Metabolism of citrate and other carboxylic acids in erythrocytes as a function of oxygen saturation and refrigerated storage

Frontiers in Medicine

Volumn 4, Issue OCT, 2017, Pages

  Nemkov, Travis ^a   Sun, Kaiqi ^b   Reisz, Julie A ^a   Yoshida, Tatsuro ^c   Dunham, Andrew ^c   Wen, Edward Y ^b,d   Wen, Alexander Q ^b   Roach, Rob C ^a   Hansen, Kirk C ^a   Xia, Yang ^b   D'Alessandro, Angelo ^a  

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

^b UNIVERSITY OF TEXAS   (United States)

^c New Health Sciences Inc   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Flux analysis; Hypoxia; Mass spectrometry; Metabolomics; Tracing experiments

Indexed keywords

EID: 85043467364     PISSN: None     EISSN: 2296858X     Source Type: Journal    
DOI: 10.3389/fmed.2017.00175     Document Type: Article

References (63)

1. Ellingson KD, Sapiano MRP, Haass KA, Savinkina AA, Baker ML, Chung K-W, et al. Continued decline in blood collection and transfusion in the United States-2015. Transfusion (2017) 57(Suppl 2):1588-98. doi:10.1111/trf.14165
2. Nemkov T, Hansen KC, Dumont LJ, D'Alessandro A. Metabolomics in transfusion medicine. Transfusion (2016) 56:980-93. doi:10.1111/trf.13442
3. Hess JR. An update on solutions for red cell storage. Vox Sang (2006) 91:13-9. doi:10.1111/j.1423-0410.2006.00778.x
4. Zimring JC. Widening our gaze of red blood storage haze: a role for metabolomics. Transfusion (2015) 55:1139-42. doi:10.1111/trf.13071
5. Hod EA, Zhang N, Sokol SA, Wojczyk BS, Francis RO, Ansaldi D, et al. Transfusion of red blood cells after prolonged storage produces harmful effects that are mediated by iron and inflammation. Blood (2010) 115:4284-92. doi:10.1182/blood-2009-10-245001
6. D'Alessandro A, Kriebardis AG, Rinalducci S, Antonelou MH, Hansen KC, Papassideri IS, et al. An update on red blood cell storage lesions, as gleaned through biochemistry and omics technologies. Transfusion (2015) 55:205-19. doi:10.1111/trf.12804
7. 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) 97:107-15. doi:10.3324/haematol.2011.051789
8. Harper VM, Oh JY, Stapley R, Marques MB, Wilson L, Barnes S, et al. Peroxiredoxin-2 recycling is inhibited during erythrocyte storage. Antioxid Redox Signal (2015) 22:294-307. doi:10.1089/ars.2014.5950
9. 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) 51:1439-49. doi:10.1111/j.1537-2995.2010.03032.x
10. Reisz JA, Wither MJ, Dzieciatkowska M, Nemkov T, Issaian A, Yoshida T, et al. Oxidative modifications of glyceraldehyde 3-phosphate dehydrogenase regulate metabolic reprogramming of stored red blood cells. Blood (2016) 128:e32-42. doi:10.1182/blood-2016-05-714816
11. Fu X, Felcyn JR, Zimring JC. Bioactive lipids are generated to micromolar levels during RBC storage, even in leukoreduced units. Blood (2015) 126:2344-2344
12. Silliman CC, Moore EE, Kelher MR, Khan SY, Gellar L, Elzi DJ. Identification of lipids that accumulate during the routine storage of prestorage leukoreduced red blood cells and cause acute lung injury. Transfusion (2011) 51:2549-54. doi:10.1111/j.1537-2995.2011.03186.x
13. D'Alessandro A, Nemkov T, Yoshida T, Bordbar A, Palsson BO, Hansen KC. Citrate metabolism in red blood cells stored in additive solution-3. Transfusion (2017) 57:325-36. doi:10.1111/trf.13892
14. Roback JD, Josephson CD, Waller EK, Newman JL, Karatela S, Uppal K, et al. Metabolomics of ADSOL (AS-1) red blood cell storage. Transfus Med Rev (2014) 28:41-55. doi:10.1016/j.tmrv.2014.01.003
15. Bordbar A, Johansson PI, Paglia G, Harrison SJ, Wichuk K, Magnusdottir M, et al. Identified metabolic signature for assessing red blood cell unit quality is associated with endothelial damage markers and clinical outcomes. Transfusion (2016) 56:852-62. doi:10.1111/trf.13460
16. Belpulsi D, Spitalnik SL, Hod EA. The controversy over the age of blood: what do the clinical trials really teach us? Blood Transfus (2017) 15:112-5. doi:10.2450/2017.0328-16
17. Kanias T, Gladwin MT. Nitric oxide, hemolysis, and the red blood cell storage lesion: interactions between transfusion, donor, and recipient. Transfusion (2012) 52:1388-92. doi:10.1111/j.1537-2995.2012.03748.x
18. Kanias T, Lanteri MC, Page GP, Guo Y, Endres SM, Stone M, et al. Ethnicity, sex, and age are determinants of red blood cell storage and stress hemolysis: results of the REDS-III RBC-Omics study. Blood Adv (2017) 1:1132-41. doi:10.1182/bloodadvances.2017004820
19. Tzounakas VL, Kriebardis AG, Georgatzakou HT, Foudoulaki-Paparizos LE, Dzieciatkowska M, Wither MJ, et al. Glucose 6-phosphate dehydrogenase deficient subjects may be better "storers" than donors of red blood cells. Free Radic Biol Med (2016) 96:152-65. doi:10.1016/j.freeradbiomed.2016.04.005
20. Tzounakas VL, Kriebardis AG, Papassideri IS, Antonelou MH. Donor-variation effect on red blood cell storage lesion: a close relationship emerges. Proteomics Clin Appl (2016) 10:791-804. doi:10.1002/prca.201500128
21. Weisenhorn EMM, van T Erve TJ, Riley NM, Hess JR, Raife TJ, Coon JJ. Multi-omics evidence for inheritance of energy pathways in red blood cells. Mol Cell Proteomics (2016) 15:3614-23. doi:10.1074/mcp.M116.062349
22. van't Erve TJ, Wagner BA, Martin SM, Knudson CM, Blendowski R, Keaton M, et al. The heritability of hemolysis in stored human red blood cells. Transfusion (2015) 55:1178-85. doi:10.1111/trf.12992
23. van't Erve TJ, Wagner BA, Martin SM, Knudson CM, Blendowski R, Keaton M, et al. The heritability of metabolite concentrations in stored human red blood cells. Transfusion (2014) 54:2055-63. doi:10.1111/trf.12605
24. de Wolski K, Fu X, Dumont LJ, Roback JD, Waterman H, Odem-Davis K, et al. Metabolic pathways that correlate with post-transfusion circulation of stored murine red blood cells. Haematologica (2016) 101:578-86. doi:10.3324/haematol.2015.139139
25. Zimring JC, Smith N, Stowell SR, Johnsen JM, Bell LN, Francis RO, et al. Strain-specific red blood cell storage, metabolism, and eicosanoid generation in a mouse model. Transfusion (2014) 54:137-48. doi:10.1111/trf.12264
26. Dumont LJ, AuBuchon JP. Evaluation of proposed FDA criteria for the evaluation of radiolabeled red cell recovery trials. Transfusion (2008) 48:1053-60. doi:10.1111/j.1537-2995.2008.01642.x
27. Yoshida T, Blair A, D'Alessandro A, Nemkov T, Dioguardi M, Silliman CC, et al. Enhancing uniformity and overall quality of red cell concentrate with anaerobic storage. Blood Transfus (2017) 15:172-81. doi:10.2450/2017.0325-16
28. D'Alessandro A, Nemkov T, Sun K, Liu H, Song A, Monte AA, et al. AltitudeOmics: red blood cell metabolic adaptation to high altitude hypoxia. J Proteome Res (2016) 15:3883-95. doi:10.1021/acs.jproteome.6b00733
29. Sun K, Zhang Y, D'Alessandro A, Nemkov T, Song A, Wu H, et al. Sphingosine-1-phosphate promotes erythrocyte glycolysis and oxygen release for adaptation to high-altitude hypoxia. Nat Commun (2016) 7:12086. doi:10.1038/ncomms12086
30. D'Alessandro A, Gevi F, Zolla L. Red blood cell metabolism under prolonged anaerobic storage. Mol Biosyst (2013) 9:1196-209. doi:10.1039/c3mb25575a
31. Prudent M, Stauber F, Rapin A, Hallen S, Pham N, Abonnenc M, et al. Small-scale perfusion bioreactor of red blood cells for dynamic studies of cellular pathways: proof-of-concept. Front Mol Biosci (2016) 3:11. doi:10.3389/fmolb.2016.00011
32. Kinoshita A, Tsukada K, Soga T, Hishiki T, Ueno Y, Nakayama Y, et al. Roles of hemoglobin allostery in hypoxia-induced metabolic alterations in erythrocytes: simulation and its verification by metabolome analysis. J Biol Chem (2007) 282:10731-41. doi:10.1074/jbc.M610717200
33. Yoshida T, Shevkoplyas SS. Anaerobic storage of red blood cells. Blood Transfus (2010) 8:220-36. doi:10.2450/2010.0022-10
34. Dumont LJ, D'Alessandro A, Szczepiorkowski ZM, Yoshida T. CO2-dependent metabolic modulation in red blood cells stored under anaerobic conditions. Transfusion (2016) 56:392-403. doi:10.1111/trf.13364
35. 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) 288:848-58. doi:10.1074/jbc.M112.428573
36. 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) 23:3159-70. doi:10.1096/fj.09-130666
37. Castagnola M, Messana I, Sanna MT, Giardina B. Oxygen-linked modulation of erythrocyte metabolism: state of the art. Blood Transfus (2010) 8:s53-8. doi:10.2450/2010.009S
38. de Korte D. New additive solutions for red cells. ISBT Sci Ser (2016) 11:165-70. doi:10.1111/voxs.12186
39. Hess JR, Hill HR, Oliver CK, Lippert LE, Greenwalt TJ. Alkaline CPD and the preservation of RBC 2,3-DPG. Transfusion (2002) 42:747-52. doi:10.1046/j.1537-2995.2002.00115.x
40. D'Alessandro A, Nemkov T, Hansen KC, Szczepiorkowski ZM, Dumont LJ. Red blood cell storage in additive solution-7 preserves energy and redox metabolism: a metabolomics approach. Transfusion (2015) 55:2955-66. doi:10.1111/trf.13253
41. D'Alessandro A, Gray AD, Szczepiorkowski ZM, Hansen K, Herschel LH, Dumont LJ. Red blood cell metabolic responses to refrigerated storage, rejuvenation, and frozen storage. Transfusion (2017) 57:1019-30. doi:10.1111/trf.14034
42. Goodman SR, Kurdia A, Ammann L, Kakhniashvili D, Daescu O. The human red blood cell proteome and interactome. Exp Biol Med (2007) 232:1391-408. doi:10.3181/0706-MR-156
43. Wilson MC, Trakarnsanga K, Heesom KJ, Cogan N, Green C, Toye AM, et al. Comparison of the proteome of adult and cord erythroid cells, and changes in the proteome following reticulocyte maturation. Mol Cell Proteomics (2016) 15:1938-46. doi:10.1074/mcp.M115.057315
44. D'Alessandro A, Dzieciatkowska M, Nemkov T, Hansen KC. Red blood cell proteomics update: is there more to discover? Blood Transfus (2017) 15:182-7. doi:10.2450/2017.0293-16
45. Rolfsson ó, Sigurjonsson óE, Magnusdottir M, Johannsson F, Paglia G, Gumundsson S, et al. Metabolomics comparison of red cells stored in four additive solutions reveals differences in citrate anticoagulant permeability and metabolism. Vox Sang (2017) 112:326-35. doi:10.1111/vox.12506
46. Bordbar A, Yurkovich JT, Paglia G, Rolfsson O, Sigurjónsson óE, Palsson BO. Elucidating dynamic metabolic physiology through network integration of quantitative time-course metabolomics. Sci Rep (2017) 7:46249. doi:10.1038/srep46249
47. Nemkov T, Hansen KC, D'Alessandro A. A three-minute method for high-throughput quantitative metabolomics and quantitative tracing experiments of central carbon and nitrogen pathways. Rapid Commun Mass Spectrom (2017) 31:663-73. doi:10.1002/rcm.7834
48. Melamud E, Vastag L, Rabinowitz JD. Metabolomic analysis and visualization engine for LC-MS data. Anal Chem (2010) 82:9818-26. doi:10.1021/ac1021166
49. Li M, Riddle S, Zhang H, D'Alessandro A, Flockton A, Serkova NJ, et al. Metabolic reprogramming regulates the proliferative and inflammatory phenotype of adventitial fibroblasts in pulmonary hypertension through the transcriptional co-repressor C-terminal binding protein-1. Circulation (2016) 134:1105-21. doi:10.1161/CIRCULATIONAHA.116.023171
50. Simpson RJ, Brindle KM, Campbell ID. Spin echo proton NMR studies of the metabolism of malate and fumarate in human erythrocytes. Biochim Biophys Acta (1982) 721:191-200. doi:10.1016/0167-4889(82)90068-4
51. Bordbar A, Jamshidi N, Palsson BO. iAB-RBC-283: a proteomically derived knowledge-base of erythrocyte metabolism that can be used to simulate its physiological and patho-physiological states. BMC Syst Biol (2011) 5:110. doi:10.1186/1752-0509-5-110
52. Paglia G, D'Alessandro A, Rolfsson ó, Sigurjónsson óE, Bordbar A, Palsson S, et al. Biomarkers defining the metabolic age of red blood cells during cold storage. Blood (2016) 128:e43-50. doi:10.1182/blood-2016-06-721688
53. Yurkovich JT, Yang L, Palsson BO. Biomarkers are used to predict quantitative metabolite concentration profiles in human red blood cells. PLoS Comput Biol (2017) 13:e1005424. doi:10.1371/journal.pcbi.1005424
54. Chouchani ET, Pell VR, Gaude E, Aksentijevic D, Sundier SY, Robb EL, et al. Ischaemic accumulation of succinate controls reperfusion injury through mitochondrial ROS. Nature (2014) 515:431-5. doi:10.1038/nature13909
55. D'Alessandro A, Moore HB, Moore EE, Reisz JA, Wither MJ, Ghasabyan A, et al. Plasma succinate is a predictor of mortality in critically injured patients. J Trauma Acute Care Surg (2017) 83:491-5. doi:10.1097/TA.0000000000001565
56. Tannahill GM, Curtis AM, Adamik J, Palsson-McDermott EM, McGettrick AF, Goel G, et al. Succinate is an inflammatory signal that induces IL-1β through HIF-1α. Nature (2013) 496:238-42. doi:10.1038/nature11986
57. Subudhi AW, Bourdillon N, Bucher J, Davis C, Elliott JE, Eutermoster M, et al. AltitudeOmics: the integrative physiology of human acclimatization to hypobaric hypoxia and its retention upon reascent. PLoS One (2014) 9:e92191. doi:10.1371/journal.pone.0092191
58. Casali E, Berni P, Spisni A, Baricchi R, Pertinhez TA. Hypoxanthine: a new paradigm to interpret the origin of transfusion toxicity. Blood Transfus (2015) 14:555-6. doi:10.2450/2015.0177-15
59. Liu H, Zhang Y, Wu H, D'Alessandro A, Yegutkin GG, Song A, et al. Beneficial role of erythrocyte adenosine A2B receptor-mediated AMP-activated protein kinase activation in high-altitude hypoxia. Circulation (2016) 134:405-21. doi:10.1161/CIRCULATIONAHA.116.021311
60. Jin M, Fuller GG, Han T, Yao Y, Alessi AF, Freeberg MA, et al. Glycolytic enzymes coalesce in G bodies under hypoxic stress. Cell Rep (2017) 20:895-908. doi:10.1016/j.celrep.2017.06.082
61. Pallotta V, Rinalducci S, Zolla L. Red blood cell storage affects the stability of cytosolic native protein complexes. Transfusion (2015) 55:1927-36. doi:10.1111/trf.13079
62. Huberts DHEW, van der Klei IJ. Moonlighting proteins: an intriguing mode of multitasking. Biochim Biophys Acta (2010) 1803:520-5. doi:10.1016/j.bbamcr.2010.01.022
63. Intlekofer AM, Dematteo RG, Venneti S, Finley LWS, Lu C, Judkins AR, et al. Hypoxia induces production of l-2-hydroxyglutarate. Cell Metab (2015) 22:304-11. doi:10.1016/j.cmet.2015.06.023