Comparison of ligand migration and binding in heme proteins of the globin family

doi:10.1088/1674-1056/24/12/128705

中国物理B ›› 2015, Vol. 24 ›› Issue (12): 128705-128705.doi: 10.1088/1674-1056/24/12/128705

• SPECIAL TOPIC—8th IUPAP International Conference on Biological Physics • 上一篇下一篇

Comparison of ligand migration and binding in heme proteins of the globin family

Karin Nienhaus^a, G. Ulrich Nienhaus^{a b c}

a Institute of Applied Physics (APH), Karlsruhe Institute of Technology (KIT), D-76049 Karlsruhe, Germany;
b Institute of Nanotechnology (INT) and Institute of Toxicology and Genetics (ITG), Karlsruhe Institute of Technology (KIT), D-76021 Karlsruhe, Germany;
c Department of Physics, University of Illinois at Urbana-Champaign, Urbana, Il 61801, USA

收稿日期:2015-01-22 修回日期:2015-03-20 出版日期:2015-12-05 发布日期:2015-12-05
通讯作者: G. Ulrich Nienhaus E-mail:uli@illinois.edu

Comparison of ligand migration and binding in heme proteins of the globin family

Karin Nienhaus^a, G. Ulrich Nienhaus^{a b c}

a Institute of Applied Physics (APH), Karlsruhe Institute of Technology (KIT), D-76049 Karlsruhe, Germany;
b Institute of Nanotechnology (INT) and Institute of Toxicology and Genetics (ITG), Karlsruhe Institute of Technology (KIT), D-76021 Karlsruhe, Germany;
c Department of Physics, University of Illinois at Urbana-Champaign, Urbana, Il 61801, USA

Received:2015-01-22 Revised:2015-03-20 Online:2015-12-05 Published:2015-12-05
Contact: G. Ulrich Nienhaus E-mail:uli@illinois.edu

摘要/Abstract

摘要： The binding of small diatomic ligands such as carbon monoxide or dioxygen to heme proteins is among the simplest biological processes known. Still, it has taken many decades to understand the mechanistic aspects of this process in full detail. Here, we compare ligand binding in three heme proteins of the globin family, myoglobin, a dimeric hemoglobin, and neuroglobin. The combination of structural, spectroscopic, and kinetic experiments over many years by many laboratories has revealed common properties of globins and a clear mechanistic picture of ligand binding at the molecular level. In addition to the ligand binding site at the heme iron, a primary ligand docking site exists that ensures efficient ligand binding to and release from the heme iron. Additional, secondary docking sites can greatly facilitate ligand escape after its dissociation from the heme. Although there is only indirect evidence at present, a preformed histidine gate appears to exist that allows ligand entry to and exit from the active site. The importance of these features can be assessed by studies involving modified proteins (via site-directed mutagenesis) and comparison with heme proteins not belonging to the globin family.

关键词: flash photolysis, ligand binding, time-resolved spectroscopy, heme protein

Abstract: The binding of small diatomic ligands such as carbon monoxide or dioxygen to heme proteins is among the simplest biological processes known. Still, it has taken many decades to understand the mechanistic aspects of this process in full detail. Here, we compare ligand binding in three heme proteins of the globin family, myoglobin, a dimeric hemoglobin, and neuroglobin. The combination of structural, spectroscopic, and kinetic experiments over many years by many laboratories has revealed common properties of globins and a clear mechanistic picture of ligand binding at the molecular level. In addition to the ligand binding site at the heme iron, a primary ligand docking site exists that ensures efficient ligand binding to and release from the heme iron. Additional, secondary docking sites can greatly facilitate ligand escape after its dissociation from the heme. Although there is only indirect evidence at present, a preformed histidine gate appears to exist that allows ligand entry to and exit from the active site. The importance of these features can be assessed by studies involving modified proteins (via site-directed mutagenesis) and comparison with heme proteins not belonging to the globin family.

Key words: flash photolysis, ligand binding, time-resolved spectroscopy, heme protein

中图分类号: (Protein-ligand interactions)

87.15.kp

87.64.-t (Spectroscopic and microscopic techniques in biophysics and medical physics) 87.80.-y (Biophysical techniques (research methods))

Karin Nienhaus, G. Ulrich Nienhaus. Comparison of ligand migration and binding in heme proteins of the globin family[J]. 中国物理B, 2015, 24(12): 128705-128705.

Karin Nienhaus, G. Ulrich Nienhaus. Comparison of ligand migration and binding in heme proteins of the globin family[J]. Chin. Phys. B, 2015, 24(12): 128705-128705.

参考文献 79

[1]	Stryer L 1995 Biochemistry, 4th edn. (San Francisco: Freeman Publications)
[2]	Frauenfelder H, Petsko G A and Tsernoglou D 1979 Nature 280 558
[3]	Doster W, Cusack S and Petry W 1989 Nature 337 754
[4]	Parak F G and Nienhaus G U
[5]	Ansari A, Berendzen J, Bowne S F, Frauenfelder H, Iben I E, Sauke T B, Shyamsunder E and Young R D 1985 Proc. Natl. Acad. Sci. USA 82 5000
[6]	Steinbach P J, Ansari A, Berendzen J, Braunstein D, Chu K, Cowen B R, Ehrenstein D, Frauenfelder H, Johnson J B, Lamb D C, Luck S, Mourant J R, Nienhaus G U, Ormos P, Philipp R, Xie A and Young R D 1991 Biochemistry 30 3988
[7]	Frauenfelder H, Sligar S G and Wolynes P G 1991 Science 254 1598
[8]	Nienhaus G U, Müller J D, McMahon B H and Frauenfelder H 1997 Physica D 107 297
[9]	Frauenfelder H, Nienhaus G U and Johnson J B 1991 Ber. Bunsenges. Phys. Chem. 95 272
[10]	Brunori M, Bonaventura J, Bonaventura C, Antonini E and Wyman J 1972 Proc. Natl. Acad. Sci. USA 69 868
[11]	Austin R H, Beeson K W, Eisenstein L, Frauenfelder H and Gunsalus I C 1975 Biochemistry 14 5355
[12]	Nienhaus G U, Frauenfelder H and Parak F 1991 Phys. Rev. B 43 3345
[13]	Alberding N, Austin R H, Beeson K W, Chan S S, Eisenstein L, Frauenfelder H and Nordlund T M 1976 Science 192 1002
[14]	Lamb D C, Prusakov V, Engler N, Ostermann A, Schellenberg P, Parak F G and Nienhaus G U 1998 J. Am .Chem. Soc. 120 2981
[15]	Henry E R, Sommer J H, Hofrichter J and Eaton W A 1983 J. Mol. Biol. 166 443
[16]	Agmon N and Hopfield J J 1983 J. Chem. Phys. 79 2042
[17]	Nienhaus G U, Mourant J R and Frauenfelder H 1992 Proc. Natl. Acad. Sci. USA 89 2902
[18]	McMahon B H, Stojkovic B P, Hay P J, Martin R L and García A E 2000 J. Chem. Phys. 113 6831
[19]	Hartmann H, Zinser S, Komninos P, Schneider R T, Nienhaus G U and Parak F 1996 Proc. Natl. Acad. Sci. USA 93 7013
[20]	Teng T Y, Srajer V and Moffat K 1994 Nat. Struct. Biol. 1 701
[21]	Schlichting I, Berendzen J, Phillips G N Jr and Sweet R M 1994 Nature 371 808
[22]	Srajer V, Teng T, Ursby T, Pradervand C, Ren Z, Adachi S, Schildkamp W, Bourgeois D, Wulff M and Moffat K 1996 Science 274 1726
[23]	Braunstein D P, Chu K, Egeberg K D, Frauenfelder H, Mourant J R, Nienhaus G U, Ormos P, Sligar S G, Springer B A and Young R D 1993 Biophys. J. 65 2447
[24]	Lim M, Jackson T A and Anfinrud P A 1995 Science 269 962
[25]	Lim M, Jackson T A and Anfinrud P A 1997 Nat. Struct. Biol. 4 209
[26]	Scott E E and Gibson Q H 1997 Biochemistry 36 11909
[27]	Tilton R F Jr, Kuntz I D Jr and Petsko G A 1984 Biochemistry 23 2849
[28]	Nienhaus G U, Chu K and Jesse K 1998 Biochemistry 37 6819
[29]	Nienhaus G U, Mourant J R, Chu K and Frauenfelder H 1994 Biochemistry 33 13413
[30]	Nienhaus K, Deng P, Kriegl J M and Nienhaus G U 2003 Biochemistry 42 9633
[31]	Ostermann A, Waschipky R, Parak F G and Nienhaus G U 2000 Nature 404 205
[32]	Chu K, Vojtechovsky J, McMahon B H, Sweet R M, Berendzen J and Schlichting I 2000 Nature 403 921
[33]	Brunori M 2000 Biophys. Chem. 86 221
[34]	Brunori M, Vallone B, Cutruzzola F, Travaglini-Allocatelli C, Berendzen J, Chu K, Sweet R M and Schlichting I 2000 Proc. Natl. Acad. Sci. USA 97 2058
[35]	Schmidt M, Nienhaus K, Pahl R, Krasselt A, Anderson S, Parak F, Nienhaus G U and Srajer V 2005 Proc. Natl. Acad. Sci. USA 102 11704
[36]	Schotte F, Lim M, Jackson T A, Smirnov A V, Soman J, Olson J S, Phillips G N Jr, Wulff M and Anfinrud P A 2003 Science 300 1944
[37]	Hummer G, Schotte F and Anfinrud P A 2004 Proc. Natl. Acad. Sci. USA 101 15330
[38]	Bourgeois D, Vallone B, Schotte F, Arcovito A, Miele A E, Sciara G, Wulff M, Anfinrud P and Brunori M 2003 Proc. Natl. Acad. Sci. USA 100 8704
[39]	Cohen J, Arkhipov A, Braun R and Schulten K 2006 Biophys. J. 91 1844
[40]	Olson J S and Phillips G N Jr 1996 J. Biol. Chem. 271 17593
[41]	Perutz M F and Mathews F S 1966 J. Mol. Biol. 199
[42]	Weber B, Nickel E, Horn M, Nienhaus K and Nienhaus G U 2014 J. Phys. Chem. Lett. 5 756
[43]	Ormos P, Braunstein D, Frauenfelder H, Hong M K, Lin S L, Sauke T B and Young R D 1988 Proc. Natl. Acad. Sci. USA 85 8492
[44]	Nienhaus K and Nienhaus G U 2011 Biochim. Biophys. Acta 1814 1030
[45]	Nienhaus K and Nienhaus G U 2008 Methods Enzymol. 437 347
[46]	Chance M R, Courtney S H, Chavez M D, Ondrias M R and Friedman J M 1990 Biochemistry 29 5537
[47]	Petrich J W, Lambry J C, Kuczera K, Karplus M, Poyart C and Martin J L 1991 Biochemistry 30 3975
[48]	Petrich J W, Poyart C and Martin J L 1988 Biochemistry 27 4049
[49]	Beece D, Eisenstein L, Frauenfelder H, Good D, Marden M C, Reinisch L, Reynolds A H, Sorensen L B and Yue K T 1980 Biochemistry 19 5147
[50]	Nienhaus K, Deng P, Kriegl J M and Nienhaus G U 2003 Biochemistry 42 9647
[51]	Doster W, Beece D, Bowne S F, DiIorio E E, Eisenstein L, Frauenfelder H, Reinisch L, Shyamsunder E, Winterhalter K H and Yue K T 1982 Biochemistry 21 4831
[52]	Scott E E, Gibson Q H and Olson J S 2001 J. Biol. Chem. 276 5177
[53]	Quillin M L, Li T, Olson J S, Phillips G N Jr, Dou Y, Ikeda-Saito M, Regan R, Carlson M, Gibson Q H, Li H and Elber R 1995 J. Mol. Biol. 245 416
[54]	Nienhaus K, Deng P, Olson J S, Warren J J and Nienhaus G U 2003 J. Biol. Chem. 278 42532
[55]	Chiancone E, Elber R, Royer W E Jr, Regan R and Gibson Q H 1993 J. Biol. Chem. 268 5711
[56]	Nienhaus K, Knapp J E, Palladino P, Royer W E Jr and Nienhaus G U 2007 Biochemistry 46 14018
[57]	Knapp J E, Gibson Q H, Cushing L and Royer W E Jr 2001 Biochemistry 40 14795
[58]	Royer W E Jr 1994 J. Mol. Biol. 235 657
[59]	Royer W E Jr, Pardanani A, Gibson Q H, Peterson E S and Friedman J M 1996 Proc. Natl. Acad. Sci. USA 93 14526
[60]	Burmester T, Weich B, Reinhardt S and Hankeln T 2000 Nature 407 520
[61]	Nienhaus K and Nienhaus G U 2007 IUBMB Life 59 490
[62]	Vallone B, Nienhaus K, Brunori M and Nienhaus G U 2004 Proteins 56 85
[63]	Vallone B, Nienhaus K, Matthes A, Brunori M and Nienhaus G U 2004 Proc. Natl. Acad. Sci. USA 101 17351
[64]	Kriegl J M, Bhattacharyya A J, Nienhaus K, Deng P, Minkow O and Nienhaus G U 2002 Proc. Natl. Acad. Sci. USA 99 7992
[65]	Nienhaus K, Kriegl J M and Nienhaus G U 2004 J. Biol. Chem. 279 22944
[66]	Lutz S, Nienhaus K, Nienhaus G U and Meuwly M 2009 J. Phys. Chem. B 113 15334
[67]	Nienhaus K, Lutz S, Meuwly M and Nienhaus G U 2010 ChemPhysChem 11 119
[68]	Lamb D C, Arcovito A, Nienhaus K, Minkow O, Draghi F, Brunori M and Nienhaus G U 2004 Biophys. Chem. 109 41
[69]	Nienhaus G U and Nienhaus K 2002 J. Biol. Phys. 28 163
[70]	Olson J S, Soman J and Phillips G N Jr 2007 IUBMB Life 59 552
[71]	Nienhaus K, Nickel E, Lu C, Yeh S R and Nienhaus G U 2011 IUBMB Life 63 153
[72]	Nienhaus K, Zosel F and Nienhaus G U 2012 J. Phys. Chem. B 116 12180
[73]	Nienhaus K, Maes E M, Weichsel A, Montfort W R and Nienhaus G U 2004 J. Biol. Chem. 279 39401
[74]	Ringe D, Petsko G A, Kerr D E and Ortiz de Montellano P R 1984 Biochemistry 3 2
[75]	Johnson K A, Olson J S and Phillips G N Jr 1989 J. Mol. Biol. 207 459
[76]	Case D A and Karplus M 1979 J. Mol. Biol. 132 343
[77]	Huang X and Boxer S G 1994 Nat. Struct. Biol. 1 226
[78]	Nienhaus K, Ostermann A, Nienhaus G U, Parak F G and Schmidt M 2005 Biochemistry 44 5095
[79]	Srajer V, Ren Z, Teng T Y, Schmidt M, Ursby T, Bourgeois D, Pradervand C, Schildkamp W, Wulff M and Moffat K 2001 Biochemistry 40 13802

Comparison of ligand migration and binding in heme proteins of the globin family

Comparison of ligand migration and binding in heme proteins of the globin family

RichHTML

PDF (PC)

赞

可视化

摘要/Abstract

引用本文

使用本文

参考文献 79

相关文章 4

Metrics

本文评价

推荐阅读 0

[1]	王洋, 王亭, 李选选, 金泽宇, 汤雷翰, 刘海广. A computational study of the chemokine receptor CXCR1 bound with interleukin-8[J]. 中国物理B, 2018, 27(3): 38702-038702.
[2]	宋海英, 李辉, 张艳杰, 谷鹏, 刘海云, 李维, 刘勋, 刘世炳. Time-resolved spectroscopy for 5s'⁴D_7/2 state transitions undergoing electron-ion recombination in femtosecond laser-produced copper plasma[J]. 中国物理B, 2017, 26(12): 124208-124208.
[3]	闫炜, 王海龙, 赵建华, 张新惠. Ultrafast optical probe of coherent acoustic phonons in Co₂MnAl Heusler film[J]. 中国物理B, 2017, 26(1): 16802-016802.
[4]	马红, 马国宏, 王文军, 高学喜, 马洪良. Size-dependent optical properties and carriers dynamics in CdSe/ZnS quantum dots[J]. 中国物理B, 2008, 17(4): 1280-1285.