Advanced search
Publication Cover
Expert Review of Endocrinology & Metabolism Volume 7, 2012 - Issue 3
Submit an article Journal homepage
16
Views
0
CrossRef citations to date
0
Altmetric
Reviews

Hormonal modulation of cholesterol: experimental evidence and possible translational impact

Alessandro Peri Department of Clinical Physiopathology, Endocrine Unit, Center for Research, Transfer and High Education on Chronic, Inflammatory, Degenerative and Neoplastic Disorders for the Development of Novel Therapies (DENOThe), University of Florence, Florence, Italy. [email protected]
,
Susanna Benvenuti Department of Clinical Physiopathology, Endocrine Unit, Center for Research, Transfer and High Education on Chronic, Inflammatory, Degenerative and Neoplastic Disorders for the Development of Novel Therapies (DENOThe), University of Florence, Florence, Italy
,
Paola Luciani Department of Clinical Physiopathology, Endocrine Unit, Center for Research, Transfer and High Education on Chronic, Inflammatory, Degenerative and Neoplastic Disorders for the Development of Novel Therapies (DENOThe), University of Florence, Florence, Italy
&
Cristiana Deledda Department of Clinical Physiopathology, Endocrine Unit, Center for Research, Transfer and High Education on Chronic, Inflammatory, Degenerative and Neoplastic Disorders for the Development of Novel Therapies (DENOThe), University of Florence, Florence, Italy
Pages 309-318 | Published online: 10 Jan 2014

References

  • Ballard C, Gauthier S, Corbett A, Brayne C, Aarsland D, Jones E. Alzheimer's disease. Lancet 377(9770), 1019–1031 (2011).
  • Greeve I, Hermans-Borgmeyer I, Brellinger C et al. The human DIMINUTO/DWARF1 homolog seladin-1 confers resistance to Alzheimer's disease-associated neurodegeneration and oxidative stress. J. Neurosci. 20(19), 7345–7352 (2000).
  • Yanagisawa K. Cholesterol and pathological processes in Alzheimer's disease. J. Neurosci. Res. 70(3), 361–366 (2002).
  • Herman GE. Disorders of cholesterol biosynthesis: prototypic metabolic malformation syndromes. Hum. Mol. Genet. 12 (Suppl. 1), R75–R88 (2003).
  • Reiss AB, Siller KA, Rahman MM, Chan ES, Ghiso J, de Leon MJ. Cholesterol in neurologic disorders of the elderly: stroke and Alzheimer's disease. Neurobiol. Aging 25(8), 977–989 (2004).
  • Björkhem I, Meaney S. Brain cholesterol: long secret life behind a barrier. Arterioscler. Thromb. Vasc. Biol. 24(5), 806–815 (2004).
  • Arispe N, Doh M. Plasma membrane cholesterol controls the cytotoxicity of Alzheimer's disease AbetaP (1-40) and (1-42) peptides. FASEB J. 16(12), 1526–1536 (2002).
  • Yao JK, Wengenack TM, Curran GL, Poduslo JF. Reduced membrane lipids in the cortex of Alzheimer's disease transgenic mice. Neurochem. Res. 34(1), 102–108 (2009).
  • Abramov AY, Ionov M, Pavlov E, Duchen MR. Membrane cholesterol content plays a key role in the neurotoxicity of β-amyloid: implications for Alzheimer's disease. Aging Cell 10(4), 595–603 (2011).
  • Crameri A, Biondi E, Kuehnle K et al. The role of seladin-1/DHCR24 in cholesterol biosynthesis, APP processing and Abeta generation in vivo. EMBO J. 25(2), 432–443 (2006).
  • Abad-Rodriguez J, Ledesma MD, Craessaerts K et al. Neuronal membrane cholesterol loss enhances amyloid peptide generation. J. Cell Biol. 167(5), 953–960 (2004).
  • Behl C. Estrogen can protect neurons: modes of action. J. Steroid Biochem. Mol. Biol. 83(1–5), 195–197 (2002).
  • Maggi A, Ciana P, Belcredito S, Vegeto E. Estrogens in the nervous system: mechanisms and nonreproductive functions. Annu. Rev. Physiol. 66, 291–313 (2004).
  • Turgeon JL, Carr MC, Maki PM, Mendelsohn ME, Wise PM. Complex actions of sex steroids in adipose tissue, the cardiovascular system, and brain: insights from basic science and clinical studies. Endocr. Rev. 27(6), 575–605 (2006).
  • Baulieu EE. Neurosteroids: a novel function of the brain. Psychoneuroendocrinology 23(8), 963–987 (1998).
  • Benarroch EE. Neurosteroids: endogenous modulators of neuronal excitability and plasticity. Neurology 68(12), 945–947 (2007).
  • Paganini-Hill A, Henderson VW. Estrogen deficiency and risk of Alzheimer's disease in women. Am. J. Epidemiol. 140(3), 256–261 (1994).
  • Pike CJ, Carroll JC, Rosario ER, Barron AM. Protective actions of sex steroid hormones in Alzheimer's disease. Front. Neuroendocrinol. 30(2), 239–258 (2009).
  • Fillit HM. The role of hormone replacement therapy in the prevention of Alzheimer disease. Arch. Intern. Med. 162(17), 1934–1942 (2002).
  • Shumaker SA, Legault C, Rapp SR et al.; WHIMS Investigators. Estrogen plus progestin and the incidence of dementia and mild cognitive impairment in postmenopausal women: the Women's Health Initiative Memory Study: a randomized controlled trial. JAMA 289(20), 2651–2662 (2003).
  • Rapp SR, Espeland MA, Shumaker SA et al.; WHIMS Investigators. Effect of estrogen plus progestin on global cognitive function in postmenopausal women: the Women's Health Initiative Memory Study: a randomized controlled trial. JAMA 289(20), 2663–2672 (2003).
  • Zhang QG, Han D, Wang RM et al. C terminus of Hsc70-interacting protein (CHIP)-mediated degradation of hippocampal estrogen receptor-alpha and the critical period hypothesis of estrogen neuroprotection. Proc. Natl Acad. Sci. USA 108(35), E617–E624 (2011).
  • MacLusky NJ. Estrogen and Alzheimer's disease: the apolipoprotein connection. Endocrinology 145(7), 3062–3064 (2004).
  • Zandi PP, Carlson MC, Plassman BLet al.; Cache County Memory Study Investigators. Hormone replacement therapy and incidence of Alzheimer disease in older women: the Cache County Study. JAMA 288(17), 2123–2129 (2002).
  • Schumacher M, Guennoun R, Ghoumari A et al. Novel perspectives for progesterone in hormone replacement therapy, with special reference to the nervous system. Endocr. Rev. 28(4), 387–439 (2007).
  • Hu XY, Qin S, Lu YP, Ravid R, Swaab DF, Zhou JN. Decreased estrogen receptor-alpha expression in hippocampal neurons in relation to hyperphosphorylated tau in Alzheimer patients. Acta Neuropathol. 106(3), 213–220 (2003).
  • Marin R, Guerra B, Hernández-Jiménez JG et al. Estradiol prevents amyloid-beta peptide-induced cell death in a cholinergic cell line via modulation of a classical estrogen receptor. Neuroscience 121(4), 917–926 (2009).
  • Carbonaro V, Caraci F, Giuffrida ML et al. Enhanced expression of ERalpha in astrocytes modifies the response of cortical neurons to beta-amyloid toxicity. Neurobiol. Dis. 33(3), 415–421 (2009).
  • Wang L, Andersson S, Warner M, Gustafsson JA. Morphological abnormalities in the brains of estrogen receptor beta knockout mice. Proc. Natl Acad. Sci. USA 98(5), 2792–2796 (2001).
  • Hawkins MB, Thornton JW, Crews D, Skipper JK, Dotte A, Thomas P. Identification of a third distinct estrogen receptor and reclassification of estrogen receptors in teleosts. Proc. Natl Acad. Sci. USA 97(20), 10751–10756 (2000).
  • Toran-Allerand CD. Minireview: a plethora of estrogen receptors in the brain: where will it end? Endocrinology 145(3), 1069–1074 (2004).
  • Vasudevan N, Pfaff DW. Membrane-initiated actions of estrogens in neuroendocrinology: emerging principles. Endocr. Rev. 28(1), 1–19 (2007).
  • Arbogast LA. Estrogen genomic and membrane actions at an intersection. Trends Endocrinol. Metab. 19(1), 1–2 (2008).
  • Dhandapani KM, Brann DW. Protective effects of estrogen and selective estrogen receptor modulators in the brain. Biol. Reprod. 67(5), 1379–1385 (2002).
  • O'Neill K, Chen S, Brinton RD. Impact of the selective estrogen receptor modulator, raloxifene, on neuronal survival and outgrowth following toxic insults associated with aging and Alzheimer's disease. Exp. Neurol. 185(1), 63–80 (2004).
  • O'Neill K, Chen S, Diaz Brinton R. Impact of the selective estrogen receptor modulator, tamoxifen, on neuronal outgrowth and survival following toxic insults associated with aging and Alzheimer's disease. Exp. Neurol. 188(2), 268–278 (2004).
  • Dong Y, Zhang H, Gao AC, Marshall JR, Ip C. Androgen receptor signaling intensity is a key factor in determining the sensitivity of prostate cancer cells to selenium inhibition of growth and cancer-specific biomarkers. Mol. Cancer Ther. 4(7), 1047–1055 (2005).
  • Yaffe K, Krueger K, Cummings SR et al. Effect of raloxifene on prevention of dementia and cognitive impairment in older women: the Multiple Outcomes of Raloxifene Evaluation (MORE) randomized trial. Am. J. Psychiatry 162(4), 683–690 (2005).
  • Selkoe DJ. Alzheimer's disease: genes, proteins, and therapy. Physiol. Rev. 81(2), 741–766 (2001).
  • Iivonen S, Hiltunen M, Alafuzoff I et al. Seladin-1 transcription is linked to neuronal degeneration in Alzheimer's disease. Neuroscience 113(2), 301–310 (2002).
  • Sarkar D, Imai T, Kambe F et al. The human homolog of Diminuto/Dwarf1 gene (hDiminuto): a novel ACTH-responsive gene overexpressed in benign cortisol-producing adrenocortical adenomas. J. Clin. Endocrinol. Metab. 86(11), 5130–5137 (2001).
  • Luciani P, Ferruzzi P, Arnaldi G et al. Expression of the novel adrenocorticotropin-responsive gene selective Alzheimer's disease indicator-1 in the normal adrenal cortex and in adrenocortical adenomas and carcinomas. J. Clin. Endocrinol. Metab. 89(3), 1332–1339 (2004).
  • Battista MC, Roberge C, Otis M, Gallo-Payet N. Seladin-1 expression in rat adrenal gland: effect of adrenocorticotropic hormone treatment. J. Endocrinol. 192(1), 53–66 (2007).
  • Luciani P, Gelmini S, Ferrante E et al. Expression of the antiapoptotic gene seladin-1 and octreotide-induced apoptosis in growth hormone-secreting and nonfunctioning pituitary adenomas. J. Clin. Endocrinol. Metab. 90(11), 6156–6161 (2005).
  • Fuller PJ, Alexiadis M, Jobling T, McNeilage J. Seladin-1/DHCR24 expression in normal ovary, ovarian epithelial and granulosa tumours. Clin. Endocrinol. 63(1), 111–115 (2005).
  • Du B, Ohmichi M, Takahashi K et al. Both estrogen and raloxifene protect against beta-amyloid-induced neurotoxicity in estrogen receptor alpha-transfected PC12 cells by activation of telomerase activity via Akt cascade. J. Endocrinol. 183(3), 605–615 (2004).
  • Hendriksen PJ, Dits NF, Kokame K et al. Evolution of the androgen receptor pathway during progression of prostate cancer. Cancer Res. 66(10), 5012–5020 (2006).
  • Biancolella M, Valentini A, Minella D et al. Effects of dutasteride on the expression of genes related to androgen metabolism and related pathway in human prostate cancer cell lines. Invest. New Drugs 25(5), 491–497 (2007).
  • Bonaccorsi L, Luciani P, Nesi G et al. Androgen receptor regulation of the seladin-1/DHCR24 gene: altered expression in prostate cancer. Lab. Invest. 88(10), 1049–1056 (2008).
  • Di Stasi D, Vallacchi V, Campi V et al. DHCR24 gene expression is upregulated in melanoma metastases and associated to resistance to oxidative stress-induced apoptosis. Int. J. Cancer 115(2), 224–230 (2005).
  • Lu X, Kambe F, Cao X et al. DHCR24 is a hydrogen peroxide scavenger, protecting cells from oxidative-stress-induced apoptosis. Endocrinology 149, 3267–3273 (2008).
  • Wu C, Miloslavskaya I, Demontis S, Maestro R, Galaktionov K. Regulation of cellular response to oncogenic and oxidative stress by seladin-1. Nature 432(7017), 640–645 (2004).
  • Kuehnle K, Crameri A, Kälin RE et al. Prosurvival effect of DHCR24/seladin-1 in acute and chronic responses to oxidative stress. Mol. Cell. Biol. 28(2), 539–550 (2008).
  • FitzPatrick DR, Keeling JW, Evans MJ et al. Clinical phenotype of desmosterolosis. Am. J. Med. Genet. 75(2), 145–152 (1998).
  • Waterham HR, Koster J, Romeijn GJ et al. Mutations in the 3beta-hydroxysterol Delta24-reductase gene cause desmosterolosis, an autosomal recessive disorder of cholesterol biosynthesis. Am. J. Hum. Genet. 69(4), 685–694 (2001).
  • Wechsler A, Brafman A, Shafir M et al. Generation of viable cholesterol-free mice. Science 302(5653), 2087 (2003).
  • Mirza R, Hayasaka S, Takagishi Y et al. DHCR24 gene knockout mice demonstrate lethal dermopathy with differentiation and maturation defects in the epidermis. J. Invest. Dermatol. 126(3), 638–647 (2006).
  • Mirza R, Hayasaka S, Kambe F et al. Increased expression of aquaporin-3 in the epidermis of DHCR24 knockout mice. Br. J. Dermatol. 158(4), 679–684 (2008).
  • Vannelli GB, Ensoli F, Zonefrati R et al. Neuroblast long-term cell cultures from human fetal olfactory epithelium respond to odors. J. Neurosci. 15(6), 4382–4394 (1995).
  • Barni T, Maggi M, Fantoni G et al. Sex steroids and odorants modulate gonadotropin-releasing hormone secretion in primary cultures of human olfactory cells. J. Clin. Endocrinol. Metab. 84(11), 4266–4273 (1999).
  • Benvenuti S, Luciani P, Vannelli GB et al. Estrogen and selective estrogen receptor modulators exert neuroprotective effects and stimulate the expression of selective Alzheimer's disease indicator-1, a recently discovered antiapoptotic gene, in human neuroblast long-term cell cultures. J. Clin. Endocrinol. Metab. 90(3), 1775–1782 (2005).
  • Luciani P, Deledda C, Rosati F et al. Seladin-1 is a fundamental mediator of the neuroprotective effects of estrogen in human neuroblast long-term cell cultures. Endocrinology 149(9), 4256–4266 (2008).
  • Lóránd T, Vigh E, Garai J. Hormonal action of plant derived and anthropogenic non-steroidal estrogenic compounds: phytoestrogens and xenoestrogens. Curr. Med. Chem. 17(30), 3542–3574 (2010).
  • Setchell KD. Soy isoflavones – benefits and risks from nature's selective estrogen receptor modulators (SERMs). J. Am. Coll. Nutr. 20(5 Suppl.), 354S–362S; discussion 381S (2001).
  • Matthews CC, Feldman EL. Insulin-like growth factor I rescues SH-SY5Y human neuroblastoma cells from hyperosmotic induced programmed cell death. J. Cell. Physiol. 166(2), 323–331 (1996).
  • Russo VC, Kobayashi K, Najdovska S, Baker NL, Werther GA. Neuronal protection from glucose deprivation via modulation of glucose transport and inhibition of apoptosis: a role for the insulin-like growth factor system. Brain Res. 1009(1–2), 40–53 (2004).
  • Russo VC, Gluckman PD, Feldman EL, Werther GA. The insulin-like growth factor system and its pleiotropic functions in brain. Endocr. Rev. 26(7), 916–943 (2005).
  • Mendez P, Azcoitia I, Garcia-Segura LM. Interdependence of oestrogen and insulin-like growth factor-I in the brain: potential for analysing neuroprotective mechanisms. J. Endocrinol. 185(1), 11–17 (2005).
  • Zou CG, Cao XZ, Zhao YS et al. The molecular mechanism of endoplasmic reticulum stress-induced apoptosis in PC-12 neuronal cells: the protective effect of insulin-like growth factor I. Endocrinology 150(1), 277–285 (2009).
  • Garcia-Segura LM, Arévalo MA, Azcoitia I. Interactions of estradiol and insulin-like growth factor-I signalling in the nervous system: new advances. Prog. Brain Res. 181, 251–272 (2010).
  • Znamensky V, Akama KT, McEwen BS, Milner TA. Estrogen levels regulate the subcellular distribution of phosphorylated Akt in hippocampal CA1 dendrites. J. Neurosci. 23(6), 2340–2347 (2003).
  • Datta SR, Dudek H, Tao X et al. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91(2), 231–241 (1997).
  • del Peso L, González-García M, Page C, Herrera R, Nuñez G. Interleukin-3-induced phosphorylation of BAD through the protein kinase Akt. Science 278(5338), 687–689 (1997).
  • Ma ZQ, Santagati S, Patrone C, Pollio G, Vegeto E, Maggi A. Insulin-like growth factors activate estrogen receptor to control the growth and differentiation of the human neuroblastoma cell line SK-ER3. Mol. Endocrinol. 8(7), 910–918 (1994).
  • Patrone C, Gianazza E, Santagati S, Agrati P, Maggi A. Divergent pathways regulate ligand-independent activation of ER alpha in SK-N-BE neuroblastoma and COS-1 renal carcinoma cells. Mol. Endocrinol. 12(6), 835–841 (1998).
  • Font de Mora J, Brown M. AIB1 is a conduit for kinase-mediated growth factor signaling to the estrogen receptor. Mol. Cell Biol. 20, 5041–5047 (2000).
  • Frago LM, Pañeda C, Dickson SL, Hewson AK, Argente J, Chowen JA. Growth hormone (GH) and GH-releasing peptide-6 increase brain insulin-like growth factor-I expression and activate intracellular signaling pathways involved in neuroprotection. Endocrinology 143(10), 4113–4122 (2002).
  • Mendez P, Garcia-Segura LM. Phosphatidylinositol 3-kinase and glycogen synthase kinase 3 regulate estrogen receptor-mediated transcription in neuronal cells. Endocrinology 147(6), 3027–3039 (2006).
  • Giannini S, Benvenuti S, Luciani P et al. Intermittent high glucose concentrations reduce neuronal precursor survival by altering the IGF system: the involvement of the neuroprotective factor DHCR24 (seladin-1). J. Endocrinol. 198(3), 523–532 (2008).
  • Ning Y, Chen S, Li X, Ma Y, Zhao F, Yin L. Cholesterol, LDL, and 25-hydroxycholesterol regulate expression of the steroidogenic acute regulatory protein in microvascular endothelial cell line (bEnd.3). Biochem. Biophys. Res. Commun. 342(4), 1249–1256 (2006).
  • Reyland ME, Evans RM, White EK. Lipoproteins regulate expression of the steroidogenic acute regulatory protein (StAR) in mouse adrenocortical cells. J. Biol. Chem. 275(47), 36637–36644 (2000).
  • Veiga S, Melcangi RC, Doncarlos LL, Garcia-Segura LM, Azcoitia I. Sex hormones and brain aging. Exp. Gerontol. 39(11–12), 1623–1631 (2004).
  • Lavaque E, Sierra A, Azcoitia I, Garcia-Segura LM. Steroidogenic acute regulatory protein in the brain. Neuroscience 138(3), 741–747 (2006).
  • Patisaul HB. Phytoestrogen action in the adult and developing brain. J. Neuroendocrinol. 17(1), 57–64 (2005).
  • Wang CN, Chi CW, Lin YL, Chen CF, Shiao YJ. The neuroprotective effects of phytoestrogens on amyloid beta protein-induced toxicity are mediated by abrogating the activation of caspase cascade in rat cortical neurons. J. Biol. Chem. 276(7), 5287–5295 (2001).
  • Obermayr RP, Mayerhofer L, Knechtelsdorfer M et al. The age-related down-regulation of the growth hormone/insulin-like growth factor-1 axis in the elderly male is reversed considerably by donepezil, a drug for Alzheimer's disease. Exp. Gerontol. 40(3), 157–163 (2005).
  • Tei E, Yamamoto H, Watanabe T et al. Use of serum insulin-like growth factor-I levels to predict psychiatric non-response to donepezil in patients with Alzheimer's disease. Growth Horm. IGF Res. 18(1), 47–54 (2008).
  • Peri A, Benvenuti S, Luciani P, Deledda C, Cellai I. Membrane cholesterol as a mediator of the neuroprotective effects of estrogens. Neuroscience 191, 107–117 (2011).

Websites

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Order Reprints Request Corporate Permissions

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

Request Academic Permissions

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.