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Beneficial and Deleterious Effects of Female Sex Hormones, Oral International Journal of Molecular Sciences Review Beneficial and Deleterious Effects of Female Sex Hormones, Oral Contraceptives, and Phytoestrogens by Immunomodulation on the Liver Luis E. Soria-Jasso 1, Raquel Cariño-Cortés 1,Víctor Manuel Muñoz-Pérez 1, Elizabeth Pérez-Hernández 2, Nury Pérez-Hernández 3 and Eduardo Fernández-Martínez 1,* 1 Laboratory of Medicinal Chemistry and Pharmacology, Centro de Investigación en Biología de la Reproducción, Área Académica de Medicina, Instituto de Ciencias de la Salud, Universidad Autónoma del Estado de Hidalgo. Calle Dr. Eliseo Ramírez Ulloa no. 400, Col. Doctores, Pachuca Hidalgo 42090, Mexico; [email protected] (L.E.S.-J.); [email protected] (R.C.-C.); [email protected] (V.M.M.-P.) 2 Hospital de Ortopedia “Dr. Victorio de la Fuente Narváez”, IMSS, Mexico 07760, Mexico; [email protected] 3 Programa Institucional de Biomedicina Molecular, Escuela Nacional de Medicina y Homeopatía, Instituto Politécnico Nacional, Mexico 07320, Mexico; [email protected] * Correspondence: [email protected] or [email protected]; Tel.: +52-771-717-2000 Received: 14 August 2019; Accepted: 20 September 2019; Published: 22 September 2019 Abstract: The liver is considered the laboratory of the human body because of its many metabolic processes. It accomplishes diverse activities as a mixed gland and is in continuous cross-talk with the endocrine system. Not only do hormones from the gastrointestinal tract that participate in digestion regulate the liver functions, but the sex hormones also exert a strong influence on this sexually dimorphic organ, via their receptors expressed in liver, in both health and disease. Besides, the liver modifies the actions of sex hormones through their metabolism and transport proteins. Given the anatomical position and physiological importance of liver, this organ is evidenced as an immune vigilante that mediates the systemic immune response, and, in turn, the immune system regulates the hepatic functions. Such feedback is performed by cytokines. Pro-inflammatory and anti-inflammatory cytokines are strongly involved in hepatic homeostasis and in pathological states; indeed, female sex hormones, oral contraceptives, and phytoestrogens have immunomodulatory effects in the liver and the whole organism. To analyze the complex and interesting beneficial or deleterious effects of these drugs by their immunomodulatory actions in the liver can provide the basis for either their pharmacological use in therapeutic treatments or to avoid their intake in some diseases. Keywords: cholestasis; cirrhosis; cytokines; immunomodulation; liver; oral contraceptives; phytoestrogens; sex hormones 1. Introduction The liver is called the body’s biochemical laboratory because of the many metabolic functions that it accomplishes. Also, the liver is the largest inner organ, with an average weight of 1.5 kg. It is considered a mixed gland: Endocrine because of the insulin-like growth factor 1 (IGF-1) production (among other functional/transport/blood proteins), and exocrine because of the bile production [1,2]. Hepatocytes are the liver parenchyma. They constitute 70%–85% of the hepatic mass that carries out more than 500 metabolic functions [1] (Figure1). Important hepatic functions include the metabolism of nutrients, storage of vitamins and minerals, production of most of plasma proteins, hormonal balance, and detoxification of compounds produced from metabolism. Also, the liver secretes bile for digestion of lipids by emulsifying fats [1]. The importance of the liver in the metabolism of Int. J. Mol. Sci. 2019, 20, 4694; doi:10.3390/ijms20194694 www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2019, 20, 4694 2 of 39 Int. J. Mol. Sci. 2019, 20, x FOR PEER REVIEW 2 of 41 digestion of lipids by emulsifying fats [1]. The importance of the liver in the metabolism of carbohydrates, proteins, and lipids is fundamental [1]. For instance, the liver regulates the plasma carbohydrates, proteins, and lipids is fundamental [1]. For instance, the liver regulates the plasma glucose concentration during fasting by glycogenolysis and gluconeogenesis, participates in the glucose concentration during fasting by glycogenolysis and gluconeogenesis, participates in the synthesis/degradation of proteins, and participates in lipogenesis and synthesis of cholesterol and synthesis/degradation of proteins, and participates in lipogenesis and synthesis of cholesterol and triglycerides [3,4]. triglycerides [3,4]. FigureFigu re 1.1. SchemeScheme ofof thethe liverliver andand hepatichepatic sinusoid.sinusoid. LiverLiver rightright lobelobe (RL),(RL), leftleft lobelobe (LL),(LL), andand thethe hepatichepatic sinusoidsinusoid that that is is composed composed by by hepatocytes hepatocytes (H), (H), sinusoidal sinusoidal endothelial endothelial cells cells (E), (E), macrophage macrophage Kup Kupfferffer cell (K),cell natural(K), natural killer killer or pit or cell pit (P), cell Ito (P), or Ito stellate or stellate cell (S), cell space (S), space of Disse of Disse (D), and(D), lumenand lumen (L). (L). TheThe liverliver su suffersffers from from diverse diverse ailments ailments such assuch fatty as liver fatty (hepatic liver steatosis),(hepatic steatosis), caused by alcoholism,caused by oralcoholism, non-alcoholic or non-alcoholic fatty liver disease fatty (NAFLD), liver disease caused (NAFLD), by diabetes caused and metabolicby diabetes syndrome and metabolic (MetS), whichsyndrome in turn (MetS), may which advance in turn to non-alcoholic may advance steatohepatitisto non-alcoholic (NASH), steatohepati cholestasistis (NASH), (mechanical cholestasis or functional(mechanical stagnation or functional of bile), stagnation viral hepatitis of bile), (inflammation viral hepatitis by(inflammation infection with by hepatitis infection B with or C hepatitis viruses, (HBVB or C or viruses, HCV)), (HBV necrosis or HCV)), (non-programmed necrosis (non-programmed cellular death by cellular infection death or injury),by infection and/ oror fibrosisinjury), (excessand/or offibrosis connective (excess tissue). of connective These all tissue). may become These chronic,all may become which results chronic, in thewhich final results stage: in Cirrhosis. the final Nonetheless,stage: Cirrhosis. cirrhosis Nonetheless, can advance cirrhosis to hepatocellular can advance to carcinoma hepatocellular (HCC), carcinoma the most (HCC), frequent the cancer most offrequent the liver cancer [5]. of There the liver are other[5]. There possible are other causes po ofssible liver causes damage, of liver such damage, as endocrine such as disruptors, endocrine whichdisruptors, are compounds which are thatcompounds alter the normalthat alter functioning the normal of hormones.functioning Endocrineof hormones. disruptors Endocrine can occurdisruptors naturally, can occur others naturally, are synthetic, others and are theysynthetic, are mainly and they considered are mainly pollutants considered such pollutants as pesticides, such industrialas pesticides, chemicals, industrial and chemicals, pharmaceutical and pharmaceut agents. Indeed,ical agents. there Indeed, are diverse there drugs are diverse that induce drugs liver that damage,induce liver either damage, by long-term either and by high-dose long-term administration and high-dose or by dietaryadministration and environmental or by dietary exposure, and forenvironmental example, acetaminophen, exposure, for cyclosporine, example, acetamin rifampicin,ophen, bosentan, cyclosporine, glibenclamide, rifampicin, anticoagulants, bosentan, phenytoin,glibenclamide, and herbalanticoagulants, products, phenytoin, as well as sex and hormones herbal products, or their metabolites as well as andsex analogs,hormones including or their drugsmetabolites with hormonal and analogs, side eincludingffects such drugs as metoprolol, with horm naproxen,onal side and effects clofibrate such as [6 ,metoprolol,7]. The liver naproxen, possesses anand extraordinary clofibrate [6,7]. regenerative The liver capacity possesses to keepan extraord its cellularinary architecture regenerative and capacity numerous to criticalkeep its functions cellular intactarchitecture despite and the constantnumerous insults critical due functions uptake, metabolism, intact despite and excretionthe constant of both insults endogenous due uptake, and exogenousmetabolism, compounds, and excretion including of both drugs. endogenous Nevertheless, and its exogenous anatomical compounds, position inthe including digestive drugs. tract, highNevertheless, blood irrigation, its anatomical and intense position activity in the makes digestiv the livere tract, extremely high blood susceptible irrigation, to injury and intense and cancer activity [8]. Interestingly,makes the liver cytokines extremely (small susceptible glycosylated to proteins injury mainlyand cancer produced [8]. Interestingly, by cells of the cytokines immune system(small butglycosylated also by many proteins others) mainly and hormones produced participateby cells of inthe cross-talk immune tosystem regulate but complex also by many processes others) in both and healthhormones and diseaseparticipate states. in cross-talk to regulate complex processes in both health and disease states. TheThe importanceimportance ofof sexsex hormoneshormones isis undeniable,undeniable, sincesince theythey regulateregulate sexualsexual didifferentiationfferentiation andand reproduction,reproduction, andand theythey alsoalso havehave aa strongstrong influenceinfluence onon thethe immuneimmune system.system. TheThe
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