Deoxynivalenol induced mouse skin cell proliferation and inflammation via MAPK pathway

Toxicology and Applied Pharmacology

Volumn 279, Issue 2, 2014, Pages 186-197

  Mishra, Sakshi ^a,b   Tripathi, Anurag ^a   Chaudhari, Bhushan P ^a   Dwivedi, Premendra D ^a   Pandey, Haushila P ^b   Das, Mukul ^a  

^a CSIR INDIAN INSTITUTE OF TOXICOLOGY RESEARCH   (India)

^b BANARAS HINDU UNIVERSITY   (India)

Author keywords

Cytokines; Deoxynivalenol; Mycotoxins; Peyer's patches; Skin cell proliferation; Skin inflammation

Indexed keywords

CYCLIN D1; CYCLOOXYGENASE 2; DNA; GAMMA INTERFERON; I KAPPA B KINASE ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1; INTERLEUKIN 17; INTERLEUKIN 4; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE; MYELOPEROXIDASE; ORNITHINE DECARBOXYLASE; PROTEIN C FOS; PROTEIN C JUN; RAS PROTEIN; THYMIDINE; VOMITOXIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; EPIDERMIS; EPIDERMIS HYPERPLASIA; FEMALE; GENE ACTIVATION; GENE OVEREXPRESSION; HAIR FOLLICLE; HISTOPATHOLOGY; HYPERPLASIA; INFLAMMATION; INTESTINE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PEYER PATCH; PROTEIN EXPRESSION; SKIN CARCINOGENESIS; SKIN CELL; SKIN EDEMA; SKIN PAPILLOMA; SKIN TOXICITY; SKINFOLD THICKNESS; TRANSCRIPTION INITIATION;

CYTOKINES; DEOXYNIVALENOL; MYCOTOXINS; PEYER'S PATCHES; SKIN CELL PROLIFERATION; SKIN INFLAMMATION;

ANIMALS; CELL PROLIFERATION; CYTOKINES; DERMATITIS; DOSE-RESPONSE RELATIONSHIP, DRUG; EDEMA; ENZYME ACTIVATION; FEMALE; GENE EXPRESSION REGULATION; HYPERPLASIA; HYPERTROPHY; INFLAMMATION MEDIATORS; MAP KINASE SIGNALING SYSTEM; MICE; ORNITHINE DECARBOXYLASE; PEROXIDASE; PEYER'S PATCHES; PHOSPHORYLATION; RISK ASSESSMENT; SKIN; TIME FACTORS; TRANSCRIPTION FACTORS; TRICHOTHECENES;

EID: 84903784772     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2014.06.003     Document Type: Article

References (88)

1. Afaq F., Adhami V.M., Ahmad N., Mukhtar H. Suppression of UVB-induced phosphorylation of mitogen-activated protein kinases and nuclear factor kappa B by green tea polyphenol in SKH-1 hairless mice. Oncogene 2003, 22:9254-9264.
2. Ahmad N., Gilliam A.C., Katiyar S.K., O'Brien T.G., Mukhtar H. A definitive role of ornithine decarboxylase in photocarcinogenesis. Am. J. Pathol. 2001, 159:885-892.
3. Almeida M.I., Almeida N.G., Carvalho K.L., Gonçalves G.A., Silva C.N., Santos E.A., Garcia J.C., Vargas E.A. Co-occurrence of aflatoxins B1, B2, G1 and G2, ochratoxin A, zearalenone, deoxynivalenol, and citreoviridin in rice in Brazil. Food Addit. Contam. Part A: Chem. Anal. Control Expo. Risk Assess. 2012, 294:694-703.
4. Angel P., Karin M. The role of Jun, Fos and the AP-1 complex in cell-proliferation and transformation. Biochim. Biophys. Acta 1991, 1072:129-157.
5. Baldwin A.S. Control of oncogenesis and cancer therapy resistance by the transcription factor NF-κB. J. Clin. Invest. 2001, 107:241-246.
6. Beck P.L., Wallace J.L. Cytokines in inflammatory bowel disease. Mediat. Inflamm. 1997, 2:95-103.
7. Bennett J.W., Klich M. Mycotoxins. Clin. Microbiol. Rev. 2003, 497-516.
8. Bhat R.V., Sashidhar R.B., Ramakrishna Y., Munshi K.L. Outbreak of trichothecene mycotoxicoses associated with consumption of mould damaged wheat products in Kashmir valley, India. Lancet 1989, I:35-37.
9. Boonen J., Malysheva S.V., Taevernier L., Diana Di, Mavungu J., DeSaeger S., Despiegeleer B. Human skin penetration of selected model mycotoxins. Toxicology 2012, 301:21-32.
10. Bowles D.W., Jimeno A. New phosphatidylinositol 3-kinase inhibitors for cancer. Expert. Opin. Investig. Drugs 2011, 20:507-518.
11. Bradley P.P., Priebat D.A., Christensen R.D., Rothstein G. Measurement of cutaneous inflammation: estimation of neutrophil content with an enzyme marker. J. Investig. Dermatol. 1982, 78:206-209.
12. Callejas N.A., Casado M., Bosca L., Martin-Sanz P. Requirement of nuclear factor κB for the constitutive expression of nitric oxide synthase-2 and cyclooxygenase-2 in rat trophoblasts. J. Cell Sci. 1999, 18:3147-3155.
13. Canady R.A., Coker R.D., Rgan S.K., Krska R., Kuiper-Goodman T., Olsen M., Pestka J.J., Resnik S., Schlatter J. Deoxynivalenol. Safety evaluation of certain mycotoxins in food. WHO Food Additives Series 2001, 47:420-555. International Programme on Chemical Safety-World Health Organization, Geneva.
14. CAST Potential economic costs of mycotoxins in the United States. Mycotoxins: Risks in Plant, Animal, and Human Systems. Task Force Report No. 139 2003, 136-142. Council for Agricultural Science and Technology, Ames, IA.
15. Castellano E., Downward J. Role of RAS in the regulation of PI 3-kinase. Curr. Top. Microbiol. Immunol. 2011, 346:143-169.
16. Chun K.S., Kang J.Y., Kim O.H., Kang H., Surh Y.J. Effects of yakuchinone A and yakuchinone B on the phorbol ester-induced expression of COX-2 and iNOS and activation of NF-κB in mouse skin. J. Environ. Pathol. Toxicol. Oncol. 2002, 21:131-139.
17. Edwards S.G., Dickin E.T., MacDonald S., Buttler D., Hazel C.M., Patel S., Scudamore K.A. Distribution of Fusarium mycotoxins in UK wheat mill fractions. Food Addit. Contam. Part A: Chem. Anal. Control Expo. Risk Assess. 2011, 28(12):1694-1704.
18. Einspahr J.G., Bowden G.T., Alberts D.S. Skin cancer chemoprevention: strategies to save our skin. Recent Results Cancer Res. 2003, 163:151-164.
19. Fujiki H., Sueoka E., Komori A., Suganuma M. Tumor promotion and TNF-a gene expression by the okadaic acid class tumor promoters. Environ. Carcinog. Ecotoxicol. Rev. 1997, 15:1-40.
20. Goyarts T., Dar̈nicke S. Bioavailability of the Fusarium toxin deoxynivalenol (DON) from naturally contaminated wheat for the pig. Toxicol. Lett. 2006, 163:171-182.
21. Gupta K.P., Mehrotra N.K. Status of ornithine decarboxylase activity and DNA synthesis in mancozeb-exposed mouse skin. Carcinogenesis 1992, 13:131-133.
22. Guttridge D.C., Albanese C., Reuther J.Y., Pestell R.G., Baldwin A.S. NF-nB controls cell growth and differentiation through transcriptional regulation of cyclin D1. Mol. Cell. Biol. 1999, 19:5785-5799.
23. Herschman H.R. Regulation of prostaglandin synthase-1 and prostaglandin synthase-2. Cancer Metastasis Rev. 1994, 13:241-256.
24. Hsia C.C., Wu J.L., Lu X.Q., Li Y.S. Natural occurrence and clastogenic effects of nivalenol, deoxynivalenol, 3-acetyl-deoxynivalenol, 15-acetyl-deoxynivalenol, and zearalenone in corn from a high-risk area of esophageal cancer. Cancer Detect. Prev. 1988, 13:79-86.
25. Huang C., Ma W.Y., Young M.R., Colburn N., Dong Z. Shortage of mitogen-activated protein kinase is responsible for resistance to AP-1 transactivation and transformation in mouse JB6 cells. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:156-161.
26. Huang X.H., Zhang X.H., Li Y.H., Wang J.L., Yan X., Xing L.X., Wang F.R. Carcinogenic effects of sterigmatocystin and deoxynivalenol in NIH mice. Chin. J. Oncol. 2004, 26(12):705-708.
27. IARC (International Agency for Research on Cancer) Monographs on the evaluation of carcinogenic risks to humans; some naturally occurring substances, food items and constituents. Heterocyclic Aromatic Amines and Mycotoxins, International Agency for Research on Cancer, World Health Organization, Lyon, France. 56 1993, 397-444.
28. Israel A. A role for phosphorylation and degradation in the control of NF-kappa B activity. Trends Genet. 1995, 11:203-205.
29. Iverson F., Armstrong C., Nera E., Truelove J., Fernie S., Scott P., Stapley R., Hayward S., Gunner S. Chronic feeding study of deoxynivalenol in B6C3F1 male and female mice. Teratog. Carcinog. Mutagen. 1995, 15:283-306.
30. JECFA Joint Food and Agriculture Organization/World Health Organization Expert Committee on Food Additives. Joint FAO/WHO Expert Committee on Food Additives Seventy-second Meeting, Rome, 16-25 February 2010: Summary and Conclusions 2010, (http://www.who.int/foodsafety/chem/summary72_rev.pdf).
31. Karin M. The regulation of AP-1 activity by mitogen-activated protein kinases. J. Biol. Chem. 1995, 270:16483-16486.
32. Katiyar S.K., Rupp C.O., Korman N.J., Agarwal R., Mukhtar H. Inhibition of 12-O-tetradecanoylphorbol-13-acetate and other skin tumor-promoter-caused induction of epidermal interleukin-1 alpha mRNA and protein expression in SENCAR mice by green tea polyphenols. J. Investig. Dermatol. 1995, 105:394-398.
33. Katiyar S.K., Agarwal R., Mukhtar H. Inhibition of tumor promotion in SENCAR mouse skin by ethanol extract of Zingiber officinale rhizome. Cancer Res. 1996, 56:1023-1030.
34. Kumar R., Dwivedi P.D., Dhawan A., Das M., Ansari K.M. Citrinin generated reactive oxygen species cause cell cycle arrest leading to apoptosis via the intrinsic mitochondrial pathway in mouse skin. Toxicol. Sci. 2011, 122:557-566.
35. Kumar R., Ansari K.M., Chaudhari B.P., Dhawan A., Dwivedi P.D., Jain S.K., Das M. Topical application of ochratoxin A causes DNA damage and tumor initiation in mouse skin. PLoS One 2012, 7:e47280.
36. Lambert L.A., Hines F.A., Eppley R.M. Lack of initiation and promotion potential of deoxynivalenol for skin tumorigenesis in Sencar mice. Food Chem. Toxicol. 1995, 33:217-222.
37. Lampe E., Heinrich M., Walczak H., Kalthoff H. CD95 and TRAIL receptor-mediated activation of protein kinase C and NF-kappaB contributes to apoptosis resistance in ductal pancreatic adenocarcinoma cells. Oncogene 2001, 20:4258-4269.
38. Lee W.Y., Fischer S.M., Butler A.P., Locniskar M.F. Modulation of interleukin-1a mRNA expression in mouse epidermis by tumor promoters and antagonists. Mol. Carcinog. 1993, 7:26-35.
39. Lee T., Lee S.H., Lee S.H., Shin J.Y., Yun J.C., Lee Y.W., Ryu J.G. Occurrence of Fusarium mycotoxins in rice and its milling by-products in Korea. J. Food Prot. 2011, 74:1169-1174.
40. Li F.Q., Luo X.Y., Yoshizawa T. Mycotoxins (trichothecenes, zearalenone and fumonisins) in cereals associated with human red-mold intoxications stored since 1989 and 1991 in China. Nat. Toxins 1999, 7:93-97.
41. Lu H., Ouyang W., Huang C. Inflammation, a key event in cancer development. Mol. Cancer Res. 2006, 4:221-233.
42. Luo Y., Yoshizawa T., Katayama T. Comparative study on the natural occurrence of Fusarium mycotoxins (trichothecenes and zearalenone) in corn and wheat from high and low-risk areas for esophageal cancer in China. Appl. Environ. Microbiol. 1990, 56:3723-3726.
43. Luque I., Gelinas C. Rel/NF-κB and IkB factors in oncogenesis. Semin. Cancer Biol. 1997, 8:103-111.
44. Ma Y.Y., Guo H.W. Mini-review of studies on the carcinogenicity of deoxynivalenol. Environ. Toxicol. Pharmacol. 2008, 25:1-9.
45. Mao J.H., To M.D., Losada J.P., Wu D., Rosario R.D., Balmain A. Mutually exclusive mutations of the Pten and RAS pathways in skin tumor progression. Genes Dev. 2004, 18:1800-1805.
46. Mishra S., Ansari K.M., Dwivedi P.D., Pandey H.P., Das M. Occurrence of deoxynivalenol in cereals and exposure risk assessment in Indian population. Food Control 2013, 30:549-555.
47. Moodie S.A., Willumsen B.M., Weber M.J., Wolfman A. Complexes of RAS.GTP with Raf-1 and mitogen-activated protein kinase kinase. Science 1993, 260:1658-1661.
48. Moon Y., Pestka J.J. Vomitoxin-induced cyclooxygenase-2 gene expression in macrophages mediated by activation of ERK and p38 but not JNK mitogen activated protein kinases. Toxicol. Sci. 2002, 69:373-382.
49. Mueller M. Inflammation in epithelial skin tumours: old stories and new ideas. Eur. J. Cancer 2006, 42:735-744.
50. Pestka J.J. Mechanisms of deoxynivalenol-induced gene expression and apoptosis. Food Addit. Contam. 2008, 25:1128-1140.
51. Pestka J.J., Smolinski A.T. Deoxynivalenol toxicity and potential effects on humans. J. Toxicol. Environ. Health B 2005, 8:39-69.
52. Pestka J.J., Dong W., Warner R.L., Rasooly L., Bond G.S. Effect of dietary administration of the trichothecene vomitoxin (deoxynivalenol) on IgA and IgG secretion by Peyer's patch and splenic lymphocytes. Food Chem. Toxicol. 1990, 28:693-699.
53. Pestka J.J., Zhou H.R., Moon Y., Chung Y.J. Cellular and molecular mechanisms for immune modulation by deoxynivalenol and other trichothecenes: unraveling a paradox. Toxicol. Lett. 2004, 15:61-73.
54. Peters G. The D-type cyclins and their role in tumorigenesis. J. Cell Sci. 1994, 18:89-96.
55. Poirier M.C. Chemical-induced DNA damage and human cancer risk. Nat. Rev. Cancer 2004, 4:630-637.
56. Potapova O., Gorospe M., Bost F., Dean N.M., Gaarde W.A., Mercola D., Holbrook N.J. c-Jun N-terminal kinase is essential for growth of human T98G glioblastoma cells. J. Biol. Chem. 2000, 275:24767-24775.
57. Raick A.N. Cell proliferation and promoting action in skin carcinogenesis. Cancer Res. 1974, 34:920-926.
58. Rastogi S., Dogra R.K.S., Khanna S.K., Das M. Skin tumorigenic potential of aflatoxin B1 in mice. Food Chem. Toxicol. 2006, 44:670-677.
59. Rayet B., Gelinas C. Aberrant rel/nfκb genes and activity in human cancer. Oncogene 1999, 18:6938-6947.
60. Roberts P.J., Der C.J. Targeting the RAF-MEK-ERK mitogen-activated protein kinase cascade for the treatment of cancer. Oncogene 2007, 26:3291-3310.
61. Rotter B.A., Prelusky D.B., Pestka J.J. Toxicology of deoxynivalenol (vomitoxin). J. Toxicol. Environ. Health 1996, 48:1-34.
62. Roux P.P., Blenis J. ERK and p38 MAPK activated protein kinases: a family of protein kinases with diverse biological functions. Microbiol. Mol. Biol. Rev. 2004, 68:320-344.
63. Rundhaug J.E., Fischer S.M. Molecular mechanisms of mouse skin tumor promotion. Cancers 2010, 2:436-482.
64. Saleem M., Afaq F., Adhami V.M., Mukhtar H. Lupeol modulates NF-kappaB and PI3K/Akt pathways and inhibits skin cancer in CD-1 mice. Oncogene 2004, 23:5203-5214.
65. Sauder D.N. The role of epidermal cytokines in inflammatory skin diseases. J. Investig. Dermatol. 1990, 95:27-28.
66. Saxena N., Ansari K.M., Kumar R., Dhawan A., Dwivedi P.D., Das M. Patulin causes DNA damage leading to cell cycle arrest and apoptosis though modulation of Bax, p53 and p21/WAF1 proteins in skin of mice. Toxicol. Appl. Pharmacol. 2009, 234:192-201.
67. Saxena N., Ansari K.M., Kumar R., Chaudhari B.P., Dwivedi P.D., Das M. Role of mitogen activated protein kinases in skin tumorigenicity of patulin. Toxicol. Appl. Pharmacol. 2011, 257:264-271.
68. Schothorst R., Van Egmond H. Report from SCOOP task 3.2.10 "collection of occurrence data of Fusarium toxins in food and assessment of dietary intake by the population of EU member states" subtask: trichothecenes. Toxicol. Lett. 2004, 153:133-143.
69. Seo H.J., Park K.K., Han S.S., Chung W.Y., Son M.W., Kim W.B., Surh Y.J. Inhibitory effects of the standardized extract (DA-9601) of Artemisia asiatica Nakai on phorbol ester-induced ornithine decarboxylase activity, papilloma formation, cyclooxygenase-2 expression, inducible nitric oxide synthase expression and nuclear transcription factor kappa B activation in mouse skin. Int. J. Cancer 2002, 100:456-462.
70. Shaulian E., Karin M. AP-1 in cell proliferation and survival. Oncogene 2001, 20:2390-2400.
71. Shaw R.J., Cantley L.C. RAS, PI(3)K and mTOR signalling controls tumour cell growth. Nature 2006, 441:424-430.
72. Shifrin V.I., Anderson P. Trichothecene mycotoxins trigger a ribotoxic stress response that activates c-Jun N-terminal kinase and p38 mitogen-activated protein kinase and induces apoptosis. J. Biol. Chem. 1999, 274:13985-13992.
73. Shishodia S., Majumdar S., Banerjee S., Aggarwal B.B. Ursolic acid inhibits nuclear factor-kappaB activation induced by carcinogenic agents through suppression of IkappaBalpha kinase and p65 phosphorylation: correlation with down-regulation of cyclooxygenase 2, matrix metalloproteinase 9, and cyclin D1. Cancer Res. 2003, 63:4375-4383.
74. Silvers A.L., Bachelor M.A., Bowden G.T. The role of JNK and p38 MAPK activities in UVA-induced signaling pathways leading to AP-1 activation and c-Fos expression 1. Neoplasia 2003, 5:319-329.
75. Slaga T.J., Fischer S.M., Nelson K., Gleason G.L. Studies on the mechanism of skin tumor promotion: evidence for several stages in promotion. Proc. Natl. Acad. Sci. U. S. A. 1980, 77:3659-3663.
76. Slaga T.J., Fischer S.M., Weeks C.E., Klein-Szanto A.J.P., Reiners J. Studies on the mechanisms involved in multistage carcinogenesis in mouse skin. J. Cell. Biochem. 1982, 18:99-119.
77. Surh Y.J., Kundu J.K. Signal transduction network leading to COX-2 induction: a road map in search of cancer chemopreventives. Arch. Pharm. Res. 2005, 28:1-15.
78. Thanos D., Maniatis T. NF-kappa B: a lesson in family values. Cell 1995, 80:529-532.
79. Thomas T., Thomas T.J. Polyamine metabolism and cancer. J. Cell. Mol. Med. 2003, 7:113-126.
80. Van Der Fels-Klerx H.J., Klemsdal S., Hietaniemic V., Lindblad M., Ioannou-Kakouri E., Van Asselta E.D. Mycotoxin contamination of cereal grain commodities in relation to climate in North West Europe. Food Addit. Contam. Part A: Chem. Anal. Control Expo. Risk Assess. 2012, 29:1581-1592.
81. Verma A.K., Shapas B.G., Rice H.M., Boutwell R.K. Correlation of the inhibition by retinoid of tumor promoter-induced mouse epidermal ornithine decarboxylase activity and skin tumor promotion. Cancer Res. 1979, 39:419-425.
82. Vivanco I., Sawyers C.L. The phosphatidylinositol 3-kinase AKT pathway in human cancer. Nat. Rev. Cancer 2002, 2:489-501.
83. Vojtek A.B., Hollenberg S.M., Cooper J.A. Mammalian RAS interacts directly with the serine/threonine kinase Raf. Cell 1993, 74:205-214.
84. Warne P.H., Viciana P.R., Downward J. Direct interaction of RAS and the amino-terminal region of Raf-1 in vitro. Nature 1993, 364:352-355.
85. WHO Food Additives Series: 47 Safety evaluation of certain mycotoxins in food. Prepared by 49th Meeting of JECFA 1998, WHO, Geneva.
86. Yang G.H., Jarvis B.B., Chung Y.J., Pestka J.J. Apoptosis induction by the satratoxins and other trichothecene mycotoxins: relationship to ERK, p38 MAPK and SAPK/JNK activation. Toxicol. Appl. Pharmacol. 2000, 164:149-160.
87. Zhang X.F., Settleman J., Kyriakis J.M., Takeuchi-Suzuki E., Elledge S.J., Marshall M.S., Bruder J.T., Rapp U.R., Avruch J. Normal and oncogenic p21RAS proteins bind to the amino-terminal regulatory domain of c-Raf-1. Nature 1993, 364:308-313.
88. Zhou H.R., Pestka J.J. Deoxynivalenol-induced apoptosis mediated by p38 MAPK-dependent p53 gene induction in RAW 264.7 macrophages. Toxicol. 2003, 72:330.