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Thermal denaturation and autoxidation profiles of carangid fish myoglobins

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Abstract

Although myoglobin (Mb) has been considered to be one of the well-characterized proteins, screening of post-genomic era databases revealed the lack of adequate information on teleost Mbs. The present study was aimed to investigate stability and functional features of Mbs from three teleosts of the same family. To unfold how primary structure influences the stability and function of proteins, Mbs were purified from the dark muscles of three carangids, namely, yellowtail, greater amberjack, and silver trevally. Thermostabilities measured by circular dichroism (CD) spectrometry revealed species-specific thermal denaturation pattern, i.e., silver trevally > yellowtail > greater amberjack Mbs. On the other hand, autoxidation rate constants of the ferrous forms of those three carangid Mbs showed positive correlation between the ferrous state of the heme iron and rising temperature. The order of autoxidation rate was in the order of greater amberjack > yellowtail > silver trevally Mbs. The finding of the present study denotes that the thermal stability is not necessarily correlated with the functional stability of carangid Mbs even though their primary structures shared high homology (84–94%).

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Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Adeyemi KD, Shittu RM, Sabow AB, Karim R, Sazili AQ (2016) Myofibrillar protein, lipid and myoglobin oxidation, antioxidant profile, phsyicochemical and sensory properties of caprine longissimus thoracis during postmortem conditioning. J Food Process Preserv 41:1–14

    Google Scholar 

  • Antonini E, Brunori M (1971) Hemoglobin and myoglobin in their reactions with ligands. North Holland Publishing Company, Amsterdam

    Google Scholar 

  • Aojula HS, Wilson MT, Morrison IG (1987) Functional consequences of haem orientational disorder in sperm-whale and yellow-fin-tuna myoglobins. Biochem J 243:205–210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bannikov AF (1987) On the taxonomy, composition and origin of the family Carangidae. J Ichthyol 27:1–8

    Google Scholar 

  • Birnbaum GI, Evans SV, Przybylska M, Rose DR (1994) 1.70 Å resolution structure of myoglobin from yellowfin tuna. An example of a myoglobin lacking the D helix. Acta Crystallogr D Biol Crystallogr 50:283–289

    Article  CAS  PubMed  Google Scholar 

  • Birukou I, Schweers RL, Olson JS (2010) Distal histidine stabilizes bound O2 and acts as a gate for ligand entry in both subunits of adult human hemoglobin. J Biol Chem 285:8840–8854

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bismuto E, Gratton E, Lamb DC (2001) Dynamics of ANS binding to tuna apomyoglobin measured with fluorescence correlation spectroscopy. Biophys J 81:3510–3521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bonaventura C, Henkens R, Alayash AI, Banerjee S, Crumbliss AL (2013) Molecular controls of the oxygenation and redox reactions of hemoglobin. Antioxi Redox Signal 18:2298–2313

    Article  CAS  Google Scholar 

  • Brantley REJ, Smerdon SJ, Wilkinson AJ, Singleton EW, Olson JS (1993) The mechanism of autoxidation of myoglobin. J Biol Chem 268:6995–7010

    Article  CAS  PubMed  Google Scholar 

  • Broumand H, Ball CO, Stier EF (1958) Factors affecting the quality of prepackaged meat. II. E. Determining the proportions of heme derivatives in fresh meat. Food Technol 12:65

    CAS  Google Scholar 

  • Brunori M (2001) Nitric oxide moves myoglobin centre stage. Trends Biochem Sci 26:21–23

    Article  CAS  PubMed  Google Scholar 

  • Cashon RE, Vayda ME, Sidell BD (1997) Kinetic characterization of myoglobins from vertebrates with vastly different body temperatures. Comp Biochem Physiol – Part B Biochem Mol Biol 117:613–620

    Article  CAS  Google Scholar 

  • Chanthai S, Neida H, Ogawa M, Tamiya T, Tsuchiya T (1996) Studies on thermal denaturation of fish myoglobins using differential scanning calorimetry, circular dichroism, and tryptophan fluorescence. Fish Sci 62:927–932

    Article  CAS  Google Scholar 

  • Chen LC, Lin SB, Chen HH (2004) Thermal stability and denaturation rate of myoglobin from various species of fish. Fish Sci 70:293–298

    Article  CAS  Google Scholar 

  • Chow CJ (1991) Relationship between the stability and autoxidation of myoglobin. J Agric Food Chem 39:22–26

    Article  CAS  Google Scholar 

  • Chow CJ, Ochiai Y, Watabe S, Hashimoto K (1989) Reduced stability and accelerated autoxidation of tuna myoglobin, in association with freezing and thawing. J Agric Food Chem 37:1391–1395

    Article  CAS  Google Scholar 

  • Chow CJ, Wu JC, Lee PF, Ochiai Y (2009) Structural and autooxidation profiles of myoglobins from three species and one hybrid of tilapia (Cichlidae, Perciformes). Comp Biochem Physiol – Part B Biochem Mol Biol 154:274–281

    Article  Google Scholar 

  • Conforth D (1994) Color-its basis and importance. In: Pearson AM, Duston TR (eds) Quality attributes and their measurement in meat, poultry and fish products. Advances in Meat Research, vol 9. Blackie Academic and Professional, London, pp 34–78

    Google Scholar 

  • Corrêa DHA, Ramos CHI (2009) The use of circular dichroism spectroscopy to study protein folding, form and function. Afr J Biochem Res 3:164–173

    Google Scholar 

  • Dasmeh P, Kepp KP, Davis RW (2013) Aerobic dive limits of seals with mutant myoglobin using combined thermochemical and physiological data. Comp Biochem Physiol A 164:119–128

    Article  CAS  Google Scholar 

  • Dong H, Sharma M, Zhou HX, Cross TA (2012) Glycines: role in α-helical membrane protein structures and a potential indicator for native conformation. Biochem 51:4779–4789

    Article  CAS  Google Scholar 

  • Edman P (1950) Method for determination of the amino acid sequence in peptides. Acta Chem Scand 4:283–293

    Article  CAS  Google Scholar 

  • Faustman C, Cassens RG (1990) The biochemical basis for discoloration in fresh meat: a review. J Muscle Foods 1:217–243

    Article  Google Scholar 

  • Fosmire GJ, Brown WD (1976) Yellowfin tuna (Thunnus albacares) myoglobin: characterization and comparative stability. Comp Biochem Physiol B 55:293–299

    Article  CAS  PubMed  Google Scholar 

  • Greenfield NJ (2006) Using circular dichroism spectra to estimate protein secondary structure. Nat Protoc 1:2876–2890

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Greer-Walker MG, Pull CA (1975) A survery of red and white muscle in marine fish. J Fish Biol 7:295–300

    Article  Google Scholar 

  • Gutzke D, Trout GR (2002) Temperature and pH dependence of the autoxidation rate of bovine, ovine, porcine, and cervine oxymyoglobin isolated from three different muscle-longissimus dorsi, gluteus medius, and biceps femoris. J Agric Food Chem 50:2673–2678

    Article  CAS  PubMed  Google Scholar 

  • Haard NF (1992) Biochemistry and chemistry of color and color change in seafoods. In: Advance in seafood biochemistry. (Flick GJ and Martin RE eds.). Technomic Publishing Co., Inc. USA.

  • Hamoir G (1953) Myoglobin from carp muscle. Nature 171:345–346

    Article  CAS  PubMed  Google Scholar 

  • Hasan MM, Watabe S, Ochiai Y (2012) Structural characterization of carangid fish myoglobins. Fish Physiol Biochem 38:1311–1322

    Article  CAS  PubMed  Google Scholar 

  • Helbo S, Fago A (2011) Allosteric modulation by S-nitrosation in the low-O2 affinity myoglobin from rainbow trout. Am J Physiol Integr Comp Physiol 300:R101–R108

    Article  CAS  Google Scholar 

  • Joseph P, Suman SP, Li S, Fontaine M, Steinke L (2012) Amino acid sequence of myoglobin from white-tailed deer (Odocoileus virginianus). Meat Sci 92:160–163

    Article  CAS  PubMed  Google Scholar 

  • Kannan G, Kouakou B, Gelaye S (2001) Color changes reflecting myoglobin and lipid oxidation in chevon cuts during refrigerated display. Small Ruminant Res 42:67–75

    Article  Google Scholar 

  • Kendrew JC, Dickerson RE, Strandberg BE, Hart RG, Davies DR, Phillips DC, Shore VC (1960) Structure of myoglobin: a three-dimensional Fourier synthesis at 2 Å. resolution. Nature 185:422–427

    Article  CAS  PubMed  Google Scholar 

  • Kitahara Y, Matsuoka A, Kobayashi N, Shikama K (1990) Autoxidation of myoglobin from bigeye tuna fish (Thunnus obesus). Biochim Biophys Acta 1038:23–28

    Article  CAS  PubMed  Google Scholar 

  • Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157:105–132

    Article  CAS  PubMed  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  CAS  PubMed  Google Scholar 

  • Livingston DJ, Brown WD (1981) The chemistry of myoglobin and its reactions. Food Technol 25:256–275

    Google Scholar 

  • Madden PW, Babcock MJ, Vayda ME, Cashon RE (2004) Structural and kinetic characterization of myoglobins from eurythermal and stenothermal fish species. Comp Biochem Physiol – Part B Biochem Mol Biol 137:341–350

    Article  Google Scholar 

  • Marcinek DJ, Bonaventura J, Wittenberg JB, Block BA (2001) Oxygen affinity and amino acid sequence of myoglobins from endothermic and ectothermic fish. Am J Physiol Regul Integr Comp Physiol 208:R1123–R1133

    Article  Google Scholar 

  • Matsuura F, Hashimoto K (1954) Determination of the content of hemoglobin, myoglobin and cytochrome C in the muscles of fishes. Bull Japan Soc Sci Fish 20:308–312

    Article  CAS  Google Scholar 

  • Matsuura F, Hashimoto K (1959) Chemical studies on the red muscle (chiai) of fishes. Bull Japan Soc Sci Fish 24:809–815

    Article  CAS  Google Scholar 

  • Mirceta S, Signore AV, Burns JM, Cossins AR, Campbell KL, Berenbrink M (2013) Evolution of mammalian diving capacity traced by myoglobin net surface charge. Science 340:1234192

    Article  PubMed  Google Scholar 

  • Naylor GJP, Gerstein M (2000) Measuring shifts in function and evolutionary opportunity using variability profiles: a case study of the globins. J Mol Evol 51:223–233

    Article  CAS  PubMed  Google Scholar 

  • Nicola NA, Minasian E, Appleby CA, Leach SJ (1975) Circular dichroism studies of myoglobin and leghemoglobin. Biochemistry 14:5141–5149

    Article  CAS  PubMed  Google Scholar 

  • Nurilmala M, Ushio H, Ochiai Y (2018) pH- and temperature- dependent denaturation profiles of tuna myoglobin. Fish Sci 84:579–587

    Article  CAS  Google Scholar 

  • Ochiai Y, Ueki N, Watabe S (2009) Effects of point mutations on the structural stability of tuna myoglobins. Comp Biochem Physiol – Part B Biochem Mol Biol 153:223–228

    Article  Google Scholar 

  • Ochiai Y, Watanabe Y, Ozawa H, Ikegami S, Uchida N, Watabe S (2010) Thermal denaturation profiles of tuna myoglobin. Biosci Biotechnol Biochem 74:1673–1679

    Article  CAS  PubMed  Google Scholar 

  • Ordway GA, Garry DJ (2004) Myoglobin: an essential hemoprotein in striated muscle. J Exp Biol 207:3441–3446

    Article  CAS  PubMed  Google Scholar 

  • Ramos CHI, Ferreira ST (2005) Protein folding, misfolding and aggregation: evolving concepts and conformational diseases. Protein Pept Lett 12:213–222

    Article  CAS  PubMed  Google Scholar 

  • Rayner BS, Wu BJ, Raftery M, Stocker R, Witting PK (2005) Human S-nitroso oxymyoglobin is a store of vasoactive nitric oxide. J. Biol. Chem. 280:9985–9993

    Article  CAS  PubMed  Google Scholar 

  • Regis WCB, Fattori J, Santoro MM, Jamin M, Ramos CHI (2005) On the difference in stability between horse and sperm whale myoglobins. Arch Biochem Biophys 436:168–177

    Article  CAS  PubMed  Google Scholar 

  • Rossi-Fanelli A, Antonini E (1955) Purification and crystallization of the myoglobin of salt water fish. Arch Biochem Biophys 58:498–500

    Article  CAS  PubMed  Google Scholar 

  • Saud S, Li G, Sun Y, Khan MI, Rehman AU, Uzzaman A, Liu W, Ding C, Xiao H, Wang Y, Cao C (2019) A facile isoelectric focusing of myoglobin and hemoglobin used as markers for screening of chicken meat quality in China. Electrophoresis 20:2767–2774

    Article  Google Scholar 

  • Schreiter ER, Rodriguez MM, Weichsel A, Montfort WR, Bonaventura J (2007) S-nitrosylation-induced conformational change in blackfin tuna myoglobin. J Biol Chem 282:19773–19780

    Article  CAS  PubMed  Google Scholar 

  • Schulz GE, Schirmer RH (1979) Principles of protein structure. Springer-Verlag, New York, USA

    Book  Google Scholar 

  • Shikama K, Matsuoka A (1994) Aplysia myoglobin with unusual properties: another prototype in myoglobin and haemeglobin biochemistry. Biol Rev 69:233–251

    Article  CAS  PubMed  Google Scholar 

  • Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150:76–85

    Article  CAS  PubMed  Google Scholar 

  • Springer BA, Egeberg KD, Sligar SG, Rohlfs RJ, Mathews AJ, Olson JS (1989) Discrimination between oxygen and carbon monoxide and inhibition of autoxidation by myoglobin. Site-directed mutagenesis of the distal histidine. J Biol Chem 264:3057–3060

    CAS  PubMed  Google Scholar 

  • Strehlow KG, Baldwin RL (1989) Effect of the substitution Ala→ Gly at each of five residue positions in the C-peptide helix. Biochemistry 28:2130–2133

    Article  CAS  PubMed  Google Scholar 

  • Suzuki N, Hashimoto K, Matsuura F (1973) Studies on the colour of skipjack meat. Bull Japan Soc Sci Fish 39:35–41

    Article  CAS  Google Scholar 

  • Tada T, Watanabe Y, Matsuoka A, Ikeda-Saito M, Imai K, Ni-Hei Y, Shikama K (1998) African elephant myoglobin with an unusual autoxidation behavior: comparison with the H64Q mutant of sperm whale myoglobin. Biochem Biophys Acta 1387:165–176

    CAS  PubMed  Google Scholar 

  • Ueki N, Ochiai Y (2005) Structural stabilities of recombinant scombridae fish myoglobins. Biosci Biotechnol Biochem 69:1935–1943

    Article  CAS  PubMed  Google Scholar 

  • Ueki N, Ochiai Y (2006) Effect of amino acid replacements on the structural stability of fish myoglobin. J Biochem 140:649–656

    Article  CAS  PubMed  Google Scholar 

  • Ueki N, Chow CJ, Ochiai Y (2005) Characterization of bullet tuna myoglobin with reference to the thermostability-structure relationship. J Agric Food Chem 53:4968–4975

    Article  CAS  PubMed  Google Scholar 

  • Whitaker TL, Berry MB, Ho EL, Hargrove MS, Philips GN, Komiyama NH, Nagai K, Olson JS (1995) The D-Helix in myoglobin and in the β subunit of hemoglobin is required for the reduction of heme. Biochemistry 34:8221–8226

    Article  CAS  PubMed  Google Scholar 

  • Wiechelman KJ, Braun RD, Fitzpatrick JD (1988) Investigation of the bicinchoninic acid protein assay: identification of the groups responsible for color formation. Anal Biochem 175:231–237

    Article  CAS  PubMed  Google Scholar 

  • Wittenberg JB, Wittenberg BA (2003) Myoglobin function reassessed. J Exp Biol 206:2011–2020

    Article  CAS  PubMed  Google Scholar 

  • Woody RW (1995) Circular dichroism. Method Enzymol 246:34–71

    Article  CAS  Google Scholar 

  • Yamada T, Takakura H, Jue T, Hashimoto T, Ishizawa R, Furuichi Y, Kato Y, Iwanaka N, Masuda K (2016) Myoglobin and the regulation of mitochondrial respiratory chain complex IV. J Physiol 594:483–495

    Article  CAS  PubMed  Google Scholar 

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Funding

This work was partly supported by the Japan Society for Promotion of Sciences (KAKENHI # 22380015 to Y. O.).

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Authors and Affiliations

  1. Graduate School of Agricultural and Life Sciences, The Univerisity of Tokyo, Bunkyo, Tokyo, 113-8657, Japan

    Muhammad Mehedi Hasan & Hideki Ushio

  2. Department of Fisheries Technology, Bangladesh Agricultural University, Mymensingh, 2202, Bangladesh

    Muhammad Mehedi Hasan

  3. Graduate School of Agricultural Science, Tohoku University, Sendai, Miyagi, 980-8572, Japan

    Purnama Arafah & Yoshihiro Ochiai

  4. Faculty of Applied Bioscience, Kanagawa Institute of Technology, Shimo-Ogino, Atsugi, Kanagawa, 243-0292, Japan

    Hideo Ozawa

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  1. Muhammad Mehedi Hasan
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  5. Yoshihiro Ochiai
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All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Muhammad Mehedi Hasan, Hideo Ozawa, and Purnama Arafah. The first draft of the manuscript was written by Muhammad Mehedi Hasan and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Muhammad Mehedi Hasan.

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Hasan, M.M., Arafah, P., Ozawa, H. et al. Thermal denaturation and autoxidation profiles of carangid fish myoglobins. Fish Physiol Biochem 47, 487–498 (2021). https://doi.org/10.1007/s10695-021-00928-7

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