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Title
Abstract
Introduction
Results
Discussion
Methods
Structural Analysis of Lipid Binding Sites (Table
Analysis of Sequence Conservation
References
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Biology
Biochemistry

Conservation of Lipid Functions in Cytochrome bc Complexes

Profile image of Julian WhiteleggeJulian Whitelegge

2011, Journal of Molecular Biology

https://doi.org/10.1016/J.JMB.2011.09.023
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31 pages

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Abstract

Lipid binding sites and properties are compared in two families of hetero-oligomeric membrane protein complexes known to have similar functions in order to gain further understanding of the role of lipid in the function, dynamics, and assembly of these complexes. Using the crystal structure information for both complexes, lipid binding properties were compared for the cytochrome b 6 f and bc 1 complexes that function in photosynthetic and respiratory membrane energy transduction. Comparison of lipid and detergent binding sites in the b 6 f complex with those in bc 1 shows significant conservation of lipid positions. Seven lipid binding sites in the cyanobacterial b 6 f complex overlap three natural sites in the C. reinhardtii algal complex, and four sites in the yeast mitochondrial bc 1 complex. The specific identity of lipids is different in b 6 f and bc 1 complexes: b 6 f contains SDG, PG, MGDG, and DGDG, whereas cardiolipin, PE, and PA are present in the yeast bc 1 complex. The lipidic chlorophyll a and β-carotene in cyanobacterial b 6 f, as well as eicosane in C. reinhardtii, are unique to the photosynthetic b 6 f complex. The inferences of lipid binding sites and functions were supported by sequence, intermolecular distance, and Bfactor information on interacting lipid groups and coordinating amino acid residues. The lipid functions inferred in the b 6 f complex are: (i) substitution of a trans-membrane helix (TMH) by a lipid and chlorin ring; (ii) lipid and β-carotene connection of peripheral and core domains; (iii) stabilization of iron-sulfur protein TMH; (iv) n-side charge and polarity compensation; (v) βcarotene-mediated super-complex with photosystem I complex.

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References (92)

  1. Kurisu G, Zhang H, Smith JL, Cramer WA. Structure of the cytochrome b 6 f complex of oxygenic photosynthesis: tuning the cavity. Science (New York, NY. 2003; 302:1009-1014.
  2. Yan J, Kurisu G, Cramer WA. Structure of the cytochrome b 6 f complex: Binding site and intraprotein transfer of the quinone analogue inhibitor 2,5-dibromo-3-methyl-6-isopropyl-p- benzoquinone. Proc Nat Acad Sci USA. 2006; 103:67-74.
  3. Yamashita E, Zhang H, Cramer WA. Structure of the cytochrome b 6 f complex: quinone analogue inhibitors as ligands of heme c n . J Mol Biol. 2007; 370:39-52. [PubMed: 17498743]
  4. Baniulis D, Yamashita E, Whitelegge JP, Zatsman AI, Hendrich MP, Hasan SS, Ryan CM, Cramer WA. Structure-Function, Stability, and Chemical Modification of the Cyanobacterial Cytochrome b 6 f Complex from Nostoc sp. PCC 7120. J Biol Chem. 2009; 284:9861-9869. [PubMed: 19189962]
  5. Stroebel D, Choquet Y, Popot JL, Picot D. An atypical heam in the cytochrome b 6 f complex. Nature. 2003; 426:413-418. [PubMed: 14647374]
  6. Zatsman AI, Zhang H, Gunderson WA, Cramer WA, Hendrich MP. Heme-heme interactions in the cytochrome b 6 f complex: EPR spectroscopy and correlation with structure. J Amer Chem Soc. 2006; 128:14246-14247. [PubMed: 17076484]
  7. Lavergne J. Membrane potential-dependent reduction of cytochrome b 6 in an algal mutant lacking photosystem I centers. Biochim Biophys Acta. 1983; 725:25-33.
  8. Joliot P, Joliot A. The low-potential electron-transfer chain in the cytochrome bf complex. Biochim Biophys Acta. 1988; 933:319-333.
  9. Baymann F, Giusti F, Picot D, Nitschke W. The ci/bH moiety in the b 6 f complex studied by EPR: a pair of strongly interacting hemes. Proc Nat Acad Sci USA. 2007; 104:519-524. [PubMed: 17202266]
  10. Twigg AI, Baniulis D, Cramer WA, Hendrich MP. EPR detection of an O 2 surrogate bound to heme c n of the cytochrome b 6 f complex. J Am Chem Soc. 2009; 131:12536-12537. [PubMed: 19689132]
  11. Xia D, Yu CA, Kim H, Xia JZ, Kachurin AM, Yu L, Deisenhofer J. Crystal structure of the cytochrome bc 1 complex from bovine heart mitochondria. Science (New York, NY. 1997; 277:60-66.
  12. Iwata S, Lee JW, Okada K, Lee JK, Iwata M, Rasmussen B, Link TA, Ramaswamy S, Jap BK. Complete structure of the 11-subunit bovine mitochondrial cytochrome bc 1 complex. Science (New York, NY. 1998; 281:64-71.
  13. Zhang Z, Huang L, Shulmeister VM, Chi YI, Kim KK, Hung LW, Crofts AR, Berry EA, Kim SH. Electron transfer by domain movement in cytochrome bc 1 . Nature. 1998; 392:677-684. [PubMed: 9565029]
  14. Berry EA, Huang LS, Zhang Z, Kim SH. Structure of the avian mitochondrial cytochrome bc 1 complex. J Bioenerg Biomem. 1999; 31:177-190.
  15. Hunte C, Koepke J, Lange C, Rossmanith T, Michel H. Structure at 2.3 Å resolution of the cytochrome bc 1 complex from the yeast Saccharomyces cerevisiae with an antibody Fv fragment. Struct Fold Des. 2000; 8:669-684.
  16. Gao X, Wen X, Yu C, Esser L, Tsao S, Quinn B, Zhang L, Yu L, Xia D. The crystal structure of mitochondrial cytochrome bc 1 in complex with famoxadone: The role of aromatic-aromatic interaction in inhibition. Biochemistry-Us. 2002; 41:11692-11702.
  17. Gao X, Wen X, Esser L, Quinn B, Yu L, Yu C, Xia D. Structural basis for the quinone reduction in the bc 1 complex: A comparative analysis of crystal structure of mitochondrial cytochrome bc 1 with bound substrate and inhibitors at the Qi site. Biochemistry-Us. 2003; 42:9067-9080.
  18. Palsdottir H, Lojero CG, Trumpower BL, Hunte C. Structure of the yeast cytochrome bc 1 complex with a hydroxyquinone anion Qo site inhibitor bound. J Biol Chem. 2003; 278:31303-31311. [PubMed: 12782631]
  19. Esser L, Quinn B, Li YF, Zhang M, Elberry M, Yu L, Yu CA, Xia D. Crystallographic studies of quinol oxidation site inhibitors: a modified classification of inhibitors for the cytochrome bc 1 complex. J Mol Biol. 2004; 341:281-302. [PubMed: 15312779]
  20. Solmaz SR, Hunte C. Structure of complex III with bound cytochrome c in reduced state and definition of a minimal core interface for electron transfer. J Biol Chem. 2008; 283:17542-17549. [PubMed: 18390544]
  21. Soriano, GM.; Smith, JL.; Cramer, WA. Cytochrome f. In: Messerschmidt, A.; Huber, R.; Wieghardt, K.; Poulos, T., editors. Handbook of Metalloproteins. Wiley; London: 2001. p. 172-181.
  22. Carrell CJ, Zhang H, Cramer WA, Smith JL. Biological identity and diversity in photosynthesis and respiration: structure of the lumen-side domain of the chloroplast Rieske protein. Structure. 1997; 5:1613-1625. [PubMed: 9438861]
  23. Cramer WA, Zhang H, Yan J, Kurisu G, Smith JL. Trans-membrane traffic in the cytochrome b 6 f complex. Ann Rev Biochem. 2006; 75:769-790. [PubMed: 16756511]
  24. Azzi, A.; Brodbeck, U.; Zahler, P., editors. Membrane Proteins: A Laboratory Manual. Springer- Verlag; Berlin: 1981.
  25. Nussberger S, Dorr K, Wang DN, Kuhlbrandt W. Lipid-protein interactions in crystals of the plant light-harvesting complex. J Mol Biol. 1993; 234:347-356. [PubMed: 8230219]
  26. Cartailler JP, Luecke H. X-ray crystallographic analysis of lipid-protein interactions in the bacteriorhodopsin purple membrane. Annu Rev Biophys Biomol Struct. 2003; 32:285-310. [PubMed: 12598369]
  27. Gantar M, Berry JP, Thomas S, Wang M, Perez R, Rein KS. Allelopathic activity among Cyanobacteria and microalgae isolated from Florida freshwater habitats. FEMS microbiology ecology. 2008; 64:55-64. [PubMed: 18266743]
  28. Hite RK, Li ZL, Walz T. Principles of membrane protein interactions with annular lipids deduced from aquaporin-0 2D crystals. Embo Journal. 2010; 29:1652-1658. [PubMed: 20389283]
  29. Escriba PV, Wedegaertner PB, Goni FM, Vogler O. Lipid-protein interactions in GPCR-associated signaling. Biochimica et biophysica acta. 2007; 1768:836-852. [PubMed: 17067547]
  30. Hanson MA, Cherezov V, Griffith MT, Roth CB, Jaakola VP, Chien EY, Velasquez J, Kuhn P, Stevens RC. A specific cholesterol binding site is established by the 2.8 A structure of the human beta2-adrenergic receptor. Structure. 2008; 16:897-905. [PubMed: 18547522]
  31. Lee SY, Lee A, Chen JY, MacKinnon R. Structure of the KvAP voltage-dependent K+ channel and its dependence on the lipid membrane. Proceedings of the National Academy of Sciences of the United States of America. 2005; 102:15441-15446. [PubMed: 16223877]
  32. Schmidt D, Cross SR, MacKinnon R. A gating model for the archeal voltage-dependent K(+) channel KvAP in DPhPC and POPE:POPG decane lipid bilayers. J Mol Biol. 2009; 390:902-912. [PubMed: 19481093]
  33. Butterwick JA, MacKinnon R. Solution structure and phospholipid interactions of the isolated voltage-sensor domain from KvAP. J Mol Biol. 2010; 403:591-606. [PubMed: 20851706]
  34. McAuley KE, Fyfe PK, Ridge JP, Isaacs NW, Cogdell RJ, Jones MR. Structural details of an interaction between cardiolipin and an integral membrane protein. Proceedings of the National Academy of Sciences of the United States of America. 1999; 96:14706-14711. [PubMed: 10611277]
  35. Camara-Artigas A, Brune D, Allen JP. Interaction between lipids and bacterial reaction centers determined by protein crystallography. Proc Nat Acad Sci USA. 2002; 99:11055-11060. [PubMed: 12167672]
  36. Fyfe PK, Hughes AV, Heathcote P, Jones MR. Proteins, chlorophylls and lipids: X-ray analysis of a three-way relationship. Trends Plant Sci. 2005; 10:275-282. [PubMed: 15949761]
  37. Jones MR. Lipids in photosynthetic reaction centres: structural roles and functional holes. Prog Lipid Res. 2007; 46:56-87. [PubMed: 16963124]
  38. Wohri AB, Wahlgren WY, Malmerberg E, Johansson LC, Neutze R, Katona G. Lipidic sponge phase crystal structure of a photosynthetic reaction center reveals lipids on the protein surface. Biochemistry-Us. 2009; 48:9831-9838.
  39. Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W. Cyanobacterial photosystem II at 2.9-A resolution and the role of quinones, lipids, channels and chloride. Nat Struct Mol Biol. 2009; 16:334-342. [PubMed: 19219048]
  40. Kern, J.; Zouni, A.; Guskov, A.; Krauss, N. Lipids in the structure of the photosystem I, photosystem II, and the cytochrome b6f complex. In: Murata, HWaN, editor. Lipids in Photosynthesis: Essential and Regulatory Functions. Springer Science; 2009. p. 203-242.
  41. Umena Y, Kawakami K, Shen JR, Kamiya N. Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 A. Nature. 2011; 473:55-60. [PubMed: 21499260]
  42. Jordan P, Fromme P, Witt HT, Klukas O, Saenger W, Krauss N. Three-dimensional structure of cyanobacterial photosystem I at 2.5 A resolution. Nature. 2001; 411:909-917. [PubMed: 11418848]
  43. Shinzawa-Itoh K, Aoyama H, Muramoto K, Terada H, Kurauchi T, Tadehara Y, Yamasaki A, Sugimura T, Kurono S, Tsujimoto K, Mizushima T, Yamashita E, Tsukihara T, Yoshikawa S. Structures and physiological roles of 13 integral lipids of bovine heart cytochrome c oxidase. The EMBO journal. 2007; 26:1713-1725. [PubMed: 17332748]
  44. Qin L, Hiser C, Mulichak A, Garavito RM, Ferguson-Miller S. Identification of conseved lipid/ detergent binding site in a high resolution structure of the memebrane protein, Cytochrome c oxidase. Proc Natl Acad Sci, USA. 2006; 103:16117-16122. [PubMed: 17050688]
  45. Qin L, Sharpe MA, Garavito RM, Ferguson-Miller S. Conserved lipid-binding sites in membrane proteins: a focus on cytochrome c oxidase. Current opinion in structural biology. 2007; 17:444- 450. [PubMed: 17719219]
  46. Palsdottir H, Hunte C. Lipids in membrane protein structures. Biochim Biophys Acta. 2004; 1666:2-18. [PubMed: 15519305]
  47. Cramer WA, Yamashita E, Hasan SS. The Q cycle of cytochrome bc complexes: a structure perspective. Biochim Biophys Acta/Bioenergetics. 2011; 1807:788-802.
  48. Schutz M, Brugna M, Lebrun E, Baymann F, Huber R, Stetter KO, Hauska G, Toci R, Lemesle- Meunier D, Tron P, Schmidt C, Nitschke W. Early evolution of cytochrome bc complexes. J Mol Biol. 2000; 300:663-675. [PubMed: 10891261]
  49. Saraste M. Location of haem-binding sites in the mitochondrial cytochrome b. FEBS letters. 1984; 166:367-372. [PubMed: 6363134]
  50. Widger WR, Cramer WA, Herrmann RG, Trebst A. Sequence homology and structural similarity between the b cytochrome of mitochondrial complex III and the chloroplast b 6 f complex: position of the cytochrome b hemes in the membrane. Proc Natl Acad Sci, U S A. 1984; 81:674-678. [PubMed: 6322162]
  51. Lange C, Nett JH, Trumpower BL, Hunte C. Specific roles of protein-phospholipid interactions in the yeast cytochrome bc1 complex structure. EMBO J. 2001; 20:6591-6600. [PubMed: 11726495]
  52. Hunte C, Palsdottir H, Trumpower BL. Protonmotive pathways and mechanisms in the cytochrome bc 1 complex. FEBS letters. 2003; 545:39-46. [PubMed: 12788490]
  53. Schagger H, Hagen T, Roth B, Brandt U, Link TA, von Jagow G. Phospholipid specificity of bovine heart bc1 complex. Eur J Biochem. 1990; 190:123-130. [PubMed: 2163831]
  54. Wenz T, Covian R, Hellwig P, Macmillan F, Meunier B, Trumpower BL, Hunte C. Mutational analysis of cytochrome b at the ubiquinol oxidation site of yeast complex III. J Biol Chem. 2007; 282:3977-3988. [PubMed: 17145759]
  55. Wenz T, Hielscher R, Hellwig P, Schagger H, Richers S, Hunte C. Role of phospholipids in respiratory cytochrome bc 1 complex catalysis and supercomplex formation. Biochim Biophys Acta. 2009; 1787:609-616. [PubMed: 19254687]
  56. Qin L, Sharpe MA, Garavito RM, Ferguson-Miller S. Conserved lipid-binding sites in membrane proteins: a focus on cytochrome c oxidase. Current Opinion in Structural Biology. 2007; 17:444- 450. [PubMed: 17719219]
  57. Zhang H, Kurisu G, Smith JL, Cramer WA. A defined protein-detergent-lipid complex for crystallization of integral membrane proteins: The cytochrome b 6 f complex of oxygenic photosynthesis. Proc Nat Acad Sci USA. 2003; 100:5160-5163. [PubMed: 12702760]
  58. de Lacroix de Lavalette A, Finazzi G, Zito F. b6f-Associated chlorophyll: structural and dynamic contribution to the different cytochrome functions. Biochemistry-Us. 2008; 47:5259-5265.
  59. Zito F, Finazzi G, Joliot P, Wollman FA. Glu78, from the conserved PEWY sequence of subunit IV, has a key function in cytochrome b6f turnover. Biochemistry-Us. 1998; 37:10395-10403.
  60. Finazzi G. Redox-coupled proton pumping activity in cytochrome b6f, as evidenced by the pH dependence of electron transfer in whole cells of Chlamydomonas reinhardtii. Biochemistry-Us. 2002; 41:7475-7482.
  61. Crofts AR, Holland JT, Victoria D, Kolling DR, Dikanov SA, Gilbreth R, Lhee S, Kuras R, Kuras MG. The Q-cycle reviewed: How well does a monomeric mechanism of the bc 1 complex account for the function of a dimeric complex? Biochim Biophys Acta. 2008; 1777:1001-1019. [PubMed: 18501698]
  62. Fyfe PK, Potter JA, Cheng J, Williams CM, Watson AJ, Jones MR. Structural responses to cavity- creating mutations in an integral membrane protein. Biochemistry-Us. 2007; 46:10461-10472.
  63. Schwenkert S, Legen J, Takami T, Shikanai T, Herrmann RG, Meurer J. Role of the low- molecular-weight subunits PetL, PetG, and PetN in assembly, stability, and dimerization of the cytochrome b6f complex in tobacco. Plant physiology. 2007; 144:1924-1935. [PubMed: 17556510]
  64. Lange C, Nett JH, Trumpower BL, Hunte C. Specific roles of protein-phospholipid interactions in the yeast cytochrome bc(1) complex structure. Embo Journal. 2001; 20:6591-6600. [PubMed: 11726495]
  65. Hunte C, Richers S. Lipids and membrane protein structures. Current Opinion in Structural Biology. 2008; 18:406-411. [PubMed: 18495472]
  66. Solmaz SRN, Hunte C. Structure of complex III with bound cytochrome c in reduced state and definition of a minimal core interface for electron transfer. Journal of Biological Chemistry. 2008; 283:17542-17549. [PubMed: 18390544]
  67. de Vitry C, Ouyang Y, Finazzi G, Wollman FA, Kallas T. The chloroplast Rieske iron-sulfur protein. At the crossroad of electron transport and signal transduction. J Biol Chem. 2004; 279:44621-44627. [PubMed: 15316016]
  68. Choquet Y, Zito F, Wostrikoff K, Wollman FA. Cytochrome f translation in Chlamydomonas chloroplast is autoregulated by its carboxyl-terminal domain. Plant Cell. 2003; 15:1443-1454. [PubMed: 12782735]
  69. Kurisu G, Zhang HM, Smith JL, Cramer WA. Structure of the cytochrome b(6)f complex of oxygenic photosynthesis: Tuning the cavity. Science. 2003; 302:1009-1014. [PubMed: 14526088]
  70. Baniulis D, Yamashita E, Whitelegge JP, Zatsman AI, Hendrich MP, Hasan SS, Ryan CM, Cramer WA. Structure-Function, Stability, and Chemical Modification of the Cyanobacterial Cytochrome b(6)f Complex from Nostoc sp PCC 7120. Journal of Biological Chemistry. 2009; 284:9861-9869. [PubMed: 19189962]
  71. Iwai M, Takizawa K, Tokutsu R, Okamuro A, Takahashi Y, MInagawa J. Isolation of the supercomplex that drives cyclic electron flow in photosynthesis. Nature. 2010; 464:1210-1213. [PubMed: 20364124]
  72. Schafer E, Dencher NA, Vonck J, Parcej DN. Three-dimensional structure of the respiratory chain supercomplex I1III2IV1 from bovine heart mitochondria. Biochemistry-Us. 2007; 46:12579- 12585.
  73. Cramer, WA.; Baniulis, D.; Yamashita, E.; Zhang, H.; Zatsman, AI.; Hendrich, MP. Structure, spectroscopy, and function of the cytochrome b 6 f complex: heme c n and n-side electron and proton transfer reactions. In: Fromme, P., editor. Photosynthetic Protein Complexes: a Structural Approach. Wiley-VCH; Weinheim: 2008. p. 155-179.
  74. Rawyler A, Siegenthaler PA. TRANSMEMBRANE DISTRIBUTION OF PHOSPHOLIPIDS AND THEIR INVOLVEMENT IN ELECTRON-TRANSPORT, AS REVEALED BY PHOSPHOLIPASE-A2 TREATMENT OF SPINACH THYLAKOIDS. Biochimica Et Biophysica Acta. 1981; 635:348-358. [PubMed: 7236668]
  75. Unitt MD, Harwood JL. SIDEDNESS STUDIES OF THYLAKOID PHOSPHATIDYLGLYCEROL IN HIGHER-PLANTS. Biochemical Journal. 1985; 228:707-711. [PubMed: 4026805]
  76. Gounaris K, Barber J, Harwood JL. THE THYLAKOID MEMBRANES OF HIGHER-PLANT CHLOROPLASTS. Biochemical Journal. 1986; 237:313-326. [PubMed: 3541898]
  77. Hunte C. Specific protein-lipid interactions in membrane proteins. Biochem Soc Trans. 2005; 33:938-942. [PubMed: 16246015]
  78. Schneider D, Volkmer T, Rogner M. PetG and PetN, but not PetL, are essential subunits of the cytochrome b 6 f complex from Synechocystis PCC 6803. Research in microbiology. 2007; 158:45- 50. [PubMed: 17224258]
  79. Kim H, Xia D, Yu CA, Xia JZ, Kachurin AM, Zhang L, Yu L, Deisenhofer J. Inhibitor binding changes domain mobility in the iron-sulfur protein of the mitochondrial bc 1 complex from bovine heart. Proc Natl Acad Sci, U S A. 1998; 95:8026-8033. [PubMed: 9653134]
  80. Dashdorj N, Zhang H, Kim H, Yan J, Cramer WA, Savikhin S. The single chlorophyll a molecule in the cytochrome b 6 f complex: unusual optical properties protect the complex against singlet oxygen. Biophysical journal. 2005; 88:4178-4187. [PubMed: 15778449]
  81. Cramer WA, Yan J, Zhang H, Kurisu G, Smith JL. Structure of the cytochrome b 6 f complex: new prosthetic groups, Q-space, and the 'hors d'oeuvres hypothesis' for assembly of the complex. Photosynth Res. 2005; 85:133-143. [PubMed: 15977064]
  82. Baniulis, D.; Zhang, H.; Yamashita, E.; Zakharova, T.; Hasan, SS.; Cramer, WA. Purification and crystallization of the cyanobacterial cytochrome b6f complex. In: Carpentier, R., editor. Methods in Molecular Biology, Photosynthesis Research Protocols. Humana Press Inc; Totowa, NJ: 2011.
  83. Zhang H, Whitelegge JP, Cramer WA. Ferredoxin:NADP + oxidoreductase is a subunit of the chloroplast cytochrome b 6 f complex. J Biol Chem. 2001; 276:38159-38165. [PubMed: 11483610]
  84. Bernstein FC, Koetzle TF, Williams GJ, Meyer EF Jr, Brice MD, Rodgers JR, Kennard O, Shimanouchi T, Tasumi M. The Protein Data Bank: a computer-based archival file for macromolecular structures. J Mol Biol. 1977; 112:535-542. [PubMed: 875032]
  85. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994; 22:4673-4680. [PubMed: 7984417]
  86. Emsley P, Lohkamp B, Scott WG, Cowtan K. Features and development of Coot. Acta Crystallogr D Biol Crystallogr. 2010; 66:486-501. [PubMed: 20383002]
  87. Sobolev V, Sorokine A, Prilusky J, Abola EE, Edelman M. Automated analysis of interatomic contacts in proteins. Bioinformatics. 1999; 15:327-332. [PubMed: 10320401]
  88. Wessel D, Fluegge U. A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal Biochem Analytical Biochemistry. 1984; 138:141-143.
  89. Whitelegge JP, Zhang H, Taylor R, Cramer WA. Full subunit coverage liquid chromatography electrospray-ionization mass spectrometry (LCMS + ) of an oligomeric membrane protein complex: the cytochrome b 6 f complex from spinach and the cyanobacterium, M. laminosus. Mol Cell Prot. 2002; 1:816-827.
  90. Dowhan W, Bogdanov M. Lipid-dependent membrane protein topogenesis. Ann Rev Biochemistry. 2006; 78:515-540.
  91. Conserved position for binding acidic lipid(s) (46) on the n-side of cyanobacterial b 6 f (PDB ID 2E74) and bc 1 complexes (PDB ID 3CX5). (A) Three lipid binding sites (1 sulfolipid and 2 UDM molecules) are observed on the n-side of the inter-monomer cavity, close to the lipid-aqueous interface, in each monomer of the cyanobacterial b 6 f complex (M. laminosus PDB ID 2E74). The head-group of the sulfolipid (color, wheat) is within an interaction distance (3.5 Å) of 1 UDM molecule (white and red), which interacts with another UDM molecule (pink and red, separation 3.
  92. Å). Disordered acyl chains of sulfolipid and detergent molecules can define a pathway for plastoquinone/plastoquinol exchange between the inter- monomer cavity and bilayer (2Fo-Fc electron density map contoured at σ=1.0 (~0.1 electrons/Å 3 ). The acidic sulfolipid molecule of cyt b 6 f interacts with Lys275 (cyt f) and Arg16 and Asn20 (ISP). (B) The sulfolipid (wheat, transparent) is located close to the acidic PA (green) and detergent UDM (teal) of the bc 1 complex suggesting an important role for this lipid binding niche.

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Conservation of Lipid Functions in Cytochrome< i> bc</i> Complexes
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2011

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Lipid functions in cytochrome bc complexes: an odd evolutionary transition in a membrane protein structure
Saif Hasan

Philosophical Transactions of the Royal Society B: Biological Sciences, 2012

Lipid-binding sites and properties were compared in the hetero-oligomeric cytochrome (cyt) b 6 f and the yeast bc 1 complexes that function, respectively, in photosynthetic and respiratory electron transport. Seven lipid-binding sites in the monomeric unit of the dimeric cyanobacterial b 6 f complex overlap four sites in the Chlamydomonas reinhardtii algal b 6 f complex and four in the yeast bc 1 complex. The proposed lipid functions include: (i) interfacial–interhelix mediation between (a) the two 8-subunit monomers of the dimeric complex, (b) between the core domain (cyt b , subunit IV) and the six trans membrane helices of the peripheral domain (cyt f , iron–sulphur protein (ISP), and four small subunits in the boundary ‘picket fence’); (ii) stabilization of the ISP domain-swapped trans-membrane helix; (iii) neutralization of basic residues in the single helix of cyt f and of the ISP; (iv) a ‘latch’ to photosystem I provided by the β-carotene chain protruding through the ‘picket ...

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Lipid functions in cytochrome <i>bc</i> complexes: an odd evolutionary transition in a membrane protein structure
Saif Hasan

Philosophical Transactions of the Royal Society B, 2012

Lipid-binding sites and properties were compared in the hetero-oligomeric cytochrome (cyt) b 6 f and the yeast bc 1 complexes that function, respectively, in photosynthetic and respiratory electron transport. Seven lipid-binding sites in the monomeric unit of the dimeric cyanobacterial b 6 f complex overlap four sites in the Chlamydomonas reinhardtii algal b 6 f complex and four in the yeast bc 1 complex. The proposed lipid functions include: (i) interfacial-interhelix mediation between (a) the two 8-subunit monomers of the dimeric complex, (b) between the core domain (cyt b, subunit IV) and the six trans membrane helices of the peripheral domain (cyt f, iron-sulphur protein (ISP), and four small subunits in the boundary 'picket fence'); (ii) stabilization of the ISP domain-swapped transmembrane helix; (iii) neutralization of basic residues in the single helix of cyt f and of the ISP; (iv) a 'latch' to photosystem I provided by the b-carotene chain protruding through the 'picket fence'; (v) presence of a lipid and chlorophyll a chlorin ring in b 6 f in place of the eighth helix in the bc 1 cyt b polypeptide. The question is posed of the function of the lipid substitution in relation to the evolutionary change between the eight and seven helix structures of the cyt b polypeptide. On the basis of the known n-side activation of light harvesting complex II (LHCII) kinase by the p-side level of plastoquinol, one possibility is that the change was directed by the selective advantage of p-to n-side trans membrane signalling functions in b 6 f, with the lipid either mediating this function or substituting for the trans membrane helix of a signalling protein lost in crystallization.

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Transmembrane signaling and assembly of the cytochrome b6f-lipidic charge transfer complex
Saif Hasan

Biochimica et Biophysica Acta (BBA) - Bioenergetics, 2013

Structure-function properties of the cytochrome b 6 f complex are sufficiently unique compared to those of the cytochrome bc 1 complex that b 6 f should not be considered a trivially modified bc 1 complex. A unique property of the dimeric b 6 f complex is its involvement in transmembrane signaling associated with the p-side oxidation of plastoquinol. Structure analysis of lipid binding sites in the cyanobacterial b 6 f complex prepared by hydrophobic chromatography shows that the space occupied by the H transmembrane helix in the cytochrome b subunit of the bc 1 complex is mostly filled by a lipid in the b 6 f crystal structure. It is suggested that this space can be filled by the domain of a transmembrane signaling protein. The identification of lipid sites and likely function defines the intra-membrane conserved central core of the b 6 f complex, consisting of the seven trans-membrane helices of the cytochrome b and subunit IV polypeptides. The other six TM helices, contributed by cytochrome f, the iron-sulfur protein, and the four peripheral single span subunits, define a peripheral less conserved domain of the complex. The distribution of conserved and non-conserved domains of each monomer of the complex, and the position and inferred function of a number of the lipids, suggests a model for the sequential assembly in the membrane of the eight subunits of the b 6 f complex, in which the assembly is initiated by formation of the cytochrome b 6-subunit IV core sub-complex in a monomer unit. Two conformations of the unique lipidic chlorophyll a, defined in crystal structures, are described, and functions of the outlying β-carotene, a possible 'latch' in supercomplex formation, are discussed. This article is part of a Special Issue entitled: Respiratory complex III and related bc complexes.

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Lipids in the Structure of Photosystem I, Photosystem II and the Cytochrome b 6 f Complex
Athina Zouni

2009

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    Proceedings of the National Academy of Sciences, 2013

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    Trans-Membrane Signaling in Photosynthetic State Transitions: Redox- and Structure- Dependent Interaction In Vitro between Stt7 Kinase and the Cytochrome b6f Complex
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    The Journal of biological chemistry, 2016

    Trans-membrane signaling involving a serine-threonine kinase (Stt7 in Chlamydomonas reinhardtii) directs light energy distribution between the two photosystems of oxygenic photosynthesis. Oxidation of plastoquinol mediated by the cytochrome b6f complex on the electrochemically positive (p) side of the thylakoid membrane, activates the kinase domain of Stt7 on the trans (negative (n)) side, leading to phosphorylation and redistribution (″state transition″) of the light-harvesting chlorophyll proteins between the two photosystems. The molecular description of the interaction of the Stt7 kinase with the cytochrome b6f complex is unclear. In this study, Stt7 kinase has been cloned, expressed, and purified in a heterologous host. Stt7 kinase is shown (a) to be active in vitro in the presence of reductant, and (b) purified as a tetramer, determined by analytical ultracentrifugation, electron microscopy and electrospray-ionization mass spectrometry, with a molecular weight of 332 kDa, cons...

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    The Journal of biological chemistry, 2015

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    Lipid functions in cytochrome bc complexes: an odd evolutionary transition in a membrane protein structure
    Saif Hasan

    Philosophical Transactions of the Royal Society B: Biological Sciences, 2012

    Lipid-binding sites and properties were compared in the hetero-oligomeric cytochrome (cyt) b 6 f and the yeast bc 1 complexes that function, respectively, in photosynthetic and respiratory electron transport. Seven lipid-binding sites in the monomeric unit of the dimeric cyanobacterial b 6 f complex overlap four sites in the Chlamydomonas reinhardtii algal b 6 f complex and four in the yeast bc 1 complex. The proposed lipid functions include: (i) interfacial–interhelix mediation between (a) the two 8-subunit monomers of the dimeric complex, (b) between the core domain (cyt b , subunit IV) and the six trans membrane helices of the peripheral domain (cyt f , iron–sulphur protein (ISP), and four small subunits in the boundary ‘picket fence’); (ii) stabilization of the ISP domain-swapped trans-membrane helix; (iii) neutralization of basic residues in the single helix of cyt f and of the ISP; (iv) a ‘latch’ to photosystem I provided by the β-carotene chain protruding through the ‘picket ...

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    Structure-Function of the Cytochrome b 6 f Lipoprotein Complex
    Saif Hasan

    Advances in Photosynthesis and Respiration, 2016

    This paper studies the classification of highdimensional Gaussian signals from low-dimensional noisy, linear measurements. In particular, it provides upper bounds (sufficient conditions) on the number of measurements required to drive the probability of misclassification to zero in the low-noise regime, both for random measurements and designed ones. Such bounds reveal two important operational regimes that are a function of the characteristics of the source: i) when the number of classes is less than or equal to the dimension of the space spanned by signals in each class, reliable classification is possible in the low-noise regime by using a one-vs-all measurement design; ii) when the dimension of the spaces spanned by signals in each class is lower than the number of classes, reliable classification is guaranteed in the low-noise regime by using a simple random measurement design. Simulation results both with synthetic and real data show that our analysis is sharp, in the sense that it is able to gauge the number of measurements required to drive the misclassification probability to zero in the low-noise regime.

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