Development of a bioengineered skin-humanized mouse model for psoriasis: Dissecting epidermal-lymphocyte interacting pathways

American Journal of Pathology

Volumn 177, Issue 6, 2010, Pages 3112-3124

  Guerrero Aspizua, Sara ^a   García, Marta ^a   Murillas, Rodolfo ^a   Retamosa, Luisa ^a   Illera, Nuria ^a   Duarte, Blanca ^a   Holguín, Almudena ^a   Puig, Susana ^b,c   Hernández, Maria Isabel ^d   Meana, Alvaro ^c,e   Jorcano, Jose Luis ^a   Larcher, Fernando ^a   Carretero, Marta ^a   Del Río, Marcela ^a  

^a CIEMAT   (Spain)

^b HOSPITAL CLÍNIC   (Spain)

^c CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED DE ENFERMEDADES RARAS CIBERER   (Spain)

^d Hospital de la Defensa   (Spain)

^e Centro Comunitario de Sangre y Tejidos Del Principado de Asturias (CCST)   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 17; INTERLEUKIN 22;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOENGINEERING; EPIDERMIS CELL; HUMAN; HUMAN CELL; LYMPHOCYTE; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE SUBPOPULATION; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PSORIASIS; SKIN GRAFT; STRATUM CORNEUM; TH17 CELL;

EID: 78650215247     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.100078     Document Type: Article

References (42)

1. Naldi L, Gambini D: The clinical spectrum of psoriasis. Clin Dermatol 2007, 25:510-518
2. Gudjonsson JE, Johnston A, Dyson M, Valdimarsson H, Elder JT: Mouse models of psoriasis. J Invest Dermatol 2007, 127:1292-1308
3. Danilenko DM: Review paper: preclinical models of psoriasis. Vet Pathol 2008, 45:563-575
4. Wrone-Smith T, Nickoloff BJ: Dermal injection of immunocytes induces psoriasis. J Clin Invest 1996, 98:1878-1887 (Pubitemid 26359206)
5. Boehncke WH, Dressel D, Zollner TM, Kaufmann R: Pulling the trigger on psoriasis. Nature 1996, 379:777
6. Del Rio M, Larcher F, Serrano F, Meana A, Munoz M, Garcia M, Munoz E, Martin C, Bernad A, Jorcano JL: A preclinical model for the analysis of genetically modified human skin in vivo. Hum Gene Ther 2002, 13:959-968
7. Llames SG, Del Rio M, Larcher F, Garcia E, Garcia M, Escamez MJ, Jorcano JL, Holguin P, Meana A: Human plasma as a dermal scaffold for the generation of a completely autologous bioengineered skin. Transplantation 2004, 77:350-355
8. Escamez MJ, Garcia M, Larcher F, Meana A, Munoz E, Jorcano JL, Del Rio M: An in vivo model of wound healing in genetically modified skin-humanized mice. J Invest Dermatol 2004, 123:1182-1191
9. Gache Y, Baldeschi C, Del Rio M, Gagnoux-Palacios L, Larcher F, Lacour JP, Meneguzzi G: Construction of skin equivalents for gene therapy of recessive dystrophic epidermolysis bullosa. Hum Gene Ther 2004, 15:921-933
10. Garcia M, Escamez MJ, Carretero M, Mirones I, Martinez-Santamaria L, Navarro M, Jorcano JL, Meana A, Del Rio M, Larcher F: Modeling normal and pathological processes through skin tissue engineering. Mol Carcinog 2007, 46:741-745
11. Schlaak JF, Buslau M, Jochum W, Hermann E, Girndt M, Gallati H, Meyer zum Buschenfelde KH, Fleischer B: T cells involved in psoriasis vulgaris belong to the Th1 subset. J Invest Dermatol 1994, 102:145-149
12. Komiyama Y, Nakae S, Matsuki T, Nambu A, Ishigame H, Kakuta S, Sudo K, Iwakura Y: IL-17 plays an important role in the development of experimental autoimmune encephalomyelitis. J Immunol 2006, 177:566-573 (Pubitemid 43939170)
13. Cua DJ, Sherlock J, Chen Y, Murphy CA, Joyce B, Seymour B, Lucian L, To W, Kwan S, Churakova T, Zurawski S, Wiekowski M, Lira SA, Gorman D, Kastelein RA, Sedgwick JD: Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 2003, 421:744-748
14. Nakae S, Nambu A, Sudo K, Iwakura Y: Suppression of immune induction of collagen-induced arthritis in IL-17-deficient mice. J Immunol 2003, 171:6173-6177
15. Murphy CA, Langrish CL, Chen Y, Blumenschein W, McClanahan T, Kastelein RA, Sedgwick JD, Cua DJ: Divergent pro- and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J Exp Med 2003, 198:1951-1957
16. Austin LM, Ozawa M, Kikuchi T, Walters IB, Krueger JG: The majority of epidermal T cells in Psoriasis vulgaris lesions can produce type 1 cytokines, interferon-gamma, interleukin-2, and tumor necrosis factor-alpha, defining TC1 (cytotoxic T lymphocyte) and TH1 effector populations: a type 1 differentiation bias is also measured in circulating blood T cells in psoriatic patients. J Invest Dermatol 1999, 113:752-759
17. Wolk K, Witte E, Wallace E, Docke WD, Kunz S, Asadullah K, Volk HD, Sterry W, Sabat R: IL-22 regulates the expression of genes responsible for antimicrobial defense, cellular differentiation, and mobility in keratinocytes: a potential role in psoriasis. Eur J Immunol 2006, 36:1309-1323
18. Blauvelt A: T-helper 17 cells in psoriatic plaques and additional genetic links between IL-23 and psoriasis. J Invest Dermatol 2008, 128:1064-1067
19. Lowes MA, Bowcock AM, Krueger JG: Pathogenesis and therapy of psoriasis. Nature 2007, 445:866-873
20. Nickoloff BJ, Xin H, Nestle FO, Qin JZ: The cytokine and chemokine network in psoriasis. Clin Dermatol 2007, 25:568-573
21. Sano S, Chan KS, Carbajal S, Clifford J, Peavey M, Kiguchi K, Itami S, Nickoloff BJ, DiGiovanni J: Stat3 links activated keratinocytes and immunocytes required for development of psoriasis in a novel transgenic mouse model. Nat Med 2005, 11:43-49
22. Zenz R, Eferl R, Kenner L, Florin L, Hummerich L, Mehic D, Scheuch H, Angel P, Tschachler E, Wagner EF: Psoriasis-like skin disease and arthritis caused by inducible epidermal deletion of Jun proteins. Nature 2005, 437:369-375
23. Zhang XJ, Huang W, Yang S, Sun LD, Zhang FY, Zhu QX, Zhang FR, Zhang C, Du WH, Pu XM, Li H, Xiao FL, Wang ZX, Cui Y, Hao F, Zheng J, Yang XQ, Cheng H, He CD, Liu XM, Xu LM, Zheng HF, Zhang SM, Zhang JZ, Wang HY, Cheng YL, Ji BH, Fang QY, Li YZ, Zhou FS, Han JW, Quan C, Chen B, Liu JL, Lin D, Fan L, Zhang AP, Liu SX, Yang CJ, Wang PG, Zhou WM, Lin GS, Wu WD, Fan X, Gao M, Yang BQ, Lu WS, Zhang Z, Zhu KJ, Shen SK, Li M, Zhang XY, Cao TT, Ren W, Zhang X, He J, Tang XF, Lu S, Yang JQ, Zhang L, Wang DN, Yuan F, Yin XY, Huang HJ, Wang HF, Lin XY, Liu JJ: Psoriasis genome-wide association study identifies susceptibility variants within LCE gene cluster at 1q21. Nat Genet 2009, 41:205-210
24. de Cid R, Riveira-Munoz E, Zeeuwen PL, Robarge J, Liao W, Dannhauser EN, Giardina E, Stuart PE, Nair R, Helms C, Escaramis G, Ballana E, Martin-Ezquerra G, den Heijer M, Kamsteeg M, Joosten I, Eichler EE, Lazaro C, Pujol RM, Armengol L, Abecasis G, Elder JT, Novelli G, Armour JA, Kwok PY, Bowcock A, Schalkwijk J, Estivill X: Deletion of the late cornified envelope LCE3B and LCE3C genes as a susceptibility factor for psoriasis. Nat Genet 2009, 41:211-215
25. Ahn SK, Hwang SM, Jiang SJ, Choi EH, Lee SH: The changes of epidermal calcium gradient and transitional cells after prolonged occlusion following tape stripping in the murine epidermis. J Invest Dermatol 1999, 113:189-195
26. Meana A, Iglesias J, Del Rio M, Larcher F, Madrigal B, Fresno MF, Martin C, San Roman F, Tevar F: Large surface of cultured human epithelium obtained on a dermal matrix based on live fibroblast-containing fibrin gels. Burns 1998, 24:621-630 (Pubitemid 29002580)
27. Serrano F, Del Rio M, Larcher F, Garcia M, Munoz E, Escamez MJ, Munoz M, Meana A, Bernad A, Jorcano JL: A comparison of targeting performance of oncoretroviral versus lentiviral vectors on human keratinocytes. Hum Gene Ther 2003, 14:1579-1585
28. Escamez MJ, Carretero M, Garcia M, Martinez-Santamaria L, Mirones I, Duarte B, Holguin A, Garcia E, Garcia V, Meana A, Jorcano JL, Larcher F, Del Rio M: Assessment of optimal virus-mediated growth factor gene delivery for human cutaneous wound healing enhancement. J Invest Dermatol 2008, 128:1565-1575
29. García M, Llames S, García E, Meana A, Cuadrado N, Recasens M, Puig S, Nagore E, Illera N, Jorcano JL, Del Rio M, Larcher F: In vivo assessment of acute UVB responses in normal and xeroderma pigmentosum (XP-C) skin-humanized mouse models. Am J Pathol 2010, 177: 865-872
30. Di Nunzio F, Maruggi G, Ferrari S, Di Iorio E, Poletti V, Garcia M, Del Rio M, De Luca M, Larcher F, Pellegrini G, Mavilio F: Correction of laminin-5 deficiency in human epidermal stem cells by transcriptionally targeted lentiviral vectors. Mol Ther 2008, 16:1977-1985
31. Llames S, Garcia E, Garcia V, del Rio M, Larcher F, Jorcano JL, Lopez E, Holguin P, Miralles F, Otero J, Meana A: Clinical results of an autologous engineered skin. Cell Tissue Bank 2006, 7:47-53
32. Nickoloff BJ, Wrone-Smith T: Injection of pre-psoriatic skin with CD4+ T cells induces psoriasis. Am J Pathol 1999, 155:145-158
33. Nickoloff BJ, Kunkel SL, Burdick M, Strieter RM: Severe combined immunodeficiency mouse and human psoriatic skin chimeras. Validation of a new animal model. Am J Pathol 1995, 146:580-588
34. Gilhar A, David M, Ullmann Y, Berkutski T, Kalish RS: T-lymphocyte dependence of psoriatic pathology in human psoriatic skin grafted to SCID mice. J Invest Dermatol 1997, 109:283-288
35. Boyman O, Hefti HP, Conrad C, Nickoloff BJ, Suter M, Nestle FO: Spontaneous development of psoriasis in a new animal model shows an essential role for resident T cells and tumor necrosis factor-alpha. J Exp Med 2004, 199:731-736
36. Albanesi C, De Pita O, Girolomoni G: Resident skin cells in psoriasis: a special look at the pathogenetic functions of keratinocytes. Clin Dermatol 2007, 25:581-588
37. Wolk K, Haugen HS, Xu W, Witte E, Waggie K, Anderson M, Vom Baur E, Witte K, Warszawska K, Philipp S, Johnson-Leger C, Volk HD, Sterry W, Sabat R: IL-22 and IL-20 are key mediators of the epidermal alterations in psoriasis while IL-17 and IFN-gamma are not. J Mol Med 2009, 87:523-536
38. Nograles KE, Zaba LC, Guttman-Yassky E, Fuentes-Duculan J, Suarez-Farinas M, Cardinale I, Khatcherian A, Gonzalez J, Pierson KC, White TR, Pensabene C, Coats I, Novitskaya I, Lowes MA, Krueger JG: Th17 cytokines interleukin (IL)-17 and IL-22 modulate distinct inflammatory and keratinocyte-response pathways. Br J Dermatol 2008, 159:1092-1102
39. Capon F, Semprini S, Chimenti S, Fabrizi G, Zambruno G, Murgia S, Carcassi C, Fazio M, Mingarelli R, Dallapiccola B, Novelli G: Fine mapping of the PSORS4 psoriasis susceptibility region on chromosome 1q21. J Invest Dermatol 2001, 116:728-730
40. Chen H, Toh TK, Szeverenyi I, Ong RT, Theng CT, McLean WH, Seielstad M, Lane EB: Association of skin barrier genes within the PSORS4 locus is enriched in Singaporean Chinese with early-onset psoriasis. J Invest Dermatol 2009, 129:606-614
41. Rio MD, Larcher F, Meana A, Segovia J, Alvarez A, Jorcano J: Nonviral transfer of genes to pig primary keratinocytes: induction of angiogenesis by composite grafts of modified keratinocytes overexpressing VEGF driven by a keratin promoter. Gene Ther 1999, 6:1734-1741
42. Larcher F, Del Rio M, Serrano F, Segovia JC, Ramirez A, Meana A, Page A, Abad JL, Gonzalez MA, Bueren J, Bernad A, Jorcano JL: A cutaneous gene therapy approach to human leptin deficiencies: correction of the murine ob/ob phenotype using leptin-targeted keratinocyte grafts. FASEB J 2001, 15:1529-1538