MicroRNA expression and regulation in the uterus during embryo implantation in rat

FEBS Journal

Volumn 281, Issue 7, 2014, Pages 1872-1891

  Xia, Hong Fei ^a,b   Jin, Xiao Hua ^a   Cao, Zong Fu ^a   Hu, Yi ^a   Ma, Xu ^a,b  

^a NATIONAL RESEARCH INSTITUTE FOR FAMILY PLANNING   (China)

^b GRADUATE SCHOOL OF PEKING UNION MEDICAL COLLEGE   (China)

Author keywords

Bcl 2 family; embryo implantation; miR 29a; miRNAs; rat uterus

Indexed keywords

MICRORNA; MICRORNA 29A; PROTEIN BCL W; PROTEIN MCL 1;

3' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BAK1 GENE; BCL W GENE; BMF GENE; CONTROLLED STUDY; DECIDUALIZATION; DOWN REGULATION; ENDOMETRIUM CELL; FEMALE; GENE EXPRESSION REGULATION; GENE LOCATION; GENE OVEREXPRESSION; GENE TARGETING; MCL1 GENE; MICROARRAY ANALYSIS; NIDATION; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RAT; RNA BINDING; SIGNAL TRANSDUCTION; STROMA CELL; UPREGULATION; UTERUS;

RATTUS;

BCL-2 FAMILY; EMBRYO IMPLANTATION; MIR-29A; MIRNAS; RAT UTERUS;

3' UNTRANSLATED REGIONS; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; APOPTOSIS; BCL-2 HOMOLOGOUS ANTAGONIST-KILLER PROTEIN; EMBRYO IMPLANTATION; ENDOMETRIUM; FEMALE; MICRORNAS; MYELOID CELL LEUKEMIA SEQUENCE 1 PROTEIN; PREGNANCY; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84897527110     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12751     Document Type: Article

References (47)

1. Wang H, &, Dey SK, (2006) Roadmap to embryo implantation: clues from mouse models. Nat Rev Genet 7, 185-199. (Pubitemid 43361530)
2. Simmons DG, &, Kennedy TG, (2002) Uterine sensitization-associated gene-1: a novel gene induced within the rat endometrium at the time of uterine receptivity/sensitization for the decidual cell reaction. Biol Reprod 67, 1638-1645. (Pubitemid 35204942)
3. Paria BC, Reese J, Das SK, &, Dey SK, (2002) Deciphering the cross-talk of implantation: advances and challenges. Science 296, 2185-2188. (Pubitemid 34680294)
4. Lim H, Ma L, Ma WG, Maas RL, &, Dey SK, (1999) Hoxa-10 regulates uterine stromal cell responsiveness to progesterone during implantation and decidualization in the mouse. Mol Endocrinol 13, 1005-1017. (Pubitemid 30645317)
5. Satokata I, Benson G, &, Maas R, (1995) Sexually dimorphic sterility phenotypes in Hoxa10-deficient mice. Nature 374, 460-463.
6. Matsumoto H, Zhao X, Das SK, Hogan BL, &, Dey SK, (2002) Indian hedgehog as a progesterone-responsive factor mediating epithelial-mesenchymal interactions in the mouse uterus. Dev Biol 245, 280-290. (Pubitemid 34521602)
7. Paria BC, Ma W, Tan J, Raja S, Das SK, Dey SK, &, Hogan BL, (2001) Cellular and molecular responses of the uterus to embryo implantation can be elicited by locally applied growth factors. Proc Natl Acad Sci USA 98, 1047-1052. (Pubitemid 32121184)
8. Song H, Lim H, Das SK, Paria BC, &, Dey SK, (2000) Dysregulation of EGF family of growth factors and COX-2 in the uterus during the preattachment and attachment reactions of the blastocyst with the luminal epithelium correlates with implantation failure in LIF-deficient mice. Mol Endocrinol 14, 1147-1161. (Pubitemid 32260477)
9. Stewart CL, Kaspar P, Brunet LJ, Bhatt H, Gadi I, Köntgen F, &, Abbondanzo SJ, (1992) Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature 359, 76-79.
10. Bartel DP, (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297.
11. Kim VN, (2005) MicroRNA biogenesis: coordinated cropping and dicing. Nat Rev Mol Cell Biol 6, 376-385. (Pubitemid 40637855)
12. Lee Y, Ahn C, Han J, Choi H, Kim J, Yim J, Lee J, Provost P, Rådmark O, Kim S, et al,. (2003) The nuclear RNase III Drosha initiates microRNA processing. Nature 425, 415-419. (Pubitemid 37187272)
13. Filipowicz W, Bhattacharyya SN, &, Sonenberg N, (2008) Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet 9, 102-114.
14. Valencia-Sanchez MA, Liu J, Hannon GJ, &, Parker R, (2006) Control of translation and mRNA degradation by miRNAs and siRNAs. Genes Dev 20, 515-524. (Pubitemid 43345317)
15. Friedman RC, Farh KK, Burge CB, &, Bartel DP, (2009) Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19, 92-105.
16. Suh N, Baehner L, Moltzahn F, Melton C, Shenoy A, Chen J, &, Blelloch R, (2010) MicroRNA function is globally suppressed in rat oocytes and early embryos. Curr Biol 20, 271-277.
17. Wang R, Hu Y, Song G, Hao CJ, Cui Y, Xia HF, &, Ma X, (2012) miR-206 regulates neural cells proliferation and apoptosis via Otx2. Cell Physiol Biochem 29, 381-390.
18. Chakrabarty A, Tranguch S, Daikoku T, Jensen K, Furneaux H, &, Dey SK, (2007) MicroRNA regulation of cyclooxygenase-2 during embryo implantation. Proc Natl Acad Sci USA 104, 15144-15149. (Pubitemid 47619608)
19. Hu SJ, Ren G, Liu JL, Zhao ZA, Yu YS, Su RW, Ma XH, Ni H, Lei W, &, Yang ZM, (2008) MicroRNA expression and regulation in mouse uterus during embryo implantation. J Biol Chem 283, 23473-23484.
20. Su RW, Lei W, Liu JL, Zhang ZR, Jia B, Feng XH, Ren G, Hu SJ, &, Yang ZM, (2010) The integrative analysis of microRNA and mRNA expression in mouse uterus under delayed implantation and activation. PLoS One 5, e15513.
21. Estella C, Herrer I, Moreno-Moya JM, Quiñonero A, Martínez S, Pellicer A, &, Simón C, (2012) miRNA signature and Dicer requirement during human endometrial stromal decidualization in vitro. PLoS One 7, e41080.
22. Willenbrock H, Salomon J, Søkilde R, Barken KB, Hansen TN, Nielsen FC, Møller S, &, Litman T, (2009) Quantitative miRNA expression analysis: comparing microarrays with next-generation sequencing. RNA 15, 2028-2034.
23. Eguchi T, Watanabe K, Hara ES, Ono M, Kuboki T, &, Calderwood SK, (2013) OstemiR: a novel panel of microRNA biomarkers in osteoblastic and osteocytic differentiation from mesencymal stem cells. PLoS One 8, e58796.
24. Langlois RA, Albrecht RA, Kimble B, Sutton T, Shapiro JS, Finch C, Angel M, Chua MA, Gonzalez-Reiche AS, Xu K, et al,. (2013) MicroRNA-based strategy to mitigate the risk of gain-of-function influenza studies. Nat Biotechnol 31, 844-847.
25. Michie HJ, &, Head JR, (1994) Tenascin in pregnant and non-pregnant rat uterus: unique spatio-temporal expression during decidualization. Biol Reprod 50, 1277-1286. (Pubitemid 24155467)
26. Shynlova O, Tsui P, Dorogin A, Langille BL, &, Lye SJ, (2007) The expression of transforming growth factor β in pregnant rat myometrium is hormone and stretch dependent. Reproduction 134, 503-511. (Pubitemid 47386897)
27. Desjobert C, Renalier MH, Bergalet J, Dejean E, Joseph N, Kruczynski A, Soulier J, Espinos E, Meggetto F, Cavaillé J, et al,. (2011) miR-29a down-regulation in ALK-positive anaplastic large cell lymphomas contributes to apoptosis blockade through MCL-1 overexpression. Blood 117, 6627-6637.
28. Meunier L, Siddeek B, Vega A, Lakhdari N, Inoubli L, Bellon RP, Lemaire G, Mauduit C, &, Benahmed M, (2012) Perinatal programming of adult rat germ cell death after exposure to xenoestrogens: role of microRNA miR-29 family in the down-regulation of DNA methyltransferases and Mcl-1. Endocrinology 153, 1936-1947.
29. Gérecová G, Kopanicová J, Jaká P, Běhalová L, Juhásová B, Bhatia- Kiššová I, Forte M, Polčic P, &, Mentel M, (2013) BH3-only proteins Noxa, Bik, Bmf, and Bid activate Bax and Bak indirectly when studied in yeast model. FEMS Yeast Res 13, 747-754.
30. Veillette A, Grenier K, Brasseur K, Fréchette-Frigon G, Leblanc V, Parent S, &, Asselin E, (2013) Regulation of the PI3-K/Akt survival pathway in the rat endometrium. Biol Reprod 88, 79.
31. Boumela I, Guillemin Y, Guérin JF, &, Aouacheria A, (2009) The Bcl-2 family pathway in gametes and preimplantation embryos. Gynecol Obstet Fertil 37, 720-732.
32. Moldoveanu T, Grace CR, Llambi F, Nourse A, Fitzgerald P, Gehring K, Kriwacki RW, &, Green DR, (2012) BID-induced structural changes in BAK promote apoptosis. Cell Signal 24, 1163-1172.
33. Gibson L, Holmgreen SP, Huang DC, Bernard O, Copeland NG, Jenkins NA, Sutherland GR, Baker E, Adams JM, &, Cory S, (1996) Bcl-w, a novel member of the bcl-2 family, promotes cell survival. Oncogene 13, 665-675. (Pubitemid 26312893)
34. Schmitt MJ, Margue C, Behrmann I, &, Kreis S, (2013) miRNA-29: a microRNA family with tumor-suppressing and immune-modulating properties. Curr Mol Med 13, 572-585.
35. Garzon R, Heaphy CE, Havelange V, Fabbri M, Volinia S, Tsao T, Zanesi N, Kornblau SM, Marcucci G, Calin GA, et al,. (2009) MicroRNA 29b functions in acute myeloid leukemia. Blood 114, 5331-5341.
36. Mott JL, Kobayashi S, Bronk SF, &, Gores GJ, (2007) mir-29 regulates Mcl-1 protein expression and apoptosis. Oncogene 26, 6133-6140. (Pubitemid 47414372)
37. Xiong Y, Fang JH, Yun JP, Yang J, Zhang Y, Jia WH, &, Zhuang SM, (2010) Effects of microRNA-29 on apoptosis, tumorigenicity, and prognosis of hepatocellular carcinoma. Hepatology 51, 836-845.
38. Park SY, Lee JH, Ha M, Nam JW, &, Kim VN, (2009) miR-29 miRNAs activate p53 by targeting p85 α and CDC42. Nat Struct Mol Biol 16, 23-29.
39. Gebeshuber CA, Zatloukal K, &, Martinez J, (2009) miR-29a suppresses tristetraprolin, which is a regulator of epithelial polarity and metastasis. EMBO Rep 10, 400-405.
40. Han YC, Park CY, Bhagat G, Zhang J, Wang Y, Fan JB, Liu M, Zou Y, Weissman IL, &, Gu H, (2010) microRNA-29a induces aberrant self-renewal capacity in hematopoietic progenitors, biased myeloid development, and acute myeloid leukemia. J Exp Med 207, 475-489.
41. Kole AJ, Swahari V, Hammond SM, &, Deshmukh M, (2011) miR-29b is activated during neuronal maturation and targets BH3-only genes to restrict apoptosis. Genes Dev 25, 125-130.
42. Berger JA, Hautaniemi S, Järvinen AK, Edgren H, Mitra SK, &, Astola J, (2004) Optimized LOWESS normalization parameter selection for DNA microarray data. BMC Bioinformatics 5, 194.
43. Chan JA, Krichevsky AM, &, Kosik KS, (2005) MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res 65, 6029-6033. (Pubitemid 40994386)
44. Thomas PD, Kejariwal A, Campbell MJ, Mi H, Diemer K, Guo N, Ladunga I, Ulitsky-Lazareva B, Muruganujan A, Rabkin S, et al,. (2003) PANTHER: a browsable database of gene products organized by biological function, using curated protein family and subfamily classification. Nucleic Acids Res 31, 334-341. (Pubitemid 36150398)
45. Zheng Q, &, Wang XJ, (2008) GOEAST: a web-based software toolkit for Gene Ontology enrichment analysis. Nucleic Acids Res 36, W358-W363.
46. Enright AJ, John B, Gaul U, Tuschl T, Sander C, &, Marks DS, (2003) MicroRNA targets in Drosophila. Genome Biol 5, R1.
47. Joung JG, Hwang KB, Nam JW, Kim SJ, &, Zhang BT, (2007) Discovery of microRNA-mRNA modules via population-based probabilistic learning. Bioinformatics 23, 1141-1147.