CoChat
Sign Up
Cited by 73Effects and risks of endocrine disrupting chemicalsViral Infections and Immunology ResearchCardiac Fibrosis and Remodeling

BPA Alters Estrogen Receptor Expression in the Heart After Viral Infection Activating Cardiac Mast Cells and T Cells Leading to Perimyocarditis and Fibrosis

Open access
Bruno, Katelyn Ann, Mathews, Jessica Elizabeth, Yang, Alex Lingyun, Frisancho, J. Augusto, Scott, Ashley Jennie, Greyner, Henry David, Molina, Frank Anthony, Greenaway, Merci Shekinah +10 more·2019·Frontiers in Endocrinology
DOI 10.3389/fendo.2019.00598PMC PMC6737078
Open this paper in CoChat — free accountOpen PDF

Abstract

Myocarditis is an inflammatory heart disease that leads to dilated cardiomyopathy (DCM) and heart failure. Sex hormones play an important role in the development of myocarditis with testosterone driving disease in males and estrogen being cardioprotective in females. The human population is widely exposed to the endocrine disruptor bisphenol A (BPA) from plastics such as water bottles, plastic food containers, copy paper and receipts. Several clinical and numerous animal studies have found an association between elevated BPA levels and cardiovascular disease. A recent report found elevated levels of BPA in the serum of patients with DCM compared to healthy controls. In this study we examined whether exposure to BPA for two weeks prior to viral infection and leading up to myocarditis at day 10 altered inflammation in female BALB/c mice housed in standard plastic cages/water bottles with soy-free food and bedding. We found that a human relevant dose of BPA (25µg/L) in drinking water, with an estimated exposure of 5µg BPA/kg BW, significantly increased myocarditis and pericarditis compared to control water without altering viral genome levels in the heart. BPA exposure activated ERa and ERb in the spleen 24 hours after infection and phosphorylated ERa and ERb during myocarditis, but decreased ERa and increased ERb mRNA in the heart as measured by qRT-PCR. Exposure to BPA significantly increased CD4+ T cells, IFNg, IL-17A, TLR4, caspase-1, and IL-1b in the heart. BPA exposure also increased cardiac fibrosis compared to controls. Mast cells, which are associated with cardiac remodeling, were found to increase in number and degranulation, particularly along the pericardium. Interestingly, plastic caging/water bottle exposure alone led to increased mast cell numbers, pericardial degranulation and fibrosis in female BALB/c mice compared to animals housed in glass cages/water bottles with soy-free food and bedding. These data suggest that BPA exposure may increase the risk of developing myocarditis after a viral infection in women.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3389/fendo.2019.00598

Cites

6 of 6 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Increased TNFα and IL-1β in the heart and perivascular fibrosis were found, which typically indicates perivascular mast cell degranulation.

    “They also found increased TNF α and IL-1 β in the heart and perivascular fibrosis, which in our experience typically indicates perivascular mast cell degranulation. 157,160,182,183”

    From COVID-19, Myocarditis and Pericarditis (2023) · cites this paper as [183]

    The Results (BPA Effect on Inflammatory Mediators; page unavailable) report increased cardiac IL-1β after BPA exposure and show perivascular fibrosis in the treated mice. They do not report increased TNFα in the heart; the Discussion mentions TNFα release in other cell studies instead. The statement about what typically indicates perivascular mast-cell degranulation is explicitly the citing authors’ own interpretation. (LLM, conf=0.87)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 74

  1. [1]Pauschinger M Phan MD Doerner A Kuehl U Schwimmbeck PL Poller W. Enteroviral RNA replication in the myocardium of patients with left ventricular dysfunction and clinically suspected myocarditis. Circulation. (1999) 99: 889– 95. 10.1161/01.CIR.99.7.889 10027811 · DOI
  2. [2]Kuhl U Pauschinger M Seeberg B Lassner D Noutsias M Poller W. Viral persistence in the myocardium is associated with progressive cardiac dysfunction. Circulation. (2005) 112: 1965– 70. 10.1161/CIRCULATIONAHA.105.548156 16172268 · DOI
  3. [4]Coronado MJ Bruno KA Blauwet LA Tschope C Cunningham MW Pankuweit S. Elevated sera sST2 is associated with heart failure in men ≤50 years old with myocarditis. J Am Heart Assoc. (2019) 8: e008968. 10.1161/JAHA.118.008968 30638108 PMC6497352 · DOI · Paper page
  4. [5]Cocker MS Abdel-Aty H Strohm O Friedrich MG. Age and gender effects on the extent of myocardial involvement in acute myocarditis: a cardiovascular magnetic resonance study. Heart. (2009) 95: 1925– 30. 10.1136/hrt.2008.164061 19710029 · DOI · Paper page
  5. [6]McNamara DM Starling RC Cooper LT Boehmer JP Mather PJ Janosko KM. Clinical and demographic predictors of outcomes in recent onset dilated cardiomyopathy: results of the IMAC (intervention in myocarditis and acute cardiomyopathy)-2 study. J Am Coll Cardiol. (2011) 58: 1112– 8. 10.1016/j.jacc.2011.05.033 21884947 PMC6467576 · DOI
  6. [7]Regitz-Zagrosek V Becher E Mahmoodzadeh S Schubert C Sex steroid hormones. In: M Bader, editors. Cardiovascular Hormone Systems: From Molecular Mechanisms to Novel Therapeutics (Weinheim: Wiley-Blackwell) (2008) 39– 64. 10.1002/9783527626236.ch2 · DOI
  7. [8]Vitale C Mendelsohn ME Rosano GMC. Gender differences in the cardiovascular effect of sex hormones. Nat Rev Cardiol. (2009) 6: 532– 42. 10.1038/nrcardio.2009.105 19564884 · DOI
  8. [9]Buskiewicz IA Huber SA Fairweather D Sex hormone receptor expression in the immune system. In: Neigh G, Mitzelfelt M, Editors. Sex Differences in Physiology. Amsterdam: Academic Press (2016). p. 45– 60.
  9. [10]Huber S. ERβ and ERα differentially regulate NKT and vγ4(+) T-cell activation and T-regulatory cell response in coxsackievirus B3 infected mice. J Clin Cell Immunol. (2015) 6: 1– 9. 10.4172/2155-9899.1000372 26925301 PMC4765002 · DOI
  10. [11]Koenig A Buskiewicz I Huber SA. Age-associated changes in estrogen receptor ratios correlate with increased female susceptibility to coxsackievirus B3-induced myocarditis. Front Immunol. (2017) 8: 1585. 10.3389/fimmu.2017.01585 29201031 PMC5696718 · DOI
  11. [12]Kararigas G Fliegner D Forler S Klein O Schubert C Gustafsson JA. Comparative proteomic analysis reveals sex and estrogen receptor beta effects in the pressure overloaded heart. J Proteome Res. (2014) 13: 5829– 36. 10.1021/pr500749j 25406860 · DOI
  12. [13]Liang Q Gao X Chen Y Hong K Wang HS. Cellular mechanism of the nonmonotonic dose response of bisphenol A in rat cardiac myocytes. Environ. Health Perspect. (2014) 122: 601– 8. 10.1289/ehp.1307491 24569941 PMC4050515 · DOI
  13. [14]Belcher SM Gear RB Kendig EL. Bisphenol A alters autonomic tone and extracellular matrix structure and induces sex-specific effects on cardiovascular function in male and female CD-1 mice. Endocrinology. (2015) 156: 882– 95. 10.1210/en.2014-1847 25594700 PMC4330319 · DOI
  14. [15]Dworatzek E Mahmoodzadeh S Schriever C Kusumoto K Kramer L Santos G. Sex-specific regulation of collagen I and III expression by 17β-estradiol in cardiac fibroblasts: Role of estrogen receptors. Cardiovasc Res. (2019) 115: 315– 27. 10.1093/cvr/cvy185 30016401 PMC6933535 · DOI
  15. [16]Mohamad Zaid SS Kassim NM Othman S. Tualang honey protects against BPA-induced morphological abnormalities and disruption of ERα, ERβ, and C3 mRNA and protein expressions in the uterus of rats. Evid Based Compl Alt Med. (2015) 2015: 1– 18. 10.1155/2015/202874 26788107 PMC4691614 · DOI
  16. [17]Birnbaum LS. State of the science of endocrine disruptors. Environ Health Perspect. (2013) 121: A107. 10.1289/ehp.1306695 23548815 PMC3620755 · DOI
  17. [18]Gerona RR Pan J Zota AR Schwartz JM Friesen M Taylor JA. Direct measurement of bisphenol A (BPA), BPA glucuronide and BPA sulfate in a diverse and low-income population of pregnant women reveals high exposure, with potential implications for previous exposure estimates: a cross-sectional study. Environ. Health. (2016) 15: 50. 10.1186/s12940-016-0131-2 27071747 PMC4828888 · DOI
  18. [19]Oldring PKT Castle L O'mahony C Dixon J. Estimates of dietary exposure to bisphenol A (BPA) from light metal packaging using food consumption and packaging usage data: A refined deterministic approach and a fully probabilistic (facet) approach. Food Addit Contaminants. (2014) 31: 466– 89. 10.1080/19440049.2013.860240 24405320 PMC3998095 · DOI
  19. [20]Corrales J Kristofco LA Baylor Steele W Yates BS Breed CS Spencer Williams E. Global assessment of bisphenol A in the environment: Review and analysis of its occurrence and bioaccumulation. Dose-Response. (2015) 13: 1– 29. 10.1177/1559325815598308 26674671 PMC4674187 · DOI
  20. [21]Lorber M Schecter A Paepke O Shropshire W Christensen K Birnbaum L. Exposure assessment of adult intake of bisphenol A (BPA) with emphasis on canned food dietary exposures. Environ. Int. (2015) 77: 55– 62. 10.1016/j.envint.2015.01.008 25645382 PMC4469126 · DOI · Paper page
  21. [22]Ndaw S Remy A Jargot D Robert A. Occupational exposure of cashiers to bisphenol A via thermal paper: urinary biomonitoring study. Int. Arch. Occup. Environ. Health. (2016) 89: 935– 46. 10.1007/s00420-016-1132-8 27126703 PMC4927604 · DOI
  22. [23]Volkel W Colnot T Csanady GA Filser JG Dekant W. Metabolism and kinetics of bisphenol A in humans at low doses following oral administration. Chem Res Toxicol. (2002) 15: 1281– 7. 10.1021/tx025548t 12387626 · DOI
  23. [25]Draganov DI Markham DA Beyer D Waechter JM Jr Dimond SS Budinsky RA Extensive metabolism and route-dependent pharmacokinetics of bisphenol A (BPA) in neonatal mice following oral or subcutaneous administration. Toxicology. (2015) 333: 168– 78. 10.1016/j.tox.2015.04.012 25929835 · DOI
  24. [26]Barrett JR. The pharmacokinetics of BPA: Similarities in human and animal metabolism suggest higher exposure than thought. Environ Health Perspect. (2011) 119: A177. 10.1289/ehp.119-a177a 21459706 PMC3080961 · DOI
  25. [27]Seillet C Laffont S Tremollieres F Rouquie N Ribot C Arnal JF. The TLR-mediated response of plasmacytoid dendritic cells is positively regulated by estradiol in vivo through cell-intrinsic estrogen receptor alpha signaling. Blood. (2012) 119: 454– 64. 10.1182/blood-2011-08-371831 22096248 · DOI
  26. [28]Matthews JB Twomey K Zacharewski TR. In vitro and in vivo interactions of bisphenol A and its metabolite, bisphenol A glucuronide, with estrogen receptors alpha and beta. Chem Res Toxicol. (2001) 14: 150– 7. 10.1021/tx0001833 11258963 · DOI
  27. [29]Li L Wang Q Zhang Y Niu Y Yao X Liu H. The molecular mechanism of bisphenol A (BPA) as an endocrine disruptor by interacting with nuclear receptors: insights from molecular dynamics (md) simulations. PLoS ONE. (2015) 10: 1– 18. 10.1371/journal.pone.0120330 25799048 PMC4370859 · DOI
  28. [30]Teng C Goodwin B Shockley K Xia M Huang R Norris J. Bisphenol A affects androgen receptor function via multiple mechanisms. Chem Biol Interact. (2013) 203: 556– 64. 10.1016/j.cbi.2013.03.013 23562765 PMC3722857 · DOI
  29. [31]Bae S Kim JH Lim Y-H Park HY Hong Y-C. Associations of bisphenol A exposure with heart rate variability and blood pressure. Hypertension. (2012) 60: 786– 93. 10.1161/HYPERTENSIONAHA.112.197715 22851732 · DOI
  30. [33]Han C Hong Y. Bisphenol A, hypertension, and cardiovascular diseases: Epidemiological, laboratory, and clinical trial evidence. Curr Hypert Rep. (2016) 18: 11. 10.1007/s11906-015-0617-2 26781251 · DOI · Paper page
  31. [34]Lind PM Lind L. Circulating levels of bisphenol A and phthalates are related to carotid atherosclerosis in the elderly. Atherosclerosis. (2011) 218: 207– 13. 10.1016/j.atherosclerosis.2011.05.001 21621210 · DOI
  32. [35]Fang C Ning B Waqar AB Niimi M Li S Satoh K. Bisphenol A exposure enhances atherosclerosis in whhl rabbits. PLoS ONE. (2014) 9: 1– 11. 10.1371/journal.pone.0110977 25333893 PMC4205098 · DOI
  33. [36]Gao X Wang HS. Impact of bisphenol A on the cardiovascular system - epidemiological and experimental evidence and molecular mechanisms. Int J Environ Res Publ Health. (2014) 11: 8399– 413. 10.3390/ijerph110808399 25153468 PMC4143868 · DOI
  34. [37]Kasneci A Lee JS Yun TJ Shang J Lampen S Gomolin T. From the cover: lifelong exposure of C57BL/6n male mice to bisphenol A or bisphenol S reduces recovery from a myocardial infarction. Toxicol Sci. (2017) 159: 189– 202. 10.1093/toxsci/kfx133 28903498 · DOI
  35. [38]Xiong Q Liu X Shen Y Yu P Chen S Hu J. Elevated serum bisphenol A level in patients with dilated cardiomyopathy. Int J Environ Res Publ Health. (2015) 12: 5329– 37. 10.3390/ijerph120505329 25996886 PMC4454970 · DOI
  36. [39]Fairweather D Petri MA Coronado MJ Cooper LT. Autoimmune heart disease: role of sex hormones and autoantibodies in disease pathogenesis. Expert Rev Clin Immunol. (2012) 8: 269– 84. 10.1586/eci.12.10 22390491 PMC3318944 · DOI
  37. [40]Myers JM Fairweather D Huber SA Cunningham MW. Autoimmune myocarditis, valvulitis, and cardiomyopathy. Curr Protocols Immunol. (2013) Unit 15.14.11-51. 10.1002/0471142735.im1514s101 PMC3672855 23564686 · DOI · Paper page
  38. [41]Jenkins S Wang J Eltoum I Desmond R Lamartiniere CA. Chronic oral exposure to bisphenol A results in a nonmonotonic dose response in mammary carcinogenesis and metastasis in mmtv-erbb2 mice. Environ Health Perspect. (2011) 119: 1604– 9. 10.1289/ehp.1103850 21988766 PMC3226508 · DOI
  39. [42]Cagen SZ Waechter JM Jr Dimond SS Breslin WJ Butala JH Jekat FW. Normal reproductive organ development in wistar rats exposed to bisphenol A in the drinking water. Regul Toxicol Pharmacol. (1999) 30 (2 Pt 1): 130– 9. 10.1006/rtph.1999.1340 10536108 · DOI
  40. [43]Vandenberg LN Maffini MV Sonnenschein C Rubin BS Soto AM. Bisphenol-A and the great divide: A review of controversies in the field of endocrine disruption. Endocr Rev. (2009) 30: 75– 95. 10.1210/er.2008-0021 19074586 PMC2647705 · DOI
  41. [44]Coronado MJ Brandt JE Kim E Bucek A Bedja D Abston ED. Testosterone and interleukin-1β increase cardiac remodeling during coxsackievirus B3 myocarditis via serpin A 3n. Am J Physiol Heart Circulat Physiol. (2012) 302: H1726– 1736. 10.1152/ajpheart.00783.2011 22328081 PMC3330806 · DOI · Paper page
  42. [45]Antoniak SAO III. Par-1 contributes to the innate immune response during viral infection. J Clin. (2013) 123: 1310– 22. 10.1172/JCI66125 23391721 PMC3582138 · DOI
  43. [47]Howdeshell KL Peterman PH Judy BM Taylor JA Orazio CE Ruhlen RL. Bisphenol A is released from used polycarbonate animal cages into water at room temperature. Environ Health Perspect. (2003) 111: 1180– 7. 10.1289/ehp.5993 12842771 PMC1241572 · DOI
  44. [48]Imazio M Cooper LT. Management of myopericarditis. Expert Rev Cardiovas Ther. (2013) 11: 193– 201. 10.1586/erc.12.184 23405840 · DOI
  45. [49]O'Brien E Dolinoy DC Mancuso P. Perinatal bisphenol a exposures increase production of pro-inflammatory mediators in bone marrow-derived mast cells of adult mice. J Immunotoxicol. (2014) 11: 205– 12. 10.3109/1547691X.2013.822036 23914806 PMC3983174 · DOI
  46. [50]Fairweather D Frisancho-Kiss S Gatewood S Njoku D Steele R Barrett M. Mast cells and innate cytokines are associated with susceptibility to autoimmune heart disease following coxsackievirus B3 infection. Autoimmunity. (2004) 37: 131– 45. 10.1080/0891693042000196200 15293883 · DOI · Paper page
  47. [51]Molina-Molina J Amaya E Grimaldi M Sáenz JM Real M Fernández MF. In vitro study on the agonistic and antagonistic activities of bisphenol-S and other bisphenol-A congeners and derivatives via nuclear receptors. Toxicol Appl Pharmacol. (2013) 272: 127– 36. 10.1016/j.taap.2013.05.015 23714657 · DOI
  48. [52]Campesi I Marino M Montella A Pais S Franconi F. Sex differences in estrogen receptor α and β levels and activation status in LPS-stimulated human macrophages. J Cellul Physiol. (2016) 232: 340– 345. 10.1002/jcp.25425 27171902 · DOI
  49. [53]Yoshino S Yamaki K Li X Sai T Yanagisawa R Takano H. Prenatal exposure to bisphenol A up-regulates immune responses, including T helper 1 and T helper 2 responses, in mice. Immunology. (2004) 112: 489– 95. 10.1111/j.1365-2567.2004.01900.x 15196218 PMC1782504 · DOI
  50. [54]Fairweather D Frisancho-Kiss S Yusung S Barrett M Gatewood S Davis S IFN-γ protects against chronic viral myocarditis by reducing mast cell degranulation, fibrosis, and the profibrotic cytokines TGF-β1, IL-1β, and IL-4 in the heart. Am J Pathol. (2004) 165: 1883– 94. 10.1016/S0002-9440(10)63241-5 15579433 PMC1618717 · DOI · Paper page
  51. [55]Rittie L. Method for picrosirius red-polarization detection of collagen fibers in tissue sections. Methods Mol Biol. (2017) 1627: 395– 407. 10.1007/978-1-4939-7113-8_26 28836216 · DOI
  52. [56]Thigpen JE Setchell KDR Kissling GE Locklear J Caviness GF Whiteside T. The estrogenic content of rodent diets, bedding, cages, and water bottles and its effect on bisphenol A studies. J Am Assoc Lab Anim Sci. (2013) 52: 130– 41. 23562095 PMC3624780
  53. [57]Honeycutt JA Nguyen JQT Kentner AC Brenhouse HC. Effects of water bottle materials and filtration on bisphenol A content in laboratory animal drinking water. J Am Assoc Lab Anim Sci. (2017) 56: 269– 72. 28535862 PMC5438920
  54. [58]Gorence GJ Pulcastro HC Lawson CA Gerona RR Friesen M Horan TS. Chemical contaminants from plastics in the animal environment. J Am Assoc Lab Anim Sci. (2019) 58: 190– 6. 10.30802/AALAS-JAALAS-18-000074 30646968 PMC6433350 · DOI
  55. [59]Grosovsky AJ Little JB. Evidence for linear response for the induction of mutations in human cells by x-ray exposures below 10 rads. Proc Natl Acad Sci USA. (1985) 82: 2092– 5. 10.1073/pnas.82.7.2092 3856885 PMC397498 · DOI
  56. [60]Spassova MA Miller DJ Eastmond DA Nikolova NS Vulimiri SV Caldwell J. Dose-response analysis of bromate-induced DNA damage and mutagenicity is consistent with low-dose linear, nonthreshold processes. Environ Mol Mutagen. (2013) 54: 19– 35. 10.1002/em.21737 23015362 · DOI
  57. [61]Mattson MP. Hormesis defined. Ageing Res Rev. (2008) 7: 1– 7. 10.1016/j.arr.2007.08.007 18162444 PMC2248601 · DOI · Paper page
  58. [64]Kharrazian D. The potential roles of bisphenol A (BPA) pathogenesis in autoimmunity. Autoimmune Dis. (2014) 2014: 743616. 10.1155/2014/743616 24804084 PMC3997912 · DOI
  59. [65]Panchanathan R Liu H Leung Y-KK Ho S-MM Choubey D. Bisphenol A (BPA) stimulates the interferon signaling and activates the inflammasome activity in myeloid cells. Mol Cell Endocrinol. (2015) 415: 45– 55. 10.1016/j.mce.2015.08.003 26277401 PMC4581997 · DOI
  60. [67]Liu Y Mei C Liu H Wang H Zeng G Lin J. Modulation of cytokine expression in human macrophages by endocrine-disrupting chemical bisphenol-A. Biochem Biophys Res Commun. (2014) 451: 592– 8. 10.1016/j.bbrc.2014.08.031 25128825 · DOI
  61. [68]Nowak K Jablonska E Ratajczak-Wrona W. Immunomodulatory effects of synthetic endocrine disrupting chemicals on the development and functions of human immune cells. Environ Int. (2019) 125: 350– 64. 10.1016/j.envint.2019.01.078 30743143 · DOI
  62. [69]Hall JM Mcdonnell DP. The estrogen receptor β-isoform (ERβ) of the human estrogen receptor modulates eralpha transcriptional activity and is a key regulator of the cellular response to estrogens and antiestrogens. Endocrinology. (1999) 140: 5566– 78. 10.1210/endo.140.12.7179 10579320 · DOI
  63. [70]Acconcia F Pallottini V Marino M. Molecular mechanisms of action of BPA. Dose-Response. (2015) 13: 1559325815610582. 10.1177/1559325815610582 26740804 PMC4679188 · DOI
  64. [71]Matsushima A Kakuta Y Teramoto T Koshiba T Liu X Okada H. Structural evidence for endocrine disruptor bisphenol A binding to human nuclear receptor ERR gamma. J Biochem. (2007) 142: 517– 24. 10.1093/jb/mvm158 17761695 · DOI
  65. [72]Baldeviano GC Barin JG Talor MV Srinivasan S Bedja D Zheng D. Interleukin-17A is dispensable for myocarditis but essential for the progression to dilated cardiomyopathy. Circul Res. (2010) 106: 1646– 55. 10.1161/CIRCRESAHA.109.213157 20378858 · DOI · Paper page
  66. [73]Cunningham MA Wirth JR Naga O Eudaly J Gilkeson GS. Estrogen receptor alpha binding to ere is required for full TLR7- and TLR9-induced inflammation. SOJ Immunol. (2014) 2: 07. 10.15226/soji.2014.00107 25061615 PMC4106444 · DOI
  67. [74]Young NA Wu LC Burd CJ Friedman AK Kaffenberger BH Rajaram MV. Estrogen modulation of endosome-associated Toll-like receptor 8: An IFNalpha-independent mechanism of sex-bias in systemic lupus erythematosus. Clin Immunol. (2014) 151: 66– 77. 10.1016/j.clim.2014.01.006 24525049 PMC4066385 · DOI
  68. [75]Liao S-L Tsai M-H Lai S-H Yao T-C Hua M-C Yeh K-W. Prenatal exposure to bisphenol-A is associated with Toll-like receptor induced cytokine suppression in neonates. Pediatric Res. (2016) 79: 438– 44. 10.1038/pr.2015.234 26571221 · DOI
  69. [76]Belcher SM Chen Y Yan S Wang H-S. Rapid estrogen receptor-mediated mechanisms determine the sexually dimorphic sensitivity of ventricular myocytes to 17β-estradiol and the environmental endocrine disruptor bisphenol A. Endocrinology. (2012) 153: 712– 20. 10.1210/en.2011-1772 22166976 PMC3275382 · DOI
  70. [77]Hu Y Zhang L Wu X Hou L Li Z Ju J Bisphenol A, an environmental estrogen-like toxic chemical, induces cardiac fibrosis by activating the ERK1 / 2 pathway. Toxicol Lett. (2016) 251: 1– 9. 10.1016/j.toxlet.2016.03.008 27025157 · DOI
  71. [78]Draber P Halova I Polakovicova I Kawakami T. Signal transduction and chemotaxis in mast cells. Eur J Pharmacol. (2016) 778: 11– 23. 10.1016/j.ejphar.2015.02.057 25941081 PMC4630209 · DOI
  72. [79]Fairweather D Frisancho-Kiss S Njoku DB Nyland JF Kaya Z Yusung SA. Complement receptor 1 and 2 deficiency increases coxsackievirus B3-induced myocarditis, dilated cardiomyopathy, and heart failure by increasing macrophages, IL-1beta, and immune complex deposition in the heart. J Immunol. (2006) 176: 3516– 24. 10.4049/jimmunol.176.6.3516 16517720 · DOI · Paper page
  73. [80]Irani AA Schechter NM Craig SS Deblois G Schwartz LB. Two types of human mast cells that have distinct neutral protease compositions. Proc Nat Acad Sci USA. (1986) 83: 4464– 8. 10.1073/pnas.83.12.4464 3520574 PMC323754 · DOI
  74. [81]Otsuka A Nonomura Y Kabashima K. Roles of basophils and mast cells in cutaneous inflammation. Semi Immunopathol. (2016) 38: 563– 70. 10.1007/s00281-016-0570-4 27170045 · DOI

Cited by

Sorted by citations

Authors
Bruno, K. A., Mathews, J. E., Yang, A. L., Frisancho, J. A., Scott, A. J., Greyner, H. D., Molina, F. A., Greenaway, M. S., Cooper, G. M., Bucek, A., Morales-Lara, A. C., Hill, A. R., Mease, A. A., Di Florio, D. N., Sousou, J. M., Coronado, A. C., Stafford, A. R., & Fairweather, D.
Affiliations
  • Mayo Clinic (US)
  • Johns Hopkins University (US)
Corresponding author
Fairweather, DeLisa
ORCID
Venue
Frontiers in Endocrinology
Publisher
Frontiers Media SA
Published
2019-09-04
Volume
10
Pages
598-598
ISSN
1664-2392 (ISSN-L)
DOI
10.3389/fendo.2019.00598
PMC
PMC6737078
OpenAlex
W2967622055
Cited by
73
References
6
Citations by year
2026: 5 · 2025: 12 · 2024: 10 · 2023: 10 · 2022: 11 · 2021: 16 · 2020: 8 · 2019: 1
FWCI
3.89
Type
journal article
Language
en
Open access
Licence
Locations
  • Frontiers in Endocrinology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • American Heart Association (16GRNT30950007)
  • National Institutes of Health (NIH-R01, ES07141, TR002380, HL111938, TL1TR002380)
  • National Heart, Lung, and Blood Institute (R01HL111938)
  • National Institute of Allergy and Infectious Diseases (R21AI145356)
  • National Institute of Environmental Health Sciences (R21ES024414, T32ES007141)
  • National Center for Advancing Translational Sciences
Topics
  • Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Effects and risks of endocrine disrupting chemicals
  • Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Viral Infections and Immunology Research
  • Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac Fibrosis and Remodeling
Keywords
bisphenol A, estrogen receptor alpha, estrogen receptor beta, myocarditis, pericarditis, myocardial fibrosis, mast cells, mast cell degranulation, CD4+ T cells, viral infection, endocrine disruptors, dilated cardiomyopathy, inflammation, sex differences, female mice

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review