Peroxisome Proliferator-Activated Receptor α Regulates a MicroRNA-Mediated Signaling Cascade Responsible for Hepatocellular Proliferation

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Published inMolecular and Cellular Biology Vol. 27; no. 12; pp. 4238 - 4247
Main Authors Shah, Yatrik M., Morimura, Keiichirou, Yang, Qian, Tanabe, Tomotaka, Takagi, Mitsuhiro, Gonzalez, Frank J.
Format Journal Article
LanguageEnglish
Published United States American Society for Microbiology 01.06.2007
Taylor & Francis
Subjects
Animals
Carcinoma, Hepatocellular - etiology
Carcinoma, Hepatocellular - pathology
Carcinoma, Hepatocellular - physiopathology
Cell Line, Tumor
Cell Proliferation
Gene Expression Profiling
Gene Expression Regulation
Genes, Reporter
Liver Neoplasms - etiology
Liver Neoplasms - pathology
Liver Neoplasms - physiopathology
Luciferases - metabolism
Mice
Mice, Knockout
MicroRNAs - metabolism
Models, Genetic
Peroxisome Proliferators - pharmacology
PPAR alpha - genetics
PPAR alpha - metabolism
Proto-Oncogene Proteins c-myc - biosynthesis
Proto-Oncogene Proteins c-myc - genetics
Pyrimidines - pharmacology
Signal Transduction
Online AccessGet full text

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Activation of peroxisome proliferator-activated receptor α (PPARα) leads to hepatocellular proliferation and liver carcinomas. The early events mediating these effects are unknown. A novel mechanism by which PPARα regulates gene expression and hepatocellular proliferation was uncovered. MicroRNA (miRNA) expression profiling demonstrated that activated PPARα was a major regulator of hepatic miRNA expression. Of particular interest, let-7C, an miRNA important in cell growth, was inhibited following 4-h treatment and 2-week and 11-month sustained treatment with the potent PPARα agonist Wy-14,643 in wild-type mice. let-7C was shown to target c-myc via direct interaction with the 3′ untranslated region of c-myc. The PPARα-mediated induction of c-myc via let-7C subsequently increased expression of the oncogenic mir-17-92 cluster; these events did not occur in Ppar α-null mice. Overexpression of let-7C decreased c-myc and mir-17 and suppressed the growth of Hepa-1 cells. Furthermore, using the human PPARα-expressing mouse model, which is responsive to Wy-14,643 effects on β-oxidation and serum triglycerides but resistant to hepatocellular proliferation and tumorigenesis, we demonstrated a critical role for let-7C in liver oncogenesis. Wy-14,643 treatment did not inhibit let-7C or induce c-myc and mir-17 expression. These observations reveal a let-7C signaling cascade critical for PPARα agonist-induced liver proliferation and tumorigenesis.
Activation of peroxisome proliferator-activated receptor α (PPARα) leads to hepatocellular proliferation and liver carcinomas. The early events mediating these effects are unknown. A novel mechanism by which PPARα regulates gene expression and hepatocellular proliferation was uncovered. MicroRNA (miRNA) expression profiling demonstrated that activated PPARα was a major regulator of hepatic miRNA expression. Of particular interest, let-7C, an miRNA important in cell growth, was inhibited following 4-h treatment and 2-week and 11-month sustained treatment with the potent PPARα agonist Wy-14,643 in wild-type mice. let-7C was shown to target c- myc via direct interaction with the 3′ untranslated region of c- myc . The PPARα-mediated induction of c- myc via let-7C subsequently increased expression of the oncogenic mir-17-92 cluster; these events did not occur in Ppar α-null mice. Overexpression of let-7C decreased c- myc and mir-17 and suppressed the growth of Hepa-1 cells. Furthermore, using the human PPARα-expressing mouse model, which is responsive to Wy-14,643 effects on β-oxidation and serum triglycerides but resistant to hepatocellular proliferation and tumorigenesis, we demonstrated a critical role for let-7C in liver oncogenesis. Wy-14,643 treatment did not inhibit let-7C or induce c- myc and mir-17 expression. These observations reveal a let-7C signaling cascade critical for PPARα agonist-induced liver proliferation and tumorigenesis.
Activation of peroxisome proliferator-activated receptor alpha (PPAR alpha ) leads to hepatocellular proliferation and liver carcinomas. The early events mediating these effects are unknown. A novel mechanism by which PPAR alpha regulates gene expression and hepatocellular proliferation was uncovered. MicroRNA (miRNA) expression profiling demonstrated that activated PPAR alpha was a major regulator of hepatic miRNA expression. Of particular interest, let-7C, an miRNA important in cell growth, was inhibited following 4-h treatment and 2-week and 11-month sustained treatment with the potent PPAR alpha agonist Wy-14,643 in wild-type mice. let-7C was shown to target c-myc via direct interaction with the 3' untranslated region of c-myc. The PPAR alpha -mediated induction of c-myc via let-7C subsequently increased expression of the oncogenic mir-17-92 cluster; these events did not occur in Ppar alpha -null mice. Overexpression of let-7C decreased c-myc and mir-17 and suppressed the growth of Hepa-1 cells. Furthermore, using the human PPAR alpha -expressing mouse model, which is responsive to Wy-14,643 effects on {szligbeta}-oxidation and serum triglycerides but resistant to hepatocellular proliferation and tumorigenesis, we demonstrated a critical role for let-7C in liver oncogenesis. Wy-14,643 treatment did not inhibit let-7C or induce c-myc and mir-17 expression. These observations reveal a let-7C signaling cascade critical for PPAR alpha agonist-induced liver proliferation and tumorigenesis.
Activation of peroxisome proliferator-activated receptor alpha (PPARalpha) leads to hepatocellular proliferation and liver carcinomas. The early events mediating these effects are unknown. A novel mechanism by which PPARalpha regulates gene expression and hepatocellular proliferation was uncovered. MicroRNA (miRNA) expression profiling demonstrated that activated PPARalpha was a major regulator of hepatic miRNA expression. Of particular interest, let-7C, an miRNA important in cell growth, was inhibited following 4-h treatment and 2-week and 11-month sustained treatment with the potent PPARalpha agonist Wy-14,643 in wild-type mice. let-7C was shown to target c-myc via direct interaction with the 3' untranslated region of c-myc. The PPARalpha-mediated induction of c-myc via let-7C subsequently increased expression of the oncogenic mir-17-92 cluster; these events did not occur in Pparalpha-null mice. Overexpression of let-7C decreased c-myc and mir-17 and suppressed the growth of Hepa-1 cells. Furthermore, using the human PPARalpha-expressing mouse model, which is responsive to Wy-14,643 effects on beta-oxidation and serum triglycerides but resistant to hepatocellular proliferation and tumorigenesis, we demonstrated a critical role for let-7C in liver oncogenesis. Wy-14,643 treatment did not inhibit let-7C or induce c-myc and mir-17 expression. These observations reveal a let-7C signaling cascade critical for PPARalpha agonist-induced liver proliferation and tumorigenesis.
Author Tomotaka Tanabe
Mitsuhiro Takagi
Qian Yang
Yatrik M. Shah
Keiichirou Morimura
Frank J. Gonzalez
AuthorAffiliation Laboratory of Metabolism, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, Maryland
AuthorAffiliation_xml – name: Laboratory of Metabolism, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, Maryland
Author_xml – sequence: 1
  givenname: Yatrik M.
  surname: Shah
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  organization: Laboratory of Metabolism, Center for Cancer Research, National Cancer Institute, National Institutes of Health
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  givenname: Keiichirou
  surname: Morimura
  fullname: Morimura, Keiichirou
  organization: Laboratory of Metabolism, Center for Cancer Research, National Cancer Institute, National Institutes of Health
– sequence: 3
  givenname: Qian
  surname: Yang
  fullname: Yang, Qian
  organization: Laboratory of Metabolism, Center for Cancer Research, National Cancer Institute, National Institutes of Health
– sequence: 4
  givenname: Tomotaka
  surname: Tanabe
  fullname: Tanabe, Tomotaka
  organization: Laboratory of Metabolism, Center for Cancer Research, National Cancer Institute, National Institutes of Health
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  surname: Gonzalez
  fullname: Gonzalez, Frank J.
  email: fjgonz@helix.nih.gov
  organization: Laboratory of Metabolism, Center for Cancer Research, National Cancer Institute, National Institutes of Health
BackLink https://www.ncbi.nlm.nih.gov/pubmed/17438130$$D View this record in MEDLINE/PubMed
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Corresponding author. Mailing address: Building 37, Room 3106, National Cancer Institute, Bethesda, MD 20892. Phone: (301) 496-9067. Fax: (301) 496-8419. E-mail: fjgonz@helix.nih.gov
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Snippet Article Usage Stats Services MCB Citing Articles Google Scholar PubMed Related Content Social Bookmarking CiteULike Delicious Digg Facebook Google+ Mendeley...
Activation of peroxisome proliferator-activated receptor α (PPARα) leads to hepatocellular proliferation and liver carcinomas. The early events mediating these...
Activation of peroxisome proliferator-activated receptor alpha (PPARalpha) leads to hepatocellular proliferation and liver carcinomas. The early events...
Activation of peroxisome proliferator-activated receptor alpha (PPAR alpha ) leads to hepatocellular proliferation and liver carcinomas. The early events...
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StartPage 4238
SubjectTerms Animals
Carcinoma, Hepatocellular - etiology
Carcinoma, Hepatocellular - pathology
Carcinoma, Hepatocellular - physiopathology
Cell Line, Tumor
Cell Proliferation
Gene Expression Profiling
Gene Expression Regulation
Genes, Reporter
Liver Neoplasms - etiology
Liver Neoplasms - pathology
Liver Neoplasms - physiopathology
Luciferases - metabolism
Mice
Mice, Knockout
MicroRNAs - metabolism
Models, Genetic
Peroxisome Proliferators - pharmacology
PPAR alpha - genetics
PPAR alpha - metabolism
Proto-Oncogene Proteins c-myc - biosynthesis
Proto-Oncogene Proteins c-myc - genetics
Pyrimidines - pharmacology
Signal Transduction
Title Peroxisome Proliferator-Activated Receptor α Regulates a MicroRNA-Mediated Signaling Cascade Responsible for Hepatocellular Proliferation
URI http://mcb.asm.org/content/27/12/4238.abstract
https://www.tandfonline.com/doi/abs/10.1128/MCB.00317-07
https://www.ncbi.nlm.nih.gov/pubmed/17438130
https://search.proquest.com/docview/19664023
https://pubmed.ncbi.nlm.nih.gov/PMC1900062
Volume 27
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