Literature DB >> 25986942

In oesophageal squamous cells, nitric oxide causes S-nitrosylation of Akt and blocks SOX2 (sex determining region Y-box 2) expression.

Kiyotaka Asanuma1, Xiaofang Huo2, Agoston Agoston3, Xi Zhang2, Chunhua Yu2, Edaire Cheng4, Qiuyang Zhang2, Kerry B Dunbar2, Thai H Pham5, David H Wang6, Katsunori Iijima7, Tooru Shimosegawa7, Robert D Odze3, Stuart J Spechler6, Rhonda F Souza6.   

Abstract

OBJECTIVE: Barrett's metaplasia might develop if GORD causes oesophageal squamous cells to convert into columnar cells. Acid and bile exposures upregulate columnar differentiation genes like CDX2 in oesophageal squamous cells, but it is not known if such exposures downregulate squamous differentiation genes like SOX2. In addition to acid and bile, patients with GORD also have high oesophageal concentrations of nitric oxide (NO). This study aims to determine how acid, bile salts and NO affect genes that influence oesophageal cell phenotype.
DESIGN: Oesophageal squamous cells from patients with Barrett's oesophagus were exposed to acidic bile salts or NOC-9 (an NO donor). SOX2, p63 (squamous transcription factor) and CDX2 mRNAs were measured by quantitative RT-PCR. SOX2 and its regulatory Akt pathway proteins were evaluated by western blotting. S-nitrosylation by NO was blocked by dithiothreitol. Immunohistochemistry for SOX2 was performed on the oesophagus of rats with surgically induced GORD which were fed diets with and without nitrite supplementation.
RESULTS: In oesophageal squamous cells, NO profoundly decreased SOX2 protein and caused a significantly greater decrease in SOX2 mRNA than did acidic bile salts. NO also decreased p63 and increased CDX2 expression. NO caused S-nitrosylation of Akt, blocking its phosphorylation. Akt pathway inhibition by LY294002 or Akt siRNA reduced SOX2 mRNA. Rats fed with nitrite-supplemented diets exhibited weaker SOX2 oesophageal staining than rats fed with normal diets.
CONCLUSIONS: In oesophageal squamous cells, NO blocks SOX2 expression through Akt S-nitrosylation. NO also increases CDX2 and decreases p63 expression. By triggering molecular events preventing squamous differentiation while promoting intestinal differentiation, NO might contribute to Barrett's pathogenesis. Published by the BMJ Publishing Group Limited. For permission to use (where not already granted under a licence) please go to http://www.bmj.com/company/products-services/rights-and-licensing/

Entities:  

Keywords:  BARRETT'S METAPLASIA; GASTROESOPHAGEAL REFLUX DISEASE; NITRIC OXIDE

Mesh:

Substances:

Year:  2015        PMID: 25986942      PMCID: PMC4651671          DOI: 10.1136/gutjnl-2015-309272

Source DB:  PubMed          Journal:  Gut        ISSN: 0017-5749            Impact factor:   23.059


  54 in total

1.  Down-regulation of a gastric transcription factor, Sox2, and ectopic expression of intestinal homeobox genes, Cdx1 and Cdx2: inverse correlation during progression from gastric/intestinal-mixed to complete intestinal metaplasia.

Authors:  Tetsuya Tsukamoto; Kenichi Inada; Harunari Tanaka; Tsutomu Mizoshita; Mami Mihara; Toshikazu Ushijima; Yoshitaka Yamamura; Shigeo Nakamura; Masae Tatematsu
Journal:  J Cancer Res Clin Oncol       Date:  2003-12-04       Impact factor: 4.553

2.  Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex.

Authors:  D D Sarbassov; David A Guertin; Siraj M Ali; David M Sabatini
Journal:  Science       Date:  2005-02-18       Impact factor: 47.728

Review 3.  PI3K: downstream AKTion blocks apoptosis.

Authors:  T F Franke; D R Kaplan; L C Cantley
Journal:  Cell       Date:  1997-02-21       Impact factor: 41.582

4.  Regulation of Cdx2 expression by promoter methylation, and effects of Cdx2 transfection on morphology and gene expression of human esophageal epithelial cells.

Authors:  Tong Liu; Xinyan Zhang; Chi-Kwong So; Su Wang; Peng Wang; Liying Yan; Rene Myers; Zhigang Chen; Amy P Patterson; Chung S Yang; Xiaoxin Chen
Journal:  Carcinogenesis       Date:  2006-09-21       Impact factor: 4.944

5.  A pSMAD/CDX2 complex is essential for the intestinalization of epithelial metaplasia.

Authors:  Luigi Mari; Francesca Milano; Kaushal Parikh; Danielle Straub; Vincent Everts; Kees K Hoeben; Paul Fockens; Navtej S Buttar; Kausilia K Krishnadath
Journal:  Cell Rep       Date:  2014-05-01       Impact factor: 9.423

Review 6.  Systematic review: role of acid, weakly acidic and weakly alkaline reflux in gastro-oesophageal reflux disease.

Authors:  G E Boeckxstaens; A Smout
Journal:  Aliment Pharmacol Ther       Date:  2010-05-18       Impact factor: 8.171

7.  SOX2 redirects the developmental fate of the intestinal epithelium toward a premature gastric phenotype.

Authors:  Lalini Raghoebir; Elvira R M Bakker; Jason C Mills; Sigrid Swagemakers; Marjon Buscop-van Kempen; Anne Boerema-de Munck; Siska Driegen; Dies Meijer; Frank Grosveld; Dick Tibboel; Ron Smits; Robbert J Rottier
Journal:  J Mol Cell Biol       Date:  2012-06-07       Impact factor: 6.216

8.  Bone morphogenetic protein 4 expressed in esophagitis induces a columnar phenotype in esophageal squamous cells.

Authors:  Francesca Milano; Jantine W P M van Baal; Navtej S Buttar; Agnieszka M Rygiel; Floor de Kort; Cathrine J DeMars; Wilda D Rosmolen; Jacques J G H M Bergman; Jan VAn Marle; Kenneth K Wang; Maikel P Peppelenbosch; Kausilia K Krishnadath
Journal:  Gastroenterology       Date:  2007-03-19       Impact factor: 22.682

9.  SOX2 expression is an early event in a murine model of EGFR mutant lung cancer and promotes proliferation of a subset of EGFR mutant lung adenocarcinoma cell lines.

Authors:  Irem Dogan; Shigeru Kawabata; Emily Bergbower; Joell J Gills; Abdullah Ekmekci; Willie Wilson; Charles M Rudin; Phillip A Dennis
Journal:  Lung Cancer       Date:  2014-03-29       Impact factor: 5.705

10.  Proteomic quantification and site-mapping of S-nitrosylated proteins using isobaric iodoTMT reagents.

Authors:  Zhe Qu; Fanjun Meng; Ryan D Bomgarden; Rosa I Viner; Jilong Li; John C Rogers; Jianlin Cheng; C Michael Greenlief; Jiankun Cui; Dennis B Lubahn; Grace Y Sun; Zezong Gu
Journal:  J Proteome Res       Date:  2014-06-13       Impact factor: 4.466

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  10 in total

1.  Aspirin prevents NF-κB activation and CDX2 expression stimulated by acid and bile salts in oesophageal squamous cells of patients with Barrett's oesophagus.

Authors:  Xiaofang Huo; Xi Zhang; Chunhua Yu; Edaire Cheng; Qiuyang Zhang; Kerry B Dunbar; Thai H Pham; John P Lynch; David H Wang; Robert S Bresalier; Stuart J Spechler; Rhonda F Souza
Journal:  Gut       Date:  2017-04-25       Impact factor: 23.059

Review 2.  From Reflux Esophagitis to Esophageal Adenocarcinoma.

Authors:  Rhonda F Souza
Journal:  Dig Dis       Date:  2016-06-22       Impact factor: 2.404

Review 3.  Pathogenesis and Cells of Origin of Barrett's Esophagus.

Authors:  Jianwen Que; Katherine S Garman; Rhonda F Souza; Stuart Jon Spechler
Journal:  Gastroenterology       Date:  2019-05-10       Impact factor: 22.682

Review 4.  Reflux esophagitis and its role in the pathogenesis of Barrett's metaplasia.

Authors:  Rhonda Frances Souza
Journal:  J Gastroenterol       Date:  2017-04-27       Impact factor: 7.527

Review 5.  Mechanisms and pathophysiology of Barrett oesophagus.

Authors:  Rhonda F Souza; Stuart J Spechler
Journal:  Nat Rev Gastroenterol Hepatol       Date:  2022-06-07       Impact factor: 73.082

6.  Kyoto international consensus report on anatomy, pathophysiology and clinical significance of the gastro-oesophageal junction.

Authors:  Kentaro Sugano; Stuart Jon Spechler; Emad M El-Omar; Kenneth E L McColl; Kaiyo Takubo; Takuji Gotoda; Mitsuhiro Fujishiro; Katsunori Iijima; Haruhiro Inoue; Takashi Kawai; Yoshikazu Kinoshita; Hiroto Miwa; Ken-Ichi Mukaisho; Kazunari Murakami; Yasuyuki Seto; Hisao Tajiri; Shobna Bhatia; Myung-Gyu Choi; Rebecca C Fitzgerald; Kwong Ming Fock; Khean-Lee Goh; Khek Yu Ho; Varocha Mahachai; Maria O'Donovan; Robert Odze; Richard Peek; Massimo Rugge; Prateek Sharma; Jose D Sollano; Michael Vieth; Justin Wu; Ming-Shiang Wu; Duowu Zou; Michio Kaminishi; Peter Malfertheiner
Journal:  Gut       Date:  2022-06-20       Impact factor: 31.793

Review 7.  SOX2 protein biochemistry in stemness, reprogramming, and cancer: the PI3K/AKT/SOX2 axis and beyond.

Authors:  Thorsten Schaefer; Claudia Lengerke
Journal:  Oncogene       Date:  2019-09-02       Impact factor: 9.867

8.  GATA4 blocks squamous epithelial cell gene expression in human esophageal squamous cells.

Authors:  Roman Stavniichuk; Ann DeLaForest; Cayla A Thompson; James Miller; Rhonda F Souza; Michele A Battle
Journal:  Sci Rep       Date:  2021-02-05       Impact factor: 4.379

9.  Nitric oxide as a regulator of B. anthracis pathogenicity.

Authors:  Taissia G Popova; Allison Teunis; Haley Vaseghi; Weidong Zhou; Virginia Espina; Lance A Liotta; Serguei G Popov
Journal:  Front Microbiol       Date:  2015-09-02       Impact factor: 5.640

Review 10.  Pillars and Gaps of S-Nitrosylation-Dependent Epigenetic Regulation in Physiology and Cancer.

Authors:  Luisa Salvatori; Francesco Spallotta; Carlo Gaetano; Barbara Illi
Journal:  Life (Basel)       Date:  2021-12-17
  10 in total

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