Sex-specific modulation of gene expression networks in murine hypothalamus

Frontiers in Neuroscience

Volumn , Issue MAY, 2012, Pages

  Mozhui, Khyobeni ^a   Lu, Lu ^a   Armstrong, William E ^a   Williams, Robert W ^a  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

eQTL; Hypothalamus; Sex specificity; Weighted gene coexpression networks

Indexed keywords

CALMODULIN BINDING PROTEIN; CATION CHANNEL; DEAD BOX PROTEIN; EPHRIN RECEPTOR; ESTROGEN RECEPTOR; HISTONE DEMETHYLASE; INITIATION FACTOR 2; NEUROKININ B; NEUROMEDIN B; NEUROPEPTIDE; OXYTOCIN RECEPTOR; PROLACTIN RECEPTOR; RNA HELICASE; SERINE PROTEINASE INHIBITOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARCUATE NUCLEUS; ARTICLE; BRAIN FUNCTION; CHROMATIN; ENDOCRINE SYSTEM; FEMALE; GENE EXPRESSION; GENETIC TRANSCRIPTION; GROWTH REGULATION; HYPOTHALAMUS; HYPOTHALAMUS VENTROMEDIAL NUCLEUS; MALE; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEUROMODULATION; NEUROTRANSMISSION; NONHUMAN; NUCLEOTIDE SEQUENCE; PREOPTIC AREA; PROTEIN EXPRESSION; QUANTITATIVE TRAIT LOCUS; REPRODUCTION; SEX DIFFERENCE; SIGNAL TRANSDUCTION; X CHROMOSOME; Y CHROMOSOME;

EID: 84862168342     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2012.00063     Document Type: Article

References (47)

1. Asarian, L., and Langhans, W. (2010). A new look on brain mechanisms of acute illness anorexia. Physiol. Behav. 100,464-471.
2. Badea, A., Johnson, G. A., and Williams, R. W. (2009). Genetic dissection of the mouse brain using high-field magnetic resonance microscopy. Neuroimage 45,1067-1079.
3. Becker, J. B. (1999). Gender differences in dopaminergic function in striatum and nucleus accum-bens. Pharmacol Biochem. Behav. 64, 803-812.
4. Becker, J. B., and Hu, M. (2008). Sex differences in drug abuse. Front. Neuroendocrinol. 29:36-47. doi: 10.1016/j.yfrne.2007.07.003
5. Bhasin, J. M., Chakrabarti, E., Peng, D. Q., Kulkarni, A., Chen, X., and Smith, J. D. (2008). Sex specific gene regulation and expression QTLs in mouse macrophages from a strain intercross. PLoS ONE 3, el435. doi:10.1371/journal.pone.0001435
6. Boone, E. M., Hawks, B. W., Li, W., and Garlow, S. J. (2008). Genetic regulation of hypothalamic cocaine and amphetamine-regulated transcript (CART) in BxD inbred mice. Brain Res. 1194, 1-7.
7. Brown, R. E., Mathieson, W. B., Sta-pleton, J., and Neumann, P. E. (1999). Maternal behavior in female C57BL/6J and DBA/2J inbred mice. Physiol Behav. 67, 599-605.
8. De Jonge, F. H., Louwerse, A. L., Ooms, M. P., Evers, P., Endert, E., and Van DePoll, N. E. (1989). Lesions of the SDN-POA inhibit sexual behavior of male Wistar rats. Brain Res. Bull 23, 483-492.
9. Dennis, G. Jr., Sherman, B. T., Hosack, D. A., Yang, J., Gao, W., Lane, H. C, and Lempicki, R. A. (2003). DAVID: database for annotation, visualization, and integrated discovery. Genome Biol 4, P3.
10. Garlow, S. J., Boone, E., Li, W., Owens, M. J., and Nemeroff, C. B. (2005). Genetic analysis of the hypothalamic corticotropin-releasing factor system. Endocrinology 146, 2362-2368.
11. Gorski, R. A., Gordon, J. H., Shryne, J. E., and Southam, A. M. (1978). Evidence for a morphological sex difference within the medial preoptic area of the rat brain. Brain Res. 148, 333-346.
12. Halbreich, U. (2006). Major depression is not a diagnosis, it is a departure point to differential diagnosis - clin ical and hormonal considerations (a commentary and elabora tion on Antonejevics paper). Psychoneuroendocrinology 31, 16-22.
13. Hofman,M. A.,andSwaab,D. F. (1989). The sexually dimorphic nucleus of the preoptic area in the human brain: a comparative morphometric study. J. Anat. 164,55-72.
14. Hong, S., Cho, Y. W., Yu, L. R., Yu, H., Veenstra, T. D., and Ge, K. (2007). Identification of JmjC domain-containing UTX and JMJD3 as his-tone H3 lysine 27 demethylases. Proc. Nad Acad. Sci. U.S.A. 104, 18439-18444.
15. Kajantie, E., and Phillips, D. I. (2006). The effects of sex and hormonal status on the physiological response to acute psychosocial stress. Psychoneuroendocrinology 31, 151-178.
16. Langfelder, P., Luo, R., Oldham, M. C, and Horvath, S. (2011). Is my network module preserved and reproducible? PLoS Comput. Biol. 7, el001057. doi:10.1371/jour-nal.pcbi. 1001057
17. Lasaga, M., and Debeljuk, L. (2011). Tachykinins and the hypothalamo-pituitary-gonadal axis: an update. Peptides 32, 1972-1978.
18. Lein, E. S., Hawrylycz, M. J., Ao, N., Ayres, M., Bensinger, A., Bernard, A., Boe, A. E, Boguski, M. S., Brock-way, K. S., Byrnes, E. J., Chen, L., Chen, T. M., Chin, M. C, Chong, J., Crook, B. E., Czaplinska, A., Dang, C. N., Datta, S., Dee, N. R., Desaki, A. L., Desta, T., Diep, E., Dolbeare, T. A., Donelan, M. J., Dong, H. W., Dougherty, J. G., Duncan, B. J., Ebbert, A. J., Eichele, G., Estin, L. K., Faber, C, Facer, B. A., Fields, R., Fischer, S. R., Fliss, T. P., Frens-ley, C, Gates, S. N., Glattfelder, K. J., Halverson, K. R., Hart, M. R., Hohmann, J. G., Howell, M. P., Jeung, D. P., Johnson, R. A., Karr, P. T., Kawal, R., Kidney, J. M., Knapik, R. H., Kuan, C. L, Lake, J. H., Laramee, A. R., Larsen, K. D., Lau, C, Lemon, T. A., Liang, A. J., Liu, Y., Luong, L. T., Michaels, J., Morgan, J. J., Morgan, R. J., Mortrud, M. T., Mosqueda, N. E, Ng, L. L., Ng, R., Orta, G. J., Overly, C. C, Pak, T. H., Parry, S. E., Pathak, S. D., Pearson, O. C, Puchalski, R. B., Riley, Z. L., Rockett, H. R., Rowland, S. A., Royall, J. J., Ruiz, M. J., Sarno, N. R., Schaffnit, K., Shapo-valova, N. V, Sivisay, T., Slaughter-beck, C. R., Smith, S. C, Smith, K. A., Smith, B. I., Sodt, A. J., Stewart, N. N., Stumpf, K. R., Sunkin, S. M., Sutram, M., Tarn, A., Teemer, C. D., Thaller, C, Thompson, C. L., Var-nam, L. R., Visel, A., Whitlock, R. M., Wohnoutka, P. E., Wolkey C. K., Wong, V.Y., Wood, M.,Yaylaoglu,M. B., Young, R. C, Youngstrom, B. L., Yuan, X. E, Zhang, B., Zwingman, T. A., and Jones, A. R. (2007). Genome-wide atlas of gene expression in the adult mouse brain. Nature 445, 168-176.
19. Lenz, K. M., and McCarthy, M. M. (2010). Organized for sex - steroid hormones and the developing hypothalamus. Eur. J. Neurosci. 32, 2096-2104.
20. Li, S. W, Arita, M., Fertala, A., Bao, Y., Kopen, G. C, Langsjo, T. K., Hyt-tinen, M. M., Helminen, H. J., and Prockop, D. J. (2001). Transgenic mice with inactive alleles for pro-collagen N-proteinase (ADAMTS-2) develop fragile skin and male sterility. Biochem. ]. 355,271-278.
21. Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 25, 402-408.
22. Lopes, A. M., Arnold-Croop, S. E., Amorim, A., and Carrel, L. (2011). Clustered transcripts that escape X inactivation at mouse XqD. Mamm. Genome 22, 572-582.
23. Majdic, G., and Tobet, S. (2011). Cooperation of sex chromosomal genes and endocrine influences for hypothalamic sexual differentiation. Front. Neuroendocrinol. 32:137-145. doi:10.1016/j.yfme.2011.02.009
24. Mathieson, W B., Taylor, S. W, Marshall, M., and Neumann, P. E. (2000). Strain and sex differences in the morphology of the medial preoptic nucleus of mice. J. Comp. Neurol. 428, 254-265.
25. Melo, J. A., Shendure, J., Pociask, K., and Silver, L. M. (1996). Identification of sex-specific quantitative trait loci controlling alcohol preference in C57BL/6 mice. Nat. Genet. 13, 147-153.
26. Mozhui, K., Ciobanu, D. C, Schiko-rski, T., Wang, X., Lu, L., and Williams, R. W. (2008). Dissection of a QTL hotspot on mouse distal chromosome 1 that modulates neu-robehavioral phenotypes and gene expression. PLoS Genet. 4,el000260. doi:10.1371/joumal.pgen.l000260
27. Navarro, V M., Ruiz-Pino, F., Sanchez-Garrido, M. A., Garcia-Galiano, D., Hobbs, S. J., Manfredi-Lozano, M., Leon, S., Sangiao-Alvarellos, S., Castellano, J. M., Clifton, D. K., Pinilla, L., Steiner, R. A., and Tena-Sempere, M. (2012). Role of neu-rokinin B in the control of female puberty and its modulation by metabolic status. J. Neurosci. 32, 2388-2397.
28. Ober, C, Loisel, D. A., and Gilad, Y. (2008). Sex-specific genetic architecture of human disease. Nat. Rev. Genet. 9,911-922.
29. Oldham, M. C, Horvath, S., and Geschwind, D. H. (2006). Conservation and evolution of gene coexpression networks in human and chimpanzee brains. Proc. Natl. Acad. Sci. U.S.A. 103, 17973-17978.
30. Oldham, M. C, Konopka, G., Iwamoto, K., Langfelder, P., Kato, T., Horvath, S., and Geschwind, D. H. (2008). Functional organization of the transcriptome in human brain. Nat. Neurosci. 11, 1271-1282.
31. Peirce, J. L., Li, H., Wang, J., Manly, K. E, Hitzemann, R. J., Belknap, J. K., Rosen, G. D., Goodwin, S., Sutter, T. R., Williams, R. W., and Lu, L. (2006). How replicable are mRNA expression QTL? Mamm. Genome 17,643-656.
32. Peirce, J. L., Lu, L., Gu, J., Silver, L. M., and Williams, R. W (2004). A new set of BXD recombinant inbred lines from advanced intercross populations in mice. BMC Genet. 5, 7. doi:10.1186/1471-2156-5-7
33. Ranee, N. E., Krajewski, S. J., Smith, M. A., Cholanian, M., and Dacks, P. A. (2010). Neurokinin B and the hypothalamic regulation of reproduction. Brain Res. 1364, 116-128.
34. Ravasz, E., Somera, A. L., Mongru, D. A., Oltvai, Z. N., and Barabasi, A. L. (2002). Hierarchical organization of modularity in metabolic networks. Science 297, 1551-1555.
35. Reinius, B., Saetre, P., Leonard, J. A., Blekhman, R., Merino-Martinez, R., Gilad, Y., and Jazin, E. (2008). An evolutionary conserved sexual signature in the primate brain. PLoS Genet. 4, elOOOlOO. doi:10.1371/journal.pgen.l000100
36. Reinius, B., Shi, C, Hengshuo, L., Sandhu, K. S., Radomska, K. J., Rosen, G. D., Lu, L, Kullander, K., Williams, R. W, and Jazin, E. (2010). Female-biased expression of long non-coding RNAs in domains that escape X-inactivation in mouse. BMC Genomics 11, 614. doi:10.1186/1471-2164-11-614
37. Rozen, S., and Skaletsky, H. (2000). Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol. 132, 365-386.
38. Simerly, R. B. (1998). Organization and regulation of sexually dimorphic neuroendocrine pathways. Behav. Brain Res. 92, 195-203.
39. Taylor, B. A., Wnek, C, Kotlus, B. S., Roemer, N., Mactaggart, T., and Phillips, S. J. (1999). Genotyp-ing new BXD recombinant inbred mouse strains and comparison of BXD and consensus maps. Mamm. Genome 10, 335-348.
40. van Nas, A., Guhathakurta, D., Wang, S. S., Yehya, N., Horvath, S., Zhang, B., Ingram-Drake,L., Chaudhuri, G., Schadt, E. E., Drake, T. A., Arnold, A. P., and Lusis, A. J. (2009). Elucidating the role of gonadal hormones in sexually dimorphic gene coexpres-sion networks. Endocrinology 150, 1235-1249.
41. Wang, S. S., Schadt, E. E., Wang, H., Wang, X., Ingram-Drake, L., Shi, W, Drake, T. A., and Lusis, A. J. (2007). Identification of pathways for atherosclerosis in mice: integration of quantitative trait locus analysis and global gene expression data. Circ. Res. 101,ell-e30.
42. Weiss, L. A., Pan, L., Abney, M., and Ober, C. (2006). The sex-specific genetic architecture of quantitative traits in humans. Nat. Genet. 38, 218-222.
43. Winden, K. D., Oldham, M. C, Mir-nics, K., Ebert, P. J., Swan, C. H., Levitt, P., Rubenstein, J. L., Horvath, S.,and Geschwind,D. H. (2009). The organization of the transcriptional network in specific neuronal classes. Mol.Syst.Biol 5,291.
44. Woods, S. C, Gotoh, K., and Clegg, D. J. (2003). Gender differences in the control of energy homeostasis. Exp. Biol Med. 228,1175-1180.
45. Xu, J., Deng, X., Watkins, R., and Dis-teche, C. M. (2008). Sex-specific differences in expression of histone demethylases Utx and Uty in mouse brain and neurons. J. Neurosci. 28, 4521-4527.
46. Yang, X., Schadt, E. E., Wang, S., Wang, H., Arnold, A. P., Ingram-Drake, L., Drake, T. A., and Lusis, A. J. (2006). Tissue-specific expression and regulation of sexually dimorphic genes in mice. Genome Res. 16, 995-1004.
47. Zhang, B., and Horvath, S. (2005). A general framework for weighted gene co-expression network analysis. Stat. Appl. Genet. Mol. Biol. 4, Article 17.