ABSTRACT
During the menstrual cycle, human endometrium undergoes extensive cyclic morphologic and biochemical modifications in preparation for embryo implantation. These processes are highly regulated by ovarian steroids and various locally expressed gene products and involve inflammatory reaction, apoptosis, cell proliferation, angiogenesis, differentiation (tissue formation), and tissue remodeling. MicroRNAs (miRNAs) have emerged as key regulators of gene expression, and their altered and/or aberrant expression has been associated with establishment and progression of various disorders, including tumorigenesis. This review highlights the endometrial expression of miRNAs and their potential regulatory functions under normal and pathologic conditions such as endometriosis, dysfunctional uterine bleeding, and endometrial cancer. Given the key regulatory function of miRNAs on gene expression stability, understanding the underlying mechanisms of how endometrial miRNAs are regulated and identifying their specific target genes and their functions might lead to the development of preventive and therapeutic strategies by regulating specific target genes associated with such reproductive disorders.
KEYWORDS
MicroRNA - endometrium - gene expression - gene regulation - endometrial disorders
REFERENCES
-
1
Achache H, Revel A.
Endometrial receptivity markers, the journey to successful embryo implantation.
Hum Reprod Update.
2006;
12
731-746
-
2 Chegini N, Williams R S. Cytokine networks in human endometrium from menstruation to implantation. In: Hill J Cytokines in Human Reproduction. Hoboken, NJ; John Wiley & Sons 2000: 93-132
-
3
Du H, Taylor H S.
Contribution of bone marrow-derived stem cells to endometrium and endometriosis.
Stem Cells.
2007;
25
2082-2086
-
4
Girling J E, Rogers P A.
Recent advances in endometrial angiogenesis research.
Angiogenesis.
2005;
8
89-99
-
5
Horcajadas J A, Pellicer A, Simon C.
Wide genomic analysis of human endometrial receptivity: new times, new opportunities.
Hum Reprod Update.
2007;
13
77-86
-
6
Jabbour H N, Kelly R W, Fraser H M et al..
Endocrine regulation of menstruation.
Endocr Rev.
2006;
27
17-46
-
7
Makker A, Singh M M.
Endometrial receptivity: clinical assessment in relation to fertility, infertility, and antifertility.
Med Res Rev.
2006;
26
699-746
-
8
Ferenczy A.
Pathophysiology of endometrial bleeding.
Maturitas.
2003;
45
1-14
-
9
Harada T, Taniguchi F, Izawa M et al..
Apoptosis and endometriosis.
Front Biosci.
2007;
12
3140-3151
-
10
Abal M, Planaguma J, Gil-Moreno A et al..
Molecular pathology of endometrial carcinoma: transcriptional signature in endometrioid tumors.
Histol Histopathol.
2006;
21
197-204
-
11
Prat J, Gallardo A, Cuatrecasas M et al..
Endometrial carcinoma: pathology and genetics.
Pathology.
2007;
39
72-87
-
12
Ambros V, Chen X.
The regulation of genes and genomes by small RNAs.
Development.
2007;
134
1635-1641
-
13
Bartel D P.
MicroRNAs: genomics, biogenesis, mechanism, and function.
Cell.
2004;
116
281-297
-
14
Bernstein E, Caudy A A, Hammond S M et al..
Role for a bidentate ribonuclease in the initiation step of RNA interference.
Nature.
2001;
409
363-366
-
15
Paroo Z, Liu Q, Wang X.
Biochemical mechanisms of the RNA-induced silencing complex.
Cell Res.
2007;
17
187-194
-
16
Bernstein E, Kim S Y, Carmell M A et al..
Dicer is essential for mouse development.
Nat Genet.
2003;
35
215-217
-
17
Zamore P D, Haley B.
Ribo-gnome: the big world of small RNAs.
Science.
2005;
309
1519-1524
-
18
Jackson R J, Standart N.
How do microRNAs regulate gene expression?.
Sci STKE.
2007;
, 2007rel
-
19
Nilsen T W.
Mechanisms of microRNA-mediated gene regulation in animal cells.
Trends Genet.
2007;
23
243-249
-
20
Pillai R S, Bhattacharyya S N, Filipowicz W.
Repression of protein synthesis by miRNAs: how many mechanisms?.
Trends Cell Biol.
2007;
17
118-126
-
21
Berezikov E, van Tetering G, Verheul M et al..
Many novel mammalian microRNA candidates identified by extensive cloning and RAKE analysis.
Genome Res.
2006;
16
1289-1298
-
22
Yu Z, Jian Z, Shen S H et al..
Global analysis of microRNA target gene expression reveals that miRNA targets are lower expressed in mature mouse and Drosophila tissues than in the embryos.
Nucleic Acids Res.
2007;
35
152-164
-
23
Brennecke J, Stark A, Russell R B et al..
Principles of microRNA-target recognition.
PLoS Biol.
2005;
3
e85
-
24
Grimson A, Farh K K, Johnston W K et al..
MicroRNA targeting specificity in mammals: determinants beyond seed pairing.
Mol Cell.
2007;
27
91-105
-
25
Lai E C.
Micro RNAs are complementary to 3′ UTR sequence motifs that mediate negative post-transcriptional regulation.
Nat Genet.
2002;
30
363-364
-
26
Ghosh D, De P, Sengupta J.
Luteal phase ovarian oestrogen is not essential for implantation and maintenance of pregnancy from surrogate embryo transfer in the rhesus monkey.
Hum Reprod.
1994;
9
629-637
-
27
Smitz J, Bourgain C, Van Waesberghe L et al..
A prospective randomized study on oestradiol valerate supplementation in addition to intravaginal micronized progesterone in buserelin and HMG induced superovulation.
Hum Reprod.
1993;
8
40-45
-
28
Groothuis P G, Dassen H H, Romano A et al..
Estrogen and the endometrium: lessons learned from gene expression profiling in rodents and human.
Hum Reprod Update.
2007;
13
405-417
-
29
Smith O P, Critchley H O.
Progestogen only contraception and endometrial break through bleeding.
Angiogenesis.
2005;
8
117-126
-
30
Smith O P, Jabbour H N, Critchley H O.
Cyclooxygenase enzyme expression and E series prostaglandin receptor signalling are enhanced in heavy menstruation.
Hum Reprod.
2007;
22
1450-1456
-
31
Kao L C, Tulac S, Lobo S et al..
Global gene profiling in human endometrium during the window of implantation.
Endocrinology.
2002;
143
2119-2138
-
32
Lee K, Jeong J, Tsai M J et al..
Molecular mechanisms involved in progesterone receptor regulation of uterine function.
J Steroid Biochem Mol Biol.
2006;
102
41-50
-
33
Sherwin R, Catalano R, Sharkey A.
Large-scale gene expression studies of the endometrium: what have we learnt?.
Reproduction.
2006;
132
1-10
-
34
Taylor R N, Mueller M D.
Anti-angiogenic treatment of endometriosis: biochemical aspects.
Gynecol Obstet Invest.
2004;
57
54-56
-
35
Chegini N, Ma C, Roberts M et al..
Differential expression of interleukins (IL) IL-13 and IL-15 throughout the menstrual cycle in endometrium of normal fertile women and women with recurrent spontaneous abortion.
J Reprod Immunol.
2002;
56
93-110
-
36
Chegini N, Roberts M, Ripps B.
Differential expression of interleukins (IL)-13 and IL-15 in ectopic and eutopic endometrium of women with endometriosis and normal fertile women.
Am J Reprod Immunol.
2003;
49
75-83
-
37
Fujimoto J, Toyoki H, Jahan I et al..
Sex steroid-dependent angiogenesis in uterine endometrial cancers.
J Steroid Biochem Mol Biol.
2005;
93
161-165
-
38
Hannan N J, Salamonsen L A.
Role of chemokines in the endometrium and in embryo implantation.
Curr Opin Obstet Gynecol.
2007;
19
266-272
-
39
Vitiello D, Kodaman P H, Taylor H S.
HOX genes in implantation.
Semin Reprod Med.
2007;
25
431-436
-
40
Pan Q, Luo X, Toloubeydokhti T et al..
The expression profile of micro-RNA in endometrium and endometriosis and the influence of ovarian steroids on their expression.
Mol Hum Reprod.
2007;
13
797-806
-
41
Ambros V.
The functions of animal microRNAs.
Nature.
2004;
431
350-355
-
42
Li S C, Tang P, Lin W C.
Intronic microRNA: discovery and biological implications.
DNA Cell Biol.
2007;
26
195-207
-
43
Lim L P, Lau N C, Garrett-Engele P et al..
Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs.
Nature.
2005;
433
769-773
-
44
Carleton M, Cleary M A, Linsley P S.
MicroRNAs and cell cycle regulation.
Cell Cycle.
2007;
6
2127-2132
-
45
Harfe B D, McManus M T, Mansfield J H et al..
The RNaseIII enzyme Dicer is required for morphogenesis but not patterning of the vertebrate limb.
Proc Natl Acad Sci U S A.
2005;
102
10898-10903
-
46
Jovanovic M, Hengartner M O.
miRNAs and apoptosis: RNAs to die for.
Oncogene.
2006;
25
6176-6187
-
47
Kuehbacher A, Urbich C, Dimmeler S.
Targeting microRNA expression to regulate angiogenesis.
Trends Pharmacol Sci.
2008;
29
12-15
-
48
Linsley P S, Schelter J, Burchard J et al..
Transcripts targeted by the microRNA-16 family cooperatively regulate cell cycle progression.
Mol Cell Biol.
2007;
27
2240-2252
-
49
Chegini N.
Peritoneal molecular environment, adhesion formation and clinical implication.
Front Biosci.
2002;
7
E91-E115
-
50
Meng F, Henson R, Wehbe-Janek H et al..
The MicroRNA let-7a modulates interleukin-6-dependent STAT-3 survival signaling in malignant human cholangiocytes.
J Biol Chem.
2007;
282
8256-8264
-
51
Meng F, Wehbe-Janek H, Henson R et al..
Epigenetic regulation of microRNA-370 by interleukin-6 in malignant human cholangiocytes.
Oncogene.
2008;
27
378-386
-
52
O'Connell R M, Taganov K D, Boldin M P et al..
MicroRNA-155 is induced during the macrophage inflammatory response.
Proc Natl Acad Sci U S A.
2007;
104
1604-1609
-
53
Tili E, Michaille J J, Cimino A et al..
Modulation of miR-155 and miR-125b levels following lipopolysaccharide/TNF-alpha stimulation and their possible roles in regulating the response to endotoxin shock.
J Immunol.
2007;
179
5082-5089
-
54
Rodriguez A, Vigorito E, Clare S et al..
Requirement of bic/microRNA-155 for normal immune function.
Science.
2007;
316
608-611
-
55
Costinean S, Zanesi N, Pekarsky Y et al..
Pre-B cell proliferation and lymphoblastic leukemia/high-grade lymphoma in E(mu)-miR155 transgenic mice.
Proc Natl Acad Sci U S A.
2006;
103
7024-7029
-
56
Bergqvist A, Bruse C, Carlberg M et al..
Interleukin 1beta, interleukin-6, and tumor necrosis factor-alpha in endometriotic tissue and in endometrium.
Fertil Steril.
2001;
75
489-495
-
57
Cao W G, Morin M, Sengers V et al..
Tumour necrosis factor-alpha up-regulates macrophage migration inhibitory factor expression in endometrial stromal cells via the nuclear transcription factor NF-kappaB.
Hum Reprod.
2006;
21
421-428
-
58
Chegini N, Dou Q, Williams R S.
An inverse relation between the expression of tumor necrosis factor alpha (TNF-alpha) and TNF-alpha receptor in human endometrium.
Am J Reprod Immunol.
1999;
42
297-302
-
59
Cork B A, Tuckerman E M, Li T C et al..
Expression of interleukin (IL)-11 receptor by the human endometrium in vivo and effects of IL-11, IL-6 and LIF on the production of MMP and cytokines by human endometrial cells in vitro.
Mol Hum Reprod.
2002;
8
841-848
-
60
Kayisli U A, Aksu C A, Berkkanoglu M et al..
Estrogenicity of isoflavones on human endometrial stromal and glandular cells.
J Clin Endocrinol Metab.
2002;
87
5539-5544
-
61
Khan K N, Masuzaki H, Fujishita A et al..
Interleukin-6- and tumour necrosis factor alpha-mediated expression of hepatocyte growth factor by stromal cells and its involvement in the growth of endometriosis.
Hum Reprod.
2005;
20
2715-2723
-
62
Taganov K D, Boldin M P, Baltimore D.
MicroRNAs and immunity: tiny players in a big field.
Immunity.
2007;
26
133-137
-
63
Neilson J R, Zheng G X, Burge C B et al..
Dynamic regulation of miRNA expression in ordered stages of cellular development.
Genes Dev.
2007;
21
578-589
-
64
Chegini N, Luo X, Pan Q et al..
Endometrial expression of epithelial neutrophil-activating peptide-78 during the menstrual cycle or in progestin-only contraceptive users with breakthrough bleeding and the influence of doxycycline therapy.
Hum Reprod.
2007;
22
427-433
-
65
Li R, Luo X, Pan Q et al..
Doxycycline alters the expression of inflammatory and immune-related cytokines and chemokines in human endometrial cells: implication in irregular uterine bleeding.
Hum Reprod.
2006;
21
2555-2563
-
66
Li R, Luo X, Archer D F et al..
Doxycycline alters the expression of matrix metalloproteases in the endometrial cells exposed to ovarian steroids and pro-inflammatory cytokine.
J Reprod Immunol.
2007;
73
118-129
-
67
Rhoton-Vlasak A, Chegini N, Hardt N et al..
Histological characteristics and altered expression of interleukins (IL) IL-13 and IL-15 in endometria of levonorgestrel users with different uterine bleeding patterns.
Fertil Steril.
2005;
83
659-665
-
68
Clark I M, Swingler T E, Sampieri C L et al..
The regulation of matrix metalloproteinases and their inhibitors.
Int J Biochem Cell Biol.
2008;
40
1362-1378
-
69
Gill S E, Parks W C.
Metalloproteinases and their inhibitors: regulators of wound healing.
Int J Biochem Cell Biol.
2008;
40
1334-1347
-
70
Goffin F, Munaut C, Frankenne F et al..
Expression pattern of metalloproteinases and tissue inhibitors of matrix-metalloproteinases in cycling human endometrium.
Biol Reprod.
2003;
69
976-984
-
71
Dalmay T, Edwards D R.
MicroRNAs and the hallmarks of cancer.
Oncogene.
2006;
25
6170-6175
-
72
Fontana L, Pelosi E, Greco P et al..
MicroRNAs 17–5p-20a-106a control monocytopoiesis through AML1 targeting and M-CSF receptor upregulation.
Nat Cell Biol.
2007;
9
775-787
-
73
Li Q J, Chau J, Ebert P J et al..
miR-181a is an intrinsic modulator of T cell sensitivity and selection.
Cell.
2007;
129
147-161
-
74
Brosens J J, Gellersen B.
Death or survival—progesterone-dependent cell fate decisions in the human endometrial stroma.
J Mol Endocrinol.
2006;
36
389-398
-
75
Meng F, Henson R, Lang M et al..
Involvement of human micro-RNA in growth and response to chemotherapy in human cholangiocarcinoma cell lines.
Gastroenterology.
2006;
130
2113-2129
-
76
Si M L, Zhu S, Wu H et al..
miR-21-mediated tumor growth.
Oncogene.
2007;
26
2799-2803
-
77
Matsubara H, Takeuchi T, Nishikawa E et al..
Apoptosis induction by antisense oligonucleotides against miR-17–5p and miR-20a in lung cancers overexpressing miR-17–92.
Oncogene.
2007;
26
6099-6105
-
78
Mertens-Talcott S U, Chintharlapalli S, Li X et al..
The oncogenic microRNA-27a targets genes that regulate specificity protein transcription factors and the G2-M checkpoint in MDA-MB-231 breast cancer cells.
Cancer Res.
2007;
67
11001-11011
-
79
Ovcharenko D, Kelnar K, Johnson C et al..
Genome-scale microRNA and small interfering RNA screens identify small RNA modulators of TRAIL-induced apoptosis pathway.
Cancer Res.
2007;
67
10782-10788
-
80
Garofalo M, Quintavalle C, Di Leva G et al..
MicroRNA signatures of TRAIL resistance in human non-small cell lung cancer.
Oncogene.
2008;
27
3845-3855
-
81
Jones R K, Searle R F, Bulmer J N.
Apoptosis and bcl-2 expression in normal human endometrium, endometriosis and adenomyosis.
Hum Reprod.
1998;
13
3496-3502
-
82
Selam B, Kayisli U A, Mulayim N et al..
Regulation of Fas ligand expression by estradiol and progesterone in human endometrium.
Biol Reprod.
2001;
65
979-985
-
83
Watanabe H, Kanzaki H, Narukawa S et al..
Bcl-2 and Fas expression in eutopic and ectopic human endometrium during the menstrual cycle in relation to endometrial cell apoptosis.
Am J Obstet Gynecol.
1997;
176
360-368
-
84
Meng F, Henson R, Wehbe-Janek H et al..
MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer.
Gastroenterology.
2007;
133
647-658
-
85
He X, He L, Hannon G J.
The guardian's little helper: microRNAs in the p53 tumor suppressor network.
Cancer Res.
2007;
67
11099-11101
-
86
He L, He X, Lowe S W et al..
microRNAs join the p53 network—another piece in the tumour-suppression puzzle.
Nat Rev Cancer.
2007;
7
819-822
-
87
Raver-Shapira N, Marciano E, Meiri E et al..
Transcriptional activation of miR-34a contributes to p53-mediated apoptosis.
Mol Cell.
2007;
26
731-743
-
88
Sylvestre Y, De G, Querido E et al..
An E2F/miR-20a autoregulatory feedback loop.
J Biol Chem.
2007;
282
2135-2143
-
89
Welch C, Chen Y, Stallings R L.
MicroRNA-34a functions as a potential tumor suppressor by inducing apoptosis in neuroblastoma cells.
Oncogene.
2007;
26
5017-5022
-
90
Woods K, Thomson J M, Hammond S M.
Direct regulation of an oncogenic micro-RNA cluster by E2F transcription factors.
J Biol Chem.
2007;
282
2130-2134
-
91
Adams J M, Cory S.
Life-or-death decisions by the Bcl-2 protein family.
Trends Biochem Sci.
2001;
26
61-66
-
92
Cimmino A, Calin G A, Fabbri M et al..
miR-15 and miR-16 induce apoptosis by targeting BCL2.
Proc Natl Acad Sci U S A.
2005;
102
13944-13949
-
93
Smith S K.
Angiogenesis and reproduction.
BJOG.
2001;
108
777-783
-
94
Yang W J, Yang D D, Na S et al..
Dicer is required for embryonic angiogenesis during mouse development.
J Biol Chem.
2005;
280
9330-9335
-
95
Suarez Y, Fernandez-Hernando C, Pober J S et al..
Dicer dependent microRNAs regulate gene expression and functions in human endothelial cells.
Circ Res.
2007;
100
1164-1173
-
96
Poliseno L, Tuccoli A, Mariani L et al..
MicroRNAs modulate the angiogenic properties of HUVECs.
Blood.
2006;
108
3068-3071
-
97
Kuehbacher A, Urbich C, Zeiher A M et al..
Role of Dicer and Drosha for endothelial microRNA expression and angiogenesis.
Circ Res.
2007;
101
59-68
-
98
Chen Y, Gorski D H.
Regulation of angiogenesis through a microRNA (miR-130a) that down-regulates antiangiogenic homeobox genes GAX and HOXA5.
Blood.
2008;
111
1217-1226
-
99
Lee D Y, Deng Z, Wang C H et al..
MicroRNA-378 promotes cell survival, tumor growth, and angiogenesis by targeting SuFu and Fus-1 expression.
Proc Natl Acad Sci U S A.
2007;
104
20350-20355
-
100
Chakrabarty A, Tranguch S, Daikoku T et al..
MicroRNA regulation of cyclooxygenase-2 during embryo implantation.
Proc Natl Acad Sci U S A.
2007;
104
15144-15149
-
101
Fanchin R, Gallot V, Rouas-Freiss N et al..
Implication of HLA-G in human embryo implantation.
Hum Immunol.
2007;
68
259-263
-
102
Giudice L C.
Microarray expression profiling reveals candidate genes for human uterine receptivity.
Am J Pharmacogenomics.
2004;
4
299-312
-
103
Hamatani T, Ko M S, Yamada M et al..
Global gene expression profiling of preimplantation embryos.
Hum Cell.
2006;
19
98-117
-
104
Laird S M, Tuckerman E M, Li T C.
Cytokine expression in the endometrium of women with implantation failure and recurrent miscarriage.
Reprod Biomed Online.
2006;
13
13-23
-
105
Lodish H F, Zhou B, Liu G et al..
Micromanagement of the immune system by microRNAs.
Nat Rev Immunol.
2008;
8
120-130
-
106
Lewis B P, Shih I H, Jones-Rhoades M W et al..
Prediction of mammalian microRNA targets.
Cell.
2003;
115
787-798
-
107
Lewis B P, Burge C B, Bartel D P.
Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets.
Cell.
2005;
120
15-20
-
108
Laschke M W, Menger M D.
In vitro and in vivo approaches to study angiogenesis in the pathophysiology and therapy of endometriosis.
Hum Reprod Update.
2007;
13
331-342
-
109
Calin G A, Croce C M.
Chromosomal rearrangements and microRNAs: a new cancer link with clinical implications.
J Clin Invest.
2007;
117
2059-2066
-
110
Cho W C.
OncomiRs: the discovery and progress of microRNAs in cancers.
Mol Cancer.
2007;
6
60
-
111
Croce C M.
Oncogenes and cancer.
N Engl J Med.
2008;
358
502-511
-
112
Huppi K, Volfovsky N, Mackiewicz M et al..
MicroRNAs and genomic instability.
Semin Cancer Biol.
2007;
17
65-73
-
113
Ma L, Teruya-Feldstein J, Weinberg R A.
MicroRNAs in malignant progression.
Cell Cycle.
2008;
7
570-572
-
114
Rajalingam K, Schreck R, Rapp U R et al..
Ras oncogenes and their downstream targets.
Biochim Biophys Acta.
2007;
1773
1177-1195
-
115
Sen C K, Roy S.
miRNA: licensed to kill the messenger.
DNA Cell Biol.
2007;
26
193-194
-
116
Wu W, Sun M, Zou G M et al..
MicroRNA and cancer: current status and prospective.
Int J Cancer.
2007;
120
953-960
-
117
Chang T C, Yu D, Lee Y S et al..
Widespread microRNA repression by Myc contributes to tumorigenesis.
Nat Genet.
2008;
40
43-50
-
118
McAvoy S, Ganapathiraju S C, Ducharme-Smith A L et al..
Non-random inactivation of large common fragile site genes in different cancers.
Cytogenet Genome Res.
2007;
118
260-269
-
119
Jones R L, Findlay J K, Farnworth P G et al..
Activin A and inhibin A differentially regulate human uterine matrix metalloproteinases: potential interactions during decidualization and trophoblast invasion.
Endocrinology.
2006;
147
724-732
-
120
Esquela-Kerscher A, Trang P, Wiggins J F et al..
The let-7 microRNA reduces tumor growth in mouse models of lung cancer.
Cell Cycle.
2008;
7
759-764
-
121
Johnson C D, Esquela-Kerscher A, Stefani G et al..
The let-7 microRNA represses cell proliferation pathways in human cells.
Cancer Res.
2007;
67
7713-7722
-
122
Lee Y S, Dutta A.
The tumor suppressor microRNA let-7 represses the HMGA2 oncogene.
Genes Dev.
2007;
21
1025-1030
-
123
Calin G A, Ferracin M, Cimmino A et al..
A microRNA signature associated with prognosis and progression in chronic lymphocytic leukemia.
N Engl J Med.
2005;
353
1793-1801
-
124
Bircan S, Ensari A, Ozturk S et al..
Immunohistochemical analysis of c-myc, c-jun and estrogen receptor in normal, hyperplastic and neoplastic endometrium.
Pathol Oncol Res.
2005;
11
32-39
-
125
Rinaldi A, Poretti G, Kwee I et al..
Concomitant MYC and microRNA cluster miR-17–92 (C13orf25) amplification in human mantle cell lymphoma.
Leuk Lymphoma.
2007;
48
410-412
-
126
Lu Y, Thomson J M, Wong H Y et al..
Transgenic over-expression of the microRNA miR-17–92 cluster promotes proliferation and inhibits differentiation of lung epithelial progenitor cells.
Dev Biol.
2007;
310
442-453
-
127
le Sage C, Nagel R, Egan D A et al..
Regulation of the p27(Kip1) tumor suppressor by miR-221 and miR-222 promotes cancer cell proliferation.
EMBO J.
2007;
26
3699-3708
-
128
Kim H K, Lee Y S, Sivaprasad U et al..
Muscle-specific microRNA miR-206 promotes muscle differentiation.
J Cell Biol.
2006;
174
677-687
-
129
Adams B D, Furneaux H, White B A.
The micro-ribonucleic acid (miRNA) miR-206 targets the human estrogen receptor-alpha (ERalpha) and represses ERalpha messenger RNA and protein expression in breast cancer cell lines.
Mol Endocrinol.
2007;
21
1132-1147
-
130
Singh M, Zaino R J, Filiaci V J et al..
Relationship of estrogen and progesterone receptors to clinical outcome in metastatic endometrial carcinoma: a Gynecologic Oncology Group Study.
Gynecol Oncol.
2007;
106
325-333
-
131
Bukulmez O, Hardy D B, Carr B R et al..
Inflammatory status influences aromatase and steroid receptor expression in endometriosis.
Endocrinology.
2008;
149
1190-1204
-
132
Gleeson N C, Gonsalves R, Bonnar J.
Plasminogen activator inhibitors in endometrial adenocarcinoma.
Cancer.
1993;
72
1670-1672
-
133
Lim L P, Glasner M E, Yekta S et al..
Vertebrate microRNA genes.
Science.
2003;
299
1540
-
134
Boren T, Xiong Y, Hakam A et al..
MicroRNAs and their target messenger RNAs associated with endometrial carcinogenesis.
Gynecol Oncol.
2008;
110
206-215
-
135
Daikoku T, Hirota Y, Tranguch S et al..
Conditional loss of uterine Pten unfailingly and rapidly induces endometrial cancer in mice.
Cancer Res.
2008;
68
5619-5627
-
136
Hong X, Luense L J, McGinnis L K, Nothnick W B, Christenson L K.
Dicer1 is essential for female fertility and normal development of the female reproductive system.
Endocrinology.
2008;
, Aug 14 [Epub ahead of print]
-
137
Nagaraja A K, Andreu-Vieyra C, Franco H L et al..
Deletion of dicer in somatic cells of the female reproductive tract causes sterility.
Mol Endocrinol.
2008;
22
2336-2352
-
138
Hu S J, Ren G, Liu J L et al..
MicroRNA expression and regulation in mouse uterus during embryo implantation.
J Biol Chem.
2008;
283
23473-23484
Nasser CheginiPh.D.
Department of Obstetrics and Gynecology, University of Florida
Gainesville, FL 32610
eMail: cheginin@obgyn.ufl.edu