Mir-29 repression in bladder outlet obstruction contributes to matrix remodeling and altered stiffness

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Ekman, Mari ^a,b   Bhattachariya, Anirban ^a   Dahan, Diana ^a   Uvelius, Bengt ^b   Albinsson, Sebastian ^a   Swärd, Karl ^a  

^a LUND UNIVERSITY   (Sweden)

^b LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 4; DICER; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MESSENGER RNA; MICRORNA 29; MYC PROTEIN; OSTEONECTIN; SMAD3 PROTEIN; TAMOXIFEN; TRANSFORMING GROWTH FACTOR BETA; TROPOELASTIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLADDER MUSCLE STIFFNESS; BLADDER NECK STENOSIS; CELLULAR PARAMETERS; CONTROLLED STUDY; DETRUSOR MUSCLE; EXTRACELLULAR MATRIX; EXTRACELLULAR MATRIX MODELING; FEMALE; GENE FUNCTION; GENE IDENTIFICATION; GENE INTERACTION; GENE REPRESSION; GENETIC CORRELATION; GENETIC TRANSFECTION; IN VITRO STUDY; KNOCKOUT MOUSE; MICROARRAY ANALYSIS; MIR 29 GENE; MOUSE; MUSCLE RIGIDITY; NONHUMAN; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT; RAT MODEL; RNA ANALYSIS; RNA GENE; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; UPREGULATION;

ANIMALS; EXTRACELLULAR MATRIX; HUMANS; MALE; MICE; MICRORNAS; NF-KAPPA B; PROTO-ONCOGENE PROTEINS C-MYC; RATS; SMAD3 PROTEIN; URINARY BLADDER NECK OBSTRUCTION;

EID: 84892417681     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0082308     Document Type: Article

References (50)

1. 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. PubMed: 18197166.
2. Lewis BP, 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. doi:10.1016/j.cell.2004.12.035. PubMed: 15652477.
3. van Rooij E, Olson EN (2012) MicroRNA therapeutics for cardiovascular disease: opportunities and obstacles. Nat Rev Drug Discov 11: 860-872. doi:10.1038/nrd3864. PubMed: 23080337.
4. Lee Y, Ahn C, Han J, Choi H, Kim J et al. (2003) The nuclear RNase III Drosha initiates microRNA processing. Nature 425: 415-419. doi:10.1038/ nature01957. PubMed: 14508493.
5. Sadegh MK, Ekman M, Rippe C, Uvelius B, Swärd K et al. (2012) Deletion of Dicer in smooth muscle affects voiding pattern and reduces detrusor contractility and neuroeffector transmission. PLOS ONE 7: e35882. doi:10.1371/journal.pone.0035882. PubMed: 22558254.
6. Zhang S, Lv JW, Yang P, Yu Q, Pang J et al. (2012) Loss of dicer exacerbates cyclophosphamide-induced bladder overactivity by enhancing purinergic signaling. Am J Pathol 181: 937-946. doi:10.1016/j.ajpath.2012.05. 035. PubMed: 22796409.
7. Jones JA, Stroud RE, O'Quinn EC, Black LE, Barth JL et al. (2011) Selective microRNA suppression in human thoracic aneurysms: relationship of miR-29a to aortic size and proteolytic induction. Circ Cardiovasc Genet 4: 605-613. doi:10.1161/CIRCGENETICS.111.960419. PubMed: 22010139.
8. Maegdefessel L, Azuma J, Toh R, Merk DR, Deng A et al. (2012) Inhibition of microRNA-29b reduces murine abdominal aortic aneurysm development. J Clin Invest 122: 497-506. doi:10.1172/JCI61598. PubMed: 22269326.
9. Merk DR, Chin JT, Dake BA, Maegdefessel L, Miller MO et al. (2012) miR-29b participates in early aneurysm development in Marfan syndrome. Circ Res 110: 312-324. doi:10.1161/CIRCRESAHA.111.253740. PubMed: 22116819.
10. van Rooij E, Sutherland LB, Thatcher JE, DiMaio JM, Naseem RH et al. (2008) Dysregulation of microRNAs after myocardial infarction reveals a role of miR-29 in cardiac fibrosis. Proc Natl Acad Sci U S A 105: 13027-13032. doi:10.1073/pnas.0805038105. PubMed: 18723672.
11. Kriegel AJ, Liu Y, Fang Y, Ding X, Liang M (2012) The miR-29 family: genomics, cell biology, and relevance to renal and cardiovascular injury. Physiol Genomics 44: 237-244. doi:10.1152/physiolgenomics.00141.2011. PubMed: 22214600.
12. Ott CE, Grünhagen J, Jäger M, Horbelt D, Schwill S et al. (2011) MicroRNAs differentially expressed in postnatal aortic development downregulate elastin via 3′ UTR and coding-sequence binding sites. PLOS ONE 6: e16250. doi:10.1371/journal.pone.0016250. PubMed: 21305018.
13. Kapinas K, Kessler CB, Delany AM (2009) miR-29 suppression of osteonectin in osteoblasts: regulation during differentiation and by canonical Wnt signaling. J Cell Biochem 108: 216-224. doi:10.1002/jcb.22243. PubMed: 19565563.
14. Long J, Wang Y, Wang W, Chang BH, Danesh FR (2011) MicroRNA-29c is a signature microRNA under high glucose conditions that targets Sprouty homolog 1, and its in vivo knockdown prevents progression of diabetic nephropathy. J Biol Chem 286: 11837-11848. doi:10.1074/jbc.M110.194969. PubMed: 21310958.
15. Martinez I, Cazalla D, Almstead LL, Steitz JA, DiMaio D (2011) miR-29 and miR-30 regulate B-Myb expression during cellular senescence. Proc Natl Acad Sci U S A 108: 522-527. doi:10.1073/pnas.1017346108. PubMed: 21187425.
16. Zhou L, Wang L, Lu L, Jiang P, Sun H et al. (2012) Inhibition of miR-29 by TGF-beta-Smad3 signaling through dual mechanisms promotes transdifferentiation of mouse myoblasts into myofibroblasts. PLOS ONE 7: e33766. doi:10.1371/journal.pone.0033766. PubMed: 22438993.
17. Moustakas A, Souchelnytskyi S, Heldin CH (2001) Smad regulation in TGF-beta signal transduction. J Cell Sci 114: 4359-4369. PubMed: 11792802.
18. Zhang X, Zhao X, Fiskus W, Lin J, Lwin T et al. (2012) Coordinated silencing of MYC-mediated miR-29 by HDAC3 and EZH2 as a therapeutic target of histone modification in aggressive B-Cell lymphomas. Cancer Cell 22: 506-523. doi:10.1016/j.ccr.2012.09.003. PubMed: 23079660.
19. Damaser MS, Arner A, Uvelius B (1996) Partial outlet obstruction induces chronic distension and increased stiffness of rat urinary bladder. Neurourol Urodyn 15: 650-665. doi:10.1002/(SICI)1520-6777(1996)15:6. PubMed: 8916117.
20. Malkowicz SB, Wein AJ, Elbadawi A, Van AK, Ruggieri MR et al. (1986) Acute biochemical and functional alterations in the partially obstructed rabbit urinary bladder. J Urol 136: 1324-1329. PubMed: 2877099.
21. Maciejewski CC, Honardoust D, Tredget EE, Metcalfe PD (2012) Differential expression of class I small leucine-rich proteoglycans in an animal model of partial bladder outlet obstruction. J Urol 188: 1543-1548. doi:10.1016/j.juro. 2012.03.045. PubMed: 22910252.
22. Collado A, Batista E, Gelabert-Más A, Corominas JM, Arañó P et al. (2006) Detrusor quantitative morphometry in obstructed males and controls. J Urol 176: 2722-2728. doi:10.1016/j.juro.2006. 07.131. PubMed: 17085203.
23. Aitken KJ, Bagli DJ (2009) The bladder extracellular matrix. Part I: architecture, development and disease. Nat. Rev Urol 6: 596-611. doi:10.1038/nrurol.2009.201.
24. Baskin LS, Sutherland RS, Thomson AA, Hayward SW, Cunha GR (1996) Growth factors and receptors in bladder development and obstruction. Lab Invest 75: 157-166. PubMed: 8765316.
25. Anumanthan G, Tanaka ST, Adams CM, Thomas JC, Wills ML et al. (2009) Bladder stromal loss of transforming growth factor receptor II decreases fibrosis after bladder obstruction. J Urol 182: 1775-1780. doi:10.1016/j.juro. 2009.05.126. PubMed: 19692014.
26. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ et al. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264. doi:10.1093/biostatistics/4. 2.249. PubMed: 12925520.
27. Turczynska KM, Sadegh MK, Hellstrand P, Swärd K, Albinsson S (2012) MicroRNAs are essential for stretch-induced vascular smooth muscle contractile differentiation via microRNA (miR)-145-dependent expression of L-type calcium channels. J Biol Chem 287: 19199-19206. doi:10.1074/jbc.M112.341073. PubMed: 22474293.
28. Sadegh MK, Ekman M, Rippe C, Sundler F, Wierup N et al. (2011) Biomechanical properties and innervation of the female caveolin-1-deficient detrusor. Br J Pharmacol 162: 1156-1170. doi:10.1111/j.1476-5381.2010.01115.x. PubMed: 21091642.
29. Veerla S, Ringnér M, Höglund M (2010) Genome-wide transcription factor binding site/promoter databases for the analysis of gene sets and co-occurrence of transcription factor binding motifs. BMC Genomics 11: 145. doi:10.1186/1471-2164-11-145. PubMed: 20193056.
30. Storey JD, Tibshirani R (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci U S A 100: 9440-9445. doi:10.1073/pnas.1530509100. PubMed: 12883005.
31. Sengupta S, den Boon JA, Chen IH, Newton MA, Stanhope SA et al. (2008) MicroRNA 29c is down-regulated in nasopharyngeal carcinomas, up-regulating mRNAs encoding extracellular matrix proteins. Proc Natl Acad Sci U S A 105: 5874-5878. doi:10.1073/pnas.0801130105. PubMed: 18390668.
32. Gheinani AH, Burkhard FC, Monastyrskaya K (2013) Deciphering microRNA code in pain and inflammation: lessons from bladder pain syndrome. Cell Mol Life Sci 70: 3773-3789. doi:10.1007/s00018-013-1275-7. PubMed: 23463234.
33. Imamura M, Sugino Y, Long X, Slivano OJ, Nishikawa N et al. (2013) Myocardin and microRNA-1 modulate bladder activity through connexin 43 expression during post-natal development. J Cell Physiol 228: 1819-1826. doi:10.1002/jcp.24333. PubMed: 23359472.
34. Liu X, Yue J, Frey RS, Zhu Q, Mulder KM (1998) Transforming growth factor beta signaling through Smad1 in human breast cancer cells. Cancer Res 58: 4752-4757. PubMed: 9788633.
35. Pannu J, Nakerakanti S, Smith E, ten DP, Trojanowska M (2007) Transforming growth factor-beta receptor type I-dependent fibrogenic gene program is mediated via activation of Smad1 and ERK1/2 pathways. J Biol Chem 282: 10405-10413. doi:10.1074/jbc.M611742200. PubMed: 17317656.
36. Wrighton KH, Lin X, Yu PB, Feng XH (2009) Transforming Growth Factor {beta} Can Stimulate Smad1 Phosphorylation Independently of Bone Morphogenic Protein Receptors. J Biol Chem 284: 9755-9763. doi:10.1074/jbc.M809223200. PubMed: 19224917.
37. Karim OM, Seki N, Mostwin JL (1992) Detrusor hyperplasia and expression of "immediate early" genes with onset of abnormal urodynamic parameters. Am J Physiol 263: R1284-R1290. PubMed: 1481940.
38. Persson K, an - Mckinney T, Steers WD, Tuttle JB (2001) Activation of the transcription factors nuclear factor-kappaB and activator protein-1 in bladder smooth muscle exposed to outlet obstruction and mechanical stretching. J Urol 165: 633-639. doi:10.1097/00005392-200102000-00086. PubMed: 11176450. Available online at: doi:10.1097/00005392-200102000-00086 Available online at: PubMed: 11176450
39. Chaqour B, Yang R, Sha Q (2006) Mechanical stretch modulates the promoter activity of the profibrotic factor CCN2 through increased actin polymerization and NF-kappaB activation. J Biol Chem 281: 20608-20622. doi:10.1074/jbc. M600214200. PubMed: 16707502.
40. Heissmeyer V, Krappmann D, Wulczyn FG, Scheidereit C (1999) NFkappaB p105 is a target of IkappaB kinases and controls signal induction of Bcl-3-p50 complexes. EMBO J 18: 4766-4778. doi:10.1093/emboj/18.17.4766. PubMed: 10469655.
41. Albinsson S, Swärd K (2013) Targeting smooth muscle microRNAs for therapeutic benefit in vascular disease. Pharmacolpharmacol Res 75: 28-36. doi:10.1016/j.phrs.2013.04.003. PubMed: 23611811.
42. Hayashi K, Takamizawa K, Nakamura T, Kato T, Tsushima N (1987) Effects of elastase on the stiffness and elastic properties of arterial walls in cholesterol-fed rabbits. Atherosclerosis 66: 259-267. doi:10.1016/0021-9150(87) 90069-4. PubMed: 3651177.
43. Tuna BG, Bakker EN, Vanbavel E (2013) Relation between active and passive biomechanics of small mesenteric arteries during remodeling. J Biomech 46: 1420-1426. doi:10.1016/j.jbiomech.2013.03.010. PubMed: 23566877.
44. Cortivo R, Pagano F, Passerini G, Abatangelo G, Castellani I (1981) Elastin and collagen in the normal and obstructed urinary bladder. Br J Urol 53: 134-137. doi:10.1111/j.1464-410X.1981.tb03151.x. PubMed: 7237045.
45. Uvelius B, Lindner P, Mattiasson A (1991) Collagen content in the rat urinary bladder following removal of an experimental infravesical outlet obstruction. Urol Int 47: 245-249. doi:10.1159/000282230. PubMed: 1781110.
46. Nielsen KK, Andersen CB, Petersen LK, Oxlund H, Nordling J (1995) Morphological, stereological, and biochemical analysis of the mini-pig urinary bladder after chronic outflow obstruction and after recovery from obstruction. Neurourol Urodyn 14: 269-284. doi:10.1002/nau.1930140308. PubMed: 7647809.
47. Bradshaw AD (2009) The role of SPARC in extracellular matrix assembly. J Cell Commun Signal 3: 239-246. doi:10.1007/s12079-009-0062-6. PubMed: 19798598.
48. Takahashi M, Eda A, Fukushima T, Hohjoh H (2012) Reduction of type IV collagen by upregulated miR-29 in normal elderly mouse and klotho-deficient, senescence-model mouse. PLOS ONE 7: e48974. doi:10.1371/journal.pone.0048974. PubMed: 23139829.
49. Hanafusa H, Torii S, Yasunaga T, Nishida E (2002) Sprouty1 and Sprouty2 provide a control mechanism for the Ras/MAPK signalling pathway. Nat Cell Biol 4: 850-858. doi:10.1038/ncb867. PubMed: 12402043.
50. Martinez I, DiMaio D (2011) B-Myb, cancer, senescence, and microRNAs. Cancer Res 71: 5370-5373. doi: 10.1158/0008-5472.CAN-11-1044. PubMed: 21828240.