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  • 1 Semmelweis University, Hungary
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Endocrine disruptors (EDs) are bound by steroid receptors, have steroid-like effects, and by this, negatively influence hormone-regulated processes. Phytoestrogens, which are consumed in enormously high amount by man, are also EDs; however, in contrast to industrial or communal EDs, in some cases have beneficial effects. As immune cells have steroid (first of all, estrogen) nuclear and plasma membrane receptors, which bind phytostrogens (genistein, daidzein, etc.), the development, lifespan, and function of them are deeply influenced by phytoestrogens. They can provoke perinatal faulty hormonal imprinting with lifelong consequences. However, faulty imprinting can be developed not only perinatally but also in other critical periods of life, as weaning, adolescence, and even in continuously dividing cells (e.g., hemopoietic cells) during the whole life. This means that the phytoestrogens could cause direct – instant or long-lasting – steroid effects and durable imprinting effects. As the effect of hormonal imprinting is epigenetically inherited, the phytoestrogen’s effects appear in the progeny generations, and the generationally repeated disruptor effects will be different from the present ones. This could also be manifested in the amount, type, and appearance of autoimmune diseases. The consumption of soy is enormously growing, and its immune effect is extended. As the immune system influences basic physiological processes, it seems likely that evolutionary alterations will be observed. In this case, some phytoestrogens will be needed for the normal life of man, as it happened in the case of vitamins A and D, which are already life-important exohormones. However, quantitatively or qualitatively enormous amount of phytoestrogens will cause pathological and epigenetically inherited alterations.

  • 1.

    Moutsatsou, P.: The spectrum of phytoestrogens in nature: Our knowledge is expanding. Hormones 6, 173193 (2007).

  • 2.

    Mueller, S. O., Simon, S., Chae, K., Metzler, M., Korach, K. S.: Phytoestrogens and their human metabolites show agonistic and antagonistic properties on estrogen receptor α (ERα) and ERβ in human cells. Toxicol Sci 80, 1425 (2004).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3.

    Casanova, M., You, L., Gaido, K. W., Archibeque-Engle, S., Janszen, D. B., Heck, H. A.: Developmental effects of dietary phytoestrogens in Sprague-Dawley rats and interactions of genistein and daidzein with rat estrogen receptors alpha and beta in vitro. Toxicol Sci 51, 236244 (1999).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4.

    Patisaul, H. B., Adewale, H. B.: Long-term effects of environmental endocrine disruptors on reproductive physiology and behavior. Front Behav Neurosci 3, 129 (2009).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5.

    Tran, L., Hammuda, M., Wood, C., Xiao, C. W.: Soy extracts suppressed iodine uptake and stimulated the production of autoimmunogen in rat thyrocytes. Exp Biol Med 238, 623630 (2013).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6.

    Hwang, K. A., Choi, K. C.: Anticancerogenic effects of dietary phytoestrogens and their chemopreventive mechanism. Nutr Cancer 67, 796783 (2015).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7.

    Trimel, S.: Estrogen emerges as most ancient of all hormones. Columbia Univ Rec 26, 14 (2001).

  • 8.

    Thornton, J. W.: Evolution of vertebrate steroid receptors from an ancestral estrogen receptor by ligand exploitation and serial genome expansions. Proc Natl Acad Sci U S A 98, 56715676 (2001).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9.

    Fox, J. E.: Chemical communication threatened by endocrine disrupting chemicals. Environ Health Perspect 112, 648653 (2004).

  • 10.

    Eick, G. N., Thornton, J. W.: Evolution of steroid receptors from an estrogen-sensitive ancestral receptor. Mol Cell Endocrinol 334, 3138 (2011).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11.

    Kovats, S.: Estrogen receptors regulate innate immune cells and signaling pathways. Cell Immunol 294, 6369 (2015).

  • 12.

    Schneider, A. E., Kárpáti, E., Schuszter, K., Tóth, E. A., Kiss, E., Kulcsár, M., László, G., Matko, J.: A dynamic network of estrogen receptors in murine lymphocytes: Fine-tuning the immune response. J Leukoc Biol 96, 857872 (2014).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13.

    Seiki, K., Sakabe, K.: Sex hormones and the thymus in relation to thymocyte proliferation and maturation. Arch Histol Cytol 60, 2938 (1997).

  • 14.

    Erlandsson, M. C., Ohlsson, C., Gustafsson, J. A., Carlsten, H.: Role of oestrogen receptors α and β in immune organ development and in oestrogen-mediated effects on thymus. Immunology 103, 1725 (2001).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15.

    Morito, K., Hirose, T., Kinjo, J., Hirakawa, T., Okawa, M., Nohara, T., Ogawa, S., Inoue, S., Muramatsu, M., Masamune, Y.: Interaction of phytoestrogens with estrogen receptors α and β. Biol Pharm Bull 24, 351356 (2001).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16.

    Sakai, T., Kogiso, M.: Soy isoflavones and immunity. J Med Invest 55, 167173 (2008).

  • 17.

    Kuo, C.-H., Yang, S.-N., Kuo, P.-L., Hung, C.-H.: Immunomodulatory effects of environmental endocrine disrupting chemicals. Kaohsiung J Med Sci 28, 537542 (2012).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18.

    Chalubisnski, M., Kowalski, M. L.: Endocrine disrupters – Potential modulators of the immune system and allergic response. Allergy 61, 13261335 (2006).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19.

    Masilamani, M., Wei, J., Sampson, H. A.: Regulation of the immune response by soybean isoflavones. Immunol Res 54, 95110 (2012).

  • 20.

    Yellayi, S., Naaz, A., Szewczikowski, M. A., Sato, T., Woods, J. A., Chang, J., Segre, M., Allred, C. D., Helferich, W. G., Cooke, P. S.: The phytoestrogen genistein induces thymic and immune changes: A human health concern? Proc Natl Acad Sci U S A 99, 76167621 (2002).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21.

    Cooke, P. S., Selvaraj, V., Yellayi, S.: Genistein, estrogen receptors, and the acquired immune system. J Nutr 136, 704708 (2006).

  • 22.

    Guo, T. L., White, K. L., Jr., Brown, R. D., Delclos, K. B., Newbold, R. R., Weis, C., Germolec, D. R., McCay, J. A.: Genistein modulates splenic natural killer cell activity, antibody-forming cell response, and phenotypic marker expression in F(0) and F (1) generation of Sprague-Dawley rats. Toxicol Appl Pharmacol 181, 219227 (2002).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23.

    Yellayi, S., Zakroczymski, M. A., Selvaraj, V., Valli, V. E., Ghanta, V., Helferich, W. G., Cooke, P. S.: The phytoestrogen genistein suppresses cell-mediated immunity in mice. J Endocrinol 176, 267274 (2003).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24.

    Ganai, A. A., Farooqi, H.: Bioactivity of genistein: A review of in vitro and in vivo studies. Biomed Pharmacother 76, 3038 (2015).

  • 25.

    Polkowski, K., Mazurek, A. P.: Biological properties of genistein. A review of in vitro and in vivo data. Acta Pol Pharm 57, 135155 (2000).

    • Search Google Scholar
    • Export Citation
  • 26.

    Klein, S. L., Wisniewski, A. B., Marson, A. L., Glass, G. E., Gearhart, J. P.: Early exposure exerts long-lasting effects on the endocrine and immune system in rats. Mol Med 8, 742749 (2002).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27.

    Ebaid, H. M., Elgawish, R. A., Abdelrazek, H. M., Gaffer, G., Tag, H. M.: Prenatal exposure to soy isoflavones altered the immunological parameters in female rat. Int J Toxicol 35, 274283 (2016).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28.

    Zoppi, G., Gasparini, R., Montovanelli, F., Crovari, P.: Diet and antibody response to vaccination in healthy infants. Lancet 322, 1114 (1983).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29.

    Selvajar, V., Bunick, D., Finnigan-Bunick, C., Johnson, R. W., Wang, H., Liu, L., Cooke, P. S.: Gene expression profiling of 17β-estradiol and genistein effects on mouse thymus. Toxicol Sci 87, 97112 (2005).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30.

    Zhang, R., Li, Y., Wang, W.: Enhancement of immune function in mice fed high doses of soy daidzein. Nutr Cancer 29, 2428 (1997).

  • 31.

    Han, D., Denison, M. S., Tachibana, H., Yamada, K.: Effects of estrogenic compounds on immunoglobulin production by mouse splenocytes. Biol Pharm Bull 25, 12631267 (2002).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 32.

    Shalaby, A., Elgawish, R. A. R.: Influence of dietary soy phytoestrogens on cytokine production and immunoglobulin in ovariectomized rats. J Adv Chem Eng Biol Sci 2, 9196 (2015).

    • Search Google Scholar
    • Export Citation
  • 33.

    Curran, E. M., Judy, B. M., Newton, L. G., Lubahn, D. B., Rottinghaus, G. E., Macdonald, R. S., Franklin, C., Estes, D. M.: Dietary soy phytoestrogens and ERα signalling modulate interferon gamma production in response to bacterial infection. Clin Exp Immunol 135, 219225 (2004).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34.

    Sirothkin, A. V., Harrath, A. H.: Phytoestrogens and their effects. Eur J Pharmacol 741, 230236 (2014).

  • 35.

    Wei, J., Bhatt, S., Chang, L. M., Sampson, H. A., Masilamani, M.: Isoflavones, genistein and daidzein, regulate mucosal immune response by suppressing dendritic cell function. PLoS One 7, e47979 (2012).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 36.

    Zhao, J. H., Sun, S. J., Horiguchi, H., Arao, Y., Kanamori, N., Kikuchi, A., Oguma, E., Kayama, F.: A soy diet accelerates renal damage in autoimmune MRL/p-IprIpr mice. Int Immunopharmacol 5, 16011610 (2005).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 37.

    Edwards, M. R., Dai, R., Heid, B., Cecere, T. E., Khan, D., Mu, Q., Cowan, C., Luo, X. M., Ahmed, S. A.: Commercial rodent diets differentially regulate autoimmune glomerulonephritis, epigenetics and microbiota in MRL/Ipr mice. Int Immunol 29, 263276 (2017).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 38.

    Tezuka, H., Imai, S.: Immunomodulatory effects of soybeans and processed soy food compounds. Recent Pat Food Nutr Agric 7, 9299 (2015).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 39.

    Guo, T. L., Germolec, D. R., Zheng, J. F., Kooistra, L., Auttachoat, W., Smith, M. J., White, K. L., Elmore, S. A.: Genistein protect female nonobese diabetic mice from developing type 1 diabetes when fed a soy- and alfalfa-free diet. Toxicol Pathol 43, 435448 (2015).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 40.

    Zhang, K., Wang, Y., Ma, W., Hu, Z., Zhao, P.: Genistein improves thyroid function in Hashimoto thyroidits patients through regulating Th1 cytokines. Immunobiology 222, 183187 (2017).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 41.

    De Paula, M. L., Rodrigues, D. H., Teixeira, H. C., Barsante, M. M., Souza, M. A., Ferreira, A. P.: Genistein down-modulates pro-inflammatory cytokines and reverses clinical signs of experimental autoimmune encephalomyelitis. Int Immunopharmacol 8, 12911297 (2008).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 42.

    Jahromi, S. R., Arrefhosseini, S. R., Ghaemi, A., Alizadeh, A., Sabethgadam, F., Togha, M.: Effect of oral genistein administration in early and late phases of allergic encephalomyelitis. Iran J Basic Med Sci 17, 509515 (2014).

    • Search Google Scholar
    • Export Citation
  • 43.

    Razeghi Jahromi, S., Arrefhosseini, S. R., Ghaemi, A., Alizadeh, A., Moradi Tabriz, H., Togha, M.: Alleviation of experimental allergic encephalomyelitis in C57BL/6 mice by soy daidzein. Iran J Allergy Asthma Immunol 13, 256264 (2014).

    • Search Google Scholar
    • Export Citation
  • 44.

    Yen, J. H., Yang, D. J., Chen, M. C., Yi-Ying, W., Hsieh, Y. F., Cheng, Y. M., Huang, W. N., Szondy, Z., Tsay, G.: Daidzein enhances efferocytosis vis transglutaminase 2 and augmentation of Rac1 activity. Mol Immunol 60, 135142 (2014).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 45.

    Edwards, M. R., Dai, R., Heid, B., Cowan, C. R., Ahmed, S. A.: The effect of dietary phytoestrogen content on the development of systemic lupus erythematosus in the MRL/lpr mouse. J Immunol 196, 118.23 (2016).

    • Search Google Scholar
    • Export Citation
  • 46.

    Pierdominici, M., Ortona, E.: Estrogen impact on autoimmunity onset and progression: The paradigm of systemic lupus erithemotosus. Int Trends Immunol 1, 2435 (2013).

    • Search Google Scholar
    • Export Citation
  • 47.

    Jin, X., Wang, S., Zhao, X., Jin, Q., Fan, C., Li, J., Shan, Z., Teng, W.: Coumestrol inhibits autoantibody production through modulating Th1 response in experimental autoimmune thyroiditis. Oncotarget 16, 5279752809 (2016).

    • Search Google Scholar
    • Export Citation
  • 48.

    Tapiero, H., Ba, G. N., Tew, K. D.: Estrogens and environmental estrogens. Biomed Pharmacother 56, 3644 (2002).

  • 49.

    Csaba, G.: Hormonal imprinting: Phylogeny, ontogeny, diseases and possible role in present-day human evolution. Cell Biochem Funct 26, 110 (2008).

  • 50.

    Csaba, G.: Immunoendocrinology: Faulty hormonal imprinting in the immune system. Acta Microbiol Immunol Hung 61, 89106 (2014).

  • 51.

    Csaba, G.: Hormones in the immune system and their possible role. A critical review. Acta Microbiol Immunol Hung 61, 241260 (2014).

  • 52.

    Csaba, G.: The faulty perinatal hormonal imprinting as functional teratogen. Curr Pediatr Rev 12, 222229 (2016).

  • 53.

    Csaba, G.: The present and future of human sexuality: Impact of faulty perinatal hormonal imprinting. Sex Med Rev 5, 163169 (2017).

  • 54.

    Csaba, G., Inczefi-Gonda, Á., Szeberényi, S.: Lasting impact of a single benzpyrene treatment in pre-natal and growing age on the thymic glucocorticoid receptors of rats. Gen Pharmacol 22, 815818 (1991).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 55.

    Csaba, G., Karabélyos, C.: Effect of a single neonatal treatment with the soy bean phytosteroid, genistein on the sexual behavior of adult rats. Acta Physiol Hung 89, 463470 (2002).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 56.

    Csaba, G.: The immunoendocrine thymus as a pacemaker of lifespan. Acta Microbiol Immunol Hung 63, 139158 (2016).

  • 57.

    Kovats, S., Carreras, E., Agrawal, H.: Sex steroid receptors in immune cells. In Arthritis and Immunology Research Program. Oklahoma Medical Research Foundation, Oklahoma City, USA, 2009, pp. 5391.

    • Search Google Scholar
    • Export Citation
  • 58.

    van Hagen, P. M., Holland, L. J., ten Bokum, A. M., Lichtenauer-Kaligis, E. G., Kwekkeboom, D. J., Ferone, D., Lamberts, S. W.: Neuropeptides and their receptors in the immune system. Ann Med 31, 1522 (1999).

    • Search Google Scholar
    • Export Citation
  • 59.

    Csaba, G.: Is there a hormonal regulation of phagocytosis at unicellular and multicellular levels? A critical review. Acta Microbiol Immunol Hung 64, 357372 (2017).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 60.

    Tan, I. J., Peeva, E., Zandman-Goddard, G.: Hormonal modulation of the immune system – A spotlight on the role of progestogens. Autoimmun Rev 14, 636642 (2015).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 61.

    Trigunaite, A., Dimo, J., Jorgensen, T. N.: Suppressive effects of androgens on the immune system. Cell Immunol 294, 8794 (2015).

  • 62.

    Seiki, K., Sakabe, K., Kawashima, I., Fuji-Hanamoto, H.: Hormone and immune response, with special reference to steroid hormone. 1. A short review. Tokai J Exp Clin Med 15, 191199 (1990).

    • Search Google Scholar
    • Export Citation
  • 63.

    Perrotta, C., Buldorini, M., Assi, E., Cazzato, D., De Palma, C., Clementi, E., Cervia, D.: The thyroid hormone, triiodothyronine controls macrophage maturation and functions: Protective role during inflammation. Am J Pathol 184, 230247 (2014).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 64.

    Pállinger, É., Kiss, G. A., Csaba, G.: Hormone (ACTH, T3) content of immunophenotyped lymphocyte subpopulations. Acta Microbiol Immunol Hung 63, 373385 (2016).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 65.

    DeVito, P., Balducci, V., Leone, S., Percario, Z., Mangino, G., Davis, P. J., Davis, F. B., Affabris, E., Luly, P., Pedersen, J. Z., Incerpi, S.: Nongenomic effects of thyroid hormones on the immune system cells: New targets, old players. Steroids 77, 988995 (2012).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 66.

    Csaba, G., Inczefi-Gonda, Á.: Effect of a single treatment (imprinting) with genistein or combined treatment with genistein plus benzpyrene on the binding capacity of glucocorticoid and estrogen receptors of adult rats. Hum Exp Toxicol 21, 231234 (2002).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 67.

    Csaba, G.: Transgenerational effects of perinatal hormonal imprinting. In Tollefsbol, T. (ed) Transgenerational Epigenetics. Elsevier, London, 2014, pp. 255267.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 68.

    Csaba, G., Inczefi-Gonda, Á.: Direct and transgenerational effect of benzpyrene treatment at adolescent age on the uterine estrogen receptor and thymic glucocorticoid receptor of the adult rat. Acta Physiol Hung 86, 2936 (1999).

    • Search Google Scholar
    • Export Citation
  • 69.

    Csaba, G.: The biological basis and clinical significance of hormonal imprinting, an epigenetic process. Clin Epigenetics 2, 187196 (2011).

  • 70.

    Karsli-Ceppioglu, S., Ngollo, M., Adjakly, M., Dagdemir, A., Judes, G., Lebert, A., Boiteux, J.-P., Penault-Llorca, F., Bignon, Y. J., Guy, L., Bernard-Gallon, D.: Genome-wide DNA methylation modified by soy phytoestrogens: Role for epigenetic therapeutics in prostate cancer? OMICS 19, 209219 (2015).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 71.

    Adjakly, M., Ngollo, M., Lebert, A., Dagdemir, A., Penault-Llorca, F., Boiteux, J-P.: Comparative effects of soy phytoestrogens and 17beta-estradiol on DNA methylation of a panel of 24 genes in prostate cancer lines. Nutr Cancer 66, 474482 (2014).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 72.

    Guerrero-Bosagna, C. M., Skinner, M. K.: Environmental epigenetics and phytoestrogen phytochemical exposures. J Steroid Biochem Mol Biol 139, 270276 (2014).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 73.

    Csaba, G.: The role of brain-pineal-thymus system in the determination of lifespan: The autoimmune aging theory. Adv Neuroimm Biol 6, 139148 (2017).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 74.

    Hall, A.: The dark side of soya: How one super crop lost its way? Ecologist, Green living food and drink May 01 (2012). Available at https://theecologist.org/

    • Search Google Scholar
    • Export Citation
  • 75.

    Barnett, A.: They hailed it as a wonderfood. TheGuardian.com, Life and style Nov 07 (2004). Available at https://www.theguardian.com/uk/lifeandstyle

    • Search Google Scholar
    • Export Citation
  • 76.

    Jacobson-Dickman, E., Lee, M. M.: The influence of endocrine disruptors on pubertal timing. Curr Opin Endocrinol Diabetes Obes 16, 2530 (2009).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 77.

    Marks, K. J., Hartman, T. J., Taylor, E. V., Rybak, M. E., Northstone, K., Marcus, M.: Exposure to phytoestrogens in utero and age at menarche in a contemporary British cohort. Environ Res 155, 287293 (2017).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 78.

    Martocchia, A., Stefanelli, M., Cola, S., Falaschi, P.: Sex steroids in autoimmune diseases. Curr Top Med Chem 11, 16681683 (2011).

  • 79.

    Csaba, G.: Vitamin-caused faulty perinatal hormonal imprinting and its consequences in adult age. Physiol Int 104, 217225 (2017).

  • 80.

    Tuohy, P. G.: Soy infant formula and phytoestrogens. J Paediatr Child Health 39, 401405 (2003).

  • 81.

    Baclottini, L., Falchetti, A., Pampaloni, B., Bartolini, E., Carossino, A. M., Brandl, M. L.: Phytoestrogens: Food or drug? Clin Cases Miner Bone Metab 4, 123130 (2007).

    • Search Google Scholar
    • Export Citation
  • 82.

    Lambert, M. R., Edwards, T. M.: Hormonally active phytochemicals and vertebrate evolution. Evol Appl 10, 419432 (2017).

  • 83.

    Wasserman, J. K.: Estrogenic plants linked to altered hormones, possible behavior changes in monkeys. Science Daily. Available at www.sciencedaily.com/releases/2012/11/121119171409.htm

    • Search Google Scholar
    • Export Citation
  • 84.

    Wasserman, M. D., Milton, K., Chapman, C. A.: The roles of phytoestrogens in primate ecology and evolution. Int J Primatol 34, 861878 (2013).

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 85.

    Csaba, G.: Faulty perinatal hormonal imprinting caused by exogeneous vitamin D – Dangers and problems. Aust J Nutr Food Sci 4, 10751079 (2016).

    • Search Google Scholar
    • Export Citation
  • 86.

    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 31, 666670 (2009).

    • Crossref
    • Search Google Scholar
    • Export Citation
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