Abstract
To study the functional role of apoptosis inhibition of myeloid lineage cells in tumor formation, apoptosis inhibitor 6 (Api6/AIM/Sp alpha) was overexpressed in a myeloid-specific c-fms-rtTA/(TetO)(7)-CMV-Api6 bitransgenic mouse model under the control of the c-fms promoter/intron 2. In this bitransgenic system, the Api6-Flag fusion protein was expressed in myeloid lineage cells after doxycycline treatment. Induction of Api6 abnormally elevated levels of macrophages, neutrophils, and dendritic cells in the bone marrow, blood, and lung in vivo. BrdU incorporation and annexin V binding studies showed systemically increased cell proliferation and inhibition of apoptosis in myeloid lineage cells. Api6 overexpression activated oncogenic signaling pathways, including Stat3, Erk1/2, and p38 in myeloid lineage cells in multiple organs of the bitransgenic mice. In the lung, severe inflammation and massive tissue remodeling were observed in association with increased expression of procancer cytokines/chemokines, decreased expression of proapoptosis molecule genes, and increased expression of matrix metalloproteinase genes as a result of Api6 overexpression. Oncogenic CD11b(+)/Gr-1(+) myeloid-derived suppressor cells were systemically increased. After Api6 overexpression, lung adenocarcinoma was observed in bitransgenic mice with a 35% incidence rate. These studies suggest that dysregulation of myeloid cell populations by extracellular Api6 signaling leads to abnormal myelopoiesis and lung cancer.
MeSH Terms
Adenocarcinoma/immunology,metabolism,pathology
Animals
Cell Movement/genetics,immunology
Cell Proliferation
Cells, Cultured
Cytokines/biosynthesis,genetics
Down-Regulation/immunology
Extracellular Space/genetics,immunology
Inflammation Mediators/metabolism,physiology
Lung Neoplasms/immunology,metabolism,pathology
Mice
Mice, Transgenic
Myeloid Cells/immunology,metabolism,pathology
Myeloproliferative Disorders/genetics,immunology,metabolism
Receptor, Macrophage Colony-Stimulating Factor/genetics
Receptors, Immunologic/antagonists & inhibitors,biosynthesis,genetics,physiology
Signal Transduction/genetics,immunology
Up-Regulation/immunology
Chemicals
Cytokines
Inflammation Mediators
Receptors, Immunologic
SPalpha protein, mouse
Receptor, Macrophage Colony-Stimulating Factor
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Qu Peng
Center for Immunobiology, Indiana University School of Medicine, Indianapolis, IN 46202, USA.
Du Hong
Li Yuan
Yan Cong
References (31)
31 references, click to expand
-
Physiological functions of caspases beyond cell death.
Am J Pathol. 2006 Sep;169(3):729-37
PMID: 16936249
-
Requirement of transcription factor PU.1 in the development of multiple hematopoietic lineages.
Science. 1994 Sep 9;265(5178):1573-7
PMID: 8079170
-
Altered macrophage differentiation and immune dysfunction in tumor development.
J Clin Invest. 2007 May;117(5):1155-66
PMID: 17476345
-
Kinetics of B cell receptor signaling in human B cell subsets mapped by phosphospecific flow cytometry.
J Immunol. 2006 Aug 1;177(3):1581-9
PMID: 16849466
-
Association of AIM, a novel apoptosis inhibitory factor, with hepatitis via supporting macrophage survival and enhancing phagocytotic function of macrophages.
J Biol Chem. 2001 Jun 22;276(25):22910-4
PMID: 11294859
-
Smoldering and polarized inflammation in the initiation and promotion of malignant disease.
Cancer Cell. 2005 Mar;7(3):211-7
PMID: 15766659
-
AIM inhibits apoptosis of T cells and NKT cells in Corynebacterium-induced granuloma formation in mice.
Am J Pathol. 2003 Mar;162(3):837-47
PMID: 12598318
-
Lysosomal acid lipase-deficient mice: depletion of white and brown fat, severe hepatosplenomegaly, and shortened life span.
J Lipid Res. 2001 Apr;42(4):489-500
PMID: 11290820
-
Increased susceptibility of thymocytes to apoptosis in mice lacking AIM, a novel murine macrophage-derived soluble factor belonging to the scavenger receptor cysteine-rich domain superfamily.
J Exp Med. 1999 Jan 18;189(2):413-22
PMID: 9892623
-
LXR-dependent gene expression is important for macrophage survival and the innate immune response.
Cell. 2004 Oct 15;119(2):299-309
PMID: 15479645
-
A macrophage colony-stimulating factor receptor-green fluorescent protein transgene is expressed throughout the mononuclear phagocyte system of the mouse.
Blood. 2003 Feb 1;101(3):1155-63
PMID: 12393599
-
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
-
High-content single-cell drug screening with phosphospecific flow cytometry.
Nat Chem Biol. 2008 Feb;4(2):132-42
PMID: 18157122
-
Overexpression of Stat3C in pulmonary epithelium protects against hyperoxic lung injury.
J Immunol. 2005 Jun 1;174(11):7250-6
PMID: 15905571
-
Macrophage functional maturation and cytokine production are impaired in C/EBP epsilon-deficient mice.
Blood. 2002 Mar 1;99(5):1794-801
PMID: 11861297
-
Maintenance of the mouse type II cell phenotype in vitro.
Am J Physiol Lung Cell Mol Physiol. 2002 Aug;283(2):L256-64
PMID: 12114186
-
Targeted disruption of the mouse lysosomal acid lipase gene: long-term survival with massive cholesteryl ester and triglyceride storage.
Hum Mol Genet. 1998 Sep;7(9):1347-54
PMID: 9700186
-
A role for the apoptosis inhibitory factor AIM/Spalpha/Api6 in atherosclerosis development.
Cell Metab. 2005 Mar;1(3):201-13
PMID: 16054063
-
Macrophages: obligate partners for tumor cell migration, invasion, and metastasis.
Cell. 2006 Jan 27;124(2):263-6
PMID: 16439202
-
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
-
Distinct role of macrophages in different tumor microenvironments.
Cancer Res. 2006 Jan 15;66(2):605-12
PMID: 16423985
-
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
-
Inhibiting Stat3 signaling in the hematopoietic system elicits multicomponent antitumor immunity.
Nat Med. 2005 Dec;11(12):1314-21
PMID: 16288283
-
A role for human Sp alpha as a pattern recognition receptor.
J Biol Chem. 2005 Oct 21;280(42):35391-8
PMID: 16030018
-
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
-
Extrinsic regulators of epithelial tumor progression: metalloproteinases.
Curr Opin Genet Dev. 2000 Feb;10(1):120-7
PMID: 10679388
-
Altered innate immune functioning of dendritic cells in elderly humans: a role of phosphoinositide 3-kinase-signaling pathway.
J Immunol. 2007 Jun 1;178(11):6912-22
PMID: 17513740
-
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
-
Molecular cloning, genomic organization and cell-binding characteristics of mouse Spalpha.
Immunology. 2000 Jan;99(1):78-86
PMID: 10651944
-
Induction and apoptotic regression of lung adenocarcinomas by regulation of a K-Ras transgene in the presence and absence of tumor suppressor genes.
Genes Dev. 2001 Dec 15;15(24):3249-62
PMID: 11751631
-
Metalloelastase is required for macrophage-mediated proteolysis and matrix invasion in mice.
Proc Natl Acad Sci U S A. 1996 Apr 30;93(9):3942-6
PMID: 8632994