Transglutaminase 2 reprogramming of glucose metabolism in mammary epithelial cells via activation of inflammatory signaling pathways

International Journal of Cancer

Volumn 134, Issue 12, 2014, Pages 2798-2807

  Kumar, Santosh ^a   Donti, Taraka R ^b   Agnihotri, Navneet ^a   Mehta, Kapil ^a  

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

^b Department of Molecular and Human Genetics ^*  (United States)

Author keywords

drug resistance; EMT; HIF 1 ; metabolism; metastasis; NF B

Indexed keywords

GLUCOSE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LACTIC ACID; OXYGEN; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 2; SYNAPTOTAGMIN I; TRANSCRIPTION FACTOR RELA;

ARTICLE; BREAST EPITHELIUM; BREAST METASTASIS; CONTROLLED STUDY; ENERGY METABOLISM; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; GLYCOLYSIS; HUMAN; HUMAN CELL; INFLAMMATION; METABOLIC REGULATION; MITOCHONDRIAL RESPIRATION; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; WARBURG EFFECT;

DRUG RESISTANCE; EMT; HIF-1Α; METABOLISM; METASTASIS; NF-ΚB;

BREAST NEOPLASMS; CELL LINE, TUMOR; CELL RESPIRATION; DOWN-REGULATION; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GLUCOSE; GLYCOLYSIS; GTP-BINDING PROTEINS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INFLAMMATION; LACTIC ACID; MAMMARY GLANDS, HUMAN; MCF-7 CELLS; MITOCHONDRIA; OXYGEN; PROMOTER REGIONS, GENETIC; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR RELA; TRANSGLUTAMINASES; UP-REGULATION;

EID: 84898011885     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.28623     Document Type: Article

References (47)

1. Warburg O,. On respiratory impairment in cancer cells. Science 1956; 124: 269-70.
2. Hanahan D, Weinberg RA,. Hallmarks of cancer: the next generation. Cell 2011; 144: 646-74.
3. Iyer NV, Kotch LE, Agani F, et al. Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1 alpha. Genes Dev 1998; 12: 149-62.
4. Denko NC,. Hypoxia, HIF1 and glucose metabolism in the solid tumor. Nat Rev Cancer 2008; 8: 705-13.
5. Ferreira LM, Hebrant A, Dumont JE,. Metabolic reprogramming of the tumor. Oncogene 2012; 31: 3999-4011.
6. Bardos JI, Ashcroft M,. Hypoxia-inducible factor-1 and oncogenic signaling. Bioessays 2004; 26: 262-69.
7. Gottlieb E, Tomlinson IP,. Mitochondrial tumour suppressors: a genetic and biochemical update. Nat Rev Cancer 2005; 5: 857-66.
8. Chen C, Pore N, Ismail-Behrooz F, et al. Regulation of glut1 mRNA by hypoxia-inducible factor-1. Interaction between H-ras and hypoxia. J Biol Chem 2001; 276: 9519-25.
9. Mathupala SP, Rempel A, Pedersen PL,. Glucose catabolism in cancer cells: identification and characterization of a marked activation response of the type II hexokinase gene to hypoxic conditions. J Biol Chem 2001; 276: 43407-12.
10. Firth JD, Ebert BL, Ratcliffe PJ,. Hypoxic regulation of lactate dehydrogenase A. Interaction between hypoxia-inducible factor 1 and cAMP response elements. J Biol Chem 1995; 270: 21021-27.
11. Papandreou I, Cairns RA, Fontana L, et al. HIF-1 mediates adaptation to hypoxia by actively downregulating mitochondrial oxygen consumption. Cell Metab 2006; 3: 187-97.
12. Zhang H, Gao P, Fukuda R, et al. HIF-1 inhibits mitochondrial biogenesis and cellular respiration in VHL-deficient renal cell carcinoma by repression of C-MYC activity. Cancer Cell 2007; 11: 407-20.
13. Kumar S, Mehta K,. Tissue transglutaminase constitutively activates HIF-1α promoter and nuclear factor-κB via a non-canonical pathway. PLoS One 2012; 7: e49321.
14. Kumar A, Xu J, Brady S, et al. Tissue transglutaminase promotes drug resistance and invasion by inducing mesenchymal transition in mammary epithelial cells. PLoS One 2010; 15: e13390.
15. Hassanein M, Weidow B, Koehler E, et al. Development of high-throughput quantitative assays for glucose uptake in cancer cell lines. Mol Imaging Biol 2011; 13: 840-52.
16. Price ND, Trent J, El-Naggar AK, et al. Highly accurate two-gene classifier for differentiating gastrointestinal stromal tumors and leiomyosarcomas. Proc Natl Acad Sci USA 2007; 104: 3414-19.
17. Wang P, Henning SM, Heber D,. Limitations of MTT and MTS-based assays for measurement of antiproliferative activity of green tea polyphenols. PLoS One 2010; 5: e10202.
18. Forsythe JA, Jiang BH, Iyer NV, et al. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 1996; 16: 4604-13.
19. Malmgren S, Nicholls DG, Taneera J, et al. Tight coupling between glucose and mitochondrial metabolism in clonal beta-cells is required for robust insulin secretion. J Biol Chem 2009; 284: 32395-404.
20. Nicholls DG, Darley-Usmar VM, Wu M, et al. Bioenergetic profile experiment using C2C12 myoblast cells. J Vis Exp 2010; 46: e2511.
21. Gaillies RJ, Robey I, Gatenby RA,. Causes and consequences of increased glucose metabolism of cancers. J Nucl Med 2008; 49: 24s-42s.
22. Lum JJ, Bui T, Gruber M, et al. The transcription factor HIF-1alpha plays a critical role in the growth factor-dependent regulation of both aerobic and anaerobic glycolysis. Genes Dev 2007; 21: 1037-49.
23. Macheda ML, Rogers S, Best JD,. Molecular and cellular regulation of glucose transporter (GLUT) proteins in cancer. J Cell Physiol 2005; 202: 654-62.
24. Pedersen PL, Mathupala S, Rempel A, et al. Mitochondrial bound type II hexokinase: a key player in the growth and survival of many cancers and an ideal prospect for therapeutic intervention. Biochim Biophys Acta 2002; 1555: 14-20.
25. Bauer DE, Hatzivassiliou G, Zhao F, et al. ATP citrate lyase is an important component of cell growth and transformation. Oncogene 2005; 24: 6314-22.
26. Kim DS, Park SS, Nam BH, et al. Reversal of drug resistance in breast cancer cells by transglutaminase 2 inhibition and nuclear factor-kappaB inactivation. Cancer Res 2006; 66: 10936-43.
27. Mann AP, Verma A, Sethi G, et al. Overexpression of tissue transglutaminase leads to constitutive activation of nuclear factor-kappaB in cancer cells: delineation of a novel pathway. Cancer Res 2006; 66: 8788-95.
28. Brown KD,. Transglutaminase 2 and NF-êB: an odd couple that shapes breast cancer phenotype. Breast Cancer Res Treat 2013; 137: 329-36.
29. Mehta K, Kumar A, Kim HI,. Transglutaminase 2: a multi-tasking protein in the complex circuitry of inflammation and cancer. Biochem Pharmacol 2010; 80: 1921-29.
30. Karin M,. Nuclear factor-kB in cancer development and progression. Nature 2006; 441: 431-36.
31. Agnihotri N, Kumar S, Mehta K,. Tissue transglutaminase as a central mediator in inflammation-induced progression of cancer. Breast Cancer Res 2013; 15: 202.
32. Herman JF, Mangala LS, Mehta K,. Implications of increased tissue transglutaminase (TG2) expression in drug-resistant breast cancer (MCF-7) cells. Oncogene 2006; 25: 3049-58.
33. Mangala LS, Fok JY, Zorrilla-Calancha IR, et al. Tissue transglutaminase expression promotes cell attachment, invasion and survival in breast cancer cells. Oncogene 2007; 26: 2459-70.
34. Ai L, Kim WJ, Demircan B, et al. The transglutaminase 2 gene (TGM2), a potential molecular marker for chemotherapeutic drug sensitivity, is epigenetically silenced in breast cancer. Carcinogenesis 2008; 29: 510-8.
35. Cao L, Shao M, Schilder J, et al. Tissue transglutaminase links TGF-β, epithelial to mesenchymal transition and a stem cell phenotype in ovarian cancer. Oncogene 2012; 31: 2521-34.
36. Kumar A, Gao H, Xu J, et al. Evidence that aberrant expression of tissue transglutaminase promotes stem cell characteristics in mammary epithelial cells. PLoS One 2011; 6: e20701.
37. Hwang JY, Mangala LS, Fok JY, et al. Clinical and biological significance of tissue transglutaminase in ovarian carcinoma. Cancer Res 2008; 68: 5849-58.
38. Verma A, Guha S, Diagaradjane P, et al. Therapeutic significance of elevated tissue transglutaminase expression in pancreatic cancer. Clin Cancer Res 2008; 14: 2476-83.
39. Oh K, Ko E, Kim HS, et al. Transglutaminase 2 facilitates the distant hematogenous metastasis of breast cancer by modulating interleukin-6 in cancer cells. Breast Cancer Res 2011; 13: R96.
40. Gilmore TD, Herscovitch M,. Inhibitors of NF-kappaB signaling: 785 and counting. Oncogene 2006; 25: 6887-99.
41. Wilson WR, Hay MP,. Targeting hypoxia in cancer therapy. Nat Rev Cancer 2011; 11: 393-410.
42. Bonello S, Zähringer C, BelAiba RS, et al. Reactive oxygen species activate the HIF-1alpha promoter via a functional NFkappaB site. Arterioscler Thromb Vasc Biol 2007; 27: 755-61.
43. Thiery JP, Sleeman JP,. Complex networks orchestrate epithelial- mesenchymal transitions. Nat Rev Mol Cell Biol 2006; 7: 131-42.
44. Voulgari A, Pintzas A,. Epithelial-mesenchymal transition in cancer metastasis: mechanisms, markers andstrategies to overcome drug resistance in the clinic. Biochim Biophys Acta 2009; 1796: 75-90.
45. Mastroberardino PG, Piacentini M,. Type 2 transglutaminase in Huntington's disease: a double-edged sword with clinical potential. J Intern Med 2010; 268: 419-31.
46. Cooper AJ, Sheu KR, Burke JR, et al. Transglutaminase-catalyzed inactivation of glyceraldehyde 3-phosphate dehydrogenase and alpha-ketoglutaratedehydrogenase complex by polyglutamine domains of pathological length. Proc Natl Acad Sci USA 1997; 94: 12604-109.
47. Kim SY, Marekov L, Bubber P, et al. Mitochondrial aconitase is a transglutaminase 2 substrate: transglutamination is a probable mechanism contributing to high-molecular-weight aggregates of aconitase and loss of aconitase activity in Huntington disease brain. Neurochem Res 2005; 30: 1245-55.