Assessing the functional mechanical properties of bioengineered organs with emphasis on the lung

Journal of Cellular Physiology

Volumn 229, Issue 9, 2014, Pages 1134-1140

  Suki, Béla ^a  

^a Boston University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; ELASTIN; PROTEOGLYCAN;

AIRWAY RESISTANCE; ARTICLE; ATOMIC FORCE MICROSCOPY; BIOARTIFICIAL ORGAN; BREATHING RATE; CELL DIFFERENTIATION; EXTRACELLULAR MATRIX; FOURIER TRANSFORMATION; HUMAN; LUNG; LUNG COMPLIANCE; MECHANICAL STRESS; MECHANICS; MULTIPHOTON MICROSCOPY; OSCILLATION; PRIORITY JOURNAL; SURFACE TENSION; TOTAL LUNG CAPACITY; VOLUMETRY;

ANIMALS; BIOARTIFICIAL ORGANS; BIOMECHANICAL PHENOMENA; CELL DIFFERENTIATION; CELL PROLIFERATION; COLLAGEN; ELASTICITY; ELASTIN; EXTRACELLULAR MATRIX; HUMANS; LUNG; LUNG VOLUME MEASUREMENTS; MICROSCOPY, ATOMIC FORCE; MODELS, BIOLOGICAL; OSCILLOMETRY; PRESSURE; PROTEOGLYCANS; REGENERATIVE MEDICINE; RESPIRATION; STEM CELLS; STRESS, MECHANICAL; TISSUE ENGINEERING; TISSUE SCAFFOLDS; X-RAY MICROTOMOGRAPHY;

EID: 84901227902     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.24600     Document Type: Article

References (68)

1. Al Jamal R, Roughley PJ, Ludwig MS. 2001. Effect of glycosaminoglycan degradation on lung tissue viscoelasticity. Am J Physiol Lung Cell Mol Physiol 280:L306-L315.
2. Alencar AM, Hantos Z, Petak F, Tolnai J, Asztalos T, Zapperi S, Andrade JS, Jr., Buldyrev SV, Stanley HE, Suki B. 1999. Scaling behavior in crackle sound during lung inflation. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics 60:4659-4663.
3. Arribas SM, Hinek A, Gonzalez MC. 2006. Elastic fibres and vascular structure in hypertension. Pharmacology & therapeutics 111:771-791.
4. Badylak SF, Weiss DJ, Caplan A, Macchiarini P. 2012. Engineered whole organs and complex tissues. Lancet 379:943-952.
5. Bates JH, Irvin CG, Farre R, Hantos Z. 2011. Oscillation mechanics of the respiratory system. Comprehensive Physiology 1:1233-1272.
6. Binnig G, Quate CF, Gerber C. 1986. Atomic force microscope. Phys Rev Lett 56:930-933.
7. Black LD, Allen PG, Morris SM, Stone PJ, Suki B. 2008. Mechanical and failure properties of extracellular matrix sheets as a function of structural protein composition. Biophys J 94:1916-1929.
8. Booth AJ, Hadley R, Cornett AM, Dreffs AA, Matthes SA, Tsui JL, Weiss K, Horowitz JC, Fiore VF, Barker TH, Moore BB, Martinez FJ, Niklason LE, White ES. 2012. Acellular normal and fibrotic human lung matrices as a culture system for in vitro investigation. Am J Respir Crit Care Med 186:866-876.
9. Boyd M, Flasza M, Johnson PA, Roberts JS, Kemp P. 2007. Integration and persistence of an investigational human living skin equivalent (ICX-SKN) in human surgical wounds. Regen Med 2:363-370.
10. Brewer KK, Sakai H, Alencar AM, Majumdar A, Arold SP, Lutchen KR, Ingenito EP, Suki B. 2003. Lung and alveolar wall elastic and hysteretic behavior in rats: Effects of in vivo elastase treatment. J Appl Physiol 95:1926-1936.
11. Brodt MD, Swan CC, Brown TD. 1998. Mechanical behavior of human morselized cancellous bone in triaxial compression testing. J Orthop Res 16:43-49.
12. Buschmann MD, Grodzinsky AJ. 1995. A molecular model of proteoglycan-associated electrostatic forces in cartilage mechanics. J Biomech Eng 117:179-192.
13. Cavalcante FS, Ito S, Brewer KK, Sakai H, Alencar AM, Almeida MP, Andrade JS, Jr., Majumdar A, Ingenito EP, Suki B. 2005. Mechanical interactions between collagen and proteoglycans: Implications for the stability of lung tissue. J Appl Physiol 98:672-679.
14. Chalmers GW, Gosline JM, Lillie MA. 1999. The hydrophobicity of vertebrate elastins. J Exp Biol 202:301-314.
15. Cheng JK, Wagenseil JE. 2012. Extracellular matrix and the mechanics of large artery development. Biomech Model Mechanobiol 11:1169-1186.
16. Chiquet M, Renedo AS, Huber F, Fluck M. 2003. How do fibroblasts translate mechanical signals into changes in extracellular matrix production? Matrix Biol 22:73-80.
17. Cigliano A, Gandaglia A, Lepedda AJ, Zinellu E, Naso F, Gastaldello A, Aguiari P, De Muro P, Gerosa G, Spina M, Formato M. 2012. Fine structure of glycosaminoglycans from fresh and decellularized porcine cardiac valves and pericardium. Biochem Res Int 2012:979351.
18. Cox G, Kable E, Jones A, Fraser I, Manconi F, Gorrell MD. 2003. 3-dimensional imaging of collagen using second harmonic generation. J Struct Biol 141:53-62.
19. Daly AB, Wallis JM, Borg ZD, Bonvillain RW, Deng B, Ballif BA, Jaworski DM, Allen GB, Weiss DJ. 2012. Initial binding and recellularization of decellularized mouse lung scaffolds with bone marrow-derived mesenchymal stromal cells. Tissue Eng Part A 18:1-16.
20. Davey BL, Bates JH. 1993. Regional lung impedance from forced oscillations through alveolar capsules. Respir Physiol 91:165-182.
21. Discher DE, Janmey P, Wang YL. 2005. Tissue cells feel and respond to the stiffness of their substrate. Science 310:1139-1143.
22. Engler AJ, Sen S, Sweeney HL, Discher DE. 2006. Matrix elasticity directs stem cell lineage specification. Cell 126:677-689.
23. Evans ND, Oreffo RO, Healy E, Thurner PJ, Man YH. 2013. Epithelial mechanobiology, skin wound healing, and the stem cell niche. J Mech Behav Biomed Mater 28:397-409.
24. Fratzl P, Daxer A. 1993. Structural transformation of collagen fibrils in corneal stroma during drying. An x-ray scattering study. Biophys J 64:1210-1214.
25. Halter JM, Steinberg JM, Schiller HJ, DaSilva M, Gatto LA, Landas S, Nieman GF. 2003. Positive end-expiratory pressure after a recruitment maneuver prevents both alveolar collapse and recruitment/derecruitment. Am J Respir Crit Care Med 167:1620-1626.
26. Hantos Z, Daroczy B, Suki B, Nagy S, Fredberg JJ. 1992. Input impedance and peripheral inhomogeneity of dog lungs. J Appl Physiol 72:168-178.
27. Ingber DE. 2002. Mechanical signaling and the cellular response to extracellular matrix in angiogenesis and cardiovascular physiology. Circ Res 91:877-887.
28. Ito S, Ingenito EP, Arold SP, Parameswaran H, Tgavalekos NT, Lutchen KR, Suki B. 2004. Tissue heterogeneity in the mouse lung: effects of elastase treatment. J Appl Physiol 97:204-212.
29. Ito S, Ingenito EP, Brewer KK, Black LD, Parameswaran H, Lutchen KR, Suki B. 2005. Mechanics, nonlinearity, and failure strength of lung tissue in a mouse model of emphysema: Possible role of collagen remodeling. J Appl Physiol 98:503-511.
30. Jesudason R, Sato S, Parameswaran H, Araujo AD, Majumdar A, Allen PG, Bartolak-Suki E, Suki B. 2010. Mechanical forces regulate elastase activity and binding site availability in lung elastin. Biophys J 99:3076-3083.
31. Keyes JT, Yan D, Rader JH, Utzinger U, Vande Geest JP. 2011. A gimbal-mounted pressurization chamber for macroscopic and microscopic assessment of ocular tissues. J Biomech Eng 133:095001.
32. Kononov S, Brewer K, Sakai H, Cavalcante FS, Sabayanagam CR, Ingenito EP, Suki B. 2001. Roles of mechanical forces and collagen failure in the development of elastase-induced emphysema. Am J Respir Crit Care Med 164:1920-1926.
33. Kroon M, Holzapfel GA. 2008. A new constitutive model for multi-layered collagenous tissues. J Biomech 41:2766-2771.
34. Laprad AS, Szabo TL, Suki B, Lutchen KR. 2010. Tidal stretches do not modulate responsiveness of intact airways in-vitro. J Appl Physiol.
35. Liao D, Zhao J, Gregersen H. 2010. 3d Mechanical properties of the partially obstructed guinea pig small intestine. J Biomech 43:2079-2086.
36. Luque T, Melo E, Garreta E, Cortiella J, Nichols J, Farre R, Navajas D. 2013. Local micromechanical properties of decellularized lung scaffolds measured with atomic force microscopy. Acta Biomater 9:6852-6859.
37. Maksym GN, Bates JH. 1997. A distributed nonlinear model of lung tissue elasticity. J Appl Physiol 82:32-41.
38. Mammoto T, Mammoto A, Ingber DE. 2013. Mechanobiology and developmental control. Annu Rev Cell Dev Biol 29:27-61.
39. Metzler SA, Digesu CS, Howard JI, Filip To SD, Warnock JN. 2012. Live en face imaging of aortic valve leaflets under mechanical stress. Biomech Model Mechanobiol 11:355-361.
40. Navajas D, Moretto A, Rotger M, Nagase T, Dallaire MJ, Ludwig MS. 1995. Dynamic elastance and tissue resistance of isolated liquid-filled rat lungs. J Appl Physiol 79:1595-1600.
41. Nonaka PN, Campillo N, Uriarte JJ, Garreta E, Melo E, de Oliveira LV, Navajas D, Farre R. 2014. Effects of freezing/thawing on the mechanical properties of decellularized lungs. J Biomed Mater Res Part A 102:413-419.
42. Otis DR, Jr., Petak F, Hantos Z, Fredberg JJ, Kamm RD. 1996. Airway closure and reopening assessed by the alveolar capsule oscillation technique. J Appl Physiol 80:2077-2084.
43. Ott HC, Clippinger B, Conrad C, Schuetz C, Pomerantseva I, Ikonomou L, Kotton D, Vacanti JP. 2010. Regeneration and orthotopic transplantation of a bioartificial lung. Nat Med 16:927-933.
44. Ott HC, Matthiesen TS, Goh SK, Black LD, Kren SM, Netoff TI, Taylor DA. 2008. Perfusion-decellularized matrix: Using nature's platform to engineer a bioartificial heart. Nat Med 14:213-221.
45. Parameswaran H, Bartolak-Suki E, Hamakawa H, Majumdar A, Allen PG, Suki B. 2009. Three-dimensional measurement of alveolar airspace volumes in normal and emphysematous lungs using micro-CT. J Appl Physiol 107:583-592.
46. Petersen TH, Calle EA, Colehour MB, Niklason LE. 2012. Matrix composition and mechanics of decellularized lung scaffolds. Cells Tissues Organs 195:222-231.
47. Petersen TH, Calle EA, Zhao L, Lee EJ, Gui L, Raredon MB, Gavrilov K, Yi T, Zhuang ZW, Breuer C, Herzog E, Niklason LE. 2010. Tissue-engineered lungs for in vivo implantation. Science 329:538-541.
48. Quint C, Arief M, Muto A, Dardik A, Niklason LE. 2012. Allogeneic human tissue-engineered blood vessel. J Vasc Sur 55:790-798.
49. Radosevich AJ, Bouchard MB, Burgess SA, Chen BR, Hillman EM. 2008. Hyperspectral in vivo two-photon microscopy of intrinsic contrast. Opt Lett 33:2164-2166.
50. Ritter MC, Jesudason R, Majumdar A, Stamenovic D, Buczek-Thomas JA, Stone PJ, Nugent MA, Suki B. 2009. A zipper network model of the failure mechanics of extracellular matrices. Proc Natl Acad Sci USA 106:1081-1086.
51. Schwenninger D, Runck H, Schumann S, Haberstroh J, Priebe HJ, Guttmann J. 2013. Endoscopic imaging to assess alveolar mechanics during quasi-static and dynamic ventilatory conditions in rats with noninjured and injured lungs. Crit Care Med 41:1286-1295.
52. Stamenovic D, Yager D. 1988. Elastic properties of air- and liquid-filled lung parenchyma. J Appl Physiol 65:2565-2570.
53. Stolz M, Raiteri R, Daniels AU, VanLandingham MR, Baschong W, Aebi U. 2004. Dynamic elastic modulus of porcine articular cartilage determined at two different levels of tissue organization by indentation-type atomic force microscopy. Biophys J 86:3269-3283.
54. Suki B, Barabasi AL, Hantos Z, Petak F, Stanley HE. 1994. Avalanches and power-law behaviour in lung inflation. Nature 368:615-618.
55. Suki B, Bates JH. 2008. Extracellular matrix mechanics in lung parenchymal diseases. Respir Physiol Neurobiol 163:33-43.
56. Suki B, Stamenovic D, Hubmayr RD. 2011. Lung Parenchymal Mechanics. In: Fredberg JJ Sieck GC Gerthoffer WT editors. Comprehensive physiology, the respiratory system, respiration mechanics: organ, cell, molecule. Wiley-Blackwell. pp 1317-1351.
57. Sullivan DC, Mirmalek-Sani SH, Deegan DB, Baptista PM, Aboushwareb T, Atala A, Yoo JJ. 2012. Decellularization methods of porcine kidneys for whole organ engineering using a high-throughput system. Biomaterials 33:7756-7764.
58. Takahashi A, Majumdar A, Parameswaran H, Bartolak-Suki E, Suki B. 2014. Proteoglycans maintain lung stability in an elastase-treated mouse model of emphysema. Am J Respir Cell Mol Biol doi: 10.1165/rcmb.2013-0179OC.
59. Tang Y, Ballarini R, Buehler MJ, Eppell SJ. 2010. Deformation micromechanisms of collagen fibrils under uniaxial tension. J R Soc Interface 7:839-850.
60. Vawter DL, Fung YC, West JB. 1978. Elasticity of excised dog lung parenchyma. J Appl Physiol Respir Environ Exerc Physiol 45:261-269.
61. Venegas JG, Harris RS, Simon BA. 1998. A comprehensive equation for the pulmonary pressure-volume curve. J Appl Physiol 84:389-395.
62. Wagner D, Fenn S, Bonenfant N, Marks E, Borg Z, Saunders P, Oldinski R, Weiss D. 2014. Design and synthesis of an artificial pulmonary pleura for high throughput studies in acellular human lungs. Cel Mol Bioeng 1-12.
63. Wallis JM, Borg ZD, Daly AB, Deng B, Ballif BA, Allen GB, Jaworski DM, Weiss DJ. 2012. Comparative assessment of detergent-based protocols for mouse lung de-cellularization and re-cellularization. Tissue Eng Part C Methods 18:420-432.
64. Withers JR, Aston DE. 2006. Nanomechanical measurements with AFM in the elastic limit. Adv Colloid Interface Sci 120:57-67.
65. Yuan H, Ingenito EP, Suki B. 1997. Dynamic properties of lung parenchyma: Mechanical contributions of fiber network and interstitial cells. J Appl Physiol 83:1420-1431. discussion 1418-1429.
66. Yuan H, Kononov S, Cavalcante FS, Lutchen KR, Ingenito EP, Suki B. 2000. Effects of collagenase and elastase on the mechanical properties of lung tissue strips. J Appl Physiol 89:3-14.
67. Zou Y, Zhang Y. 2009. An experimental and theoretical study on the anisotropy of elastin network. Ann Biomed Eng 37:1572-1583.
68. Zou Y, Zhang Y. 2012. Mechanical evaluation of decellularized porcine thoracic aorta. J Surg Res 175:359-368.