Mesenchymal Stromal Cells are Readily Recoverable from Lung Tissue, but not the Alveolar Space, in Healthy Humans

Stem Cells

Volumn 34, Issue 10, 2016, Pages 2548-2558

  Sinclair, K A ^a,b   Yerkovich, S T ^a,b   Chen, T ^a   McQualter, J L ^c   Hopkins, P M A ^a,b   Wells, C A ^a   Chambers, D C ^a,b  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b THE PRINCE CHARLES HOSPITAL   (Australia)

^c CEDARS SINAI MEDICAL CENTER   (United States)

Author keywords

Lung; Mesenchymal stem cells; Mesenchymal stromal cells; Microarray; Transcriptome

Indexed keywords

5' NUCLEOTIDASE; ALPHA SMOOTH MUSCLE ACTIN; CD45 ANTIGEN; COLLAGEN TYPE 1; COLLAGEN TYPE 1A1; ENDOGLIN; THY 1 ANTIGEN; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ADULT; ARTICLE; BONE MARROW STROMA CELL; BRONCHOALVEOLAR LAVAGE FLUID; CELL ACTIVATION; CELL DIFFERENTIATION; CELL ISOLATION; CELL LINEAGE; CELL MIGRATION; CELL POPULATION; CLINICAL ARTICLE; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FEMALE; FIBROBLAST; GENE EXPRESSION; GENE FUNCTION; GENETIC TRANSCRIPTION; GRAFT RECIPIENT; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOPHENOTYPING; LUNG ALVEOLUS; LUNG PARENCHYMA; LUNG TRANSPLANTATION; MALE; MESENCHYMAL STROMA CELL; MULTIPOTENT STEM CELL; PHENOTYPE;

EID: 84990851665     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.2419     Document Type: Article

References (48)

1. Mendez-Ferrer S, Michurina TV, Ferraro F et al. Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 2010;466:829–834.
2. Barkauskas CE, Cronce MJ, Rackley CR et al. Type 2 alveolar cells are stem cells in adult lung. J Clin Investig 2013;123:3025–3036.
3. Tropea KA, Leder E, Aslam M et al. Bronchioalveolar stem cells increase after mesenchymal stromal cell treatment in a mouse model of bronchopulmonary dysplasia. Am J Physiol Lung Cell Mol Physiol 2012;302:L829–L837.
4. Spees JL, Olson SD, Whitney MJ et al. Mitochondrial transfer between cells can rescue aerobic respiration. Proc Natl Acad Sci USA 2006;103:1283–1288.
5. Islam MN, Das SR, Emin MT et al. Mitochondrial transfer from bone-marrow-derived stromal cells to pulmonary alveoli protects against acute lung injury. Nat Med 2012;18:759–765.
6. Jun D, Garat C, West J et al. The pathology of bleomycin-induced fibrosis is associated with loss of resident lung mesenchymal stem cells that regulate effector T-cell proliferation. Stem Cells 2011;29:725–735.
7. Dominici M, Le Blanc K, Mueller I et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The international society for cellular therapy position statement. Cytotherapy 2006;8:315–317.
8. Sabatini F, Petecchia L, Tavian M et al. Human bronchial fibroblasts exhibit a mesenchymal stem cell phenotype and multilineage differentiating potentialities. Lab Investig 2005;85:962–971.
9. Karoubi G, Cortes-Dericks L, Breyer I et al. Identification of mesenchymal stromal cells in human lung parenchyma capable of differentiating into aquaporin 5-expressing cells. Lab Investig 2009;89:1100–1114.
10. Lama VN, Smith L, Badri L et al. Evidence for tissue-resident mesenchymal stem cells in human adult lung from studies of transplanted allografts. J Clin Investig 2007;117:989–996.
11. Badri L, Walker NM, Ohtsuka T et al. Epithelial interactions and local engraftment of lung-resident mesenchymal stem cells. Am J Respir Cell Mol Biol 2011;45:809–816.
12. Jarvinen L, Badri L, Wettlaufer S et al. Lung resident mesenchymal stem cells isolated from human lung allografts inhibit T cell proliferation via a soluble mediator. J Immunol 2008;181:4389–4396.
13. Wagner W, Wein F, Seckinger A et al. Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbilical cord blood. Exp Hematol 2005;33:1402–1416.
14. Kern S, Eichler H, Stoeve J et al. Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells 2006;24:1294–1301.
15. Rohart F, Mason EA, Matigian N et al. A molecular classification of human mesenchymal stromal cells. Peer J 2016;4:e1845.
16. Verleden GM, Raghu G, Meyer KC et al. A new classification system for chronic lung allograft dysfunction. J Heart Lung Transplant 2014;33:127–133.
17. McQualter JL, McCarty RC, Van der Velden J et al. TGF-beta signaling in stromal cells acts upstream of FGF-10 to regulate epithelial stem cell growth in the adult lung. Stem Cell Res 2013;11:1222–1233.
18. McCarty RC, Gronthos S, Zannettino AC et al. Characterisation and developmental potential of ovine bone marrow derived mesenchymal stem cells. J Cell Physiol 2009;219:324–333.
19. Wells CA, Mosbergen R, Korn O et al. Stemformatics: Visualisation and sharing of stem cell gene expression. Stem Cell Res 2013;10:387–395.
20. Muller FJ, Laurent LC, Kostka D et al. Regulatory networks define phenotypic classes of human stem cell lines. Nature 2008;455:401–405.
21. de Lange T. Shelterin: The protein complex that shapes and safeguards human telomeres. Genes Dev 2005;19:2100–2110.
22. Marriott S, Baskir RS, Gaskill C et al. ABCG2pos lung mesenchymal stem cells are a novel pericyte subpopulation that contributes to fibrotic remodeling. Am J Physiol Cell Physiol 2014;307:C684–C698.
23. Naiche LA, Papaioannou VE. Loss of Tbx4 blocks hindlimb development and affects vascularization and fusion of the allantois. Development 2003;130:2681–2693.
24. Yin Z, Gonzales L, Kolla V et al. Hop functions downstream of Nkx2.1 and GATA6 to mediate HDAC-dependent negative regulation of pulmonary gene expression. Am J Physiol Lung Cell Mol Physiol 2006;291:L191–L199.
25. Pelekanos RA, Li J, Gongora M et al. Comprehensive transcriptome and immunophenotype analysis of renal and cardiac MSC-like populations supports strong congruence with bone marrow MSC despite maintenance of distinct identities. Stem Cell Res 2012;8:58–73.
26. Sinclair K, Yerkovich ST, Chambers DC. Mesenchymal stem cells and the lung. Respirology 2013;18:397–411.
27. McQualter JL, Yuen K, Williams B et al. Evidence of an epithelial stem/progenitor cell hierarchy in the adult mouse lung. Proc Natl Acad Sci USA 2010;107:1414–1419.
28. Campioni D, Lanza F, Moretti S et al. Loss of Thy-1 (CD90) antigen expression on mesenchymal stromal cells from hematologic malignancies is induced by in vitro angiogenic stimuli and is associated with peculiar functional and phenotypic characteristics. Cytotherapy 2008;10:69–82.
29. Campioni D, Rizzo R, Stignani M et al. A decreased positivity for CD90 on human mesenchymal stromal cells (MSCs) is associated with a loss of immunosuppressive activity by MSCs. Cytometry Part B Clin Cytom 2009;76:225–230.
30. Verleden SE, Ruttens D, Vandermeulen E et al. Elevated bronchoalveolar lavage eosinophilia correlates with poor outcome after lung transplantation. Transplantation 2014;97:83–89.
31. Selman M, Pardo A. Idiopathic pulmonary fibrosis: An epithelial/fibroblastic cross-talk disorder. Respir Res 2002;3:3.
32. Chambers DC. In the end it's a replication problem: What measuring telomere length can tell us about idiopathic pulmonary fibrosis. Respirology 2015;20:855–856.
33. Badri L, Murray S, Liu LX et al. Mesenchymal stromal cells in bronchoalveolar lavage as predictors of bronchiolitis obliterans syndrome. Am J Respir Crit Care Med 2011;183:1062–1070.
34. Ahmad T, Mukherjee S, Pattnaik B et al. Miro1 regulates intercellular mitochondrial transport & enhances mesenchymal stem cell rescue efficacy. EMBO J 2014;33:994–1010.
35. Li X, Zhang Y, Yeung SC et al. Mitochondrial transfer of induced pluripotent stem cell-derived mesenchymal stem cells to airway epithelial cells attenuates cigarette smoke-induced damage. Am J Respir Cell Mol Biol 2014;51:455–465.
36. Spees JL, Olson SD, Ylostalo J et al. Differentiation, cell fusion, and nuclear fusion during ex vivo repair of epithelium by human adult stem cells from bone marrow stroma. Proc Natl Acad Sci USA 2003;100:2397–2402.
37. Zhu YG, Feng XM, Abbott J et al. Human mesenchymal stem cell microvesicles for treatment of Escherichia coli endotoxin-induced acute lung injury in mice. Stem Cells 2014;32:116–125.
38. Bruno S, Grange C, Deregibus MC et al. Mesenchymal stem cell-derived microvesicles protect against acute tubular injury. J Am Soc Nephrol JASN 2009;20:1053–1067.
39. Bruno S, Grange C, Collino F et al. Microvesicles derived from mesenchymal stem cells enhance survival in a lethal model of acute kidney injury. PloS one 2012;7:e33115.
40. He J, Wang Y, Lu X et al. Micro-vesicles derived from bone marrow stem cells protect the kidney both in vivo and in vitro by microRNA-dependent repairing. Nephrology 2015;20:591–600.
41. Bergmann M, Tiroke A, Schafer H et al. Gene expression of profibrotic mediators in bronchiolitis obliterans syndrome after lung transplantation. Scand Cardiovasc J SCJ 1998;32:97–103.
42. El-Gamel A, Awad MR, Hasleton PS et al. Transforming growth factor-beta (TGF-beta1) genotype and lung allograft fibrosis. J Heart Lung Transplant 1999;18:517–523.
43. El-Gamel A, Sim E, Hasleton P et al. Transforming growth factor beta (TGF-beta) and obliterative bronchiolitis following pulmonary transplantation. The Journal of heart and lung transplantation 1999;18:828–837.
44. Desmouliere A, Geinoz A, Gabbiani F et al. Transforming growth factor-beta 1 induces alpha-smooth muscle actin expression in granulation tissue myofibroblasts and in quiescent and growing cultured fibroblasts. J Cell Biol 1993;122:103–111.
45. Midgley AC, Rogers M, Hallett MB et al. Transforming growth factor-beta1 (TGF-beta1)-stimulated fibroblast to myofibroblast differentiation is mediated by hyaluronan (HA)-facilitated epidermal growth factor receptor (EGFR) and CD44 co-localization in lipid rafts. J Biol Chem 2013;288:14824–14838.
46. Walker N, Badri L, Wettlaufer S et al. Resident tissue-specific mesenchymal progenitor cells contribute to fibrogenesis in human lung allografts. Am J Pathol 2011;178:2461–2469.
47. Sworder BJ, Yoshizawa S, Mishra PJ et al. Molecular profile of clonal strains of human skeletal stem/progenitor cells with different potencies. Stem Cell Res 2015;14:297–306.
48. Reger RL, Prockop DJ. Should publications on mesenchymal stem/progenitor cells include in-process data on the preparation of the cells? Stem Cells Transl Med 2014;3:632–635.