Characterization of the "sporadically lurking HAP1-immunoreactive (SLH) cells" in the hippocampus, with special reference to the expression of steroid receptors, GABA, and progenitor cell markers

Neuroscience

Volumn 210, Issue , 2012, Pages 67-81

  Islam, Md N ^a   Fujinaga, R ^a   Yanai, A ^a   Jahan, M R ^a   Takeshita, Y ^a,b   Kokubu, K ^a   Shinoda, K ^a  

^a YAMAGUCHI UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b JAPAN SOCIETY FOR THE PROMOTION OF SCIENCE   (Japan)

Author keywords

Ammon's horn; Dentate gyrus; Estrogen receptor ; Huntingtin associated protein 1; Immunohistochemistry; Neurogenesis

Indexed keywords

4 AMINOBUTYRIC ACID; ANDROGEN RECEPTOR; CELL MARKER; CELL PROTEIN; CHOLECYSTOKININ; CYCLINE; DOUBLECORTIN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUCOCORTICOID RECEPTOR; HUNTINGTIN ASSOCIATED PROTEIN 1; KI 67 ANTIGEN; NEURON SPECIFIC NUCLEAR PROTEIN; PARVALBUMIN; STEROID RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; DENTATE GYRUS; FEMALE; HIPPOCAMPUS; IMMUNOREACTIVITY; MALE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROANATOMY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; STRATUM LACUNOSUM MOLECULARE; STRATUM RADIATUM; SUBGRANULAR ZONE;

ADULT STEM CELLS; ANIMALS; CELL COUNT; ESTROGEN RECEPTOR ALPHA; FEMALE; GAMMA-AMINOBUTYRIC ACID; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; MICROSCOPY, FLUORESCENCE; MICROSCOPY, IMMUNOELECTRON; NERVE TISSUE PROTEINS; NEURAL STEM CELLS; NEURONS; RATS; RATS, WISTAR;

EID: 84861184101     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.02.029     Document Type: Article

References (98)

1. Amann-Zalcenstein D., Avidan N., Kanyas K., Ebstein R.P., Kohn Y., Hamdan A., Ben-Asher E., Karni O., Mujaheed M., Segman R.H., Maier W., Macciardi F., Beckmann J.S., Lancet D., Lerer B. AHI1, a pivotal neurodevelopmental gene, and C6orf217 are associated with susceptibility to schizophrenia. Eur J Hum Genet 2006, 14:1111-1119.
2. Bamberger C.M., Bamberger A.M., de Castro M., Chrousos G.P. Glucocorticoid receptor beta, a potential endogenous inhibitor of glucocorticoid action in humans. J Clin Invest 1995, 95:2435-2441.
3. Bamberger C.M., Schulte H.M., Chrousos G.P. Molecular determinants of glucocorticoid receptor function and tissue sensitivity to glucocorticoids. Endocr Rev 1996, 17:245-261.
4. Barrett-Connor E., Laughlin G.A. Endogenous and exogenous estrogen, cognitive function, and dementia in postmenopausal women: evidence from epidemiologic studies and clinical trials. Semin Reprod Med 2009, 27:275-282.
5. Bender R.A., Zhou L., Wilkars W., Fester L., Lanowski J.S., Paysen D., König A., Rune G.M. Roles of 17ss-estradiol involve regulation of reelin expression and synaptogenesis in the dentate gyrus. Cereb Cortex 2010, 20:2985-2995.
6. Brown J.P., Couillard-Després S., Cooper-Kuhn C.M., Winkler J., Aigner L., Kuhn H.G. Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 2003, 467:1-10.
7. Cameron H.A., McKay R.D. Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 2001, 435:406-417.
8. Chan E.Y., Nasir J., Gutekunst C.A., Coleman S., Maclean A., Maas A., Metzler M., Gertsenstein M., Ross C.A., Nagy A., Hayden M.R. Targeted disruption of huntingtin-associated protein-1 (Hap1) results in postnatal death due to depressed feeding behavior. Hum Mol Genet 2002, 11:945-959.
9. Clarke C.H., Norfleet A.M., Clarke M.S., Watson C.S., Cunningham K.A., Thomas M.L. Perimembrane localization of the estrogen receptor alpha protein in neuronal processes of cultured hippocampal neurons. Neuroendocrinology 2000, 71:34-42.
10. De Castro M., Elliot S., Kino T., Bamberger C., Karl M., Webster E., Chrousos G.P. The non-ligand binding beta-isoform of the human glucocorticoid receptor (hGR beta): tissue levels, mechanism of action, and potential physiologic role. Mol Med 1996, 2:597-607.
11. Dixon-Salazar T., Silhavy J.L., Marsh S.E., Louie C.M., Scott L.C., Gururaj A., Al-Gazali L., Al-Tawari A.A., Kayserili H., Sztriha L., Gleeson J.G. Mutations in the AHI1 gene, encoding jouberin, cause Joubert syndrome with cortical polymicrogyria. Am J Hum Genet 2004, 75:979-987.
12. Dragatsis I., Zeitlin S., Dietrich P. Huntingtin-associated protein 1 (Hap1) mutant mice bypassing the early postnatal lethality are neuroanatomically normal and fertile but display growth retardation. Hum Mol Genet 2004, 13:3115-3125.
13. Ellinwood W.E., Hess D.L., Roselli C.E., Spies H.G., Resko J.A. Inhibition of aromatization stimulates luteinizing hormone and testosterone secretion in adult male rhesus monkeys. J Clin Endocrinol Metab 1984, 59:1088-1096.
14. Encio I.J., Detera-Wadleigh S.D. The genomic structure of the human glucocorticoid receptor. J Biol Chem 1991, 266:7182-7188.
15. Ferland R.J., Eyaid W., Collura R.V., Tully L.D., Hill R.S., Al-Nouri D., Al-Rumayyan A., Topcu M., Gascon G., Bodell A., Shugart Y.Y., Ruvolo M., Walsh C.A. Abnormal cerebellar development and axonal decussation due to mutations in AHI1 in Joubert syndrome. Nat Genet 2004, 36:1008-1013.
16. Fujinaga R., Kawano J., Matsuzaki Y., Kamei K., Yanai A., Sheng Z., Tanaka M., Nakahama K., Nagano M., Shinoda K. Neuroanatomical distribution of huntingtin-associated protein 1-mRNA in the male mouse brain. J Comp Neurol 2004, 478:88-109.
17. Fujinaga R., Takeshita Y., Uozumi K., Yanai A., Yoshioka K., Kokubu K., Shinoda K. Microtubule-dependent formation of the stigmoid body as a cytoplasmic inclusion distinct from pathological aggresomes. Histochem Cell Biol 2009, 132:305-318.
18. Fujinaga R., Takeshita Y., Yoshida K., Kametani Y., Nakatsuka H., Yanai A., Shinoda K. Comparative distributions of huntingtin-associated protein 1 (HAP1) and androgen receptor (AR) in the rat brain and their functional interaction in vitro. Acta Histochem Cytochem 2005, 38(Suppl):IA-11.
19. Fujinaga R., Takeshita Y., Yoshioka K., Nakamura H., Shinoda S., Islam M.N., Jahan M.R., Yanai A., Kokubu K., Shinoda K. Intracellular colocalization of HAP1/STBs with steroid hormone receptors and its enhancement by a proteasome inhibitor. Exp Cell Res 2011, 317:1689-1700.
20. Fujinaga R., Yanai A., Nakatsuka H., Yoshida K., Takeshita Y., Uozumi K., Zhao C., Hirata K., Kokubu K., Nagano M., Shinoda K. Anti-human placental antigen complex X-P2 (hPAX-P2) anti-serum recognizes C-terminus of huntingtin-associated protein 1A common to 1B as a determinant marker for the stigmoid body. Histochem Cell Biol 2007, 128:335-348.
21. Funakoshi T., Yanai A., Shinoda K., Kawano M.M., Mizukami Y. G protein-coupled receptor 30 is an estrogen receptor in the plasma membrane. Biochem Biophys Res Commun 2006, 346:904-910.
22. Galea L.A., Spritzer M.D., Barker J.M., Pawluski J.L. Gonadal hormone modulation of hippocampal neurogenesis in the adult. Hippocampus 2006, 16:225-232.
23. Garcia-Segura L.M., Veiga S., Sierra A., Melcangi R.C., Azcoitia I. Aromatase: a neuroprotective enzyme. Prog Neurobiol 2003, 71:31-41.
24. Gleeson J.G., Lin P.T., Flanagan L.A., Walsh C.A. Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 1999, 23:257-271.
25. Greco B., Allegretto E.A., Tetel M.J., Blaustein J.D. Coexpression of ER beta with ER alpha and progestin receptor proteins in the female rat forebrain: effects of estradiol treatment. Endocrinology 2001, 142:5172-5181.
26. Gutekunst C.A., Li S.H., Yi H., Ferrante R.J., Li X.J., Hersch S.M. The cellular and subcellular localization of huntingtin-associated protein 1 (HAP1): comparison with huntingtin in rat and human. J Neurosci 1998, 18:7674-7686.
27. Hajszan T., MacLusky N.J., Leranth C. Role of androgens and the androgen receptor in remodeling of spine synapses in limbic brain areas. Horm Behav 2008, 53:638-646.
28. Han F., Ozawa H., Matsuda K.I., Nishi M., Kawata M. Colocalization of mineralocorticoid receptor and glucocorticoid receptor in the hippocampus and hypothalamus. Neurosci Res 2005, 51:371-381.
29. Han Z.S., Buhl E.H., Lörinczi Z., Somogyi P. A high degree of spatial selectivity in the axonal and dendritic domains of physiologically identified local-circuit neurons in the dentate gyrus of the rat hippocampus. Eur J Neurosci 1993, 5:395-410.
30. Hart S.A., Patton J.D., Woolley C.S. Quantitative analysis of ER alpha and GAD colocalization in the hippocampus of the adult female rat. J Comp Neurol 2001, 440:144-155.
31. Hollenberg S.M., Weinberger C., Ong E.S., Cerelli G., Oro A., Lebo R., Thompson E.B., Rosenfeld M.G., Evans R.M. Primary structure and expression of a functional human glucocorticoid receptor cDNA. Nature 1985, 318:635-641.
32. Ingason A., Sigmundsson T., Steinberg S., Sigurdsson E., Haraldsson M., Magnusdottir B.B., Frigge M.L., Kong A., Gulcher J., Thorsteinsdottir U., Stefansson K., Petursson H., Stefansson H. Support for involvement of the AHI1 locus in schizophrenia. Eur J Hum Genet 2007, 15:988-991.
33. Ito T., Morita N., Nishi M., Kawata M. In vitro and in vivo immunocytochemistry for the distribution of mineralocorticoid receptor with the use of specific antibody. Neurosci Res 2000, 37:173-182.
34. Jaffe D.B., Gutierrez R. Mossy fiber synaptic transmission: communication from the dentate gyrus to area CA3. Prog Brain Res 2007, 163:109-132.
35. Jin K., Minami M., Lan J.Q., Mao X.O., Batteur S., Simon R.P., Greenberg D.A. Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat. Proc Natl Acad Sci U S A 2001, 98:4710-4715.
36. Jinno S., Kosaka T. Patterns of expression of neuropeptides in GABAergic nonprincipal neurons in the mouse hippocampus: quantitative analysis with optical disector. J Comp Neurol 2003, 461:333-349.
37. Jinno S., Kosaka T. Stereological estimation of numerical densities of glutamatergic principal neurons in the mouse hippocampus. Hippocampus 2010, 20:829-840.
38. Kalita K., Szymczak S., Kaczmarek L. Non-nuclear estrogen receptor beta and alpha in the hippocampus of male and female rats. Hippocampus 2005, 15:404-412.
39. Kamei K., Matsuzaki Y., Hanada K., Nagano M., Nakahama K., Shinoda K. Distribution of HAP1 mRNA in the rat brain. Acta Anat Nippon 2001, 76(Suppl):A-91.
40. 2+-binding protein parvalbumin in the rat hippocampus and dentate gyrus. Brain Res 1987, 419:119-130.
41. Kosaka T., Kosaka K., Tateishi K., Hamaoka Y., Yanaihara N., Wu J.Y., Hama K. GABAergic neurons containing CCK-8-like and/or VIP-like immunoreactivities in the rat hippocampus and dentate gyrus. J Comp Neurol 1985, 239:420-430.
42. Kretz O., Fester L., Wehrenberg U., Zhou L., Brauckmann S., Zhao S., Prange-Kiel J., Naumann T., Jarry H., Frotscher M., Rune G.M. Hippocampal synapses depend on hippocampal estrogen synthesis. J Neurosci 2004, 24:5913-5921.
43. Kuroki Y., Fukushima K., Kanda Y., Mizuno K., Watanabe Y. Putative membrane-bound estrogen receptors possibly stimulate mitogen-activated protein kinase in the rat hippocampus. Eur J Pharmacol 2000, 400:205-209.
44. Li H., Wyman T., Yu Z.X., Li S.H., Li X.J. Abnormal association of mutant huntingtin with synaptic vesicles inhibits glutamate release. Hum Mol Genet 2003, 12:2021-2030.
45. Li S.H., Gutekunst C.A., Hersch S.M., Li X.J. Association of HAP1 isoforms with a unique cytoplasmic structure. J Neurochem 1998, 71:2178-2185.
46. Li S.H., Hosseini S.H., Gutekunst C.A., Hersch S.M., Ferrante R.J., Li X.J. A human HAP1 homologue. Cloning, expression, and interaction with huntingtin. J Biol Chem 1998, 273:19220-19227.
47. Li S.H., Li H., Torre E.R., Li X.J. Expression of huntingtin-associated protein-1 in neuronal cells implicates a role in neuritic growth. Mol Cell Neurosci 2000, 16:168-183.
48. Li X.J., Li S.H., Sharp A.H., Nucifora F.C., Schilling G., Lanahan A., Worley P., Snyder S.H., Ross C.A. A huntingtin-associated protein enriched in brain with implications for pathology. Nature 1995, 378:398-402.
49. Li X.J., Sharp A.H., Li S.H., Dawson T.M., Snyder S.H., Ross C.A. Huntingtin-associated protein (HAP1): discrete neuronal localizations in the brain resemble those of neuronal nitric oxide synthase. Proc Natl Acad Sci U S A 1996, 93:4839-4844.
50. Lin Y.F., Xu X., Cape A., Li S., Li X.J. Huntingtin-associated protein-1 deficiency in orexin-producing neurons impairs neuronal process extension and leads to abnormal behavior in mice. J Biol Chem 2010, 285:15941-15949.
51. Loy R., Gerlach J.L., McEwen B.S. Autoradiographic localization of estradiol-binding neurons in the rat hippocampal formation and entorhinal cortex. Brain Res 1988, 467:245-251.
52. MacLusky N.J., Naftolin F. Sexual differentiation of the central nervous system. Science 1981, 211:1294-1302.
53. McCullough L.D., Blizzard K., Simpson E.R., Oz O.K., Hurn P.D. Aromatase cytochrome P450 and extragonadal estrogen play a role in ischemic neuroprotection. J Neurosci 2003, 23:8701-8705.
54. McEwen B.S., Lieberburg I., Chaptal C., Krey L.C. Aromatization: important for sexual differentiation of the neonatal rat brain. Horm Behav 1977, 9:249-263.
55. Metzger S., Rong J., Nguyen H.P., Cape A., Tomiuk J., Soehn A.S., Propping P., Freudenberg-Hua Y., Freudenberg J., Tong L., Li S.H., Li X.J., Riess O. Huntingtin-associated protein-1 is a modifier of the age-at-onset of Huntington's disease. Hum Mol Genet 2008, 17:1137-1146.
56. Milner T.A., McEwen B.S., Hayashi S., Li C.J., Reagan L.P., Alves S.E. Ultrastructural evidence that hippocampal alpha estrogen receptors are located at extranuclear sites. J Comp Neurol 2001, 429:355-371.
57. Mitra S.W., Hoskin E., Yudkovitz J., Pear L., Wilkinson H.A., Hayashi S., Pfaff D.W., Ogawa S., Rohrer S.P., Schaeffer J.M., McEwen B.S., Alves S.E. Immunolocalization of estrogen receptor beta in the mouse brain: comparison with estrogen receptor alpha. Endocrinology 2003, 144:2055-2067.
58. Mitterling K.L., Spencer J.L., Dziedzic N., Shenoy S., McCarthy K., Waters E.M., McEwen B.S., Milner T.A. Cellular and subcellular localization of estrogen and progestin receptor immunoreactivities in the mouse hippocampus. J Comp Neurol 2010, 518:2729-2743.
59. Mullen R.J., Buck C.R., Smith A.M. NeuN, a neuronal specific nuclear protein in vertebrates. Development 1992, 116:201-211.
60. Nagano M., Shinoda K. Coexistence of the stigmoid body and estrogen receptor in some neuronal groups involved in rat reproductive functions. Brain Res 1994, 634:296-304.
61. Nishi M. Dynamics of corticosteroid receptors: lessons from live cell imaging. Acta Histochem Cytochem 2011, 44:1-7.
62. Oakley R.H., Sar M., Cidlowski J.A. The human glucocorticoid receptor beta isoform. J Biol Chem 1996, 16:9550-9559.
63. Ogiue-Ikeda M., Tanabe N., Mukai H., Hojo Y., Murakami G., Tsurugizawa T., Takata N., Kimoto T., Kawato S. Rapid modulation of synaptic plasticity by estrogens as well as endocrine disrupters in hippocampal neurons. Brain Res Rev 2008, 57:363-375.
64. Olariu A., Cleaver K.M., Cameron H.A. Decreased neurogenesis in aged rats results from loss of granule cell precursors without lengthening of the cell cycle. J Comp Neurol 2007, 501:659-667.
65. Orikasa C., McEwen B.S., Hayashi H., Sakuma Y., Hayashi S. Estrogen receptor alpha, but not beta, is expressed in the interneurons of the hippocampus in prepubertal rats: an in situ hybridization study. Brain Res Dev Brain Res 2000, 120:245-254.
66. Page K.J., Potter L., Aronni S., Everitt B.J., Dunnett S.B. The expression of huntingtin-associated protein (HAP1) mRNA in developing, adult and ageing rat CNS: implications for Huntington's disease neuropathology. Eur J Neurosci 1998, 10:1835-1845.
67. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1998, Vol. 2. Academic Press, Tokyo.
68. Perez S.E., Chen E.Y., Mufson E.J. Distribution of estrogen receptor alpha and beta immunoreactive profiles in the postnatal rat brain. Brain Res Dev Brain Res 2003, 145:117-139.
69. Prange-Kiel J., Rune G.M. Direct and indirect effects of estrogen on rat hippocampus. Neuroscience 2006, 138:765-772.
70. Prigge J.R., Schmidt E.E. HAP1 can sequester a subset of TBP in cytoplasmic inclusions via specific interaction with the conserved TBP(CORE). BMC Mol Biol 2007, 8:76.
71. Reul J.M.H.M., Gesing A., Droste S., Stec I.S.M., Weber A., Bachmann C., Bilang-Bleuel A., Holsboer F., Linthorst A.C.E. The brain mineralocorticoid receptor: greedy for ligand, mysterious in function. Eur J Pharmacol 2000, 405:235-249.
72. Ribak C.E., Shapiro L.A. Ultrastructure and synaptic connectivity of cell types in the adult rat dentate gyrus. Prog Brain Res 2007, 163:155-166.
73. Sarabdjitsingh R.A., Meijer O.C., de Kloet E.R. Specificity of glucocorticoid receptor primary antibodies for analysis of receptor localization patterns in cultured cells and rat hippocampus. Brain Res 2010, 1331:1-11.
74. Scholzen T., Gerdes J. The Ki-67 protein: from the known and the unknown. J Cell Physiol 2000, 182:311-322.
75. Segal M., Murphy D. Estradiol induces formation of dendritic spines in hippocampal neurons: functional correlates. Horm Behav 2001, 40:156-159.
76. Seidman S.N., Walsh B.T. Testosterone and depression in aging men. Am J Geriatr Psychiatry 1999, 7:18-33.
77. Seress L., Pokorny J. Structure of the granular layer of the rat dentate gyrus. A light microscopic and Golgi study. J Anat 1981, 133:181-195.
78. Seress L., Ribak C.E. GABAergic cells in the dentate gyrus appear to be local circuit and projection neurons. Exp Brain Res 1983, 50:173-182.
79. Seri B., García-Verdugo J.M., McEwen B.S., Alvarez-Buylla A. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 2001, 21:7153-7160.
80. Sharma S.C., Clemens J.W., Pisarska M.D., Richards J.S. Expression and function of estrogen receptor subtypes in granulosa cells: regulation by estradiol and forskolin. Endocrinology 1999, 140:4320-4334.
81. Sheng G., Chang G.Q., Lin J.Y., Yu Z.X., Fang Z.H., Rong J., Lipton S.A., Li S.H., Tong G., Leibowitz S.F., Li X.J. Hypothalamic huntingtin-associated protein 1 as a mediator of feeding behavior. Nat Med 2006, 12:526-533.
82. Sheng G., Xu X., Lin Y.F., Wang C.E., Rong J., Cheng D., Peng J., Jiang X., Li S.H., Li X.J. Huntingtin-associated protein 1 interacts with Ahi1 to regulate cerebellar and brainstem development in mice. J Clin Invest 2008, 118:2785-2795.
83. Sheng Z., Kawano J., Yanai A., Fujinaga R., Tanaka M., Watanabe Y., Shinoda K. Expression of estrogen receptors (alpha, beta) and androgen receptor in serotonin neurons of the rat and mouse dorsal raphe nuclei; sex and species differences. Neurosci Res 2004, 49:185-196.
84. Sheng Z., Yanai A., Fujinaga R., Kawano J., Tanaka M., Watanabe Y., Shinoda K. Gonadal and adrenal effects on the glucocorticoid receptor in the rat hippocampus, with special reference to regulation by estrogen from an immunohistochemical view-point. Neurosci Res 2003, 46:205-218.
85. Shinoda K., Mori S., Ohtsuki T., Osawa Y. An aromatase-associated cytoplasmic inclusion, the "stigmoid body," in the rat brain: I. Distribution in the forebrain. J Comp Neurol 1992, 322:360-376.
86. Shinoda K., Nagano M., Osawa Y. An aromatase-associated cytoplasmic inclusion, the "stigmoid body," in the rat brain: II. Ultrastructure (with a review of its history and nomenclature). J Comp Neurol 1993, 329:1-19.
87. Shinoda K., Nagano M., Osawa Y. Neuronal aromatase expression in preoptic, strial, and amygdaloid regions during late prenatal and early postnatal development in the rat. J Comp Neurol 1994, 343:113-129.
88. Shinoda K., Tohyama M., Shiotani Y. Hippocampofugal gamma-aminobutyric acid (GABA)-containing neuron system in the rat: a study using a double-labeling method that combines retrograde tracing and immunocytochemistry. Brain Res 1987, 409:181-186.
89. Shughrue P.J., Merchenthaler I. Distribution of estrogen receptor beta immunoreactivity in the rat central nervous system. J Comp Neurol 2001, 436:64-81.
90. Snyder J.S., Choe J.S., Clifford M.A., Jeurling S.I., Hurley P., Brown A., Kamhi J.F., Cameron H.A. Adult-born hippocampal neurons are more numerous, faster maturing, and more involved in behavior in rats than in mice. J Neurosci 2009, 29:14484-14495.
91. Soriano E., Frotscher M. A GABAergic axo-axonic cell in the fascia dentata controls the main excitatory hippocampal pathway. Brain Res 1989, 503:170-174.
92. Takeshita Y., Fujinaga R., Kokubu K., Islam M.N., Jahan M.R., Yanai A., Kakizuka A., Shinoda K. Interaction of ataxin-3 with huntingtin-associated protein 1 through Josephin domain. Neuroreport 2011, 22:232-238.
93. Takeshita Y., Fujinaga R., Zhao C., Yanai A., Shinoda K. Huntingtin-associated protein 1 (HAP1) interacts with androgen receptor (AR) and suppresses SBMA-mutant-AR-induced apoptosis. Hum Mol Genet 2006, 15:2298-2312.
94. Vagell M.E., McGinnis M.Y. The role of aromatization in the restoration of male rat reproductive behavior. J Neuroendocrinol 1997, 9:415-421.
95. von Bohlen Und Halbach O. Immunohistological markers for staging neurogenesis in adult hippocampus. Cell Tissue Res 2007, 329:409-420.
96. Woolley C.S., McEwen B.S. Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J Neurosci 1992, 12:2549-2554.
97. Zhao C., Fujinaga R., Tanaka M., Yanai A., Nakahama K., Shinoda K. Region-specific expression and sex-steroidal regulation on aromatase and its mRNA in the male rat brain: immunohistochemical and in situ hybridization analyses. J Comp Neurol 2007, 500:557-573.
98. Zhe D., Fang H., Yuxiu S. Expression of hippocampal mineralocorticoid receptor (MR) and glucocorticoid receptor (GR) in the single-prolonged sress-rats. Acta Histochem Cytochem 2008, 41:89-95.