DOI QR코드

DOI QR Code

Forced swimming stress increases natatory activity of lead-exposed mice

  • Araujo, Ulisses C. (Laboratorio de Neurofisiologia, Departamento de Ciencias Fisiologicas, Instituto de Biologia Roberto Alcantara Gomes, Centro Biomedico, Universidade Do Estado Do Rio de Janeiro) ;
  • Krahe, Thomas E. (Departamento de Psicologia, Pontificia Universidade Catolica Do Rio de Janeiro) ;
  • Ribeiro‑Carvalho, Anderson (Departamento de Ciencias, Faculdade de Formacao de Professores da, Universidade Do Estado Do Rio de Janeiro) ;
  • Gomes, Regina A.A. (Centro de Estudos da Saude Do Trabalhador E Ecologia Humana, Escola Nacional de Saude Publica, Fundacao Oswaldo Cruz) ;
  • Lotufo, Bruna M. (Laboratorio de Neurofisiologia, Departamento de Ciencias Fisiologicas, Instituto de Biologia Roberto Alcantara Gomes, Centro Biomedico, Universidade Do Estado Do Rio de Janeiro) ;
  • Moreira, Maria de Fatima R. (Centro de Estudos da Saude Do Trabalhador E Ecologia Humana, Escola Nacional de Saude Publica, Fundacao Oswaldo Cruz) ;
  • de Abreu-Villaca, Yael (Laboratorio de Neurofisiologia, Departamento de Ciencias Fisiologicas, Instituto de Biologia Roberto Alcantara Gomes, Centro Biomedico, Universidade Do Estado Do Rio de Janeiro) ;
  • Manhaes, Alex C. (Laboratorio de Neurofisiologia, Departamento de Ciencias Fisiologicas, Instituto de Biologia Roberto Alcantara Gomes, Centro Biomedico, Universidade Do Estado Do Rio de Janeiro) ;
  • Filgueiras, Claudio C. (Laboratorio de Neurofisiologia, Departamento de Ciencias Fisiologicas, Instituto de Biologia Roberto Alcantara Gomes, Centro Biomedico, Universidade Do Estado Do Rio de Janeiro)
  • Received : 2019.10.02
  • Accepted : 2020.03.26
  • Published : 2021.01.15

Abstract

Recent evidence points to the relationship between lead toxicity and the function of the hypothalamic-pituitary-adrenal axis, which suggests that lead exposure could influence how an individual cope with stress. Here we test this hypothesis by investigating the behavioral effects of lead exposure in mice during the forced swimming test (FST), a parading in which animals are exposed to a stressful situation and environment. Swiss mice received either 180 ppm or 540 ppm of lead acetate (Pb) in their ad-lib water supply for 60-90 days, starting at postnatal day 30. Control (Ctrl) mice drank tap water. At the end of the exposure period, mice were submitted to a 5-min session of FST or to an open-field session of the same duration. Data from naïve animals showed that corticosterone levels were higher for animals tested in the FST compared to animals tested in the open-field. Blood-lead levels (BLL) in Pb-exposed mice ranged from 14.3 to 106.9 ㎍/dL. No differences were observed in spontaneous locomotion between Ctrl and Pb-exposed groups in the open-field. However, in the FST, Pb-treated mice displayed higher swimming activity than Ctrl ones and this effect was observed even for animals with BLL higher than 20 ㎍/dL. Furthermore, significant differences in brain glutathione levels, used as an indicator of led toxicity, were only observed for BLL higher than 40 ㎍/dL. Overall, these findings suggest that swimming activity in the FST is a good indicator of lead toxicity and confirm our prediction that lead toxicity influences behavioral responses associated to stress.

Keywords

Acknowledgement

This work was supported by grants from: Fundacao de Amparo a Pesquisa do Estado do Rio de Janeiro (FAPERJ-BRAZIL), Conselho Nacional de Desenvolvimento Cientifico e Tecnologico (CNPq-BRAZIL) and SR2-UERJ. The authors are thankful to to Ulisses Risso for animal care.

References

  1. Benson SM, Talbott EO, Brink LAL et al (2017) Environmental lead and childhood blood lead levels in US children: NHANES, 1999-2006. Arch Environ Occup Heal 72:70-78. https://doi.org/10.1080/19338244.2016.1157454
  2. Bodeau-Livinec F, Glorennec P, Cot M et al (2016) Elevated blood lead levels in infants and mothers in benin and potential sources of exposure. Int J Environ Res Public Health 13:1-14. https://doi.org/10.3390/ijerph13030316
  3. Olympio KPK, Goncalves CG, Salles FJ et al (2017) What are the blood lead levels of children living in Latin America and the Caribbean? Environ Int 101:46-58. https://doi.org/10.1016/j.envint.2016.12.022
  4. Pelc W, Pawlas N, Dobrakowski M, Kasperczyk S (2016) Environmental and socioeconomic factors contributing to elevated blood lead levels in children from an industrial area of Upper Silesia. Environ Toxicol Chem 35:2597-2603. https://doi.org/10.1002/etc.3429
  5. Cecil KM, Brubaker CJ, Adler CM et al (2008) Decreased brain volume in adults with childhood lead exposure. PLoS Med 5:0741-0749. https://doi.org/10.1371/journal.pmed.0050112
  6. Garza A, Vega R, Soto E (2006) Cellular mechanisms of lead neurotoxicity. Med Sci Monit 12:57-65
  7. Lidsky TI, Schneider JS (2003) Lead neurotoxicity in children: basic mechanisms and clinical correlates. Brain 126:5-19. https://doi.org/10.1093/brain/awg014
  8. Toscano CD, Guilarte TR (2005) Lead neurotoxicity: from exposure to molecular effects. Brain Res Rev 49:529-554. https://doi.org/10.1016/j.brainresrev.2005.02.004
  9. Costa LG, Aschner M, Vitalone A et al (2004) Developmental neuropathology of environmental agents. Annu Rev Pharmacol Toxicol 44:87-110. https://doi.org/10.1146/annurev.pharmtox.44.101802.121424
  10. Fenga C, Gangemi S, Alibrandi A et al (2016) Relationship between lead exposure and mild cognitive impairment. J Prev Med Hyg 57:205-210
  11. Murata K, Iwata T, Dakeishi M, Karita K (2009) Lead toxicity: does the critical level of lead resulting in adverse effects differ between adults and children? J Occup Health 51:1-12. https://doi.org/10.1539/joh.k8003
  12. Shih RA, Hu H, Weisskopf MG, Schwartz BS (2007) Cumulative lead dose and cognitive function in adults: a review of studies that measured both blood lead and bone lead. Environ Health Perspect 115:483-492. https://doi.org/10.1289/ehp.9786
  13. Kazi TG, Shah F, Afridi HI (2015) Occupational and environmental lead exposure to adolescent workers in battery recycling workshops. Toxicol Ind Health 31:1288-1295. https://doi.org/10.1177/0748233713485883
  14. La-Llave-Leon O, Salas Pacheco JM, Estrada Martinez S et al (2016) The relationship between blood lead levels and occupational exposure in a pregnant population. BMC Public Health 16:1-9. https://doi.org/10.1186/s12889-016-3902-3
  15. Laidlaw MAS, Filippelli G, Mielke H et al (2017) Lead exposure at firing ranges - a review. Environ Heal A Glob Access Sci Source 16:1-15. https://doi.org/10.1186/s12940-017-0246-0
  16. Nie LH, Wright RO, Bellinger DC et al (2011) Blood lead levels and cumulative blood lead index (CBLI) as predictors of late neurodevelopment in lead poisoned children. Biomarkers 16:517-524. https://doi.org/10.3109/1354750X.2011.604133
  17. Santa Maria MP, Hill BD, Kline J (2018) Lead (Pb) neurotoxicology and cognition. Appl Neuropsychol Child. https://doi.org/10.1080/21622965.2018.1428803
  18. Bellinger DC (2008) Lead neurotoxicity and socioeconomic status: Conceptual and analytical issues. Neurotoxicology 29:828-832. https://doi.org/10.1016/j.neuro.2008.04.005
  19. Healey N (2009) Lead toxicity, vulnerable subpopulations and emergency preparedness. Radiat Prot Dosimetry 134:1-9. https://doi.org/10.1093/rpd/ncp068
  20. Peters JL, Kubzansky L, McNeely E et al (2007) Stress as a potential modifier of the impact of lead levels on blood pressure: the normative aging study. Environ Health Perspect 115:1154-1159. https://doi.org/10.1289/ehp.10002
  21. Rice DC (2006) Animal models of cognitive impairment produced by developmental lead exposure. In: Levin ED, Buccafusco JJ (eds) Animal models of cognitive impairment. CRC Press/Taylor and Francis Group LLC., Boca Raton
  22. Cory-Slechta DA, Virgolini MB, Rossi-George A et al (2008) Lifetime consequences of combined maternal lead and stress. Basic Clin Pharmacol Toxicol 102:218-227. https://doi.org/10.1111/j.1742-7843.2007.00189.x
  23. Glass TA, Bandeen-Roche K, McAtee M et al (2009) Neighborhood psychosocial hazards and the association of cumulative lead dose with cognitive function in older adults. Am J Epidemiol 169:683-692. https://doi.org/10.1093/aje/kwn390
  24. Virgolini MB, Chen K, Weston DD et al (2005) Interactions of chronic lead exposure and intermittent stress: consequences for brain catecholamine systems and associated behaviors and HPA axis function. Toxicol Sci 87:469-482. https://doi.org/10.1093/toxsci/kfi269
  25. Yamamoto BK, Kutscher CL (2002) Drug and food-deprivation modulation of activity in rats given chronic dietary lead: significance of type of activity measure. Pharmacol Biochem Behav 15:505-512. https://doi.org/10.1016/0091-3057(81)90285-9
  26. Porsolt RD, Le Pichon M, Jalfre M (1977) Depression: a new animal model sensitive to antidepressant treatments. Nature 266:730-732 https://doi.org/10.1038/266730a0
  27. Porsolt RD, Anton G, Blavet N, Jalfre M (1978) Behavioural despair in rats: a new model sensitive to antidepressant treatments. Eur J Pharmacol 47:379-391. https://doi.org/10.1016/0014-2999(78)90118-8
  28. Bulduk S, Canbeyli R (2004) Effect of inescapable tones on behavioral despair in Wistar rats. Prog Neuro-Psychopharmacol Biol Psychiatry 28:471-475. https://doi.org/10.1016/j.pnpbp.2003.11.012
  29. Christianson JP, Drugan RC (2005) Intermittent cold water swim stress increases immobility and interferes with escape performance in rat. Behav Brain Res 165:58-62. https://doi.org/10.1016/j.bbr.2005.06.028
  30. Drugan RC, Eren S, Hazi A et al (2005) Impact of water temperature and stressor controllability on swim stress-induced changes in body temperature, serum corticosterone, and immobility in rats. Pharmacol Biochem Behav 82:397-403. https://doi.org/10.1016/j.pbb.2005.09.011
  31. Filgueiras CC, Abreu-Villaca Y, Krahe TE, Manhaes AC (2006) Unilateral hemispherectomy at adulthood asymmetrically affects immobile behavior of male Swiss mice. Behav Brain Res 172:33-38. https://doi.org/10.1016/j.bbr.2006.04.015
  32. Krahe TE, Filgueiras CC, Schmidt SL (2002) Effects of rotational side preferences on immobile behavior of normal mice in the forced swimming test. Prog Neuro-Psychopharmacol Biol Psychiatry 26:169-176. https://doi.org/10.1016/S0278-5846(01)00248-2
  33. Thierry B, Steru L, Chermat R, Simon P (1984) Searching-waiting strategy: a candidate for an evolutionary model of depression? Behav Neural Biol 41:180-189 https://doi.org/10.1016/S0163-1047(84)90555-7
  34. de Kloet ER, Molendijk ML (2016) Coping with the forced swim stressor: Towards understanding an adaptive mechanism. Neural Plast 2016:1-13. https://doi.org/10.1155/2016/6503162
  35. Leasure JL, Giddabasappa A, Chaney S et al (2008) Low-level human equivalent gestational lead exposure produces sex-specific motor and coordination abnormalities and late-onset obesity in year-old mice. Environ Health Perspect 116:355-361. https://doi.org/10.1289/ehp.10862
  36. Moreira EG, Vassilieff I, Vassilieff VS (2001) Developmental lead exposure: Behavioral alterations in the short and long term. Neurotoxicol Teratol 23:489-495. https://doi.org/10.1016/S0892-0362(01)00159-3
  37. Silbergeld EK, Goldberg AM (1974) Hyperactivity: a lead induced behavior disorder. Environ Health Perspect 7:227-232 https://doi.org/10.1289/ehp.747227
  38. Szczerbak G, Nowak P, Kostrzewa RM, Brus R (2007) Maternal lead exposure produces long-term enhancement of dopaminergic reactivity in rat offspring. Neurochem Res 32:1791-1798. https://doi.org/10.1007/s11064-007-9306-0
  39. Trombini TV, Pedroso CG, Ponce D et al (2001) Developmental lead exposure in rats: Is a behavioral sequel extended at F2 generation? Pharmacol Biochem Behav 68:743-751. https://doi.org/10.1016/S0091-3057(01)00473-7
  40. Bains JS, Shaw CA (1997) Neurodegenerative disorders in humans: the role of glutathione in oxidative stress-mediated neuronal death. Brain Res Rev 25:335-358. https://doi.org/10.1016/S0165-0173(97)00045-3
  41. Coyle J, Puttfarcken P (1993) Oxidative stress, glutamate, and neurodegenerative disorders. Science 80(262):689-695 https://doi.org/10.1126/science.7901908
  42. Schulz JB, Lindenau J, Seyfried J, Dichgans J (2000) Glutathione, oxidative stress and neurodegeneration. Eur J Biochem 267:4904-4911 https://doi.org/10.1046/j.1432-1327.2000.01595.x
  43. Dobrakowski M, Pawlas N, Hudziec E et al (2016) Glutathione, glutathione-related enzymes, and oxidative stress in individuals with subacute occupational exposure to lead. Environ Toxicol Pharmacol 45:235-240. https://doi.org/10.1016/j.etap.2016.06.008
  44. Engstrom AK, Xia Z (2017) Lead exposure in late adolescence through adulthood impairs short-term spatial memory and the neuronal differentiation of adult-born cells in C57BL/6 male mice. Neurosci Lett 661:108-113. https://doi.org/10.1016/j.neulet.2017.09.060
  45. Fan Y, Zhao X, Yu J et al (2020) Lead-induced oxidative damage in rats/mice: a meta-analysis. J Trace Elem Med Biol 58:126443. https://doi.org/10.1016/j.jtemb.2019.126443
  46. Carocci A, Catalano A, Lauria G et al (2016) Lead toxicity, antioxidant defense and environment. Rev Environ Contam Toxicol 238:45-67. https://doi.org/10.1007/398_2015_5003
  47. Filgueiras CC, Ribeiro-Carvalho A, Nunes F et al (2009) Early ethanol exposure in mice increases laterality of rotational side preference in the free-swimming test. Pharmacol Biochem Behav 93:148-154. https://doi.org/10.1016/j.pbb.2009.04.023
  48. Schmidt SL, Filgueiras CC, Krahe TE (1999) Effects of sex and laterality on the rotatory swimming behavior of normal mice. Physiol Behav 65:607-616. https://doi.org/10.1016/S0031-9384(98)00184-X
  49. Dutra-Tavares AC, Manhaes AC, Silva JO et al (2015) Locomotor response to acute nicotine in adolescent mice is altered by maternal undernutrition during lactation. Int J Dev Neurosci 47:278-285. https://doi.org/10.1016/j.ijdevneu.2015.10.002
  50. Griffith OW (1999) Biologic and pharmacologic regulation of mammalian glutathione synthesis. Free Radic Biol Med 27:922-935. https://doi.org/10.1016/S0891-5849(99)00176-8
  51. Correa M, Miquel M, Sanchis-Segura C, Aragon CMG (1999) Effects of chronic lead administration on ethanol-induced locomotor and brain catalase activity. Alcohol 19:43-49. https://doi.org/10.1016/S0741-8329(99)00023-3
  52. Nieto-Fernandez FE, Ruiz A, Ntukogu N et al (2006) Short term lead exposure induces a stress-like response in adult mice. Med Sci Monit 12:325-329
  53. Rice DC (1996) PCBs and behavioral impairment: are there lessons we can learn from lead? Neurotoxicol Teratol 18:229-232 https://doi.org/10.1016/S0892-0362(96)90003-3
  54. Salinas JA, Huff NC (2002) Lead and spatial vs. cued open field performance. Neurotoxicol Teratol 24:551-557. https://doi.org/10.1016/S0892-0362(02)00266-0
  55. Abdulmajeed WI, Sulieman HB, Zubayr MO et al (2015) Honey prevents neurobehavioural deficit and oxidative stress induced by lead acetate exposure in male wistar rats- a preliminary study. Metab Brain Dis 31:37-44. https://doi.org/10.1007/s11011-015-9733-6
  56. Villeda-Hernandez J, Barroso-Moguel R, Mendez-Armenta M et al (2001) Enhanced brain regional lipid peroxidation in developing rats exposed to low level lead acetate. Brain Res Bull 55:247-251. https://doi.org/10.1016/S0361-9230(01)00512-3
  57. Rodrigues ALS, Rocha JBT, Mello CF, Souza DO (1996) Effect of perinatal lead exposure on rat behaviour in open-field and two-way avoidance tasks. Pharmacol Toxicol 79:150-156. https://doi.org/10.1111/j.1600-0773.1996.tb00259.x
  58. Ennaceur A, Michalikova S, Chazot PL (2009) Do rats really express neophobia towards novel objects? Experimental evidence from exposure to novelty and to an object recognition task in an open space and an enclosed space. Behav Brain Res 197:417-434. https://doi.org/10.1016/j.bbr.2008.10.007
  59. Commons KG, Cholanians AB, Babb JA, Ehlinger DG (2017) The rodent forced swim test measures stress-coping strategy, not depression-like behavior. ACS Chem Neurosci 8:955-960. https://doi.org/10.1021/acschemneuro.7b00042
  60. Cabib S, Puglisi-Allegra S (2012) The mesoaccumbens dopamine in coping with stress. Neurosci Biobehav Rev 36:79-89. https://doi.org/10.1016/j.neubiorev.2011.04.012
  61. Tye KM, Mirzabekov JJ, Warden MR et al (2013) Dopamine neurons modulate neural encoding and expression of depression-related behaviour. Nature 493:537-541. https://doi.org/10.1038/nature11740
  62. Commissaris RL, Tavakoli-Nezhad M, Barron AJ, Pitts DK (2000) Effects of chronic low-level oral lead exposure on prepulse inhibition of acoustic startle in the rat. Neurotoxicol Teratol 22:55-60. https://doi.org/10.1016/S0892-0362(99)00042-2
  63. Cory-Slechta DA, O'Mara DJ, Brockel BJ (1998) Nucleus accumbens dopaminergic medication of fixed interval schedule-controlled behavior and its modulation by low-level lead exposure. J Pharmacol Exp Ther 286:794-805
  64. McKlveen JM, Myers B, Flak JN et al (2013) Role of prefrontal cortex glucocorticoid receptors in stress and emotion. Biol Psychiatry 74:672-679. https://doi.org/10.1016/j.biopsych.2013.03.024
  65. Myers B, McKlveen JM, Herman JP (2014) Glucocorticoid actions on synapses, circuits, and behavior: implications for the energetics of stress. Front Neuroendocrinol 35:180-196. https://doi.org/10.1016/j.yfrne.2013.12.003
  66. Virgolini MB, Bauter MR, Weston DD, Cory-Slechta DA (2006) Permanent alterations in stress responsivity in female offspring subjected to combined maternal lead exposure and/or stress. Neurotoxicology 27:11-21. https://doi.org/10.1016/j.neuro.2005.05.012
  67. White LD, Cory-Slechta DA, Gilbert ME et al (2007) New and evolving concepts in the neurotoxicology of lead. Toxicol Appl Pharmacol 225:1-27. https://doi.org/10.1016/j.taap.2007.08.001
  68. Servatius RJ, Ottenweller JE, Bergen MT et al (1994) Persistent stress-induced sensitization of adrenocortical and startle responses. Physiol Behav 56:945-954. https://doi.org/10.1016/0031-9384(94)90328-X
  69. Gump BB, Stewart P, Reihman J et al (2008) Low-level prenatal and postnatal blood lead exposure and adrenocortical responses to acute stress in children. Environ Health Perspect 116:249-255. https://doi.org/10.1289/ehp.10391
  70. Anyan J, Amir S (2018) Too depressed to swim or too afraid to stop? A reinterpretation of the forced swim test as a measure of anxiety-like behavior. Neuropsychopharmacology 43:931-933. https://doi.org/10.1038/npp.2017.260
  71. Jozefczak M, Remans T, Vangronsveld J, Cuypers A (2012) Glutathione is a key player in metal-induced oxidative stress defenses. Int J Mol Sci 13:3145-3175. https://doi.org/10.3390/ijms13033145
  72. Ralf D (2000) Metabolism and functions of glutathione in brain. Prog Neurobiol 62:649-671. https://doi.org/10.1016/s0301-0082(99)00060-x
  73. Hunaiti AA, Soud M (2000) Effect of lead concentration on the level of glutathione, glutathione S-transferase, reductase and peroxidase in human blood. Sci Total Environ 248:45-50 https://doi.org/10.1016/S0048-9697(99)00548-3
  74. Li XM, Gu Y, She JQ et al (2006) Lead inhibited N-methyl-d-aspartate receptor-independent long-term potentiation involved ryanodine-sensitive calcium stores in rat hippocampal area CA1. Neuroscience 139:463-473. https://doi.org/10.1016/j.neuroscience.2005.12.033

Cited by

  1. Does nicotine exposure during adolescence modify the course of schizophrenia-like symptoms? Behavioral analysis in a phencyclidine-induced mice model vol.16, pp.9, 2021, https://doi.org/10.1371/journal.pone.0257986