The host response to allogeneic and xenogeneic biological scaffold materials

Journal of Tissue Engineering and Regenerative Medicine

Volumn 9, Issue 5, 2015, Pages 504-511

  Keane, Timothy J ^a,b   Badylak, Stephen F ^a,b,c  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b University of Pittsburgh   (United States)

^c UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

Author keywords

Allogeneic; Biological scaffolds; Decellularization; Extracellular matrix (ECM); Host response; Xenogeneic

Indexed keywords

PROCESSING; SCAFFOLDS (BIOLOGY);

ALLOGENIC; BIOLOGICAL SCAFFOLDS; CLINICAL USE; DECELLULARIZATION; EXTRACELLULAR MATRICES; EXTRACELLULAR MATRIX; HOST RESPONSE; PROCESSING METHOD; SCAFFOLD MATERIALS; XENOGENIC;

TISSUE;

ACELLULAR DERMAL MATRIX; ADAPTIVE IMMUNITY; ALLOGENEIC SCAFFOLD MATERIAL; CELL DIFFERENTIATION; CELL MIGRATION; CELL SURVIVAL; EXTRACELLULAR MATRIX; GENE EXPRESSION; HUMAN; HUMORAL IMMUNITY; IMMUNE RESPONSE; INNATE IMMUNITY; NONHUMAN; OXYGEN CONCENTRATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; T LYMPHOCYTE ACTIVATION; TISSUE REGENERATION; TISSUE SCAFFOLD; XENOGENEIC SCAFFOLD MATERIAL; ALLOTRANSPLANTATION; ANIMAL; CHEMISTRY; IMMUNE SYSTEM; METABOLISM; PATHOLOGY; PROCEDURES; SKIN; TISSUE ENGINEERING;

BIOMATERIAL; EPITOPE;

ADAPTIVE IMMUNITY; ANIMALS; BIOCOMPATIBLE MATERIALS; EPITOPES; EXTRACELLULAR MATRIX; HUMANS; IMMUNE SYSTEM; IMMUNITY, INNATE; SKIN; TISSUE ENGINEERING; TISSUE SCAFFOLDS; TRANSPLANTATION, HOMOLOGOUS;

EID: 84928273485     PISSN: 19326254     EISSN: 19327005     Source Type: Journal    
DOI: 10.1002/term.1874     Document Type: Review

References (79)

1. Adams JE, Zobitz ME, Reach JS Jr. et al. 2006; Rotator cuff repair using an acellular dermal matrix graft: an in vivo study in a canine model. Arthroscopy 22(7): 700-709.
2. Agrawal V, Johnson SA, Reing J et al. 2010; Epimorphic regeneration approach to tissue replacement in adult mammals. Proc Natl Acad Sci U S A 107(8): 3351-3355.
3. Allman AJ, McPherson TB, Badylak SF et al. 2001; Xenogeneic extracellular matrix grafts elicit a TH2-restricted immune response. Transplantation 71(11): 1631-1640.
4. Allman AJ, McPherson TB, Merrill LC et al. 2002; The Th2-restricted immune response to xenogeneic small intestinal submucosa does not influence systemic protective immunity to viral and bacterial pathogens. Tissue Eng 8(1): 53-62.
5. Ansaloni L, Cambrini P, Catena F et al. 2007; Immune response to small intestinal submucosa (surgisis) implant in humans: preliminary observations. J Invest Surg 20(4): 237-241.
6. Armour AD, Fish JS, Woodhouse KA et al. 2006; A comparison of human and porcine acellularized dermis: interactions with human fibroblasts in vitro. Plast Reconstr Surg 117(3): 845-856.
7. Arnold L, Henry A, Poron F et al. 2007; Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J Exp Med 204(5): 1057-1069.
8. Badylak SF. 2007; The extracellular matrix as a biologic scaffold material. Biomaterials 28(25): 3587-3593.
9. Badylak SF, Gilbert TW. 2008; Immune response to biologic scaffold materials. Semin Immunol 20(2): 109-116.
10. Badylak SF, Hoppo T, Nieponice A et al. 2011; Esophageal preservation in five male patients after endoscopic inner-layer circumferential resection in the setting of superficial cancer: a regenerative medicine approach with a biologic scaffold. Tissue Eng A 17(11-12): 1643-1650.
11. Badylak SF, Kochupura PV, Cohen IS et al. 2006; The use of extracellular matrix as an inductive scaffold for the partial replacement of functional myocardium. Cell Transpl 15(suppl 1): S29-40.
12. Bissell MJ, Aggeler J. 1987; Dynamic reciprocity: how do extracellular matrix and hormones direct gene expression? Prog Clin Biol Res 249: 251-262.
13. Bisset LR, Boni J, Lutz H et al. 2007; Lack of evidence for PERV expression after apoptosis-mediated horizontal gene transfer between porcine and human cells. Xenotransplantation 14(1): 13-24.
14. Boruch AV, Nieponice A, Qureshi IR et al. 2010; Constructive remodeling of biologic scaffolds is dependent on early exposure to physiologic bladder filling in a canine partial cystectomy model. J Surg Res 161(2): 217-225.
15. Brown BN, Londono R, Tottey S et al. 2012; Macrophage phenotype as a predictor of constructive remodeling following the implantation of biologically derived surgical mesh materials. Acta Biomater 8(3): 978-987.
16. Brown BN, Valentin JE, Stewart-Akers AM et al. 2009; Macrophage phenotype and remodeling outcomes in response to biologic scaffolds with and without a cellular component. Biomaterials 30(8): 1482-1491.
17. Burgeson RE, Christiano AM. 1997; The dermal-epidermal junction. Curr Opin Cell Biol 9(5): 651-658.
18. Calve S, Odelberg SJ, Simon HG. 2010; A transitional extracellular matrix instructs cell behavior during muscle regeneration. Dev Biol 344(1): 259-271.
19. Campbell KT, Burns NK, Rios CN et al. 2011; Human versus non-cross-linked porcine acellular dermal matrix used for ventral hernia repair: comparison of in vivo fibrovascular remodeling and mechanical repair strength. Plast Reconstr Surg 127(6): 2321-2332.
20. Colwell AS, Longaker MT, Lorenz HP. 2005; Mammalian fetal organ regeneration. Adv Biochem Eng Biotechnol 93: 83-100.
21. Constantinou CD, Jimenez SA. 1991; Structure of cDNAs encoding the triple-helical domain of murine α2 (VI) collagen chain and comparison to human and chick homologues. Use of polymerase chain reaction and partially degenerate oligonucleotide for generation of novel cDNA clones. Matrix 11(1): 1-9.
22. Cook JL, Fox DB, Kuroki K et al. 2008; In vitro and in vivo comparison of five biomaterials used for orthopedic soft tissue augmentation. Am J Vet Res 69(1): 148-156.
23. Crapo PM, Gilbert TW, Badylak SF. 2011; An overview of tissue and whole organ decellularization processes. Biomaterials 32(12): 3233-3243.
24. Daly KA, Liu S, Agrawal V et al. 2012; Damage associated molecular patterns within xenogeneic biologic scaffolds and their effects on host remodeling. Biomaterials 33(1): 91-101.
25. Daly KA, Stewart-Akers AM, Hara H et al. 2009; Effect of the αGal epitope on the response to small intestinal submucosa extracellular matrix in a nonhuman primate model. Tissue Eng A 15(12): 3877-3888.
26. Exposito JY, D'Alessio M, Solursh M et al. 1992; Sea urchin collagen evolutionarily homologous to vertebrate pro-α2(I) collagen. J Biol Chem 267(22): 15559-15562.
27. Freytes DO, Stoner RM, Badylak SF 2008a; Uniaxial and biaxial properties of terminally sterilized porcine urinary bladder matrix scaffolds. J Biomed Mater Res B Appl Biomater 84(2): 408-414.
28. Freytes DO, Tullius RS, Valentin JE et al. 2008b; Hydrated versus lyophilized forms of porcine extracellular matrix derived from the urinary bladder. J Biomed Mater Res A 87(4): 862-872.
29. Galili U, Clark MR, Shohet SB et al. 1987; Evolutionary relationship between the natural anti-Gal antibody and the Gal α1-3Gal epitope in primates. Proc Natl Acad Sci U S A 84(5): 1369-1373.
30. Garkavenko O, Croxson MC, Irgang M et al. 2004; Monitoring for presence of potentially xenotic viruses in recipients of pig islet xenotransplantation. J Clin Microbiol 42(11): 5353-5356.
31. Garkavenko O, Dieckhoff B, Wynyard S et al. 2008; Absence of transmission of potentially xenotic viruses in a prospective pig to primate islet xenotransplantation study. J Med Virol 80(11): 2046-2052.
32. Gilbert TW, Sellaro TL, Badylak SF et al. 2006; Decellularization of tissues and organs. Biomaterials 27(19): 3675-3683.
33. Gilbert TW, Wognum S, Joyce EM et al. 2008; Collagen fiber alignment and biaxial mechanical behavior of porcine urinary bladder derived extracellular matrix. Biomaterials 29(36): 4775-4782.
34. Glasberg SB, Light D. 2012; AlloDerm and Strattice in breast reconstruction: a comparison and techniques for optimizing outcomes. Plast Reconstr Surg 129(6): 1223-1233.
35. Godwin JW, Pinto AR, Rosenthal NA. 2013; Macrophages are required for adult salamander limb regeneration. Proc Natl Acad Sci U S A 110(23): 9415-9420.
36. Guo S, Dipietro LA. 2010; Factors affecting wound healing. J Dent Res 89(3): 219-229.
37. Hoppo T, Badylak SF, Jobe BA. 2012; A novel esophageal-preserving approach to treat high-grade dysplasia and superficial adenocarcinoma in the presence of chronic gastroesophageal reflux disease. World J Surg 36(10): 2390-2393.
38. Hutter H, Vogel BE, Plenefisch JD et al. 2000; Conservation and novelty in the evolution of cell adhesion and extracellular matrix genes. Science 287(5455): 989-994.
39. Hynes RO, Zhao Q. 2000; The evolution of cell adhesion. J Cell Biol 150(2): F89-96.
40. Ingulli E. 2010; Mechanism of cellular rejection in transplantation. Pediatr Nephrol 25(1): 61-74.
41. Iozzo RV. 1994; Perlecan: a gem of a proteoglycan. Matrix Biol 14(3): 203-208.
42. Jenkins ED, Yip M, Melman L et al. 2010; Informed consent: cultural and religious issues associated with the use of allogeneic and xenogeneic mesh products. J Am Coll Surg 210(4): 402-410.
43. Keane TJ, Londono R, Turner NJ et al. 2012; Consequences of ineffective decellularization of biologic scaffolds on the host response. Biomaterials 33(6): 1771-1781.
44. Konakci KZ, Bohle B, Blumer R et al. 2005; α-Gal on bioprostheses: xenograft immune response in cardiac surgery. Eur J Clin Invest 35(1): 17-23.
45. Kramer JM. 1997; Extracellular matrix. In C. elegans II, Riddle DL, Blumenthal T, Meyer BJ, Priess JR (eds). Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY.
46. Kulig KM, Luo X, Finkelstein EB et al. 2013; Biologic properties of surgical scaffold materials derived from dermal ECM. Biomaterials 34(23): 5776-5784.
47. Liu C, Dib-Hajj SD, Waxman SG. 2001; Fibroblast growth factor homologous factor 1B binds to the C terminus of the tetrodotoxin-resistant sodium channel rNav1.9a (NaN). J Biol Chem 276(22): 18925-18933.
48. Macher BA, Galili U. 2008; The Galα1, 3Galβ1, 4GlcNAc-R (α-Gal) epitope: a carbohydrate of unique evolution and clinical relevance. Biochim Biophys Acta 1780(2): 75-88.
49. Mantovani A, Sica A, Locati M. 2005; Macrophage polarization comes of age. Immunity 23(4): 344-346.
50. Mantovani A, Sica A, Sozzani S et al. 2004; The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 25(12): 677-686.
51. Martinez FO, Gordon S, Locati M et al. 2006; Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization: new molecules and patterns of gene expression. J Immunol 177(10): 7303-7311.
52. McPherson TB, Liang H, Record RD et al. 2000; Galα(1, 3)Gal epitope in porcine small intestinal submucosa. Tissue Eng 6(3): 233-239.
53. Mills CD, Kincaid K, Alt JM et al. 2000; M-1/M-2 macrophages and the Th1/Th2 paradigm. J Immunol 164(12): 6166-6173.
54. Mirza R, DiPietro LA, Koh TJ. 2009; Selective and specific macrophage ablation is detrimental to wound healing in mice. Am J Pathol 175(6): 2454-2462.
55. Nelson CM, Bissell MJ. 2006; Of extracellular matrix, scaffolds, and signaling: tissue architecture regulates development, homeostasis, and cancer. Annu Rev Cell Dev Biol 22: 287-309.
56. Ngo MD, Aberman HM, Hawes ML et al. 2011; Evaluation of human acellular dermis versus porcine acellular dermis in an in vivo model for incisional hernia repair. Cell Tissue Bank 12(2): 135-145.
57. Okumura M, Matthews RJ, Robb B et al. 1996; Comparison of CD45 extracellular domain sequences from divergent vertebrate species suggests the conservation of three fibronectin type III domains. J Immunol 157(4): 1569-1575.
58. Ponce ML, Nomizu M, Delgado MC et al. 1999; Identification of endothelial cell binding sites on the laminin γ1 chain. Circ Res 84(6): 688-694.
59. Porcheray F, Viaud FS, Rimaniol AC et al. 2005; Macrophage activation switching: an asset for the resolution of inflammation. Clin Exp Immunol 142(3): 481-489.
60. Quarti A, Nardone S, Colaneri M et al. 2011; Preliminary experience in the use of an extracellular matrix to repair congenital heart diseases. Interact Cardiovasc Thorac Surg 13(6): 569-572.
61. Reddy PP, Barrieras DJ, Wilson G et al. 2000; Regeneration of functional bladder substitutes using large segment acellular matrix allografts in a porcine model. J Urol 164(3, pt 2): 936-941.
62. Reing JE, Zhang L, Myers-Irvin J et al. 2009; Degradation products of extracellular matrix affect cell migration and proliferation. Tissue Eng A 15(3): 605-614.
63. Sacks MS, Gloeckner DC. 1999; Quantification of the fiber architecture and biaxial mechanical behavior of porcine intestinal submucosa. J Biomed Mater Res 46(1): 1-10.
64. Schwarzbauer JE. 1991; Fibronectin: from gene to protein. Curr Opin Cell Biol 3(5): 786-791.
65. Scott JE. 1995; Extracellular matrix, supramolecular organisation and shape. J Anat 187(2): 259-269.
66. Shah BC, Tiwari MM, Goede MR et al. 2011; Not all biologics are equal! Hernia 15(2): 165-171.
67. Sicari BM, Johnson SA, Siu BF et al. 2012; The effect of source animal age upon the in vivo remodeling characteristics of an extracellular matrix scaffold. Biomaterials 33(22): 5524-5533.
68. Soler JA, Gidwani S, Curtis MJ. 2007; Early complications from the use of porcine dermal collagen implants (Permacol) as bridging constructs in the repair of massive rotator cuff tears. A report of four cases. Acta Orthop Belg 73(4): 432-436.
69. Stone KR, Abdel-Motal UM, Walgenbach AW et al. 2007; Replacement of human anterior cruciate ligaments with pig ligaments: a model for anti-non-gal antibody response in long-term xenotransplantation. Transplantation 83(2): 211-219.
70. Turner NJ, Yates AJ Jr., Weber DJ et al. 2010; Xenogeneic extracellular matrix as an inductive scaffold for regeneration of a functioning musculotendinous junction. Tissue Eng A 16(11): 3309-3317.
71. Valdes-Gonzalez R, Dorantes LM, Bracho-Blanchet E et al. 2010; No evidence of porcine endogenous retrovirus in patients with type 1 diabetes after long-term porcine islet xenotransplantation. J Med Virol 82(2): 331-334.
72. Valentin JE, Badylak JS, McCabe GP et al. 2006; Extracellular matrix bioscaffolds for orthopaedic applications. A comparative histologic study. J Bone Joint Surg Am 88(12): 2673-2686.
73. Valentin JE, Stewart-Akers AM, Gilbert TW et al. 2009; Macrophage participation in the degradation and remodeling of extracellular matrix scaffolds. Tissue Eng A 15(7): 1687-1694.
74. Valentin JE, Turner NJ, Gilbert TW et al. 2010; Functional skeletal muscle formation with a biologic scaffold. Biomaterials 31(29): 7475-7484.
75. van der Rest M, Garrone R. 1991; Collagen family of proteins. FASEB J 5(13): 2814-2823.
76. Voytik-Harbin SL, Brightman AO, Kraine MR et al. 1997; Identification of extractable growth factors from small intestinal submucosa. J Cell Biochem 67(4): 478-491.
77. Walton JR, Bowman NK, Khatib Y et al. 2007; Restore orthobiologic implant: not recommended for augmentation of rotator cuff repairs. J Bone Joint Surg Am 89(4): 786-791.
78. Zalavras CG, Gardocki R, Huang E et al. 2006; Reconstruction of large rotator cuff tendon defects with porcine small intestinal submucosa in an animal model. J Shoulder Elbow Surg 15(2): 224-231.
79. Zheng MH, Chen J, Kirilak Y et al. 2005; Porcine small intestine submucosa (SIS) is not an acellular collagenous matrix and contains porcine DNA: possible implications in human implantation. J Biomed Mater Res B Appl Biomater 73(1): 61-67.