Flavin redox switching of protein functions

Antioxidants and Redox Signaling

Volumn 14, Issue 6, 2011, Pages 1079-1091

  Becker, Donald F ^a   Zhu, Weidong ^a   Moxley, Michael A ^a  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FLAVOPROTEIN; FUNGAL PROTEIN; PROTEIN NIFL; PROTEIN PUTA; PROTEIN VIVID; PYRUVATE OXIDASE; QUERCETIN; REGULATOR PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

CRYSTAL STRUCTURE; NITROGEN FIXATION; NONHUMAN; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE; REGULATORY MECHANISM; REVIEW; RNA TRANSLATION;

BACTERIAL PROTEINS; FLAVINS; FLAVOPROTEINS; FUNGAL PROTEINS; MEMBRANE PROTEINS; OXIDATION-REDUCTION; PROTEIN STRUCTURE, SECONDARY; PYRUVATE OXIDASE;

EID: 79951871588     PISSN: 15230864     EISSN: None     Source Type: Journal    
DOI: 10.1089/ars.2010.3417     Document Type: Review

References (91)

1. Abdel-Hamid AM, Attwood MM, and Guest JR. Pyruvate oxidase contributes to the aerobic growth efficiency of Escherichia coli. Microbiology 147: 1483-1498, 2001. (Pubitemid 32544813)
2. Abrahamson JLA, Baker LG, Stephenson JT, and Wood JM. Proline dehydrogenase from Escherichia K12, properties of the membrane-associated enzyme. Eur J Biochem 134: 77-82, 1983.
3. Anderson S, Dragnea V, Masuda S, Ybe J, Moffat K, and Bauer C. Structure of a novel photoreceptor, the BLUF domain of AppA from Rhodobacter sphaeroides. Biochemistry 44: 7998-8005, 2005. (Pubitemid 40776660)
4. Avila- Perez M, Vreede J, Tang YF, Bende O, Losi A, Gartner W, and Hellingwerf K. In vivo mutational analysis of YtvA from Bacillus subtilis. Mechanism of light activation of the general stress response. J Biol Chem 284: 24958-24964, 2009.
5. Becker DF and Thomas EA. Redox properties of the PutA protein from Escherichia coli and the influence of the flavin redox state on PutA-DNA interactions. Biochemistry 40: 4714-4722, 2001.
6. Bertagnolli BL and Hager LP. Activation of Escherichia coli pyruvate oxidase enhances the oxidation of hydroxyethylthiamin pyrophosphate. J Biol Chem 266: 10168-10173, 1991. (Pubitemid 21906783)
7. Brown E and Wood JM. Redesigned purification yields a fully functional PutA protein dimer from Escherichia coli. J Biol Chem 267: 13086-13092, 1992.
8. Brown ED and Wood JM. Conformational change and membrane association of the PutA protein are coincident with reduction of its FAD cofactor by proline. J Biol Chem 268: 8972-8979, 1993. (Pubitemid 23118692)
9. Brunner M and Kaldi K. Interlocked feedback loops of the circadian clock of Neurospora crassa. Mol Microbiol 68: 255-262, 2008. (Pubitemid 351422954)
10. Carter K and Gennis RB. Reconstitution of the ubiquinone-dependent pyruvate oxidase system of Escherichia coli with the cytochrome o terminal oxidase complex. J Biol Chem 260: 10986-10990, 1985. (Pubitemid 16253253)
11. Chang YY, Wang AY, and Cronan JE, Jr. Expression of Escherichia coli pyruvate oxidase (PoxB) depends on the sigma factor encoded by the rpoS (katF) gene. Mol Microbiol 11: 1019-1028, 1994.
12. Churbanova IY and Sevrioukova IF. Redox-dependent changes in molecular properties of mitochondrial apoptosis-inducing factor. J Biol Chem 283: 5622-5631, 2008.
13. Crosson S, Rajagopal S, and Moffat K. The LOV domain family: Photoresponsive signaling modules coupled to diverse output domains. Biochemistry 42: 2-10, 2003. (Pubitemid 36083846)
14. Cunningham CC and Hager LP. Crystalline pyruvate oxidase from Escherichia coli. 3. Phospholipid as an allosteric effector for the enzyme. J Biol Chem 246: 1583-1589, 1971.
15. Demarsy E and Fankhauser C. Higher plants use LOV to perceive blue light. Curr Opin Plant Biol 12: 69-74, 2009.
16. Dunlap JC and Loros JJ. How fungi keep time: Circadian system in Neurospora and other fungi. Curr Opin Microbiol 9: 579-587, 2006. (Pubitemid 44791992)
17. Forneris F, Battaglioli E, Mattevi A, and Binda C. New roles of flavoproteins in molecular cell biology: Histone demethylase LSD1 and chromatin. FEBS J 276: 4304-4312, 2009.
18. Fraaije MW and Mattevi A. Flavoenzymes: Diverse catalysts with recurrent features. Trends Biochem Sci 25: 126-132, 2000. (Pubitemid 30122424)
19. Gorke B, Reinhardt J, and Rak B. Activity of Lac repressor anchored to the Escherichia coli inner membrane. Nucleic Acids Res 33: 2504-2511, 2005.
20. Grabau C, Chang YY, and Cronan JE, Jr. Lipid binding by Escherichia coli pyruvate oxidase is disrupted by small alterations of the carboxyl-terminal region. J Biol Chem 264: 12510-12519, 1989. (Pubitemid 19191143)
21. Grabau C and Cronan JE, Jr. In vivo function of Escherichia coli pyruvate oxidase specifically requires a functional lipid binding site. Biochemistry 25: 3748-3751, 1986.
22. Grabau C and Cronan JE, Jr. Molecular cloning of the gene (poxB) encoding the pyruvate oxidase of Escherichia coli, a lipid-activated enzyme. J Bacteriol 160: 1088-1092, 1984. (Pubitemid 15219484)
23. Grabbe R and Schmitz RA. Oxygen control of nif gene expression in Klebsiella pneumoniae depends on NifL reduction at the cytoplasmic membrane by electrons derived from the reduced quinone pool. Eur J Biochem 270: 1555-1566, 2003. (Pubitemid 36459594)
24. Gu D, Zhou Y, Kallhoff V, Baban B, Tanner JJ, and Becker DF. Identification and characterization of the DNA-binding domain of the multifunctional PutA flavoenzyme. J Biol Chem 279: 31171-31176, 2004. (Pubitemid 39037780)
25. Halouska S, Zhou Y, Becker DF, and Powers R. Solution structure of the Pseudomonas putida protein PpPutA45 and its DNA complex. Proteins 75: 12-27, 2009.
26. Hefti MH, Francoijs KJ, de Vries SC, Dixon R, and Vervoort J. The PAS fold. A redefinition of the PAS domain based upon structural prediction. Eur J Biochem 271: 1198-1208, 2004. (Pubitemid 38373052)
27. Heintzen C, Loros JJ, and Dunlap JC. The PAS protein VIVID defines a clock-associated feedback loop that represses light input, modulates gating, and regulates clock resetting. Cell 104: 453-464, 2001. (Pubitemid 32206465)
28. Hill S, Austin S, Eydmann T, Jones T, and Dixon R. Azotobacter vinelandii NIFL is a flavoprotein that modulates transcriptional activation of nitrogen-fixation genes via a redoxsensitive switch. Proc Natl Acad Sci USA 93: 2143-2148, 1996. (Pubitemid 26079895)
29. Key J, Hefti M, Purcell EB, and Moffat K. Structure of the redox sensor domain of Azotobacter vinelandii NifL at atomic resolution: Signaling, dimerization, and mechanism. Biochemistry 46: 3614-3623, 2007. (Pubitemid 46493462)
30. Koland JG, Miller MJ, and Gennis RB. Reconstitution of the membrane-bound, ubiquinone-dependent pyruvate oxidase respiratory chain of Escherichia coli with the cytochrome d terminal oxidase. Biochemistry 23: 445-453, 1984.
31. Kottke T, Hegemann P, Dick B, and Heberle J. The photochemistry of the light-, oxygen-, and voltage-sensitive domains in the algal blue light receptor phot. Biopolymers 82: 373-378, 2006. (Pubitemid 44000907)
32. Krishnan N and Becker DF. Characterization of a bifunctional PutA homologue from Bradyrhizobium japonicum and identification of an active site residue that modulates proline reduction of the flavin adenine dinucleotide cofactor. Biochemistry 44: 9130-9139, 2005. (Pubitemid 40943228)
33. Lamb JS, Zoltowski BD, Pabit SA, Li L, Crane BR, and Pollack L. Illuminating solution responses of a LOV domain protein with photocoupled small-angle X-ray scattering. J Mol Biol 393: 909-919, 2009.
34. Larson JD, Jenkins JL, Schuermann JP, Zhou Y, Becker DF, and Tanner JJ. Crystal structures of the DNA-binding domain of Escherichia coli proline utilization. A flavoprotein and analysis of the role of Lys9 in DNA recognition. Protein Sci 15: 2630-2641, 2006.
35. Lee YH, Nadaraia S, Gu D, Becker DF, and Tanner JJ. Structure of the proline dehydrogenase domain of the multifunctional PutA flavoprotein. Nat Struct Biol 10: 109-114, 2003. (Pubitemid 36177090)
36. Linden H. Circadian rhythms. A white collar protein senses blue light. Science 297: 777-778, 2002.
37. Ling M, Allen SW, and Wood JM. Sequence analysis identifies the proline dehydrogenase and pyrroline-5-carboxylate dehydrogenase domains of the multifunctional Escherichia coli PutA protein. J Mol Biol 245: 950-956, 1994. (Pubitemid 24348862)
38. Little R, Martinez-Argudo I, and Dixon R. Role of the central region of NifL in conformational switches that regulate nitrogen fixation. Biochem Soc T 34: 162-164, 2006. (Pubitemid 43235561)
39. Liu Y, He Q, and Cheng P. Photoreception in Neurospora: A tale of two White Collar proteins. Cell Mol Life Sci 60: 2131-2138, 2003. (Pubitemid 37357421)
40. Losi A. Flavin-based Blue-Light photosensors: A photobiophysics update. Photochem Photobiol 83: 1283-1300, 2007. (Pubitemid 350132622)
41. Macheroux P, Hill S, Austin S, Eydmann T, Jones T, Kim S-O, Poole R, and Dixon R. Electron donation to the flavoprotein NifL, a redox-sensing transcriptional regulator. Biochem J 332: 413-419, 1998. (Pubitemid 28271873)
42. Marchal D, Pantigny J, Laval JM, Moiroux J, and Bourdillon C. Rate constants in two dimensions of electron transfer between pyruvate oxidase, a membrane enzyme, and ubiquinone (coenzyme Q8), its water-insoluble electron carrier. Biochemistry 40: 1248-1256, 2001. (Pubitemid 32142885)
43. Martinez-Argudo I, Little R, Shearer N, Johnson P, and Dixon R. The NifL-NifA system: A multidomain transcriptional regulatory complex that integrates environmental signals. J Bacteriol 186: 601-610, 2004. (Pubitemid 38129636)
44. Martinez-Argudo I, Little R, Shearer N, Johnson P, and Dixon R. Nitrogen fixation: Key genetic regulatory mechanisms. Biochem Soc Trans 33: 152-156, 2005. (Pubitemid 40313786)
45. Massey V. The chemical and biological versatility of riboflavin. Biochem Soc Trans 28: 283-296, 2000.
46. Mather MW and Gennis RB. Kinetic studies of the lipid-activated pyruvate oxidase flavoprotein of Escherichia coli. J Biol Chem 260: 16148-16155, 1985. (Pubitemid 16176999)
47. Menzel R and Roth J. Purification of the putA gene product. J Biol Chem 256: 9755-9761, 1981.
48. Moglich A and Moffat K. Structural basis for light-dependent signaling in the dimeric LOV domain of the photosensor YtvA. J Mol Biol 373: 112-126, 2007. (Pubitemid 47390713)
49. Muller YA and Schulz GE. Structure of the thiamine- and flavin-dependent enzyme pyruvate oxidase. Science 259: 965-967, 1993. (Pubitemid 23080664)
50. Neumann P, Weidner A, Pech A, Stubbs MT, and Tittmann K. Structural basis for membrane binding and catalytic activation of the peripheral membrane enzyme pyruvate oxidase from Escherichia coli. Proc Natl Acad Sci USA 105: 17390-17395, 2008.
51. Ostrovsky De Spicer P and Maloy S. PutA protein, a membrane-associated flavin dehydrogenase, acts as a redox-dependent transcriptional regulator. Proc Natl Acad Sci USA 90: 4295-4298, 1993. (Pubitemid 23134213)
52. Ostrovsky De Spicer P, O'Brian K, and Maloy S. Regulation of proline utilization in Salmonella typhimurium: A membrane-associated dehydrogenase binds DNA in vitro. J Bacteriol 173: 211-219, 1991.
53. Partch CL and Sancar A. Photochemistry and photobiology of cryptochrome blue-light photopigments: the search for a photocycle. Photochem Photobiol 81: 1291-1304, 2005. (Pubitemid 43035838)
54. Qi YN, Rao F, Luo Z, and Liang ZX. A flavin cofactor-binding PAS domain regulates c-di-GMP synthesis in AxDGC2 from Acetobacter xylinum. Biochemistry 48: 10275-10285, 2009.
55. Rebbapragada A, Johnson MS, Harding GP, Zuccarelli AJ, Fletcher HM, Zhulin IB, and Taylor BL. The Aer protein and the serine chemoreceptor Tsr independently sense intracellular energy levels and transduce oxygen, redox, and energy signals for Escherichia coli behavior. Proc Natl Acad Sci USA 94: 10541-10546, 1997. (Pubitemid 27430770)
56. Recny MA, Grabau C, Cronan JE, Jr., and Hager LP. Characterization of the alpha-peptide released upon protease activation of pyruvate oxidase. J Biol Chem 260: 14287-14291, 1985. (Pubitemid 16197501)
57. Recny MA and Hager LP. Isolation and characterization of the protease-activated form of pyruvate oxidase. Evidence for a conformational change in the environment of the flavin prosthetic group. J Biol Chem 258: 5189-5195, 1983.
58. Russell P, Hager LP, and Gennis RB. Characterization of the proteolytic activation of pyruvate oxidase. J Biol Chem 252: 7877-7882, 1977.
59. Russell P, Schrock HL, and Gennis RB. Lipid activation and protease activation of pyruvate oxidase. J Biol Chem 252: 7883-7887, 1977.
60. Scarpulla RC and Soffer RL. Membrane-bound proline dehydrogenase from Escherichia coli. J Biol Chem 253: 5997-6001, 1978.
61. Schreiner ME and Eikmanns BJ. Pyruvate:quinone oxidoreductase from Corynebacterium glutamicum: Purification and biochemical characterization. J Bacteriol 187: 862-871, 2005. (Pubitemid 40189760)
62. Schreiner ME, Riedel C, Holatko J, Patek M, and Eikmanns BJ. Pyruvate:quinone oxidoreductase in Corynebacterium glutamicum: Molecular analysis of the pqo gene, significance of the enzyme, and phylogenetic aspects. J Bacteriol 188: 1341-1350, 2006. (Pubitemid 43228667)
63. Schrock HL and Gennis RB. High affinity lipid binding sites on the peripheral membrane enzyme pyruvate oxidase. J Biol Chem 252: 5990-5995, 1977.
64. Schwerdtfeger C and Linden H. VIVID is a flavoprotein and serves as a fungal blue light photoreceptor for photoadaptation. EMBO J 22: 4846-4855, 2003. (Pubitemid 37162920)
65. Slavny P, Little R, Salinas P, Clarke TA, and Dixon R. Quaternary structure changes in a second Per-Arnt-Sim domain mediate intramolecular redox signal relay in the NifL regulatory protein. Mol Microbiol 75: 61-75, 2010.
66. Soderback E, Reyes-Ramirez F, Eydmann T, Austin S, Hill S, and Dixon R. The redox- and fixed nitrogen-responsive regulatory protein NIFL from Azotobacter vinelandii comprises discrete flavin and nucleotide-binding domains. Mol Microbiol 28: 179-192, 1998. (Pubitemid 28160123)
67. Sollner S, Schober M, Wagner A, Prem A, Lorkova L, Palfey BA, Groll M, and Macheroux P. Quinone reductase acts as a redox switch of the 20S yeast proteasome. EMBO Rep 10: 65-70, 2009.
68. Srivastava D, Schuermann JP, White TA, Krishnan N, Sanyal N, Hura GL, Tan A, Henzl MT, Becker DF, and Tanner JJ. Crystal structure of the bifunctional proline utilization A flavoenzyme from Bradyrhizobium japonicum. Proc Natl Acad Sci USA 107: 2878-2883, 2010.
69. Srivastava D, Zhu W, Johnson WH, Jr., Whitman CP, Becker DF, and Tanner JJ. The structure of the proline utilization a proline dehydrogenase domain inactivated by N-propargylglycine provides insight into conformational changes induced by substrate binding and flavin reduction. Biochemistry 49: 560-569, 2010.
70. Surber MW and Maloy S. Regulation of flavin dehydrogenase compartmentalization: Requirements for PutA-membrane association in Salmonella typhimurium. Biochim Biophys Acta 1421: 5-18, 1999. (Pubitemid 29421853)
71. Tanner JJ. Structural biology of proline catabolism. Amino Acids 35: 719-730, 2008.
72. Taylor BL and Zhulin IB. PAS domains: Internal sensors of oxygen, redox potential, and light. Microbiol Mol Biol Rev 63: 479-506, 1999. (Pubitemid 29264980)
73. Thummer R, Klimmek O, and Schmitz RA. Biochemical studies of Klebsiella pneumoniae NifL reduction using reconstituted partial anaerobic respiratory chains of Wolinella succinogenes. J Biol Chem 282: 12517-12526, 2007. (Pubitemid 47100626)
74. Tittmann K, Golbik R, Ghisla S, and Hubner G. Mechanism of elementary catalytic steps of pyruvate oxidase from Lactobacillus plantarum. Biochemistry 39: 10747-10754, 2000.
75. Ukaegbu UE and Rosenzweig AC. Structure of the redox sensor domain of Methylococcus capsulatus (Bath) MmoS. Biochemistry 48: 2207-2215, 2009.
76. van der Horst MA and Hellingwerf KJ. Photoreceptor proteins, "star actors of modern times": A review of the functional dynamics in the structure of representative members of six different photoreceptor families. Acc Chem Res 37: 13-20, 2004.
77. Wang AY, Chang YY, and Cronan JE, Jr. Role of the tetrameric structure of Escherichia coli pyruvate oxidase in enzyme activation and lipid binding. J Biol Chem 266: 10959-10966, 1991.
78. Watts KJ, Johnson MS, and Taylor BL. Structure-function relationships in the HAMP and proximal signaling domains of the aerotaxis receptor Aer. J Bacteriol 190: 2118-2127, 2008. (Pubitemid 351355335)
79. Wille G, Meyer D, Steinmetz A, Hinze E, Golbik R, and Tittmann K. The catalytic cycle of a thiamin diphosphate enzyme examined by cryocrystallography. Nat Chem Biol 2: 324-328, 2006. (Pubitemid 43787214)
80. Wood J. Membrane association of proline dehydrogenase in Escherichia coli is redox dependent. Proc Natl Acad Sci USA 84: 373-377, 1987. (Pubitemid 17006197)
81. Zhang M, White TA, Schuermann JP, Baban BA, Becker DF, and Tanner JJ. Structures of the Escherichia coli PutA proline dehydrogenase domain in complex with competitive inhibitors. Biochemistry 43: 12539-12548, 2004. (Pubitemid 39314715)
82. Zhang TF and Hager LP. Binding of pyruvate oxidase alpha-peptide to phospholipid vesicles. Arch Biochem Biophys 255: 201-204, 1987.
83. Zhang W, Zhang M, Zhu W, Zhou Y, Wanduragala S, Rewinkel D, Tanner JJ, and Becker DF. Redox-induced changes in flavin structure and roles of flavin N(5) and the ribityl 2′-OH group in regulating PutA-membrane binding. Biochemistry 46: 483-491, 2007. (Pubitemid 46105437)
84. Zhang W, Zhou Y, and Becker DF. Regulation of PutA-membrane associations by flavin adenine dinucleotide reduction. Biochemistry 43: 13165-13174, 2004. (Pubitemid 39362785)
85. Zhou Y, Larson JD, Bottoms CA, Arturo EC, Henzl MT, Jenkins JL, Nix JC, Becker DF, and Tanner JJ. Structural basis of the transcriptional regulation of the proline utilization regulon by multifunctional PutA. J Mol Biol 381: 174-188, 2008.
86. Zhou Y, Zhu W, Bellur PS, Rewinkel D, and Becker DF. Direct linking of metabolism and gene expression in the proline utilization A protein from Escherichia coli. Amino Acids 35: 711-718, 2008.
87. Zhu W and Becker DF. Exploring the proline-dependent conformational change in the multifunctional PutA flavoprotein by tryptophan fluorescence spectroscopy. Biochemistry 44: 12297-12306, 2005. (Pubitemid 41324323)
88. Zhu W and Becker DF. Flavin redox state triggers conformational changes in the PutA protein from Escherichia coli. Biochemistry 42: 5469-5477, 2003. (Pubitemid 36560444)
89. Zoltowski BD and Crane BR. Light activation of the LOV protein vivid generates a rapidly exchanging dimer. Biochemistry 47: 7012-7019, 2008. (Pubitemid 351956350)
90. Zoltowski BD, Schwerdtfeger C, Widom J, Loros JJ, Bilwes AM, Dunlap JC, and Crane BR. Conformational switching in the fungal light sensor Vivid. Science 316: 1054-1057, 2007. (Pubitemid 46799496)
91. Zoltowski BD, Vaccaro B, and Crane BR. Mechanism-based tuning of a LOV domain photoreceptor. Nat Chem Biol 5: 827-834, 2009.