Apoptosis of human primary B lymphocytes is inhibited by N-acetyl-L-cysteine

Journal of Leukocyte Biology

Volumn 76, Issue 1, 2004, Pages 152-161

  Rosati, Emanuela ^a   Sabatini, Rita ^a   Ayroldi, Emira ^a   Tabilio, Antonio ^a   Bartoli, Andrea ^a   Bruscoli, Stefano ^a   Simoncelli, Costantino ^a   Rossi, Ruggero ^a   Marconi, Pierfrancesco ^a  

^a UNIVERSITY OF PERUGIA   (Italy)

Author keywords

Caspases; Survival; Thiols

Indexed keywords

ACETYLCYSTEINE; CASPASE 3; CASPASE 7; CASPASE 8; CASPASE 9; CYCLOHEXIMIDE; CYTOCHROME C; DNA FRAGMENT; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BCL 2; PROTEIN BCL XL; THIOL DERIVATIVE;

APOPTOSIS; ARTICLE; B LYMPHOCYTE; CELL CULTURE; CELL SURVIVAL; CONTROLLED STUDY; ENZYME INHIBITION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; TONSIL;

ACETYLCYSTEINE; ANTIVIRAL AGENTS; APOPTOSIS; B-LYMPHOCYTES; BLOTTING, WESTERN; CASPASE 3; CASPASE 7; CASPASES; CELLS, CULTURED; CYTOCHROMES C; HUMANS; TIME FACTORS; TONSIL;

EID: 3042740439     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0403148     Document Type: Article

References (52)

1. DeFranco, A. L. (1997) The complexity of signaling pathways activated by the BCR. Curr. Opin. Immunol. 9, 296-308.
2. Pogue, S. L., Kurosaki, T., Bolen, J., Herbst, R. (2000) B cell antigen receptor-induced activation of Akt promotes B cell survival and is dependent on Syk kinase. J. Immunol. 165, 1300-1306.
3. Ruuth, K., Carlsson, L., Hallberg, B., Lundgren, E. (2001) Interferon-α promotes survival of human primary B-lymphocytes via phosphatidylinositol 3-kinase. Biochem. Biophys. Res. Commun. 284, 583-586.
4. Wagner, E. F., Hanna, N., Fast, L. D., Kouttab, N., Shank, P. R., Vasquez, A., Sharma, S. (2000) Novel diversity in IL-4-mediated responses in resting human naive B cells versus germinal center/memory B cells. J. Immunol. 165, 5573-5579.
5. Lomo, J., Blomhoff, H. K., Jacobsen, S. E., Krajewski, S., Reed, J. C., Smeland, E. B. (1997) Interleukin-13 in combination with CD40 ligand potently inhibits apoptosis in human B lymphocytes: upregulation of Bcl-xL and Mcl-1. Blood 89, 4415-4424.
6. Tsubata, T., Wu, J., Honjo, T. (1993) B-cell apoptosis induced by antigen receptor crosslinking is blocked by a T-cell signal through CD40. Nature 364, 645-648.
7. Hayashida, K., Shimaoka, Y., Ochi, T., Lipsky, P. E. (2000) Rheumatoid arthritis synovial stromal cells inhibit apoptosis and up-regulate Bcl-xL expression by B cells in a CD49/CD29-CD106-dependent mechanism. J. Immunol. 164, 1110-1116.
8. Koopman, G., Keehnen, R. M., Lindhout, E., Newman, W., Shimizu, Y., van Seventer, G. A., de Groot, C., Pals, S. T. (1994) Adhesion through the LFA-1 (CD11a/CD18)-ICAM-1 (CD54) and the VLA-4 (CD 49d)-VCAM-1 (CD 106) pathways prevents apoptosis of germinal center B cell. J. Immunol. 152, 3760-3767.
9. Guedez, L., Stetler-Stevenson, W. G., Wolff, L., Wang, J., Fukushima, P., Mansoor, A., Stetler-Stevenson, M. (1998) In vitro suppression of programmed cell death of B cells by tissue inhibitor of metalloproteinases-1. J. Clin. Invest. 102, 2002-2010.
10. Yan, C. Y. I., Green, L. A. (1998) Prevention of PC12 by N-acetylcysteine requires activation of the RAS pathway. J. Neurosci. 18, 4042-4049.
11. Li, W. Q., Dehnade, F., Zafarullah, M. (2000) Thiol antioxidant, N-acetylcysteine, activates extracellular signal-regulated kinase signaling pathway in articular chondrocytes. Biochem. Biophys. Res. Commun. 275, 789-794.
12. Ki-Yong, K., TaiYoun, R., Inpyo, C., Soung-Soo, K. (2001) N-acetylcysteine induces cell cycle arrest in hepatic stellate cells through its reducing activity. J. Biol. Chem. 276, 40591-40598.
13. Herrlich, P., Böhmer, F. D. (2000) Redox regulation of signal transduction in mammalian cells. Biochem. Pharmacol. 59, 35-41.
14. Arrigo, A. P. (1999) Gene expression and the thiol redox state. Free Radic. Biol. Med. 27, 936-944.
15. Janssen-Heininger, Y. M. V., Poynter, M. E., Baeuerle, P. A. (2000) Recent advances towards understanding redox mechanisms in the activation of nuclear factor κB. Free Radic. Biol. Med. 28, 1317-1327.
16. Kamata, H., Hirata, H. (1999) Redox regulation of cellular signalling. Cell. Signal. 11, 1-14.
17. Hampton, M. B., Fadeel, B., Orrenius, S. (1998) Redox regulation of the caspases during apoptosis. Ann. N. Y. Acad. Sci. 854, 328-335.
18. Ueda, S., Nakamura, H., Masutani, H., Sasada, T., Yonhara, S., Takabayashi, A., Yamaoka, Y., Yodoi, J. (1998) Redox regulation of caspase-3(-like) protease activity: regulatory roles of thioredoxin and cytochrome c. J. Immunol. 161, 6689-6695.
19. Baker, A., Santos, B. D., Powis, G. (2000) Redox control of caspase-3 activity by thioredoxin and other reduced proteins. Biochem. Biophys. Res. Commun. 268, 78-81.
20. Moran, L. K., Gutteridge, J. M., Quinlan, G. J. (2001) Thiols in cellular redox signalling and control. Curr. Med. Chem. 8, 763-772.
21. Yan, C. Y., Ferrari, G., Greene, L. A. (1995) N-acetylcysteine-promoted survival of PC12 cells is glutathione-independent but transcription-dependent. J. Biol. Chem. 270, 26827-26832.
22. Abate, C., Patel, L., Rauscher III, F. J., Curran, T. (1990) Redox regulation of fos and jun DNA-binding activity in vitro. Science 249, 1157-1161.
23. Anderson, M. T., Staal, F. J., Gitler, C., Herzenberg, L. A., Herzenberg, L. A. (1994) Separation of oxidant-initiated and redox-regulated steps in the NF-κB signal transduction pathway. Proc. Natl. Acad. Sci. USA 91, 11527-11531.
24. Furuke, K., Shiraishi, M., Mostowski, H. S., Bloom, E. T. (1999) Fas ligand induction in human NK cells is regulated by redox through a calcineurin-nuclear factor of activated T-cell dependent pathway. J. Immunol. 162, 1988-1993.
25. Tamatani, M., Che, Y. H., Matsuzaki, H., Ogawa, S., Okado, H., Miyake, S., Mizuno, T., Tohyama, M. (1999) Tumor necrosis factor induces Bcl-2 and Bcl-x expression through NF-κB activation in primary hippocampal neurons. J. Biol. Chem. 274, 8531-8538.
26. Gomez, J., Martinez-A, C., Gonzalez, A., Garcia, A., Rebollo, A. (1998) The Bcl-2 gene is differentially regulated by IL-2 and IL-4: role of the transcription factor NF-AT. Oncogene 17, 1235-1243.
27. L. Mol. Cell. Biol. 20, 2687-2695.
28. Wang, C. Y., Mayo, M. W., Korneluk, R. G., Goeddel, D. V., Baldwin Jr., A. S. (1998) NF-κB antiapoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation. Science 281, 1680-1683.
29. Lin, H., Chen, C., Li, X., Chen, B. D. (2002) Activation of the MEK/MAPK pathway is involved in bryostatin 1-induced monocytic differentiation and up-regulation of X-linked inhibitor of apoptosis protein. Exp. Cell Res. 272, 192-198.
30. Nicoletti, I., Migliorati, G., Pagliacci, M. C., Grignani, F., Riccardi, C. (1991) A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J. Immunol. Methods 139, 271-279.
31. Bergsten, P., Yu, R., Kehrl, J., Levine, M. (1995) Ascorbic acid transport and distribution in human B lymphocytes. Arch. Biochem. Biophys. 317, 208-214.
32. Day, B. J., Fridovich, I., Crapo, J. D. (1997) Manganic porphyrins possess catalase activity and protect endothelial cells against hydrogen peroxide-mediated injury. Arch. Biochem. Biophys. 347, 256-262.
33. Enari, M., Sakahira, H., Yokoyama, H., Okawa, K., Iwamatsu, A., Nagata, S. (1998) A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD. Nature 391, 43-50.
34. Liu, X., Zou, H., Slaughter, C., Wang, X. (1997) DFF, a heterodimeric protein that functions downstream of caspase-3 to trigger DNA fragmentation during apoptosis. Cell 89, 175-184.
35. Herceg, Z., Wang, Z-Q. (2001) Functions of poly (ADP-ribose) polymerase (PARP) in DNA repair, genomic integrity and cell death. Mutat. Res. 477, 97-110.
36. Li, H., Zhu, H., Xu, C. J., Yuan, J. (1998) Cleavage of BID by caspase-8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94, 491-501.
37. Gross, A., Yin, X. M., Wang, K., Wei, M. C., Jackel, J., Milliman, C., Erdjument-Bromage, H., Tempst, P., Korsmeyer, S. J. (1999) Caspase cleaved BID targets mitochondria and is required for cytochrome c release, while BCL-XL prevents this release but not tumor necrosis factor-R1/Fas death. J. Biol. Chem. 274, 1156-1163.
38. Kluck, R. M., Bossy, W. E., Green, D. R., Newmeyer, D. D. (1997) The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275, 1132-1136.
39. Yang, J., Liu, X., Bhalla, K., Kim, C. N., Ibrado, A. M., Cai, J., Peng, T. I., Jones, D. P., Wang, X. (1997) Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275, 1129-1132.
40. XL inhibits Ara-C-induced mitochondrial loss of cytochrome c and other perturbations that activate the molecular cascade of apoptosis. Cancer Res. 57, 3115-3120.
41. Sandstrom, P. A., Manne, M. D., Buttke, T. M. (1994) Inhibition of activation-induced death in T cell hybridomas by thiol antioxidants: oxidative stress as a mediator of apoptosis. J. Leukoc. Biol. 55, 221-226.
42. Jones, D. P., Maellaro, E., Jiang, S., Slater, A. F., Orrenius, S. (1995) Effect of N-acetyl-L-cysteine on T-cell apoptosis are not mediated by increased cellular glutathione. Immunol. Lett. 45, 205-209.
43. Buttke, T. M., Sandstrom, P. A. (1994) Oxidative stress as a mediator of apoptosis. Immunol. Today 15, 7-10.
44. Wilson, K. P., Black, J. A., Thomson, J. A., Kim, E. E., Griffith, J. P., Navia, M. A., Murcko, M. A., Chambers, S. P., Aldape, R. A., Raybuck, S. A., Livingston, D. J. (1994) Structure and mechanism of interleukin-1 β converting enzyme. Nature 370, 270-275.
45. Nobel, C. S. I., Burgess, D. H., Zhivotovski, B., Burkitt, M. J., Orrenius, S., Slater, A. F. G. (1997) Mechanisms of dithiocarbamate inhibition of apoptosis: thiol oxidation by dithiocarbamate disulfides directly inhibits processing of the caspase-3 proenzyme. Chem. Res. Toxicol. 10, 636-643.
46. Liu, W., Kato, M., Akhand, A. A., Hayakawa, A., Suzuki, H., Miyata, T., Kurokawa, K., Hotta, Y., Ishikawa, N., Nakashima, I. (2000) 4-Hydrixynonenal induces a cellular redox status-related activation of the caspase cascade for apoptotic cell death. J. Cell Sci. 113, 635-641.
47. Sakahira, H., Iwamatsu, A., Nagata, S. (2000) Specific chaperone-like activity of inhibitor of caspase-activated DNase for caspase-activated DNase. J. Biol. Chem. 275, 8091-8096.
48. Tewari, M., Quan, L. T., O'Rourke, K., Desnoyers, S., Zeng, Z., Beidler, D. R., Poirier, G. G., Salvesen, G. S., Dixit, V. M. (1995) Yama/CPP32 β, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly (ADP-ribose) polymerase. Cell 81, 801-809.
49. Janicke, R. U., Ng, P., Sprengart, M. L., Porter, A. G. (1998) Caspase-3 is required for α-fodrin cleavage but dispensable for cleavage of other death substrates in apoptosis. J. Biol. Chem. 273, 15540-15545.
50. Waoo, M., Hakem, R., Soengas, M. S., Duncan, G. S., Shahinian, A., Kagi, D., Hakem, A., McCurrach, M., Khoo, W., Kaufman, S. A., Senaldi, G., Howard, T., Lowe, S. W., Mak, T. W. (1998) Essential contribution of caspase 3/CPP32 to apoptosis and its associated nuclear changes. Genes Dev. 12, 806-819.
51. Slee, E. A., Adrain, C., Martin, S. J. (2001) Executioner caspase-3, -6, and -7 perform distinct, non-redundant roles during the demolition phase of apoptosis. J. Biol. Chem. 276, 7320-7326.
52. Anto, R. J., Mukhopadhyaj, A., Denning, K., Aggarwal, B. B. (2002) Curcumin (diferuloylmethane) induces apoptosis through activation of caspase-8, BID cleavage and cytochrome c release: its suppression by ectopic expression of Bcl-2 and Bcl-XL. Carcinogenesis 23, 143-150.