Table of Contents Author Guidelines Submit a Manuscript
Journal of Immunology Research
Volume 2015 (2015), Article ID 589648, 13 pages
http://dx.doi.org/10.1155/2015/589648
Review Article

Acceleration of Wound Healing by -gal Nanoparticles Interacting with the Natural Anti-Gal Antibody

Department of Surgery, University of Massachusetts Medical School, Worcester, MA 01655, USA

Received 19 November 2014; Accepted 18 March 2015

Academic Editor: Mario Clerici

Copyright © 2015 Uri Galili. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. C. K. Sen, G. M. Gordillo, S. Roy et al., “Human skin wounds: a major and snowballing threat to public health and the economy,” Wound Repair and Regeneration, vol. 17, no. 7, pp. 763–771, 2009. View at Publisher · View at Google Scholar · View at Scopus
  2. S. J. Leibovich and R. Ross, “The role of the macrophage in wound repair. A study with hydrocortisone and anti-macrophage serum,” American Journal of Pathology, vol. 78, no. 1, pp. 71–99, 1975. View at Google Scholar · View at Scopus
  3. L. A. DiPietro, “Wound healing: the role of the macrophage and other immune cells,” Shock, vol. 4, no. 4, pp. 233–240, 1995. View at Publisher · View at Google Scholar · View at Scopus
  4. A. J. Singer and R. A. F. Clark, “Cutaneous wound healing,” The New England Journal of Medicine, vol. 341, no. 10, pp. 738–746, 1999. View at Publisher · View at Google Scholar · View at Scopus
  5. P. Martin, “Wound healing—aiming for perfect skin regeneration,” Science, vol. 276, no. 5309, pp. 75–81, 1997. View at Publisher · View at Google Scholar · View at Scopus
  6. P. Martin and S. J. Leibovich, “Inflammatory cells during wound repair: the good, the bad and the ugly,” Trends in Cell Biology, vol. 15, no. 11, pp. 599–607, 2005. View at Publisher · View at Google Scholar · View at Scopus
  7. M. G. Franz, D. L. Steed, and M. C. Robson, “Optimizing healing of the acute wound by minimizing complications,” Current Problems in Surgery, vol. 44, no. 11, pp. 691–763, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. G. C. Gurtner, S. Werner, Y. Barrandon, and M. T. Longaker, “Wound repair and regeneration,” Nature, vol. 453, no. 193, pp. 314–321, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. A. Sica and A. Mantovani, “Macrophage plasticity and polarization: in vivo veritas,” Journal of Clinical Investigation, vol. 122, no. 3, pp. 787–795, 2012. View at Publisher · View at Google Scholar · View at Scopus
  10. M.-T. S. Piccolo, Y. Wang, P. Sannomiya et al., “Chemotactic mediator requirements in lung injury following skin burns in rats,” Experimental and Molecular Pathology, vol. 66, no. 3, pp. 220–226, 1999. View at Publisher · View at Google Scholar · View at Scopus
  11. J. A. Shukaliak and K. Dorovini-Zis, “Expression of the β-chemokines RANTES and MIP-1β by human brain microvessel endothelial cells in primary culture,” Journal of Neuropathology and Experimental Neurology, vol. 59, no. 5, pp. 339–352, 2000. View at Google Scholar · View at Scopus
  12. Q. E. H. Low, I. A. Drugea, L. A. Duffner et al., “Wound healing in MIP-1α(−/−) and MCP-1(−/−) mice,” The American Journal of Pathology, vol. 159, no. 2, pp. 457–463, 2001. View at Publisher · View at Google Scholar · View at Scopus
  13. G. W. Wood, E. Hausmann, and R. Choudhuri, “Relative role of CSF-1, MCP-1/JE, and RANTES in macrophage recruitment during successful pregnancy,” Molecular Reproduction and Development, vol. 46, no. 1, pp. 62–70, 1997. View at Publisher · View at Google Scholar
  14. S. A. Heinrich, K. A. N. Messingham, M. S. Gregory et al., “Elevated monocyte chemoattractant protein-1 levels following thermal injury precede monocyte recruitment to the wound site and are controlled, in part, by tumor necrosis factor-α,” Wound Repair and Regeneration, vol. 11, no. 2, pp. 110–119, 2003. View at Publisher · View at Google Scholar · View at Scopus
  15. H. Shallo, T. P. Plackett, S. A. Heinrich, and E. J. Kovacs, “Monocyte chemoattractant protein-1 (MCP-1) and macrophage infiltration into the skin after burn injury in aged mice,” Burns, vol. 29, no. 7, pp. 641–647, 2003. View at Publisher · View at Google Scholar · View at Scopus
  16. R. Snyderman and M. C. Pike, “Chemoattractant receptors on phagocytic cells,” Annual Review of Immunology, vol. 2, no. 1, pp. 257–281, 1984. View at Publisher · View at Google Scholar · View at Scopus
  17. B. Damerau, “Biological activities of complement-derived peptides,” Reviews of Physiology, Biochemistry and Pharmacology, vol. 108, no. 1, pp. 151–206, 1987. View at Publisher · View at Google Scholar · View at Scopus
  18. M. R. Haeney, “The role of the complement cascade in sepsis,” Journal of Antimicrobial Chemotherapy, vol. 41, pp. 41–46, 1998. View at Google Scholar · View at Scopus
  19. K. M. Wigglesworth, W. J. Racki, R. Mishra, E. Szomolanyi-Tsuda, D. L. Greiner, and U. Galili, “Rapid recruitment and activation of macrophages by anti-gal/α-gal liposome interaction accelerates wound healing,” The Journal of Immunology, vol. 186, no. 7, pp. 4422–4432, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. U. Galili, K. Wigglesworth, and U. M. Abdel-Motal, “Accelerated healing of skin burns by anti-Gal/α-gal liposomes interaction,” Burns, vol. 36, no. 2, pp. 239–251, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. Z. M. Hurwitz, R. Ignotz, J. F. Lalikos, and U. Galili, “Accelerated porcine wound healing after treatment with α-gal nanoparticles,” Plastic & Reconstructive Surgery, vol. 129, no. 2, pp. 242–251, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. U. Galili, E. A. Rachmilewitz, A. Peleg, and I. Flechner, “A unique natural human IgG antibody with anti-α-galactosyl specificity,” Journal of Experimental Medicine, vol. 160, no. 5, pp. 1519–1531, 1984. View at Publisher · View at Google Scholar · View at Scopus
  23. U. Galili, “Macrophages recruitment and activation by α-gal nanoparticles accelerate regeneration and can improve biomaterials efficacy in tissue engineering,” The Open Tissue Engineering and Regenerative Medicine Journal, vol. 6, no. 1, pp. 1–11, 2013. View at Publisher · View at Google Scholar · View at Scopus
  24. M. S. Sandrin, H. A. Vaughan, P. L. Dabkowski, and I. F. C. McKenzie, “Anti-pig IgM antibodies in human serum react predominantly with Gal(α 1—3)Gal epitopes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 90, no. 23, pp. 11391–11395, 1993. View at Publisher · View at Google Scholar · View at Scopus
  25. R. M. Hamadeh, U. Galili, P. Zhou, and J. M. Griffiss, “Anti-α-galactosyl immunoglobulin A (IgA), IgG, and IgM in human secretions,” Clinical and Diagnostic Laboratory Immunology, vol. 2, no. 2, pp. 125–131, 1995. View at Google Scholar · View at Scopus
  26. Z. E. Holzknecht and J. L. Platt, “Identification of porcine endothelial cell membrane antigens recognized by human xenoreactive natural antibodies,” The Journal of Immunology, vol. 154, no. 9, pp. 4565–4575, 1995. View at Google Scholar · View at Scopus
  27. K. Teranishi, R. Manez, M. Awwad, and D. K. C. Cooper, “Anti-Galα1–3Gal IgM and IgG antibody levels in sera of humans and old world non-human primates,” Xenotransplantation, vol. 9, no. 2, pp. 148–154, 2002. View at Publisher · View at Google Scholar · View at Scopus
  28. U. Galili, B. A. Macher, J. Buehler, and S. B. Shohet, “Human natural anti-α-galactosyl IgG. II. The specific recognition of α(1 → 3)-linked galactose residues,” Journal of Experimental Medicine, vol. 162, no. 2, pp. 573–582, 1985. View at Publisher · View at Google Scholar · View at Scopus
  29. U. Galili, R. E. Mandrell, R. M. Hamadeh, S. B. Shohet, and J. M. Griffiss, “Interaction between human natural anti-α-galactosyl immunoglobulin G and bacteria of the human flora,” Infection and Immunity, vol. 56, no. 7, pp. 1730–1737, 1988. View at Google Scholar · View at Scopus
  30. U. Galili, F. Anaraki, A. Thall, C. Hill-Black, and M. Radic, “One percent of human circulating B lymphocytes are capable of producing the natural anti-Gal antibody,” Blood, vol. 82, no. 8, pp. 2485–2493, 1993. View at Google Scholar · View at Scopus
  31. A. H. Good, D. K. C. Cooper, A. J. Malcolm et al., “Identification of carbohydrate structures which bind human anti-porcine antibodies: implication for discordant xenografting in man,” Transplantation Proceedings, vol. 24, no. 2, pp. 559–562, 1992. View at Google Scholar · View at Scopus
  32. W. Bennet, A. Björkland, B. Sundberg et al., “A comparison of fetal and adult porcine islets with regard to Gal α (1,3)Gal expression and the role of human immunoglobulins and complement in islet cell cytotoxicity,” Transplantation, vol. 69, no. 8, pp. 1711–1717, 2000. View at Google Scholar · View at Scopus
  33. B. C. Baumann, G. Stussi, K. Huggel, R. Rieben, and J. D. Seebach, “Reactivity of human natural antibodies to endothelial cells from Galα(1,3)Gal-deficient pigs,” Transplantation, vol. 83, no. 2, pp. 193–201, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. P. M. Repik, J. M. Strizki, and U. Galili, “Differential host-dependent expression of α-galactosyl epitopes on viral glycoproteins: a study of eastern equine encephalitis virus as a model,” Journal of General Virology, vol. 75, no. 5, pp. 1177–1181, 1994. View at Publisher · View at Google Scholar · View at Scopus
  35. Y. Takeuchi, C. D. Porter, K. M. Strahan et al., “Sensitization of cells and retroviruses to human serum by (α1–3) galactosyltransferase,” Nature, vol. 379, no. 6560, pp. 85–88, 1996. View at Publisher · View at Google Scholar · View at Scopus
  36. R. M. Welsh, C. L. O'Donnell, D. J. Reed, and R. P. Rother, “Evaluation of the Galα1–3Gal epitope as a host modification factor eliciting natural humoral immunity to enveloped viruses,” Journal of Virology, vol. 72, no. 6, pp. 4650–4656, 1998. View at Google Scholar · View at Scopus
  37. U. Galili, M. R. Clark, S. B. Shohet, J. Buehler, and B. A. Macher, “Evolutionary relationship between the natural anti-Gal antibody and the Galα1—3Gal epitope in primates,” Proceedings of the National Academy of Sciences of the United States of America, vol. 84, no. 5, pp. 1369–1373, 1987. View at Publisher · View at Google Scholar · View at Scopus
  38. U. Galili, S. B. Shohet, E. Kobrin, C. L. M. Stults, and B. A. Macher, “Man, apes, and Old World monkeys differ from other mammals in the expression of alpha-galactosyl epitopes on nucleated cells,” The Journal of Biological Chemistry, vol. 263, no. 33, pp. 17755–17762, 1988. View at Google Scholar · View at Scopus
  39. U. Galili, “Interaction of the natural anti-Gal antibody with α-galactosyl epitopes: a major obstacle for xenotransplantation in humans,” Immunology Today, vol. 14, no. 10, pp. 480–482, 1993. View at Publisher · View at Google Scholar · View at Scopus
  40. P. M. Simon, F. A. Neethling, S. Taniguchi et al., “Intravenous infusion of Galα1–3Gal oligosaccharides in baboons delays hyperacute rejection of porcine heart xenografts,” Transplantation, vol. 65, no. 3, pp. 346–353, 1998. View at Publisher · View at Google Scholar · View at Scopus
  41. B. H. Collins, A. H. Cotterell, K. R. McCurry et al., “Cardiac xenografts between primate species provide evidence for the importance of the α-galactosyl determinant in hyperacute rejection,” The Journal of Immunology, vol. 154, no. 10, pp. 5500–5510, 1995. View at Google Scholar · View at Scopus
  42. Y. Xu, T. Lorf, T. Sablinski et al., “Removal of anti-porcine natural antibodies from human and nonhuman primate plasma in vitro and in vivo by a Galα1-3Galβ1-4βGlc-X immunoaffinity column,” Transplantation, vol. 65, no. 2, pp. 172–179, 1998. View at Google Scholar · View at Scopus
  43. H. Watier, J.-M. Guillaumin, I. Vallée et al., “Human NK cell-mediated direct and IgG-dependent cytotoxicity against xenogeneic porcine endothelial cells,” Transplant Immunology, vol. 4, no. 4, pp. 293–299, 1996. View at Publisher · View at Google Scholar · View at Scopus
  44. M. Kumagai-Braesch, M. Satake, Y. Qian, J. Holgersson, and E. Möller, “Human NK cell and ADCC reactivity against xenogeneic porcine target cells including fetal porcine islet cells,” Xenotransplantation, vol. 5, no. 2, pp. 132–145, 1998. View at Publisher · View at Google Scholar · View at Scopus
  45. D. C. LaTemple, J. T. Abrams, S. Y. Zhang, and U. Galili, “Increased immunogenicity of tumor vaccines complexed with anti-Gal: studies in knockout mice for α1,3galactosyltransferase,” Cancer Research, vol. 59, no. 14, pp. 3417–3423, 1999. View at Google Scholar · View at Scopus
  46. G. R. Rossi, M. R. Mautino, R. C. Unfer, T. M. Seregina, N. Vahanian, and C. J. Link, “Effective treatment of preexisting melanoma with whole cell vaccines expressing α(1,3)-galactosyl epitopes,” Cancer Research, vol. 65, no. 22, pp. 10555–10561, 2005. View at Publisher · View at Google Scholar · View at Scopus
  47. U. Galili, K. Wigglesworth, and U. M. Abdel-Motal, “Intratumoral injection of α-gal glycolipids induces xenograft-like destruction and conversion of lesions into endogenous vaccines,” The Journal of Immunology, vol. 178, no. 7, pp. 4676–4687, 2007. View at Publisher · View at Google Scholar · View at Scopus
  48. U. M. Abdel-Motal, H. M. Guay, K. Wigglesworth, R. M. Welsh, and U. Galili, “Increased immunogenicity of influenza virus vaccine by anti-Gal mediated targeting to antigen presenting cells,” Journal of Virology, vol. 81, pp. 9131–9141, 2007. View at Google Scholar
  49. U. Abdel-Motal, S. Wang, S. Lu, K. Wigglesworth, and U. Galili, “Increased immunogenicity of human immunodeficiency virus gp120 engineered to express Galα1-3Galβ1-4GlcNAc-R epitopes,” Journal of Virology, vol. 80, no. 14, pp. 6943–6951, 2006. View at Publisher · View at Google Scholar · View at Scopus
  50. T. Eto, Y. Iichikawa, K. Nishimura, S. Ando, and T. Yamakawa, “Chemistry of lipids of the posthemolytic residue or stroma of erythrocytes. XVI. Occurance of ceramide pentasaccharide in the membrane of erythrocytes and reticulocytes in rabbit,” Journal of Biochemistry, vol. 64, no. 2, pp. 205–213, 1968. View at Google Scholar
  51. K. Stellner, H. Saito, and S. Hakomori, “Determination of aminosugar linkage in glycolipids by methylation. Aminosugar linkage of ceramide pentasaccharides of rabbit erythrocytes and of Forssman antigen,” Archives of Biochemistry and Biophysics, vol. 133, no. 2, pp. 464–472, 1973. View at Google Scholar
  52. U. Dabrowski, P. Hanfland, H. Egge, S. Kuhn, and J. Dabrowski, “Immunochemistry of I/i-active oligo- and polyglycosylceramides from rabbit erythrocyte membranes. Determination of branching patterns of a ceramide pentadecasaccharide by 1H nuclear magnetic resonance,” Journal of Biological Chemistry, vol. 259, no. 12, pp. 7648–7651, 1984. View at Google Scholar · View at Scopus
  53. H. Egge, M. Kordowicz, J. Peter-Katalinic, and P. Hanfland, “Immunochemistry of I/i-active oligo- and polyglycosylceramides from rabbit erythrocyte membranes. Characterization of linear, di-, and triantennary neolactoglycosphingolipids,” The Journal of Biological Chemistry, vol. 260, no. 8, pp. 4927–4935, 1985. View at Google Scholar · View at Scopus
  54. P. Hanfland, M. Kordowicz, J. Peter-Katalinić, H. Egge, J. Dabrowski, and U. Dabrowski, “Structure elucidation of blood group B-like and I-active ceramide eicosa- and pentacosa-saccharides from rabbit erythrocyte membranes by combined gas chromatography-mass spectrometry; electron-impact and fast-atom-bombardment mass spectrometry; and two-dimensional correlated, relayed-coherence transfer, and nuclear overhauser effect 500-MHz 1H-N.m.r. spectroscopy,” Carbohydrate Research, vol. 178, no. 1, pp. 1–21, 1988. View at Publisher · View at Google Scholar · View at Scopus
  55. K. Honma, H. Manabe, M. Tomita, and A. Hamada, “Isolation and partial structural characterization of macroglycolipid from rabbit erythrocyte membranes,” Journal of Biochemistry, vol. 90, no. 4, pp. 1187–1196, 1981. View at Google Scholar · View at Scopus
  56. U. Galili, “Anti-Gal: an abundant human natural antibody of multiple pathogeneses and clinical benefits,” Immunology, vol. 140, no. 1, pp. 1–11, 2013. View at Publisher · View at Google Scholar · View at Scopus
  57. A. D. Thall, P. Maly, and J. B. Lowe, “Oocyte Galα1–3Gal epitopes implicated in sperm adhesion to the zona pellucida glycoprotein ZP3 are not required for fertilization in the mouse,” Journal of Biological Chemistry, vol. 270, no. 37, pp. 21437–21440, 1995. View at Publisher · View at Google Scholar · View at Scopus
  58. R. G. Tearle, M. J. Tange, Z. L. Zannettino et al., “The α-1,3-galactosyltransferase knockout mouse: implications for xenotransplantation,” Transplantation, vol. 61, no. 1, pp. 13–19, 1996. View at Publisher · View at Google Scholar · View at Scopus
  59. L. Lai, D. Kolber-Simonds, K.-W. Park et al., “Production of α-1,3-galactosyltransferase knockout pigs by nuclear transfer cloning,” Science, vol. 295, no. 5557, pp. 1089–1092, 2002. View at Publisher · View at Google Scholar · View at Scopus
  60. C. J. Phelps, C. Koike, T. D. Vaught et al., “Production of α1,3-galactosyltransferase-deficient pigs,” Science, vol. 299, no. 5605, pp. 411–414, 2003. View at Publisher · View at Google Scholar · View at Scopus
  61. D. Kolber-Simonds, L. Lai, S. R. Watt et al., “Production of α-1,3-galactosyltransferase null pigs by means of nuclear transfer with fibroblasts bearing loss of heterozygosity mutations,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 19, pp. 7335–7340, 2004. View at Publisher · View at Google Scholar · View at Scopus
  62. F. J. M. F. Dor, Y.-L. Tseng, J. Cheng et al., “α1-3-galactosyltransferase gene-knockout miniature swine produce natural cytotoxic anti-gal antobodies,” Transplantation, vol. 78, no. 1, pp. 15–20, 2004. View at Publisher · View at Google Scholar · View at Scopus
  63. J. Fang, A. Walters, H. Hara et al., “Anti-gal antibodies in α1,3-galactosyltransferase gene-knockout pigs,” Xenotransplantation, vol. 19, no. 5, pp. 305–310, 2012. View at Publisher · View at Google Scholar · View at Scopus
  64. K. Yamada, K. Yazawa, A. Shimizu et al., “Marked prolongation of porcine renal xenograft survival in baboons through the use of α1,3-galactosyltransferase gene-knockout donors and the cotransplantation of vascularized thymic tissue,” Nature Medicine, vol. 11, no. 1, pp. 32–34, 2005. View at Publisher · View at Google Scholar · View at Scopus
  65. G. Chen, H. Qian, T. Starzl et al., “Acute rejection is associated with antibodies to non-Gal antigens in baboons using Gal-knockout pig kidneys,” Nature Medicine, vol. 11, no. 12, pp. 1295–1298, 2005. View at Publisher · View at Google Scholar · View at Scopus
  66. Y.-L. Tseng, K. Kuwaki, F. J. M. F. Dor et al., “α1,3-galactosyltransferase gene-knockout pig heart transplantation in baboons with survival approaching 6 months,” Transplantation, vol. 80, no. 10, pp. 1493–1500, 2005. View at Publisher · View at Google Scholar · View at Scopus
  67. U. Galili, “Avoiding detrimental human immune response against mammalian extracellular matrix implants,” Tissue Engineering Part B: Reviews, vol. 21, no. 2, pp. 231–241, 2015. View at Publisher · View at Google Scholar
  68. M. J. van Amerongen, M. C. Harmsen, N. van Rooijen, A. H. Petersen, and M. J. A. Van Luyn, “Macrophage depletion impairs wound healing and increases left ventricular remodeling after myocardial injury in mice,” The American Journal of Pathology, vol. 170, no. 3, pp. 818–829, 2007. View at Publisher · View at Google Scholar · View at Scopus
  69. N. Mokarram, A. Merchant, V. Mukhatyar, G. Patel, and R. V. Bellamkonda, “Effect of modulating macrophage phenotype on peripheral nerve repair,” Biomaterials, vol. 33, no. 34, pp. 8793–8801, 2012. View at Publisher · View at Google Scholar · View at Scopus
  70. B. Chazaud, M. Brigitte, H. Yacoub-Youssef et al., “Dual and beneficial roles of macrophages during skeletal muscle regeneration,” Exercise and Sport Sciences Reviews, vol. 37, no. 1, pp. 18–22, 2009. View at Publisher · View at Google Scholar · View at Scopus
  71. M. Radisic and K. L. Christman, “Materials science and tissue engineering: repairing the heart,” Mayo Clinic Proceedings, vol. 88, no. 8, pp. 884–898, 2013. View at Publisher · View at Google Scholar · View at Scopus
  72. A. F. Bayomy, M. Bauer, Y. Qiu, and R. Liao, “Regeneration in heart disease—is ECM the key?” Life Sciences, vol. 91, no. 17-18, pp. 823–827, 2012. View at Publisher · View at Google Scholar · View at Scopus
  73. C. Dray, G. Rougon, and F. Debarbieux, “Quantitative analysis by in vivo imaging of the dynamics of vascular and axonal networks in injured mouse spinal cord,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 23, pp. 9459–9464, 2009. View at Publisher · View at Google Scholar · View at Scopus