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Journal of Comparative Physiology B

, Volume 188, Issue 6, pp 919–927 | Cite as

Soluble calcium-binding proteins (SCBPs) of the earthworm Lumbricus terrestris: possible role as relaxation factors in muscle

  • Prasath Thiruketheeswaran
  • Ralf Huch
  • Jochen D’Haese
Original Paper
  • 42 Downloads

Abstract

The soluble Ca2+-binding protein (SCBP) from the earthworm Lumbricus terrestris was analyzed with regard to its role as a soluble muscle relaxation factor. The actomyosin ATPase activity was inhibited by the addition of decalcified SCBP as it binds Ca2+ stronger than the regulatory proteins associated with the actomyosin. Competitive 45Ca2+-binding assays with decalcified actomyosin and SCBP showed that 45Ca2+ is first bound to actomyosin and is subsequently taken over by SCBP with increasing incubation time. Ca2+ competition experiments carried out with 45Ca2+ loaded SCBP and fragmented sarcoplasmic reticulum vesicles revealed that 45Ca2+ bound to SCBP can be deprived by the ATP-dependent Ca2+ uptake of the sarcoplasmic reticulum. Furthermore, experiments in a diffusion chamber showed that the addition of SCBP significantly enhances the 45Ca2+ flux in a concentration dependent manner. The amount of the Ca2+ flux increase tends to reach a maximum value of about 70%. With all protein components isolated from the obliquely striated muscle, our in vitro experiments consistently show that SCBP may accelerate muscle relaxation similar as assumed for vertebrate parvalbumin.

Keywords

Lumbricus terrestris Soluble calcium-binding protein (SCBP) Sarcoplasmic reticulum Competition for Ca2+ Facilitated Ca2+ diffusion Soluble relaxing factor 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

References

  1. Arif SH (2009) A Ca2+-binding protein with numerous roles and uses: parvalbumin in molecular biology and physiology. Bioessays 31:410–421CrossRefGoogle Scholar
  2. Balmain N (1991) Calbindin-D9k. A vitamin-D-dependent, calcium-binding protein in mineralized tissues. Clin Orthop Relat Res 265:265–276Google Scholar
  3. Bastianelli E (2003) Distribution of calcium-binding proteins in the cerebellum. Cerebellum 2:242–262CrossRefGoogle Scholar
  4. Belge H, Gailly P, Schwaller B, Loffing J, Debaix H, Riveira-Munoz E, Beauwens R, Devogelaer JP, Hoenderop JG, Bindels RJ, Devuyst O (2007) Renal expression of parvalbumin is critical for NaCl handling and response to diuretics. Proc Natl Acad Sci USA 104:14849–14854CrossRefGoogle Scholar
  5. Berchtold MW, Celio MR, Heizmann CW (1984) Parvalbumin in non-muscle tissues of the rat. Quantitation and immunohistochemical localization. J Biol Chem 259:5189–5196PubMedGoogle Scholar
  6. Berridge MJ, Lipp P, Bootman MD (2000) The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1:11–21CrossRefGoogle Scholar
  7. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  8. Carlhoff D (1988) Dissertation. Charakterisierung der Proteine aus der schräggestreiften Muskulatur des Regenwurms Lumbricus terrestris mit besonderer Berücksichtigung der Myosin-gekoppelten Ca2+-Regulation. Heinrich-Heine-University, DüsseldorfGoogle Scholar
  9. Carlhoff D, D’Haese J (1987) Slow type muscle cells in the earthworm gizzard with a distinct, Ca2+-regulated myosin isoform. J Comp Physiol B 157:589–597CrossRefGoogle Scholar
  10. Celio MR, Pauls T, Schwaller B (1996) Guidebook to the calcium-binding proteins. Oxford University Press, New YorkGoogle Scholar
  11. Chin D, Means AR (2000) Calmodulin: a prototypical calcium sensor. Trends Cell Biol 10:322–328CrossRefGoogle Scholar
  12. Cook WJ, Ealick SE, Babu YS, Cox JA, Vijay-Kumar S (1991) Three-dimensional structure of a sarcoplasmic calcium-binding protein from Nereis diversicolor. J Biol Chem 266:652–656PubMedGoogle Scholar
  13. Cook WJ, Jeffrey LC, Cox JA, Vijay-Kumar S (1993) Structure of a sarcoplasmic calcium-binding protein from amphioxus refined at 2.4 A resolution. J Mol Biol 229:461–471CrossRefGoogle Scholar
  14. Cox JA (1990) Calcium vector protein and sarcoplasmic calcium binding proteins from invertebrate muscle. In: Dedman JR, Smith VL (eds) Stimulus-response coupling: the role of intracellular calcium. Telford Press, Caldwell, pp 85–110Google Scholar
  15. Cox JA, Wnuk W, Stein EA (1976) Isolation and properties of a sarcoplasmic calcium-binding protein from crayfish. Biochemistry 15:2613–2618CrossRefGoogle Scholar
  16. D’Haese J, Carlhoff D (1987) Localization and histochemical characterization of myosin isoforms in earthworm body wall muscle. J Comp Physiol B 157:171–179CrossRefGoogle Scholar
  17. D’Haese J, Ditgens A (1980) Double regulation in the obliquely striated muscle of Lumbricus terrestris. Musc Res Cell Motility 1:208Google Scholar
  18. Engelborghs Y, Mertens K, Willaert K, Luan-Rilliet Y, Cox JA (1990) Kinetics of conformational changes in Nereis sarcoplasmic calcium-binding protein upon binding of divalent ions. J Biol Chem 265:18809–18815PubMedGoogle Scholar
  19. Feher JJ (1983) Facilitated calcium diffusion by intestinal calcium-binding protein. Am J Physiol 244:C303–C307CrossRefGoogle Scholar
  20. Feher JJ (1984) Measurement of facilitated calcium diffusion by a soluble calcium-binding protein. Biochim Biophys Acta 773:91–98CrossRefGoogle Scholar
  21. Feher JJ, Fullmer CS, Fritzsch GK (1989) Comparison of the enhanced steady-state diffusion of calcium by calbindin-D9K and calmodulin: possible importance in intestinal calcium absorption. Cell Calcium 10:189–203CrossRefGoogle Scholar
  22. Fiske CH, Subbarow Y (1925) The colorimetric determination of phophorus. J Biol Chem 66:375–400Google Scholar
  23. Gao Y, Gillen CM, Wheatly MG (2006) Molecular characterization of the sarcoplasmic calcium-binding protein (SCP) from crayfish Procambarus clarkii. Comp Biochem Physiol B Biochem Mol Biol 144:478–487CrossRefGoogle Scholar
  24. Gerday C (1988) Soluble calcium binding proteins in vertebrate and invertebrate muscles. Calcium and calcium-binding Proteins. Springer, Berlin, pp 23–39Google Scholar
  25. Gerday C, Gillis JM (1976) Proceedings: the possible role of parvalbumins in the control of contraction. J Physiol 258:96P–97PGoogle Scholar
  26. Gillis JM (1985) Relaxation of vertebrate skeletal muscle. A synthesis of the biochemical and physiological approaches. Biochim Biophys Acta 811:97–145CrossRefGoogle Scholar
  27. Haeseleer F, Palczewski K (2002) Calmodulin and Ca2+-binding proteins (CaBPs): variations on a theme. Adv Exp Med Biol 514:303–317CrossRefGoogle Scholar
  28. Haiech J, Derancourt J, Pechere JF, Demaille JG (1979) Magnesium and calcium binding to parvalbumins: evidence for differences between parvalbumins and an explanation of their relaxing function. Biochemistry 18:2752–2758CrossRefGoogle Scholar
  29. Heilmann C, Brdiczka D, Nickel E, Pette D (1977) ATPase activities, Ca2+ transport and phosphoprotein formation in sarcoplasmic reticulum subfractions of fast and slow rabbit muscles. Eur J Biochem 81:211–222CrossRefGoogle Scholar
  30. Heizmann CW (1988) Parvalbumin in non-muscle cells. Calcium and calcium binding proteins. Springer, Berlin, pp 93–101CrossRefGoogle Scholar
  31. Hermann A, Cox JA (1995) Sarcoplasmic calcium-binding protein. Comp Biochem Physiol B Biochem Mol Biol 111:337–345CrossRefGoogle Scholar
  32. Hou TT, Johnson JD, Rall JA (1992) Effect of temperature on relaxation rate and Ca2+, Mg2+ dissociation rates from parvalbumin of frog muscle fibres. J Physiol 449:399–410CrossRefGoogle Scholar
  33. Huch R, D’Haese J (1992) Quantification of the soluble calcium-binding protein (SCBP) in various muscle tissues of the terrestrial oligochaete Lumbricus terrestris. Soil Biol Biochem 24:1231–1235CrossRefGoogle Scholar
  34. Huch R, D’Haese J, Gerday C (1988) A soluble calcium-binding protein from the terrestrial annelid Lumbricus terrestris. J Comp Physiol B 158:325–334CrossRefGoogle Scholar
  35. Jewell BR, Rüegg JC (1966) Oscillatory contraction of insect fibrillar muscle after glycerol extraction. Proc R Soc B 164:428–459CrossRefGoogle Scholar
  36. Johnson CK (2006) Calmodulin, conformational states, and calcium signaling. A single-molecule perspective. Biochemistry 45:14233–14246CrossRefGoogle Scholar
  37. Kelly LE, Phillips AM, Delbridge M, Stewart R (1997) Identification of a gene family from Drosophila melanogaster encoding proteins with homology to invertebrate sarcoplasmic calcium-binding proteins (SCPS). Insect Biochem Mol Biol 27:783–792CrossRefGoogle Scholar
  38. Kiehl E, D’Haese J (1992) A soluble calcium-binding protein (SCBP) present in Drosophila melanogaster and Calliphora erythrocephala muscle cells. Comp Biochem Physiol B 102:475–482CrossRefGoogle Scholar
  39. Kretsinger RH, Nockolds CE (1973) Carp muscle calcium-binding protein. II. Structure determination and general description. J Biol Chem 248:3313–3326PubMedGoogle Scholar
  40. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685CrossRefGoogle Scholar
  41. Martonosi A, Feretos R (1964) Sarcoplasmic reticulum. I. The uptake of Ca2+ by sarcoplasmic reticulum fragments. J Biol Chem 239:648–658PubMedGoogle Scholar
  42. Mazumder M, Padhan N, Bhattacharya A, Gourinath S (2014) Prediction and analysis of canonical EF-hand loop and qualitative estimation of Ca2+ binding affinity. PLoS One 9:e96202CrossRefGoogle Scholar
  43. Olinger E, Schwaller B, Loffing J, Gailly P, Devuyst O (2012) Parvalbumin: calcium and magnesium buffering in the distal nephron. Nephrol Dial Transplant 27:3988–3994CrossRefGoogle Scholar
  44. Pechere JF, Derancourt J, Haiech J (1977) The participation of parvalbumins in the activation-relaxation cycle of vertebrate fast skeletal-muscle. FEBS Lett 75:111–114CrossRefGoogle Scholar
  45. Raymackers JM, Gailly P, Schoor MC, Pette D, Schwaller B, Hunziker W, Celio MR, Gillis JM (2000) Tetanus relaxation of fast skeletal muscles of the mouse made parvalbumin deficient by gene inactivation. J Physiol 2:355–364CrossRefGoogle Scholar
  46. Romani A, Scarpa A (1992) Regulation of cell magnesium. Arch Biochem Biophys 298:1–12CrossRefGoogle Scholar
  47. Rüegg JC (2012) Calcium in muscle contraction: cellular and molecular physiology. Springer, BerlinGoogle Scholar
  48. Schwaller B (2010) Cytosolic Ca2+ buffers. Cold Spring Harb Perspect Biol 2:13CrossRefGoogle Scholar
  49. Semich R, Volmer H (1985) Calcium-uptake by sarcoplasmic reticulum prepared from the asynchronous flight muscles of Phormia terraenovae. Comp Biochem Physiol B 80:805–812CrossRefGoogle Scholar
  50. Sillen A, Verheyden S, Delfosse L, Braem T, Robben J, Volckaert G, Engelborghs Y (2003) Mechanism of fluorescence and conformational changes of the sarcoplasmic calcium binding protein of the sand worm Nereis diversicolor upon Ca2+ or Mg2+ binding. Biophys J 85:1882–1893CrossRefGoogle Scholar
  51. Stammers AN, Susser SE, Hamm NC, Hlynsky MW, Kimber DE, Kehler DS, Duhamel TA (2015) The regulation of sarco(endo)plasmic reticulum calcium-ATPases (SERCA). Can J Physiol Pharmacol 93:843–854CrossRefGoogle Scholar
  52. Stössel W, Zebe E (1968) Zur intrazellulären Regulation der Kontraktionsaktivität. Pflüger`s Arch 302:38–56CrossRefGoogle Scholar
  53. Sturm H, D’Haese J, Heide G (1993) Contraction modes of the gizzard muscle and body wall muscles in the earthworm Lumbricus. J Muscle Res Cell Motil 14:262Google Scholar
  54. Takagi T, Kobayashi A, Konishi K (1984) Amino-acid sequence of sarcoplasmic calcium-binding protein from scallop (Patinopecten yessoensis) adductor striated muscle. Biochim Biophys Acta 787:252–257CrossRefGoogle Scholar
  55. Takagi T, Kazuhiko K, Cox JA (1986) Amino acid sequence of two sarcoplasmic calcium-binding proteins from the protochordate Amphioxus. Biochemistry 25:3585–3592CrossRefGoogle Scholar
  56. Tashiro N, Yamamoto T (1971) The phasic and tonic contraction in the longitudinal muscle of the earthworm. J Exp Biol 55:111–122Google Scholar
  57. Thiruketheeswaran P, Kiehl E, D’Haese J (2016) Soluble calcium-binding proteins (SCBPs) of the earthworm Lumbricus terrestris: molecular characterization and localization by FISH in muscle and neuronal tissue. Histochem Cell Biol 146:635–644Google Scholar
  58. Ushio H, Watabe S (1994) Carp parvalbumin binds to and directly interacts with the sarcoplasmic reticulum for Ca2+ translocation. Biochem Biophys Res Commun 199:56–62CrossRefGoogle Scholar
  59. White AJ, Northcutt MJ, Rohrback SE, Carpenter RO, Niehaus-Sauter MM, Gao Y, Wheatly MG, Gillen CM (2011) Characterization of sarcoplasmic calcium binding protein (SCP) variants from freshwater crayfish Procambarus clarkii. Comp Biochem Physiol B Biochem Mol Biol 160:8–14CrossRefGoogle Scholar
  60. Wnuk W, Cox J, Stein EA (1982) Parvalbumin and other sarcoplasmic Ca2+-binding proteins. In: Cheung WY (ed) Calcium and cell function, vol II. Academic Press, New York, pp 243–278CrossRefGoogle Scholar
  61. Zot HG, Potter JD (1984) The role of calcium in the regulation of the skeletal muscle contraction-relaxation cycle. In: Sigel H (ed) Metal ions in biological systems, vol 17. Dekker, New York, pp 381–410Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Institute for Cell Biology, Department BiologyHeinrich-Heine-University DüsseldorfDüsseldorfGermany

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