Direct isolation of myofibroblasts and fibroblasts from bleomycin-injured lungs reveals their functional similarities and differences

Fibrogenesis and Tissue Repair

Volumn 6, Issue 1, 2013, Pages

  Akamatsu, Taisuke ^a   Arai, Yosifumi ^a,b   Kosugi, Isao ^a   Kawasaki, Hideya ^a   Meguro, Shiori ^a   Sakao, Makiko ^a   Shibata, Kiyoshi ^a   Suda, Takafumi ^a   Chida, Kingo ^a   Iwashita, Toshihide ^a  

^a HAMAMATSU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b SEIREI HAMAMATSU GENERAL HOSPITAL   (Japan)

Author keywords

smooth muscle actin; Chemokine; Collagen; Fibroblasts; Myofibroblasts

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; ATAXIN 1; BLEOMYCIN; CD146 ANTIGEN; CD31 ANTIGEN; CD45 ANTIGEN; CD94E ANTIGEN; CELL SURFACE MARKER; COLLAGEN TYPE 1; CXCL14 CHEMOKINE; CXCL2 CHEMOKINE; ENZYME; EOTAXIN; EPITHELIAL CELL ADHESION MOLECULE; EPITHELIAL DERIVED NEUTROPHIL ACTIVATING FACTOR 78; FRACTALKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; HEAT SHOCK PROTEIN 47; LYMPHOCYTE ANTIGEN; LYVE 1; MONOCYTE CHEMOTACTIC PROTEIN 1; MONOCYTE CHEMOTACTIC PROTEIN 3; PROTEIN P4HA1; PROTEIN P4HA2; PROTEIN P4HA3; PROTEIN P4HB; PROTEIN PLOD1; RANTES; STROMAL CELL DERIVED FACTOR 1; TER119 ANTIGEN; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CCL11 GENE; CCL2 GENE; CCL5 GENE; CCL7 GENE; CELL CULTURE; CELL FUNCTION; CELL ISOLATION; CELL LINEAGE; CELL PROLIFERATION; CELL SURFACE; COL1A1 GENE; COL1A2 GENE; COL1A3 GENE; COLLAGEN SYNTHESIS; CONTROLLED STUDY; CX3CL1 GENE; CXCL1 GENE; CXCL10 GENE; CXCL12 GENE; CXCL14 GENE; CXCL2 GENE; CXCL5 GENE; DRUG INDUCED DISEASE; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; GENE; GENE EXPRESSION; GENE EXPRESSION PROFILING; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LUNG FIBROBLAST; LUNG INJURY; MOUSE; MYOFIBROBLAST; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

EID: 84883744574     PISSN: None     EISSN: 17551536     Source Type: Journal    
DOI: 10.1186/1755-1536-6-15     Document Type: Article

References (63)

1. Douglas IS, Diaz del Valle F, Winn RA, Voelkel NF. β-catenin in the fibroproliferative response to acute lung injury. Am J Respir Cell Mol Biol 2006, 34:274-285. 10.1165/rcmb.2005-0277OC, 2644193, 16272459.
2. Dobaczewski M, Gonzalez-Quesada C, Frangogiannis NG. The extracellular matrix as a modulator of the inflammatory and reparative response following myocardial infarction. J Mol Cell Cardiol 2010, 48:504-511. 10.1016/j.yjmcc.2009.07.015, 2824059, 19631653.
3. Hardie WD, Glasser SW, Hagood JS. Emerging concepts in the pathogenesis of lung fibrosis. Am J Pathol 2009, 175:3-16. 10.2353/ajpath.2009.081170, 2708789, 19497999.
4. Hinz B, Phan SH, Thannickal VJ, Galli A, Bochaton-Piallat ML, Gabbiani G. The myofibroblast: one function, multiple origins. Am J Pathol 2007, 170:1807-1816. 10.2353/ajpath.2007.070112, 1899462, 17525249.
5. Hinz B. Formation and function of the myofibroblast during tissue repair. J Invest Dermatol 2007, 127:526-537. 10.1038/sj.jid.5700613, 17299435.
6. Pache JC, Christakos PG, Gannon DE, Mitchell JJ, Low RB, Leslie KO. Myofibroblasts in diffuse alveolar damage of the lung. Mod Pathol 1998, 11:1064-1070.
7. Micallef L, Vedrenne N, Billet F, Coulomb B, Darby IA, Desmoulière A. The myofibroblast, multiple origins for major roles in normal and pathological tissue repair. Fibrogenesis Tissue Repair 2012, 5:S5. 10.1186/1755-1536-5-5, 3368789, 23259712.
8. Hinz B, Phan SH, Thannickal VJ, Prunotto M, Desmoulière A, Varga J, De Wever O, Mareel M, Gabbiani G. Recent developments in myofibroblast biology: paradigms for connective tissue remodeling. Am J Pathol 2012, 180:1340-1355. 10.1016/j.ajpath.2012.02.004, 3640252, 22387320.
9. Phan SH. Genesis of the myofibroblast in lung injury and fibrosis. Proc Am Thorac Soc 2012, 9:148-152. 10.1513/pats.201201-011AW, 22802289.
10. Wynn TA. Cellular and molecular mechanisms of fibrosis. J Pathol 2008, 214:199-210. 10.1002/path.2277, 2693329, 18161745.
11. Oda D, Gown AM, Vande Berg JS, Stern R. The fibroblast-like nature of myofibroblasts. Exp Mol Pathol 1988, 49:316-329. 10.1016/0014-4800(88)90004-4, 3197813.
12. Hinz B, Celetta G, Tomasek JJ, Gabbiani G, Chaponnier C. Alpha-smooth muscle actin expression upregulates fibroblast contractile activity. Mol Biol Cell 2001, 12:2730-2741. 10.1091/mbc.12.9.2730, 59708, 11553712.
13. Zhang HY, Gharaee-Kermani M, Zhang K, Karmiol S, Phan SH. Lung fibroblast alpha-smooth muscle actin expression and contractile phenotype in bleomycin-induced pulmonary fibrosis. Am J Pathol 1996, 148:527-537. 1861697, 8579115.
14. Chambers RC, Leoni P, Kaminski N, Laurent GJ, Heller RA. Global expression profiling of fibroblast responses to transforming growth factor-β1 reveals the induction of inhibitor of differentiation-1 and provides evidence of smooth muscle cell phenotypic switching. Am J Pathol 2003, 162:533-546. 10.1016/S0002-9440(10)63847-3, 1851161, 12547711.
15. Thannickal VJ, Lee DY, White ES, Cui Z, Larios JM, Chacon R, Horowitz JC, Day RM, Thomas PE. Myofibroblast differentiation by transforming growth factor-β1 is dependent on cell adhesion and integrin signaling via focal adhesion kinase. J Biol Chem 2003, 278:12384-12389. 10.1074/jbc.M208544200, 12531888.
16. Evans RA, Tian YC, Steadman R, Phillips AO. TGF-β1-mediated fibroblast-myofibroblast terminal differentiation-the role of smad proteins. Exp Cell Res 2003, 282:90-100. 10.1016/S0014-4827(02)00015-0, 12531695.
17. Hu B, Wu Z, Liu T, Ullenbruch MR, Jin H, Phan SH. Gut-enriched Krüppel-like factor interaction with Smad3 inhibits myofibroblast differentiation. Am J Respir Cell Mol Biol 2007, 36:78-84. 10.1165/rcmb.2006-0043OC, 1899300, 16858008.
18. Wygrecka M, Zakrzewicz D, Taborski B, Didiasova M, Kwapiszewska G, Preissner KT, Markart P. TGF-β1 induces tissue factor expression in human lung fibroblasts in a PI3K/JNK/Akt-dependent and AP-1-dependent manner. Am J Respir Cell Mol Biol 2012, 47:614-627. 10.1165/rcmb.2012-0097OC, 22771387.
19. Meneghin A, Choi ES, Evanoff HL, Kunkel SL, Martinez FJ, Flaherty KR, Toews GB, Hogaboam CM. TLR9 is expressed in idiopathic interstitial pneumonia and its activation promotes in vitro myofibroblast differentiation. Histochem Cell Biol 2008, 130:979-992. 10.1007/s00418-008-0466-z, 18633634.
20. Liu T, Dhanasekaran SM, Jin H, Hu B, Tomlins SA, Chinnaiyan AM, Phan SH. FIZZ1 stimulation of myofibroblast differentiation. Am J Pathol 2004, 164:1315-1326. 10.1016/S0002-9440(10)63218-X, 1615359, 15039219.
21. Moore BB, Hogaboam CM. Murine models of pulmonary fibrosis. Am J Physiol Lung Cell Mol Physiol 2008, 294:L152-L160.
22. Moore B, Lawson WE, Oury TD, Sisson TH, Raghavendran K, Hogaboam CM. Animal models of fibrotic lung disease. Am J Respir Cell Mol Biol in press.
23. Ponticos M, Partridge T, Black CM, Abraham DJ, Bou-Gharios G. Regulation of collagen type I in vascular smooth muscle cells by competition between Nkx2.5 and δEF1/ZEB1. Mol Cell Biol 2004, 24:6151-6161. 10.1128/MCB.24.14.6151-6161.2004, 434261, 15226419.
24. Qiao H, Bell J, Juliao S, Li L, May JM. Ascorbic acid uptake and regulation of type I collagen synthesis in cultured vascular smooth muscle cells. J Vasc Res 2009, 46:15-24. 10.1159/000135661, 3724476, 18515971.
25. Zhu X, Bergles DE, Nishiyama A. NG2 cells generate both oligodendrocytes and gray matter astrocytes. Development 2008, 135:145-157.
26. Goswami RS, Waldron L, Machado J, Cervigne NK, Xu W, Reis PP, Bailey DJ, Jurisica I, Crump MR, Kamel-Reid S. Optimization and analysis of a quantitative real-time PCR-based technique to determine microRNA expression in formalin-fixed paraffin-embedded samples. BMC Biotechnol 2010, 10:47. 10.1186/1472-6750-10-47, 2902407, 20573258.
27. McQualter JL, Brouard N, Williams B, Baird BN, Sims-Lucas S, Yuen K, Nilsson SK, Simmons PJ, Bertoncello I. Endogenous fibroblastic progenitor cells in the adult mouse lung are highly enriched in the Sca-1 positive cell fraction. Stem Cells 2009, 27:623-633. 10.1634/stemcells.2008-0866, 19074419.
28. Masur SK, Dewal HS, Dinh TT, Erenburg I, Petridou S. Myofibroblasts differentiate from fibroblasts when plated at low density. Proc Natl Acad Sci USA 1996, 93:4219-4223. 10.1073/pnas.93.9.4219, 39515, 8633044.
29. Taguchi T, Nazneen A, Al-Shihri AA, Turkistani KA, Razzaque MS. Heat shock protein 47: a novel biomarker of phenotypically altered collagen-producing cells. Acta Histochem Cytochem 2011, 44:35-41. 10.1267/ahc.11001, 3096080, 21614164.
30. Chen CZ, Raghunath M. Focus on collagen: in vitro systems to study fibrogenesis and antifibrosis - state of the art. Fibrogenesis Tissue Repair 2009, 2:7. 10.1186/1755-1536-2-7, 2805599, 20003476.
31. Todd NW, Luzina IG, Atamas SP. Molecular and cellular mechanisms of pulmonary fibrosis. Fibrogenesis Tissue Repair 2012, 5:11. 10.1186/1755-1536-5-11, 3443459, 22824096.
32. Chen W, Xu X, Bai L, Padilla MT, Gott KM, Leng S, Tellez CS, Wilder JA, Belinsky SA, Scott BR, Lin Y. Low-dose gamma-irradiation inhibits IL-6 secretion from human lung fibroblasts that promotes bronchial epithelial cell transformation by cigarette-smoke carcinogen. Carcinogenesis 2012, 33:1368-1374. 10.1093/carcin/bgs159, 22556270.
33. Choi ES, Jakubzick C, Carpenter KJ, Kunkel SL, Evanoff H, Martinez FJ, Flaherty KR, Toews GB, Colby TV, Kazerooni EA, Gross BH, Travis WD, Hogaboam CM. Enhanced monocyte chemoattractant protein-3/CC chemokine ligand-7 in usual interstitial pneumonia. Am J Respir Crit Care Med 2004, 170:508-515. 10.1164/rccm.200401-002OC, 15191918.
34. Deng X, Mercer PF, Scotton CJ, Gilchrist A, Chambers RC. Thrombin induces fibroblast CCL2/JE production and release via coupling of PAR1 to Galphaq and cooperation between ERK1/2 and Rho kinase signaling pathways. Mol Biol Cell 2008, 19:2520-2533. 10.1091/mbc.E07-07-0720, 2397294, 18353977.
35. Glista-Baker EE, Taylor AJ, Sayers BC, Thompson EA, Bonner JC. Nickel nanoparticles enhance platelet-derived growth factor-induced chemokine expression by mesothelial cells via prolonged mitogen-activated protein kinase activation. Am J Respir Cell Mol Biol 2012, 47:552-561. 10.1165/rcmb.2012-0023OC, 22700867.
36. Huaux F, Gharaee-Kermani M, Liu T, Morel V, McGarry B, Ullenbruch M, Kunkel SL, Wang J, Xing Z, Phan SH. Role of eotaxin-1 (CCL11) and CC chemokine receptor 3 (CCR3) in bleomycin-induced lung injury and fibrosis. Am J Pathol 2005, 167:1485-1496. 10.1016/S0002-9440(10)61235-7, 1613185, 16314464.
37. Isozaki T, Otsuka K, Sato M, Takahashi R, Wakabayashi K, Yajima N, Miwa Y, Kasama T. Synergistic induction of CX3CL1 by interleukin-1β and interferon-γ in human lung fibroblasts: involvement of signal transducer and activator of transcription 1 signaling pathways. Transl Res 2011, 157:64-70. 10.1016/j.trsl.2010.11.007, 21256458.
38. Teran LM, Mochizuki M, Bartels J, Valencia EL, Nakajima T, Hirai K, Schröder JM. Th1- and Th2-type cytokines regulate the expression and production of eotaxin and RANTES by human lung fibroblasts. Am J Respir Cell Mol Biol 1999, 20:777-786. 10.1165/ajrcmb.20.4.3508, 10101011.
39. Yang X, Walton W, Cook DN, Hua X, Tilley S, Haskell CA, Horuk R, Blackstock AW, Kirby SL. The chemokine, CCL3, and its receptor, CCR1, mediate thoracic radiation-induced pulmonary fibrosis. Am J Respir Cell Mol Biol 2011, 45:127-135. 10.1165/rcmb.2010-0265OC, 3145066, 20870892.
40. Zhou X, Chen Q, Moore J, Kolls JK, Halperin S, Wang J. Critical role of the interleukin-17/interleukin-17 receptor axis in regulating host susceptibility to respiratory infection with Chlamydia species. Infect Immun 2009, 77:5059-5070. 10.1128/IAI.00403-09, 2772560, 19737908.
41. Moeller A, Ask K, Warburton D, Gauldie J, Kolb M. The bleomycin animal model: a useful tool to investigate treatment options for idiopathic pulmonary fibrosis?. Int J Biochem Cell Biol 2008, 40:362-382. 10.1016/j.biocel.2007.08.011, 2323681, 17936056.
42. Scotton CJ, Chambers RC. Bleomycin revisited: towards a more representative model of IPF?. Am J Physiol Lung Cell Mol Physiol 2010, 299:L439-L441. 10.1152/ajplung.00258.2010, 20675435.
43. Fukuda Y, Basset F, Ferrans VJ, Yamanaka N. Significance of early intra-alveolar fibrotic lesions and integrin expression in lung biopsy specimens from patients with idiopathic pulmonary fibrosis. Hum Pathol 1995, 26:53-61. 10.1016/0046-8177(95)90114-0, 7529742.
44. Peng R, Sridhar S, Tyagi G, Phillips JE, Garrido R, Harris P, Burns L, Renteria L, Woods J, Chen L, Allard J, Ravindran P, Bitter H, Liang Z, Hogaboam CM, Kitson C, Budd DC, Fine JS, Bauer CM, Stevenson CS. Bleomycin induces molecular changes directly relevant to idiopathic pulmonary fibrosis: a model for " active" disease. PLoS One 2013, 8:e59348. 10.1371/journal.pone.0059348, 3614979, 23565148.
45. Barry-Hamilton V, Spangler R, Marshall D, McCauley S, Rodriguez HM, Oyasu M, Mikels A, Vaysberg M, Ghermazien H, Wai C, et al. Allosteric inhibition of lysyl oxidase-like-2 impedes the development of a pathologic microenvironment. Nat Med 2010, 16:1009-1017. 10.1038/nm.2208, 20818376.
46. Zuckerman JE, Hollinger MA, Giri SN. Evaluation of antifibrotic drugs in bleomycin-induced pulmonary fibrosis in hamsters. J Pharmacol Exp Ther 1980, 213:425-431.
47. Ledwozyw A. The effect of beta-aminopropionitrile on bleomycin-induced lung injury in rats. Acta Physiol Hung 1995, 83:91-99.
48. Wynn TA, Ramalingam TR. Mechanisms of fibrosis: therapeutic translation for fibrotic disease. Nat Med 2012, 18:1028-1040. 10.1038/nm.2807, 3405917, 22772564.
49. Rock JR, Barkauskas CE, Cronce MJ, Xue Y, Harris JR, Liang J, Noble PW, Hogan BL. Multiple stromal populations contribute to pulmonary fibrosis without evidence for epithelial to mesenchymal transition. Proc Natl Acad Sci USA 2011, 108:E1475-E1483. 10.1073/pnas.1117988108, 3248478, 22123957.
50. Dulauroy S, Di Carlo SE, Langa F, Eberl G, Peduto L. Lineage tracing and genetic ablation of ADAM12+ perivascular cells identify a major source of profibrotic cells during acute tissue injury. Nat Med 2012,
51. Bonner JC. Mesenchymal cell survival in airway and interstitial pulmonary fibrosis. Fibrogenesis Tissue Repair 2010, 3:15. 10.1186/1755-1536-3-15, 2940818, 20738867.
52. Hashimoto N, Phan SH, Imaizumi K, Matsuo M, Nakashima H, Kawabe T, Shimokata K, Hasegawa Y. Endothelial-mesenchymal transition in bleomycin-induced pulmonary fibrosis. Am J Respir Cell Mol Biol 2010, 43:161-172. 10.1165/rcmb.2009-0031OC, 2937229, 19767450.
53. Zolak JS, Jagirdar R, Surolia R, Karki S, Oliva O, Hock T, Guroji P, Ding Q, Liu RM, Bolisetty S, Agarwal A, Thannickal VJ, Antony VB. Pleural mesothelial cell differentiation and invasion in fibrogenic lung injury. Am J Pathol 2013, 182:1239-1247. 10.1016/j.ajpath.2012.12.030, 23399488.
54. Vannella KM, McMillan TR, Charbeneau RP, Wilke CA, Thomas PE, Toews GB, Peters-Golden M, Moore BB. Cysteinyl leukotrienes are autocrine and paracrine regulators of fibrocyte function. J Immunol 2007, 179:7883-7890. 3646370, 18025235.
55. Sun L, Louie MC, Vannella KM, Wilke CA, LeVine AM, Moore BB, Shanley TP. New concepts of IL-10-induced lung fibrosis: fibrocyte recruitment and M2 activation in a CCL2/CCR2 axis. Am J Physiol Lung Cell Mol Physiol 2011, 300:L341-L353. 10.1152/ajplung.00122.2010, 3064283, 21131395.
56. Shenoy V, Ferreira AJ, Qi Y, Fraga-Silva RA, Díez-Freire C, Dooies A, Jun JY, Sriramula S, Mariappan N, Pourang D, Venugopal CS, Francis J, Reudelhuber T, Santos RA, Patel JM, Raizada MK, Katovich MJ. The angiotensin-converting enzyme 2/angiogenesis-(1-7)/Mas axis confers cardiopulmonary protection against lung fibrosis and pulmonary hypertension. Am J Respir Crit Care Med 2010, 182:1065-1072. 10.1164/rccm.200912-1840OC, 2970847, 20581171.
57. Kruger GM, Mosher JT, Bixby S, Joseph N, Iwashita T, Morrison SJ. Neural crest stem cells persist in the adult gut but undergo changes in self-renewal, neuronal subtype potential, and factor responsiveness. Neuron 2002, 35:657-669. 10.1016/S0896-6273(02)00827-9, 2728576, 12194866.
58. Primer 3 http://frodo.wi.mit.edu.
59. Fink L, Seeger W, Ermert L, Hänze J, Stahl U, Grimminger F, Kummer W, Bohle RM. Real-time quantitative RT-PCR after laser-assisted cell picking. Nat Med 1998, 4:1329-1333. 10.1038/3327, 9809560.
60. Iwashita T, Kruger GM, Pardal R, Kiel MJ, Morrison SJ. Hirschsprung disease is linked to defects in neural crest stem cell function. Science 2003, 301:972-976. 10.1126/science.1085649, 2614078, 12920301.
61. Eisen Lab Evolution of Gene Expression and Gene Regulation in Flies, Fungi and Beyond http://www.eisenlab.org/eisen/?page_id=42, Eisen Lab.
62. Java TreeView http://jtreeview.sourceforge.net/.
63. Chanrion M, Fontaine H, Rodriguez C, Negre V, Bibeau F, Theillet C, Hénaut A, Darbon JM. A new molecular breast cancer subclass defined from a large scale real-time quantitative RT-PCR study. BMC Cancer 2007, 7:39. 10.1186/1471-2407-7-39, 1828062, 17338809.