Sulfur mustard induces apoptosis in lung epithelial cells via a caspase amplification loop

Toxicology

Volumn 271, Issue 3, 2010, Pages 94-99

  Ray, Radharaman ^a   Simbulan Rosenthal, Cynthia M ^b   Keyser, Brian M ^a   Benton, Betty ^a   Anderson, Dana ^a   Holmes, Wesley ^a   Trabosh, Valerie A ^b   Daher, Ahmad ^b   Rosenthal, Dean S ^b  

^a US ARMY MEDICAL RESEARCH INSTITUTE OF CHEMICAL DEFENSE   (United States)

^b GEORGETOWN UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Amplification loop; Apoptosis; Bronchial tracheal epithelial cells; Caspases; Rat lung; Small airway epithelial cells; Sulfur mustard

Indexed keywords

CASPASE; CASPASE 3; CASPASE 8; CASPASE 9; CASPASE INHIBITOR; DEATH RECEPTOR; MUSTARD GAS; CHEMICAL WARFARE AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; BRONCHUS MUCOSA; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; EPITHELIUM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INHALATION; LUNG ALVEOLUS EPITHELIUM; MALE; NONHUMAN; NORMAL HUMAN; POSITIVE FEEDBACK; PRIORITY JOURNAL; RAT; RESPIRATORY EPITHELIUM; TRACHEA MUCOSA; ANIMAL; CELL CULTURE; DRUG ANTAGONISM; DRUG EFFECT; LUNG; METABOLISM;

RATTUS;

ANIMALS; APOPTOSIS; CASPASE 3; CASPASE 8; CASPASE 9; CASPASES; CELLS, CULTURED; CHEMICAL WARFARE AGENTS; EPITHELIAL CELLS; HUMANS; LUNG; MALE; MUSTARD GAS; RATS;

EID: 77952501283     PISSN: 0300483X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tox.2010.03.008     Document Type: Article

References (40)

1. Anderson D.R., Yourick J.J., Moeller R.B., Petrali J.P., Young G.D., Byers S.L. Pathologic changes in rat lungs following acute sulfur mustard inhalation. Inhal. Toxicol. 1996, 8:285-297.
2. Aragane Y., Kulms D., Metze D., Wilkes G., Poppelmann B., Luger T.A., Schwarz T. Ultraviolet light induces apoptosis via direct activation of CD95 (Fas/APO-1) independently of its ligand CD95L. J. Cell Biol. 1998, 140:171-182.
3. Balali-Mood M., Hefazi M. Comparison of early and late toxic effects of sulfur mustard in Iranian veterans. Basic Clin. Pharmacol. Toxicol. 2006, 99:273-282.
4. Bijani K., Moghadamnia A. Long-term effects of chemical weapons on respiratory tract in Iraq-Iran war victims living in Babol (North of Iran). Ecotoxicol. Environ. Saf. 2002, 53:422-424.
5. Bratton S.B., Cohen G. Death receptors leave a caspase footprint that smacs of XIAP. Cell Death Differ. 2003, 10:4-6.
6. Cowling V., Downward J. Caspase-6 is the direct activator of caspase-8 in the cytochrome c-induced apoptosis pathway: absolute requirement for removal of caspase-6 prodomain. Cell Death Differ. 2002, 9:1046-1056.
7. Dabrowska M.I., Becks L.L., Lelli J.L., Levee M.G., Hinshaw D.B. Sulfur mustard induces apoptosis and necrosis in endothelial cells. Toxicol. Appl. Pharmacol. 1996, 141:568-583.
8. Dacre J.C., Goldman M. Toxicology and pharmacology of the chemical warfare agent sulfur mustard. Pharmacol. Rev. 1996, 48:289-326.
9. Emad A., Emad Y. Increased in CD8 T lymphocytes in the BAL fluid of patients with sulfur mustard gas-induced pulmonary fibrosis. Respir. Med. 2007, 101:786-792.
10. Fujita E., Egashira J., Urase K., Kiuda K., Momoi T. Caspase-9 processing by caspase-3 via a feedback amplification loop in vivo. Cell Death Differ. 2001, 8:334-344.
11. Fulda S., Meyer E., Friesen C., Susin S.A., Kroemer G., Debatin K.M. Cell type specific involvement of death receptor and mitochondrial pathways in drug-induced apoptosis. Oncogene 2001, 20:1063-1075.
12. Ghanei M., Harandi A. Long term consequences from exposure to sulfur mustard: a review. Inhal. Toxicol. 2007, 19:451-456.
13. Gross C.L., Innace J.K., Smith W.J., Krebs R.C., Meier H.L. Alteration of lymphocyte glutathione levels affects sulfur mustard cytotoxicity. Proc. Meeting NATO Res. Study Group, Panel VIII/RSG-3 1988.
14. Hefazi M., Attaran D., Mahmoudi M., Balali-Mood M. Late respiratory complications of mustard gas poisoning in Iranian veterans. Inhal. Toxicol. 2005, 17:587-592.
15. Kehe K., Balszuweit F., Steinritz D., Thiermann H. Molecular toxicology of sulfur mustard-induced cutaneous inflammation and blistering. Toxicology 2009, 263:12-19.
16. Kumar S. Regulation of caspase activation in apoptosis: implication in pathogenesis and treatment of disease. Clin. Exp. Pharmacol. Physiol. 1999, 26:295-303.
17. Meier H.L., Gross C.L., Papirmeister B., Daszkiewicz J.E. The use of human leukocytes as a model for studying the biochemical effects of chemical warfare (CW) agents. Proc. Fourth Annual Chemical Defense Biosci. Rev. 1984.
18. Mol M.A., va den Berg R.M., Benschop H.P. Involvement of caspases and transmembrane metalloproteases in sulphur mustard-induced microvesication in adult human skin in organ culture: directions for therapy. Toxicology 2009, 258:39-46.
19. Papirmeister B., Feister A.J., Robinson S.I., Ford R.D. Medical Defense Against Mustard Gas: Toxic Mechanisms and Pharmacological Implications 1991, CRC Press, Boca Raton.
20. Petrali J.P., Oglesby S.B., Mills K.R. Ultrastructural correlates of sulfur mustard toxicity. J. Toxicol. Cutan. Ocul. Toxicol. 1990, 9:193-214.
21. Porter A.G., Janicke R.U. Emerging role of caspase-3 in apoptosis. Cell Death Differ. 1999, 6:99-104.
22. Rappeneau S., Baeza-Squiban A., Marano F., Calvet J.-H. Efficient protection of human bronchial epithelial cells against sulfur and nitrogen mustard cytotoxicity using drug combinations. Toxicol. Sci. 2000, 58:153-160.
23. Ray R., Legere R.H., Majerus B.J., Petrali J.P. Sulfur mustard-induced increase in intracellular free calcium level and arachidonic acid release from cell membrane. Toxicol. Appl. Pharmacol. 1995, 131:44-52.
24. Ray R., Keyser B., Benton B., Daher A., Simbulan-Rosenthal C.M., Rosenthal D.S. Sulfur mustard induces apoptosis in cultured normal human airway epithelial cells: evidence of a dominant caspase-8-mediated pathway and differential cellular responses. Drug Chem. Toxicol. 2008, 31:137-148.
25. 2+-calmodulin and caspase-dependent pathway. J. Invest. Dermatol. 1998, 111:64-71.
26. Rosenthal D.S., Simbulan-Rosenthal C.M., Iyer S., Smith W.J., Ray R., Smulson M.E. Calmodulin, poly(ADP-ribose)polymerase and p53 are targets for modulating the effects of sulfur mustard. J. Appl. Toxicol. 2000, 20:S43-S49.
27. Rosenthal D.S., Velena A., Chou F.P., Schlegel R., Ray R., Benton B., Anderson D., Smith W.J., Simbulan-Rosenthal C.M. Expression of dominant-negative Fas-associated death domain blocks human keratinocyte apoptosis and vesication induced by sulfur mustard. J. Biol. Chem. 2003, 278:8531-8540. Epub 2002 Dec 8512.
28. Saladi R., Smith E., Persaud A. Mustard: a potential agent of chemical warfare and terrorism. Clin. Exp. Dermatol. 2006, 31:1-5.
29. Scaffidi C., Fulda S., Srinivasan A., Friesen C., Li F., Tomaselli K.J., Debatin K.M., Krammer P.H., Peter M.E. Two CD95 (APO-1/Fas) signaling pathways. EMBO J. 1998, 17:1675-1687.
30. Simbulan-Rosenthal C.M., Velena A., Veldman T., Schlegel R., Rosenthal D.S. HPV-16 E6/7 immortalization sensitizes human keratinocytes to ultraviolet B by altering the pathway from caspase-8 to caspase-9-dependent apoptosis. J. Biol. Chem. 2002, 277:24709-24716.
31. Simbulan-Rosenthal C., Ray R., Benton B., Soeda E., Daher A., Anderson D., Smith W., Rosenthal D. Calmodulin mediates sulfur mustard toxicity in human keratinocytes. Toxicology 2006, 227:21-35.
32. Smith W.J., Gross C.L., Chan P., Meier H.L. The use of human epidermal keratinocytes in culture as a model for studying the biochemical mechanisms of sulfur mustard toxicity. Cell Biol. Toxicol. 1990, 6:285-291.
33. Smith W.J., Sanders K.M., Gales Y.A., Gross C.L. Flow cytometric analysis of toxicity by vesicating agents in human cells in vitro. Cutan. Ocul. Toxicol. 1991, 10:33-42.
34. Sourdeval M., Lemaire C., Deniaud A., Taysse L., Daulon S., Breton P., Brenner C., Boisvieux-Ulrich E., Marano F. Inhibition of caspase-dependent mitochondrial permeability transition protects airway epithelial cells against mustard-induced apoptosis. Apoptosis 2006, 11:1545-1559.
35. Srinivasula S.M., Hegde R., Saleh A., Datta P., Shiozaki E., Chai J., Lee R.A., Robbins P.D., Fernandes-Alnemri T., Shi Y., Alnemri E.S. A conserved XIAP-interaction motif in caspase-9 and Smac/DIABLO regulates caspase activity and apoptosis. Nature 2001, 410:112-116.
36. Sun X.M., Bratton S.B., Butterworth W., MacFarlane M., Cohen G.M. Bcl-2 and Bcl-xL inhibit CD95-mediated apoptosis by preventing mitochondrial release of Smac/DIABLO and subsequent inactivation of X-linked inhibitor-of-apoptosis protein. J. Biol. Chem. 2002, 277:11345-11351.
37. Trincheri N.F., Nicotra G., Follo G., Castino R., Isidoro C. Resveratrol induces cell death in colorectal cancer cells by a novel pathway involving lysosomal capthepsin D. Carcinogenesis 2007, 28:922-931.
38. Urbannetti J. Battlefield Chemical Inhalation Injury 1988, Dekker, New York.
39. Wong W.W., Puthalakath H. Bcl-2 family proteins: the sentinels of the mitochondrial apoptosis pathway. IUBMB Life 2008, 60:390-397.
40. Zou H., Yang R., Hao J., Wang J., Sun C., Fesik S.W., Wu J.C., Tomaselli K.J., Armstrong R.C. Regulation of the Apaf-1/caspase-9 apoptosome by caspase-3 and XIAP. J. Biol. Chem. 2003, 278:8091-8098.