Skip to main content

Sustained High Power Performance

Possible Strategies for Integrating Energy Supply and Demand in Flight Muscle

  • Chapter
Nature’s Versatile Engine: Insect Flight Muscle Inside and Out

Part of the book series: Molecular Biology Intelligence Unit ((MBIU))

Abstract

The high power output necessary for insect flight has resulted in the evolution of muscles with large and abundant myofibrils, the so called ‘myofibrillar’ muscles. In principle, this modification should come with a trade-off as the broader diameter of the myofibril would slow ATP/ADP flux and potentially constrain muscle speed (myosin ATPase). However asynchronous flight muscle exhibits no such trade-off as it simultaneously displays speed, power, and endurance. Insect flight muscle appears to lack the components for a phosphagen shuttle system that would provide temporal and spatial buffering of nucleotides. The reliance on a phosphagen shuttle is partly alleviated by the proximity of mitochondria to myofibrils. We present a model for how IFM meets its operational demands by minimizing nucleotide diffusion and facilitating the import and export of nucleotides to the myofibril.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Harrison JF, Roberts SP. Flight respiration and energetics. Annu Rev Physiol 2000; 62:179–205.

    Article  PubMed  CAS  Google Scholar 

  2. Kammer AE, Heinrich B. Insect flight metabolism. In: Treherne JE, Berridge MJ, Wigglesworth VB, eds. Advances in Insect Physiology, Vol. 13. London: Academic Press, 1978:133–228.

    Google Scholar 

  3. Sacktor B. Utilization of fuels by muscle. In: Candy DJ, Kilby BA, eds. Insect Biochemistry and Function. London: Chapman and Hall, 1975:1–81.

    Google Scholar 

  4. Beenakkers AMT, Van der Horst DJ, Van Marrewijk WJA. Biochemical processes directed to flight muscle metabolism. In: Kerkut GA, Gilbert LI, eds. Comprehensive Insect Physiology, Biochemistry and Pharmacology. Oxford: Pergamon Press, 1985:10:451–486.

    Google Scholar 

  5. Lindstedt SL, Hokanson JF, Wells DJ et al. Running energetics in the pronghorn antelope. Nature 1991; 353(6346):748–750.

    Article  PubMed  CAS  Google Scholar 

  6. Casey TM, Ellington CP, Gabriel JM. Allometric scaling of muscle performance and metabolism: Insects. Adv Biosci 1992; 84:152–162.

    CAS  Google Scholar 

  7. Hochachka PW. Muscles as molecular and metabolic machines. Boca Raton: CRC Press, 1994.

    Google Scholar 

  8. Josephson RK, Malamud JG, Stokes DR. Asynchronous muscle: A primer. J Exp Biol 2000; 203(Pt 18):2713–2722.

    PubMed  CAS  Google Scholar 

  9. Swank DM, Bartoo ML, Knowles AF et al. Alternative exon-encoded regions of Drosophila myosin heavy chain modulate ATPase rates and actin sliding velocity. J Biol Chem 2001; 276(18):15117–15124.

    Article  PubMed  CAS  Google Scholar 

  10. Squire JM. Muscle: Design, Diversity, and Disease. Menlo Park: Benjamin/Cummings Publishing Co., 1986.

    Google Scholar 

  11. Lindstedt SL, McGlothlin T, Percy E et al. Task-specific design of skeletal muscle: Balancing muscle structural composition. Comp Biochem Physiol B Biochem Mol Biol 1998; 120(1):35–40.

    Article  PubMed  CAS  Google Scholar 

  12. Crabtree B, Newsholme EA. Comparative aspects of fuel utilization and metabolism by muscle. In: Usherwood PNR, ed. Insect Muscle. London: Academic Press, 1975.

    Google Scholar 

  13. O’Brien DM, Suarez RK. Fuel use in hawkmoth (Amphion floridensis) flight muscle: Enzyme activities and flux rates. J Exp Zool 2001; 290(2):108–114.

    Article  PubMed  CAS  Google Scholar 

  14. Crabtree B, Newsholme EA. The activities of phosphorylase, hexokinase, phosphofructokinase, lactate dehydrogenase and the glycerol 3-phosphate dehydrogenases in muscles from vertebrates and invertebrates. Biochem J 1972; 126(1):49–58.

    PubMed  CAS  Google Scholar 

  15. Sacktor B. Biochemical adaptations for flight in the insect. Biochem Soc Symp 1976; (41):111–131.

    PubMed  CAS  Google Scholar 

  16. Wojtas K, Slepecky N, von Kalm L et al. Flight muscle function in Drosophila requires colocalization of glycolytic enzymes. Mol Biol Cell 1997; 8(9):1665–1675.

    PubMed  CAS  Google Scholar 

  17. Sullivan DT, MacIntyre R, Fuda N et al. Analysis of glycolytic enzyme colocalization in Drosophila flight muscle. J Exp Biol 2003; 206(Pt 12):2031–2038.

    Article  PubMed  CAS  Google Scholar 

  18. Sacktor B, Hurlbut EC. Regulation of metabolism in working muscle in vivo. II. Concentrations of adenine nucleotides, arginine phosphate, and inorganic phosphate in insect flight muscle during flight. J Biol Chem 1966; 241(3):632–634.

    PubMed  CAS  Google Scholar 

  19. Pette D. Cytosolic organization of carbohydrate-metabolism enzymes in cross-striated muscle. Biochem Soc Trans 1978; 6(1):9–11.

    PubMed  CAS  Google Scholar 

  20. Lange S, Auerbach D, McLoughlin P et al. Subcellular targeting of metabolic enzymes to titin in heart muscle may be mediated by DRAL/FHL-2. J Cell Sci 2002; 115(Pt 24):4925–4936.

    Article  PubMed  CAS  Google Scholar 

  21. Kraft T, Hornemann T, Stolz M et al. Coupling of creatine kinase to glycolytic enzymes at the sarcomeric I-band of skeletal muscle: A biochemical study in situ. J Muscle Res Cell Motil 2000; 21(7):691–703.

    Article  PubMed  CAS  Google Scholar 

  22. Wegener G. Flying insects: Model systems in exercise physiology. Experientia 1996; 52(5):404–412.

    Article  PubMed  CAS  Google Scholar 

  23. Suarez RK. Shaken and stirred: Muscle structure and metabolism. J Exp Biol 2003; 206(Pt 12):2021–2029.

    Article  PubMed  CAS  Google Scholar 

  24. Sweeney HL. The importance of the creatine kinase reaction: The concept of metabolic capacitance. Med Sci Sports Exerc 1994; 26(1):30–36.

    PubMed  CAS  Google Scholar 

  25. Ellington WR. Evolution and physiological roles of phosphagen systems. Annu Rev Physiol 2001; 63:289–325.

    Article  PubMed  CAS  Google Scholar 

  26. Kushmerick MJ, Conley KE. Energetics of muscle contraction: The whole is less than the sum of its parts. Biochem Soc Trans 2002; 30(2):227–231.

    Article  PubMed  CAS  Google Scholar 

  27. Wyss M, Maughan DM, Wallimann T. Reevaluation of the structure and physiological function of guanidino kinases in fruitfly (Drosophila), sea urchin (Psammechinus miliaris) and man. Biochem J 1995; 309:255–261.

    PubMed  CAS  Google Scholar 

  28. Yoshizaki K, Watari H, Radda GK. Role of phosphocreatine in energy transport in skeletal muscle of bullfrog studied by 31P-NMR. Biochim Biophys Acta 1990; 1051(2):144–150.

    Article  PubMed  CAS  Google Scholar 

  29. Jacobus WE. Theoretical support for the heart phosphocreatine energy transport shuttle based on the intracellular diffusion limited mobility of ADP. Biochem Biophys Res Commun 1985; 133(3):1035–1041.

    Article  PubMed  CAS  Google Scholar 

  30. de Graaf RA, van Kranenburg A, Nicolay K. In vivo (31)P-NMR diffusion spectroscopy of ATP and phosphocreatine in rat skeletal muscle. Biophys J 2000; 78(4):1657–1664.

    Article  PubMed  Google Scholar 

  31. Kongas O, van Beek JH. Diffusion barriers for ADP in the cardiac cell. Mol Biol Rep 2002; 29(1–2):141–144.

    Article  PubMed  CAS  Google Scholar 

  32. Bagnato P, Barone V, Giacomello E et al. Binding of an ankyrin-1 isoform to obscurin suggests a molecular link between the sarcoplasmic reticulum and myofibrils in striated muscles. J Cell Biol 2003; 160(2):245–253.

    Article  PubMed  CAS  Google Scholar 

  33. Kaasik A, Veksler V, Boehm E et al. Energetic crosstalk between organelles: Architectural integration of energy production and utilization. Circ Res 2001; 89(2):153–159.

    PubMed  CAS  Google Scholar 

  34. Andrienko T, Kuznetsov AV, Kaambre T et al. Metabolic consequences of functional complexes of mitochondria, myofibrils and sarcoplasmic reticulum in muscle cells. J Exp Biol 2003; 206(Pt 12):2059–2072.

    Article  PubMed  CAS  Google Scholar 

  35. Vendelin M, Eimre M, Seppet E et al. Intracellular diffusion of adenosine phosphates is locally restricted in cardiac muscle. Mol Cell Biochem 2004; 256–257(1–2):229–241.

    Article  PubMed  Google Scholar 

  36. Ashman K, Houthaeve T, Clayton J et al. The application of robotics and mass spectrometry to the characterisation of the Drosophila melanogaster indirect flight muscle proteome. Letters Peptide Science 1997; 4:57–65.

    CAS  Google Scholar 

  37. Ventura-Clapier R, Veksler V, Hoerter JA. Myofibrillar creatine kinase and cardiac contraction. Mol Cell Biochem 1994; 133–134:125–144.

    Article  PubMed  Google Scholar 

  38. Rikhy R, Ramaswami M, Krishnan KS. A temperaturesensitive allele of Drosophila sesB reveals acute functions for the mitochondrial adenine nucleotide translocase in synaptic transmission and dynamin regulation. Genetics 2003; 165(3):1243–1253.

    PubMed  CAS  Google Scholar 

  39. Jiang X, Wang X. Cytochrome C-Mediated Apoptosis. Annu Rev Biochem 2004; 73:87–106.

    Article  PubMed  CAS  Google Scholar 

  40. Martinez LO, Jacquet S, Esteve JP et al. Ectopic beta-chain of ATP synthase is an apolipoprotein A-I receptor in hepatic HDL endocytosis. Nature 2003; 421(6918):75–79.

    Article  PubMed  CAS  Google Scholar 

  41. Buettner R, Papoutsoglou G, Scemes E et al. Evidence for secretory pathway localization of a voltage-dependent anion channel isoform. Proc Natl Acad Sci USA 2000; 97(7):3201–3206.

    Article  PubMed  CAS  Google Scholar 

  42. Frommer WB, Schulze WX, Lalonde S. Plant science. Hexokinase, Jack-of-all-trades. Science 2003; 300(5617):261–263.

    Article  PubMed  CAS  Google Scholar 

  43. Conley KE, Kemper WF, Crowther GJ. Limits to sustainable muscle performance: Interaction between glycolysis and oxidative phosphorylation. J Exp Biol 2001; 204(Pt 18):3189–3194.

    PubMed  CAS  Google Scholar 

  44. Klowden MJ. Physiological systems in insects. San Diego: Academic Press, 2002.

    Google Scholar 

  45. Montooth KL, Marden JH, Clark AG. Mapping determinants of variation in energy metabolism, respiration and flight in Drosophila. Genetics 2003; 165(2):623–635.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

Copyright information

© 2006 Eurekah.com and Springer Science+Business Media

About this chapter

Cite this chapter

Vishnudas, V., Vigoreaux, J.O. (2006). Sustained High Power Performance. In: Nature’s Versatile Engine: Insect Flight Muscle Inside and Out. Molecular Biology Intelligence Unit. Springer, Boston, MA. https://doi.org/10.1007/0-387-31213-7_15

Download citation

Publish with us

Policies and ethics