Sidechain biology and the immunogenicity of PDC-E2, the major autoantigen of primary biliary cirrhosis

Hepatology

Volumn 40, Issue 6, 2004, Pages 1241-1248

  Mao, Tin K ^a   Davis, Paul A ^a   Odin, Joseph A ^b   Coppel, Ross L ^c   Gershwin, M Eric ^a,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c MONASH UNIVERSITY   (Australia)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL COENZYME A; AUTOANTIGEN; FATTY ACID; GLUTATHIONE; HEAT SHOCK PROTEIN 70; LYSINE; PEPTIDE; PYRUVATE DEHYDROGENASE COMPLEX; THIOCTIC ACID; XENOBIOTIC AGENT;

ACYLATION; APOPTOSIS; B LYMPHOCYTE; BIOCHEMISTRY; CELL LINE; CELL STRAIN CACO 2; DISEASE PREDISPOSITION; EPITHELIUM CELL; EPITOPE MAPPING; GENETIC TRANSFECTION; HUMAN; IMMUNE SYSTEM; IMMUNOGENICITY; IMMUNOREACTIVITY; LABORATORY; LEUKEMIA CELL LINE; LIVER MITOCHONDRION; PRIMARY BILIARY CIRRHOSIS; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN METABOLISM; RNA TRANSLATION; SALIVARY GLAND; SERUM; SHORT SURVEY; T LYMPHOCYTE; UBIQUITINATION;

AMINO ACID SEQUENCE; ANIMALS; AUTOANTIGENS; DIHYDROLIPOYLLYSINE-RESIDUE ACETYLTRANSFERASE; HUMANS; LIVER CIRRHOSIS, BILIARY; PYRUVATE DEHYDROGENASE COMPLEX;

EID: 10644262224     PISSN: 02709139     EISSN: None     Source Type: Journal    
DOI: 10.1002/hep.20491     Document Type: Short Survey

References (69)

1. Van de Water J, Cooper A, Surh CD, Coppel R, Danner D, Ansari A, et al. Detection of autoantibodies to recombinant mitochondrial proteins in patients with primary biliary cirrhosis. N Engl J Med 1989;320:1377-1380.
2. Mutimer DJ, Fussey SP, Yeaman SJ, Kelly PJ, James OF, Bassendine MF. Frequency of IgG and IgM autoantibodies to four specific M2 mitochondrial autoantigens in primary biliary cirrhosis. HEPATOLOGY 1989;10:403-407.
3. Milne JL, Shi D, Rosenthal PB, Sunshine JS, Domingo GJ, Wu X, et al. Molecular architecture and mechanism of an icosahedral pyruvate dehydrogenase complex: a multifunctional catalytic machine. EMBO J 2002; 21:5587-5598.
4. Pfanner N, Geissler A. Versatility of the mitochondrial protein import machinery. Nat Rev Mol Cell Biol 2001;2:339-349.
5. Da Silva LA, De Marcucci OL, Kuhnle ZR. Dietary polyunsaturated fats suppress the high-sucrose-induced increase of rat liver pyruvate dehydrogenase levels. Biochim Biophys Acta 1993;1169:126-134.
6. Amessou M, Fouque F, Soussi N, Desbuquois B, Hainaut I, Girard J, Benelli C. Longitudinal study of tissue- and subunit-specific obesity-induced regulation of the pyruvate dehydrogenase complex. Mol Cell Endocrinol 1998;144:139-147.
7. LeBlanc PJ, Peters SJ, Tunstall RJ, Cameron-Smith D, Heigenhauser GJ. Effects of aerobic training on pyruvate dehydrogenase and pyruvate dehydrogenase kinase in human skeletal muscle. J Physiol 2004;557:559-570.
8. Odin JA, Huebert RC, Casciola-Rosen L, LaRusso NF, Rosen A. Bcl-2-dependent oxidation of pyruvate dehydrogenase-E2, a primary biliary cirrhosis autoantigen, during apoptosis. J Clin Invest 2001;108:223-232.
9. Long SA, Quan C, Van de Water J, Nantz MH, Kurth MJ, Barsky D, et al. Immunoreactivity of organic mimeotopes of the E2 component of pyruvate dehydrogenase: connecting xenobiotics with primary biliary cirrhosis. J Immunol 2001;167:2956-2963.
10. Bruggraber SF, Leung PS, Amano K, Quan C, Kurth MJ, Nantz MH, et al. Autoreactivity to lipoate and a conjugated form of lipoate in primary biliary cirrhosis. Gastroenterology 2003;125:1705-1713.
11. Leung PS, Quan C, Park O, Van de Water J, Kurth MJ, Nantz MH, et al. Immunization with a xenobiotic 6-bromohexanoate bovine serum albumin conjugate induces antimitochondrial antibodies. J Immunol 2003; 170:5326-5332.
12. Amano K, Leung PS, Xu Q, Marik J, Quan C, Kurth MJ, et al. Xenobiotic-induced loss of tolerance in rabbits to the mitochondrial autoantigen of primary biliary cirrhosis is reversible. J Immunol 2004;172:6444-6452.
13. Gershwin ME, Mackay IR, Sturgess A, Coppel RL. Identification and specificity of a cDNA encoding the 70 kd mitochondrial antigen recognized in primary biliary cirrhosis. J Immunol 1987;138:3525-3531.
14. Coppel RL, McNeilage LJ, Surh CD, Van de Water J, Spithill TW, Whittingham S, et al. Primary structure of the human M2 mitochondrial autoantigen of primary biliary cirrhosis: dihydrolipoamide acetyltransferase. Proc Natl Acad Sci U S A 1988;85:7317-7321.
15. Fussey SP, Guest JR, James OF, Bassendine MF, Yeaman SJ. Identification and analysis of the major M2 autoantigens in primary biliary cirrhosis. Proc Natl Acad Sci USA 1988;85:8654-8658.
16. Van de Water J, Gershwin ME, Leung P, Ansari A, Coppel RL. The autoepitope of the 74-kD mitochondrial autoantigen of primary biliary cirrhosis corresponds to the functional site of dihydrolipoamide acetyltransferase. J Exp Med 1988;167:1791-1799.
17. Surh CD, Roche TE, Danner DJ, Ansari A, Coppel RL, Prindiville T, et al. Antimitochondrial autoantibodies in primary biliary cirrhosis recognize cross-reactive epitope(s) on protein X and dihydrolipoamide acetyltransferase of pyruvate dehydrogenase complex. HEPATOLOGY 1989;10:127-133.
18. Fregeau DR, Roche TE, Davis PA, Coppel R, Gershwin ME. Primary biliary cirrhosis. Inhibition of pyruvate dehydrogenase complex activity by autoantibodies specific for E1 alpha, a non-lipoic acid containing mitochondrial enzyme. J Immunol 1990;144:1671-1676.
19. Dubel L, Tanaka A, Leung PS, Van de Water J, Coppel R, Roche T, et al. Autoepitope mapping and reactivity of autoantibodies to the dihydrolipoamide dehydrogenase-binding protein (E3BP) and the glycine cleavage proteins in primary biliary cirrhosis. HEPATOLOGY 1999;29:1013-1018.
20. Perham RN. Domains, motifs, and linkers in 2-oxo acid dehydrogenase multienzyme complexes: a paradigm in the design of a multifunctional protein. Biochemistry 1991;30:8501-8512.
21. Rahmatullah M, Gopalakrishnan S, Radke GA, Roche TE. Domain structures of the dihydrolipoyl transacetylase and the protein X components of mammalian pyruvate dehydrogenase complex: selective cleavage by protease Arg C. J Biol Chem 1989;264:1245-1251.
22. Rahmatullah M, Gopalakrishnan S, Andrews PC, Chang CL, Radke GA, Roche TE. Subunit associations in the mammalian pyruvate dehydrogenase complex: structure and role of protein X and the pyruvate dehydrogenase component binding domain of the dihydrolipoyl transacetylase component. J Biol Chem 1989;264:2221-2227.
23. Neagle J, De Marcucci O, Dunbar B, Lindsay JG. Component X of mammalian pyruvate dehydrogenase complex: structural and functional relationship to the lipoate acetyltransferase (E2) component. FEBS Lett 1989; 253:11-15.
24. Sanderson SJ, Khan SS, McCartney RG, Miller C, Lindsay JG. Reconstitution of mammalian pyruvate dehydrogenase and 2-oxoglutarate dehydrogenase complexes: analysis of protein X involvement and interaction of homologous and heterologous dihydrolipoamide dehydrogenases. Biochem J 1996;319 (Pt 1):109-116.
25. Surh CD, Coppel R, Gershwin ME. Structural requirement for autoreactivity on human pyruvate dehydrogenase-E2, the major autoantigen of primary biliary cirrhosis: implication for a conformational autoepitope. J Immunol 1990;144:3367-3374.
26. Cha S, Leung PS, Coppel RL, Van de Water J, Ansari AA, Gershwin ME. Heterogeneity of combinatorial human autoantibodies against PDC-E2 and biliary epithelial cells in patients with primary biliary cirrhosis. HEPATOLOGY 1994;20:574-583.
27. Leung PS, Chuang DT, Wynn RM, Cha S, Danner DJ, Ansari A, et al. Autoantibodies to BCOADC-E2 in patients with primary biliary cirrhosis recognize a conformational epitope. HEPATOLOGY 1995;22:505-513.
28. Moteki S, Leung PS, Coppel RL, Dickson ER, Kaplan MM, Munoz S, et al. Use of a designer triple expression hybrid clone for three different lipoyl domain for the detection of antimitochondrial autoantibodies. HEPATOLOGY 1996;24:97-103.
29. Quinn J, Diamond AG, Palmer JM, Bassendine MF, James OF, Yeaman SJ. Lipoylated and unlipoylated domains of human PDC-E2 as autoantigens in primary biliary cirrhosis: significance of lipoate attachment. HEPATOLOGY 1993;18:1384-1391.
30. Shimoda S, Nakamura M, Ishibashi H, Hayashida K, Niho Y. HLA DRB4 0101-restricted immunodominant T cell autoepitope of pyruvate dehydrogenase complex in primary biliary cirrhosis: evidence of molecular mimicry in human autoimmune diseases. J Exp Med 1995;181:1835-1845.
31. Shimoda S, Van de Water J, Ansari A, Nakamura M, Ishibashi H, Coppel RL, et al. Identification and precursor frequency analysis of a common T cell epitope motif in mitochondrial autoantigens in primary biliary cirrhosis. J Clin Invest 1998;102:1831-1840.
32. Kita H, Lian ZX, Van de Water J, He XS, Matsumura S, Kaplan M, et al. Identification of HLA-A2-restricted CD8(+) cytotoxic T cell responses in primary biliary cirrhosis: T cell activation is augmented by immune complexes cross-presented by dendritic cells. J Exp Med 2002;195:113-123.
33. Pelfrey CM, Trotter JL, Tranquill LR, McFarland HF. Identification of a novel T cell epitope of human proteolipid protein (residues 40-60) recognized by proliferative and cytolytic CD4+ T cells from multiple sclerosis patients. J Neuroimmunol 1993;46:33-42.
34. Honma K, Parker KC, Becker KG, McFarland HF, Coligan JE, Biddison WE. Identification of an epitope derived from human proteolipid protein that can induce autoreactive CD8 + cytotoxic T lymphocytes restricted by HLA-A3: evidence for cross-reactivity with an environmental microorganism. J Neuroimmunol 1997;73:7-14.
35. Panina-Bordignon P, Lang R, van Enden PM, Benazzi E, Felix AM, Pastore RM, et al. Cytotoxic T cells specific for glutamic acid decarboxylase in autoimmune diabetes. J Exp Med 1995;181:1923-1927.
36. Wicker LS, Chen SL, Nepom GT, Elliott JF, Freed DC, Bansal A, et al. Naturally processed T cell epitopes from human glutamic acid decarboxylase identified using mice transgenic for the type 1 diabetes-associated human MHC class II allele, DRB1*0401. J Clin Invest 1996;98:2597-2603.
37. Ackerman AL, Cresswell P. Cellular mechanisms governing cross-presentation of exogenous antigens. Nat Immunol 2004;5:678-684.
38. Morikawa T, Yasuno R, Wada H. Do mammalian cells synthesize lipoic acid? Identification of a mouse cDNA encoding a lipoic acid synthase located in mitochondria. FEBS Lett 2001;498:16-21.
39. Zhao X, Miller JR, Jiang Y, Marietta MA, Cronan JE. Assembly of the covalent linkage between lipoic acid and its cognate enzymes. Chem Biol 2003;10:1293-1302.
40. Prasad PD, Wang H, Kekuda R, Fujita T, Fei YJ, Devoe LD, et al. Cloning and functional expression of a cDNA encoding a mammalian sodium-dependent vitamin transporter mediating the uptake of pantothenate, biotin, and lipoate. J Biol Chem 1998;273:7501-7506.
41. Tsunoda JN, Yasunobu KT. Mammalian lipoic acid activating enzyme. Arch Biochem Biophys 1967;118:395-401.
42. Fujiwara K, Okamura-Ikeda K, Motokawa Y. Purification and characterization of lipoyl-AMP:N epsilon-lysine lipoyltransferase from bovine liver mitochondria. J Biol Chem 1994;269:16605-16609.
43. Fujiwara K, Okamura-Ikeda K, Motokawa Y. Lipoylation of acyltransferase components of alpha-ketoacid dehydrogenase complexes. J Biol Chem 1996;271:12932-12936.
44. Fujiwara K, Takeuchi S, Okamura-Ikeda K, Motokawa Y. Purification, characterization, and cDNA cloning of lipoate-activating enzyme from bovine liver. J Biol Chem 2001;276:28819-28823.
45. Aas M. Organ and subcellular distribution of fatty acid activating enzymes in the rat. Biochim Biophys Acta 1971;231:32-47.
46. Killenberg PG, Davidson ED, Webster LT, Jr. Evidence for a medium-chain fatty acid: coenzyme A ligase (adenosine monophosphate) that activates salicylate. Mol Pharmacol 1971;7:260-268.
47. Groot PH, Scholte HR, Hulsmann WC. Fatty acid activation: specificity, localization, and function. Adv Lipid Res 1976;14:75-126.
48. Vessey DA, Hu J. Isolation from bovine liver mitochondria and characterization of three distinct carboxylic acid: CoA ligases with activity toward xenobiotics. J Biochem Toxicol 1995;10:329-337.
49. Vessey DA. Comprehensive Toxicology. Oxford, England: Eiservier Science, 1997:455-475.
50. Vessey DA, Kelley M, Warren RS. Characterization of the CoA ligases of human liver mitochondria catalyzing the activation of short- and medium-chain fatty acids and xenobiotic carboxylic acids. Biochim Biophys Acta 1999;1428:455-462.
51. Vessey DA, Lau E, Kelley M, Warren RS. Isolation, sequencing, and expression of a cDNA for the HXM-A form of xenobiotic/medium-chain fatty acid:CoA ligase from human liver mitochondria. J Biochem Mol Toxicol 2003;17:1-6.
52. Fussey SP, Ali ST, Guest JR, James OF, Bassendine MF, Yeaman SJ. Reactivity of primary biliary cirrhosis sera with Escherichia coli dihydrolipoamide acetyltransferase (E2p): characterization of the main immunogenic region. Proc Natl Acad Sci U S A 1990;87:3987-3991.
53. Pickart CM. Mechanisms underlying ubiquitination. Annu Rev Biochem 2001;70:503-533.
54. Ballinger CA, Connell P, Wu Y, Hu Z, Thompson LJ, Yin LY, et al. Identification of CHIP, a novel tetratricopeptide repeat-containing protein that interacts with heat shock proteins and negatively regulates chaperone functions. Mol Cell Biol 1999;19:4535-4545.
55. McClellan AJ, Frydman J. Molecular chaperones and the art of recognizing a lost cause. Nat Cell Biol 2001;3:E51-E53.
56. Connell P, Ballinger CA, Jiang J, Wu Y, Thompson LJ, Hohfeld J, et al. The co-chaperone CHIP regulates protein triage decisions mediated by heat-shock proteins. Nat Cell Biol 2001;3:93-96.
57. Meacham GC, Patterson C, Zhang W, Younger JM, Cyr DM. The Hsc70 co-chaperone CHIP targets immature CFTR for proteasomal degradation. Nat Cell Biol 2001;3:100-105.
58. Koegl M, Hoppe T, Schlenker S, Ulrich HD, Mayer TU, Jentsch S. A novel ubiquitination factor, E4, is involved in multiubiquitin chain assembly. Cell 1999;96:635-644.
59. Mendel-Hartvig I, Nelson BD, Loof L, Totterman TH. Primary biliary cirrhosis: further biochemical and immunological characterization of mitochondrial antigens. Clin Exp Immunol 1985;62:371-379.
60. Tyurin VA, Tyurina YY, Quinn PJ, Schor NF, Balachandran R, Day BW, et al. Glutamate-induced cytotoxicity in P12 pheochromocytoma cells: role of oxidation of phospholipids, glutathione and protein sulfhydryls revealed by bcl-2 transfection. Brain Res Mol Brain Res 1998;60:270-281.
61. Celli A, Que FG, Gores GJ, LaRusso NF. Glutathione depletion is associated with decreased Bcl-2 expression and increased apoptosis in cholangiocytes. Am J Physiol 1998;275:G749-G757.
62. Charlotte F, L'Hermine A, Martin N, Geleyn Y, Nollet M, Gaulard P, et al. Immunohistochemical detection of bcl-2 protein in normal and pathological human liver. Am J Pathol 1994;144:460-465.
63. Nakopoulou L, Stefanaki K, Vourlakou C, Manolaki N, Gakiopoulou H, Michalopoulos G. Bcl-2 protein expression in acute and chronic hepatitis, cirrhosis and hepatocellular carcinoma. Pathol Res Pract 1999;195:19-24.
64. Que FG, Gores GJ, LaRusso NF. Development and initial application of an in vitro model of apoptosis in rodent cholangiocytes. Am J Physiol 1997;272:G106-115.
65. Schafer FQ, Buettner GR. Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic Biol Med 2001;30:1191-1212.
66. Grant CM. Role of the glutathione/glutaredoxin and thioredoxin systems in yeast growth and response to stress conditions. Mol Microbiol 2001;39: 533-541.
67. Domingo GJ, Orru S, Perham RN. Multiple display of peptides and proteins on a macromolecular scaffold derived from a multienzyme complex. J Mol Biol 2001;305:259-267.
68. Casagrande S, Bonetto V, Fratelli M, Gianazza E, Eberini I, Massignan T, et al. Glutathionylation of human thioredoxin: a possible crosstalk between the glutathione and thioredoxin systems. Proc Natl Acad Sci USA 2002; 99:9745-9749.
69. Fratelli M, Demol H, Puype M, Casagrande S, Villa P, Eberini I, et al. Identification of proteins undergoing glutathionylation in oxidatively stressed hepatocytes and hepatoma cells. Proteomics 2003;3:1154-1161.