Estrogen is a novel regulator of Tnfaip1 in mouse hippocampus

  • Authors:
    • Hui Liu
    • Liping Yang
    • Yingchun Zhao
    • Guihua Zeng
    • Yaosong Wu
    • Yulong Chen
    • Jian Zhang
    • Qingru Zeng
  • View Affiliations

  • Published online on: April 11, 2014     https://doi.org/10.3892/ijmm.2014.1742
  • Pages: 219-227
Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )
Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )


Abstract

Tumor necrosis factor‑induced protein 1 (Tnfaip1), also known as B12, has been previously identified as a tumor necrosis factor-α (TNF-α)-inducible protein and is involved in the cytokinesis signaling pathway, DNA synthesis, innate immunity, cell apoptosis, Alzheimer's disease (AD) and type 2 diabetic nephropathy. However, little is known regarding the expression of Tnfaip1 in various tissues or its accurate role in these physiological functions. The focus of this study was on Tnfaip1 expression in different tissues, with a high expression in mouse hippocampus being identified. The age- and gender‑related expression of Tnfaip1 in hippocampus was also investigated. The distribution of Tnfaip1 was mapped using fluorescent immunostaining. Although immunoactivity was found in the CA1, CA3 and DG subregions of the hippocampus in E17.5 and P6 mice, strong staining was only detected in the CA3 subregion in adult mice. These data suggested that Tnfaip1 expression in hippocampus may be regulated by estrogen. Further study showed that the expression of Tnfaip1 in the hippocampus was significantly increased in ovariecto­mized mice compared to Sham mice. In cultured primary hippocampal cells, Tnfaip1 showed different expression levels in different treatments of estrogen or estrogen receptor antagonists. Additional experiments demonstrated the existence of a binding site of ERβ in the Tnfaip1 promoter region, and that ERβ was able to upregulate Tnfaip1 expression. Our study identified a new regulatory factor and a primary regulatory mechanism of Tnfaip1 expression in hippocampus. Since both hippocampus and estrogen are crucial in AD, the results also showed a potential association between Tnfaip1 and hippocampal-related diseases, such as AD, which may be affected by the estrogen level.

References

1 

Wolf FW, Marks RM, Sarma V, et al: Characterization of a novel tumor necrosis factor-alpha-induced endothelial primary response gene. J Biol Chem. 267:1317–1326. 1992.PubMed/NCBI

2 

Zhou J, Hu X, Xiong X, et al: Cloning of two rat PDIP1 related genes and their interactions with proliferating cell nuclear antigen. J Exp Zool A Comp Exp Biol. 303:227–240. 2005. View Article : Google Scholar : PubMed/NCBI

3 

Link CD, Taft A, Kapulkin V, et al: Gene expression analysis in a transgenic Caenorhabditis elegans Alzheimer’s disease model. Neurobiol Aging. 24:397–413. 2003. View Article : Google Scholar : PubMed/NCBI

4 

Zhou J, Ren K, Liu X, Xiong X, Hu X and Zhang J: A novel PDIP1-related protein, KCTD10, that interacts with proliferating cell nuclear antigen and DNA polymerase delta. Biochim Biophys Acta. 1729:200–203. 2005. View Article : Google Scholar : PubMed/NCBI

5 

Smith TC, Fang Z and Luna EJ: Novel interactors and a role for supervillin in early cytokinesis. Cytoskeleton (Hoboken). 67:346–364. 2010.PubMed/NCBI

6 

Liu XW, Lu FG, Zhang GS, et al: Proteomics to display tissue repair opposing injury response to LPS-induced liver injury. World J Gastroenterol. 10:2701–2705. 2004.PubMed/NCBI

7 

Yang LP, Zhou AD, Li H, et al: Expression profile in the cell lines of human TNFAIP1 gene. Yi Chuan. 28:918–922. 2006.(In Chinese).

8 

Yang L, Liu N, Hu X, et al: CK2 phosphorylates TNFAIP1 to affect its subcellular localization and interaction with PCNA. Mol Biol Rep. 37:2967–2973. 2010. View Article : Google Scholar : PubMed/NCBI

9 

Gupta J, Gaikwad AB and Tikoo K: Hepatic expression profiling shows involvement of PKC epsilon, DGK eta, Tnfaip, and Rho kinase in type 2 diabetic nephropathy rats. J Cell Biochem. 111:944–954. 2010. View Article : Google Scholar : PubMed/NCBI

10 

Kuiper GG, Shughrue PJ, Merchenthaler I and Gustafsson JA: The estrogen receptor beta subtype: a novel mediator of estrogen action in neuroendocrine systems. Front Neuroendocrinol. 19:253–286. 1998. View Article : Google Scholar : PubMed/NCBI

11 

Hultcrantz M, Simonoska R and Stenberg AE: Estrogen and hearing: a summary of recent investigations. Acta Otolaryngol. 126:10–14. 2006. View Article : Google Scholar : PubMed/NCBI

12 

Nilsson S, Mäkelä S, Treuter E, et al: Mechanisms of estrogen action. Physiol Rev. 81:1535–1565. 2001.

13 

Wehrenberg U, Prange-Kiel J and Rune GM: Steroidogenic factor-1 expression in marmoset and rat hippocampus: co-localization with StAR and aromatase. J Neurochem. 76:1879–1886. 2001. View Article : Google Scholar : PubMed/NCBI

14 

Prange-Kiel J, Wehrenberg U, Jarry H and Rune GM: Para/autocrine regulation of estrogen receptors in hippocampal neurons. Hippocampus. 13:226–234. 2003. View Article : Google Scholar : PubMed/NCBI

15 

Kretz O, Fester L, Wehrenberg U, et al: Hippocampal synapses depend on hippocampal estrogen synthesis. J Neurosci. 24:5913–5921. 2004. View Article : Google Scholar : PubMed/NCBI

16 

Prange-Kiel J and Rune GM: Direct and indirect effects of estrogen on rat hippocampus. Neuroscience. 138:765–772. 2006. View Article : Google Scholar : PubMed/NCBI

17 

Green PS, Yang SH, Nilsson KR, Kumar AS, Covey DF and Simpkins JW: The nonfeminizing enantiomer of 17beta-estradiol exerts protective effects in neuronal cultures and a rat model of cerebral ischemia. Endocrinology. 142:400–406. 2001.PubMed/NCBI

18 

Gould E, Woolley CS, Frankfurt M and McEwen BS: Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J Neurosci. 10:1286–1291. 1990.PubMed/NCBI

19 

Woolley CS, Gould E, Frankfurt M and McEwen BS: Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. J Neurosci. 10:4035–4039. 1990.PubMed/NCBI

20 

Moran AL, Warren GL and Lowe DA: Removal of ovarian hormones from mature mice detrimentally affects muscle contractile function and myosin structural distribution. J Appl Physiol. 100:548–559. 2006. View Article : Google Scholar

21 

Moran AL, Nelson SA, Landisch RM, Warren GL and Lowe DA: Estradiol replacement reverses ovariectomy-induced muscle contractile and myosin dysfunction in mature female mice. J Appl Physiol. 102:1387–1393. 2007. View Article : Google Scholar : PubMed/NCBI

22 

Flavin MP, Coughlin K and Ho LT: Soluble macrophage factors trigger apoptosis in cultured hippocampal neurons. Neuroscience. 80:437–448. 1997. View Article : Google Scholar : PubMed/NCBI

23 

Viesselmann C, Ballweg J, Lumbard D and Dent EW: Nucleofection and primary culture of embryonic mouse hippocampal and cortical neurons. J Vis Exp. pii: 2373 View Article : Google Scholar

24 

Hyman BT, Van Hoesen GW, Kromer LJ and Damasio AR: Perforant pathway changes and the memory impairment of Alzheimer’s disease. Ann Neurol. 20:472–481. 1986.

25 

Li XG, Somogyi P, Ylinen A and Buzsaki G: The hippocampal CA3 network: an in vivo intracellular labeling study. J Comp Neurol. 339:181–208. 1994. View Article : Google Scholar : PubMed/NCBI

26 

Barger SW, Hörster D, Furukawa K, Goodman Y, Krieglstein J and Mattson MP: Tumor necrosis factors alpha and beta protect neurons against amyloid beta-peptide toxicity: evidence for involvement of a kappa B-binding factor and attenuation of peroxide and Ca2+ accumulation. Proc Natl Acad Sci USA. 92:9328–9332. 1995. View Article : Google Scholar

27 

Amaral DG and Witter MP: The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience. 31:571–591. 1989. View Article : Google Scholar : PubMed/NCBI

28 

Hasselmo ME: The role of hippocampal regions CA3 and CA1 in matching entorhinal input with retrieval of associations between objects and context: theoretical comment on Lee et al (2005). Behav Neurosci. 119:342–345. 2005. View Article : Google Scholar : PubMed/NCBI

29 

Lee I and Kesner RP: Differential contribution of NMDA receptors in hippocampal subregions to spatial working memory. Nat Neurosci. 5:162–168. 2002. View Article : Google Scholar : PubMed/NCBI

30 

Kesner RP, Lee I and Gilbert P: A behavioral assessment of hippocampal function based on a subregional analysis. Rev Neurosci. 15:333–351. 2004. View Article : Google Scholar : PubMed/NCBI

31 

Hunsaker MR, Allan KD and Kesner RP: Role of dCA3 efferents via the fimbria in the acquisition of a delay nonmatch to place task. Hippocampus. 17:494–502. 2007. View Article : Google Scholar : PubMed/NCBI

32 

Lee I, Jerman TS and Kesner RP: Disruption of delayed memory for a sequence of spatial locations following CA1- or CA3-lesions of the dorsal hippocampus. Neurobiol Learn Mem. 84:138–147. 2005. View Article : Google Scholar : PubMed/NCBI

33 

Tanila H: Hippocampal place cells can develop distinct representations of two visually identical environments. Hippocampus. 9:235–246. 1999. View Article : Google Scholar : PubMed/NCBI

34 

Leutgeb JK, Leutgeb S, Moser MB and Moser EI: Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science. 315:961–966. 2007. View Article : Google Scholar : PubMed/NCBI

35 

Palmer A and Good M: Hippocampal synaptic activity, pattern separation and episodic-like memory: implications for mouse models of Alzheimer’s disease pathology. Biochem Soc Trans. 39:902–909. 2011.PubMed/NCBI

36 

McEwen B: Estrogen actions throughout the brain. Recent Prog Horm Res. 57:357–384. 2002. View Article : Google Scholar : PubMed/NCBI

37 

Leranth C, Shanabrough M and Redmond DE Jr: Gonadal hormones are responsible for maintaining the integrity of spine synapses in the CA1 hippocampal subfield of female nonhuman primates. J Comp Neurol. 447:34–42. 2002. View Article : Google Scholar : PubMed/NCBI

38 

Leranth C, Shanabrough M and Horvath TL: Hormonal regulation of hippocampal spine synapse density involves subcortical mediation. Neuroscience. 101:349–356. 2000. View Article : Google Scholar : PubMed/NCBI

39 

Prange-Kiel J, Rune GM and Leranth C: Median raphe mediates estrogenic effects to the hippocampus in female rats. Eur J Neurosci. 19:309–317. 2004. View Article : Google Scholar : PubMed/NCBI

40 

Leranth C and Shanabrough M: Supramammillary area mediates subcortical estrogenic action on hippocampal synaptic plasticity. Exp Neurol. 167:445–450. 2001. View Article : Google Scholar : PubMed/NCBI

41 

Lâm TT and Leranth C: Role of the medial septum diagonal band of Broca cholinergic neurons in oestrogen-induced spine synapse formation on hippocampal CA1 pyramidal cells of female rats. Eur J Neurosci. 17:1997–2005. 2003.

42 

Leranth C, Shanabrough M and Horvath TL: Estrogen receptor-alpha in the raphe serotonergic and supramammillary area calretinin-containing neurons of the female rat. Exp Brain Res. 128:417–420. 1999. View Article : Google Scholar : PubMed/NCBI

43 

Leranth C and Vertes RP: Median raphe serotonergic innervation of medial septum/diagonal band of broca (MSDB) parvalbumin-containing neurons: possible involvement of the MSDB in the desynchronization of the hippocampal EEG. J Comp Neurol. 410:586–598. 1999. View Article : Google Scholar

44 

Bryant DN, Sheldahl LC, Marriott LK, Shapiro RA and Dorsa DM: Multiple pathways transmit neuroprotective effects of gonadal steroids. Endocrine. 29:199–207. 2006. View Article : Google Scholar : PubMed/NCBI

45 

Kelly MJ and Rønnekleiv OK: Membrane-initiated estrogen signaling in hypothalamic neurons. Mol Cell Endocrinol. 290:14–23. 2008. View Article : Google Scholar : PubMed/NCBI

46 

Singer CA, Figueroa-Masot XA, Batchelor RH and Dorsa DM: The mitogen-activated protein kinase pathway mediates estrogen neuroprotection after glutamate toxicity in primary cortical neurons. J Neurosci. 19:2455–2463. 1999.

47 

Mize AL, Shapiro RA and Dorsa DM: Estrogen receptor-mediated neuroprotection from oxidative stress requires activation of the mitogen-activated protein kinase pathway. Endocrinology. 144:306–312. 2003. View Article : Google Scholar

48 

Honda K, Sawada H, Kihara T, et al: Phosphatidylinositol 3-kinase mediates neuroprotection by estrogen in cultured cortical neurons. J Neurosci Res. 60:321–327. 2000. View Article : Google Scholar : PubMed/NCBI

49 

Harms C, Lautenschlager M, Bergk A, et al: Differential mechanisms of neuroprotection by 17 beta-estradiol in apoptotic versus necrotic neurodegeneration. J Neurosci. 21:2600–2609. 2001.PubMed/NCBI

50 

Cimarosti H, Zamin LL, Frozza R, et al: Estradiol protects against oxygen and glucose deprivation in rat hippocampal organotypic cultures and activates Akt and inactivates GSK-3beta. Neurochem Res. 30:191–199. 2005. View Article : Google Scholar : PubMed/NCBI

51 

Funakoshi T, Yanai A, Shinoda K, Kawano MM and Mizukami Y: G protein-coupled receptor 30 is an estrogen receptor in the plasma membrane. Biochem Biophys Res Commun. 346:904–910. 2006. View Article : Google Scholar : PubMed/NCBI

52 

Toran-Allerand CD: Estrogen and the brain: beyond ER-alpha, ER-beta, and 17beta-estradiol. Ann NY Acad Sci. 1052:136–144. 2005. View Article : Google Scholar : PubMed/NCBI

53 

Gruber CJ, Gruber DM, Gruber IM, Wieser F and Huber JC: Anatomy of the estrogen response element. Trends Endocrinol Metab. 15:73–78. 2004. View Article : Google Scholar : PubMed/NCBI

54 

Paech K, Webb P, Kuiper GG, et al: Differential ligand activation of estrogen receptors ERalpha and ERbeta at AP1 sites. Science. 277:1508–1510. 1997. View Article : Google Scholar : PubMed/NCBI

55 

Xiao CW and Goff AK: Hormonal regulation of oestrogen and progesterone receptors in cultured bovine endometrial cells. J Reprod Fertil. 115:101–109. 1999. View Article : Google Scholar : PubMed/NCBI

56 

Murata T, Narita K, Honda K and Higuchi T: Changes of receptor mRNAs for oxytocin and estrogen during the estrous cycle in rat uterus. J Vet Med Sci. 65:707–712. 2003. View Article : Google Scholar : PubMed/NCBI

57 

Tena-Sempere M, Navarro VM, Mayen A, Bellido C and Sanchez-Criado JE: Regulation of estrogen receptor (ER) isoform messenger RNA expression by different ER ligands in female rat pituitary. Biol Reprod. 70:671–678. 2004. View Article : Google Scholar : PubMed/NCBI

Related Articles

Journal Cover

July 2014
Volume 34 Issue 1

Print ISSN: 1107-3756
Online ISSN:1791-244X

Sign up for eToc alerts

Recommend to Library

Copy and paste a formatted citation
APA
Liu, H., Yang, L., Zhao, Y., Zeng, G., Wu, Y., Chen, Y. ... Zeng, Q. (2014). Estrogen is a novel regulator of Tnfaip1 in mouse hippocampus. International Journal of Molecular Medicine, 34, 219-227. https://doi.org/10.3892/ijmm.2014.1742
MLA
Liu, H., Yang, L., Zhao, Y., Zeng, G., Wu, Y., Chen, Y., Zhang, J., Zeng, Q."Estrogen is a novel regulator of Tnfaip1 in mouse hippocampus". International Journal of Molecular Medicine 34.1 (2014): 219-227.
Chicago
Liu, H., Yang, L., Zhao, Y., Zeng, G., Wu, Y., Chen, Y., Zhang, J., Zeng, Q."Estrogen is a novel regulator of Tnfaip1 in mouse hippocampus". International Journal of Molecular Medicine 34, no. 1 (2014): 219-227. https://doi.org/10.3892/ijmm.2014.1742