Skip to main content
SpringerLink
Log in

Inter- and intra-specific variation in myosin light chain and troponin I composition in fast muscle fibres from two species of fish (genusOreochromis) which have different temperature-dependent contractile properties

  • Papers
  • Published:
Journal of Muscle Research & Cell Motility Aims and scope Submit manuscript

Summary

The contractile properties and myofibrillar protein composition of fast muscle have been characterized in pure strains of two tropical fishOreochromis niloticus andO. andersoni. Single fast muscle fibres were isolated from the abdominal myotomes and chemically skinned. The maximum tension-temperature relationships of fibres were similar at 25–30° C, but diverged below 17° C. At 10° C, maximum tension was around 60% higher inO. andersoni (160 ± 15 kN m−2) thanO. niloticus (105 ±13 kN m−2) (mean ±sd). The myofibrillar protein composition of fast fibres was investigated using one-dimensional and two-dimensional gel electrophoresis and peptide mapping. The twoOreochromis species differed with respect to the composition of myosin light chains, troponin I and mysoin heavy chains (V8 protease and chymotrypsin peptide maps). An unexpected finding was the presence of two isoforms of myosin light chain 1 inO. andersoni, with apparent molecular masses of 27.5 kDa (LC1f1) and 26.9 kDa (LC1f2). Individuals with LC1f1 (n=20) and LC1f1+LC1f2 (n=12) were represented in the population studied. The myosin light chain 3 (LC3f) content of fibres was similar in both cases. Breeding experiments established that these intra-specific variations in isoform composition were heritable. Fast muscle fromO. niloticus andO. andersoni contain two isoforms of troponin I (TNIf1+TNIf2) which were both expressed in single fibres. The identity of TNI was confirmed using a stationary phase troponin-C affinity column. Of the 20O. niloticus studied seven contained only TNIf1. The twoOreochromis species studied produce fertile F1 hybrids, are susceptible to ploidy manipulation, have a short generation time and rapid growth rates. They therefore represent a good model for investigating the genetic mechanisms underlying the inheritance of different force-generating capacities in fish.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Altringham, J. D. &Johnston, I. A. (1982) The pCa-tension and force-velocity characteristics of skinned fibres isolated from fish fast and slow muscles.J. Physiol. (Lond.) 333, 421–49.

    Google Scholar 

  • Allington, W. B., Cordry, A. L., McCullough, G. A., Mitchell, D. E. &Nelson, J. W. (1978) Electrophoretic concentration of macromolecules.Anal. Biochem. 85, 188–96.

    PubMed  Google Scholar 

  • Amphlett, G. W., Perry, S. V., Syska, H., Brown, M. D. &Vrbova, G. (1975) Cross innervation and the regulatory protein system of rabbit soleus muscle.Nature 257, 602–4.

    PubMed  Google Scholar 

  • Breitbart, R. E., Nguyen, H. T., Medford, R. M., Destree, A. T., Mahdavi, V. &Nadal-Ginard, B. (1985) Intricate combinatorial patterns of exon splicing generate multiple regulated troponin T isoforms from a single gene.Cell 41, 67–82.

    PubMed  Google Scholar 

  • Bucher, A. E., Maisonpierre, P. C., Konieczny, S. F. &Emerson, C. P. (1988) Expression of the troponin complex genes: transcriptional coactivation during myoblast differentiation and independent control in heart and skeletal muscles.Mol. Cell. Biol. 8, 4134–42.

    PubMed  Google Scholar 

  • Campbell, K. P., MacLennan, D. H. &Jorgensen, A. O. (1983) Staining of the Ca2+-binding proteins, calsequestrin, calmodulin, troponin C, and S-100, with the cationic carbocyanine dye ‘Stains-all’.J. Biol. Chem. 258, 11267–73.

    PubMed  Google Scholar 

  • Crockford, T. &Johnston, I. A. (1990) Temperature acclimation and the expression of contractile protein isoforms in the skeletal muscles of the common carp (Cyprinus carpio L).J. Comp. Physiol. (B)160, 23–30.

    Google Scholar 

  • Dhoot, G. K. &Perry, S. V. (1980) The components of the troponin complex and development in skeletal muscle.Exp. Cell Res. 127, 75–87.

    PubMed  Google Scholar 

  • Dhoot, G. K. &Perry, S. V. (1982) The effect of denervation on the polymorphic forms of troponin components in fast and slow muscles of the adult rat.Cell Tissues Res. 225, 201–15.

    Google Scholar 

  • Dhoot, G. K., Gell, P. G. H. &Perry, S. V. (1978) The localisation of the different forms of troponin I in skeletal and cardiac muscle cells.Exp. Cell Res. 117, 357–70.

    PubMed  Google Scholar 

  • Dhoot, G. K., Frearson, N. &Perry, S. V. (1979) Polymorphic forms of troponin T and troponin C and their localisation in striated muscle cell types.Exp. Cell Res. 122, 339–50.

    PubMed  Google Scholar 

  • Dhoot, G. K., Perry, S. V. &Vrbova, G. (1981) Changes in the distribution of the components of the troponin complex in muscle fibres after cross-innervation.Exp. Neurol. 72, 513–30.

    PubMed  Google Scholar 

  • Focant, B., Huriaux, F. &Johnston, I. A. (1976) Subunit composition of fish myofibrils: the light chains of myosin.Int. J. Biochem. 7, 129–33.

    Google Scholar 

  • Frank, G. &Weeds, A. G. (1974) The amino acid sequence of the alkali light chains of rabbit skeletal-muscle myosin.Eur. J. Biochem. 44, 317–34.

    PubMed  Google Scholar 

  • Gerlach, G., Turay, L., Mailik, K., Lida, J., Scutt, A. &Goldspink, G. (1990) Mechanisms of temperature acclimation in carp: a molecular biology approach.Am. J. Physiol. 259 (Regulatory Integrative Comp. Physiol.28), R237-R244.

    PubMed  Google Scholar 

  • Greaser, M. L., Moss, R. S. &Reiser, P. J. (1988) Variations in contractile properties of rabbit single fibres in relation to troponin T isoforms and myosin light chains.J. Physiol. 406, 85–98.

    PubMed  Google Scholar 

  • Hallauer, P. L., Hastings, K. E. M. &Peterson, A. C. (1988) Fast skeletal muscle-specific expression of a quail troponin I gene in transgenic mice.Mol. Cell. Biol. 8, 5072–9.

    PubMed  Google Scholar 

  • Hussain, M. G., Chatterji, A., Mcandrew, B. J. &Johnstone, R. (1990) Triploidy induction in Nile tilapiaOreochromis niloticus L. using pressure, heat and cold shock.Theor. Appl. Genet. 80 (in press).

  • Imai, H., Hirai, S., Hirono, H. &Hirabayashi, T. (1986) Many isoforms of fast muscle troponin T from chicken legs.J. Biochem. 99, 923–30.

    PubMed  Google Scholar 

  • Johnston, I. A. &Brill, R. (1984) Thermal dependance of contractile properties of single skinned muscle fibres from Antarctic and various warm water marine fishes including skipjack tuna (Katsuwonus pelamis) and kawakawa (Euthynnus affinis).J. Comp. Physiol. 155B, 63–70.

    Google Scholar 

  • Johnston, I. A. &Altringham, J. D. (1985) Evolutionary adaptation of muscle power output to environmental temperature: force-velocity characteristics of skinned fibres isolated from antarctic, temperate and tropical marine fish.Pflügers Arch. ges. Physiol 405, 136–40.

    Google Scholar 

  • Johnston, I. A. &Altringham, J. D. (1988) Muscle contraction in polar fishes: experiments with demembranated muscle fibres.Comp. Biochem. Physiol. 90B, 547–55.

    Google Scholar 

  • Johnston, I. A. &Altringham, J. D. (1989) Muscular energetics and environment in ectotherms. InEnergy Transformations in Cells and Organism (edited byWieser, W. &Gnaiger, E.), pp. 71–80. Stuttgart, New York: Georg Thieme.

    Google Scholar 

  • Johnston, T. P. &Johnston, I. A. (1991) Temperature adaptation and the contractile properties of live muscle fibres from teleost fish.J. Comp. Physiol. (B) 161, 27–36.

    Google Scholar 

  • Johnston, I. A., Davison, W. &Goldspink, G. (1977) Energy metabolism of carp swimming muscles.J. Comp. Physiol. 114, 203–16.

    Google Scholar 

  • Johnston, I. A., Fleming, J. D. &Crockford, T. (1990) Thermal acclimation and muscle contractile properties in cyprinid fish.Am. J. Physiol. 259, R231-R236.

    PubMed  Google Scholar 

  • Johnston, I. A., Sidell, B. D. &Driedzic, W. (1985) Force-velocity characteristics and metabolism of carp muscle fibres following temperature Acclimation,J. Exp. Bio. 119, 239–49.

    Google Scholar 

  • Karasinksi, J. &Kilarski, W. (1989) Polymorphism of myosin isoenzymes and myosin heavy chains in histochemically typed skeletal muscles of the roach (Rutilus rutilus L., cyprinidae, fish).Comp. Biochem. Physiol. 92B, 727–31.

    Google Scholar 

  • Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4.Nature 227, 680–5.

    PubMed  Google Scholar 

  • Lannergren, J. (1987) Contractile properties and myosin isoenzymes of various kinds ofXenopus twitch muscle fibres.J. Muscle Res. Cell Motil. 8, 260–73.

    PubMed  Google Scholar 

  • McAndrew, B. J. (1981) Muscle biopsy technique for fish stock management.Vet. Rec. 108, 516.

    PubMed  Google Scholar 

  • McAndrew, B. J. &Majumdar, K. C. (1983) Tilapia stock identification using electrophoretic markers.Aquaculture 30, 249–61.

    Google Scholar 

  • Maniatis, T. &Reed, R. (1987) the role of small nuclear riboneucleoprotein particles in pre-mRNA splicing.Nature 325, 673–8.

    PubMed  Google Scholar 

  • Mutungi, G. &Johnston, I. A. (1988) Influence of pH on force development and shortening velocity in skinned muscle fibres from fish.Fish Physiol. Biochem. 5, 257–62.

    Google Scholar 

  • Nabeshima, Y., Fujii-Kuriyama, Y., Muramatsu, M. &Ogata, K. (1984) Alternate transcription and two modes of splicing result in two myosin light chains from a single gene.Nature 308, 333–8.

    PubMed  Google Scholar 

  • Nakamura, M., Imai, H. &Hirabayashi, T. (1989) Coordinate accumulation of troponin subunits in chicken breast muscle.Dev. Biol. 132, 389–97.

    PubMed  Google Scholar 

  • Nicol, J. C. M. (1985) A microcomputer program to determine the composition of solutions containing multiple metal ions and complexing ligands.J. Physiol. 367, 10P.

    Google Scholar 

  • Periasamy, M., Strehler, E. E., Garfinkel, L. I., Gubits, R. M., Ruis-Opaso, N. &Nadal-Ginard, B. (1984) Fast skeletal muscle myosin light chains 1 and 3 are produced from a single gene by a combined process of differential RNA transcription and splicing.J. Biol. Chem. 259, 13595–604.

    PubMed  Google Scholar 

  • Reiser, P. J., Moss, R. L., Giulan, G. G. &Greaser, M. L. (1985) Shortening velocity in single fibres from adult rabbit soleus muscles is correlated with myosin heavy chain composition.J. Biol. Chem. 260, 9077–80.

    PubMed  Google Scholar 

  • Robert, B., Barton, P., Minty, A., Daubas, P., Weydert, A., Bonhomme, F., Catalan, J., Chazottes, D., Guenet, J.-L. &Buckingham, M. (1985) Investigation of genetic linkage between mysoin and actin genes using an inter-specific mouse back-cross.Nature 314, 181–3.

    PubMed  Google Scholar 

  • Syska, H., Perry, S. V. &Trayer, I. P. (1974) A new method of preparation of troponin I (inhibitory protein) using affinity chromatography. Evidence for three different forms of troponin I in striated muscle.FEBs Lett. 40, 253–7.

    PubMed  Google Scholar 

  • Toyota, N. &Shimada, Y. (1981) Differentiation of troponin in cardiac and skeletal muscles in chicken embryos as studied by immunofluorescence microscopy.J. Cell Biol. 91, 497–504.

    PubMed  Google Scholar 

  • Trewavas, E. (1983) Tilapiine fishes of the generaSarotherodon, Oreochromis andDanakilia. Brit. Museum (Natl Hist.) pp. 583.

  • Wilkinson, J. M. (1978) The components of troponin from chicken fast skeletal muscle.Biochem. J. 169, 229–38.

    PubMed  Google Scholar 

  • Wilkinson, J. M. &Grand, R. J. A. (1978) Comparison of amino acid sequence of troponin I from different striated muscles.Nature 271, 31–5.

    PubMed  Google Scholar 

Download references

Author information

Author notes

  1. K. E. Wommack

    Present address: Department of Biology, University of Maryland, Maryland, USA

  2. G. Mutungi

    Present address: Department of Animal Physiology, University of Nairobi, Kenya

Authors and Affiliations

  1. Gatty Marine Laboratory, Department of Biology and Preclinical Medicine, The University, St Andrews, KY16 8LB, Fife, UK

    T. Crockford, K. E. Wommack, I. A. Johnston, G. Mutungi & T. P. Johnson

  2. Institute of Aquaculture, University of Stirling, FK9 4LA, Stirling, UK

    B. J. McAndrew

Authors
  1. T. Crockford
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. K. E. Wommack
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. I. A. Johnston
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. B. J. McAndrew
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. G. Mutungi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. T. P. Johnson
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Crockford, T., Wommack, K.E., Johnston, I.A. et al. Inter- and intra-specific variation in myosin light chain and troponin I composition in fast muscle fibres from two species of fish (genusOreochromis) which have different temperature-dependent contractile properties. J Muscle Res Cell Motil 12, 439–446 (1991). https://doi.org/10.1007/BF01738328

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01738328

Keywords

Search

Navigation