Skip to main content
Top
Published in: BMC Pulmonary Medicine 1/2013

Open Access 01-12-2013 | Research article

Altered microRNA expression profile during epithelial wound repair in bronchial epithelial cells

Authors: Aleksandra Szczepankiewicz, Peter M Lackie, John W Holloway

Published in: BMC Pulmonary Medicine | Issue 1/2013

Login to get access

Abstract

Background

Airway epithelial cells provide a protective barrier against environmental particles including potential pathogens. Epithelial repair in response to tissue damage is abnormal in asthmatic airway epithelium in comparison to the repair of normal epithelium after damage. The complex mechanisms coordinating the regulation of the processes involved in wound repair requires the phased expression of networks of genes. Small non-coding RNA molecules termed microRNAs (miRNAs) play a critical role in such coordinated regulation of gene expression. We aimed to establish if the phased expression of specific miRNAs is correlated with the repair of mechanically induced damage to the epithelium.

Methods

To investigate the possible involvement of miRNA in epithelial repair, we analyzed miRNA expression profiles during epithelial repair in a cell culture model using TaqMan-based quantitative real-time PCR in a TaqMan Low Density Array format. The expression of 754 miRNA genes at seven time points in a 48-hour period during the wound repair process was profiled using the bronchial epithelial cell line 16HBE14o- growing in monolayer.

Results

The expression levels of numerous miRNAs were found to be altered during the wound repair process. These miRNA genes were clustered into 3 different patterns of expression that correlate with the further regulation of several biological pathways involved in wound repair. Moreover, it was observed that expression of some miRNA genes were significantly altered only at one time point, indicating their involvement in a specific stage of the epithelial wound repair.

Conclusions

In summary, miRNA expression is modulated during the normal repair processes in airway epithelium in vitro suggesting a potential role in regulation of wound repair.
Appendix
Available only for authorised users
Literature
1.
go back to reference Hammad H, Lambrecht BN: Dendritic cells and epithelial cells: linking innate and adaptive immunity in asthma. Nat Rev Immunol. 2008, 8: 193-204. 10.1038/nri2275.CrossRefPubMed Hammad H, Lambrecht BN: Dendritic cells and epithelial cells: linking innate and adaptive immunity in asthma. Nat Rev Immunol. 2008, 8: 193-204. 10.1038/nri2275.CrossRefPubMed
2.
go back to reference Holgate ST: Epithelium dysfunction in asthma. J Allergy Clin Immunol. 2007, 120: 1233-1244. 10.1016/j.jaci.2007.10.025. quiz 1245–1236CrossRefPubMed Holgate ST: Epithelium dysfunction in asthma. J Allergy Clin Immunol. 2007, 120: 1233-1244. 10.1016/j.jaci.2007.10.025. quiz 1245–1236CrossRefPubMed
3.
go back to reference Holgate ST: The epithelium takes centre stage in asthma and atopic dermatitis. Trends Immunol. 2007, 28: 248-251. 10.1016/j.it.2007.04.007.CrossRefPubMed Holgate ST: The epithelium takes centre stage in asthma and atopic dermatitis. Trends Immunol. 2007, 28: 248-251. 10.1016/j.it.2007.04.007.CrossRefPubMed
4.
go back to reference Kato A, Schleimer RP: Beyond inflammation: airway epithelial cells are at the interface of innate and adaptive immunity. Curr Opin Immunol. 2007, 19: 711-720. 10.1016/j.coi.2007.08.004.CrossRefPubMedPubMedCentral Kato A, Schleimer RP: Beyond inflammation: airway epithelial cells are at the interface of innate and adaptive immunity. Curr Opin Immunol. 2007, 19: 711-720. 10.1016/j.coi.2007.08.004.CrossRefPubMedPubMedCentral
5.
go back to reference Sha Q, Truong-Tran AQ, Plitt JR, Beck LA, Schleimer RP: Activation of airway epithelial cells by toll-like receptor agonists. Am J Respir Cell Mol Biol. 2004, 31: 358-364. 10.1165/rcmb.2003-0388OC.CrossRefPubMed Sha Q, Truong-Tran AQ, Plitt JR, Beck LA, Schleimer RP: Activation of airway epithelial cells by toll-like receptor agonists. Am J Respir Cell Mol Biol. 2004, 31: 358-364. 10.1165/rcmb.2003-0388OC.CrossRefPubMed
6.
go back to reference Erjefalt JS, Erjefalt I, Sundler F, Persson CG: In vivo restitution of airway epithelium. Cell Tissue Res. 1995, 281: 305-316. 10.1007/BF00583399.CrossRefPubMed Erjefalt JS, Erjefalt I, Sundler F, Persson CG: In vivo restitution of airway epithelium. Cell Tissue Res. 1995, 281: 305-316. 10.1007/BF00583399.CrossRefPubMed
7.
go back to reference Heguy A, Harvey BG, Leopold PL, Dolgalev I, Raman T, Crystal RG: Responses of the human airway epithelium transcriptome to in vivo injury. Physiol Genomics. 2007, 29: 139-148.CrossRefPubMed Heguy A, Harvey BG, Leopold PL, Dolgalev I, Raman T, Crystal RG: Responses of the human airway epithelium transcriptome to in vivo injury. Physiol Genomics. 2007, 29: 139-148.CrossRefPubMed
8.
go back to reference He L, Hannon GJ: MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet. 2004, 5: 522-531. 10.1038/nrg1379.CrossRefPubMed He L, Hannon GJ: MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet. 2004, 5: 522-531. 10.1038/nrg1379.CrossRefPubMed
9.
go back to reference Eder M, Scherr M: MicroRNA and lung cancer. N Engl J Med. 2005, 352: 2446-2448. 10.1056/NEJMcibr051201.CrossRefPubMed Eder M, Scherr M: MicroRNA and lung cancer. N Engl J Med. 2005, 352: 2446-2448. 10.1056/NEJMcibr051201.CrossRefPubMed
10.
go back to reference Hurteau GJ, Carlson JA, Spivack SD, Brock GJ: Overexpression of the microRNA hsa-miR-200c leads to reduced expression of transcription factor 8 and increased expression of E-cadherin. Cancer Res. 2007, 67: 7972-7976. 10.1158/0008-5472.CAN-07-1058.CrossRefPubMed Hurteau GJ, Carlson JA, Spivack SD, Brock GJ: Overexpression of the microRNA hsa-miR-200c leads to reduced expression of transcription factor 8 and increased expression of E-cadherin. Cancer Res. 2007, 67: 7972-7976. 10.1158/0008-5472.CAN-07-1058.CrossRefPubMed
11.
go back to reference Jay C, Nemunaitis J, Chen P, Fulgham P, Tong AW: miRNA profiling for diagnosis and prognosis of human cancer. DNA Cell Biol. 2007, 26: 293-300. 10.1089/dna.2006.0554.CrossRefPubMed Jay C, Nemunaitis J, Chen P, Fulgham P, Tong AW: miRNA profiling for diagnosis and prognosis of human cancer. DNA Cell Biol. 2007, 26: 293-300. 10.1089/dna.2006.0554.CrossRefPubMed
12.
go back to reference Miller RL, Ho SM: Environmental epigenetics and asthma: current concepts and call for studies. Am J Respir Crit Care Med. 2008, 177: 567-573. 10.1164/rccm.200710-1511PP.CrossRefPubMedPubMedCentral Miller RL, Ho SM: Environmental epigenetics and asthma: current concepts and call for studies. Am J Respir Crit Care Med. 2008, 177: 567-573. 10.1164/rccm.200710-1511PP.CrossRefPubMedPubMedCentral
13.
go back to reference Nana-Sinkam SP, Karsies T, Riscili B, Ezzie M, Piper M: Lung microRNA: from development to disease. Expert Rev Respir Med. 2009, 3: 373-385. 10.1586/ers.09.30.CrossRefPubMed Nana-Sinkam SP, Karsies T, Riscili B, Ezzie M, Piper M: Lung microRNA: from development to disease. Expert Rev Respir Med. 2009, 3: 373-385. 10.1586/ers.09.30.CrossRefPubMed
14.
go back to reference Takamizawa J, Konishi H, Yanagisawa K, Tomida S, Osada H, Endoh H, Harano T, Yatabe Y, Nagino M, Nimura Y, et al: Reduced expression of the let-7 microRNAs in human lung cancers in association with shortened postoperative survival. Cancer Res. 2004, 64: 3753-3756. 10.1158/0008-5472.CAN-04-0637.CrossRefPubMed Takamizawa J, Konishi H, Yanagisawa K, Tomida S, Osada H, Endoh H, Harano T, Yatabe Y, Nagino M, Nimura Y, et al: Reduced expression of the let-7 microRNAs in human lung cancers in association with shortened postoperative survival. Cancer Res. 2004, 64: 3753-3756. 10.1158/0008-5472.CAN-04-0637.CrossRefPubMed
15.
go back to reference Solberg OD, Ostrin EJ, Love MI, Peng JC, Bhakta NR, Hou L, Nguyen C, Solon M, Nguyen C, Barczak AJ, et al: Airway epithelial miRNA expression is altered in asthma. Am J Respir Crit Care Med. 2012, 186: 965-974. 10.1164/rccm.201201-0027OC.CrossRefPubMedPubMedCentral Solberg OD, Ostrin EJ, Love MI, Peng JC, Bhakta NR, Hou L, Nguyen C, Solon M, Nguyen C, Barczak AJ, et al: Airway epithelial miRNA expression is altered in asthma. Am J Respir Crit Care Med. 2012, 186: 965-974. 10.1164/rccm.201201-0027OC.CrossRefPubMedPubMedCentral
16.
go back to reference Harris KS, Zhang Z, McManus MT, Harfe BD, Sun X: Dicer function is essential for lung epithelium morphogenesis. Proc Natl Acad Sci USA. 2006, 103: 2208-2213. 10.1073/pnas.0510839103.CrossRefPubMedPubMedCentral Harris KS, Zhang Z, McManus MT, Harfe BD, Sun X: Dicer function is essential for lung epithelium morphogenesis. Proc Natl Acad Sci USA. 2006, 103: 2208-2213. 10.1073/pnas.0510839103.CrossRefPubMedPubMedCentral
17.
go back to reference Williams AE, Moschos SA, Perry MM, Barnes PJ, Lindsay MA: Maternally imprinted microRNAs are differentially expressed during mouse and human lung development. Dev Dyn. 2007, 236: 572-580. 10.1002/dvdy.21047.CrossRefPubMedPubMedCentral Williams AE, Moschos SA, Perry MM, Barnes PJ, Lindsay MA: Maternally imprinted microRNAs are differentially expressed during mouse and human lung development. Dev Dyn. 2007, 236: 572-580. 10.1002/dvdy.21047.CrossRefPubMedPubMedCentral
18.
go back to reference Lu Y, Thomson JM, Wong HY, Hammond SM, Hogan BL: Transgenic over-expression of the microRNA miR-17-92 cluster promotes proliferation and inhibits differentiation of lung epithelial progenitor cells. Dev Biol. 2007, 310: 442-453. 10.1016/j.ydbio.2007.08.007.CrossRefPubMedPubMedCentral Lu Y, Thomson JM, Wong HY, Hammond SM, Hogan BL: Transgenic over-expression of the microRNA miR-17-92 cluster promotes proliferation and inhibits differentiation of lung epithelial progenitor cells. Dev Biol. 2007, 310: 442-453. 10.1016/j.ydbio.2007.08.007.CrossRefPubMedPubMedCentral
19.
go back to reference Liu X, Nelson A, Wang X, Kanaji N, Kim M, Sato T, Nakanishi M, Li Y, Sun J, Michalski J, et al: MicroRNA-146a modulates human bronchial epithelial cell survival in response to the cytokine-induced apoptosis. Biochem Biophys Res Commun. 2009, 380: 177-182. 10.1016/j.bbrc.2009.01.066.CrossRefPubMed Liu X, Nelson A, Wang X, Kanaji N, Kim M, Sato T, Nakanishi M, Li Y, Sun J, Michalski J, et al: MicroRNA-146a modulates human bronchial epithelial cell survival in response to the cytokine-induced apoptosis. Biochem Biophys Res Commun. 2009, 380: 177-182. 10.1016/j.bbrc.2009.01.066.CrossRefPubMed
20.
go back to reference Rodriguez A, Vigorito E, Clare S, Warren MV, Couttet P, Soond DR, van Dongen S, Grocock RJ, Das PP, Miska EA, et al: Requirement of bic/microRNA-155 for normal immune function. Science. 2007, 316: 608-611. 10.1126/science.1139253.CrossRefPubMedPubMedCentral Rodriguez A, Vigorito E, Clare S, Warren MV, Couttet P, Soond DR, van Dongen S, Grocock RJ, Das PP, Miska EA, et al: Requirement of bic/microRNA-155 for normal immune function. Science. 2007, 316: 608-611. 10.1126/science.1139253.CrossRefPubMedPubMedCentral
21.
go back to reference Thai TH, Calado DP, Casola S, Ansel KM, Xiao C, Xue Y, Murphy A, Frendewey D, Valenzuela D, Kutok JL, et al: Regulation of the germinal center response by microRNA-155. Science. 2007, 316: 604-608. 10.1126/science.1141229.CrossRefPubMed Thai TH, Calado DP, Casola S, Ansel KM, Xiao C, Xue Y, Murphy A, Frendewey D, Valenzuela D, Kutok JL, et al: Regulation of the germinal center response by microRNA-155. Science. 2007, 316: 604-608. 10.1126/science.1141229.CrossRefPubMed
22.
go back to reference Bertero T, Gastaldi C, Bourget-Ponzio I, Imbert V, Loubat A, Selva E, Busca R, Mari B, Hofman P, Barbry P, et al: miR-483-3p controls proliferation in wounded epithelial cells. FASEB J. 2011, 25: 3092-3105. 10.1096/fj.10-168401.CrossRefPubMed Bertero T, Gastaldi C, Bourget-Ponzio I, Imbert V, Loubat A, Selva E, Busca R, Mari B, Hofman P, Barbry P, et al: miR-483-3p controls proliferation in wounded epithelial cells. FASEB J. 2011, 25: 3092-3105. 10.1096/fj.10-168401.CrossRefPubMed
23.
go back to reference Adam EC, Holgate ST, Lackie PM: Epithelial repair is inhibited by an alpha(1,6)-fucose binding lectin. Am J Physiol Lung Cell Mol Physiol. 2007, 292: L462-L468.CrossRefPubMed Adam EC, Holgate ST, Lackie PM: Epithelial repair is inhibited by an alpha(1,6)-fucose binding lectin. Am J Physiol Lung Cell Mol Physiol. 2007, 292: L462-L468.CrossRefPubMed
24.
go back to reference Schneider CA, Rasband WS, Eliceiri KW: NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012, 9: 671-675. 10.1038/nmeth.2089.CrossRefPubMed Schneider CA, Rasband WS, Eliceiri KW: NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012, 9: 671-675. 10.1038/nmeth.2089.CrossRefPubMed
25.
go back to reference Schmittgen TD, Livak KJ: Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc. 2008, 3: 1101-1108. 10.1038/nprot.2008.73.CrossRefPubMed Schmittgen TD, Livak KJ: Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc. 2008, 3: 1101-1108. 10.1038/nprot.2008.73.CrossRefPubMed
26.
go back to reference Ernst J, Bar-Joseph Z: STEM: a tool for the analysis of short time series gene expression data. BMC Bioinformatics. 2006, 7: 191-10.1186/1471-2105-7-191.CrossRefPubMedPubMedCentral Ernst J, Bar-Joseph Z: STEM: a tool for the analysis of short time series gene expression data. BMC Bioinformatics. 2006, 7: 191-10.1186/1471-2105-7-191.CrossRefPubMedPubMedCentral
27.
go back to reference da Huang W, Sherman BT, Lempicki RA: Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009, 4: 44-57.CrossRefPubMed da Huang W, Sherman BT, Lempicki RA: Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009, 4: 44-57.CrossRefPubMed
28.
go back to reference da Huang W, Sherman BT, Zheng X, Yang J, Imamichi T, Stephens R, Lempicki RA: Extracting biological meaning from large gene lists with DAVID. Curr Protoc Bioinformatics. 2009, Chapter 13:Unit 13 11 da Huang W, Sherman BT, Zheng X, Yang J, Imamichi T, Stephens R, Lempicki RA: Extracting biological meaning from large gene lists with DAVID. Curr Protoc Bioinformatics. 2009, Chapter 13:Unit 13 11
29.
go back to reference D. N: BioCarta. Biotech Softw Internet Rep. 2001, 2: 117-120. 10.1089/152791601750294344.CrossRef D. N: BioCarta. Biotech Softw Internet Rep. 2001, 2: 117-120. 10.1089/152791601750294344.CrossRef
30.
go back to reference Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M: The KEGG resource for deciphering the genome. Nucleic Acids Res. 2004, 32: D277-D280. 10.1093/nar/gkh063.CrossRefPubMedPubMedCentral Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M: The KEGG resource for deciphering the genome. Nucleic Acids Res. 2004, 32: D277-D280. 10.1093/nar/gkh063.CrossRefPubMedPubMedCentral
31.
go back to reference Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, et al: Gene ontology: tool for the unification of biology. The gene ontology consortium. Nat Genet. 2000, 25: 25-29. 10.1038/75556.CrossRefPubMedPubMedCentral Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, et al: Gene ontology: tool for the unification of biology. The gene ontology consortium. Nat Genet. 2000, 25: 25-29. 10.1038/75556.CrossRefPubMedPubMedCentral
32.
go back to reference Adam EC, Holgate ST, Fildew CJ, Lackie PM: Role of carbohydrates in repair of human respiratory epithelium using an in vitro model. Clin Exp Allergy. 2003, 33: 1398-1404. 10.1046/j.1365-2222.2003.01771.x.CrossRefPubMed Adam EC, Holgate ST, Fildew CJ, Lackie PM: Role of carbohydrates in repair of human respiratory epithelium using an in vitro model. Clin Exp Allergy. 2003, 33: 1398-1404. 10.1046/j.1365-2222.2003.01771.x.CrossRefPubMed
33.
go back to reference Howat WJ, Holgate ST, Lackie PM: TGF-beta isoform release and activation during in vitro bronchial epithelial wound repair. Am J Physiol Lung Cell Mol Physiol. 2002, 282: L115-L123.PubMed Howat WJ, Holgate ST, Lackie PM: TGF-beta isoform release and activation during in vitro bronchial epithelial wound repair. Am J Physiol Lung Cell Mol Physiol. 2002, 282: L115-L123.PubMed
34.
go back to reference Leir SH, Holgate ST, Lackie PM: Inflammatory cytokines can enhance CD44-mediated airway epithelial cell adhesion independently of CD44 expression. Am J Physiol Lung Cell Mol Physiol. 2003, 285: L1305-L1311.CrossRefPubMed Leir SH, Holgate ST, Lackie PM: Inflammatory cytokines can enhance CD44-mediated airway epithelial cell adhesion independently of CD44 expression. Am J Physiol Lung Cell Mol Physiol. 2003, 285: L1305-L1311.CrossRefPubMed
35.
go back to reference Hahn C, Islamian AP, Renz H, Nockher WA: Airway epithelial cells produce neurotrophins and promote the survival of eosinophils during allergic airway inflammation. J Allergy Clin Immunol. 2006, 117: 787-794. 10.1016/j.jaci.2005.12.1339.CrossRefPubMed Hahn C, Islamian AP, Renz H, Nockher WA: Airway epithelial cells produce neurotrophins and promote the survival of eosinophils during allergic airway inflammation. J Allergy Clin Immunol. 2006, 117: 787-794. 10.1016/j.jaci.2005.12.1339.CrossRefPubMed
36.
go back to reference Lommatzsch M, Braun A, Renz H: Neurotrophins in allergic airway dysfunction: what the mouse model is teaching us. Ann N Y Acad Sci. 2003, 992: 241-249. 10.1111/j.1749-6632.2003.tb03154.x.CrossRefPubMed Lommatzsch M, Braun A, Renz H: Neurotrophins in allergic airway dysfunction: what the mouse model is teaching us. Ann N Y Acad Sci. 2003, 992: 241-249. 10.1111/j.1749-6632.2003.tb03154.x.CrossRefPubMed
37.
go back to reference Olgart Hoglund C, Frossard N: Nerve growth factor and asthma. Pulm Pharmacol Ther. 2002, 15: 51-60. 10.1006/pupt.2001.0314.CrossRefPubMed Olgart Hoglund C, Frossard N: Nerve growth factor and asthma. Pulm Pharmacol Ther. 2002, 15: 51-60. 10.1006/pupt.2001.0314.CrossRefPubMed
38.
go back to reference Prakash Y, Thompson MA, Meuchel L, Pabelick CM, Mantilla CB, Zaidi S, Martin RJ: Neurotrophins in lung health and disease. Expert Rev Respir Med. 2010, 4: 395-411. 10.1586/ers.10.29.CrossRefPubMedPubMedCentral Prakash Y, Thompson MA, Meuchel L, Pabelick CM, Mantilla CB, Zaidi S, Martin RJ: Neurotrophins in lung health and disease. Expert Rev Respir Med. 2010, 4: 395-411. 10.1586/ers.10.29.CrossRefPubMedPubMedCentral
39.
go back to reference Kilic A, Sonar SS, Yildirim AO, Fehrenbach H, Nockher WA, Renz H: Nerve growth factor induces type III collagen production in chronic allergic airway inflammation. J Allergy Clin Immunol. 2011, 128: 1058-1066. 10.1016/j.jaci.2011.06.017. e1051-1054CrossRefPubMed Kilic A, Sonar SS, Yildirim AO, Fehrenbach H, Nockher WA, Renz H: Nerve growth factor induces type III collagen production in chronic allergic airway inflammation. J Allergy Clin Immunol. 2011, 128: 1058-1066. 10.1016/j.jaci.2011.06.017. e1051-1054CrossRefPubMed
40.
go back to reference Palazzo E, Marconi A, Truzzi F, Dallaglio K, Petrachi T, Humbert P, Schnebert S, Perrier E, Dumas M, Pincelli C: Role of neurotrophins on dermal fibroblast survival and differentiation. J Cell Physiol. 2012, 227: 1017-1025. 10.1002/jcp.22811.CrossRefPubMed Palazzo E, Marconi A, Truzzi F, Dallaglio K, Petrachi T, Humbert P, Schnebert S, Perrier E, Dumas M, Pincelli C: Role of neurotrophins on dermal fibroblast survival and differentiation. J Cell Physiol. 2012, 227: 1017-1025. 10.1002/jcp.22811.CrossRefPubMed
41.
go back to reference Adam L, Zhong M, Choi W, Qi W, Nicoloso M, Arora A, Calin G, Wang H, Siefker-Radtke A, McConkey D, et al: miR-200 expression regulates epithelial-to-mesenchymal transition in bladder cancer cells and reverses resistance to epidermal growth factor receptor therapy. Clin Cancer Res. 2009, 15: 5060-5072. 10.1158/1078-0432.CCR-08-2245.CrossRefPubMed Adam L, Zhong M, Choi W, Qi W, Nicoloso M, Arora A, Calin G, Wang H, Siefker-Radtke A, McConkey D, et al: miR-200 expression regulates epithelial-to-mesenchymal transition in bladder cancer cells and reverses resistance to epidermal growth factor receptor therapy. Clin Cancer Res. 2009, 15: 5060-5072. 10.1158/1078-0432.CCR-08-2245.CrossRefPubMed
42.
go back to reference Ogawa H, Azuma M, Uehara H, Takahashi T, Nishioka Y, Sone S, Izumi K: Nerve growth factor derived from bronchial epithelium after chronic mite antigen exposure contributes to airway hyperresponsiveness by inducing hyperinnervation, and is inhibited by in vivo siRNA. Clin Exp Allergy. 2012, 42: 460-470. 10.1111/j.1365-2222.2011.03918.x.CrossRefPubMed Ogawa H, Azuma M, Uehara H, Takahashi T, Nishioka Y, Sone S, Izumi K: Nerve growth factor derived from bronchial epithelium after chronic mite antigen exposure contributes to airway hyperresponsiveness by inducing hyperinnervation, and is inhibited by in vivo siRNA. Clin Exp Allergy. 2012, 42: 460-470. 10.1111/j.1365-2222.2011.03918.x.CrossRefPubMed
43.
go back to reference Puchelle E, Zahm JM, Tournier JM, Coraux C: Airway epithelial repair, regeneration, and remodeling after injury in chronic obstructive pulmonary disease. Proc Am Thorac Soc. 2006, 3: 726-733. 10.1513/pats.200605-126SF.CrossRefPubMed Puchelle E, Zahm JM, Tournier JM, Coraux C: Airway epithelial repair, regeneration, and remodeling after injury in chronic obstructive pulmonary disease. Proc Am Thorac Soc. 2006, 3: 726-733. 10.1513/pats.200605-126SF.CrossRefPubMed
44.
45.
go back to reference Ware LB, Matthay MA: The acute respiratory distress syndrome. N Engl J Med. 2000, 342: 1334-1349. 10.1056/NEJM200005043421806.CrossRefPubMed Ware LB, Matthay MA: The acute respiratory distress syndrome. N Engl J Med. 2000, 342: 1334-1349. 10.1056/NEJM200005043421806.CrossRefPubMed
46.
go back to reference Zahm JM, Chevillard M, Puchelle E: Wound repair of human surface respiratory epithelium. Am J Respir Cell Mol Biol. 1991, 5: 242-248. 10.1165/ajrcmb/5.3.242.CrossRefPubMed Zahm JM, Chevillard M, Puchelle E: Wound repair of human surface respiratory epithelium. Am J Respir Cell Mol Biol. 1991, 5: 242-248. 10.1165/ajrcmb/5.3.242.CrossRefPubMed
47.
go back to reference Zahm JM, Kaplan H, Herard AL, Doriot F, Pierrot D, Somelette P, Puchelle E: Cell migration and proliferation during the in vitro wound repair of the respiratory epithelium. Cell Motil Cytoskeleton. 1997, 37: 33-43. 10.1002/(SICI)1097-0169(1997)37:1<33::AID-CM4>3.0.CO;2-I.CrossRefPubMed Zahm JM, Kaplan H, Herard AL, Doriot F, Pierrot D, Somelette P, Puchelle E: Cell migration and proliferation during the in vitro wound repair of the respiratory epithelium. Cell Motil Cytoskeleton. 1997, 37: 33-43. 10.1002/(SICI)1097-0169(1997)37:1<33::AID-CM4>3.0.CO;2-I.CrossRefPubMed
48.
go back to reference Zahm JM, Pierrot D, Chevillard M, Puchelle E: Dynamics of cell movement during the wound repair of human surface respiratory epithelium. Biorheology. 1992, 29: 459-465.PubMed Zahm JM, Pierrot D, Chevillard M, Puchelle E: Dynamics of cell movement during the wound repair of human surface respiratory epithelium. Biorheology. 1992, 29: 459-465.PubMed
Metadata
Title
Altered microRNA expression profile during epithelial wound repair in bronchial epithelial cells
Authors
Aleksandra Szczepankiewicz
Peter M Lackie
John W Holloway
Publication date
01-12-2013
Publisher
BioMed Central
Published in
BMC Pulmonary Medicine / Issue 1/2013
Electronic ISSN: 1471-2466
DOI
https://doi.org/10.1186/1471-2466-13-63

Other articles of this Issue 1/2013

BMC Pulmonary Medicine 1/2013 Go to the issue