Combined analysis of microRNome and 3′-UTRome reveals a species-specific regulation of progesterone receptor expression in the endometrium of rhesus monkey

Journal of Biological Chemistry

Volumn 287, Issue 17, 2012, Pages 13899-13910

  Liu, Ji Long ^a   Liang, Xiao Huan ^a   Su, Ren Wei ^b   Lei, Wei ^b   Jia, Bo ^c   Feng, Xu Hui ^c   Li, Zhi Xiong ^d   Yang, Zeng Ming ^a,c  

^a SHANTOU UNIVERSITY   (China)

^b NORTHEAST AGRICULTURAL UNIVERSITY   (China)

^c XIAMEN UNIVERSITY   (China)

^d Fujian Family Planning Institute   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL MODEL; BINDING PATTERN; COMBINED ANALYSIS; COMPLEX MECHANISMS; EXPRESSION PROFILE; MICRORNAS; MOLECULAR MECHANISM; NON-CODING RNAS; PROGESTERONE RECEPTOR; QUANTITATIVE RT-PCR; RHESUS MONKEY; TARGET GENES;

GENE EXPRESSION; POLYMERASE CHAIN REACTION; RNA;

MAMMALS;

MICRORNA;

3' UNTRANSLATED REGION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING SITE; CONTROLLED STUDY; ENDOMETRIUM; FEMALE; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE LIBRARY; GENE SEQUENCE; GENE TARGETING; GENETIC CONSERVATION; GENETIC VARIABILITY; LUTEAL PHASE; NONHUMAN; PRIORITY JOURNAL; PROGESTERONE RECEPTOR GENE; RECEPTOR GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RHESUS MONKEY; RNA BINDING;

3' UNTRANSLATED REGIONS; ANIMALS; BASE SEQUENCE; BINDING SITES; EMBRYO IMPLANTATION; ENDOMETRIUM; FEMALE; GENE EXPRESSION REGULATION; MACACA MULATTA; MICE; MICRORNAS; MOLECULAR SEQUENCE DATA; PREGNANCY; PREGNANCY, ANIMAL; RECEPTORS, PROGESTERONE; UTERUS;

EID: 84859985286     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.301275     Document Type: Article

References (54)

1. O'Malley, B. W., and Tsai, M. J. (1992) Molecular pathways of steroid receptor action. Biol. Reprod. 46, 163-167
2. Gidley-Baird, A. A. (1981) Endocrine control of implantation and delayed implantation in rats and mice. J. Reprod. Fertil. Suppl. 29, 97-109
3. de Ziegler, D., Bergeron, C., Cornel, C., Medalie, D. A., Massai, M. R., Milgrom, E., Frydman, R., and Bouchard, P. (1992) Effects of luteal estradiol on the secretory transformation of human endometrium and plasma gonadotropins. J. Clin. Endocrinol. Metab. 74, 322-331
4. Ghosh, D., De, P., and Sengupta, J. (1994) Luteal phase ovarian oestrogen is not essential for implantation and maintenance of pregnancy from surrogate embryo transfer in the rhesus monkey. Hum. Reprod. 9, 629-637 (Pubitemid 24132338)
5. Nilsen, T. W. (2007) Mechanisms of microRNA-mediated gene regulation in animal cells. Trends Genet. 23, 243-249
6. Friedman, R. C., Farh, K. K., Burge, C. B., and Bartel, D. P. (2009) Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 19, 92-105
7. Gonzalez, G., and Behringer, R. R. (2009) Dicer is required for female reproductive tract development and fertility in the mouse. Mol. Reprod. Dev. 76, 678-688
8. Nagaraja, A. K., Andreu-Vieyra, C., Franco, H. L., Ma, L., Chen, R., Han, D. Y., Zhu, H., Agno, J. E., Gunaratne, P. H., DeMayo, F. J., and Matzuk, M. M. (2008) Deletion of Dicer in somatic cells of the female reproductive tract causes sterility. Mol. Endocrinol. 22, 2336-2352
9. Hong, X., Luense, L. J., McGinnis, L. K., Nothnick, W. B., and Christenson, L. K. (2008) Dicer1 is essential for female fertility and normal development of the female reproductive system. Endocrinology 149, 6207-6212
10. Nothnick, W. B., and Healy, C. (2010) Estrogen induces distinct patterns of microRNA expression within the mouse uterus. Reprod. Sci. 17, 987-994
11. Qian, K., Hu, L., Chen, H., Li, H., Liu, N., Li, Y., Ai, J., Zhu, G., Tang, Z., and Zhang, H. (2009) Hsa-miR-222 is involved in differentiation of endometrial stromal cells in vitro. Endocrinology 150, 4734-4743
12. Kuokkanen, S., Chen, B., Ojalvo, L., Benard, L., Santoro, N., and Pollard, J. W. (2010) Genomic profiling of microRNAs and messenger RNAs reveals hormonal regulation in microRNA expression in human endometrium. Biol. Reprod. 82, 791-801
13. Hu, S. J., Ren, G., Liu, J. L., Zhao, Z. A., Yu, Y. S., Su, R. W., Ma, X. H., Ni, H., Lei, W., and Yang, Z. M. (2008) MicroRNA expression and regulation in mouse uterus during embryo implantation. J. Biol. Chem. 283, 23473-23484
14. Chakrabarty, A., Tranguch, S., Daikoku, T., Jensen, K., Furneaux, H., and Dey, S. K. (2007) MicroRNA regulation of cyclooxygenase-2 during embryo implantation. Proc. Natl. Acad. Sci. U.S.A. 104, 15144-15149 (Pubitemid 47619608)
15. Dey, S. K., Lim, H., Das, S. K., Reese, J., Paria, B. C., Daikoku, T., and Wang, H. (2004) Molecular cues to implantation. Endocr. Rev. 25, 341-373 (Pubitemid 38780665)
16. Wang, H., and Dey, S. K. (2006) Roadmap to embryo implantation: clues from mouse models. Nat. Rev. Genet. 7, 185-199 (Pubitemid 43361530)
17. Liao, B. Y., and Zhang, J. (2008) Null mutations in human and mouse orthologs frequently result in different phenotypes. Proc. Natl. Acad. Sci. U.S.A. 105, 6987-6992
18. Lee, K. Y., and DeMayo, F. J. (2004) Animal models of implantation. Reproduction 128, 679-695 (Pubitemid 40028544)
19. Brameier, M. (2010) Genome-wide comparative analysis of microRNAs in three non-human primates. BMC Res. Notes 3, 64
20. Creighton, C. J., Reid, J. G., and Gunaratne, P. H. (2009) Expression profiling of microRNAs by deep sequencing. Brief Bioinform. 10, 490-497
21. Creighton, C. J., Benham, A. L., Zhu, H., Khan, M. F., Reid, J. G., Nagaraja, A. K., Fountain, M. D., Dziadek, O., Han, D., Ma, L., Kim, J., Hawkins, S. M., Anderson, M. L., Matzuk, M. M., and Gunaratne, P. H. (2010) Discovery of novel microRNAs in female reproductive tract using next generation sequencing. PLoS One 5, e9637
22. Ji, Z., Lee, J. Y., Pan, Z., Jiang, B., and Tian, B. (2009) Progressive lengthening of 3′-untranslated regions of mRNAs by alternative polyadenylation during mouse embryonic development. Proc. Natl. Acad. Sci. U.S.A. 106, 7028-7033
23. Mangone, M., Manoharan, A. P., Thierry-Mieg, D., Thierry-Mieg, J., Han, T., Mackowiak, S. D., Mis, E., Zegar, C., Gutwein, M. R., Khivansara, V., Attie, O., Chen, K., Salehi-Ashtiani, K., Vidal, M., Harkins, T. T., Bouffard, P., Suzuki, Y., Sugano, S., Kohara, Y., Rajewsky, N., Piano, F., Gunsalus, K. C., and Kim, J. K. (2010) The landscape of C. elegans 3′-UTRs. Science 329, 432-435
24. Jan, C. H., Friedman, R. C., Ruby, J. G., and Bartel, D. P. (2011) Formation, regulation, and evolution of Caenorhabditis elegans 3′-UTRs. Nature 469, 97-101
25. Pauerstein, C. J., Eddy, C. A., Croxatto, H. D., Hess, R., Siler-Khodr, T. M., and Croxatto, H. B. (1978) Temporal relationships of estrogen, progesterone, and luteinizing hormone levels to ovulation in women and infrahuman primates. Am. J. Obstet. Gynecol. 130, 876-886 (Pubitemid 8314528)
26. Critchley, H. O., and Saunders, P. T. (2009) Hormone receptor dynamics in a receptive human endometrium. Reprod. Sci. 16, 191-199
27. Spencer, T. E., and Bazer, F. W. (2002) Biology of progesterone action during pregnancy recognition and maintenance of pregnancy. Front. Biosci. 7, d1879-1898
28. Conneely, O. M., Mulac-Jericevic, B., Lydon, J. P., and De Mayo, F. J. (2001) Reproductive functions of the progesterone receptor isoforms: lessons from knock-out mice. Mol. Cell Endocrinol. 179, 97-103 (Pubitemid 32564956)
29. Ho, P. C. (2001) Mifepristone: a potential postcoital contraceptive. Expert Opin. Pharmacother. 2, 1383-1388
30. Thornton, J. W. (2001) Evolution of vertebrate steroid receptors from an ancestral estrogen receptor by ligand exploitation and serial genome expansions. Proc. Natl. Acad. Sci. U.S.A. 98, 5671-5676
31. Tan, J., Paria, B. C., Dey, S. K., and Das, S. K. (1999) Differential uterine expression of estrogen and progesterone receptors correlates with uterine preparation for implantation and decidualization in the mouse. Endocrinology 140, 5310-5321
32. Jensen, K. P., and Covault, J. (2011) Human miR-1271 is a miR-96 paralog with distinct non-conserved brain expression pattern. Nucleic Acids Res. 39, 701-711
33. Kloosterman, W. P., Lagendijk, A. K., Ketting, R. F., Moulton, J. D., and Plasterk, R. H. (2007) Targeted inhibition of miRNA maturation with morpholinos reveals a role for miR-375 in pancreatic islet development. PLoS Biol. 5, e203
34. Yue, X., Schwartz, J. C., Chu, Y., Younger, S. T., Gagnon, K. T., Elbashir, S., Janowski, B. A., and Corey, D. R. (2010) Transcriptional regulation by small RNAs at sequences downstream from 3′ gene termini. Nat. Chem. Biol. 6, 621-629
35. Wang, J., Liu, X., Wu, H., Ni, P., Gu, Z., Qiao, Y., Chen, N., Sun, F., and Fan, Q. (2010) CREB up-regulates long non-coding RNA, HULC expression through interaction with microRNA-372 in liver cancer. Nucleic Acids Res. 38, 5366-5383
36. Forrest, A. R., Kanamori-Katayama, M., Tomaru, Y., Lassmann, T., Ninomiya, N., Takahashi, Y., de Hoon, M. J., Kubosaki, A., Kaiho, A., Suzuki, M., Yasuda, J., Kawai, J., Hayashizaki, Y., Hume, D. A., and Suzuki, H. (2010) Induction of microRNAs, mir-155, mir-222, mir-424, and mir-503, promotes monocytic differentiation through combinatorial regulation. Leukemia 24, 460-466
37. Poliseno, L., Salmena, L., Zhang, J., Carver, B., Haveman, W. J., and Pandolfi, P. P. (2010) A coding-independent function of gene and pseudogene mRNAs regulates tumour biology. Nature 465, 1033-1038
38. Meyer, M. E., Quirin-Stricker, C., Lerouge, T., Bocquel, M. T., and Gronemeyer, H. (1992) A limiting factor mediates the differential activation of promoters by the human progesterone receptor isoforms. J. Biol. Chem. 267, 10882-10887
39. Wen, D. X., Xu, Y. F., Mais, D. E., Goldman, M. E., and McDonnell, D. P. (1994) The A and B isoforms of the human progesterone receptor operate through distinct signaling pathways within target cells. Mol. Cell Biol. 14, 8356-8364 (Pubitemid 24373584)
40. Horne, A. W., Lalani, E. N., Margara, R. A., Ryder, T. A., Mobberley, M. A., and White, J. O. (2005) The expression pattern of MUC1 glycoforms and other biomarkers of endometrial receptivity in fertile and infertile women. Mol. Reprod. Dev. 72, 216-229 (Pubitemid 41099411)
41. Julian, J., Enders, A. C., Fazleabas, A. T., and Carson, D. D. (2005) Compartmental distinctions in uterine Muc-1 expression during early pregnancy in cynomolgous macaque (Macaca fascicularis) and baboon (Papio anubis). Hum. Reprod. 20, 1493-1503 (Pubitemid 40852238)
42. Aplin, J. D. (1999) MUC-1 glycosylation in endometrium: possible roles of the apical glycocalyx at implantation. Hum. Reprod. 14, (Suppl. 2), 17-25
43. Palomino, W. A., Fuentes, A., González, R. R., Gabler, F., Boric, M. A., Vega, M., and Devoto, L. (2005) Differential expression of endometrial integrins and progesterone receptor during the window of implantation in normo-ovulatory women treated with clomiphene citrate. Fertil. Steril. 83, 587-593 (Pubitemid 40348568)
44. Maillot, G., Lacroix-Triki, M., Pierredon, S., Gratadou, L., Schmidt, S., Bènés, V., Roché, H., Dalenc, F., Auboeuf, D., Millevoi, S., and Vagner, S. (2009) Widespread estrogen-dependent repression of micrornas involved in breast tumor cell growth. Cancer Res. 69, 8332-8340
45. Rosa, A., Spagnoli, F. M., and Brivanlou, A. H. (2009) The miR-430/427/302 family controls mesendodermal fate specification via species-specific target selection. Dev. Cell 16, 517-527
46. Rajewsky, N. (2006) MicroRNA target predictions in animals. Nat. Genet. 38, (suppl.), S8-S13
47. Lewis, B. P., Shih, I. H., Jones-Rhoades, M. W., Bartel, D. P., and Burge, C. B. (2003) Prediction of mammalian microRNA targets. Cell 115, 787-798 (Pubitemid 38058492)
48. Alexander, R. P., Fang, G., Rozowsky, J., Snyder, M., and Gerstein, M. B. (2010) Annotating non-coding regions of the genome. Nat. Rev. Genet. 11, 559-571
49. Pang, K. C., Frith, M. C., and Mattick, J. S. (2006) Rapid evolution of noncoding RNAs: lack of conservation does not mean lack of function. Trends Genet. 22, 1-5 (Pubitemid 43011990)
50. Marques, A. C., and Ponting, C. P. (2009) Catalogues of mammalian long noncoding RNAs: modest conservation and incompleteness. Genome Biol. 10, R124
51. Langmead, B., Trapnell, C., Pop, M., and Salzberg, S. L. (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25
52. Tabaska, J. E., and Zhang, M. Q. (1999) Detection of polyadenylation signals in human DNA sequences. Gene 231, 77-86 (Pubitemid 29307775)
53. Lewis, B. P., Burge, C. B., and Bartel, D. P. (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120, 15-20 (Pubitemid 40094598)
54. Kong, L., Zhang, Y., Ye, Z. Q., Liu, X. Q., Zhao, S. Q., Wei, L., and Gao, G. (2007) CPC: assess the protein-coding potential of transcripts using sequence features and support vector machine. Nucleic Acids Res. 35, W345-349