Oxidative modifications of glyceraldehyde 3-phosphate dehydrogenase regulate metabolic reprogramming of stored red blood cells

Blood

Volumn 128, Issue 12, 2016, Pages e32-e42

  Reisz, Julie A ^a   Wither, Matthew J ^a   Dzieciatkowska, Monika ^a   Nemkov, Travis ^a   Issaian, Aaron ^a   Yoshida, Tatsuro ^b   Dunham, Andrew J ^b   Hill, Ryan C ^a   Hansen, Kirk C ^a   D'Alessandro, Angelo ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b New Health Sciences Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HYDROGEN PEROXIDE; LACTIC ACID; THIOL; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE (NADP); REACTIVE OXYGEN METABOLITE;

ARTICLE; CELL HYPOXIA; CELL METABOLISM; CONTROLLED STUDY; ERYTHROCYTE CONCENTRATE; ERYTHROCYTE PRESERVATION; EX VIVO STUDY; GLYCOLYSIS; HUMAN; HUMAN CELL; HYPEROXIA; LIQUID CHROMATOGRAPHY-MASS SPECTROMETRY; MEMBRANE BINDING; METABOLIC FLUX ANALYSIS; NUCLEAR REPROGRAMMING; OXIDATION; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PENTOSE PHOSPHATE CYCLE; PRIORITY JOURNAL; PROTEOMICS; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY; BLOOD STORAGE; CHEMISTRY; ERYTHROCYTE; METABOLISM; METABOLOMICS; TANDEM MASS SPECTROMETRY;

BLOOD PRESERVATION; ERYTHROCYTES; GLUCOSE; GLYCERALDEHYDE 3-PHOSPHATE DEHYDROGENASE (NADP+); GLYCOLYSIS; HUMANS; METABOLOMICS; OXIDATION-REDUCTION; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; TANDEM MASS SPECTROMETRY;

EID: 85015612019     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2016-05-714816     Document Type: Article

References (61)

1. Ralser M, Wamelink MM, Kowald A, et al. Dynamic rerouting of the carbohydrate flux is key to counteracting oxidative stress. J Biol. 2007; 6(4):10.
2. Jeong J, Jung Y, Na S, et al. Novel oxidative modifications in redox-active cysteine residues. Mol Cell Proteomics. 2011;10(3): M110.000513.
3. Boradia VM, Raje M, Raje CI. Protein moonlighting in iron metabolism: glyceraldehyde- 3-phosphate dehydrogenase (GAPDH). Biochem Soc Trans. 2014;42(6):1796-1801.
4. Seo J, Jeong J, Kim YM, Hwang N, Paek E, Lee KJ. Strategy for comprehensive identification of post-translational modifications in cellular proteins, including low abundant modifications: application to glyceraldehyde-3-phosphate dehydrogenase. J Proteome Res. 2008;7(2): 587-602.
5. D'Alessandro A, Kriebardis AG, Rinalducci S, et al. An update on red blood cell storage lesions, as gleaned through biochemistry and omics technologies. Transfusion. 2015;55(1):205-219.
6. Nemkov T, Hansen KC, Dumont LJ, D'Alessandro A. Metabolomics in transfusion medicine. Transfusion. 2016;56(4):980-993.
7. Puchulu-Campanella E, Chu H, Anstee DJ, Galan JA, Tao WA, Low PS. Identification of the components of a glycolytic enzyme metabolon on the human red blood cell membrane. J Biol Chem. 2013;288(2):848-858.
8. Messana I, Ferroni L, Misiti F, et al. Blood bank conditions and RBCs: the progressive loss of metabolic modulation. Transfusion. 2000;40(3): 353-360.
9. D'Alessandro A, Nemkov T, Kelher M, et al. Routine storage of red blood cell (RBC) units in additive solution-3: a comprehensive investigation of the RBC metabolome. Transfusion. 2015;55(6): 1155-1168.
10. D'Amici GM, Mirasole C, D'Alessandro A, Yoshida T, Dumont LJ, Zolla L. Red blood cell storage in SAGM and AS3: a comparison through the membrane two-dimensional electrophoresis proteome. Blood Transfus. 2012;10(suppl 2): s46-s54.
11. Sparrow RL. Time to revisit red blood cell additive solutions and storage conditions: a role for "omics" analyses. Blood Transfus. 2012;10(suppl 2): s7-s11.
12. Bianchi M, Vaglio S, Pupella S, et al. Leucoreduction of blood components: an effective way to increase blood safety? Blood Transfus. 2016;14(2):214-227.
13. D'alessandro A. Leucoreduction of blood components: clinical and molecular evidence. Blood Transfus. 2016;14(2):212-213.
14. Gevi F, D'Alessandro A, Rinalducci S, Zolla L. Alterations of red blood cell metabolome during cold liquid storage of erythrocyte concentrates in CPD-SAGM. J Proteomics. 2012;76(Spec No): 168-180.
15. Rinalducci S, Marrocco C, Zolla L. Thiol-based regulation of glyceraldehyde-3-phosphate dehydrogenase in blood bank-stored red blood cells: a strategy to counteract oxidative stress. Transfusion. 2015;55(3):499-506.
16. Dandekar T, Fieselmann A, Majeed S, Ahmed Z. Software applications toward quantitative metabolic flux analysis and modeling. Brief Bioinform. 2014;15(1):91-107.
17. D'Alessandro A, Dzieciatkowska M, Hill RC, Hansen KC. Supernatant protein biomarkers of red blood cell storage hemolysis as determined through an absolute quantification proteomics technology. Transfusion. 2016;56(6):1329-1339.
18. Chouchani ET, James AM, Fearnley IM, Lilley KS, Murphy MP. Proteomic approaches to the characterization of protein thiol modification. Curr Opin Chem Biol. 2011;15(1):120-128.
19. Clasquin MF, Melamud E, Rabinowitz JD. LC-MS data processing with MAVEN: a metabolomic analysis and visualization engine. Curr Protoc Bioinformatics. 2012;Chapter 14:Unit14.11.
20. Nemkov T, D'Alessandro A, Hansen KC. Threeminute method for amino acid analysis by UHPLC and high-resolution quadrupole orbitrap mass spectrometry. Amino Acids. 2015;47(11): 2345-2357.
21. Dzieciatkowska M, Hill R, Hansen KC. GeLC-MS/MS analysis of complex protein mixtures. Methods Mol Biol. 2014;1156:53-66.
22. Dzieciatkowska M, D'Alessandro A, Hill RC, Hansen KC. Plasma QconCATs reveal a genderspecific proteomic signature in apheresis platelet plasma supernatants. J Proteomics. 2015;120: 1-6.
23. Eisenmesser EZ, Post CB. Insights into tyrosine phosphorylation control of protein-protein association from the NMR structure of a band 3 peptide inhibitor bound to glyceraldehyde-3- phosphate dehydrogenase. Biochemistry. 1998; 37(3):867-877.
24. Yoshida T, AuBuchon JP, Tryzelaar L, Foster KY, Bitensky MW. Extended storage of red blood cells under anaerobic conditions. Vox Sang. 2007; 92(1):22-31.
25. Bachi A, Dalle-Donne I, Scaloni A. Redox proteomics: chemical principles, methodological approaches and biological/biomedical promises. Chem Rev. 2013;113(1):596-698.
26. Wither M, Dzieciatkowska M, Nemkov T, Strop P, D'Alessandro A, Hansen KC. Hemoglobin oxidation at functional amino acid residues during routine storage of red blood cells. Transfusion. 2016;56(2):421-426.
27. Hess JR. An update on solutions for red cell storage. Vox Sang. 2006;91(1):13-19.
28. Dhabangi A, Ainomugisha B, Cserti-Gazdewich C, et al. Effect of transfusion of red blood cells with longer vs shorter storage duration on elevated blood lactate levels in children with severe anemia: The TOTAL Randomized Clinical Trial. JAMA. 2015;314(23):2514-2523.
29. Lacroix J, Hébert PC, Fergusson DA, et al; ABLE Investigators; Canadian Critical Care Trials Group. Age of transfused blood in critically ill adults. N Engl J Med. 2015;372(15):1410-1418.
30. Steiner ME, Ness PM, Assmann SF, et al. Effects of red-cell storage duration on patients undergoing cardiac surgery. N Engl J Med. 2015;372(15):1419-1429.
31. Heddle NM, Arnold DM, Acker JP, et al. Red blood cell processing methods and in-hospital mortality: a transfusion registry cohort study. Lancet Haematol. 2016;3(5):e246-e254.
32. Spitalnik SL, Triulzi D, Devine DV, et al; State of the Science in Transfusion Medicine Working Groups. 2015 proceedings of the National Heart, Lung, and Blood Institute's State of the Science in Transfusion Medicine symposium. Transfusion. 2015;55(9):2282-2290.
33. de Korte D. New additive solutions for red cells. ISBT Sci Ser. 2016;11:165-170.
34. Delobel J, Prudent M, Tissot J-D, Lion N. Proteomics of the red blood cell carbonylome during blood banking of erythrocyte concentrates. Proteomics Clin Appl. 2016;10(3):257-266.
35. Kriebardis AG, Antonelou MH, Stamoulis KE, Economou-Petersen E, Margaritis LH, Papassideri IS. Progressive oxidation of cytoskeletal proteins and accumulation of denatured hemoglobin in stored red cells. J Cell Mol Med. 2007;11(1):148-155.
36. D'Alessandro A, D'Amici GM, Vaglio S, Zolla L. Time-course investigation of SAGM-stored leukocyte-filtered red bood cell concentrates: from metabolism to proteomics. Haematologica. 2012; 97(1):107-115.
37. Pratt JM, Simpson DM, Doherty MK, Rivers J, Gaskell SJ, Beynon RJ. Multiplexed absolute quantification for proteomics using concatenated signature peptides encoded by QconCAT genes. Nat Protoc. 2006;1(2):1029-1043.
38. Bayer SB, Hampton MB, Winterbourn CC. Accumulation of oxidized peroxiredoxin 2 in red blood cells and its prevention. Transfusion. 2015; 55(8):1909-1918.
39. Rinalducci S, D'Amici GM, Blasi B, Vaglio S, Grazzini G, Zolla L. Peroxiredoxin-2 as a candidate biomarker to test oxidative stress levels of stored red blood cells under blood bank conditions. Transfusion. 2011;51(7):1439-1449.
40. Willekens FL, Werre JM, Groenen-Döpp YA, Roerdinkholder-Stoelwinder B, de Pauw B, Bosman GJ. Erythrocyte vesiculation: a selfprotective mechanism? Br J Haematol. 2008; 141(4):549-556.
41. Antonelou MH, Kriebardis AG, Papassideri IS. Aging and death signalling in mature red cells: from basic science to transfusion practice. Blood Transfus. 2010;8(suppl 3):s39-s47.
42. Rubin O, Crettaz D, Tissot J-D, Lion N. Microparticles in stored red blood cells: submicron clotting bombs? Blood Transfus. 2010;8(suppl 3):s31-s38.
43. Sirover MA. New insights into an old protein: the functional diversity of mammalian glyceraldehyde- 3-phosphate dehydrogenase. Biochim Biophys Acta. 1999;1432(2):159-184.
44. Pallotta V, Rinalducci S, Zolla L. Red blood cell storage affects the stability of cytosolic native protein complexes. Transfusion. 2015;55(8):1927-1936.
45. Sirover MA. On the functional diversity of glyceraldehyde-3-phosphate dehydrogenase: biochemical mechanisms and regulatory control. Biochim Biophys Acta. 2011;1810(8):741-751.
46. Tristan C, Shahani N, Sedlak TW, Sawa A. The diverse functions of GAPDH: views from different subcellular compartments. Cell Signal. 2011; 23(2):317-323.
47. Yang H-Y, Lee T-H. Antioxidant enzymes as redox-based biomarkers: a brief review. BMB Rep. 2015;48(4):200-208.
48. Antonelou MH, Tzounakas VL, Velentzas AD, Stamoulis KE, Kriebardis AG, Papassideri IS. Effects of pre-storage leukoreduction on stored red blood cells signaling: a time-course evaluation from shape to proteome. J Proteomics. 2012; 76(Spec No):220-238.
49. Rogers SC, Said A, Corcuera D, McLaughlin D, Kell P, Doctor A. Hypoxia limits antioxidant capacity in red blood cells by altering glycolytic pathway dominance. FASEB J. 2009;23(9): 3159-3170.
50. Harper VM, Oh JY, Stapley R, et al. Peroxiredoxin-2 recycling is inhibited during erythrocyte storage. Antioxid Redox Signal. 2015;22(4):294-307.
51. D'Alessandro A, Gevi F, Zolla L. Red blood cell metabolism under prolonged anaerobic storage. Mol Biosyst. 2013;9(6):1196-1209.
52. Longo V, D'alessandro A, Zolla L. Deoxygenation of leucofiltered erythrocyte concentrates preserves proteome stability during storage in the blood bank. Blood Transfus. 2014;12(4):599-604.
53. Zolla L, D'Alessandro A. An efficient apparatus for rapid deoxygenation of erythrocyte concentrates for alternative banking strategies. J Blood Transfus. 2013;2013:896537.
54. Francis RO, Jhang J, Hendrickson JE, Zimring JC, Hod EA, Spitalnik SL. Frequency of glucose- 6-phosphate dehydrogenase-deficient red blood cell units in a metropolitan transfusion service. Transfusion. 2013;53(3):606-611.
55. Peters AL, van Bruggen R, de Korte D, Van Noorden CJF, Vlaar APJ. Glucose-6-phosphate dehydrogenase activity decreases during storage of leukoreduced red blood cells. Transfusion. 2016;56(2):427-432.
56. Tzounakas VL, Kriebardis AG, Georgatzakou HT, et al. Glucose 6-phosphate dehydrogenase deficient subjects may be better "storers" than donors of red blood cells. Free Radic Biol Med. 2016;96:152-165.
57. Buescher JM, Antoniewicz MR, Boros LG, et al. A roadmap for interpreting (13)C metabolite labeling patterns from cells. Curr Opin Biotechnol. 2015; 34:189-201.
58. Wu L, Mashego MR, van Dam JC, et al. Quantitative analysis of the microbial metabolome by isotope dilution mass spectrometry using uniformly 13C-labeled cell extracts as internal standards. Anal Biochem. 2005;336(2):164-171.
59. Polati R, Castagna A, Bossi AM, et al. Murine macrophages response to iron. J Proteomics. 2012;76(Spec No):10-27.
60. Hod EA, Spitalnik SL. Stored red blood cell transfusions: iron, inflammation, immunity, and infection. Transfus Clin Biol. 2012;19(3):84-89.
61. Queiroz RF, Lima ES. Oxidative stress in sickle cell disease. Rev Bras Hematol Hemoter. 2013; 35(1):16-17.