Preparation of immunogen-reduced and biocompatible extracellular matrices from porcine liver

Journal of Bioscience and Bioengineering

Volumn 115, Issue 2, 2013, Pages 207-215

  Park, Kyung Mee ^a   Park, Sung Min ^a   Yang, Se Ran ^a   Hong, Seok Ho ^a   Woo, Heung Myong ^a,b  

^a Kangwon National University   (South Korea)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

1,3 gal; Biomaterial; Biomatrix; ECM; Extracellular matrices (ECM); GAGs; H E; Immunogen; Liver; PERV; Porcine; SDS; SLA 2; SLA DRA; TX

Indexed keywords

1,3 GAL; BIOMATRIX; EXTRACELLULAR MATRICES; GAGS; IMMUNOGEN; PERV; PORCINE; SDS; SLA-2; SLA-DRA; TX;

ANTIGENS; BIOMATERIALS; BIOMEDICAL ENGINEERING; DNA SEQUENCES; LIVER; MEDICAL APPLICATIONS; MILITARY ELECTRONIC COUNTERMEASURES; TISSUE; VIRUSES;

POLYMERASE CHAIN REACTION;

COLLAGEN; DNA FRAGMENT; GALACTOSE ALPHA 1,3 GALACTOSE BETA 1,4 N ACETYLGLUCOSAMINE; GLYCOSAMINOGLYCAN; LEUKOCYTE ANTIGEN; N ACETYLGLUCOSAMINE; SWINE LEUKOCYTE ANTIGEN; UNCLASSIFIED DRUG; VIRUS ANTIGEN;

ARTICLE; BIOCOMPATIBILITY; CONTROLLED STUDY; DNA SEQUENCE; ENDOGENOUS RETROVIRUS; EXTRACELLULAR MATRIX; EXTRACELLULAR SPACE; LIVER; LIVER TRANSPLANTATION; NONHUMAN; POLYMERASE CHAIN REACTION; PORCINE ENDOGENOUS RETROVIRUS;

ANIMALS; ANTIGENS; BIOCOMPATIBLE MATERIALS; CELL SEPARATION; COLLAGEN; DNA; ENDOGENOUS RETROVIRUSES; EXTRACELLULAR MATRIX; GLYCOSAMINOGLYCANS; GRAFT REJECTION; GUIDED TISSUE REGENERATION; HISTOCOMPATIBILITY ANTIGENS CLASS II; LIVER; LIVER TRANSPLANTATION; SUS SCROFA; TISSUE ENGINEERING; TISSUE SCAFFOLDS; TRANSPLANTATION, HETEROLOGOUS;

PORCINE ENDOGENOUS RETROVIRUS; SUIDAE; SUS;

EID: 84871933113     PISSN: 13891723     EISSN: 13474421     Source Type: Journal    
DOI: 10.1016/j.jbiosc.2012.08.023     Document Type: Article

References (65)

1. Uygun B.E., Soto-Gutierrez A., Yagi H., Izamis M.L., Guzzardi M.A., Shulman C., Milwid J., Kobayashi N., Tilles A., Berthiaume F., other 9 authors Organ reengineering through development of a transplantable recellularized liver graft using decellularized liver matrix. Nat. Med. 2010, 16:814-820.
2. Lin P., Chan W.C., Badylak S.F., Bhatia S.N. Assessing porcine liver-derived biomatrix for hepatic tissue engineering. Tissue Eng. 2004, 10:1046-1053.
3. Fukumitsu K., Yagi H., Soto-Gutierrez A. Bioengineering in organ transplantation: targeting the liver. Transplant. Proc. 2011, 43:2137-2138.
4. Baptista P.M., Orlando G., Mirmalek-Sani S.H., Siddiqui M., Atala A., Soker S. Whole organ decellularization - a tool for bioscaffold fabrication and organ bioengineering. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2009, 2009:6526-6529.
5. Badylak S.F. Xenogeneic extracellular matrix as a scaffold for tissue reconstruction. Transpl. Immunol. 2004, 12:367-377.
6. Crapo P.M., Gilbert T.W., Badylak S.F. An overview of tissue and whole organ decellularization processes. Biomaterials 2011, 32:3233-3243.
7. Ning L.J., Zhang Y., Chen X.H., Luo J.C., Li X.Q., Yang Z.M., Qin T.W. Preparation and characterization of decellularized tendon slices for tendon tissue engineering. J. Biomed. Mater. Res. A 2012, 100:1448-1456.
8. Wang B., Borazjani A., Tahai M., Curry A.L., Simionescu D.T., Guan J., To F., Elder S.H., Liao J. Fabrication of cardiac patch with decellularized porcine myocardial scaffold and bone marrow mononuclear cells. J. Biomed. Mater. Res. A 2010, 94:1100-1110.
9. Tudorache I., Cebotari S., Sturz G., Kirsch L., Hurschler C., Hilfiker A., Haverich A., Lichtenberg A. Tissue engineering of heart valves: biomechanical and morphological properties of decellularized heart valves. J. Heart Valve Dis. 2007, 16:567-573. discussion 574.
10. Gentile P., Colicchia G.M., Nicoli F., Cervelli G., Curcio C.B., Brinci L., Cervelli V. Complex abdominal wall repair using a porcine dermal matrix. Surg. Innov. 2011, (published online 16 October 2011). 10.1177/1553350611421022.
11. 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.
12. Barakat O., Abbasi S., Rodriguez G., Rios J., Wood R.P., Ozaki C., Holley L.S., Gauthier P.K. Use of decellularized porcine liver for engineering humanized liver organ. J. Surg. Res. 2012, 173:e11-e25.
13. Park K.M., Woo H.M. Systemic decellularization for multi-organ scaffolds in rats. Transplant. Proc. 2012, 44:1151-1154.
14. Park K.M., Woo H.M. Porcine bioengineered scaffolds as new frontiers in regenerative medicine. Transplant. Proc. 2012, 44:1146-1150.
15. Soto-Gutierrez A., Zhang L., Medberry C., Fukumitsu K., Faulk D., Jiang H., Reing J., Gramignoli R., Komori J., Ross M., other 9 authors A whole-organ regenerative medicine approach for liver replacement. Tissue Eng. Part C Methods 2011, 17:677-686.
16. 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.
17. Badylak S.F., Gilbert T.W. Immune response to biologic scaffold materials. Semin. Immunol. 2008, 20:109-116.
18. Popp S.K., Mann D.A., Milburn P.J., Gibbs A.J., McCullagh P.J., Wilson J.D., Tonjes R.R., Simeonovic C.J. Transient transmission of porcine endogenous retrovirus to fetal lambs after pig islet tissue xenotransplantation. Immunol. Cell Biol. 2007, 85:238-248.
19. 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.
20. Kheir E., Stapleton T., Shaw D., Jin Z., Fisher J., Ingham E. Development and characterization of an acellular porcine cartilage bone matrix for use in tissue engineering. J. Biomed. Mater. Res. A 2011, 99:283-294.
21. Valentin J.E., Stewart-Akers A.M., Gilbert T.W., Badylak S.F. Macrophage participation in the degradation and remodeling of extracellular matrix scaffolds. Tissue Eng. Part A 2009, 15:1687-1694.
22. Wu J.J., Eyre D.R. Identification of hydroxypyridinium cross-linking sites in type II collagen of bovine articular cartilage. Biochemistry 1984, 23:1850-1857.
23. Singelyn J.M., DeQuach J.A., Seif-Naraghi S.B., Littlefield R.B., Schup-Magoffin P.J., Christman K.L. Naturally derived myocardial matrix as an injectable scaffold for cardiac tissue engineering. Biomaterials 2009, 30:5409-5416.
24. Ross E.A., Williams M.J., Hamazaki T., Terada N., Clapp W.L., Adin C., Ellison G.W., Jorgensen M., Batich C.D. Embryonic stem cells proliferate and differentiate when seeded into kidney scaffolds. J. Am. Soc. Nephrol. 2009, 20:2338-2347.
25. Eitan Y., Sarig U., Dahan N., Machluf M. Acellular cardiac extracellular matrix as a scaffold for tissue engineering: in vitro cell support, remodeling, and biocompatibility. Tissue Eng. Part C Methods 2010, 16:671-683.
26. Totonelli G., Maghsoudlou P., Garriboli M., Riegler J., Orlando G., Burns A.J., Sebire N.J., Smith V.V., Fishman J.M., Ghionzoli M., other 9 authors A rat decellularized small bowel scaffold that preserves villus-crypt architecture for intestinal regeneration. Biomaterials 2012, 33:3401-3410.
27. Takeda M., Yamamoto M., Isoda K., Higashiyama S., Hirose M., Ohgushi H., Kawase M., Yagi K. Availability of bone marrow stromal cells in three-dimensional coculture with hepatocytes and transplantation into liver-damaged mice. J. Biosci. Bioeng. 2005, 100:77-81.
28. Higashiyama S., Noda M., Muraoka S., Hirose M., Ohgushi H., Kawase M., Yagi K. Transplantation of hepatocytes cultured on hydroxyapatite into Nagase analbuminemia rats. J. Biosci. Bioeng. 2003, 96:83-85.
29. Katsuda T., Teratani T., Ochiya T., Sakai Y. Transplantation of a fetal liver cell-loaded hyaluronic acid sponge onto the mesentery recovers a Wilson's disease model rat. J. Biochem. 2010, 148:281-288.
30. 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. 2010, 16:927-933.
31. Ott H.C., Matthiesen T.S., Goh S.K., Black L.D., Kren S.M., Netoff T.I., Taylor D.A. Perfusion-decellularized matrix: using nature's platform to engineer a bioartificial heart. Nat. Med. 2008, 14:213-221.
32. Wainwright J.M., Czajka C.A., Patel U.B., Freytes D.O., Tobita K., Gilbert T.W., Badylak S.F. Preparation of cardiac extracellular matrix from an intact porcine heart. Tissue Eng. Part C Methods 2010, 16:525-532.
33. Rutkowska J., Interewiczi B., Rydzewski A., Swietek M., Dominiak A., Durlik M., Olszewski W.L. Donor DNA is detected in recipient blood for years after kidney transplantation using sensitive forensic medicine methods. Ann. Transplant. 2007, 12:12-14.
34. Olszewski W.L., Interewicz B., Maksymowicz M., Stanislawska J. Transplantation of organs is transplantations of donor DNA: fate of DNA disseminated in recipient. Transpl. Int. 2005, 18:412-418.
35. Knoop C., Andrien M., Defleur V., Antonine M., de Francquen P., Goldman M., Estenne M. Detection of blood chimerism after lung and heart-lung transplantation. The superiority of nested as compared with standard polymerase chain reaction amplification. Transplantation 1994, 58:1335-1338.
36. Spriewald B.M., Wassmuth R., Carl H.D., Kockerling F., Reichstetter S., Kleeberger A., Klein M., Hohenberger M.W., Kalden J.R. Microchimerism after liver transplantation: prevalence and methodological aspects of detection. Transplantation 1998, 66:77-83.
37. Kallenbach K., Leyh R.G., Lefik E., Walles T., Wilhelmi M., Cebotari S., Schmiedl A., Haverich A., Mertsching H. Guided tissue regeneration: porcine matrix does not transmit PERV. Biomaterials 2004, 25:3613-3620.
38. Leyh R.G., Wilhelmi M., Walles T., Kallenbach K., Rebe P., Oberbeck A., Herden T., Haverich A., Mertsching H. Acellularized porcine heart valve scaffolds for heart valve tissue engineering and the risk of cross-species transmission of porcine endogenous retrovirus. J. Thorac. Cardiovasc. Surg. 2003, 126:1000-1004.
39. Lodén M. The simultaneous penetration of water and sodium lauryl sulfate through isolated human skin. J. Soc. Cosmet. Chem. 1990, 41:227-233.
40. Faucher J., Goddard E. Interaction of keratinous substrates with sodium lauryl sulfate: I. Sorption. J. Soc. Cosmet. Chem. 1978, 29:323-337.
41. Rhein L.D., Simion F.A., Hill R.L., Cagan R.H., Mattai J., Maibach H.I. Human cutaneous response to a mixed surfactant system: role of solution phenomena in controlling surfactant irritation. Dermatologica 1990, 180:18-23.
42. Vilaplana J., Mascaro J.M., Trullas C., Coll J., Romaguera C., Zemba C., Pelejero C. Human irritant response to different qualities and concentrations of cocoamidopropylbetaines: a possible model of paradoxical irritant response. Contact Dermatitis 1992, 26:289-294.
43. Wilhelm K.P., Cua A.B., Wolff H.H., Maibach H.I. Surfactant-induced stratum corneum hydration in vivo: prediction of the irritation potential of anionic surfactants. J. Invest. Dermatol. 1993, 101:310-315.
44. Moore P.N., Puvvada S., Blankschtein D. Challenging the surfactant monomer skin penetration model: penetration of sodium dodecyl sulfate micelles into the epidermis. J. Cosmet. Sci. 2003, 54:29-46.
45. Farrell E., O'Brien F.J., Doyle P., Fischer J., Yannas I., Harley B.A., O'Connell B., Prendergast P.J., Campbell V.A. A collagen-glycosaminoglycan scaffold supports adult rat mesenchymal stem cell differentiation along osteogenic and chondrogenic routes. Tissue Eng. 2006, 12:459-468.
46. Tierney C.M., Jaasma M.J., O'Brien F.J. Osteoblast activity on collagen-GAG scaffolds is affected by collagen and GAG concentrations. J. Biomed. Mater. Res. A 2009, 91:92-101.
47. Linhardt R.J., Toida T. Role of glycosaminoglycans in cellular communication. Acc. Chem. Res. 2004, 37:431-438.
48. Wollmann L.C., Laurindo C.A., Costa F.D., Moreno A.N. Effects of cryopreservation and/or decellularization on extracellular matrix of porcine valves. Rev. Bras. Cir. Cardiovasc. 2011, 26:490-496.
49. Pridgen B.C., Woon C.Y., Kim M., Thorfinn J., Lindsey D., Pham H., Chang J. Flexor tendon tissue engineering: acellularization of human flexor tendons with preservation of biomechanical properties and biocompatibility. Tissue Eng. Part C Methods 2011, 17:819-828.
50. Cyganek-Niemiec A., Strzalka-Mrozik B., Pawlus-Lachecka L., Wszolek J., Adamska J., Kudrjavtseva J., Zhuravleva I., Kimsa M., Okla H., Kimsa M., Gudek A., Mazurek U. Degradation effect of diepoxide fixation on porcine endogenous retrovirus DNA in heart valves: molecular aspects. Int. J. Artif. Organs 2012, 35:25-33.
51. Akiyoshi D.E., Denaro M., Zhu H., Greenstein J.L., Banerjee P., Fishman J.A. Identification of a full-length cDNA for an endogenous retrovirus of miniature swine. J. Virol. 1998, 72:4503-4507.
52. Prabha S., Verghese S. Existence of proviral porcine endogenous retrovirus in fresh and decellularised porcine tissues. Indian J. Med. Microbiol. 2008, 26:228-232.
53. Yamada K., Sachs D.H., DerSimonian H. Human anti-porcine xenogeneic T cell response. Evidence for allelic specificity of mixed leukocyte reaction and for both direct and indirect pathways of recognition. J. Immunol. 1995, 155:5249-5256.
54. Logan J.S. Prospects for xenotransplantation. Curr. Opin. Immunol. 2000, 12:563-568.
55. Bravery C.A., Batten P., Yacoub M.H., Rose M.L. Direct recognition of SLA- and HLA-like class II antigens on porcine endothelium by human T cells results in T cell activation and release of interleukin-2. Transplantation 1995, 60:1024-1033.
56. Macleod T.M., Williams G., Sanders R., Green C.J. Histological evaluation of Permacol as a subcutaneous implant over a 20-week period in the rat model. Br. J. Plast. Surg. 2005, 58:518-532.
57. Lautenschlager I., Hockerstedt K., Taskinen E., Korsback C., Makisalo H., Hayry P. Fine-needle aspiration biopsy in the monitoring of liver allografts. I. Correlation between aspiration biopsy and core biopsy in experimental pig liver allografts. Transplantation 1988, 46:41-46.
58. Hausen B., Berry G.J., Dagum P., Ikonen T., Christians U., Briffa N., Hook L., Morris R.E. The histology of subcutaneously implanted donor bronchial rings correlates with rejection scores of lung allografts in a primate lung transplant model. J. Heart Lung Transplant. 1999, 18:714-724.
59. Gilbert T.W., Stewart-Akers A.M., Simmons-Byrd A., Badylak S.F. Degradation and remodeling of small intestinal submucosa in canine Achilles tendon repair. J. Bone Joint Surg. Am. 2007, 89:621-630.
60. Record R.D., Hillegonds D., Simmons C., Tullius R., Rickey F.A., Elmore D., Badylak S.F. In vivo degradation of 14C-labeled small intestinal submucosa (SIS) when used for urinary bladder repair. Biomaterials 2001, 22:2653-2659.
61. Takahashi S., Yamazoe H., Sassa F., Suzuki H., Fukuda J. Preparation of coculture system with three extracellular matrices using capillary force lithography and layer-by-layer deposition. J. Biosci. Bioeng. 2009, 108:544-550.
62. Duan Y., Liu Z., O'Neill J., Wan L.Q., Freytes D.O., Vunjak-Novakovic G. Hybrid gel composed of native heart matrix and collagen induces cardiac differentiation of human embryonic stem cells without supplemental growth factors. J. Cardiovasc. Transl. Res. 2011, 4:605-615.
63. Dutta R.C., Dutta A.K. Cell-interactive 3D-scaffold; advances and applications. Biotechnol. Adv. 2009, 27:334-339.
64. De Kock J., Ceelen L., De Spiegelaere W., Casteleyn C., Claes P., Vanhaecke T., Rogiers V. Simple and quick method for whole-liver decellularization: a novel in vitro three-dimensional bioengineering tool?. Arch. Toxicol. 2011, 85:607-612.
65. Jia S., Liu L., Pan W., Meng G., Duan C., Zhang L., Xiong Z., Liu J. Oriented cartilage extracellular matrix-derived scaffold for cartilage tissue engineering. J. Biosci. Bioeng. 2012, 113:647-653.