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Intracellular Oxygen Dynamics Observed by NIRS During Skeletal Muscle Contraction

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Application of Near Infrared Spectroscopy in Biomedicine

Part of the book series: Handbook of Modern Biophysics ((HBBT,volume 4))

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Abstract

Cellular respiration depends upon a coordinated response of the cardiovasculature and metabolism to meet changing energy demands in muscle. Even though the adjustments in blood flow, O2 gradient, and myoglobin (Mb) saturation will enhance O2 flux to the mitochondria at the initiation of contraction, the relative contribution of Mb vs. Hb remains an issue for contentious debate. Some researchers have ascribed no significant role for Mb in supplying O2 during muscle contraction. Since Mb has an extremely high affinity for O2, it cannot readily release its O2 store. Hb must then supply all the O2 from the onset of contraction. This viewpoint underpins many interpretations of the noninvasive near-infrared spectroscopy (NIRS) data. Although NIRS cannot discriminate between the Hb and Mb signals, many researchers have assumed that NIRS monitors only Hb oxygen saturation and desaturation kinetics. The present chapter introduces an experiment system that allows for the observations of Mb saturation during muscle contraction. The results then provide insights into the relative Hb vs. Mb contribution in the NIRS signal and into the mechanisms of oxygen delivery and consumption regulation.

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References

  1. Popel AS (1989) Theory of oxygen transport to tissue. Crit Rev Biomed Eng 17:257–321

    PubMed  CAS  Google Scholar 

  2. Costes F, Barthelemy JC, Feasson L, Busso T, Geyssant A, Denis C (1996) Comparison of muscle near-infrared spectroscopy and femoral blood gases during steady-state exercise in humans. J Appl Physiol 80:1345–1350

    Article  PubMed  CAS  Google Scholar 

  3. Seiyama A, Hazeki O, Tamura M (1988) Noninvasive quantitative analysis of blood oxygenation in rat skeletal muscle. J Biochem 103:419–424

    PubMed  CAS  Google Scholar 

  4. Theorell H (1938) Kristallinisches myoglobin. Biochem Z 268:73–82

    Google Scholar 

  5. Wilson JR, Mancini DM, McCully K, Ferraro N, Lanoce V, Chance B (1989) Noninvasive detection of skeletal muscle underperfusion with near-infrared spectroscopy in patients with heart failure. Circulation 80:1668–1674

    Article  PubMed  CAS  Google Scholar 

  6. Bank W, Chance B (1994) An oxidative defect in metabolic myopathies: diagnosis by noninvasive tissue oximetry. Ann Neurol 36:830–837

    Article  PubMed  CAS  Google Scholar 

  7. McCully KK, Hamaoka T (2000) Near-infrared spectroscopy: what can it tell us about oxygen saturation in skeletal muscle? Exerc Sport Sci Rev 28:123–127

    PubMed  CAS  Google Scholar 

  8. Harper AJ, Ferreira LF, Lutjemeier BJ, Townsend DK, Barstow TJ (2006) Human femoral artery and estimated muscle capillary blood flow kinetics following the onset of exercise. Exp Physiol 91:661–671

    Article  PubMed  Google Scholar 

  9. Kindig CA, Richardson TE, Poole DC (2002) Skeletal muscle capillary hemodynamics from rest to contractions: implications for oxygen transfer. J Appl Physiol 92:2513–2520

    PubMed  Google Scholar 

  10. Mole PA, Chung Y, Tran TK, Sailasuta N, Hurd R, Jue T (1999) Myoglobin desaturation with exercise intensity in human gastrocnemius muscle. Am J Physiol 277:R173–R180

    PubMed  CAS  Google Scholar 

  11. Richardson RS, Newcomer SC, Noyszewski EA (2001) Skeletal muscle intracellular PO2 assessed by myoglobin desaturation: response to graded exercise. J Appl Physiol 91:2679–2685

    PubMed  CAS  Google Scholar 

  12. Chung YR, 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  PubMed  CAS  Google Scholar 

  13. Tran TK, Sailasuta N, Kreutzer U, Hurd R, Chung Y, Mole P, Kuno S, Jue T (1999) Comparative analysis of NMR and NIRS measurements of intracellular PO2 in human skeletal muscle. Am J Physiol 276:R1682–R1690

    PubMed  CAS  Google Scholar 

  14. Nioka S, Wang DJ, Im J, Hamaoka T, Wang ZJ, Leigh JS, Chance B (2006) Simulation of Mb/Hb in NIRS and oxygen gradient in the human and canine skeletal muscles using H-NMR and NIRS. Adv Exp Med Biol 578:223–228

    Article  PubMed  CAS  Google Scholar 

  15. Hoofd L, Colier W, Oeseburg B (2003) A modeling investigation to the possible role of myoglobin in human muscle in near-infrared spectroscopy (NIRS) measurements. Adv Exp Med Biol 530:637–643

    Article  PubMed  Google Scholar 

  16. Antonini E, Brunori M (eds) (1971) Hemoglobin and myoglobin in their reactions with ligands. North-Holland, Amsterdam

    Google Scholar 

  17. Schenkman KA, Marble DR, Feigl EO, Burns DH (1999) Near-infrared spectroscopic measurement of myoglobin oxygen saturation in the presence of hemoglobin using partial least-squares analysis. Appl Spectrosc 53:325–331

    Article  CAS  Google Scholar 

  18. Reynafarje B (1963) Simplified method for the determination of myoglobin. J Lab Clin Med 61:138–145

    PubMed  CAS  Google Scholar 

  19. 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  PubMed  CAS  Google Scholar 

  20. Lewis SB, Schultz TA, Westbie DK, Gerich JE, Wallin JD (1977) Insulin-glucose dynamics during flow-through perfusion of the isolated rat hindlimb. Horm Metab Res 9:190–195

    Article  PubMed  CAS  Google Scholar 

  21. Masuda K, Takakura H, Furuichi Y, Iwase S, Jue T (2010) NIRS measurement of O2 dynamics in contracting blood and buffer perfused hindlimb muscle. Adv Exp Med Biol 662:323–328

    Article  PubMed  CAS  Google Scholar 

  22. Seiyama A (2006) Virtual cooperativity in myoglobin oxygen saturation curve in skeletal muscle in vivo. Dyn Med 5:3

    Article  PubMed  Google Scholar 

  23. Takakura H, Masuda K, Hashimoto T, Iwase S, Jue T (2010) Quantification of myoglobin deoxygenation and intracellular partial pressure of O2 during muscle contraction during haemoglobin-free medium perfusion. Exp Physiol 95:630–640

    Article  PubMed  CAS  Google Scholar 

  24. Constantin-Teodosiu D, Baker D, Constantin D, Greenhaff P (2008) PPARdelta agonism inhibits skeletal muscle PDC activity, mitochondrial ATP production and force generation during prolonged contraction. J Physiol 587:231–239

    Article  PubMed  Google Scholar 

  25. Raney MA, Turcotte LP (2006) Regulation of contraction-induced FA uptake and oxidation by AMPK and ERK1/2 is intensity dependent in rodent muscle. Am J Physiol Endocrinol Metab 291:E1220–E1227

    Article  PubMed  CAS  Google Scholar 

  26. Raney MA, Turcotte LP (2008) Evidence for the involvement of CaMKII and AMPK in Ca2+-dependent signaling pathways regulating FA uptake and oxidation in contracting rodent muscle. J Appl Physiol 104:1366–1373

    Article  PubMed  CAS  Google Scholar 

  27. Ruderman NB, Houghton CR, Hems R (1971) Evaluation of the isolated perfused rat hindquarter for the study of muscle metabolism. Biochem J 124:639–651

    PubMed  CAS  Google Scholar 

  28. Shiota M, Golden S, Katz J (1984) Lactate metabolism in the perfused rat hindlimb. Biochem J 222:281–292

    PubMed  CAS  Google Scholar 

  29. Shiota M, Sugano T (1986) Characteristics of rat hindlimbs perfused with erythrocyte- and albumin-free medium. Am J Physiol 251:C78–C84

    PubMed  CAS  Google Scholar 

  30. Seiyama A, Kosaka H, Maeda N, Shiga T (1996) Effect of hypothermia on skeletal muscle metabolism in perfused rat hindlimb. Cryobiology 33:338–346

    Article  PubMed  CAS  Google Scholar 

  31. Bonen A, Clark MG, Henriksen EJ (1994) Experimental approaches in muscle metabolism: hindlimb perfusion and isolated muscle incubations. Am J Physiol Endocrinol Metab 266:E1–E16

    CAS  Google Scholar 

  32. Philip LA, Dorothy SD (1971) Respiration and circulation. FASEB, Bethesda

    Google Scholar 

  33. Richardson RS, Duteil S, Wary C, Wray DW, Hoff J, Carlier PG (2006) Human skeletal muscle intracellular oxygenation: the impact of ambient oxygen availability. J Physiol 571:415–424

    Article  PubMed  CAS  Google Scholar 

  34. Schenkman KA, Marble DR, Burns DH, Feigl EO (1997) Myoglobin oxygen dissociation by multi-wavelength spectroscopy. J Appl Physiol 82:86–92

    PubMed  CAS  Google Scholar 

  35. Behnke BJ, Kindig CA, McDonough P, Poole DC, Sexton WL (2002) Dynamics of microvascular oxygen pressure during rest-contraction transition in skeletal muscle of diabetic rats. Am J Physiol Heart Circ Physiol 283:H926–H932

    PubMed  CAS  Google Scholar 

  36. Rossiter HB, Ward SA, Doyle VL, Howe FA, Griffiths JR, Whipp BJ (1999) Inferences from pulmonary O2 uptake with respect to intramuscular [phosphocreatine] kinetics during moderate exercise in humans. J Physiol 518(Pt 3):921–932

    Article  PubMed  CAS  Google Scholar 

  37. Deblasi RA, Ferrari M, Natali A, Conti G, Mega A, Gasparetto A (1994) Noninvasive measurement of forearm blood-blow and oxygen consumption by near-infrared spectroscopy. J Appl Physiol 76:1388–1393

    CAS  Google Scholar 

  38. Richardson RS, Noyszewski EA, Kendrick KF, Leigh JS, Wagner PD (1995) Myoglobin O2 desaturation during exercise: evidence of limited O2 transport. J Clin Invest 96:1916–1926

    Article  PubMed  CAS  Google Scholar 

  39. Kreutzer U, Jue T (1995) Critical intracellular O2 in myocardium as determined by 1H nuclear magnetic resonance signal of myoglobin. Am J Physiol 268:H1675–H1681

    PubMed  CAS  Google Scholar 

  40. Kreutzer U, Wang DS, Jue T (1992) Observing the 1H NMR signal of the myoglobin Val-E11 in myocardium: an index of cellular oxygenation. Proc Natl Acad Sci USA 89:4731–4733

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  42. Guyton GP, Stanek KS, Schneider RC, Hochachka PW, Hurford WE, Zapol DG, Liggins GC, Zapol WM (1995) Myoglobin saturation in free-diving Weddell seals. J Appl Physiol 79:1148–1155

    PubMed  CAS  Google Scholar 

  43. 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

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  46. 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  PubMed  CAS  Google Scholar 

  47. 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  PubMed  CAS  Google Scholar 

  48. Wittenberg JB (1970) Myoglobin-facilitated oxygen diffusion: role of myoglobin in oxygen entry into muscle. Physiol Rev 50:559–636

    PubMed  CAS  Google Scholar 

  49. Johnson RL, Heigenhauser GJF, Hsia CCW, Jones NL, Wagner PD (1996) Determinants of gas exchange and acid–base balance during exercise. In: Rowell LB, Shepher JT (eds) Regulation and integration of multiple systems. Oxford University Press, New York, pp 515–584

    Google Scholar 

  50. Baylor SM, Pape PC (1988) Measurement of myoglobin diffusivity in the myoplasm of frog skeletal muscle fibres. J Physiol 406:247–275

    PubMed  CAS  Google Scholar 

  51. 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  PubMed  CAS  Google Scholar 

  52. Verkman AS (2003) Diffusion in cells measured by fluorescence recovery after photobleaching. Methods Enzymol 360:635–648

    Article  PubMed  CAS  Google Scholar 

  53. Riveros-Moreno V, Wittenberg JB (1972) The self-diffusion coefficients of myoglobin and hemoglobin in concentrated solutions. J Biol Chem 247:895–901

    PubMed  CAS  Google Scholar 

  54. Groebe K (1995) An easy-to-use model for O2 supply to red muscle: validity of assumptions, sensitivity to errors in data. Biophys J 68:1246–1269

    Article  PubMed  CAS  Google Scholar 

  55. Lai N, Zhou H, Saidel GM, Wolf M, McCully K, Gladden LB, Cabrera ME (2009) Modeling oxygenation in venous blood and skeletal muscle in response to exercise using near-infrared spectroscopy. J Appl Physiol 106:1858–1874

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  58. Bentley TB, Meng H, Pittman RN (1993) Temperature dependence of oxygen diffusion and consumption in mammalian striated muscle. Am J Physiol 264:H1825–H1830

    PubMed  CAS  Google Scholar 

  59. Kreutzer U, Mekhamer Y, Chung Y, Jue T (2001) Oxygen supply and oxidative phosphorylation limitation in rat myocardium in situ. Am J Physiol Heart Circ Physiol 280:H2030–H2037

    PubMed  CAS  Google Scholar 

  60. Zhang J, Murakami Y, Zhang Y, Cho YK, Ye Y, Gong G, Bache RJ, Uğurbil K, From AH (1999) Oxygen delivery does not limit cardiac performance during high work states. Am J Physiol 277:H50–H57

    PubMed  CAS  Google Scholar 

  61. Hickson RC (1981) Skeletal muscle cytochrome c and myoglobin, endurance, and frequency of training. J Appl Physiol 51:746–749

    PubMed  CAS  Google Scholar 

  62. Masuda K, Kano Y, Nakano H, Inaki M, Katsuta S (1998) Adaptations of myoglobin in rat skeletal muscles to endurance running training: effects of intensity, duration, and period of training. Jpn J Phys Fitness Sports Med 47:561–571

    Google Scholar 

  63. Kindig CA, Kelley KM, Howlett RA, Stary CM, Hogan MC (2003) Assessment of O2 uptake dynamics in isolated single skeletal myocytes. J Appl Physiol 94:353–357

    PubMed  Google Scholar 

  64. Kreutzer U, Mekhamer Y, Tran TK, Jue T (1998) Role of oxygen in limiting respiration in the in situ myocardium. J Mol Cell Cardiol 30:2651–2655

    Article  PubMed  CAS  Google Scholar 

  65. Mancini DM, Wilson JR, Bolinger L, Li H, Kendrick K, Chance B, Leigh JS (1994) In vivo magnetic resonance spectroscopy measurement of deoxymyoglobin during exercise in patients with heart failure: demonstration of abnormal muscle metabolism despite adequate oxygenation. Circulation 90:500–508

    Article  PubMed  CAS  Google Scholar 

  66. Behnke BJ, Kindig CA, Musch TI, Koga S, Poole DC (2001) Dynamics of microvascular oxygen pressure across the rest-exercise transition in rat skeletal muscle. Respir Physiol 126:53–63

    Article  PubMed  CAS  Google Scholar 

  67. Kindig CA, Howlett RA, Hogan MC (2003) Effect of extracellular PO2 on the fall in intracellular PO2 in contracting single myocytes. J Appl Physiol 94:1964–1970

    PubMed  Google Scholar 

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Acknowledgments

I would like to acknowledge a grant-in-aid for Scientific Research from the Japanese Ministry of Education, Science, Sports and Culture (20680032, 23300237, KM) and partial support from the Yamaha Motor Foundation for Sports (KM). I also greatly appreciate invaluable scientific discussions with Dr. Hisashi Takakura.

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Authors and Affiliations

  1. Faculty of Human Sciences, Kanazawa University, Kanazawa, Ishikawa, 920-1192, Japan

    Kazumi Masuda Ph.D.

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  1. Kazumi Masuda Ph.D.
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Correspondence to Kazumi Masuda Ph.D. .

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Editors and Affiliations

  1. BIOCHEMISTRY & MOLECULAR MEDICINE, University of California Davis BIOCHEMISTRY & MOLECULAR MEDICINE, Davis, California, USA

    Thomas Jue

  2. Kanazawa University, Kanazawa, Japan

    Kazumi Masuda

Appendices

Problem

  1. 6.1.

    NIRS measurement of Mb saturation (SMbO2) at different tensions during muscle contraction shows the following:

Table 2
Full size table

What is the corresponding change in PO2, given an Mb P50 of 2.37 at 37°C? What is the change in O2 gradient, given a resting PO2 of 10 mmHg? Plot out the curves. Does the change in SMbO2, PO2, and O2 gradient show a linear relationship? What is the physiological implication in interpreting the SMbO2 data with respect to O2 gradient?

Further Reading

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

Kreutzer U, Jue T (1995) Critical intracellular O2 in myocardium as determined by 1H nuclear magnetic resonance signal of myoglobin. Am J Physiol 268:H1675–H1681

Lai N, Zhou H, Saidel GM, Wolf M, McCully K, Gladden LB, Cabrera ME (2009) Modeling oxygenation in venous blood and skeletal muscle in response to exercise using near-infrared spectroscopy. J Appl Physiol 106:1,858–1,874

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

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Masuda, K. (2013). Intracellular Oxygen Dynamics Observed by NIRS During Skeletal Muscle Contraction. In: Jue, T., Masuda, K. (eds) Application of Near Infrared Spectroscopy in Biomedicine. Handbook of Modern Biophysics, vol 4. Springer, Boston, MA. https://doi.org/10.1007/978-1-4614-6252-1_6

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