RNA interference-induced hepatotoxicity results from loss of the first synthesized isoform of microRNA-122 in mice

Nature Medicine

Volumn 22, Issue 5, 2016, Pages 557-562

  Valdmanis, Paul N ^a   Gu, Shuo ^a,c   Chu, Kirk ^a   Jin, Lan ^a   Zhang, Feijie ^a   Munding, Elizabeth M ^a   Zhang, Yue ^a   Huang, Yong ^a   Kutay, Huban ^b   Ghoshal, Kalpana ^b   Lisowski, Leszek ^a,d   Kay, Mark A ^a  

^a STANFORD UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d CHILDREN'S MEDICAL RESEARCH INSTITUTE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MICRORNA 122; MICRORNA 122 5P; NUCLEOTIDE; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; ALANINE AMINOTRANSFERASE; ALPHA 1 ANTITRYPSIN; MESSENGER RNA; MIRN122 MICRORNA, HUMAN; MIRN122 MICRORNA, MOUSE; RNA ISOFORM; SMALL INTERFERING RNA;

ADENO ASSOCIATED VIRUS; ANIMAL EXPERIMENT; ARTICLE; CHOLESTEROL SYNTHESIS; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; GENE REPRESSION; HOMEOSTASIS; LETHALITY; LIVER TOXICITY; MACHINE; MOUSE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; RNA INTERFERENCE; RNAI THERAPEUTICS; STEROID METABOLISM; TURNOVER TIME; ADVERSE EFFECTS; ANIMAL; DEPENDOPARVOVIRUS; EPIGENETIC REPRESSION; GENE SILENCING; GENE VECTOR; GENETICS; HEK293 CELL LINE; HUMAN; KNOCKOUT MOUSE; LIVER DISEASES; METABOLISM; NORTHERN BLOTTING; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS;

ALANINE TRANSAMINASE; ALPHA 1-ANTITRYPSIN; ANIMALS; BLOTTING, NORTHERN; DEPENDOVIRUS; EPIGENETIC REPRESSION; GENE KNOCKDOWN TECHNIQUES; GENETIC VECTORS; HEK293 CELLS; HUMANS; LIVER DISEASES; MICE; MICE, KNOCKOUT; MICRORNAS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA ISOFORMS; RNA, MESSENGER; RNA, SMALL INTERFERING; RNAI THERAPEUTICS; SEQUENCE ANALYSIS, RNA;

EID: 84963553305     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.4079     Document Type: Article

References (44)

1. Kay, M.A. State-of-the-art gene-based therapies: the road ahead. Nat. Rev. Genet. 12, 316-328 (2011).
2. Grimm, D. et al. Fatality in mice due to oversaturation of cellular microRNA-short hairpin RNA pathways. Nature 441, 537-541 (2006).
3. Lares, M.R., Rossi, J.J., Ouellet, D.L. RNAi and small interfering RNAs in human disease therapeutic applications. Trends Biotechnol. 28, 570-579 (2010).
4. Maguire, A.M. et al. Age-dependent effects of RPE65 gene therapy for Leber's congenital amaurosis: a phase 1 dose-escalation trial. Lancet 374, 1597-1605 (2009).
5. Rodino-Klapac, L.R., Chicoine, L.G., Kaspar, B.K., Mendell, J.R. Gene therapy for Duchenne muscular dystrophy: expectations and challenges. Arch. Neurol. 64, 1236-1241 (2007).
6. Nakai, H. et al. Large-scale molecular characterization of adeno-associated virus vector integration in mouse liver. J. Virol. 79, 3606-3614 (2005).
7. Grimm, D. et al. Argonaute proteins are key determinants of RNAi efficacy, toxicity and persistence in the adult mouse liver. J. Clin. Invest. 120, 3106-3119 (2010).
8. Sekine, S. et al. Disruption of Dicer1 induces dysregulated fetal gene expression and promotes hepatocarcinogenesis. Gastroenterology 136, 2304-2315.e1-4 (2009).
9. Hand, N.J., Master, Z.R., Le Lay, J., Friedman, J.R. Hepatic function is preserved in the absence of mature microRNAs. Hepatology 49, 618-626 (2009).
10. Hsu, S.H. et al. Essential metabolic, anti-inflammatory and antitumorigenic functions of miR-122 in liver. J. Clin. Invest. 122, 2871-2883 (2012).
11. Tsai, W.C. et al. MicroRNA-122 plays a critical role in liver homeostasis and hepatocarcinogenesis. J. Clin. Invest. 122, 2884-2897 (2012).
12. Gu, S. et al. The loop position of shRNAs and pre-miRNAs is critical for the accuracy of dicer processing in vivo. Cell 151, 900-911 (2012).
13. Lagos-Quintana, M. et al. Identification of tissue-specific microRNAs from mouse. Curr. Biol. 12, 735-739 (2002).
14. Chang, J. et al. miR-122, a mammalian liver-specific microRNA, is processed from hcr mRNA and may downregulate the high-affinity cationic amino acid transporter CAT-1. RNA Biol. 1, 106-113 (2004).
15. Landgraf, P. et al. A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 129, 1401-1414 (2007).
16. Katoh, T. et al. Selective stabilization of mammalian microRNAs by 3? adenylation mediated by the cytoplasmic poly(A) polymerase GLD-2. Genes Dev. 23, 433-438 (2009).
17. Cross, N.C., Tolan, D.R., Cox, T.M. Catalytic deficiency of human aldolase B in hereditary fructose intolerance caused by a common missense mutation. Cell 53, 881-885 (1988).
18. Luna, J.M. et al. Hepatitis C virus RNA functionally sequesters miR-122. Cell 160, 1099-1110 (2015).
19. Castoldi, M. et al. The liver-specific microRNA miR-122 controls systemic iron homeostasis in mice. J. Clin. Invest. 121, 1386-1396 (2011).
20. Esau, C. et al. miR-122 regulation of lipid metabolism revealed by in vivo antisense targeting. Cell Metab. 3, 87-98 (2006).
21. Gatfield, D. et al. Integration of microRNA miR-122 in hepatic circadian gene expression. Genes Dev. 23, 1313-1326 (2009).
22. Krützfeldt, J. et al. Silencing of microRNAs in vivo with 'antagomirs'. Nature 438, 685-689 (2005).
23. Xie, J. et al. Long-term, efficient inhibition of microRNA function in mice using rAAV vectors. Nat. Methods 9, 403-409 (2012).
24. Hommes, F.A., Draisma, M.I. The development of L-and M-type aldolases in rat liver. Biochim. Biophys. Acta 222, 251-252 (1970).
25. Numazaki, M., Tsutsumi, K., Tsutsumi, R., Ishikawa, K. Expression of aldolase isozyme mRNAs in fetal rat liver. Eur. J. Biochem. 142, 165-170 (1984).
26. Bhattacharyya, S.N., Habermacher, R., Martine, U., Closs, E.I., Filipowicz, W. Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell 125, 1111-1124 (2006).
27. Kandathil, A.J. et al. Use of laser-capture microdissection to map hepatitis C virus-positive hepatocytes in human liver. Gastroenterology 145, 1404-13.e1-10 (2013).
28. Elmén, J. et al. Antagonism of microRNA-122 in mice by systemically administered LNA-antimiR leads to upregulation of a large set of predicted target mRNAs in the liver. Nucleic Acids Res. 36, 1153-1162 (2008).
29. Helwak, A., Kudla, G., Dudnakova, T., Tollervey, D. Mapping the human miRNA interactome by CLASH reveals frequent noncanonical binding. Cell 153, 654-665 (2013).
30. Loeb, G.B. et al. Transcriptome-wide miR-155 binding map reveals widespread noncanonical microRNA targeting. Mol. Cell 48, 760-770 (2012).
31. Betel, D., Koppal, A., Agius, P., Sander, C., Leslie, C. Comprehensive modeling of microRNA targets predicts functional nonconserved and noncanonical sites. Genome Biol. 11, R90 (2010).
32. Jenkins, D.D. et al. Donor-derived, liver-specific protein expression after bone marrow transplantation. Transplantation 78, 530-536 (2004).
33. 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 120, 15-20 (2005).
34. Langmead, B., Trapnell, C., Pop, M., Salzberg, S.L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).
35. Ers, S., Huber, W. Differential expression analysis for sequence-count data. Genome Biol. 11, R106 (2010).
36. Selitsky, S.R. et al. Small tRNA-derived RNAs are increased and more abundant than microRNAs in chronic hepatitis B and C. Sci. Rep. 5, 7675 (2015).
37. Trapnell, C. et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562-578 (2012).
38. Trapnell, C. et al. Transcript assembly and quantification by RNA-seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28, 511-515 (2010).
39. Huang, W., Sherman, B.T., Lempicki, R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57 (2009).
40. Huang, W., Sherman, B.T., Lempicki, R.A. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37, 1-13 (2009).
41. Bartonicek, N., Enright, A.J. SylArray: a web server for automated detection of miRNA effects from expression data. Bioinformatics 26, 2900-2901 (2010).
42. Paraskevopoulou, M.D. et al. DIANA-microT web server v5.0: service integration into miRNA functional-analysis workflows. Nucleic Acids Res. 41, W169-W173 (2013).
43. Lu, J., Zhang, F., Kay, M.A. A mini-intronic plasmid (MIP): a novel robust transgene expression vector in vivo and in vitro. Mol. Ther. 21, 954-963 (2013).
44. Bogerd, H.P., Whisnant, A.W., Kennedy, E.M., Flores, O., Cullen, B.R. Derivation and characterization of Dicer-and microRNA-deficient human cells. RNA 20, 923-937 (2014).