Estrogen regulation of proteins in the rat ventromedial nucleus of the hypothalamus

Journal of Proteome Research

Volumn 7, Issue 11, 2008, Pages 5040-5048

  Mo, Bing ^a   Callegari, Eduardo ^b   Telefont, Martin ^a   Renner, Kenneth J ^a  

^a UNIVERSITY OF SOUTH DAKOTA   (United States)

^b UNIVERSITY OF SOUTH DAKOTA   (United States)

Author keywords

Estradiol; Rat; Ventromedial hypothalamus

Indexed keywords

ESTRADIOL; MEMBRANE PROTEIN; PROGESTERONE; SESAME SEED OIL; VESICULAR TRANSPORT PROTEIN; ESTROGEN; PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROSPRAY MASS SPECTROMETRY; ESTROGEN ACTIVITY; FEMALE; HORMONAL REGULATION; HYPOTHALAMUS VENTROMEDIAL NUCLEUS; NERVE CELL PLASTICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; OVARIECTOMY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RAT; REVERSED PHASE LIQUID CHROMATOGRAPHY; SEXUAL BEHAVIOR; SIGNAL TRANSDUCTION; TWO DIMENSIONAL GEL ELECTROPHORESIS; ANIMAL; BIOLOGICAL PHENOMENA AND FUNCTIONS CONCERNING THE ENTIRE ORGANISM; CHEMISTRY; DRUG EFFECT; GENE EXPRESSION REGULATION; METABOLISM; METHODOLOGY; PROTEOMICS; RANDOMIZATION; SPRAGUE DAWLEY RAT;

RATTUS;

ANIMALS; BIOLOGICAL PROCESSES; ESTRADIOL; ESTROGENS; FEMALE; GENE EXPRESSION REGULATION; OVARIECTOMY; PROTEINS; PROTEOMICS; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; VENTROMEDIAL HYPOTHALAMIC NUCLEUS;

EID: 58149375915     PISSN: 15353893     EISSN: None     Source Type: Journal    
DOI: 10.1021/pr8005974     Document Type: Article

References (80)

1. Pfaff, D. W.; Lewis, C. Film analysis of lordosis in female rats. Horm. Behav. 1974, 5, 317-335.
2. Sodersten, P. Estradiol-progesterone interactions in the reproductive behavior of female rats. In Current Topics in Neuroendocrinology, Vol. 5; Ganten, D., Pfaff, D., Eds.; Springer-Verlag: Berlin, 1985.
3. Pfaff, D. W.; Schwartz-Giblin, S.; McCarthy, M. M.; Kow, L. M. Cellular and molecular mechanisms of female reproductive behaviors. In Physiology and Reproduction; Knobil, E.; Neill, J. D., Eds.; Raven Press: New York, 1994.
4. Pfaff, D. W.; Keiner, M. Atlas of estradiol concentrating cells in the central nervous system of the female rat. J. Comp. Neurol. 1973, 151, 121-158.
5. Rubin, B. S.; Barfield, R. J. Induction of estrous behavior in ovariectomized rats by sequential replacement of estrogen and progesterone into the ventromedial hypothalamus. Neuroendo-crinology 1983, 37, 218-224.
6. Meisel, R. L.; Dohanich, G. P.; McEwen, B. S.; Pfaff, D. W. Antagonism of sexual behavior in female rats by ventromedial hypothalamic implants of antiestrogen. Neuroendocrinology 1987, 45, 201-207.
7. Elliston, J. F.; Fawell, S. E.; klein.Hitpass, L.; Tsai, S. Y.; Tsai, M.-J.; Parker, M. G.; O'Malley, B. W. Mechanism of estrogen receptor-dependent transcription in a cell-free system. MoL Cell Biol. 1991, 10, 6607-6612.
8. Beato, M.; Herrlich, P.; Schutz, G. Steroid hormone receptors: many actors in search of a plot. Cell 1995, 83, 851-857.
9. Pfaff, D. W. Mechanisms of estrogenic effects on neurobiological functions. Ernst Schering Res. Found. Workshop 2004, 46, 79-88.
10. Mong, J. A.; Pfaff, D. W. Hormonal symphony: steroid orchestration of gene modules for sociosexual behaviors. MoL Psychiatry 2004, 9, 550-556.
11. Gygi, S. P.; Rochon, Y.; Franza, B. R.; Aebersold, R. Correlation between protein and mRNA abundance in yeast. MoL Cell. Biol. 1999, 19, 1720-1730.
12. Lubec, G.; Krapfenbauer, K.; Fountoulakis, M. Proteomics in brain research: potentials and limitations. Prog. Neurobiol. 2003, 69,193- 211.
13. Palkovits, M.; Brownstein, M. J. Maps and Guide to Microdissection of the Rat Brain J Elsevier: New York, 1988.
14. Mo, B.; Callegari, E.; Telefont, M.; Renner, K. J. Proteomic analysis of the ventromedial nucleus of the hypothalamus (pars lateralis) in the female rat. Proteomics 2006, 6, 6066-6074.
15. Davidson, J. M.; Smith, E. R.; Rodgers, C. H.; Bloch, G. J. Relative thresholds of behavioral and somatic responses to estrogen. Physiol. Behav. 1968, 3, 351-353.
16. Hardy, D. F.; DeBold, J. F. The relationship between levels of exogenous hormonesand the display of lordosis by the female rat. Horm. Behav. 1971, 2, 287-297.
17. Fanner, C. J.; Isakson, T. R.; Coy, D. J.; Renner, K. J. In vivo evidence for progesterone dependent decreases in serotonin release in the hypothalamus and midbrain central grey: relation to the induction of lordosis. Brain Res. 1996, 711, 84-92.
18. Bradford, M. M. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72, 248-254.
19. Olazabal, U. E.; Pfaff, D. W.; Mobbs, C. V. Sex differences in the regulation of heat shock protein 70 kDa and 90 kDa in the rat ventromedial hypothalamus by estrogen. Brain Res. 1992, 596, 311-314.
20. Olazabal, U. E.; Pfaff, D. W.; Mobbs, C. V. Estrogenic regulation of heat shock protein 90 kDa in the rat ventromedial hypothalamus and uterus. Mol. Cell. Endocrinol. 1992, 84, 175-183.
21. Sakisaka, T.; Meerlo, T.; Matteson, J.; Plutner, H.; Balch, W. E. Rab.alphaGDI activity is regulated by a Hsp90 chaperone complex. EMBO J. 2002, 21, 6125-6135.
22. Chen, C. Y.; Balch, W. E. The Hsp90 chaperone complex regulates GDI-dependent Rab recycling. MoL Biol. Cell 2006, 17, 3494-3507.
23. Chamberlain, L. H.; Burgoyne, R. D. Cysteine-string protein: the chaperone at the synapse. J. Neurochem. 2000, 74, 1781-1789.
24. Sudhof, T. The synaptic vesicle cycle. Annu. Rev. Neurosci. 2004, 27, 509-547.
25. Geppert, M.; Goda, Y.; Stevens, C. F.; Sudhof, T. C. The small GTP-binding protein Rab3A regulates a late step in synaptic vesicle fusion. Nature 1997, 387, 810-814.
26. Raptis, A.; Torrejon-Escribano, B.; Gomez de Aranda, I.; Blasi, J. Distribution of synaptobrevin/VAMP 1 and 2 in rat brain. J. Chem. Neuroanat. 2005, 30, 201-211.
27. Weber, T.; Zemelman, B. V.; McNew, J. A.; Westermann, B.; Gmachl, M.; Parlati, F.; Sollner, T. H.; Rothman, J. E. SNAREpins: minimal machinery for membrane fusion. Cell 1998, 92, 759-772.
28. Sollner, T. SNAREs and targeted membrane fusion. FEBS Lett. 1995, 69, 80-83.
29. Whiteheart, S. W.; Griff, I. C; Brunner, M.; Clary, D. O.; Mayer, T.; Buhrow, S. A.; Rothman, J. E. SNAP family of NSF attachment proteins includes a brain-specific isoform. Nature 1993, 362, 353- 355.
30. Xu, J.; Xu, Y.; EUis.Davies, G. C; Augustine, G. J.; Tse, F. W. Differential regulation of exocytosis by alpha-and beta-SNAPs. J. Neurosci. 2002, 22, 53-61.
31. Hanley, J. G.; Khatri, L.; Hanson, P. I.; Ziff, E. B. NSF ATPase and alpha-/beta-SNAPs disassemble the AMPA receptor-PICKl complex. Neuron 2002, 34, 53-67.
32. Georgescu, M.; Pfaus, J. G. Role of glutamate receptors in the ventromedial hypothalamus in the regulation of female rat sexual behaviors. II. Behavioral effects of selective glutamate receptor antagonists AP-5, CNQX, and DNQX. Pharmacol, Biochem. Behav. 2006, 83, 333-341.
33. Georgescu, M.; Pfaus, J. G. Role of glutamate receptors in the ventromedial hypothalamus in the regulation of female rat sexual behaviors I. Behavioral effects of glutamate and its selective receptor agonists AMPA, NMDA and kainate. Pharmacol., Biochem. Behav. 2006, 83, 322-332.
34. Katoh, K.; Shibata, H.; Suzuki, H.; Nara, A.; Ishidoh, K.; Kominami, E.; Yoshimori, T.; Maki, M. The ALG-2-interacting protein Alix associates with CHMP4b, a human homologue of yeast Snf7 that is involved in multivesicular body sorting. J. Biol. Chem. 2003, 278, 39104-39113.
35. Frankfurt, M.; Gould, E.; Woolley, C. S.; McEwen, B. S. Gonadal steroids modify dendritic spine density in ventromedial hypothalamic neurons: A golgi study in the adult rat. Neuroendocrinology 1990, 58, 352-358.
36. Calizo, L. H.; Flanagan-Cato, L. M. Estrogen-induced dendritic spine elimination on female rat ventromedial hypothalamic neurons that project to the periaqueductal gray. J. Comp. Neurol. 2002, 447, 234-248.
37. Flanagan-Cato, L. M.; Calizo, L. H.; Daniels, D. The synaptic organization of VMH neurons that mediate the effects of estrogen on sexual behavior. Horm. Behav. 2001, 40, 178-182.
38. Racz, B.; Weinberg, R. J. Spatial organization of cofilin in dendrtic spines. Neurosci. 2006, 138, 447-456.
39. Brady, S. T. Molecular motors in the nervous system. Neuron 1991, 7, 521-533.
40. Lo, K. W.; Kan, H. M.; Pflster, K. K. Identification of a novel region of the cytoplasmic Dynein intermediate chain important for dimerization in the absence of the light chains. J. Biol Chem. 2006, 281, 9552-9559.
41. Salata, M. W.; Dillman, J. F., III; Lye, R. J.; Pflster, K. K. Growth factor regulation of cytoplasmic dynein intermediate chain subunit expression preceding neurite extension. J. Neurosci. Res. 2001, 65, 408-416.
42. Minturn, J. E.; Fryer, H. J.; Geschwind, D. H.; Hockfield, S. TOAD- 64, a gene expressed early in neuronal differentiation in the rat, is related to unc-33, a C. elegans gene involved in axon outgrowth. J. Neurosci. 1995, 15, 6757-6766.
43. Inagaki, N.; Chihara, K.; Arimura, N.; Menager, C; Kawano, Y.; Matsuo, N.; Nashimura, T.; Amano, M.; Kaibuchi, K. CRMP-2 induces axons in cultured hippocampal neurons. Nat Neurosci. 2001, 4, 781-782.
44. Takahashi, K.; Yamada, M.; Ohata, H.; Honda, K.; Yamada, M. Ndrg2 promotes neurite outgrowth of NGF-differentiated PC12 cells. Neurosci. Lett. 2005, 388, 157-162.
45. Theodosis, D. T.; Piet, R.; Poulain, D. A.; Oliet, S. H. Neuronal, glial and synaptic remodeling in the adult hypothalamus: functional consequences and role of cell surface and extracellular matrix adhesion molecules. Neurochem. Int. 2004, 45, 491-501.
46. Garcia-Segura, L. M.; Naftolin, F.; Hutchison, J. B.; Azcoitia, I.; Chowen, J. A. Role of astroglia in estrogen regulation of synaptic plasticity and brain repair. J. Neurobiol. 1999, 40, 574-584.
47. Mong, J. A.; Blutstein, T. Estradiol modulation of astrocytic form and function: implications for hormonal control of synaptic communication. Neurosci. 2006, 138, 967-975.
48. Colombini, M. VDAC: the channel at the interface between mitochondria and the cytosol. Mol. Cell. Biochem. 2004, 256/257, 107-115.
49. Jonas, E. A.; Hickman, J. A.; Chachar, M.; Polster, B. M.; Brandt, T. A.; Fannjiang, Y; Ivanovska, I.; Basanez, G.; Kinnally, K. W.; Zimmerberg, J.; Hardwick, J. M.; Kaczmarek, L. K. Proapoptotic N-truncated BCL-xL protein activates endogenous mitochondrial channels in living synaptic terminals. Proc. Natl. Acad. Sci. U.SA. 2004, 101, 13590-13595.
50. Zolnierowicz, S. Type 2A protein phosphatase, the complex regulator of numerous signaling pathways. Biochem. Pharmacol. 2000, 60, 1225-1235.
51. Belcher, S. M.; Le, H. H.; Spurting, L.; Wong, J. K. Rapid estrogenic regulation of extracellular signal- regulated kinase 1/2 signaling in cerebellar granule cells involves a G protein-and protein kinase A-dependent mechanism and intracellular activation of protein phosphatase 2A. Endocrinology 2005, 146, 5397-5406.
52. Yi, K. D.; Chung, J.; Pang, P.; Simpkins, J. W. Role of protein phosphatases in estrogen-mediated neuroprotection. J. Neurosci. 2005, 25, 7191-7198.
53. Adams, D. G., Jr.; Zhang, H.; Pelech, S.; Strack, S.; Wadzinski, B. E. Positive regulation of Rafl-MEKl/2-ERKl/2 signaling by protein serine/threonine phosphatase 2A holoenzymes. J. Biol. Chem. 2005, 280, 42644-42654.
54. Westphal, R. S.; Coffee, R. L., Jr.; Marotta, A.; Pelech, S. L.; Wadzinski, B. E. Identification of kinase-phosphatase signaling modules composed of p70 S6 kinase-proteln phosphatase 2A (PP2A) and p21-activated kinase-PP2A. J. Biol. Chem. 1999, 274, 687-692.
55. Etgen, A. M.; Acosta-Martinez, M. Participation of growth factor signal transduction pathways in estradiol facilitation of female reproductive behavior. Endocrinology 2003, 144, 3828-3835.
56. Etgen, A. M.; Gonzalez-Flores, O.; Todd, B. J. The role of insulinlike growth factor-I and growth factor-associated signal transduction pathways in estradiol and progesterone facilitation of female reproductive behaviors. Front. Neuroendocrinology 2006, 27,363- 375.
57. Bi, R.; Foy, M. R.; Vouimba, R. F.; Thompson, M.; Baudry, M. Cyclic changes in estradiol regulate synaptic plasticity through the MAP kinase pathway. Proc. Natl. Acad. Sci. U.SA. 2001, 98, 13391-13395.
58. Hayashi, K.; Ohshima, T.; Mikoshiba, K. Pakl is involved in dendrite initiation as a downstream effector of Racl in cortical neurons. Mol. Cell. Neurosci. 2002, 20, 579-594.
59. Tudor, E. L.; Perkinton, M. S.; Schmidt, A.; Ackerley, S.; Brownlees, J.; Jacobsen, N. J.; Byers, H. L.; Ward, M.; Hall, A.; Leigh, P. N.; Shaw, C. E.; McLoughlin, D. M.; Miller, C. C. ALS2/Alsin regulates Rac-PAK signaling and neurite outgrowth. J. Biol. Chem. 2005, 280, 34735-34740.
60. Keen, J. C; Zhou, Q.; Park, B. H.; Pettit, C; Mack, K. M.; Blair, B.; Brenner, K.; Davidson, N. E. Protein phosphatase 2A regulates estrogen receptor alpha (ER) expression through modulation of ER mRNA stability. J. Biol. Chem. 2005, 280, 29519-29524.
61. Lu, Q.; Surks, H. K.; Ebling, H.; Baur, W. E.; Brown, D.; Pallas, D. C; Karas, R. H. Regulation of estrogen receptor alpha-mediated transcription by a direct interaction with protein phosphatase 2A. J. Biol. Chem. 2003, 278, 4639-4645.
62. Rogner, U. C; Spyropoulos, D. D.; Novere, N. L.; Changeux, J.-P.; Avner, P. Control of neurulation by the nucleosome assembly protein-1-like 2. Nat. Genet. 2000, 25, 431-435.
63. Smith, R. J.; Dean, W.; Konfortova, G.; Kelsey, G. Identification of novel imprinted genes in a genome-wide screen for maternal methylation. Genome Res. 2003, 13, 558-569.
64. Park, Y. J.; Luger, K. Structure and function of nucleosome assembly proteins. Biochem. Cell. Biol. 2006, 84, 549-558.
65. Balakirev, M. Y.; Tcherniuk, S. O.; Jaquinod, M.; Chroboczek, J. Otubains: a new family of cysteine proteases in the ubiquitin pathway. EMBO Rep. 2003, 4, 517-522.
66. Passmore, L. A.; Barford, D. Getting into position: the catalystic mechanisms of protein ubiquitylation. Biochem. J. 2004, 379, 513- 525.
67. Millard, S. M.; Wood, S. A. Riding the DUBway: regulation of protein trafficking by deubiquitylating enzymes. J. Cell Biol. 2006, 173, 463-468.
68. Raiborg, C; Rusten, T. E.; Stenmark, H. Protein sorting into multivesicular endosomes. Curr. Opin. Cell Biol. 2003, 15, 446-455.
69. MacLusky, N. J.; McEwen, B. S. Oestrogen modulates progestin receptor concentrations in some brain regions but not others. Nature 1978, 274, 276-278.
70. Blaustein, J. D.; Feder, H. H. Cytoplamic receptors in female guinea pig brain and their relationship to refractoriness in expression of female sexual behavior. Brain Res. 1979, 177, 489-498.
71. Parsons, B.; Rainbow, T. C; Pfaff, D. W.; McEwen, B. S. Oestradiol, sexual receptivity and cytosol progestin receptors in rat hypothalamus. Nature 1981, 292, 58-59.
72. Savouret, J. F.; Bailly, A.; Misrahi, M.; Rauch, C; Redeuilh, G.; Chauchereau, A.; Milgrom, A. Characterization of the hormone responsive element involved in the regulation of the progesterone receptor gene. EMBO J. 1991, 10, 1875-1883.
73. Kosano, H.; Stensgard, B.; Charlesworth, M. C; McMahon, N.; Toft, D. The assembly of progesterone receptor-hsp90 complexes using purified proteins. J. Biol. Chem. 1998, 273, 32973-32979.
74. Hernandez, M. P.; Chadli, A.; Toft, D. O. HSP40 binding is the first step in the HSP90 chaperoning pathway for the progesterone receptor. J. Biol. Chem. 2002, 277, 11873-11881.
75. Song, Y.; Zweier, J. L.; Xia, Y. Determination of the enhancing action of HSP90 on neuronal nitric oxide synthase by EPR spectroscopy. Am. J. Physiol.: Cell Physiol. 2001, 281, C1819-1824.
76. Song, Y.; Cardounel, A. J.; Zweier, J. L.; Xia, Y. Inhibition of superoxide generation from neuronal nitric oxide synthase by heat shock protein 90: implications in NOS regulation. Biochemistry 2002, 41, 10616-10622.
77. Mani, S. K.; Allen, J. M.; Rettori, V.; McCann, S. M.; O'Malley, B. W.; Clark, J. H. Nitric oxide mediates sexual behavior in female rats. Proc. Natl. Acad. Sci. U.SA. 1994, 91, 6468-6472.
78. Chu, H. P.; Etgen, A. M. Ovarian hormone dependence of alpha(l)-adrenoceptor activation of the nitric oxide-cGMP pathway: relevance for hormonal facilitation of lordosis behavior. J. Neurosci. 1999, 19, 7191-7197.
79. Gabai, V. L.; Meriin, A. B.; Yaglom, J. A.; Volloch, V. Z.; Sherman, M. Y. Role of Hsp70 in regulation of stress kinase JNK: implications in apoptosis and aging. FEBS Lett. 1998, 438, 1-4.
80. Papaconstantinou, A. D.; Coering, P. L.; Umbreit, T. H.; Brown, K. M. Regulation of uterine hsp90alpha, hsp72 and HSF-1 transcription in B6C3F1 mice by beta-estradiol and bisphenol A: involvement of estrogen receptor and protein kinase C. Toxicol. Lett. 2003, 144, 257-270.