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Differential Interaction of Myoglobin with Select Fatty Acids of Carbon Chain Lengths C8 to C16

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Lipids

Abstract

Previous studies have shown that palmitic acid (PAM) and oleic acid (OLE) can bind myoglobin (Mb). How fatty acids (FA) with different carbon chain lengths and sulfate substitution interact with Mb remains uncertain. Indeed, C8:0 and C10:0 fatty acids do not perturb the intensities of the 1H-NMR MbCN signal intensity at FA:Mb ratios below 2:1. Starting with C12:0, C12:0-C16:0, FA induce a noticeable spectral change. C12:0 and C14:0 FA affect both the 5- and 8-heme methyl signals, whereas the C16:0 FA perturbs only the 8-heme methyl signal. All C12:0–C16:0 saturated FA induce upfield shifts in the –CH2 peak of different FA in the presence of Mb. Increasing the apparent solubility with a sulfate group substitution enhances the FA interaction of lauric sulfate (LAU 1-SO4) but not palmitate sulfate acid (PAM 1-SO4). The detergent (DET) property of FA has no significant contribution. Common positive, neutral, and negative DET at DET:Mb ratio of 1:1 induce no perturbation of the MbCN spectra. The experiment observations establish a basis to investigate the molecular mechanism underlying the FA interaction with Mb.

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Abbreviations

FA:

Fatty acid(s)

OCT:

Octanoic acid, C8:0

DEC:

Decanoic acid, C10:0

LAU:

Lauric acid, C12:0

MYR:

Myristic acid, C14:0

PAM:

Palmitic acid, C16:0

LAU 1-SO4 :

Lauryl sulfate

PAM 1-SO4 :

Palmityl sulfate

FABP:

Fatty acid binding protein

Mb:

Myoglobin

MbCN:

Cyanometmyoglobin

References

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

    Article  CAS  PubMed  Google Scholar 

  2. Gros G, Wittenberg B, Jue T (2010) Myoglobin’s old and new clothes: from molecular structure to function in living cells. J Exp Biol 213:2713–2725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Chung Y, Mole PA, Sailasuta N, Tran TK, Hurd R, Jue T (2005) Control of respiration and bioenergetics during muscle contraction. Am J Physiol Cell Physiol 288:C730–C738

    Article  CAS  PubMed  Google Scholar 

  4. Ponganis PJ, Kreutzer U, Sailasuta N, Knower T, Hurd R, Jue T (2002) Detection of myoglobin desaturation in Mirounga angustirostris during apnea. Am J Physiol Regul Integr Comp Physiol 282:R267–R272

    Article  CAS  PubMed  Google Scholar 

  5. Wittenberg BA, Wittenberg JB (1989) Transport of oxygen in muscle. Annu Rev Physiol 51:857–878

    Article  CAS  PubMed  Google Scholar 

  6. Chung Y, Jue T (1996) Cellular response to reperfused oxygen in the postischemic myocardium. Am J Physiol 271:H687–H695

    CAS  PubMed  Google Scholar 

  7. Chung Y, Huang SJ, Glabe A, Jue T (2006) Implication of CO inactivation on myoglobin function. Am J Physiol Cell Physiol 290:C1616–C1624

    Article  CAS  PubMed  Google Scholar 

  8. Glabe A, Chung Y, Xu D, Jue T (1998) Carbon monoxide inhibition of regulatory pathways in myocardium. Am J Physiol 274:H2143–H2151

    CAS  PubMed  Google Scholar 

  9. Garry DJ, Ordway GA, Lorenz JN, Radford NB, Chin ER, Grange RW, Bassel-Duby R, Williams RS (1998) Mice without myoglobin. Nature 395:905–908

    Article  CAS  PubMed  Google Scholar 

  10. Godecke A, Flogel U, Zanger K, Ding Z, Hirchenhain J, Decking UK, Schrader J (1999) Disruption of myoglobin in mice induces multiple compensatory mechanisms. Proc Natl Acad Sci USA 96:10495–10500

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Lin PC, Kreutzer U, Jue T (2007) Myoglobin translational diffusion in myocardium and its implication on intracellular oxygen transport. J Physiol 578:595–603

    Article  CAS  PubMed  Google Scholar 

  12. Lin PC, Kreutzer U, Jue T (2007) Anisotropy and temperature dependence of myoglobin translational diffusion in myocardium: implication on oxygen transport and cellular architecture. Biophy J 92:2608–2620

    Article  CAS  Google Scholar 

  13. Papadopoulos S, Endeward V, Revesz-Walker B, Jurgens KD, Gros G (2001) Radial and longitudinal diffusion of myoglobin in single living heart and skeletal muscle cells. Proc Natl Acad Sci USA 98:5904–5909

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Papadopoulos S, Jurgens KD, Gros G (1995) Diffusion of myoglobin in skeletal muscle cells -dependence on fibre type, contraction and temperature. Pflugers Arch Eur J Physiol 430:519–525

    Article  CAS  Google Scholar 

  15. Flogel U, Merx MW, Godecke A, Decking UKM, Schrader J (2001) Myoglobin: a scavenger of bioactive NO. Proc Natl Acad Sci 98:735–740

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Kreutzer U, Jue T (2004) The role of myoglobin as a scavenger of cellular NO in myocardium. Am J Physiol 286:H985–H991

    CAS  Google Scholar 

  17. Kreutzer U, Jue T (2006) Investigation of bioactive NO-scavenging role of myoglobin in myocardium. Eur J Physiol 452:36–42

    Article  CAS  Google Scholar 

  18. Rassaf T, Flogel U, Drexhage C, Hendgen-Cotta U, Kelm M, Schrader J (2007) Nitrite reductase function of deoxymyoglobin: oxygen sensor and regulator of cardiac energetics and function. Circ Res 100:1749–1754

    Article  CAS  PubMed  Google Scholar 

  19. Flogel U, Laussmann T, Godecke A, Abanador N, Schafers M, Fingas CD, Metzger S, Levkau B, Jacoby C, Schrader J (2005) Lack of myoglobin causes a switch in cardiac substrate selection. Circ Res 96:e68–e75

    Article  PubMed  Google Scholar 

  20. Gloster J (1977) Studies on fatty-acid binding characteristics of myoglobin and Z-protein. J Mol Cell Cardiol 9:15

    Article  Google Scholar 

  21. Gloster J, Harris P (1977) Fatty-acid binding to cytoplasmic proteins of myocardium and red and white skeletal-muscle in rat—possible new role for myoglobin. Biochem Biophys Res Commun 74:506–513

    Article  CAS  PubMed  Google Scholar 

  22. Gotz FM, Hertel M, Groschelstewart U (1994) Fatty-acid-binding of myoglobin depends on its oxygenation. Bio Chem Hoppe-Seyler 375:387–392

    Article  CAS  Google Scholar 

  23. Shih L, Chung Y, Sriram R, Jue T (2014) Palmitate interaction with physiological states of myoglobin. Biochim Biophys Acta 1840:656–666

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Sriram R, Kreutzer U, Shih L, Jue T (2008) Interaction of fatty acid with myoglobin. FEBS Lett 582:3643–3649

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. La Mar GN, De Ropp JS (1993) NMR methodology for paramagnetic proteins. In: Berliner LJ, Reuben J (eds) NMR of paramagnetic molecules. Plenum, New York

    Google Scholar 

  26. La Mar GN, Horrocks WD Jr, Holm RH (1973) NMR of paramagnetic molecules. Academic Press, Inc., New York

    Google Scholar 

  27. La Mar GN, Shulman RG (1979) Model compounds as aids in interpreting NMR spectra of hemoproteins. Biological applications of magnetic resonance. Academic, New York

    Google Scholar 

  28. Bertini I, Luchinat C, Parigi G (2001) Solution NMR of paramagnetic molecules. Elsevier, Amsterdam

    Google Scholar 

  29. Tofani L, Feis A, Snoke RE, Berti D, Baglioni P, Smulevich G (2004) Spectroscopic and interfacial properties of myoglobin/surfactant complexes. Biophys J 87:1186–1195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Shih L, Chung Y, Sriram R, Jue T (2015) Interaction of myoglobin with oleic acid. Chem Phys Lipids 191:115–122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Jue T, Simond G, Wright TJ, Shih L, Chung Y, Sriram R, Kreutzer U, and Davis RW (2017) Effect of fatty acid interaction on myoglobin oxygen affinity and triglyceride metabolism. J Physiol Biochem. doi:10.1007/s13105-017-0559-z

  32. Tomita A, Kreutzer U, Adachi S, Koshihara SY, Jue T (2010) ‘It’s hollow’: the function of pores within myoglobin. J Exp Biol 213:2748–2754

    Article  CAS  PubMed  Google Scholar 

  33. Case DA, Karplus M (1979) Dynamics of ligand binding to heme proteins. J Mol Biol 132:343–368

    Article  CAS  PubMed  Google Scholar 

  34. Lecomte JT, La Mar GN (1985) 1H NMR study of labile proton exchange in the heme cavity as a probe for the potential ligand entry channel in myoglobin. Biochemistry 24:7388–7395

    Article  CAS  PubMed  Google Scholar 

  35. Aki H, Yamamoto M (1992) Thermodynamic aspects of fatty acids binding to human serum albumin: a microcalorimetric investigation. Chem Pharm Bull (Tokyo) 40:1553–1558

    Article  CAS  Google Scholar 

  36. Ashbrook JD, Spector AA, Santos EC, Fletcher JE (1975) Long chain fatty acid binding to human plasma albumin. J Biol Chem 250:2333–2338

    CAS  PubMed  Google Scholar 

  37. Vorum H, Brodersen R, Kraghhansen U, Pedersen AO (1992) Solubility of long-chain fatty-acids in phosphate buffer at pH-7.4. Biochem Biophys Acta 1126:135–142

    Article  CAS  PubMed  Google Scholar 

  38. Vorum H, Brodersen R (1994) Adsorption and physical state of medium and long chain fatty acids in neutral aqueous buffer solution. Chem Phys Lipids 74:43–48

    Article  CAS  Google Scholar 

  39. Akhrem AA, Andreiuk GM, Gurinovich NA, Kisel MA, Kiselev PA (1987) Fatty-acid initiated auto-oxidation of hemoglobin. Biokhimiia 52:2015–2021

    CAS  PubMed  Google Scholar 

  40. Nakamura Y, Nishida T (1971) Effect of hemoglobin concentration on the oxidation of linoleic acid. J Lipid Res 12:149–154

    CAS  PubMed  Google Scholar 

  41. Bienfait HF, Jacobs JM, Slater EC (1975) Mitochondrial oxygen affinity as a function of redox and phosphate potentials. Biochim Biophys Acta 376:446–457

    Article  CAS  PubMed  Google Scholar 

  42. Masuda K, Truscott K, Lin PC, Kreutzer U, Chung Y, Sriram R, Jue T (2008) Determination of myoglobin concentration in blood-perfused tissue. Eur J Appl Physiol 104:41–48

    Article  CAS  PubMed  Google Scholar 

  43. Wang D, Kreutzer U, Chung Y, Jue T (1997) Myoglobin and hemoglobin rotational diffusion in the cell. Biophys J 73:2764–2770

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Richieri GV, Ogata RT, Kleinfeld AM (1994) Equilibrium constants for the binding of fatty acids with fatty acid-binding proteins from adipocyte, intestine, heart, and liver measured with the fluorescent probe ADIFAB. J Biol Chem 269:23918–23930

    CAS  PubMed  Google Scholar 

  45. Vork MM, Glatz JF, van der Vusse GJ (1993) On the mechanism of long chain fatty acid transport in cardiomyocytes as facilitated by cytoplasmic fatty acid-binding protein. JtheorBiol 160:207–222

    CAS  Google Scholar 

  46. Thumser AE, Storch J (2007) Characterization of a BODIPY-labeled fluorescent fatty acid analogue. Binding to fatty acid-binding proteins, intracellular localization, and metabolism. Mol Cell Biochem 299:67–73

    Article  CAS  PubMed  Google Scholar 

  47. Storch J, Bass NM (1990) Transfer of fluorescent fatty acids from liver and heart fatty acid-binding proteins to model membranes. J Biol Chem 265:7827–7831

    CAS  PubMed  Google Scholar 

  48. Storch J, Thumser AE (2000) The fatty acid transport function of fatty acid-binding proteins. Biochim Biophys Acta 1486:28–44

    Article  CAS  PubMed  Google Scholar 

  49. Luxon BA, Milliano MT (1997) Cytoplasmic codiffusion of fatty acids is not specific for fatty acid binding protein. Am J Physiol 273:C859–C867

    CAS  PubMed  Google Scholar 

  50. Vork MM, Glatz JF, van der Vusse GJ (1997) Modelling intracellular fatty acid transport: possible mechanistic role of cytoplasmic fatty acid-binding protein. Prostaglandins Leukot Essent Fatty Acids 57:11–16

    Article  CAS  PubMed  Google Scholar 

  51. Chintapalli SV, Jayanthi S, Mallipeddi PL, Gundampati R, Suresh Kumar TK, van Rossum DB, Anishkin A, Adams SH (2016) Novel molecular interactions of acylcarnitines and fatty acids with myoglobin. J Biol Chem 291:25133–25143

    Article  CAS  PubMed  Google Scholar 

  52. Chintapalli SV, Bhardwaj G, Patel R, Shah N, Patterson RL, van Rossum DB, Anishkin A, Adams SH (2015) Molecular dynamic simulations reveal the structural determinants of fatty acid binding to oxy-myoglobin. PLoS One 10:e0128496

    Article  PubMed  PubMed Central  Google Scholar 

  53. Jones MN (1992) Surfactant interaction with biomembranes and proteins. Chem Soc Rev 2:127–136

    Article  Google Scholar 

  54. La Mar GN (1979) Model compounds as aids in interpreting NMR spectra of hemoproteins. In: Shulman RG (ed) Biological applications of magnetic resonance. Academic, New York

    Google Scholar 

  55. La Mar GN, Budd DL, Smith KM, Langry KC (1980) Nuclear magnetic resonance of high-spin ferric hemoproteins. Assignment of proton resonances in met-aquo myoglobins using deuterium-labeled hemes. J Am Chem Soc 102:1822–1827

    Article  Google Scholar 

  56. La Mar GN, Davis NL, Parish DW, Smith KM (1983) Heme orientational disorder in reconstituted and native sperm whale myoglobin. J Mol Biol 168:887–896

    Article  PubMed  Google Scholar 

  57. Busse SC, Jue T (1994) Two-dimensional NMR characterization of the deoxymyoglobin heme pocket. Biochemistry 33:10934–10943

    Article  CAS  PubMed  Google Scholar 

  58. La Mar GN, Dalichow F, Zhao X, Dou Y, Ikeda-Saito M, Chiu ML, Sligar SG (1994) 1H NMR investigation of distal mutant deoxy myoglobins. Interpretation of proximal His contact shifts in terms of a localized distal water molecule. J Biol Chem 269:29629–29635

    PubMed  Google Scholar 

  59. Otzen D (2011) Protein–surfactant interactions: a tale of many states. Biochim Biophys Acta 1814:562–591

    Article  CAS  PubMed  Google Scholar 

  60. Tanford C (1968) Protein denaturation. Adv Protein Chem 23:121–282

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We gratefully acknowledge funding support from NIH GM 58688 (TJ), the guidance of Dr. Ulrike Kreutzer, and scientific discussion with Clayton Germolus and Jessica Gregory.

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  1. Department of Biochemistry and Molecular Medicine, University of California Davis, Davis, CA, 95616-8635, USA

    Thomas Jue, Lifan Shih & Youngran Chung

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  1. Thomas Jue
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Correspondence to Thomas Jue.

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Jue, T., Shih, L. & Chung, Y. Differential Interaction of Myoglobin with Select Fatty Acids of Carbon Chain Lengths C8 to C16. Lipids 52, 711–727 (2017). https://doi.org/10.1007/s11745-017-4272-z

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