Skip to main content
Top
Published in: Diagnostic Pathology 1/2014

Open Access 01-12-2014 | Research

A gene therapy induced emphysema model and the protective role of stem cells

Authors: Paul Zarogoulidis, Wolfgang Hohenforst-Schmidt, Haidong Huang, Despoina Sahpatzidou, Lutz Freitag, Leonidas Sakkas, Aggeliki Rapti, Ioannis Kioumis, Georgia Pitsiou, Kokkona Kouzi-Koliakos, Anna Papamichail, Antonis Papaiwannou, Theodora Tsiouda, Kosmas Tsakiridis, Konstantinos Porpodis, Sofia Lampaki, John Organtzis, Andreas Gschwendtner, Konstantinos Zarogoulidis

Published in: Diagnostic Pathology | Issue 1/2014

Login to get access

Abstract

Background

Chronic obstructive pulmonary disease presents with two different phenotypes: chronic bronchitis and emphysema with parenchymal destruction. Decreased expression of vascular endothelial growth factor and increased endothelial cell apoptosis are considered major factors for emphysema. Stem cells have the ability of vascular regeneration and function as a repair mechanism for the damaged endothelial cells. Currently, minimally invasive interventional procedures such as placement of valves, bio-foam or coils are performed in order to improve the disturbed mechanical function in emphysema patients. However, these procedures cannot restore functional lung tissue. Additionally stem cell instillation into the parenchyma has been used in clinical studies aiming to improve overall respiratory function and quality of life.

Methods

In our current experiment we induced emphysema with a DDMC non-viral vector in BALBC mice and simultaneously instilled stem cells testing the hyposthesis that they might have a protective role against the development of emphysema. The mice were divided into four groups: a) control, b) 50.000 cells, c) 75.000 and d) 100.000 cells.

Results

Lung pathological findings revealed that all treatment groups had less damage compared to the control group. Additionally, we observed that emphysema lesions were less around vessels in an area of 10μm.

Conclusions

Our findings indicate that stem cell instillation can have a regenerative role if applied upon a tissue scaffold with vessel around.

Virtual Slides

Appendix
Available only for authorised users
Literature
1.
go back to reference Postolache P, Cojocaru DC: Pulmonary rehabilitation-from guidelines to practice. Rev Med Chir Soc Med Nat Iasi. 2013, 117: 380-387.PubMed Postolache P, Cojocaru DC: Pulmonary rehabilitation-from guidelines to practice. Rev Med Chir Soc Med Nat Iasi. 2013, 117: 380-387.PubMed
2.
go back to reference Barua A, Vaughan P, Wotton R, Naidu B: Do endobronchial valves improve outcomes in patients with emphysema?. Interact Cardiovasc Thorac Surg. 2012, 15: 1072-1076. 10.1093/icvts/ivs371.PubMedPubMedCentralCrossRef Barua A, Vaughan P, Wotton R, Naidu B: Do endobronchial valves improve outcomes in patients with emphysema?. Interact Cardiovasc Thorac Surg. 2012, 15: 1072-1076. 10.1093/icvts/ivs371.PubMedPubMedCentralCrossRef
3.
go back to reference Herth FJ, Eberhard R, Gompelmann D, Slebos DJ, Ernst A: Bronchoscopic lung volume reduction with a dedicated coil: a clinical pilot study. Ther Adv Respir Dis. 2010, 4: 225-231. 10.1177/1753465810368553.PubMedCrossRef Herth FJ, Eberhard R, Gompelmann D, Slebos DJ, Ernst A: Bronchoscopic lung volume reduction with a dedicated coil: a clinical pilot study. Ther Adv Respir Dis. 2010, 4: 225-231. 10.1177/1753465810368553.PubMedCrossRef
4.
go back to reference Falkenstern-Ge RF, Ingerl H, Kohlhaufl M: Severe emphysema treated by endoscopic bronchial volume reduction with lung sealant (AeriSeal). Case Rep Pulmonol. 2013, 2013: 361391-PubMedPubMedCentral Falkenstern-Ge RF, Ingerl H, Kohlhaufl M: Severe emphysema treated by endoscopic bronchial volume reduction with lung sealant (AeriSeal). Case Rep Pulmonol. 2013, 2013: 361391-PubMedPubMedCentral
5.
go back to reference Elbehairy AF, Webb KA, Alberto Neder J, O'Donnell DE: Should mild COPD be treated? Evidence for early pharmacological intervention. Drugs. 2013, 73: 1991-2001. 10.1007/s40265-013-0145-9.PubMedCrossRef Elbehairy AF, Webb KA, Alberto Neder J, O'Donnell DE: Should mild COPD be treated? Evidence for early pharmacological intervention. Drugs. 2013, 73: 1991-2001. 10.1007/s40265-013-0145-9.PubMedCrossRef
6.
go back to reference Chrystyn H, Small M, Milligan G, Higgins V, Gil EG, Estruch J: Impact of patients' satisfaction with their inhalers on treatment compliance and health status in COPD. Respir Med. 2014, 108 (2): 358-365. 10.1016/j.rmed.2013.09.021. doi:10.1016/j.rmed.2013.09.021. Epub 2013 Oct 2.PubMedCrossRef Chrystyn H, Small M, Milligan G, Higgins V, Gil EG, Estruch J: Impact of patients' satisfaction with their inhalers on treatment compliance and health status in COPD. Respir Med. 2014, 108 (2): 358-365. 10.1016/j.rmed.2013.09.021. doi:10.1016/j.rmed.2013.09.021. Epub 2013 Oct 2.PubMedCrossRef
7.
go back to reference Siafakas NM, Antoniou KM, Tzortzaki EG: Role of angiogenesis and vascular remodeling in chronic obstructive pulmonary disease. Int J Chron Obstruct Pulmon Dis. 2007, 2: 453-462.PubMedPubMedCentral Siafakas NM, Antoniou KM, Tzortzaki EG: Role of angiogenesis and vascular remodeling in chronic obstructive pulmonary disease. Int J Chron Obstruct Pulmon Dis. 2007, 2: 453-462.PubMedPubMedCentral
8.
go back to reference Shapiro SD: Proteinases in chronic obstructive pulmonary disease. Biochem Soc Trans. 2002, 30: 98-102. 10.1042/BST0300098.PubMedCrossRef Shapiro SD: Proteinases in chronic obstructive pulmonary disease. Biochem Soc Trans. 2002, 30: 98-102. 10.1042/BST0300098.PubMedCrossRef
9.
go back to reference MacNee W: Pulmonary and systemic oxidant/antioxidant imbalance in chronic obstructive pulmonary disease. Proc Am Thorac Soc. 2005, 2: 50-60. 10.1513/pats.200411-056SF.PubMedCrossRef MacNee W: Pulmonary and systemic oxidant/antioxidant imbalance in chronic obstructive pulmonary disease. Proc Am Thorac Soc. 2005, 2: 50-60. 10.1513/pats.200411-056SF.PubMedCrossRef
10.
go back to reference Curtis JL, Freeman CM, Hogg JC: The immunopathogenesis of chronic obstructive pulmonary disease: insights from recent research. Proc Am Thorac Soc. 2007, 4: 512-521. 10.1513/pats.200701-002FM.PubMedPubMedCentralCrossRef Curtis JL, Freeman CM, Hogg JC: The immunopathogenesis of chronic obstructive pulmonary disease: insights from recent research. Proc Am Thorac Soc. 2007, 4: 512-521. 10.1513/pats.200701-002FM.PubMedPubMedCentralCrossRef
11.
go back to reference Willemse BW, ten Hacken NH, Rutgers B, Lesman-Leegte IG, Postma DS, Timens W: Effect of 1-year smoking cessation on airway inflammation in COPD and asymptomatic smokers. Eur Respir J. 2005, 26: 835-845. 10.1183/09031936.05.00108904.PubMedCrossRef Willemse BW, ten Hacken NH, Rutgers B, Lesman-Leegte IG, Postma DS, Timens W: Effect of 1-year smoking cessation on airway inflammation in COPD and asymptomatic smokers. Eur Respir J. 2005, 26: 835-845. 10.1183/09031936.05.00108904.PubMedCrossRef
12.
go back to reference Kotton DN, Summer R, Fine A: Lung stem cells: new paradigms. Exp Hematol. 2004, 32: 340-343. 10.1016/j.exphem.2004.01.009.PubMedCrossRef Kotton DN, Summer R, Fine A: Lung stem cells: new paradigms. Exp Hematol. 2004, 32: 340-343. 10.1016/j.exphem.2004.01.009.PubMedCrossRef
13.
go back to reference Lajtha LG: Stem cell concepts. Differentiation. 1979, 14: 23-34. 10.1111/j.1432-0436.1979.tb01007.x.PubMedCrossRef Lajtha LG: Stem cell concepts. Differentiation. 1979, 14: 23-34. 10.1111/j.1432-0436.1979.tb01007.x.PubMedCrossRef
14.
15.
go back to reference Mitalipov S, Wolf D: Totipotency, pluripotency and nuclear reprogramming. Adv Biochem Eng Biotechnol. 2009, 114: 185-199.PubMedPubMedCentral Mitalipov S, Wolf D: Totipotency, pluripotency and nuclear reprogramming. Adv Biochem Eng Biotechnol. 2009, 114: 185-199.PubMedPubMedCentral
16.
go back to reference Fortier LA: Stem cells: classifications, controversies, and clinical applications. Vet Surg. 2005, 34: 415-423. 10.1111/j.1532-950X.2005.00063.x.PubMedCrossRef Fortier LA: Stem cells: classifications, controversies, and clinical applications. Vet Surg. 2005, 34: 415-423. 10.1111/j.1532-950X.2005.00063.x.PubMedCrossRef
17.
go back to reference Mavroudi M, Zarogoulidis P, Porpodis K, Kioumis I, Lampaki S, Yarmus L, Malecki R, Zarogoulidis K, Malecki M: Stem cells' guided gene therapy of cancer: new frontier in personalized and targeted therapy. J Cancer Res Ther (Manch). 2014, 2: 22-33. 10.14312/2052-4994.2014-4.CrossRef Mavroudi M, Zarogoulidis P, Porpodis K, Kioumis I, Lampaki S, Yarmus L, Malecki R, Zarogoulidis K, Malecki M: Stem cells' guided gene therapy of cancer: new frontier in personalized and targeted therapy. J Cancer Res Ther (Manch). 2014, 2: 22-33. 10.14312/2052-4994.2014-4.CrossRef
18.
go back to reference Keller G: Embryonic stem cell differentiation: emergence of a new era in biology and medicine. Genes Dev. 2005, 19: 1129-1155. 10.1101/gad.1303605.PubMedCrossRef Keller G: Embryonic stem cell differentiation: emergence of a new era in biology and medicine. Genes Dev. 2005, 19: 1129-1155. 10.1101/gad.1303605.PubMedCrossRef
19.
go back to reference Tuch BE: Stem cells'a clinical update. Aust Fam Physician. 2006, 35: 719-721.PubMed Tuch BE: Stem cells'a clinical update. Aust Fam Physician. 2006, 35: 719-721.PubMed
20.
go back to reference Baksh D, Song L, Tuan RS: Adult mesenchymal stem cells: characterization, differentiation, and application in cell and gene therapy. J Cell Mol Med. 2004, 8: 301-316. 10.1111/j.1582-4934.2004.tb00320.x.PubMedCrossRef Baksh D, Song L, Tuan RS: Adult mesenchymal stem cells: characterization, differentiation, and application in cell and gene therapy. J Cell Mol Med. 2004, 8: 301-316. 10.1111/j.1582-4934.2004.tb00320.x.PubMedCrossRef
22.
go back to reference Patel DM, Shah J, Srivastava AS: Therapeutic potential of mesenchymal stem cells in regenerative medicine. Stem Cells Int. 2013, 2013: 496218-10.1155/2013/496218.PubMedPubMedCentralCrossRef Patel DM, Shah J, Srivastava AS: Therapeutic potential of mesenchymal stem cells in regenerative medicine. Stem Cells Int. 2013, 2013: 496218-10.1155/2013/496218.PubMedPubMedCentralCrossRef
24.
go back to reference Cipriani P, Carubbi F, Liakouli V, Marrelli A, Perricone C, Perricone R, Alesse E, Giacomelli R: Stem cells in autoimmune diseases: implications for pathogenesis and future trends in therapy. Autoimmun Rev. 2012, 12: 709-716. 10.1016/j.autrev.2012.10.004.PubMedCrossRef Cipriani P, Carubbi F, Liakouli V, Marrelli A, Perricone C, Perricone R, Alesse E, Giacomelli R: Stem cells in autoimmune diseases: implications for pathogenesis and future trends in therapy. Autoimmun Rev. 2012, 12: 709-716. 10.1016/j.autrev.2012.10.004.PubMedCrossRef
25.
go back to reference Cipriani P, Di Benedetto P, Liakouli V, Del Papa B, Di Padova M, Di Ianni M, Marrelli A, Alesse E, Giacomelli R: Mesenchymal stem cells (MSCs) from scleroderma patients (SSc) preserve their immunomodulatory properties although senescent and normally induce T regulatory cells (Tregs) with a functional phenotype: implications for cellular-based therapy. Clin Exp Immunol. 2013, 173: 195-206. 10.1111/cei.12111.PubMedPubMedCentralCrossRef Cipriani P, Di Benedetto P, Liakouli V, Del Papa B, Di Padova M, Di Ianni M, Marrelli A, Alesse E, Giacomelli R: Mesenchymal stem cells (MSCs) from scleroderma patients (SSc) preserve their immunomodulatory properties although senescent and normally induce T regulatory cells (Tregs) with a functional phenotype: implications for cellular-based therapy. Clin Exp Immunol. 2013, 173: 195-206. 10.1111/cei.12111.PubMedPubMedCentralCrossRef
26.
go back to reference Cipriani P, Marrelli A, Benedetto PD, Liakouli V, Carubbi F, Ruscitti P, Alvaro S, Pantano I, Campese AF, Grazioli P, Screpanti I, Giacomelli R: Scleroderma Mesenchymal Stem Cells display a different phenotype from healthy controls; implications for regenerative medicine. Angiogenesis. 2013, 16: 595-607. 10.1007/s10456-013-9338-9.PubMedCrossRef Cipriani P, Marrelli A, Benedetto PD, Liakouli V, Carubbi F, Ruscitti P, Alvaro S, Pantano I, Campese AF, Grazioli P, Screpanti I, Giacomelli R: Scleroderma Mesenchymal Stem Cells display a different phenotype from healthy controls; implications for regenerative medicine. Angiogenesis. 2013, 16: 595-607. 10.1007/s10456-013-9338-9.PubMedCrossRef
27.
go back to reference Guan XJ, Song L, Han FF, Cui ZL, Chen X, Guo XJ, Xu WG: Mesenchymal stem cells protect cigarette smoke-damaged lung and pulmonary function partly via VEGF-VEGF receptors. J Cell Biochem. 2013, 114: 323-335. 10.1002/jcb.24377.PubMedCrossRef Guan XJ, Song L, Han FF, Cui ZL, Chen X, Guo XJ, Xu WG: Mesenchymal stem cells protect cigarette smoke-damaged lung and pulmonary function partly via VEGF-VEGF receptors. J Cell Biochem. 2013, 114: 323-335. 10.1002/jcb.24377.PubMedCrossRef
28.
go back to reference Ribeiro-Paes JT, Bilaqui A, Greco OT, Ruiz MA, Marcelino MY, Stessuk T, de Faria CA, Lago MR: Unicentric study of cell therapy in chronic obstructive pulmonary disease/pulmonary emphysema. Int J Chron Obstruct Pulmon Dis. 2011, 6: 63-71. 10.2147/COPD.S15292.PubMedPubMedCentralCrossRef Ribeiro-Paes JT, Bilaqui A, Greco OT, Ruiz MA, Marcelino MY, Stessuk T, de Faria CA, Lago MR: Unicentric study of cell therapy in chronic obstructive pulmonary disease/pulmonary emphysema. Int J Chron Obstruct Pulmon Dis. 2011, 6: 63-71. 10.2147/COPD.S15292.PubMedPubMedCentralCrossRef
29.
go back to reference Weiss DJ, Casaburi R, Flannery R, LeRoux-Williams M, Tashkin DP: A placebo-controlled, randomized trial of mesenchymal stem cells in COPD. Chest. 2013, 143: 1590-1598. 10.1378/chest.12-2094.PubMedCrossRef Weiss DJ, Casaburi R, Flannery R, LeRoux-Williams M, Tashkin DP: A placebo-controlled, randomized trial of mesenchymal stem cells in COPD. Chest. 2013, 143: 1590-1598. 10.1378/chest.12-2094.PubMedCrossRef
30.
go back to reference Kim JK, Vinarsky V, Wain J, Zhao R, Jung K, Choi J, Lam A, Pardo-Saganta A, Breton S, Rajagopal J, Yun SH: In vivo imaging of tracheal epithelial cells in mice during airway regeneration. Am J Respir Cell Mol Biol. 2012, 47: 864-868. 10.1165/rcmb.2012-0164OC.PubMedPubMedCentralCrossRef Kim JK, Vinarsky V, Wain J, Zhao R, Jung K, Choi J, Lam A, Pardo-Saganta A, Breton S, Rajagopal J, Yun SH: In vivo imaging of tracheal epithelial cells in mice during airway regeneration. Am J Respir Cell Mol Biol. 2012, 47: 864-868. 10.1165/rcmb.2012-0164OC.PubMedPubMedCentralCrossRef
31.
go back to reference Hackett TL, Knight DA, Sin DD: Potential role of stem cells in management of COPD. Int J Chron Obstruct Pulmon Dis. 2010, 5: 81-88.PubMedPubMedCentral Hackett TL, Knight DA, Sin DD: Potential role of stem cells in management of COPD. Int J Chron Obstruct Pulmon Dis. 2010, 5: 81-88.PubMedPubMedCentral
32.
go back to reference Zarogoulidis P, Kontakiotis T, Zarogoulidis K: Inhaled gene therapy in lung cancer: "as for the future, our task is not to foresee it, but to enable it". Ther Deliv. 2012, 3: 919-921. 10.4155/tde.12.71.PubMedCrossRef Zarogoulidis P, Kontakiotis T, Zarogoulidis K: Inhaled gene therapy in lung cancer: "as for the future, our task is not to foresee it, but to enable it". Ther Deliv. 2012, 3: 919-921. 10.4155/tde.12.71.PubMedCrossRef
33.
go back to reference Zarogoulidis P, Darwiche K, Sakkas A, Yarmus L, Huang H, Li Q, Freitag L, Zarogoulidis K, Malecki M: Suicide gene therapy for cancer - current strategies. J Cancer Res. 2014, 2 (1): 22-33. Zarogoulidis P, Darwiche K, Sakkas A, Yarmus L, Huang H, Li Q, Freitag L, Zarogoulidis K, Malecki M: Suicide gene therapy for cancer - current strategies. J Cancer Res. 2014, 2 (1): 22-33.
34.
go back to reference Zarogoulidis P, Darwiche K, Hohenforst-Schmidt W, Huang H, Li Q, Freitag L, Zarogoulidis K: Inhaled gene therapy in lung cancer: proof-of-concept for nano-oncology and nanobiotechnology in the management of lung cancer. Future Oncol. 2013, 9: 1171-1194. 10.2217/fon.13.67.PubMedCrossRef Zarogoulidis P, Darwiche K, Hohenforst-Schmidt W, Huang H, Li Q, Freitag L, Zarogoulidis K: Inhaled gene therapy in lung cancer: proof-of-concept for nano-oncology and nanobiotechnology in the management of lung cancer. Future Oncol. 2013, 9: 1171-1194. 10.2217/fon.13.67.PubMedCrossRef
35.
go back to reference Zarogoulidis P, Hohenforst-Schmidt W, Darwiche K, Krauss L, Sparopoulou D, Sakkas L, Gschwendtner A, Huang H, Turner FJ, Freitag L, Zarogoulidis K: 2-diethylaminoethyl-dextran methyl methacrylate copolymer nonviral vector: still a long way toward the safety of aerosol gene therapy. Gene Ther. 2013, 20: 1022-1028. 10.1038/gt.2013.27.PubMedCrossRef Zarogoulidis P, Hohenforst-Schmidt W, Darwiche K, Krauss L, Sparopoulou D, Sakkas L, Gschwendtner A, Huang H, Turner FJ, Freitag L, Zarogoulidis K: 2-diethylaminoethyl-dextran methyl methacrylate copolymer nonviral vector: still a long way toward the safety of aerosol gene therapy. Gene Ther. 2013, 20: 1022-1028. 10.1038/gt.2013.27.PubMedCrossRef
36.
go back to reference Goldkorn T, Filosto S, Chung S: Lung Injury and Lung Cancer Caused by Cigarette Smoke-Induced Oxidative Stress: Molecular Mechanisms and Therapeutic Opportunities Involving the Ceramide Generating Machinery and Egf Receptor.Antioxid Redox Signal 2014, Epub ahead of print., Goldkorn T, Filosto S, Chung S: Lung Injury and Lung Cancer Caused by Cigarette Smoke-Induced Oxidative Stress: Molecular Mechanisms and Therapeutic Opportunities Involving the Ceramide Generating Machinery and Egf Receptor.Antioxid Redox Signal 2014, Epub ahead of print.,
37.
go back to reference Angelis N, Porpodis K, Zarogoulidis P, Spyratos D, Kioumis I, Papaiwannou A, Pitsiou G, Tsakiridis K, Mpakas A, Arikas S, Tsiouda T, Katsikogiannis N, Kougioumtzi I, Machairiotis N, Argyriou M, Kessisis G, Zarogoulidis K: Airway inflammation in chronic obstructive pulmonary disease. J Thorac Dis. 2014, 6: S167-S172.PubMedPubMedCentral Angelis N, Porpodis K, Zarogoulidis P, Spyratos D, Kioumis I, Papaiwannou A, Pitsiou G, Tsakiridis K, Mpakas A, Arikas S, Tsiouda T, Katsikogiannis N, Kougioumtzi I, Machairiotis N, Argyriou M, Kessisis G, Zarogoulidis K: Airway inflammation in chronic obstructive pulmonary disease. J Thorac Dis. 2014, 6: S167-S172.PubMedPubMedCentral
38.
go back to reference Milara J, Lluch J, Almudever P, Freire J, Xiaozhong Q, Cortijo J: Roflumilast N-oxide reverses corticosteroid resistance in neutrophils from patients with chronic obstructive pulmonary disease. J Allergy Clin Immunol. 2014, 134 (2): 314-322. 10.1016/j.jaci.2014.02.001.PubMedCrossRef Milara J, Lluch J, Almudever P, Freire J, Xiaozhong Q, Cortijo J: Roflumilast N-oxide reverses corticosteroid resistance in neutrophils from patients with chronic obstructive pulmonary disease. J Allergy Clin Immunol. 2014, 134 (2): 314-322. 10.1016/j.jaci.2014.02.001.PubMedCrossRef
39.
go back to reference Ulrik CS: Clinical benefit of fixed-dose dual bronchodilation with glycopyrronium and indacaterol once daily in patients with chronic obstructive pulmonary disease: a systematic review. Int J Chron Obstruct Pulmon Dis. 2014, 9: 331-338. 10.2147/COPD.S60362.PubMedPubMedCentralCrossRef Ulrik CS: Clinical benefit of fixed-dose dual bronchodilation with glycopyrronium and indacaterol once daily in patients with chronic obstructive pulmonary disease: a systematic review. Int J Chron Obstruct Pulmon Dis. 2014, 9: 331-338. 10.2147/COPD.S60362.PubMedPubMedCentralCrossRef
40.
go back to reference Kew KM, Dias S, Cates CJ: Long-acting inhaled therapy (beta-agonists, anticholinergics and steroids) for COPD: a network meta-analysis. Cochrane Database Syst Rev. 2014, 3: CD010844-PubMed Kew KM, Dias S, Cates CJ: Long-acting inhaled therapy (beta-agonists, anticholinergics and steroids) for COPD: a network meta-analysis. Cochrane Database Syst Rev. 2014, 3: CD010844-PubMed
41.
go back to reference Zarogoulidis P, Papanas N, Kioumis I, Chatzaki E, Maltezos E, Zarogoulidis K: Macrolides: from in vitro anti-inflammatory and immunomodulatory properties to clinical practice in respiratory diseases. Eur J Clin Pharmacol. 2012, 68: 479-503. 10.1007/s00228-011-1161-x.PubMedCrossRef Zarogoulidis P, Papanas N, Kioumis I, Chatzaki E, Maltezos E, Zarogoulidis K: Macrolides: from in vitro anti-inflammatory and immunomodulatory properties to clinical practice in respiratory diseases. Eur J Clin Pharmacol. 2012, 68: 479-503. 10.1007/s00228-011-1161-x.PubMedCrossRef
42.
go back to reference Caramori G, Rigolin GM, Mazzoni F, Leprotti S, Campioni P, Papi A: Circulating endothelial stem cells are not decreased in pulmonary emphysema or COPD. Thorax. 2010, 65: 554-555. 10.1136/thx.2009.121640.PubMedCrossRef Caramori G, Rigolin GM, Mazzoni F, Leprotti S, Campioni P, Papi A: Circulating endothelial stem cells are not decreased in pulmonary emphysema or COPD. Thorax. 2010, 65: 554-555. 10.1136/thx.2009.121640.PubMedCrossRef
43.
go back to reference Sala E, Villena C, Balaguer C, Rios A, Fernandez-Palomeque C, Cosio BG, Garcia J, Noguera A, Agusti A: Abnormal levels of circulating endothelial progenitor cells during exacerbations of COPD. Lung. 2010, 188: 331-338. 10.1007/s00408-009-9225-8.PubMedCrossRef Sala E, Villena C, Balaguer C, Rios A, Fernandez-Palomeque C, Cosio BG, Garcia J, Noguera A, Agusti A: Abnormal levels of circulating endothelial progenitor cells during exacerbations of COPD. Lung. 2010, 188: 331-338. 10.1007/s00408-009-9225-8.PubMedCrossRef
44.
go back to reference Cha HJ, Hwang ES: Current status of biology, bioengineering, and therapeutic potential of stem cells. Arch Pharm Res. 2012, 35: 193-196. 10.1007/s12272-012-0200-1.PubMedCrossRef Cha HJ, Hwang ES: Current status of biology, bioengineering, and therapeutic potential of stem cells. Arch Pharm Res. 2012, 35: 193-196. 10.1007/s12272-012-0200-1.PubMedCrossRef
45.
go back to reference Roomans GM: Tissue engineering and the use of stem/progenitor cells for airway epithelium repair. Eur Cell Mater. 2010, 19: 284-299.PubMed Roomans GM: Tissue engineering and the use of stem/progenitor cells for airway epithelium repair. Eur Cell Mater. 2010, 19: 284-299.PubMed
46.
go back to reference Huh JW, Kim SY, Lee JH, Lee JS, Van Ta Q, Kim M, Oh YM, Lee YS, Lee SD: Bone marrow cells repair cigarette smoke-induced emphysema in rats. Am J Physiol Lung Cell Mol Physiol. 2011, 301: L255-L266. 10.1152/ajplung.00253.2010.PubMedCrossRef Huh JW, Kim SY, Lee JH, Lee JS, Van Ta Q, Kim M, Oh YM, Lee YS, Lee SD: Bone marrow cells repair cigarette smoke-induced emphysema in rats. Am J Physiol Lung Cell Mol Physiol. 2011, 301: L255-L266. 10.1152/ajplung.00253.2010.PubMedCrossRef
47.
go back to reference de Faria CA, de las Heras Kozma R, Stessuk T, Ribeiro-Paes JT: Experimental basis and new insights for cell therapy in Chronic Obstructive Pulmonary Disease. Stem Cell Rev. 2012, 8: 1236-1244. 10.1007/s12015-012-9410-7.PubMedCrossRef de Faria CA, de las Heras Kozma R, Stessuk T, Ribeiro-Paes JT: Experimental basis and new insights for cell therapy in Chronic Obstructive Pulmonary Disease. Stem Cell Rev. 2012, 8: 1236-1244. 10.1007/s12015-012-9410-7.PubMedCrossRef
48.
go back to reference Kim CF: Paving the road for lung stem cell biology: bronchioalveolar stem cells and other putative distal lung stem cells. Am J Physiol Lung Cell Mol Physiol. 2007, 293: L1092-L1098. 10.1152/ajplung.00015.2007.PubMedCrossRef Kim CF: Paving the road for lung stem cell biology: bronchioalveolar stem cells and other putative distal lung stem cells. Am J Physiol Lung Cell Mol Physiol. 2007, 293: L1092-L1098. 10.1152/ajplung.00015.2007.PubMedCrossRef
49.
go back to reference Rock JR, Randell SH, Hogan BL: Airway basal stem cells: a perspective on their roles in epithelial homeostasis and remodeling. Dis Model Mech. 2010, 3: 545-556. 10.1242/dmm.006031.PubMedPubMedCentralCrossRef Rock JR, Randell SH, Hogan BL: Airway basal stem cells: a perspective on their roles in epithelial homeostasis and remodeling. Dis Model Mech. 2010, 3: 545-556. 10.1242/dmm.006031.PubMedPubMedCentralCrossRef
50.
go back to reference Martinez-Llorens J, Casadevall C, Lloreta J, Orozco-Levi M, Barreiro E, Broquetas J, Gea J: [Activation of satellite cells in the intercostal muscles of patients with chronic obstructive pulmonary disease]. Arch Bronconeumol. 2008, 44: 239-244. 10.1157/13119938.PubMedCrossRef Martinez-Llorens J, Casadevall C, Lloreta J, Orozco-Levi M, Barreiro E, Broquetas J, Gea J: [Activation of satellite cells in the intercostal muscles of patients with chronic obstructive pulmonary disease]. Arch Bronconeumol. 2008, 44: 239-244. 10.1157/13119938.PubMedCrossRef
51.
go back to reference Foronjy RF, Majka SM: The potential for resident lung mesenchymal stem cells to promote functional tissue regeneration: understanding microenvironmental cues. Cells. 2012, 1: 874-10.3390/cells1040874.PubMedPubMedCentralCrossRef Foronjy RF, Majka SM: The potential for resident lung mesenchymal stem cells to promote functional tissue regeneration: understanding microenvironmental cues. Cells. 2012, 1: 874-10.3390/cells1040874.PubMedPubMedCentralCrossRef
52.
go back to reference Kobayashi S, Fujinawa R, Ota F, Angata T, Ueno M, Maeno T, Kitazume S, Yoshida K, Ishii T, Gao C, Ohtsubo K, Yamaguchi Y, Betsuyaku T, Kida K, Taniguchi N: A single dose of lipopolysaccharide into mice with emphysema mimics human chronic obstructive pulmonary disease exacerbation as assessed by micro-computed tomography. Am J Respir Cell Mol Biol. 2013, 49: 971-977. 10.1165/rcmb.2013-0074OC.PubMedCrossRef Kobayashi S, Fujinawa R, Ota F, Angata T, Ueno M, Maeno T, Kitazume S, Yoshida K, Ishii T, Gao C, Ohtsubo K, Yamaguchi Y, Betsuyaku T, Kida K, Taniguchi N: A single dose of lipopolysaccharide into mice with emphysema mimics human chronic obstructive pulmonary disease exacerbation as assessed by micro-computed tomography. Am J Respir Cell Mol Biol. 2013, 49: 971-977. 10.1165/rcmb.2013-0074OC.PubMedCrossRef
53.
go back to reference Karathanasis V, Petrakis S, Topouridou K, Koliakou E, Koliakos G, Demiri E: Intradermal injection of GFP-producing adipose stromal cells promotes survival of random-pattern skin flaps in rats. Eur J Plast Surg. 2013, 36: 281-288. 10.1007/s00238-013-0810-y.CrossRef Karathanasis V, Petrakis S, Topouridou K, Koliakou E, Koliakos G, Demiri E: Intradermal injection of GFP-producing adipose stromal cells promotes survival of random-pattern skin flaps in rats. Eur J Plast Surg. 2013, 36: 281-288. 10.1007/s00238-013-0810-y.CrossRef
Metadata
Title
A gene therapy induced emphysema model and the protective role of stem cells
Authors
Paul Zarogoulidis
Wolfgang Hohenforst-Schmidt
Haidong Huang
Despoina Sahpatzidou
Lutz Freitag
Leonidas Sakkas
Aggeliki Rapti
Ioannis Kioumis
Georgia Pitsiou
Kokkona Kouzi-Koliakos
Anna Papamichail
Antonis Papaiwannou
Theodora Tsiouda
Kosmas Tsakiridis
Konstantinos Porpodis
Sofia Lampaki
John Organtzis
Andreas Gschwendtner
Konstantinos Zarogoulidis
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Diagnostic Pathology / Issue 1/2014
Electronic ISSN: 1746-1596
DOI
https://doi.org/10.1186/s13000-014-0195-7

Other articles of this Issue 1/2014

Diagnostic Pathology 1/2014 Go to the issue