJ, Clifton DK, Steiner RA, Dhamija S, et al. (2011) Regulation of Kiss1 expression by sex steroids in the amygdala of the rat and mouse. Endocrinology 152: 2020–2030.
[81]  Kauffman AS (2010) Gonadal and nongonadal regulation of sex differences in hypothalamic Kiss1 neurones. J Neuroendocrinol 22: 682–691.
[82]  Simerly RB (2002) Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Annu Rev Neurosci 25: 507–536.
[83]  Scott V, Brown CH (2011) Kisspeptin activation of supraoptic nucleus neurons in vivo. Endocrinology 152: 3862–3870.
[84]  Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, et al. (2004) Epigenetic programming by maternal behavior. Nat Neurosci 7: 847–854.
[85]  McGowan PO, Sasaki A, D'Alessio AC, Dymov S, Labonte B, et al. (2009) Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat Neurosci 12: 342–348.
[86]  Dolinoy DC, Weidman JR, Jirtle RL (2007) Epigenetic gene regulation: linking early developmental environment to adult disease. Reprod Toxicol 23: 297–307.
[87]  Setchell KD, Zimmer-Nechemias L, Cai J, Heubi JE (1997) Exposure of infants to phyto-oestrogens from soy-based infant formula. Lancet 350: 23–27.
[88]  Todaka E, Sakurai K, Fukata H, Miyagawa H, Uzuki M, et al. (2005) Fetal exposure to phytoestrogens–the difference in phytoestrogen status between mother and fetus. Environ Res 99: 195–203.
[89]  Frye CA, Bo E, Calamandrei G, Calza L, Dessi-Fulgheri F, et al. (2012) Endocrine disrupters: a review of some sources, effects, and mechanisms of actions on behaviour and neuroendocrine systems. Journal of Neuroendocrinology 24: 144–159.
[90]  Murakami G, Hunter RG, Fontaine C, Ribeiro A, Pfaff D (2011) Relationships among estrogen receptor, oxytocin and vasopressin gene expression and social interaction in male mice. The European journal of neuroscience 34: 469–477.
[91]  American Psychiatric Association (2000) Diagnostic and statistical manual of mental disorders. Washington, DC: American Psychiatric Association.
[92]  Martel MM, Klump K, Nigg JT, Breedlove SM, Sisk CL (2009) Potential hormonal mechanisms of attention-deficit/hyperactivity disorder and major depressive disorder: a new perspective. Hormones and Behavior 55: 465–479.
[93]  Rodriguez-Landa JF, Hernandez-Figueroa JD, Hernandez-Calderon Bdel C, Saavedra M (2009) Anxiolytic-like effect of phytoestrogen genistein in rats with long-term absence of ovarian hormones in the black and white model. Progress in neuro-psychopharmacology & biological psychiatry 33: 367–372.
[94]  Landgraf R, Wigger A (2002) High vs low anxiety-related behavior rats: an animal model of extremes in trait anxiety. Behav Genet 32: 301–314.
[95]  Koolhaas JM, de Boer SF, Buwalda B, van Reenen K (2007) Individual variation in coping with stress: a multidimensional approach of ultimate and proximate mechanisms. Brain Behav Evol 70: 218–226.
[96]  Hovatta I, Barlow C (2008) Molecular genetics of anxiety in mice and men. Ann Med 40: 92–109.
[97]  Hohoff C (2009) Anxiety in mice and men: a comparison. J Neural Transm 116: 679–687.
[98]  Donner J, Pirkola S, Silander K, Kananen L, Terwilliger JD, et al. (2008) An association analysis of murine anxiety genes in humans implicates novel candidate genes for anxiety disorders. Biol Psychiatry 64: 672–680.

Full-Text

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133