Sex differences in the cerebellum and frontal cortex: Roles of estrogen receptor alpha and sex chromosome genes

Neuroendocrinology

Volumn 93, Issue 4, 2011, Pages 230-240

  Abel, Jean M ^a   Witt, Diane M ^a   Rissman, Emilie F ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Autism; Calbindin; Fragile X; Sex differences; X inactivation

Indexed keywords

CALBINDIN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; MESSENGER RNA;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CEREBELLUM; CONTROLLED STUDY; FEMALE; FRONTAL CORTEX; GENE DELETION; GENE EXPRESSION; GENETIC COMPLEMENTATION; GONAD; HIPPOCAMPUS; HYPOTHALAMUS; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SEX CHROMOSOME; SEX DIFFERENCE; X CHROMOSOME; Y CHROMOSOME;

ANIMALS; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CEREBELLUM; CEREBRAL CORTEX; ESTROGEN RECEPTOR ALPHA; FEMALE; FRONTAL LOBE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, ANIMAL; RNA, MESSENGER; SEX CHARACTERISTICS; SEX CHROMOSOMES;

EID: 79959380120     PISSN: 00283835     EISSN: 14230194     Source Type: Journal    
DOI: 10.1159/000324402     Document Type: Article

References (70)

1. Jazin E, Cahill L: Sex differences in molecu-lar neuroscience: From fruit flies to humans. Nat Rev Neurosci 2010; 11: 9-17.
2. Dalla C, Shors TJ: Sex differences in learning processes of classical and operant condition-ing. Physiol Behav 2009; 97: 229-238.
3. Cohen-Bendahan CC, van de Beek C, Beren-baum SA: Prenatal sex hormone effects on child and adult sex-typed behavior: methods and findings. Neurosci Biobehav Rev 2005; 29: 353-384. (Pubitemid 40461750)
4. Cooke B, Hegstrom CD, Villeneuve LS, Breedlove SM: Sexual differentiation of the vertebrate brain: principles and mecha-nisms. Front Neuroendocrinol 1998; 19: 323-362. (Pubitemid 28487799)
5. McCarthy MM, Wright CL, Schwarz JM: New tricks by an old dogma: mechanisms of the organizational/activational hypothesis of steroid-mediated sexual differentiation of brain and behavior. Horm Behav 2009; 55: 655-665.
6. Dean SL, McCarthy MM: Steroids, sex and the cerebellar cortex: implications for hu-man disease. Cerebellum 2008; 7:38-47.
7. Arnold AP: Mouse models for evaluating sex chromosome effects that cause sex differenc-es in non-gonadal tissues. J Neuroendocrinol 2009; 21: 377-386.
8. De Vries GJ, Rissman EF, Simerly RB, Yang LY, Scordalakes EM, Auger CJ, Swain A, Lovell-Badge R Burgoyne PS, Arnold AP: A model system for study of sex chromosome effects on sexually dimorphic neural and be-havioral traits. J Neurosci 2002; 22:9005-9014. (Pubitemid 35379070)
9. 2+-loaded calbindin-D(28K). Nat Struct Mol Biol 2006; 13: 641-647. (Pubitemid 44036475)
10. Bastianelli E: Distribution of calcium-bind-ing proteins in the cerebellum. Cerebellum 2003; 2:242-262.
11. Budefeld T, Grgurevic N, Tobet SA, Majdic G: Sex differences in brain developing in the presence or absence of gonads. Dev Neurobiol 2008; 68:981-995. (Pubitemid 351794117)
12. Edelmann M, Wolfe C, Scordalakes EM, Rissman EF, Tobet S: Neuronal nitric oxide synthase and calbindin delineate sex differ-ences in the developing hypothalamus and preoptic area. Dev Neurobiol 2007; 67:1371-1381. (Pubitemid 47242763)
13. Sickel MJ, McCarthy MM: Calbindin-D28K immunoreactivity is a marker for a subdivi-sion of the sexually dimorphic nucleus of the preoptic area of the rat: developmental pro-file and gonadal steroid modulation. J Neu-roendocrinol 2000; 12: 397-402. (Pubitemid 30223985)
14. Welborn BL, Papademetris X, Reis DL, Ra-jeevan N, Bloise SM, Gray JR: Variation in orbitofrontal cortex volume: relation to sex, emotion regulation and affect. Soc Cogn Affect Neurosci 2009; 4:328-339.
15. Tiemeier H, Lenroot RK, Greenstein DK, Tran L, Pierson R, Giedd JN: Cerebellum development during childhood and adoles-cence: a longitudinal morphometric MRI study. Neuroimage 2010; 49:63-70.
16. Gauthier CT, Duyme M, Zanca M, Capron C: Sex and performance level effects on brain activation during a verbal fluency task: a functional magnetic resonance imaging study. Cortex 2009; 45: 164-176.
17. Servais L, Bearzatto B, Schwaller B, Dumont M, De Saedeleer C, Dan B, Barski JJ, Schiff-mann SN, Cheron G: Mono-and dual-fre-quency fast cerebellar oscillation in mice lacking parvalbumin and/or calbindin D-28k. Eur J Neurosci 2005; 22:861-870. (Pubitemid 41243327)
18. Farre-Castany MA, Schwaller B, Gregory P, Barski J, Mariethoz C, Eriksson JL, Tetko IV, Wolfer D Celio MR Schmutz I, Albrecht U, Villa AE: Differences in locomotor behavior revealed in mice deficient for the calcium-binding proteins parvalbumin, calbindin D-28k or both. Behav Brain Res 2007; 178:250-261. (Pubitemid 46341442)
19. Kriegsfeld LJ, Mei DF, Yan L, Witkovsky P, Lesauter J, Hamada T, Silver R: Targeted mu-tation of the calbindin D28K gene disrupts circadian rhythmicity and entrainment. Eur J Neurosci 2008; 27:2907-2921. (Pubitemid 351832210)
20. Airaksinen MS, Eilers J, Garaschuk O, Thoenen H, Konnerth A, Meyer M: Ataxia and altered dendritic calcium signaling in mice carrying a targeted null mutation of the calbindin D28k gene. Proc Natl Acad Sci USA 1997; 94: 1488-1493. (Pubitemid 27087878)
21. Barski JJ, Hartmann J, Rose CR, Hoebeek F, Morl K, Noll-Hussong M, De Zeeuw CI, Konnerth A, Meyer M: Calbindin in cerebel-lar Purkinje cells is a critical determinant of the precision of motor coordination. J Neurosci 2003; 23: 3469-3477. (Pubitemid 36531989)
22. Vecellio M, Schwaller B, Meyer M, Hunziker W, Celio MR: Alterations in Purkinje cell spines of calbindin D-28 k and parvalbumin knock-out mice. Eur J Neurosci 2000; 12: 945-954. (Pubitemid 30168772)
23. Jouvenceau A, Potier B, Poindessous-Jazat F, Dutar P, Slama A, Epelbaum J, Billard JM: Decrease in calbindin content significantly alters LTP but not NMDA receptor and cal-cium channel properties. Neuropharmacol-ogy 2002; 42: 444-458. (Pubitemid 34304238)
24. Dupont S, Krust A, Gansmuller A, Dierich A, Chambon P, Mark M: Effect of single and compound knockouts of estrogen receptors alpha (ERalpha) and beta (ERbeta) on mouse reproductive phenotypes. Development 2000; 127:4277-4291.
25. Stornetta RL, Sevigny CP, Schreihofer AM, Rosin DL, Guyenet PG: Vesicular glutamate transporter DPNI/VGLUT2 is expressed by both C1 adrenergic and nonaminergic pre-sympathetic vasomotor neurons of the rat medulla. J Comp Neurol 2002; 444: 207-220. (Pubitemid 34117086)
26. Iacopino AM, Rhoten WB, Christakos S: Calcium binding protein (calbindin-D28k) gene expression in the developing and aging mouse cerebellum. Brain Res Mol Brain Res 1990; 8:283-290. (Pubitemid 20297024)
27. Celio MR: Calbindin D-28k and parvalbu-min in the rat nervous system. Neuroscience 1990; 35: 375-475. (Pubitemid 20176750)
28. Amenta F, Cavalotta D, Del Valle ME, Man-cini M, Sabbatini M, Torres JM, Vega JA: Cal-bindin D-28k immunoreactivity in the rat cerebellar cortex: age-related changes. Neurosci Lett 1994; 178: 131-134. (Pubitemid 24274379)
29. Abe H, Watanabe M, Yamakuni T, Kuwano R, Takahashi Y, Kondo H: Localization of gene expression of calbindin in the brain of adult rats. Neurosci Lett 1992; 138: 211-215.
30. Stuart E, Lephart ED: Dimorphic expression of medial basal hypothalamic-preoptic area calbindin-D(28K) mRNA during perinatal development and adult distribution of cal-bindin-D(28K) mRNA in Sprague-Dawley rats. Brain Res Mol Brain Res 1999; 73: 60-67.
31. Sequier JM, Hunziker W, Andressen C, Celio MR: Calbindin D-28k protein and mRNA localization in the rat brain. Eur J Neurosci 1990; 2:1118-1126.
32. Wanner I, Baader SL, Brich M, Oberdick J, Schilling K: Subcellular localization of spe-cific mRNAs and their protein products in Purkinje cells by combined fluorescence in situ hybridization and immunocytochemis-try. Histochem Cell Biol 1997; 108:345-357. (Pubitemid 27468136)
33. Jinno S, Jeromin A, Kosaka T: Expression and possible role of neuronal calcium sen-sor-1 in the cerebellum. Cerebellum 2004; 3: 83-88. (Pubitemid 38797067)
34. Gill RK, Christakos S: Regulation by estro-gen through the 5'-flanking region of the mouse calbindin-D28k gene. Mol Endocrinol 1995; 9: 319-326.
35. Mitra SW, Hoskin E, Yudkovitz J, Pear L, Wilkinson HA, Hayashi S, Pfaff DW, Ogawa S, Rohrer SP, Schaeffer JM, McEwen BS, Alves SE: Immunolocalization of estrogen receptor beta in the mouse brain: compari-son with estrogen receptor alpha. Endocrinology 2003; 144:2055-2067. (Pubitemid 36543346)
36. Merchenthaler I, Lane MV, Numan S, Dell-ovade TL: Distribution of estrogen receptor alpha and beta in the mouse central nervous system: in vivo autoradiographic and immu-nocytochemical analyses. J Comp Neurol 2004; 473: 270-291. (Pubitemid 38569232)
37. Kornack DR, Lu B, Black IB: Sexually dimor-phic expression of the NGF receptor gene in the developing rat brain. Brain Res 1991; 542: 171-174.
38. Hamson DK, Csupity AS, Gaspar JM, Wat-son NV: Analysis of Foxp2 expression in the cerebellum reveals a possible sex difference. Neuroreport 2009; 20:611-616.
39. Andreano JM, Cahill L: Sex influences on the neurobiology of learning and memory. Learn Mem 2009; 16: 248-266.
40. Nakanishi S: Genetic manipulation study of information processing in the cerebellum. Neuroscience 2009; 162:723-731.
41. Chen X, Grisham W, Arnold AP: X chromo-some number causes sex differences in gene expression in adult mouse striatum. Eur J Neurosci 2009; 29:768-776.
42. Carruth LL, Reisert I, Arnold AP: Sex chro-mosome genes directly affect brain sexual differentiation. Nat Neurosci 2002; 5: 933-934.
43. Gatewood JD, Wills A, Shetty S, Xu J, Arnold AP, Burgoyne PS, Rissman EF: Sex chromo-some complement and gonadal sex influence aggressive and parental behaviors in mice. J Neurosci 2006; 26: 2335-2342. (Pubitemid 44699043)
44. Markham JA, Jurgens HA, Auger CJ, De Vries GJ, Arnold AP, Juraska JM: Sex differ-ences in mouse cortical thickness are inde-pendent of the complement of sex chromo-somes. Neuroscience 2003; 116: 71-75. (Pubitemid 36110433)
45. De Vries GJ, Wang Z, Bullock NA, Numan S: Sex differences in the effects of testosterone and its metabolites on vasopressin messen-ger RNA levels in the bed nucleus of the stria terminalis of rats. J Neurosci 1994; 14:1789-1794. (Pubitemid 24080026)
46. Han TM, De Vries GJ: Organizational effects of testosterone, estradiol, and dihydrotestos-terone on vasopressin mRNA expression in the bed nucleus of the stria terminalis. J Neurobiol 2003; 54:502-510. (Pubitemid 36152574)
47. Scordalakes EM, Rissman EF: Aggression and arginine vasopressin immunoreactivity regulation by androgen receptor and estro-gen receptor alpha. Genes Brain Behav 2004; 3:20-26. (Pubitemid 38160238)
48. Amateau SK, Alt JJ, Stamps CL, McCarthy MM: Brain estradiol content in newborn rats: sex differences, regional heterogeneity and possible de novo synthesis by the female telencephalon. Endocrinology 2004; 145: 2906-2917. (Pubitemid 38686240)
49. Tsutsui K: Neurosteroids in the purkinje cell: biosynthesis, mode of action and functional significance. Mol Neurobiol 2008; 37: 116-125.
50. Lavaque E, Mayen A, Azcoitia I, Tena-Sem-pere M, Garcia-Segura LM: Sex differences, developmental changes, response to injury and cAMP regulation of the mRNA levels of steroidogenic acute regulatory protein, cyto-chrome p450scc, and aromatase in the olivo-cerebellar system. J Neurobiol 2006; 66:308-318. (Pubitemid 43202767)
51. Biamonte F, Assenza G, Marino R, DAmelio M, Panteri R, Caruso D, Scurati S, Yague JG, Garcia-Segura LM, Cesa R, Strata P, Mel-cangi RC, Keller F: Interactions between neuroactive steroids and reelin haploinsuf-ficiency in Purkinje cell survival. Neurobiol Dis 2009; 36:103-115.
52. Xu J, Disteche CM: Sex differences in brain expression of X-and Y-linked genes. Brain Res 2006; 1126:50-55. (Pubitemid 44880928)
53. Xu J, Watkins R, Arnold AP: Sexually dimor-phic expression of the X-linked gene Eif2s3x mRNA but not protein in mouse brain. Gene Expr Patterns 2006; 6:146-155. (Pubitemid 43071909)
54. Allis CD, Berger SL, Cote J, Dent S, Jenuwien T, Kouzarides T, Pillus L, Reinberg D, Shi Y Shiekhattar R, Shilatifard A, Workman J, Zhang Y: New nomenclature for chromatin-modifying enzymes. Cell 2007; 131: 633-636. (Pubitemid 350089969)
55. Iwase S, Lan F, Bayliss P, de la Torre-Ubieta L, Huarte M, Qi HH, Whetstine JR, Bonni A, Roberts TM, Shi Y: The X-linked mental re-tardation gene SMCX/JARID1C defines a family of histone H3 lysine 4 demethylases. Cell 2007; 128:1077-1088. (Pubitemid 46437259)
56. Mehedint MG, Niculescu MD, Craciunescu CN, Zeisel SH: Choline deficiency alters global histone methylation and epigenetic marking at the Re1 site of the calbindin 1 gene. FASEB J 2010; 24: 184-195.
57. Wooten GF, Currie LJ, Bovbjerg VE, Lee JK Patrie J: Are men at greater risk for Parkin-son's disease than women? J Neurol Neurosurg Psychiatry 2004; 75: 637-639. (Pubitemid 38406668)
58. McGrath J, Saha S, Chant D, Welham J: Schizophrenia: a concise overview of inci-dence, prevalence, and mortality. Epidemiol Rev 2008; 30:67-76.
59. Honda H, Shimizu Y, Imai M, Nitto Y: Cumulative incidence of childhood autism: a total population study of better accuracy and precision. Dev Med Child Neurol 2005; 47: 10-18.
60. Merikangas KR, He JP, Brody D, Fisher PW, Bourdon K, Koretz DS: Prevalence and treat-ment of mental disorders among US children in the 2001-2004 NHANES. Pediatrics 2010; 125: 75-81.
61. Mazzocco MM: Advances in research on the fragile X syndrome. Ment Retard Dev Dis-abil Res Rev 2000; 6:96-106. (Pubitemid 30399532)
62. Candore G, Balistreri CR, Grimaldi MP, Vasto S, Listi F, Chiappelli M, Licastro F, Lio D, Caruso C: Age-related inflammatory diseases: role of genetics and gender in the pathophysiology of Alzheimer's disease. Ann NY Acad Sci 2006; 1089:472-486. (Pubitemid 47092063)
63. Zahn-Waxler C, Shirtcliff EA, Marceau K: Disorders of childhood and adolescence: gender and psychopathology. Annu Rev Clin Psychol 2008; 4:275-303. (Pubitemid 351668619)
64. Abrahams BS, Geschwind DH: Connecting genes to brain in the autism spectrum disor-ders. Arch Neurol 2010; 67: 395-399.
65. Ackermann H: Cerebellar contributions to speech production and speech perception: psycholinguistic and neurobiological per-spectives. Trends Neurosci 2008; 31: 265-272.
66. Iacopino AM, Christakos S: Specific reduc-tion of calcium-binding protein (28-kilodal-ton calbindin-D) gene expression in aging and neurodegenerative diseases. Proc Natl Acad Sci USA 1990; 87: 4078-4082.
67. Sutherland MK, Wong L, Somerville MJ, Yoong LK, Bergeron C, Parmentier M, McLachlan DR: Reduction of calbindin-28k mRNA levels in Alzheimer as compared to Huntington hippocampus. Brain Res Mol Brain Res 1993; 18: 32-42.
68. Kiyama H, Seto-Ohshima A, Emson PC: Calbindin D28K as a marker for the degen-eration of the striatonigral pathway in Hun-tington's disease. Brain Res 1990; 525:209-214. (Pubitemid 20257738)
69. Bauman ML, Kemper TL: The neuropathology of the autism spectrum disorders: what have we learned? Novartis Found Symp 2003; 251: 112-122, discussion 122-128, 281-297.
70. Fatemi SH, Halt AR, Realmuto G, Earle J, Kist DA, Thuras P, Merz A: Purkinje cell size is reduced in cerebellum of patients with au-tism. Cell Mol Neurobiol 2002; 22:171-175.