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Published Online: 9 August 2013

Interplay Between Heme Oxygenase-1 and miR-378 Affects Non-Small Cell Lung Carcinoma Growth, Vascularization, and Metastasis

Publication: Antioxidants & Redox Signaling
Volume 19, Issue Number 7

Abstract

Aims: Heme oxygenase-1 (HO-1, HMOX1) can prevent tumor initiation; while in various tumors, it has been demonstrated to promote growth, angiogenesis, and metastasis. Here, we investigated whether HMOX1 can modulate microRNAs (miRNAs) and regulate human non-small cell lung carcinoma (NSCLC) development. Results: Stable HMOX1 overexpression in NSCLC NCI-H292 cells up-regulated tumor-suppressive miRNAs, whereas it significantly diminished the expression of oncomirs and angiomirs. The most potently down-regulated was miR-378. HMOX1 also up-regulated p53, down-regulated angiopoietin-1 (Ang-1) and mucin-5AC (MUC5AC), reduced proliferation, migration, and diminished angiogenic potential. Carbon monoxide was a mediator of HMOX1 effects on proliferation, migration, and miR-378 expression. In contrast, stable miR-378 overexpression decreased HMOX1 and p53; while enhanced expression of MUC5AC, vascular endothelial growth factor (VEGF), interleukin-8 (IL-8), and Ang-1, and consequently increased proliferation, migration, and stimulation of endothelial cells. Adenoviral delivery of HMOX1 reversed miR-378 effect on the proliferation and migration of cancer cells. In vivo, HMOX1 overexpressing tumors were smaller, less vascularized and oxygenated, and less metastatic. Overexpression of miR-378 exerted opposite effects. Accordingly, in patients with NSCLC, HMOX1 expression was lower in metastases to lymph nodes than in primary tumors. Innovation and Conclusion: In vitro and in vivo data indicate that the interplay between HMOX1 and miR-378 significantly modulates NSCLC progression and angiogenesis, suggesting miR-378 as a new therapeutic target. Rebound Track: This work was rejected during standard peer review and rescued by Rebound Peer Review (Antioxid Redox Signal 16, 293–296, 2012) with the following serving as open reviewers: James F. George, Mahin D. Maines, Justin C. Mason, and Yasufumi Sato. Antioxid. Redox Signal. 19, 644–660.

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Information & Authors

Information

Published In

cover image Antioxidants & Redox Signaling
Antioxidants & Redox Signaling
Volume 19Issue Number 7September 1, 2013
Pages: 644 - 660
PubMed: 23617628

History

Published in print: September 1, 2013
Published online: 9 August 2013
Published ahead of print: 27 June 2013
Published ahead of production: 25 April 2013
Accepted: 8 April 2013
Revision received: 29 March 2013
Received: 11 January 2013

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    Authors

    Affiliations

    Klaudia Skrzypek
    Department of Medical Biotechnology, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Krakow, Poland.
    Centre de Biophysique Moléculaire, CNRS UPR 4301, Orleans, France.
    Magdalena Tertil
    Department of Medical Biotechnology, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Krakow, Poland.
    Centre de Biophysique Moléculaire, CNRS UPR 4301, Orleans, France.
    Slawomir Golda
    Department of Medical Biotechnology, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Krakow, Poland.
    Maciej Ciesla
    Department of Medical Biotechnology, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Krakow, Poland.
    Kazimierz Weglarczyk
    Centre de Biophysique Moléculaire, CNRS UPR 4301, Orleans, France.
    Department of Clinical Immunology, Polish-American Institute of Paediatrics, Jagiellonian University Medical College, Krakow, Poland.
    Guillaume Collet
    Centre de Biophysique Moléculaire, CNRS UPR 4301, Orleans, France.
    Alan Guichard
    Centre de Biophysique Moléculaire, CNRS UPR 4301, Orleans, France.
    Magdalena Kozakowska
    Department of Medical Biotechnology, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Krakow, Poland.
    Jorge Boczkowski
    Inserm U955, Creteil, France.
    Halina Was
    Department of Medical Biotechnology, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Krakow, Poland.
    Tomasz Gil
    Department of Thoracic Surgery, Jagiellonian University Medical College, Krakow, Poland.
    Jaroslaw Kuzdzal
    Department of Thoracic Surgery, Jagiellonian University Medical College, Krakow, Poland.
    Lucie Muchova
    Fourth Department of Internal Medicine and Institute of Medical Biochemistry and Laboratory Medicine, First Faculty of Medicine, Charles University in Prague, Prague, Czech Republic.
    Libor Vitek
    Fourth Department of Internal Medicine and Institute of Medical Biochemistry and Laboratory Medicine, First Faculty of Medicine, Charles University in Prague, Prague, Czech Republic.
    Agnieszka Loboda
    Department of Medical Biotechnology, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Krakow, Poland.
    Alicja Jozkowicz
    Department of Medical Biotechnology, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Krakow, Poland.
    Claudine Kieda
    *
    Centre de Biophysique Moléculaire, CNRS UPR 4301, Orleans, France.
    Jozef Dulak*
    Department of Medical Biotechnology, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Krakow, Poland.

    Notes

    Address correspondence to:Prof. Jozef DulakDepartment of Medical BiotechnologyFaculty of Biochemistry, Biophysics and BiotechnologyJagiellonian UniversityGronostajowa 730-387 KrakowPoland
    E-mail: [email protected]
    Sponsoring Peers: James F. George, Mahin D. Maines, Justin C. Mason, and Yasufumi Sato (see Review Comments in shaded box).

    Author Disclosure Statement

    All authors declare that no competing financial interests exist.

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