Picosecond primary structural transition of the heme is retarded after nitric oxide binding to heme proteins

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 31, 2010, Pages 13678-13683

  Kruglik, Sergei G ^a,b   Yoo, Byung Kuk ^a   Franzen, Stefan ^c   Vos, Marten H ^a   Martin, Jean Louis ^a   Negrerie, Michel ^a  

^a LABORATOIRE D OPTIQUE ET BIOSCIENCES   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Allostery; Structural dynamics; Time resolved raman spectroscopy

Indexed keywords

CYTOCHROME C; GLOBIN; HEME; HEMOGLOBIN; HEMOPROTEIN; HISTIDINE; IRON; MYOGLOBIN; NITRIC OXIDE;

ARTICLE; HYDROGEN BOND; PHOTOLYSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STRUCTURE; RAMAN SPECTROMETRY; ALLOSTERISM; CHEMISTRY; GENETICS; KINETICS; METABOLISM; MUTATION; TIME;

ALLOSTERIC REGULATION; HEME; HEMOGLOBINS; HYDROGEN BONDING; KINETICS; MUTATION; MYOGLOBIN; NITRIC OXIDE; PROTEIN BINDING; TIME FACTORS;

EID: 77956390441     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0912938107     Document Type: Article

References (47)

1. Ignarro LJ, Buga GM, Wood KS, Byrns RE, Chaudhuri G (1987) Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc Natl Acad Sci USA 84:9265-9269.
2. Knowles RG, Palacios M, Palmer RMJ, Moncada S (1989) Formation of nitric oxide from L-arginine in the central nervous system - A tranduction mechanism for stimulation of the soluble guanylate cyclase. Proc Natl Acad Sci USA 86:5159-5162. (Pubitemid 19182253)
3. Verma A, Hirsch DJ, Glatt CE, Ronnet GV, Snyder SH (1993) Carbon monoxide - a putative neuronal messenger. Science 259:381-384. (Pubitemid 23055683)
4. Kim HP, Ryter SW, Choi AMK (2006) CO as a cellular signaling molecule. Annu Rev Pharmacol Toxicol 46:411-449.
5. Ghosh A, ed. (2008) The Smallest Biomolecules: Diatomics and Their Interactions with Heme Proteins (Elsevier, Amsterdam).
6. Brunori M (2001) Nitric oxide moves myoglobin centre stage. Trends Biochem Sci 26:209-210.
7. Brunori M, Vallone B (2006) A globin for the brain. FASEB J 20:2192-2197.
8. Monod J, Wyman J, Changeux JP (1965) On nature of allosteric transitions - a plausible model. J Mol Biol 12:88-118.
9. Perutz MF (1970) Stereochemistry of cooperative effects in haemoglobin. Nature 228:726-793.
10. Perutz MF, Wilkinson AJ, Paoli M, Dodson GG (1998) The stereochemical mechanism of the cooperative effects in hemoglobin revisited. Annu Rev Biophys Biomol Struct 27:1-34. (Pubitemid 28286007)
11. Franzen S, Lambry JC, Bohn B, Poyart C, Martin JL (1994) Direct evidence for the role of heme doming as the primary event in the cooperative transition of hemoglobin. Nat Struct Biol 1:230-233. (Pubitemid 24974843)
12. Zhu L, Sage JT, Champion PM (1994) Observation of coherent reaction dynamics in heme-proteins. Science 266:629-632. (Pubitemid 24363518)
13. Kachalova GS, Popov AN, Bartunik HD (1999) A steric mechanism for inhibition of CO binding to heme proteins. Science 284:473-476.
14. Vos MH (2008) Ultrafast dynamics of ligands within heme proteins. Biochim Biophys Acta Bioenergetics 1777:15-31.
15. Ionascu D, et al. (2005) Temperature-dependent studies of NO recombination to heme and heme proteins. J Am Chem Soc 127:16921-16934. (Pubitemid 41772852)
16. Lim MH, Jackson TA, Anfinrud PA (1997) Ultrafast rotation and trapping of carbon monoxide dissociated from myoglobin. Nat Struct Biol 4:209-214.
17. Kim S, Jin G, Lim M (2004) Dynamics of geminate recombination of NO with myoglobin in aqueous solution probed by femtosecond mid-IR spectroscopy. J Phys Chem B 108:20366-20375.
18. Mizutani Y, Kitagawa T (1997) Direct observation of cooling of heme upon photodissociation of carbonmonoxy myoglobin. Science 278:443-446.
19. Findsen EW, Friedman JM, Ondrias MR, Simon SR (1985) Picosecond time resolved resonance Raman studies of hemoglobin - implications for reactivity. Science 229:661-665.
20. Schlichting I, Berendzen J, Phillips GN, Sweet RM (1994) Crystal structure of photolyzed caronmonoxy-myoglobin. Nature 371:808-812.
21. Schotte F, et al. (2003) Watching a protein as it functions with 150-ps time-resolved X-ray crystallography. Science 300:1944-1947.
22. Bourgeois D, et al. (2006) Extended subnanosecond structural dynamics of myoglobin revealed by Laue crystallography. Proc Natl Acad Sci USA 103:4924-4929.
23. Schotte F, Soman J, Olson JS, Wulff M, Anfinrud PA (2004) Picosecond time-resolved X-ray crystallography: probing protein function in real time. J Struct Biol 147:235-246. (Pubitemid 39144389)
24. Kruglik SG, et al. (2007) Subpicosecond oxygen trapping in the heme pocket of the oxygen sensor FixL observed by time-resolved resonance Raman spectroscopy. Proc Natl Acad Sci USA 104:7408-7413.
25. Mizutani Y, Kitagawa T (2001) Ultrafast structural relaxation of myoglobin following photodissociation of carbon monoxide probed by time-resolved resonance Raman spectroscopy. J Phys Chem B 105:10992-10999.
26. Kitagawa T, Li X-Y (1988) Heme protein structure and the iron-histidine stretching mode. Biological Applications of Raman Spectroscopy, ed TG Spiro (Wiley, New York), 3, pp 97-131.
27. Stavrov SS (1993) The effect of iron displacement out of the porphyrin plane on the resonance Raman spectra of heme-proteins and iron porphyrins. Biophys J 6:1942-1950.
28. Negrerie M, Cianetti S, Vos MH, Martin JL, Kruglik SG (2006) Photoinduced coordination dynamics of cytochrome c: Ferrous versus ferric species studied by time-resolved resonance Raman and transient absorption spectroscopies. J Phys Chem B 110:12766-12781.
29. Negrerie M, et al. (2006) Role of heme iron coordination and protein structure in the dynamics and geminate rebinding of nitric oxide to H93G myoglobin: Implications for NO-sensors. J Biol Chem 281:10389-10398.
30. Ye X, et al. (2003) Investigations of heme protein absorption line shapes, vibrational relaxation, and resonance Raman scattering on ultrafast time scales. J Phys Chem A 107:8156-8165.
31. Spiro TG (1988) Resonance Raman spectroscopy of metalloporphyrins. Biological Applications of Raman Spectroscopy, ed TG Spiro (Wiley, New York), 3, pp 1-37.
32. Shreve AP, Franzen S, Simpson MC, Dyer RB (1999) Dependence of NO recombination dynamics in horse myoglobin on solution glycerol content. J Phys Chem B 103:7969-7975.
33. Haddad RE, et al. (2003) Origin of the red shifts in the optical absorption bands of nonplanar tetraalkylporphyrins. J Am Chem Soc 125:1253-1268.
34. Stavrov SS (2001) Optical absorption band III of deoxyheme proteins as a probe of their structure and dynamics. Chem Phys 271:145-154.
35. 2, NO, and CO by electrostatic interactions with the bound ligand. J Biol Inorg Chem 2:544-552.
36. Miksovska J, Horsa S, Davis MF, Franzen S (2008) Conformational dynamics associated with photodissociation of CO from dehaloperoxidase studied using photoacoustic calorimetry. Biochemistry 47:11510-11517.
37. Franzen S (2002) Spin-dependent mechanism for diatomic ligand binding to heme. Proc Natl Acad Sci USA 99:16754-16759.
38. Dartigalongue T, Hache F (2005) Observation of sub-100 ps conformational changes in photolyzed carbonmonoxy-myoglobin probed by time-resolved circular dichroism. Chem Phys Lett 415:313-316. (Pubitemid 41562358)
39. Sato A, Gao Y, Kitagawa T, Mizutani Y (2007) Primary protein response after ligand photodissociation in carbonmonoxy myoglobin. Proc Natl Acad Sci USA 104:9627-9632.
40. Dartigalongue T (2005) Conformational dynamics of myoglobin studied by time-resolved circular dichroism. PhD thesis (Ecole Polytechnique, Palaiseau, France).
41. Rodgers KR, Spiro TG (1994) Nanosecond dynamics of the R → T transition in hemoglobin: Ultraviolet Raman studies. Science 265:1697-1699.
42. Paoli M, Dodson G, Liddington RC, Wilkinson AJ (1997) Tension in haemoglobin revealed by Fe-His(F8) bond rupture in the fully liganded T-state. J Mol Biol 271:161-167.
43. Goodey NM, Benkovic SJ (2008) Allosteric regulation and catalysis emerge via a common route. Nat Chem Biol 4:474-482.
44. Armstrong MR, Ogilvie JP, Cowan ML, Miller RJD (2003) Observation of the cascaded atomic-to-global length scales driving protein motion. Proc Natl Acad Sci USA 100:4990-4994.
45. Popovych N, Sun S, Ebright RH, Kalodimos CG (2006) Dynamically driven protein allostery. Nat Struct Mol Biol 13:831-838.
46. Kruglik SG, et al. (2007) Molecular basis for nitric oxide dynamics and affinity with Alcaligenes xylosoxidanscytochrome c′. J Biol Chem 282:5053-5062.
47. Kruglik SG, Lambry J-C, Martin J-L, Vos MH, Negrerie M (2010) Sub-picosecond Raman spectrometer for time-resolved studies of structural dynamics in heme proteins. J Raman Spectrosc doi:10.1002/jrs.2685.