Cell surface estrogen receptor alpha is upregulated during subchronic metabolic stress and inhibits neuronal cell degeneration

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Barbati, Cristiana ^a,b   Pierdominici, Marina ^b   Gambardella, Lucrezia ^b   Malchiodi Albedi, Fiorella ^b   Karas, Richard H ^c   Rosano, Giuseppe ^d   Malorni, Walter ^a,b   Ortona, Elena ^a,b  

^a San Raffaele Institute Sulmona   (Italy)

^b ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^c TUFTS MEDICAL CENTER   (United States)

^d IRCCS SAN RAFFAELE PISANA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANT; BOVINE SERUM ALBUMIN; CHAPERONE; CYTIDINE PHOSPHATE; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR ALPHA ANTAGONIST; ESTROGEN RECEPTOR BETA; LIGAND; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PEROXIDE; RECEPTOR BLOCKING AGENT; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL DEATH; CELL FATE; CELL STRESS; CELL SURFACE; CELL SURVIVAL; CHRONIC STRESS; CONTROLLED STUDY; CYTOSKELETON; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; METABOLIC STRESS; MICROFILAMENT; MOUSE; NERVE CELL DEGENERATION; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; PATHOPHYSIOLOGY; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TRANSPORT; RECEPTOR UPREGULATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; UPREGULATION;

APOPTOSIS; AUTOPHAGY; CELL LINE; CELL LINEAGE; CELL MEMBRANE; CELL SURVIVAL; ESTROGEN RECEPTOR ALPHA; GENE KNOCKDOWN TECHNIQUES; HUMANS; NEURONS; STRESS, PHYSIOLOGICAL; UP-REGULATION;

BOVINAE;

EID: 84864480763     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042339     Document Type: Article

References (46)

1. Carrer HF, Cambiasso MJ, Gorosito S, (2005) Effects of estrogen on neuronal growth and differentiation. J Steroid Biochem Mol Biol 93: 319-323.
2. Gillies GE, McArthur S, (2010) Estrogen actions in the brain and the basis for differential action in men and women: a case for sex-specific medicines. Pharmacol Rev 62: 155-198.
3. Srivastava DP, Waters EM, Mermelstein PG, Kramar EA, Shors TJ, et al. (2011) Rapid estrogen signaling in the brain: implications for the fine-tuning of neuronal circuitry. J Neurosci 31: 16056-16063.
4. Ascenzi P, Bocedi A, Marino M, (2006) Structure-function relationship of estrogen receptor alpha and beta: impact on human health. Mol Aspects Med 27: 299-402.
5. Levin ER, (2009) Plasma membrane estrogen receptors. Trends Endocrinol Metab 20: 477-482.
6. Vasudevan N, Pfaff DW, (2008) Non-genomic actions of estrogens and their interaction with genomic actions in the brain. Front Neuroendocrinol 29: 238-257.
7. Wu Q, Chambliss K, Umetani M, Mineo C, Shaul PW, (2011) Non-nuclear estrogen receptor signaling in the endothelium. J Biol Chem 286: 14737-14743.
8. Madak-Erdogan Z, Kieser KJ, Kim SH, Komm B, Katzenellenbogen JA, et al. (2008) Nuclear and extranuclear pathway inputs in the regulation of global gene expression by estrogen receptors. Mol Endocrinol 22: 2116-2127.
9. Wu TW, Wang JM, Chen S, Brinton RD, (2005) 17Beta-estradiol induced Ca2+ influx via L-type calcium channels activates the Src/ERK/cyclic-AMP response element binding protein signal pathway and BCL-2 expression in rat hippocampal neurons: a potential initiation mechanism for estrogen-induced neuroprotection. Neuroscience 135: 59-72.
10. Zhao L, Brinton RD, (2007) Estrogen receptor alpha and beta differentially regulate intracellular Ca(2+) dynamics leading to ERK phosphorylation and estrogen neuroprotection in hippocampal neurons. Brain Res 1172: 48-59.
11. Alkayed NJ, Goto S, Sugo N, Joh HD, Klaus J, et al. (2001) Estrogen and Bcl-2: gene induction and effect of transgene in experimental stroke. J Neurosci 21: 7543-7550.
12. Yang LC, Zhang QG, Zhou CF, Yang F, Zhang YD, et al. (2010) Extranuclear estrogen receptors mediate the neuroprotective effects of estrogen in the rat hippocampus. PLoS One 5: e9851.
13. Acconcia F, Totta P, Ogawa S, Cardillo I, Inoue S, et al. (2005) Survival versus apoptotic 17beta-estradiol effect: role of ER alpha and ER beta activated non-genomic signaling. J Cell Physiol 203: 193-201.
14. Mendoza RA, Enriquez MI, Mejia SM, Moody EE, Thordarson G, (2011) Interactions between IGF-I, estrogen receptor-alpha (ERalpha), and ERbeta in regulating growth/apoptosis of MCF-7 human breast cancer cells. J Endocrinol 208: 1-9.
15. Klionsky DJ, (2007) Autophagy: from phenomenology to molecular understanding in less than a decade. Nat Rev Mol Cell Biol 8: 931-937.
16. Levine B, Kroemer G, (2008) Autophagy in the pathogenesis of disease. Cell 132: 27-42.
17. Mizushima N, (2007) Autophagy: process and function. Genes Dev 21: 2861-2873.
18. Mizushima N, Klionsky DJ, (2007) Protein turnover via autophagy: implications for metabolism. Annu Rev Nutr 27: 19-40.
19. Rubinsztein DC, (2006) The roles of intracellular protein-degradation pathways in neurodegeneration. Nature 443: 780-786.
20. Corcelle E, Djerbi N, Mari M, Nebout M, Fiorini C, et al. (2007) Control of the autophagy maturation step by the MAPK ERK and p38: lessons from environmental carcinogens. Autophagy 3: 57-59.
21. Brann DW, Dhandapani K, Wakade C, Mahesh VB, Khan MM, (2007) Neurotrophic and neuroprotective actions of estrogen: basic mechanisms and clinical implications. Steroids 72: 381-405.
22. Chadwick W, Zhou Y, Park SS, Wang L, Mitchell N, et al. (2010) Minimal peroxide exposure of neuronal cells induces multifaceted adaptive responses. PLoS One 5: e14352.
23. Gorosito SV, Lorenzo AG, Cambiasso MJ, (2008) Estrogen receptor alpha is expressed on the cell-surface of embryonic hypothalamic neurons. Neuroscience 154: 1173-1177.
24. Mendelsohn ME, Karas RH, (2010) Rapid progress for non-nuclear estrogen receptor signaling. J Clin Invest 120: 2277-2279.
25. Pierdominici M, Maselli A, Colasanti T, Giammarioli AM, Delunardo F, et al. (2010) Estrogen receptor profiles in human peripheral blood lymphocytes. Immunol Lett 132: 79-85.
26. Russell KS, Haynes MP, Sinha D, Clerisme E, Bender JR, (2000) Human vascular endothelial cells contain membrane binding sites for estradiol, which mediate rapid intracellular signaling. Proc Natl Acad Sci U S A 97: 5930-5935.
27. Burgunder JM, Varriale A, Lauterburg BH, (1989) Effect of N-acetylcysteine on plasma cysteine and glutathione following paracetamol administration. Eur J Clin Pharmacol 36: 127-131.
28. Sanchez AM, Simoncini T, (2010) Extra-nuclear signaling of ERalpha to the actin cytoskeleton in the central nervous system. Steroids 75: 528-532.
29. Dehmelt L, Halpain S, (2005) The MAP2/Tau family of microtubule-associated proteins. Genome Biol 6: 204.
30. Bodart JF Extracellular-regulated kinase-mitogen-activated protein kinase cascade: unsolved issues. J Cell Biochem 109: 850-857.
31. Zarubin T, Han J, (2005) Activation and signaling of the p38 MAP kinase pathway. Cell Res 15: 11-18.
32. Marino G, Madeo F, Kroemer G, (2011) Autophagy for tissue homeostasis and neuroprotection. Curr Opin Cell Biol 23: 198-206.
33. Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, et al. (2008) Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 4: 151-175.
34. Seglen PO, Gordon PB, (1982) 3-Methyladenine: specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc Natl Acad Sci U S A 79: 1889-92.
35. Ohtani-Kaneko R, Iwafuchi M, Iwakura T, Muraoka D, Yokosuka M, et al. (2010) Effects of estrogen on synapsin I distribution in developing hypothalamic neurons. Neurosci Res 66: 180-188.
36. O'Neill EE, Blewett AR, Loria PM, Greene GL, (2008) Modulation of alphaCaMKII signaling by rapid ERalpha action. Brain Res 1222: 1-17.
37. Camacho-Arroyo I, Gonzalez-Arenas A, Espinosa-Raya J, Pina-Medina AG, Picazo O, (2011) Short- and long-term treatment with estradiol or progesterone modifies the expression of GFAP, MAP2 and Tau in prefrontal cortex and hippocampus. Life Sci 89: 123-128.
38. Cesca F, Baldelli P, Valtorta F, Benfenati F, (2010) The synapsins: key actors of synapse function and plasticity. Prog Neurobiol 91: 313-348.
39. Larsen KE, Sulzer D, (2002) Autophagy in neurons: a review. Histol Histopathol 17: 897-908.
40. Lista P, Straface E, Brunelleschi S, Franconi F, Malorni W, (2011) On the role of autophagy in human diseases: a gender perspective. J Cell Mol Med 15: 1443-1457.
41. Wang X, Michaelis EK, (2010) Selective neuronal vulnerability to oxidative stress in the brain. Front Aging Neurosci 2: 12.
42. Brewer GJ, Cotman CW, (1989) Survival and growth of hippocampal neurons in defined medium at low density: advantages of a sandwich culture technique or low oxygen. Brain Res 494: 65-74.
43. Malchiodi-Albedi F, Domenici MR, Paradisi S, Bernardo A, Ajmone-Cat MA, et al. (2001) Astrocytes contribute to neuronal impairment in beta A toxicity increasing apoptosis in rat hippocampal neurons. Glia 34: 68-72.
44. Vacirca D, Delunardo F, Matarrese P, Colasanti T, Margutti P, et al. (2012) Autoantibodies to the adenosine triphosphate synthase play a pathogenetic role in Alzheimer's disease. Neurobiol Aging 33: 753-766.
45. Colasanti T, Maselli A, Conti F, Sanchez M, Alessandri C, et al. (2012) Autoantibodies to estrogen receptor alpha interfere with T lymphocyte homeostasis and are associated with disease activity in systemic lupus erythematosus. Arthritis Rheum 64: 778-787.
46. Young IT, (1977) Proof without prejudice: use of the Kolmogorov-Smirnov test for the analysis of histograms from flow systems and other sources. J Histochem Cytochem 25: 935-941.