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Original Articles

Granuloma Formation Induced by Low-Dose Chronic Silica Inhalation is Associated with an Anti-Apoptotic Response in Lewis Rats

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Pages 669-683 | Received 10 Aug 2009, Accepted 02 Dec 2009, Published online: 23 Mar 2010

REFERENCES

  • Agarwal , B. , Halmos , B. , Feoktistov , A. S. , Protiva , P. , Ramey , W. G. , Chen , M. , Pothoulakis , C. , Lamont , J. T. and Holt , P. R. 2002 . Mechanism of lovastatin-induced apoptosis in intestinal epithelial cells . Carcinogenesis , 23 : 521 – 528 .
  • Agostini , C. , Perin , A. and Semenzato , G. 1998 . Cell apoptosis and granulomatous lung diseases . Curr. Opin. Pulmon. Med. , 4 : 261 – 266 .
  • Ardley , H. C. and Robinson , P. A. 2004 . The role of ubiquitin-protein ligases in neurodegenerative disease . Neurodegener. Dis. , 1 : 71 – 87 .
  • Ashkenazi , A. and Dixit , V. M. 1998 . Death receptors: Signaling and modulation . Science , 281 : 1305 – 1308 .
  • Barbarin , V. , Xing , Z. , Delos , M. , Lison , D. and Huaux , F. 2005 . Pulmonary overexpression of IL-10 augments lung fibrosis and Th2 responses induced by silica particles . Am. J. Physiol. Lung Cell Mol. Physiol. , 288 : L841 – L848 .
  • Barbaro , M. , Cutroneo , G. , Costa , C. , Sciorio , S. , Trimarchi , F. , Favaloro , A. , Fenga , C. , Barbaro , M. L. , Spatari , G. , Abbate , C. and Bramanti , P. 2002 . Early events of experimental exposure to amorphous and crystalline silica in the rat: Time course of surfactant protein D . Ital. J. Anat. Embryol. , 107 : 243 – 256 .
  • Bauer , A. , Villunger , A. , Labi , V. , Fischer , S. F. , Strasser , A. , Wagner , H. , Schmid , R. M. and Hacker , G. 2006 . The NF-kappaB regulator Bcl-3 and the BH3-only proteins Bim and Puma control the death of activated T cells . Proc. Natl. Acad. Sci. USA , 103 : 10979 – 10984 .
  • Belka , C. and Budach , W. 2002 . Anti-apoptotic Bcl-2 proteins: structure, function and relevance for radiation biology . Int. J. Radiat. Biol. , 78 : 643 – 658 .
  • Boatright , K. M. and Salvesen , G. S. 2003 . Mechanisms of caspase activation . Curr. Opin. Cell Biol. , 15 : 725 – 731 .
  • Borges , V. M. , Falcao , H. , Leite-Junior , J. H. , Alvim , L. , Teixeira , G. P. , Russo , M. , Nobrega , A. F. , Lopes , M. F. , Rocco , P. M. , Davidson , W. F. , Linden , R. , Yagita , H. , Zin , W. A. and DosReis , G. A. 2001 . Fas ligand triggers pulmonary silicosis . J. Exp. Med. , 194 : 155 – 164 .
  • Borges , V. M. , Lopes , M. F. , Falcao , H. , Leite-Junior , J. H. , Rocco , P. R. , Davidson , W. F. , Linden , R. , Zin , W. A. and DosReis , G. A. 2002 . Apoptosis underlies immunopathogenic mechanisms in acute silicosis . Am. J. Respir. Cell Mol. Biol. , 27 : 78 – 84 .
  • Budinger , G. R. , Mutlu , G. M. , Eisenbart , J. , Fuller , A. C. , Bellmeyer , A. A. , Baker , C. M. , Wilson , M. , Ridge , K. , Barrett , T. A. , Lee , V. Y. and Chandel , N. S. 2006 . Proapoptotic Bid is required for pulmonary fibrosis . Proc. Natl. Acad. Sci. USA , 103 : 4604 – 4609 .
  • Burlacu , A. 2003 . Regulation of apoptosis by Bcl-2 family proteins . J. Cell Mol. Med. , 7 : 249 – 257 .
  • Castranova , V. , Porter , D. , Millecchia , L. , Ma , J. Y. , Hubbs , A. F. and Teass , A. 2002 . Effect of inhaled crystalline silica in a rat model: Time course of pulmonary reactions . Mol. Cell Biochem. , 234–235 : 177 – 184 .
  • Catz , S. D. and Johnson , J. L. 2001 . Transcriptional regulation of bcl-2 by nuclear factor kappa B and its significance in prostate cancer . Oncogene , 20 : 7342 – 7351 .
  • Chambers , T. J. 1978 . Multinucleate giant cells . J. Pathol. , 126 : 125 – 148 .
  • Chong , S. , Lee , K. S. , Chung , M. J. , Han , J. , Kwon , O. J. and Kim , T. S. 2006 . Pneumoconiosis: comparison of imaging and pathologic findings . Radiographics , 26 : 59 – 77 .
  • Cox , G. , Crossley , J. and Xing , Z. 1995 . Macrophage engulfment of apoptotic neutrophils contributes to the resolution of acute pulmonary inflammation in vivo . Am. J. Respir. Cell Mol. Biol. , 12 : 232 – 237 .
  • Er , E. , Oliver , L. , Cartron , P. F. , Juin , P. , Manon , S. and Vallette , F. M. 2006 . Mitochondria as the target of the pro-apoptotic protein Bax . Biochim. Biophys. Acta , 1757 : 1301 – 1311 .
  • 1996 . Guide for the Care and Use of Laboratory Animals , Washington, D.C : Institute of Laboratory Animal Resources, Commission on Life Sciences, National Research Council, National Academy Press .
  • Haslett , C. 1992 . Resolution of acute inflammation and the role of apoptosis in the tissue fate of granulocytes . Clin. Sci. (Lond.) , 83 : 639 – 648 .
  • Hnizdo , E. and Sluis-Cremer , G. K. 1993 . Risk of silicosis in a cohort of white South African gold miners . Am. J. Ind. Med , 24 : 447 – 457 .
  • Hnizdo , E. and Vallyathan , V. 2003 . Chronic obstructive pulmonary disease due to occupational exposure to silica dust: A review of epidemiological and pathological evidence . Occup. Environ. Med. , 60 : 237 – 243 .
  • Hubbard , A. K. , Timblin , C. R. , Shukla , A. , Rincon , M. and Mossman , B. T. 2002 . Activation of NF-kappaB-dependent gene expression by silica in lungs of luciferase reporter mice . Am. J. Physiol. Lung Cell Mol. Physiol. , 282 : L968 – L975 .
  • Hughes , J. M. , Weill , H. , Checkoway , H. , Jones , R. N. , Henry , M. M. , Heyer , N. J. , Seixas , N. S. and Demers , P. A. 1998 . Radiographic evidence of silicosis risk in the diatomaceous earth industry . Am. J. Respir. Crit. Care Med. , 158 : 807 – 814 .
  • Kadenbach , B. , Arnold , S. , Lee , I. and Huttemann , M. 2004 . The possible role of cytochrome c oxidase in stress-induced apoptosis and degenerative diseases . Biochim. Biophys. Acta , 1655 : 400 – 408 .
  • Kang , J. L. , Go , Y. H. , Hur , K. C. and Castranova , V. 2000 . Silica-induced nuclear factor-kappaB activation: Involvement of reactive oxygen species and protein tyrosine kinase activation . J. Toxicol. Environ. Health A , 60 : 27 – 46 .
  • Karin , M. and Lin , A. 2002 . NF-kappaB at the crossroads of life and death . Nat. Immunol. , 3 : 221 – 227 .
  • Kreiss , K. and Zhen , B. 1996 . Risk of silicosis in a Colorado mining community . Am. J. Ind. Med. , 30 : 529 – 539 .
  • Kunitake , R. , Kuwano , K. , Miyazaki , H. , Hagimoto , N. , Nomoto , Y. and Hara , N. 1999 . Apoptosis in the course of granulomatous inflammation in pulmonary sarcoidosis . Eur. Respir. J. , 13 : 1329 – 1337 .
  • Kuwano , K. , Kawasaki , M. , Maeyama , T. , Hagimoto , N. , Nakamura , N. , Shirakawa , K. and Hara , N. 2000 . Soluble form of fas and fas ligand in BAL fluid from patients with pulmonary fibrosis and bronchiolitis obliterans organizing pneumonia . Chest , 118 : 451 – 458 .
  • Kuwata , H. , Watanabe , Y. , Miyoshi , H. , Yamamoto , M. , Kaisho , T. , Takeda , K. and Akira , S. 2003 . IL-10-inducible Bcl-3 negatively regulates LPS-induced TNF-alpha production in macrophages . Blood , 102 : 4123 – 4129 .
  • Langley , R. J , Kalra , R. , Mishra , N. C. , Hahn , F. F. , Razani-Boroujerdi , S. , Singh , S. P. , Benson , J. M. , Pena-Philippides , J. C. , Barr , E. B. and Sopori , M. L. 2004 . A biphasic response to silica: I. Immunostimulation is restricted to the early stage of silicosis in Lewis rats . Am. J. Respir. Cell Mol. Biol. , 30 : 823 – 829 .
  • Laza-Stanca , V. , Stanciu , L. A. , Message , S. D. , Edwards , M. R. , Gern , J. E. and Johnston , S. L. 2006 . Rhinovirus replication in human macrophages induces NF-kappaB-dependent tumor necrosis factor alpha production . J. Virol. , 80 : 8248 – 8258 .
  • Li , X. Y. , Lamb , D. and Donaldson , K. 1993 . The production of TNF-alpha and IL-1-like activity by bronchoalveolar leucocytes after intratracheal instillation of crocidolite asbestos . Int. J. Exp. Pathol. , 74 : 403 – 410 .
  • Mancino , D. and Caselli , P. 1966 . Granulomatous reactions induced by silica. I. Relationships between particles size and multinucleated giant cells . Folia Med. (Napoli) , 49 : 85 – 121 .
  • McLaughlin , J. K. , Chow , W. H. and Levy , L. S. 1997 . Amorphous silica: A review of health effects from inhalation exposure with particular reference to cancer . J. Toxicol. Environ. Health , 50 : 553 – 566 .
  • Mitchell , T. C. , Hildeman , D. , Kedl , R. M. , Teague , T. K. , Schaefer , B. C. , White , J. , Zhu , Y. , Kappler , J. and Marrack , P. 2001 . Immunological adjuvants promote activated T cell survival via induction of Bcl-3 . Nat. Immunol. , 2 : 397 – 402 .
  • Mutsaers , S. E. , Harrison , N. K. , McAnulty , R. J. , Liao , J. Y. , Laurent , G. J. and Musk , A. W. 1998 . Fibroblast mitogens in bronchoalveolar lavage (BAL) fluid from asbestos-exposed subjects with and without clinical evidence of asbestosis: No evidence for the role of PDGF, TNF-alpha, IGF-1, or IL-1 beta . J. Pathol. , 185 : 199 – 203 .
  • Nguyen , D. M. , Yeow , W. S. , Ziauddin , M. F. , Baras , A. , Tsai , W. , Reddy , R. M. , Chua , A. , Cole , G. W. Jr. and Schrump , D. S. 2006 . The essential role of the mitochondria-dependent death-signaling cascade in chemotherapy-induced potentiation of Apo2L/TRAIL cytotoxicity in cultured thoracic cancer cells: Amplified caspase 8 is indispensable for combination-mediated massive cell death . Cancer J. , 12 : 257 – 273 .
  • Ordway , D. , Henao-Tamayo , M. , Orme , I. M. and Gonzalez-Juarrero , M. 2005 . Foamy macrophages within lung granulomas of mice infected with Mycobacterium tuberculosis express molecules characteristic of dendritic cells and antiapoptotic markers of the TNF receptor-associated factor family . J. Immunol. , 175 : 3873 – 3881 .
  • Otsuki , T. , Sakaguchi , H. , Tomokuni , A. , Aikoh , T. , Matsuki , T. , Isozaki , Y. , Hyodoh , F. , Kawakami , Y. , Kusaka , M. , Kita , S. and Ueki , A. 2000 . Detection of alternatively spliced variant messages of Fas gene and mutational screening of Fas and Fas ligand coding regions in peripheral blood mononuclear cells derived from silicosis patients . Immunol. Lett. , 72 : 137 – 143 .
  • Poljakovic , M. , Porter , D. W. , Millecchia , L. , Kepka-Lenhart , D. , Beighley , C. , Wolfarth , M. G. , Castranova , V. and Morris , S. M. Jr. 2007 . Cell- and isoform-specific increases in arginase expression in acute silica-induced pulmonary inflammation . J. Toxicol. Environ. Health A , 70 : 118 – 127 .
  • Porter , D. W. , Barger , M. , Robinson , V. A. , Leonard , S. S. , Landsittel , D. and Castranova , V. 2002 . Comparison of low doses of aged and freshly fractured silica on pulmonary inflammation and damage in the rat . Toxicology , 175 : 63 – 71 .
  • Porter , D. W. , Hubbs , A. F. , Mercer , R. , Robinson , V. A. , Ramsey , D. , McLaurin , J. , Khan , A. , Battelli , L. , Brumbaugh , K. , Teass , A. and Castranova , V. 2004 . Progression of lung inflammation and damage in rats after cessation of silica inhalation . Toxicol. Sci. , 79 : 370 – 380 .
  • Porter , D. W. , Millecchia , L. L. , Willard , P. , Robinson , V. A. , Ramsey , D. , McLaurin , J. , Khan , A. , Brumbaugh , K. , Beighley , C. M. , Teass , A. and Castranova , V. 2006 . Nitric oxide and reactive oxygen species production causes progressive damage in rats after cessation of silica inhalation . Toxicol. Sci. , 90 : 188 – 197 .
  • Razani-Boroujerdi , S. and Sopori , M. L. 2007 . Early manifestations of NNK-induced lung cancer: Role of lung immunity in tumor susceptibility . Am. J. Respir. Cell Mol. Biol. , 36 : 13 – 19 .
  • Rossi , A. G. , Sawatzky , D. A. , Walker , A. , Ward , C. , Sheldrake , T. A. , Riley , N. A. , Caldicott , A. , Martinez-Losa , M. , Walker , T. R. , Duffin , R. , Gray , M. , Crescenzi , E. , Martin , M. C. , Brady , H. J. , Savill , J. S. , Dransfield , I. and Haslett , C. 2006 . Cyclin-dependent kinase inhibitors enhance the resolution of inflammation by promoting inflammatory cell apoptosis . Nat. Med , 12 : 1056 – 1064 .
  • Santarelli , L. , Recchioni , R. , Moroni , F. , Marcheselli , F. and Governa , M. 2004 . Crystalline silica induces apoptosis in human endothelial cells in vitro . Cell Biol. Toxicol , 20 : 97 – 108 .
  • Shi , X. , Castranova , V. , Halliwell , B. and Vallyathan , V. 1998 . Reactive oxygen species and silica-induced carcinogenesis . J. Toxicol. Environ. Health B , 1 : 181 – 197 .
  • Shikuwa , C. , Kadota , J. , Mukae , H. , Iwashita , T. , Kaida , H. , Ishii , H. , Ishimatsu , Y. and Kohno , S. 2002 . High concentrations of soluble Fas ligand in bronchoalveolar lavage fluid of patients with pulmonary sarcoidosis . Respiration , 69 : 242 – 246 .
  • Sinicrope , F. A. , Half , E. , Morris , J. S. , Lynch , P. M. , Morrow , J. D. , Levin , B. , Hawk , E. T. , Cohen , D. S. , Ayers , G. D. and Stephens , L. C. 2004a . Cell proliferation and apoptotic indices predict adenoma regression in a placebo-controlled trial of celecoxib in familial adenomatous polyposis patients . Cancer Epidemiol. Biomarkers Prev , 13 : 920 – 927 .
  • Sinicrope , F. A. , Penington , R. C. and Tang , X. M. 2004b . Tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis is inhibited by Bcl-2 but restored by the small molecule Bcl-2 inhibitor, HA 14-1, in human colon cancer cells . Clin. Cancer Res. , 10 : 8284 – 8292 .
  • Takemura , T. , Rom , W. N. , Ferrans , V. J. and Crystal , R. G. 1989 . Morphologic characterization of alveolar macrophages from subjects with occupational exposure to inorganic particles . Am. Rev. Respir. Dis. , 140 : 1674 – 1685 .
  • Tomokuni , A. , Aikoh , T. , Matsuki , T. , Isozaki , Y. , Otsuki , T. , Kita , S. , Ueki , H. , Kusaka , M. , Kishimoto , T. and Ueki , A. 1997 . Elevated soluble Fas/APO-1 (CD95) levels in silicosis patients without clinical symptoms of autoimmune diseases or malignant tumours . Clin. Exp. Immunol. , 110 : 303 – 309 .
  • Vallyathan , V. , Green , F. , Ducatman , B. and Schulte , P. 1998 . Roles of epidemiology, pathology, molecular biology, and biomarkers in the investigation of occupational lung cancer . J. Toxicol. Environ. Health B , 1 : 91 – 116 .
  • Vanden Berghe , W. , Vermeulen , L. , Delerive , P. , De Bosscher , K. , Staels , B. and Haegeman , G. 2003 . A paradigm for gene regulation: Inflammation, NF-kappaB and PPAR . Adv. Exp. Med. Biol. , 544 : 181 – 196 .
  • Viatour , P. , Bentires-Alj , M. , Chariot , A. , Deregowski , V. , de Leval , L. , Merville , M. P. and Bours , V. 2003 . NF- kappa B2/p100 induces Bcl-2 expression . Leukemia , 17 : 1349 – 1356 .
  • Williams , G. T. and Williams , W, J. 1983 . Granulomatous inflammation—A review . J. Clin. Pathol. , 36 : 723 – 733 .
  • Zhang , D. D. , Hartsky , M. A. and Warheit , D. B. 2002 . Time course of quartz and TiO(2) particle-induced pulmonary inflammation and neutrophil apoptotic responses in rats . Exp. Lung Res. , 28 : 641 – 670 .
  • Zhang , K. and Phan , S. H. 1996 . Cytokines and pulmonary fibrosis . Biol. Signals , 5 : 232 – 239 .

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