Advertisement

Journal of Molecular Evolution

, Volume 59, Issue 2, pp 218–226 | Cite as

Evolution and Divergence of the Genes for Cytoplasmic, Mitochondrial, and Flagellar Creatine Kinases

  • Tomohiko Suzuki
  • Chisa Mizuta
  • Kouji Uda
  • Keiko Ishida
  • Kanae Mizuta
  • Sona Sona
  • Deanne M. Compaan
  • W. Ross Ellington
Articles

Abstract

Creatine kinase (CK) plays a central role in energy homeostasis in cells that display high and variable rates of energy turnover. A number of CK genes exist, each being targeted to particular intracellular compartments. In the vertebrates, two genes code for proteins which form homo- and heterodimers targeted to the cytoplasm, while two additional genes code for primarily octameric proteins targeted to the mitochondrial intermembrane space. Yet another gene is present in certain groups which codes for three fused, complete CK domains and is typically targeted to the flagellar membrane of primitive-type spermatozoa. CK is widely distributed in protochordates and both protostome and deuterostome invertebrate groups. The evolutionary relationships of these CK genes have not been fully elucidated. The present communication reports new cDNA-derived deduced amino acid sequences for four cytoplasmic and three mitochondrial CKs and one flagellar CK from lophotrochozoan, protostome invertebrates as well as a new cytoplasmic CK sequence from a protochordate tunicate. These new sequences, coupled with available sequences in the databases and sequences extracted from genome sequencing projects, provide revealing insights into the evolution and divergence of CK genes. Phylogenetic analyses showed that single cytoplasmic, mitochondrial, and flagellar CK genes were present prior to the divergence of the protostomes and deuterostomes. The flagellar CK gene may have evolved within the cytoplasmic gene clade, although the evidence is somewhat equivocal. The two cytoplasmic genes in the vertebrates, and most likely the two mitochondrial genes, evolved after the divergence of the craniates from the protochordates. Comparison of the structure of the genes for selected cytoplasmic, mitochondrial, and flagellar CKs revealed two identical intron boundaries, further reinforcing the notion of a common evolutionary origin, but also showed patterns of changes in structure consistent with each gene type. These studies show that the cytoplasmic, mitochondrial, and flagellar CK genes are rather ancient and that there has been a systematic pattern of duplication and divergence consistent with changing nature of energy demands and physicochemical environment in the cells where they are expressed.

Keywords

Creatine kinase Isoforms 

Notes

Acknowledgments

T. Suzuki thanks Drs. K. Kawamura and S. Fujiwara of Kochi University for providing us the cDNA library of Polyandrocarpa misakiensis. We also thank Dr. Hajime Julie Yuasa and Sachiko Tsukamoto for assistance with sequence determination of Marphysa CK and Siphonosoma MiCK. W. R. Ellington thanks the staff of the Florida State University Cloning and DNA Sequencing Facilities for technical support in this effort. This work was supported by a grant from the President of Kochi University (to T.S.) and U.S. National Science Foundation Grant IBN-0130024 (to W.R.E.). We gratefully acknowledge the comments of two anonymous referees who provided very constructive input in the formulation of the manuscript.

References

  1. Borson, ND, Salo, WL, Drewes, LR 1992A lock-docking oligo (DT) primer for 5’ and 3’ RACE PCRPCR Methods Appl2144148PubMedGoogle Scholar
  2. Chomczynski, P, Sacchi, N 1987Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extractionAnal Biochem162156159CrossRefPubMedGoogle Scholar
  3. Dehal, P, Satou, Y, Campbell, RK,  et al. 2002The draft genome of Ciona intestinalis: Insights into chordate and vertebrate originsScience29821572167CrossRefPubMedGoogle Scholar
  4. Ellington, WR 2001Evolution and physiological roles of phosphagen systemsAnnu Rev Physiol63289325PubMedGoogle Scholar
  5. Feng, D-F, Doolittle, RF 1987Progressive sequence alignments as a prerequisite to correct phylogenetic treesJ Mol Evol25351360PubMedGoogle Scholar
  6. Frohman, MA, Dush, MK, Martin, GR 1988Rapid production of full length cDNAs from rare transcripts: Amplification using a single gene-specific primerProc Natl Acad Sci USA8589989002PubMedGoogle Scholar
  7. Graber, NA, Ellington, WR 2001Gene duplication events producing muscle (M) and brain (B) isoforms of cytoplasmic creatine kinase: cDNA and deduced amino acid sequences from two lower chordatesMol Biol Evol1813051314PubMedGoogle Scholar
  8. Klein, SC, Haas, RC, Perryman, MB, Billadello, JJ, Strauss, AW 1991Regulatory element analysis and structural characterization of the human sarcomeric mitochondrial creatine kinase geneJ Biol Chem2661805818065PubMedGoogle Scholar
  9. Mariman, E, Wieringa, B 1991Expression of the gene encoding human brain creatine kinase depends on sequences immediately following the transcription start pointGene102205212PubMedGoogle Scholar
  10. Mühlebach, SM, Gross, M, Wirz, T, Wallimann, T, Perriard, J-C, Wyss, M 1994Sequence homology and structure predictions of the creatine kinase isoenzymesMol Cell Biochem133/134245262Google Scholar
  11. Pineda, AO, Ellington, WR 1999Structural and functional implications of the amino acid sequences of dimeric, cytoplasmic and octameric, mitochondrial creatine kinases from a protostome invertebrateEur J Biochem2646773PubMedGoogle Scholar
  12. Pineda, AO,Jr, Ellington, WR 2001Organization of the gene for an invertebrate mitochondrial creatine kinase: Comparisons with genes of higher forms and correlation of exon boundaries with functional domainsGene265115121PubMedGoogle Scholar
  13. Qin, W, Khuchua, Z, Cheng, J, Boero, J, Payne, RM, Strauss, AW 1998Molecular characterization of the creatine kinases and some histrorical perspectivesMol Cell Biochem184153167PubMedGoogle Scholar
  14. Quest, AFG, Harvey, DJ, McIlhinney, RAJ 1997Myristoylated and non myristoylated pools of sea urchin sperm flagellar creatine kinase exist side-by-side: Myristoylation is necessary for efficient lipid associationBiochemistry3669937002PubMedGoogle Scholar
  15. Quest, AFG, Chadwick, JK, Wothe, DD, McIlhinney, RAJ, Shapiro, BM 1992Myristoylation of flagellar creatine kinase in the sperm phosphocreatine shuttle is linked to its membrane association propertiesJ Biol Chem2671508015085PubMedGoogle Scholar
  16. Ratto, A, Shapiro, BM, Christen, R 1989Phosphagen kinase evolution: expression in echinodermsEur J Biochem186195203PubMedGoogle Scholar
  17. Suzuki, T, Furukohri, T 1994Evolution of phosphagen kinase. Primary structure of glycocyamine kinase and arginine kinase from invertebratesJ Mol Biol237353357PubMedGoogle Scholar
  18. Suzuki, T, Kawasaki, Y, Furukohri, T, Ellington, WR 1997Evolution of phosphagen kinase VI. Isolation, characterization and cDNA-derived amino acid sequence of lombricine kinase from the earthworm Eisenia foetida, and identification of a possible candidate for the guanidine substrate recognition siteBiochim Biophys Acta1343152159PubMedGoogle Scholar
  19. Suzuki, T, Kamidochi, M, Inoue, N, Kawamichi, H, Yazawa, Y, Furukohri, T, Ellington, WR 1999Arginine kinase evolved twice: Evidence that echinoderm arginine kinase originated from creatine kinaseBiochem J340371375PubMedGoogle Scholar
  20. Suzuki, T, Yamamoto, Y, Umekawa, M 2000Stichopus japonicus arginine kinase: Gene structure and unique substrate recognition systemBiochem J351579585PubMedGoogle Scholar
  21. Tombes, RM, Shapiro, BM 1987Enzyme termini of the phosphocreatine shuttleJ Biol Chem2621601116019PubMedGoogle Scholar
  22. Tombes, RM, Shapiro, BM 1989Energy transport and cell polarity: Relationship of phosphagen kinase activity to sperm functionJ Exp Zool2518290PubMedGoogle Scholar
  23. Trask, RV, Strauss, AW, Billadello, JJ 1988Developmental regulation and tissue-specific expression of the human muscle creatine kinase geneJ Biol Chem2631714217149PubMedGoogle Scholar
  24. Uda, K, Suzuki, T, Ellington, WR 2003Some elements of the major myofibrillar binding peptide motif are present in the earliest of true muscle type creatine kinasesInt J Biochem Cell Biol36785794Google Scholar
  25. Wallimann, T, Wyss, M, Brdiczka, D, Nicolay, K, Eppenberger, HM 1992Intracellular compartmentation, structure and function of creatine kinase isoenzymes: The “phosphocreatine circuit” for cellular energy homeostasisBiochem J2812140PubMedGoogle Scholar
  26. Wothe, DD, Charbonneau, H, Shapiro, BM 1990The phosphocreatine shuttle of sea urchin sperm: Flagellar creatine kinase resulted from a gene triplicationProc Natl Acad Sci USA8752035207PubMedGoogle Scholar
  27. Wyss, M, Smeitink, J, Wevers, RA, Wallimann, T 1992Mitochondrial creatine kinase: A key enzyme of aerobic energy metabolismBiochim Biophys Acta1102119166PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Tomohiko Suzuki
    • 1
  • Chisa Mizuta
    • 1
  • Kouji Uda
    • 1
  • Keiko Ishida
    • 1
  • Kanae Mizuta
    • 1
  • Sona Sona
    • 2
  • Deanne M. Compaan
    • 2
    • 3
  • W. Ross Ellington
    • 2
  1. 1.Laboratory of Biochemistry, Faculty of ScienceKochi UniversityKochiJapan
  2. 2.Department of Biological Science and Institute of Molecular BiophysicsFlorida State UniversityTallahasseeUSA
  3. 3.GenentechSouth San FranciscoUSA

Personalised recommendations