Los Disruptores Endocrinos Como Obesógenos Ambientales: Efectos en Proteínas Adipogénicas Clave

  • Fernando Guerrero-Meza Centro de Investigación Biomédica Avanzada, Facultad de Medicina, Universidad Autónoma de Querétaro, Querétaro, México
  • Paulina Vega-Morales Centro de Investigación Biomédica Avanzada, Facultad de Medicina, Universidad Autónoma de Querétaro, Querétaro, México
  • Vianey Rubio Centro de Investigación Biomédica Avanzada, Facultad de Medicina, Universidad Autónoma de Querétaro, Querétaro, México
  • Haydé Vergara-Castañeda Centro de Investigación Biomédica Avanzada, Facultad de Medicina, Universidad Autónoma de Querétaro, Querétaro, México
  • Ana Sánchez-Tusie Centro de Investigación Biomédica Avanzada, Facultad de Medicina, Universidad Autónoma de Querétaro, Querétaro, México
  • Marisela Ahumada-Solórzano Facultad de Ciencias Naturales, Universidad Autónoma de Querétaro, Querétaro, México
  • Juan Carlos Solis-Sáinz Centro de Investigación Biomédica Avanzada, Facultad de Medicina, Universidad Autónoma de Querétaro, Querétaro, México
  • Gabriela Hernández-Puga Centro de Investigación Biomédica Avanzada, Facultad de Medicina, Universidad Autónoma de Querétaro, Querétaro, México
Keywords: EDC, obesogen, adipogenesis, PPARγ, endocrine disruptor

Abstract

Los disruptores endocrinos (EDC) son compuestos químicos exógenos de origen sintético o natural que interfieren en las funciones hormonales. Se estima que más de 1000 compuestos químicos presentes en el medio ambiente poseen una posible actividad disruptora. La exposición a EDC se ha relacionado con el desarrollo de múltiples enfermedades como la obesidad. Los obesógenos son compuestos químicos xenobióticos que regulan y promueven inadecuadamente la acumulación de lípidos y la adipogénesis. La adipogénesis es el proceso mediante el cual las células progenitoras similares a fibroblastos restringen su destino a las células adipogénicas, acumulan nutrientes y se convierten en adipocitos maduros. Para conocer las principales evidencias científicas de la última década sobre los efectos obesogénicos de los EDC, se realizó una búsqueda en la literatura empleando las plataformas Scopus y Pubmed. El análisis arrojó 60 artículos originales de los cuales 24 fueron seleccionados por brindar información sobre proteínas adipogénicas clave. Los datos muestran que los EDC como los compuestos de organoestaño, ftalatos y bisfenoles estimulan vías de señalización adipogénicas clave mediadas por el receptor activado por el proliferador de peroxisomas-γ y la CCAAT/proteína de unión al potenciador-α, factores similares a krüppel y receptores de hormonas tiroideas, estrógeno y glucocorticoides; en relación a factores como el tipo, la concentración y el período de exposición al disruptor. Además, sus efectos podrían ser potenciados por la presencia de una dieta alta en grasas o una mezcla de diferentes tipos de EDC. En conclusión, los EDC inducen efectos obesogénicos a través de la estimulación de vías de señalización adipogénicas; y se requieren más estudios para comprender los mecanismos moleculares que subyacen a los efectos de los EDC para determinar su relevancia fisiológica y promover aún más su regulación en la industria.

Endocrine disruptors (EDC) are exogenous chemical compounds of synthetic or natural origin which interfere with hormonal functions. It is estimated that more than 1000 chemical compounds present in the enviroment have possible disruptive activity. Exposure to endocrine disruptors has been linked to the development of multiple diseases such as obesity. Obesogens are xenobiotic chemical compounds that inappropriately regulate and promote lipid accumulation and adipogenesis. Adipogenesis is the process by which fibroblast-like progenitor cells restrict their fate to adipogenic cells, accumulate nutrients, and develop into mature adipocytes. To know the main scientific evidence from the last decade regarding the obesogenic effects of EDC, a literature research was conducted using Scopus and Pubmed platforms. The analysis showed 60 original articles from which 24 were selected for providing information on key adipogenic proteins. Data shows that EDC such as organotin compounds, phthalates and bisphenols stimulate key adipogenic signaling pathways mediated by peroxisome proliferator activated receptor-γ and CCAAT-enhancer binding protein-α, krüppel like factors, and thyroid, estrogen and glucocorticoid receptors; in relation to factors like type, concentration and period of exposure to the disruptor. Furthermore, their effects could be potentiated by the presence of a high fat diet or a mix of diferent types of EDC. In conclusion, EDC induce obesogenic effects through the stimulation of adipogenic signaling pathways; in addition, more studies are required to understand the molecular mechanisms that underlie EDC effects to determine their physiological relevance, and to further promote their regulation in the industry.

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References

1. Adoamnei, E., Mendiola, J., Vela-Soria, F., Fernández, M. F., Olea, N., Jørgensen, N., Swan, S. H., & Torres-Cantero, A. M. (2018). Urinary bisphenol A concentrations are associated with reproductive parameters in young men. Environmental Research, 161, 122–128. https://doi.org/10.1016/j.envres.2017.11.002
2. Ambele, M. A., Dhanraj, P., Giles, R., & Pepper, M. S. (2020). Adipogenesis: A complex interplay of multiple molecular determinants and pathways. International Journal of Molecular Sciences, 21(12), 4283. https://doi.org/10.3390/ijms21124283
3. Angle, B. M., Do, R. P., Ponzi, D., Stahlhut, R. W., Drury, B. E., Nagel, S. C., Welshons, W. V., Besch-Williford, C. L., Palanza, P., Parmigiani, S., vom Saal, F. S., & Taylor, J. A. (2013). Metabolic disruption in male mice due to fetal exposure to low but not high doses of bisphenol A (BPA): Evidence for effects on body weight, food intake, adipocytes, leptin, adiponectin, insulin and glucose regulation. Reproductive Toxicology, 42, 256–268. https://doi.org/10.1016/j.reprotox.2013.07.017
4. Ariemma, F., D’Esposito, V., Liguoro, D., Oriente, F., Cabaro, S., Liotti, A., Cimmino, I., Longo, M., Beguinot, F., Formisano, P., & Valentino, R. (2016). Low-dose bisphenol-a impairs adipogenesis and generates dysfunctional 3T3-L1 adipocytes. PLOS ONE, 11(3). https://doi.org/10.1371/journal.pone.0150762
5. Arsenescu, V., Arsenescu, R. I., King, V., Swanson, H., & Cassis, L. A. (2008). Polychlorinated biphenyl-77 induces adipocyte differentiation and proinflammatory adipokines and promotes obesity and atherosclerosis. Environmental Health Perspectives, 116(6), 761–768. https://doi.org/10.1289/ehp.10554
6. Artacho-Cordón, F., Fernández, M. F., Frederiksen, H., Iribarne-Durán, L. M., Jiménez-Díaz, I., Vela-Soria, F., Andersson, A. M., Martin-Olmedo, P., Peinado, F. M., Olea, N., & Arrebola, J. P. (2018). Environmental phenols and parabens in adipose tissue from hospitalized adults in southern Spain. Environment International, 119, 203–211. https://doi.org/10.1016/j.envint.2018.05.052
7. Atlas, E., Pope, L., Wade, M. G., Kawata, A., Boudreau, A., & Boucher, J. G. (2014). Bisphenol A increases aP2 expression in 3T3L1 by enhancing the transcriptional activity of nuclear receptors at the promoter. Adipocyte, 3 (3), 170–179. https://doi.org/10.4161/adip.28436
8. Bansal, A., Henao-Mejia, J., & Simmons, R. A. (2018). Immune System: An Emerging Player in Mediating Effects of Endocrine Disruptors on Metabolic Health. Endocrinology, 159(1). 32–45. https://10.1210/en.2017-00882
9. Biemann, R., Fischer, B., & Navarrete Santos, A. (2014). Adipogenic effects of a combination of the endocrine-disrupting compounds bisphenol A, diethylhexylphthalate, and Tributyltin. Obesity Facts, 7(1), 48–56. https://doi.org/10.1159/000358913
10. Boucher, J. G., Boudreau, A., & Atlas, E. (2014). Bisphenol A induces differentiation of human preadipocytes in the absence of glucocorticoid and is inhibited by an estrogen-receptor antagonist. Nutrition & diabetes, 4(1), e102. https://doi.org/10.1038/nutd.2013.43
11. Bourguignon, J. P., Slama, R., Bergman, Å., Demeneix, B., Ivell, R., Kortenkamp, A., Panzica, G., Trasande, L., & Zoeller, R. T. (2016). Science-based regulation of endocrine disrupting chemicals in Europe: which approach?. The lancet. Diabetes & endocrinology, 4(8), 643–646. https://doi.org/10.1016/S2213-8587(16)30121-8
12. Casals-Casas, C., & Desvergne, B. (2011). Endocrine disruptors: From endocrine to metabolic disruption. Annual Review of Physiology, 73(1), 135–162. https://doi.org/10.1146/annurev-physiol-012110-142200
13. Chamorro-García, R., Shoucri, B. M., Willner, S., Käch, H., Janesick, A., & Blumberg, B. (2018). Effects of perinatal exposure to dibutyltin chloride on fat and glucose metabolism in mice, and molecular mechanisms, in vitro. Environmental Health Perspectives, 126(5), 057006. https://doi.org/10.1289/ehp3030
14. Chappell, V. A., Janesick, A., Blumberg, B., & Fenton, S. E. (2018). Tetrabromobisphenol-A promotes early adipogenesis and lipogenesis in 3T3-L1 cells. Toxicological Sciences, 166(2), 332–344. https://doi.org/10.1093/toxsci/kfy209
15. Chung, S., Kim, Y. J., Yang, S. J., Lee, Y., & Lee, M. (2016). Nutrigenomic functions of ppars in obesogenic environments. PPAR Research, 2016, 1–17. https://doi.org/10.1155/2016/4794576
16. Cimmino, I., Fiory, F., Perruolo, G., Miele, C., Beguinot, F., Formisano, P., & Oriente, F. (2020). Potential mechanisms of bisphenol A (BPA) contributing to human disease. International Journal of Molecular Sciences, 21(16), 5761. https://doi.org/10.3390/ijms21165761
17. Colborn, T., vom Saal, F. S., & Soto, A. M. (1993). Developmental effects of endocrine-disrupting chemicals in wildlife and humans. Environmental health perspectives, 101(5), 378–384. https://doi.org/10.1289/ehp.93101378
18. Darbre. P. D. (2017). Endocrine Disruptors and Obesity. Current Obesity Report, 6, 18-27. doi:10.1007/s13679-017-0240-4
19. Darbre, P. D. (2019). The history of endocrine-disrupting chemicals. Current Opinion in Endocrine and Metabolic Research, 7, 26–33. https://doi.org/10.1016/j.coemr.2019.06.007
20. Decherf, S., & Demeneix, B. A. (2011). The obesogen hypothesis: A shift of focus from the periphery to the hypothalamus. Journal of Toxicology and Environmental Health, Part B, 14(5-7), 423–448. https://doi.org/10.1080/10937404.2011.578561
21. Demeneix, B., Vandenberg, L. N., Ivell, R., & Zoeller, R. T. (2020). Thresholds and endocrine disruptors: An endocrine society policy perspective. Journal of the Endocrine Society, 4(10). https://doi.org/10.1210/jendso/bvaa085
22. Encuesta Nacional de Salud y Nutrición México 2018. (2019). Secretaría de Salud, Instituto Nacional de Salud Pública, Instituto Nacional de Estadística y Geografía, México. https://ensanut.insp.mx/encuestas/ensanut2018/informes.php
23. Fransway, A. F., Fransway, P. J., Belsito, D. V., & Yiannias, J. A. (2019). Paraben toxicology. Dermatitis, 30(1), 32–45. https://doi.org/10.1097/der.0000000000000428
24. García-Arévalo, M., Alonso-Magdalena, P., Servitja, J.-M., Boronat-Belda, T., Merino, B., Villar-Pazos, S., Medina-Gómez, G., Novials, A., Quesada, I., & Nadal, A. (2016). Maternal exposure to bisphenol-A during pregnancy increases pancreatic β-cell growth during early life in male mice offspring. Endocrinology, 157(11), 4158–4171. https://doi.org/10.1210/en.2016-1390
25. García-Solís P, García OP, Hernández-Puga G, Sánchez-Tusie AA, Sáenz-Luna CE, Hernández-Montiel HL, Solis-S JC. Thyroid hormones and obesity: a known but poorly understood relationship. Endokrynol Pol. 2018;69(3):292-303. doi: 10.5603/EP.2018.0032.
26. Ghaben, A. L., & Scherer, P. E. (2019). Adipogenesis and metabolic health. Nature Reviews Molecular Cell Biology, 20(4), 242–258. https://doi.org/10.1038/s41580-018-0093-z
27. González-Casanova, J. E., Pertuz-Cruz, S. L., Caicedo-Ortega, N. H., & Rojas-Gomez, D. M. (2020). Adipogenesis regulation and endocrine disruptors: Emerging insights in Obesity. BioMed Research International, 2020, 1–13. https://doi.org/10.1155/2020/7453786
28. González-Castro, M. I., Olea-Serrano, M. F., Rivas-Velasco, A. M., Medina-Rivero, E., Ordoñez-Acevedo, L. G., & De León-Rodríguez, A. (2011). Phthalates and bisphenols migration in Mexican food cans and plastic food containers. Bulletin of Environmental Contamination and Toxicology, 86(6), 627–631. https://doi.org/10.1007/s00128-011-0266-3
29. Gore, A. C., Chappell, V. A., Fenton, S. E., Flaws, J. A., Nadal, A., Prins, G. S., Toppari, J., & Zoeller, R. T. (2015). Executive summary to EDC-2: The endocrine society's second scientific statement on endocrine-disrupting chemicals. Endocrine Reviews, 36(6), 593–602. https://doi.org/10.1210/er.2015-1093
30. Gore, A. C., Crew, D., Doan, L. L., La Merrill, M., Patisaul, H., & Zota, A. (2014). Introduction to endocrine-disrupting chemicals. Endocrine-Disrupting Chemicals, 3–8. https://doi.org/10.1007/1-59745-107-x_1
31. Grün F, Watanabe H, Zamanian Z, Maeda L, Arima K, Cubacha R, Gardiner DM, Kanno J, Iguchi T, Blumberg B. (2006). Endocrine-disrupting organotin compounds are potent inducers of adipogenesis in vertebrates. Molecular Endocrinology. 20(9), 2141-2155. https://doi: 10.1210/me.2005-0367.
32. Grün, F., Blumberg, B. (2006). Environmental obesogens: Organotins and endocrine disruption via nuclear receptor signaling. Endocrinology, 147(6). https://doi.org/10.1210/en.2005-1129
33. Guarnotta, V., Amodei, R., Frasca, F., Aversa, A., & Giordano, C. (2022). Impact of chemical endocrine disruptors and hormone modulators on the endocrine system. International Journal of Molecular Sciences, 23(10), 5710. https://doi.org/10.3390/ijms23105710
34. Hao, C., Cheng, X., Xia, H., & Ma, X. (2013). The endocrine Disruptor Mono-(2-Ethylhexyl)Phthalate promotes adipocyte differentiation and induces obesity in mice. Bioscience Reports, 33(1), 619–629. https://doi.org/10.1042/bsr033e017
35. Heindel, J. J., Blumberg, B., Cave, M., Machtinger, R., Mantovani, A., Mendez, M. A., Nadal, A., Palanza, P., Panzica, G., Sargis, R., Vandenberg, L. N., & Vom Saal, F. (2017). Metabolism disrupting chemicals and metabolic disorders. Reproductive toxicology, 68, 3–33.
36. Heindel, J. J., & Blumberg, B. (2019). Environmental obesogens: Mechanisms and controversies. Annual Review of Pharmacology and Toxicology, 59(1), 89–106. https://doi.org/10.1146/annurev-pharmtox-010818-021304
37. Holm, L. J., Mønsted, M. Ø., Haupt-Jorgensen, M., & Buschard, K. (2020). PPARs and the development of type 1 diabetes. PPAR Research, 2020, 1–11. https://doi.org/10.1155/2020/6198628
38. Hu, P., Chen, X., Whitener, R. J., Boder, E. T., Jones, J. O., Porollo, A., Chen, J., & Zhao, L. (2012). Effects of parabens on adipocyte differentiation. Toxicological Sciences, 131(1), 56–70. https://doi.org/10.1093/toxsci/kfs262
39. Hu, P., Overby, H., Heal, E., Wang, S., Chen, J., Shen, C.-li, & Zhao, L. (2017). Methylparaben and butylparaben alter multipotent mesenchymal stem cell fates towards adipocyte lineage. Toxicology and Applied Pharmacology, 329, 48–57. https://doi.org/10.1016/j.taap.2017.05.019
40. Janesick, A. S., & Blumberg, B. (2016). Obesogens: An emerging threat to public health. American Journal of Obstetrics and Gynecology, 214(5), 559–565. https://doi.org/10.1016/j.ajog.2016.01.182
41. Jiang, Y., Berry, D. C., Tang, W., & Graff, J. M. (2014). Independent stem cell lineages regulate adipose organogenesis and adipose homeostasis. Cell Reports, 9(3), 1007–1022. https://doi.org/10.1016/j.celrep.2014.09.049
42. Kannan, A., Davila, J., Gao, L., Rattan, S., Flaws, J. A., Bagchi, M. K., & Bagchi, I. C. (2021). Maternal high-fat diet during pregnancy with concurrent phthalate exposure leads to abnormal placentation. Scientific Reports, 11(1). https://doi.org/10.1038/s41598-021-95898-4
43. Kassotis, C. D., Kollitz, E. M., Hoffman, K., Sosa, J. A., & Stapleton, H. M. (2019). Thyroid receptor antagonism as a contributory mechanism for adipogenesis induced by environmental mixtures in 3T3-L1 cells. Science of The Total Environment, 666, 431–444. https://doi.org/10.1016/j.scitotenv.2019.02.273
44. Kim, M. J., & Park, Y. J. (2019). Bisphenols and thyroid hormone. Endocrinology and Metabolism, 34(4), 340. https://doi.org/10.3803/enm.2019.34.4.340
45. Ko, C.-Y., Chang, W.-C., & Wang, J.-M. (2015). Biological roles of CCAAT/enhancer-binding protein delta during inflammation. Journal of Biomedical Science, 22(1). https://doi.org/10.1186/s12929-014-0110-2
46. Kovačič, A., Gys, C., Gulin, M. R., Kosjek, T., Heath, D., Covaci, A., & Heath, E. (2020). The migration of bisphenols from beverage cans and reusable sports bottles. Food Chemistry, 331, 127326. https://doi.org/10.1016/j.foodchem.2020.127326
47. Krais, A., Andersen, C., Eriksson, A., Johnsson, E., Nielsen, J., Pagels, J., Gudmundsson, A., Lindh, C., & Wierzbicka, A. (2018). Excretion of urinary metabolites of the phthalate esters DEP and DEHP in 16 volunteers after inhalation and dermal exposure. International Journal of Environmental Research and Public Health, 15(11), 2514. https://doi.org/10.3390/ijerph15112514
48. Lee M. J. (2017). Hormonal Regulation of Adipogenesis. Comprehensive Physiology, 7(4), 1151–1195. https://doi.org/10.1002/cphy.c160047
49. Lefterova, M. I., Haakonsson, A. K., Lazar, M. A., & Mandrup, S. (2014). PPARγ and the global map of adipogenesis and beyond. Trends in Endocrinology & Metabolism, 25(6), 293–302. https://doi.org/10.1016/j.tem.2014.04.001
50. Lind, P. M., & Lind, L. (2018). Endocrine-disrupting chemicals and risk of diabetes: An evidence-based review. Diabetologia, 61(7), 1495–1502. https://doi.org/10.1007/s00125-018-4621-3
51. Lowe, C. E., O'Rahilly, S., & Rochford, J. J. (2011). Adipogenesis at a glance. Journal of Cell Science, 124(21), 3726–3726. https://doi.org/10.1242/jcs.101741
52. Lutfi, E., Riera-Heredia, N., Córdoba, M., Porte, C., Gutiérrez, J., Capilla, E., & Navarro, I. (2017). Tributyltin and triphenyltin exposure promotes in vitro adipogenic differentiation but alters the adipocyte phenotype in rainbow trout. Aquatic toxicology, 188, 148–158. https://doi.org/10.1016/j.aquatox.2017.05.001
53. Lyche, J. L., Nourizadeh-Lillabadi, R., Almaas, C., Stavik, B., Berg, V., Skåre, J. U., Alestrøm, P., & Ropstad, E. (2010). Natural mixtures of persistent organic pollutants (POP) increase weight gain, advance puberty, and induce changes in gene expression associated with steroid hormones and obesity in female zebrafish. Journal of Toxicology and Environmental Health, Part A, 73(15), 1032–1057. https://doi.org/10.1080/15287394.2010.481618
54. Maradonna, F., & Carnevali, O. (2018). Lipid metabolism alteration by endocrine disruptors in animal models: An overview. Frontiers in Endocrinology, 9. https://doi.org/10.3389/fendo.2018.00654
55. Martínez-Ibarra, A., Martínez-Razo, L. D., Vázquez-Martínez, E. R., Martínez-Cruz, N., Flores-Ramírez, R., García-Gómez, E., López-López, M., Ortega-González, C., Camacho-Arroyo, I., & Cerbón, M. (2019). Unhealthy levels of phthalates and bisphenol A in Mexican pregnant women with gestational diabetes and its association to altered expression of mirnas involved with Metabolic Disease. International Journal of Molecular Sciences, 20(13), 3343. https://doi.org/10.3390/ijms20133343
56. Melzer, D., Gates, P., Osborn, N. J., Henley, W. E., Cipelli, R., Young, A., Money, C., McCormack, P., Schofield, P., Mosedale, D., Grainger, D., & Galloway, T. S. (2012). Correction: Urinary bisphenol A concentration and angiography-defined coronary artery stenosis. PLoS ONE, 7(11). https://doi.org/10.1371/annotation/5f293018-48a3-40ae-96b7-04438d1d9cb9
57. Mirza, A. Z., Althagafi, I. I., & Shamshad, H. (2019). Role of PPAR receptor in different diseases and their ligands: Physiological importance and clinical implications. European Journal of Medicinal Chemistry, 166, 502–513. https://doi.org/10.1016/j.ejmech.2019.01.067
58. Mishra, A., Zhu, X.-guang, Ge, K., & Cheng, S.-Y. (2010). Adipogenesis is differentially impaired by thyroid hormone receptor mutant isoforms. Journal of Molecular Endocrinology, 44(4), 247–255. https://doi.org/10.1677/jme-09-0137
59. Moon, S., Yu, S. H., Lee, C. B., Park, Y. J., Yoo, H. J., & Kim, D. S. (2021). Effects of bisphenol A on cardiovascular disease: An epidemiological study using National Health and Nutrition Examination survey 2003–2016 and Meta-analysis. Science of The Total Environment, 763, 142941. https://doi.org/10.1016/j.scitotenv.2020.142941
60. Moreno-Navarrete, J. M. & Fernández-Real, J. M. (2017). Adipocyte differentiation. Adipose tissue biology. 19-38. Springer, Cham. https://link.springer.com/book/10.1007/978-1-4614-0965-6
61. Nappi, F., Barrea, L., Di Somma, C., Savanelli, M., Muscogiuri, G., Orio, F., & Savastano, S. (2016). Endocrine aspects of environmental “Obesogen” pollutants. International Journal of Environmental Research and Public Health, 13(8), 765. https://doi.org/10.3390/ijerph13080765
62. Obregón, M.-J. (2014). Adipose tissues and thyroid hormones. Frontiers in Physiology, 5. https://doi.org/10.3389/fphys.2014.00479
63. Pang, L., Li, L., Zhu, L., Lang, J., & Bi., Y. (2019). Malignant transformation of vaginal adenosis to clear cell carcinoma without prenatal diethylstilbestrol exposure: a case report and literature review. BMC Cancer, 19. 2-8. https://10.1186/s12885-019-6026-1
64. Patisaul, H. B., Roberts, S. C., Mabrey, N., McCaffrey, K. A., Gear, R. B., Braun, J., Belcher, S. M., & Stapleton, H. M. (2013). Accumulation and endocrine disrupting effects of the flame retardant mixture firemaster®550 in rats: An exploratory assessment. Journal of Biochemical and Molecular Toxicology, 27(2), 124–136. https://doi.org/10.1002/jbt.21439
65. Pomatto, V., Cottone, E., Cocci, P., Mozzicafreddo, M., Mosconi, G., Nelson, E. R., Palermo, F. A., & Bovolin, P. (2018). Plasticizers used in food-contact materials affect adipogenesis in 3T3-L1 cells. The Journal of Steroid Biochemistry and Molecular Biology, 178, 322–332. https://doi.org/10.1016/j.jsbmb.2018.01.014
66. Riu, A., le Maire, A., Grimaldi, M., Audebert, M., Hillenweck, A., Bourguet, W., Balaguer, P., & Zalko, D. (2011). Characterization of novel ligands of ERΑ, ERΒ, and PPARγ: The case of halogenated bisphenol A and their conjugated metabolites. Toxicological Sciences, 122(2), 372–382. https://doi.org/10.1093/toxsci/kfr132
67. Rivollier, F., Krebs, M.-O., & Kebir, O. (2019). Perinatal exposure to environmental endocrine disruptors in the emergence of Neurodevelopmental Psychiatric Diseases: A systematic review. International Journal of Environmental Research and Public Health, 16(8), 1318. https://doi.org/10.3390/ijerph16081318
68. Sargis, R. M., Johnson, D. N., Choudhury, R. A., & Brady, M. J. (2010). Environmental endocrine disruptors promote adipogenesis in the 3T3-L1 cell line through glucocorticoid receptor activation. Obesity (Silver Spring, Md.), 18(7), 1283–1288. https://doi.org/10.1038/oby.2009.419
69. Sarjeant, K., & Stephens, J. M. (2012). Adipogenesis. Cold Spring Harbor Perspectives in Biology, 4(9). https://doi.org/10.1101/cshperspect.a008417
70. Shahnazaryan, U., Wójcik, M., Bednarczuk, T., & Kuryłowicz, A. (2019). Role of obesogens in the pathogenesis of obesity. Medicina, 55(9), 515. https://doi.org/10.3390/medicina55090515
71. Shoucri, B. M., Martinez, E. S., Abreo, T. J., Hung, V. T., Moosova, Z., Shioda, T., & Blumberg, B. (2017). Retinoid X receptor activation alters the chromatin landscape to commit mesenchymal stem cells to the adipose lineage. Endocrinology, 158(10), 3109–3125. https://doi.org/10.1210/en.2017-00348
72. Silva, B. S., Bertasso, I. M., Pietrobon, C. B., Lopes, B. P., Santos, T. R., Peixoto-Silva, N., Carvalho, J. C., Claudio-Neto, S., Manhães, A. C., Cabral, S. S., Kluck, G. E. G., Atella, G. C., Oliveira, E., Moura, E. G., & Lisboa, P. C. (2019). Effects of maternal bisphenol A on behavior, sex steroid and thyroid hormones levels in the adult rat offspring. Life Sciences, 218, 253–264. https://doi.org/10.1016/j.lfs.2018.12.039
73. Somm, E., Schwitzgebel, V. M., Toulotte, A., Cederroth, C. R., Combescure, C., Nef, S., Aubert, M. L., & Hüppi, P. S. (2009). Perinatal exposure to bisphenol A alters early adipogenesis in the rat. Environmental Health Perspectives, 117(10), 1549–1555. https://doi.org/10.1289/ehp.11342
74. Taylor, J. A., vom Saal, F. S., Welshons, W. V., Drury, B., Rottinghaus, G., Hunt, P. A., Toutain, P.-L., Laffont, C. M., & VandeVoort, C. A. (2011). Similarity of bisphenol A pharmacokinetics in rhesus monkeys and mice: Relevance for human exposure. Environmental Health Perspectives, 119(4), 422–430. https://doi.org/10.1289/ehp.1002514
75. Thoene, M., Dzika, E., Gonkowski, S., & Wojtkiewicz, J. (2020). Bisphenol S in food causes hormonal and obesogenic effects comparable to or worse than Bisphenol a: A literature review. Nutrients, 12(2), 532. https://doi.org/10.3390/nu12020532
76. Tonini, C., Segatto, M., Bertoli, S., Leone, A., Mazzoli, A., Cigliano, L., Barberio, L., Mandalà, M., & Pallottini, V. (2021). Prenatal exposure to BPA: The effects on hepatic lipid metabolism in male and female rat fetuses. Nutrients, 13(6), 1970. https://doi.org/10.3390/nu13061970
77. Trasino, S. E., & Gudas, L. J. (2015). Vitamin A: A missing link in diabetes? Diabetes Management, 5(5), 359–367. https://doi.org/10.2217/dmt.15.30
78. Veiga-Lopez, A., Pu, Y., Gingrich, J., & Padmanabhan, V. (2018). Obesogenic endocrine disrupting chemicals: Identifying knowledge gaps. Trends in Endocrinology & Metabolism, 29(9), 607–625. https://doi.org/10.1016/j.tem.2018.06.003
79. Wang, J., Sun, B., Hou, M., Pan, X., & Li, X. (2013). The environmental obesogen bisphenol A promotes adipogenesis by increasing the amount of 11β-hydroxysteroid dehydrogenase type 1 in the adipose tissue of children. International journal of obesity (2005), 37(7), 999–1005. https://doi.org/10.1038/ijo.2012.173
80. Wang, X., Ha, D., Yoshitake, R., Chan, Y. S., Sadava, D., & Chen, S. (2021). Exploring the biological activity and mechanism of xenoestrogens and phytoestrogens in cancers: Emerging methods and concepts. International Journal of Molecular Sciences, 22(16), 8798. https://doi.org/10.3390/ijms22168798
81. Zhang, J., Powell, C. A., Kay, M. K., Park, M. H., Meruvu, S., Sonkar, R., & Choudhury, M. (2020). A moderate physiological dose of benzyl butyl phthalate exacerbates the high fat diet-induced diabesity in male mice. Toxicology Research, 9(4), 353–370. https://doi.org/10.1093/toxres/tfaa037
82. Zhao, S., Kusminski, C. M., & Scherer, P. E. (2021). Adiponectin, leptin and cardiovascular disorders. Circulation Research, 128(1), 136–149. https://doi.org/10.1161/circresaha.120.314458
Published
2022-08-31
How to Cite
Guerrero-Meza, F., Vega-Morales, P., Rubio, V., Vergara-Castañeda, H., Sánchez-Tusie, A., Ahumada-Solórzano, M., Solis-Sáinz, J. C., & Hernández-Puga, G. (2022). Los Disruptores Endocrinos Como Obesógenos Ambientales: Efectos en Proteínas Adipogénicas Clave. European Scientific Journal, ESJ, 18(27), 77. https://doi.org/10.19044/esj.2022.v18n27p77
Section
ESJ Natural/Life/Medical Sciences