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Scientifica
Volume 2014 (2014), Article ID 215426, 7 pages
http://dx.doi.org/10.1155/2014/215426
Review Article

Bcl2 Family Functions as Signaling Target in Nicotine-/NNK-Induced Survival of Human Lung Cancer Cells

Division of Cancer Biology, Department of Radiation Oncology, Emory University School of Medicine and Winship Cancer Institute of Emory University, Atlanta, GA 30322, USA

Received 3 March 2014; Accepted 7 May 2014; Published 20 May 2014

Academic Editor: Patrick Auberger

Copyright © 2014 Xingming Deng. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. Jemal, R. Siegel, E. Ward, T. Murray, J. Xu, and M. J. Thun, “Cancer statistics, 2007,” CA: A Cancer Journal for Clinicians, vol. 57, no. 1, pp. 43–66, 2007. View at Publisher · View at Google Scholar · View at Scopus
  2. H. M. Schuller, P. K. Tithof, M. Williams, and H. Plummer 3rd, “The tobacco-specific carcinogen 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone is a beta-adrenergic agonist and stimulates DNA synthesis in lung adenocarcinoma via beta-adrenergic receptor-mediated release of arachidonic acid,” Cancer Research, vol. 59, no. 18, pp. 4510–4515, 1999. View at Google Scholar · View at Scopus
  3. S. S. Hecht, “Lung carcinogenesis by tobacco smoke,” International Journal of Cancer, vol. 131, no. 12, pp. 2724–2732, 2012. View at Publisher · View at Google Scholar
  4. H. M. Schuller, “Mechanisms of smoking-related lung and pancreatic adenocarcinoma development,” Nature Reviews Cancer, vol. 2, no. 6, pp. 455–463, 2002. View at Google Scholar · View at Scopus
  5. H. Mai, W. S. May, F. Gao, Z. Jin, and X. Deng, “A functional role for nicotine in Bcl2 phosphorylation and suppression of apoptosis,” Journal of Biological Chemistry, vol. 278, no. 3, pp. 1886–1891, 2003. View at Publisher · View at Google Scholar · View at Scopus
  6. K. A. West, J. Brognard, A. S. Clark et al., “Rapid Akt activation by nicotine and a tobacco carcinogen modulates the phenotype of normal human airway epithelial cells,” Journal of Clinical Investigation, vol. 111, no. 1, pp. 81–90, 2003. View at Publisher · View at Google Scholar · View at Scopus
  7. B. Jull, H. Plummer, and H. Schuller, “Nicotinic receptor-mediated activation by the tobacco-specific nitrosamine NNK of a Raf-1/MAP kinase pathway, resulting in phosphorylation of c-myc in human small cell lung carcinoma cells and pulmonary neuroendocrine cells,” Journal of Cancer Research and Clinical Oncology, vol. 127, no. 12, pp. 707–717, 2001. View at Google Scholar · View at Scopus
  8. R. Jorquera, A. Castonguay, and H. M. Schuller, “DNA single-strand breaks and toxicity induced by 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone or N-nitrosodimethylamine in hamster and rat liver,” Carcinogenesis, vol. 15, no. 2, pp. 389–394, 1994. View at Google Scholar · View at Scopus
  9. A. Gross, J. M. McDonnell, and S. J. Korsmeyer, “BCL-2 family members and the mitochondria in apoptosis,” Genes and Development, vol. 13, no. 15, pp. 1899–1911, 1999. View at Google Scholar · View at Scopus
  10. J. M. Adams and S. Cory, “The Bcl-2 protein family: arbiters of cell survival,” Science, vol. 281, no. 5381, pp. 1322–1326, 1998. View at Google Scholar · View at Scopus
  11. M. Suzuki, R. J. Youle, and N. Tjandra, “Structure of bax: coregulation of dimer formation and intracellular localization,” Cell, vol. 103, no. 4, pp. 645–654, 2000. View at Google Scholar · View at Scopus
  12. S. N. Farrow and R. Brown, “New members of the Bcl-2 family and their protein partners,” Current Opinion in Genetics & Development, vol. 6, no. 1, pp. 45–49, 1996. View at Publisher · View at Google Scholar
  13. Z. N. Oltvai, C. L. Milliman, and S. J. Korsmeyer, “Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programed cell death,” Cell, vol. 74, no. 4, pp. 609–619, 1993. View at Publisher · View at Google Scholar · View at Scopus
  14. G. Kroemer, “The proto-oncogene Bcl-2 and its role in regulating apoptosis,” Nature Medicine, vol. 3, no. 6, pp. 614–620, 1997. View at Publisher · View at Google Scholar
  15. H. Li, H. Zhu, C. Xu, and J. Yuan, “Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis,” Cell, vol. 94, no. 4, pp. 491–501, 1998. View at Google Scholar · View at Scopus
  16. W. Zong, T. Lindsten, A. J. Ross, G. R. MacGregor, and C. B. Thompson, “BH3-only proteins that bind pro-survival Bcl-2 family members fail to induce apoptosis in the absence of Bax and Bak,” Genes and Development, vol. 15, no. 12, pp. 1481–1486, 2001. View at Publisher · View at Google Scholar · View at Scopus
  17. A. Kelekar and C. B. Thompson, “Bcl-2-family proteins: the role of the BH3 domain in apoptosis,” Trends in Cell Biology, vol. 8, no. 8, pp. 324–330, 1998. View at Publisher · View at Google Scholar · View at Scopus
  18. A. De Biasio, J. A. Vrana, P. Zhou et al., “N-terminal truncation of antiapoptotic MCL1, but not G2/M- induced phosphorylation, is associated with stabilization and abundant expression in tumor cells,” Journal of Biological Chemistry, vol. 282, no. 33, pp. 23919–23936, 2007. View at Publisher · View at Google Scholar · View at Scopus
  19. L. Chen, S. N. Willis, A. Wei et al., “Differential targeting of prosurvival Bcl-2 proteins by their BH3-only ligands allows complementary apoptotic function,” Molecular Cell, vol. 17, no. 3, pp. 393–403, 2005. View at Publisher · View at Google Scholar · View at Scopus
  20. T. Kuwana, L. Bouchier-Hayes, J. E. Chipuk et al., “BH3 domains of BH3-only proteins differentially regulate Bax-mediated mitochondrial membrane permeabilization both directly and indirectly,” Molecular Cell, vol. 17, no. 4, pp. 525–535, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. L. J. Pagliari, T. Kuwana, C. Bonzon et al., “The multidomain proapoptotic molecules Bax and Bak are directly activated by heat,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 50, pp. 17975–17980, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. A. Letai, “BCL-2: found bound and drugged!,” Trends in Molecular Medicine, vol. 11, no. 10, pp. 442–444, 2005. View at Publisher · View at Google Scholar · View at Scopus
  23. J. Zhao, M. Xin, T. Wang, Y. Zhang, and X. Deng, “Nicotine enhances the antiapoptotic function of Mcl-1 through phosphorylation,” Molecular Cancer Research, vol. 7, no. 12, pp. 1954–1961, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. M. Xin and X. Deng, “Nicotine inactivation of the proapoptotic function of Bax through phosphorylation,” Journal of Biological Chemistry, vol. 280, no. 11, pp. 10781–10789, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. Z. Jin, F. Gao, T. Flagg, and X. Deng, “Nicotine induces multi-site phosphorylation of Bad in association with suppression of apoptosis,” Journal of Biological Chemistry, vol. 279, no. 22, pp. 23837–23844, 2004. View at Publisher · View at Google Scholar · View at Scopus
  26. S. D. Stellman, T. Takezaki, L. Wang et al., “Smoking and lung cancer risk in American and Japanese men: an international case-control study,” Cancer Epidemiology Biomarkers and Prevention, vol. 10, no. 11, pp. 1193–1199, 2001. View at Google Scholar · View at Scopus
  27. C. M. Dresler, “Is it more important to quit smoking than which chemotherapy is used?” Lung Cancer, vol. 39, no. 2, pp. 119–124, 2003. View at Publisher · View at Google Scholar · View at Scopus
  28. Centers for Disease Control and Prevention, “Annual smoking-attributable mortality, years of potential life lost, and economic costs—United States, 1995–1999,” Morbidity and Mortality Weekly Report, vol. 51, no. 14, pp. 300–303, 2002. View at Google Scholar
  29. S. S. Hecht, “Tobacco smoke carcinogens and lung cancer,” Journal of the National Cancer Institute, vol. 91, no. 14, pp. 1194–1210, 1999. View at Google Scholar · View at Scopus
  30. N. L. Benowitz, “Drug therapy. Pharmacologic aspects of cigarette smoking and nicotine addiction,” The New England Journal of Medicine, vol. 319, no. 20, pp. 1318–1330, 1988. View at Google Scholar · View at Scopus
  31. M. F. Denissenko, A. Pao, M. Tang, and G. P. Pfeifer, “Preferential formation of benzo[a]pyrene adducts at lung cancer mutational hotspots in P53,” Science, vol. 274, no. 5286, pp. 430–432, 1996. View at Publisher · View at Google Scholar
  32. R. Maneckjee and J. D. Minna, “Opioid and nicotine receptors affect growth regulation of human lung cancer cell lines,” Proceedings of the National Academy of Sciences of the United States of America, vol. 87, no. 9, pp. 3294–3298, 1990. View at Publisher · View at Google Scholar · View at Scopus
  33. S. C. Wright, J. Zhong, H. Zheng, and J. W. Larrick, “Nicotine inhibition of apoptosis suggests a role in tumor promotion,” The FASEB Journal, vol. 7, no. 11, pp. 1045–1051, 1993. View at Google Scholar · View at Scopus
  34. W. L. Heusch and R. Maneckjee, “Signalling pathways involved in nicotine regulation of apoptosis of human lung cancer cells,” Carcinogenesis, vol. 19, no. 4, pp. 551–556, 1998. View at Publisher · View at Google Scholar · View at Scopus
  35. S. G. Rhee and Y. S. Bae, “Regulation of phosphoinositide-specific phospholipase C isozymes,” The Journal of Biological Chemistry, vol. 272, pp. 15045–15048, 1997. View at Publisher · View at Google Scholar
  36. J. Shen, L. Xu, T. K. Owonikoko et al., “NNK promotes migration and invasion of lung cancer cells through activation of c-Src/PKCι/FAK loop,” Cancer Letters, vol. 318, no. 1, pp. 106–113, 2012. View at Publisher · View at Google Scholar · View at Scopus
  37. X. Deng, P. Ruvolo, B. Carr, and W. S. May Jr., “Survival function of ERK1/2 as IL-3-activated, staurosporine-resistant Bcl2 kinases,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 4, pp. 1578–1583, 2000. View at Publisher · View at Google Scholar · View at Scopus
  38. E. Yang and S. J. Korsmeyer, “Molecular thanatopsis: a discourse on the BCL2 family and cell death,” Blood, vol. 88, no. 2, pp. 386–401, 1996. View at Google Scholar
  39. E. S. Alnemri, N. M. Robertson, T. F. Fernandes, C. M. Croce, and G. Litwack, “Overexpressed full-length human BCL2 extends the survival of baculovirus- infected Sf9 insect cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 89, no. 16, pp. 7295–7299, 1992. View at Google Scholar · View at Scopus
  40. W. S. May, P. G. Tyler, T. Ito, D. K. Armstrong, K. A. Qatsha, and N. E. Davidson, “Interleukin-3 and bryostatin-1 mediate hyperphosphorylation of Bcl2α in association with suppression of apoptosis,” Journal of Biological Chemistry, vol. 269, no. 43, pp. 26865–26870, 1994. View at Google Scholar · View at Scopus
  41. K. Yamamoto, H. Ichijo, and S. J. Korsmeyer, “BCL-2 is phosphorylated and inactivated by an ASK1/Jun N-terminal protein kinase pathway normally activated at G(2)/M,” Molecular and Cellular Biology, vol. 19, no. 12, pp. 8469–8478, 1999. View at Google Scholar · View at Scopus
  42. T. Ito, X. Deng, B. Carr, and W. S. May, “Bcl-2 phosphorylation required for anti-apoptosis function,” The Journal of Biological Chemistry, vol. 272, pp. 11671–11673, 1997. View at Publisher · View at Google Scholar
  43. P. P. Ruvolo, X. Deng, B. K. Carr, and W. S. May, “A functional role for mitochondrial protein kinase Cα in Bcl2 phosphorylation and suppression of apoptosis,” Journal of Biological Chemistry, vol. 273, no. 39, pp. 25436–25442, 1998. View at Publisher · View at Google Scholar · View at Scopus
  44. H. M. Schuller, H. K. Plummer 3rd, and B. A. Jull, “Receptor-mediated effects of nicotine and its nitrosated derivative NNK on pulmonary neuroendocrine cells,” Anatomical Record A: Discoveries in Molecular, Cellular, and Evolutionary Biology, vol. 270, no. 1, pp. 51–58, 2003. View at Google Scholar · View at Scopus
  45. G. P. Linette, J. L. Hess, C. L. Sentman, and S. J. Korsmeyer, “Peripheral T-cell lymphoma in lckpr-bcl-2 transgenic mice,” Blood, vol. 86, no. 4, pp. 1255–1260, 1995. View at Google Scholar · View at Scopus
  46. N. Ikegaki, M. Katsumata, J. Minna, and Y. Tsujimoto, “Expression of bcl-2 in small cell lung carcinoma cells,” Cancer Research, vol. 54, no. 1, pp. 6–8, 1994. View at Google Scholar · View at Scopus
  47. Z. Jin, F. Gao, T. Flagg, and X. Deng, “Tobacco-specific nitrosamine 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone promotes functional cooperation of Bcl2 and c-Myc through phosphorylation in regulating cell survival and proliferation,” Journal of Biological Chemistry, vol. 279, no. 38, pp. 40209–40219, 2004. View at Publisher · View at Google Scholar · View at Scopus
  48. Z. Jin, W. S. May, F. Gao, T. Flagg, and X. Deng, “Bcl2 suppresses DNA repair by enhancing c-Myc transcriptional activity,” Journal of Biological Chemistry, vol. 281, no. 20, pp. 14446–14456, 2006. View at Publisher · View at Google Scholar · View at Scopus
  49. L. Song, D. Coppola, S. Livingston, D. Cress, and E. B. Haura, “Mcl-1 regulates survival and sensitivity to diverse apoptotic stimuli in human non-small cell lung cancer cells,” Cancer Biology and Therapy, vol. 4, no. 3, pp. 267–276, 2005. View at Google Scholar · View at Scopus
  50. S. Kobayashi, S. Lee, X. W. Meng et al., “Serine 64 phosphorylation enhances the antiapoptotic function of Mcl-1,” Journal of Biological Chemistry, vol. 282, no. 25, pp. 18407–18417, 2007. View at Publisher · View at Google Scholar · View at Scopus
  51. J. Chao, J. M. Wang, S. F. Lee et al., “Mcl-1 is an immediate-early gene activated by the granulocyte-macrophage colony-stimulating factor (GM-CSF) signaling pathway and is one component of the GM-CSF viability response,” Molecular and Cellular Biology, vol. 18, no. 8, pp. 4883–4898, 1998. View at Google Scholar · View at Scopus
  52. D. Nijhawan, M. Fang, E. Traer et al., “Elimination of Mcl-1 is required for the initiation of apoptosis following ultraviolet irradiation,” Genes and Development, vol. 17, no. 12, pp. 1475–1486, 2003. View at Publisher · View at Google Scholar · View at Scopus
  53. H. Liu, H. W. Peng, Y. S. Cheng, H. S. Yuan, and H. F. Yang-Yen, “Stabilization and enhancement of the antiapoptotic activity of Mcl-1 by TCTP,” Molecular and Cellular Biology, vol. 25, no. 8, pp. 3117–3126, 2005. View at Publisher · View at Google Scholar · View at Scopus
  54. A. M. Domina, J. A. Vrana, M. A. Gregory, S. R. Hann, and R. W. Craig, “MCL1 is phosphorylated in the PEST region and stabilized upon ERK activation in viable cells, and at additional sites with cytotoxic okadaic acid or taxol,” Oncogene, vol. 23, no. 31, pp. 5301–5315, 2004. View at Publisher · View at Google Scholar · View at Scopus
  55. A. M. Domina, J. H. Smith, and R. W. Craig, “Myeloid cell leukemia 1 is phosphorylated through two distinct pathways, one associated with extracellular signal-regulated kinase activation and the other with G2/M accumulation or protein phosphatase 1/2A inhibition,” Journal of Biological Chemistry, vol. 275, no. 28, pp. 21688–21694, 2000. View at Publisher · View at Google Scholar · View at Scopus
  56. V. Y. Shin, W. K. Wu, K. M. Chu et al., “Functional role of β-adrenergic receptors in the mitogenic action of nicotine on gastric cancer cells,” Toxicological Sciences, vol. 96, no. 1, pp. 21–29, 2007. View at Publisher · View at Google Scholar · View at Scopus
  57. I. Hirai and H.-G. Wang, “Survival-factor-induced phosphorylation of Bad results in its dissociation from Bcl-x(L) but not Bcl-2,” Biochemical Journal, vol. 359, no. 2, pp. 345–352, 2001. View at Publisher · View at Google Scholar · View at Scopus
  58. Y. Tan, M. R. Demeter, H. Ruan, and M. J. Comb, “BAD Ser-155 phosphorylation regulates BAD/Bcl-XL interaction and cell survival,” Journal of Biological Chemistry, vol. 275, no. 33, pp. 25865–25869, 2000. View at Publisher · View at Google Scholar · View at Scopus
  59. A. Bergmann, “Survival signaling goes BAD,” Developmental Cell, vol. 3, no. 5, pp. 607–608, 2002. View at Publisher · View at Google Scholar · View at Scopus
  60. S. R. Datta, A. Katsov, L. Hu et al., “14-3-3 proteins and survival kinases cooperate to inactivate BAD by BH3 domain phosphorylation,” Molecular Cell, vol. 6, no. 1, pp. 41–51, 2000. View at Google Scholar · View at Scopus
  61. M. P. Scheid, K. M. Schubert, and V. Duronio, “Regulation of bad phosphorylation and association with Bcl-x(L) by the MAPK/Erk kinase,” Journal of Biological Chemistry, vol. 274, no. 43, pp. 31108–31113, 1999. View at Publisher · View at Google Scholar · View at Scopus
  62. S. R. Datta, H. Dudek, X. Tao et al., “Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery,” Cell, vol. 91, no. 2, pp. 231–241, 1997. View at Publisher · View at Google Scholar
  63. X. M. Zhou, Y. Liu, G. Payne, R. J. Lutz, and T. Chittenden, “Growth factors inactivate the cell death promoter BAD by phosphorylation of its BH3 domain on Ser155,” Journal of Biological Chemistry, vol. 275, no. 32, pp. 25046–25051, 2000. View at Publisher · View at Google Scholar · View at Scopus
  64. X. Fang, S. Yu, A. Eder et al., “Regulation of BAD phosphorylation at serine 112 by the Ras-mitogen-activated protein kinase pathway,” Oncogene, vol. 18, no. 48, pp. 6635–6640, 1999. View at Google Scholar · View at Scopus
  65. Z. Jin, M. Xin, and X. Deng, “Survival function of protein kinase C{iota} as a novel nitrosamine 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone-activated bad kinase,” Journal of Biological Chemistry, vol. 280, no. 16, pp. 16045–16052, 2005. View at Publisher · View at Google Scholar · View at Scopus
  66. M. C. Wei, W. X. Zong, E. H. Cheng et al., “Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death,” Science, vol. 292, no. 5517, pp. 727–730, 2001. View at Publisher · View at Google Scholar · View at Scopus
  67. S. J. Gardai, D. A. Hildeman, S. K. Frankel et al., “Phosphorylation of Bax Ser184 by Akt regulates its activity and apoptosis in neutrophils,” Journal of Biological Chemistry, vol. 279, no. 20, pp. 21085–21095, 2004. View at Publisher · View at Google Scholar · View at Scopus
  68. M. Xin, F. Gao, W. S. May, T. Flagg, and X. Deng, “Protein kinase Czeta abrogates the proapoptotic function of Bax through phosphorylation,” Journal of Biological Chemistry, vol. 282, no. 29, pp. 21268–21277, 2007. View at Publisher · View at Google Scholar · View at Scopus
  69. E. L. Soucie, M. G. Annis, J. Sedivy et al., “Myc potentiates apoptosis by stimulating Bax activity at the mitochondria,” Molecular and Cellular Biology, vol. 21, no. 14, pp. 4725–4736, 2001. View at Publisher · View at Google Scholar · View at Scopus
  70. D. Hanahan and R. A. Weinberg, “The hallmarks of cancer,” Cell, vol. 100, no. 1, pp. 57–70, 2000. View at Publisher · View at Google Scholar · View at Scopus
  71. G. I. Evan, A. H. Wyllie, C. S. Gilbert et al., “Induction of apoptosis in fibroblasts by c-myc protein,” Cell, vol. 69, no. 1, pp. 119–128, 1992. View at Publisher · View at Google Scholar · View at Scopus
  72. R. Sears, F. Nuckolls, E. Haura, Y. Taya, K. Tamai, and J. R. Nevins, “Multiple Ras-dependent phosphorylation pathways regulate Myc protein stability,” Genes and Development, vol. 14, no. 19, pp. 2501–2514, 2000. View at Publisher · View at Google Scholar · View at Scopus
  73. J. C. Reed, M. Cuddy, S. Haldar et al., “BCL2-mediated tumorigenicity of a human T-lymphoid cell line: synergy with MYC and inhibiton by BCL2 antisense,” Proceedings of the National Academy of Sciences of the United States of America, vol. 87, no. 10, pp. 3660–3664, 1990. View at Publisher · View at Google Scholar · View at Scopus
  74. A. Fanidi, E. A. Harrington, and G. I. Evan, “Cooperative interaction between c-myc and bcl-2 proto-oncogenes,” Nature, vol. 359, no. 6395, pp. 554–556, 1992. View at Publisher · View at Google Scholar · View at Scopus
  75. R. P. Bissonnette, F. Echeverri, A. Mahboubi, and D. R. Green, “Apoptotic cell death induced by c-myc is inhibited by bcl-2,” Nature, vol. 359, no. 6395, pp. 552–554, 1992. View at Publisher · View at Google Scholar · View at Scopus