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Published in: Multidisciplinary Respiratory Medicine 1/2015

Open Access 01-12-2016 | Original research article

Increased expression of A Proliferation-inducing Ligand (APRIL) in lung leukocytes and alveolar epithelial cells in COPD patients with non small cell lung cancer: a possible link between COPD and lung cancer?

Authors: Francesca Polverino, Maria Laucho-Contreras, Joselyn Rojas Quintero, Miguel Divo, Victor Pinto-Plata, Lynette Sholl, Juan P. de-Torres, Bartolome R. Celli, Caroline A. Owen

Published in: Multidisciplinary Respiratory Medicine | Issue 1/2015

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Abstract

Background

Chronic Obstructive Pulmonary Disease (COPD) is characterized by an excessive activation of the adaptive immune system and, in particular, uncontrolled expansion of the B-cell pool. One of the key promoters of B cell expansion is A PRoliferation-Inducing Ligand (APRIL). APRIL has been strongly linked to non small cell lung cancer (NSCLC) onset and progression previously. However, little is known about the expression of APRIL in the lungs of COPD patients.

Methods

Using immuno-fluorescence staining, the expression of APRIL was assessed in sections of lungs from 4 subjects with primary diagnosis of COPD (FEV1 33 ± 20 % predicted), 4 subjects with primary diagnosis of NSCLC, 4 subjects diagnosed with both COPD and NSCLC, smokers without COPD or NSCLC and 3 healthy never-smokers. The percentage of B cells, alveolar macrophages (AMs) and polymorphonuclear neutrophils (PMNs) in the lung and alveolar epithelial cells (AECs) that stained positively for APRIL was quantified using epi-fluorescence microscopy and image analysis software.

Results

The percentage of APRIL-expressing B cells, AMs, PMNs and alveolar epithelial cells (AECs) was higher in patients having both COPD and NSCLC than in patients with either COPD or NSCLC alone, SC or NSC (p < 0.03 for all comparisons). The percentage of APRIL-expressing AMs and AECs (but not in B cells) was higher in patients with NSCLC alone than in patients with COPD alone. The percentage of APRIL-expressing AECs (but not B cells or AMs) was higher in COPD patients than in SC and NSC (p < 0.05 for all comparisons). The percentage of APRIL-expressing B cells, AMs and AECs cells was similar in NSC and SC.

Conclusion

The percentage of APRIL-expressing B cells, AMs and AECs is higher in the lungs of patients with both COPD and NSCLC than in patients with COPD or NSCLC alone or control subjects. These findings suggest that APRIL may contribute to the pathogenesis of both COPD and NSCLC, and possibly to the development of NSCLC in patients with established COPD.
Literature
1.
go back to reference Dillon SR, Harder B, Lewis KB, Moore MD, Liu H, Bukowski TR, et al. B-lymphocyte stimulator/a proliferation-inducing ligand heterotrimers are elevated in the sera of patients with autoimmune disease and are neutralized by atacicept and B-cell maturation antigen-immunoglobulin. Arthritis Res Ther. 2010;12(2):R48.CrossRefPubMedPubMedCentral Dillon SR, Harder B, Lewis KB, Moore MD, Liu H, Bukowski TR, et al. B-lymphocyte stimulator/a proliferation-inducing ligand heterotrimers are elevated in the sera of patients with autoimmune disease and are neutralized by atacicept and B-cell maturation antigen-immunoglobulin. Arthritis Res Ther. 2010;12(2):R48.CrossRefPubMedPubMedCentral
2.
go back to reference Young RP, Hopkins RJ, Christmas T, Black PN, Metcalf P, Gamble GD. COPD prevalence is increased in lung cancer, independent of age, sex and smoking history. Eur Respir J. 2009;34(2):380–6.CrossRefPubMed Young RP, Hopkins RJ, Christmas T, Black PN, Metcalf P, Gamble GD. COPD prevalence is increased in lung cancer, independent of age, sex and smoking history. Eur Respir J. 2009;34(2):380–6.CrossRefPubMed
4.
go back to reference Cooke MS, Evans MD, Dizdaroglu M, Lunec J. Oxidative DNA damage: mechanisms, mutation, and disease. FASEB J. 2003;17(10):1195–214.CrossRefPubMed Cooke MS, Evans MD, Dizdaroglu M, Lunec J. Oxidative DNA damage: mechanisms, mutation, and disease. FASEB J. 2003;17(10):1195–214.CrossRefPubMed
5.
6.
go back to reference Saetta M, Di SA, Turato G, Facchini FM, Corbino L, Mapp CE, et al. CD8+ T-lymphocytes in peripheral airways of smokers with chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 1998;157(3 Pt 1):822–6.CrossRefPubMed Saetta M, Di SA, Turato G, Facchini FM, Corbino L, Mapp CE, et al. CD8+ T-lymphocytes in peripheral airways of smokers with chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 1998;157(3 Pt 1):822–6.CrossRefPubMed
7.
go back to reference Cosio MG, Guerassimov A. Chronic obstructive pulmonary disease. Inflammation of small airways and lung parenchyma. Am J Respir Crit Care Med. 1999;160(5 Pt 2):S21–5.CrossRefPubMed Cosio MG, Guerassimov A. Chronic obstructive pulmonary disease. Inflammation of small airways and lung parenchyma. Am J Respir Crit Care Med. 1999;160(5 Pt 2):S21–5.CrossRefPubMed
8.
go back to reference van der Strate BW, Postma DS, Brandsma CA, Melgert BN, Luinge MA, Geerlings M, et al. Cigarette smoke-induced emphysema: A role for the B cell? Am J Respir Crit Care Med. 2006;173(7):751–8.CrossRefPubMed van der Strate BW, Postma DS, Brandsma CA, Melgert BN, Luinge MA, Geerlings M, et al. Cigarette smoke-induced emphysema: A role for the B cell? Am J Respir Crit Care Med. 2006;173(7):751–8.CrossRefPubMed
9.
go back to reference Hogg JC, Chu F, Utokaparch S, Woods R, Elliott WM, Buzatu L, et al. The nature of small-airway obstruction in chronic obstructive pulmonary disease. N Engl J Med. 2004;350(26):2645–53.CrossRefPubMed Hogg JC, Chu F, Utokaparch S, Woods R, Elliott WM, Buzatu L, et al. The nature of small-airway obstruction in chronic obstructive pulmonary disease. N Engl J Med. 2004;350(26):2645–53.CrossRefPubMed
10.
go back to reference Polverino F, Doyle-Eisele M, McDonald J, Wilder JA, Royer C, Laucho-Contreras M, et al. A novel nonhuman primate model of cigarette smoke-induced airway disease. Am J Pathol. 2015;185(3):741–55.CrossRefPubMedPubMedCentral Polverino F, Doyle-Eisele M, McDonald J, Wilder JA, Royer C, Laucho-Contreras M, et al. A novel nonhuman primate model of cigarette smoke-induced airway disease. Am J Pathol. 2015;185(3):741–55.CrossRefPubMedPubMedCentral
11.
go back to reference Simmons MS, Connett JE, Nides MA, Lindgren PG, Kleerup EC, Murray RP, et al. Smoking reduction and the rate of decline in FEV(1): results from the Lung Health Study. Eur Respir J. 2005;25(6):1011–7.CrossRefPubMed Simmons MS, Connett JE, Nides MA, Lindgren PG, Kleerup EC, Murray RP, et al. Smoking reduction and the rate of decline in FEV(1): results from the Lung Health Study. Eur Respir J. 2005;25(6):1011–7.CrossRefPubMed
13.
go back to reference Polverino F, Cosio BG, Pons J, Laucho-Contreras M, Tejera P, Iglesias A, et al. B Cell-Activating Factor. An Orchestrator of Lymphoid Follicles in Severe Chronic Obstructive Pulmonary Disease. Am J Respir Crit Care Med. 2015;192(6):695–705.CrossRefPubMed Polverino F, Cosio BG, Pons J, Laucho-Contreras M, Tejera P, Iglesias A, et al. B Cell-Activating Factor. An Orchestrator of Lymphoid Follicles in Severe Chronic Obstructive Pulmonary Disease. Am J Respir Crit Care Med. 2015;192(6):695–705.CrossRefPubMed
14.
go back to reference Wauters E, Janssens W, Vansteenkiste J, Decaluwé H, Heulens N, Thienpont B, et al. DNA methylation profiling of non-small cell lung cancer reveals a COPD-driven immune-related signature. Thorax. 2015;70(12):1113–22.CrossRefPubMed Wauters E, Janssens W, Vansteenkiste J, Decaluwé H, Heulens N, Thienpont B, et al. DNA methylation profiling of non-small cell lung cancer reveals a COPD-driven immune-related signature. Thorax. 2015;70(12):1113–22.CrossRefPubMed
15.
16.
go back to reference Rizvi NA, Hellmann MD, Snyder A, Kvistborg P, Makarov V, Havel JJ, et al. Cancer immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science. 2015;348(6230):124–8.CrossRefPubMed Rizvi NA, Hellmann MD, Snyder A, Kvistborg P, Makarov V, Havel JJ, et al. Cancer immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science. 2015;348(6230):124–8.CrossRefPubMed
17.
go back to reference Germain C, Gnjatic S, Tamzalit F, Knockaert S, Remark R, Goc J, et al. Presence of B cells in tertiary lymphoid structures is associated with a protective immunity in patients with lung cancer. Am J Respir Crit Care Med. 2014;189(7):832–44.CrossRefPubMed Germain C, Gnjatic S, Tamzalit F, Knockaert S, Remark R, Goc J, et al. Presence of B cells in tertiary lymphoid structures is associated with a protective immunity in patients with lung cancer. Am J Respir Crit Care Med. 2014;189(7):832–44.CrossRefPubMed
18.
go back to reference Liu J, Wang H, Yu Q, Zheng S, Jiang Y, Liu Y, et al. Aberrant Frequency of IL-10-Producing B Cells and Its Association with Treg and MDSC Cells in Non Small Cell Lung Carcinoma Patients. Hum Immunol. 2015. doi: 10.1016/j.humimm.2015.10.015. [Epub ahead of print]. Liu J, Wang H, Yu Q, Zheng S, Jiang Y, Liu Y, et al. Aberrant Frequency of IL-10-Producing B Cells and Its Association with Treg and MDSC Cells in Non Small Cell Lung Carcinoma Patients. Hum Immunol. 2015. doi: 10.​1016/​j.​humimm.​2015.​10.​015. [Epub ahead of print].
20.
go back to reference Fagarasan S, Honjo T. T-Independent immune response: new aspects of B cell biology. Science. 2000;290(5489):89–92.CrossRefPubMed Fagarasan S, Honjo T. T-Independent immune response: new aspects of B cell biology. Science. 2000;290(5489):89–92.CrossRefPubMed
21.
go back to reference Yan M, Marsters SA, Grewal IS, Wang H, Ashkenazi A, Dixit VM. Identification of a receptor for BLyS demonstrates a crucial role in humoral immunity. Nat Immunol. 2000;1(1):37–41.CrossRefPubMed Yan M, Marsters SA, Grewal IS, Wang H, Ashkenazi A, Dixit VM. Identification of a receptor for BLyS demonstrates a crucial role in humoral immunity. Nat Immunol. 2000;1(1):37–41.CrossRefPubMed
22.
go back to reference Suzuki K, Setoyama Y, Yoshimoto K, Tsuzaka K, Abe T, Takeuchi T. Effect of interleukin-2 on synthesis of B cell activating factor belonging to the tumor necrosis factor family (BAFF) in human peripheral blood mononuclear cells. Cytokine. 2008;44(1):44–8.CrossRefPubMed Suzuki K, Setoyama Y, Yoshimoto K, Tsuzaka K, Abe T, Takeuchi T. Effect of interleukin-2 on synthesis of B cell activating factor belonging to the tumor necrosis factor family (BAFF) in human peripheral blood mononuclear cells. Cytokine. 2008;44(1):44–8.CrossRefPubMed
23.
go back to reference Chu VT, Enghard P, Riemekasten G, Berek C. In vitro and in vivo activation induces BAFF and APRIL expression in B cells. J Immunol. 2007;179(9):5947–57.CrossRefPubMed Chu VT, Enghard P, Riemekasten G, Berek C. In vitro and in vivo activation induces BAFF and APRIL expression in B cells. J Immunol. 2007;179(9):5947–57.CrossRefPubMed
24.
go back to reference Kato A, Truong-Tran AQ, Scott AL, Matsumoto K, Schleimer RP. Airway epithelial cells produce B cell-activating factor of TNF family by an IFN-beta-dependent mechanism. J Immunol. 2006;177(10):7164–72.CrossRefPubMedPubMedCentral Kato A, Truong-Tran AQ, Scott AL, Matsumoto K, Schleimer RP. Airway epithelial cells produce B cell-activating factor of TNF family by an IFN-beta-dependent mechanism. J Immunol. 2006;177(10):7164–72.CrossRefPubMedPubMedCentral
25.
go back to reference Polverino F, Baraldo S, Bazzan E, Agostini S, Turato G, Lunardi F, et al. A novel insight into adaptive immunity in chronic obstructive pulmonary disease: B cell activating factor belonging to the tumor necrosis factor family. Am J Respir Crit Care Med. 2010;182(8):1011–9.CrossRefPubMed Polverino F, Baraldo S, Bazzan E, Agostini S, Turato G, Lunardi F, et al. A novel insight into adaptive immunity in chronic obstructive pulmonary disease: B cell activating factor belonging to the tumor necrosis factor family. Am J Respir Crit Care Med. 2010;182(8):1011–9.CrossRefPubMed
26.
go back to reference Chu VT, Enghard P, Schurer S, Steinhauser G, Rudolph B, Riemekasten G, et al. Systemic activation of the immune system induces aberrant BAFF and APRIL expression in B cells in patients with systemic lupus erythematosus. Arthritis Rheum. 2009;60(7):2083–93.CrossRefPubMed Chu VT, Enghard P, Schurer S, Steinhauser G, Rudolph B, Riemekasten G, et al. Systemic activation of the immune system induces aberrant BAFF and APRIL expression in B cells in patients with systemic lupus erythematosus. Arthritis Rheum. 2009;60(7):2083–93.CrossRefPubMed
27.
go back to reference Jonsson MV, Szodoray P, Jellestad S, Jonsson R, Skarstein K. Association between circulating levels of the novel TNF family members APRIL and BAFF and lymphoid organization in primary Sjogren’s syndrome. J Clin Immunol. 2005;25(3):189–201.CrossRefPubMed Jonsson MV, Szodoray P, Jellestad S, Jonsson R, Skarstein K. Association between circulating levels of the novel TNF family members APRIL and BAFF and lymphoid organization in primary Sjogren’s syndrome. J Clin Immunol. 2005;25(3):189–201.CrossRefPubMed
28.
go back to reference Matsuda Y, Haneda M, Kadomatsu K, Kobayashi T. A proliferation-inducing ligand sustains the proliferation of human naive (CD27(−)) B cells and mediates their differentiation into long-lived plasma cells in vitro via transmembrane activator and calcium modulator and cyclophilin ligand interactor and B-cell mature antigen. Cell Immunol. 2015;295(2):127–36.CrossRefPubMed Matsuda Y, Haneda M, Kadomatsu K, Kobayashi T. A proliferation-inducing ligand sustains the proliferation of human naive (CD27(−)) B cells and mediates their differentiation into long-lived plasma cells in vitro via transmembrane activator and calcium modulator and cyclophilin ligand interactor and B-cell mature antigen. Cell Immunol. 2015;295(2):127–36.CrossRefPubMed
29.
go back to reference Sun B, Wang H, Wang X, Huang H, Ding W, Jing R, et al. A proliferation-inducing ligand: a new biomarker for non-small cell lung cancer. Exp Lung Res. 2009;35(6):486–500.CrossRefPubMed Sun B, Wang H, Wang X, Huang H, Ding W, Jing R, et al. A proliferation-inducing ligand: a new biomarker for non-small cell lung cancer. Exp Lung Res. 2009;35(6):486–500.CrossRefPubMed
30.
go back to reference Qian Z, Qingshan C, Chun J, Huijun Z, Feng L, Qiang W, et al. High expression of TNFSF13 in tumor cells and fibroblasts is associated with poor prognosis in non-small cell lung cancer. Am J Clin Pathol. 2014;141(2):226–33.CrossRefPubMed Qian Z, Qingshan C, Chun J, Huijun Z, Feng L, Qiang W, et al. High expression of TNFSF13 in tumor cells and fibroblasts is associated with poor prognosis in non-small cell lung cancer. Am J Clin Pathol. 2014;141(2):226–33.CrossRefPubMed
31.
go back to reference Hahne M, Kataoka T, Schroter M, Hofmann K, Irmler M, Bodmer JL, et al. APRIL, a new ligand of the tumor necrosis factor family, stimulates tumor cell growth. J Exp Med. 1998;188(6):1185–90.CrossRefPubMedPubMedCentral Hahne M, Kataoka T, Schroter M, Hofmann K, Irmler M, Bodmer JL, et al. APRIL, a new ligand of the tumor necrosis factor family, stimulates tumor cell growth. J Exp Med. 1998;188(6):1185–90.CrossRefPubMedPubMedCentral
32.
go back to reference Roth W, Wagenknecht B, Klumpp A, Naumann U, Hahne M, Tschopp J, et al. APRIL, a new member of the tumor necrosis factor family, modulates death ligand-induced apoptosis. Cell Death Differ. 2001;8(4):403–10.CrossRefPubMed Roth W, Wagenknecht B, Klumpp A, Naumann U, Hahne M, Tschopp J, et al. APRIL, a new member of the tumor necrosis factor family, modulates death ligand-induced apoptosis. Cell Death Differ. 2001;8(4):403–10.CrossRefPubMed
33.
go back to reference Kelly K, Manos E, Jensen G, Nadauld L, Jones DA. APRIL/TRDL-1, a tumor necrosis factor-like ligand, stimulates cell death. Cancer Res. 2000;60(4):1021–7.PubMed Kelly K, Manos E, Jensen G, Nadauld L, Jones DA. APRIL/TRDL-1, a tumor necrosis factor-like ligand, stimulates cell death. Cancer Res. 2000;60(4):1021–7.PubMed
34.
go back to reference Lopez-Fraga M, Fernandez R, Albar JP, Hahne M. Biologically active APRIL is secreted following intracellular processing in the Golgi apparatus by furin convertase. EMBO Rep. 2001;2(10):945–51.CrossRefPubMedPubMedCentral Lopez-Fraga M, Fernandez R, Albar JP, Hahne M. Biologically active APRIL is secreted following intracellular processing in the Golgi apparatus by furin convertase. EMBO Rep. 2001;2(10):945–51.CrossRefPubMedPubMedCentral
35.
go back to reference Seys LJ, Verhamme FM, Schinwald A, Hammad H, Cunoosamy DM, Bantsimba-Malanda C, et al. Role of B Cell-Activating Factor in Chronic Obstructive Pulmonary Disease. Am J Respir Crit Care Med. 2015;192(6):706–18.CrossRefPubMed Seys LJ, Verhamme FM, Schinwald A, Hammad H, Cunoosamy DM, Bantsimba-Malanda C, et al. Role of B Cell-Activating Factor in Chronic Obstructive Pulmonary Disease. Am J Respir Crit Care Med. 2015;192(6):706–18.CrossRefPubMed
36.
go back to reference Sawicka-Powierza J, Jablonska E, Kloczko J, Piszcz J, Garley M, Ratajczk-Wrona W. Evaluation of TNF superfamily molecules release by neutrophils and B leukemic cells of patients with chronic B - cell lymphocytic leukemia. Neoplasma. 2011;58(1):45–50.CrossRefPubMed Sawicka-Powierza J, Jablonska E, Kloczko J, Piszcz J, Garley M, Ratajczk-Wrona W. Evaluation of TNF superfamily molecules release by neutrophils and B leukemic cells of patients with chronic B - cell lymphocytic leukemia. Neoplasma. 2011;58(1):45–50.CrossRefPubMed
37.
go back to reference Jang YS, Kim HA, Park SR, Lee MR, Park JB, Kim PH. IL-4 stimulates mouse macrophages to express APRIL through p38MAPK and two different downstream molecules, CREB and Stat6. Cytokine. 2009;47(1):43–7.CrossRefPubMed Jang YS, Kim HA, Park SR, Lee MR, Park JB, Kim PH. IL-4 stimulates mouse macrophages to express APRIL through p38MAPK and two different downstream molecules, CREB and Stat6. Cytokine. 2009;47(1):43–7.CrossRefPubMed
38.
go back to reference Jang YS, Kim JH, Seo GY, Kim PH. TGF-beta1 stimulates mouse macrophages to express APRIL through Smad and p38MAPK/CREB pathways. Mol Cells. 2011;32(3):251–5.CrossRefPubMedPubMedCentral Jang YS, Kim JH, Seo GY, Kim PH. TGF-beta1 stimulates mouse macrophages to express APRIL through Smad and p38MAPK/CREB pathways. Mol Cells. 2011;32(3):251–5.CrossRefPubMedPubMedCentral
39.
go back to reference Lee SM, Kim EJ, Suk K, Lee WH. BAFF and APRIL induce inflammatory activation of THP-1 cells through interaction with their conventional receptors and activation of MAPK and NF-kappaB. Inflamm Res. 2011;60(9):807–15.CrossRefPubMed Lee SM, Kim EJ, Suk K, Lee WH. BAFF and APRIL induce inflammatory activation of THP-1 cells through interaction with their conventional receptors and activation of MAPK and NF-kappaB. Inflamm Res. 2011;60(9):807–15.CrossRefPubMed
40.
go back to reference Wright JG, Christman JW. The role of nuclear factor kappa B in the pathogenesis of pulmonary diseases: implications for therapy. Am J Respir Med. 2003;2(3):211–9.CrossRefPubMed Wright JG, Christman JW. The role of nuclear factor kappa B in the pathogenesis of pulmonary diseases: implications for therapy. Am J Respir Med. 2003;2(3):211–9.CrossRefPubMed
41.
go back to reference Li D, Beisswenger C, Herr C, Hellberg J, Han G, Zakharkina T, et al. Myeloid cell RelA/p65 promotes lung cancer proliferation through Wnt/beta-catenin signaling in murine and human tumor cells. Oncogene. 2014;33(10):1239–48.CrossRefPubMed Li D, Beisswenger C, Herr C, Hellberg J, Han G, Zakharkina T, et al. Myeloid cell RelA/p65 promotes lung cancer proliferation through Wnt/beta-catenin signaling in murine and human tumor cells. Oncogene. 2014;33(10):1239–48.CrossRefPubMed
42.
go back to reference He B, Xu W, Santini PA, Polydorides AD, Chiu A, Estrella J, et al. Intestinal bacteria trigger T cell-independent immunoglobulin A(2) class switching by inducing epithelial-cell secretion of the cytokine APRIL. Immunity. 2007;26(6):812–26.CrossRefPubMed He B, Xu W, Santini PA, Polydorides AD, Chiu A, Estrella J, et al. Intestinal bacteria trigger T cell-independent immunoglobulin A(2) class switching by inducing epithelial-cell secretion of the cytokine APRIL. Immunity. 2007;26(6):812–26.CrossRefPubMed
43.
go back to reference Pilette C, Ouadrhiri Y, Godding V, Vaerman JP, Sibille Y. Lung mucosal immunity: immunoglobulin-A revisited. Eur Respir J. 2001;18(3):571–88.CrossRefPubMed Pilette C, Ouadrhiri Y, Godding V, Vaerman JP, Sibille Y. Lung mucosal immunity: immunoglobulin-A revisited. Eur Respir J. 2001;18(3):571–88.CrossRefPubMed
44.
go back to reference Kheradmand F, Mattewal AS, Corry DB. At last, an immune organ we can call our own? Am J Respir Crit Care Med. 2009;179(7):525–7.CrossRefPubMed Kheradmand F, Mattewal AS, Corry DB. At last, an immune organ we can call our own? Am J Respir Crit Care Med. 2009;179(7):525–7.CrossRefPubMed
45.
go back to reference Hellermann GR, Nagy SB, Kong X, Lockey RF, Mohapatra SS. Mechanism of cigarette smoke condensate-induced acute inflammatory response in human bronchial epithelial cells. Respir Res. 2002;3:22.CrossRefPubMedPubMedCentral Hellermann GR, Nagy SB, Kong X, Lockey RF, Mohapatra SS. Mechanism of cigarette smoke condensate-induced acute inflammatory response in human bronchial epithelial cells. Respir Res. 2002;3:22.CrossRefPubMedPubMedCentral
46.
go back to reference Floreani AA, Wyatt TA, Stoner J, Sanderson SD, Thompson EG, Allen-Gipson D, et al. Smoke and C5a induce airway epithelial intercellular adhesion molecule-1 and cell adhesion. Am J Respir Cell Mol Biol. 2003;29(4):472–82.CrossRefPubMed Floreani AA, Wyatt TA, Stoner J, Sanderson SD, Thompson EG, Allen-Gipson D, et al. Smoke and C5a induce airway epithelial intercellular adhesion molecule-1 and cell adhesion. Am J Respir Cell Mol Biol. 2003;29(4):472–82.CrossRefPubMed
47.
go back to reference Takizawa H, Tanaka M, Takami K, Ohtoshi T, Ito K, Satoh M, et al. Increased expression of transforming growth factor-beta1 in small airway epithelium from tobacco smokers and patients with chronic obstructive pulmonary disease (COPD). Am J Respir Crit Care Med. 2001;163(6):1476–83.CrossRefPubMed Takizawa H, Tanaka M, Takami K, Ohtoshi T, Ito K, Satoh M, et al. Increased expression of transforming growth factor-beta1 in small airway epithelium from tobacco smokers and patients with chronic obstructive pulmonary disease (COPD). Am J Respir Crit Care Med. 2001;163(6):1476–83.CrossRefPubMed
48.
go back to reference Bozinovski S, Vlahos R, Anthony D, McQualter J, Anderson G, Irving L, et al. COPD and squamous cell lung cancer: aberrant inflammation and immunity is the common link. Br J Pharmacol. 2015. doi: 10.1111/bph.13198. [Epub ahead of print]. Bozinovski S, Vlahos R, Anthony D, McQualter J, Anderson G, Irving L, et al. COPD and squamous cell lung cancer: aberrant inflammation and immunity is the common link. Br J Pharmacol. 2015. doi: 10.​1111/​bph.​13198. [Epub ahead of print].
49.
go back to reference Hogg JC, Macklem PT, Thurlbeck WM. Site and nature of airway obstruction in chronic obstructive lung disease. N Engl J Med. 1968;278(25):1355–60.CrossRefPubMed Hogg JC, Macklem PT, Thurlbeck WM. Site and nature of airway obstruction in chronic obstructive lung disease. N Engl J Med. 1968;278(25):1355–60.CrossRefPubMed
50.
go back to reference Maeno T, Houghton AM, Quintero PA, Grumelli S, Owen CA, Shapiro SD. CD8+ T Cells are required for inflammation and destruction in cigarette smoke-induced emphysema in mice. J Immunol. 2007;178(12):8090–6.CrossRefPubMed Maeno T, Houghton AM, Quintero PA, Grumelli S, Owen CA, Shapiro SD. CD8+ T Cells are required for inflammation and destruction in cigarette smoke-induced emphysema in mice. J Immunol. 2007;178(12):8090–6.CrossRefPubMed
51.
go back to reference Lanca T, Silva-Santos B. The split nature of tumor-infiltrating leukocytes: Implications for cancer surveillance and immunotherapy. Oncoimmunology. 2012;1(5):717–25.CrossRefPubMedPubMedCentral Lanca T, Silva-Santos B. The split nature of tumor-infiltrating leukocytes: Implications for cancer surveillance and immunotherapy. Oncoimmunology. 2012;1(5):717–25.CrossRefPubMedPubMedCentral
55.
go back to reference Stockmann C, Schadendorf D, Klose R, Helfrich I. The impact of the immune system on tumor: angiogenesis and vascular remodeling. Front Oncol. 2014;4:69.CrossRefPubMedPubMedCentral Stockmann C, Schadendorf D, Klose R, Helfrich I. The impact of the immune system on tumor: angiogenesis and vascular remodeling. Front Oncol. 2014;4:69.CrossRefPubMedPubMedCentral
Metadata
Title
Increased expression of A Proliferation-inducing Ligand (APRIL) in lung leukocytes and alveolar epithelial cells in COPD patients with non small cell lung cancer: a possible link between COPD and lung cancer?
Authors
Francesca Polverino
Maria Laucho-Contreras
Joselyn Rojas Quintero
Miguel Divo
Victor Pinto-Plata
Lynette Sholl
Juan P. de-Torres
Bartolome R. Celli
Caroline A. Owen
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Multidisciplinary Respiratory Medicine / Issue 1/2015
Electronic ISSN: 2049-6958
DOI
https://doi.org/10.1186/s40248-016-0051-6

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