Synergistic Effect of Distal Polar Interactions in Myoglobin and Their Structural Consequences
- Miho WatanabeMiho WatanabeDepartment of Chemistry, University of Tsukuba, Tsukuba 305-8571, JapanMore by Miho Watanabe,
- Yuki Kanai ,
- Shunpei NakamuraShunpei NakamuraDepartment of Chemistry, University of Tsukuba, Tsukuba 305-8571, JapanMore by Shunpei Nakamura,
- Ryu NishimuraRyu NishimuraDepartment of Chemistry, University of Tsukuba, Tsukuba 305-8571, JapanMore by Ryu Nishimura,
- Tomokazu ShibataTomokazu ShibataDepartment of Chemistry, University of Tsukuba, Tsukuba 305-8571, JapanMore by Tomokazu Shibata,
- Atsuya MomotakeAtsuya MomotakeDepartment of Chemistry, University of Tsukuba, Tsukuba 305-8571, JapanMore by Atsuya Momotake,
- Sachiko YanagisawaSachiko YanagisawaDepartment of Life Science, Graduate School of Life Science, University of Hyogo, Sayo-cho, Sayo-gun, Hyogo 678-1297, JapanMore by Sachiko Yanagisawa,
- Takashi OguraTakashi OguraDepartment of Life Science, Graduate School of Life Science, University of Hyogo, Sayo-cho, Sayo-gun, Hyogo 678-1297, JapanMore by Takashi Ogura,
- Takashi MatsuoTakashi MatsuoDivision of Materials Science, Graduate School of Science and Technology, Nara Institute of Science and Technology, Ikoma, Nara 630-0192, JapanMore by Takashi Matsuo,
- Shun HirotaShun HirotaDivision of Materials Science, Graduate School of Science and Technology, Nara Institute of Science and Technology, Ikoma, Nara 630-0192, JapanMore by Shun Hirota,
- Saburo NeyaSaburo NeyaDepartment of Physical Chemistry, Graduate School of Pharmaceutical Sciences, Chiba University, Chuoh-Inohana, Chiba 260-8675, JapanMore by Saburo Neya,
- Akihiro SuzukiAkihiro SuzukiDepartment of Materials Engineering, National Institute of Technology, Nagaoka College, Nagaoka 940-8532, JapanMore by Akihiro Suzuki, and
- Yasuhiko Yamamoto*Yasuhiko Yamamoto*E-mail: [email protected]. Phone/Fax: +81 29 853 6521.Department of Chemistry, Tsukuba Research Center for Energy Materials Science, , University of Tsukuba, Tsukuba 305-8571, JapanLife Science Center for Survival Dynamics, Tsukuba Advanced Research Alliance, University of Tsukuba, Tsukuba 305-8577, JapanMore by Yasuhiko Yamamoto
Abstract
In the L29F variant of myoglobin (Mb), the coordination of oxygen (O2) to the heme Fe atom is stabilized by favorable electrostatic interactions between the polar Fe–O2 moiety and the multipole of the phenyl ring of the Phe29 side chain (Phe29 interaction), in addition to the well-known hydrogen bond (H-bond) between the Fe-bound O2 and the 64th residue (distal H-bond; Carver, T. E.; Brantley, R. E., Jr.; Singleton, E. W.; Arduini, R. M.; Quillin, M. L.; Phillips, G. N., Jr.; Olson, J. S. J. Biol. Chem.1992, 267, 14443–14450). The O2 and carbon monoxide (CO) binding properties and autoxidation of the L29F/H64L and L29F/H64Q variants reconstituted with a series of chemically modified heme cofactors were analyzed and then compared with those of native Mb, and the L29F, H64Q, and H64L variants similarly reconstituted with the chemically modified heme cofactors in order to elucidate the relationship between the Phe29 interaction and the distal H-bond that critically contributes to stabilization of Fe-bound O2. We found that the Phe29 interaction and distal H-bond act cooperatively to stabilize the Fe-bound O2 in such a manner that the Phe29 interaction strengthens with increasing strength of the distal H-bond. Comparison of the functional properties between the L29F and H64L variants indicated that the synergistic effect of the two interactions decreases the O2 dissociation and autoxidation rate constants of the protein by factors of ∼1/2000 and ∼1/400, respectively. Although the CO binding properties of the proteins were not greatly affected by the distal polar interactions, their synergistic effects were clearly and sharply manifested in the vibrational frequencies of the Fe-bound C–O stretching of the proteins.
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