Thiol/redox metabolomic profiling implicates GSH dysregulation in early experimental Graft versus Host Disease (GVHD)

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Suh, Jung H ^a   Kanathezhath, Bindu ^b   Shenvi, Swapna ^a   Guo, Hua ^b   Zhou, Alicia ^a   Tiwana, Anureet ^a   Kuypers, Frans ^a   Ames, Bruce N ^a   Walters, Mark C ^b  

^a CHILDREN S HOSPITAL OAKLAND RESEARCH INSTITUTE   (United States)

^b CHILDREN S HOSPITAL OAKLAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ALANINE; BRANCHED CHAIN AMINO ACID; CYSTATHIONINE; CYSTEINE; CYSTEINYLGLYCINE; GLUTAMATE CYSTEINE LIGASE; GLUTATHIONE; GLUTATHIONE DISULFIDE; LIVER PROTEIN; REACTIVE OXYGEN METABOLITE; THIOL DERIVATIVE; TUMOR NECROSIS FACTOR ALPHA; AMINO ACID; ANTIOXIDANT;

ALLOGENIC BONE MARROW TRANSPLANTATION; AMINO ACID BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; ENZYME DEFECT; EXPERIMENTAL MODEL; FEMALE; GLUTATHIONE METABOLISM; GRAFT RECIPIENT; GRAFT VERSUS HOST REACTION; ISOGRAFT; LIVER INJURY; METABOLOMICS; MOUSE; NONHUMAN; OXIDATION; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PATHOGENESIS; PRINCIPAL COMPONENT ANALYSIS; PROTEIN BLOOD LEVEL; REAL TIME POLYMERASE CHAIN REACTION; ALLOTRANSPLANTATION; ANIMAL; BIOSYNTHESIS; BLOOD; LIVER; METABOLISM; OXIDATION REDUCTION REACTION; UPREGULATION;

AMINO ACIDS; ANIMALS; ANTIOXIDANTS; FEMALE; GLUTAMATE-CYSTEINE LIGASE; GLUTATHIONE; GRAFT VS HOST DISEASE; LIVER; METABOLOMICS; MICE; OXIDATION-REDUCTION; SULFHYDRYL COMPOUNDS; TRANSPLANTATION, HOMOLOGOUS; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION;

EID: 84895879554     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0088868     Document Type: Article

References (63)

1. Ferrara JL, Levine JE, Reddy P, Holler E (2009) Graft-versus-host disease. The Lancet 373: 1550-1561. doi:10.1016/S0140-6736(09)60237-3.
2. Blazar BR, Murphy WJ, Abedi M (2012) Advances in graft-versus-host disease biology and therapy. Nat Med 12: 443-458. doi:10.1038/nri3212.
3. Abhyankar S, Gilliland DG, Ferrara JL (1993) Interleukin-1 is a critical effector molecule during cytokine dysregulation in graft versus host disease to minor histocompatibility antigens. Transplantation 56: 1518-1523. (Pubitemid 24018815)
4. Shin HJ, Baker J, Leveson-Gower DB, Smith AT, Sega EI, et al. (2011) Rapamycin and IL-2 reduce lethal acute graft-versus-host disease associated with increased expansion of donor type CD4+CD25+Foxp3+ regulatory T cells. Blood 118: 2342-2350. doi:10.1182/blood-2010-10-313684.
5. Paczesny S, Krijanovski OI, Braun TM, Choi SW, Clouthier SG, et al. (2009) A biomarker panel for acute graft-versus-host disease. Blood 113: 273-278. doi:10.1182/blood-2008-07-167098.
6. Maeda Y, Levy RB, Reddy P, Liu C, Clouthier SG, et al. (2005) Both perforin and Fas ligand are required for the regulation of alloreactive CD8+ T cells during acute graft-versus-host disease. Blood 105: 2023-2027. doi:10.1182/blood-2004-08-3036. (Pubitemid 40731787)
7. Jonas CR, Puckett AB, Jones DP, Griffith DP, Szeszycki EE, et al. (2000) Plasma antioxidant status after high-dose chemotherapy: a randomized trial of parenteral nutrition in bone marrow transplantation patients. Am J Clin Nutr 72:181-189. Available: http://www.google.com/search?client=safari&rls=10-7- 4&q= Plasma+antioxidant+status+after+high+dose+chemotherapy+a+randomized+trial+of+ parenteral+nutrition+in+bone+marrow+transplantation+patients&ie= UTF-8&oe=UTF-8.
8. Lu SG, Konmaz BS,Eetinkaya DC, Scedil H (2011) Evaluation of oxidative and antioxidative parameters in pediatric hematopoietic SCT patients. 47: 651-656. doi:10.1038/bmt.2011.145.
9. Evens AM, Mehta J, Gordon L (2004) Rust and corrosion in hematopoietic stem cell transplantation: the problem of iron and oxidative stress. Nat Med 34: 561-571. doi:10.1038/sj.bmt.1704591. (Pubitemid 39341534)
10. Pullarkat V, Blanchard S, Tegtmeier B, Dagis A, Patane K, et al. (2008) Iron overload adversely affects outcome of allogeneic hematopoietic cell transplantation. Bone Marrow Transplant 42: 799-805. doi:10.1038/bmt.2008.262.
11. Vodanovic-Jankovic S (2006) NF- B as a target for the prevention of graft-versus-host disease: comparative efficacy of bortezomib and PS-1145. Blood 107: 827-834. doi:10.1182/blood-2005-05-1820.
12. Blackwell TS, Christman JW, Hagan T, Price P, Edens T, et al. (2000) Oxidative Stress and NF-κ B Activation: Correlation in Patients Following Allogeneic Bone Marrow Transplantation. Antioxid Redox Signal 2: 93-102. (Pubitemid 30202458)
13. Weiss G, Schwaighofer H, Herold M, Nachbaur D, Wachter H, et al. (1995) Nitric Oxide Formation As Predictive Parameter for Acute Graft-Versus-Host Disease After Human Allogeneic Bone Marrow Transplantation. Transplantation 60: 1239.
14. Vora A, Monaghan J, Nuttall P, Crowther D (1997) Cytokine-mediated nitric oxide release-a common cytotoxic pathway in host-versus-graft and graft-versus-host reactions? Bone Marrow Transplant 20: 385-389. doi:10.1038/sj.bmt.1700898. (Pubitemid 27390412)
15. Yang S, Porter VA, Cornfield DN, Milla C, Panoskaltsis-Mortari A, et al. (2001) Effects of oxidant stress on inflammation and survival of iNOS knockout mice after marrow transplantation. Am J Physiol Lung Cell Mol Physiol 281: L922-L930.
16. Ellison CA, Natuik SA, McIntosh AR, Scully SA, Danilenko DM, et al. (2003) The role of interferon-gamma, nitric oxide and lipopolysaccharide in intestinal graft-versus-host disease developing in F1-hybrid mice. Immunology 109: 440-449. (Pubitemid 36783271)
17. Gatza E, Wahl DR, Opipari AW, Sundberg TB, Reddy P, et al. (2011) Manipulating the bioenergetics of alloreactive T cells causes their selective apoptosis and arrests graft versus host disease. Science Translational Medicine 3: 67ra8.
18. Themeli M, Petrikkos L, Waterhouse M, Bertz H, Lagadinou E, et al. (2010) Alloreactive microenvironment after human hematopoietic cell transplantation induces genomic alterations in epithelium through an ROS-mediated mechanism: in vivo and in vitro study and implications to secondary neoplasia. Leukemia 24: 536-543. doi:10.1038/leu.2009.284.
19. Brosnan JT, Brosnan ME (2006) The sulfur-containing amino acids: an overview. J Nutr 136: 1636S-1640S. (Pubitemid 43765374)
20. Jones DP (2006) Redefining oxidative stress. Antioxid Redox Signal 8: 1865-1879. doi:10.1089/ars.2006.8.1865.
21. Maccarrone M, Brüne B (2009) Redox regulation in acute and chronic inflammation. Nat Med 16: 1184-1186. doi:10.1038/cdd.2009.65.
22. Iyer SS, Jones DP, Brigham KL, Rojas M (2008) Oxidation of Plasma Cysteine/Cystine Redox State in Endotoxin-Induced Lung Injury. American Journal of Respiratory Cell and Molecular Biology 40: 90-98. doi:10.1165/rcmb.2007- 0447OC.
23. Iyer SS, Torres-Gonzalez E, Neujahr DC, Kwon M, Brigham KL, et al. (2010) Effect of Bone Marrow-Derived Mesenchymal Stem Cells on Endotoxin-Induced Oxidation of Plasma Cysteine and Glutathione in Mice. Stem Cells International 2010: 1-9. doi:10.1182/blood-2008-09-176198.
24. Moriarty-Craige SE, Jones DP (2004) Extracellular Thiols and Thiol/Disulfide Redox in metabolism. Annu Rev Nutr 24: 481-509. doi:10.1146/annurev.-nutr.24.012003.132208. (Pubitemid 38938801)
25. Melissa D Shelton JJM (2008) Regulation by Reversible S-Glutathionylation: Molecular Targets Implicated in Inflammatory Diseases. Molecules and Cells 25: 332.
26. Dalle Donne I, Milzani A, Gagliano N, Colombo R, Giustarini D, et al. (2008) Molecular Mechanisms and Potential Clinical Significance of S-Glutathionylation. Antioxid Redox Signal 10: 445-474. doi:10.1089/ars.2007. 1716.
27. Ziegler TR, Panoskaltsus-Mortari A, Gu LH, Jonas CR, Farrell CL, et al. (2001) Regulation of glutathione redox status in lung and liver by conditioning regimens and keratinocyte growth factor in murine allogeneic bone marrow transplantation. Transplantation 72: 1354-1362. (Pubitemid 33015758)
28. Amer J, Weiss L, Reich S, Shapira MY, Slavin S, et al. (2007) The oxidative status of blood cells in a murine model of graft-versus-host disease. Annals of Hematology 86: 753-758. Available: http://link.springer.com/article/ 10.1007/s00277-007-0321-7/fulltext.html.
29. Suh JH, Kim R, Yavuz B, Lee D, Lal A, et al. (2009) Clinical assay of four thiol amino acid redox couples by LC-MS/MS: utility in thalassemia. J Chromatogr B Analyt Technol Biomed Life Sci 877: 3418-3427. doi:10.1016/j. jchromb.2009.06.041.
30. Suh JH, Kim RY, Lee DS (2012) A new metabolomic assay to examine inflammation and redox pathways following LPS challenge. J Inflamm (Lond) 9: 37. doi:10.1186/1476-9255-9-37.
31. Carta S, Castellani P, Delfino L, Tassi S, Vene R, et al. (2009) DAMPs and inflammatory processes: the role of redox in the different outcomes. Journal of Leukocyte Biology 86: 549-555. doi:10.1189/jlb.1008598.
32. Go Y-M, Jones DP (2011) Cysteine/cystine redox signaling in cardiovascular disease. Free Radic Biol Med 50: 495-509. doi:10.1016/j. freeradbiomed.2010.11.029.
33. Grimble RF (2006) The effects of sulfur amino acid intake on immune function in humans. J Nutr 136: 1660S-1665S.
34. Yan Z, Garg SK, Kipnis J, Banerjee R (2009) Extracellular redox modulation by regulatory T cells. Nat Meth 5: 721-723. doi:10.1038/nchembio.212.
35. Kuypers FA, WATSON G, SAGE E, WALTERS MC, HAMRICK J, et al. (2005) Stem Cell Transplantation with S-59 Photochemically Treated T-Cell Add-Backs to Establish Allochimerism in Murine Thalassemia. Ann N Y Acad Sci 1054: 214-222. doi:10.1196/annals.1345.026.
36. Kanathezhath B, Mizokami M, Stanislaus S, Hounshell C, Neumayr L, et al. (2011) Improved engraftment with minimal graft-versus-host disease after major histocompatibility complex-mismatched cord blood transplantation with photochemically treated donor lymphocytes. Experimental Biology and Medicine 236: 492-504. doi:10.1258/ebm.2011.010216.
37. Hill GR, Crawford JM, Cooke KR, Brinson YS, Pan L, et al. (1997) Total body irradiation and acute graft-versus-host disease: the role of gastrointestinal damage and inflammatory cytokines. Blood 90: 3204-3213. (Pubitemid 27444217)
38. Xia J, Wishart DS (2002) Current Protocols in Bioinformatics. Baxevanis AD, Petsko GA, Stein LD, Stormo GD, editors Hoboken, NJ, USA: John Wiley &Sons, Inc. doi:10.1002/0471250953.bi1410s34.
39. Deneke SM, Fanburg BL (1989) Regulation of cellular glutathione. Am J Physiol 257: L163-L173.
40. Tschetter JR, Mozes E, Shearer GM (2000) Progression from acute to chronic disease in a murine parent-into-F1 model of graft-versus-host disease. J Immunol 165: 5987-5994.
41. Sprangers B, Van Wijmeersch B, Luyckx A, Sagaert X, Verbinnen B, et al. (2010) Subclinical GvHD in non-irradiated F1 hybrids: severe lymphoid-tissue GvHD causing prolonged immune dysfunction. Nat Med 46: 586-596. doi:10.1038/bmt.2010.162.
42. Szymańska E, Saccenti E, Smilde AK, Westerhuis JA (2012) Double-check: validation of diagnostic statistics for PLS-DA models in metabolomics studies. Metabolomics 8: 3-16. doi:10.1007/s11306-011-0330-3.
43. Landfried K, Zhu W, Waldhier MC, Schulz U, Ammer J, et al. (2012) IDO in Human Gut Graft-versus-Host Disease. Biology of Blood and Marrow Transplantation 18: 150-155. doi:10.1016/j.bbmt.2011.08.002.
44. Sari I, Cetin A, Kaynar L, Saraymen R, Hacioglu SK, et al. (2008) Disturbance of pro-oxidative/antioxidative balance in allogeneic peripheral blood stem cell transplantation. Ann Clin Lab Sci 38: 120-125. (Pubitemid 351671393)
45. Adams JD, Lauterburg BH, Mitchell JR (1983) Plasma glutathione and glutathione disulfide in the rat: regulation and response to oxidative stress. J Pharmacol Exp Ther 227: 749-754. (Pubitemid 14215063)
46. Ookhtens M, Hobdy K, Corvasce MC, Aw TY, Kaplowitz N (1985) Sinusoidal efflux of glutathione in the perfused rat liver. Evidence for a carrier-mediated process. J Clin Invest 75: 258-265. doi:10.1172/JCI111682. (Pubitemid 15163992)
47. Sies H, Akerboom TP (1984) Glutathione disulfide (GSSG) efflux from cells and tissues. Meth Enzymol 105: 445-451. (Pubitemid 14165410)
48. Brechbuhl HM, Gould N, Kachadourian R, Riekhof WR, Voelker DR, et al. (2010) Glutathione Transport Is a Unique Function of the ATP-binding Cassette Protein ABCG2. Journal of Biological Chemistry 285: 16582-16587. doi:10.1074/jbc.M109.090506.
49. Franco R, Cidlowski JA (2012) Glutathione Efflux and Cell Death. Antioxid Redox Signal 17: 1694-1713. doi:10.1089/ars.2012.4553.
50. Morgan B, Ezeriņa D, Amoako TNE, Riemer J, Seedorf M, et al. (2012) Multiple glutathione disulfide removal pathways mediate cytosolic redox homeostasis. Nat Chem Biol 9: 119-125. doi:10.1038/nchembio.1142.
51. Beilhack A, Schulz S, Baker J, Beilhack GF, Wieland CB, et al. (2005) In vivo analyses of early events in acute graft-versus-host disease reveal sequential infiltration of T-cell subsets. Blood 106: 1113-1122. doi:10.1182/blood-2005-02-0509. (Pubitemid 41076462)
52. Bubici C, Papa S, Dean K, Franzoso G (2006) Mutual cross-talk between reactive oxygen species and nuclear factor-kappa B: molecular basis and biological significance. Oncogene 25: 6731-6748. doi:10.1038/sj.onc.1209936. (Pubitemid 44657849)
53. Flohé L, Brigelius-Flohé R, Saliou C, Traber MG, Packer L (1997) Redox Regulation of NF-kappa B Activation. Free Radic Biol Med 22: 1115-1126. doi:10.1016/S0891-5849(96)00501-1. (Pubitemid 27084148)
54. Anderson MT, Staal FJ, Gitler C, Herzenberg LA, Herzenberg LA (1994) Separation of oxidant-initiated and redox-regulated steps in the NF-kappa B signal transduction pathway. Proc Natl Acad Sci USA 91: 11527-11531. (Pubitemid 24356377)
55. Tephly LA, Carter AB (2007) Differential Expression and Oxidation of MKP-1 Modulates TNF-α Gene Expression. American Journal of Respiratory Cell and Molecular Biology 37: 366-374. doi:10.1165/rcmb.2006-0268OC. (Pubitemid 350067616)
56. Jung Y, Kim H, Min SH, Rhee SG, Jeong W (2008) Dynein light chain LC8 negatively regulates NF-kappaB through the redox-dependent interaction with IkappaBalpha. J Biol Chem 283: 23863-23871. doi:10.1074/jbc.M803072200.
57. Hoppe G, Talcott KE, Bhattacharya SK, Crabb JW, Sears JE (2006) Molecular basis for the redox control of nuclear transport of the structural chromatin protein Hmgb1. Exp Cel l Res 312: 3526-3538. doi:10.1016/j.yexcr.2006.07.020. (Pubitemid 44470773)
58. Ullala AJ, Pisetskyb DS (2009) Post-Translational Modification of HMGB1 and Its Role in Immune Activation. The Epigenetics of Autoimmune Diseases: 165-178. Available: http://www.worldcat.org/title/epigenetics-of-autoimmune- diseases/oclc/352840058.
59. Schlegel PG, Vaysburd M, Chen Y, Butcher EC, Chao NJ (1995) Inhibition of T cell costimulation by VCAM-1 prevents murine graft-versus-host disease across minor histocompatibility barriers. J Immunol 155: 3856-3865.
60. Liu S-Y, Tsai M-Y, Chuang K-P, Huang Y-F, Shieh C-C (2008) Ligand binding of leukocyte integrin very late antigen-4 involves exposure of sulfhydryl groups and is subject to redox modulation. Eur J Immunol 38: 410-423. doi:10.1002/eji.200737556.
61. Mukherjee TK, Mishra AK, Mukhopadhyay S, Hoidal JR (2007) High concentration of antioxidants N-acetylcysteine and mitoquinone-Q induces intercellular adhesion molecule 1 and oxidative stress by increasing intracellular glutathione. J Immunol 178: 1835-1844. (Pubitemid 46154656)
62. Karlsson H, Nava S, Remberger M, Hassan Z, Hassan M, et al. (2011) N-acetyl-L-cysteine increases acute graft-versus-host disease and promotes T-cell-mediated immunity in vitro. Eur J Immunol 41: 1143-1153. doi:10.1002/eji.201040589.
63. Barkholt L, Remberger M, Hassan Z, Fransson K, Omazic B, et al. (2008) A prospective randomized study using N-acetyl-L-cysteine for early liver toxicity after allogeneic hematopoietic stem cell transplantation. Bone Marrow Transplant 41: 785-790. doi:10.1038/sj.bmt.1705969. (Pubitemid 351696342)