Transglutaminase-mediated activation of nuclear transcription factor-κB in cancer cells: A new therapeutic opportunity

Current Cancer Drug Targets

Volumn 7, Issue 6, 2007, Pages 559-565

  Verma, Amit ^a   Mehta, Kapil ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; CISPLATIN; CYTARABINE; DAUNORUBICIN; DOXORUBICIN; ETOPOSIDE; GUANINE NUCLEOTIDE BINDING PROTEIN; I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LYMPHOTOXIN BETA; PACLITAXEL; PROTEIN BCL XL; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; PROTEIN P100; SMALL INTERFERING RNA; TAMOXIFEN; TISSUE TYPE TRANSGLUTAMINASE; UNCLASSIFIED DRUG; VINBLASTINE; VINCRISTINE;

APOPTOSIS; CANCER; CANCER CELL; CANCER CHEMOTHERAPY; CANCER RESEARCH; CARCINOGENESIS; DRUG TARGETING; ENZYME INHIBITION; HUMAN; METASTASIS; OXIDATIVE STRESS; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; RADIOSENSITIVITY; REVIEW; TUMOR GROWTH;

GENE EXPRESSION REGULATION; HUMANS; NEOPLASMS; NF-KAPPA B; PROTEIN CONFORMATION; TRANSGLUTAMINASES;

EID: 34548399498     PISSN: 15680096     EISSN: None     Source Type: Journal    
DOI: 10.2174/156800907781662275     Document Type: Review

References (68)

1. Sen, R.; Baltimore, D. Inducibility of κ immunoglobulins enhancer-binding protein NF-κB by a posttranslational mechanism. Cell 1986, 47, 921-929.
2. Baeuerle, P.; Henkel, T. Function and activation of NF-κB in the immune system. Annu. Rev. Immunol. 1994, 12, 141-179.
3. Barnes, P. J.; Karin, M. Nuclear factor-kappaB: a pivotal transcription factor in chronic inflammatory diseases. N. Engl. J. Med. 1997, 336, 1066-1071.
4. Bours, V.; Bonizzi, G.; Bentires-Alj, M.; Bureau, F.; Piette, J.; Lekeux, P.; Merville, M. NF-κB activation in response to toxical and therapeutical agents: role in inflammation and cancer treatment. Toxicology 2000, 153, 27-38.
5. Karin, M.; Cao, Y.; Greten, F.; Li, Z. NF-κB in cancer: from innocent bystander to major culprit, Nature Rev. Cancer 2002, 2, 301-310.
6. Baeuerle, P. A.; Baltimore, D. NF-κB: ten years after. Cell 1996, 87, 13-20.
7. Baldwin, A. S. Jr. The NF-κB and I kappa B proteins: new discoveries and insights. Annu. Rev. Immunol. 1996, 14, 649-693.
8. Siebenlist, U.; Franzoso, G.; Brown, K. Structure, regulation and function of NF-κB. Annu. Rev. Cell Biol. 1994, 10, 405-455.
9. Pahl, H. Activators and target genes of Rel/ NF-κB transcription factors. Oncogene 1999, 18, 6853-6866.
10. Karin, M. The beginning of the end: IkappaB kinase (IKK) and NF-kappaB activation. J. Biol. Chem. 1999, 274, 27339-27342.
11. Zandi, E.; Karin, M. Bridging the gap: composition, regulation, and physiological function of the IkappaB kinase complex. Mol. Cell Biol. 1999, 19, 4547-4551.
12. Sachdev, S.; Hoffmann, A.; Hannink, M. Nuclear localization of IkappaB alpha is mediated by the second ankyrin repeat: the IkappaB alpha ankyrin repeats define a novel class of cisacting nuclear import sequences. Mol. Cell Biol. 1998, 18, 2524-2534.
13. Ghosh, G.; van Duyne, G.; Ghosh, S.; Sigler, P. B. Structure of NF-κB p50 homodimer bound to a kappa B site. Nature 1995, 373, 303-310.
14. Gilmore, T. D. The Rel/NF-kappaB signal transduction pathway: introduction. Oncogene 1999, 18, 6842-6844.
15. Senftleben, U.; Cao, Y.; Xiao, G.; Greten, F. R.; Krahn, G.; Bonizzi, G.; Chen, Y.; Hu, Y.; Fong, A.; Sun, S. C.; Karin, M. Activation by IKK alpha of a second, evolutionary conserved, NF-kappa B signaling pathway. Science 2001, 293, 1495-1499.
16. Imbert, V.; Rupec, R. A.; Livolsi, A.; Pahl, H. L.; Traenckner, E. B.; Mueller-Dieckmann, C.; Farahifar, D.; Rossi, B.; Auberger, P.; Baeuerle, P. A.; Peyron, J. F. Tyrosine phosphorylation of IκB activates NF-κB without proteolytic degradation of IκBα. Cell 1996, 86, 787-798.
17. Livolsi, A.; Busuttil, V.; Imbert, V.; Abraham, R. T.; Peyron, J. F. Tyrosine phosphorylation-dependent activation of NFκB. Requirement for p56 LCK and ZAP-70 protein tyrosine kinases. Eur. J. Biochem. 2001, 268, 1508-1515.
18. Liu, R.; Aupperle, K.; Terkeltaub, R. Src family protein tyrosine kinase signaling mediates monosodium urate crystal-induced IL-8 expression by monocytic THP-1 cells. J. Leukoc. Biol. 2001, 70, 961-968.
19. al-Ramadi, B. K.; Welte, T.; Fernandez-Cabezudo, M. J.; Galadari, S.; Dittel, B.; Fu, X. Y.; Bothwell, A. L. The Src-protein tyrosine kinase Lck is required for IL-1-mediated costimulatory signaling in Th2 cells. J. Immunol. 2001, 167, 6827-6833.
20. Abu-Amer, Y.; Dowdy, S. F.; Ross, F. P.; Clohisy, J. C.; Teitelbaum, S. L. TAT fusion proteins containing tyrosine 42-deleted IkappaBalpha arrest osteoclastogenesis. J. Biol. Chem. 2001, 276, 30499-30503.
21. Beraud, C.; Henzel, W. J.; Baeuerle, P. A. Involvement of regulatory and catalytic subunits of phosphoinositide 3-kinase in NFκB activation. Proc. Natl. Acad. Sci. USA 1999, 96, 429-434.
22. Algül, H.; Tando, Y.; Beil, M.; Weber, C. K.; Von Weyhern, C.; Schneider, G.; Adler, G.; Schmid, R. M. Different modes of NF-kappaB/Rel activation in pancreatic lobules. Am. J. Physiol. Gastrointest. Liver Physiol. 2002, 283, G270-G281.
23. Li, N.; Karin, M. Ionizing radiation and short wavelength UV activate NF-κB through two distinct mechanisms. Proc. Natl. Acad. Sci. USA 1998, 95, 13012-13017.
24. Anest, V.; Cogswell, P. C.; Baldwin, A. S., Jr. IκB Kinase αand p65/RelA contribute to optimal epidermal growth factor-induced c-fos gene expression independent of IκBα degradation. J. Biol. Chem. 2004, 279, 31183-31189.
25. Bharti, A. C.; Aggarwal, B. B. Nuclear factor-kappa B and cancer: its role in prevention and therapy (review). Biochem. Pharmacol. 2002, 64, 883-888.
26. Yan, Z.; Subbaramaiah, K.; Camilli, T.; Zhang, F.; Tanabe, T.; McCaffrey, T. A.; Dannenberg, A. J.; Weksler, B. B. Benzo[a]pyrene induces the transcription of cyclooxygenase-2 in vascular smooth muscle cells. Evidence for the involvement of extracellular signal-regulated kinase and NF-kappaB. J. Biol. Chem. 2000, 275, 4949-4955.
27. Rioux, N.; Castonguay, A. The induction of cyclooxygenase-1 by a tobacco carcinogen in U937 human macrophages is correlated to the activation of NF-kappaB. Carcinogenesis 2000, 21, 1745-1751.
28. Li, N.; Karin, M. Ionizing radiation and short wavelength UV activate NF-kappaB through two distinct mechanisms. Proc. Natl. Acad. Sci. USA 1998, 95, 13012-13017.
29. Baeuerle, P. A.; Lenardo, M.; Pierce, J. W.; Baltimore, D. Phorbol-ester-induced activation of the NF-kappa B transcription factor involves dissociation of an apparently cytoplasmic NF-kappa B/inhibitor complex. Cold Spring Harbor Symp. Quant. Biol. 1988, 53, 789-798.
30. Wu, M.; Lee, H.; Bellas, R. E.; Schauer, S. L.; Arsura, M.; Katz, D.; FitzGerald, M. J.; Rothstein, T. L.; Sherr, D. H.; Sonenshein, G. E. Inhibition of NF-kappaB/Rel induces apoptosis of murine B cells. EMBO J. 1996, 15, 4682-4690.
31. Beg, A. A.; Baltimore, D. An essential role for NF-kappaB in preventing TNF-alpha-induced cell death. Science 1996, 274, 782-784.
32. Wang, C. Y.; Mayo, M. W.; Baldwin, A. S. Jr. TNF- and cancer therapy-induced apoptosis: potentiation by inhibition of NF-kappaB. Science 1996, 274, 784-787.
33. Van Antwerp, D. J.; Martin, S. J.; Kafri, T.; Green, D. R.; Verma, I. M. Suppression of TNF-alpha-induced apoptosis by NF-kappaB. Science 1996, 274, 787-789.
34. Pahl, H. L. Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene 1999, 18, 6853-6866.
35. Mukhopadhyay, A.; Bueso-Ramos, C.; Chatterjee, D.; Pantazis, P.; Aggarwal, B. B. Curcumin downregulates cell survival mechanisms in human prostate cancer cell lines. Oncogene 2001, 20, 7597-7609.
36. Mori, N.; Fujii, M.; Ikeda, S.; Yamada, Y.; Tomonaga, M.; Ballard, D. W.; Yamamoto, N. Constitutive activation of NF-kappaB in primary adult T-cell leukemia cells. Blood 1999, 93, 2360-2368.
37. Bargou, R. C.; Emmerich, F.; Krappmann, D.; Bommert, K.; Mapara, M. Y.; Arnold, W.; Royer, H. D.; Grinstein, E.; Greiner, A.; Scheidereit, C.; Dorken, B. Constitutive nuclear factor-kappaB-RelA activation is required for proliferation and survival of Hodgkin's disease tumor cells. J. Clin. Invest. 1997, 100, 2961-2969.
38. Bours, V.; Dejardin, E.; Goujon-Letawe, F.; Merville, M. P.; Castronovo, V. The NF-kappa B transcription factor and cancer: high expression of NF-kappa B- and I kappa B-related proteins in tumor cell lines. Biochem. Pharmacol. 1994, 47, 145-149.
39. Fesus, L.; Piacentini, M. Transglutaminase 2: an enigmatic enzyme with diverse functions. Trends Biochem. Sci. 2002, 27, 534-539.
40. Chen, J. S.; Mehta, K. Tissue transglutaminase: an enzyme with a split personality. Int. J. Biochem. Cell. Biol. 1999, 31, 817-836.
41. Griffin, M.; Casadio, R.; Bergamini, C. M. Transglutaminases: nature's biological glues. Biochem. J. 2002, 368, 377-396.
42. Lorand, L.; Graham, R. M. Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat. Rev. Mol. Cell Biol. 2003, 4, 140-156.
43. Skill, N. J.; Johnson, T. S.; Coutts, I. G.; Saint, R. E.; Fisher, M.; Huang, L.; El Nahas, A. M.; Collighan, R. J.; Griffin M. Inhibition of transglutaminase activity reduces extracellular matrix accumulation induced by high glucose levels in proximal tubular epithelial cells. J. Biol. Chem. 2004, 279, 47754-47762.
44. Jeong, J. M.; Murthy, S. N.; Radek, J. T.; Lorand, L. The fibronectin-binding domain of transglutaminase. J. Biol. Chem. 1995, 270, 5654-5658.
45. Ballestar, E.; Boix-Chornet, M.; Franco, L. Conformational changes in the nucleosome followed by the selective accessibility of histone glutamines in the transglutaminase reaction: effects of ionic strength. Biochemistry 2001, 40, 1922-1929.
46. Fesus, L.; Thomazy, V.; Falus, A. Induction and activation of tissue transglutaminase during programmed cell death. FEBS Lett. 1987, 224, 104-108.
47. Fesus, L.; Szondy, Z. Transglutaminase 2 in the balance of cell death and survival (review). FEBS Lett. 2005, 579, 3297-3302.
48. Szondy, Z.; Sarang, Z.; Molnar, P.; Nemeth, T.; Piacentini, M.; Mastroberardino, P. G.; Falasca, L.; Aeschlimann, D.; Kovacs, J.; Kiss, I.; Szegezdi, E.; Lakos, G.; Rajnavolgyi, E.; Birckbichler, P. J.; Melino, G.; Fesus, L. Transglutaminase 2-/-mice reveal a phagocytosis-associated crosstalk between macrophages and apoptotic cells. Proc. Natl. Acad. Sci. USA 2003, 100, 7812-7817.
49. De Laurenzi, V.; Melino, G. Gene disruption of tissue transglutaminase. Mol. Cell Biol. 2001, 21, 148-155.
50. Antonyak, M. A.; McNeill, C. J.; Wakshlag, J. J.; Boehm, J. E.; Cerione, R. A. Activation of the Ras-ERK pathway inhibits retinoic acid-induced stimulation of tissue transglutaminase expression in NIH3T3 cells. J. Biol. Chem. 2003, 278, 15859-15866.
51. Boehm, J. E.; Singh, U.; Combs, C.; Antonyak, M. A.; Cerione, R. A. Tissue transglutaminase protects against apoptosis by modifying the tumor suppressor protein p110 Rb. J. Biol. Chem. 2002, 277, 20127-20130.
52. Mehta, K.; Fok, J. Y.; Mangala, L. S. Tissue transglutaminase: from biological glue to cell survival cues. Front. Biosci. 2006, 11, 173-185.
53. Fesus, L.; Szondy, Z. Transglutaminase 2 in the balance of cell death and survival. FEBS Lett. 2005, 579, 3297-3302.
54. Mehta, K.; Fok, J.; Miller, F. R.; Koul, D.; Sahin, A. A. Prognostic significance of tissue transglutaminase in drug resistant and metastatic breast cancer. Clin. Cancer Res. 2004, 10, 8068-8076.
55. Fok, J.; Ekmekcioglu, S.; Mehta, K. Tissue transglutaminase expression in melanomas: a potential target for intervention. Mol. Cancer Ther. 2006, 5, 1493-1503.
56. Verma, A.; Wang, H.; Manavathi, B.; Fok, J. Y.; Mann, A. P.; Kumar, R.; Mehta, K. Increased expression of tissue transglutaminase in pancreatic ductal adenocarcinoma and its implications in drug resistance and metastasis. Cancer Res. 2006, 66, 10525-10533.
57. Han, J. A.; Park, S. C. Reduction of transglutaminase 2 expression is associated with an induction of drug sensitivity in the PC-14 human lung cancer cell line. J. Cancer Res. Clin. Oncol. 1999, 125, 89-95.
58. McLean, G. W.; Carragher, N. O.; Avizienyte, E.; Evans, J.; Brunton, V. G.; Frame, M. C. The role of focal-adhesion kinase in cancer-a new therapeutic opportunity. Nat. Rev. Cancer 2005, 5, 505-515.
59. Herman, J. F.; Mangala, L. S.; Mehta, K. Implications of increased tissue transglutaminase (TG2)expression in drug-resistant breast cancer (MCF-7) cells. Oncogene 2006, 25, 3049-3058.
60. Mangala, L. S.; Fok, J. Y.; Zorrilla-Calancha, I. R.; Verma, A.; Mehta, K. Tissue transglutaminase expression promotes cell attachment, invasion and survival in breast cancer cells. Oncogene 2007, 26(17), 2459-2470.
61. Mann, A. P.; Verma, A.; Sethi, G.; Manavathi, B.; Wang, H.; Fok, J. Y.; Kunnumakkara, A. B.; Kumar, R.; Aggarwal, B. B.; Mehta, K. Overexpression of tissue transglutaminase leads to constitutive activation of nuclear factor-{kappa}B in cancer cells: delineation of a novel pathway. Cancer Res. 2006, 66, 8788-8795.
62. Kim, D. S.; Park, S. S.; Nam, B. H.; Kim, I. H.; Kim, S. Y. Reversal of Drug Resistance in Breast Cancer Cells by Transglutaminase 2 Inhibition and Nuclear. Cancer Res. 2006, 66, 10936-10943.
63. Lee, J.; Kim, Y. S.; Choi, D. H.; Bang, M. S.; Han, T. R.; Joh, T. H.; Kim, S. Y. Transglutaminase 2 induces nuclear factor-κB activation via a novel pathway in BV-2 microglia. J. Biol. Chem. 2004, 279, 53725-53735.
64. Mishra, S.; Saleh, A.; Espino, P. S.; Davie, J. R.; Murphy, L. J. Phosphorylation of histones by tissue transglutaminase. J. Biol. Chem. 2006, 281, 5532-5538.
65. Mishra, S.; Murphy, L. J. The p53 oncoprotein is a substrate for tissue transglutaminase kinase activity. Biochem. Biophys. Res. Commun. 2006, 339, 726-730.
66. Bohuslav, J.; Chen, L. F.; Kwon, H.; Mu, Y.; Greene, W. C. p53 induces NF-κB activation by an IκB kinase-independent mechanism involving phosphorylation of p65 by ribosomal S6 kinase 1. J. Biol. Chem. 2004, 279, 26115-26125.
67. Douillette, A.; Bibeau-Poirier, A.; Gravel, S. P.; Clement, J. F.; Chenard, V.; Moreau, P.; Servant, M. J. The proinflammatory actions of angiotensin II are dependent on p65 phosphorylation by the IκB kinase complex. J. Biol. Chem. 2006, 281, 13275-13284.
68. Lavon, I.; Goldberg, I.; Amit, S.; Landsman, L.; Jung, S.; Tsuberi, B. Z.; Barshack, I.; Kopolovic, J.; Galun, E.; Bujard, H.; Ben-Neriah, Y. High susceptibility to bacterial infection, but no liver dysfunction, in mice compromised for hepatocyte NF-κB activation. Nat. Med. 2000, 6, 573-577.