Zinc deficiency activates S100A8 inflammation in the absence of COX-2 and promotes murine oral-esophageal tumor progression

International Journal of Cancer

Volumn 129, Issue 2, 2011, Pages 331-345

  Wan, Shao Gui ^a   Taccioli, Cristian ^b   Jiang, Yubao ^a   Chen, Hongping ^a   Smalley, Karl J ^c   Huang, Kun ^b   Liu, Xiu Ping ^b   Farber, John L ^a   Croce, Carlo M ^b   Fong, Louise Y Y ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

Cox 2 null mice; S100A8 inflammation; Tongue cancer prevention; Transcriptome profiling; Zinc deficiency

Indexed keywords

ADVANCED GLYCATION END PRODUCT RECEPTOR; CALGRANULIN A; CALGRANULIN B; CYCLIN D1; CYCLOOXYGENASE 2; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN P53; TRANSCRIPTION FACTOR RELA; 4 NITROQUINOLINE 1 OXIDE; CARCINOGEN; DIMETHYLNITROSAMINE; DRUG DERIVATIVE; N METHYL N NITROSO (4 METHYLPHENYL)METHYLAMINE; N-METHYL-N-NITROSO-(4-METHYLPHENYL)METHYLAMINE; S100A8 PROTEIN, MOUSE; ZINC;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CARCINOGENESIS; CONTROLLED STUDY; ESOPHAGUS CANCER; FEMALE; GENE; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; MOUTH CANCER; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; S100A8 GENE; S100A9 GENE; SIGNAL TRANSDUCTION; WILD TYPE; ZINC DEFICIENCY; ANIMAL; CHEMICALLY INDUCED DISORDER; DISEASE COURSE; DISEASE MODEL; ENZYMOLOGY; ESOPHAGUS TUMOR; GENE DELETION; GENETICS; INFLAMMATION; METABOLISM; MOUSE MUTANT; PATHOLOGY; STOMACH TUMOR; TONGUE TUMOR;

4-NITROQUINOLINE-1-OXIDE; ANIMALS; CALGRANULIN A; CARCINOGENS; CYCLOOXYGENASE 2; DIMETHYLNITROSAMINE; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; ESOPHAGEAL NEOPLASMS; FEMALE; GENE DELETION; INFLAMMATION; MALE; MICE; MICE, KNOCKOUT; STOMACH NEOPLASMS; TONGUE NEOPLASMS; ZINC;

EID: 79961114271     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.25688     Document Type: Article

References (50)

1. Parkin DM, Bray F, Ferlay J, Pisani P. Estimating the world cancer burden: Globocan 2000. Int J Cancer 2001;94: 153-6. (Pubitemid 32911406)
2. Slaughter DP, Southwick HW, Smejkal W. Field cancerization in oral stratified squamous epithelium; clinical implications of multicentric origin. Cancer 1953;6:963-8.
3. Moore SR, Johnson NW, Pierce AM, Wilson DF. The epidemiology of tongue cancer: A review of global incidence. Oral Dis 2000;6:75-84. (Pubitemid 30159034)
4. Prasad AS, Beck FW, Doerr TD, Shamsa FH, Penny HS, Marks SC, Kaplan J, Kucuk O, Mathog RH. Nutritional and zinc status of head and neck cancer patients: An interpretive review. J Am Coll Nutr 1998; 17:409-18. (Pubitemid 28445329)
5. Buntzel J, Bruns F, Glatzel M, Garayev A, Mucke R, Kisters K, Schafer U, Schonekaes K, Micke O. Zinc concentrations in serum during head and neck cancer progression. Anticancer Res 2007;27:1941-3. (Pubitemid 46954703)
6. Abnet CC, Lai B, Qiao YL, Vogt S, Luo XM, Taylor PR, Dong ZW, Mark SD, Dawsey SM. Zinc concentration in esophageal biopsy specimens measured by x-ray fluorescence and esophageal cancer risk. J Natl Cancer Inst 2005;97:301-6. (Pubitemid 40310278)
7. Doerr TD, Marks SC, Shamsa FH, Mathog RH, Prasad AS. Effects of zinc and nutritional status on clinical outcomes in head and neck cancer. Nutrition 1998;14: 489-95. (Pubitemid 28285281)
8. Vallee BL, Falchuk KH. The biochemical basis of zinc physiology. Physiol Rev 1993; 73:79-118. (Pubitemid 23065434)
9. Rink L, Haase H. Zinc homeostasis and immunity. Trends Immunol 2007;28:1-4. (Pubitemid 44960160)
10. O'Halloran TV. Transition metals in control of gene expression. Science 1993; 261:715-25. (Pubitemid 23278386)
11. Prasad AS, Beck FW, Snell DC, Kucuk O. Zinc in cancer prevention. Nutr Cancer 2009;61:879-87.
12. Maret W, Sandstead HH. Zinc requirements and the risks and benefits of zinc supplementation. J Trace Elem Med Biol 2006;20:3-18.
13. Fong LY, Zhang L, Jiang Y, Farber JL. Dietary zinc modulation of COX-2 expression and lingual and esophageal carcinogenesis in rats. J Natl Cancer Inst 2005;97:40-50.
14. Taccioli C, Wan SG, Liu CG, Alder H, Volinia S, Farber JL, Croce CM, Fong LY. Zinc replenishment reverses overexpression of the proinflammatory mediator S100A8 and esophageal preneoplasia in the rat. Gastroenterology 2009;136:953-66.
15. Fong LY, Nguyen VT, Farber JL. Esophageal cancer prevention in zincdeficient rats: Rapid induction of apoptosis by replenishing zinc. J Natl Cancer Inst 2001;93:1525-33. (Pubitemid 32998481)
16. Fong LY, Jiang Y, Riley M, Liu X, Smalley KJ, Guttridge DC, Farber JL. Prevention of upper aerodigestive tract cancer in zincdeficient rodents: Inefficacy of genetic or pharmacological disruption of COX-2. Int J Cancer 2008;122:978-89. (Pubitemid 351213994)
17. William WN, Jr, Heymach JV, Kim ES, Lippman SM. Molecular targets for cancer chemoprevention. Nat Rev Drug Discov 2009;8:213-25.
18. Zimmermann KC, Sarbia M, Weber AA, Borchard F, Gabbert HE, Schror K. Cyclooxygenase-2 expression in human esophageal carcinoma. Cancer Res 1999;59: 198-204. (Pubitemid 29062978)
19. Renkonen J, Wolff H, Paavonen T. Expression of cyclo-oxygenase-2 in human tongue carcinoma and its precursor lesions. Virchows Arch 2002;440:594-7. (Pubitemid 34809690)
20. Smith WL, DeWitt DL, Garavito RM. Cyclooxygenases: Structural, cellular, and molecular biology. Annu Rev Biochem 2000;69:145-82.
21. Oshima M, Dinchuk JE, Kargman SL, Oshima H, Hancock B, Kwong E, Trzaskos JM, Evans JF, Taketo MM. Suppression of intestinal polyposis in Apc delta716 knockout mice by inhibition of cyclooxygenase 2 (COX-2). Cell 1996;87: 803-9. (Pubitemid 26404280)
22. Menter DG, Schilsky RL, Dubois RN. Cyclooxygenase-2 and cancer treatment: Understanding the risk should be worth the reward. Clin Cancer Res 2010;16:1384-90.
23. Dawson SJ, Michael M, Biagi J, Foo KF, Jefford M, Ngan SY, Leong T, Hui A, Milner AD, Thomas RJ, Zalcberg JR. A phase I/II trial of celecoxib with chemotherapy and radiotherapy in the treatment of patients with locally advanced oesophageal cancer. Invest New Drugs 2007;25:123-9. (Pubitemid 46020870)
24. Bernier J, Bentzen SM, Vermorken JB. Molecular therapy in head and neck oncology. Nat Rev Clin Oncol 2009;6: 266-77.
25. Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009;4:44-57.
26. Newcombe RG. Two-sided confidence intervals for the single proportion: Comparison of seven methods. Stat Med 1998;17:857-72. (Pubitemid 28185165)
27. Kim MM, Glazer CA, Mambo E, Chatterjee A, Zhao M, Sidransky D, Califano JA. Head and neck cancer cell lines exhibit differential mitochondrial repair deficiency in response to 4NQO. Oral Oncol 2006;42:201-7. (Pubitemid 43106885)
28. Ide F, Oda H, Nakatsuru Y, Kusama K, Sakashita H, Tanaka K, Ishikawa T. Xeroderma pigmentosum group A gene action as a protection factor against 4-nitroquinoline 1-oxide-induced tongue carcinogenesis. Carcinogenesis 2001;22: 567-72. (Pubitemid 32288656)
29. Tang XH, Knudsen B, Bemis D, Tickoo S, Gudas LJ. Oral cavity and esophageal carcinogenesis modeled in carcinogentreated mice. Clin Cancer Res 2004;10: 301-13. (Pubitemid 38114193)
30. Tiano HF, Loftin CD, Akunda J, Lee CA, Spalding J, Sessoms A, Dunson DB, Rogan EG, Morham SG, Smart RC, Langenbach R. Deficiency of either cyclooxygenase (COX)-1 or COX-2 alters epidermal differentiation and reduces mouse skin tumorigenesis. Cancer Res 2002;62: 3395-401. (Pubitemid 34651385)
31. Karin M, Greten FR. NF-kappaB: Linking inflammation and immunity to cancer development and progression. Nat Rev Immunol 2005;5:749-59. (Pubitemid 41400849)
32. Gebhardt C, Nemeth J, Angel P, Hess J. S100A8 and S100A9 in inflammation and cancer. Biochem Pharmacol 2006;72: 1622-31. (Pubitemid 44666730)
33. Hinz M, Krappmann D, Eichten A, Heder A, Scheidereit C, Strauss M. NF-kappaB function in growth control: Regulation of cyclin D1 expression and G0/G1-to-Sphase transition. Mol Cell Biol 1999;19: 2690-8. (Pubitemid 29144513)
34. Pich A, Chiusa L, Navone R. Prognostic relevance of cell proliferation in head and neck tumors. Ann Oncol 2004;15:1319-29. (Pubitemid 39295019)
35. Shin DM, Lee JS, Lippman SM, Lee JJ, Tu ZN, Choi G, Heyne K, Shin HJ, Ro JY, Goepfert H, Hong WK, Hittelman WN. p53 expressions: Predicting recurrence and second primary tumors in head and neck squamous cell carcinoma. J Natl Cancer Inst 1996;88:519-29. (Pubitemid 26118722)
36. Greenblatt MS, Bennett WP, Hollstein M, Harris CC. Mutations in the p53 tumor suppressor gene: Clues to cancer etiology and molecular pathogenesis. Cancer Res 1994;54:4855-78. (Pubitemid 24289415)
37. Lee TL, Yang XP, Yan B, Friedman J, Duggal P, Bagain L, Dong G, Yeh NT, Wang J, Zhou J, Elkahloun A, Van Waes C, et al. A novel nuclear factor-kappaB gene signature is differentially expressed in head and neck squamous cell carcinomas in association with TP53 status. Clin Cancer Res 2007;13:5680-91. (Pubitemid 47591640)
38. Bowcock AM, Shannon W, Du F, Duncan J, Cao K, Aftergut K, Catier J, Fernandez-Vina MA, Menter A. Insights into psoriasis and other inflammatory diseases from large-scale gene expression studies. Hum Mol Genet 2001;10:1793-805. (Pubitemid 32899097)
39. Sugiura H, Ebise H, Tazawa T, Tanaka K, Sugiura Y, Uehara M, Kikuchi K, Kimura T. Large-scale DNA microarray analysis of atopic skin lesions shows overexpression of an epidermal differentiation gene cluster in the alternative pathway and lack of protective gene expression in the cornified envelope. Br J Dermatol 2005;152:146-9.
40. Ehrchen JM, Sunderkotter C, Foell D, Vogl T, Roth J. The endogenous Toll-like receptor 4 agonist S100A8/S100A9 (calprotectin) as innate amplifier of infection, autoimmunity, and cancer. J Leukoc Biol 2009;86:557-66.
41. Lo WY, Lai CC, Hua CH, Tsai MH, Huang SY, Tsai CH, Tsai FJ. S100A8 is identified as a biomarker of HPV18-infected oral squamous cell carcinomas by suppression subtraction hybridization, clinical proteomics analysis, and immunohistochemistry staining. J Proteome Res 2007;6:2143-51.
42. Gebhardt C, Riehl A, Durchdewald M, Nemeth J, Furstenberger G, Muller-Decker K, Enk A, Arnold B, Bierhaus A, Nawroth PP, Hess J, Angel P. RAGE signaling sustains inflammation and promotes tumor development. J Exp Med 2008;205:275-85. (Pubitemid 351281593)
43. Hiratsuka S, Watanabe A, Sakurai Y, Akashi-Takamura S, Ishibashi S, Miyake K, Shibuya M, Akira S, Aburatani H, Maru Y. The S100A8-serum amyloid A3-TLR4 paracrine cascade establishes a premetastatic phase. Nat Cell Biol 2008;10: 1349-55.
44. Turovskaya O, Foell D, Sinha P, Vogl T, Newlin R, Nayak J, Nguyen M, Olsson A, Nawroth PP, Bierhaus A, Varki N, Kronenberg M, et al. RAGE, carboxylated glycans and S100A8/A9 play essential roles in colitis-associated carcinogenesis. Carcinogenesis 2008;29:2035-43.
45. Nemeth J, Stein I, Haag D, Riehl A, Longerich T, Horwitz E, Breuhahn K, Gebhardt C, Schirmacher P, Hahn M, Ben-Neriah Y, Pikarsky E, et al. S100A8 and S100A9 are novel nuclear factor kappa B target genes during malignant progression of murine and human liver carcinogenesis. Hepatology 2009;50: 1251-62.
46. Taguchi A, Blood DC, del Toro G, Canet A, Lee DC, Qu W, Tanji N, Lu Y, Lalla E, Fu C, Hofmann MA, Kislinger T, et al. Blockade of RAGE-amphoterin signalling suppresses tumour growth and metastases. Nature 2000;405:354-60. (Pubitemid 30337069)
47. Wang F, Arun P, Friedman J, Chen Z, Van Waes C. Current and potential inflammation targeted therapies in head and neck cancer. Curr Opin Pharmacol 2009;9:389-95.
48. Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature 2008;454:436-44.
49. Lin LC, Que J, Lin KL, Leung HW, Lu CL, Chang CH. Effects of zinc supplementation on clinical outcomes in patients receiving radiotherapy for head and neck cancers: A double-blinded randomized study. Int J Radiat Oncol Biol Phys 2008;70:368-73.
50. Lin YS, Lin LC, Lin SW. Effects of zinc supplementation on the survival of patients who received concomitant chemotherapy and radiotherapy for advanced nasopharyngeal carcinoma: Follow-up of a double-blind randomized study with subgroup analysis. Laryngoscope 2009;119:1348-52.