Hyper-O-GlcNAcylation is anti-apoptotic and maintains constitutive NF-κB activity in pancreatic cancer cells

Journal of Biological Chemistry

Volumn 288, Issue 21, 2013, Pages 15121-15130

  Ma, Zhiyuan ^a   Vocadlo, David J ^b   Vosseller, Keith ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b SIMON FRASER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DUCTAL ADENOCARCINOMAS; EPITHELIAL CELL GROWTH; NUCLEAR TRANSLOCATIONS; OXIDATIVE PHOSPHORYLATION; PHARMACOLOGICAL INHIBITION; POST-TRANSLATIONAL MODIFICATIONS; TARGET GENE EXPRESSION; TRANSCRIPTIONAL ACTIVITY;

AMINO ACIDS; BIOSYNTHESIS; CELL ADHESION; CELL DEATH; CELL PROLIFERATION; ENZYMES; GENE EXPRESSION;

CHEMICAL ACTIVATION;

HYDROLASE; I KAPPA B KINASE ALPHA; I KAPPA B KINASE BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; N ACETYLGLUCOSAMINE; O GLCNAC TRANSFERASE; O GLCNACASE; TRANSCRIPTION FACTOR RELA; TRANSFERASE; UNCLASSIFIED DRUG;

ACYLATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER CELL; CELL GROWTH; CELL SURVIVAL; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PANCREAS ADENOCARCINOMA; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TUMOR GROWTH;

APOPTOSIS; NF-KAPPA B (NF-ΚB); O-GLCNAC; O-GLCNACYLATION; PANCREATIC CANCER; WARBURG EFFECT;

ACTIVE TRANSPORT, CELL NUCLEUS; ACYLATION; AMINO ACID SUBSTITUTION; ANIMALS; APOPTOSIS; CARCINOMA, PANCREATIC DUCTAL; CELL LINE, TRANSFORMED; CELL NUCLEUS; CELL PROLIFERATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICE; MUTATION, MISSENSE; NEOPLASM PROTEINS; PANCREATIC NEOPLASMS; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION, GENETIC; URIDINE DIPHOSPHATE N-ACETYLGALACTOSAMINE;

EID: 84878225772     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.470047     Document Type: Article

References (47)

1. Warburg, O. (1956) On the origin of cancer cells. Science 123, 309-314
2. Kroemer, G., and Pouyssegur, J. (2008) Tumor cell metabolism: cancer's Achilles' heel. Cancer Cell 13, 472-482 (Pubitemid 351766797)
3. Vander Heiden, M. G., Cantley, L. C., and Thompson, C. B. (2009) Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324, 1029-1033
4. Yuneva, M., Zamboni, N., Oefner, P., Sachidanandam, R., and Lazebnik, Y. (2007) Deficiency in glutamine but not glucose induces MYC-dependent apoptosis in human cells. J. Cell Biol. 178, 93-105 (Pubitemid 47026405)
5. DeBerardinis, R. J. (2008) Is cancer a disease of abnormal cellular metabolism? New angles on an old idea. Genet. Med. 10, 767-777
6. Hart, G. W., Slawson, C., Ramirez-Correa, G., and Lagerlof, O. (2011) Cross talk between O-GlcNAcylation and phosphorylation: roles in signaling, transcription, and chronic disease. Annu. Rev. Biochem. 80, 825-858
7. Wells, L., Vosseller, K., and Hart, G. W. (2003) A role for N-acetylglucosamine as a nutrient sensor and mediator of insulin resistance. Cell Mol. Life Sci. 60, 222-228 (Pubitemid 36343902)
8. Caldwell, S. A., Jackson, S. R., Shahriari, K. S., Lynch, T. P., Sethi, G., Walker, S., Vosseller, K., and Reginato, M. J. (2010) Nutrient sensor O-GlcNAc transferase regulates breast cancer tumorigenesis through targeting of the oncogenic transcription factor FoxM1. Oncogene 29, 2831-2842
9. Lynch, T. P., Ferrer, C. M., Jackson, S. R., Shahriari, K. S., Vosseller, K., and Reginato, M. J. (2012) Critical Role of O-Linked β-N- Acetylglucosamine Transferase in Prostate Cancer Invasion, Angiogenesis, and Metastasis. J. Biol. Chem. 287, 11070-11081
10. Karin, M., and Greten, F. R. (2005) NF-κB: linking inflammation and immunity to cancer development and progression. Nat. Rev. Immunol. 5, 749-759 (Pubitemid 41400849)
11. Karin, M. (2006) Nuclear factor-κB in cancer development and progression. Nature 441, 431-436
12. Wang, W., Abbruzzese, J. L., Evans, D. B., Larry, L., Cleary, K. R., and Chiao, P. J. (1999) The nuclear factor-κB RelA transcription factor is constitutively activated in human pancreatic adenocarcinoma cells. Clin. Cancer Res. 5, 119-127 (Pubitemid 29045184)
13. Liptay, S., Weber, C. K., Ludwig, L., Wagner, M., Adler, G., and Schmid, R. M. (2003) Mitogenic and antiapoptotic role of constitutive NF-κB/Rel activity in pancreatic cancer. Int. J. Cancer 105, 735-746 (Pubitemid 36706095)
14. Siegel, R., Naishadham, D., and Jemal, A. (2012) Cancer statistics, 2012. CA Cancer J. Clin. 62, 10-29
15. Guttridge, D. C., Albanese, C., Reuther, J. Y., Pestell, R. G., and Baldwin, A. S., Jr. (1999) NF-κB controls cell growth and differentiation through transcriptional regulation of cyclin D1. Mol. Cell Biol. 19, 5785-5799 (Pubitemid 29339933)
16. Kawauchi, K., Araki, K., Tobiume, K., and Tanaka, N. (2008) p53 regulates glucose metabolism through an IKK-NF-κB pathway and inhibits cell transformation. Nat. Cell Biol. 10, 611-618 (Pubitemid 351627381)
17. James, L. R., Tang, D., Ingram, A., Ly, H., Thai, K., Cai, L., and Scholey, J. W. (2002) Flux through the hexosamine pathway is a determinant of nuclear factor κB- dependent promoter activation. Diabetes 51, 1146-1156 (Pubitemid 34438362)
18. Yang, W. H., Park, S. Y., Nam, H. W., Kim do, H., Kang, J. G., Kang, E. S., Kim, Y. S., Lee, H. C., Kim, K. S., and Cho, J. W. (2008) NFκB activation is associated with its O-GlcNAcylation state under hyperglycemic conditions. Proc. Natl. Acad. Sci. U.S.A. 105, 17345-17350
19. Comer, F. I., Vosseller, K., Wells, L., Accavitti, M. A., and Hart, G. W. (2001) Characterization of a mouse monoclonal antibody specific for O-linked N-acetylglucosamine. Anal. Biochem. 293, 169-177 (Pubitemid 32547901)
20. Macauley, M. S., Whitworth, G. E., Debowski, A. W., Chin, D., and Vocadlo, D. J. (2005) O-GlcNAcase uses substrate-assisted catalysis: kinetic analysis and development of highly selective mechanism-inspired inhibitors. J. Biol. Chem. 280, 25313-25322 (Pubitemid 40962233)
21. Gloster, T. M., Zandberg, W. F., Heinonen, J. E., Shen, D. L., Deng, L., and Vocadlo, D. J. (2011) Hijacking a biosynthetic pathway yields a glycosyltransferase inhibitor within cells. Nature Chemical Biol. 7, 174-181
22. Fan, Y., Mao, R., Zhao, Y., Yu, Y., Sun, W., Song, P., Shi, Z., Zhang, D., Yvon, E., Zhang, H., Fu, S., and Yang, J. (2009) Tumor necrosis factor-α induces RelA degradation via ubiquitination at lysine 195 to prevent excessive nuclear factor-κB activation. J. Biol. Chem. 284, 29290-29297
23. Furukawa, T., Duguid, W. P., Rosenberg, L., Viallet, J., Galloway, D. A., and Tsao, M. S. (1996) Long-term culture and immortalization of epithelial cells from normal adult human pancreatic ducts transfected by the E6E7 gene of human papilloma virus 16. Am. J. Pathol. 148, 1763-1770 (Pubitemid 26171674)
24. Wice, B. M., Trugnan, G., Pinto, M., Rousset, M., Chevalier, G., Dussaulx, E., Lacroix, B., and Zweibaum, A. (1985) The intracellular accumulation of UDP-N-acetylhexosamines is concomitant with the inability of human colon cancer cells to differentiate. J. Biol. Chem. 260, 139-146 (Pubitemid 15165293)
25. Robinson, K. A., Weinstein, M. L., Lindenmayer, G. E., and Buse, M. G. (1995) Effects of diabetes and hyperglycemia on the hexosamine synthesis pathway in rat muscle and liver. Diabetes 44, 1438-1446
26. Rhim, A. D., Mirek, E. T., Aiello, N. M., Maitra, A., Bailey, J. M., McAllister, F., Reichert, M., Beatty, G. L., Rustgi, A. K., Vonderheide, R. H., Leach, S. D., and Stanger, B. Z. (2012) EMT and dissemination precede pancreatic tumor formation. Cell 148, 349-361
27. Duxbury, M. S., Ito, H., Zinner, M. J., Ashley, S. W., and Whang, E. E. (2004) CEACAM6 gene silencing impairs anoikis resistance and in vivo metastatic ability of pancreatic adenocarcinoma cells. Oncogene 23, 465-473 (Pubitemid 38175001)
28. Maier, H. J., Schmidt-Strassburger, U., Huber, M. A., Wiedemann, E. M., Beug, H., and Wirth, T. (2010) NF-κB promotes epithelial-mesenchymal transition, migration and invasion of pancreatic carcinoma cells. Cancer Lett. 295, 214-228
29. Varadhachary, G. R., Tamm, E. P., Abbruzzese, J. L., Xiong, H. Q., Crane, C. H., Wang, H., Lee, J. E., Pisters, P. W., Evans, D. B., and Wolff, R. A. (2006) Borderline resectable pancreatic cancer: definitions, management, and role of preoperative therapy. Ann. Surg. Oncol. 13, 1035-1046 (Pubitemid 44337962)
30. Wolff, R. A. (2007) Chemotherapy for pancreatic cancer: from metastatic disease to adjuvant therapy. Cancer J. 13, 175-184
31. Schneiderhan, W., Scheler, M., Holzmann, K. H., Marx, M., Gschwend, J. E., Bucholz, M., Gress, T. M., Seufferlein, T., Adler, G., and Oswald, F. (2009) CD147 silencing inhibits lactate transport and reduces malignant potential of pancreatic cancer cells in in vivo and in vitro models. Gut 58, 1391-1398
32. Ito, H., Duxbury, M., Zinner, M. J., Ashley, S. W., and Whang, E. E. (2004) Glucose transporter-1 gene expression is associated with pancreatic cancer invasiveness and MMP-2 activity. Surgery 136, 548-556 (Pubitemid 39186566)
33. Maher, J. C., Savaraj, N., Priebe, W., Liu, H., and Lampidis, T. J. (2005) Differential sensitivity to 2-deoxy-D-glucose between two pancreatic cell lines correlates with GLUT-1 expression. Pancreas 30, e34-39
34. Wu, M. C., Arimura, G. K., and Yunis, A. A. (1978) Mechanism of sensitivity of cultured pancreatic carcinoma to asparaginase. Int. J. Cancer 22, 728-733 (Pubitemid 9069793)
35. Kaadige, M. R., Looper, R. E., Kamalanaadhan, S., and Ayer, D. E. (2009) Glutamine-dependent anapleurosis dictates glucose uptake and cell growth by regulating MondoA transcriptional activity. Proc. Natl. Acad. Sci. U.S.A. 106, 14878-14883
36. Ying, H., Kimmelman, A. C., Lyssiotis, C. A., Hua, S., Chu, G. C., Fletcher-Sananikone, E., Locasale, J. W., Son, J., Zhang, H., Coloff, J. L., Yan, H., Wang, W., Chen, S., Viale, A., Zheng, H., Paik, J. H., Lim, C., Guimaraes, A. R., Martin, E. S., Chang, J., Hezel, A. F., Perry, S. R., Hu, J., Gan, B., Xiao, Y., Asara, J. M., Weissleder, R., Wang, Y. A., Chin, L., Cantley, L. C., and DePinho, R. A. (2012) Oncogenic Kras maintains pancreatic tumors through regulation of anabolic glucose metabolism. Cell 149, 656-670
37. Shi, Y., Tomic, J., Wen, F., Shaha, S., Bahlo, A., Harrison, R., Dennis, J. W., Williams, R., Gross, B. J., Walker, S., Zuccolo, J., Deans, J. P., Hart, G. W., and Spaner, D. E. (2010) Aberrant O-GlcNAcylation characterizes chronic lymphocytic leukemia. Leukemia 24, 1588-1598
38. Krzelak, A., Forma, E., Bernaciak, M., Romanowicz, H., and Bry, M. (2012) Gene expression of O-GlcNAc cycling enzymes in human breast cancers. Clin. Exp. Med. 12, 61-65
39. Mi, W., Gu, Y., Han, C., Liu, H., Fan, Q., Zhang, X., Cong, Q., and Yu, W. (2011) O-GlcNAcylation is a novel regulator of lung and colon cancer malignancy. Biochim. Biophys. Acta 1812, 514-519
40. Zhu, Q., Zhou, L., Yang, Z., Lai, M., Xie, H., Wu, L., Xing, C., Zhang, F., and Zheng, S. (2012) O-GlcNAcylation plays a role in tumor recurrence of hepatocellular carcinoma following liver transplantation. Medical Oncology 29, 985-993
41. Park, S. Y., Kim, H. S., Kim, N. H., Ji, S., Cha, S. Y., Kang, J. G., Ota, I., Shimada, K., Konishi, N., Nam, H. W., Hong, S. W., Yang, W. H., Roth, J., Yook, J. I., and Cho, J. W. (2010) Snail1 is stabilized by O-GlcNAc modification in hyperglycaemic condition. EMBO J. 29, 3787-3796
42. Kawauchi, K., Araki, K., Tobiume, K., and Tanaka, N. (2009) Loss of p53 enhances catalytic activity of IKKβ through O-linked β-N-acetyl glucosamine modification. Proc. Natl. Acad. Sci. U.S.A. 106, 3431-3436
43. Ahmad, R., Raina, D., Trivedi, V., Ren, J., Rajabi, H., Kharbanda, S., and Kufe, D. (2007) MUC1 oncoprotein activates the IκB kinase β complex and constitutive NF-κB signalling. Nat. Cell Biol. 9, 1419-1427 (Pubitemid 350201755)
44. Wilson, W., 3rd, and Baldwin, A. S. (2008) Maintenance of constitutive IκB kinase activity by glycogen synthase kinase-3α/β in pancreatic cancer. Cancer Res. 68, 8156-8163
45. Lee, H., Herrmann, A., Deng, J. H., Kujawski, M., Niu, G., Li, Z., Forman, S., Jove, R., Pardoll, D. M., and Yu, H. (2009) Persistently activated Stat3 maintains constitutive NF-κB activity in tumors. Cancer Cell 15, 283-293
46. Kong, R., Sun, B., Jiang, H., Pan, S., Chen, H., Wang, S., Krissansen, G. W., and Sun, X. (2010) Downregulation of nuclear factor-κB p65 subunit by small interfering RNA synergizes with gemcitabine to inhibit the growth of pancreatic cancer. Cancer Lett. 291, 90-98
47. Ren, Q., Kari, C., Quadros, M. R., Burd, R., McCue, P., Dicker, A. P., and Rodeck, U. (2006) Malignant transformation of immortalized HaCaT keratinocytes through deregulated nuclear factor κB signaling. Cancer Res. 66, 5209-5215 (Pubitemid 43844944)