Role of Stem Cells in the Pathogenesis of Chronic Obstructive Pulmonary Disease and Pulmonary Emphysema

References

• Global Initiative for Chronic Obstructive Lung Disease. Global Strategy for the Diagnosis, Management and Prevention of Chronic Obstructive Pulmonary Disease. Latest update 2018;1–123. goldcopd.org.
   Google Scholar
• GBD 2015 Chronic Respiratory Disease Collaborators. Global, regional, and national deaths, prevalence, disability-adjusted life years, and years lived with disability for chronic obstructive pulmonary disease and asthma, 1990–2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet Respir Med. 2017;5(9):691–706. doi:10.1016/S2213-2600(17)30293-X.
   PubMed Web of Science ®Google Scholar
• Caramori G, Casolari P, Barczyk A, Durham AL, Di Stefano A, Adcock I. COPD immunopathology. Semin Immunopathol. 2016;38(4):497–515. doi:10.1007/s00281-016-0561-5.
   PubMed Web of Science ®Google Scholar
• Kajstura J, Rota M, Hall SR, Hosoda T, D’Amario D, Sanada F, Zheng H, Ogórek B, Rondon-Clavo C, Ferreira-Martins J, et al. Evidence for human lung stem cells. N Engl J Med. 2011;364(19):1795–1806. doi:10.1056/NEJMoa1101324.
   PubMed Web of Science ®Google Scholar
• Sueblinvong V, Weiss DJ. Stem cells and cell therapy approaches in lung biology and diseases. Transl Res. 2010;156(3):188–205. doi:10.1016/j.trsl.2010.06.007.
   PubMed Web of Science ®Google Scholar
• Adachi Y, Oyaizu H, Taketani S, Minamino K, Yamaguchi K, Shultz LD, Iwasaki M, Tomita M, Suzuki Y, Nakano K, et al. Treatment and transfer of emphysema by a new bone marrow transplantation method from normal mice to Tsk mice and vice versa. Stem Cells. 2006;24(9):2071–2077. doi:10.1634/stemcells.2005-0575.
   PubMed Web of Science ®Google Scholar
• Ishizawa K, Kubo H, Yamada M, Kobayashi S, Numasaki M, Ueda S, Suzuki T, Sasaki H. Bone marrow-derived cells contribute to lung regeneration after elastase-induced pulmonary emphysema. FEBS Lett. 2004;556(1–3):249–252. doi:10.1016/S0014-5793(03)01399-1.
   PubMed Web of Science ®Google Scholar
• Spees JL, Olson SD, Ylostalo J, Lynch PJ, Smith J, Perry A, Peister A, Wang MY, Prockop DJ. 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(5):2397–402. doi:10.1073/pnas.0437997100.
   PubMed Web of Science ®Google Scholar
• Yuhgetsu H, OhnoY, Funaguchi N, Asai T, Sawada M, Takemura G, Minatoguchi S, Fujiwara H, Fujiwara T. Beneficial effects of autologous bone marrow mononuclear cell transplantation against elastase-induced emphysema in rabbits. Exp Lung Res. 2006;32(9):413–426. doi:10.1080/01902140601047633.
   PubMed Web of Science ®Google Scholar
• Zhen G, Liu H, Gu N, Zhang H, Xu Y, Zhang Z. Mesenchymal stem cells transplantation protects against rat pulmonary emphysema. Front Biosci. 2008;13:3415–3422. doi:10.2741/2936.
   PubMed Web of Science ®Google Scholar
• Bittmann I, Dose T, Baretton GB, Müller C, Schwaiblmair M, Kur F, Löhrs U. Cellular chimerism of the lung after transplantation. An interphase cytogenetic study. Am J Clin Pathol. 2001;115(4):525–533. doi:10.1309/GAFN-5MPA-LY8E-DTPQ.
   PubMed Web of Science ®Google Scholar
• Kleeberger W, Versmold A, Rothamel T, Glockner S, Bredt M, Haverich A, Lehmann U, Kreipe H. Increased chimerism of bronchial and alveolar epithelium in human lung allografts undergoing chronic injury. Am J Pathol. 2003;162(5):1487–1494. doi:10.1016/S0002-9440(10)64281-2.
   PubMed Web of Science ®Google Scholar
• Kotton DN, Ma BY, Cardoso WV, Sanderson EA, Summer RS, Williams MC, Fine A. Bone marrow-derived cells as progenitors of lung alveolar epithelium. Development. 2001;128(24):5181–5188. https://www.ncbi.nlm.nih.gov/pubmed/11748153
   PubMed Web of Science ®Google Scholar
• Kotton DN, Fabian AJ, Mulligan RC. Failure of bone marrow to reconstitute lung epithelium. Am J Respir Cell Mol Biol. 2005;33(4):328–334. doi:10.1165/rcmb.2005-0175RC.
   PubMed Web of Science ®Google Scholar
• Krause DS, Theise ND, Collector MI, Henegariu O, Hwang S, Gardner R, Neutzel S, Sharkis SJ. Multi-organ, multi-lineage engraftment by a single bone marrow-derived stem cell. Cell. 2001;105(3):369–377. doi:10.1016/S0092-8674(01)00328-2.
   PubMed Web of Science ®Google Scholar
• Lama VN, Smith L, Badri L, Flint A, Andrei AC, Murray S, Wang Z, Liao H, Toews GB, Krebsbach PH, et al. Evidence for tissue-resident mesenchymal stem cells in human adult lung from studies of transplanted allografts. J Clin Invest. 2007;117(4):989–996. doi:10.1172/JCI29713.
   PubMed Web of Science ®Google Scholar
• Schrepfer S, Deuse T, Reichenspurner H, Fischbein MP, Robbins RC, Pelletier MP. Stem cell transplantation: the lung barrier. Transplant Proc. 2007;39(2):573–576. doi:10.1016/j.transproceed.2006.12.019.
   PubMed Web of Science ®Google Scholar
• Suratt BT, Cool CD, Serls AE, Chen L, Varella-Garcia M, Shpall EJ, Brown KK, Worthen GS. Human pulmonary chimerism after hematopoietic stem cell transplantation. Am J Respir Crit Care Med. 2003;168(3):318–322. doi:10.1164/rccm.200301-145OC.
   PubMed Web of Science ®Google Scholar
• Yamada M, Kubo H, Kobayashi S, Ishizawa K, Numasaki M, Ueda S, Suzuki T, Sasaki H. Bone marrow-derived progenitor cells are important for lung repair after lipopolysaccharide-induced lung injury. J Immunol. 2004;172(2):1266–1272. https://www.ncbi.nlm.nih.gov/pubmed/14707105
   PubMed Web of Science ®Google Scholar
• Weiss DJ, Kolls JK, Ortiz LA, Panoskaltsis-Mortari A, Prockop DJ. Stem cells and cell therapies in lung biology and lung diseases. Proc Am Thorac Soc. 2008;5(5):637–667. doi:10.1513/pats.200804-037DW.
   PubMedGoogle Scholar
• Van de Laar E, Clifford M, Hasenoeder S, Kim BR, Wang D, Lee S, Paterson J, Vu NM, Waddell TK, Keshavjee S, et al. Cell surface marker profiling of human tracheal basal cells reveals distinct subpopulations, identifies MST1/MSP as a mitogenic signal, and identifies new biomarkers for lung squamous cell carcinomas. Respir Res. 2014;15:160. doi:10.1186/s12931-014-0160-8.
   PubMedGoogle Scholar
• Ghosh M, Ahmad S, Jian A, Li B, Smith RW, Helm KM, Seibold MA, Groshong SD, White CW, Reynolds SD. Human tracheobronchial basal cells. Normal versus remodeling/repairing phenotypes in vivo and in vitro. Am J Respir Cell Mol Biol. 2013;49(6):1127–1134. doi:10.1165/rcmb.2013-0049OC.
   PubMed Web of Science ®Google Scholar
• Hegab AE, Ha VL, Darmawan DO, Gilbert JL, Ooi AT, Attiga YS, Bisht B, Nickerson DW, Gomperts BN. Isolation and in vitro characterization of basal and submucosal gland duct stem/progenitor cells from human proximal airways. Stem Cells Transl Med. 2012;1(10):719–724. doi:10.5966/sctm.2012-0056.
   PubMed Web of Science ®Google Scholar
• Rock JR, Onaitis MW, Rawlins EL, Lu Y, Clark CP, Xue Y, Randell SH, Hogan BLM. Basal cells as stem cells of the mouse trachea and human airway epithelium. Proc Natl Acad Sci USA. 2009;106(31):12771–12775. doi:10.1073/pnas.0906850106.
   PubMed Web of Science ®Google Scholar
• Shaykhiev R, Zuo WL, Chao IW, Fukui T, Witover B, Brekman A, Crystal RG. EGF shifts human airway basal cell fate toward a smoking-associated airway epithelial phenotype. Proc Natl Acad Sci USA. 2013;110(29):12102–12107. doi:10.1073/pnas.1303058110.
   PubMed Web of Science ®Google Scholar
• Evans MJ, Van Winkle LS, Fanucchi MV, Plopper CG. Cellular and molecular characteristics of basal cells in airway epithelium. Exp Lung Res. 2001;27(5):401–415. doi:10.1080/01902140120740.
   PubMed Web of Science ®Google Scholar
• Nakajima M, Kawanami O, Jin E, Ghazizadeh M, Honda M, Asano G, Horiba K, Ferrans VJ. Immunohistochemical and ultrastructural studies of basal cells, clara cells and bronchiolar cuboidal cells in normal human airways. Pathol Int. 1998;48(12):944–953. doi:10.1111/j.1440-1827.1998.tb03865.x.
   PubMed Web of Science ®Google Scholar
• Daniely Y, Liao G, Dixon D, Linnoila RI, Lori A, Randell SH, Oren M, Jetten AM. Critical role of p63 in the development of a normal esophageal and tracheobronchial epithelium. Am J Physiol Cell Physiol 2004;287(1):C171–181. doi:10.1152/ajpcell.00226.2003.
   PubMed Web of Science ®Google Scholar
• Gonfloni S, Caputo V, Iannizzotto V. p63 in health and cancer. Int J Dev Biol. 2015;59(1–3):87–93. doi:10.1387/ijdb.150045sg.
   PubMed Web of Science ®Google Scholar
• Chilosi M, Doglioni C. Constitutive p63 expression in airway basal cells. A molecular target in diffuse lung diseases. Sarcoidosis Vasc Diffuse Lung Dis. 2001;18(1):23–26. https://www.ncbi.nlm.nih.gov/pubmed/?term=Constitutive+p63+expression+in+airway+basal+cells.+A+molecular+target+in+diffuse+lung+diseases
   PubMed Web of Science ®Google Scholar
• Arason AJ, Jonsdottir HR, Halldorsson S, Benediktsdottir BE, Bergthorsson JT, Ingthorsson S, Baldursson O, Sinha S, Gudjonsson T, Magnusson MK. deltaNp63 has a role in maintaining epithelial integrity in airway epithelium. PLoS One. 2014;9(2):e88683. doi:10.1371/journal.pone.0088683.
   PubMed Web of Science ®Google Scholar
• Ghosh M, Ahmad S, White CW, Reynolds SD. Transplantation of airway epithelial stem/progenitor cells: a future for cell-based therapy. Am J Respir Cell Mol Biol. 2017;56(1):1–10. doi:10.1165/rcmb.2016-0181MA.
   PubMed Web of Science ®Google Scholar
• Zuo WL, Yang J, Gomi K, Chao I, Crystal RG, Shaykhiev R. EGF-amphiregulin interplay in airway stem/progenitor cells links the pathogenesis of smoking-induced lesions in the human airway epithelium. Stem Cells. 2017;35(3):824–837. doi:10.1002/stem.2512.
   PubMed Web of Science ®Google Scholar
• Liu Q, Li H, Wang Q, Zhang Y, Wang W, Dou S, Xiao W. Increased expression of TROP2 in airway basal cells potentially contributes to airway remodeling in chronic obstructive pulmonary disease. Respir Res. 2016;17(1):159–173. doi:10.1186/s12931-016-0463-z.
   PubMedGoogle Scholar
• Shvartsur A, Bonavida B. Trop2 and its overexpression in cancers: regulation and clinical/therapeutic implications. Genes Cancer. 2015;6(3–4):84–105. doi:10.18632/genesandcancer.40.
   PubMedGoogle Scholar
• Yang J, Zuo WL, Fukui T, Chao I, Gomi K, Lee B, Staudt MR, Kaner RJ, Strulovici-Barel Y, Salit J, et al. Smoking-dependent distal-to-proximal repatterning of the adult human small airway epithelium. Am J Respir Crit Care Med. 2017;196(3):340–352. doi:10.1164/rccm.201608-1672OC.
   PubMed Web of Science ®Google Scholar
• Ghosh M, Miller YE, Nakachi I, Kwon JB, Barón AE, Brantley AE, Merrick DT, Franklin WA, Keith RL, Vandivier RW. Exhaustion of airway basal progenitor cells in early and established chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2018;197(7):885–896. doi:10.1164/rccm.201704-0667OC.
   PubMed Web of Science ®Google Scholar
• Staudt MR, Buro-Auriemma LJ, Walters MS, Salit J, Vincent T, Shaykhiev R, Mezey JG, Tilley AE, Kaner RJ, Ho MW, Crystal RG. Airway basal stem/progenitor cells have diminished capacity to regenerate airway epithelium in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2014;190(8):955–958. doi:10.1164/rccm.201406-1167LE.
   PubMed Web of Science ®Google Scholar
• Ryan DM, Vincent TL, Salit J, Walters MS, Agosto-Perez F, Shaykhiev R, Strulovici-Barel Y, Downey RJ, Buro-Auriemma LJ, Staudt MR, et al. Smoking dysregulates the human airway basal cell transcriptome at COPD risk locus 19q13.2. PLoS One. 2014;9(2):e88051. doi:10.1371/journal.pone.0088051.
   PubMed Web of Science ®Google Scholar
• Wansleeben C, Barkauskas CE, Rock JR, Hogan BL. Stem cells of the adult lung: their development and role in homeostasis, regeneration, and disease. Wiley Interdiscip Rev Dev Biol. 2013;2(1):131–148. doi:10.1002/wdev.58.
   PubMed Web of Science ®Google Scholar
• Engelhardt JF, Schlossberg H, Yankaskas JR, Dudus L. Progenitor cells of the adult human airway involved in submucosal gland development. Development. 1995;121(7):2031–2046. https://www.ncbi.nlm.nih.gov/pubmed/?term=Progenitor+cells+of+the+adult+human+airway+involved+in+submucosal+gland+development.
   PubMed Web of Science ®Google Scholar
• Swatek AM, Lynch TJ, Crooke AK, Anderson PJ, Tyler SR, Brooks L, Ivanovic M, Klesney-Tait JA, Eberlein M, Pena T, et al. Depletion of airway submucosal glands and TP63 + KRT5+ basal cells in obliterative bronchiolitis. Am J Respir Crit Care Med. 2018;197(8):1045–1057. doi:10.1164/rccm.201707-1368OC.
   PubMed Web of Science ®Google Scholar
• Kim CF, Jackson EL, Woolfenden AE, Lawrence S, Babar I, Vogel S, Crowley D, Bronson RT, Jacks T. Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell. 2005;121(6):823–835. doi:10.1016/j.cell.2005.03.032.
   PubMed Web of Science ®Google Scholar
• Driscoll B, Kikuchi A, Lau AN, Lee J, Reddy R, Jesudason E, Kim CF, Warburton D. Isolation and characterization of distal lung progenitor cells. Methods Mol Biol. 2012;879:109–122. doi:10.1007/978-1-61779-815-3_7.
   PubMedGoogle Scholar
• 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(5):L1092–1098. doi:10.1152/ajplung.00015.2007.
   PubMed Web of Science ®Google Scholar
• Kato T, Oka K, Nakamura T, Ito A. Bronchioalveolar morphogenesis of human bronchial epithelial cells depending upon hepatocyte growth factor. J Cell Mol Med. 2015;19(12):2818–2826. doi:10.1111/jcmm.12672.
   PubMed Web of Science ®Google Scholar
• Suzuki T, Suzuki S, Fujino N, Ota C, Yamada M, Suzuki T, Yamaya M, Kondo T, Kubo H. c-Kit immunoexpression delineates a putative endothelial progenitor cell population in developing human lungs. Am J Physiol Lung Cell Mol Physiol. 2014;306(9):L855–865. doi:10.1152/ajplung.00211.2013.
   PubMed Web of Science ®Google Scholar
• Lòpez-Giraldo A, Cruz T, Molins L, Guirao A, Cuerpo S, Ramirez J, Agusti A, Faner R. Characterization, localization and comparison of c-kit + lung cells in never smokers and smokers with and without COPD. BMC Pulm Med. 2018;18(1):123. doi:10.1186/s12890-018-0688-3.
   PubMedGoogle Scholar
• Foronjy RF, Majka SM. The potential for resident lung mesenchymal stem cells to promote functional tissue regeneration: understanding microenvironmental cues. Cells. 2012;1(4):874. doi:10.3390/cells1040874.
   PubMedGoogle Scholar
• Hogan B. Stemming lung disease? N Engl J Med. 2018;378(25):2439–2440. doi:10.1056/NEJMcibr1803540.
   PubMed Web of Science ®Google Scholar
• Nabhan AN, Brownfield DG, Harbury PB, Krasnow MA, Desai TJ. Single-cell Wnt signaling niches maintain stemness of alveolar type 2 cells. Science. 2018;359(6380):1118–1123. doi:10.1126/science.aam6603.
   PubMed Web of Science ®Google Scholar
• Zacharias WJ, Frank DB, Zepp JA, Morley MP1, Alkhaleel FA, Kong J, Zhou S, Cantu E, Morrisey EE. Regeneration of the lung alveolus by an evolutionarily conserved epithelial progenitor. Nature. 2018;555(7695):251–255. doi:10.1038/nature25786.
   PubMed Web of Science ®Google Scholar
• Chen R, Zhang K, Chen H, Zhao X, Wang J, Li L, Cong Y, Ju Z, Xu D, Williams BR, et al. Telomerase deficiency causes alveolar stem cell senescence-associated low-grade inflammation in lungs. J Biol Chem. 2015;290(52):30813–30829. doi:10.1074/jbc.M115.681619.
   PubMed Web of Science ®Google Scholar
• Fujino N, Kubo H, Suzuki T, Ota C, Hegab AE, He M, Suzuki S, Suzuki T, Yamada M, Kondo T, et al. Isolation of alveolar epithelial type II progenitor cells from adult human lungs. Lab Invest. 2011;91(3):363–378. doi:10.1038/labinvest.2010.187.
   PubMed Web of Science ®Google Scholar
• Horiguchi M, Kojima H, Sakai H, Kubo H, Yamashita C. Pulmonary administration of integrin-nanoparticles regenerates collapsed alveoli. J Control Release. 2014;187:167–174. doi:10.1016/j.jconrel.2014.05.050.
   PubMed Web of Science ®Google Scholar
• Sakai H, Horiguchi M, Ozawa C, Akita T, Hirota K, Shudo K, Terada H, Makino K, Kubo H, Yamashita C. Pulmonary administration of Am80 regenerates collapsed alveoli. J Control Release. 2014;196:154–160. doi:10.1016/j.jconrel.2014.10.004.
   PubMed Web of Science ®Google Scholar
• Horiguchi M, Oiso Y, Sakai H, Motomura T, Yamashita C. Pulmonary administration of phosphoinositide 3-kinase inhibitor is a curative treatment for chronic obstructive pulmonary disease by alveolar regeneration. J Control Release. 2015;213:112–119. doi:10.1016/j.jconrel.2015.07.004.
   PubMed Web of Science ®Google Scholar
• Fadini GP, Schiavon M, Cantini M, Baesso I, Facco M, Miorin M, Tassinato M, de Kreutzenberg S, Avogaro A, Agostini C. Circulating progenitor cells are reduced in patients with severe lung disease. Stem Cells. 2006;24(7):1806–1813. doi:10.1634/stemcells.2005-0440.
   PubMed Web of Science ®Google Scholar
• Huertas A, Testa U, Riccioni R, Petrucci E, Riti V, Savi D, Serra P, Bonsignore MR, Palange P. Bone marrow-derived progenitors are greatly reduced in patients with severe COPD and low-BMI. Respir Physiol Neurobiol. 2010;170(1):23–31. doi:10.1016/j.resp.2009.10.003.
   PubMed Web of Science ®Google Scholar
• Palange P, Testa U, Huertas A, Calabrò L, Antonucci R, Petrucci E, Pelosi E, Pasquini L, Satta A, Morici G, et al. Circulating haemopoietic and endothelial progenitor cells are decreased in COPD. Eur Respir J. 2006;27(3):529–541. doi:10.1183/09031936.06.00120604.
   PubMed Web of Science ®Google Scholar
• Liu Y, Liu X, Lin G, Sun L, Li H, Xie C. Decreased CD34+ cell number is correlated with cardiac dysfunction in patients with acute exacerbation of COPD. Heart Lung Circ. 2014;23(9):875–882. doi:10.1016/j.hlc.2014.03.008.
   PubMed Web of Science ®Google Scholar
• Pizarro S, García-Lucio J, Peinado VI, Tura-Ceide O, Díez M, Blanco I, Sitges M, Petriz J, Torralba Y, Marín P, et al. Circulating progenitor cells and vascular dysfunction in chronic obstructive pulmonary disease. PLoS One. 2014;9(8):e106163. doi:10.1371/journal.pone.0106163.
   PubMed Web of Science ®Google Scholar
• Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop Dj, Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The international society for cellular therapy position statement. Cytotherapy. 2006;8(4):315–317. doi:10.1080/14653240600855905.
   PubMed Web of Science ®Google Scholar
• Singer NG, Caplan AI. Mesenchymal stem cells: mechanisms of inflammation. Annu Rev Pathol. 2011;6:457–478. doi:10.1146/annurev-pathol-011110-130230.
   PubMed Web of Science ®Google Scholar
• Beier JP, Bitto FF, Lange C, Klumpp D, Arkudas A, Bleiziffer O, Boos AM, Horch RE, Kneser U. Myogenic differentiation of mesenchymal stem cells co-cultured with primary myoblasts. Cell Biol Int. 2011;35(4):397–406. doi:10.1042/CBI20100417.
   PubMed Web of Science ®Google Scholar
• Ricciardi M, Malpeli G, Bifari F, Bassi G, Pacelli L, Nwabo Kamdje AH, Chilosi M, Krampera M. Comparison of epithelial differentiation and immune regulatory properties of mesenchymal stromal cells derived from human lung and bone marrow. PLoS One 2012;7(5):e35639. doi:10.1371/journal.pone.0035639.
   PubMed Web of Science ®Google Scholar
• Sinclair KA, Yerkovich ST, Chen T, McQualter JL, Hopkins PM, Wells CA, Chambers DC. Mesenchymal stromal cells are readily recoverable from lung tissue, but not the alveolar space, in healthy humans. Stem Cells. 2016;34(10):2548–2558. doi:10.1002/stem.2419.
   PubMed Web of Science ®Google Scholar
• Walker N, Badri L, Wettlaufer S, Flint A, Sajjan U, Krebsbach PH, Keshamouni VG, Peters-Golden M, Lama VN. Resident tissue-specific mesenchymal progenitor cells contribute to fibrogenesis in human lung allografts. Am J Pathol. 2011;178(6):2461–2469. doi:10.1016/j.ajpath.2011.01.058.
   PubMed Web of Science ®Google Scholar
• Badri L, Murray S, Liu LX, Walker NM, Flint A, Wadhwa A, Chan KM, Toews GB, Pinsky DJ, Martinez FJ, et al. Mesenchymal stromal cells in bronchoalveolar lavage as predictors of bronchiolitis obliterans syndrome. Am J Respir Crit Care Med. 2011;183(8):1062–1070. doi:10.1164/rccm.201005-0742OC.
   PubMed Web of Science ®Google Scholar
• Nejad-Moghaddam A, Panahi Y, Abdollahpour Alitappeh M, Borna H, Shokrgozar MA, Ghanei M. Therapeutic potential of mesenchymal stem cells for the treatment of airway remodeling in pulmonary diseases. Iran J Allergy Asthma Immunol. 2015;14(6):552–568. https://www.ncbi.nlm.nih.gov/pubmed/26725553
   PubMed Web of Science ®Google Scholar
• Hocking AM. The role of chemokines in mesenchymal stem cell homing to wounds. Adv Wound Care (New Rochelle). 2015;4(11):623–630. doi:10.1089/wound.2014.0579.
   PubMed Web of Science ®Google Scholar
• Kruk DMLW, Heijink IH, Slebos DJ, Timens W, Ten Hacken NH. Mesenchymal stromal cells to regenerate emphysema: on the horizon? Respiration. 2018: 96(2):148–158. doi:10.1159/000488149.
   Google Scholar
• 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(2):323–335. doi:10.1002/jcb.24377.
   PubMed Web of Science ®Google Scholar
• Skurikhin EG, Pakhomova AV, Krupin VA, Pershina OV, Pan ES, Ermolaeva LA, Vaizova OE, Rybalkina OY, Dygai AM. Response of inflammatory mediators, extracellular matrix proteins and stem and progenitor cells to emphysema. Bull Exp Biol Med. 2016;161(4):566–570. doi:10.1007/s10517-016-3462-7.
   PubMed Web of Science ®Google Scholar
• Cappetta D, De Angelis A, Spaziano G, Tartaglione G, Piegari E, Esposito G, Ciuffreda LP, Liparulo A, Sgambato M, Russo TP, et al. Lung mesenchymal stem cells ameliorate elastase-induced damage in an animal model of emphysema. Stem Cells Int. 2018;2018:9492038. doi:10.1155/2018/9492038.
   PubMedGoogle Scholar
• Katsha AM1, Ohkouchi S, Xin H, Kanehira M, Sun R, Nukiwa T, Saijo Y. Paracrine factors of multipotent stromal cells ameliorate lung injury in an elastase-induced emphysema model. Mol Ther. 2011;19(1):196–203. doi:10.1038/mt.2010.192.
   PubMed Web of Science ®Google Scholar
• Liu X, Fang Q, Kim H. Preclinical studies of mesenchymal stem cell (MSC) administration in chronic obstructive pulmonary disease (COPD): a systematic review and meta-analysis. PLoS One. 2016;11(6):e0157099. doi:10.1371/journal.pone.0157099.
   PubMed Web of Science ®Google Scholar
• Jin Z, Pan X, Zhou K, Bi H, Wang L, Yu L, Wang Q. Biological effects and mechanisms of action of mesenchymal stem cell therapy in chronic obstructive pulmonary disease. J Int Med Res. 2015;43(3):303–310. doi:10.1177/0300060514568733.
   PubMed Web of Science ®Google Scholar
• Gu W, Song L, Li XM, Wang D, Guo XJ, Xu WG. Mesenchymal stem cells alleviate airway inflammation and emphysema in COPD through down-regulation of cyclooxygenase-2 via p38 and ERK MAPK pathways. Sci Rep. 2015;5:8733. doi:10.1038/srep08733.
   PubMed Web of Science ®Google Scholar
• Karagiannis K, Proklou A, Tsitoura E, Lasithiotaki I, Kalpadaki C, Moraitaki D, Sperelakis I, Kontakis G, Antoniou KM, Tzanakis N. Impaired mRNA expression of the migration related chemokine receptor CXCR4 in mesenchymal stem cells of COPD Patients. Int J Inflam. 2017;2017:6089425. doi:10.1155/2017/6089425.
   PubMedGoogle Scholar
• Broekman W, Roelofs H, Zarcone MC, Taube C, Stolk J, Hiemstra PS. Functional characterisation of bone marrow-derived mesenchymal stromal cells from COPD patients. ERJ Open Res. 2016;2(2): pii: 00045–2015. doi:10.1183/23120541.00045-2015.
   Google Scholar
• Figeac F, Dagouassat M, Mahrouf-Yorgov M, Le Gouvello S, Trébeau C, Sayed A, Stern JB, Validire P, Dubois-Randé JL, Boczkowski J, et al. Lung fibroblasts share mesenchymal stem cell features which are altered in chronic obstructive pulmonary disease via the overactivation of the Hedgehog signaling pathway. PLoS One. 2015;10(3):e0121579. doi:10.1371/journal.pone.0121579.
   PubMed Web of Science ®Google Scholar
• Bi W, Deng JM, Zhang Z, Behringer RR, de Crombrugghe B. Sox9 is required for cartilage formation. Nat Genet. 1999;22(1):85–89. doi:10.1038/8792.
   PubMed Web of Science ®Google Scholar
• Tontonoz P, Hu E, Graves RA, Budavari AI, Spiegelman BM. mPPAR gamma 2: tissue-specific regulator of an adipocyte enhancer. Genes Dev. 1994;8(10):1224–1234. doi:10.1101/gad.8.10.1224.
   PubMed Web of Science ®Google Scholar
• Watanabe H, Tsuchiya T, Shimoyama K, Shimizu A, Akita S, Yukawa H, Baba Y, Nagayasu T. Adipose-derived mesenchymal stem cells attenuate rejection in a rat lung transplantation model. J Surg Res. 2018;227:17–27. doi:10.1016/j.jss.2018.01.016.
   PubMed Web of Science ®Google Scholar
• Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, Benhaim P, Lorenz HP, Hedrick MH. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng. 2001;7(2):211–228. doi:10.1089/107632701300062859.
   PubMedGoogle Scholar
• Ra JC, Shin IS, Kim SH, Kang SK, Kang BC, Lee HY, Kim YJ, Jo JY, Yoon EJ, Choi HJ, et al. Safety of intravenous infusion of human adipose tissue-derived mesenchymal stem cells in animals and humans. Stem Cells Dev. 2011;20(8):1297–308. doi:10.1089/scd.2010.0466.
   PubMed Web of Science ®Google Scholar
• Kern S, Eichler H, Stoeve J, Klüter H, Bieback K. Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells. 2006;24(5):1294–1301. doi:10.1634/stemcells.2005-0342.
   PubMed Web of Science ®Google Scholar
• Fotia C, Massa A, Boriani F, Baldini N, Granchi D. Hypoxia enhances proliferation and stemness of human adipose-derived mesenchymal stem cells. Cytotechnology. 2015;67(6):1073–1084. doi:10.1007/s10616-014-9731-2.
   PubMed Web of Science ®Google Scholar
• Melief SM, Zwaginga JJ, Fibbe WE, Roelofs H. Adipose tissue-derived multipotent stromal cells have a higher immunomodulatory capacity than their bone marrow-derived counterparts. Stem Cells Transl Med. 2013;2(6):455–463. doi:10.5966/sctm.2012-0184.
   PubMed Web of Science ®Google Scholar
• Strioga M, Viswanathan S, Darinskas A, Slaby O, Michalek J. Same or not the same? Comparison of adipose tissue-derived versus bone marrow-derived mesenchymal stem and stromal cells. Stem Cells Dev. 2012;21(14):2724–2752. doi:10.1089/scd.2011.0722.
   PubMed Web of Science ®Google Scholar
• Cho RJ, Kim YS, Kim JY, Oh YM. Human adipose-derived mesenchymal stem cell spheroids improve recovery in a mouse model of elastase-induced emphysema. BMB Rep. 2017;50(2):79–84. doi:10.5483/BMBRep.2017.50.2.101.
   PubMed Web of Science ®Google Scholar
• Kim YS, Kim JY, Shin DM, Huh JW, Lee SW, Oh YM. Tracking intravenous adipose-derived mesenchymal stem cells in a model of elastase-induced emphysema. Tuberc Respir Dis. 2014;77(3):116–123. doi:10.4046/trd.2014.77.3.116.
   PubMedGoogle Scholar
• Shigemura N, Okumura M, Mizuno S, Imanishi Y, Nakamura T, Sawa Y. Autologous transplantation of adipose tissue-derived stromal cells ameliorates pulmonary emphysema. Am J Transplant. 2006;6(11):2592–2600. doi:10.1111/j.1600-6143.2006.01522.x.
   PubMed Web of Science ®Google Scholar
• Hong Y, Kim YS, Hong SH, Oh YM. Therapeutic effects of adipose-derived stem cells pretreated with pioglitazone in an emphysema mouse model. Exp Mol Med. 2016;48(10):e266. doi:10.1038/emm.2016.93.
   PubMed Web of Science ®Google Scholar
• Schweitzer KS, Johnstone BH, Garrison J, Rush NI, Cooper S, Traktuev DO, Feng D, Adamowicz JJ, Van Demark M, Fisher AJ, et al. Adipose stem cell treatment in mice attenuates lung and systemic injury induced by cigarette smoking. Am J Respir Crit Care Med. 2011;183(2):215–225. doi:10.1164/rccm.201001-0126OC.
   PubMed Web of Science ®Google Scholar
• Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, Isner JM. Isolation of putative progenitor endothelial cells for angiogenesis. Science. 1997;275(5302):964–967. doi:10.1126/science.275.5302.964.
   PubMed Web of Science ®Google Scholar
• Hristov M, Erl W, Weber PC. Endothelial progenitor cells: mobilization, differentiation, and homing. Arterioscler Thromb Vasc Biol. 2003;23(7):1185–1189. doi:10.1161/01.ATV.0000073832.49290.B5.
   PubMed Web of Science ®Google Scholar
• Khakoo AY, Finkel T. Endothelial progenitor cells. Annu Rev Med. 2005;56:79–101. doi:10.1146/annurev.med.56.090203.104149.
   PubMed Web of Science ®Google Scholar
• Mund JA, Case J. The ontogeny of endothelial progenitor cells through flow cytometry. Curr Opin Hematol. 2011;18(3):166–170. doi:10.1097/MOH.0b013e328345a16a.
   PubMed Web of Science ®Google Scholar
• Mund JA, Estes ML, Yoder MC, Ingram DA Jr, Case J. Flow cytometric identification and functional characterization of immature and mature circulating endothelial cells. Arterioscler Thromb Vasc Biol. 2012;32(4):1045–1053. doi:10.1161/ATVBAHA.111.244210.
   PubMed Web of Science ®Google Scholar
• Estes ML, Mund JA, Ingram DA, Case J. Identification of endothelial cells and progenitor cell subsets in human peripheral blood. Curr Protoc Cytom. 2010;9:1–11. doi:10.1002/0471142956.cy0933s52.
   Google Scholar
• Schmidt-Lucke C, Fichtlscherer S, Aicher A, Tschöpe C, Schultheiss HP, Zeiher AM, Dimmeler S. Quantification of circulating endothelial progenitor cells using the modified ISHAGE protocol. PLoS One. 2010;5(11):e13790. doi:10.1371/journal.pone.0013790.
   PubMed Web of Science ®Google Scholar
• Yang Y, Gan Y, Cao J, Chen Y, He ZH, Luo H, Cai S, Xiang XD, Zhou R, Chen P. Decreased and dysfunctional circulating endothelial progenitor cells in patients with chronic obstructive pulmonary disease. Chin Med J. 2013;126(17):3222–3227.
   PubMed Web of Science ®Google Scholar
• Paschalaki KE, Starke RD, Hu Y, Mercado N, Margariti A, Gorgoulis VG, Randi AM, Barnes PJ. Dysfunction of endothelial progenitor cells from smokers and chronic obstructive pulmonary disease patients due to increased DNA damage and senescence. Stem Cells. 2013;31(12):2813–2826. doi:10.1002/stem.1488.
   PubMed Web of Science ®Google Scholar
• Tilling L, Chowienczyk P, Clapp B. Progenitors in motion: mechanisms of mobilization of endothelial progenitor cells. Br J Clin Pharmacol. 2009;68(4): 484–492. doi:10.1111/j.1365-2125.2009.03486.x.
   PubMed Web of Science ®Google Scholar
• Werner N, Kosiol S, Schiegl T, Ahlers P, Walenta K, Link A, Bohm M, Nickenig G. Circulating endothelial progenitor cells and cardiovascular outcomes. N Engl J Med. 2005;353(10):999–1007. doi:10.1056/NEJMoa043814.
   PubMed Web of Science ®Google Scholar
• Hill JM, Zalos G, Halcox JP, Schenke WH, Waclawiw MA, Quyyumi AA, Finkel T. Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N Engl J Med. 2003;348(7):593–600. doi:10.1056/NEJMoa022287.
   PubMed Web of Science ®Google Scholar
• Samman TA, Hammadah M1, Sandesara PB, Hayek SS, Kalogeropoulos AP, Alkhoder A, Mohamed Kelli H, Topel M, Ghasemzadeh N, Chivukula K, et al. Progenitor cells and clinical outcomes in patients with heart failure. Circ Heart Fail. 2017;10(8). pii: e004106. doi:10.1161/CIRCHEARTFAILURE.117.004106.
   Web of Science ®Google Scholar
• Dimmeler S, Aicher A, Vasa M, Mildner-Rihm C, Adler K, Tiemann M, Rütten H, Fichtlscherer S, Martin H, Zeiher AM. HMG-CoA reductase inhibitors (statins) increase endothelial progenitor cells via the PI 3-kinase/Akt pathway. J Clin Invest. 2001;108(3):391–397. doi:10.1172/JCI13152.
   PubMed Web of Science ®Google Scholar
• Chen C, Yang S, Feng Y, Wu X, Chen D, Yu Q, Wang X, Li J, Chen J. Impairment of two types of circulating endothelial progenitor cells in patients with glucocorticoid-induced avascular osteonecrosis of the femoral head. Joint Bone Spine. 2013;80(1):70–76. doi:10.1016/j.jbspin.2012.02.015.
   PubMed Web of Science ®Google Scholar
• Peplow PV. Growth factor- and cytokine-stimulated endothelial progenitor cells in post-ischemic cerebral neovascularization. Neural Regen Res. 2014;9(15):1425–1429. doi:10.4103/1673-5374.139457.
   PubMed Web of Science ®Google Scholar
• Maltais S, Perrault LP, Ly HQ. The bone marrow-cardiac axis: role of endothelial progenitor cells in heart failure. Eur J Cardiothorac Surg. 2011;39(3):368–374. doi:10.1016/j.ejcts.2010.04.022.
   PubMed Web of Science ®Google Scholar
• Kasahara Y, Tuder RM, Taraserviciene-Stewart L, Le Cras TD, Abman S, Hirth PK, Waltenberg J, Voelkel NF. Inhibition of VEGF receptors causes lung cell apoptosis and emphysema. J Clin Invest. 2000;106(11):1311–1319. doi:10.1172/JCI10259.
   PubMed Web of Science ®Google Scholar
• Kasahara Y, Tuder RM, Cool CD, Lynch DA, Flores SC, Voelkel NF. Endothelial cell death and decreased expression of vascular endothelial growth factor and vascular endothelial growth factor receptor 2 in emphysema. Am J Respir Crit Care Med. 2001;163(3 Pt 1):737–744. doi:10.1164/ajrccm.163.3.2002117.
   PubMed Web of Science ®Google Scholar
• Caramori G, Casolari P, Giuffrè S, Barczyk A, Adcock I, Papi A. COPD pathology in the small airways. Panminerva Med. 2011;53(1):51–70. https://www.ncbi.nlm.nih.gov/pubmed/?term=Caramori+G%2C+Casolari+P%2C+Giuffr%C3%A8+S%2C+Barczyk+A%2C+Adcock+I%2C+Papi+A.+COPD+pathology+in+the+small+airways
   PubMed Web of Science ®Google Scholar
• Sala E, Villena C, Balaguer C, Ríos A, Fernández-Palomeque C, Cosío BG, García J, Noguera A, Agustí A. Abnormal levels of circulating endothelial progenitor cells during exacerbations of COPD. Lung. 2010;188(4):331–338. doi:10.1007/s00408-009-9225-8.
   PubMed Web of Science ®Google Scholar
• Liu P, Zhang H, Liu J, Sheng C, Zhang L, Zeng Y. Changes of number and function of late endothelial progenitor cells in peripheral blood of COPD patients combined with pulmonary hypertension. Thorac Cardiovasc Surg. 2016;64(4):323–329. doi:10.1055/s-0034-1389261.
   PubMed Web of Science ®Google Scholar
• 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(6):554–555. doi:10.1136/thx.2009.121640.
   PubMed Web of Science ®Google Scholar
• Peinado VI, Ramìrez J, Roca J, Rodriguez-Roisin R, Barberà JA. Identification of vascular progenitor cells in pulmonary arteries of patients with chronic obstructive pulmonary disease. Am J Respir Cell Mol Biol. 2006;34(3): 257–263. doi:10.1165/rcmb.2005-0255OC.
   PubMed Web of Science ®Google Scholar
• Brittan M, Hoogenboom MM, Padfield GJ, Tura O, Fujisawa T, Maclay JD, Macnee W, Mills NL. Endothelial progenitor cells in patients with chronic obstructive pulmonary disease. Am J Physiol Lung Cell Mol Physiol. 2013;305(12):964–969. doi:10.1152/ajplung.00183.2013.
   Web of Science ®Google Scholar
• Janssen WJ, Yunt ZX, Muldrow A, Kearns MT, Kloepfer A, Barthel L, Bratton DL, Bowler RP, Henson PM. Circulating hematopoietic progenitor cells are decreased in COPD. COPD. 2014;11(3):277–289. doi:10.3109/15412555.2013.841668.
   PubMedGoogle Scholar
• Doyle MF, Tracy RP, Parikh MA, Hoffman EA, Shimbo D, Austin JH, Smith BM, Hueper K, Vogel-Claussen J, Lima J, et al. Endothelial progenitor cells in chronic obstructive pulmonary disease and emphysema. PLoS One. 2017;12(3):e0173446. doi:10.1371/journal.pone.0173446.
   PubMed Web of Science ®Google Scholar
• Takahashi T, Suzuki S, Kubo H, Yamaya M, Kurosawa S, Kato M. Impaired endothelial progenitor cell mobilization and colony-forming capacity in chronic obstructive pulmonary disease. Respirology. 2011;16(4):680–687. doi:10.1111/j.1440-1843.2011.01959.x.
   PubMed Web of Science ®Google Scholar
• Liu X, Xie C. Human endothelial progenitor cells isolated from COPD patients are dysfunctional. Mol Cell Biochem. 2012;363(1–2):53–63. doi:10.1007/s11010-011-1157-y.
   PubMed Web of Science ®Google Scholar
• Salter BM, Manzoor F, Beaudin S, Kjarsgaard M, Nair P, Gauvreau GM, Sehmi R. Dysregulation of vascular endothelial progenitor cells lung-homing in subjects with COPD. Can Respir J. 2016;2016:1472823. doi:10.1155/2016/1472823.
   PubMedGoogle Scholar
• Kim EK, Lee JH, Jeong HC, Oh D, Hwang SG, Cho YW, Lee SJ, Oh YM, Lee SD. Impaired colony-forming capacity of circulating endothelial progenitor cells in patients with emphysema. Tohoku J Exp Med. 2012;227(4):321–331. doi:10.1620/tjem.227.321.
   PubMed Web of Science ®Google Scholar
• Herzog EL, Bucala R. Fibrocytes in health and disease. Exp Hematol. 2010;38(7):548–556. doi:10.1016/j.exphem.2010.03.004.
   PubMed Web of Science ®Google Scholar
• Dupin I, Allard B, Ozier A, Maurat E, Ousova O, Delbrel E, Trian T, Bui HN, Dromer C, Guisset O, et al. Blood fibrocytes are recruited during acute exacerbations of chronic obstructive pulmonary disease through a CXCR4-dependent pathway. J Allergy Clin Immunol. 2016;137(4):1036–1042. doi:10.1016/j.jaci.2015.08.043.
   PubMed Web of Science ®Google Scholar
• Keeley EC, Mehrad B, and Strieter RM. Fibrocytes: bringing new insights into mechanisms of inflammation and fibrosis. Int J Biochem Cell Biol. 2010;42(4):535–542. doi:10.1016/j.biocel.2009.10.014.
   PubMed Web of Science ®Google Scholar
• Bucala R. Fibrocytes at 20 years. Mol Med. 2015;21:3–5. doi:10.2119/molmed.2015.00043.
   Web of Science ®Google Scholar
• Peng H, Herzog E. Fibrocytes: emerging effector cells in chronic inflammation. Curr Opin Pharmacol. 2012;12(4):491–496. doi:10.1016/j.coph.2012.03.002.
   PubMed Web of Science ®Google Scholar
• Florez-Sampedro L, Song S, Melgert BN. The diversity of myeloid immune cells shaping wound repair and fibrosis in the lung. Regeneration (Oxf). 2018;5(1):3–25. doi:10.1002/reg2.97.
   PubMed Web of Science ®Google Scholar
• Bucala R. Review series-Inflammation & fibrosis. Fibrocytes and fibrosis. QJM. 2012;105(6):505–508. doi:10.1093/qjmed/hcs068.
   PubMed Web of Science ®Google Scholar
• Wright AK, Newby C, Hartley RA, Mistry V, Gupta S, Berair R, Roach KM, Saunders R, Thornton T, Shelley M, et al. Myeloid-derived suppressor cell-like fibrocytes are increased and associated with preserved lung function in chronic obstructive pulmonary disease. Allergy. 2017;72(4):645–655. doi:10.1111/all.13061.
   PubMed Web of Science ®Google Scholar
• Yin H, Price F, Rudnicki MA. Satellite cells and the muscle stem cell niche. Physiol Rev. 2013;93(1):23–67. doi:10.1152/physrev.00043.2011.
   PubMed Web of Science ®Google Scholar
• Lindström M, Thornell LE. New multiple labelling method for improved satellite cell identification in human muscle: application to a cohort of power-lifters and sedentary men. Histochem Cell Biol. 2009;132(2):141–157. doi:10.1007/s00418-009-0606-0.
   PubMed Web of Science ®Google Scholar
• Thériault ME, Paré MÈ, Lemire BB, Maltais F, Debigaré R. Regenerative defect in vastus lateralis muscle of patients with chronic obstructive pulmonary disease. Respir Res. 2014;15:35. doi:10.1186/1465-9921-15-35.
   PubMed Web of Science ®Google Scholar
• Menon MK, Houchen L, Singh SJ, Morgan MD, Bradding P, Steiner MC. Inflammatory and satellite cells in the quadriceps of patients with COPD and response to resistance training. Chest. 2012;142(5):1134–1142. doi:10.1378/chest.11-2144.
   PubMed Web of Science ®Google Scholar
• Thériault ME, Paré MÈ, Maltais F, Debigaré R. Satellite cells senescence in limb muscle of severe patients with COPD. PLoS One. 2012;7(6):e39124. doi:10.1371/journal.pone.0039124.
   PubMed Web of Science ®Google Scholar
• Pomiès P, Rodriguez J, Blaquière M, Sedraoui S, Gouzi F, Carnac G, Laoudj-Chenivesse D, Mercier J, Préfaut C, Hayot M. Reduced myotube diameter, atrophic signalling and elevated oxidative stress in cultured satellite cells from COPD patients. J Cell Mol Med. 2015;19(1):175–186. doi:10.1111/jcmm.12390.
   PubMed Web of Science ®Google Scholar
• Gouzi F, Blaquière M, Catteau M, Bughin F, Maury J, Passerieux E, Ayoub B, Mercier J, Hayot M, Pomiès P. Oxidative stress regulates autophagy in cultured muscle cells of patients with chronic obstructive pulmonary disease. J Cell Physiol. 2018; 233(12):9629–9639. doi:10.1002/jcp.26868.
   PubMed Web of Science ®Google Scholar
• Sovalat H, Scrofani M, Eidenschenk A, Pasquet S, Rimelen V, Hénon P. Identification and isolation from either adult human bone marrow or G-CSF-mobilized peripheral blood of CD34(+)/CD133(+)/CXCR4(+)/ Lin(-)CD45(-) cells, featuring morphological, molecular, and phenotypic characteristics of very small embryonic-like (VSEL) stem cells. Exp Hematol. 2011;39(4):495–505. doi:10.1016/j.exphem.2011.01.003.
   PubMed Web of Science ®Google Scholar
• Havens AM, Sun H, Shiozawa Y, Jung Y, Wang J, Mishra A, Jiang Y, O’Neill DW, Krebsbach PH, Rodgerson DO, et al. Human and murine very small embryonic-like cells represent multipotent tissue progenitors, in vitro and in vivo. Stem Cells Dev. 2014;23(7):689–701. doi:10.1089/scd.2013.0362.
   PubMed Web of Science ®Google Scholar
• Guerin CL, Blandinières A, Planquette B, Silvestre JS, Israel-Biet D, Sanchez O, Smadja DM. Very small embryonic-like stem cells are mobilized in human peripheral blood during hypoxemic COPD exacerbations and pulmonary hypertension. Stem Cell Rev. 2017;13(4):561–566. doi:10.1007/s12015-017-9732-6.
   PubMed Web of Science ®Google Scholar
• Caramori G, Casolari P, Cavallesco GN, Giuffrè S, Adcock I, Papi A. Mechanisms involved in lung cancer development in COPD. Int J Biochem Cell Biol. 2011;43:1030–1044. doi:10.1016/j.biocel.2010.08.022.
   PubMed Web of Science ®Google Scholar
• Teisanu RM, Lagasse E, Whitesides JF, Stripp BR. Prospective isolation of bronchiolar stem cells based upon immunophenotypic and autofluorescence characteristics. Stem Cells. 2009;27(3):612–622. doi:10.1634/stemcells.2008-0838.
   PubMed Web of Science ®Google Scholar
• Regala RP, Davis RK, Kunz A, Khoor A, Leitges M, Fields AP. Atypical protein kinase C{iota} is required for bronchioalveolar stem cell expansion and lung tumorigenesis. Cancer Res. 2009;69(19):7603–7611. doi:10.1158/0008-5472.CAN-09-2066.
   PubMed Web of Science ®Google Scholar
• Butler JP, Loring SH, Patz S, Tsuda A, Yablonskiy DA, Mentzer SJ. Evidence for adult lung growth in humans. N Engl J Med. 2012;367(3):244–247. doi:10.1056/NEJMoa1203983.
   PubMed Web of Science ®Google Scholar
• Hare JM, Traverse JH, Henry TD, Dib N, Strumpf RK, Schulman SP, Gerstenblith G, DeMaria AN, Denktas AE, Gammon RS, et al. A randomized, double-blind, placebo-controlled, dose-escalation study of intravenous adult human mesenchymal stem cells (prochymal) after acute myocardial infarction. J Am Coll Cardiol. 2009;54(24):2277–2286. doi:10.1016/j.jacc.2009.06.055.
   PubMed Web of Science ®Google Scholar
• 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(6):1590–1598. doi:10.1378/chest.12-2094.
   PubMed Web of Science ®Google Scholar
• Stolk J, Broekman W, Mauad T, Zwaginga JJ, Roelofs H, Fibbe WE, Oostendorp J, Bajema I, Versteegh MI, Taube C, et al. A phase I study for intravenous autologous mesenchymal stromal cell administration to patients with severe emphysema. QJM. 2016;109(5):331–336. doi:10.1093/qjmed/hcw001.
   PubMed Web of Science ®Google Scholar
• Jin H, Aiyer A, Su J, Borgstrom P, Stupack D, Friedlander M, and Varner J. A homing mechanism for bone marrow-derived progenitor cell recruitment to the neovasculature. J Clin Invest. 2006;116(3):652–662. doi:10.1172/JCI24751.
   PubMed Web of Science ®Google Scholar
• Johnsen HE, Jensen L, Gaarsdal E, Hansen PB, Ersbøll J, Hansen NE. Priming with recombinant human hematopoietic cytokines before bone marrow harvest expands in vivo and enhances ex vivo recovery of myeloid progenitors in short-term liquid cultures. Exp Hematol. 1994;22(1):80–86. https://www.ncbi.nlm.nih.gov/pubmed/?term=Priming+with+recombinant+human+hematopoietic+cytokines+before+bone+marrow+harvest+expands+in+vivo+and+enhances+ex+vivo+recovery+of+myeloid+progenitors+in+short-term+liquid+cultures
   PubMed Web of Science ®Google Scholar
• Mizrak D, Brittan M, Alison MR. CD133: molecule of the moment. J Pathol. 2008;214(1):3–9. doi:10.1002/path.2283.
   PubMed Web of Science ®Google Scholar
• Slowman S, Danielson C, Graves V, Kotylo P, Broun R, McCarthy L. Administration of GM-/G-CSF prior to bone marrow harvest increases collection of CD34+ cells. Prog Clin Biol Res. 1994;389:363–369. https://www.ncbi.nlm.nih.gov/pubmed/?term=Administration+of+GM-%2FG-CSF+prior+to+bone+marrow+harvest+increases+collection+of+CD34%2B+cells
   PubMedGoogle Scholar
• 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. doi:10.2147/COPD.S15292.
   PubMed Web of Science ®Google Scholar
• Stessuk T, Ruiz MA, Greco OT, Bilaqui A, Ribeiro-Paes MJ, Ribeiro-Paes JT. Phase I clinical trial of cell therapy in patients with advanced chronic obstructive pulmonary disease: follow-up of up to 3 years. Rev Bras Hematol Hemoter. 2013;35(5):352–357. doi:10.5581/1516-8484.20130113.
   PubMedGoogle Scholar
• De Oliveira HG, Cruz FF, Antunes MA, de Macedo Neto AV, Oliveira GA, Svartman FM, Borgonovo T, Rebelatto CL, Weiss DJ, Brofman PR et al. Combined bone marrow-derived mesenchymal stromal cell therapy and one-way endobronchial valve placement in patients with pulmonary emphysema: a phase I clinical trial. Stem Cells Transl Med. 2017;6:962–969. doi:10.1002/sctm.16-0315.
   PubMed Web of Science ®Google Scholar
• Comella K, Blas JAP, Ichim T, Lopez J, Limon J, Moreno RC. Autologous stromal vascular fraction in the intravenous treatment of end-stage chronic obstructive pulmonary disease: a phase I trial of safety and tolerability. J Clin Med Res. 2017;9(8):701–708. doi:10.14740/jocmr3072w.
   PubMedGoogle Scholar
• Nejad-Moghaddam A, Ajdari S, Tahmasbpour E, Goodarzi H, Panahi Y, Ghanei M. Adipose-derived mesenchymal stem cells for treatment of airway injuries in a patient after long-term exposure to sulfur mustard. Cell J. 2017;19(1):117–126. doi:10.22074/cellj.2016.4864.
   PubMed Web of Science ®Google Scholar
• Cheng SL, Lin CH, Yao CL. Mesenchymal stem cell administration in patients with chronic obstructive pulmonary disease: state of the science. Stem Cells Int. 2017;2017:8916570. doi:10.1155/2017/8916570.
   PubMedGoogle Scholar
• Bateman ME, Strong AL, Gimble JM, Bunnell BA. Concise review: Using fat to fight disease: a systematic review of non-homologous adipose-derived stromal/stem cell therapies. Stem Cells. 2018;36(9):1311–1328. doi:10.1002/stem.2847
   PubMed Web of Science ®Google Scholar
• Lin F, Josephs SF, Alexandrescu DT, Ramos F, Bogin V, Gammill V, Dasanu CA, De Necochea-Campion R, Patel AN, Carrier E, et al. Lasers, stem cells, and COPD. J Transl Med. 2010;8:16. doi:10.1186/1479-5876-8-16.
   PubMed Web of Science ®Google Scholar
• Zhao R, Su Z, Wu J, Ji HL. Serious adverse events of cell therapy for respiratory diseases: a systematic review and meta-analysis. Oncotarget. 2017;8(18):30511–30523. doi:10.18632/oncotarget.15426.
   PubMedGoogle Scholar
• Mummery C. Induced pluripotent stem cells-a cautionary note. N Engl J Med. 2011;364(22):2160–2162. doi:10.1056/NEJMcibr1103052.
   PubMed Web of Science ®Google Scholar