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PMID: 19706765 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Matrix metalloproteinase 12 overexpression in lung epithelial cells plays a key role in emphysema to lung bronchioalveolar adenocarcinoma transition.

Cancer research ·Vol. 69 ·No. 18 ·2009-09-15 ·Pages 7252-61

Qu P, Du H, Wang X, Yan C

Abstract

Chronic obstructive pulmonary disease (COPD) and lung cancer are two diseases that are related to smoking in humans. The molecular mechanism linking these two diseases is poorly understood. Matrix metalloproteinase 12 (MMP12) is a member of the MMP family, which can be induced by smoking. Because MMP12 overexpression in epithelial cells has been reported in inflammation-triggered lung remodeling, a murine CCSP-rtTA/(tetO)(7)-MMP12 bitransgenic model was created. In this model, MMP12-Flag fusion protein overexpression and its increased enzymatic activity were observed in the lung in an inducible manner, which led to inflammatory cell infiltration and increased epithelial growth. In sequential events, spontaneous emphysema and bronchioalveolar adenocarcinoma were developed as a result of MMP12 overexpression. During this process, the concentration of interleukin-6 was steadily increased in bronchioalveolar lavage fluid, which activated the oncogenic signal transducer and activator of transcription 3 (Stat3) in alveolar type II epithelial cells. Expression of Stat3 downstream genes that are known to stimulate inflammation and tumor formation was significantly increased in the lung. When tested in humans, MMP12 up-regulation was highly associated with COPD and lung cancer in patients. Together, these studies support that MMP12 is a potent proinflammatory and oncogenic molecule. MMP12 up-regulation plays a critical role in emphysema to lung cancer transition that is facilitated by inflammation.

MeSH Terms
Adenocarcinoma, Bronchiolo-Alveolar/enzymology,genetics,pathology Animals Apoptosis/physiology Carcinoma, Squamous Cell/enzymology,genetics,pathology Cell Growth Processes/physiology Cell Transformation, Neoplastic/genetics,metabolism,pathology Humans Lung Neoplasms/enzymology,genetics,pathology Matrix Metalloproteinase 12/biosynthesis,genetics Mice Mice, Transgenic Pulmonary Disease, Chronic Obstructive/enzymology,genetics,pathology Pulmonary Emphysema/enzymology,genetics,pathology Up-Regulation
Chemicals
Matrix Metalloproteinase 12
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Qu Peng
The Center for Immunobiology, Simon Cancer Center and Department of Pathology and Laboratory Medicine, Indiana University School of Medicine, Indianapolis, Indiana 46202-5188, USA.
Du Hong
Wang Xi
Yan Cong
References (30)
30 references, click to expand
  1. Elastase secretion by stimulated macrophages. Characterization and regulation.
    J Exp Med. 1975 Aug 1;142(2):361-77 PMID: 167096
  2. Airway hyperresponsiveness and airway obstruction in transgenic mice. Morphologic correlates in mice overexpressing interleukin (IL)-11 and IL-6 in the lung.
    Am J Respir Cell Mol Biol. 2000 Mar;22(3):289-95 PMID: 10696065
  3. Haplotypes in matrix metalloproteinase gene cluster on chromosome 11q22 contribute to the risk of lung cancer development and progression.
    Clin Cancer Res. 2006 Dec 1;12(23):7009-17 PMID: 17145822
  4. Stat3 downstream genes serve as biomarkers in human lung carcinomas and chronic obstructive pulmonary disease.
    Lung Cancer. 2009 Mar;63(3):341-7 PMID: 18614255
  5. Matrix metalloproteinases and the regulation of tissue remodelling.
    Nat Rev Mol Cell Biol. 2007 Mar;8(3):221-33 PMID: 17318226
  6. Activated PPARgamma Targets Surface and Intracellular Signals That Inhibit the Proliferation of Lung Carcinoma Cells.
    PPAR Res. 2008;2008:254108 PMID: 18704200
  7. Gene delivery by the hSP-B promoter to lung alveolar type II epithelial cells in LAL-knockout mice through bone marrow mesenchymal stem cells.
    Gene Ther. 2007 Oct;14(20):1461-70 PMID: 17700706
  8. Lysosomal acid lipase deficiency causes respiratory inflammation and destruction in the lung.
    Am J Physiol Lung Cell Mol Physiol. 2004 Apr;286(4):L801-7 PMID: 14644759
  9. Neutral lipids and peroxisome proliferator-activated receptor-{gamma} control pulmonary gene expression and inflammation-triggered pathogenesis in lysosomal acid lipase knockout mice.
    Am J Pathol. 2005 Sep;167(3):813-21 PMID: 16127159
  10. Regulation of matrix metalloproteinase expression in tumor invasion.
    FASEB J. 1999 May;13(8):781-92 PMID: 10224222
  11. Requirement for macrophage elastase for cigarette smoke-induced emphysema in mice.
    Science. 1997 Sep 26;277(5334):2002-4 PMID: 9302297
  12. Transcriptional inactivation of STAT3 by PPARgamma suppresses IL-6-responsive multiple myeloma cells.
    Immunity. 2004 Feb;20(2):205-18 PMID: 14975242
  13. Matrix metalloproteinase-12 expression correlates with local recurrence and metastatic disease in non-small cell lung cancer patients.
    Clin Cancer Res. 2005 Feb 1;11(3):1086-92 PMID: 15709175
  14. Lung morphometry: a new generation of tools and experiments for organ, tissue, cell, and molecular biology.
    Am J Physiol. 1993 Dec;265(6 Pt 1):L521-48 PMID: 8279570
  15. Critical roles of lysosomal acid lipase in T cell development and function.
    Am J Pathol. 2009 Mar;174(3):944-56 PMID: 19179613
  16. Altered macrophage differentiation and immune dysfunction in tumor development.
    J Clin Invest. 2007 May;117(5):1155-66 PMID: 17476345
  17. Activation of the signal transducers and activators of the transcription 3 pathway in alveolar epithelial cells induces inflammation and adenocarcinomas in mouse lung.
    Cancer Res. 2007 Sep 15;67(18):8494-503 PMID: 17875688
  18. Overexpression of Stat3C in pulmonary epithelium protects against hyperoxic lung injury.
    J Immunol. 2005 Jun 1;174(11):7250-6 PMID: 15905571
  19. Macrophage-specific expression of human lysosomal acid lipase corrects inflammation and pathogenic phenotypes in lal-/- mice.
    Am J Pathol. 2006 Sep;169(3):916-26 PMID: 16936266
  20. Cloning and characterization of a unique elastolytic metalloproteinase produced by human alveolar macrophages.
    J Biol Chem. 1993 Nov 15;268(32):23824-9 PMID: 8226919
  21. Retinoic acid treatment abrogates elastase-induced pulmonary emphysema in rats.
    Nat Med. 1997 Jun;3(6):675-7 PMID: 9176496
  22. Hydrolysis of a broad spectrum of extracellular matrix proteins by human macrophage elastase.
    J Biol Chem. 1997 May 2;272(18):12189-94 PMID: 9115292
  23. Myeloid-specific expression of Api6/AIM/Sp alpha induces systemic inflammation and adenocarcinoma in the lung.
    J Immunol. 2009 Feb 1;182(3):1648-59 PMID: 19155514
  24. Matrix metalloproteinases as modulators of inflammation and innate immunity.
    Nat Rev Immunol. 2004 Aug;4(8):617-29 PMID: 15286728
  25. Low lung function and incident lung cancer in the United States: data From the First National Health and Nutrition Examination Survey follow-up.
    Arch Intern Med. 2003 Jun 23;163(12):1475-80 PMID: 12824098
  26. The regulation of neovascularization of matrix metalloproteinases and their inhibitors.
    Stem Cells. 1997;15(3):180-9 PMID: 9170209
  27. Identification of a CD11b(+)/Gr-1(+)/CD31(+) myeloid progenitor capable of activating or suppressing CD8(+) T cells.
    Blood. 2000 Dec 1;96(12):3838-46 PMID: 11090068
  28. Chromosomal aberrations and gene expression profiles in non-small cell lung cancer.
    Lung Cancer. 2007 May;56(2):175-84 PMID: 17258348
  29. Matrix metalloproteinases. Matrix degradation and more.
    Am J Respir Cell Mol Biol. 1999 Jun;20(6):1100-2 PMID: 10340927
  30. Conditional expression of fibroblast growth factor-7 in the developing and mature lung.
    J Biol Chem. 2000 Apr 21;275(16):11858-64 PMID: 10766812
Article Info
Journal
Cancer research
Abbr.
Cancer Res
ISSN
1538-7445
Published
2009-09-15
Epub
2009-00-25
Pages
7252-61
Language
English
Region
United States
NLM ID
2984705R
PMCID
PMC2753283
Subset
IM
Grants
NHLBI NIH HHS · HL-061803 · United States
NHLBI NIH HHS · R01 HL087001-02 · United States
NHLBI NIH HHS · R01 HL067862 · United States
NHLBI NIH HHS · R01 HL067862-05 · United States
NHLBI NIH HHS · R01 HL061803-09 · United States
NHLBI NIH HHS · R01 HL067862-04 · United States
NHLBI NIH HHS · HL087001 · United States
NHLBI NIH HHS · R01 HL061803-08 · United States
NHLBI NIH HHS · R01 HL087001 · United States
NHLBI NIH HHS · HL-067862 · United States
NHLBI NIH HHS · R01 HL061803 · United States
NCI NIH HHS · CA138759 · United States
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