MiRNA-451 is a potential biomarker for estrogenicity in mouse uterus

Lingyan HOU , Yun LU , Ying LI , Li LI

Front. Environ. Sci. Eng. ›› 2014, Vol. 8 ›› Issue (1) : 99 -105.

PDF (220KB)
Front. Environ. Sci. Eng. ›› 2014, Vol. 8 ›› Issue (1) : 99 -105. DOI: 10.1007/s11783-013-0490-7
RESEARCH ARTICLE
RESEARCH ARTICLE

MiRNA-451 is a potential biomarker for estrogenicity in mouse uterus

Author information +
History +
PDF (220KB)

Abstract

The uterotrophic assay has been commonly used to test environmental estrogens in vivo, however, it is often not sensitive enough sometimes. An alternative way is to evaluate estrogenicity through biomarker genes. MicroRNA (miRNA) is a class of regulatory gene, which has been shown to be a good biomarker for many diseases and toxicological effects in recent years, and some evidences showed that estrogen induced response was partially mediated by miRNAs. In this study, two types of microarrays were used to test the 17β-estradiol (E2) induced miRNA expression profile at different time points in the immature mouse uterus. Statistical analysis showed the aldehyde slide based array had less variation than the amino slide based array, and 11 dysregulated miRNAs were screened out for significant fold change. Real-time PCR was performed to further confirm that 4 out of 7 selected miRNAs, namely miR-451, miR-155, miR-335-5p, and miR-365, are E2 regulated miRNAs in the uterus. The function of the predicted targets of these miRNAs is involved in cell grow control, which is consistent with the main E2 function in the uterus. MiR-451 had similar strong responses to E2 in the uterus of both immature and overiectomized mice, and could be a potential biomarker for estrogenicity in the uterus.

Keywords

estrogen / microRNA (miRNA) / microarray / biomarker

Cite this article

Download citation ▾
Lingyan HOU, Yun LU, Ying LI, Li LI. MiRNA-451 is a potential biomarker for estrogenicity in mouse uterus. Front. Environ. Sci. Eng., 2014, 8(1): 99-105 DOI:10.1007/s11783-013-0490-7

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Dechering K, Boersma C, Mosselman S. Estrogen receptors α and β: two receptors of a kind? Current Medicinal Chemistry, 2000, 7(8): 561–576

[2]

Nilsson S, Gustafsson J A. Biological role of estrogen and estrogen receptors. Critical Reviews in Biochemistry and Molecular Biology, 2002, 37(1): 1–28

[3]

Gruber C J, Tschugguel W, Schneeberger C, Huber J C. Production and actions of estrogens. The New England Journal of Medicine, 2002, 346(5): 340–352

[4]

Erickson B E. Next-generation risk assessment. Chemical and Engineering News, 2009, 87(25): 30–33

[5]

Moggs J G. Molecular responses to xenoestrogens: mechanistic insights from toxicogenomics. Toxicology, 2005, 213(3): 177–193

[6]

Sharpe R M. The ‘oestrogen hypothesis’–where do we stand now? International Journal of Andrology, 2003, 26(1): 2–15

[7]

Sikka S C, Wang R. Endocrine disruptors and estrogenic effects on male reproductive axis. Asian Journal of Andrology, 2008, 10(1): 134–145

[8]

Markey C M, Michaelson C L, Veson E C, Sonnenschein C, Soto A M. The mouse uterotrophic assay: a reevaluation of its validity in assessing the estrogenicity of bisphenol A. Environmental Health Perspectives, 2001, 109(1): 55–60

[9]

Choi K C, Jeung E B. The biomarker and endocrine disruptors in mammals. Journal of Reproduction and Development, 2003, 49(5): 337–345

[10]

Heppell S A, Denslow N D, Folmar L C, Sullivan C V. Universal assay of vitellogenin as a biomarker for environmental estrogens. Environmental Health Perspectives, 1995, 103(Suppl 7): 9–15

[11]

An B S, Choi K C, Kang S K. Novel Calbindin-D(9K) protein as a useful biomarker for environmental estrogenic compounds in the uterus of immature rats. Reproductive Toxicology (Elmsford, N.Y.), 2003, 17(3): 311–319

[12]

Jung Y W, Hong E J, Choi K C, Jeung E B. Novel progestogenic activity of environmental endocrine disruptors in the upregulation of calbindin-D9k in an immature mouse model. Toxicological sciences, 2005, 83(1): 78–88

[13]

An B S, Kang S K, Shin J H, Jeung E B. Stimulation of calbindin- D(9k) mRNA expression in the rat uterus by octyl-phenol, nonylphenol and bisphenol. Molecular and Cellular Endocrinology, 2002, 191(2): 177–186

[14]

Ciesla M, Skrzypek K, Kozakowska M, Loboda A, Jozkowicz A, Dulak J. MicroRNAs as biomarkers of disease onset. Analytical and Bioanalytical Chemistry, 2011, 401(7): 2051–2061

[15]

Wang B, Majumder S, Nuovo G, Kutay H, Volinia S, Patel T, Schmittgen T D, Croce C, Ghoshal K, Jacob S T. Role of microRNA-155 at early stages of hepatocarcinogenesis induced by choline-deficient and amino acid-defined diet in c57BL/6 mice. Hepatology (Baltimore, Md.), 2009, 50(4): 1152–1161

[16]

Wang W X, Rajeev B W, Stromberg A J, Ren N, Tang G L, Huang Q W, Rigoutsos I, Nelson P T. The expression of microRNA miR-107 decreases early in Alzheimer’s disease and may accelerate disease progression through regulation of beta-site amyloid precursor protein-cleaving enzyme 1. The Journal of Neuroscience, 2008, 28(5): 1213–1223

[17]

Wang K, Marzolf B, Troisch P, Brightman A, Hu Z Y, Hood L E, Zhang S L, Galas D J. Circulating microRNAs, potential biomarkers for drug-induced liver injury. In: Proceedings of the National Academy of Sciences of the United, 2009, 106(11): 4402–4407

[18]

Ambros V. The functions of animal microRNAs. Nature, 2004, 431(7006): 350–355

[19]

Bartel D P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 2004, 116(2): 281–297

[20]

Griffiths-Jones S,Saini H K, Dongen S, Enright A J. MiRbase: tools for microRNA genomics. Nucleic Acids Receaprch, 2008, 36(S1): 1540–158

[21]

Yokoi T, Nakajima M. Toxicological implications of modulation of gene expression by microRNAs. Toxicological Sciences, 2011, 123(1): 1–14

[22]

Couzin J. Genetics-Erasing microRNAs reveals their powerful punch. Science, 2007, 316(5824): 530–530

[23]

Kovalchuk O, Tryndyak V P, Montgomery B, Boyko A, Kutanzi K, Zemp F, Warbritton A R, Latendresse J R, Kovalchuk I, Beland F A, Pogribny I P. Estrogen-induced rat breast carcinogenesis is characterized by alterations in DNA methylation, histone modifications and aberrant microRNA expression. Cell Cycle (Georgetown, Tex.), 2007, 6(16): 2010–2018

[24]

Dai R, Phillips R A, Zhang Y, Khan D, Crasta O, Ahmed S A. Suppression of LPS-induced Interferon-gamma and nitric oxide in splenic lymphocytes by select estrogen-regulated microRNAs: a novel mechanism of immune modulation. Blood, 2008, 112(12): 4591–4597

[25]

Nothnick W B, Healy C. Estrogen induces distinct patterns of microRNA expression within the mouse uterus. Reproductive Sciences (Thousand Oaks, Calif.), 2010, 17(11): 987–994

[26]

Lewis B P, Shih I H, Jones-Rhoades M W, Bartel D P, Burge C B. Prediction of mammalian microRNA targets. Cell, 2003, 115(7): 787–798

[27]

Krek A, Grün D, Poy M N, Wolf R, Rosenberg L, Epstein E J, MacMenamin P, da Piedade I, Gunsalus K C, Stoffel M, Rajewsky N. Combinatorial microRNA target predictions. Nature Genetics, 2005, 37(5): 495–500

[28]

John B, Enright A J, Aravin A, Tuschl T, Sander C, Marks D S. Human microRNA targets. PLoS Biology, 2004, 2(11): 1862–1879

[29]

Moggs J G, Tinwell H, Spurway T, Chang H S, Pate I, Lim F L, Moore D J, Soames A, Stuckey R, Currie R, Zhu T, Kimber I, Ashby J, Orphanides G. Phenotypic anchoring of gene expression changes during estrogen-induced uterine growth. Environmental Health Perspectives, 2004, 112(16): 1589–1606

[30]

Klinge C M. Estrogen regulation of microRNA expression. Current Genomics, 2009, 10(3): 169–183

[31]

Hewitt S C, Deroo B J, Hansen K, Collins J, Grissom S, Afshari C A, Korach K S. Estrogen receptor-dependent genomic responses in the uterus mirror the biphasic physiological response to estrogen. Molecular Endocrinology (Baltimore, Md.), 2003, 17(10): 2070–2083

[32]

Hong S H, Nah H Y, Lee J Y, Gye M C, Kim C H, Kim M K. Analysis of estrogen-regulated genes in mouse uterus using cDNA microarray and laser capture microdissection. Journal of Endocrinology, 2004, 181(1): 157–167

[33]

Watanabe H, Suzuki A, Kobayashi M, Takahashi E, Itamoto M, Lubahn D B, Handa H, Iguchi T. Analysis of temporal changes in the expression of estrogen-regulated genes in the uterus. The Journal of Molecular Endocrinology, 2003, 30(3): 347–358

[34]

Naciff J M, Overmann G J, Torontali S M, Carr G J, Tiesman J P, Richardson B D, Daston G P. Gene expression profile induced by 17 alpha-ethynyl estradiol in the prepubertal female reproductive system of the rat. Toxicological Sciences, 2003, 72(2): 314–330

[35]

Wu X, Pang S T, Sahlin L, Blanck A, Norstedt G, Flores-Morales A. Gene expression profiling of the effects of castration and estrogen treatment in the rat uterus. Biology of Reproduction, 2003, 69(4): 1308–1317

[36]

Kang K S, Kim H S, Ryu D Y, Che J H, Lee Y S. Immature uterotrophic assay is more sensitive than ovariectomized uterotrophic assay for the detection of estrogenicity of p-nonylphenol in Sprague-Dawley rats. Toxicology Letters, 2000, 118(1–2): 109–115

[37]

Nothnick W B, Healy C. Estrogen induces distinct patterns of microRNA expression within the mouse uterus. Reproductive Sciences (Thousand Oaks, Calif.), 2010, 17(11): 987–994

[38]

Moggs J G, Tinwell H, Spurway T, Chang H S, Pate I, Lim F L, Moore D J, Soames A, Stuckey R, Currie R, Zhu T, Kimber I, Ashby J, Orphanides G. Phenotypic anchoring of gene expression changes during estrogen-induced uterine growth. Environmental Health Perspectives, 2004, 112(16): 1589–1606

[39]

Ferenczy A. Studies on the cytodynamics of human endometrial regeneration. I. Scanning electron microscopy. American Journal of Obstetrics and Gynecology, 1976, 124(1): 64–74

[40]

Punyadeera C, Verbost P, Groothuis P. Oestrogen and progestin responses in human endometrium. The Journal of Steroid Biochemistry and Molecular Biology, 2003, 84(4): 393–410

[41]

Rosenfeld C S, Roberts R M, Lubahn D B. Estrogen receptor- and aromatase-deficient mice provide insight into the roles of estrogen within the ovary and uterus. Molecular Reproduction and Development, 2001, 59(3): 336–346

[42]

Honda K, Sawada H, Kihara T, Urushitani M, Nakamizo T, Akaike A, Shimohama S. Phosphatidylinositol 3-kinase mediates neuroprotection by estrogen in cultured cortical neurons. Journal of Neuroscience Research, 2000, 60(3): 321–327

[43]

Ivanova T, Mendez P, Garcia-Segura L M, Beyer C. Rapid stimulation of the PI3-kinase/Akt signalling pathway in developing midbrain neurones by oestrogen. Journal of Neuroendocrinology, 2002, 14(1): 73–79

[44]

Castoria G, Migliaccio A, Bilancio A, Di Domenico M, de Falco A, Lombardi M, Fiorentino R, Varricchio L, Barone M V, Auricchio F. PI3-kinase in concert with Src promotes the S-phase entry of oestradiol-stimulated MCF-7 cells. The EMBO Journal, 2001, 20(21): 6050–6059

[45]

Sun M, Paciga J E, Feldman R I, Yuan Z, Coppola D, Lu Y Y, Shelley S A, Nicosia S V, Cheng J Q. Phosphatidylinositol-3-OH kinase (PI3K)/Akt2, activated in breast cancer, regulates and is induced by estrogen receptor alpha (ER alpha) via interaction between ERa and PI3K. Cancer Research, 2001, 61(16): 5985–5991

[46]

Lee Y R, Park J, Yu H N, Kim J S, Youn H J, Jung S H.Up-regulation of PI3K/Akt signaling by 17b-estradiol through activation of estrogen receptor-a, but not estrogen receptor-b, and stimulates cell growth in breast cancer cells. Biochemist biophysics Research Commune, 2005, 336: 1221–1226

[47]

Dery M C, Leblanc V, Shooner C, Asselin E. Regulation of Akt expression and phosphorylation by 17beta-estradiol in the rat uterus during estrous cycle. Reproductive biology and endocrinology, 2003, 1(1): 47

[48]

Lengyel F, Vértes Z, Kovács K A, Környei J L, Sumegi B, Vértes M. Expression and activation of Akt/protein kinase B in sexually immature and mature rat uterus. The Journal of Steroid Biochemistry and Molecular Biology, 2004, 91(4–5): 285–288

[49]

Chen B, Pan H, Zhu L, Deng Y, Pollard J W. Progesterone inhibits the estrogen-induced phosphoinositide 3-kinase→AKT→GSK-3beta→cyclin D1→pRB pathway to block uterine epithelial cell proliferation. Molecular Endocrinology (Baltimore, Md.), 2005, 19(8): 1978–1990

RIGHTS & PERMISSIONS

Higher Education Press and Springer-Verlag Berlin Heidelberg

AI Summary AI Mindmap
PDF (220KB)

2134

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/