The miR-424(322)/503 cluster orchestrates remodeling of the epithelium in the involuting mammary gland

Genes and Development

Volumn 28, Issue 7, 2014, Pages 765-782

  Llobet Navas, David ^a,b   Rodríguez Barrueco, Ruth ^a,b   Castro, Verónica ^a   Ugalde, Alejandro P ^c   Sumazin, Pavel ^a   Jacob Sendler, Damian ^a   Demircan, Berna ^d   Castillo Martín, Mireia ^b   Putcha, Preeti ^a   Marshall, Netonia ^a   Villagrasa, Patricia ^a   Chan, Joseph ^a   Sanchez Garcia, Félix ^a   Pe'er, Dana ^a   Rabadán, Raul ^a   Iavarone, Antonio ^a   Cordón Cardó, Carlos ^b   Califano, Andrea ^a   López Otín, Carlos ^c   Ezhkova, Elena ^b   Silva, Jose M ^a,b   more..

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c DEPARTAMENTO DE BIOQUÍMICA Y BIOLOGÍA MOLECULAR   (Spain)

^d ISTANBUL MEDENIYET UNIVERSITY   (Turkey)

Author keywords

BCL2; IGF1R; Mammary gland development; miR 424; miR 503; TGF

Indexed keywords

DOXYCYCLINE; INSULIN GROWTH FACTOR 1 RECEPTOR; MICRORNA; MICRORNA 322; MICRORNA 424; MICRORNA 503; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN BCL 2; PROTEIN KINASE B; SOMATOMEDIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; BREAST EPITHELIUM; CARCINOGENESIS; CELL DEATH; CLINICAL PATHWAY; DOWN REGULATION; EPITHELIUM CELL; FEMALE; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; INVOLUTION; KNOCKOUT MOUSE; LIFE CYCLE; MAMMARY GLAND; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATOR GENE; SIGNAL TRANSDUCTION; UPREGULATION; WEANING;

BCL2; IGF1R; MAMMARY GLAND DEVELOPMENT; MIR-424; MIR-503; TGFΒ;

ANIMALS; CELL DEATH; CELL LINE; EPITHELIUM; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCKOUT TECHNIQUES; HUMANS; MAMMARY GLANDS, ANIMAL; MICE, KNOCKOUT; MICRORNAS; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS C-BCL-2; RECEPTOR, IGF TYPE 1; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA1; WEANING;

EID: 84898869604     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.237404.114     Document Type: Article

References (63)

1. Ackler S., Ahmad S, Tobias C, Johnson MD, Glazer RI. 2002. Delayed mammary gland involution in MMTV-AKT1 transgenic mice. Oncogene 21: 198-206.
2. Ahn H. W, Morin RD, Zhao H, Harris RA, Coarfa C, Chen ZJ, Milosavljevic A., Marra MA, Rajkovic A. 2010. MicroRNA transcriptome in the newborn mouse ovaries determined by massive parallel sequencing. Mol Hum Reprod 16: 463-471.
3. Allan G. J, Beattie J, Flint DJ. 2004. The role of IGFBP-5 in mammary gland development and involution. Domest Anim Endocrinol 27: 257-266.
4. Aqeilan R. I, Calin GA, Croce CM. 2010. miR-15a and miR-16-1 in cancer: discovery, function and future perspectives. Cell Death Differ 17: 215-220.
5. Avril-Sassen S, Goldstein LD, Stingl J, Blenkiron C, Le Quesne J, Spiteri I., Karagavriilidou K, Watson CJ, Tavare S, Miska EA, et al. 2009. Characterisation of microRNA expression in post-natal mouse mammary gland development. BMC Genomics 10: 548.
6. Bartel D.P. 2004. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116: 281-297.
7. Bartel D.P. 2009. MicroRNAs: target recognition and regulatory functions. Cell 136: 215-233.
8. Bernstein B. E, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J., Fry B, Meissner A, Wernig M, Plath K, et al. 2006. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125: 315-326.
9. Bhola N. E, Balko JM, Dugger TC, Kuba MG, Sanchez V, Sanders M, Stanford J, Cook RS, Arteaga CL. 2013. TGF-β inhibition enhances chemotherapy action against triple-negative breast cancer. J Clin Invest 123: 1348-1358.
10. Bouquet F., Pal A, Pilones KA, Demaria S, Hann B, Akhurst RJ, Babb J. S, Lonning SM, DeWyngaert JK, Formenti SC, et al. 2011. TGFβ1 inhibition increases the radiosensitivity of breast cancer cells in vitro and promotes tumor control by radiation in vivo. Clin Cancer Res 17: 6754-6765.
11. Calon A., Espinet E, Palomo-Ponce S, Tauriello DV, Iglesias M, Cespedes M. V, Sevillano M, Nadal C, Jung P, Zhang XH, et al. 2012. Dependency of colorectal cancer on a TGF-β-driven program in stromal cells for metastasis initiation. Cancer Cell 22: 571-584.
12. Chapman R. S, Lourenco PC, Tonner E, Flint DJ, Selbert S, Takeda K., Akira S, Clarke AR, Watson CJ. 1999. Suppression of epithelial apoptosis and delayed mammary gland involution in mice with a conditional knockout of Stat3. Genes Dev 13: 2604-2616.
13. Colitti M. 2012. BCL-2 family of proteins and mammary cellular fate. Anat Histol Embryol 41: 237-247.
14. Cui W., Li Q, Feng L, Ding W. 2011. MiR-126-3p regulates progesterone receptors and involves development and lactation of mouse mammary gland. Mol Cell Biochem 355: 17-25.
15. Davis B. N, Hilyard AC, Lagna G, Hata A. 2008. SMAD proteins control DROSHA-mediated microRNA maturation. Nature 454: 56-61.
16. Davis B. N, Hilyard AC, Nguyen PH, Lagna G, Hata A. 2010. Smad proteins bind a conserved RNA sequence to promote microRNA maturation by Drosha. Mol Cell 39: 373-384.
17. Dvinge H., Git A, Graf S, Salmon-Divon M, Curtis C, Sottoriva A, Zhao Y, Hirst M, Armisen J, Miska EA, et al. 2013. The shaping and functional consequences of the microRNA landscape in breast cancer. Nature 497: 378-382.
18. Faure E., Heisterkamp N, Groffen J, Kaartinen V. 2000. Differential expression of TGF-β isoforms during postlactational mammary gland involution. Cell Tissue Res 300: 89-95.
19. Finnerty J. R, Wang WX, Hebert SS, Wilfred BR, Mao G, Nelson PT. 2010. The miR-15/107 group of microRNA genes: evolutionary biology, cellular functions, and roles in human diseases. J Mol Biol 402: 491-509.
20. Forrest A. R, Kanamori-Katayama M, Tomaru Y, Lassmann T, Ninomiya N., Takahashi Y, de Hoon MJ, Kubosaki A, Kaiho A, Suzuki M, et al. 2010. Induction of microRNAs, mir-155, mir-222, mir-424 and mir-503, promotes monocytic differentiation through combinatorial regulation. Leukemia 24: 460-466.
21. Ghosh G., Subramanian IV, Adhikari N, Zhang X, Joshi HP, Basi D, Chandrashekhar YS, Hall JL, Roy S, Zeng Y, et al. 2010. Hypoxia-induced microRNA-424 expression in human endothelial cells regulates HIF-α isoforms and promotes angiogenesis. J Clin Invest 120: 4141-4154.
22. Gorska A. E, Jensen RA, Shyr Y, Aakre ME, Bhowmick NA, Moses H.L. 2003. Transgenic mice expressing a dominantnegative mutant type II transforming growth factor-β receptor exhibit impaired mammary development and enhanced mammary tumor formation. Am J Pathol 163: 1539-1549.
23. Grimson A., Farh KK, Johnston WK, Garrett-Engele P, Lim LP, Bartel D.P. 2007. MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol Cell 27: 91-105.
24. Guo H., Ingolia NT, Weissman JS, Bartel DP. 2010. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466: 835-840.
25. Hafner M., Landthaler M, Burger L, Khorshid M, Hausser J, Berninger P., Rothballer A, Ascano M Jr, Jungkamp AC, Munschauer M., et al. 2010. Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 141: 129-141.
26. Howard B. A, Gusterson BA. 2000. Human breast development. J Mammary Gland Biol Neoplasia 5: 119-137.
27. Hynes N. E, Watson CJ. 2010. Mammary gland growth factors: roles in normal development and in cancer. Cold Spring Harb Perspect Biol 2: a003186.
28. Iavarone A., Massague J. 1997. Repression of the CDK activator Cdc25A and cell-cycle arrest by cytokine TGF-β in cells lacking the CDK inhibitor p15. Nature 387: 417-422.
29. Inui M., Martello G, Piccolo S. 2010. MicroRNA control of signal transduction. Nat Rev Mol Cell Biol 11: 252-263.
30. Ip M. M, Asch BB. 2000. Introduction: an histology atlas of the rodent mammary gland and human breast during normal postnatal development and in cancer. J Mammary Gland Biol Neoplasia 5: 117-118.
31. Jager R., Herzer U, Schenkel J, Weiher H. 1997. Overexpression of Bcl-2 inhibits alveolar cell apoptosis during involution and accelerates c-myc-induced tumorigenesis of the mammary gland in transgenic mice. Oncogene 15: 1787-1795.
32. Johnson K., Kirkpatrick H, Comer A, Hoffmann FM, Laughon A. 1999. Interaction of Smad complexes with tripartite DNAbinding sites. J Biol Chem 274: 20709-20716.
33. Karakas B., Weeraratna A, Abukhdeir A, Blair BG, Konishi H, Arena S., Becker K, Wood W 3rd, Argani P, De Marzo AM, et al. 2006. Interleukin-1α mediates the growth proliferative effects of transforming growth factor-β in p21 null MCF-10A human mammary epithelial cells. Oncogene 25: 5561-5569.
34. Kim J., Kang Y, Kojima Y, Lighthouse JK, Hu X, Aldred MA, McLean DL, Park H, Comhair SA, Greif DM, et al. 2013. An endothelial apelin-FGF link mediated by miR-424 and miR-503 is disrupted in pulmonary arterial hypertension. Nat Med 19: 74-82.
35. Le Guillou S, Sdassi N, Laubier J, Passet B, Vilotte M, Castille J, Laloe D., Polyte J, Bouet S, Jaffrezic F, et al. 2012. Overexpression of miR-30b in the developing mouse mammary gland causes a lactation defect and delays involution. PLoS ONE 7: e45727.
36. Lewis B. P, Burge CB, Bartel DP. 2005. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120: 15-20.
37. Liu H., Kohane IS. 2009. Tissue and process specific microRNA-mRNA co-expression in mammalian development and malignancy. PLoS ONE 4: e5436.
38. Liu Q., Fu H, Sun F, Zhang H, Tie Y, Zhu J, Xing R, Sun Z, Zheng X. 2008. miR-16 family induces cell cycle arrest by regulating multiple cell cycle genes. Nucleic Acids Res 36: 5391-5404.
39. Macias H., Hinck L. 2012. Mammary gland development. Wiley Interdiscip Rev Dev Biol 1: 533-557.
40. Massague J., Seoane J, Wotton D. 2005. Smad transcription factors. Genes Dev 19: 2783-2810.
41. Melisi D., Ishiyama S, Sclabas GM, Fleming JB, Xia Q, Tortora G, Abbruzzese J. L, Chiao PJ. 2008. LY2109761, a novel transforming growth factor β receptor type I and type II dual inhibitor, as a therapeutic approach to suppressing pancreatic cancer metastasis. Mol Cancer Ther 7: 829-840.
42. Metcalfe A. D, Gilmore A, Klinowska T, Oliver J, Valentijn AJ, Brown R., Ross A, MacGregor G, Hickman JA, Streuli CH. 1999. Developmental regulation of Bcl-2 family protein expression in the involuting mammary gland. J Cell Sci 112: 1771-1783.
43. Modha G., Blanchard A, Iwasiow B, Mao XJ, Troup S, Adeyinka A, Watson P, Shiu R, Myal Y. 2004. Developmental changes in insulin-like growth factor I receptor gene expression in the mouse mammary gland. Endocr Res 30: 127-140.
44. Nakashima T., Jinnin M, Etoh T, Fukushima S, Masuguchi S, Maruo K., Inoue Y, Ishihara T, Ihn H. 2010. Down-regulation of mir-424 contributes to the abnormal angiogenesis via MEK1 and cyclin E1 in senile hemangioma: its implications to therapy. PLoS ONE 5: e14334.
45. Neuenschwander S., Schwartz A, Wood TL, Roberts CT Jr, Hennighausen L., LeRoith D. 1996. Involution of the lactating mammary gland is inhibited by the IGF system in a transgenic mouse model. J Clin Invest 97: 2225-2232.
46. Nguyen A. V, Pollard JW. 2000. Transforming growth factor β3 induces cell death during the first stage of mammary gland involution. Development 127: 3107-3118.
47. Pollak M. 2012. The insulin and insulin-like growth factor receptor family in neoplasia: an update. Nat Rev Cancer 12: 159-169.
48. Pollard K. S, Hubisz MJ, Rosenbloom KR, Siepel A. 2010. Detection of nonneutral substitution rates on mammalian phylogenies. Genome Res 20: 110-121.
49. Rissland O. S, Hong SJ, Bartel DP. 2011. MicroRNA destabilization enables dynamic regulation of the miR-16 family in response to cell-cycle changes. Mol Cell 43: 993-1004.
50. Rosa A., Ballarino M, Sorrentino A, Sthandier O, De Angelis FG, Marchioni M., Masella B, Guarini A, Fatica A, Peschle C, et al. 2007. The interplay between the master transcription factor PU.1 and miR-424 regulates human monocyte/macrophage differentiation. Proc Natl Acad Sci 104: 19849-19854.
51. Schorr K., Li M, Bar-Peled U, Lewis A, Heredia A, Lewis B, Knudson C. M, Korsmeyer SJ, Jager R, Weiher H, et al. 1999. Gain of Bcl-2 is more potent than bax loss in regulating mammary epithelial cell survival in vivo. Cancer Res 59: 2541-2545.
52. Schwertfeger K. L, Richert MM, Anderson SM. 2001. Mammary gland involution is delayed by activated Akt in transgenic mice. Mol Endocrinol 15: 867-881.
53. Shirdel E. A, Xie W, Mak TW, Jurisica I. 2011. NAViGaTing the micronome-using multiple microRNA prediction databases to identify signalling pathway-associated microRNAs. PLoS ONE 6: e17429.
54. Stein T., Salomonis N, Gusterson BA. 2007. Mammary gland involution as a multi-step process. J Mammary Gland Biol Neoplasia 12: 25-35.
55. Tanaka T., Haneda S, Imakawa K, Sakai S, Nagaoka K. 2009. A microRNA, miR-101a, controls mammary gland development by regulating cyclooxygenase-2 expression. Differentiation 77: 181-187.
56. Tiffen P. G, Omidvar N, Marquez-Almuina N, Croston D, Watson C. J, Clarkson RW. 2008. A dual role for oncostatin M signaling in the differentiation and death of mammary epithelial cells in vivo. Mol Endocrinol 22: 2677-2688.
57. Ucar A., Vafaizadeh V, Jarry H, Fiedler J, Klemmt PA, Thum T, Groner B., Chowdhury K. 2010. miR-212 and miR-132 are required for epithelial stromal interactions necessary for mouse mammary gland development. Nat Genet 42: 1101-1108.
58. Urnov F. D, Rebar EJ, Holmes MC, Zhang HS, Gregory PD. 2010. Genome editing with engineered zinc finger nucleases. Nat Rev Genet 11: 636-646.
59. Watson C.J. 2006. Post-lactational mammary gland regression: molecular basis and implications for breast cancer. Expert Rev Mol Med 8: 1-15.
60. Watson C. J, Kreuzaler PA. 2011. Remodeling mechanisms of the mammary gland during involution. Int J Dev Biol 55: 757-762.
61. Xu J., Li Y, Wang F, Wang X, Cheng B, Ye F, Xie X, Zhou C, Lu W. 2013. Suppressed miR-424 expression via upregulation of target gene Chk1 contributes to the progression of cervical cancer. Oncogene 32: 976-987.
62. Yang X., Lin X, Zhong X, Kaur S, Li N, Liang S, Lassus H, Wang L, Katsaros D, Montone K, et al. 2010. Double-negative feedback loop between reprogramming factor LIN28 and microRNA let-7 regulates aldehyde dehydrogenase 1-positive cancer stem cells. Cancer Res 70: 9463-9472.
63. Yip K. W, Reed JC. 2008. Bcl-2 family proteins and cancer. Oncogene 27: 6398-6406.