Skip to main content

Advertisement

Log in

Differential Proteome Analysis of Hagfish Dental and Somatic Skeletal Muscles

  • Original Article
  • Published:
Marine Biotechnology Aims and scope Submit manuscript

Abstract

Hagfish, the plesiomorphic sister group of all vertebrates, are deep-sea scavengers. The large musculus (m.) longitudinalis linguae (dental muscle) is a specialized element of the feeding apparatus that facilitates the efficient ingestion of food. In this article, we compare the protein expression in hagfish dental and somatic (the m. parietalis) skeletal muscles via two-dimensional gel electrophoresis and mass spectrometry in order to characterize the former muscle. Of the 500 proteins screened, 24 were identified with significant differential expression between these muscles. The proteins that were overexpressed in the dental muscle compared to the somatic muscle were troponin C (TnC), glycogen phosphorylase, β-enolase, fructose-bisphosphate aldolase A (aldolase A), and glyceraldehyde-3-phosphate dehydrogenase (GAPDH). In contrast, myosin light chain 1 (MLC 1) and creatine kinase (CK) were over-expressed in the somatic muscle relative to the dental muscle. These results suggest that these two muscles have different energy sources and contractile properties and provide an initial representative map for comparative studies of muscle-protein expression in low craniates.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5

Similar content being viewed by others

References

  • Bessman SP, Geiger PJ (1981) Transport of energy in muscle: the phosphorylcreatine shuttle. Science 211, 448–452

    Article  PubMed  CAS  Google Scholar 

  • Biron DG, Agnew P, Marche L, Renault L, Sidobre C, Michalakis Y (2005) Proteome of Aedes aegypti larvae in response to infection by the intracellular parasite Vavraia culicis. Int J Parasitol 35, 1385–1397

    Article  PubMed  CAS  Google Scholar 

  • Bosworth CA, Chou CW, Cole RB, Rees BB (2005) Protein expression patterns in zebrafish skeletal muscle: initial characterization and the effects of hypoxic exposure. Proteomics 5, 1362–1371

    Article  PubMed  CAS  Google Scholar 

  • Bouley J, Chambon C, Picard B (2003) Proteome analysis applied to the study of muscle development and sensorial qualities of bovine meat. Sci Aliments 23, 75–78

    Article  CAS  Google Scholar 

  • Bouley J, Chambon C, Picard B (2004) Mapping of bovine skeletal muscle proteins using two-dimensional gel electrophoresis and mass spectrometry. Proteomics 4, 1811–1824

    Article  PubMed  CAS  Google Scholar 

  • Candiano G, Bruschi M, Musante L, Santucci L, Ghiggeri GM, Carnemolla B, Orecchia P, Zardi L, Righetti PG (2004) Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis 25, 1327–1333

    Article  PubMed  CAS  Google Scholar 

  • Capitanio D, Vigano A, Ricci E, Cerretelli P, Wait R, Gelfi C (2005) Comparison of protein expression in human deltoideus and vastus lateralis muscles using two-dimensional gel electrophoresis. Proteomics 5, 2577–2586

    Article  PubMed  CAS  Google Scholar 

  • Childress JJ (1995) Are there physiological and biochemical adaptations of metabolism in deep-sea animals? Trends Ecol Evol 10, 30–36

    Article  Google Scholar 

  • Childress JJ, Somero GN (1979) Depth-related enzymic activities in muscle, brain and heart of deep-living pelagic marine teleosts. Mar Biol 52, 273–283

    Google Scholar 

  • Dupont A, Corseaux D, Dekeyzer O, Drobecq H, Guihot AL, Susen S, Vincentelli A, Amouyel P, Jude B, Pinet F (2005) The proteome and secretome of human arterial smooth muscle cells. Proteomics 5, 585–596

    Article  PubMed  CAS  Google Scholar 

  • Flood PR (1979) The vascular supply of three fibre types in the parietal trunk muscle of the Atlantic hagfish (Myxine glutinosa, L). A light microscopic quantitative analysis and an evaluation of various methods to express capillary density relative to fibre types. Microvasc Res 17, 55–70

    Article  PubMed  CAS  Google Scholar 

  • Gage JD, Tyler PA (1991) Deep-Sea Biology: A Natural History of Organisms at the Deep-Sea Floor. (Cambridge, NY: Cambridge University Press)

    Google Scholar 

  • Gelfi C, De Palma S, Cerretelli P, Begum S, Wait R (2003) Two-dimensional protein map of human vastus lateralis muscle. Electrophoresis 24, 286–295

    Article  PubMed  CAS  Google Scholar 

  • Gelfi C, Vigano A, De Palma S, Ripamonti M, Begum S, Cerretelli P, Wait R (2006) 2-D protein maps of rat gastrocnemius and soleus muscles: A tool for muscle plasticity assessment. Proteomics 6, 321–340

    Article  PubMed  CAS  Google Scholar 

  • Hemmer W, Skarli M, Perriard JC, Wallimann T (1993) Effect of okadaic acid on protein phosphorylation patterns of chicken myogenic cells with special reference to creatine kinase. FEBS Lett 327, 35–40

    Article  PubMed  CAS  Google Scholar 

  • Herbert BR, Molloy MP, Gooley AA, Walsh BJ, Bryson WG, Williams KL (1998) Improved protein solubility in two-dimensional electrophoresis using tributyl phosphine as reducing agent. Electrophoresis 19, 845–851

    Article  PubMed  CAS  Google Scholar 

  • Hoh JFY (2002) “Superfast” or masticatory myosin and the evolution of jaw-closing muscles of vertebrates. J Exp Biol 205, 2203–2210

    PubMed  Google Scholar 

  • Horikoshi K (1998) Barophiles: deep-sea microorganisms adapted to an extreme environment. Curr Opin Microbiol 1, 291–295

    Article  PubMed  CAS  Google Scholar 

  • Korneliussen H, Nicolaysen K (1973) Ultrastructure of four types of striated muscle fibers in the Atlantic hagfish (Myxine glutinosa, L.). Z Zellforsch Mikrosk Anat 143, 273–290

    Article  PubMed  CAS  Google Scholar 

  • Li ZB, Lehar M, Samlan R, Flint PW (2005) Proteomic analysis of rat laryngeal muscle following denervation. Proteomics 5, 4764–4776

    Article  PubMed  CAS  Google Scholar 

  • Liem KF, Bemis WE Jr, Walker WF, Grande L (2001) Functional Anatomy of the Vertebrates: An Evolutionary Perspective. (Fort Worth, TX: Harcourt)

    Google Scholar 

  • López JL, Marina A, Vázquez J, Alvarez G (2002) A proteomic approach to the study of the marine mussels Mytilus edulis and M. galloprovincialis. Mar Biol 141, 217–223

    Article  Google Scholar 

  • McMillan CB, Wisner RL (2004) Review of the hagfishes (Myxinidae, Myxiniformes) of the northwestern Pacific Ocean, with descriptions of three new species, Eptatretus fernholmi, Paramyxine moki, and P. walkeri. Zool Stud 43, 51–73

    Google Scholar 

  • Merkulova T, Lucas M, Jabet C, Lamande N, Rouzeau JD, Gros F, Lazar M, Keller A (1997) Biochemical characterization of the mouse muscle-specific enolase: developmental changes in electrophoretic variants and selective binding to other proteins. Biochem J 323, 791–800

    PubMed  CAS  Google Scholar 

  • Nelson DL, Cox MM (2004) Lehninger Principles of Biochemistry, 4th ed (New York: WH Freeman)

    Google Scholar 

  • Okumura N, Hashida-Okumura A, Kita K, Matsubae M, Matsubara T, Takao T, Nagai K (2005) Proteomic analysis of slow- and fast-twitch skeletal muscles. Proteomics 5, 2896–2906

    Article  PubMed  CAS  Google Scholar 

  • Peter JB, Barnard RJ, Edgerton VR, Gillespie CA, Stempel KE (1972) Metabolic profiles of three fiber types of skeletal muscle in guinea pigs and rabbits. Biochemistry 11, 2627–2633

    Article  PubMed  CAS  Google Scholar 

  • Pineiro C, Barros-Velazquez J, Vazquez J, Figueras A, Gallardo JM (2003) Proteomics as a tool for the investigation of seafood and other marine products. J Proteome Res 2, 127–135

    Article  PubMed  CAS  Google Scholar 

  • Ross MH, Romrell LJ, Kaye GI (1995) Histology: A Text and Atlas, 3rd ed (Baltimore: Williams & Wilkins)

    Google Scholar 

  • Rowlerson A, Mascarello F, Veggetti A, Carpene E (1983) The fiber-type composition of the first branchial arch muscles in Carnivora and Primates. J Muscle Res Cell Motil 4, 443–472

    Article  PubMed  CAS  Google Scholar 

  • Sanchez JC, Chiappe D, Converset V, Hoogland C, Binz PA, Paesano S, Appel RD, Wang S, Sennitt M, Nolan A, Cawthorne MA, Hochstrasser DF (2001) The mouse SWISS-2D PAGE database: a tool for proteomics study of diabetes and obesity. Proteomics 1, 136–163

    Article  PubMed  CAS  Google Scholar 

  • Sebert P (2002) Fish at high pressure: a hundred year history. Comp Biochem Physiol 131A, 575–585

    CAS  Google Scholar 

  • Sebert P, Peragon J, Barroso JB, Simon B, Melendez-Hevia E (1998) High hydrostatic pressure (101 ATA) changes the metabolic design of yellow freshwater eel muscle. Comp Biochem Physiol 121B, 195–200

    CAS  Google Scholar 

  • Simon B, Sebert P, Cannmoisan C, Barthelemy L (1992) Muscle energetics in yellow fresh-water eels (Anguilla-Anguilla, L) exposed to high hydrostatic pressure (101-ATA) for 30 days. Comp Biochem Physiol 102B, 205–208

    CAS  Google Scholar 

  • Somero GN (1992) Adaptations to high hydrostatic pressure. Annu Rev Physiol 54, 557–577

    Article  PubMed  CAS  Google Scholar 

  • Somero GN (2003) Protein adaptations to temperature and pressure: complementary roles of adaptive changes in amino acid sequence and internal milieu. Comp Biochem Physiol 136B, 577–591

    CAS  Google Scholar 

  • Staron RS, Pette D (1986) Correlation between myofibrillar ATPase activity and myosin heavy chain composition in rabbit muscle fibers. Histochem Cell Biol 86, 19–23

    Article  CAS  Google Scholar 

  • Stevens L, Bastide B, Bozzo C, Mounier Y (2004) Hybrid fibres under slow-to-fast transformations: expression is of myosin heavy and light chains in rat soleus muscle. Pflugers Arch 448, 507–514

    Article  PubMed  CAS  Google Scholar 

  • Sullivan KM, Somero GN (1980) Enzyme activities of fish skeletal muscle and brain as influenced by depth of occurrence and habits of feeding and locomotion. Mar Biol 60, 91–99

    Article  CAS  Google Scholar 

  • Sun HW, Hui CF, Wu JL (1998) Cloning, characterization, and expression in Escherichia coli of three creatine kinase muscle isoenzyme cDNAs from carp (Cyprinus carpio) striated muscle. J Biol Chem 273, 33774–33780

    Article  PubMed  CAS  Google Scholar 

  • Theron M, Guerrero F, Sebert P (2000) Improvement in the efficiency of oxidative phosphorylation in the freshwater eel acclimated to 10.1 MPa hydrostatic pressure. J Exp Biol 203, 3019–3023

    PubMed  CAS  Google Scholar 

  • Treberg JR, Martin RA, Driedzic WR (2003) Muscle enzyme activities in a deep-sea squaloid shark, Centroscyllium fabricii, compared with its shallow-living relative, Squalus acanthias. J Exp Zool 300A, 133–139

    Article  CAS  Google Scholar 

  • Westermeier R, Naven T (2002) Proteomics in Practice: A Laboratory Manual of Proteome Analysis. (Weinheim, Germany: Wiley-VCH Verlag-GmbH)

    Google Scholar 

  • Wilkins MR, Williams KL (1997) Cross-species protein identification using amino acid composition, peptide mass fingerprinting, isoelectric point and molecular mass: a theoretical evaluation. J Theor Biol 186, 7–15

    Article  PubMed  CAS  Google Scholar 

  • Winnard P, Cashon RE, Sidell BD, Vayda ME (2003) Isolation, characterization and nucleotide sequence of the muscle isoforms of creatine kinase from the Antarctic teleost Chaenocephalus aceratus. Comp Biochem Physiol 134B, 651–667

    CAS  Google Scholar 

Download references

Acknowledgments

We thank Dr. Jen-taie Shiea from Department of Chemistry, National Sun Yat-sen University, for making equipment available to us. This study was partially supported by a grant of the National Science Council of the Republic of China to Hin-Kiu Mok (NSC94-2311-B-110-002). We also thank Dr. Philippe Sebert for reviewing the first draft of the manuscript and two anonymous reviewers for providing helpful comments on a draft of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hin-Kiu Mok.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chiu, KH., Huang, HW. & Mok, HK. Differential Proteome Analysis of Hagfish Dental and Somatic Skeletal Muscles. Mar Biotechnol 9, 689–700 (2007). https://doi.org/10.1007/s10126-007-9020-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-007-9020-6

Keywords

Navigation