Protein-bound water as the determinant of asymmetric functional conversion between light-driven proton and chloride pumps

Biochemistry

Volumn 51, Issue 23, 2012, Pages 4677-4684

  Muroda, Kosuke ^a   Nakashima, Keisuke ^a   Shibata, Mikihiro ^a   Demura, Makoto ^b   Kandori, Hideki ^a  

^a NAGOYA INSTITUTE OF TECHNOLOGY   (Japan)

^b HOKKAIDO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIORHODOPSIN (BR); HALORHODOPSIN; IONIC SPECIFICITY; PROTEIN ARCHITECTURES; PROTON PUMP; REVERSE MUTATION; SCHIFF-BASE; TRANSPORT MECHANISM;

AMINO ACIDS; CHLORINE COMPOUNDS; FOURIER TRANSFORM INFRARED SPECTROSCOPY; FUNCTIONAL GROUPS; HYDROGEN BONDS; OPHTHALMOLOGY; PROTONS;

PUMPS;

AMINO ACID; BACTERIORHODOPSIN; CHLORIDE; HALORHODOPSIN; PROTON; SCHIFF BASE; WATER;

ARTICLE; CHLORIDE PUMP; HYDROGEN BOND; INFRARED SPECTROSCOPY; MUTANT; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; BACTERIORHODOPSINS; CHLORIDES; GENE EXPRESSION REGULATION, BACTERIAL; HALORHODOPSINS; LIGHT; MUTATION; PROTON PUMPS; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; WATER;

EID: 84862203706     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi300485r     Document Type: Article

References (60)

1. Deisseroth, K. (2011) Optogenetics Nat. Methods 8, 26-29
2. Hegemann, P. and Möglich, A. (2011) Channelrhodopsin engineering and expolation of new optogenetic tools Nat. Methods 8, 39-42
3. Kato, H. E., Zhang, F., Yizhar, O., Ramakrishnan, C., Nishizawa, T., Hirata, K., Ito, J., Aita, Y., Tsukazaki, T., Hayashi, S., Hegemann, P., Maturana, A. D., Ishitani, R., Deisseroth, K., and Nureki, O. (2012) Crystal structure of the channelrhodopsin light-gated cation channel Nature 482, 369-374
4. Zhang, F., Wang, L. P., Brauner, M., Liewald, J. F., Kay, K., Watzke, N., Wood, P. G., Bamberg, E., Nagel, G., Gottschalk, A., and Deisseroth, K. (2007) Multimodal fast optical interrogation of neural circuitry Nature 446, 633-639 (Pubitemid 46606891)
5. Chow, B. Y., Han, X., Dobry, A. S., Qian, X., Chuong, A. S., Li, M., Henninger, M. A., Belfort, G. M., Lin, Y., Monahan, P. E., and Boyden, E. S. (2010) High-performance genetically targetable optical neural silencing by light-driven proton pumps Nature 463, 98-102
6. Haupts, U., Tittor, J., and Oesterhelt, D. (1999) Closing in on bacteriorhodopsin: Progress in understanding the molecules Annu. Rev. Biophys. Biomol. Struct. 28, 367-399 (Pubitemid 29319263)
7. Lanyi, J. K. (2004) Bacteriorhodopsin Annu. Rev. Physiol. 66, 665-688 (Pubitemid 40614459)
8. Váró, G. (2000) Analogies between halorhodopsin and bacteriorhodopsin Biochim. Biophys. Acta 1460, 220-229
9. Essen, L.-O. (2002) Halorhodopsin: Light-driven ion pumping made simple? Curr. Opin. Struct. Biol. 12, 516-522
10. Kandori, H. (2011) Protein-Controlled Ultrafast Photoisomerization in Rhodopsin and Bacteriorhodopsin. In Supramolecular Photochemistry: Controlling Photochemical Processes (Ramamurthy, V. and Inoue, Y., Eds.) pp 571-596, John Wiley & Sons, Inc., Hoboken, NJ.
11. Luecke, H., Schobert, B., Richter, H.-T., Cartailler, J. P., and Lanyi, J. K. (1999) Structure of bacteriorhodopsin at 1.55 Å resolution J. Mol. Biol. 291, 899-911
12. Kolbe, M., Besir, H., Essen, L.-O., and Oesterhelt, D. (2000) Structure of the light-driven chloride pump halorhodopsin at 1.8 Å resolution Science 288, 1390-1396 (Pubitemid 30366319)
13. Kouyama, T., Kanada, S., Takeguchi, Y., Narusawa, A., Murakami, M., and Ihara, K. (2010) Crystal structure of the light-driven chloride pump halorhodopsin from Natronomonas pharaonis J. Mol. Biol. 396, 564-579
14. Sasaki, J., Brown, L. S., Chon, Y.-S., Kandori, H., Maeda, A., Needleman, R., and Lanyi, J. K. (1995) Conversion of bacteriorhodopsin into a chloride ion pump Science 269, 73-75
15. Facciotti, M. T., Cheung, V. S., Nguyen, D., Rouhani, S., and Glaeser, R. M. (2003) Crystal structure of the bromide-bound D85S mutant of bacteriorhodopsin: Principles of ion pumping Biophys. J. 85, 451-458 (Pubitemid 36753649)
16. Shibata, M., Ihara, K., and Kandori, H. (2006) Hydrogen-bonding interaction of the protonated Schiff base with halides in a chloride-pumping bacteriorhodopsin mutant Biochemistry 45, 10633-10640 (Pubitemid 44320478)
17. Havelka, W. A., Henderson, R., and Oesterhelt, D. (1995) Three-dimensional structure of halorhodopsin at 7 Å resolution J. Mol. Biol. 247, 726-738
18. Váró, G., Brown, L. S., Needleman, R., and Lanyi, J. K. (1996) Proton transport by halorhodopsin Biochemistry 35, 6604-6611 (Pubitemid 26172418)
19. Bamberg, E., Tittor, J., and Oesterhelt, D. (1993) Light-driven proton or chloride pumping by halorhodopsin Proc. Natl. Acad. Sci. U.S.A. 90, 639-643 (Pubitemid 23028919)
20. Haupts, U., Tittor, J., Bamberg, E., and Oesterhelt, D. (1997) General concept for ion translocation by halobacterial retinal proteins: The isomerization/switch/transfer (IST) model Biochemistry 36, 2-7 (Pubitemid 27024671)
21. Sato, M., Kanamori, T., Kamo, N., Demura, M., and Nitta, K. (2002) Stopped-flow analysis on anion binding to blue-form halorhodopsin from Natronomonas pharaonis: Comparison with the anion-uptake process during the photocycle Biochemistry 41, 2452-2458 (Pubitemid 34160909)
22. Sato, M., Kubo, M., Aizawa, T., Kamo, N., Kikukawa, T., Nitta, K., and Demura, M. (2005) Role of putative anion-binding sites in cytoplasmic and extracellular channels of Natronomonas pharaonis halorhodopsin Biochemistry 44, 4775-4784 (Pubitemid 40396756)
23. Shibata, M., Muneda, M., Sasaki, T., Shimono, K., Kamo, N., Demura, M., and Kandori, H. (2005) Hydrogen-bonding alterations of the protonated Schiff base and water molecule in the chloride pump of Natronobacterium pharaonis Biochemistry 44, 12279-12286 (Pubitemid 41324321)
24. Shimono, K., Furutani, Y., Kamo, N., and Kandori, H. (2003) Vibrational models of the protonated Schiff base in pharaonis phoborhodopsin Biochemistry 42, 7801-7806 (Pubitemid 36758945)
25. Shibata, M., Yoshitsugu, M., Mizuide, N., Ihara, K., and Kandori, H. (2007) Halide binding by the D212N mutant of bacteriorhodopsin affects hydrogen bonding of water in the active site Biochemistry 46, 7525-7535 (Pubitemid 46992028)
26. Yoshitsugu, M., Yamada, J., and Kandori, H. (2009) Color-changing mutation in the E-F loop of propeorhodopsin Biochemistry 48, 4324-4330
27. Yamada, K., Kawanabe, A., and Kandori, H. (2010) Importance of alanine at position 178 in proteorhodopsin for absorption of prevalent ambient light in the marine environment Biochemistry 49, 2416-2423
28. Muneda, N., Shibata, M., Demura, M., and Kandori, H. (2006) Internal water molecules of the proton-pumping halorhodopsin in the presence of azide J. Am. Chem. Soc. 128, 6294-6295 (Pubitemid 43727248)
29. Rothschild, K. J., Bousché, O., Braiman, M. S., Hasselbacher, C. A., and Spudich, J. L. (1988) Fourier transform infrared study of the halorhodopsin chloride pump Biochemistry 27, 2420-2424
30. Hackmann, C., Guijarro, J., Chizhov, I., Engelhard, M., Rödig, C., and Siebert, F. (2001) Static and time-resolved step-scan Fourier transform infrared investigations of the photoreaction of halorhodopsin from Natronobacterium pharaonis: Consequences for models of the anion translocation mechanism Biophys. J. 81, 394-406 (Pubitemid 32605979)
31. Kandori, H., Belenky, M., and Herzfeld, J. (2002) Vibrational frequency and dipolar orientation of the protonated Schiff base in bacteriorhodopsin before and after photoisomerization Biochemistry 41, 6026-6031 (Pubitemid 34498908)
32. Shimono, K., Furutani, Y., Kamo, N., and Kandori, H. (2003) Vibrational models of the protonated Schiff base in pharaonis phoborhodopsin Biochemistry 42, 7801-7806 (Pubitemid 36758945)
33. Ikeda, D., Furutani, Y., and Kandori, H. (2007) FTIR study of the retinal Schiff base and internal water molecules of proteorhodopsin Biochemistry 46, 5365-5373 (Pubitemid 46717261)
34. Kawanabe, A., Furutani, Y., Jung, K.-H., and Kandori, H. (2006) FTIR study of the photoisomerization processes in the 13-cis and all-trans forms of Anabaena sensory rhodopsin at 77 K Biochemistry 45, 4362-4370
35. Hashimoto, K., Choi, A. R., Furutani, F., Jung, K.-H., and Kandori, H. (2010) Low-temperature FTIR study of Gloeobacter rhodopsin: Presence of strongly hydrogen-bonded water and long-range structural protein perturbation upon retinal photoisomerization Biochemistry 49, 3343-3350
36. Shibata, M. and Kandori, H. (2005) FTIR studies of internal water molecules in the Schiff base region of bacteriorhodopsin Biochemistry 44, 7406-7413 (Pubitemid 40695994)
37. Garczarek, F. and Gerwert, K. (2006) Functional waters in intraprotein proton transfer monitored by FTIR difference spectroscopy Nature 439, 109-112 (Pubitemid 43053638)
38. Wolf, S., Freier, E., Potschies, M., Hofmann, E., and Gerwert, K. (2010) Directional proton transfer in membrane proteins achieved through protonated protein-bound water molecules: A proton diode Angew. Chem., Int. Ed. 49, 6889-6893
39. Freier, E., Wolf, S., and Gerwert, K. (2011) Proton transfer via a transient linear water-molecule chain in a membrane protein Proc. Natl. Acad. Sci. U.S.A. 108, 11435-11439
40. Kandori, H. (2000) Role of internal water molecules in bacteriorhodopsin Biochim. Biophys. Acta 1460, 177-191
41. Kandori, H. (2004) Hydration switch model for the proton transfer in the Schiff base region of bacteriorhodopsin Biochim. Biophys. Acta 1658, 72-79 (Pubitemid 39013236)
42. Hayashi, S., Tajkhorshid, E., Kandori, H., and Schulten, K. (2004) Role of hydrogen-bond network in energy storage of bacteriorhodopsin's light-driven proton pump revealed by ab initio normal-mode analysis J. Am. Chem. Soc. 126, 10516-10517 (Pubitemid 39129135)
43. Bogomolni, R. A., Stoeckenius, W., Szundi, I., Perozo, E., Olson, K. D., and Spudich, J. L. (1994) Removal of transducer HtrI allows electrogenic proton translocation by sensory rhodopsin I Proc. Natl. Acad. Sci. U.S.A. 91, 10188-10192 (Pubitemid 24311974)
44. Sudo, Y., Iwamoto, M., Shimono, K., Sumi, M., and Kamo, N. (2001) Photo-induced proton transport of pharaonis phoborhodopsin (sensory rhodopsin II) is ceased by association with the transducer Biophys. J. 80, 916-922 (Pubitemid 32128342)
45. Sineshchekov, O. A., Spudich, E. N., Trivedi, V. D., and Spudich, J. L. (2006) Role of the cytoplasmic domain in Anabaena sensory rhodopsin photocycling: Vectoriality of Schiff base deprotonation Biophys. J. 91, 4519-4527 (Pubitemid 44904236)
46. Brown, L. S., Dioumaev, A. K., Lanyi, J. K., Spudich, E. N., and Spudich, J. L. (2001) Photochemical reaction cycle and proton transfers in Neurospora rhodopsin J. Biol. Chem. 276, 32495-32505
47. Furutani, Y., Kawanabe, A., Jung, K.-H., and Kandori, H. (2005) FTIR spectroscopy of the all-trans form of Anabaena sensory rhodopsin at 77 K: Hydrogen bond of a water between the Schiff base and Asp75 Biochemistry 44, 12287-12296 (Pubitemid 41324322)
48. Furutani, Y., Bezerra, A. G., Jr., Waschuk, S., Sumii, M., Brown, L. S., and Kandori, H. (2004) FTIR spectroscopy of the K photointermediate of Neurospora rhodopsin: Structural changes of the retinal, protein, and water molecules after photoisomerization Biochemistry 43, 9636-9646 (Pubitemid 38993814)
49. Birge, R. R. (1990) Nature of the primary photochemical events in rhodopsin and bacteriorhodopsin Biochim. Biophys. Acta 1016, 293-327
50. Kukura, P., McCamant, D. W., Yoon, S., Wandschneider, D. B., and Mathies, R. A. (2005) Structural observation of the primary isomerization in vision with femtosecond-stimulated Raman Science 310, 1006-1009 (Pubitemid 41611910)
51. Sharma, A. K., Spudich, J. L., and Doolittle, W. F. (2006) Microbial rhodopsins: Functional versatility and genetic mobility Trends Microbiol. 14, 463-469 (Pubitemid 44537809)
52. Mizuide, N., Shibata, M., Friedman, N., Sheves, M., Belenky, M., Herzfeld, J., and Kandori, H. (2006) Structural changes in bacteriorhodopsin following retinal photoisomerization from the 13- cis form Biochemistry 45, 10674-10681 (Pubitemid 44320482)
53. Shibata, M., Yoshitsugu, M., Mizuide, N., Ihara, K., and Kandori, H. (2007) Halide binding by the D212N mutant of bacteriorhodopsin affects hydrogen bonding of water in the active site Biochemistry 46, 7525-7535 (Pubitemid 46992028)
54. Suzuki, D., Sudo, Y., Furutani, Y., Takahashi, H., Homma, M., and Kandori, H. (2008) Structural changes of Salinibacter sensory rhodopsin I upon formation of the K and M photointermediates Biochemistry 47, 12750-12759
55. Kandori, H., Furutani, Y., Shimono, K., Shichida, Y., and Kamo, N. (2001) Internal water molecules of pharaonis phoborhodopsin studied by low-temperature infrared spectroscopy Biochemistry 40, 15693-15698 (Pubitemid 34015197)
56. Sumii, M., Furutani, Y., Waschuk, S. A., Brown, L. S., and Kandori, H. (2005) Strongly hydrogen-bonded water molecule present near the retinal chromophore of Leptosphaeria rhodopsin, bacteriorhodopsin-like proton pump from a eukaryote Biochemistry 44, 15159-15166 (Pubitemid 41681450)
57. Furutani, Y., Shichida, Y., and Kandori, H. (2003) Structural changes of water molecules during the photoactivation processes in bovine rhodopsin Biochemistry 42, 9619-9625 (Pubitemid 37006305)
58. Ota, T., Furutani, Y., Terakita, A., Shichida, Y., and Kandori, H. (2006) Structural changes in the Schiff base region of squid rhodopsin upon photoisomerization studied by low-temperature FTIR spectroscopy Biochemistry 45, 2845-2851 (Pubitemid 43334533)
59. Katayama, K., Furutani, Y., Imai, H., and Kandori, H. (2012) Protein-bound water molecules in primate red- and green-sensitive visual pigments Biochemistry 51, 1126-1133
60. Shibata, M., Muneda, N., Ihara, K., Sasaki, T., Demura, M., and Kandori, H. (2004) Internal water molecules of light-driven chloride pump proteins Chem. Phys. Lett. 392, 330-333