Acute and long-term transcriptional responses in sulfur mustard-exposed SKH-1 hairless mouse skin

Cutaneous and Ocular Toxicology

Volumn 31, Issue 1, 2012, Pages 38-47

  Vallet, V ^a   Poyot, T ^a   Clery Barraud C ^a   Coulon, D ^a   Sentenac, C ^a   Peinnequin, A ^a   Boudry, I ^a  

^a CENTRE DE RECHERCHES   (France)

Author keywords

SKH 1; Skin; Sulfur mustard; Transcriptionnal response

Indexed keywords

CYTOKERATIN 1; GELATINASE A; GELATINASE B; INTERLEUKIN 1BETA; INTERLEUKIN 6; LAMININ GAMMA1; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 2; MESSENGER RNA; MUSTARD GAS; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; GENE EXPRESSION; GENETIC TRANSCRIPTION; HAIRLESS MOUSE; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION; VAPOR; WOUND HEALING;

ANIMALS; CHEMICAL WARFARE AGENTS; CYTOKINES; GENE EXPRESSION; KERATIN-1; LAMININ; MALE; MATRIX METALLOPROTEINASE 9; MICE; MICE, HAIRLESS; MUSTARD GAS; RECEPTORS, CCR1; RNA, MESSENGER; SKIN; TRANSCRIPTION, GENETIC;

ANIMALIA;

EID: 84856832929     PISSN: 15569527     EISSN: 15569535     Source Type: Journal    
DOI: 10.3109/15569527.2011.609206     Document Type: Article

References (62)

1. Young RA, Bast C. (2009). Handbook of Toxicology of Chemical Warfare Agents. In: Gupta RC, ed. Mustards and Vesicants. San Diego: Academic Press, 93-108.
2. Wattana M, Bey T. Mustard gas or sulfur mustard: an old chemical agent as a new terrorist threat. Prehosp Disaster Med 2009;24:19-29; discussion 30.
3. Ghabili K, Agutter PS, Ghanei M, Ansarin K, Shoja MM. Mustard gas toxicity: the acute and chronic pathological efects. J Appl Toxicol 2010;30:627-643.
4. Kehe K, Tiermann H, Balszuweit F, Eyer F, Steinritz D, Zilker T. Acute efects of sulfur mustard injury-Munich experiences. Toxicology 2009;263:3-8.
5. Yaraee R, Ghazanfari T, Ebtekar M, Ardestani SK, Rezaei A, Kariminia A et al. Alterations in serum levels of infammatory cytokines (TNF, IL-1α, IL-1β and IL-1Ra) 20 years after sulfur mustard exposure: Sardasht-Iran cohort study. Int Immunopharmacol 2009;9:1466-1470.
6. Firooz A, Sadr B, Davoudi SM, Nassiri-Kashani M, Panahi Y, Dowlati Y. Long-term skin damage due to chemical weapon exposure. Cutan Ocul Toxicol 2011;30:64-68.
7. Gerecke DR, Gray JP, Shakarjian MP, Casillas RP. (2009). Handbook of Toxicology of Chemical Warfare Agents. In: Gupta RC, ed. Dermal Toxicity of Sulfur Mustard. San Diego: Academic Press, 611-630.
8. Graham JS, Gerlach TW, Logan TP, Bonar JP, Fugo RJ, Lee RB et al. Methods of advanced wound management for care of combined traumatic and chemical warfare injuries. Eplasty 2008;8:e34.
9. Dacre JC, Goldman M. Toxicology and pharmacology of the chemical warfare agent sulfur mustard. Pharmacol Rev 1996;48:289-326.
10. Smith WJ, Dunn MA. Medical defense against blistering chemical warfare agents. Arch Dermatol 1991;127:1207-1213.
11. Shohrati M, Peyman M, Peyman A, Davoudi M, Ghanei M. Cutaneous and ocular late complications of sulfur mustard in Iranian veterans. Cutan Ocul Toxicol 2007;26:73-81. (Pubitemid 47027134)
12. Shakarjian MP, Heck DE, Gray JP, Sinko PJ, Gordon MK, Casillas RP et al. Mechanisms mediating the vesicant actions of sulfur mustard after cutaneous exposure. Toxicol Sci 2010;114:5-19.
13. Ghanei M, Poursaleh Z, Harandi AA, Emadi SE, Emadi SN. Acute and chronic efects of sulfur mustard on the skin: A comprehensive review. Cutan Ocul Toxicol 2010;29:269-277.
14. Smith KJ, Graham JS, Hamilton TA, Skelton HG, Petrali JP, Hurst CG. Immunohistochemical studies of basement membrane proteins and proliferation and apoptosis markers in sulfur mustard induced cutaneous lesions in weanling pigs. J Dermatol Sci 1997;15:173-182. (Pubitemid 27390883)
15. Lindsay CD, Rice P. Changes in connective tissue macromolecular components of Yucatan mini-pig skin following application of sulphur mustard vapour. Hum Exp Toxicol 1995;14:341-348.
16. Petrali JP, Oglesby-Megee S. Toxicity of mustard gas skin lesions. Microsc Res Tech 1997;37:221-228. (Pubitemid 27197742)
17. Ries C, Popp T, Egea V, Kehe K, Jochum M. Matrix metalloproteinase-9 expression and release from skin fbroblasts interacting with keratinocytes: Upregulation in response to sulphur mustard. Toxicology 2009;263:26-31.
18. Sabourin CL, Danne MM, Buxton KL, Casillas R P, Schlager JJ. Cytokine, chemokine, and matrix metalloproteinase response after sulfur mustard injury to weanling pig skin. J Biochem Mol Toxicol 2002;16:263-272. (Pubitemid 36097621)
19. Rogers J V, McDougal JN, Price JA, Reid FM, Graham JS. Transcriptional responses associated with sulfur mustard and thermal burns in porcine skin. Cutan Ocul Toxicol 2008;27:135-160.
20. Kan RK, Pleva CM, Hamilton TA, Anderson DR, Petrali JP. Sulfur mustard-induced apoptosis in hairless guinea pig skin. Toxicol Pathol 2003;31:185-190. (Pubitemid 36374007)
21. Mishra NC, Rir-sima-ah J, March T, Weber W, Benson J, Jaramillo R et al. Sulfur mustard induces immune sensitization in hairless guinea pigs. Int Immunopharmacol 2010;10:193-199.
22. Smith KJ, Graham JS, Moeller RB, Okerberg C V, Skelton H, Hurst CG. Histopathologic features seen in sulfur mustard induced cutaneous lesions in hairless guinea pigs. J Cutan Pathol 1995;22:260-268.
23. Snider TH, Matthews MC, Braue EH Jr. Model for assessing efcacy of topical skin protectants against sulfur mustard vapor using hairless guinea pigs. J Appl Toxicol 1999;19 Suppl 1:S55-S58. (Pubitemid 30093522)
24. Wormser U, Brodsky B, Sintov A. Skin toxicokinetics of mustard gas in the guinea pig: Efect of hypochlorite and safety aspects. Arch Toxicol 2002;76:517-522.
25. Yourick JJ, Clark CR, Mitcheltree LW. Niacinamide pretreatment reduces microvesicle formation in hairless guinea pigs cutaneously exposed to sulfur mustard. Fundam Appl Toxicol 1991;17:533-542.
26. Tsuruta J, Sugisaki K, Dannenberg AM Jr, Yoshimura T, Abe Y, Mounts P. Te cytokines NAP-1 (IL-8), MCP-1, IL-1 β, and GRO in rabbit infammatory skin lesions produced by the chemical irritant sulfur mustard. Infammation 1996;20:293-318. (Pubitemid 26246170)
27. Blank JA, Lane LA, Menton RG, Casillas RP. Procedure for assessing myeloperoxidase and infammatory mediator responses in hairless mouse skin. J Appl Toxicol 2000;20 Suppl 1:S137-S139.
28. Ricketts KM, Santai CT, France JA, Graziosi AM, Doyel TD, Gazaway MY et al. Infammatory cytokine response in sulfur mustard-exposed mouse skin. J Appl Toxicol 2000;20 Suppl 1:S73-S76.
29. Rogers JV, Choi YW, Kiser RC, Babin MC, Casillas RP, Schlager JJ et al. Microarray analysis of gene expression in murine skin exposed to sulfur mustard. J Biochem Mol Toxicol 2004;18:289-299. (Pubitemid 40165432)
30. Wormser U, Brodsky B, Proscura E, Foley J F, Jones T, Nyska A. Involvement of tumor necrosis factor-α in sulfur mustard-induced skin lesion; efect of topical iodine. Arch Toxicol 2005;79:660-670. (Pubitemid 41618949)
31. Sabourin CLK, Danne MM, Buxton KL, Rogers JV, Niemuth NA, Blank JA, et al. Modulation of sulfur mustard-induced infammation and gene expression by olvanil in the hairless mouse vesicant model. Cutan Ocul Toxicol 2003;22:125-36. (Pubitemid 36962042)
32. Smith KJ, Casillas R, Graham J, Skelton HG, Stemler F, Hackley BE Jr. Histopathologic features seen with diferent animal models following cutaneous sulfur mustard exposure. J Dermatol Sci 1997;14:126-135. (Pubitemid 27107148)
33. Benavides F, Oberyszyn TM, VanBuskirk AM, Reeve VE, Kusewitt DF. Te hairless mouse in skin research. J Dermatol Sci 2009;53:10-18.
34. Andersen F, Hedegaard K, Fullerton A, Petersen TK, Bindslev-Jensen C, Andersen KE. Te hairless guinea-pig as a model for treatment of acute irritation in humans. Skin Res Technol 2006;12:183-189. (Pubitemid 43985012)
35. Kim TH, Ananthaswamy HN, Kripke ML, Ullrich SE. Advantages of using hairless mice versus haired mice to test sunscreen efcacy against photoimmune suppressions. Photochem Photobiol 2003;78:37-42.
36. Sueki D. Hairless guinea pig skin: Anatomical basis for studies of cutaneous biology. Eur J Dermatol 2000;10:577.
37. Dachir S, Cohen M, Fishbeine E, Sahar R, Brandies R, Horwitz V et al. Characterization of acute and long-term sulfur mustard-induced skin injuries in hairless guinea-pigs using non-invasive methods. Skin Res Technol 2010;16:114-124.
38. Dorandeu F, Taysse L, Boudry I, Foquin A, Hérodin F, Mathieu J et al. Cutaneous challenge with chemical warfare agents in the SKH-1 hairless mouse. (I) Development of a model for screening studies in skin decontamination and protection. Hum Exp Toxicol 2011;30:470-490.
39. Sabourin CL, Petrali JP, Casillas RP. Alterations in infammatory cytokine gene expression in sulfur mustard-exposed mouse skin. J Biochem Mol Toxicol 2000;14:291-302.
40. Pal A, Tewari-Singh N, Gu M, Agarwal C, Huang J, Day BJ et al. Sulfur mustard analog induces oxidative stress and activates signaling cascades in the skin of SKH-1 hairless mice. Free Radic Biol Med 2009;47:1640-1651.
41. Tewari-Singh N, Agarwal C, Huang J, Day BJ, White CW, Agarwal R. Efcacy of glutathione in ameliorating sulfur mustard analog-induced toxicity in cultured skin epidermal cells and in SKH-1 mouse skin in vivo. J Pharmacol Exp Ter 2011;336:450-459.
42. Jain AK, Tewari-Singh N, Orlicky DJ, White CW, Agarwal R. 2-Chloroethyl ethyl sulfde causes microvesication and infammation-related histopathological changes in male hairless mouse skin. Toxicology 2011;282:129-138.
43. Nolan T, Hands RE, Bustin SA. Quantifcation of mRNA using realtime RT-PCR. Nat Protoc 2006;1:1559-1582.
44. Peinnequin A, Mouret C, Birot O, Alonso A, Mathieu J, Clarençon D et al. Rat pro-infammatory cytokine and cytokine related mRNA quantifcation by real-time polymerase chain reaction using SYBR green. Bmc Immunol 2004;5:3.
45. Pfaf MW. A new mathematical model for relative quantifcation in real-time RT-PCR. Nucleic Acids Res 2001;29:e45.
46. Cikos S, Bukovská A, Koppel J. Relative quantifcation of mRNA: Comparison of methods currently used for real-time PCR data analysis. Bmc Mol Biol 2007;8:113.
47. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002;3:RESEARCH0034.
48. Mershon MM, Mitcheltree LW, Petrali JP, Braue EH, Wade JV. Hairless guinea pig bioassay model for vesicant vapor exposures. Fundam Appl Toxicol 1990;15:622-630. (Pubitemid 20362407)
49. Mitcheltree LW, Mershon MM, Wall HG, Pulliam JD, Manthei JH. Microblister Formation in Vesicant-Exposed Pig Skin. Cutan Ocul Toxicol 1989;8:309-319. (Pubitemid 19253374)
50. Gerecke DR, Chen M, Isukapalli SS, Gordon MK, Chang YC, Tong W et al. Diferential gene expression profling of mouse skin after sulfur mustard exposure: Extended time response and inhibitor efect. Toxicol Appl Pharmacol 2009;234:156-165.
51. Sabourin CL, Rogers J V, Choi YW, Kiser RC, Casillas RP, Babin MC et al. Time-and dose-dependent analysis of gene expression using microarrays in sulfur mustard-exposed mice. J Biochem Mol Toxicol 2004;18:300-312. (Pubitemid 40165433)
52. Price JA, Rogers JV, McDougal JN, Shaw MQ, Reid FM, Graham JS. Transcriptional changes in porcine skin at 7 days following sulfur mustard and thermal burn injury. Cutan Ocul Toxicol 2009;28:129-140.
53. Wolpe SD, Cerami A. Macrophage infammatory proteins 1 and 2: Members of a novel superfamily of cytokines. Faseb J 1989;3:2565-2573. (Pubitemid 20013270)
54. Shakarjian MP, Bhatt P, Gordon MK, Chang YC, Casbohm SL, Rudge TL et al. Preferential expression of matrix metalloproteinase-9 in mouse skin after sulfur mustard exposure. J Appl Toxicol 2006;26:239-246. (Pubitemid 43773884)
55. Woessner JF Jr, Dannenberg AM Jr, Pula PJ, Selzer MG, Ruppert CL, Higuchi K et al. Extracellular collagenase, proteoglycanase and products of their activity, released in organ culture by intact dermal infammatory lesions produced by sulfur mustard. J Invest Dermatol 1990;95:717-726.
56. Greenberg S, Kamath P, Petrali J, Hamilton T, Garfeld J, Garlick JA. Characterization of the initial response of engineered human skin to sulfur mustard. Toxicol Sci 2006;90:549-557.
57. Chang YC, Sabourin CL, Lu SE, Sasaki T, Svoboda KK, Gordon MK et al. Upregulation of γ-2 laminin-332 in the mouse ear vesicant wound model. J Biochem Mol Toxicol 2009;23:172-184.
58. Koshikawa N, Moriyama K, Takamura H, Mizushima H, Nagashima Y, Yanoma S et al. Overexpression of laminin γ2 chain monomer in invading gastric carcinoma cells. Cancer Res 1999;59:5596-5601. (Pubitemid 29526479)
59. Porter RM, Lane EB. Phenotypes, genotypes and their contribution to understanding keratin function. Trends Genet 2003;19:278-285. (Pubitemid 36507010)
60. Mansbridge JN, Knapp AM. Changes in keratinocyte maturation during wound healing. J Invest Dermatol 1987;89:253-263. (Pubitemid 17135369)
61. HogenEsch H, Boggess D, Sundberg JP. Changes in keratin and flaggrin expression in the skin of chronic proliferative dermatitis (cpdm) mutant mice. Pathobiology 1999;67:45-50. (Pubitemid 29037611)
62. Leigh IM, Purkis PE, Whitehead P, Lane EB. Monospecifc monoclonal antibodies to keratin 1 carboxy terminal (synthetic peptide) and to keratin 10 as markers of epidermal diferentiation. Br J Dermatol 1993;129:110-119. (Pubitemid 23250719)