Mesenchymal stem cells for repair of the airway epithelium in asthma

Expert Review of Respiratory Medicine

Volumn 4, Issue 6, 2010, Pages 747-758

  Knight, Darryl A ^a   Rossi, Fabio M ^a   Hackett, Tillie Louise ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

airway; asthma; epithelial repair; injury; lung; mesenchymal stem cells; tissue resident stem cells

Indexed keywords

BLEOMYCIN; EPIDERMAL GROWTH FACTOR RECEPTOR; IMMUNOSUPPRESSIVE AGENT; PROTEIN ZO1; UVOMORULIN;

ADAPTIVE IMMUNITY; ALLERGIC RHINITIS; ASTHMA; BONE MARROW CELL; CELL DAMAGE; CELL DIFFERENTIATION; CELL LOSS; CELL POPULATION; CELL PROLIFERATION; CELL REGENERATION; CELL SPECIFICITY; CELL STRUCTURE; CHRONIC OBSTRUCTIVE LUNG DISEASE; CLARA CELL; CLINICAL TRIAL; CYTOKINE PRODUCTION; DESMOSOME; DISEASE COURSE; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM CELL; GENETIC ASSOCIATION; GOBLET CELL; HEMATOPOIETIC STEM CELL; HUMAN; IMMUNOMODULATION; LUNG FIBROBLAST; LUNG FUNCTION; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; MYOFIBROBLAST; NONHUMAN; NOSE POLYP; PARACRINE SIGNALING; PLACEBO EFFECT; RESPIRATORY EPITHELIUM; REVIEW; STEM CELL; T LYMPHOCYTE; WOUND HEALING;

EID: 78650071868     PISSN: 17476348     EISSN: 17476356     Source Type: Journal    
DOI: 10.1586/ers.10.72     Document Type: Review

References (133)

1. Pascual RM, Peters SP. Airway remodeling contributes to the progressive loss of lung function in asthma: an overview. J. Allergy Clin. Immunol. 116(3), 477-486; quiz 487 (2005).
2. Pascual RM, Peters SP. The irreversible component of persistent asthma. J. Allergy Clin. Immunol. 124(5), 883-890 (2009).
3. Masoli M, Fabian D, Holt S, Beasley R. The global burden of asthma: executive summary of the GINA Dissemination Committee report. Allergy 59(5), 469-478 (2004).
4. Holgate ST. Asthma: more than an infammatory disease. Curr. Opin Allergy Clin. Immunol. 2(1), 27-29 (2002).
5. Holgate ST. Epithelium dysfunction in asthma. J. Allergy Clin. Immunol. 120(6), 1233-1244; quiz 1245-1236 (2007).
6. Jeffery PK, Wardlaw AJ, Nelson FC, Collins J V, Kay AB. Bronchial biopsies in asthma. An ultrastructural, quantitative study and correlation with hyperreactivity. Am. Rev. Respir. Dis. 140(6), 1745-1753 (1989).
7. Laitinen LA, Heino M, Laitinen A, Kava T, Haahtela T. Damage of the airway epithelium and bronchial reactivity in patients with asthma. Am. Rev. Respir. Dis. 131(4), 599-606 (1985).
8. Puddicombe SM, Polosa R, Richter A et al. Involvement of the epidermal growth factor receptor in epithelial repair in asthma. FASEB J. 14(10), 1362-1374 (2000).
9. Mullings RE, Wilson SJ, Puddicombe SM et al. Signal transducer and activator of transcription 6 (STAT-6) expression and function in asthmatic bronchial epithelium. J. Allergy Clin. Immunol. 108(5), 832-838 (2001).
10. Fedorov IA, Wilson SJ, Davies DE, Holgate ST. Epithelial stress and structural remodelling in childhood asthma. Thorax 60(5), 389-394 (2005).
11. Knight DA, Holgate ST. The airway epithelium: structural and functional properties in health and disease. Respirology 8(4), 432-446 (2003).
12. Barbato A, Turato G, Baraldo S et al. Epithelial damage and angiogenesis in the airways of children with asthma. Am. J. Respir. Crit. Care Med. 174, 975-981 (2006).
13. Payne DN, Rogers AV, Adelroth E et al. Early thickening of the reticular basement membrane in children with diffcult asthma. Am. J. Respir. Crit. Care Med. 167(1), 78-82 (2003).
14. Kicic A, Sutanto EN, Stevens PT, Knight DA, Stick SM. Intrinsic biochemical and functional differences in bronchial epithelial cells of asthmatic children. Am. J. Respir. Crit. Care Med. 174, 1110-1118 (2006).
15. Pearce N, Pekkanen J, Beasley R. How much asthma is really attributable to atopy? Thorax 54(3), 268-272 (1999).
16. Holgate ST. Epithelial damage and response. Clin. Exp. Allergy 30(Suppl. 1), 37-41 (2000).
17. Holgate ST. The epithelium takes centre stage in asthma and atopic dermatitis. Trends Immunol. 28(6), 248-251 (2007).
18. Holgate ST. The infammation-repair cycle in asthma: the pivotal role of the airway epithelium. Clin. Exp. Allergy, 28(Suppl. 5), 97-103 (1998).
19. Trautmann A, Kruger K, Akdis M et al. Apoptosis and loss of adhesion of bronchial epithelial cells in asthma. Int. Arch. Allergy Immunol. 138(2), 142-150 (2005).
20. de Boer WI, Sharma HS, Baelemans SM, Hoogsteden HC, Lambrecht BN, Braunstahl GJ. Altered expression of epithelial junctional proteins in atopic asthma: possible role in infammation. Can. J. Physiol. Pharmacol. 86(3), 105-112 (2008).
21. Shahana S, Bjornsson E, Ludviksdottir D et al. Ultrastructure of bronchial biopsies from patients with allergic and non-allergic asthma. Respir. Med. 99(4), 429-443 (2005).
22. Shahana S, Jaunmuktane Z, Asplund MS, Roomans GM. Ultrastructural investigation of epithelial damage in asthmatic and non-asthmatic nasal polyps. Respir. Med. 100(11), 2018-2028 (2006).
23. Sumi Y, Hamid Q. Airway remodeling in asthma. Allergol. Int. 56(4), 341-348 (2007).
24. Cohen L, Ea X, Tarsi J et al. Epithelial cell proliferation contributes to airway remodeling in severe asthma. Am. J. Respir. Crit. Care Med. 176(2), 138-145 (2007).
25. Ricciardolo FL, Di Stefano A, van Krieken JH et al. Proliferation and infammation in bronchial epithelium after allergen in atopic asthmatics. Clin. Exp. Allergy 33(7), 905-911 (2003).
26. Stevens PT, Kicic A, Sutanto EN, Knight DA, Stick SM. Dysregulated repair in asthmatic paediatric airway epithelial cells: the role of plasminogen activator inhibitor-1. Clin. Exp. Allergy 38(12), 1901-1910 (2008).
27. Kicic A, Hallstrand TS, Sutanto EN et al. Decreased fbronectin production signifcantly contributes to dysregulated repair of asthmatic epithelium. Am. J. Respir. Crit. Care Med. 181, 889-898 (2010).
28. Lackie PM, Baker JE, Gunthert U, Holgate ST. Expression of CD44 isoforms is increased in the airway epithelium of asthmatic subjects. Am. J. Respir. Cell Mol. Biol. 16(1), 14-22 (1997).
29. Davies DE, Polosa R, Puddicombe SM, Richter A, Holgate ST. The epidermal growth factor receptor and its ligand family: their potential role in repair and remodelling in asthma. Allergy 54(8), 771-783 (1999).
30. Puddicombe SM, Torres-Lozano C, Richter A et al. Increased expression of p21(waf) cyclin-dependent kinase inhibitor in asthmatic bronchial epithelium. Am. J. Respir. Cell Mol. Biol. 28(1), 61-68 (2003).
31. Allahverdian S, Harada N, Singhera GK, Knight DA, Dorscheid DR. Secretion of IL-13 by airway epithelial cells enhances epithelial repair via HB-EGF. Am. J. Respir. Cell Mol. Biol. 38(2), 153-160 (2008).
32. Cookson W. The immunogenetics of asthma and eczema: a new focus on the epithelium. Nat. Rev. Immunol. 4(12), 978-988 (2004).
33. Holgate ST, Davies DE, Powell RM, Howarth PH, Haitchi HM, Holloway JW. Local genetic and environmental factors in asthma disease pathogenesis: chronicity and persistence mechanisms. Eur. Respir. J. 29(4), 793-803 (2007).
34. Liu X, Engelhardt JF. The glandular stem/progenitor cell niche in airway development and repair. Proc. Am. Thorac. Soc. 5(6), 682-688 (2008).
35. Lajtha LG. Stem cell concepts. Differentiation 14(1-2), 23-34 (1979).
36. McQualter JL, Yuen K, Williams B, Bertoncello I. Evidence of an epithelial stem/progenitor cell hierarchy in the adult mouse lung. Proc. Natl Acad. Sci. USA 107(4), 1414-1419 (2010).
37. Breuer R, Christensen TG, Lucey EC, Stone PJ, Snider GL. An ultrastructural morphometric analysis of elastase-treated hamster bronchi shows discharge followed by progressive accumulation of secretory granules. Am. Rev. Respir. Dis. 136(3), 698-703 (1987).
38. Hong KU, Reynolds SD, Watkins S, Fuchs E, Stripp BR. In vivo differentiation potential of tracheal basal cells: evidence for multipotent and unipotent subpopulations. Am. J. Physiol. Lung Cell. Mol. Physiol. 286, L643-L649 (2004).
39. Hong KU, Reynolds SD, Watkins S, Fuchs E, Stripp BR. Basal cells are a multipotent progenitor capable of renewing the bronchial epithelium. Am. J. Pathol. 164, 577-588 (2004).
40. Hong KU, Reynolds SD, Giangreco A, Hurley CM, Stripp BR. Clara cell secretory protein-expressing cells of the airway neuroepithelial body microenvironment include a label-retaining subset and are critical for epithelial renewal after progenitor cell depletion. Am. J. Respir. Cell Mol. Biol. 24, 671-681 (2001).
41. Reynolds SD, Giangreco A, Power JH, Stripp BR. Neuroepithelial bodies of pulmonary airways serve as a reservoir of progenitor cells capable of epithelial regeneration. Am. J. Pathol. 156(1), 269-278 (2000).
42. Rock JR, Onaitis M W, Rawlins EL et al. Basal cells as stem cells of the mouse trachea and human airway epithelium. Proc. Natl Acad. Sci. USA 106(31), 12771-12775 (2009).
43. Engelhardt JF, Schlossberg H, Yankaskas JR, Dudus L. Progenitor cells of the adult human airway involved in submucosal gland development. Development 121(7), 2031-2046 (1995).
44. Avril-Delplanque A, Casal I, Castillon N, Hinnrasky J, Puchelle E, Péault B. Aquaporin-3 expression in human fetal airway epithelial progenitor cells. Stem Cells 23(7), 992-1001 (2005).
45. Hajj R, Baranek T, Le Naour R, Lesimple P, Puchelle E, Coraux C. Basal cells of the human adult airway surface epithelium retain transit-amplifying cell properties. Stem Cells 25(1), 139-148 (2007).
46. Hackett TL, Shaheen F, Johnson A et al. Characterization of side population cells from human airway epithelium. Stem Cells 26(10), 2576-2585 (2008).
47. Rock JR, Randell SH, Hogan BLM. Airway basal stem cells: a perspective on their roles in epithelial homeostasis and remodeling. Dis. Model Mech. 3(9-10), 545-556 (2010).
48. Erjefalt JS, Erjefalt I, Sundler F, Persson CGA. In vivo restitution of airway epithelium. Cell Tiss. Res. 281, 305-316 (1995).
49. Erjefalt JS, Korsgren M, Nilsson MC, Sundler F, Persson CGA. Prompt epithelial damage and restitution processes in allergen challenged guinea pig trachea in vivo. Clin. Exp. Allergy 27, 1458-1470 (1997).
50. Erjefalt JS, Korsgren M, Nilsson MC, Sundler F, Persson CGA. Association between infammation and epithelial damage-restitution processes in allergic airways in vivo. Clin. Exp. Allergy 27, 1344-1355 (1997).
51. Wong AP, Keating A, Waddell TK. Airway regeneration: the role of the Clara cell secretory protein and the cells that express it. Cytotherapy 11(6), 676-687 (2009).
52. Giangreco A, Arwert EN, Rosewell IR, Snyder J, Watt FM, Stripp BR. Stem cells are dispensable for lung homeostasis but restore airways after injury. Proc. Natl Acad. Sci. USA 106(23), 9286-9291 (2009).
53. Dolgachev VA, Ullenbruch MR, Lukacs N W, Phan SH. Role of stem cell factor and bone marrow-derived fbroblasts in airway remodeling. Am. J. Pathol. 174(2), 390-400 (2009).
54. Le Blanc K, Samuelsson H, Gustafsson B et al. Transplantation of mesenchymal stem cells to enhance engraftment of hematopoietic stem cells. Leukemia 21(8), 1733-1738 (2007).
55. Kleeberger W, Versmold A, Rothamel T et al. Increased chimerism of bronchial and alveolar epithelium in human lung allografts undergoing chronic injury. Am. J. Pathol. 162(5), 1487-1494 (2003).
56. van Haaften T, Byrne R, Bonnet S et al. Airway delivery of mesenchymal stem cells prevents arrested alveolar growth in neonatal lung injury in rats. Am. J. Respir. Crit. Care Med. 180(11), 1131-1142 (2009).
57. Kaplan RN, Psaila B, Lyden D. Niche-to-niche migration of bone-marrow-derived cells. Trends Mol. Med. 13(2), 72-81 (2007).
58. Gregory CA, Prockop DJ, Spees JL. Non-hematopoietic bone marrow stem cells: molecular control of expansion and differentiation. Exp. Cell Res. 306(2), 330-335 (2005).
59. Steinmetz M, Nickenig G, Werner N. Endothelial-regenerating cells: an expanding universe. Hypertension 55(3), 593-599 (2010).
60. Asosingh K, Hanson JD, Cheng G, Aronica MA, Erzurum SC. Allergen-induced, eotaxin-rich, proangiogenic bone marrow progenitors: a blood-borne cellular envoy for lung eosinophilia. J. Allergy Clin. Immunol. 125(4), 918-925 (2010).
61. Huertas A, Testa U, Riccioni R et al. Bone marrow-derived progenitors are greatly reduced in patients with severe COPD and low-BMI. Respir. Physiol. Neurobiol. 170(1), 23-31 (2010).
62. Sala E, Villena C, Balaguer C et al. Abnormal levels of circulating endothelial progenitor cells during exacerbations of COPD. Lung 188(4), 331-338 (2010).
63. 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 65(6), 554-555 (2010).
64. Umar S, de Visser Y P, Steendijk P et al. Allogenic stem cell therapy improves right ventricular function by improving lung pathology in rats with pulmonary hypertension. Am. J. Physiol. Heart Circ. Physiol. 297(5), H1606-H1616 (2009).
65. Yamada M, Kubo H, Ishizawa K, Kobayashi S, Shinkawa M, Sasaki H. Increased circulating endothelial progenitor cells in patients with bacterial pneumonia: evidence that bone marrow derived cells contribute to lung repair. Thorax 60(5), 410-413 (2005).
66. Zhen G, Xue Z, Zhao J et al. Mesenchymal stem cell transplantation increases expression of vascular endothelial growth factor in papain-induced emphysematous lungs and inhibits apoptosis of lung cells. Cytotherapy 12(5), 605-614 (2010).
67. Barbato A, Turato G, Baraldo S et al. Epithelial damage and angiogenesis in the airways of children with asthma. Am. J. Respir. Crit. Care Med. 174(9), 975-981 (2006).
68. Alviano F, Fossati V, Marchionni C et al. Term amniotic membrane is a high throughput source for multipotent mesenchymal stem cells with the ability to differentiate into endothelial cells in vitro. BMC Dev. Biol. 7, 11 (2007).
69. da Silva Meirelles L, Chagastelles PC, Nardi NB. Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J. Cell Sci. 119(Pt 11), 2204-2213 (2006).
70. Fukuchi Y, Nakajima H, Sugiyama D, Hirose I, Kitamura T, Tsuji K. Human placenta-derived cells have mesenchymal stem/progenitor cell potential. Stem Cells 22(5), 649-658 (2004).
71. Donald GP, Katy H, Charles M et al. Biological activities encoded by the murine mesenchymal stem cell transcriptome provide a basis for their developmental potential and broad therapeutic effcacy. Stem Cells 24(1), 186-198 (2006).
72. Gang EJ, Darabi R, Bosnakovski D et al. Engraftment of mesenchymal stem cells into dystrophin-defcient mice is not accompanied by functional recovery. Exp. Cell Res. 315(15), 2624-2636 (2009).
73. Lindolfo da Silva M, Arnold IC, Nance Beyer N. In search of the in vivo identity of mesenchymal stem cells. Stem Cells 26(9), 2287-2299 (2008).
74. Sethe S, Scutt A, Stolzing A. Aging of mesenchymal stem cells. Age. Res. Rev. 5(1), 91-116 (2006).
75. Dominici M, Le Blanc K, Mueller I et al. Minimal criteria for defning multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8(4), 315-317 (2006).
76. Colter DC, Sekiya I, Prockop DJ. Identifcation of a subpopulation of rapidly self-renewing and multipotential adult stem cells in colonies of human marrow stromal cells. Proc. Natl Acad. Sci. USA 98(14), 7841-7845 (2001).
77. Ennis J, Sarugaser R, Gomez A, Baksh D, Davies JE. Isolation, characterization, and differentiation of human umbilical cord perivascular cells (HUCPVCs). Methods Cell. Biol. 86, 121-136 (2008).
78. Hung SC, Chen NJ, Hsieh SL, Li H, Ma HL, Lo WH. Isolation and characterization of size-sieved stem cells from human bone marrow. Stem Cells 20(3), 249-258 (2002).
79. Antonio G, Umberto G, Ignazio RM. From the laboratory bench to the patient's bedside: an update on clinical trials with mesenchymal stem cells. J. Cell. Physiol. 211(1), 27-35 (2007).
80. Le Blanc K, Pittenger MF. Mesenchymal stem cells: progress toward promise. Cytotherapy 7(1), 36-45 (2005).
81. Ghannam S, Pene J, Torcy-Moquet G, Jorgensen C, Yssel H. Mesenchymal stem cells inhibit human Th17 cell differentiation and function and induce a T regulatory cell phenotype. J. Immunol. 185, 302-312 (2010).
82. Sueblinvong V, Weiss DJ. Cell therapy approaches for lung diseases: current status. Curr. Opin. Pharmacol. 9(3), 268-273 (2009).
83. Uccelli A, Moretta L, Pistoia V. Mesenchymal stem cells in health and disease. Nat. Rev. Immunol. 8(9), 726-736 (2008).
84. Ortiz LA, Gambelli F, McBride C et al. Mesenchymal stem cell engraftment in lung is enhanced in response to bleomycin exposure and ameliorates its fbrotic effects. Proc. Natl Acad. Sci. USA 100(14), 8407-8411 (2003).
85. Liebler JM, Lutzko C, Banfalvi A et al. Retention of human bone marrow-derived cells in murine lungs following bleomycin-induced lung injury. Am. J. Physiol. Lung Cell. Mol. Physiol. 295(2), L285-L292 (2008).
86. Kotton DN, Ma BY, Cardoso WV et al. Bone marrow-derived cells as progenitors of lung alveolar epithelium. Development 128(24), 5181-5188 (2001).
87. Kotton DN, Fabian AJ, Mulligan RC. Failure of bone marrow to reconstitute lung epithelium. Am. J. Respir. Cell Mol. Biol. 33(4), 328-334 (2005).
88. Ortiz LA, Dutreil M, Fattman C et al. Interleukin 1 receptor antagonist mediates the antiinfammatory and antifbrotic effect of mesenchymal stem cells during lung injury. Proc. Natl Acad. Sci. USA 104(26), 11002-11007 (2007).
89. Gupta N, Su X, Popov B, Lee JW, Serikov V, Matthay MA. Intrapulmonary delivery of bone marrow-derived mesenchymal stem cells improves survival and attenuates endotoxin-induced acute lung injury in mice. J. Immunol. 179(3), 1855-1863 (2007).
90. Lee JW, Fang X, Gupta N, Serikov V, Matthay MA. Allogeneic human mesenchymal stem cells for treatment of E. coli endotoxin-induced acute lung injury in the ex vivo perfused human lung. Proc. Natl Acad. Sci. USA 106(38), 16357-16362 (2009).
91. Xu J, Qu J, Cao L et al. Mesenchymal stem cell-based angiopoietin-1 gene therapy for acute lung injury induced by lipopolysaccharide in mice. J. Pathol. 214(4), 472-481 (2008).
92. Fang X, Neyrinck AP, Matthay MA, Lee J W. Allogeneic human mesenchymal stem cells restore epithelial protein permeability in cultured human alveolar type II cells by secretion of angiopoietin-1. J. Biol. Chem. 285(34), 26211-26222 (2010).
93. Kumamoto M, Nishiwaki T, Matsuo N, Kimura H, Matsushima K. Minimally cultured bone marrow mesenchymal stem cells ameliorate fbrotic lung injury. Eur. Respir. J. 34(3), 740-748 (2009).
94. Wang Y, Sun Z, Qiu X, Li Y, Qin J, Han X. Roles of Wnt/b-catenin signaling in epithelial differentiation of mesenchymal stem cells. Biochem. Biophys. Res. Commun. 390(4), 1309-1314 (2009).
95. Wong AP, Keating A, Lu WY et al. Identifcation of a bone marrow-derived epithelial-like population capable of repopulating injured mouse airway epithelium. J. Clin. Invest. 119(2), 336-348 (2009).
96. Wong A P, Dutly AE, Sacher A et al. Targeted cell replacement with bone marrow cells for airway epithelial regeneration. Am. J. Physiol. Lung Cell. Mol. Physiol. 293(3), L740-L752 (2007).
97. Yan X, Liu Y, Han Q et al. Injured microenvironment directly guides the differentiation of engrafted Flk-1(+) mesenchymal stem cell in lung. Exp. Hematol. 35(9), 1466-1475 (2007).
98. Leblond AL, Naud P, Forest V et al. Developing cell therapy techniques for respiratory disease: intratracheal delivery of genetically engineered stem cells in a murine model of airway injury. Hum. Gene Ther. 20(11), 1329-1343 (2009).
99. Murry CE, Soonpaa MH, Reinecke H et al. Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature 428(6983), 664-668 (2004).
100. Snyder JC, Zemke AC, Stripp BR. Reparative capacity of airway epithelium impacts deposition and remodeling of extracellular matrix. Am. J. Respir. Cell Mol. Biol. 40(6), 633-642 (2009).
101. Gomperts BN, Belperio JA, Rao PN et al. Circulating progenitor epithelial cells traffc via CXCR4/CXCL12 in response to airway injury. J. Immunol. 176(3), 1916-1927 (2006).
102. Gomperts BN, Strieter RM. Fibrocytes in lung disease. J. Leukoc. Biol. 82(3), 449-456 (2007).
103. Strieter RM, Keeley EC, Hughes MA, Burdick MD, Mehrad B. The role of circulating mesenchymal progenitor cells (fbrocytes) in the pathogenesis of pulmonary fbrosis. J. Leukoc. Biol. 86(5), 1111-1118 (2009).
104. Hong KM, Belperio JA, Keane MP, Burdick MD, Strieter RM. Differentiation of human circulating fbrocytes as mediated by transforming growth factor-b and peroxisome proliferator-activated receptor gamma. J. Biol. Chem. 282(31), 22910-22920 (2007).
105. Ogawa M, LaRue A, Watson P, Watson D. Hematopoietic stem cell origin of mesenchymal cells: opportunity for novel therapeutic approaches. Int. J. Hematol. 91(3), 353-359 (2010).
106. Moeller A, Gilpin SE, Ask K et al. Circulating fbrocytes are an indicator of poor prognosis in idiopathic pulmonary fbrosis. Am. J. Respir. Crit. Care Med. 179(7), 588-594 (2009).
107. Nihlberg K, Larsen K, Hultgardh-Nilsson A, Malmstrom A, Bjermer L, Westergren-Thorsson G. Tissue fbrocytes in patients with mild asthma: a possible link to thickness of reticular basement membrane? Respir. Res. 7, 50 (2006).
108. Schmidt M, Sun G, Stacey MA, Mori L, Mattoli S. Identifcation of circulating fbrocytes as precursors of bronchial myofbroblasts in asthma. J. Immunol. 171(1), 380-389 (2003).
109. Popova AP, Bozyk PD, Goldsmith AM et al. Autocrine production of TGF-b1 promotes myofbroblastic differentiation of neonatal lung mesenchymal stem cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 298(6), L735-L743 (2010).
110. Hackett TL, Warner SM, Stefanowicz D et al. Induction of epithelial-mesenchymal transition in primary airway epithelial cells from patients with asthma by transforming growth factor-beta1. Am. J. Respir. Crit. Care Med. 180(2), 122-133 (2009).
111. Heijink IH, Postma DS, Noordhoek JA, Broekema M, Kapus A. House dust mite-promoted epithelial-to-mesenchymal transition in human bronchial epithelium. Am. J. Respir. Cell Mol. Biol. 42(1), 69-79 (2010).
112. Kim KK, Kugler MC, Wolters PJ et al. Alveolar epithelial cell mesenchymal transition develops in vivo during pulmonary fbrosis and is regulated by the extracellular matrix. Proc. Natl Acad. Sci. USA 103(35), 13180-13185 (2006).
113. Chaffer CL, Thompson EW, Williams ED. Mesenchymal to epithelial transition in development and disease. Cells Tissues Organs 185(1-3), 7-19 (2007).
114. Chaffer CL, Brennan JP, Slavin JL, Blick T, Thompson EW, Williams ED. Mesenchymal-to-epithelial transition facilitates bladder cancer metastasis: role of fbroblast growth factor receptor-2. Cancer Res. 66(23), 11271-11278 (2006).
115. Zeisberg M, Shah AA, Kalluri R. Bone morphogenic protein-7 induces mesenchymal to epithelial transition in adult renal fbroblasts and facilitates regeneration of injured kidney. J. Biol. Chem. 280(9), 8094-8100 (2005).
116. Humphreys BD, Lin SL, Kobayashi A et al. Fate tracing reveals the pericyte and not epithelial origin of myofbroblasts in kidney fbrosis. Am. J. Pathol. 176(1), 85-97 (2010).
117. Joe AW, Yi L, Natarajan A et al. Muscle injury activates resident fbro/adipogenic progenitors that facilitate myogenesis. Nat. Cell Biol. 12(2), 153-163 (2010).
118. Go T, Jungebluth P, Baiguero S et al. Both epithelial cells and mesenchymal stem cell-derived chondrocytes contribute to the survival of tissue-engineered airway transplants in pigs. J. Thorac. Cardiovasc. Surg. 139(2), 437-443 (2010).
119. Omori K, Tada Y, Suzuki T et al. Clinical application of in situ tissue engineering using a scaffolding technique for reconstruction of the larynx and trachea. Ann. Otol. Rhinol. Laryngol. 117(9), 673-678 (2008).
120. Urita Y, Komuro H, Chen G, Shinya M, Saihara R, Kaneko M. Evaluation of diaphragmatic hernia repair using PLGA mesh-collagen sponge hybrid scaffold: an experimental study in a rat model. Pediatr. Surg. Int. 24(9), 1041-1045 (2008).
121. Omori K, Nakamura T, Kanemaru S, Magrufov A, Yamashita M, Shimizu Y. In situ tissue engineering of the cricoid and trachea in a canine model. Ann. Otol. Rhinol. Laryngol. 117(8), 609-613 (2008).
122. Macchiarini P, Jungebluth P, Go T et al. Clinical transplantation of a tissue-engineered airway. Lancet 372(9655), 2023-2030 (2008).
123. Tomei AA, Boschetti F, Gervaso F, Swartz MA. 3D collagen cultures under well-defned dynamic strain: a novel strain device with a porous elastomeric support. Biotechnol. Bioeng. 103(1), 217-225 (2009).
124. Mondrinos MJ, Koutzaki S, Lelkes PI, Finck CM. A tissue-engineered model of fetal distal lung tissue. Am. J. Physiol. Lung Cell. Mol. Physiol. 293(3), L639-L650 (2007).
125. Zani BG, Kojima K, Vacanti CA, Edelman ER. Tissue-engineered endothelial and epithelial implants differentially and synergistically regulate airway repair. Proc. Natl Acad. Sci. USA 105(19), 7046-7051 (2008).
126. Semont A, Mouiseddine M, Francois A et al. Mesenchymal stem cells improve small intestinal integrity through regulation of endogenous epithelial cell homeostasis. Cell Death Differ. 17(6), 952-961 (2010).
127. Nemeth K, Keane-Myers A, Brown JM et al. Bone marrow stromal cells use TGF-b to suppress allergic responses in a mouse model of ragweed-induced asthma. Proc. Natl Acad. Sci. USA 107(12), 5652-5657 (2010).
128. Wang G, Bunnell BA, Painter RG et al. Adult stem cells from bone marrow stroma differentiate into airway epithelial cells: potential therapy for cystic fbrosis. Proc. Natl Acad. Sci. USA 102(1), 186-191 (2005).
129. Cho KS, Park HK, Park HY et al. IFATS collection: immunomodulatory effects of adipose tissue-derived stem cells in an allergic rhinitis mouse model. Stem Cells 27(1), 259-265 (2009).
130. Park HK, Cho KS, Park HY et al. Adipose-derived stromal cells inhibit allergic airway infammation in mice. Stem Cells Dev. 19(11), 1811-1818 (2010).
131. Hirota JA, Hackett T-L, Inman MD, Knight DA. Modeling asthma in mice: what have we learned about the airway epithelium? Am. J. Respir. Cell Mol. Biol. DOI: 10.1165/rcmb.2010-0146TR (2010) (Epub ahead of print).
132. Tolar J, Le Blanc K, Keating A, Blazar BR. Hitting the right spot with mesenchymal stromal cells (MSCs). Stem Cells 28(8), 1446-1455 (2010).
133. Kassmer SH, Krause DS. Detection of bone marrow-derived lung epithelial cells. Exp. Hematol. 38(7), 564-573 (2010).