Cell-based therapy in lung regenerative medicine

Siniscalco D, Sullo N, Maione S, Rossi F, D’Agostino B: Stem cell therapy: the great promise in lung disease. Ther Adv Respir Dis 2008, 2: 173–177. 10.1177/1753465808092340 Sueblinvong V, Weiss DJ: Stem cells and cell therapy approaches in lung biology and diseases. Transl Res 2010, 156: 188–205. 10.1016/j.trsl.2010.06.007 Christie JD, Edwards LB, Kucheryavaya AY, Benden C, Dobbels F, Kirk R, Rahmel AO, Stehlik J, Hertz MI: The Registry of the International Society for Heart and Lung Transplantation: Twenty-eighth Adult Lung and Heart-Lung Transplant Report–2011. J Heart Lung Transplant 2011, 30: 1104–1122. 10.1016/j.healun.2011.08.004 Weber DJ, Wilkes DS: The role of autoimmunity in obliterative bronchiolitis after lung transplantation. Am J Physiol Lung Cell Mol Physiol 2013, 304: L307-L311. 10.1152/ajplung.00378.2012 Kolios G, Moodley Y: Introduction to stem cells and regenerative medicine. Respiration 2013, 85: 3–10. 10.1159/000345615 Evans MJ, Kaufman MH: Establishment in culture of pluripotential cells from mouse embryos. Nature 1981, 292: 154–156. 10.1038/292154a0 Takahashi K, Yamanaka S: Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006, 126: 663–676. 10.1016/j.cell.2006.07.024 Moodley Y, Ilancheran S, Samuel C, Vaghjiani V, Atienza D, Williams ED, Jenkin G, Wallace E, Trounson A, Manuelpillai U: Human amnion epithelial cell transplantation abrogates lung fibrosis and augments repair. Am J Respir Crit Care Med 2010, 182: 643–651. 10.1164/rccm.201001-0014OC Kajstura J, Rota M, Hall SR, Hosoda T, D’Amario D, Sanada F, Zheng H, Ogorek B, Rondon-Clavo C, Ferreira-Martins J, Matsuda A, Arranto C, Goichberg P, Giordano G, Haley KJ, Bardelli S, Rayatzadeh H, Liu X, Quaini F, Liao R, Leri A, Perrella MA, Loscalzo J, Anversa P: Evidence for human lung stem cells. N Engl J Med 2011, 364: 1795–1806. 10.1056/NEJMoa1101324 Anversa P, Kajstura J, Leri A, Loscalzo J: Tissue-specific adult stem cells in the human lung. Nat Med 2011, 17: 1038–1039. 10.1038/nm.2463 Lung stem cells: Looking beyond the hype. Nat Med 2011, 17: 788–789. Hoffman AM, Ingenito EP: Alveolar epithelial stem and progenitor cells: emerging evidence for their role in lung regeneration. Curr Med Chem 2012, 19: 6003–6008. 10.2174/092986712804485872 Anversa P, Perrella MA, Kourembanas S, Choi AM, Loscalzo J: Regenerative pulmonary medicine: potential and promise, pitfalls and challenges. Eur J Clin Invest 2012, 42: 900–913. 10.1111/j.1365-2362.2012.02667.x 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: 131–148. 10.1002/wdev.58 Austin S: A glossary for stem-cell biology. Nature 2006, 441: 1060. 10.1038/nature04954 Barkauskas CE, Cronce MJ, Rackley CR, Bowie EJ, Keene DR, Stripp BR, Randell SH, Noble PW, Hogan BL: Type 2 alveolar cells are stem cells in adult lung. J Clin Investig 2013, 123: 3025–3036. 10.1172/JCI68782 Rock JR, Hogan BL: Epithelial progenitor cells in lung development, maintenance, repair, and disease. Annu Rev Cell Dev Biol 2011, 27: 493–512. 10.1146/annurev-cellbio-100109-104040 Garcia O, Carraro G, Navarro S, Bertoncello I, McQualter J, Driscoll B, Jesudason E, Warburton D: Cell-based therapies for lung disease. Br Med Bull 2012, 101: 147–161. 10.1093/bmb/ldr051 Rock JR, Onaitis MW, Rawlins EL, Lu Y, Clark CP, Xue Y, Randell SH, Hogan BL: Basal cells as stem cells of the mouse trachea and human airway epithelium. Proc Natl Acad Sci U S A 2009, 106: 12771–12775. 10.1073/pnas.0906850106 Roy MG, Rahmani M, Hernandez JR, Alexander SN, Ehre C, Ho SB, Evans CM: Mucin production during prenatal and postnatal murine lung development. Am J Respir Cell Mol Biol 2011, 44: 755–760. 10.1165/rcmb.2010-0020RC 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: 823–835. 10.1016/j.cell.2005.03.032 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 U S A 2011, 108: E1475-E1483. 10.1073/pnas.1117988108 Chapman HA, Li X, Alexander JP, Brumwell A, Lorizio W, Tan K, Sonnenberg A, Wei Y, Vu TH: Integrin alpha6beta4 identifies an adult distal lung epithelial population with regenerative potential in mice. J Clin Investig 2011, 121: 2855–2862. 10.1172/JCI57673 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 U S A 2010, 107: 1414–1419. 10.1073/pnas.0909207107 Bertoncello I, McQualter J: Isolation and clonal assay of adult lung epithelial stem/progenitor cells. Curr Protoc Stem Cell Biol 2011, 16: 2G.1.1–2G.1.12. Wong AP, Keating A, Lu WY, Duchesneau P, Wang X, Sacher A, Hu J, Waddell TK: Identification of a bone marrow-derived epithelial-like population capable of repopulating injured mouse airway epithelium. J Clin Investig 2009, 119: 336–348. Albera C, Polak JM, Janes S, Griffiths MJ, Alison MR, Wright NA, Navaratnarasah S, Poulsom R, Jeffery R, Fisher C, Burke M, Bishop AE: Repopulation of human pulmonary epithelium by bone marrow cells: a potential means to promote repair. Tissue Eng 2005, 11: 1115–1121. 10.1089/ten.2005.11.1115 Friedenstein AJ, Petrakova KV, Kurolesova AI, Frolova GP: Heterotopic of bone marrow. Analysis of precursor cells for osteogenic and hematopoietic tissues. Transplantation 1968, 6: 230–247. 10.1097/00007890-196803000-00009 Bieback K, Kern S, Kluter H, Eichler H: Critical parameters for the isolation of mesenchymal stem cells from umbilical cord blood. Stem Cells 2004, 22: 625–634. 10.1634/stemcells.22-4-625 Yanez R, Lamana ML, Garcia-Castro J, Colmenero I, Ramirez M, Bueren JA: Adipose tissue-derived mesenchymal stem cells have in vivo immunosuppressive properties applicable for the control of the graft-versus-host disease. Stem Cells 2006, 24: 2582–2591. 10.1634/stemcells.2006-0228 Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop D, Horwitz E: Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006, 8: 315–317. 10.1080/14653240600855905 Mailleux AA, Kelly R, Veltmaat JM, De Langhe SP, Zaffran S, Thiery JP, Bellusci S: Fgf10 expression identifies parabronchial smooth muscle cell progenitors and is required for their entry into the smooth muscle cell lineage. Development 2005, 132: 2157–2166. 10.1242/dev.01795 Hegab AE, Kubo H, Fujino N, Suzuki T, He M, Kato H, Yamaya M: Isolation and characterization of murine multipotent lung stem cells. Stem Cells Dev 2010, 19: 523–536. 10.1089/scd.2009.0287 Chow K, Fessel JP, Kaoriihida S, Schmidt EP, Gaskill C, Alvarez D, Graham B, Harrison DG, Wagner DH Jr, Nozik-Grayck E, West JD, Klemm DJ, Majka SM: Dysfunctional resident lung mesenchymal stem cells contribute to pulmonary microvascular remodeling. Pulm Circ 2013, 3: 31–49. 10.4103/2045-8932.109912 Lama VN, Smith L, Badri L, Flint A, Andrei AC, Murray S, Wang Z, Liao H, Toews GB, Krebsbach PH, Peters-Golden M, Pinsky DJ, Martinez FJ, Thannickal VJ: Evidence for tissue-resident mesenchymal stem cells in human adult lung from studies of transplanted allografts. J Clin Invest 2007, 117: 989–996. 10.1172/JCI29713 Gazdhar A, Susuri N, Hostettler K, Gugger M, Knudsen L, Roth M, Ochs M, Geiser T: HGF Expressing Stem Cells in Usual Interstitial Pneumonia Originate from the Bone Marrow and Are Antifibrotic. PLoS One 2013, 8: e65453. 10.1371/journal.pone.0065453 Akram KM, Samad S, Spiteri MA, Forsyth NR: Mesenchymal stem cells promote alveolar epithelial cell wound repair in vitro through distinct migratory and paracrine mechanisms. Respir Res 2013, 14: 9. 10.1186/1465-9921-14-9 Li L, Zhang S, Zhang Y, Yu B, Xu Y, Guan Z: Paracrine action mediate the antifibrotic effect of transplanted mesenchymal stem cells in a rat model of global heart failure. Mol Biol Rep 2009, 36: 725–731. 10.1007/s11033-008-9235-2 Ohnishi S, Sumiyoshi H, Kitamura S, Nagaya N: Mesenchymal stem cells attenuate cardiac fibroblast proliferation and collagen synthesis through paracrine actions. FEBS Lett 2007, 581: 3961–3966. 10.1016/j.febslet.2007.07.028 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: 964–967. 10.1126/science.275.5302.964 Du R, Lu KV, Petritsch C, Liu P, Ganss R, Passegue E, Song H, Vandenberg S, Johnson RS, Werb Z, Bergers G: HIF1alpha induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion. Cancer Cell 2008, 13: 206–220. 10.1016/j.ccr.2008.01.034 Hristov M, Erl W, Weber PC: Endothelial progenitor cells: mobilization, differentiation, and homing. Arterioscler Thromb Vasc Biol 2003, 23: 1185–1189. 10.1161/01.ATV.0000073832.49290.B5 Duda DG, Cohen KS, Scadden DT, Jain RK: A protocol for phenotypic detection and enumeration of circulating endothelial cells and circulating progenitor cells in human blood. Nat Protoc 2007, 2: 805–810. 10.1038/nprot.2007.111 Resch T, Pircher A, Kahler CM, Pratschke J, Hilbe W: Endothelial progenitor cells: current issues on characterization and challenging clinical applications. Stem Cell Rev 2012, 8: 926–939. 10.1007/s12015-011-9332-9 Ribatti D: The discovery of endothelial progenitor cells. An historical review, Leuk Res 2007, 31: 439–444. Ardhanareeswaran K, Mirotsou M: Lung stem and progenitor cells. Respiration 2013, 85: 89–95. 10.1159/000346500 Kalka C, Masuda H, Takahashi T, Kalka-Moll WM, Silver M, Kearney M, Li T, Isner JM, Asahara T: Transplantation of ex vivo expanded endothelial progenitor cells for therapeutic neovascularization. Proc Natl Acad Sci U S A 2000, 97: 3422–3427. 10.1073/pnas.97.7.3422 Zhao YD, Courtman DW, Deng Y, Kugathasan L, Zhang Q, Stewart DJ: Rescue of monocrotaline-induced pulmonary arterial hypertension using bone marrow-derived endothelial-like progenitor cells: efficacy of combined cell and eNOS gene therapy in established disease. Circ Res 2005, 96: 442–450. 10.1161/01.RES.0000157672.70560.7b Takahashi M, Nakamura T, Toba T, Kajiwara N, Kato H, Shimizu Y: Transplantation of endothelial progenitor cells into the lung to alleviate pulmonary hypertension in dogs. Tissue Eng 2004, 10: 771–779. 10.1089/1076327041348563 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: 318–322. 10.1164/rccm.200301-145OC Wang XX, Zhang FR, Shang YP, Zhu JH, Xie XD, Tao QM, Chen JZ: Transplantation of autologous endothelial progenitor cells may be beneficial in patients with idiopathic pulmonary arterial hypertension: a pilot randomized controlled trial. J Am Coll Cardiol 2007, 49: 1566–1571. 10.1016/j.jacc.2006.12.037 Rafat N, Tonshoff B, Bierhaus A, Beck GC: Endothelial progenitor cells in regeneration after acute lung injury: do they play a role? Am J Respir Cell Mol Biol 2013, 48: 399–405. 10.1165/rcmb.2011-0132TR McQualter JL, Bertoncello I: Concise review: Deconstructing the lung to reveal its regenerative potential. Stem Cells 2012, 30: 811–816. 10.1002/stem.1055 Fishman JM, De Coppi P, Elliott MJ, Atala A, Birchall MA, Macchiarini P: Airway tissue engineering. Expert Opin Biol Ther 2011, 11: 1623–1635. 10.1517/14712598.2011.623696 Badylak SF, Weiss DJ, Caplan A, Macchiarini P: Engineered whole organs and complex tissues. Lancet 2012, 379: 943–952. 10.1016/S0140-6736(12)60073-7 Macchiarini P, Jungebluth P, Go T, Asnaghi MA, Rees LE, Cogan TA, Dodson A, Martorell J, Bellini S, Parnigotto PP, Dickinson SC, Hollander AP, Mantero S, Conconi MT, Birchall MA: Clinical transplantation of a tissue-engineered airway. Lancet 2008, 372: 2023–2030. 10.1016/S0140-6736(08)61598-6 Cortiella J, Nichols JE, Kojima K, Bonassar LJ, Dargon P, Roy AK, Vacant MP, Niles JA, Vacanti CA: Tissue-engineered lung: an in vivo and in vitro comparison of polyglycolic acid and pluronic F-127 hydrogel/somatic lung progenitor cell constructs to support tissue growth. Tissue Eng 2006, 12: 1213–1225. 10.1089/ten.2006.12.1213 Petersen TH, Calle EA, Zhao L, Lee EJ, Gui L, Raredon MB, Gavrilov K, Yi T, Zhuang ZW, Breuer C, Herzog E, Niklason LE: Tissue-engineered lungs for in vivo implantation. Science 2010, 329: 538–541. 10.1126/science.1189345 Weiss DJ: Current status of stem cells and regenerative medicine in lung biology and diseases. Stem Cells 2014,32(1):16–25. 10.1002/stem.1506 Nichols JE, Niles JA, Cortiella J: Production and utilization of acellular lung scaffolds in tissue engineering. J Cell Biochem 2012, 113: 2185–2192. 10.1002/jcb.24112 Raghu G, Weycker D, Edelsberg J, Bradford WZ, Oster G: Incidence and prevalence of idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 2006, 174: 810–816. 10.1164/rccm.200602-163OC Taniguchi H, Ebina M, Kondoh Y, Ogura T, Azuma A, Suga M, Taguchi Y, Takahashi H, Nakata K, Sato A, Takeuchi M, Raghu G, Kudoh S, Nukiwa T: Pirfenidone in idiopathic pulmonary fibrosis. Eur Respir J 2010, 35: 821–829. Noble PW, Albera C, Bradford WZ, Costabel U, Glassberg MK, Kardatzke D, King TE Jr, Lancaster L, Sahn SA, Szwarcberg J, Valeyre D, du Bois RM: Pirfenidone in patients with idiopathic pulmonary fibrosis (CAPACITY): two randomised trials. Lancet 2011, 377: 1760–1769. 10.1016/S0140-6736(11)60405-4 Hung C, Linn G, Chow YH, Kobayashi A, Mittelsteadt K, Altemeier WA, Gharib SA, Schnapp LM, Duffield JS: Role of lung pericytes and resident fibroblasts in the pathogenesis of pulmonary fibrosis. Am J Respir Crit Care Med 2013, 188: 820–830. 10.1164/rccm.201212-2297OC Yang J, Wheeler SE, Velikoff M, Kleaveland KR, Lafemina MJ, Frank JA, Chapman HA, Christensen PJ, Kim KK: Activated Alveolar Epithelial Cells Initiate Fibrosis through Secretion of Mesenchymal Proteins. Am J Pathol 2013, 183: 1559–1570. 10.1016/j.ajpath.2013.07.016 Moeller A, Gilpin SE, Ask K, Cox G, Cook D, Gauldie J, Margetts PJ, Farkas L, Dobranowski J, Boylan C, O’Byrne PM, Strieter RM, Kolb M: Circulating fibrocytes are an indicator of poor prognosis in idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 2009, 179: 588–594. 10.1164/rccm.200810-1534OC Ortiz LA, Gambelli F, McBride C, Gaupp D, Baddoo M, Kaminski N, Phinney DG: Mesenchymal stem cell engraftment in lung is enhanced in response to bleomycin exposure and ameliorates its fibrotic effects. Proc Natl Acad Sci U S A 2003, 100: 8407–8411. 10.1073/pnas.1432929100 Ortiz LA, Dutreil M, Fattman C, Pandey AC, Torres G, Go K, Phinney DG: Interleukin 1 receptor antagonist mediates the antiinflammatory and antifibrotic effect of mesenchymal stem cells during lung injury. Proc Natl Acad Sci U S A 2007, 104: 11002–11007. 10.1073/pnas.0704421104 Rojas M, Xu J, Woods CR, Mora AL, Spears W, Roman J, Brigham KL: Bone marrow-derived mesenchymal stem cells in repair of the injured lung. Am J Respir Cell Mol Biol 2005, 33: 145–152. 10.1165/rcmb.2004-0330OC Cargnoni A, Gibelli L, Tosini A, Signoroni PB, Nassuato C, Arienti D, Lombardi G, Albertini A, Wengler GS, Parolini O: Transplantation of allogeneic and xenogeneic placenta-derived cells reduces bleomycin-induced lung fibrosis. Cell Transplant 2009, 18: 405–422. 10.3727/096368909788809857 Moodley Y, Atienza D, Manuelpillai U, Samuel CS, Tchongue J, Ilancheran S, Boyd R, Trounson A: Human umbilical cord mesenchymal stem cells reduce fibrosis of bleomycin-induced lung injury. Am J Pathol 2009, 175: 303–313. 10.2353/ajpath.2009.080629 Aguilar S, Scotton CJ, McNulty K, Nye E, Stamp G, Laurent G, Bonnet D, Janes SM: Bone marrow stem cells expressing keratinocyte growth factor via an inducible lentivirus protects against bleomycin-induced pulmonary fibrosis. PLoS One 2009, 4: e8013. 10.1371/journal.pone.0008013 Liang J, Zhang H, Hua B, Wang H, Lu L, Shi S, Hou Y, Zeng X, Gilkeson GS, Sun L: Allogenic mesenchymal stem cells transplantation in refractory systemic lupus erythematosus: a pilot clinical study. Ann Rheum Dis 2010, 69: 1423–1429. 10.1136/ard.2009.123463 Tzouvelekis A, Paspaliaris V, Koliakos G, Ntolios P, Bouros E, Oikonomou A, Zissimopoulos A, Boussios N, Dardzinski B, Gritzalis D, Antoniadis A, Froudarakis M, Kolios G, Bouros D: A prospective, non-randomized, no placebo-controlled, phase Ib clinical trial to study the safety of the adipose derived stromal cells-stromal vascular fraction in idiopathic pulmonary fibrosis. J Transl Med 2013, 11: 171. 10.1186/1479-5876-11-171 Antoniou KM, Papadaki HA, Soufla G, Kastrinaki MC, Damianaki A, Koutala H, Spandidos DA, Siafakas NM: Investigation of bone marrow mesenchymal stem cells (BM MSCs) involvement in Idiopathic Pulmonary Fibrosis (IPF). Respir Med 2010, 104: 1535–1542. 10.1016/j.rmed.2010.04.015 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: 2461–2469. 10.1016/j.ajpath.2011.01.058 Retamales I, Elliott WM, Meshi B, Coxson HO, Pare PD, Sciurba FC, Rogers RM, Hayashi S, Hogg JC: Amplification of inflammation in emphysema and its association with latent adenoviral infection. Am J Respir Crit Care Med 2001, 164: 469–473. 10.1164/ajrccm.164.3.2007149 Elnakish MT, Kuppusamy P, Khan M: Stem cell transplantation as a therapy for cardiac fibrosis. J Pathol 2013, 229: 347–354. 10.1002/path.4111 Le Blanc K, Fibbe W: A new cell therapy registry coordinated by the European Group for Blood and Marrow Transplantation (EBMT). Bone Marrow Transplant 2008, 41: 319. 10.1038/sj.bmt.1705920 D’Agostino B, Sullo N, Siniscalco D, De Angelis A, Rossi F: Mesenchymal stem cell therapy for the treatment of chronic obstructive pulmonary disease. Expert Opin Biol Ther 2010, 10: 681–687. 10.1517/14712591003610614 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: 1590–1598. 10.1378/chest.12-2094