The immunology of the porcine skin and its value as a model for human skin

Molecular Immunology

Volumn 66, Issue 1, 2015, Pages 14-21

  Summerfield, Artur ^a   Meurens, François ^b   Ricklin, Meret E ^a  

^a INSTITUTE OF VIROLOGY AND IMMUNOLOGY   (Switzerland)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

Animal model; Dendritic cells; Dermis; Epidermis; Lymphocytes; Porcine skin

Indexed keywords

DENDRITIC CELL; HUMAN; IMMUNOLOGY; KERATINOCYTE; LANGERHANS CELL; LYMPHOCYTE; MACROPHAGE; NONHUMAN; PORCINE MODEL; PRIORITY JOURNAL; REVIEW; SKIN; ANIMAL; DISEASE MODEL; MONOCYTE; PATHOLOGY; PIG; PLASMA CELL; SKIN DISEASE;

ANIMALIA; SUIDAE; SUS;

DIFFERENTIATION ANTIGEN;

ANIMALS; ANTIGENS, DIFFERENTIATION; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; HUMANS; MACROPHAGES; MONOCYTES; PLASMA CELLS; SKIN; SKIN DISEASES; SWINE;

EID: 84924559653     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2014.10.023     Document Type: Review

References (75)

1. Abdullahi A., Amini-Nik S., Jeschke M.G. Animal models in burn research. Cell. Mol. Life Sci. 2014, 71:3241-3255.
2. Agay D., Scherthan H., Forcheron F., Grenier N., Herodin F., Meineke V., Drouet M. Multipotent mesenchymal stem cell grafting to treat cutaneous radiation syndrome: development of a new minipig model. Exp. Hematol. 2010, 38:945-956.
3. Ansell D.M., Holden K.A., Hardman M.J. Animal models of wound repair: are they cutting it?. Exp. Dermatol. 2012, 21:581-585.
4. Auffray C., Sieweke M.H., Geissmann F. Blood monocytes: development, heterogeneity, and relationship with dendritic cells. Annu. Rev. Immunol. 2009, 27:669-692.
5. Barbero A.M., Frasch H.F. Pig and guinea pig skin as surrogates for human in vitro penetration studies: a quantitative review. Toxicol. In Vitro 2009, 23:1-13.
6. Bennett C.L., Fallah-Arani F., Conlan T., Trouillet C., Goold H., Chorro L., Flutter B., Means T.K., Geissmann F., Chakraverty R. Langerhans cells regulate cutaneous injury by licensing CD8 effector cells recruited to the skin. Blood 2011, 117:7063-7069.
7. Boltjes A., van Wijk F. Human dendritic cell functional specialization in steady-state and inflammation. Front. Immunol. 2014, 5:131.
8. Brancato S.K., Albina J.E. Wound macrophages as key regulators of repair: origin, phenotype, and function. Am. J. Pathol. 2011, 178:19-25.
9. Brozyna A., Wasilewska K., Wesierska K., Chwirot B.W. Porcine skin as a model system for studies of adverse effects of narrow-band UVB pulses on human skin. J. Toxicol. Environ. Health A 2009, 72:789-795.
10. Carr M.M., Howard C.J., Sopp P., Manser J.M., Parsons K.R. Expression on porcine gamma delta lymphocytes of a phylogenetically conserved surface antigen previously restricted in expression to ruminant gamma delta T lymphocytes. Immunology 1994, 81:36-40.
11. Carrasco C.P., Rigden R.C., Schaffner R., Gerber H., Neuhaus V., Inumaru S., Takamatsu H., Bertoni G., McCullough K.C., Summerfield A. Porcine dendritic cells generated in vitro: morphological, phenotypic and functional properties. Immunology 2001, 104:175-184.
12. Clark R.A., Chong B., Mirchandani N., Brinster N.K., Yamanaka K., Dowgiert R.K., Kupper T.S. The vast majority of CLA+ T cells are resident in normal skin. J. Immunol. 2006, 176:4431-4439.
13. Debeer S., Le Luduec J.B., Kaiserlian D., Laurent P., Nicolas J.F., Dubois B., Kanitakis J. Comparative histology and immunohistochemistry of porcine versus human skin. Eur. J. Dermatol. 2013, 23:456-466.
14. Di Meglio P., Perera G.K., Nestle F.O. The multitasking organ: recent insights into skin immune function. Immunity 2011, 35:857-869.
15. Eldardiri M., Martin Y., Roxburgh J., Lawrence-Watt D.J., Sharpe J.R. Wound contraction is significantly reduced by the use of microcarriers to deliver keratinocytes and fibroblasts in an in vivo pig model of wound repair and regeneration. Tissue Eng. Part A 2012, 18:587-597.
16. Elias P.M. The skin barrier as an innate immune element. Semin. Immunopathol. 2007, 29:3-14.
17. Ezquerra A., Revilla C., Alvarez B., Perez C., Alonso F., Dominguez J. Porcine myelomonocytic markers and cell populations. Dev. Comp. Immunol. 2009, 33:284-298.
18. Forbes P.D. Vascular Supply of the Skin and Hair in Swine 1969, vol. 9:419-432. Pergamon, Oxford.
19. Gebhardt T., Wakim L.M., Eidsmo L., Reading P.C., Heath W.R., Carbone F.R. Memory T cells in nonlymphoid tissue that provide enhanced local immunity during infection with herpes simplex virus. Nat. Immunol. 2009, 10:524-530.
20. Godin B., Touitou E. Transdermal skin delivery: predictions for humans from in vivo, ex vivo and animal models. Adv. Drug Deliv. Rev. 2007, 59:1152-1161.
21. Gregorio J., Meller S., Conrad C., Di Nardo A., Homey B., Lauerma A., Arai N., Gallo R.L., Digiovanni J., Gilliet M. Plasmacytoid dendritic cells sense skin injury and promote wound healing through type I interferons. J. Exp. Med. 2010, 207:2921-2930.
22. Grice E.A., Segre J.A. The skin microbiome. Nat. Rev. Microbiol. 2011, 9:244-253.
23. Guzylack-Piriou L., Alves M.P., McCullough K.C., Summerfield A. Porcine Flt3 ligand and its receptor: generation of dendritic cells and identification of a new marker for porcine dendritic cells. Dev. Comp. Immunol. 2010, 34:455-464.
24. Hammond S.A., Tsonis C., Sellins K., Rushlow K., Scharton-Kersten T., Colditz I., Glenn G.M. Transcutaneous immunization of domestic animals: opportunities and challenges. Adv. Drug Deliv. Rev. 2000, 43:45-55.
25. Haniffa M., Collin M., Ginhoux F. Ontogeny and functional specialization of dendritic cells in human and mouse. Adv. Immunol. 2013, 120:1-49.
26. Hao Y., Wax D., Zhong Z., Murphy C., Ross J.W., Rieke A., Samuel M., Spate L., Dyce P., Li J., Sutovsky P., Prather R.S. Porcine skin-derived stem cells can serve as donor cells for nuclear transfer. Cloning Stem Cells 2009, 11:101-110.
27. Heath W.R., Carbone F.R. The skin-resident and migratory immune system in steady state and memory: innate lymphocytes, dendritic cells and T cells. Nat. Immunol. 2013, 14:978-985.
28. Huang Y.W., Dryman B.A., Li W., Meng X.J. Porcine DC-SIGN: molecular cloning, gene structure, tissue distribution and binding characteristics. Dev. Comp. Immunol. 2009, 33:464-480.
29. Igyarto B.Z., Haley K., Ortner D., Bobr A., Gerami-Nejad M., Edelson B.T., Zurawski S.M., Malissen B., Zurawski G., Berman J., Kaplan D.H. Skin-resident murine dendritic cell subsets promote distinct and opposing antigen-specific T helper cell responses. Immunity 2011, 35:260-272.
30. Imkhieo S., Nakthong C., Kespichayawattana W., Sirimujalin R., Suwannaprapha P., Ratanabanangkoon K. Pig as an experimental model for the study of snake venom induced local tissue necrosis. Toxicon 2009, 53:317-322.
31. Jenkins D.M., Murray W.B., Kennett M.J., Hughes E.L., Werner J.R. The effects of continuous application of the TASER X26 waveform on Sus scrofa. J. Forensic Sci. 2013, 58:684-692.
32. Jung Y., Son D., Kwon S., Kim J., Han K. Experimental pig model of clinically relevant wound healing delay by intrinsic factors. Int. Wound J. 2013, 10:295-305.
33. Kawamata S., Ozawa J., Hashimoto M., Kurose T., Shinohara H. Structure of the rat subcutaneous connective tissue in relation to its sliding mechanism. Arch. Histol. Cytol. 2003, 66:273-279.
34. Kiwanuka E., Hackl F., Philip J., Caterson E.J., Junker J.P., Eriksson E. Comparison of healing parameters in porcine full-thickness wounds transplanted with skin micrografts, split-thickness skin grafts, and cultured keratinocytes. J. Am. Coll. Surg. 2011, 213:728-735.
35. Klechevsky E. Human dendritic cells - stars in the skin. Eur. J. Immunol. 2013, 43:3147-3155.
36. Kong R., Bhargava R. Characterization of porcine skin as a model for human skin studies using infrared spectroscopic imaging. Analyst 2011, 136:2359-2366.
37. Mahl J.A., Vogel B.E., Court M., Kolopp M., Roman D., Nogues V. The minipig in dermatotoxicology: methods and challenges. Exp. Toxicol. Pathol. 2006, 57:341-345.
38. Mair K.H., Sedlak C., Kaser T., Pasternak A., Levast B., Gerner W., Saalmuller A., Summerfield A., Gerdts V., Wilson H.L., Meurens F. The porcine innate immune system: an update. Dev. Comp. Immunol. 2014, 45:321-343.
39. Malissen B., Tamoutounour S., Henri S. The origins and functions of dendritic cells and macrophages in the skin. Nat. Rev. Immunol. 2014, 14:417-428.
40. Marquet F., Bonneau M., Pascale F., Urien C., Kang C., Schwartz-Cornil I., Bertho N. Characterization of dendritic cells subpopulations in skin and afferent lymph in the swine model. PLoS ONE 2011, 6:e16320.
41. Merad M., Sathe P., Helft J., Miller J., Mortha A. The dendritic cell lineage: ontogeny and function of dendritic cells and their subsets in the steady state and the inflamed setting. Annu. Rev. Immunol. 2013, 31:563-604.
42. Meurens F., Summerfield A., Nauwynck H., Saif L., Gerdts V. The pig: a model for human infectious diseases. Trends Microbiol. 2012, 20:50-57.
43. Meyer W., Schwarz R., Neurand K. The skin of domestic mammals as a model for the human skin, with special reference to the domestic pig. Curr. Probl. Dermatol. 1978, 7:39-52.
44. Miossec P., Korn T., Kuchroo V.K. Interleukin-17 and type 17 helper T cells. N. Engl. J. Med. 2009, 361:888-898.
45. Montagna W., Yun J.S. The skin of the domestic pig. J. Invest. Dermatol. 1964, 42:11-21.
46. Moreno S., Alvarez B., Poderoso T., Revilla C., Ezquerra A., Alonso F., Dominguez J. Porcine monocyte subsets differ in the expression of CCR2 and in their responsiveness to CCL2. Vet. Res. 2010, 41:76.
47. Mounsey K., Ho M.F., Kelly A., Willis C., Pasay C., Kemp D.J., McCarthy J.S., Fischer K. A tractable experimental model for study of human and animal scabies. PLoS Negl. Trop. Dis. 2010, 4:e756.
48. Nestle F.O., Di Meglio P., Qin J.Z., Nickoloff B.J. Skin immune sentinels in health and disease. Nat. Rev. Immunol. 2009, 9:679-691.
49. Nfon C.K., Dawson H., Toka F.N., Golde W.T. Langerhans cells in porcine skin. Vet. Immunol. Immunopathol. 2008, 126:236-247.
50. Pascale F., Contreras V., Bonneau M., Epardaud M., Niborsky V., Riffault S., Balazuc A., Foulon L., Guzylack-Piriou L., Riteau B., Hope J., Bertho N., Charley B., Schwartz-Cornil I. Plasmacytoid dendritic cells migrate in afferent skin lymph. J. Immunol. 2008, 180:5963-5972.
51. Pfutzner W., Joari M.R., Foster R.A., Vogel J.C. A large preclinical animal model to assess ex vivo skin gene therapy applications. Arch. Dermatol. Res. 2006, 298:16-22.
52. Proksch E., Brandner J.M., Jensen J.M. The skin: an indispensable barrier. Exp. Dermatol. 2008, 17:1063-1072.
53. Rampton M., Walton S.F., Holt D.C., Pasay C., Kelly A., Currie B.J., McCarthy J.S., Mounsey K.E. Antibody responses to Sarcoptes scabiei apolipoprotein in a porcine model: relevance to immunodiagnosis of recent infection. PLOS ONE 2013, 8:e65354.
54. Ricklin M.E., Roosje P., Summerfield A. Characterization of canine dendritic cells in healthy, atopic, and non-allergic inflamed skin. J. Clin. Immunol. 2010, 30:845-854.
55. Rushmer R.F., Buettner K.J., Short J.M., Odland G.F. The skin. Science 1966, 154:343-348.
56. San Mateo L.R., Toffer K.L., Orndorff P.E., Kawula T.H. Immune cells are required for cutaneous ulceration in a swine model of chancroid. Infect. Immun. 1999, 67:4963-4967.
57. Sang Y., Blecha F. Porcine host defense peptides: expanding repertoire and functions. Dev. Comp. Immunol. 2009, 33:334-343.
58. Schlitzer A., Ginhoux F. Organization of the mouse and human DC network. Curr. Opin. Immunol. 2014, 26:90-99.
59. Sheridan B.S., Lefrancois L. Regional and mucosal memory T cells. Nat. Immunol. 2011, 12:485-491.
60. Sheu S.Y., Wang W.L., Fu Y.T., Lin S.C., Lei Y.C., Liao J.H., Tang N.Y., Kuo T.F., Yao C.H. The pig as an experimental model for mid-dermal burns research. Burns 2014, http://dx.doi.org/10.1016/j.burns.2014.04.023.
61. Simon G.A., Maibach H.I. The pig as an experimental animal model of percutaneous permeation in man: qualitative and quantitative observations - an overview. Skin Pharmacol. Appl. Skin Physiol. 2000, 13:229-234.
62. Smirnova O.A., Hu S., Cucinotta F.A. Dynamics of acutely irradiated skin epidermal epithelium in swine: modeling studies. Health Phys. 2014, 107:47-59.
63. Sonnenberg G.F., Fouser L.A., Artis D. Border patrol: regulation of immunity, inflammation and tissue homeostasis at barrier surfaces by IL-22. Nat. Immunol. 2011, 12:383-390.
64. Sullivan T.P., Eaglstein W.H., Davis S.C., Mertz P. The pig as a model for human wound healing. Wound Repair Regen. 2001, 9:66-76.
65. Summerfield A., Guzylack-Piriou L., Schaub A., Carrasco C.P., Tache V., Charley B., McCullough K.C. Porcine peripheral blood dendritic cells and natural interferon-producing cells. Immunology 2003, 110:440-449.
66. Summerfield A., McCullough K.C. The porcine dendritic cell family. Dev. Comp. Immunol. 2009, 33:299-309.
67. Summerfield A., Auray G., Ricklin M. Comparative dendritic cells biology of veterinary mammals. Annu. Rev. Anim. Biosc. 2015, 10.1146/annurev-animal-022114-111009.
68. Tfaili S., Gobinet C., Josse G., Angiboust J.F., Manfait M., Piot O. Confocal Raman microspectroscopy for skin characterization: a comparative study between human skin and pig skin. Analyst 2012, 137:3673-3682.
69. Vana G., Meingassner J.G. Morphologic and immunohistochemical features of experimentally induced allergic contact dermatitis in Gottingen minipigs. Vet. Pathol. 2000, 37:565-580.
70. Vardaxis N.J., Brans T.A., Boon M.E., Kreis R.W., Marres L.M. Confocal laser scanning microscopy of porcine skin: implications for human wound healing studies. J. Anat. 1997, 190(Pt 4):601-611.
71. Wakim L.M., Waithman J., van Rooijen N., Heath W.R., Carbone F.R. Dendritic cell-induced memory T cell activation in nonlymphoid tissues. Science 2008, 319:198-202.
72. Wang Y.I., Sanders J. Skin Model Studies 2005, 263-285. Springer, Berlin. D.L. Bader, C.V.C. Bouten, D. Colin, C.W.J. Oomens (Eds.).
73. Yan G., Sun H., Wang F., Wang J., Wang F., Zou Z., Cheng T., Ai G., Su Y. Topical application of hPDGF-A-modified porcine BMSC and keratinocytes loaded on acellular HAM promotes the healing of combined radiation-wound skin injury in minipigs. Int. J. Radiat. Biol. 2011, 87:591-600.
74. Yu M., Guo F., Ling Y., Li N., Tan F. Topical skin targeting effect of penetration modifiers on hairless mouse skin, pig abdominal skin and pig ear skin. Drug Deliv. 2013, 10.3109/10717544.2013.869276.
75. Zhao M.T., Yang X., Lee K., Mao J., Teson J.M., Whitworth K.M., Samuel M.S., Spate L.D., Murphy C.N., Prather R.S. The in vivo developmental potential of porcine skin-derived progenitors and neural stem cells. Stem Cells Dev. 2012, 21:2682-2688.