Spectral characterization of the recombinant mouse tumor suppressor 101F6 protein

European Biophysics Journal

Volumn 39, Issue 8, 2010, Pages 1129-1142

  Bérczi, Alajos ^a   Desmet, Filip ^b   Van Doorslaer, Sabine ^b   Asard, Han ^b  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

101F6 protein; Ascorbate; Auto oxidation; Cyt b561 protein; EPR; Raman; UV VIS

Indexed keywords

101F6 PROTEIN, MOUSE; CYTOCHROME B; DITHIONITE; HEME; RECOMBINANT PROTEIN; TUMOR SUPPRESSOR PROTEIN; CYB561D2 PROTEIN, MOUSE; MEMBRANE PROTEIN; MICELLE;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CHEMISTRY; ELECTRON SPIN RESONANCE; GENETICS; METHODOLOGY; MICELLE; MOUSE; OXIDATION REDUCTION REACTION; RAMAN SPECTROMETRY; SACCHAROMYCES; SEQUENCE HOMOLOGY; SPECTROSCOPY; TEMPERATURE; ULTRAVIOLET RADIATION; PROCEDURES;

AMINO ACID SEQUENCE; ANIMALS; CYTOCHROME B GROUP; DITHIONITE; ELECTRON SPIN RESONANCE SPECTROSCOPY; HEME; MICE; MICELLES; OXIDATION-REDUCTION; RECOMBINANT PROTEINS; SACCHAROMYCES; SEQUENCE HOMOLOGY, AMINO ACID; SPECTRUM ANALYSIS; SPECTRUM ANALYSIS, RAMAN; TEMPERATURE; TUMOR SUPPRESSOR PROTEINS; ULTRAVIOLET RAYS; MEMBRANE PROTEINS;

EID: 77955654011     PISSN: 01757571     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00249-009-0564-4     Document Type: Article

References (75)

1. DK Apps JG Pryde JH Phillips 1980 Cytochrome b561 is identical with chromomembrin B, a major polypeptide of chromaffin granule membranes Neuroscience 5 2279 2287 10.1016/0306-4522(80)90143-8 1:CAS:528: DyaL3MXmtVWksw%3D%3D 7465055 (Pubitemid 11200024)
2. DK Apps MD Boisclair FS Gavine GW Pettigrew 1984 Unusual redox behaviour of cytochrome b-561 from bovine chromaffin granule membranes Biochim Biophys Acta 764 8 16 10.1016/0005-2728(84)90134-8 1:CAS:528:DyaL2cXotFGitQ%3D%3D 6696883
3. A Asada T Kusakawa H Orii K Agata K Watanabe M Tsubaki 2002 Planarian cytochrome b561: conservation of a six trans-membrane structure and localization along the central and peripheral nervous system J Biochem 131 175 182 1:CAS:528:DC%2BD38XjtVOhtL0%3D 11820929
4. H Asard J Kapila W Verelst A Bérczi 2001 Higher-plant plasma membrane cytochrome b561: a protein in search of a function Protoplasma 217 77 93 10.1007/BF01289417 1:CAS:528:DC%2BD3MXotFGgsbY%3D 11732342 (Pubitemid 32657050)
5. GT Babcock WR Widger WA Cramer WA Oertling JG Metz 1985 Axial ligands of chloroplast cytochrome b-559: identification and requirement for a heme-cross-linked polypeptide structure Biochemistry 24 3638 3645 10.1021/bi00335a036 1:CAS:528:DyaL2MXktlelt7o%3D 2994713
6. PD Baker EP Nerou MR Cheesman AJ Thomson P de Oliveira HAO Hill 1996 Bis-Methionine ligation to heme iron in mutants of cytochrome b. 1. Spectroscopic and electrochemical characterization of the electronic properties Biochemistry 35 13618 13626 10.1021/bi961127x (Pubitemid 26359174)
7. D Bashtovyy A Bérczi H Asard T Páli 2003 Structure prediction for di-heme cytochrome b561 protein family Protoplasma 221 31 40 10.1007/s00709-002-0065-0 1:CAS:528:DC%2BD3sXmvVWqurw%3D 12768339 (Pubitemid 36658581)
8. A Bérczi H Asard 2008 Expression and purification of the recombinant mouse tumor suppressor cytochrome b561 protein Acta Biol Szeged 52 257 265
9. A Bérczi D Su M Lakshminarasimhan A Vargas H Asard 2005 Heterologous expression and site-directed mutagenesis of an ascorbate-reducible cytochrome b561 Arch Biochem Biophys 443 82 92 10.1016/j.abb.2005.09.006 16256064 (Pubitemid 41562329)
10. A Bérczi D Su H Asard 2007 An Arabidopsis cytochrome b561 with trans-membrane ferrireductase capability FEBS Lett 581 1505 1508 10.1016/j.febslet.2007.03.006 17376442 (Pubitemid 46452628)
11. Blumberg WE, Peisach J (1971) A unified theory for low-spin forms of all ferric heme proteins as studied by EPR. In: Chance B, Yonetani T, Mildvan AS (eds) Probes of structure and function of macromolecules and membranes. Probes of enzymes and hemoproteins, vol 2. Academic Press, New York, pp 215-229
12. 5 Eur J Biochem 2 361 365 10.1111/j.1432-1033.1967.tb00146.x 1:CAS:528:DyaF2sXltVGgsL4%3D 4294947
13. 4 from the purple sulfur photosynthetic bacterium Thiocapsa roseopersicina Arch Biochem Biophys 467 174 184 10.1016/j.abb.2007.07. 031 1:CAS:528:DC%2BD2sXht12gurzJ 17931594 (Pubitemid 350050887)
14. JF Cerda-Colon E Silfa J Lopez-Garriga 1998 CO-dependent activity controlling mechanism of heme-containing CO-sensor protein, NPAS2 J Am Chem Soc 120 9312 9317 10.1021/ja972654m 1:CAS:528:DyaK1cXlsVyqt7k%3D (Pubitemid 28452705)
15. MR Cheesman AJ Thomson C Greenwood GR Moore F Kadir 1990 Bis-methionine axial ligation of haem in bacterioferritin from Pseudomonas aeruginosa Nature 346 771 773 10.1038/346771a0 1:CAS:528:DyaK3cXlsVOms7w%3D 2167456 (Pubitemid 20251094)
16. MR Cheesman FHA Kadir J Al-Basseet F Al-Massad J Farrar C Greenwood AJ Thomson GF Moore 1992 E.P.R. and magnetic circular dichroism spectroscopic characterization of bacterioferritin from Pseudomonas aeruginosa and Azotobacter vinelandii Biochem J 286 361 367 1:CAS:528:DyaK38XlsVGltbg%3D 1326939
17. S Dewilde B Ebner E Vinck K Gilany T Hankeln T Burmester J Kreiling C Reinisch JR Vanfleteren L Kiger MC Marden C Hundahl A Fago S Van Doorslaer L Moens 2006 The nerve hemoglobin of the bivalve mollusc Spisula solidissima: molecular cloning, ligand binding studies, and phylogenetic analysis J Biol Chem 281 5364 5372 10.1074/jbc.M509486200 1:CAS:528:DC%2BD28XhvVejs78%3D 16352603 (Pubitemid 43847630)
18. T Flatmark M Grønberg 1981 Cytochrome b-561 of the bovine adrenal chromaffin granules. Molecular weight and hydrodynamic properties in micellar solutions of Triton X-100 Biochem Biophys Res Commun 99 292 301 10.1016/0006-291X(81)91744-7 1:CAS:528:DyaL3MXhsFaitrc%3D 7236267
19. 561 of the bovine adrenal chromaffin granules. A high potential b-type cytochrome Biochim Biophys Acta 253 487 491 10.1016/0005-2728(71)90052-1 1:CAS:528:DyaE38Xkt12rsg%3D%3D 4332308
20. PJ Fleming UM Kent 1991 Cytochrome b561, ascorbic acid, and transmembrane electron transfer Am J Clin Nutr 54 1173S 1178S 1:CAS:528:DyaK38Xitlyn 1962566
21. D Griesen D Su A Bérczi H Asard 2004 Localization of an ascorbate-reducible cytochrome b561 in the plant tonoplast Plant Physiol 134 726 734 10.1104/pp.103.032359 1:CAS:528:DC%2BD2cXhs1Cntrs%3D 14730083 (Pubitemid 38261545)
22. B Hagihara R Oshino T Iizuka 1974 Studies on low temperature spectra of respiratory pigments. II. Spectra of cytochromes in respiratory systems between liquid helium and room temperatures J Biochem 75 45 51 1:CAS:528: DyaE2cXht12msb8%3D 4363684
23. ER Henry J Hofrichter 1992 Singular value decomposition: application to analysis of experimental data Meth Enzymol 210 129 193 10.1016/0076-6879(92) 10010-B 1:CAS:528:DyaK3sXjt1Wg
24. S Hu IK Morris JP Singh KM Smith TG Spiro 1993 Complete assignment of cytochrome c resonance Raman spectra via enzymatic reconstitution with isotopically labeled hemes J Am Chem Soc 115 12446 12458 10.1021/ja00079a028 1:CAS:528:DyaK2cXjtFWl
25. S Hu KM Smith TG Spiro 1996 Assignment of protoheme resonance Raman spectrum by heme labeling in myoglobin J Am Chem Soc 118 12638 12646 10.1021/ja962239e 1:CAS:528:DyaK28XntFSgtb4%3D (Pubitemid 27041986)
26. 558 J Biol Chem 266 1627 1634 1:CAS:528:DyaK3MXhtFOiurg%3D 1846361
27. 5 Biochim Biophys Acta 226 15 24
28. HA Jahn E Teller 1937 Stability of polyatomic molecules in degenerate electronic states. I. Orbital degeneracy Proc R Soc Lond Ser A 161 220 235 10.1098/rspa.1937.0142 1:CAS:528:DyaA1cXht1Y%3D
29. L Ji M Nizhizaki B Gao D Burbee M Kondo C Kamibayashi K Xu N Yen 2002 Expression of several genes in the human chromosome 3p21.3 homozygous deletion region by an adenovirus vector results in tumor suppressor activities in vitro and in vivo Cancer Res 62 2715 2720 1:CAS:528:DC%2BD38XjtlGrtL0%3D 11980673
30. YA Kamensky G Palmer 2001 Chromaffin granule membranes contain at least three heme centers: direct evidence from EPR and absorption spectroscopy FEBS Lett 491 119 122 10.1016/S0014-5793(01)02173-1 1:CAS:528:DC%2BD3MXhsFShsLw%3D 11226432 (Pubitemid 32172014)
31. Y Kamensky W Liu A-L Tsai RJ Kulmacz G Plamer 2007 Axial ligation and stoichiometry of heme centers in adrenal cytochrome b561 Biochemistry 46 8647 8658 10.1021/bi700054g 1:CAS:528:DC%2BD2sXntVyjt7g%3D 17602662 (Pubitemid 47106115)
32. PM Kelley D Njus 1986 Cytochrome b561 spectral changes associated with electron transfer in chromaffin-vesicle ghosts J Biol Chem 261 6429 6432 1:CAS:528:DyaL28Xit1Sqs7Y%3D 3700398
33. 561 catalyzes transmembrane electron transfer for dopamine β-hydroxylase and peptidyl glycine α-amidating monooxygenase activities in reconstituted systems J Biol Chem 262 8174 8178 1:CAS:528:DyaL2sXksFCksLk%3D 3597367
34. GN La Mar H Toi R Krishnamoorthi 1984 Proton NMR investigation of the rate and mechanism of heme rotation in sperm whale myoglobin: evidence for intramolecular reorientation about a heme two-fold axis J Am Chem Soc 106 6395 6401 10.1021/ja00333a050 1:CAS:528:DyaL2cXls1Gktrc%3D
35. Leenstra WR (1979) The triplet state of porphyrins. Ph.D. Thesis, University of Washington, Seattle, WA, USA
36. MI Lerman JD Minna 2000 The 630-kb lung cancer homozygous deletion region on human chromosome 3p21.3: identification and evaluation of the resident candidate tumor suppressor genes Cancer Res 60 6116 6133 1:CAS:528: DC%2BD3cXotV2lsbw%3D 11085536
37. W Liu Y Kamensky R Kakkar E Foley RJ Kulmacz G Palmer 2005 Purification and characterization of bovine adrenal cytochrome b561 expressed in insect and yeast cell systems Protein Expr Purif 40 429 439 10.1016/j.pep.2004.12.027 1:CAS:528:DC%2BD2MXit1CjsLo%3D 15766887 (Pubitemid 40335928)
38. 561 Protein Expr Purif 56 145 152 10.1016/j.pep.2007.04. 010 1:CAS:528:DC%2BD2sXht1anur3P 17521920 (Pubitemid 47633215)
39. W Liu CE Rogge GFZ da Silva VP Shinkarev A-L Tsai Y Kamensky G Palmer RJ Kulmacz 2008 His92 and His110 selectively affect different heme centers of adrenal cytochrome b561 Biochim Biophys Acta 1777 1218 1228 10.1016/j.bbabio. 2008.04.039 1:CAS:528:DC%2BD1cXpvF2qu78%3D 18501187
40. BS Lou JK Snyder P Marshall JS Wang G Wu RJ Kulmacz AL Tsai J Wang 2000 Resonance Raman studies indicate a unique heme active site in prostaglandin H synthase Biochemistry 39 12424 12434 10.1021/bi001257c 1:CAS:528: DC%2BD3cXmtlSis7Y%3D 11015223
41. MAK Markwell SB Haas LL Bieber NE Tolbert 1978 A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples Anal Biochem 87 206 210 10.1016/0003-2697(78)90586-9 1:CAS:528:DyaE1cXktF2mt7w%3D 98070
42. AT McKie D Barrow GO Latunde-Dada A Rolfs G Sager E Mudaly M Mudaly C Richardson D Barlow A Bomford RJ Peters KB Raja S Shirali MA Hediger F Farzaneh RJ Simpson 2001 As iron-regulated ferric reductase associated with the absorption of dietary iron Science 291 1755 1759 10.1126/science.1057206 1:CAS:528:DC%2BD3MXhslSkurY%3D 11230685 (Pubitemid 32198974)
43. McKnight J, Cheesman MR, Reed CA, Orosz R, Thomson AJ (1991) Comparative study of the optical and magnetic circular dichroism spectra of bis-thioether and -imidazole complexes of iron(III) tetraphenyl and octaethyl-porphyrin. Models of haem coordination in bacterioferritins. J Chem Soc Dalton Trans 1991(8):1887-1894
44. 561, in the reduction of ferric ions J Biochem 142 699 705 10.1093/jb/mvm185 1:CAS:528:DC%2BD1cXkvV2jt7o%3D 17938141 (Pubitemid 351197704)
45. D Njus PM Kelley 1993 The secretory-vesicle ascorbate-regenerating system: a chain of concerted H+/e(-)-transfer reactions Biochim Biophys Acta 1144 235 248 10.1016/0005-2728(93)90108-R 1:CAS:528:DyaK2cXivVOn 8399278 (Pubitemid 23290251)
46. O Ohtani A Iwamaru W Deng K Ueda G Wu G Jayachandran S Kondo EN Atkinson JD Minna JA Roth L Ji 2007 Tumor suppressor 101F6 and ASC synergistically and selectively inhibit non-small cell lung cancer growth by caspase-independent apoptosis and autophagy Cancer Res 67 6293 6303 10.1158/0008-5472.CAN-06-3884 1:CAS:528:DC%2BD2sXnsVyqt7Y%3D 17616688 (Pubitemid 47037512)
47. RG Pearson 1975 Concerning Jahn-Teller effects Proc Natl Acad Sci USA 72 2104 2106 10.1073/pnas.72.6.2104 1:CAS:528:DyaE2MXkvVOmt74%3D 16592247
48. Peisach J (1998) EPR of metalloproteins: truth tables revisited. In: Eaton GR, Eaton SS, Salikov K (eds) Foundations of modern EPR, 1st edn. World Scientific Publishing, Singapore, pp 346-360
49. J Peisach WE Blumberg 1974 Structural implications derived from the analysis of electron paramagnetic resonance spectra of natural and artificial copper proteins Arch Biochem Biophys 165 691 708 10.1016/0003-9861(74)90298-7 1:CAS:528:DyaE2MXntVSjtQ%3D%3D 4374138
50. CP Ponting 2001 Domain homologues of dopamine β-hydroxylase and ferric reductase: roles for iron metabolism in neurodegenerative disorders Human Mol Gen 10 1853 1858 10.1093/hmg/10.17.1853 1:CAS:528:DC%2BD3MXntFCitbg%3D
51. R Quinn JS Valentine MP Byrn CE Strouse 1987 Electronic structure of low-spin ferric porphyrins: a single-crystal EPR and structural investigation of the influence of axial ligand orientation and the effects of pseudo-Jahn-Teller distortion J Am Chem Soc 109 3301 3308 10.1021/ja00245a019 1:CAS:528: DyaL2sXit1Cqs7k%3D
52. Y Ran H Zhu M Liu M Fabian JS Olson R Aranda IV GN Phillips DM Dooley B Lei 2007 Bis methionine ligation to heme iron in the streptococcal cell surface protein Shp facilitates rapid hemin transfer to HtsA of the HtsABC transporter J Biol Chem 282 31380 31388 10.1074/jbc.M705967200 1:CAS:528:DC%2BD2sXhtFykurjL 17699155 (Pubitemid 350044855)
53. MC Recuenco M Fujito M Rahman Y Sakamoto F Takeuchi M Tsubaki 2009 Functional expression and characterization of human 101F6 protein, a homologue of cytochrome b561 and a candidate tumor suppressor gene product Biofactors 34 219 230 10.1002/biof.5520340306 19734123
54. KS Reddy PJ Angiolillo WW Wright M Laberge JM Vanderkooi 1996 Spectral splitting in the α (Q0, 0) absorption band of ferrous cytochrome c and other heme proteins Biochemistry 35 12820 12830 10.1021/bi960895l 1:CAS:528:DyaK28XlsVyntLs%3D 8841125 (Pubitemid 26337336)
55. JM Shifman BR Gibney RE Sharp PL Dutton 2000 Heme redox potential control in de novo designed four-α-helix bundle proteins Biochemistry 39 14813 14821 10.1021/bi000927b 1:CAS:528:DC%2BD3cXnslaqsLw%3D 11101297
56. RI Shrager 1986 Chemical transitions measured by spectra and resolved using singular value decomposition Chem Intell Lab Syst 1 59 70 10.1016/0169-7439(86)80026-0 1:CAS:528:DyaL2sXnsFeiug%3D%3D
57. S Stoll A Schweiger 2006 EasySpin, a comprehensive software package for spectral simulation and analysis in EPR J Magn Reson 178 42 55 10.1016/j.jmr.2005.08.013 1:CAS:528:DC%2BD2MXht12it7bE 16188474 (Pubitemid 41774010)
58. 561 are ascorbate dependent ferrireductases FEBS J 273 3722 3734 10.1111/j.1742-4658. 2006.05381.x 1:CAS:528:DC%2BD28XovFynsbo%3D 16911521 (Pubitemid 44166653)
59. F Takeuchi K Kobayashi S Tagawa M Tsubaki 2001 Ascorbate inhibits the carbethoxylation of two histidyl and one tyrosyl residues indispensable for the transmembrane electron transfer reaction of cytochrome b561 Biochemistry 40 4067 4076 10.1021/bi002240x 1:CAS:528:DC%2BD3MXhsFKht7k%3D 11300787 (Pubitemid 32280444)
60. F Takeuchi H Hori E Obayashi Y Shiro M Tsubaki 2004 Properties of two distinct centers of cytochrome b561 from bovine chromaffin vesicles studied by EPR, resonance Raman, and ascorbate reduction assay J Biochem 135 53 64 10.1093/jb/mvh006 1:CAS:528:DC%2BD2cXjt1Smu7w%3D 14999009 (Pubitemid 38405161)
61. 2g hole model to the directional properties of the g-tensor, and a new method for calculating the ligand field parameters Biochim Biophys Acta 491 137 149 1:CAS:528:DyaE2sXhvVSiuro%3D 191085
62. M Teixeira AP Campos AP Aguiar HS Costa H Santos DL Turner AV Xavier 1993 Pitfalls in assigning heme axial coordination by EPR. C-type cytochromes with atypical Met-His ligation FEBS Lett 317 233 236 10.1016/0014-5793(93)81282-5 1:CAS:528:DyaK3sXhs1Cms7Y%3D 8381094 (Pubitemid 23045795)
63. SN Terekhov SG Kruglik 1995 Photoreduction of ferric-tetraphenylporphyrin in oxygen-containing solvents revealed by resonance Raman and absorption spectroscopy Chem Phys Lett 245 268 272 10.1016/0009-2614(95)01004-S 1:CAS:528:DyaK2MXptVegsbc%3D
64. M Tsubaki M Nakayama E Okuyam Y Ichikawa H Hori 1997 Existence of two heme B centers in cytochrome b561 from bovine adrenal chromaffin vesicles as revealed by a new purification procedure and EPR spectroscopy J Biol Chem 272 23206 23210 10.1074/jbc.272.37.23206 1:CAS:528:DyaK2sXmt1Wju7k%3D 9287327 (Pubitemid 27392454)
65. M Tsubaki F Takeuchi N Nakanashi 2005 Cytochrome b561 protein family: expanding roles and versatile transmembrane electron transfer abilities as predicted by a new classification system and protein sequence motif analyses Biochim Biophys Acta 1753 174 190 1:CAS:528:DC%2BD2MXht1Ghtr7J 16169296
66. GE Tusnády I Simon 1998 Principles governing amino acid composition of integral membrane proteins: application to topology prediction J Mol Biol 283 489 506 10.1006/jmbi.1998.2107 9769220 (Pubitemid 28470424)
67. GE Tusnády I Simon 2001 The HMMTOP transmembrane topology prediction server Bioinformatics 17 849 850 10.1093/bioinformatics/17.9.849 11590105
68. T Uchida E Sato A Sato I Sagami T Shimizu T Kitagawa 2005 CO-dependent activity-controlling mechanism of heme-containing CO-sensor protein, neuronal PAS domain protein 2 J Biol Chem 280 21358 21368 10.1074/jbc.M412350200 1:CAS:528:DC%2BD2MXks1elsb8%3D 15797872 (Pubitemid 40805699)
69. W Verelst H Asard 2003 A phylogenetic study of cytochrome b561 proteins Genome Biol 4 R38 10.1186/gb-2003-4-6-r38 12801412
70. GC Wagner RJ Kassner 1975 Spectroscopic properties of low-spin ferrous heme complexes and heme proteins at 77°K Biochem Biophys Res Commun 63 385 391 10.1016/0006-291X(75)90700-7 1:CAS:528:DyaE2MXktVaktbs%3D 164862
71. LM Wakefield AEG Cass GK Radda 1984 Isolation of a membrane protein by chromatofocusing: Cytochrome b-561 of the adrenal chromaffin granule J Biochem Biophys Methods 9 331 341 10.1016/0165-022X(84)90017-4 1:CAS:528: DyaL2cXlvVOhsb0%3D 6491155
72. FA Walker 1999 Magnetic spectroscopic (EPR, ESEEM, Mössbauer, MCD and NMR) studies of low-spin ferriheme centers and their corresponding heme proteins Coord Chem Rev 185-186 471 534 10.1016/S0010-8545(99)00029-6
73. DF Wilson 1967 Effect of temperature on the spectral properties of some ferrocytochromes Arch Biochem Biophys 121 757 768 10.1016/0003-9861(67)90065-3 1:CAS:528:DyaF2sXkvVOku78%3D 6078101
74. D Zhang D Su A Bérczi A Vargas H Asard 2006 An ascorbate-reducible cytochrome b561 is localized in macrophage lysosomes Biochim Biophys Acta 1760 1903 1913 1:CAS:528:DC%2BD28XhtF2qurbM 16996694 (Pubitemid 44692367)
75. Zopellaro G, Bren KL, Ensign AA, Herbitz E, Kaur R, Hersleth HP, Ryde U, Hederstedt L, Andersson KK (2009) Studies of ferric heme proteins with highly anisotropic/highly axial low spin (S = 1/2) electron paramagnetic resonance signals with bis-histidine and histidine-methionine axial iron coordination. Biopolymers. doi: 10.1002/bip.21267