Exposure to bisphenol a exacerbates migraine-like behaviors in a multibehavior model of rat migraine

Toxicological Sciences

Volumn 137, Issue 2, 2014, Pages 416-427

  Vermeer, Lydia M M ^a   Gregory, Eugene ^a   Winter, Michelle K ^b   McCarson, Kenneth E ^a,b   Berman, Nancy E J ^a,b  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

Author keywords

Behavioral model; Bisphenol A; Migraine; Xenoestrogens

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; ESTROGEN RECEPTOR ALPHA; FATTY ACID AMIDASE; G PROTEIN COUPLED RECEPTOR 30; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; SODIUM CHANNEL NAV1.8;

ACOUSTIC REFLEX; ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AVERSION; CONTROLLED STUDY; DISEASE EXACERBATION; DURA MATER; ENZYME ACTIVATION; EXPOSURE; FEMALE; GENE EXPRESSION; GROOMING; INTRACELLULAR SIGNALING; LATENT PERIOD; LIGHT; LIGHT SENSITIVITY; LOCOMOTION; MIGRAINE; NOCICEPTION; NOISE; NONHUMAN; PHONOPHOBIA; PHOTOPHOBIA; RAT; SENSITIVITY AND SENSIBILITY; SOUND SENSITIVITY; STARTLE REFLEX; WESTERN BLOTTING;

BEHAVIORAL MODEL; BISPHENOL A; MIGRAINE; XENOESTROGENS.;

ANIMALS; BEHAVIOR, ANIMAL; BENZHYDRYL COMPOUNDS; BRAIN; DISEASE MODELS, ANIMAL; ESTROGEN RECEPTOR ALPHA; ESTROGENS, NON-STEROIDAL; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; GROOMING; MIGRAINE DISORDERS; MOTOR ACTIVITY; PHENOLS; RATS; RATS, SPRAGUE-DAWLEY; SEX CHARACTERISTICS; STARTLE REACTION; TRANSCRIPTOME;

EID: 84893383357     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kft245     Document Type: Article

References (43)

1. Afra, J., Proietti Cecchini, A., Sandor, P. S., and Schoenen, J. (2000). Comparison of visual and auditory evoked cortical potentials in migraine patients between attacks. Clin. Neurophysiol. 111, 1124-1129.
2. Al-Mana, D., Ceranic, B., Djahanbakhch, O., and Luxon, L. M. (2010). Alteration in auditory function during the ovarian cycle. Hear. Res. 268, 114-122. doi:10.1016/j.heares.2010.05.007.
3. Aloisi, A. M., Della Seta, D., Ceccarelli, I., and Farabollini, F. (2001). Bisphenol-A differently affects estrogen receptors-alpha in estrous-cycling and lactating female rats. Neurosci. Lett. 310, 49-52.
4. Aloisi, A. M., Della Seta, D., Rendo, C., Ceccarelli, I., Scaramuzzino, A., and Farabollini, F. (2002). Exposure to the estrogenic pollutant bisphenol A affects pain behavior induced by subcutaneous formalin injection in male and female rats. Brain Res. 937, 1-7.
5. Bernstein, C., and Burstein, R. (2012). Sensitization of the trigeminovascular pathway: Perspective and implications to migraine pathophysiology. J. Clin. Neurol. 8, 89-99. doi:10.3988/jcn.2012.8.2.89.
6. Bohacek, J., and Daniel, J. M. (2009). The ability of oestradiol administration to regulate protein levels of oestrogen receptor alpha in the hippocampus and prefrontal cortex of middle-aged rats is altered following long-term ovarian hormone deprivation. J. Neuroendocrinol. 21, 640-647. doi:10.1111/j.1365-2826.2009.01882.x.
7. Burstein, R., Jakubowski, M., and Rauch, S. D. (2011). The science of migraine. J. Vestib. Res. 21, 305-314. doi:10.3233/VES-2012-0433.
8. Burstein, R., Yamamura, H., Malick, A., and Strassman, A. M. (1998). Chemical stimulation of the intracranial dura induces enhanced responses to facial stimulation in brain stem trigeminal neurons. J. Neurophysiol 79, 964-982.
9. Buse, D. C., Loder, E. W., Gorman, J. A., Stewart, W. F., Reed, M. L., Fanning, K. M., Serrano, D., and Lipton, R. B. (2013). Sex differences in the prevalence, symptoms, and associated features of migraine, probable migraine and other severe headache: Results of the American Migraine Prevalence and Prevention (AMPP) Study. Headache. 53, 1278-1299. doi:10.1111/head.12150.
10. Cairns, B. E., and Gazerani, P. (2009). Sex-related differences in pain. Maturitas 63, 292-296. doi:10.1016/j.maturitas.2009.06.004.
11. Calafat, A. M., Ye, X., Wong, L. Y., Reidy, J. A., and Needham, L. L. (2008). Exposure of the U.S. population to bisphenol A and 4-tertiary-octylphenol: 2003-2004. Environ. Health Perspect. 116, 39-44. doi:10.1289/ehp.10753.
12. Ceccarelli, I., Fiorenzani, P., Della Seta, D., Massafra, C., Cinci, G., Bocci, A., and Aloisi, A. M. (2009). Perinatal exposure to xenoestrogens affects pain in adult female rats. Neurotoxicol. Teratol. 31, 203-209. doi:10.1016/j. ntt.2009.02.004.
13. Chang, F. Y., and Lu, C. L. (2013). Irritable bowel syndrome and migraine: Bystanders or partners? J. Neurogastroenterol. Motil. 19, 301-311. doi:10.5056/jnm.2013.19.3.301.
14. Cupini, L. M., Bari, M., Battista, N., Argiro, G., Finazzi-Agro, A., Calabresi, P., and Maccarrone, M. (2006). Biochemical changes in endocannabinoid system are expressed in platelets of female but not male migraineurs. Cephalalgia 26, 277-281. doi:10.1111/j.1468-2982.2005.01031.x.
15. De Coster, S., and van Larebeke, N. (2012). Endocrine-disrupting chemicals: associated disorders and mechanisms of action. J. Environ. Public Health 2012, 52. doi:10.1155/2012/713696.
16. Duncko, R., Cui, L., Hille, J., Grillon, C., and Merikangas, K. R. (2008). Startle reactivity in children at risk for migraine. Clin. Neurophysiol. 119, 2733-2737. doi:10.1016/j.clinph.2008.09.005.
17. Greco, R., Gasperi, V., Sandrini, G., Bagetta, G., Nappi, G., Maccarrone, M., and Tassorelli, C. (2010). Alterations of the endocannabinoid system in an animal model of migraine: evaluation in cerebral areas of rat. Cephalalgia 30, 296-302. doi:10.1111/j.1468-2982.2009.01924.x.
18. Gupta, S., McCarson, K. E., Welch, K. M., and Berman, N. E. (2011). Mechanisms of pain modulation by sex hormones in migraine. Headache 51, 905-922. doi:10.1111/j.1526-4610.2011.01908.x.
19. Hudmon, A., Choi, J. S., Tyrrell, L., Black, J. A., Rush, A. M., Waxman, S. G., and Dib-Hajj, S. D. (2008). Phosphorylation of sodium channel Na(v)1.8 by p38 mitogen-activated protein kinase increases current density in dorsal root ganglion neurons. J. Neurosci. 28, 3190-3201. doi:10.1523/JNEUROSCI.4403-07.2008.
20. Lapensee, E. W., Tuttle, T. R., Fox, S. R., and Ben-Jonathan, N. (2009). Bisphenol A at low nanomolar doses confers chemoresistance in estrogen receptor-alpha-positive and -negative breast cancer cells. Environ. Health Perspect. 117, 175-180. doi:10.1289/ehp.11788.
21. Leranth, C., Hajszan, T., Szigeti-Buck, K., Bober, J., and MacLusky, N. J. (2008). Bisphenol A prevents the synaptogenic response to estradiol in hippocampus and prefrontal cortex of ovariectomized nonhuman primates. Proc. Natl Acad. Sci. USA. 105, 14187-14191. doi:10.1073/pnas.0806139105.
22. Levy, D., and Strassman, A. M. (2002). Mechanical response properties of A and C primary afferent neurons innervating the rat intracranial dura. J. Neurophysiol. 88, 3021-3031. doi:10.1152/jn.00029.2002.
23. Liverman, C. S., Brown, J. W., Sandhir, R., Klein, R. M., McCarson, K., and Berman, N. E. (2009a). Oestrogen increases nociception through ERK activation in the trigeminal ganglion: evidence for a peripheral mechanism of allodynia. Cephalalgia 29, 520-531. doi:10.1111/j.1468-2982.2008.01755.x.
24. Liverman, C. S., Brown, J. W., Sandhir, R., McCarson, K. E., and Berman, N. E. (2009b). Role of the oestrogen receptors GPR30 and ERalpha in peripheral sensitization: relevance to trigeminal pain disorders in women. Cephalalgia 29, 729-741. doi:10.1111/j.1468-2982.2008.01789.x.
25. Matulenko, M. A., Scanio, M. J., and Kort, M. E. (2009). Voltage-gated sodium channel blockers for the treatment of chronic pain. Curr. Top. Med. Chem. 9, 362-376.
26. Oshinsky, M. L., and Gomonchareonsiri, S. (2007). Episodic dural stimulation in awake rats: a model for recurrent headache. Headache 47, 1026-1036. doi:10.1111/j.1526-4610.2007.00871.x.
27. Panneton, W. M., Gan, Q., and Livergood, R. S. (2011). A trigeminoreticular pathway: Implications in pain. PLoS ONE 6, e24499. doi:10.1371/journal. pone.0024499.
28. Pottenger, L. H., Domoradzki, J. Y., Markham, D. A., Hansen, S. C., Cagen, S. Z., and Waechter, J. M., Jr. (2000). The relative bioavailability and metabolism of bisphenol A in rats is dependent upon the route of administration. Toxicol. Sci. 54, 3-18.
29. Rudel, R. A., Gray, J. M., Engel, C. L., Rawsthorne, T. W., Dodson, R. E., Ackerman, J. M., Rizzo, J., Nudelman, J. L., and Brody, J. G. (2011). Food packaging and bisphenol A and bis(2-ethyhexyl) phthalate exposure: findings from a dietary intervention. Environ. Health Perspect. 119, 914-920. doi:10.1289/ehp.1003170.
30. Schuelert, N., and McDougall, J. J. (2012). Involvement of Nav 1.8 sodium ion channels in the transduction of mechanical pain in a rodent model of osteoarthritis. Arthritis Res. Ther. 14, R5. doi:10.1186/ar3553.
31. Shapiro, R. E., and Goadsby, P. J. (2007). The long drought: the dearth of public funding for headache research. Cephalalgia 27, 991-994. doi:10.1111/j.1468-2982.2007.01396.x.
32. Society, I. H. (2013). The International Classification of Headache Disorders, 3rd Edition (beta version). Cephalalgia 33, 629-808. doi:10.1177/0333102413485658.
33. Society, I. H. (2004). The International Classification of Headache Disorders: 2nd edition. Cephalalgia 24 (Suppl. 1), 9-160.
34. Somerville, B. W. (1975). Estrogen-withdrawal migraine. II. Attempted prophylaxis by continuous estradiol administration. Neurology 25, 245-250.
35. Stang, P. E., and Osterhaus, J. T. (1993). Impact of migraine in the United States: data from the National Health Interview Survey. Headache 33, 29-35.
36. Stucky, N. L., Gregory, E., Winter, M. K., He, Y. Y., Hamilton, E. S., McCarson, K. E., and Berman, N. E. (2011). Sex differences in behavior and expression of CGRP-related genes in a rodent model of chronic migraine. Headache 51, 674-692. doi:10.1111/j.1526-4610.2011.01882.x.
37. Turvin, J. C., Messer, W. S., and Kritzer, M. F. (2007). On again, off again effect of gonadectomy on the acoustic startle reflex in male rats. Physiol. Behav. 90, 473-482.
38. Ueda, N., Puffenbarger, R. A., Yamamoto, S., and Deutsch, D. G. (2000). The fatty acid amide hydrolase (FAAH). Chem. Phys. Lipids 108, 107-121.
39. Vandenberg, L. N., Chahoud, I., Heindel, J. J., Padmanabhan, V., Paumgartten, F. J., and Schoenfelder, G. (2012). Urinary, circulating, and tissue biomonitoring studies indicate widespread exposure to bisphenol A. Cienc. saude coletiva 17, 407-434.
40. Vandenberg, L. N., Hauser, R., Marcus, M., Olea, N., and Welshons, W. V. (2007). Human exposure to bisphenol A (BPA). Reprod. Toxicol. 24, 139-177. doi:10.1016/j.reprotox.2007.07.010.
41. Vandenberg, L. N., Hunt, P. A., Myers, J. P., and Vom Saal, F. S. (2013). Human exposures to bisphenol A: Mismatches between data and assumptions. Rev. Environ. Health 28, 37-58. doi:10.1515/reveh-2012-0034.
42. Vandenberg, L. N., Maffini, M. V., Sonnenschein, C., Rubin, B. S., and Soto, A. M. (2009). Bisphenol-A and the great divide: A review of controversies in the field of endocrine disruption. Endocr. Rev. 30, 75-95. doi:10.1210/er.2008-0021.
43. Zhang, Y., Lu, N., Zhao, Z. Q., and Zhang, Y. Q. (2012). Involvement of estrogen in rapid pain modulation in the rat spinal cord. Neurochem. Res. 37, 2697-2705. doi:10.1007/s11064-012-0859-1.