Perfusion-decellularized pancreas as a natural 3D scaffold for pancreatic tissue and whole organ engineering

Biomaterials

Volumn 34, Issue 28, 2013, Pages 6760-6772

  Goh, Saik Kia ^a   Bertera, Suzanne ^b   Olsen, Phillip ^a   Candiello, Joseph E ^a   Halfter, Willi ^c   Uechi, Guy ^d   Balasubramani, Manimalha ^d   Johnson, Scott A ^d   Sicari, Brian M ^c,d   Kollar, Elizabeth ^d   Badylak, Stephen F ^a,d,e   Banerjee, Ipsita ^a,d  

^a University of Pittsburgh   (United States)

^b CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF PITTSBURGH   (United States)

^e UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

Author keywords

Extracellular matrix scaffold; Pancreatic cells; Tissue and organ engineering; Whole organ decellularization

Indexed keywords

CELLULAR FUNCTION; DECELLULARIZATION; EXTRACELLULAR MATRICES; MICRO ARCHITECTURES; PANCREATIC TISSUE; REGENERATIVE MEDICINE; TISSUE DEVELOPMENT; TREATMENT MEASURES;

BIOMECHANICS; CELL CULTURE; CELL ENGINEERING; CELLS; COMPUTER ARCHITECTURE; GENE EXPRESSION; INSULIN; RADIOACTIVE MATERIALS; TISSUE;

SCAFFOLDS (BIOLOGY);

TISSUE SCAFFOLD;

ACINAR CELL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ATOMIC FORCE MICROSCOPY; CELL COMPOSITION; CELL FUNCTION; ENGRAFTMENT; EXTRACELLULAR MATRIX; FEASIBILITY STUDY; FEMALE; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MASS SPECTROMETRY; MOUSE; NONHUMAN; PANCREAS; PANCREAS CELL; PERFUSION; PRIORITY JOURNAL; PROTEOMICS; REGENERATIVE MEDICINE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCANNING ELECTRON MICROSCOPY; TISSUE ENGINEERING; TISSUE STRUCTURE; TRANSMISSION ELECTRON MICROSCOPY; UPREGULATION;

ANIMALS; EXTRACELLULAR MATRIX; FEMALE; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED ICR; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, ELECTRON, TRANSMISSION; PANCREAS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84879459481     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2013.05.066     Document Type: Article

References (69)

1. Shaw J.E., Sicree R.A., Zimmet P.Z. Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Res Clin Pract 2010, 87:4-14.
2. Bloomgarden Z.T. Diabetes complications. Diabetes Care 2004, 27:1506-1514.
3. Langer R., Vacanti J.P. Tissue engineering. Science 1993, 260:920-926.
4. Griffith L.G., Naughton G. Tissue engineering-current challenges and expanding opportunities. Science 2002, 295:1009-1014.
5. Shin H., Jo S., Mikos A.G. Biomimetic materials for tissue engineering. Biomaterials 2003, 24:4353-4364.
6. Stendahl J.C., Kaufman D.B., Stupp S.I. Extracellular matrix in pancreatic islets: relevance to scaffold design and transplantation. Cell Transplant 2009, 18:1-12.
7. Vaithilingam V., Tuch B.E. Islet transplantation and encapsulation: an update on recent developments. Rev Diabet Stud 2011, 8:51-67.
8. Brown B.N., Barnes C.A., Kasick R.T., Michel R., Gilbert T.W., Beer-Stolz D., et al. Surface characterization of extracellular matrix scaffolds. Biomaterials 2010, 31:428-437.
9. Sellaro T.L., Ravindra A.K., Stolz D.B., Badylak S.F. Maintenance of hepatic sinusoidal endothelial cell phenotype invitro using organ-specific extracellular matrix scaffolds. Tissue Eng 2007, 13:2301-2310.
10. Cheng J.Y., Raghunath M., Whitelock J., Poole-Warren L. Matrix components and scaffolds for sustained islet function. Tissue Eng Part B Rev 2011, 17:235-247.
11. Candiello J., Cole G.J., Halfter W. Age-dependent changes in the structure, composition and biophysical properties of a human basement membrane. Matrix Biol 2010, 29:402-410.
12. Brafman D.A., Shah K.D., Fellner T., Chien S., Willert K. Defining long-term maintenance conditions of human embryonic stem cells with arrayed cellular microenvironment technology. Stem Cells Dev 2009, 18:1141-1154.
13. Flaim C.J., Teng D., Chien S., Bhatia S.N. Combinatorial signaling microenvironments for studying stem cell fate. Stem Cells Dev 2008, 17:29-39.
14. Weber L.M., Anseth K.S. Hydrogel encapsulation environments functionalized with extracellular matrix interactions increase islet insulin secretion. Matrix Biol 2008, 27:667-673.
15. Weber L.M., Hayda K.N., Anseth K.S. Cell-matrix interactions improve beta-cell survival and insulin secretion in three-dimensional culture. Tissue Eng Part A 2008, 14:1959-1968.
16. Ott H.C., Matthiesen T.S., Goh S.K., Black L.D., Kren S.M., Netoff T.I., et al. Perfusion-decellularized matrix: using nature's platform to engineer a bioartificial heart. Nat Med 2008, 14:213-221.
17. Wainwright J.M., Czajka C.A., Patel U.B., Freytes D.O., Tobita K., Gilbert T.W., et al. Preparation of cardiac extracellular matrix from an intact porcine heart. Tissue Eng Part C Methods 2010, 16:525-532.
18. Remlinger N.T., Wearden P.D., Gilbert T.W. Procedure for decellularization of porcine heart by retrograde coronary perfusion. JVis Exp 2012, e50059.
19. Ng S.L., Narayanan K., Gao S., Wan A.C. Lineage restricted progenitors for the repopulation of decellularized heart. Biomaterials 2011, 32:7571-7580.
20. Uygun B.E., Soto-Gutierrez A., Yagi H., Izamis M.L., Guzzardi M.A., Shulman C., et al. Organ reengineering through development of a transplantable recellularized liver graft using decellularized liver matrix. Nat Med 2010, 16:814-820.
21. Soto-Gutierrez A., Zhang L., Medberry C., Fukumitsu K., Faulk D., Jiang H., et al. Awhole-organ regenerative medicine approach for liver replacement. Tissue Eng Part C Methods 2011, 17:677-686.
22. Shupe T., Williams M., Brown A., Willenberg B., Petersen B.E. Method for the decellularization of intact rat liver. Organogenesis 2010, 6:134-136.
23. Baptista P.M., Siddiqui M.M., Lozier G., Rodriguez S.R., Atala A., Soker S. The use of whole organ decellularization for the generation of a vascularized liver organoid. Hepatology 2011, 53:604-617.
24. Ott H.C., Clippinger B., Conrad C., Schuetz C., Pomerantseva I., Ikonomou L., et al. Regeneration and orthotopic transplantation of a bioartificial lung. Nat Med 2010, 16:927-933.
25. Petersen T.H., Calle E.A., Zhao L., Lee E.J., Gui L., Raredon M.B., et al. Tissue-engineered lungs for invivo implantation. Science 2010, 329:538-541.
26. 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 2010, 16:2581-2591.
27. Daly A.B., Wallis J.M., Borg Z.D., Bonvillain R.W., Deng B., Ballif B.A., et al. Initial binding and recellularization of decellularized mouse lung scaffolds with bone marrow-derived mesenchymal stromal cells. Tissue Eng Part A 2012, 18:1-16.
28. Wallis J.M., Borg Z.D., Daly A.B., Deng B., Ballif B.A., Allen G.B., et al. Comparative assessment of detergent-based protocols for mouse lung de-cellularization and re-cellularization. Tissue Eng Part C Methods 2012, 18:420-432.
29. Bonvillain R.W., Danchuk S., Sullivan D.E., Betancourt A.M., Semon J.A., Eagle M.E., et al. Anonhuman primate model of lung regeneration: detergent-mediated decellularization and initial invitro recellularization with mesenchymal stem cells. Tissue Eng Part A 2012, 18:2437-2452.
30. Sullivan D.C., Mirmalek-Sani S.H., Deegan D.B., Baptista P.M., Aboushwareb T., Atala A., et al. Decellularization methods of porcine kidneys for whole organ engineering using a high-throughput system. Biomaterials 2012, 33:7756-7764.
31. Ross E.A., Williams M.J., Hamazaki T., Terada N., Clapp W.L., Adin C., et al. Embryonic stem cells proliferate and differentiate when seeded into kidney scaffolds. JAm Soc Nephrol 2009, 20:2338-2347.
32. Song J.J., Guyette J.P., Gilpin S.E., Gonzalez G., Vacanti J.P., Ott H.C. Regeneration and experimental orthotopic transplantation of a bioengineered kidney. Nat Med 2013, 19:646-651.
33. Conrad C., Schuetz C., Clippinger B., Vacanti J.P., Markmann J.F., Ott H.C. Bio-engineered endocrine pancreas based on decellularized pancreatic matrix and mesenchymal stem cell/islet cell coculture. JAm Coll Surgeons 2010, 211:S62.
34. Goh S.-K., Bertera S., Banerjee I. Perfusion-decellularization of pancreatic matrix- a scaffold for bio-engineered pancreas 2011, AIChE. Minneapolis Convention Center, Minnesota.
35. Goh S.K., Bertera S., Banerjee I. Perfusion-decellularization of pancreas as a scaffold for the differentiation of human embryonic stem cells into insulin-producing cells. 10th annual scientific meeting of int soc stem cell res. Yokohama, Japan 2012, 67.
36. Mirmalek-Sani S.-H., Orlando G., McQuilling J.P., Pareta R., Mack D.L., Salvatori M., et al. Porcine pancreas extracellular matrix as a platform for endocrine pancreas bioengineering. Biomaterials 2013, 34:5488-5495.
37. Thivolet C.H., Chatelain P., Nicoloso H., Durand A., Bertrand J. Morphological and functional effects of extracellular matrix on pancreatic islet cell cultures. Exp Cell Res 1985, 159:313-322.
38. Nikolova G., Jabs N., Konstantinova I., Domogatskaya A., Tryggvason K., Sorokin L., et al. The vascular basement membrane: a niche for insulin gene expression and beta cell proliferation. Dev Cell 2006, 10:397-405.
39. Tian X.H., Xue W.J., Ding X.M., Pang X.L., Teng Y., Tian P.X., et al. Small intestinal submucosa improves islet survival and function during invitro culture. World J Gastroenterol 2005, 11:7378-7383.
40. Woods E.J., Walsh C.M., Sidner R.A., Zieger M.A.J., Lakey J.R.T., Ricordi C., et al. Improved invitro function of islets using small intestinal submucosa. Transplant Proc 2004, 36:1175-1177.
41. De Carlo E., Baiguera S., Conconi M.T., Vigolo S., Grandi C., Lora S., et al. Pancreatic acellular matrix supports islet survival and function in a synthetic tubular device: invitro and invivo studies. Int J Mol Med 2010, 25:195-202.
42. Cukierman E., Pankov R., Stevens D.R., Yamada K.M. Taking cell-matrix adhesions to the third dimension. Science 2001, 294:1708-1712.
43. Goh S.-K., Olsen P., Banerjee I. Extracellular matrix aggregates from differentiating embryoid bodies as a scaffold to support ESC proliferation and differentiation. PLoS One 2013, 8:e61856.
44. Balasubramani M., Schreiber E.M., Candiello J., Balasubramani G.K., Kurtz J., Halfter W. Molecular interactions in the retinal basement membrane system: a proteomic approach. Matrix Biol 2010, 29:471-483.
45. Candiello J., Balasubramani M., Schreiber E.M., Cole G.J., Mayer U., Halfter W., et al. Biomechanical properties of native basement membranes. FEBS J 2007, 274:2897-2908.
46. Meyer T., Chodnewska I., Czub S., Hamelmann W., Beutner U., Otto C., et al. Extracellular matrix proteins in the porcine pancreas: a structural analysis for directed pancreatic islet isolation. Transplant Proc 1998, 30:354.
47. Meyer T., Czub S., Chodnewska I., Beutner U., Hamelmann W., Klock G., et al. Expression pattern of extracellular matrix proteins in the pancreas of various domestic pig breeds, the goettingen minipig and the wild boar. Ann Transplant 1997, 2:17-26.
48. Crapo P.M., Gilbert T.W., Badylak S.F. An overview of tissue and whole organ decellularization processes. Biomaterials 2011, 32:3233-3243.
49. Keane T.J., Londono R., Turner N.J., Badylak S.F. Consequences of ineffective decellularization of biologic scaffolds on the host response. Biomaterials 2012, 33:1771-1781.
50. Schuppin G.T., Bonner-Weir S., Montana E., Kaiser N., Weir G.C. Replication of adult pancreatic-beta cells cultured on bovine corneal endothelial cell extracellular matrix. InVitro Cell Dev Biol Anim 1993, 29A:339-344.
51. Daoud J., Petropavlovskaia M., Rosenberg L., Tabrizian M. The effect of extracellular matrix components on the preservation of human islet function invitro. Biomaterials 2010, 31:1676-1682.
52. Wang R.N., Rosenberg L. Maintenance of beta-cell function and survival following islet isolation requires re-establishment of the islet-matrix relationship. JEndocrinol 1999, 163:181-190.
53. Badylak S.F., Taylor D., Uygun K. Whole-organ tissue engineering: decellularization and recellularization of three-dimensional matrix scaffolds. Annu Rev Biomed Eng 2011, 13:27-53.
54. Cortiella J., Niles J., Cantu A., Brettler A., Pham A., Vargas G., et al. Influence of acellular natural lung matrix on murine embryonic stem cell differentiation and tissue formation. Tissue Eng Part A 2010, 16:2565-2580.
55. Shamis Y., Hasson E., Soroker A., Bassat E., Shimoni Y., Ziv T., et al. Organ-specific scaffolds for invitro expansion, differentiation, and organization of primary lung cells. Tissue Eng Part C Methods 2011, 17:861-870.
56. Nakayama K.H., Batchelder C.A., Lee C.I., Tarantal A.F. Decellularized rhesus monkey kidney as a three-dimensional scaffold for renal tissue engineering. Tissue Eng Part A 2010, 16:2207-2216.
57. Mauck R.L., Baker B.M., Nerurkar N.L., Burdick J.A., Li W.J., Tuan R.S., et al. Engineeringon the straight and narrow: the mechanics of nanofibrous assemblies for fiber-reinforced tissue regeneration. Tissue Eng Part B Rev 2009, 15:171-193.
58. Soto-Gutierrez A., Wertheim J.A., Ott H.C., Gilbert T.W. Perspectives on whole-organ assembly: moving toward transplantation on demand. JClin Invest 2012, 122:3817-3823.
59. Song J.J., Ott H.C. Organ engineering based on decellularized matrix scaffolds. Trends Mol Med 2011, 17:424-432.
60. Nagata S., Hanayama R., Kawane K. Autoimmunity and the clearance of dead cells. Cell 2010, 140:619-630.
61. Brown B.N., Valentin J.E., Stewart-Akers A.M., McCabe G.P., Badylak S.F. Macrophage phenotype and remodeling outcomes in response to biologic scaffolds with and without a cellular component. Biomaterials 2009, 30:1482-1491.
62. Williams C., Liao J., Joyce E.M., Wang B., Leach J.B., Sacks M.S., et al. Altered structural and mechanical properties in decellularized rabbit carotid arteries. Acta Biomater 2009, 5:993-1005.
63. Gratzer P.F., Harrison R.D., Woods T. Matrix alteration and not residual sodium dodecyl sulfate cytotoxicity affects the cellular repopulation of a decellularized matrix. Tissue Eng 2006, 12:2975-2983.
64. Engler A.J., Sen S., Sweeney H.L., Discher D.E. Matrix elasticity directs stem cell lineage specification. Cell 2006, 126:677-689.
65. Discher D.E., Janmey P., Wang Y.L. Tissue cells feel and respond to the stiffness of their substrate. Science 2005, 310:1139-1143.
66. Wang Y., Cui C.B., Yamauchi M., Miguez P., Roach M., Malavarca R., et al. Lineage restriction of human hepatic stem cells to mature fates is made efficient by tissue-specific biomatrix scaffolds. Hepatology 2011, 53:293-305.
67. Chun T.-H., Hotary K.B., Sabeh F., Saltiel A.R., Allen E.D., Weiss S.J. Apericellular collagenase directs the 3-dimensional development of white adipose tissue. Cell 2006, 125:577-591.
68. Hotary K.B., Allen E.D., Brooks P.C., Datta N.S., Long M.W., Weiss S.J. Membrane type I matrix metalloproteinase usurps tumor growth control imposed by the three-dimensional extracellular matrix. Cell 2003, 114:33-45.
69. Badylak S.F., Freytes D.O., Gilbert T.W. Extracellular matrix as a biological scaffold material: structure and function. Acta Biomater 2009, 5:1-13.