Hormonal Imprinting: The First Cellular-level Evidence of Epigenetic Inheritance and its Present State

Author(s): György Csaba*

Journal Name: Current Genomics

Volume 20 , Issue 6 , 2019


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Graphical Abstract:


Abstract:

Hormonal imprinting takes place perinatally at the first encounter between the developing hormone receptor and its target hormone. This process is needed for the normal function of the receptor- hormone pair and its effect is life-long. However, in this critical period, when the developmental window is open, related molecules (members of the same hormone family, synthetic hormones and hormone-like molecules, endocrine disruptors) also can be bound by the receptor, causing life-long faulty imprinting. In this case, the receptors’ binding capacity changes and alterations are caused at adult age in the sexual and behavioral sphere, in the brain and bones, inclination to diseases and manifestation of diseases, etc. Hereby, faulty hormonal imprinting is the basis of metabolic and immunological imprinting as well as the developmental origin of health and disease (DOHaD). Although the perinatal period is the most critical for faulty imprinting, there are other critical periods as weaning and adolescence, when the original imprinting can be modified or new imprintings develop. Hormonal imprinting is an epigenetic process, without changing the base sequence of DNA, it is inherited in the cell line of the imprinted cells and also transgenerationally (up to 1000 generations in unicellulars and up to the 3rd generation in mammals are justified). Considering the enormously growing number and amount of faulty imprinters (endocrine disruptors) and the hereditary character of faulty imprinting, this latter is threatening the whole human endocrine system.

Keywords: Hormonal imprinting, epigenetic inheritance, developmental window, endocrine disruptors, faulty imprinting, heredity.

[1]
Csaba, G.; Németh, G.; Vargha, P. Development and persistence of receptor ‘memory’ in a unicellular model system. Exp. Cell Biol., 1982, 50(5), 291-294.
[PMID: 6292015]
[2]
Csaba, G.; Németh, G.; Vargha, P. Attempt to disturb receptor memory in a unicellular (Tetrahymena) model system. Acta Physiol. Hung., 1983, 61(3), 131-136.
[PMID: 6316726]
[3]
Köhidai, L.; Csaba, G.; László, V. Persistence of receptor “memory” induced in Tetrahymena by insulin imprinting. Acta Microbiol. Hung., 1990, 37(3), 269-275.
[PMID: 2129253]
[4]
Adams, M.B. The politics of human heredity in the USSR, 1920-1940. Genome, 1989, 31(2), 879-884.
[http://dx.doi.org/10.1139/g89-155] [PMID: 2698846]
[5]
Gordin, M.D. How lysenkoism became pseudoscience: Dobzhansky to velikovsky. J. Hist. Biol., 2012, 45(3), 443-468.
[http://dx.doi.org/10.1007/s10739-011-9287-3] [PMID: 21698424]
[6]
Csaba, G. Phylogeny and ontogeny of hormone receptors: The selection theory of receptor formation and hormonal imprinting. Biol. Rev. Camb. Philos. Soc., 1980, 55(1), 47-63.
[http://dx.doi.org/10.1111/j.1469-185X.1980.tb00687.x] [PMID: 6244865]
[7]
Deftos, L.J.; LeRoith, D.; Shiloach, J.; Roth, J. Salmon calcitonin-like immunoactivity in extracts of Tetrahymena pyriformis. Horm. Metab. Res., 1985, 17(2), 82-85.
[http://dx.doi.org/10.1055/s-2007-1013457] [PMID: 3921450]
[8]
Le Roith, D.; Shiloach, J.; Berelowitz, M.; Frohman, L.A.; Liotta, A.S.; Krieger, D.T.; Roth, J. Are messenger molecules in microbes the ancestors of the vertebrate hormones and tissue factors? Fed. Proc., 1983, 42(9), 2602-2607.
[PMID: 6133783]
[9]
Christensen, S.T. Insulin rescues the unicellular eukaryote Tetrahymena from dying in a complete, synthetic nutrient medium. Cell Biol. Int., 1993, 17(9), 833-837.
[http://dx.doi.org/10.1006/cbir.1993.1145] [PMID: 8220309]
[10]
Feix, M.; Hoch, M. Phylogeny and evolution of hormone systems. Anasthesiol. Intensivmed. Notfallmed. Schmerzther., 2002, 37(11), 651-658.
[http://dx.doi.org/10.1055/s-2002-35121] [PMID: 12404141]
[11]
Shemarova, I.V.; Selivanova, G.V.; Vlasova, T.D. The influence of epidermal growth factor and insulin on proliferation and DNA synthesis in ciliates Tetrahymena pyriformis. Tsitologiia, 2002, 44(11), 1097-1103.
[PMID: 12561730]
[12]
Koch, A.S.; Fehér, G.; Lukovits, I. A simple model of dynamic receptor pattern generation. Biol. Cybern., 1979, 32(3), 125-138.
[http://dx.doi.org/10.1007/BF00337389] [PMID: 427229]
[13]
Koch, A.S.; Nienhaus, R.; Lautsch, M.; Lukovits, I. An advanced version of the dynamic receptor pattern generation model: The flux model. Biol. Cybern., 1981, 39(2), 105-109.
[http://dx.doi.org/10.1007/BF00336736] [PMID: 7236745]
[14]
Kovács, P.; Nozawa, Y.; Csaba, G. Induction of hormone receptor formation in the unicellular Tetrahymena. Biosci. Rep., 1989, 9(1), 87-92.
[http://dx.doi.org/10.1007/BF01117514] [PMID: 2541827]
[15]
Fülöp, A.K.; Csaba, G. Insulin pretreatment (imprinting) produces elevated capacity in the insulin binding of Tetrahymena. Different binding by the cilia of the body and oral field. Biosci. Rep., 1994, 14(6), 301-308.
[http://dx.doi.org/10.1007/BF01199054] [PMID: 7620081]
[16]
Csaba, G. Hormonal imprinting in the unicellular Tetrahymena: The proto-model of epigenetics. Acta Microbiol. Immunol. Hung., 2012, 59(3), 291-310.
[http://dx.doi.org/10.1556/AMicr.59.2012.3.1] [PMID: 22982634]
[17]
Kovács, P.; Sundermann, C.; Estridge, B.H.; Csaba, G. A confocal microscopic evaluation of the effects of insulin imprinting on the binding of Concanavalin A by Tetrahymena Pyriformis. Cell Biol. Int., 1995, 19(12), 973-978.
[http://dx.doi.org/10.1006/cbir.1995.1038] [PMID: 9721621]
[18]
Köhidai, L.; Schiess, N.; Csaba, G. Chemotactic selection of Tetrahymena pyriformis GL induced with histamine, di-iodotyrosine or insulin. Comp. Biochem. Physiol. C Toxicol. Pharmacol., 2000, 126(1), 1-9.
[PMID: 11048659]
[19]
Csaba, G.; Kovács, P. Impact of 5-azacytidine on insulin binding and insulin-induced receptor formation in tetrahymena. Biochem. Biophys. Res. Commun., 1990, 168(2), 709-713.
[http://dx.doi.org/10.1016/0006-291X(90)92379-E] [PMID: 1692214]
[20]
Christopher, G.K.; Sundermann, C.A. Intracellular insulin binding in Tetrahymena pyriformis. Tissue Cell, 1996, 28(4), 427-437.
[http://dx.doi.org/10.1016/S0040-8166(96)80028-0] [PMID: 8760857]
[21]
Leick, V.; Bøg-Hansen, T.C.; Juhl, H.A. Insulin/FGF-binding ciliary membrane glycoprotein from Tetrahymena. J. Membr. Biol., 2001, 181(1), 47-53.
[http://dx.doi.org/10.1007/s0023200100064] [PMID: 11331937]
[22]
Csaba, G.; Kovács, P. Insulin treatment (hormonal imprinting) increases the insulin production of the unicellular tetrahymena long term. Is there a simultaneous formation of hormone receptor and hormone? Cell Biol. Int., 1995, 19(12), 1011-1014.
[http://dx.doi.org/10.1006/cbir.1995.1043] [PMID: 9721626]
[23]
Csaba, G. Insulin at a unicellular eukaryote level. Cell Biol. Int., 2013, 37(4), 267-275.
[http://dx.doi.org/10.1002/cbin.10054] [PMID: 23456783]
[24]
Kőhidai, L.; Lajkó, E.; Pállinger, E.; Csaba, G. Verification of epigenetic inheritance in a unicellular model system: Multigenerational effects of hormonal imprinting. Cell Biol. Int., 2012, 36(10), 951-959.
[http://dx.doi.org/10.1042/CBI20110677] [PMID: 22770530]
[25]
Csaba, G.; Kovács, P. Insulin uptake, localization and production in previously insulin treated and untreated Tetrahymena. Data on the mechanism of hormonal imprinting. Cell Biochem. Funct., 2000, 18(3), 161-167.
[http://dx.doi.org/10.1002/1099-0844(200009)18:3<161:AID-CBF869>3.0.CO;2-R] [PMID: 10965353]
[26]
Csaba, G.; Kovács, P. Localization of beta-endorphin in tetrahymena by confocal microscopy. Induction of the prolonged production of the hormone by hormonal imprinting. Cell Biol. Int., 1999, 23(10), 695-702.
[http://dx.doi.org/10.1006/cbir.1999.0437] [PMID: 10736193]
[27]
Csaba, G.; Gaál, A.; Kovács, P.; Simon, G.; Köhidai, L. Prolonged elevation of insulin content in the unicellular tetrahymena after insulin treatment: Induction of insulin production or storage? Cell Biochem. Funct., 1999, 17(3), 165-173.
[http://dx.doi.org/10.1002/(SICI)1099-0844(199909)17:3<165:AID-CBF824>3.0.CO;2-W] [PMID: 10451537]
[28]
Fülöp, A.K.; Csaba, G. Accumulation of insulin-gold particles in the oral apparatus of Tetrahymena after insulin pretreatment (imprinting). Microbios, 1997, 90(363), 123-128.
[PMID: 9345790]
[29]
Kovács, P.; Lovas, G.; Csaba, G. Influence of insulin on the movement of Tetrahymena pyriformis. Hormonal imprinting alters the velocity. Comp. Biochem. Physiol. Part A. Physiol., 1994, 107(2), 375-379.
[http://dx.doi.org/10.1016/0300-9629(94)90395-6] [PMID: 7907964]
[30]
Csaba, G.; Kovács, P.; Noszál, B. Imprinting effects of three amino acids (alanine, lysine and glycine) and their oligopeptides in Tetrahymena pyriformis. Data from the hormone and hormone receptor evolution. Cell Biol. Int., 1996, 20(5), 339-342.
[http://dx.doi.org/10.1006/cbir.1996.0038] [PMID: 8688849]
[31]
Csaba, G.; Kovács, P. Studies into disturbing receptor ‘memory’ in a unicellular (Tetrahymena) model system: Changes in the imprinting potential on exposure to combinations of related and unrelated hormones. Exp. Cell Biol., 1986, 54(5-6), 333-337.
[PMID: 3026863]
[32]
Csaba, G.; Kovács, P.; Török, O.; Bohdaneczky, E.; Bajusz, S. Suitability of oligopeptides for induction of hormonal imprinting-implications on receptor and hormone evolution. Biosystems, 1986, 19(4), 285-288.
[http://dx.doi.org/10.1016/0303-2647(86)90005-5] [PMID: 3026508]
[33]
Kóhidai, L.; Thomka, M.; Csaba, G. Age of the cell culture: A factor influencing hormonal imprinting of Tetrahymena. Acta Microbiol. Hung., 1986, 33(4), 295-300.
[PMID: 2888256]
[34]
Csaba, G.; Németh, G.; Vargha, P. Influence of hormone treatment applied or begun in different phases of the cell cycle on hormonal imprinting in Tetrahymena. Acta Biol. Hung., 1985, 36(2), 141-145.
[PMID: 3019049]
[35]
Csaba, G.; Poteczin, E.; Fehér, T.; Kovács, P. Steroid hormone (hydrocortisone, oestradiol and testosterone) uptake, storage or induced synthesis in tetrahymena. Cell Biol. Int., 1998, 22(11-12), 875-878.
[http://dx.doi.org/10.1006/cbir.1998.0326] [PMID: 10873299]
[36]
Csaba, G.; Inczefi-Gonda, A.; Fehér, T. Induction of steroid binding sites (receptors) and presence of steroid hormones in the unicellular Tetrahymena pyriformis. Comp. Biochem. Physiol. A Comp. Physiol., 1985, 82(3), 567-570.
[http://dx.doi.org/10.1016/0300-9629(85)90434-7] [PMID: 2866877]
[37]
Shpakov, A.O.; Derkach, K.V.; Pertseva, M.N. Hormonal signal system of the lower eukaryotes. Tsitologiia, 2003, 45(3), 223-234.
[PMID: 14520878]
[38]
Christman, J.K. 5-Azacytidine and 5-aza-2′-deoxycytidine as inhibitors of DNA methylation: mechanistic studies and their implications for cancer therapy. Oncogene, 2002, 21(35), 5483-5495.
[http://dx.doi.org/10.1038/sj.onc.1205699] [PMID: 12154409]
[39]
Kouzmenko, A.; Ohtake, F.; Fujiki, R.; Kato, S. Hormonal gene regulation through DNA methylation and demethylation. Epigenomics, 2010, 2(6), 765-774.
[http://dx.doi.org/10.2217/epi.10.58] [PMID: 22122081]
[40]
Ništiar, F.; Rácz, O.; Brenišin, M. Can imprinting play a role in the response of Tetrahymena pyriformis to toxic substance exposure? Environ. Epigenet., 2016, 2(2)dvw010
[http://dx.doi.org/10.1093/eep/dvw010] [PMID: 29492290]
[41]
Csaba, G.; Hegyesi, H. Immunocytochemical verification of the insulin receptor’s specificity in the nuclear envelope of Tetrahymena. Comparison with receptors of the plasma membrane. Biosci. Rep., 1994, 14(1), 25-31.
[http://dx.doi.org/10.1007/BF01901635] [PMID: 8032006]
[42]
Petraglia, F.; Santuz, M.; Florio, P.; Simoncini, T.; Luisi, S.; Plaino, L.; Genazzani, A.R.; Genazzani, A.D.; Volpe, A. Paracrine regulation of human placenta: Control of hormonogenesis. J. Reprod. Immunol., 1998, 39(1-2), 221-233.
[http://dx.doi.org/10.1016/S0165-0378(98)00024-2] [PMID: 9786464]
[43]
de Escobar, G.M.; Obregón, M.J.; del Rey, F.E. Maternal thyroid hormones early in pregnancy and fetal brain development. Best Pract. Res. Clin. Endocrinol. Metab., 2004, 18(2), 225-248.
[http://dx.doi.org/10.1016/j.beem.2004.03.012] [PMID: 15157838]
[44]
Patel, J.; Landers, K.; Li, H.; Mortimer, R.H.; Richard, K. Thyroid hormones and fetal neurological development. J. Endocrinol., 2011, 209(1), 1-8.
[http://dx.doi.org/10.1530/JOE-10-0444] [PMID: 21212091]
[45]
Colicchia, M.; Campagnolo, L.; Baldini, E.; Ulisse, S.; Valensise, H.; Moretti, C. Molecular basis of thyrotropin and thyroid hormone action during implantation and early development. Hum. Reprod. Update, 2014, 20(6), 884-904.
[http://dx.doi.org/10.1093/humupd/dmu028] [PMID: 24943836]
[46]
Gnainsky, Y.; Dekel, N.; Granot, I. Implantation: Mutual activity of sex steroid hormones and the immune system guarantee the maternal-embryo interaction. Semin. Reprod. Med., 2014, 32(5), 337-345.
[http://dx.doi.org/10.1055/s-0034-1376353] [PMID: 24959815]
[47]
Csaba, G.; Nagy, S.U. Influence of the neonatal suppression of TSH production (neonatal hyperthyroidism) on response to TSH in adulthood. J. Endocrinol. Invest., 1985, 8(6), 557-559.
[http://dx.doi.org/10.1007/BF03348561] [PMID: 3833900]
[48]
Csaba, G.; Kovács, P.; Pállinger, E. Single treatment (hormonal imprinting) of newborn rats with serotonin increases the serotonin content of cells in adults. Cell Biol. Int., 2002, 26(8), 663-668.
[http://dx.doi.org/10.1006/cbir.2002.0916] [PMID: 12175669]
[49]
Csaba, G.; Kovács, P.; Pállinger, E. Effect of a single neonatal endorphin treatment on the hormone content of adult rat white blood cells and mast cells. Cell Biol. Int., 2003, 27(5), 423-427.
[http://dx.doi.org/10.1016/S1065-6995(03)00034-9] [PMID: 12758090]
[50]
Tekes, K.; Gyenge, M.; Sótonyi, P.; Csaba, G. Effect of neonatal nociceptin or nocistatin imprinting on the brain concentration of biogenic amines and their metabolites. Brain Dev., 2009, 31(4), 282-287.
[http://dx.doi.org/10.1016/j.braindev.2008.05.007] [PMID: 18597961]
[51]
Csaba, G.; Inczefi-Gonda, A. Effect of vitamin D(3) treatment in the neonatal or adolescent age (hormonal imprinting) on the thymic glucocorticoid receptor of the adult male rat. Horm. Res., 1999, 51(6), 280-283.
[PMID: 10640889]
[52]
Csaba, G.; Kovács, P.; Pállinger, E. Impact of neonatal imprinting with vitamin A or D on the hormone content of rat immune cells. Cell Biochem. Funct., 2007, 25(6), 717-721.
[http://dx.doi.org/10.1002/cbf.1381] [PMID: 17099924]
[53]
Gaál, A.; Csaba, G. Effect of retinoid (vitamin A or retinoic acid) treatment (hormonal imprinting) through breastmilk on the glucocorticoid receptor and estrogen receptor binding capacity of the adult rat offspring. Hum. Exp. Toxicol., 1998, 17(10), 560-563.
[http://dx.doi.org/10.1177/096032719801701006] [PMID: 9821019]
[54]
Csaba, G.; Gaál, A.; Inczefi-Gonda, A. The effect of perinatal hormonal imprinting with 13-cis-retinoic acid (isotretinoin) on the thymic glucocorticoid receptors of female and testosterone level of male adult rats. Horm. Metab. Res., 1999, 31(9), 505-507.
[http://dx.doi.org/10.1055/s-2007-978784] [PMID: 10569251]
[55]
Csaba, G.; Inczefi-Gonda, A. Effect of a single treatment (imprinting) with genistein or combined treatment with genistein+benzpyrene on the binding capacity of glucocorticoid and estrogen receptors of adult rats. Hum. Exp. Toxicol., 2002, 21(5), 231-234.
[http://dx.doi.org/10.1191/0960327102ht242oa] [PMID: 12141392]
[56]
Inczefi-Gonda, A. The environmental pollutant aromatic hydrocarbon, benzpyrene has deleterious effect on hormone receptor development. Acta Biol. Hung., 1999, 50(4), 355-361.
[PMID: 10735172]
[57]
Tekes, K.; Tóthfalusi, L.; Hantos, M.; Csaba, G. Effect of neonatal benzpyrene imprinting on the brain serotonin content and nocistatin level in adult male rats. Acta Physiol. Hung., 2007, 94(3), 183-189.
[http://dx.doi.org/10.1556/APhysiol.94.2007.3.3] [PMID: 17853770]
[58]
Mirzahosseini, S.; Karabélyos, C.; Dobozy, O.; Csaba, G. Changes in sexual behavior of adult male and female rats neonatally treated with vitamin D3. Hum. Exp. Toxicol., 1996, 15(7), 573-576.
[http://dx.doi.org/10.1177/096032719601500704] [PMID: 8818710]
[59]
Singh, J.; Handelsman, D.J. Imprinting by neonatal sex steroids on the structure and function of the mature mouse prostate. Biol. Reprod., 1999, 61(1), 200-208.
[http://dx.doi.org/10.1095/biolreprod61.1.200] [PMID: 10377050]
[60]
Dei, M.; Verni, A.; Bigozzi, L.; Bruni, V. Sex steroids and libido. Eur. J. Contracept. Reprod. Health Care, 1997, 2(4), 253-258.
[http://dx.doi.org/10.3109/13625189709165303] [PMID: 9678082]
[61]
Singh, J.; Handelsman, D.J. Morphometric studies of neonatal estrogen imprinting in the mature mouse prostate. J. Endocrinol., 1999, 162(1), 39-48.
[http://dx.doi.org/10.1677/joe.0.1620039] [PMID: 10396019]
[62]
Csaba, G. The present and future of human sexuality: Impact of faulty perinatal hormonal imprinting. Sex. Med. Rev., 2017, 5(2), 163-169.
[http://dx.doi.org/10.1016/j.sxmr.2016.10.002] [PMID: 27989781]
[63]
Sifakis, S.; Androutsopoulos, V.P.; Tsatsakis, A.M.; Spandidos, D.A. Human exposure to endocrine disrupting chemicals: Effects on the male and female reproductive systems. Environ. Toxicol. Pharmacol., 2017, 51, 56-70.
[http://dx.doi.org/10.1016/j.etap.2017.02.024] [PMID: 28292651]
[64]
Fenichel, P.; Chevalier, N.; Brucker-Davis, F.; Bisphenol, A. An endocrine and metabolic disruptor. Ann. Endocrinol. (Paris), 2013, 74(3), 211-220.
[http://dx.doi.org/10.1016/j.ando.2013.04.002] [PMID: 23796010]
[65]
Lymperi, S.; Giwercman, A. Endocrine disruptors and testicular function. Metabolism, 2018, 86, 79-90.
[http://dx.doi.org/10.1016/j.metabol.2018.03.022] [PMID: 29605435]
[66]
Annamalai, J.; Namasivayam, V. Endocrine disrupting chemicals in the atmosphere: Their effects on humans and wildlife. Environ. Int., 2015, 76, 78-97.
[http://dx.doi.org/10.1016/j.envint.2014.12.006] [PMID: 25569353]
[67]
Mouritsen, A.; Aksglaede, L.; Sørensen, K.; Mogensen, S.S.; Leffers, H.; Main, K.M.; Frederiksen, H.; Andersson, A.M.; Skakkebaek, N.E.; Juul, A. Hypothesis: Exposure to endocrine-disrupting chemicals may interfere with timing of puberty. Int. J. Androl., 2010, 33(2), 346-359.
[http://dx.doi.org/10.1111/j.1365-2605.2010.01051.x] [PMID: 20487042]
[68]
Schneider, J.E.; Brozek, J.M.; Keen-Rhinehart, E. Our stolen figures: The interface of sexual differentiation, endocrine disruptors, maternal programming, and energy balance. Horm. Behav., 2014, 66(1), 104-119.
[http://dx.doi.org/10.1016/j.yhbeh.2014.03.011] [PMID: 24681201]
[69]
Schoeters, G.; Den Hond, E.; Dhooge, W.; van Larebeke, N.; Leijs, M. Endocrine disruptors and abnormalities of pubertal development. Basic Clin. Pharmacol. Toxicol., 2008, 102(2), 168-175.
[http://dx.doi.org/10.1111/j.1742-7843.2007.00180.x] [PMID: 18226071]
[70]
Massart, F.; Parrino, R.; Seppia, P.; Federico, G.; Saggese, G. How do environmental estrogen disruptors induce precocious puberty? Minerva Pediatr., 2006, 58(3), 247-254.
[PMID: 16832329]
[71]
Leonardi, A.; Cofini, M.; Rigante, D.; Lucchetti, L.; Cipolla, C.; Penta, L.; Esposito, S. The effect of bisphenol A on puberty: A critical review of the medical literature. Int. J. Environ. Res. Public Health, 2017, 14(9)E1044
[http://dx.doi.org/10.3390/ijerph14091044] [PMID: 28891963]
[72]
Parent, A.S.; Franssen, D.; Fudvoye, J.; Pinson, A.; Bourguignon, J.P. Current changes in pubertal timing: Revised vision in relation with environmental factors including endocrine disruptors. Endocr. Dev., 2016, 29, 174-184.
[http://dx.doi.org/10.1159/000438885] [PMID: 26680578]
[73]
Den Hond, E.; Schoeters, G. Endocrine disrupters and human puberty. Int. J. Androl., 2006, 29(1), 264-271.
[http://dx.doi.org/10.1111/j.1365-2605.2005.00561.x] [PMID: 16466548]
[74]
Kubo, K.; Arai, O.; Omura, M.; Watanabe, R.; Ogata, R.; Aou, S. Low dose effects of bisphenol A on sexual differentiation of the brain and behavior in rats. Neurosci. Res., 2003, 45(3), 345-356.
[http://dx.doi.org/10.1016/S0168-0102(02)00251-1] [PMID: 12631470]
[75]
Rubin, B.S.; Paranjpe, M.; DaFonte, T.; Schaeberle, C.; Soto, A.M.; Obin, M.; Greenberg, A.S. Perinatal BPA exposure alters body weight and composition in a dose specific and sex specific manner: The addition of peripubertal exposure exacerbates adverse effects in female mice. Reprod. Toxicol., 2017, 68, 130-144.
[http://dx.doi.org/10.1016/j.reprotox.2016.07.020] [PMID: 27496714]
[76]
Chen, F.; Zhou, L.; Bai, Y.; Zhou, R.; Chen, L. Sex differences in the adult HPA axis and affective behaviors are altered by perinatal exposure to a low dose of bisphenol A. Brain Res., 2014, 1571, 12-24.
[http://dx.doi.org/10.1016/j.brainres.2014.05.010] [PMID: 24857958]
[77]
Nakamura, K.; Itoh, K. Dai, 45, 91-99.H., Han, L.; Wang, X.; Kato, S.; Sugimoto, T.; Fushiki, S. Prenatal and lactational exposure to low doses of bisphenol A alters adult mice behavior. Brain Dev., 2012, 34, 57-63.
[http://dx.doi.org/10.1016/j.braindev.2010.12.011] [PMID: 21277127]
[78]
Wolstenholme, J.T.; Taylor, J.A.; Shetty, S.R.J; Edwards, M.; Connelly, J.J.; Rissman, E.F. Gestational exposure to low dose bisphenol A alters social behavior in juvenile mice. PLoS One, 2011, 6(9) e 25448.
[79]
Evans, S.F.; Kobrosly, R.W.; Barrett, E.S.; Thurston, S.W.; Calafat, A.M.; Weiss, B.; Stahlhut, R.; Yolton, K.; Swan, S.H. Prenatal bisphenol A exposure and maternally reported behavior in boys and girls. Neurotoxicology, 2014, 45, 91-99.
[http://dx.doi.org/10.1016/j.neuro.2014.10.003] [PMID: 25307304]
[80]
Csaba, G.; Tekes, K. Is the brain hormonally imprintable? Brain Dev., 2005, 27(7), 465-471.
[http://dx.doi.org/10.1016/j.braindev.2004.12.008] [PMID: 16198202]
[81]
Hashemi, F.; Tekes, K.; Laufer, R.; Szegi, P.; Tóthfalusi, L.; Csaba, G. Effect of a single neonatal oxytocin treatment (hormonal imprinting) on the biogenic amine level of the adult rat brain: Could oxytocin-induced labor cause pervasive developmental diseases? Reprod. Sci., 2013, 20(10), 1255-1263.
[http://dx.doi.org/10.1177/1933719113483010] [PMID: 23548412]
[82]
Bigsby, R.; Chapin, R.E.; Daston, G.P.; Davis, B.J.; Gorski, J.; Gray, L.E.; Howdeshell, K.L.; Zoeller, R.T.; vom Saal, F.S. Evaluating the effects of endocrine disruptors on endocrine function during development. Environ. Health Perspect., 1999, 107(Suppl. 4), 613-618.
[PMID: 10421771]
[83]
Tekes, K.; Gyenge, M.; Hantos, M.; Csaba, G. Transgenerational hormonal imprinting caused by vitamin A and vitamin D treatment of newborn rats. Alterations in the biogenic amine contents of the adult brain. Brain Dev., 2009, 31(9), 666-670.
[http://dx.doi.org/10.1016/j.braindev.2008.10.007] [PMID: 19091501]
[84]
Stein, T.P.; Schluter, M.D.; Steer, R.A.; Guo, L.; Ming, X. Bisphenol A exposure in children with autism spectrum disorder. Autism Res., 2015, 8(3), 272-283.
[http://dx.doi.org/10.1002/aur.1444] [PMID: 25641946]
[85]
Pinson, A.; Bourguignon, J.P.; Parent, A.S. Exposure to endocrine disrupting chemicals and neurodevelopmental alterations. Andrology, 2016, 4(4), 706-722.
[http://dx.doi.org/10.1111/andr.12211] [PMID: 27285165]
[86]
Perera, F.; Nolte, E.L.R.; Wang, Y.; Margolis, A.E.; Calafat, A.M.; Wang, S.; Garcia, W.; Hoepner, L.A.; Peterson, B.S.; Rauh, V.; Herbstman, J. Bisphenol A exposure and symptoms of anxiety and depression among inner city children at 10-12 years of age. Environ. Res., 2016, 151, 195-202.
[http://dx.doi.org/10.1016/j.envres.2016.07.028] [PMID: 27497082]
[87]
Braun, J.M. Early-life exposure to EDCs: Role in childhood obesity and neurodevelopment. Nat. Rev. Endocrinol., 2017, 13(3), 161-173.
[http://dx.doi.org/10.1038/nrendo.2016.186] [PMID: 27857130]
[88]
Mari-Bauset, S.; Donat-Vargas, C.; Llópis-Gonzalez, A.; Mari-Sanchis, A.; Peraita-Costa, I.; Llopis-Morales, J.; Morales-Suarez-Varela, M. Endocrine disruptors and autism spectrum disorder in pregnancy: A review and evaluation of the quality of the epidemiological evidence. Children (Basel), 5(12)E157
[http://dx.doi.org/10.3390/children5120157]
[89]
Csaba, G. The faulty perinatal hormonal imprinting as functional teratogen. Curr. Pediatr. Rev., 2016, 12(3), 222-229.
[http://dx.doi.org/10.2174/1573396312666160709031510] [PMID: 27396910]
[90]
Csaba, G. Immunoendocrinology: faulty hormonal imprinting in the immune system. Acta Microbiol. Immunol. Hung., 2014, 61(2), 89-106.
[http://dx.doi.org/10.1556/AMicr.61.2014.2.1] [PMID: 24939679]
[91]
Lemke, H.; Tanasa, R.I.; Trad, A.; Lange, H. Benefits and burden of the maternally-mediated immunological imprinting. Autoimmun. Rev., 2009, 8(5), 394-399.
[http://dx.doi.org/10.1016/j.autrev.2008.12.005] [PMID: 19135180]
[92]
Rogers, J.A.; Metz, L.; Yong, V.W. Review: Endocrine disrupting chemicals and immune responses: A focus on bisphenol-A and its potential mechanisms. Mol. Immunol., 2013, 53(4), 421-430.
[http://dx.doi.org/10.1016/j.molimm.2012.09.013] [PMID: 23123408]
[93]
Csaba, G.; Pállinger, E. In vitro effect of hormones on the hormone content of rat peritoneal and thymic cells. Is there an endocrine network inside the immune system? Inflamm. Res., 2007, 56(11), 447-451.
[http://dx.doi.org/10.1007/s00011-007-7021-6] [PMID: 18224286]
[94]
Csaba, G. Hormones in the immune system and their possible role. A critical review. Acta Microbiol. Immunol. Hung., 2014, 61(3), 241-260.
[http://dx.doi.org/10.1556/AMicr.61.2014.3.1] [PMID: 25261940]
[95]
Csaba, G. The immunoendocrine thymus as a pacemaker of lifespan. Acta Microbiol. Immunol. Hung., 2016, 63(2), 139-158.
[http://dx.doi.org/10.1556/030.63.2016.2.1] [PMID: 27352969]
[96]
Karabélyos, C.; Horváth, C.; Holló, I.; Csaba, G. Effect of neonatal glucocorticoid treatment on bone mineralization of adult nontreated, dexamethasone-treated or vitamin D3-treated rats. Gen. Pharmacol., 1998, 31(5), 789-791.
[http://dx.doi.org/10.1016/S0306-3623(98)00093-7] [PMID: 9809479]
[97]
Csaba, G. Bone manifestation of faulty perinatal hormonal imprinting: A review. Curr. Pediatr. Rev., 2018, 25.
[http://dx.doi.org/10.2174/15733963] [PMID: 30474530]
[98]
Karabélyos, C.; Horváth, C.; Holló, I.; Csaba, G. Effect of single neonatal vitamin D3 treatment (hormonal imprinting) on the bone mineralization of adult non-treated and dexamethasone treated rats. Hum. Exp. Toxicol., 1998, 17(8), 424-429.
[http://dx.doi.org/10.1177/096032719801700803] [PMID: 9756134]
[99]
Karabélyos, C.; Horváth, C.; Holló, I.; Csaba, G. Effect of perinatal synthetic steroid hormone (allylestrenol, diethylstilbestrol) treatment (hormonal imprinting) on the bone mineralization of the adult male and female rat. Life Sci., 1999, 64(9), PL105-PL110.
[http://dx.doi.org/10.1016/S0024-3205(98)00624-9] [PMID: 10075115]
[100]
Csaba, G.; Kovács, P.; Pállinger, E. Effect of endorphin exposure at weaning on the endorphin and serotonin content of white blood cells and mast cells in adult rat. Cell Biochem. Funct., 2004, 22(3), 197-200.
[http://dx.doi.org/10.1002/cbf.1089] [PMID: 15124185]
[101]
Csaba, G.; Knippel, B.; Karabélyos, C.; Inczefi-Gonda, A.; Hantos, M.; Tekes, K. Endorphin excess at weaning durably influences sexual activity, uterine estrogen receptor’s binding capacity and brain serotonin level of female rats. Horm. Metab. Res., 2004, 36(1), 39-43.
[http://dx.doi.org/10.1055/s-2004-814101] [PMID: 14983405]
[102]
Csaba, G.; Inczefi-Gonda, A. Molecules acting on receptor level at weaning, durably influence liver glucocorticoid receptors. Acta Physiol. Hung., 2005, 92(1), 33-38.
[http://dx.doi.org/10.1556/APhysiol.92.2005.1.5] [PMID: 16003943]
[103]
Csaba, G.; Pállinger, E. Prolonged impact of pubertal serotonin treatment (hormonal imprinting) on the later serotonin content of white blood cells. Life Sci., 2002, 71(8), 879-885.
[http://dx.doi.org/10.1016/S0024-3205(02)01776-9] [PMID: 12084385]
[104]
Gattinoni, L.; Speiser, D.E.; Lichterfeld, M.; Bonini, C. T memory stem cells in health and disease. Nat. Med., 2017, 23(1), 18-27.
[http://dx.doi.org/10.1038/nm.4241] [PMID: 28060797]
[105]
Pállinger, É.; Kiss, G.A.; Csaba, G. Hormone (ACTH, T3) content of immunophenotyped lymphocyte subpopulations. Acta Microbiol. Immunol. Hung., 2016, 63(4), 373-385.
[http://dx.doi.org/10.1556/030.63.2016.016] [PMID: 28166641]
[106]
Thompson, R.F.; Einstein, F.H. Epigenetic basis for fetal origins of age-related disease. J. Womens Health (Larchmt.), 2010, 19(3), 581-587.
[http://dx.doi.org/10.1089/jwh.2009.1408] [PMID: 20136551]
[107]
Martin, J.T. Sexual dimorphism in immune function: The role of prenatal exposure to androgens and estrogens. Eur. J. Pharmacol., 2000, 405(1-3), 251-261.
[http://dx.doi.org/10.1016/S0014-2999(00)00557-4] [PMID: 11033332]
[108]
Capra, L.; Tezza, G.; Mazzei, F.; Boner, A.L. The origins of health and disease: The influence of maternal diseases and lifestyle during gestation. Ital. J. Pediatr., 2013, 23, 397.
[http://dx.doi.org/10.1186/1824-7288-39-7]
[109]
Bolhuis, J.J. The development of animal behavior: From Lorenz to neural nets. Naturwissenschaften, 1999, 86(3), 101-111.
[http://dx.doi.org/10.1007/s001140050582] [PMID: 10189629]
[110]
McLachlan, J.A. Environmental signaling: From environmental estrogens to endocrine-disrupting chemicals and beyond. Andrology, 2016, 4(4), 684-694.
[http://dx.doi.org/10.1111/andr.12206] [PMID: 27230799]
[111]
Crews, D. Epigenetic modifications of brain and behavior: Theory and practice. Horm. Behav., 2011, 59(3), 393-398.
[http://dx.doi.org/10.1016/j.yhbeh.2010.07.001] [PMID: 20633562]
[112]
Titus-Ernstoff, L.; Troisi, R.; Hatch, E.E.; Wise, L.A.; Palmer, J.; Hyer, M.; Kaufman, R.; Adam, E.; Strohsnitter, W.; Noller, K.; Herbst, A.L.; Gibson-Chambers, J.; Hartge, P.; Hoover, R.N. Menstrual and reproductive characteristics of women whose mothers were exposed in utero to diethylstilbestrol (DES). Int. J. Epidemiol., 2006, 35(4), 862-868.
[http://dx.doi.org/10.1093/ije/dyl106] [PMID: 16723367]
[113]
Gapp, K.; Corcoba, A.; van Steenwyk, G.; Mansuy, I.M.; Duarte, J.M. Brain metabolic alterations in mice subjected to postnatal traumatic stress and in their offspring. J. Cereb. Blood Flow Metab., 2017, 37(7), 2423-2432.
[http://dx.doi.org/10.1177/0271678X16667525] [PMID: 27604311]
[114]
Crews, D.; Gillette, R.; Miller-Crews, I.; Gore, A.C.; Skinner, M.K. Nature, nurture and epigenetics. Mol. Cell. Endocrinol., 2014, 398(1-2), 42-52.
[http://dx.doi.org/10.1016/j.mce.2014.07.013] [PMID: 25102229]
[115]
Crews, D.; McLachlan, J.A. Epigenetics, evolution, endocrine disruption, health, and disease. Endocrinology, 2006, 147(Suppl. 6), S4-S10.
[http://dx.doi.org/10.1210/en.2005-1122] [PMID: 16690812]
[116]
Morrison, K.E.; Rodgers, A.B.; Morgan, C.P.; Bale, T.L. Epigenetic mechanisms in pubertal brain maturation. Neuroscience, 2014, 264, 17-24.
[http://dx.doi.org/10.1016/j.neuroscience.2013.11.014] [PMID: 24239720]
[117]
Pfinder, M.; Liebig, S.; Feldmann, R. Adolescents’ use of alcohol, tobacco and illicit drugs in relation to prenatal alcohol exposure: Modifications by gender and ethnicity. Alcohol Alcohol., 2014, 49(2), 143-153.
[http://dx.doi.org/10.1093/alcalc/agt166] [PMID: 24217955]
[118]
Slotkin, T.A.; Card, J.; Seidler, F.J. Nicotine administration in adolescence reprograms the subsequent response to nicotine treatment and withdrawal in adulthood: Sex-selective effects on cerebrocortical serotonergic function. Brain Res. Bull., 2014, 102, 1-8.
[http://dx.doi.org/10.1016/j.brainresbull.2014.01.004] [PMID: 24487013]
[119]
Viveros, M.P.; Llorente, R.; Moreno, E.; Marco, E.M. Behavioural and neuroendocrine effects of cannabinoids in critical developmental periods. Behav. Pharmacol., 2005, 16(5-6), 353-362.
[http://dx.doi.org/10.1097/00008877-200509000-00007] [PMID: 16148439]
[120]
Campolongo, P.; Trezza, V.; Ratano, P.; Palmery, M.; Cuomo, V. Developmental consequences of perinatal cannabis exposure: Behavioral and neuroendocrine effects in adult rodents. Psychopharmacology (Berl.), 2011, 214(1), 5-15.
[http://dx.doi.org/10.1007/s00213-010-1892-x] [PMID: 20556598]
[121]
Barthelemy, O.J.; Richardson, M.A.; Cabral, H.J.; Frank, D.A. Prenatal, perinatal, and adolescent exposure to marijuana: Relationships with aggressive behavior. Neurotoxicol. Teratol., 2016, 58, 60-77.
[http://dx.doi.org/10.1016/j.ntt.2016.06.009] [PMID: 27345271]
[122]
Sheridan, P.J.; Buchanan, J.M. The effects of opiates on androgen binding in the forebrain of the rat. Int. J. Fertil., 1980, 25(1), 36-43.
[PMID: 6104640]
[123]
Spano, M.S.; Fadda, P.; Fratta, W.; Fattore, L. Cannabinoid-opioid interactions in drug discrimination and self-administration: Effect of maternal, postnatal, adolescent and adult exposure to the drugs. Curr. Drug Targets, 2010, 11(4), 450-461.
[http://dx.doi.org/10.2174/138945010790980295] [PMID: 20017729]
[124]
Navarro, M.; Rubio, P.; de Fonseca, F.R. Behavioural consequences of maternal exposure to natural cannabinoids in rats. Psychopharmacology (Berl.), 1995, 122(1), 1-14.
[http://dx.doi.org/10.1007/BF02246436] [PMID: 8711059]
[125]
Fernández-Ruiz, J.; Gómez, M.; Hernández, M.; de Miguel, R.; Ramos, J.A. Cannabinoids and gene expression during brain development. Neurotox. Res., 2004, 6(5), 389-401.
[http://dx.doi.org/10.1007/BF03033314] [PMID: 15545023]
[126]
Trezza, V.; Cuomo, V.; Vanderschuren, L.J. Cannabis and the developing brain: Insights from behavior. Eur. J. Pharmacol., 2008, 585(2-3), 441-452.
[http://dx.doi.org/10.1016/j.ejphar.2008.01.058] [PMID: 18413273]
[127]
Scheyer, A. Prenatal exposure to cannabis affects the developing brain. Scientist, 2019.
[128]
Kubota, T. Epigenetic effect on environmental factors on neurodevelopmental disorders. Nippon Eiseigaku Zasshi, 2016, 71(3), 200-207.
[http://dx.doi.org/10.1265/jjh.71.200] [PMID: 27725423]
[129]
Mileva, G.; Baker, S.L.; Konkle, A.T.; Bielajew, C. Bisphenol-A: Epigenetic reprogramming and effects on reproduction and behavior. Int. J. Environ. Res. Public Health, 2014, 11(7), 7537-7561.
[http://dx.doi.org/10.3390/ijerph110707537] [PMID: 25054232]
[130]
Dyer, J.S.; Rosenfeld, C.R. Metabolic imprinting by prenatal, perinatal, and postnatal overnutrition: A review. Semin. Reprod. Med., 2011, 29(3), 266-276.
[http://dx.doi.org/10.1055/s-0031-1275521] [PMID: 21769766]
[131]
Vieau, D.; Laborie, C.; Eberlé, D.; Lesage, J.; Breton, C. Maternal nutritional manipulations: Is the adipose tissue a key target of programming? Med. Sci. (Paris), 2016, 32(1), 81-84.
[http://dx.doi.org/10.1051/medsci/20163201013] [PMID: 26850611]
[132]
Mikolajewska, K.; Stragierowitz, J.; Gromadzinska, J.; Bisphenol, A. Application, sources of exposure and potential risks in infants and pregnant women. In J Occup Med. Environ. Health, 2015, 28, 209-241.
[PMID: 26182919]
[133]
Konieczna, A.; Rutkowska, A.; Rachoń, D. Health risk of exposure to Bisphenol A (BPA). Rocz. Panstw. Zakl. Hig., 2015, 66(1), 5-11.
[PMID: 25813067]
[134]
Sullivan, E.L.; Grove, K.L. Metabolic imprinting in obesity. Forum Nutr., 2010, 63, 186-194.
[http://dx.doi.org/10.1159/000264406] [PMID: 19955786]
[135]
Barlow, D.P.; Bartolomei, M.S. Genomic imprinting in mammals. Cold Spring Harb. Perspect. Biol., 2014, 6(2), 6.
[http://dx.doi.org/10.1101/cshperspect.a018382] [PMID: 24492710]
[136]
Reddehase, M.J. Adverse immunological imprinting by cytomegalovirus sensitizing for allergic airway disease. Med. Microbiol. Immunol. (Berl.), 2019, 208(3-4), 469-473.
[http://dx.doi.org/10.1007/s00430-019-00610-z] [PMID: 31076879]
[137]
Jirtle, R.L.; Sander, M.; Barrett, J.C. Genomic imprinting and environmental disease susceptibility, 2000, 108, 271-278.
[http://dx.doi.org/10.1289/ehp.00108271]
[138]
Suzuki, K. The developing world of DOHaD. J. Dev. Orig. Health Dis., 2018, 9(3), 266-269.
[http://dx.doi.org/10.1017/S2040174417000691] [PMID: 28870276]
[139]
Csaba, G. Transgenerational effects of perinatal hormonal imprinting.Transgenerational epigenetics; Tollefsbol, T., Ed.; Elsevier, 2014, pp. 255-267.
[http://dx.doi.org/10.1016/B978-0-12-405944-3.00019-2]
[140]
Csaba, G. The biological basis and clinical significance of hormonal imprinting, an epigenetic process. Clin. Epigenetics, 2011, 2(2), 187-196.
[http://dx.doi.org/10.1007/s13148-011-0024-8] [PMID: 22704336]


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VOLUME: 20
ISSUE: 6
Year: 2019
Published on: 02 January, 2020
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DOI: 10.2174/1389202920666191116113524
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