Temperature-dependent Structural Perturbation of Tuna Myoglobin
To unveil the mechanism of fast autooxidation of fish
myoglobins, the effect of temperature on the structural change of tuna
myoglobin was investigated. Purified myoglobin was subjected to
preincubation at 5, 20, 50 and 40oC. Overall helical structural decay
through thermal treatment up to 95oC was monitored by circular
dichroism spectrometry, while the structural changes around the heme
pocket was measured by ultraviolet/visible absorption spectrophotometry.
As a result, no essential structural change of myoglobin
was observed under 30oC, roughly equivalent to their body
temperature, but the structure was clearly damaged at 40oC. The Soret
band absorption hardly differed irrespective of preincubation
temperature, suggesting that the structure around the heme pocket was
not perturbed even after thermal treatment.
[1] S. E. V. Phillips and B.P. Schoenborn, "Neutron diffraction reveals
oxygen-histidine hydrogen bond in oxymyoglobin," Nature, vol. 292,
pp.81-82, 1981.
[2] J. Vojtechovsky, K. Chu, J. Berendzen, R. M. Sweet, and I. Schlichting,
"Crystal structures of myoglobin-ligand complexes at near-atomic
resolution," Biophysical Journal, vol. 77, pp.2153-2174, 1999.
[3] G. I. Birnbaum, S. V. Evans, M. Przybylska, and D. R. Rose, "1.70 Å
resolution structure of myoglobin from yellowfin tuna. An example of a
myoglobin lacking the D helix," Acta Crystallographica, vol. D50,
pp.283-289, 1994.
[4] F. Matsuura and K. Hashimoto, "Chemical studies on the red muscle
("chiai") of fishes-X. A new method for determination of myoglobin,"
Nippon Suisan Gakkaishi, vol. 24, pp.809-815, 1959.
[5] N. Ueki and Y. Ochiai, "Primary structure and thermostability of bigeye
tuna myoglobin in relation to those from other scombridae fish," Fisheries
Science, vol. 70, pp.875-884, 2004.
[6] N. Ueki, C. J. Chow, and Y. Ochiai, "Characterization of bullet tuna
myoglobin with reference to thermostability-structure relationship",
Journal of Agricultural and Food Chemistry, vol. 53, pp.4968-4975, 2005.
[7] S. J. Smerdon, S. Krzywda, A. J. Wilkinson, R. E. Brantley, Jr., T. E.
Carver, M. S. Hargrove, and J. S. Olsen, "Serine92 (F7) contributes to the
control of heme reactivity and stability in myoglobin," Biochemistry, vol.
32, pp.5132-5138, 1993.
[8] Y. Luo, M. S. Kay, and R. L. Baldwin, "Cooperativity of folding of the
apomyoglobin pH 4 intermediate studies by glycine and proline
mutations," Nature Structure Biology, vol.4, pp.925-930, 1997.
[9] N. Ueki and Y. Ochiai, "Effect of amino acid replacements on the
structural stability of fish myoglobin," Journal of Biochemistry, vol.140,
pp.649-656, 2006.
[10] Y. Ochiai, N. Ueki and S. Watabe, "Effects of point mutations on the
structural stability of tuna myoglobins," Comparative Biochemistry and
Physiology, vol. 153B, pp.223-228, 2009.
[11] P. W. Madden, M. J. Babcock, M. E. Vayda, and R. E. Cashon, "Structural
and kinetic characterization of myoglobins from eurythermal and
stenothermal fish species," Comparative Biochemistry and Physiology,
vol.137B, pp.341-350, 2004.
[12] Y. Kitahara, A. Matsuoka, N. Kobayashi, and K. Shikama,
"Autooxidation of myoglobin from bigeye tuna fish (Thunnus obesus),"
Biochimica Biophysica Acta, vol. 1038, pp.23-28, 1990.
[13] S. Chanthai, M. Ogawa, T. Tamiya, and T. Tsuchiya, "Studies on thermal
denaturation of fish myoglobins using differential scanning calorimetry,
circular dichroism, and tryptophan fluorescence," Fisheries Science,
vol.62, pp.927-932, 1996.
[14] C. J. Chow, Y. Ochiai, S. Watabe, and K. Hashimoto, "Reduced stability
and accelerated autooxidation of tuna myoglobin in association with
freezing and thawing," Journal of Agricultural and Food Chemistry, vol.
37, pp.1391-1395, 1989.
[15] C. J. Chow, J. C. Wu, P. F. Lee, and Y. Ochiai, "Effects of acid and
alkaline pretreatment on the discoloration rates of dark muscle and
myoglobin extract of skinned tilapia fillet during iced storage," Fisheries
Science vol.75, pp.1481-1488, 2009.
[16] C. J. Chow, "Relationship between the stability and autoxidation of
myoglobin," Journal of Agricultural and Food Chemistry, vol.39,
pp.22-26, 1991.
[17] Y. Ochiai, Y. Watanabe, N. Uchida, H. Ozawa, S. Ikegami, and S. Watabe,
"Thermal denaturation profiles of tuna myoglobin," Bioscience,
Biotechnology and Biochemistry, vol.74, pp.1673-1679, 2010.
[18] H. Ozawa, S. Watabe, and Y. Ochiai, "Thermostability of striated and
smooth adductor muscle tropomyosins from Yesso scallop Mizuhopecten
yessoensis," Journal of Biochemistry, vol.147, pp.823-832, 2010.
[19] B. A. Block, H. Dewar, S. B. Blackwell, T. D. Williams, E. D. Prince, C. J.
Farwell, A. Boustany, S. L. H. Teo, A. Seitz, A. Walli, and D. Fudge,
"Migratory movements, depth preferences, and thermal biology of
Atlantic bluefin tuna," Science, vol.293, pp.1310-1314, 2001.
[20] E. Bismuto, E. Gratton, and D. C. Lamb, "Dynamics of ANS Binding to
tuna apomyoglobin measured with fluorescence correlation
spectroscopy," Biophysical Journal, vol.81, pp.3510-3521, 2001.
[21] M. Fandrich, V. Forge, K. Buder, M. Kittler, C. M. Dobson, and S.
Diekmann, "Myoglobin forms amyloid fibrils by association of unfolded
polypeptide segments," Proceedings of the National Academy of
Sciences U.S.A., vol.100, pp.15463-15468, 2003.
[22] G. G. Tartaglia, A. P. Pawar, S. Campioni, C. M. Dobson, F. Chiti, and M.
Vendruscolo, "Prediction of aggregation-prone regions in structured
proteins," Journal of Molecular Biology, vol.380, pp.425-436, 2008.
[23] S. N. Loh, M. S. Kay, and R. L. Baldwin, "Structure and stability of a
second molten globule intermediate in the apomyoglobin folding
pathway," Proceedings of the National Academy of Sciences U.S.A.,
vol.92, 5446-5450, 1995.
[24] D. Barrick and R. L. Baldwin, "The molten globule intermediate of
apomyoglobin and the process of protein folding," Protein Science, vol.2,
pp.869-876, 1993.
[25] E. Bismuto, G. Irace, L. Servillo, A. Giovane, and G. Colonna,
"Conformational stability and basal metabolic rate: reexamination of the
case of myoglobin," Experientia, vol.40, pp.1400-1401, 1984.
[26] R. E. Cashon, M. E. Vayda, and B. D. Sidell, "Kinetic characterization of
myoglobins from vertebrates with vastly different body temperatures,"
Comparative Biochemistry and Physiology, vol. 117B, 613-620, 1997.
[27] D. J. Marcinek, J. Bonaventura, J. B. Wittenberg, and B. A. Block,
"Oxygen affinity and amino acid sequence of myoglobins from
endothermic and ectothermic fish," American Journal of Physiology-
Regulatory, Integrative and Comparative Physiology, vol.280,
pp.R1123-1133, 2001.
[28] S. Hirota, K. Azuma, M. Fukuba, S. Kuroiwa, and N. Funasaki, "Heme
reduction by intramolecular electron transfer in cysteine mutant
myoglobin under carbon monoxide atmosphere," Biochemistry, vol.44,
pp.10322-10327, 2005.
[29] D. Bourgeois, B. Vallone, A. Arcovito, G. Sciara, F. Schotte, P. A.
Anfinrud, and M. Brunori, "Extended subnanosecond structural dynamics
of myoglobin revealed by Laue crystallography," Proceedings of the
National Academy of Sciences U.S.A., vol.103, pp.4924-4929, 2006.
[30] P. Picotti, A. Marabotti, A. Negro, V. Musi, B. Spolaore, M. Zambonin,
and A. Fontana, "Modulation of structural integrity of helix F in
apomyoglobin by single amino acid replacements," Protein Science,
vol.13, pp.1572-1585, 2004.
[31] A. E. Dyuysekina, D. A. Dolgikh, E. N. Samatova Baryshnikova, E. I.
Tiktopulo, V. A. Balobanov, and V. E. Bychkova, "pH-induced
equilibrium unfolding of apomyoglobin: substitutions at conserved Trp14
and Met131 and non-conserved Val17 positions," Biochemistry
(Moscow), vol.73, pp.693-701, 2008.
[32] R. Musto, M. G. Bigotti, C. Travaglini-Allocatelli, M. Brunori, and F.
Cutruzzola, "Folding of Aplysia limacina apomyoglobin involves an
intermediate in common with other evolutionarily distant globins,"
Biochemistry, vol.43, pp.230-236, 2004.
[33] M. S. Hargrove, E. W. Singleton, M. L. Quillin, L. A. Ortiz, G. N. Phillips
Jr., J. S. Olsen, and A. J. Mathews, "His64(E7)  Tyr apomyoglobin as a
reagent for measuring rates of hemin dissociation," Journal of Biological
Chemistry, vol.269, pp.4207-4214, 1994.
[34] E. Bismuto, E. Di Maggio, S. Pleus, M. Sikor, C. Rocker, G. H. Nienhaus,
and D. C. Lamb, "Molecular dynamics simulation of the acidic compact
state of apomyoglobin from yellowfin tuna," Proteins, vol.74, pp.273-290,
2008.
[35] M. Dametto and A. E. Cardenas, "Computer simulations of the refolding
of sperm whale apomyoglobin from high-temperature denaturated state,"
Journal of Physical Chemistry B, vol.112, pp.9501-9506, 2008.
[1] S. E. V. Phillips and B.P. Schoenborn, "Neutron diffraction reveals
oxygen-histidine hydrogen bond in oxymyoglobin," Nature, vol. 292,
pp.81-82, 1981.
[2] J. Vojtechovsky, K. Chu, J. Berendzen, R. M. Sweet, and I. Schlichting,
"Crystal structures of myoglobin-ligand complexes at near-atomic
resolution," Biophysical Journal, vol. 77, pp.2153-2174, 1999.
[3] G. I. Birnbaum, S. V. Evans, M. Przybylska, and D. R. Rose, "1.70 Å
resolution structure of myoglobin from yellowfin tuna. An example of a
myoglobin lacking the D helix," Acta Crystallographica, vol. D50,
pp.283-289, 1994.
[4] F. Matsuura and K. Hashimoto, "Chemical studies on the red muscle
("chiai") of fishes-X. A new method for determination of myoglobin,"
Nippon Suisan Gakkaishi, vol. 24, pp.809-815, 1959.
[5] N. Ueki and Y. Ochiai, "Primary structure and thermostability of bigeye
tuna myoglobin in relation to those from other scombridae fish," Fisheries
Science, vol. 70, pp.875-884, 2004.
[6] N. Ueki, C. J. Chow, and Y. Ochiai, "Characterization of bullet tuna
myoglobin with reference to thermostability-structure relationship",
Journal of Agricultural and Food Chemistry, vol. 53, pp.4968-4975, 2005.
[7] S. J. Smerdon, S. Krzywda, A. J. Wilkinson, R. E. Brantley, Jr., T. E.
Carver, M. S. Hargrove, and J. S. Olsen, "Serine92 (F7) contributes to the
control of heme reactivity and stability in myoglobin," Biochemistry, vol.
32, pp.5132-5138, 1993.
[8] Y. Luo, M. S. Kay, and R. L. Baldwin, "Cooperativity of folding of the
apomyoglobin pH 4 intermediate studies by glycine and proline
mutations," Nature Structure Biology, vol.4, pp.925-930, 1997.
[9] N. Ueki and Y. Ochiai, "Effect of amino acid replacements on the
structural stability of fish myoglobin," Journal of Biochemistry, vol.140,
pp.649-656, 2006.
[10] Y. Ochiai, N. Ueki and S. Watabe, "Effects of point mutations on the
structural stability of tuna myoglobins," Comparative Biochemistry and
Physiology, vol. 153B, pp.223-228, 2009.
[11] P. W. Madden, M. J. Babcock, M. E. Vayda, and R. E. Cashon, "Structural
and kinetic characterization of myoglobins from eurythermal and
stenothermal fish species," Comparative Biochemistry and Physiology,
vol.137B, pp.341-350, 2004.
[12] Y. Kitahara, A. Matsuoka, N. Kobayashi, and K. Shikama,
"Autooxidation of myoglobin from bigeye tuna fish (Thunnus obesus),"
Biochimica Biophysica Acta, vol. 1038, pp.23-28, 1990.
[13] S. Chanthai, M. Ogawa, T. Tamiya, and T. Tsuchiya, "Studies on thermal
denaturation of fish myoglobins using differential scanning calorimetry,
circular dichroism, and tryptophan fluorescence," Fisheries Science,
vol.62, pp.927-932, 1996.
[14] C. J. Chow, Y. Ochiai, S. Watabe, and K. Hashimoto, "Reduced stability
and accelerated autooxidation of tuna myoglobin in association with
freezing and thawing," Journal of Agricultural and Food Chemistry, vol.
37, pp.1391-1395, 1989.
[15] C. J. Chow, J. C. Wu, P. F. Lee, and Y. Ochiai, "Effects of acid and
alkaline pretreatment on the discoloration rates of dark muscle and
myoglobin extract of skinned tilapia fillet during iced storage," Fisheries
Science vol.75, pp.1481-1488, 2009.
[16] C. J. Chow, "Relationship between the stability and autoxidation of
myoglobin," Journal of Agricultural and Food Chemistry, vol.39,
pp.22-26, 1991.
[17] Y. Ochiai, Y. Watanabe, N. Uchida, H. Ozawa, S. Ikegami, and S. Watabe,
"Thermal denaturation profiles of tuna myoglobin," Bioscience,
Biotechnology and Biochemistry, vol.74, pp.1673-1679, 2010.
[18] H. Ozawa, S. Watabe, and Y. Ochiai, "Thermostability of striated and
smooth adductor muscle tropomyosins from Yesso scallop Mizuhopecten
yessoensis," Journal of Biochemistry, vol.147, pp.823-832, 2010.
[19] B. A. Block, H. Dewar, S. B. Blackwell, T. D. Williams, E. D. Prince, C. J.
Farwell, A. Boustany, S. L. H. Teo, A. Seitz, A. Walli, and D. Fudge,
"Migratory movements, depth preferences, and thermal biology of
Atlantic bluefin tuna," Science, vol.293, pp.1310-1314, 2001.
[20] E. Bismuto, E. Gratton, and D. C. Lamb, "Dynamics of ANS Binding to
tuna apomyoglobin measured with fluorescence correlation
spectroscopy," Biophysical Journal, vol.81, pp.3510-3521, 2001.
[21] M. Fandrich, V. Forge, K. Buder, M. Kittler, C. M. Dobson, and S.
Diekmann, "Myoglobin forms amyloid fibrils by association of unfolded
polypeptide segments," Proceedings of the National Academy of
Sciences U.S.A., vol.100, pp.15463-15468, 2003.
[22] G. G. Tartaglia, A. P. Pawar, S. Campioni, C. M. Dobson, F. Chiti, and M.
Vendruscolo, "Prediction of aggregation-prone regions in structured
proteins," Journal of Molecular Biology, vol.380, pp.425-436, 2008.
[23] S. N. Loh, M. S. Kay, and R. L. Baldwin, "Structure and stability of a
second molten globule intermediate in the apomyoglobin folding
pathway," Proceedings of the National Academy of Sciences U.S.A.,
vol.92, 5446-5450, 1995.
[24] D. Barrick and R. L. Baldwin, "The molten globule intermediate of
apomyoglobin and the process of protein folding," Protein Science, vol.2,
pp.869-876, 1993.
[25] E. Bismuto, G. Irace, L. Servillo, A. Giovane, and G. Colonna,
"Conformational stability and basal metabolic rate: reexamination of the
case of myoglobin," Experientia, vol.40, pp.1400-1401, 1984.
[26] R. E. Cashon, M. E. Vayda, and B. D. Sidell, "Kinetic characterization of
myoglobins from vertebrates with vastly different body temperatures,"
Comparative Biochemistry and Physiology, vol. 117B, 613-620, 1997.
[27] D. J. Marcinek, J. Bonaventura, J. B. Wittenberg, and B. A. Block,
"Oxygen affinity and amino acid sequence of myoglobins from
endothermic and ectothermic fish," American Journal of Physiology-
Regulatory, Integrative and Comparative Physiology, vol.280,
pp.R1123-1133, 2001.
[28] S. Hirota, K. Azuma, M. Fukuba, S. Kuroiwa, and N. Funasaki, "Heme
reduction by intramolecular electron transfer in cysteine mutant
myoglobin under carbon monoxide atmosphere," Biochemistry, vol.44,
pp.10322-10327, 2005.
[29] D. Bourgeois, B. Vallone, A. Arcovito, G. Sciara, F. Schotte, P. A.
Anfinrud, and M. Brunori, "Extended subnanosecond structural dynamics
of myoglobin revealed by Laue crystallography," Proceedings of the
National Academy of Sciences U.S.A., vol.103, pp.4924-4929, 2006.
[30] P. Picotti, A. Marabotti, A. Negro, V. Musi, B. Spolaore, M. Zambonin,
and A. Fontana, "Modulation of structural integrity of helix F in
apomyoglobin by single amino acid replacements," Protein Science,
vol.13, pp.1572-1585, 2004.
[31] A. E. Dyuysekina, D. A. Dolgikh, E. N. Samatova Baryshnikova, E. I.
Tiktopulo, V. A. Balobanov, and V. E. Bychkova, "pH-induced
equilibrium unfolding of apomyoglobin: substitutions at conserved Trp14
and Met131 and non-conserved Val17 positions," Biochemistry
(Moscow), vol.73, pp.693-701, 2008.
[32] R. Musto, M. G. Bigotti, C. Travaglini-Allocatelli, M. Brunori, and F.
Cutruzzola, "Folding of Aplysia limacina apomyoglobin involves an
intermediate in common with other evolutionarily distant globins,"
Biochemistry, vol.43, pp.230-236, 2004.
[33] M. S. Hargrove, E. W. Singleton, M. L. Quillin, L. A. Ortiz, G. N. Phillips
Jr., J. S. Olsen, and A. J. Mathews, "His64(E7)  Tyr apomyoglobin as a
reagent for measuring rates of hemin dissociation," Journal of Biological
Chemistry, vol.269, pp.4207-4214, 1994.
[34] E. Bismuto, E. Di Maggio, S. Pleus, M. Sikor, C. Rocker, G. H. Nienhaus,
and D. C. Lamb, "Molecular dynamics simulation of the acidic compact
state of apomyoglobin from yellowfin tuna," Proteins, vol.74, pp.273-290,
2008.
[35] M. Dametto and A. E. Cardenas, "Computer simulations of the refolding
of sperm whale apomyoglobin from high-temperature denaturated state,"
Journal of Physical Chemistry B, vol.112, pp.9501-9506, 2008.
@article{"International Journal of Biological, Life and Agricultural Sciences:53139", author = "Yoshihiro Ochiai", title = "Temperature-dependent Structural Perturbation of Tuna Myoglobin", abstract = "To unveil the mechanism of fast autooxidation of fish
myoglobins, the effect of temperature on the structural change of tuna
myoglobin was investigated. Purified myoglobin was subjected to
preincubation at 5, 20, 50 and 40oC. Overall helical structural decay
through thermal treatment up to 95oC was monitored by circular
dichroism spectrometry, while the structural changes around the heme
pocket was measured by ultraviolet/visible absorption spectrophotometry.
As a result, no essential structural change of myoglobin
was observed under 30oC, roughly equivalent to their body
temperature, but the structure was clearly damaged at 40oC. The Soret
band absorption hardly differed irrespective of preincubation
temperature, suggesting that the structure around the heme pocket was
not perturbed even after thermal treatment.", keywords = "denaturation, myoglobin, stability, tuna.", volume = "5", number = "2", pages = "48-5", }
