Role of the sex hormone estrogen in the prevention of lipid disorder

Current Medicinal Chemistry

Volumn 21, Issue 24, 2014, Pages 2734-2742

  Pellegrini, M ^a   Pallottini, V ^a   Marin R ^b   Marino, M ^a  

^a ROMA TRE UNIVERSITY   (Italy)

^b UNIVERSIDAD DE LA LAGUNA   (Spain)

Author keywords

Estrogen; Estrogen receptors; Hypercholesterolemia; Lipid disorders; Lipid rafts; Neurodegeneration; Obesity; Steatosis

Indexed keywords

ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR;

ADIPOSE TISSUE; ARTICLE; ATHEROGENIC DYSLIPIDEMIA; BODY WEIGHT; BRAIN; CHOLESTEROL ESTERIFICATION; DISEASE COURSE; DISORDERS OF LIPID AND LIPOPROTEIN METABOLISM; DYSLIPIDEMIA; FAT MASS; FATTY LIVER; HORMONE DETERMINATION; HORMONE STRUCTURE; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INTRAABDOMINAL FAT; LIPID HOMEOSTASIS; LIPID METABOLISM; LIVER; NERVE CELL; NONHUMAN; OBESITY; PALMITOYLATION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; SEX DIFFERENCE; SUBCUTANEOUS FAT; UBIQUITINATION; DRUG EFFECTS; FEMALE; LIPID METABOLISM DISORDERS; MALE; METABOLISM; SEXUAL DEVELOPMENT;

ESTRADIOL; ESTROGENS; FEMALE; HUMANS; LIPID METABOLISM; LIPID METABOLISM DISORDERS; MALE; SEX CHARACTERISTICS;

EID: 84903702796     PISSN: 09298673     EISSN: 1875533X     Source Type: Journal    
DOI: 10.2174/0929867321666140303123602     Document Type: Article

References (123)

1. Marino, M.; Masella, R.; Bulzomi, P.; Campesi, I.; Malorni, W.; Franconi, F. Nutrition and human health from a sex-gender perspective. Mol. Aspects Med., 2011, 32(1), 1-70.
2. Williams, C.M. Lipid metabolism in women. Proc. Nutr. Soc., 2004, 63(1), 153-160.
3. Bjorntorp, P. Regional patterns of fat distribution. Ann. Intern. Med., 1985, 103(6 (Pt 2)), 994-995.
4. Ley, C.J.; Lees, B.; Stevenson, J.C. Sex-and menopause-associated changes in body-fat distribution. Am. J. Clin. Nutr., 1992, 55(5), 950-954.
5. Kotani, K.; Tokunaga, K.; Fujioka, S.; Kobatake, T.; Keno, Y.; Yoshida, S.; Shimomura, I.; Tarui, S.; Matsuzawa, Y. Sexual dimorphism of age-related changes in whole-body fat distribution in the obese. Int. J. Obes. Relat. Metab. Disord., 1994, 18(4), 207-202.
6. Lemieux, S.; Prud'homme, D.; Bouchard, C.; Tremblay, A.; Despres, J.P. Sex differences in the relation of visceral adipose tissue accumulation to total body fatness. Am. J. Clin. Nutr., 1993, 58(4), 463-467.
7. Snijder, M.B.; Zimmet, P.Z.; Visser, M.; Dekker, J.M.; Seidell, J.C.; Shaw, J.E. Independent association of hip circumference with metabolic profile in different ethnic groups. Obes. Res., 2004, 12(9), 1370-1374.
8. Peverill, R.E.; Teede, H.J.; Malan, E.; Kotsopoulos, D.; Smolich, J.J.; McGrath, B.P. Relationship of waist and hip circumferenc ewith coagulation and fibrinolysis in postmenopausal women. Clin. Sci. (Lond.), 2007, 113(9), 383-391.
9. Lovejoy, J.C.; Sainsbury, A. Sex differences in obesity and the regulation of energy homeostasis. Obes. Rev., 2009, 10(2), 154-167.
10. Kim, A.M.; Tingen, C.M.; Woodruff, T.K. Sex bias in trials and treatment must end. Nature, 2010, 465(7299), 688-689.
11. Mattiasson, I.; Rendell, M.; Tornquist, C.; Jeppsson, S.; Hulthen, U.L. Effects of estrogen replacement therapy on abdominal fat compartments as related to glucose and lipid metabolism in early postmenopausal women. Horm. Metab. Res., 2002, 34(10), 583-588.
12. Jones, M.E.; Thorburn, A.W.; Britt, K.L.; Hewitt, K.N.; Wreford, N.G.; Proietto, J.; Oz, O.K.; Leury, B.J.; Robertson, K.M.; Yao, S.; Simpson, E.R. Aromatase-deficient (ArKO) mice have a phenotype of increased adiposity. Proc. Natl. Acad. Sci. U.S.A., 2000, 97(23), 12735-12740.
13. Barros, R.P.; Gustafsson, J.A. Estrogen receptors and the metabolic network. Cell Metab., 2011, 14(3), 289-299.
14. Ascenzi, P.; Bocedi, A.; Marino, M. Structure-function relationship of estrogen receptor and ß: impact on human health. Mol. Aspects Med., 2006, 27(4), 299-402.
15. Le Romancer, M.; Poulard, C.; Cohen, P.; Sentis, S.; Renoir, J.M.; Corbo, L. Cracking the estrogen receptor's posttranslational code in breast tumors. Endocr. Rev., 2011, 32(5), 597-622.
16. Safe, S. Transcriptional activation of genes by 17β-estradiol through estrogen receptor-Sp1 interactions. Vitam. Horm., 2001, 62, 231-252.
17. Pearce, S.T.; Jordan, V.C.The biological role of estrogen receptors alpha and beta in cancer. Crit. Rev. Oncol. Hematol., 2004, 50(1), 3-22.
18. Greaves, E. ; Collins, F. ; Critchley, H.O. ; Saunders, P.T. ERβ-dependent effects on uterine endothelial cells are cell specific and mediated via Sp1. Hum. Reprod., 2013, 28(9), 2490-2501.
19. Acconcia, F.; Marino, M. The Effects of 17β-estradiol in Cancer are Mediated by Estrogen Receptor Signaling at the Plasma Membrane. Front. Physiol., 2011, 2, 30.
20. Deroo, B.J.; Korach, K.S. Estrogen receptors and human disease. J. Clin. Invest., 2006, 116(3), 561-570.
21. Marino, M.; Ascenzi, P. Membrane association of estrogen receptor a and ß influences 17β-estradiol-mediated cancer cell proliferation. Steroids, 2008, 73(9-10), 853-858.
22. Acconcia, F.; Ascenzi, P.; Bocedi, A.; Spisni, E.; Tomasi, V.; Trentalance, A.; Visca, P.; Marino, M. Palmitoylation-dependent estrogen receptor α membrane localization: regulation by 17 β-estradiol. Mol. Biol. Cell., 2005, 16(1), 231-237.
23. Galluzzo, P.; Caiazza, F.; Moreno, S.; Marino, M. Role of ERβ palmitoylation in the inhibition of human colon cancer cell proliferation. Endocr. Relat. Cancer, 2007, 14(1), 153-167.
24. La Rosa, P.; Acconcia, F. Signaling functions of ubiquitin in the 17β-estradiol (E2): estrogen receptor (ER) network. J. Steroid Biochem. Mol. Biol., 2011, 127(3-5), 223-230.
25. La Rosa, P.; Marino, M.; Acconcia, F. 17β-estradiol regulates estrogen receptor α monoubiquitination. IUBMB Life, 2011, 63(1), 49-53.
26. La Rosa, P.; Pesiri, V.; Marino, M.; Acconcia, F. 17β- Estradiolinduced cell proliferation requires estrogen receptor (ER) α monoubiquitination. Cell. Signal., 2011, 23(7), 1128-1135.
27. Frayn, K.N.; Karpe, F.; Fielding, B.A.; Macdonald, I.A.; Coppack, S.W. Integrative physiology of human adipose tissue. Int. J. Obes. Relat. Metab. Disord., 2003, 27(8), 875-888.
28. Oosthuyse, T.; Bosch, A.N. Oestrogen's regulation of fat metabolism during exercise and gender specific effects. Curr. Opin. Pharmacol., 2012, 12(3), 363-371.
29. Tchernof, A.; Despres, J.P. Pathophysiology of Human Visceral Obesity: An Update. Physiol. Rev., 2013, 93(1), 359-404.
30. Rodriguez-Cuenca, S.; Monjo, M.; Frontera, M.; Gianotti, M.; Proenza, A.M.; Roca, P. Sex steroid receptor expression profile in brown adipose tissue. Effects of hormonal status. Cell. Physiol. Biochem., 2007, 20(6), 877-886.
31. Shi, H.; Seeley, R.J.; Clegg, D.J. Sexual differences in the control of energy homeostasis. Front. Neuroendocrinol., 2009, 30(3), 396-404.
32. Asarian, L.; Geary, N. Cyclic estradiol treatment normalizes body weight and restores physiological patterns of spontaneous feeding and sexual receptivity in ovariectomized rats. Horm. Behav., 2002, 42(4), 461-471.
33. Ordóñez, P.; Moreno, M.; Alonso, A.; Llaneza, P.; Díaz, F.; González, C. 17 β-Estradiol and/or progesterone protect from insulin resistance in STZ-induced diabetic rats. J. Steroid Biochem. Mol. Biol., 2008, 111(3-5), 287-294.
34. Wohlers, L.M.; Spangenburg, E.E. 17β-estradiol supplementation attenuates ovariectomy-induced increases in ATGL signaling and reduced perilipin expression in visceral adipose tissue. J. Cell. Biochem., 2010, 110(2), 420-427.
35. Bryzgalova, G.; Lundholm, L.; Portwood, N.; Gustafsson, J.A.; Khan, A.; Efendic, S.; Dahlman-Wright, K. Mechanisms of antidiabetogenic and body weight-lowering effects of estrogen in highfatdiet-fedmice. Am. J. Physiol. Endocrinol. Metab., 2008, 295(4), E904-E912.
36. Jones, M.E.; Boon, W.C.; Proietto, J.; Simpson, E.R. Of mice and men: the evolving phenotype of aromatase deficiency. Trends Endocrinol. Metab., 2006, 17(2), 55-64.
37. Pallottini, V.; Bulzomi, P.; Galluzzo, P.; Martini, C.; Marino, M. Estrogen regulation of adipose tissue functions: involvement of estrogen receptor isoforms. Infect. Disord. Drug Targets, 2008, 8(1), 52-60.
38. Bjorntorp, P. On the integration of research. Int. J. Obes. Relat. Metab. Disord., 1996, 20(10), 973.
39. D'Eon, T.M.; Souza, S.C.; Aronovitz, M.; Obin, M.S.; Fried, S.K.; Greenberg, A.S. Estrogen regulation of adiposity and fuel partitioning. Evidence of genomic and non-genomic regulation of lipogenic and oxidative pathways. J. Biol. Chem., 2005, 280(43), 35983-35991.
40. Brown, L.M.; Clegg, D.J. Central effects of estradiol in the regulation of food intake, body weight, and adiposity. J. Steroid Biochem. Mol. Biol., 2010, 122(1-3), 65-73.
41. Crandall, D.L.; Busler, D.E.; Novak, T.J.; Weber, R.V.; Kral, J.G. Identification of estrogen receptor beta RNA in human breast and abdominal subcutaneous adipose tissue. Biochem. Biophys. Res. Commun., 1998, 248(3), 523-526.
42. Dieudonne, M.N.; Leneveu, M.C.; Giudicelli, Y.; Pecquery, R. Evidence for functional estrogen receptors alpha and beta in human adipose cells: regional specificities and regulation by estrogens. Am. J. Physiol. Cell. Physiol., 2004, 286(3), C655-C661.
43. Casazza, K.; Page, G.P.; Fernandez, J.R. The association between the rs2234693 and rs9340799 estrogen receptor alpha gene polymorphisms and risk factors for cardiovascular disease: a review. Biol. Res. Nurs., 2010, 12(1), 84-97.
44. Heine, P.A.; Taylor, J.A.; Iwamoto, G.A.; Lubahn, D.B.; Cooke, P.S. Increased adipose tissue in male and female estrogen receptoralpha knockout mice. Proc. Natl. Acad. Sci. USA, 2000, 97(23), 12729-12734.
45. Foryst-Ludwig, A.; Clemenz, M.; Hohmann, S.; Hartge, M.; Sprang, C.; Frost, N.; Krikov, M.; Bhanot, S.; Barros, R.; Morani, A.; Gustafsson, J.A.; Unger, T.; Kintscher, U. Metabolic actions of estrogen receptor (ERβ) are mediated by a negative cross-talk with PPAR. PLoS Genet., 2008, 4(6), e1000108.
46. Ohlsson, C.; Hellberg, N.; Parini, P.; Vidal, O.; Bohlooly, Y.M.; Rudling, M.; Lindberg, M.K.; Warner, M.; Angelin, B.; Gustafsson, J.A. Obesity and disturbed lipoprotein profile in estrogen receptor-deficient male mice. Biochem. Biophys. Res. Commun., 2000, 278(3), 640-645.
47. Meyer, M.R.; Clegg, D.J.; Prossnitz, E.R.; Barton, M. Obesity, insulin resistance and diabetes: sex differences and role of oestrogen receptors. Acta Physiol. (Oxf.), 2011, 203(1), 259-269.
48. Matthews, J.; Gustafsson, J.A. Estrogen signaling: a subtle balance between ER alpha and ER beta. Mol. Interv., 2003, 3(5), 281-292.
49. Revankar, C.M.; Cimino, D.F.; Sklar, L.A.; Arterburn, J.B.; Prossnitz, E.R., A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science, 2005, 307(5715), 1625-1630.
50. Ford, J.; Hajibeigi, A.; Long, M.; Hahner, L.; Gore, C.; Hsieh, J.T.; Clegg, D.; Zerwekh, J.; Oz, O.K. GPR30 deficiency causes increased bone mass, mineralization, and growth plate proliferative activity in male mice. J. Bone Miner. Res., 2011, 26(2), 298-307.
51. Prossnitz, E.R.; Barton, M. The G-protein-coupled estrogen receptor GPER in health and disease. Nat. Rev. Endocrinol., 2011, 7(12), 715-726.
52. Farrell, G.C.; Larter, C.Z. Nonalcoholic fatty liver disease: from steatosis to cirrhosis. Hepatology, 2006, 43(2(Suppl 1)), S99-S112.
53. Marchesini, G.; Forlani, G. NASH: from liver diseases to metabolic disorders and back to clinical hepatology. Hepatology, 2002, 35(2), 497-499.
54. Matsuzawa, N.; Takamura, T.; Kurita, S.; Misu, H.; Ota, T.; Ando, H.; Yokoyama, M.; Honda, M.; Zen, Y.; Nakanuma, Y.; Miyamoto, K.; Kaneko, S. Lipid-induced oxidative stress causes steatohepatitis in mice fed an atherogenic diet. Hepatology, 2007, 46(5), 1392-1403. (Pubitemid 350155521)
55. Wouters, K.; van Gorp, P.J.; Bieghs, V.; Gijbels, M.J.; Duimel, H.; Lutjohann, D.; Kerksiek, A.; van Kruchten, R.; Maeda, N.; Staels, B.; van Bilsen, M.; Shiri-Sverdlov, R.; Hofker, M.H. Dietary cholesterol, rather than liver steatosis, leads to hepatic inflammation in hyperlipidemic mouse models of nonalcoholic steatohepatitis. Hepatology, 2008, 48(2), 474-486.
56. Puri, P.; Baillie, R.A.; Wiest, M.M.; Mirshahi, F.; Choudhury, J.; Cheung, O.; Sargeant, C.; Contos, M.J.; Sanyal, A.J. A lipidomic analysis of nonalcoholic fatty liver disease. Hepatology, 2007, 46(4), 1081-1090. (Pubitemid 350144772)
57. Trapani, L.; Segatto, M.; Pallottini, V. Regulation and deregulation of cholesterol homeostasis: The liver as a metabolic "power station". World J. Hepatol., 2012, 4(6), 184-190.
58. Nemoto, Y.; Toda, K.; Ono, M.; Fujikawa-Adachi, K.; Saibara, T.; Onishi, S.; Enzan, H.; Okada, T.; Shizuta, Y. Altered expression of fatty acid-metabolizing enzymes in aromatase-deficient mice. J. Clin. Invest., 2000, 105(12), 1819-1825.
59. Chow, J.D.; Jones, M.E.; Prelle, K.; Simpson, E.R.; Boon, W.C. A selective estrogen receptor agonist ameliorates hepatic steatosis in the male aromatase knockout mouse. J. Endocrinol., 2011, 210(3), 323-334.
60. Kamada, Y.; Kiso, S.; Yoshida, Y.; Chatani, N.; Kizu, T.; Hamano, M.; Tsubakio, M.; Takemura, T.; Ezaki, H.; Hayashi, N.; Takehara, T.Estrogen deficiency worsens steatohepatitis in mice fed high-fat and high-cholesterol diet. Am. J. Physiol. Gastrointest. Liver Physiol., 2010, 301(6), G1031-G1043.
61. Redig, A.J.; Munshi, H.G. Care of the cancer survivor: metabolic syndrome after hormone-modifying therapy. Am. J. Med., 2010, 123(1), 87 e1-e6.
62. Fisher, C.R.; Graves, K.H.; Parlow, A.F.; Simpson, E.R. Characterization of mice deficient in aromatase (ArKO) because of targeted disruption of the cyp19 gene. Proc. Natl. Acad. Sci. USA, 1998, 95(12), 6965-6970.
63. Tian, G.X.; Sun, Y.; Pang, C.J.; Tan, A.H.; Gao, Y.; Zhang, H.Y.; Yang, X.B.; Li, Z.X.; Mo, Z.N. Oestradiol is a protective factor for non-alcoholic fatty liver disease in healthy men. Obes. Rev., 2012, 13(4), 381-387.
64. Volzke, H.; Schwarz, S.; Baumeister, S.E.; Wallaschofski, H.; Schwahn, C.; Grabe, H.J.; Kohlmann, T.; John, U.; Doren, M. Menopausal status and hepatic steatosis in a general female population. Gut, 2007, 56(4), 594-595. (Pubitemid 46580520)
65. Espeland, M.A.; Marcovina, S.M.; Miller, V.; Wood, P.D.; Wasilauskas, C.; Sherwin, R.; Schrott, H.; Bush, T.L. Effect of postmenopausal hormonetherapy on lipoprotein(a) concentration. PEPI Investigators. Postmenopausal Estrogen/ProgestinInterventions. Circulation, 1998, 97(10), 979-986.
66. Musunuru, K. Atherogenic dyslipidemia: cardiovascular risk and dietary intervention. Lipids, 2010, 45(10), 907-914.
67. De Marinis, E.; Martini, C.; Trentalance, A.; Pallottini, V., Sex differences in hepatic regulation of cholesterol homeostasis. J. Endocrinol., 2008, 198(3), 635-643.
68. Weber, L.W.; Boll, M.; Stampfl, A. Maintaining cholesterol homeostasis: sterol regulatory element-binding proteins. World J. Gastroenterol., 2004, 10(21), 3081-3087.
69. Di Croce, L.; Vicent, G.P.; Pecci, A.; Bruscalupi, G.; Trentalance, A.; Beato, M. The promoter of the rat 3-hydroxy-3-methylglutaryl coenzyme A reductase gene contains a tissue-specific estrogenresponsive region. Mol. Endocrinol., 1999, 13(8), 1225-1236.
70. Marino, M.; Distefano, E.; Pallottini, V.; Caporali, S.; Bruscalupi, G.; Trentalance, A. Activation of IP(3)-protein kinase C-α signal transduction pathway precedes the changes of plasma cholesterol, hepatic lipid metabolism and induction of low-density lipoprotein receptor expression in 17-β-oestradiol-treated rats. Exp. Physiol., 2001, 86(1), 39-45.
71. Galluzzo, P.; Rastelli, C.; Bulzomi, P.; Acconcia, F.; Pallottini, V.; Marino, M. 17β-Estradiol regulates the first steps of skeletal muscle cell differentiation via ER-α-mediated signals. Am. J. Physiol. Cell Physiol., 2009, 297(5), C1249-C1262.
72. Moreno, M.; Ordoñez, P.; Alonso, A.; Díaz, F.; Tolivia, J.; González, C. Chronic 17β-estradiol treatment improves skeletal muscle insulin signaling pathway components in insulin resistance associated with aging. Age (Dordr.), 2010, 32(1), 1-13.
73. Gao, H.; Falt, S.; Sandelin, A.; Gustafsson, J.A.; Dahlman-Wright, K. Genome-wide identification of estrogen receptor α-binding sites in mouse liver. Mol. Endocrinol., 2008, 22(1), 10-22.
74. Brandenberger, A.W.; Tee, M.K.; Lee, J.Y.; Chao, V.; Jaffe, R.B. Tissue distribution of estrogen receptors alpha (ER-β) and beta (ERβ) mRNA in the midgestational human fetus. J. Clin. Endocrinol. Metab., 1997, 82(10), 3509-3512.
75. Inoue, H.; Shimizu, I.; Lu, G.; Itonaga, M.; Cui, X.; Okamura, Y.; Shono, M.; Honda, H.; Inoue, S.; Muramatsu, M.; Ito, S. Idoxifene and estradiol enhance antiapoptotic activity through estrogen receptor-beta in cultured rat hepatocytes. Dig. Dis. Sci., 2003, 48(3), 570-580.
76. Bryzgalova, G.; Gao, H.; Ahren, B.; Zierath, J.R.; Galuska, D.; Steiler, T.L.; Dahlman-Wright, K.; Nilsson, S.; Gustafsson, J.A.; Efendic, S.; Khan, A. Evidence that oestrogen receptor-alpha plays an important role in the regulation of glucose homeostasis in mice: insulin sensitivity in the liver. Diabetologia, 2006, 49(3), 588-597. (Pubitemid 43277883)
77. Pedram, A.; Razandi, M.; O'Mahony, F.; Harvey, H.; Harvey, B.J.; Levin, E.R. Estrogen reduces lipid content in the liver exclusively from membrane receptor signaling. Sci. Signal., 2013, 6(276), ra36.
78. Evans, M.J.; Lai, K.; Shaw, L.J.; Harnish, D.C.; Chadwick, C.C. Estrogen receptor alpha inhibits IL-1beta induction of gene expression in the mouse liver. Endocrinology, 2002, 143(7), 2559-2570. (Pubitemid 34701319)
79. Farooqui, A.A.; Farooqui, T.; Panza, F.; Frisardi, V. Metabolic syndrome as a risk factor for neurological disorders. Cell Mol. Life Sci., 2012, 69(5), 741-762.
80. Peri, A.; Benvenuti, S.; Luciani, P.; Deledda, C.; Cellai, I. Membrane cholesterol as a mediator of the neuroprotective effects of estrogens. Neuroscience, 2011, 191, 107-117.
81. Simons, K.; Toomre, D. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell. Biol., 2000, 1(1), 31-39.
82. Brown, D.A.; London, E. Structure and function of sphingolipidand cholesterol-rich membrane rafts. J. Biol. Chem., 2000, 275(23), 17221-17224.
83. Stillwell, W.; Wassall, S.R. Docosahexaenoic acid: Membrane properties of a unique fatty acid. Chem. Phys. Lipids, 2003, 126(1), 1-27.
84. Benarroch, E.E. Lipid rafts, protein scaffolds, and neurologic disease. Neurology, 2007, 69(16), 1635-1639. (Pubitemid 350287148)
85. Lingwood, D.; Simons, K. Lipid rafts as a membrane-organizing principle. Science, 2010, 327(5961), 46-50.
86. Chung, T.H.; Wang, S.M.; Liang, J.Y.; Yang, S.H.; Wu, J.C. The interaction of estrogen receptor alpha and caveolin-3 regulates connexin43 phosphorylation in metabolic inhibition-treated rat cardiomyocytes. Int. J. Biochem. Cell. Biol., 2009, 41(11), 2323-2333.
87. Reineri, S.; Bertoni, A.; Sanna, E.; Baldassarri, S.; Sarasso, C.; Zanfa, M.; Canobbio, I.; Torti, M.; Sinigaglia, F. Membrane lipi drafts coordinate estrogen-dependent signaling in human platelets. Biochim. Biophys. Acta, 2007, 1773(2), 273-278.
88. Marìn, R.; Diaz, M.; Alonso, R.; Sanz, A.; Arevalo, M.A.; Garcia-Segura, L.M. Role of estrogen receptor alpha in membraneinitiated signaling in neural cells: interaction with IGF-1 receptor. J. Steroid Biochem. Mol. Biol., 2009, 114(1-2), 2-7.
89. Ramirez, C.M.; Gonzalez, M.; Diaz, M.; Alonso, R.; Ferrer, I.; Santpere, G.; Puig, B.; Meyer, G.; Marin, R. VDAC and ERalpha interaction in caveolae from human cortex is altered in Alzheimer's disease. Mol. Cell. Neurosci., 2009, 42(3), 172-183.
90. Marin, R.; Ramirez, C.M.; Gonzalez, M.; Gonzalez-Munoz, E.; Zorzano, A.; Camps, M.; Alonso, R.; Diaz, M. Voltage-dependent anion channel (VDAC) participates in amyloid beta-induced toxicity and interacts with plasma membrane estrogen receptor alpha in septal and hippocampal neurons. Mol. Membr. Biol., 2007, 24(2), 148-160.
91. Toran-Allerand, C.D. Mini review: A plethora of estrogen receptors in the brain: where will it end? Endocrinology, 2004, 45, 1069-1074.
92. Marin, R. Signalosomes in the brain: relevance in the development of certain neuropathologies such as Alzheimer's disease. Front. Physiol., 2011, 2, 23.
93. Luoma, J.I.; Boulware, M.I.; Mermelstein, P.G. Caveolin proteins and estrogen signaling in the brain. Mol. Cell. Endocrinol., 2008, 290(1-2), 8-13.
94. De Marinis, E.; Ascenzi, P.; Pellegrini, M.; Galluzzo, P.; Bulzomi, P.; Arevalo, M.A.; Garcia-Segura, L.M.; Marino, M. 17β-estradiola new modulator of neuroglobinlevels in neurons: role in neuroprotection against H2O2-induced toxicity. Neurosignals, 2010,18(4) 223-235.
95. De Marinis, E.; Acaz-Fonseca, E.; Arevalo, M.A.; Ascenzi, P.; Fiocchetti, M.; Marino, M.; Garcia-Segura, L.M. 17β-Oestradiol anti-inflammatory effects in primary astrocytes require oestrogen receptor β-mediated neuroglobin up-regulation. J. Neuroendocrinol., 2013, 25(3), 260-270.
96. Garcia-Segura, L.M.; Diz-Chaves, Y.; Perez-Martin, M.; Darnaudery, M. Estradiol, insulin-like growth factor-I and brain aging. Psychoneuroendocrinology, 2007, 32(Suppl 1), S57-S61.
97. Garcia-Segura, L.M.; Arevalo, M.A.; Azcoitia, I. Interactions of estradiol and insulin-like growth factor-I signalling in the nervous system: new advances. Prog. Brain Res., 2010, 181, 251-272.
98. Mermelstein, P.G. Membrane-localised oestrogen receptor alpha and beta influence neuronal activity through activation of metabotropic glutamate receptors. J. Neuroendocrinol., 2009, 21(4), 257-262.
99. Micevych, P.; Christensen, A. Membrane-initiated estradiol actions mediate structural plasticity and reproduction. Front. Neuroendocrinol., 2012, 33(4), 331-341.
100. Simons, K.; Gerl, M.J. Revitalizing membrane rafts: new tools and insights. Nat. Rev. Mol. Cell. Biol., 2010, 11(10), 688-699.
101. Herrera, J.L.; Fernandez, C.; Diaz, M.; Cury, D.; Marin, R. Estradiol and tamoxifen differentially regulate a plasmalemmal voltagedependent anion channel involved in amyloid-beta induced neurotoxicity. Steroids, 2011, 76(9), 840-844.
102. Marin, R.; Marrero-Alonso, J.; Fernandez, C.; Cury, D.; Diaz, M. Estrogen receptors in lipid raft signalling complexes for neuroprotection. Front. Biosci. (Elite Ed.), 2012, 4, 1420-1433.
103. Martin, V.; Fabelo, N.; Santpere, G.; Puig, B.; Marin, R.; Ferrer, I.; Diaz, M. Lipid alterations in lipid rafts from Alzheimer's disease human brain cortex. J. Alzheimers Dis., 2010, 19(2), 489-502.
104. Soderberg, M.; Edlund, C.; Alafuzoff, I.; Kristensson, K.; Dallner, G. Lipid alterations in lipidraftsfromAlzheimer'sdisease human braincortex. J. Neurochem., 1992, 59(5), 1646-1653.
105. Thomann, P.A.; Wustenberg, T.; Nolte, H.M.; Menzel, P.B.; Wolf, R.C.; Essig, M.; Schroder, J. Hippocampal and entorhinal cortex volume decline in cognitively intact elderly. Psychiatry Res., 2013, 211(1), 31-36.
106. Plourde, M.; Fortier, M.; Vandal, M.; Tremblay-Mercier, J.; Freemantle, E.; Begin, M.; Pifferi, F.; Cunnane, S.C. Unresolved issues in the link between docosahexaenoicacid and Alzheimer's disease. Prostaglandins Leukot. Essent. Fatty Acids, 2007, 77(5-6), 301-308.
107. Fabelo, N.; Martin, V.; Marin, R.; Santpere, G.; Aso, E.; Ferrer, I.; Diaz, M.Evidence for premature lipid raft aging in APP/PS1 double-transgenic mice, a model of familial Alzheimer disease. J. Neuropathol. Exp. Neurol., 2012, 71(10), 868-881.
108. Duyckaerts, C.; Potier, M.C.; Delatour, B. An Alzheimer disease models and human neuropathology: similarities and differences. Acta Neuropathol., 2008, 115(1), 5-38. (Pubitemid 50005258)
109. Fabelo, N.; Martin, V.; Santpere, G.; Marin, R.; Torrent, L.; Ferrer, I.; Diaz, M. Severe alterations in lipid composition of frontal cortex lipid rafts from Parkinson's disease and incidental Parkinson's disease. Mol. Med., 2011, 17(9-10), 1107-1118.
110. Diaz, M.L.; Fabelo, N.; Marin, R. Genotype-induced changes in biophysical properties of frontal cortex lipid raft from APP/PS1 transgenic mice. Front. Physiol., 2012, 3, 454.
111. Chapkin, R.S.; Wang, N.; Fan, Y.Y.; Lupton, J.R.; Prior, I.A. Docosahexaenoic acid alters the size and distribution of cell surface micro domains. Biochim. Biophys. Acta, 2008, 1778(2), 466-471.
112. Marin, R.; Casañas, V.; Pérez, J.A.; Fabelo, N.; Fernandez, C.E.; Diaz, M. Oestrogens as modulators of neuronal signalosomes and brain lipid homeostasis related to protection against neurodegeneration. J. Neuroendocrinol., 2013, 25(11), 1104-1115.
113. Plourde, M.; Cunnane, S.C. Extremely limited synthesis of long chain polyunsaturates in adults: implications for their dietary essentiality and use as supplements. Appl. Physiol. Nutr. Metab., 2007, 32(4), 619-634.
114. Robson, L.G.; Dyall, S.; Sidloff, D.; Michael-Titus, A.T. Omega-3 polyunsaturated fatty acids increase the neurite outgrowth of rat sensory neurons throughout development and in aged animals. Neurobiol. Aging, 2010, 31(4), 678-687.
115. Akbar, M.; Calderon, F.; Wen, Z.; Kim, H.Y. Docosahexaenoic acid: a positive modulator of Akt signaling in neuronal survival. Proc. Natl. Acad. Sci. U.S.A., 2005, 102(31), 10858-10863.
116. Minano, A.; Xifro, X.; Perez, V.; Barneda-Zahonero, B.; Saura, C.A.; Rodriguez-Alvarez, J. Estradiol facilitates neurite maintenance by a Src/Ras/ERK signalling pathway. Mol. Cell. Neurosci., 2008, 39(2), 143-151.
117. Extier, A.; Perruchot, M.H.; Baudry, C.; Guesnet, P.; Lavialle, M.; Alessandri, J.M. Differential effects of steroids on the synthesis of polyunsaturated fatty acids by human neuroblastoma cells. Neurochem. Int., 2009, 55(5), 295-301.
118. Arendt, T.; Schindler, C.; Bruckner, M.K.; Eschrich, K.; Bigl, V.; Zedlick, D.; Marcova, L. Plastic neuronal remodeling is impaired in patients with Alzheimer's disease carrying apolipoprotein ε4 allele. J. Neurosci., 1997, 17(2), 516-529. (Pubitemid 27024565)
119. Maayan, R.; Abou-Kaud, M.; Strous, R.D.; Kaplan, B.; Fisch, B.; Shinnar, N.; Weizman, A. The influence of parturition on the level and synthesis of sulfated and free neurosteroids in rats. Neuropsychobiology, 2004, 49(1), 17-23. (Pubitemid 38134863)
120. Alessandrini, A.; Facci, P. Unraveling lipid/protein interaction in model lipid bilayers by Atomic Force Microscopy. J. Mol. Recognit., 2011, 24(3), 387-396.
121. Marin, R.; Rojo, J.A.; Fabelo, N.; Fernandez, C.E.; Diaz, M. Lipid raft disarrangement as a result of neuropathological progresses: a novel strategy for early diagnosis? Neuroscience, 2013, 245, 26-39.
122. Rossouw, J.E.; Anderson, G.L.; Prentice, R.L.; LaCroix, A.Z.; Kooperberg, C.; Stefanick, M.L.; Jackson, R.D.; Beresford, S.A.; Howard, B.V.; Johnson, K.C.; Kotchen, J.M.; Ockene, J. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results From the Women's Health Initiative randomized controlled trial. JAMA, 2002, 288(3), 321-333.
123. de Villiers, T.J.; Gass, M.L.; Haines, C.J.; Hall, J.E.; Lobo, R.A.; Pierroz, D.D.; Rees, M. Global consensus statement on menopausal hormone therapy. Climacteric, 2013, 16(2), 203-204.