Future prospects for tissue engineered lung transplantation: Decellularization and recellularization-based whole lung regeneration

Organogenesis

Volumn 10, Issue 2, 2014, Pages 196-207

  Tsuchiya, Tomoshi ^a   Sivarapatna, Amogh ^b   Rocco, Kevin ^b   Nanashima, Atsushi ^a   Nagayasu, Takeshi ^a   Niklason, Laura E ^b  

^a NAGASAKI UNIVERSITY GRADUATE SCHOOL OF BIOMEDICAL SCIENCES   (Japan)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Decellularization; Extracellular matrix; Induced pluripotent stem cells; Lung transplantation; Recellularization; Stem progenitor cells

Indexed keywords

BIOMATERIAL; GROWTH FACTOR;

CELL COMPONENT; CELL POPULATION; CELL REPOPULATION; DECELLULARIZATION; EMBRYONIC STEM CELL; ENDOTHELIUM CELL; EPITHELIUM CELL; EXTRACELLULAR MATRIX; GAMMA IRRADIATION; GRAFT REJECTION; HUMAN; IMMUNOHISTOCHEMISTRY; LUNG TRANSPLANTATION; MASS SPECTROMETRY; MATURATION; MESENCHYMAL STEM CELL; NONHUMAN; PLURIPOTENT STEM CELL; PROCEDURES CONCERNING CELLS; PROTEIN CROSS LINKING; RECELLULARIZATION; REVIEW; SEQUENCE HOMOLOGY; TISSUE ENGINEERING; TISSUE REGENERATION; TISSUE SCAFFOLD; LUNG; METABOLISM; PROCEDURES; REGENERATION;

EXTRACELLULAR MATRIX; HUMANS; LUNG; LUNG TRANSPLANTATION; REGENERATION; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84903282119     PISSN: 15476278     EISSN: 15558592     Source Type: Journal    
DOI: 10.4161/org.27846     Document Type: Review

References (114)

1. Orens JB, Estenne M, Arcasoy S, Conte JV, Corris P, Egan JJ, Egan T, Keshavjee S, Knoop C, Kotloff R, et al.; Pulmonary Scientific Council of the International Society for Heart and Lung Transplantation. International guidelines for the selection of lung transplant candidates: 2006 update-a consensus report from the Pulmonary Scientific Council of the International Society for Heart and Lung Transplantation. J Heart Lung Transplant 2006; 25:745-55; PMID:16818116; http://dx.doi.org/10.1016/j.healun.2006.03.011
2. Sherry M, Xu J, Kenneth M, Kochanek M. Deaths: Final data for 2010. Natl Vital Stat Rep 2013; 61:1-116
3. Orens JB, Garrity ER Jr. General overview of lung transplantation and review of organ allocation. Proc Am Thorac Soc 2009; 6:13-9; PMID:19131526; http://dx.doi.org/10.1513/pats.200807-072GO
4. Kotsimbos T, Williams TJ, Anderson GP. Update on lung transplantation: programmes, patients and prospects. Eur Respir Rev 2012; 21:271-305; PMID:23204117; http://dx.doi.org/10.1183/09059180.00006312
5. O'Grady NP, Murray PR, Ames N. Preventing ventilator-associated pneumonia: does the evidence support the practice? JAMA 2012; 307:2534-9; PMID:22797453
6. Grover FL, Fullerton DA, Zamora MR, Mills C, Ackerman B, Badesch D, Brown JM, Campbell DN, Chetham P, Dhaliwal A, et al. The past, present, and future of lung transplantation. Am J Surg 1997; 173:523-33; PMID:9207168; http://dx.doi.org/10.1016/S0002-9610(97)00004-4
7. Zafar SY, Howell DN, Gockerman J P. Malignancy after solid organ transplantation: an overview. Oncologist 2008; 13:769-78; PMID:18614590; http://dx.doi.org/10.1634/theoncologist.2007-0251
8. Valapour M, Paulson K, Smith JM, Hertz MI, Skeans MA, Heubner BM, Edwards LB, Snyder JJ, Israni AK, Kasiske BL. OPTN/SRTR 2011 Annual Data Report: lung. Am J Transplant 2013; 13(Suppl 1): 149-77; PMID:23237700; http://dx.doi.org/10.1111/ajt.12024
9. Oto T, Okada Y, Bando T, Minami M, Shiraishi T, Nagayasu T, Chida M, Okumura M, Date H, Miyoshi S, et al.; Japanese Society of Lung and Heart-Lung Transplantation. Registry of the Japanese society of lung and heart-lung transplantation: the official Japanese lung transplantation report 2012. Gen Thorac Cardiovasc Surg 2013; 61:208-11; PMID:23436117; http://dx.doi.org/10.1007/s11748-013-0215-7
10. Cooper DKC, Ekser B, Burlak C, Ezzelarab M, Hara H, Paris L, Tector AJ, Phelps C, Azimzadeh AM, Ayares D, et al. Clinical lung xenotransplantation-what donor genetic modifications may be necessary? Xenotransplantation 2012; 19:144-58; PMID:22702466; http://dx.doi.org/10.1111/j.1399-3089.2012.00708.x
11. Franzdóttir SR, Axelsson IT, Arason AJ, Baldursson O, Gudjonsson T, Magnusson MK. Airway branching morphogenesis in three dimensional culture. Respir Res 2010; 11:162-72; PMID:21108827; http://dx.doi.org/10.1186/1465-9921-11-162
12. Huh D, Matthews BD, Mammoto A, Montoya-Zavala M, Hsin HY, Ingber DE. Reconstituting organ-level lung functions on a chip. Science 2010; 328:1662-8; PMID:20576885; http://dx.doi.org/10.1126/science.1188302
13. Petersen TH, Calle EA, Zhao L, Lee EJ, Gui L, Raredon MB, Gavrilov K, Yi T, Zhuang ZW, Breuer C, et al. Tissue-engineered lungs for in vivo implantation. Science 2010; 329:538-41; PMID:20576850; http://dx.doi.org/10.1126/science.1189345
14. Ott HC, Clippinger B, Conrad C, Schuetz C, Pomerantseva I, Ikonomou L, Kotton D, Vacanti JP. Regeneration and orthotopic transplantation of a bioartificial lung. Nat Med 2010; 16:927-33; PMID:20628374; http://dx.doi.org/10.1038/nm.2193
15. Gilbert T W, Sellaro TL, Badylak SF. Decellularization of tissues and organs. Biomaterials 2006; 27:3675-83; PMID:16519932
16. Badylak SF. Xenogeneic extracellular matrix as a scaffold for tissue reconstruction. Transpl Immunol 2004; 12: 367-77; PMID:15157928; http://dx.doi.org/10.1016/j.trim.2003.12.016
17. McDevitt CA, Wildey GM, Cutrone RM. Transforming growth factor-beta1 in a sterilized tissue derived from the pig small intestine sub-mucosa. J Biomed Mater Res A 2003; 67:637-40; PMID:14566807; http://dx.doi.org/10.1002/jbm.a.10144
18. Crapo PM, Gilbert TW, Badylak SF. An overview of tissue and whole organ decellularization processes. Biomaterials 2011; 32:3233-43; PMID:21296410; http://dx.doi.org/10.1016/j.biomaterials.2011.01.057
19. Gerson CJ, Elkins RC, Goldstein S, Heacox AE. Structural integrity of collagen and elas-tin in SynerGraft® decellularized-cryopreserved human heart valves. Cryobiology 2012; 64:33-42; PMID:22119932; http://dx.doi.org/10.1016/j.cryobiol.2011.11.001
20. Yagi H, Soto-Gutierrez A, Kitagawa Y. Whole-organ re-engineering: a regenerative medicine approach to digestive organ replacement. Surg Today 2013; 43:587-94; PMID:23184357; http://dx.doi.org/10.1007/s00595-012-0396-1
21. Schenke-Layland K, Vasilevski O, Opitz F, König K, Riemann I, Halbhuber KJ, Wahlers T, Stock UA. Impact of decellularization of xenogeneic tissue on extracellular matrix integrity for tissue engineering of heart valves. J Struct Biol 2003; 143:201-8; PMID:14572475; http://dx.doi.org/10.1016/j.jsb.2003.08.002
22. Gulbins H, Goldemund A, Anderson I, Haas U, Uhlig A, Meiser B, Reichart B. Preseeding with autologous fibroblasts improves endothelialization of glutaralde-hyde-fixed porcine aortic valves. J Thorac Cardiovasc Surg 2003; 125:592-601; PMID:12658201; http://dx.doi.org/10.1067/mtc.2003.48
23. Steinhoff G, Stock U, Karim N, Mertsching H, Timke A, Meliss RR, Pethig K, Haverich A, Bader A. Tissue engineering of pulmonary heart valves on allo-genic acellular matrix conduits: in vivo restoration of valve tissue. Circulation 2000; 102(Suppl 3):III50-5; PMID:11082362; http://dx.doi.org/10.1161/01.CIR.102.suppl-3.III-50
24. Sayk F, Bos I, Schubert U, Wedel T, Sievers H-H. Histopathologic findings in a novel decellularized pulmonary homograft: an autopsy study. Ann Thorac Surg 2005; 79:1755-8; PMID:15854972; http://dx.doi.org/10.1016/j.athoracsur.2003.11.049
25. Takagi K, Fukunaga S, Nishi A, Shojima T, Yoshikawa K, Hori H, Akashi H, Aoyagi S. In vivo recellulariza-tion of plain decellularized xenografts with specific cell characterization in the systemic circulation: histological and immunohistochemical study. Artif Organs 2006; 30:233-41; PMID:16643381; http://dx.doi.org/10.1111/j.1525-1594.2006.00210.x
26. Ketchedjian A, Jones AL, Krueger P, Robinson E, Crouch K, Wolfinbarger L Jr., Hopkins R. Recellularization of decellularized allograft scaffolds in ovine great vessel reconstructions. Ann Thorac Surg 2005; 79:888-96, discussion 896; PMID:15734400; http://dx.doi.org/10.1016/j.athoracsur.2004.09.033
27. Macchiarini P, Jungebluth P, Go T, Asnaghi MA, Rees LE, Cogan TA, Dodson A, Martorell J, Bellini S, Parnigotto PP, et al. Clinical transplantation of a tissue-engineered airway. Lancet 2008; 372:2023-30; PMID:19022496; http://dx.doi.org/10.1016/S0140-6736(08)61598-6
28. Atala A, Bauer SB, Soker S, Yoo JJ, Retik AB. Tissue-engineered autologous bladders for patients needing cystoplasty. Lancet 2006; 367:1241-6; PMID:16631879; http://dx.doi.org/10.1016/S0140-6736(06)68438-9
29. Biancosino C, Zardo P, Walles T, Wildfang I, Macchiarini P, Mertsching H. Generation of a bio-artificial fibromuscular tissue with autoregenerative capacities for surgical reconstruction. Cytotherapy 2006; 8:178-83; PMID:16698691; http://dx.doi.org/10.1080/14653240600621166
30. Cebotari S, Lichtenberg A, Tudorache I, Hilfiker A, Mertsching H, Leyh R, Breymann T, Kallenbach K, Maniuc L, Batrinac A, et al. Clinical application of tissue engineered human heart valves using autologous progenitor cells. Circulation 2006; 114(Suppl):I132-7; PMID:16820562; http://dx.doi.org/10.1161/CIRCULATIONAHA.105.001065
31. Hermanns MI, Unger RE, Kehe K, Peters K, Kirkpatrick CJ. Lung epithelial cell lines in coculture with human pulmonary microvascular endothelial cells: development of an alveolo-capillary barrier in vitro. Lab Invest 2004; 84:736-52; PMID:15077120; http://dx.doi.org/10.1038/labinvest.3700081
32. Lwebuga-Mukasa J, Inggar D, Madri J. Repopulation of a human alveolar matrix by adult rat type II pneumocytes in vitro. A novel system for type II pneumocyte culture. Exp Cell Res 1986; 162: 423-35; PMID:3510880; http://dx.doi.org/10.1016/0014-4827(86)90347-2
33. Price A P, England KA, Matson AM, Blazar BR, Panoskaltsis-Mortari A. Development of a decel-lularized lung bioreactor system for bioengineering the lung: the matrix reloaded. Tissue Eng Part A 2010; 16:2581-91; PMID:20297903; http://dx.doi.org/10.1089/ten.tea.2009.0659
34. Song JJ, Kim SS, Liu Z, Madsen JC, Mathisen DJ, Vacanti JP, Ott HC. Enhanced in vivo function of bioartificial lungs in rats. Ann Thorac Surg 2011; 92:998-1005, discussion 1005-6; PMID:21871290; http://dx.doi.org/10.1016/j.athoracsur.2011.05.018
35. Shamis Y, Hasson E, Soroker A, Bassat E, Shimoni Y, Ziv T, Sionov RV, Mitrani E. Organ-specific scaffolds for in vitro expansion, differentiation, and organization of primary lung cells. Tissue Eng Part C Methods 2011; 17:861-70; PMID:21595544; http://dx.doi.org/10.1089/ten.tec.2010.0717
36. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. Embryonic stem cell lines derived from human blastocysts. Science 1998; 282:1145-7; PMID:9804556; http://dx.doi.org/10.1126/science.282.5391.1145
37. Wang D, Haviland DL, Burns AR, Zsigmond E, Wetsel RA. A pure population of lung alveolar epithelial type II cells derived from human embryonic stem cells. Proc Natl Acad Sci USA 2007; 104:4449-54; PMID:17360544; http://dx.doi.org/10.1073/pnas.0700052104
38. Samadikuchaksaraei A, Cohen S, Isaac K, Rippon HJ, Polak JM, Bielby RC, Bishop AE. Derivation of distal airway epithelium from human embryonic stem cells. Tissue Eng 2006; 12:867-75; PMID:16674299; http://dx.doi.org/10.1089/ten.2006.12.867
39. Cortiella J, Niles J, Cantu A, Brettler A, Pham A, Vargas G, Winston S, Wang J, Walls S, Nichols JE. Influence of acellular natural lung matrix on murine embryonic stem cell differentiation and tissue formation. Tissue Eng Part A 2010; 16:2565-80; PMID:20408765; http://dx.doi.org/10.1089/ten.tea.2009.0730
40. Jensen T, Sc M, Roszell B, Ph D, Zang F, Girard E, Matson A, Thrall R, Jaworski DM, Hatton C, et al. A rapid lung de-cellularization protocol supports embryonic stem cell differentiation in vitro and following implantation. Tissue Eng Part C Methods 2012; 18:632-46; PMID:22404373; http://dx.doi.org/10.1089/ten.tec.2011.0584
41. Longmire TA, Ikonomou L, Hawkins F, Christodoulou C, Cao Y, Jean JC, Kwok LW, Mou H, Rajagopal J, Shen SS, et al. Efficient derivation of purified lung and thyroid progenitors from embryonic stem cells. Cell Stem Cell 2012; 10:398-411; PMID:22482505; http://dx.doi.org/10.1016/j.stem.2012.01.019
42. 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 multi-potent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006; 8:315-7; PMID:16923606; http://dx.doi.org/10.1080/14653240600855905
43. Yamada M, Kubo H, Ishizawa K, Kobayashi S, Shinkawa M, Sasaki H. Increased circulating endo-thelial progenitor cells in patients with bacterial pneumonia: evidence that bone marrow derived cells contribute to lung repair. Thorax 2005; 60:410-3; PMID:15860717; http://dx.doi.org/10.1136/thx.2004.034058
44. Burnham EL, Taylor WR, Quyyumi AA, Rojas M, Brigham KL, Moss M. Increased circulating endo-thelial progenitor cells are associated with survival in acute lung injury. Am J Respir Crit Care Med 2005; 172:854-60; PMID:15976374; http://dx.doi.org/10.1164/rccm.200410-1325OC
45. Wong AP, Keating A, Lu W-Y, 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 Invest 2009; 119:336-48; PMID:19164856
46. 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; 172:1266-72; PMID:14707105
47. Hegab AE, Kubo H, Yamaya M, Asada M, He M, Fujino N, Mizuno S, Nakamura T. Intranasal HGF administration ameliorates the physiologic and morphologic changes in lung emphysema. Mol Ther 2008; 16:1417-26; PMID:18560414; http://dx.doi.org/10.1038/mt.2008.137
48. 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; 556:249-52; PMID:14706858; http://dx.doi.org/10.1016/S0014-5793(03)01399-1
49. Nolen-Walston RD, Kim CF, Mazan MR, Ingenito EP, Gruntman AM, Tsai L, Boston R, Woolfenden AE, Jacks T, Hoffman AM. Cellular kinetics and modeling of bronchioalveolar stem cell response during lung regeneration. Am J Physiol Lung Cell Mol Physiol 2008; 294:L1158-65; PMID:18375744; http://dx.doi.org/10.1152/ajplung.00298.2007
50. Daly AB, Wallis JM, Borg ZD, Bonvillain RW, Deng B, Ballif BA, Jaworski DM, Allen GB, Weiss DJ. Initial binding and recellularization of decellularized mouse lung scaffolds with bone marrow-derived mesenchymal stromal cells. Tissue Eng Part A 2012; 18:1-16; PMID:21756220; http://dx.doi.org/10.1089/ten.tea.2011.0301
51. Wallis JM, Borg ZD, Daly AB, Deng B, Ballif BA, Allen GB, Jaworski DM, Weiss DJ. Comparative assessment of detergent-based protocols for mouse lung de-cellularization and re-cellularization. Tissue Eng Part C Methods 2012; 18:420-32; PMID:22165818; http://dx.doi.org/10.1089/ten.tec.2011.0567
52. Sokocevic D, Bonenfant NR, Wagner DE, Borg ZD, Lathrop MJ, Lam YW, Deng B, Desarno MJ, Ashikaga T, Loi R, et al. The effect of age and emphy-sematous and fibrotic injury on the re-cellularization of de-cellularized lungs. Biomaterials 2013; 34:3256-69; PMID:23384794; http://dx.doi.org/10.1016/j.biomaterials.2013.01.028
53. Bonenfant NR, Sokocevic D, Wagner DE, Borg ZD, Lathrop MJ, Lam YW, Deng B, Desarno MJ, Ashikaga T, Loi R, et al. The effects of storage and sterilization on de-cellularized and re-cellular-ized whole lung. Biomaterials 2013; 34:3231-45; PMID:23380353; http://dx.doi.org/10.1016/j.biomaterials.2013.01.031
54. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006; 126:663-76; PMID:16904174; http://dx.doi.org/10.1016/j.cell.2006.07.024
55. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S. Induction of pluripotent stem cells from adult human fibro-blasts by defined factors. Cell 2007; 131:861-72; PMID:18035408; http://dx.doi.org/10.1016/j.cell.2007.11.019
56. Ghaedi M, Calle EA, Mendez JJ, Gard AL, Balestrini J, Booth A, Bove PF, Gui L, White ES, Niklason LE. Human iPS cell-derived alveolar epithelium repopulates lung extracellular matrix. J Clin Invest 2013; 123:4950-62; PMID:24135142; http://dx.doi.org/10.1172/JCI68793
57. Ghaedi M, Mendez JJ, Bove PF, Sivarapatna A, Raredon MSB, Niklason LE. Alveolar epithelial differentiation of human induced pluripotent stem cells in a rotating bioreactor. Biomaterials 2014; 35:699-710; PMID:24144903; http://dx.doi.org/10.1016/j.biomaterials.2013.10.018
58. 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; 91:363-78; PMID:21079581; http://dx.doi.org/10.1038/labinvest.2010.187
59. 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; 364:1795-806; PMID:21561345; http://dx.doi.org/10.1056/NEJMoa1101324
60. Oeztuerk-Winder F, Guinot A, Ochalek A, Ventura J-J. Regulation of human lung alveolar multipotent cells by a novel p38α MAPK/miR-17-92 axis. EMBO J 2012; 31:3431-41; PMID:22828869; http://dx.doi.org/10.1038/emboj.2012.192
61. Chavakis E, Urbich C, Dimmeler S. Homing and engraftment of progenitor cells: a prerequisite for cell therapy. J Mol Cell Cardiol 2008; 45:514-22; PMID:18304573; http://dx.doi.org/10.1016/j.yjmcc.2008.01.004
62. Petersen TH, Calle EA, Colehour MB, Niklason LE. Bioreactor for the long-term culture of lung tissue. Cell Transplant 2011; 20: 1117-26; PMID:21092411; http://dx.doi.org/10.3727/096368910X544933
63. Petersen TH, Calle EA, Colehour MB, Niklason LE. Matrix composition and mechanics of decel-lularized lung scaffolds. Cells Tissues Organs 2012; 195:222-31; PMID:21502745; http://dx.doi.org/10.1159/000324896
64. Dunsmore SE, Rannels DE. Extracellular matrix biology in the lung. Am J Physiol 1996; 270:L3-27; PMID:8772523
65. van der Rest M, Garrone R. Collagen family of proteins. FASEB J 1991; 5:2814-23; PMID:1916105
66. Schwarzbauer JE. Fibronectin: from gene to protein. Curr Opin Cell Biol 1991; 3:786-91; PMID:1931080; http://dx.doi.org/10.1016/0955-0674(91)90051-Y
67. Nguyen NM, Senior RM. Laminin isoforms and lung development: all isoforms are not equal. Dev Biol 2006; 294:271-9; PMID:16643883; http://dx.doi.org/10.1016/j.ydbio.2006.03.032
68. Miner JH, Yurchenco PD. Laminin functions in tissue morphogenesis. Annu Rev Cell Dev Biol 2004; 20:255-84; PMID:15473841; http://dx.doi.org/10.1146/annurev.cellbio.20.010403.094555
69. Badylak SF, Taylor D, Uygun K. Whole-organ tissue engineering: decellularization and recellularization of three-dimensional matrix scaffolds. Annu Rev Biomed Eng 2011; 13:27-53; PMID:21417722; http://dx.doi.org/10.1146/annurev-bioeng-071910-124743
70. Schwarzbauer J. Basement membranes: Putting up the barriers. Curr Biol 1999; 9:R242-4; PMID:10209113; http://dx.doi.org/10.1016/S0960-9822(99)80153-5
71. Ponce ML, Nomizu M, Delgado MC, Kuratomi Y, Hoffman MP, Powell S, Yamada Y, Kleinman HK, Malinda KM. Identification of endothelial cell binding sites on the laminin gamma 1 chain. Circ Res 1999; 84:688-94; PMID:10189356; http://dx.doi.org/10.1161/01.RES.84.6.688
72. Ferdous Z, Grande-Allen KJ. Utility and control of proteoglycans in tissue engineering. Tissue Eng 2007; 13:1893-904; PMID:17518731; http://dx.doi.org/10.1089/ten.2006.0056
73. Yuan H, Kononov S, Cavalcante FS, Lutchen KR, Ingenito EP, Suki B. Effects of collagenase and elastase on the mechanical properties of lung tissue strips. J Appl Physiol (1985) 2000; 89:3-14; PMID:10904029
74. Kielty CM, Sherratt MJ, Shuttleworth CA. Elastic fibres. J Cell Sci 2002; 115:2817-28; PMID:12082143
75. Isenburg JC, Simionescu DT, Vyavahare NR. Tannic acid treatment enhances biostabil-ity and reduces calcification of glutaralde-hyde fixed aortic wall. Biomaterials 2005; 26:1237-45; PMID:15475053; http://dx.doi.org/10.1016/j.biomaterials.2004.04.034
76. Wallis JM, Borg ZD, Daly AB, Deng B, Ballif BA, Allen GB, Jaworski DM, Weiss DJ. Comparative assessment of detergent-based protocols for mouse lung de-cellularization and re-cellularization. Tissue Eng Part C Methods 2012; 18:420-32; PMID:22165818; http://dx.doi.org/10.1089/ten.tec.2011.0567
77. Bonvillain RW, Danchuk S, Sullivan DE, Betancourt AM, Semon JA, Eagle ME, Mayeux JP, Gregory AN, Wang G, Townley IK, et al. A nonhuman primate model of lung regeneration: detergent-mediated decellularization and initial in vitro recellularization with mesenchymal stem cells. Tissue Eng Part A 2012; 18:2437-52; PMID:22764775; http://dx.doi.org/10.1089/ten.tea.2011.0594
78. Booth AJ, Hadley R, Cornett AM, Dreffs AA, Matthes SA, Tsui JL, Weiss K, Horowitz JC, Fiore VF, Barker TH, et al. Acellular normal and fibrotic human lung matrices as a culture system for in vitro investigation. Am J Respir Crit Care Med 2012; 186:866-76; PMID:22936357; http://dx.doi.org/10.1164/rccm.201204-0754OC
79. Nichols JE, Niles J, Riddle M, Vargas G, Schilagard T, Ma L, Edward K, La Francesca S, Sakamoto J, Vega S, et al. Production and assessment of decellular-ized pig and human lung scaffolds. Tissue Eng Part A 2013; 19:2045-62; PMID:23638920; http://dx.doi.org/10.1089/ten.tea.2012.0250
80. Nakayama KH, Lee CCI, Batchelder CA, Tarantal AF. Tissue specificity of decellularized rhesus monkey kidney and lung scaffolds. PLoS One 2013; 8:e64134; PMID:23717553; http://dx.doi.org/10.1371/journal.pone.0064134
81. O'Neill JD, Anfang R, Anandappa A, Costa J, Javidfar J, Wobma HM, Singh G, Freytes DO, Bacchetta MD, Sonett JR, et al. Decellularization of human and porcine lung tissues for pulmonary tissue engineering. Ann Thorac Surg 2013; 96:1046-55, discussion 1055-6; PMID:23870827; http://dx.doi.org/10.1016/j.athoracsur.2013.04.022
82. Sun H, Calle EA, Chen X, Mathur A, Zhu Y, Mendez J, Zhao L, Niklason LE, Peng X, Peng H, et al. Fibroblast engraftment in the decellularized mouse lung occurs via a β1 integrin dependent, FAK dependent pathway that is mediated by ERK and opposed by AKT. Am J Physiol Lung Cell Mol Physiol 2013; (Forthcoming); PMID:24337923; http://dx.doi.org/10.1152/ajplung.00100.2013
83. Elizabeth Gilpin S, Guyette J P, Gonzalez G, Ren X, Asara JM, Mathisen DJ, Vacanti J P, Ott HC. Perfusion decellularization of human and porcine lungs: Bringing the matrix to clinical scale. J Heart Lung Transplant 2013; (Forthcoming)
84. Gilbert T W, Freund JM, Badylak SF. Quantification of DNA in biologic scaffold materials. J Surg Res 2009; 152:135-9; PMID:18619621; http://dx.doi.org/10.1016/j.jss.2008.02.013
85. Strom TB, Roy-Chaudhury P, Manfro R, Zheng XX, Nickerson PW, Wood K, Bushell A. The Th1/Th2 paradigm and the allograft response. Curr Opin Immunol 1996; 8:688-93; PMID:8902395; http://dx.doi.org/10.1016/S0952-7915(96)80087-2
86. Allman AJ, McPherson TB, Badylak SF, Merrill LC, Kallakury B, Sheehan C, Raeder RH, Metzger DW. Xenogeneic extracellular matrix grafts elicit a TH2-restricted immune response. Transplantation 2001; 71:1631-40; PMID:11435976; http://dx.doi.org/10.1097/00007890-200106150-00024
87. Gehr P, Bachofen M, Weibel ER. The normal human lung: ultrastructure and morphometric estimation of diffusion capacity. Respir Physiol 1978; 32:121-40; PMID:644146; http://dx.doi.org/10.1016/0034-5687(78)90104-4
88. Maghsoudlou P, Georgiades F, Tyraskis A, Totonelli G, Loukogeorgakis SP, Orlando G, Shangaris P, Lange P, Delalande J-M, Burns AJ, et al. Preservation of micro-architecture and angiogenic potential in a pulmonary acellular matrix obtained using intermittent intra-tracheal flow of detergent enzymatic treatment. Biomaterials 2013; 34:6638-48; PMID:23727263; http://dx.doi.org/10.1016/j.biomaterials.2013.05.015
89. Maeda Y, Davé V, Whitsett JA. Transcriptional control of lung morphogenesis. Physiol Rev 2007; 87:219-44; PMID:17237346; http://dx.doi.org/10.1152/physrev.00028.2006
90. Liu M, Post M. Invited review: mechanochemical signal transduction in the fetal lung. J Appl Physiol (1985) 2000; 89:2078-84; PMID:11053365
91. Bolt RJ, van Weissenbruch MM, Lafeber HN, Delemarre-van de Waal HA. Glucocorticoids and lung development in the fetus and preterm infant. Pediatr Pulmonol 2001; 32:76-91; PMID:11416880; http://dx.doi.org/10.1002/ppul.1092
92. Inanlou MR, Baguma-Nibasheka M, Kablar B. The role of fetal breathing-like movements in lung organogenesis. Histol Histopathol 2005; 20:1261-6; PMID:16136506
93. Chytil F. Retinoids in lung development. FASEB J 1996; 10:986-92; PMID:8801181
94. Harding R, Hooper SB. Regulation of lung expansion and lung growth before birth. J Appl Physiol (1985) 1996; 81:209-24; PMID:8828667
95. Liu M, Skinner SJ, Xu J, Han RNN, Tanswell AK, Post M. Stimulation of fetal rat lung cell proliferation in vitro by mechanical stretch. Am J Physiol 1992; 263:L376-83; PMID:1415562
96. Xu J, Liu M, Tanswell AK, Post M. Mesenchymal determination of mechanical strain-induced fetal lung cell proliferation. Am J Physiol 1998; 275:L545-50; PMID:9728049
97. Nakamura T, Liu M, Mourgeon E, Slutsky A, Post M. Mechanical strain and dexamethasone selectively increase surfactant protein C and tropoelastin gene expression. Am J Physiol Lung Cell Mol Physiol 2000; 278:L974-80; PMID:10781428
98. Rose F, Kürth-Landwehr C, Sibelius U, Reuner KH, Aktories K, Seeger W, Grimminger F. Role of actin depolymerization in the surfactant secretory response of alveolar epithelial type II cells. Am J Respir Crit Care Med 1999; 159:206-12; PMID:9872840; http://dx.doi.org/10.1164/ajrccm.159.1.9801106
99. Rose F, Zwick K, Ghofrani HA, Sibelius U, Seeger W, Walmrath D, Grimminger F. Prostacyclin enhances stretch-induced surfactant secretion in alveolar epithelial type II cells. Am J Respir Crit Care Med 1999; 160:846-51; PMID:10471607; http://dx.doi.org/10.1164/ajrccm.160.3.9812155
100. Mourgeon E, Xu J, Tanswell AK, Liu M, Post M. Mechanical strain-induced posttranscriptional regulation of fibronectin production in fetal lung cells. Am J Physiol 1999; 277:L142-9; PMID:10409241
101. Xu J, Liu M, Liu J, Caniggia I, Post M. Mechanical strain induces constitutive and regulated secretion of glycosaminoglycans and proteoglycans in fetal lung cells. J Cell Sci 1996; 109:1605-13; PMID:8799847
102. Xu J, Liu M, Post M. Differential regulation of extracellular matrix molecules by mechanical strain of fetal lung cells. Am J Physiol 1999; 276:L728-35; PMID:10330028
103. Daly KA, Stewart-Akers AM, Hara H, Ezzelarab M, Long C, Cordero K, Johnson SA, Ayares D, Cooper DKC, Badylak SF. Effect of the alphaGal epitope on the response to small intestinal submucosa extracellular matrix in a nonhuman primate model. Tissue Eng Part A 2009; 15:3877-88; PMID:19563260; http://dx.doi.org/10.1089/ten.tea.2009.0089
104. McPherson TB, Liang H, Record RD, Badylak SF. Galalpha(1, 3)Gal epitope in porcine small intestinal submucosa. Tissue Eng 2000; 6:233-9; PMID:10941218; http://dx.doi.org/10.1089/10763270050044416
105. Badylak S, Kokini K, Tullius B, Simmons-Byrd A, Morff R. Morphologic study of small intestinal submucosa as a body wall repair device. J Surg Res 2002; 103:190-202; PMID:11922734; http://dx.doi.org/10.1006/jsre.2001.6349
106. Nuininga JE, van Moerkerk H, Hanssen A, Hulsbergen CA, Oosterwijk-Wakka J, Oosterwijk E, de Gier RPE, Schalken JA, van Kuppevelt T, Feitz WFJ. Rabbit urethra replacement with a defined biomatrix or small intestinal submucosa. Eur Urol 2003; 44:266-71; PMID:12875948; http://dx.doi.org/10.1016/S0302-2838(03)00249-5
107. Nieponice A, McGrath K, Qureshi I, Beckman EJ, Luketich JD, Gilbert TW, Badylak SF. An extracellular matrix scaffold for esophageal stricture prevention after circumferential EMR. Gastrointest Endosc 2009; 69:289-96; PMID:18657808; http://dx.doi.org/10.1016/j.gie.2008.04.022
108. Cantu E, Parker W, Platt JL, Duane Davis R. Pulmonary xenotransplantation: rapidly progressing into the unknown. Am J Transplant 2004; 4(Suppl 6):25-35; PMID:14871271; http://dx.doi.org/10.1111/j.1600-6135.2004.0342.x
109. Toledo-Pereyra LH, Lopez-Neblina F. Xenotransplantation: a view to the past and an unrealized promise to the future. Exp Clin Transplant 2003; 1:1-7; PMID:15859901
110. Ekser B, Rigotti P, Gridelli B, Cooper DKC. Xenotransplantation of solid organs in the pig-to-primate model. Transpl Immunol 2009; 21:87-92; PMID:18955143; http://dx.doi.org/10.1016/j.trim.2008.10.005
111. Lai L, Kolber-Simonds D, Park K-W, Cheong H-T, Greenstein JL, Im G-S, Samuel M, Bonk A, Rieke A, Day BN, et al. Production of alpha-1, 3-galactos-yltransferase knockout pigs by nuclear transfer cloning. Science 2002; 295:1089-92; PMID:11778012; http://dx.doi.org/10.1126/science.1068228
112. Bush EL, Barbas AS, Holzknecht ZE, Byrne GW, McGregor CG, Parker W, Davis RD, Lin SS. Coagulopathy in a-galactosyl transferase knockout pulmonary xenotransplants. Xenotransplantation 2011; 18:6-13; PMID:21342283; http://dx.doi.org/10.1111/j.1399-3089.2011.00621.x
113. Nakakuki S. Bronchial tree, lobular division and blood vessels of the pig lung. J Vet Med Sci 1994; 56:685-9; PMID:7999892; http://dx.doi.org/10.1292/jvms.56.685
114. Daggett CW, Yeatman M, Lodge AJ, Chen EP, Linn SS, Gullotto C, Frank MM, Platt JL, Davis RD. Total respiratory support from swine lungs in primate recipients. J Thorac Cardiovasc Surg 1998; 115:19-27; PMID:9451041; http://dx.doi.org/10.1016/S0022-5223(98)70438-6