Systemic delivery of scAAV8-encoded MiR-29a ameliorates hepatic fibrosis in carbon tetrachloride-treated mice

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Knabel, Matthew K ^a   Ramachandran, Kalyani ^a   Karhadkar, Sunil ^b   Hwang, Hun Way ^c   Creamer, Tyler J ^a   Chivukula, Raghu R ^d   Sheikh, Farooq ^e   Clark, K Reed ^f,j   Torbenson, Michael ^g   Montgomery, Robert A ^a   Cameron, Andrew M ^a   Mendell, Joshua T ^h,i   Warren, Daniel S ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

^e WASHINGTON HOSPITAL CENTER   (United States)

^f NATIONWIDE CHILDREN S HOSPITAL   (United States)

^g MAYO CLINIC   (United States)

^h UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

ⁱ UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^j ULTRAGENYX PHARMACEUTICAL INC   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CARBON TETRACHLORIDE; MICRORNA; MICRORNA 29A; MICRORNA 29B; MICRORNA 29C; PARVOVIRUS VECTOR; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; MIRN29 MICRORNA, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFECT; DRUG EFFICACY; DRUG MEGADOSE; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; LIVER CELL; LIVER FIBROSIS; LIVER PROTECTION; MOUSE; NONHUMAN; STELLATE CELL; SYSTEMIC THERAPY; TRANSGENE; VIRAL GENE DELIVERY SYSTEM; ADMINISTRATION AND DOSAGE; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL LINE; CHEMICAL AND DRUG INDUCED LIVER INJURY; CHEMICALLY INDUCED; DEPENDOPARVOVIRUS; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; GENE VECTOR; GENETICS; HEPATIC STELLATE CELL; LIVER CIRRHOSIS; METABOLISM; PATHOLOGY;

ADENO-ASSOCIATED VIRUS; MUS;

ANIMALS; CARBON TETRACHLORIDE; CELL LINE; CHEMICAL AND DRUG INDUCED LIVER INJURY; DEPENDOVIRUS; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; GENETIC VECTORS; HEPATIC STELLATE CELLS; HEPATOCYTES; HUMANS; LIVER CIRRHOSIS; MICE; MICRORNAS; TRANSFORMING GROWTH FACTOR BETA;

EID: 84928632182     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0124411     Document Type: Article

References (38)

1. Wynn TA. Cellular and molecular mechanisms of fibrosis. Altmann DM, Douek DC, editors. J Pathol [Internet]. 2007 ed. 2008 Jan; 214(2):199-210. Available from: http://www.ncbi.nlm.nih.gov/entrez/query. fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list-uids=18161745 PMID: 18161745
2. Vettori S. Role of MicroRNAs in Fibrosis. TORJ. Bentham Science Publishers; 2012 Jun 15; 6(1):130-9.
3. Bowen T, Jenkins RH, Fraser DJ. MicroRNAs, transforming growth factor beta-1, and tissue fibrosis. J Pathol. 2013 Jan; 229(2):274-85. doi: 10.1002/path.4119 PMID: 23042530
4. Rutnam ZJ, Wight TN, Yang BB. miRNAs regulate expression and function of extracellular matrix molecules. Matrix Biology. 2013 Mar; 32(2):74-85. doi: 10.1016/j.matbio.2012.11.003 PMID: 23159731
5. Bartel DP. MicroRNAs: Target Recognition and Regulatory Functions. Cell [Internet]. 2009 ed. 2009 Jan 23; 136(2):215-33. Available from: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list-uids=19167326 doi: 10.1016/j.cell.2009.01.002 PMID: 19167326
6. Chang T-C, Mendell JT. microRNAs in vertebrate physiology and human disease. Annu Rev Genomics Hum Genet. 2007 ed. 2007; 8:215-39. PMID: 17506656
7. Mendell JT, Olson EN. MicroRNAs in Stress Signaling and Human Disease. Cell. 2012 Mar; 148 (6):1172-87. doi: 10.1016/j.cell.2012.02.005 PMID: 22424228
8. Thorsen SB, Obad S, Jensen NF, Stenvang J, Kauppinen S. The Therapeutic Potential of MicroRNAs in Cancer. The Cancer Journal. 2012; 18(3):275-84. doi: 10.1097/PPO.0b013e318258b5d6 PMID: 22647365
9. Bader AG, Brown D, Stoudemire J, Lammers P. Developing therapeutic microRNAs for cancer. Gene Therapy. 2011 Jun 2; 18(12):1121-6. doi: 10.1038/gt.2011.79 PMID: 21633392
10. van Rooij E, Sutherland LB, Thatcher JE, DiMaio JM, Naseem RH, Marshall WS, et al. Dysregulation of microRNAs after myocardial infarction reveals a role of miR-29 in cardiac fibrosis. Proc Natl Acad Sci USA. 2008 ed. 2008 Sep 2; 105(35):13027-32. doi: 10.1073/pnas.0805038105 PMID: 18723672
11. Li Z, Hassan MQ, Jafferji M, Aqeilan RI, Garzon R, Croce CM, et al. Biological functions of miR-29b contribute to positive regulation of osteoblast differentiation. J Biol Chem. 2009 ed. 2009 Jun 5; 284 (23):15676-84. doi: 10.1074/jbc.M809787200 PMID: 19342382
12. Ott CE, Grunhagen J, Jager M, Horbelt D, Schwill S, Kallenbach K, et al. MicroRNAs differentially expressed in postnatal aortic development downregulate elastin via 3' UTR and coding-sequence binding sites. PLoS ONE. 2011 ed. 2011; 6(1):e16250. doi: 10.1371/journal.pone.0016250 PMID: 21305018
13. Abonnenc M, Nabeebaccus AA, Mayr U, Barallobre-Barreiro J, Dong X, Cuello F, et al. Extracellular Matrix Secretion by Cardiac Fibroblasts: Role of microRNA-29b and microRNA-30c. Circ Res. Lippincott Williams & Wilkins; 2013 Sep 4; 113(10):1138-47. doi: 10.1161/CIRCRESAHA.113.302400 PMID: 24006456
14. Kwiecinski M, Noetel A, Elfimova N, Trebicka J, Schievenbusch S, Strack I, et al. Hepatocyte Growth Factor (HGF) Inhibits Collagen I and IV Synthesis in Hepatic Stellate Cells by miRNA-29 Induction. PLoS ONE. 2011 Sep 9; 6(9):e24568. doi: 10.1371/journal.pone.0024568 PMID: 21931759
15. Wang B, Komers R, Carew R, Winbanks CE, Xu B, Herman-Edelstein M, et al. Suppression of micro-RNA-29 expression by TGF-β1 promotes collagen expression and renal fibrosis. Journal of the American Society of Nephrology. 2012 Feb; 23(2):252-65. doi: 10.1681/ASN.2011010055 PMID: 22095944
16. Cushing L, Kuang PP, Qian J, Shao F, Wu J, Little F, et al. miR-29 Is a Major Regulator of Genes Associated with Pulmonary Fibrosis. Am J Respir Cell Mol Biol. 2010 ed. 2011 Aug; 45(2):287-94. doi: 10.1165/rcmb.2010-0323OC PMID: 20971881
17. Luna C, Li G, Qiu J, Epstein DL, Gonzalez P. Cross-talk between miR-29 and transforming growth factor-betas in trabecular meshwork cells. Invest Ophthalmol Vis Sci. 2011 ed. 2011 May; 52(6):3567-72. doi: 10.1167/iovs.10-6448 PMID: 21273536
18. Maurer B, Stanczyk J, Jüngel A, Akhmetshina A, Trenkmann M, Brock M, et al. MicroRNA-29, a key regulator of collagen expression in systemic sclerosis. Arthritis & Rheumatism [Internet]. 2010 ed. 2010 Mar 3; 62(6):1733-43. Available from: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list-uids=20201077
19. Qin W, Chung ACK, Huang XR, Meng XM, Hui DSC, Yu CM, et al. TGF-{beta}/Smad3 Signaling Promotes Renal Fibrosis by Inhibiting miR-29. Journal of the American Society of Nephrology [Internet]. 2011 ed. 2011 Jul 29; 22(8):1462-74. Available from: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi? cmd=Retrieve&db=PubMed&dopt=Citation&list-uids=21784902 doi: 10.1681/ASN.2010121308 PMID: 21784902
20. Villarreal G, Oh DJ, Kang MH, Rhee DJ. Coordinated Regulation of Extracellular Matrix Synthesis by the MicroRNA-29 Family in the Trabecular Meshwork. Investigative Ophthalmology & Visual Science. Association for Research in Vision and Ophthalmology; 2011 May 2; 52(6):3391-7.
21. Roderburg C, Urban G-W, Bettermann K, Vucur M, Zimmermann H, Schmidt S, et al. Micro-RNA profiling reveals a role for miR-29 in human and murine liver fibrosis. Hepatology [Internet]. 2010 ed. 2010 Oct 1; 53(1):209-18. Available from: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list-uids=20890893 doi: 10.1002/hep.23922 PMID: 20890893
22. Kriegel AJ, Liu Y, Fang Y, Ding X, Liang M. The miR-29 family: genomics, cell biology, and relevance to renal and cardiovascular injury. physiolgenomicsphysiologyorg.
23. Zhang Y, Wu L, Wang Y, Zhang M, Li L, Zhu D, et al. Protective Role of Estrogen-induced miRNA-29 Expression in Carbon Tetrachloride-induced Mouse Liver Injury. Journal of Biological Chemistry. 2012 Apr 27; 287(18):14851-62. doi: 10.1074/jbc.M111.314922 PMID: 22393047
24. Mingozzi F, High KA. Therapeutic in vivo gene transfer for genetic disease using AAV: progress and challenges. Nat Rev Genet. 2011 ed. 2011 May; 12(5):341-55. doi: 10.1038/nrg2988 PMID: 21499295
25. Kota J, Chivukula RR, O'Donnell KA, Wentzel EA, Montgomery CL, Hwang HW, et al. Therapeutic microRNA delivery suppresses tumorigenesis in a murine liver cancer model. Cell. 2009 ed. 2009 Jun 12; 137(6):1005-17. doi: 10.1016/j.cell.2009.04.021 PMID: 19524505
26. Wakabayashi-Ito N, Nagata S. Characterization of the regulatory elements in the promoter of the human elongation factor-1 alpha gene. J Biol Chem. 1994 ed. 1994 Nov 25; 269(47):29831-7. PMID: 7961976
27. Song S, Lu Y, Choi YK, Han Y, Tang Q, Zhao G, et al. DNA-dependent PK inhibits adeno-associated virus DNA integration. Proc Natl Acad Sci USA. 2004 ed. 2004 Feb 17; 101(7):2112-6. PMID: 14766968
28. Kogure T, Costinean S, Yan I, Braconi C, Croce C, Patel T. Hepatic miR-29ab1 expression modulates chronic hepatic injury. Journal of Cellular and Molecular Medicine. 2012 Nov; 16(11):2647-54. doi: 10.1111/j.1582-4934.2012.01578.x PMID: 22469499
29. Xiao J, Meng X-M, Huang XR, Chung AC, Feng Y-L, Hui DS, et al. miR-29 Inhibits Bleomycin-induced Pulmonary Fibrosis in Mice. Mol Ther. 2012 Mar 6; 20(6):1251-60. doi: 10.1038/mt.2012.36 PMID: 22395530
30. Wang L, Zhou L, Jiang P, Lu L, Chen X, Lan H, et al. Loss of miR-29 in Myoblasts Contributes to Dystrophic Muscle Pathogenesis. Mol Ther. 2012 Mar 20; 20(6):1222-33. doi: 10.1038/mt.2012.35 PMID: 22434133
31. Grimm D, Pandey K, Nakai H, Storm TA, Kay MA. Liver transduction with recombinant adeno-associated virus is primarily restricted by capsid serotype not vector genotype. J Virol. 2006 Jan; 80(1):426-39. PMID: 16352567
32. Nakai H, Fuess S, Storm TA, Muramatsu SI, Nara Y, Kay MA. Unrestricted Hepatocyte Transduction with Adeno-Associated Virus Serotype 8 Vectors in Mice. J Virol. 2004 Dec 13; 79(1):214-24.
33. Katakowski M, Buller B, Wang X, Rogers T, Chopp M. Functional microRNA is transferred between glioma cells. Cancer Research. 2010 Nov 1; 70(21):8259-63. doi: 10.1158/0008-5472.CAN-10-0604 PMID: 20841486
34. Montecalvo A, Larregina AT, Shufesky WJ, Stolz DB, Sullivan MLG, Karlsson JM, et al. Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes. Blood. 2012 Jan 19; 119(3):756-66. doi: 10.1182/blood-2011-02-338004 PMID: 22031862
35. Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, Lötvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007 Jun; 9(6):654-9. PMID: 17486113
36. Mittelbrunn M, Gutiérrez-Vázquez C, Villarroya-Beltri C, González S, Sánchez-Cabo F, González MÁ, et al. Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells. Nat Commun. 2011; 2:282. doi: 10.1038/ncomms1285 PMID: 21505438
37. Hu G, Yao H, Chaudhuri AD, Duan M, Yelamanchili SV, Wen H, et al. Exosome-mediated shuttling of microRNA-29 regulates HIV Tat and morphine-mediated Neuronal dysfunction. Cell Death Dis. Nature Publishing Group; 2012 Aug; 3(8):e381.
38. Lim PK, Bliss SA, Patel SA, Taborga M, Dave MA, Gregory LA, et al. Gap junction-mediated import of microRNA from bone marrow stromal cells can elicit cell cycle quiescence in breast cancer cells. Cancer Research. American Association for Cancer Research; 2011 Mar 1; 71(5):1550-60. doi: 10.1158/0008-5472.CAN-10-2372 PMID: 21343399