Effects of estradiol on the endocytic transport of vitamin D carrier protein in hepatocytes

Biochimica et Biophysica Acta - General Subjects

Volumn 1830, Issue 6, 2013, Pages 3421-3426

  Pirani, T ^a   Chen, J ^a   Vieira, A ^a  

^a SIMON FRASER UNIVERSITY   (Canada)

Author keywords

Endocytosis; Estradiol; Fulvestrant; Hepatocytes; Nutrient carrier proteins; Vitamin D binding protein

Indexed keywords

CARRIER PROTEIN; ESTRADIOL; ESTROGEN RECEPTOR; ETHINYLESTRADIOL; FULVESTRANT; RETINOL BINDING PROTEIN; VITAMIN D BINDING PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CELL DIFFERENTIATION; COMPARATIVE STUDY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENDOCYTOSIS; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL; MALE; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

ANIMALS; CELLS, CULTURED; ENDOCYTOSIS; ESTRADIOL; ESTROGEN ANTAGONISTS; ESTROGENS; FEMALE; HEPATOCYTES; MALE; MICE; PROTEIN TRANSPORT; RETINOL-BINDING PROTEINS; SEX CHARACTERISTICS; VITAMIN D-BINDING PROTEIN;

MURINAE;

EID: 84875997912     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2013.01.025     Document Type: Article

References (82)

1. J.M. Alessandri, A. Extier, K.H. Al-Gubory, B. Langelier, C. Baudry, C. LePoupon, M. Lavialle, and P. Guesnet Ovariectomy and 17β-estradiol alter transcription of lipid metabolism genes and proportions of neo-formed n-3 and n-6 long-chain polyunsaturated fatty acids differently in brain and liver J. Nutr. Biochem. 22 2011 820 827
2. D.C. Leitman, S. Paruthiyil, O.I. Vivar, E.F. Saunier, C.B. Herber, I. Cohen, M. Tagliaferri, and T.P. Speed Regulation of specific target genes and biological responses by estrogen receptor subtype agonists Curr. Opin. Pharmacol. 10 2010 629 636
3. L.M. Garcia-Segura, D. Muller, and Y. Dunant Increase in the number of presynaptic large intramembrane particles during synaptic transmission at the Torpedo nerve-electroplaque junction Neuroscience 19 1986 63 79
4. L.M. Garcia-Segura, G. Olmos, R.J. Robbins, P. Hernandez, J.H. Meyer, and F. Naftolin Estradiol induces rapid remodelling of plasma membranes in developing rat cerebrocortical neurons in culture Brain Res. 498 1989 339 343
5. T. Watanabe, M. Akishita, T. Nakaoka, H. He, Y. Miyahara, N. Yamashita, Y. Wada, H. Aburatani, M. Yoshizumi, K. Kozaki, and Y. Ouchi Caveolin-1, Id3a and two LIM protein genes are upregulated by estrogen in vascular smooth muscle cells Life Sci. 75 2004 1219 1229
6. K.H. Kim, D. Toomre, and J.R. Bender Splice isoform estrogen receptors as integral transmembrane proteins Mol. Biol. Cell 22 2011 4415 4423
7. J.H. Park, M.Y. Lee, and H.J. Han A potential role for caveolin-1 in estradiol-17β-induced proliferation of mouse embryonic stem cells: involvement of Src, PI3K/Akt, and MAPKs pathways Int. J. Biochem. Cell Biol. 41 2011 659 665
8. R. Dominguez, and P. Micevych Estradiol rapidly regulates membrane estrogen receptor levels in hypothalamic neurons J. Neurosci. 30 2010 12589 12596
9. E.R. Levin Extranuclear steroid receptors: roles in modulation of cell functions Mol. Endocrinol. 25 2011 377 384
10. N.E. Cooke, and E.V. David Serum vitamin D-binding protein is a third member of the albumin and alpha fetoprotein gene family J. Clin. Invest. 76 1985 2420 2424
11. J.L. Hunt, and P. Licht Identification and structural characterization of a novel member of the vitamin D binding protein family Comp. Biochem. Physiol. B 121 1998 397 406
12. M. Osawa, T. Tsuji, N. Yukawa, T. Saito, and S. Takeichi Cloning and sequence analysis of cDNA encoding rabbit vitamin D-binding protein (Gc globulin) Biochem. Mol. Biol. Int. 34 1994 1003 1009
13. L. Yang, J. Liang, G. Yao, P. Chen, and Y. Hou 17Beta-estradiol regulates the numbers, endocytosis, stimulative capacity and IL-10 secretion of mouse spleen dendritic cells Toxicol. Lett. 155 2005 239 246
14. D.D. Bikle, E. Gee, B. Halloran, M.A. Kowalski, E. Ryzen, and J.G. Haddad Assessment of the free fraction of 25-hydroxyvitamin D in serum and its regulation by albumin and the vitamin D-binding protein J. Clin. Endocrinol. Metab. 63 1986 954 959
15. M. Speeckaert, G. Huang, J.R. Delanghe, and Y.E. Taes Biological and clinical aspects of the vitamin D binding protein (Gc-globulin) and its polymorphism Clin. Chim. Acta 372 2006 33 42
16. P. White, and N. Cooke The multifunctional properties and characteristics of vitamin D-binding protein Trends Endocrinol. Metab. 11 2000 320 327
17. S.J. di Martino, and R.R. Kew Initial characterization of the vitamin D binding protein (Gc-globulin) binding site on the neutrophil plasma membrane: evidence for a chondroitin sulfate proteoglycan J. Immunol. 163 1999 2135 2142
18. O.A. Gressner, B. Lahme, and A.M. Gressner Gc-globulin (vitamin D binding protein) is synthesized and secreted by hepatocytes and internalized by hepatic stellate cells through Ca(2 +)-dependent interaction with the megalin/gp330 receptor Clin. Chim. Acta 390 2008 28 37
19. L.A. McVoy, and R.R. Kew CD44 and annexin A2 mediate the C5a chemotactic cofactor function of the vitamin D binding protein J. Immunol. 175 2005 4754 4760
20. U. Meier, O. Gressner, F. Lammert, and A.M. Gressner Gc-globulin: roles in response to injury Clin. Chem. 52 2006 1247 1253
21. A. Nykjaer, J.C. Fyfe, R. Kozyraki, J.R. Leheste, C. Jacobsen, M.S. Nielsen, P.J. Verroust, M. Aminoff, A. de la Chapelle, S.K. Moestrup, R. Ray, J. Gliemann, T.E. Willnow, and E.I. Christensen Cubilin dysfunction causes abnormal metabolism of the steroid hormone 25(OH) vitamin D(3) Proc. Natl. Acad. Sci. U. S. A. 98 2001 13895 13900
22. E.I. Christensen, and H. Birn Megalin and cubilin: multifunctional endocytic receptors Nat. Rev. Mol. Cell Biol. 3 2002 256 266
23. A. Nykjaer, D. Dragun, D. Walther, H. Vorum, C. Jacobsen, J. Herz, F. Melsen, E.I. Christensen, and T.E. Willnow An endocytic pathway essential for renal uptake and activation of the steroid 25-(OH) vitamin D3 Cell 96 1999 507 515
24. D.N. D'Ambrosio, R.D. Clugston, and W.S. Blaner Vitamin A metabolism: an update Nutrients 3 2011 63 103
25. A.V. Vieira Retinoid endocrinology from metabolism to cellular signaling Subcell. Biochem. 30 1998 29 51
26. J. Huang, and A. Vieira Evidence for a specific cell membrane retinol-binding protein transport mechanism in a human keratinocyte line Int. J. Mol. Med. 17 2006 627 631
27. R. Kawaguchi, J. Yu, J. Honda, J. Hu, J. Whitelegge, P. Ping, P. Wiita, D. Bok, and H. Sun A membrane receptor for retinol binding protein mediates cellular uptake of vitamin A Science 315 2007 820 825
28. P.N. MacDonald, D. Bok, and D.E. Ong Localization of cellular retinol-binding protein and retinol-binding protein in cells comprising the blood-brain barrier of rat and human Proc. Natl. Acad. Sci. U. S. A. 87 1990 4265 4269
29. A. Mansouri, J.L. Gueant, J. Capiaumont, P. Pelosi, P. Nabet, and T. Haertle Plasma membrane receptor for beta-lactoglobulin and retinol-binding protein in murine hybridomas Biofactors 7 1998 287 298
30. C. Redondo, M. Vouropoulou, J. Evans, and J.B. Findlay Identification of the retinol-binding protein (RBP) interaction site and functional state of RBPs for the membrane receptor FASEB J. 22 2008 1043 1054
31. H. Senoo, S. Smeland, L. Malaba, T. Bjerknes, E. Stang, N. Roos, T. Berg, K.R. Norum, and R. Blomhoff Transfer of retinol-binding protein from HepG2 human hepatoma cells to cocultured rat stellate cells Proc. Natl. Acad. Sci. U. S. A. 90 1993 3616 3620
32. S. Smeland, T. Bjerknes, L. Malaba, W. Eskild, K.R. Norum, and R. Blomhoff Tissue distribution of the receptor for plasma retinol-binding protein Biochem. J. 305 1995 419 424
33. M. Sundaram, A. Sivaprasadarao, M.M. DeSousa, and J.B. Findlay The transfer of retinol from serum retinol-binding protein to cellular retinol-binding protein is mediated by a membrane receptor J. Biol. Chem. 273 1998 3336 3342
34. A. Vahlquist, and H. Torma Retinol uptake by human keratinocytes - receptor-mediated or not? J. Invest. Dermatol. 99 1992 512 514
35. A.V. Vieira, E.J. Sanders, and W.J. Schneider Transport of serum transthyretin into chicken oocytes. A receptor-mediated mechanism J. Biol. Chem. 270 1995 2952 2956
36. M. Marinó, D. Andrews, D. Brown, and R.T. McCluskey Transcytosis of retinol-binding protein across renal proximal tubule cells after megalin (gp 330)-mediated endocytosis J. Am. Soc. Nephrol. 12 2001 637 648
37. G.J. Doherty, and H.T. McMahon Mechanisms of endocytosis Annu. Rev. Biochem. 78 2009 857 902
38. T.A. Blanpied, D.B. Scott, and M.D. Ehlers Age-related regulation of dendritic endocytosis associated with altered clathrin dynamics Neurobiol. Aging 24 2003 1095 1104
39. M.T. Mizwicki, D. Menegaz, J. Zhang, A. Barrientos-Durán, S. Tse, J.R. Cashman, P.R. Griffin, and M. Fiala Genomic and nongenomic signaling induced by 1α,25(OH)2-vitamin D3 promotes the recovery of amyloid-β phagocytosis by Alzheimer's disease macrophages J. Alzheimers Dis. 29 2012 51 62
40. J.R. Cirrito, J.E. Kang, J. Lee, F.R. Stewart, D.K. Verges, L.M. Silverio, G. Bu, S. Mennerick, and D.M. Holtzman Endocytosis is required for synaptic activity-dependent release of amyloid-beta in vivo Neuron 58 2008 42 51
41. S. Treusch, S. Hamamichi, J.L. Goodman, K.E. Matlack, C.Y. Chung, V. Baru, J.M. Shulman, A. Parrado, B.J. Bevis, J.S. Valastyan, H. Han, M. Lindhagen-Persson, E.M. Reiman, D.A. Evans, D.A. Bennett, A. Olofsson, P.L. DeJager, R.E. Tanzi, K.A. Caldwell, G.A. Caldwell, and S. Lindquist Functional links between Aβ toxicity, endocytic trafficking, and Alzheimer's disease risk factors in yeast Science 334 2011 1241 1245
42. R.A. Nixon Endosome function and dysfunction in Alzheimer's disease and other neurodegenerative diseases Neurobiol. Aging 26 2005 373 382
43. M. Gutiérrez, P. Isa, C. Sánchez-San Martin, J. Pérez-Vargas, R. Espinosa, C.F. Arias, and S. López Different rotavirus strains enter MA104 cells through different endocytic pathways: the role of clathrin-mediated endocytosis J. Virol. 84 2011 9161 9169
44. E. Veiga, and P. Cossart Listeria hijacks the clathrin-dependent endocytic machinery to invade mammalian cells Nat. Cell Biol. 7 2005 894 900
45. N. Crosetto, R. Tikkanen, and I. Dikic Oncogenic breakdowns in endocytic adaptor proteins FEBS Lett. 579 2005 3231 3238
46. D.S. Rao, S.V. Bradley, P.D. Kumar, T.S. Hyun, D. Saint-Dic, K. Oravecz-Wilson, C.G. Kleer, and T.S. Ross Altered receptor trafficking in Huntingtin Interacting Protein 1-transformed cells Cancer Cell 3 2003 471 482
47. Y. Sato, K. Murase, J. Kato, M. Kobune, T. Sato, Y. Kawano, R. Takimoto, K. Takada, K. Miyanishi, T. Matsunaga, T. Takayama, and Y. Niitsu Resolution of liver cirrhosis using vitamin A-coupled liposomes to deliver siRNA against a collagen-specific chaperone Nat. Biotechnol. 26 2008 431 442
48. S.M. Hyder, C. Chiappetta, and G.M. Stancel Synthetic estrogen 17alpha-ethinyl estradiol induces pattern of uterine gene expression similar to endogenous estrogen 17beta-estradiol J. Pharmacol. Exp. Ther. 290 1999 740 747
49. R. Krattenmacher, R. Knauthe, K. Parczyk, A. Walker, U. Hilgenfeldt, and K.H. Fritzemeier Estrogen action on hepatic synthesis of angiotensinogen and IGF-I: direct and indirect estrogen effects J. Steroid Biochem. Mol. Biol. 48 1994 207 214
50. W. Marr, M.G. Elder, and L. Lim The effects of oestrogens and progesterone on oestrogen receptors in female rat liver Biochem. J. 190 1980 563 570
51. R.F. Aten, and A.J. Eisenfeld Estradiol is less potent than ethinyl estradiol for in vivo translocation of the mammalian liver estrogen receptor to the nucleus Endocrinologist 111 1982 1292 1298
52. Z. Madar, N.J. MacLusky, and F. Naftolin Estrogen stimulation of 3-o-methyl-d-glucose uptake in isolated rat hepatocytes Endocrinologist 110 1982 330 335
53. J.J. Li, X. Hou, J. Bentel, E.M. Yazlovitskaya, and S.A. Li Prevention of estrogen carcinogenesis in the hamster kidney by ethinylestradiol: some unique properties of a synthetic estrogen Carcinogenic 19 1998 471 477
54. B.K. Beyer, and M.R. Juchau Contrasting effects of estradiol-17 beta and 17 alpha-ethinyl estradiol-17 beta on cultured whole embryos J. Steroid Biochem. 29 1988 629 634
55. S.E. Wardell, J.R. Marks, and D.P. McDonnell The turnover of estrogen receptor α by the selective estrogen receptor degrader (SERD) fulvestrant is a saturable process that is not required for antagonist efficacy Biochem. Pharmacol. 82 2011 122 130
56. L. Kravchenko, A. Petrenko, I. Shanina, and B. Fuller A simple non-enzymatic method for the isolation of high yields of functional rat hepatocytes Cell Biol. Int. 26 2002 1003 1006
57. L. Yang, J. Liang, G. Yao, P. Chen, and Y. Hou 17Beta-estradiol regulates the numbers, endocytosis, stimulative capacity and IL-10 secretion of mouse spleen dendritic cells Toxicol. Lett. 155 2005 239 246
58. J.E. Morris, S.W. Potter, and G. Gaza-Bulseco Estradiol-stimulated turnover of heparan sulfate proteoglycan in mouse uterine epithelium J. Biol. Chem. 263 1988 4712 4718
59. Y.S. Oh, T.S. Lee, G.J. Cheon, I.S. Jang, H.S. Jun, and S.C. Park Modulation of insulin sensitivity and caveolin-1 expression by orchidectomy in a nonobese type 2 diabetes animal model Mol. Med. 17 2011 4 11
60. Y. Urata, Y. Ihara, H. Murata, S. Goto, T. Koji, J. Yodoi, S. Inoue, and T. Kondo 17Beta-estradiol protects against oxidative stress-induced cell death through the glutathione/glutaredoxin-dependent redox regulation of Akt in myocardiac H9c2 cells J. Biol. Chem. 281 2006 13092 13102
61. L.H. Long, D. Kirkland, J. Whitwell, and B. Halliwell Different cytotoxic and clastogenic effects of epigallocatechin gallate in various cell-culture media due to variable rates of its oxidation in the culture medium Mutat. Res. 634 2007 177 183
62. T.R. Dugas, D.W. Morel, and E.H. Harrison Novel cell culture medium for use in oxidation experiments provides insights into mechanisms of endothelial cell-mediated oxidation of LDL In Vitro Cell. Dev. Biol. Anim. 36 2000 571 577
63. J. Cheng, and A. Vieira Oxidative stress disrupts internalization and endocytic trafficking of transferrin in a human malignant keratinocyte line Cell Biochem. Biophys. 45 2006 177 184
64. F. Kano, T. Arai, M. Matsuto, H. Hayashi, M. Sato, and M. Murata Hydrogen peroxide depletes phosphatidylinositol-3-phosphate from endosomes in a p38 MAPK-dependent manner and perturbs endocytosis Biochim. Biophys. Acta 1813 2011 784 801
65. R. de Wit, M. Makkinje, J. Boonstra, A.J. Verkleij, and J.A. Post Hydrogen peroxide reversibly inhibits epidermal growth factor (EGF) receptor internalization and coincident ubiquitination of the EGF receptor and Eps15 FASEB J. 15 2001 306 308
66. L. Bonaccorsi, D. Nosi, M. Muratori, L. Formigli, G. Forti, and E. Baldi Altered endocytosis of epidermal growth factor receptor in androgen receptor positive prostate cancer cell lines J. Mol. Endocrinol. 38 2007 51 66
67. M. Nakai, J. Bouma, R. Nie, Q. Zhou, K. Carnes, D.B. Lubahn, and R.A. Hess Morphological analysis of endocytosis in efferent ductules of estrogen receptor-alpha knockout male mouse Anat. Rec. 263 2001 10 18
68. K. Kitani, and I. Zs-Nagy The effect of ethinyl-estradiol treatment on the lateral mobility of lipids and proteins in hepatocyte plasma membrane of male rats (FRAP studies on liver smears) Int. Hepatol. Commun. 5 1996 236 243
69. H.L. Lin, and P.F. Hollenberg The inactivation of cytochrome P450 3A5 by 17alpha-ethynylestradiol is cytochrome b5-dependent: metabolic activation of the ethynyl moiety leads to the formation of glutathione conjugates, a heme adduct, and covalent binding to the apoprotein J. Pharmacol. Exp. Ther. 321 2007 276 287
70. J. Rosario, E. Sutherland, L. Zaccaro, and F.R. Simon Ethinylestradiol administration selectively alters liver sinusoidal membrane lipid fluidity and protein composition Biochemistry 27 1988 3939 3946
71. R.W. Van Dyke, and K.V. Root Ethinyl estradiol decreases acidification of rat liver endocytic vesicles Hepatology 18 1993 604 613
72. M.A. Goldsmith, A.L. Jones, B.J. Underdown, and J.M. Schiff Alterations in protein transport events in rat liver after estrogen treatment Am. J. Physiol. 253 1987 G195 G200
73. Z. Nawaz, G.M. Stancel, and S.M. Hyder The pure antiestrogen ICI 182,780 inhibits progestin-induced transcription Cancer Res. 59 1999 372 376
74. S.M. Schwartz, and G.N. Wade Effects of estradiol and progesterone on food intake, body weight, and carcass adiposity in weanling rats Am. J. Physiol. 240 1981 E499 E503
75. M. Guerre-Millo, A. Leturque, M. Lavau, and J. Girard Effect of insulin on glucose transport and metabolism in isolated fat-cells of gonadal adipose tissue from mature age-matched male and female rats Biochem. J. 225 1985 343 348
76. F. Suarez, C. Rossignol, and M. Garabédian Interactive effect of estradiol and vitamin D receptor gene polymorphisms as a possible determinant of growth in male and female infants J. Clin. Endocrinol. Metab. 83 1998 3563 3568
77. R. Olivares-Navarrete, S.L. Hyzy, R.A. Chaudhri, G. Zhao, B.D. Boyan, and Z. Schwartz Sex dependent regulation of osteoblast response to implant surface properties by systemic hormones Biol. Sex Differ. 1 2010 4 (http://www.bsd- journal.com/content/1/1/4)
78. E. de Marinis, C. Martini, A. Trentalance, and V. Pallottini Sex differences in hepatic regulation of cholesterol homeostasis J. Endocrinol. 198 2008 635 643
79. C. Orikasa, and Y. Sakuma Estrogen configures sexual dimorphism in the preoptic area of C57BL/6J and ddN strains of mice J. Comp. Neurol. 518 2010 3618 3629
80. Y. Nys, R. Bouillon, H. Van Baelen, and J. Williams Ontogeny and oestradiol dependence of vitamin D-binding protein blood levels in chickens J. Endocrinol. 108 1986 81 87
81. A.V. Vieira, K. Kuchler, and W.J. Schneider Retinol in avian oogenesis: molecular properties of the carrier protein DNA Cell Biol. 14 1995 403 410
82. Y. Yao, and A. Vieira Comparative 17beta-estradiol response and lipoprotein interactions of an avian apolipoprotein Gen. Comp. Endocrinol. 127 2002 89 93