Home LiteratureArticle Details
PMID: 23759744 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

miR-17~92 miRNA cluster promotes kidney cyst growth in polycystic kidney disease.

Patel V, Williams D, Hajarnis S, Hunter R, Pontoglio M, Somlo S, Igarashi P

Abstract

Polycystic kidney disease (PKD), the most common genetic cause of chronic kidney failure, is characterized by the presence of numerous, progressively enlarging fluid-filled cysts in the renal parenchyma. The cysts arise from renal tubules and are lined by abnormally functioning and hyperproliferative epithelial cells. Despite recent progress, no Food and Drug Administration-approved therapy is available to retard cyst growth. MicroRNAs (miRNAs) are short noncoding RNAs that inhibit posttranscriptional gene expression. Dysregulated miRNA expression is observed in PKD, but whether miRNAs are directly involved in kidney cyst formation and growth is not known. Here, we show that miR-17∼92, an oncogenic miRNA cluster, is up-regulated in mouse models of PKD. Kidney-specific transgenic overexpression of miR-17∼92 produces kidney cysts in mice. Conversely, kidney-specific inactivation of miR-17∼92 in a mouse model of PKD retards kidney cyst growth, improves renal function, and prolongs survival. miR-17∼92 may mediate these effects by promoting proliferation and through posttranscriptional repression of PKD genes Pkd1, Pkd2, and hepatocyte nuclear factor-1β. These studies demonstrate a pathogenic role of miRNAs in mouse models of PKD and identify miR-17∼92 as a therapeutic target in PKD. Our results also provide a unique hypothesis for disease progression in PKD involving miRNAs and regulation of PKD gene dosage.

Keywords
autosomal dominant polycystic kidney disease cilia kinesin family member 3A
MeSH Terms
Animals Base Sequence Cell Proliferation Disease Models, Animal Disease Progression Kidney Tubules/metabolism,pathology Mice Mice, Knockout Mice, Transgenic MicroRNAs/antagonists & inhibitors,genetics,metabolism Polycystic Kidney, Autosomal Dominant/genetics,metabolism,pathology TRPP Cation Channels/genetics Up-Regulation/genetics
Chemicals
MIRN17-92 microRNA, mouse MicroRNAs TRPP Cation Channels polycystic kidney disease 1 protein polycystic kidney disease 2 protein
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Patel Vishal
Department of Internal Medicine, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA. vishald.patel@utsouthwestern.edu
Williams Darren
Hajarnis Sachin
Hunter Ryan
Pontoglio Marco
Somlo Stefan
Igarashi Peter
References (43)
43 references, click to expand
  1. Mutation of hepatocyte nuclear factor-1beta inhibits Pkhd1 gene expression and produces renal cysts in mice.
    J Clin Invest. 2004 Mar;113(6):814-25 PMID: 15067314
  2. MicroRNAs and fibrosis.
    Curr Opin Nephrol Hypertens. 2012 Jul;21(4):410-6 PMID: 22622653
  3. Polycystin-1 and polycystin-2 regulate the cell cycle through the helix-loop-helix inhibitor Id2.
    Nat Cell Biol. 2005 Dec;7(12):1202-12 PMID: 16311606
  4. Genetics and pathogenesis of polycystic kidney disease.
    J Am Soc Nephrol. 2002 Sep;13(9):2384-98 PMID: 12191984
  5. The RNA-binding protein bicaudal C regulates polycystin 2 in the kidney by antagonizing miR-17 activity.
    Development. 2010 Apr;137(7):1107-16 PMID: 20215348
  6. MicroRNAs: target recognition and regulatory functions.
    Cell. 2009 Jan 23;136(2):215-33 PMID: 19167326
  7. Epithelial-specific Cre/lox recombination in the developing kidney and genitourinary tract.
    J Am Soc Nephrol. 2002 Jul;13(7):1837-46 PMID: 12089379
  8. Kidney-specific inactivation of the KIF3A subunit of kinesin-II inhibits renal ciliogenesis and produces polycystic kidney disease.
    Proc Natl Acad Sci U S A. 2003 Apr 29;100(9):5286-91 PMID: 12672950
  9. Mutations in multiple PKD genes may explain early and severe polycystic kidney disease.
    J Am Soc Nephrol. 2011 Nov;22(11):2047-56 PMID: 22034641
  10. miRiad roles for the miR-17-92 cluster in development and disease.
    Cell. 2008 Apr 18;133(2):217-22 PMID: 18423194
  11. Systems biology approach to identify transcriptome reprogramming and candidate microRNA targets during the progression of polycystic kidney disease.
    BMC Syst Biol. 2011 Apr 25;5:56 PMID: 21518438
  12. Trans-heterozygous Pkd1 and Pkd2 mutations modify expression of polycystic kidney disease.
    Hum Mol Genet. 2002 Aug 1;11(16):1845-54 PMID: 12140187
  13. miR-17~92 cooperates with RB pathway mutations to promote retinoblastoma.
    Genes Dev. 2011 Aug 15;25(16):1734-45 PMID: 21816922
  14. Genetic interaction studies link autosomal dominant and recessive polycystic kidney disease in a common pathway.
    Hum Mol Genet. 2007 Aug 15;16(16):1940-50 PMID: 17575307
  15. MicroRNA-17 post-transcriptionally regulates polycystic kidney disease-2 gene and promotes cell proliferation.
    Mol Biol Rep. 2010 Jul;37(6):2951-8 PMID: 19821056
  16. Advances in the pathogenesis and treatment of polycystic kidney disease.
    Curr Opin Nephrol Hypertens. 2009 Mar;18(2):99-106 PMID: 19430332
  17. The miR-17-5p microRNA is a key regulator of the G1/S phase cell cycle transition.
    Genome Biol. 2008;9(8):R127 PMID: 18700987
  18. Kidney cysts, pancreatic cysts, and biliary disease in a mouse model of autosomal recessive polycystic kidney disease.
    Pediatr Nephrol. 2008 May;23(5):733-41 PMID: 18286309
  19. Lymphoproliferative disease and autoimmunity in mice with increased miR-17-92 expression in lymphocytes.
    Nat Immunol. 2008 Apr;9(4):405-14 PMID: 18327259
  20. Incompletely penetrant PKD1 alleles suggest a role for gene dosage in cyst initiation in polycystic kidney disease.
    Kidney Int. 2009 Apr;75(8):848-55 PMID: 19165178
  21. Microarray-based approach identifies microRNAs and their target functional patterns in polycystic kidney disease.
    BMC Genomics. 2008 Dec 23;9:624 PMID: 19102782
  22. PKD1 induces p21(waf1) and regulation of the cell cycle via direct activation of the JAK-STAT signaling pathway in a process requiring PKD2.
    Cell. 2002 Apr 19;109(2):157-68 PMID: 12007403
  23. A transcriptional network in polycystic kidney disease.
    EMBO J. 2004 Apr 7;23(7):1657-68 PMID: 15029248
  24. Loss of oriented cell division does not initiate cyst formation.
    J Am Soc Nephrol. 2010 Feb;21(2):295-302 PMID: 19959710
  25. Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters.
    Cell. 2008 Mar 7;132(5):875-86 PMID: 18329372
  26. Fibrocystin/polyductin modulates renal tubular formation by regulating polycystin-2 expression and function.
    J Am Soc Nephrol. 2008 Mar;19(3):455-68 PMID: 18235088
  27. Mutations of HNF-1beta inhibit epithelial morphogenesis through dysregulation of SOCS-3.
    Proc Natl Acad Sci U S A. 2007 Dec 18;104(51):20386-91 PMID: 18077349
  28. MicroRNAs in stress signaling and human disease.
    Cell. 2012 Mar 16;148(6):1172-87 PMID: 22424228
  29. Pervasive roles of microRNAs in cardiovascular biology.
    Nature. 2011 Jan 20;469(7330):336-42 PMID: 21248840
  30. c-Myc-regulated microRNAs modulate E2F1 expression.
    Nature. 2005 Jun 9;435(7043):839-43 PMID: 15944709
  31. Polycystic kidney disease.
    Annu Rev Med. 2009;60:321-37 PMID: 18947299
  32. Cyst formation and activation of the extracellular regulated kinase pathway after kidney specific inactivation of Pkd1.
    Hum Mol Genet. 2008 Jun 1;17(11):1505-16 PMID: 18263604
  33. Bilineal disease and trans-heterozygotes in autosomal dominant polycystic kidney disease.
    Am J Hum Genet. 2001 Feb;68(2):355-63 PMID: 11156533
  34. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets.
    Cell. 2005 Jan 14;120(1):15-20 PMID: 15652477
  35. Synthetic lethality between Rb, p53 and Dicer or miR-17-92 in retinal progenitors suppresses retinoblastoma formation.
    Nat Cell Biol. 2012 Sep;14(9):958-65 PMID: 22864477
  36. Toward microRNA-based therapeutics for heart disease: the sense in antisense.
    Circ Res. 2008 Oct 24;103(9):919-28 PMID: 18948630
  37. A genetic interaction network of five genes for human polycystic kidney and liver diseases defines polycystin-1 as the central determinant of cyst formation.
    Nat Genet. 2011 Jun 19;43(7):639-47 PMID: 21685914
  38. Lowering of Pkd1 expression is sufficient to cause polycystic kidney disease.
    Hum Mol Genet. 2004 Dec 15;13(24):3069-77 PMID: 15496422
  39. MicroRNAs regulate renal tubule maturation through modulation of Pkd1.
    J Am Soc Nephrol. 2012 Dec;23(12):1941-8 PMID: 23138483
  40. Acute kidney injury and aberrant planar cell polarity induce cyst formation in mice lacking renal cilia.
    Hum Mol Genet. 2008 Jun 1;17(11):1578-90 PMID: 18263895
  41. A missense mutation in PKD1 attenuates the severity of renal disease.
    Kidney Int. 2012 Feb;81(4):412-7 PMID: 22031115
  42. Functional polycystin-1 dosage governs autosomal dominant polycystic kidney disease severity.
    J Clin Invest. 2012 Nov;122(11):4257-73 PMID: 23064367
  43. A mitotic transcriptional switch in polycystic kidney disease.
    Nat Med. 2010 Jan;16(1):106-10 PMID: 19966811
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2013-06-25
Epub
2013-00-12
Pages
10765-70
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC3696812
Subset
IM
Grants
NIDDK NIH HHS · R37DK042921 · United States
NIDDK NIH HHS · R01 DK054053 · United States
NIDDK NIH HHS · P30DK079328 · United States
NIDDK NIH HHS · RC1 DK086887 · United States
NIDDK NIH HHS · K08 DK084311 · United States
NIDDK NIH HHS · RC1DK086887 · United States
NIDDK NIH HHS · R01DK54053 · United States
NIDDK NIH HHS · R37 DK042921 · United States
NIDDK NIH HHS · P30 DK079328 · United States
NIDDK NIH HHS · K08DK084311 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com