Literature DB >> 23238769

A20 promotes liver regeneration by decreasing SOCS3 expression to enhance IL-6/STAT3 proliferative signals.

Cleide G da Silva1, Peter Studer, Marco Skroch, Jerome Mahiou, Darlan C Minussi, Clayton R Peterson, Suzhuei W Wilson, Virendra I Patel, Averil Ma, Eva Csizmadia, Christiane Ferran.   

Abstract

UNLABELLED: Liver regeneration is of major clinical importance in the setting of liver injury, resection, and transplantation. A20, a potent antiinflammatory and nuclear factor kappa B (NF-κB) inhibitory protein, has established pro-proliferative properties in hepatocytes, in part through decreasing expression of the cyclin dependent kinase inhibitor, p21. Both C-terminal (7-zinc fingers; 7Zn) and N-terminal (Nter) domains of A20 were required to decrease p21 and inhibit NF-κB. However, both independently increased hepatocyte proliferation, suggesting that additional mechanisms contributed to the pro-proliferative function of A20 in hepatocytes. We ascribed one of A20's pro-proliferative mechanisms to increased and sustained interleukin (IL)-6-induced signal transducer and activator of transcription 3 (STAT3) phosphorylation, as a result of decreased hepatocyte expression of the negative regulator of IL-6 signaling, suppressor of cytokine signaling 3 (SOCS3). This novel A20 function segregates with its 7Zn not Nter domain. Conversely, total and partial loss of A20 in hepatocytes increased SOCS3 expression, hampering IL-6-induced STAT3 phosphorylation. Following liver resection in mice pro-proliferative targets downstream of IL-6/STAT3 signaling were increased by A20 overexpression and decreased by A20 knockdown. In contrast, IL-6/STAT3 proinflammatory targets were increased in A20-deficient livers, and decreased or unchanged in A20 overexpressing livers. Upstream of SOCS3, levels of its microRNA regulator miR203 were significantly decreased in A20-deficient livers.
CONCLUSION: A20 enhances IL-6/STAT3 pro-proliferative signals in hepatocytes by down-regulating SOCS3, likely through a miR203-dependent manner. This finding together with A20 reducing the levels of the potent cell cycle brake p21 establishes its pro-proliferative properties in hepatocytes and prompts the pursuit of A20-based therapies to promote liver regeneration and repair.
Copyright © 2013 American Association for the Study of Liver Diseases.

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Year:  2013        PMID: 23238769      PMCID: PMC3626749          DOI: 10.1002/hep.26197

Source DB:  PubMed          Journal:  Hepatology        ISSN: 0270-9139            Impact factor:   17.425


  35 in total

1.  STAT3 contributes to the mitogenic response of hepatocytes during liver regeneration.

Authors:  Wei Li; Xianping Liang; Christoph Kellendonk; Valeria Poli; Rebecca Taub
Journal:  J Biol Chem       Date:  2002-05-24       Impact factor: 5.157

2.  Interleukin-6-induced STAT3 and AP-1 amplify hepatocyte nuclear factor 1-mediated transactivation of hepatic genes, an adaptive response to liver injury.

Authors:  J I Leu; M A Crissey; J P Leu; G Ciliberto; R Taub
Journal:  Mol Cell Biol       Date:  2001-01       Impact factor: 4.272

3.  Regulatory effect of SOCS on NF-kappaB activity in murine monocytes/macrophages.

Authors:  Sun-Hee Park; Kyoung-Eun Kim; Ha-Young Hwang; Tae Yoon Kim
Journal:  DNA Cell Biol       Date:  2003-02       Impact factor: 3.311

4.  A20 protects mice from D-galactosamine/lipopolysaccharide acute toxic lethal hepatitis.

Authors:  Maria B Arvelo; Jeffrey T Cooper; Christopher Longo; Soizic Daniel; Shane T Grey; Jerome Mahiou; Eva Czismadia; Graziella Abu-Jawdeh; Christiane Ferran
Journal:  Hepatology       Date:  2002-03       Impact factor: 17.425

5.  Stem cell factor restores hepatocyte proliferation in IL-6 knockout mice following 70% hepatectomy.

Authors:  Xiaodan Ren; Cory Hogaboam; Audra Carpenter; Lisa Colletti
Journal:  J Clin Invest       Date:  2003-11       Impact factor: 14.808

6.  De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-kappaB signalling.

Authors:  Ingrid E Wertz; Karen M O'Rourke; Honglin Zhou; Michael Eby; L Aravind; Somasekar Seshagiri; Ping Wu; Christian Wiesmann; Rohan Baker; David L Boone; Averil Ma; Eugene V Koonin; Vishva M Dixit
Journal:  Nature       Date:  2004-07-18       Impact factor: 49.962

7.  A20 protects endothelial cells from TNF-, Fas-, and NK-mediated cell death by inhibiting caspase 8 activation.

Authors:  Soizic Daniel; Maria B Arvelo; Virendra I Patel; Christopher R Longo; Gautam Shrikhande; Tala Shukri; Jerome Mahiou; David W Sun; Christina Mottley; Shane T Grey; Christiane Ferran
Journal:  Blood       Date:  2004-07-13       Impact factor: 22.113

8.  Interleukin 6 is important for survival after partial hepatectomy in mice.

Authors:  Alex Blindenbacher; Xueya Wang; Igor Langer; Rocco Savino; Luigi Terracciano; Markus H Heim
Journal:  Hepatology       Date:  2003-09       Impact factor: 17.425

9.  SOCS3 negatively regulates IL-6 signaling in vivo.

Authors:  Ben A Croker; Danielle L Krebs; Jian-Guo Zhang; Sam Wormald; Tracy A Willson; Edouard G Stanley; Lorraine Robb; Christopher J Greenhalgh; Irmgard Förster; Björn E Clausen; Nicos A Nicola; Donald Metcalf; Douglas J Hilton; Andrew W Roberts; Warren S Alexander
Journal:  Nat Immunol       Date:  2003-05-18       Impact factor: 25.606

10.  A20 modulates lipid metabolism and energy production to promote liver regeneration.

Authors:  Scott M Damrauer; Peter Studer; Cleide G da Silva; Christopher R Longo; Haley E Ramsey; Eva Csizmadia; Gautam V Shrikhande; Salvatore T Scali; Towia A Libermann; Manoj K Bhasin; Christiane Ferran
Journal:  PLoS One       Date:  2011-03-17       Impact factor: 3.240

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  33 in total

1.  Significant lethality following liver resection in A20 heterozygous knockout mice uncovers a key role for A20 in liver regeneration.

Authors:  P Studer; C G da Silva; J M Revuelta Cervantes; A Mele; E Csizmadia; J J Siracuse; S M Damrauer; C R Peterson; D Candinas; D M Stroka; A Ma; M Bhasin; C Ferran
Journal:  Cell Death Differ       Date:  2015-05-15       Impact factor: 15.828

2.  Blockade of the apelin-APJ system promotes mouse liver regeneration by activating Kupffer cells after partial hepatectomy.

Authors:  Shohei Yoshiya; Ken Shirabe; Daisuke Imai; Takeo Toshima; Yo-ichi Yamashita; Toru Ikegami; Shinji Okano; Tomoharu Yoshizumi; Hirofumi Kawanaka; Yoshihiko Maehara
Journal:  J Gastroenterol       Date:  2014-08-23       Impact factor: 7.527

3.  A20 Attenuates Liver Fibrosis in NAFLD and Inhibits Inflammation Responses.

Authors:  Xiaohan Wang; Luoyan Ai; Qingqing Xu; Changwei Wu; Zhiwei Chen; Dazhi Su; Xiaoke Jiang; Zhuping Fan
Journal:  Inflammation       Date:  2017-06       Impact factor: 4.092

4.  Induction of the inflammatory regulator A20 by gibberellic acid in airway epithelial cells.

Authors:  J A Reihill; B Malcomson; A Bertelsen; S Cheung; A Czerwiec; R Barsden; J S Elborn; H Dürkop; B Hirsch; M Ennis; C Kelly; B C Schock
Journal:  Br J Pharmacol       Date:  2015-07-21       Impact factor: 8.739

5.  Activation of the IL-6/JAK/STAT3 signaling pathway in human middle ear cholesteatoma epithelium.

Authors:  Wei Liu; Shumin Xie; Xing Chen; Xingwang Rao; Hongmiao Ren; Bing Hu; Tuanfang Yin; Yuyan Xiang; Jihao Ren
Journal:  Int J Clin Exp Pathol       Date:  2014-01-15

6.  SOCS1 is a negative regulator of metabolic reprogramming during sepsis.

Authors:  Annie Rocio Piñeros Alvarez; Nicole Glosson-Byers; Stephanie Brandt; Soujuan Wang; Hector Wong; Sarah Sturgeon; Brian Paul McCarthy; Paul R Territo; Jose Carlos Alves-Filho; C Henrique Serezani
Journal:  JCI Insight       Date:  2017-07-06

Review 7.  A20 at the Crossroads of Cell Death, Inflammation, and Autoimmunity.

Authors:  Arne Martens; Geert van Loo
Journal:  Cold Spring Harb Perspect Biol       Date:  2020-01-02       Impact factor: 10.005

8.  A20 deficiency causes spontaneous neuroinflammation in mice.

Authors:  Renata Padilha Guedes; Eva Csizmadia; Herwig P Moll; Averil Ma; Christiane Ferran; Cleide Gonçalves da Silva
Journal:  J Neuroinflammation       Date:  2014-07-16       Impact factor: 8.322

9.  Interleukin-6 and rs1800796 locus single nucleotide polymorphisms in response to hypoxia/reoxygenation in hepatocytes.

Authors:  Zhaowen Wang; Shaohan Wu; Jianhua Liao; Lin Zhong; Tonghai Xing; Junwei Fan; Zhihai Peng
Journal:  Int J Mol Med       Date:  2016-05-18       Impact factor: 4.101

10.  miR-382 targeting PTEN-Akt axis promotes liver regeneration.

Authors:  Yihua Bei; Yang Song; Fei Wang; Jasmina Dimitrova-Shumkovska; Yang Xiang; Yingying Zhao; Jingqi Liu; Junjie Xiao; Changqing Yang
Journal:  Oncotarget       Date:  2016-01-12
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