MicroRNA MiR-199a-5p regulates smooth muscle cell proliferation and morphology by targeting WNT2 signaling pathway

Journal of Biological Chemistry

Volumn 290, Issue 11, 2015, Pages 7067-7086

  Gheinani, Ali Hashemi ^a   Burkhard, Fiona C ^b   Rehrauer, Hubert ^c   Fournier, Catharine Aquino ^c   Monastyrskaya, Katia ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b UNIVERSITY OF BERN   (Switzerland)

^c FUNCTIONAL GENOMICS CENTER ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROLIFERATION; CELLS; CYTOLOGY; MUSCLE; PIGMENTS; PROTEINS; RECOMBINANT PROTEINS; RNA; TRANSCRIPTION; TRANSCRIPTION FACTORS;

BLADDER PAIN SYNDROMES; DIFFERENTIATION PROCESS; SMOOTH MUSCLE CELL PROLIFERATION; SMOOTH MUSCLE LAYER; TIGHT JUNCTION FORMATIONS; TRANSCRIPTIONAL ACTIVATORS; TRANSCRIPTOME ANALYSIS; WNT SIGNALING PATHWAYS;

CELL SIGNALING;

ALPHA SMOOTH MUSCLE ACTIN; CYCLIN DEPENDENT KINASE INHIBITOR 1A; INHIBITOR OF DIFFERENTIATION 3; KRUPPEL LIKE FACTOR 4; MESSENGER RNA; MICRORNA; MICRORNA 199A 5P; MYOCARDIN; MYOSIN HEAVY CHAIN; MYOSIN LIGHT CHAIN; SHORT HAIRPIN RNA; TRANSCRIPTOME; TRANSFORMING GROWTH FACTOR BETA1; TRANSGELIN; UNCLASSIFIED DRUG; WNT2 PROTEIN; MIRN199 MICRORNA, HUMAN; NUCLEAR PROTEIN; SMALL INTERFERING RNA; TRANSACTIVATOR PROTEIN; WNT2 PROTEIN, HUMAN;

ACTG2 GENE; ARTICLE; BLADDER MUSCLE; CDKN1A GENE; CELL PROLIFERATION; CELL SIZE; CELL STRUCTURE; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENE TARGETING; GENETIC REGULATION; HUMAN; HUMAN CELL; ID3 GENE; INTRACELLULAR SIGNALING; MUSCLE DEVELOPMENT; MYL9 GENE; MYOCARDIN GENE; PRIORITY JOURNAL; PROTEIN TARGETING; SM ALPHA ACTIN GENE; SM MYOSIN HEAVY CHAIN GENE; SM22 GENE; SMOOTH MUSCLE FIBER; TGFB1I1 GENE; TRANSCRIPTOMICS; WNT SIGNALING PATHWAY; WNT2 GENE; BLADDER; CELL CYCLE; CELL DIFFERENTIATION; CELL LINE; CYTOLOGY; DOWN REGULATION; GENETICS; METABOLISM; RNA INTERFERENCE; UPREGULATION; UROTHELIUM;

CELL CYCLE; CELL DIFFERENTIATION; CELL LINE; CELL PROLIFERATION; CELL SIZE; DOWN-REGULATION; GENE EXPRESSION REGULATION; HUMANS; MICRORNAS; MYOCYTES, SMOOTH MUSCLE; NUCLEAR PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING; TRANS-ACTIVATORS; UP-REGULATION; URINARY BLADDER; UROTHELIUM; WNT SIGNALING PATHWAY; WNT2 PROTEIN;

EID: 84924873556     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.618694     Document Type: Article

References (59)

1. Slobodov, G., Feloney, M., Gran, C., Kyker, K. D., Hurst, R. E., and Culkin, D. J. (2004) Abnormal expression of molecular markers for bladder impermeability and differentiation in the urothelium of patients with interstitial cystitis. J. Urol. 171, 1554-1558
2. Sanchez Freire, V., Burkhard, F. C., Kessler, T. M., Kuhn, A., Draeger, A., and Monastyrskaya, K. (2010) MicroRNAs may mediate the down-regulation of neurokinin-1 receptor in chronic bladder pain syndrome. Am. J. Pathol. 176, 288-303
3. Adam, R. M. (2006) Recent insights into the cell biology of bladder smooth muscle. Nephron Exp. Nephrol. 102, e1-e7
4. Andersson, K. E., and Arner, A. (2004) Urinary bladder contraction and relaxation: physiology and pathophysiology. Physiol. Rev. 84, 935-986
5. Hypolite, J. A., Chang, S., Zheng, Y., DiSanto, M. E., Zderic, S. A., Wein, A. J., and Chacko, S. (2006) Partial bladder outlet obstruction induces urethral smooth muscle hypertrophy and decreased force generation. J. Urol. 175, 777-782
6. Myers, J. B., Dall'era, J. E., Koul, S., Kumar, B., Khandrika, L., Flynn, B. J., and Koul, H. K. (2009) Biochemical alterations in partial bladder outlet obstruction in mice: up-regulation of the mitogen activated protein kinase pathway. J. Urol. 181, 1926-1931
7. Chacko, S., Chang, S., Hypolite, J., Disanto, M., and Wein, A. (2004) Alteration of contractile and regulatory proteins following partial bladder outlet obstruction. Scand. J. Urol. Nephrol. Suppl. 215, 26-36
8. Bartel, D. P. (2009) MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233
9. Lu, M., Zhang, Q., Deng, M., Miao, J., Guo, Y., Gao, W., and Cui, Q. (2008) An analysis of human microRNA and disease associations. PLoS One 3, e3420
10. Wilmott, J. S., Zhang, X. D., Hersey, P., and Scolyer, R. A. (2011) The emerging important role of microRNAs in the pathogenesis, diagnosis and treatment of human cancers. Pathology 43, 657-671
11. Gheinani, A. H., Burkhard, F. C., and Monastyrskaya, K. (2013) Deciphering microRNA code in pain and inflammation: lessons from bladder pain syndrome. Cell. Mol. Life Sci. 70, 3773-3789
12. Pekow, J. R., and Kwon, J. H. (2012) MicroRNAs in inflammatory bowel disease. Inflamm. Bowel Dis. 18, 187-193
13. Sadegh, M. K., Ekman, M., Rippe, C., Uvelius, B., Swärd, K., and Albinsson, S. (2012) Deletion of Dicer in smooth muscle affects voiding pattern and reduces detrusor contractility and neuroeffector transmission. PLoS One 7, e35882
14. Zhang, S., Lv, J. W., Yang, P., Yu, Q., Pang, J., Wang, Z., Guo, H., Liu, S., Hu, J., Li, J., Leng, J., Huang, Y., Ye, Z., and Wang, C. Y. (2012) Loss of dicer exacerbates cyclophosphamide-induced bladder overactivity by enhancing purinergic signaling. Am. J. Pathol. 181, 937-946
15. Ekman, M., Bhattachariya, A., Dahan, D., Uvelius, B., Albinsson, S., and Swärd, K. (2013) Mir-29 repression in bladder outlet obstruction contributes to matrix remodeling and altered stiffness. PLoS One 8, e82308
16. Imamura, M., Sugino, Y., Long, X., Slivano, O. J., Nishikawa, N., Yoshimura, N., and Miano, J. M. (2013) Myocardin and microRNA-1 modulate bladder activity through connexin 43 expression during post-natal development. J. Cell. Physiol. 228, 1819-1826
17. Monastyrskaya, K., Sánchez-Freire, V., Hashemi Gheinani, A., Klumpp, D. J., Babiychuk, E. B., Draeger, A., and Burkhard, F. C. (2013) miR- 199a-5p regulates urothelial permeability and may play a role in bladder pain syndrome. Am. J. Pathol. 182, 431-448
18. Klumpp, D. J., Weiser, A. C., Sengupta, S., Forrestal, S. G., Batler, R. A., and Schaeffer, A. J. (2001) Uropathogenic Escherichia coli potentiates type 1 pilus-induced apoptosis by suppressing NF-κB. Infect. Immun. 69, 6689-6695
19. Rickard, A., Dorokhov, N., Ryerse, J., Klumpp, D. J., and McHowat, J. (2008) Characterization of tight junction proteins in cultured human urothelial cells. In Vitro Cell. Dev. Biol. Anim. 44, 261-267
20. 2+ signaling complex with ryanodine receptors and BKCa channels. Circ. Res. 97, 1270-1279
21. Sánchez Freire, V., Burkhard, F. C., Schmitz, A., Kessler, T. M., and Monastyrskaya, K. (2011) Structural differences between the bladder dome and trigone revealed by mRNA expression analysis of cold-cut biopsies. BJU Int. 108, E126-E135
22. 2+ entry by stabilizing the cortical actin cytoskeleton. J. Biol. Chem. 284, 17227-17242
23. Li, B., and Dewey, C. N. (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12, 323
24. Gentleman, R. C., Carey, V. J., Bates, D. M., Bolstad, B., Dettling, M., Dudoit, S., Ellis, B., Gautier, L., Ge, Y., Gentry, J., Hornik, K., Hothorn, T., Huber, W., Iacus, S., Irizarry, R., Leisch, F., Li, C., Maechler, M., Rossini, A. J., Sawitzki, G., Smith, C., Smyth, G., Tierney, L., Yang, J. Y., and Zhang, J. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5, R80
25. Kropp, B. P., Zhang, Y., Tomasek, J. J., Cowan, R., Furness, P. D., 3rd, Vaughan, M. B., Parizi, M., and Cheng, E. Y. (1999) Characterization of cultured bladder smooth muscle cells: assessment of in vitro contractility. J. Urol. 162, 1779-1784
26. Martin, A. F., Bhatti, S., Pyne-Geithman, G. J., Farjah, M., Manaves, V., Walker, L., Franks, R., Strauch, A. R., and Paul, R. J. (2007) Expression and function of COOH-terminal myosin heavy chain isoforms in mouse smooth muscle. Am. J. Physiol. Cell Physiol. 293, C238-C245
27. Alexander, M. S., Kawahara, G., Motohashi, N., Casar, J. C., Eisenberg, I., Myers, J. A., Gasperini, M. J., Estrella, E. A., Kho, A. T., Mitsuhashi, S., Shapiro, F., Kang, P. B., and Kunkel, L. M. (2013) MicroRNA-199a is induced in dystrophic muscle and affects WNT signaling, cell proliferation, and myogenic differentiation. Cell Death Differ. 20, 1194-1208
28. Ueki, N., Sobue, K., Kanda, K., Hada, T., and Higashino, K. (1987) Expression of high and low molecular weight caldesmons during phenotypic modulation of smooth muscle cells. Proc. Natl. Acad. Sci. U.S.A. 84, 9049-9053
29. Zheng, X. L. (2014) Myocardin and smooth muscle differentiation. Arch. Biochem. Biophys. 543, 48-56
30. Luo, X. G., Zhang, C. L., Zhao, W. W., Liu, Z. P., Liu, L., Mu, A., Guo, S., Wang, N., Zhou, H., and Zhang, T. C. (2014) Histone methyltransferase SMYD3 promotes MRTF-A-mediated transactivation of MYL9 and migration of MCF-7 breast cancer cells. Cancer Lett. 344, 129-137
31. Iwasaki, K., Hayashi, K., Fujioka, T., and Sobue, K. (2008) Rho/Rho-associated kinase signal regulates myogenic differentiation via myocardin-related transcription factor-A/Smad-dependent transcription of the Id3 gene. J. Biol. Chem. 283, 21230-21241
32. Applebaum, M., Ben-Yair, R., and Kalcheim, C. (2014) Segregation of striated and smooth muscle lineages by a Notch-dependent regulatory network. BMC Biol. 12, 53
33. Cowan, C. E., Kohler, E. E., Dugan, T. A., Mirza, M. K., Malik, A. B., and Wary, K. K. (2010) Kruppel-like factor-4 transcriptionally regulates VEcadherin expression and endothelial barrier function. Circ. Res. 107, 959-966
34. Chan, Y. C., Roy, S., Huang, Y., Khanna, S., and Sen, C. K. (2012) The microRNA miR-199a-5p down-regulation switches on wound angiogenesis by derepressing the v-ets erythroblastosis virus E26 oncogene homolog 1-matrix metalloproteinase-1 pathway. J. Biol. Chem. 287, 41032-41043
35. Rane, S., He, M., Sayed, D., Vashistha, H., Malhotra, A., Sadoshima, J., Vatner, D. E., Vatner, S. F., and Abdellatif, M. (2009) Downregulation of miR-199a derepresses hypoxia-inducible factor-1α and Sirtuin 1 and recapitulates hypoxia preconditioning in cardiac myocytes. Circ. Res. 104, 879-886
36. Song, X. W., Li, Q., Lin, L., Wang, X. C., Li, D. F., Wang, G. K., Ren, A. J., Wang, Y. R., Qin, Y. W., Yuan, W. J., and Jing, Q. (2010) MicroRNAs are dynamically regulated in hypertrophic hearts, and miR-199a is essential for the maintenance of cell size in cardiomyocytes. J. Cell. Physiol. 225, 437-443
37. Cheung, H. H., Davis, A. J., Lee, T. L., Pang, A. L., Nagrani, S., Rennert, O. M., and Chan, W. Y. (2011) Methylation of an intronic region regulates miR-199a in testicular tumor malignancy. Oncogene 30, 3404-3415
38. Bowen, T., Jenkins, R. H., and Fraser, D. J. (2013) MicroRNAs, transforming growth factor β-1, and tissue fibrosis. J. Pathol. 229, 274-285
39. Meng, X. M., Chung, A. C., and Lan, H. Y. (2013) Role of the TGF-β/BMP-7/Smad pathways in renal diseases. Clin. Sci. 124, 243-254
40. Lino Cardenas, C. L., Henaoui, I. S., Courcot, E., Roderburg, C., Cauffiez, C., Aubert, S., Copin, M. C., Wallaert, B., Glowacki, F., Dewaeles, E., Milosevic, J., Maurizio, J., Tedrow, J., Marcet, B., Lo-Guidice, J. M., Kaminski, N., Barbry, P., Luedde, T., Perrais, M., Mari, B., and Pottier, N. (2013) miR-199a-5p Is upregulated during fibrogenic response to tissue injury and mediates TGFβ-induced lung fibroblast activation by targeting caveolin-1. PLoS Genet. 9, e1003291
41. Mendell, J. T., and Olson, E. N. (2012) MicroRNAs in stress signaling and human disease. Cell 148, 1172-1187
42. Shen, Q., Cicinnati, V. R., Zhang, X., Iacob, S., Weber, F., Sotiropoulos, G. C., Radtke, A., Lu, M., Paul, A., Gerken, G., and Beckebaum, S. (2010) Role of microRNA-199a-5p and discoidin domain receptor 1 in human hepatocellular carcinoma invasion. Mol. Cancer 9, 227
43. Hu, Y., Liu, J., Jiang, B., Chen, J., Fu, Z., Bai, F., Jiang, J., and Tang, Z. (2014) MiR-199a-5p loss up-regulated DDR1 aggravated colorectal cancer by activating epithelial-to-mesenchymal transition related signaling. Dig. Dis. Sci. 59, 2163-2172
44. Roncarati, R., Viviani Anselmi, C., Losi, M. A., Papa, L., Cavarretta, E., Da Costa Martins, P., Contaldi, C., Saccani Jotti, G., Franzone, A., Galastri, L., Latronico, M. V., Imbriaco, M., Esposito, G., De Windt, L., Betocchi, S., and Condorelli, G. (2014) Circulating miR-29a, among other up-regulated microRNAs, is the only biomarker for both hypertrophy and fibrosis in patients with hypertrophic cardiomyopathy. J. Am. Coll. Cardiol. 63, 920-927
45. Reya, T., and Clevers, H. (2005) Wnt signalling in stem cells and cancer. Nature 434, 843-850
46. Onizuka, T., Yuasa, S., Kusumoto, D., Shimoji, K., Egashira, T., Ohno, Y., Kageyama, T., Tanaka, T., Hattori, F., Fujita, J., Ieda, M., Kimura, K., Makino, S., Sano, M., Kudo, A., and Fukuda, K. (2012) Wnt2 accelerates cardiac myocyte differentiation from ES-cell derived mesodermal cells via non-canonical pathway. J. Mol. Cell. Cardiol. 52, 650-659
47. Goodwin, A. M., and D'Amore, P. A. (2002) Wnt signaling in the vasculature. Angiogenesis 5, 1-9
48. Goss, A. M., Tian, Y., Cheng, L., Yang, J., Zhou, D., Cohen, E. D., and Morrisey, E. E. (2011) Wnt2 signaling is necessary and sufficient to activate the airway smooth muscle program in the lung by regulating myocardin/ Mrtf-B and Fgf10 expression. Dev. Biol. 356, 541-552
49. Wang, H., Gilner, J. B., Bautch, V. L., Wang, D. Z., Wainwright, B. J., Kirby, S. L., and Patterson, C. (2007) Wnt2 coordinates the commitment of mesoderm to hematopoietic, endothelial, and cardiac lineages in embryoid bodies. J. Biol. Chem. 282, 782-791
50. Tsaousi, A., Williams, H., Lyon, C. A., Taylor, V., Swain, A., Johnson, J. L., and George, S. J. (2011) Wnt4/β-catenin signaling induces VSMC proliferation and is associated with intimal thickening. Circ. Res. 108, 427-436
51. Sasaki, T., Hwang, H., Nguyen, C., Kloner, R. A., and Kahn, M. (2013) The small molecule Wnt signaling modulator ICG-001 improves contractile function in chronically infarcted rat myocardium. PLoS One 8, e75010
52. Liu, Y., Sinha, S., McDonald, O. G., Shang, Y., Hoofnagle, M. H., and Owens, G. K. (2005) Kruppel-like factor 4 abrogates myocardin-induced activation of smooth muscle gene expression. J. Biol. Chem. 280, 9719-9727
53. Zhang, X., Azhar, G., Helms, S. A., and Wei, J. Y. (2011) Regulation of cardiac microRNAs by serum response factor. J. Biomed. Sci. 18, 15
54. Lu, T. Y., Lin, B., Li, Y., Arora, A., Han, L., Cui, C., Coronnello, C., Sheng, Y., Benos, P. V., and Yang, L. (2013) Overexpression of microRNA-1 promotes cardiomyocyte commitment from human cardiovascular progenitors via suppressing WNT and FGF signaling pathways. J. Mol. Cell. Cardiol. 63, 146-154
55. Wu, Z. Y., Lu, L., Liang, J., Guo, X. R., Zhang, P. H., and Luo, S. J. (2014) Keloid microRNA expression analysis and the influence of miR-199a-5p on the proliferation of keloid fibroblasts. Genet. Mol. Res. 13, 2727-2738
56. Hsu, C. Y., Hsieh, T. H., Tsai, C. F., Tsai, H. P., Chen, H. S., Chang, Y., Chuang, H. Y., Lee, J. N., Hsu, Y. L., and Tsai, E. M. (2014) miRNA-199a-5p regulates VEGFA in endometrial mesenchymal stem cells and contributes to the pathogenesis of endometriosis. J. Pathol. 232, 330-343
57. Yang, J., Li, X., Li, Y., Southwood, M., Ye, L., Long, L., Al-Lamki, R. S., and Morrell, N. W. (2013) Id proteins are critical downstream effectors of BMP signaling in human pulmonary arterial smooth muscle cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 305, L312-L321
58. Mohamed, J. S., Lopez, M. A., Cox, G. A., and Boriek, A. M. (2013) Ankyrin repeat domain protein 2 and inhibitor of DNA binding 3 cooperatively inhibit myoblast differentiation by physical interaction. J. Biol. Chem. 288, 24560-24568
59. Guo, Y., Xiao, L., Sun, L., and Liu, F. (2012) Wnt/β-catenin signaling: a promising new target for fibrosis diseases. Physiol. Res. 61, 337-346