Structural analysis of heme proteins: Implications for design and prediction

BMC Structural Biology

Volumn 11, Issue , 2011, Pages

  Li, Ting ^a   Bonkovsky, Herbert L ^a,b,c,d   Guo, Jun Tao ^e  

^a CAROLINAS MEDICAL CENTER   (United States)

^b UNIVERSITY OF NORTH CAROLINA AT CHARLOTTE   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^e University of North Carolina at Charlotte   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOPROTEIN; CYSTEINE; HEME; HOLOPROTEIN; PROLINE; UNCLASSIFIED DRUG; HEMOPROTEIN;

ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; ANIMAL; BINDING SITE; BIOLOGY; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; HUMAN; METABOLISM; METHODOLOGY; PROTEIN CONFORMATION; PROTEIN ENGINEERING; PROTEIN MOTIF;

AMINO ACID MOTIFS; ANIMALS; APOPROTEINS; BINDING SITES; COMPUTATIONAL BIOLOGY; HEME; HEMEPROTEINS; HUMANS; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN ENGINEERING;

EID: 79952107782     PISSN: None     EISSN: 14726807     Source Type: Journal    
DOI: 10.1186/1472-6807-11-13     Document Type: Article

References (74)

1. Structure of myoglobin: A three-dimensional Fourier synthesis at 2 A. resolution. JC Kendrew RE Dickerson BE Strandberg RG Hart DR Davies DC Phillips VC Shore, Nature 1960 185 4711 422 427 10.1038/185422a0 18990802
2. Structure of haemoglobin: a three-dimensional Fourier synthesis at 5.5-A. resolution, obtained by X-ray analysis. MF Perutz MG Rossmann AF Cullis H Muirhead G Will AC North, Nature 1960 185 4711 416 422 10.1038/185416a0 18990801
3. The Janus nature of heme. TL Poulos, Nat Prod Rep 2007 24 3 504 510 10.1039/b604195g 17534526 (Pubitemid 46848714)
4. Structure-function relationships in heme-proteins. M Paoli J Marles-Wright A Smith, DNA Cell Biol 2002 21 4 271 280 10.1089/ 104454902753759690 12042067 (Pubitemid 34594541)
5. Hemoprotein Bach1 regulates enhancer availability of heme oxygenase-1 gene. J Sun H Hoshino K Takaku O Nakajima A Muto H Suzuki S Tashiro S Takahashi S Shibahara J Alam MM Taketo M Yamamoto K Igarashi, The EMBO journal 2002 21 19 5216 5224 10.1093/emboj/cdf516 12356737
6. Heme induces ubiquitination and degradation of the transcription factor Bach1. Y Zenke-Kawasaki Y Dohi Y Katoh T Ikura M Ikura T Asahara F Tokunaga K Iwai K Igarashi, Molecular and cellular biology 2007 27 19 6962 6971 10.1128/MCB.02415-06 17682061 (Pubitemid 47483643)
7. Haem can bind to and inhibit mammalian calcium-dependent Slo1 BK channels. XD Tang R Xu MF Reynolds ML Garcia SH Heinemann T Hoshi, Nature 2003 425 6957 531 535 10.1038/nature02003 14523450 (Pubitemid 37237050)
8. Reciprocal regulation of haem biosynthesis and the circadian clock in mammals. K Kaasik CC Lee, Nature 2004 430 6998 467 471 10.1038/nature02724 15269772 (Pubitemid 38987910)
9. Heme is involved in microRNA processing. M Faller M Matsunaga S Yin JA Loo F Guo, Nature structural & molecular biology 2007 14 1 23 29 (Pubitemid 46067419)
10. Identification of heme as the ligand for the orphan nuclear receptors REV-ERBalpha and REV-ERBbeta. S Raghuram KR Stayrook P Huang PM Rogers AK Nosie DB McClure LL Burris S Khorasanizadeh TP Burris F Rastinejad, Nature structural & molecular biology 2007 14 12 1207 1213 (Pubitemid 350223341)
11. Rev-erbalpha, a heme sensor that coordinates metabolic and circadian pathways. L Yin N Wu JC Curtin M Qatanani NR Szwergold RA Reid GM Waitt DJ Parks KH Pearce GB Wisely MA Lazar, Science 2007 318 5857 1786 1789 10.1126/science.1150179 18006707 (Pubitemid 350274391)
12. Orphan nuclear hormone receptor Rev-erbalpha regulates the human apolipoprotein CIII promoter. H Coste JC Rodriguez, J Biol Chem 2002 277 30 27120 27129 10.1074/jbc.M203421200 12021280 (Pubitemid 34951726)
13. Rev-erbalpha upregulates NF-kappaB-responsive genes in vascular smooth muscle cells. H Migita J Morser K Kawai, FEBS letters 2004 561 1-3 69 74 10.1016/S0014-5793(04)00118-8 15013753 (Pubitemid 38317298)
14. The orphan nuclear receptor REV-ERBalpha controls circadian transcription within the positive limb of the mammalian circadian oscillator. N Preitner F Damiola L Lopez-Molina J Zakany D Duboule U Albrecht U Schibler, Cell 2002 110 2 251 260 10.1016/S0092-8674(02)00825-5 12150932 (Pubitemid 34876552)
15. Nuclear receptors, metabolism, and the circadian clock. X Yang KA Lamia RM Evans, Cold Spring Harb Symp Quant Biol 2007 72 387 394 10.1101/sqb.2007.72. 058 18419296
16. Towards fully automated structure-based function prediction in structural genomics: a case study. JD Watson S Sanderson A Ezersky A Savchenko A Edwards C Orengo A Joachimiak RA Laskowski JM Thornton, Journal of molecular biology 2007 367 5 1511 1522 10.1016/j.jmb.2007.01.063 17316683 (Pubitemid 46420706)
17. Automated prediction of protein function and detection of functional sites from structure. F Pazos MJ Sternberg, Proceedings of the National Academy of Sciences of the United States of America 2004 101 41 14754 14759 10.1073/pnas.0404569101 15456910 (Pubitemid 39410747)
18. The Protein Data Bank. HM Berman J Westbrook Z Feng G Gilliland TN Bhat H Weissig IN Shindyalov PE Bourne, Nucleic acids research 2000 28 1 235 242 10.1093/nar/28.1.235 10592235 (Pubitemid 30047768)
19. Heme protein assemblies. CJ Reedy BR Gibney, Chem Rev 2004 104 2 617 649 10.1021/cr0206115 14871137
20. Design of a novel heme protein with a non-heme globin scaffold. Y Isogai M Ishida, Biochemistry 2009 48 34 8136 8142 10.1021/bi900518q 19601582
21. Design and engineering of an O(2) transport protein. RL Koder JL Anderson LA Solomon KS Reddy CC Moser PL Dutton, Nature 2009 458 7236 305 309 10.1038/nature07841 19295603
22. Design of functional metalloproteins. Y Lu N Yeung N Sieracki NM Marshall, Nature 2009 460 7257 855 862 10.1038/nature08304 19675646
23. Roles of glutamates and metal ions in a rationally designed nitric oxide reductase based on myoglobin. YW Lin N Yeung YG Gao KD Miner S Tian H Robinson Y Lu, Proceedings of the National Academy of Sciences of the United States of America 2010 107 19 8581 8586 10.1073/pnas.1000526107 20421510
24. Design of a heme-binding 4-helix bundle. CT Choma JD Lear MJ Nelson PL Dutton DE Robertson WF Degrado, Journal of the American Chemical Society 1994 116 3 856 865 10.1021/ja00082a005
25. Design and synthesis of multi-haem proteins. DE Robertson RS Farid CC Moser JL Urbauer SE Mulholland R Pidikiti JD Lear AJ Wand WF DeGrado PL Dutton, Nature 1994 368 6470 425 432 10.1038/368425a0 8133888 (Pubitemid 24115348)
26. Development of a heme protein structure-electrochemical function database. CJ Reedy MM Elvekrog BR Gibney, Nucleic acids research 2008 36 Database 307 313 17933771
27. Diversity and conservation of interactions for binding heme in b-type heme proteins. S Schneider J Marles-Wright KH Sharp M Paoli, Nat Prod Rep 2007 24 3 621 630 10.1039/b604186h 17534534 (Pubitemid 46848710)
28. The chemistry and biochemistry of heme c: functional bases for covalent attachment. SE Bowman KL Bren, Nat Prod Rep 2008 25 6 1118 1130 10.1039/b717196j 19030605
29. Structure of a nonheme globin in environmental stress signaling. JW Murray O Delumeau RJ Lewis, Proceedings of the National Academy of Sciences of the United States of America 2005 102 48 17320 17325 10.1073/pnas.0506599102 16301540 (Pubitemid 41740864)
30. Creating functional artificial proteins. R Razeghifard BB Wallace RJ Pace T Wydrzynski, Curr Protein Pept Sci 2007 8 1 3 18 10.2174/138920307779941479 17305556 (Pubitemid 46322265)
31. Elucidation of the heme binding site of heme-regulated eukaryotic initiation factor 2alpha kinase and the role of the regulatory motif in heme sensing by spectroscopic and catalytic studies of mutant proteins. J Igarashi M Murase A Iizuka F Pichierri M Martinkova T Shimizu, J Biol Chem 2008 283 27 18782 18791 10.1074/jbc.M801400200 18450746
32. Involvement of heme regulatory motif in heme-mediated ubiquitination and degradation of IRP2. H Ishikawa M Kato H Hori K Ishimori T Kirisako F Tokunaga K Iwai, Molecular cell 2005 19 2 171 181 10.1016/j.molcel.2005.05.027 16039587 (Pubitemid 41019665)
33. Regulation by heme of mitochondrial protein transport through a conserved amino acid motif. JT Lathrop MP Timko, Science 1993 259 5094 522 525 10.1126/science.8424176 8424176 (Pubitemid 23058711)
34. A novel heme-regulatory motif mediates heme-dependent degradation of the circadian factor period 2. J Yang KD Kim A Lucas KE Drahos CS Santos SP Mury DG Capelluto CV Finkielstein, Molecular and cellular biology 2008 28 15 4697 4711 10.1128/MCB.00236-08 18505821
35. Heme binds to a short sequence that serves a regulatory function in diverse proteins. L Zhang L Guarente, The EMBO journal 1995 14 2 313 320 7835342
36. What is the relationship between the global structures of apo and holo proteins? M Brylinski J Skolnick, Proteins 2008 70 2 363 377 10.1002/prot.21510 17680687
37. Ligand binding-induced conformational changes in riboflavin kinase: structural basis for the ordered mechanism. S Karthikeyan Q Zhou AL Osterman H Zhang, Biochemistry 2003 42 43 12532 12538 10.1021/bi035450t 14580199 (Pubitemid 37337543)
38. Side-chain flexibility in proteins upon ligand binding. R Najmanovich J Kuttner V Sobolev M Edelman, Proteins 2000 39 3 261 268 10.1002/(SICI)1097- 0134(20000515)39:3<261::AID-PROT903.0.CO;2-4 10737948 (Pubitemid 30226508)
39. Side-chain flexibility in protein-ligand binding: the minimal rotation hypothesis. MI Zavodszky LA Kuhn, Protein Sci 2005 14 4 1104 1114 10.1110/ps.041153605 15772311 (Pubitemid 40389381)
40. PSI-2: structural genomics to cover protein domain family space. BH Dessailly R Nair L Jaroszewski JE Fajardo A Kouranov D Lee A Fiser A Godzik B Rost C Orengo, Structure 2009 17 6 869 881 10.1016/j.str.2009.03.015 19523904
41. Heme proteins - diversity in structural characteristics, function, and folding. LJ Smith A Kahraman JM Thornton, Proteins 2010 78 10 2349 2368 10.1002/prot.22747 20544970
42. SCOP: a structural classification of proteins database for the investigation of sequences and structures. AG Murzin SE Brenner T Hubbard C Chothia, Journal of molecular biology 1995 247 4 536 540 7723011
43. PISCES: a protein sequence culling server. G Wang RL Dunbrack Jr, Bioinformatics 2003 19 12 1589 1591 10.1093/bioinformatics/btg224 12912846 (Pubitemid 37038881)
44. His-tag impact on structure. M Carson DH Johnson H McDonald C Brouillette LJ Delucas, Acta Crystallogr D Biol Crystallogr 2007 63 Pt 3 295 301 10.1107/S0907444906052024 17327666 (Pubitemid 46438522)
45. Systematic analysis of short internal indels and their impact on protein folding. R Kim JT Guo, BMC Struct Biol 2010 10 1 24 10.1186/1472-6807-10-24 20684774
46. Mapping PDB chains to UniProtKB entries. AC Martin, Bioinformatics 2005 21 23 4297 4301 10.1093/bioinformatics/bti694 16188924 (Pubitemid 41724310)
47. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. W Kabsch C Sander, Biopolymers 1983 22 12 2577 2637 10.1002/bip.360221211 6667333
48. Interior and surface of monomeric proteins. S Miller J Janin AM Lesk C Chothia, Journal of molecular biology 1987 196 3 641 656 10.1016/0022-2836(87) 90038-6 3681970
49. PROSPECT II: protein structure prediction program for genome-scale applications. D Kim D Xu JT Guo K Ellrott Y Xu, Protein engineering 2003 16 9 641 650 10.1093/protein/gzg081 14560049 (Pubitemid 37314391)
50. Basic local alignment search tool. SF Altschul W Gish W Miller EW Myers DJ Lipman, Journal of molecular biology 1990 215 3 403 410 2231712
51. Crystallographic refinement of ligand complexes. GJ Kleywegt, Acta Crystallogr D Biol Crystallogr 2007 63 Pt 1 94 100 17164531 (Pubitemid 46141484)
52. SuperLigands-a database of ligand structures derived from the Protein Data Bank. E Michalsky M Dunkel A Goede R Preissner, BMC bioinformatics 2005 6 122 10.1186/1471-2105-6-122 15943884
53. FAST: a novel protein structure alignment algorithm. J Zhu Z Weng, Proteins 2005 58 3 618 627 10.1002/prot.20331 15609341 (Pubitemid 40176034)
54. Protein structure alignment by incremental combinatorial extension (CE) of the optimal path. IN Shindyalov PE Bourne, Protein engineering 1998 11 9 739 747 10.1093/protein/11.9.739 9796821 (Pubitemid 28434482)
55. CASTp: computed atlas of surface topography of proteins with structural and topographical mapping of functionally annotated residues. J Dundas Z Ouyang J Tseng A Binkowski Y Turpaz J Liang, Nucleic acids research 2006 34 Web Server 116 118 10.1093/nar/gkl282 16844972
56. Cavities and atomic packing in protein structures and interfaces. S Sonavane P Chakrabarti, PLoS Comput Biol 2008 4 9 1000188 10.1371/journal.pcbi. 1000188 19005575
57. PGH2 degradation pathway catalyzed by GSH-heme complex bound microsomal prostaglandin E2 synthase type 2: the first example of a dual-function enzyme. T Yamada F Takusagawa, Biochemistry 2007 46 28 8414 8424 10.1021/bi700605m 17585783 (Pubitemid 47075978)
58. Product release rather than chelation determines metal specificity for ferrochelatase. AE Medlock M Carter TA Dailey HA Dailey WN Lanzilotta, Journal of molecular biology 2009 393 2 308 319 10.1016/j.jmb.2009.08.042 19703464
59. Cytochrome P450 and the individuality of species. DR Nelson, Archives of biochemistry and biophysics 1999 369 1 1 10 10.1006/abbi.1999.1352 10462435 (Pubitemid 29434533)
60. Molecular-genetic analysis of plant cytochrome P450-dependent monooxygenases. C Chapple, Annu Rev Plant Physiol Plant Mol Biol 1998 49 311 343 10.1146/annurev.arplant.49.1.311 15012237
61. What common structural features and variations of mammalian P450 s are known to date? M Otyepka J Skopalik E Anzenbacherova P Anzenbacher, Biochimica et biophysica acta 2007 1770 3 376 389 17069978 (Pubitemid 46136748)
62. Heme regulatory motifs in heme oxygenase-2 form a thiol/disulfide redox switch that responds to the cellular redox state. L Yi PM Jenkins LI Leichert U Jakob JR Martens SW Ragsdale, J Biol Chem 2009 284 31 20556 20561 10.1074/jbc.M109.015651 19473966
63. Heme mediates derepression of Maf recognition element through direct binding to transcription repressor Bach1. K Ogawa J Sun S Taketani O Nakajima C Nishitani S Sassa N Hayashi M Yamamoto S Shibahara H Fujita K Igarashi, The EMBO journal 2001 20 11 2835 2843 10.1093/emboj/20.11.2835 11387216 (Pubitemid 32938566)
64. Identification of a thiol/disulfide redox switch in the human BK channel that controls its affinity for heme and CO. L Yi JT Morgan SW Ragsdale, J Biol Chem 2010 285 26 20117 20127 10.1074/jbc.M110.116483 20427280
65. Evidence that the heme regulatory motifs in heme oxygenase-2 serve as a thiol/disulfide redox switch regulating heme binding. L Yi SW Ragsdale, J Biol Chem 2007 282 29 21056 21067 10.1074/jbc.M700664200 17540772 (Pubitemid 47099923)
66. The structural basis of gas-responsive transcription by the human nuclear hormone receptor REV-ERBbeta. KI Pardee X Xu J Reinking A Schuetz A Dong S Liu R Zhang J Tiefenbach G Lajoie AN Plotnikov A Botchkarev HM Krause A Edwards, PLoS Biol 2009 7 2 43 10.1371/journal.pbio.1000043 19243223
67. Allostery: absence of a change in shape does not imply that allostery is not at play. CJ Tsai A del Sol R Nussinov, Journal of molecular biology 2008 378 1 1 11 10.1016/j.jmb.2008.02.034 18353365
68. Dynamic energy landscape view of coupled binding and protein conformational change: induced-fit versus population-shift mechanisms. K Okazaki S Takada, Proceedings of the National Academy of Sciences of the United States of America 2008 105 32 11182 11187 10.1073/pnas.0802524105 18678900
69. The role of dynamic conformational ensembles in biomolecular recognition. DD Boehr R Nussinov PE Wright, Nat Chem Biol 2009 5 11 789 796 10.1038/nchembio.232 19841628
70. Kinetics and mechanism of heme-induced refolding of human alpha-globin. Y Leutzinger S Beychok, Proceedings of the National Academy of Sciences of the United States of America 1981 78 2 780 784 10.1073/pnas.78.2.780 6940147 (Pubitemid 11159509)
71. Role of heme in the unfolding and assembly of myoglobin. DS Culbertson JS Olson, Biochemistry 2010 49 29 6052 6063 10.1021/bi1006942 20540498
72. Identification and functions of usefully disordered proteins. AK Dunker CJ Brown Z Obradovic, Unfolded Proteins 2002 62 25 49 full-text (Pubitemid 35204867)
73. Intrinsically unstructured proteins and their functions. HJ Dyson PE Wright, Nat Rev Mol Cell Biol 2005 6 3 197 208 10.1038/nrm1589 15738986 (Pubitemid 40314921)
74. WebLogo: a sequence logo generator. GE Crooks G Hon JM Chandonia SE Brenner, Genome research 2004 14 6 1188 1190 10.1101/gr.849004 15173120 (Pubitemid 38811555)