Long-term study of ovine pulmonary adenocarcinogenesis in sheep with marginal vs. sufficient nutritional selenium supply: Results from computed tomography, pathology, immunohistochemistry, JSRV-PCR and lung biochemistry

Journal of Trace Elements in Medicine and Biology

Volumn 27, Issue 4, 2013, Pages 391-399

  Humann Ziehank, Esther ^a   Renko, Kostja ^b   Bruegmann, Michael L ^c   Devi, Vemuri Rama ^a   Hewicker Trautwein, Marion ^a   Andreae, Arnim ^a   Ganter, Martin ^a  

^a UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c Abteilung Pathologie   (Germany)

Author keywords

Carcinogenesis; GPx; Lung; Selenium; Sheep model

Indexed keywords

GLUTATHIONE PEROXIDASE; GLUTATHIONE PEROXIDASE 1; SELENIUM; THIOREDOXIN REDUCTASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; AUTOPSY; BIOCHEMISTRY; CANCER GROWTH; CANCER PREVENTION; CELL INFILTRATION; COMPUTER ASSISTED TOMOGRAPHY; CONTROLLED STUDY; DIABETES MELLITUS; DIET; FOOD INTAKE; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; JAAGSIEKTE; JAAGSIEKTE SHEEP RETROVIRUS; LIVER BIOPSY; LUNG ABSCESS; LUNG ALVEOLUS CELL; LUNG CANCER; LUNG CARCINOGENESIS; LUNG LAVAGE; LUNG PARENCHYMA; LYMPH NODE; NONHUMAN; NUTRIENT SUPPLY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SHEEP; ANIMAL; CELL PROLIFERATION; DEFICIENCY; DIET SUPPLEMENTATION; DISEASE MODEL; ENZYMOLOGY; GENETICS; LUNG; METABOLISM; PATHOLOGY; TIME;

ANIMALIA; JAAGSIEKTE SHEEP RETROVIRUS; OVIS; OVIS ARIES;

ANIMALS; CELL PROLIFERATION; DIETARY SUPPLEMENTS; DISEASE MODELS, ANIMAL; GLUTATHIONE PEROXIDASE; IMMUNOHISTOCHEMISTRY; LUNG; POLYMERASE CHAIN REACTION; PULMONARY ADENOMATOSIS, OVINE; SELENIUM; SHEEP; TIME FACTORS; TOMOGRAPHY, X-RAY COMPUTED;

EID: 84884590715     PISSN: 0946672X     EISSN: 18783252     Source Type: Journal    
DOI: 10.1016/j.jtemb.2013.03.002     Document Type: Article

References (53)

1. Parkin D.M., Bray F., Ferlay J., Pisani P. Global cancer statistics, 2002. CA Cancer J Clin 2005, 55:74-108.
2. Alwahaibi N., Mohamed J., Alhamadani A. Supplementation of selenium reduces chemical hepatocarcinogenesis in male Sprague-Dawley rats. J Trace Elem Med Biol 2010, 24:119-123.
3. Peters U., Chatterjee N., Church T.R., Mayo C., Sturup S., Foster C.B., et al. High serum selenium and reduced risk of advanced colorectal adenoma in a colorectal cancer early detection program. Cancer Epidemiol Biomarkers Prev 2006, 15:315-320.
4. Duffield-Lillico A.J., Reid M.E., Turnbull B.W., Combs G.F., Slate E.H., Fischbach L.A., et al. Baseline characteristics and the effect of selenium supplementation on cancer incidence in a randomized clinical trial: a summary report of the Nutritional Prevention of Cancer Trial. Cancer Epidemiol Biomarkers Prev 2002, 11:630-639.
5. Fritz H., Kennedy D., Fergusson D., Fernandes R., Cooley K., Seely A., et al. Selenium and lung cancer: a systematic review and meta analysis. PLoS ONE 2011, 6:11.
6. Dennert G., Zwahlen M., Brinkman M., Vinceti M., Zeegers M.P., Horneber M. Selenium for preventing cancer. Cochrane Database Syst Rev 2011, 10.1002/14651858.CD005195.pub2.
7. Mueller A.S., Bosse A.C., Most E., Klomann S.D., Schneider S., Pallauf J. Regulation of the insulin antagonistic protein tyrosine phosphatase 1B by dietary Se studied in growing rats. J Nutr Biochem 2009, 20:235-247.
8. Steinbrenner H., Speckmann B., Pinto A., Sies H. High selenium intake and increased diabetes risk: experimental evidence for interplay between selenium and carbohydrate metabolism. J Clin Biochem Nutr 2011, 48:40-45.
9. Papp L.V., Lu J., Holmgren A., Khanna K.K. From selenium to selenoproteins: synthesis, identity, and their role in human health. Antioxid Redox Signal 2007, 9:775-806.
10. Wingler K., Bocher M., Flohe L., Kollmus H., Brigelius-Flohe R. mRNA stability and selenocysteine insertion sequence efficiency rank gastrointestinal glutathione peroxidase high in the hierarchy of selenoproteins. Eur J Biochem 1999, 259:149-157.
11. Brigelius-Flohe R., Kipp A. Glutathione peroxidases in different stages of carcinogenesis. Biochim Biophys Acta 2009, 1790:1555-1568.
12. Griffiths D.J., Martineau H.M., Cousens C. Pathology and pathogenesis of ovine pulmonary adenocarcinoma. J Comp Pathol 2010, 142:260-283.
13. Palmarini M., Sharp J.M., de las Heras M., Fan H. Jaagsiekte sheep retrovirus is necessary and sufficient to induce a contagious lung cancer in sheep. J Virol 1999, 73:6964-6972.
14. Palmarini M., Fan H. Retrovirus-induced ovine pulmonary adenocarcinoma, an animal model for lung cancer. J Natl Cancer Inst 2001, 93:1603-1614.
15. Humann-Ziehank E., Wolf P., Renko K., Schomburg L., Bruegmann M.L., Andreae A., et al. Ovine pulmonary adenocarcinoma as an animal model of progressive lung cancer and the impact of nutritional selenium supply. J Trace Elem Med Biol 2011, 25:S30-S34.
16. Humann-Ziehank E., Brauer C., Kuks A., Andreae A., Bruegmann M.L., Ganter M. Imaging and score-based quantification of ovine pulmonary adenocarcinoma using computed tomography as an additional tool in advanced clinical diagnosis. Small Rumin Res 2011, 96:201-210.
17. Voigt K., Brugmann M., Huber K., Dewar P., Cousens C., Hall M., et al. PCR examination of bronchoalveolar lavage samples is a useful tool in pre-clinical diagnosis of ovine pulmonary adenocarcinoma (Jaagsiekte). Res Vet Sci 2007, 83:419-427.
18. Paglia D.E., Valentine W.N. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 1967, 70:158-169.
19. Holmgren A., Bjornstedt M. Thioredoxin and thioredoxin reductase. Methods Enzymol 1995, 252:199-208.
20. Arner E.S., Zhong L., Holmgren A. Preparation and assay of mammalian thioredoxin and thioredoxin reductase. Methods Enzymol 1999, 300:226-239.
21. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254.
22. Humann-Ziehank E., Ganter M., Hennig-Pauka I., Binder A. Trace element status and liver and blood parameters in sheep without mineral supply compared to local roe deer (Capreolus capreolus) populations. Small Rumin Res 2008, 75:185-191.
23. NRC Nutrient requirements of sheep: selenium. National Research Council - Committee on animal nutrition. 6 ed. 1985, 20-22. National Academical Press, Washington D.C.
24. Suttle N.F. Selenium. The mineral nutrition of livestock 2010, 377-425. Cabi, Oxfordshire/Cambridge. 4th ed. N.F. Suttle (Ed.).
25. Liu J., Johnston M.R. Animal models for studying lung cancer and evaluating novel intervention strategies. Surg Oncol 2002, 11:217-227.
26. Petkovska I., Brown M.S., Goldin J.G., Kim H.J., McNitt-Gray M.F., Abtin F.G., et al. The effect of lung volume on nodule size on CT. Acad Radiol 2007, 14:476-485.
27. Boll D.T., Gilkeson R.C., Fleiter T.R., Blackham K.A., Duerk J.L., Lewin J.S. Volumetric assessment of pulmonary nodules with ECG-Gated MDCT. Am J Roentgenol 2004, 183:1217-1223.
28. Rampinelli C., De Fiori E., Raimondi S., Veronesi G., Bellomi M. In vivo repeatability of automated volume calculations of small pulmonary nodules with CT. Am J Roentgenol 2009, 192:1657-1661.
29. Cousens C., Thonur L., Imlach S., Crawford J., Sales J., Griffiths D.J. Jaagsiekte sheep retrovirus is present at high concentration in lung fluid produced by ovine pulmonary adenocarcinoma-affected sheep and can survive for several weeks at ambient temperatures. Res Vet Sci 2009, 87:154-156.
30. Summers C., Benito A., Ortin A., Garcia de Jalon J.A., Gonzalez L., Norval M., et al. The distribution of immune cells in the lungs of classical and atypical ovine pulmonary adenocarcinoma. Vet Immunol Immunopathol 2012, 146:1-7.
31. Murgia C., Caporale M., Ceesay O., Di Francesco G., Ferri N., Varasano V., et al. Lung adenocarcinoma originates from retrovirus infection of proliferating type 2 pneumocytes during pulmonary post-natal development or tissue repair. PLoS Pathog 2011, 7:e1002014.
32. Summers C., Norval M., de las Heras M., Gonzalez L., Sharp J.M., Woods G.M. An influx of macrophages is the predominant local immune response in ovine pulmonary adenocarcinoma. Vet Immunol Immunopathol 2005, 106:285-294.
33. Eckert H., Lux M., Lachmann B. The role of alveolar macrophages in surfactant turnover. An experimental study with metabolite VIII of bromhexine (Ambroxol). Lung 1983, 161:213-218.
34. Myer M.S., Verwoerd D.W., Garnett H.M. Production of a macrophage chemotactic factor by cultured jaagsiekte tumour cells. Onderstepoort J Vet Res 1987, 54:9-15.
35. Suadicani P., Hein H.O., Gyntelberg F. Serum selenium level and risk of lung cancer mortality: a 16-year follow-up of the Copenhagen Male Study. Eur Respir J 2012, 39:1443-1448.
36. Ratnasinghe D., Tangrea J.A., Forman M.R., Hartman T., Gunter E.W., Qiao Y.L., et al. Serum tocopherols, selenium and lung cancer risk among tin miners in China. Cancer Causes Control 2000, 11:129-135.
37. Kabuto M., Imai H., Yonezawa C., Neriishi K., Akiba S., Kato H., et al. Prediagnostic serum selenium and zinc levels and subsequent risk of lung and stomach cancer in Japan. Cancer Epidemiol Biomarkers Prev 1994, 3:465-469.
38. Romanowska M., Kikawa K.D., Fields J.R., Maciag A., North S.L., Shiao Y.H., et al. Effects of selenium supplementation on expression of glutathione peroxidase isoforms in cultured human lung adenocarcinoma cell lines. Lung Cancer 2007, 55:35-42.
39. Brigelius-Flohe R. Glutathione peroxidases and redox-regulated transcription factors. Biol Chem 2006, 387:1329-1335.
40. Ho Y.S., Magnenat J.L., Bronson R.T., Cao J., Gargano M., Sugawara M., et al. Mice deficient in cellular glutathione peroxidase develop normally and show no increased sensitivity to hyperoxia. J Biol Chem 1997, 272:16644-16651.
41. Baliga M.S., Diwadkar-Navsariwala V., Koh T., Fayad R., Fantuzzi G., Diamond A.M. Selenoprotein deficiency enhances radiation-induced micronuclei formation. Mol Nutr Food Res 2008, 52:1300-1304.
42. Banning A., Kipp A., Schmitmeier S., Lowinger M., Florian S., Krehl S., et al. Glutathione peroxidase 2 inhibits cyclooxygenase-2-mediated migration and invasion of HT-29 adenocarcinoma cells but supports their growth as tumors in nude mice. Cancer Res 2008, 68:9746-9753.
43. Brigelius-Flohe R., Muller M., Lippmann D., Kipp A.P. The yin and yang of nrf2-regulated selenoproteins in carcinogenesis. Int J Cell Biol 2012, 10.1155/2012/486147.
44. Di Ilio C., Del Boccio G., Casaccia R., Aceto A., Di Giacomo F., Federici G. Selenium level and glutathione-dependent enzyme activities in normal and neoplastic human lung tissues. Carcinogenesis 1987, 8:281-284.
45. Howie A.F., Forrester L.M., Glancey M.J., Schlager J.J., Powis G., Beckett G.J., et al. Glutathione S-transferase and glutathione peroxidase expression in normal and tumour human tissues. Carcinogenesis 1990, 11:451-458.
46. Korotkina R.N., Matskevich G.N., Devlikanova A., Vishnevskii A.A., Kunitsyn A.G., Karelin A.A. Activity of glutathione-metabolizing and antioxidant enzymes in malignant and benign tumors of human lungs. Bull Exp Biol Med 2002, 133:606-608.
47. Gresner P., Gromadzinska J., Jablonska E., Kaczmarski J., Wasowicz W. Expression of selenoprotein-coding genes SEPP1, SEP15 and hGPX1 in non-small cell lung cancer. Lung Cancer 2009, 65:34-40.
48. Perquin M., Oster T., Maul A., Froment N., Untereiner M., Bagrel D. The glutathione-related detoxification system is increased in human breast cancer in correlation with clinical and histopathological features. J Cancer Res Clin Oncol 2001, 127:368-374.
49. Hill K.E., McCollum G.W., Boeglin M.E., Burk R.F. Thioredoxin reductase activity is decreased by selenium deficiency. Biochem Biophys Res Commun 1997, 234:293-295.
50. Erkhembayar S., Mollbrink A., Eriksson M., Larsen E.H., Eriksson L.C. Selenium homeostasis and induction of thioredoxin reductase during long term selenite supplementation in the rat. J Trace Elem Med Biol 2011, 25:254-259.
51. Fernandes A.P., Capitanio A., Selenius M., Brodin O., Rundlof A.K., Bjornstedt M. Expression profiles of thioredoxin family proteins in human lung cancer tissue: correlation with proliferation and differentiation. Histopathology 2009, 55:313-320.
52. Soini Y., Kahlos K., Napankangas U., Kaarteenaho-Wiik R., Saily M., Koistinen P., et al. Widespread expression of thioredoxin and thioredoxin reductase in non-small cell lung carcinoma. Clin Cancer Res 2001, 7:1750-1757.
53. Park J.H., Kim Y.S., Lee H.L., Shim J.Y., Lee K.S., Oh Y.J., et al. Expression of peroxiredoxin and thioredoxin in human lung cancer and paired normal lung. Respirology 2006, 11:269-275.