Comparative biology of decellularized lung matrix: Implications of species mismatch in regenerative medicine

Biomaterials

Volumn 102, Issue , 2016, Pages 220-230

  Balestrini, Jenna L ^a,b   Gard, Ashley L ^a   Gerhold, Kristin A ^c   Wilcox, Elise C ^a   Liu, Angela ^a   Schwan, Jonas ^a   Le, Andrew V ^b   Baevova, Pavlina ^b   Dimitrievska, Sashka ^a   Zhao, Liping ^b   Sundaram, Sumati ^b   Sun, Huanxing ^c   Rittié, Laure ^d   Dyal, Rachel ^d   Broekelmann, Tom J ^e   Mecham, Robert P ^e   Schwartz, Martin A ^a,c   Niklason, Laura E ^a,b   White, Eric S ^d  

^a Yale University   (United States)

^b YALE UNIVERSITY   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^e WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Bioactivity; Decellularization; Extracellular matrix; Lung tissue engineering

Indexed keywords

BIOACTIVITY; BIOLOGICAL ORGANS; BIOMECHANICS; CELL ADHESION; CELL ENGINEERING; CELLS; COLLAGEN; CYTOLOGY; ELASTIN; ENDOTHELIAL CELLS; GLYCOPROTEINS; RATS; TISSUE; TISSUE ENGINEERING;

CELL MATRIX INTERACTIONS; DECELLULARIZATION; DECELLULARIZED MATRICES; EXTRACELLULAR MATRICES; GLYCOSAMINOGLYCANS; HUMAN ENDOTHELIAL CELLS; REGENERATIVE MEDICINE; VASCULAR CELL ADHESION;

SCAFFOLDS (BIOLOGY);

COLLAGEN; DNA; ELASTIN; GLYCOSAMINOGLYCAN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN;

ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DECELLULARIZED LUNG MATRIX; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; INFLAMMATION; LUNG PARENCHYMA; LUNG SLICE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGENERATIVE MEDICINE; TISSUE ENGINEERING; ANIMAL; CELL LINE; CHEMISTRY; COMPARATIVE STUDY; CYTOLOGY; LUNG; PHYSIOLOGY; PIG; PROCEDURES; RAT; REGENERATION; TENSILE STRENGTH; TISSUE SCAFFOLD; ULTRASTRUCTURE;

ANIMALS; CELL LINE; COLLAGEN; ELASTIN; ENDOTHELIAL CELLS; EXTRACELLULAR MATRIX; GLYCOSAMINOGLYCANS; HUMANS; LUNG; RATS; REGENERATION; REGENERATIVE MEDICINE; SWINE; TENSILE STRENGTH; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84975887110     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2016.06.025     Document Type: Article

References (63)

1. [1] Yusen, R.D., Edwards, L.B., Kucheryavaya, A.Y., Benden, C., Dipchand, A.I., Dobbels, F., Goldfarb, S.B., Levvey, B.J., Lund, L.H., Meiser, B., Stehlik, J., International Society for H, Lung T. The registry of the International Society for Heart and Lung Transplantation: thirty-first adult lung and heart-lung transplant report–2014; focus theme: retransplantation. J. Heart Lung Transpl. 33 (2014), 1009–1024.
2. [2] Ott, H.C., Clippinger, B., Conrad, C., Schuetz, C., Pomerantseva, I., Ikonomou, L., Kotton, D., Vacanti, J.P., Regeneration and orthotopic transplantation of a bioartificial lung. Nat. Med. 16 (2010), 927–933.
3. [3] Price, A.P., England, K.A., Matson, A.M., Blazar, B.R., Panoskaltsis-Mortari, A., Development of a decellularized lung bioreactor system for bioengineering the lung: the matrix reloaded. Tissue Eng. Part A 16 (2010), 2581–2591.
4. [4] Nichols, J.E., Niles, J., Riddle, M., Vargas, G., Schilagard, T., Ma, L., Edward, K., La Francesca, S., Sakamoto, J., Vega, S., Ogadegbe, M., Mlcak, R., Deyo, D., Woodson, L., McQuitty, C., Lick, S., Beckles, D., Melo, E., Cortiella, J., Production and assessment of decellularized pig and human lung scaffolds. Tissue Eng. Part A 19 (2013), 2045–2062.
5. [5] Bonvillain, R.W., Danchuk, S., Sullivan, D.E., Betancourt, A.M., Semon, J.A., Eagle, M.E., Mayeux, J.P., Gregory, A.N., Wang, G., Townley, I.K., Borg, Z.D., Weiss, D.J., Bunnell, B.A., A nonhuman primate model of lung regeneration: detergent-mediated decellularization and initial in vitro recellularization with mesenchymal stem cells. Tissue Eng. Part A 18 (2012), 2437–2452.
6. [6] Vorotnikova, E., McIntosh, D., Dewilde, A., Zhang, J., Reing, J.E., Zhang, L., Cordero, K., Bedelbaeva, K., Gourevitch, D., Heber-Katz, E., Badylak, S.F., Braunhut, S.J., Extracellular matrix-derived products modulate endothelial and progenitor cell migration and proliferation in vitro and stimulate regenerative healing in vivo. Matrix Biol. 29 (2010), 690–700.
7. [7] Murray, J.C., Liotta, L., Rennard, S.I., Martin, G.R., Adhesion characteristics of murine metastatic and nonmetastatic tumor cells in vitro. Cancer Res. 40 (1980), 347–351.
8. [8] Clark, R.A., Nielsen, L.D., Welch, M.P., McPherson, J.M., Collagen matrices attenuate the collagen-synthetic response of cultured fibroblasts to TGF-beta. J. Cell Sci. 108:Pt 3 (1995), 1251–1261.
9. [9] Crapo, P.M., Medberry, C.J., Reing, J.E., Tottey, S., van der Merwe, Y., Jones, K.E., Badylak, S.F., Biologic scaffolds composed of central nervous system extracellular matrix. Biomaterials 33 (2012), 3539–3547.
10. [10] Reing, J.E., Brown, B.N., Daly, K.A., Freund, J.M., Gilbert, T.W., Hsiong, S.X., Huber, A., Kullas, K.E., Tottey, S., Wolf, M.T., Badylak, S.F., The effects of processing methods upon mechanical and biologic properties of porcine dermal extracellular matrix scaffolds. Biomaterials 31 (2010), 8626–8633.
11. [11] Balestrini, J.L., Billiar, K.L., Magnitude and duration of stretch modulate fibroblast remodeling. J. Biomech. Eng., 131, 2009, 051005.
12. [12] Balestrini, J.L., Chaudhry, S., Sarrazy, V., Koehler, A., Hinz, B., The mechanical memory of lung myofibroblasts. Integr. Biol. (Camb) 4 (2012), 410–421.
13. [13] Padmanabhan, P., Radhakrishnan, A., Venkataraman, A.P., Gupta, N., Srinivasan, B., Corneal changes following collagen cross linking and simultaneous topography guided photoablation with collagen cross linking for keratoconus. Indian J. Ophthalmol. 62 (2014), 229–235.
14. [14] Balestrini, J.L., Niklason, L.E., Extracellular matrix as a driver for lung regeneration. Ann. Biomed. Eng. 43:3 (March 2015), 568–576.
15. [15] O'Neill, J.D., Anfang, R., Anandappa, A., Costa, J., Javidfar, J., Wobma, H.M., Singh, G., Freytes, D.O., Bacchetta, M.D., Sonett, J.R., Vunjak-Novakovic, G., Decellularization of human and porcine lung tissues for pulmonary tissue engineering. Ann. Thorac. Surg. 96 (2013), 1046–1055 discussion 1055–1046.
16. [16] Wagner, D.E., Bonenfant, N.R., Sokocevic, D., DeSarno, M.J., Borg, Z.D., Parsons, C.S., Brooks, E.M., Platz, J.J., Khalpey, Z.I., Hoganson, D.M., Deng, B., Lam, Y.W., Oldinski, R.A., Ashikaga, T., Weiss, D.J., Three-dimensional scaffolds of acellular human and porcine lungs for high throughput studies of lung disease and regeneration. Biomaterials 35 (2014), 2664–2679.
17. [17] Gilpin, S.E., Guyette, J.P., Gonzalez, G., Ren, X., Asara, J.M., Mathisen, D.J., Vacanti, J.P., Ott, H.C., Perfusion decellularization of human and porcine lungs: bringing the matrix to clinical scale. J. Heart Lung Transpl. 33 (2014), 298–308.
18. [18] Price, A.P., Godin, L.M., Domek, A., Cotter, T., D'Cunha, J., Taylor, D.A., Panoskaltsis-Mortari, A., Automated decellularization of intact, human-sized lungs for tissue engineering. Tissue Eng. Part C Methods 21 (2015), 94–103.
19. [19] Cantu, E., Balsara, K.R., Li, B., Lau, C., Gibson, S., Wyse, A., Baig, K., Gaca, J., Gonzalez-Stawinski, G.V., Nichols, T., Parker, W., Davis, R.D., Prolonged function of macrophage, von Willebrand factor-deficient porcine pulmonary xenografts. Am. J. Transpl. 7 (2007), 66–75.
20. [20] Nguyen, B.N., Azimzadeh, A.M., Zhang, T., Wu, G., Schuurman, H.J., Sachs, D.H., Ayares, D., Allan, J.S., Pierson, R.N. 3rd, Life-supporting function of genetically modified swine lungs in baboons. J. Thorac. Cardiovasc Surg. 133 (2007), 1354–1363.
21. [21] Nguyen, B.N., Azimzadeh, A.M., Schroeder, C., Buddensick, T., Zhang, T., Laaris, A., Cochrane, M., Schuurman, H.J., Sachs, D.H., Allan, J.S., Pierson, R.N. 3rd, Absence of Gal epitope prolongs survival of swine lungs in an ex vivo model of hyperacute rejection. Xenotransplantation 18 (2011), 94–107.
22. [22] Stahl, W.R., Scaling of respiratory variables in mammals. J. Appl. Physiol. 22 (1967), 453–460.
23. [23] Tillery, S.I., Lehnert, B.E., Age-bodyweight relationships to lung growth in the F344 rat as indexed by lung weight measurements. Lab. Anim. 20 (1986), 189–194.
24. [24] Balestrini, J.L., Gard, A.L., Leiby, K.L., Calle, E., Sivarapatna, A., Kunkemoeller, B., Lin, T., Dimitrievska, S., Niklason, L.E., Production of decellularized porcine lung scaffolds for use in tissue engineering. Integr. Biol. (Camb.) 7:12 (2015 Dec), 1598–1610.
25. [25] Woessner, J.F., Boucek, R.J., Connective tissue development in subcutaneously implanted polyvinyl sponge. Arch. Biochem. Biophys. 93 (1961), 85–94.
26. [26] Swaminathan, G., Gadepalli, V.S., Stoilov, I., Mecham, R.P., Rao, R.R., Ramamurthi, A., Pro-elastogenic effects of bone marrow mesenchymal stem cell-derived smooth muscle cells on cultured aneurysmal smooth muscle cells. J. Tissue Eng. Regen. Med., 2014 Nov 6, 10.1002/term.1964.
27. [27] Warda, M., Gouda, E.M., Toida, T., Chi, L., Linhardt, R.J., Isolation and characterization of raw heparin from dromedary intestine: evaluation of a new source of pharmaceutical heparin. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 136 (2003), 357–365.
28. [28] Tsuchiya, T., Balestrini, J.L., Mendez, J., Calle, E.A., Zhao, L., Niklason, L.E., Influence of pH on extracellular matrix preservation during lung decellularization. Tissue Eng. Part C Methods 20 (2014), 1028–1036.
29. [29] Booth, A.J., Hadley, R., Cornett, A.M., Dreffs, A.A., Matthes, S.A., Tsui, J.L., Weiss, K., Horowitz, J.C., Fiore, V.F., Barker, T.H., Moore, B.B., Martinez, F.J., Niklason, L.E., White, E.S., Acellular normal and fibrotic human lung matrices as a culture system for in vitro investigation. Am. J. Respir. Crit. Care Med. 186 (2012), 866–876.
30. [30] Dimitrievska, S., Cai, C., Weyers, A., Balestrini, J.L., Lin, T., Sundaram, S., Hatachi, G., Spiegel, D.A., Kyriakides, T.R., Miao, J., Li, G., Niklason, L.E., Linhardt, R.J., Click-coated, heparinized, decellularized vascular grafts. Acta Biomater. 13 (2015), 177–187.
31. [31] Balestrini, J.L., Gard, A.L., Liu, A., Leiby, K.L., Schwan, J., Kunkemoeller, B., Calle, E.A., Sivarapatna, A., Lin, T., Dimitrievska, S., Cambpell, S.G., Niklason, L.E., Production of decellularized porcine lung scaffolds for use in tissue engineering. Integr. Biol. (Camb.) 7:12 (2015 Dec), 1598–1610.
32. [32] Balestrini, J.L., Liu, A., Gard, A.L., Huie, J.L., Blatt, K.M., Schwan, J., Broekelmann, T., Mecham, R., Wilcox, E.C., Zhao, L., Niklason, L., Sterilization of lung matrices by supercritical carbon dioxide. Tissue Eng. Part C Methods 22:3 (2016 Mar), 260–269.
33. [33] Hynes, R.O., The extracellular matrix: not just pretty fibrils. Science 326 (2009), 1216–1219.
34. [34] Hsia, C.C., Schmitz, A., Lambertz, M., Perry, S.F., Maina, J.N., Evolution of air breathing: oxygen homeostasis and the transitions from water to land and sky. Compr. Physiol. 3 (2013), 849–915.
35. [35] Section 3- selected biological properties of tissues: potential determinants of susceptibility to ultrasound-induced bioeffects. J. ultrasound Med. official J. Am. Inst. Ultrasound Med. 19 (2000), 85–168.
36. [36] Mercer, R.R., Russell, M.L., Crapo, J.D., Alveolar septal structure in different species. J. Appl. Physiol. 1994:77 (1985), 1060–1066.
37. [37] Hoyt, J.R., Hawkins, J.V., St Clair, M.B., Kennett, M.J., The Mouse in Biomedical Research: Normative Biology, Husbandry, and Models Burlington. 2006, Academic Press, Massachusetts.
38. [38] Mansell, A.L., Collins, M.H., Johnson, E. Jr., Gil, J., Postnatal growth of lung parenchyma in the piglet: morphometry correlated with mechanics. Anat. Rec. 241 (1995), 99–104.
39. [39] Starcher, B.C., Elastin and the lung. Thorax 41 (1986), 577–585.
40. [40] Salerno, F.G., Ludwig, M.S., Elastic moduli of excised constricted rat lungs. J. Appl. Physiol. 86 (1999), 66–70.
41. [41] Liu, F., Tschumperlin, D.J., Micro-mechanical characterization of lung tissue using atomic force microscopy. J. Vis. Exp., 2011 Aug 28 (54).
42. [42] Crapo, J.D., Barry, B.E., Gehr, P., Bachofen, M., Weibel, E.R., Cell number and cell characteristics of the normal human lung. Am. Rev. Respir. Dis. 126 (1982), 332–337.
43. [43] Pinkerton, K.E., Gehr, P., Crapo, J.D., Architecture and cellular composition of the air-blood barrier. Comp. Biol. Normal Lung 1 (1992), 121–128.
44. [44] Tsukahara, H., Noiri, E., Jiang, M.Z., Hiraoka, M., Mayumi, M., Role of nitric oxide in human pulmonary microvascular endothelial cell adhesion. Life Sci. 67 (2000), 1–11.
45. [45] Petersen, T.H., Calle, E.A., Colehour, M.B., Niklason, L.E., Matrix composition and mechanics of decellularized lung scaffolds. Cells Tissues Organs 195 (2012), 222–231.
46. [46] Al Jamal, R., Roughley, P.J., Ludwig, M.S., Effect of glycosaminoglycan degradation on lung tissue viscoelasticity. Am. J. Physiol. Lung Cell Mol. Physiol. 280 (2001), L306–L315.
47. [47] Houghton, A.M., Quintero, P.A., Perkins, D.L., Kobayashi, D.K., Kelley, D.G., Marconcini, L.A., Mecham, R.P., Senior, R.M., Shapiro, S.D., Elastin fragments drive disease progression in a murine model of emphysema. J. Clin. Invest. 116 (2006), 753–759.
48. [48] Massaro, D., Teich, N., Maxwell, S., Massaro, G.D., Whitney, P., Postnatal development of alveoli. Regulation and evidence for a critical period in rats. J. Clin. Invest. 76 (1985), 1297–1305.
49. [49] Winkler, G.C., Cheville, N.F., Morphometry of postnatal development in the porcine lung. Anat. Rec. 211 (1985), 427–433.
50. [50] Hyde, D.M., Robinson, N.E., Gillespie, J.R., Tyler, W.S., Morphometry of the distal air spaces in lungs of aging dogs. J. Appl. Physiol. Respir. Environ. Exerc Physiol. 43 (1977), 86–91.
51. [51] Shimura, S., Boatman, E.S., Martin, C.J., Effects of ageing on the alveolar pores of Kohn and on the cytoplasmic components of alveolar type II cells in monkey lungs. J. Pathol. 148 (1986), 1–11.
52. [52] Sokocevic, D., Bonenfant, N.R., Wagner, D.E., Borg, Z.D., Lathrop, M.J., Lam, Y.W., Deng, B., Desarno, M.J., Ashikaga, T., Loi, R., Hoffman, A.M., Weiss, D.J., The effect of age and emphysematous and fibrotic injury on the re-cellularization of de-cellularized lungs. Biomaterials 34 (2013), 3256–3269.
53. [53] Godin, L.M., Sandri, B.J., Wagner, D.E., Meyer, C.M., Price, A.P., Akinnola, I., Weiss, D.J., Panoskaltsis-Mortari, A., Decreased laminin expression by human lung epithelial cells and fibroblasts cultured in acellular lung scaffolds from aged mice. PLoS One, 11, 2016, e0150966.
54. [54] Versaevel, M., Grevesse, T., Gabriele, S., Spatial coordination between cell and nuclear shape within micropatterned endothelial cells. Nat. Commun., 3, 2012, 671.
55. [55] Orr, A.W., Hahn, C., Blackman, B.R., Schwartz, M.A., p21-activated kinase signaling regulates oxidant-dependent NF-kappa B activation by flow. Circ. Res. 103 (2008), 671–679.
56. [56] Wong, D., Dorovini-Zis, K., Expression of vascular cell adhesion molecule-1 (VCAM-1) by human brain microvessel endothelial cells in primary culture. Microvasc. Res. 49 (1995), 325–339.
57. [57] Kubicki, N., Laird, C., Burdorf, L., Pierson, R.N. 3rd, Azimzadeh, A.M., Current status of pig lung xenotransplantation. Int. J. Surg. 23:Pt B (2015 Nov), 247–254.
58. [58] Tible, M., Loupy, A., Vernerey, D., Suberbielle, C., Beuscart, T., Cazes, A., Guillemain, R., Amrein, C., Pezzella, V., Fabiani, J.N., Nochy, D., Hill, G., Empana, J.P., Jouven, X., Charron, D., Bruneval, P., Duong Van Huyen, J.P., Pathologic classification of antibody-mediated rejection correlates with donor-specific antibodies and endothelial cell activation. J. Heart Lung Transpl. 32 (2013), 769–776.
59. [59] Calle, E.A., Ghaedi, M., Sundaram, S., Sivarapatna, A., Tseng, M.K., Niklason, L.E., Strategies for whole lung tissue engineering. IEEE Trans. Biomed. Eng. 61 (2014), 1482–1496.
60. [60] Petersen, T.H., Calle, E.A., Zhao, L., Lee, E.J., Gui, L., Raredon, M.B., Gavrilov, K., Yi, T., Zhuang, Z.W., Breuer, C., Herzog, E., Niklason, L.E., Tissue-engineered lungs for in vivo implantation. Science 329 (2010), 538–541.
61. [61] Gilpin, S.E., Ott, H.C., Using nature's platform to engineer bio-artificial lungs. Ann. Am. Thorac. Soc. 12:Suppl 1 (2015), S45–S49.
62. [62] Wagner, D.E., Bonenfant, N.R., Parsons, C.S., Sokocevic, D., Brooks, E.M., Borg, Z.D., Lathrop, M.J., Wallis, J.D., Daly, A.B., Lam, Y.W., Deng, B., Desarno, M.J., Ashikaga, T., Loi, R., Weiss, D.J., Comparative decellularization and recellularization of normal versus emphysematous human lungs. Biomaterials 35 (2014), 3281–3297.
63. [63] Zvarova, B., Uhl, F.E., Uriarte, J.J., Borg, Z.D., Coffey, A.L., Bonenfant, N.R., Weiss, D.J., Wagner, D.E., Residual detergent detection method for non-destructive cytocompatibility evaluation of decellularized whole lung scaffolds. Tissue Eng. Part C Methods 22:5 (2016 May), 418–428.