Glycation of glutamate cysteine ligase by 2-deoxy-d-ribose and its potential impact on chemoresistance in glioblastoma

Neurochemical Research

Volumn 38, Issue 9, 2013, Pages 1838-1849

  Backos, Donald S ^a   Fritz, Kristofer S ^a   McArthur, Debbie G ^a   Kepa, Jadwiga K ^a   Donson, Andrew M ^b   Petersen, Dennis R ^a   Foreman, Nicholas K ^b,c   Franklin, Christopher C ^a,c   Reigan, Philip ^a,c  

^a UNIVERSITY OF COLORADO   (United States)

^b Children's Hospital Colorado   (United States)

^c UNIVERSITY OF COLORADO CANCER CENTER   (United States)

Author keywords

2 Deoxyribose; Glioblastoma; Glutamate cysteine ligase; Glutathione; Glycation; Thymidine phosphorylase

Indexed keywords

2 DEOXYRIBOSE; ALDEHYDE; GLUTAMATE CYSTEINE LIGASE; SHORT HAIRPIN RNA; THYMIDINE; THYMIDINE PHOSPHORYLASE;

ARTICLE; CANCER RADIOTHERAPY; CANCER RESISTANCE; CELL DEATH; CELL MIGRATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME INHIBITION; ENZYME KINETICS; ENZYME SYNTHESIS; GLIOBLASTOMA; GLYCATION; HUMAN; HUMAN CELL; HUMAN TISSUE; LIPID PEROXIDATION; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; UPREGULATION;

BRAIN NEOPLASMS; CATALYSIS; CELL LINE, TUMOR; DEOXYRIBOSE; DRUG RESISTANCE, NEOPLASM; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GLIOBLASTOMA; GLUCOSE; GLUTAMATE-CYSTEINE LIGASE; HUMANS; KINETICS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 84881481439     PISSN: 03643190     EISSN: 15736903     Source Type: Journal    
DOI: 10.1007/s11064-013-1090-4     Document Type: Article

References (54)

1. Meloche J, Paulin R, Courboulin A, Lambert C, Barrier M, Bonnet P, Bisserier M, Roy M, Sussman MA, Agharazii M, Bonnet S (2011) RAGE-dependent activation of the oncoprotein Pim1 plays a critical role in systemic vascular remodeling processes. Arterioscler Thromb Vasc Biol 31(9):2114-2124. doi: 10.1161/ATVBAHA.111.230573
2. Sparvero LJ, Asafu-Adjei D, Kang R, Tang D, Amin N, Im J, Rutledge R, Lin B, Amoscato AA, Zeh HJ, Lotze MT (2009) RAGE (Receptor for Advanced Glycation Endproducts), RAGE ligands, and their role in cancer and inflammation. J Transl Med 7:17. doi: 10.1186/1479-5876-7-17
3. Singh R, Barden A, Mori T, Beilin L (2001) Advanced glycation end-products: a review. Diabetologia 44(2):129-146. doi: 10.1007/s001250051591
4. Goldin A, Beckman JA, Schmidt AM, Creager MA (2006) Advanced glycation end products: sparking the development of diabetic vascular injury. Circulation 114(6):597-605. doi: 10.1161/CIRCULATIONAHA.106.621854
5. Cho SJ, Roman G, Yeboah F, Konishi Y (2007) The road to advanced glycation end products: a mechanistic perspective. Curr Med Chem 14(15):1653-1671
6. Watkins NG, Thorpe SR, Baynes JW (1985) Glycation of amino groups in protein. Studies on the specificity of modification of RNase by glucose. J Biol Chem 260(19):10629-10636
7. Horiuchi S (1996) Advanced glycation end products (AGE)-modified proteins and their potential relevance to atherosclerosis. Trends Cardiovasc Med 6(5):163-168. doi: 10.1016/1050-1738(96)00050-3
8. Syrovy I (1994) Glycation of albumin: reaction with glucose, fructose, galactose, ribose or glyceraldehyde measured using four methods. J Biochem Biophys Methods 28(2):115-121
9. Khalifah RG, Todd P, Booth AA, Yang SX, Mott JD, Hudson BG (1996) Kinetics of nonenzymatic glycation of ribonuclease A leading to advanced glycation end products. Paradoxical inhibition by ribose leads to facile isolation of protein intermediate for rapid post-Amadori studies. Biochemistry 35(15):4645-4654. doi: 10.1021/bi9525942
10. Brown NS, Bicknell R (1998) Thymidine phosphorylase, 2-deoxy-d-ribose and angiogenesis. Biochem J 334(Pt 1):1-8
11. Brown NS, Jones A, Fujiyama C, Harris AL, Bicknell R (2000) Thymidine phosphorylase induces carcinoma cell oxidative stress and promotes secretion of angiogenic factors. Cancer Res 60(22):6298-6302
12. de Bruin M, Smid K, Laan AC, Noordhuis P, Fukushima M, Hoekman K, Pinedo HM, Peters GJ (2003) Rapid disappearance of deoxyribose-1-phosphate in platelet derived endothelial cell growth factor/thymidine phosphorylase overexpressing cells. Biochem Biophys Res Commun 301(3):675-679
13. Takino J, Yamagishi S, Takeuchi M (2012) Glycer-AGEs-RAGE signaling enhances the angiogenic potential of hepatocellular carcinoma by upregulating VEGF expression. World J Gastroenterol 18(15):1781-1788. doi: 10.3748/wjg.v18.i15.1781
14. Rojas A, Gonzalez I, Morales E, Perez-Castro R, Romero J, Figueroa H (2011) Diabetes and cancer: looking at the multiligand/RAGE axis. World J Diabetes 2(7):108-113. doi: 10.4239/wjd.v2.i7.108
15. Bijnsdorp IV, Capriotti F, Kruyt FA, Losekoot N, Fukushima M, Griffioen AW, Thijssen VL, Peters GJ (2011) Thymidine phosphorylase in cancer cells stimulates human endothelial cell migration and invasion by the secretion of angiogenic factors. Br J Cancer 104(7):1185-1192. doi: 10.1038/bjc.2011.74
16. Takebayashi Y, Yamada K, Miyadera K, Sumizawa T, Furukawa T, Kinoshita F, Aoki D, Okumura H, Yamada Y, Akiyama S, Aikou T (1996) The activity and expression of thymidine phosphorylase in human solid tumours. Eur J Cancer 32A(7):1227-1232
17. Hirano H, Tanioka K, Yokoyama S, Akiyama S, Kuratsu J (2001) Angiogenic effect of thymidine phosphorylase on macrophages in glioblastoma multiforme. J Neurosurg 95(1):89-95. doi: 10.3171/jns.2001.95.1.0089
18. Takano S, Tsuboi K, Matsumura A, Tomono Y, Mitsui Y, Nose T (2000) Expression of the angiogenic factor thymidine phosphorylase in human astrocytic tumors. J Cancer Res Clin Oncol 126(3):145-152
19. Tanioka K, Takeshima H, Hirano H, Kimura T, Nagata S, Akiyama S, Kuratsu J (2001) Biological role of thymidine phosphorylase in human astrocytic tumors. Oncol Rep 8(3):491-496
20. Yao Y, Kubota T, Sato K, Kitai R (2001) Macrophage infiltration- associated thymidine phosphorylase expression correlates with increased microvessel density and poor prognosis in astrocytic tumors. Clin Cancer Res 7(12):4021-4026
21. Noch E, Khalili K (2009) Molecular mechanisms of necrosis in glioblastoma: the role of glutamate excitotoxicity. Cancer Biol Ther 8(19):1791-1797
22. Raza SM, Fuller GN, Rhee CH, Huang S, Hess K, Zhang W, Sawaya R (2004) Identification of necrosis-associated genes in glioblastoma by cDNA microarray analysis. Clin Cancer Res 10(1 Pt 1):212-221
23. Miyadera K, Sumizawa T, Haraguchi M, Yoshida H, Konstanty W, Yamada Y, Akiyama S (1995) Role of thymidine phosphorylase activity in the angiogenic effect of platelet derived endothelial cell growth factor/thymidine phosphorylase. Cancer Res 55(8):1687-1690
24. Griffiths L, Stratford IJ (1997) Platelet-derived endothelial cell growth factor thymidine phosphorylase in tumour growth and response to therapy. Br J Cancer 76(6):689-693
25. Nakajima Y, Madhyastha R, Maruyama M (2009) 2-Deoxy-d-ribose, a downstream mediator of thymidine phosphorylase, regulates tumor angiogenesis and progression. Anticancer Agents Med Chem 9(2):239-245
26. Ikeda R, Furukawa T, Kitazono M, Ishitsuka K, Okumura H, Tani A, Sumizawa T, Haraguchi M, Komatsu M, Uchimiya H, Ren XQ, Motoya T, Yamada K, Akiyama S (2002) Molecular basis for the inhibition of hypoxia-induced apoptosis by 2-deoxy-d-ribose. Biochem Biophys Res Commun 291(4):806-812. doi: 10.1006/bbrc.2002.6432
27. Moghaddam A, Zhang HT, Fan TP, Hu DE, Lees VC, Turley H, Fox SB, Gatter KC, Harris AL, Bicknell R (1995) Thymidine phosphorylase is angiogenic and promotes tumor growth. Proc Natl Acad Sci USA 92(4):998-1002
28. Schmidt MM, Greb H, Koliwer-Brandl H, Kelm S, Dringen R (2010) 2-deoxyribose deprives cultured astrocytes of their glutathione. Neurochem Res 35(11):1848-1856. doi: 10.1007/s11064-010-0251-y
29. Fico A, Manganelli G, Cigliano L, Bergamo P, Abrescia P, Franceschi C, Martini G, Filosa S (2008) 2-deoxy-d-ribose induces apoptosis by inhibiting the synthesis and increasing the efflux of glutathione. Free Radic Biol Med 45(2):211-217. doi: 10.1016/j.freeradbiomed.2008.04.017
30. Ardestani A, Yazdanparast R, Nejad AS (2008) 2-Deoxy-d-ribose-induced oxidative stress causes apoptosis in human monocytic cells: prevention by pyridoxal-5′-phosphate. Toxicol In Vitro 22(4):968-979. doi: 10.1016/j.tiv.2008.02.010
31. Franklin CC, Backos DS, Mohar I, White CC, Forman HJ, Kavanagh TJ (2009) Structure, function, and post-translational regulation of the catalytic and modifier subunits of glutamate cysteine ligase. Mol Aspects Med 30(1-2):86-98
32. Ramamurthy B, Jones AD, Larsson L (2003) Glutathione reverses early effects of glycation on myosin function. Am J Physiol Cell Physiol 285(2):C419-C424. doi: 10.1152/ajpcell.00502.2002
33. Ajiboye R, Harding JJ (1989) The non-enzymic glycosylation of bovine lens proteins by glucosamine and its inhibition by aspirin, ibuprofen and glutathione. Exp Eye Res 49(1):31-41
34. Jain SK (1998) Glutathione and glucose-6-phosphate dehydrogenase deficiency can increase protein glycosylation. Free Radic Biol Med 24(1):197-201
35. Backos DS, Franklin CC, Reigan P (2012) The role of glutathione in brain tumor drug resistance. Biochem Pharmacol 83(8):1005-1012. doi: 10.1016/j.bcp.2011.11.016
36. Lu SC (2009) Regulation of glutathione synthesis. Mol Aspects Med 30(1-2):42-59
37. Griffith OW, Mulcahy RT (1999) The enzymes of glutathione synthesis: gamma-glutamylcysteine synthetase. Adv Enzymol Relat Areas Mol Biol 73:209-267
38. Yang Y, Chen Y, Johansson E, Schneider SN, Shertzer HG, Nebert DW, Dalton TP (2007) Interaction between the catalytic and modifier subunits of glutamate-cysteine ligase. Biochem Pharmacol 74(2):372-381. doi: 10.1016/j.bcp.2007.02.003
39. Tu Z, Anders MW (1998) Expression and characterization of human glutamate-cysteine ligase. Arch Biochem Biophys 354(2):247-254
40. Backos DS, Fritz KS, Roede JR, Petersen DR, Franklin CC (2011) Posttranslational modification and regulation of glutamate-cysteine ligase by the alpha, beta-unsaturated aldehyde 4-hydroxy-2-nonenal. Free Radic Biol Med 50(1):14-26. doi: 10.1016/j.freeradbiomed.2010.10.694c
41. Krzywanski DM, Dickinson DA, Iles KE, Wigley AF, Franklin CC, Liu RM, Kavanagh TJ, Forman HJ (2004) Variable regulation of glutamate cysteine ligase subunit proteins affects glutathione biosynthesis in response to oxidative stress. Arch Biochem Biophys 423(1):116-125
42. Backos DS, Brocker CN, Franklin CC (2010) Manipulation of cellular GSH biosynthetic capacity via TAT-mediated protein transduction of wild-type or a dominant-negative mutant of glutamate cysteine ligase alters cell sensitivity to oxidant-induced cytotoxicity. Toxicol Appl Pharmacol 243(1):35-45. doi: 10.1016/j.taap.2009.11.010
43. White CC, Viernes H, Krejsa CM, Botta D, Kavanagh TJ (2003) Fluorescence-based microtiter plate assay for glutamate-cysteine ligase activity. Anal Biochem 318(2):175-180
44. Munanairi A, O'Banion SK, Gamble R, Breuer E, Harris AW, Sandwick RK (2007) The multiple Maillard reactions of ribose and deoxyribose sugars and sugar phosphates. Carbohydr Res 342(17):2575-2592. doi: 10.1016/j.carres.2007. 08.003
45. Luers L, Rysiewski K, Dumpitak C, Birkmann E (2012) Kinetics of advanced glycation end products formation on bovine serum albumin with various reducing sugars and dicarbonyl compounds in equimolar ratios. Rejuvenation Res 15(2):201-205. doi: 10.1089/rej.2011.1284
46. Yoshida S, Yamada K, Hamaguchi K, Nishimura M, Hatakeyama E, Tsuchida H, Sakamoto K, Kashiwabara H, Yokoyama T, Ikeda K, Horiuchi S (1998) Immunohistochemical study of human advanced glycation end-products (AGE) and growth factors in cardiac tissues of patients on maintenance dialysis and with kidney transplantation. Clin Nephrol 49(5):273-280
47. Kohler BA, Ward E, McCarthy BJ, Schymura MJ, Ries LA, Eheman C, Jemal A, Anderson RN, Ajani UA, Edwards BK (2011) Annual report to the nation on the status of cancer, 1975-2007, featuring tumors of the brain and other nervous system. J Natl Cancer Inst 103(9):714-736. doi: 10.1093/jnci/djr077
48. Van Meir EG, Hadjipanayis CG, Norden AD, Shu HK, Wen PY, Olson JJ (2010) Exciting new advances in neuro-oncology: the avenue to a cure for malignant glioma. CA Cancer J Clin 60(3):166-193. doi: 10.3322/caac.20069
49. Kaur B, Khwaja FW, Severson EA, Matheny SL, Brat DJ, Van Meir EG (2005) Hypoxia and the hypoxia-inducible-factor pathway in glioma growth and angiogenesis. Neuro Oncol 7(2):134-153. doi: 10.1215/S1152851704001115
50. Januel C, Fay LB, Ruggiero D, Lagarde M, Vericel E (2003) Covalent coupling of reduced glutathione with ribose: loss of cosubstrate ability to glutathione peroxidase. Biochim Biophys Acta 1620(1-3):125-132
51. Linetsky MD, Shipova EV, Legrand RD, Argirov OO (2005) Glucose-derived Amadori compounds of glutathione. Biochim Biophys Acta 1724(1-2):181-193. doi: 10.1016/j.bbagen.2005.04.003
52. Krejsa CM, Franklin CC, White CC, Ledbetter JA, Schieven GL, Kavanagh TJ (2010) Rapid activation of glutamate cysteine ligase following oxidative stress. J Biol Chem 285(21):16116-16124. doi: 10.1074/jbc.M110.116210
53. Chang LS (1996) The functional involvement of Lys-38 in the heavy subunit of rat kidney gamma-glutamylcysteine synthetase: chemical modification and mutagenesis studies. J Protein Chem 15(3):321-326
54. Gamcsik MP, Kasibhatla MS, Teeter SD, Colvin OM (2012) Glutathione levels in human tumors. Biomarkers 17(8):671-691. doi: 10.3109/1354750X.2012.715672