Journal of Molecular Evolution

, Volume 34, Issue 5, pp 416–448 | Cite as

Evolution of EF-hand calcium-modulated proteins. II. Domains of several subfamilies have diverse evolutionary histories

  • Susumu Nakayama
  • Nancy D. Moncrief
  • Robert H. Kretsinger
Article

Summary

In the first report in this series we described the relationships and evolution of 152 individual proteins of the EF-hand subfamilies. Here we add 66 additional proteins and define eight (CDC, TPNV, CLNB, LPS, DGK, 1 F8, VIS, TCBP) new subfamilies and seven (CAL, SQUD, CDPK, EFH5, TPP, LAV, CRGP) new unique proteins, which we assume represent new subfamilies.

The main focus of this study is the classification of individual EF-hand domains. Five subfamilies—calmodulin, troponin C, essential light chain, regulatory light chain, CDC31/caltractin-and three uniques—call, squidulin, and calcium-dependent protein kinase-are congruent in that all evolved from a common four-domain precursor. In contrast calpain and sarcoplasmic calcium-binding protein (SARC) each evolved from its own one-domain precursor. The remaining 19 subfamilies and uniques appear to have evolved by translocation and splicing of genes encoding the EF-hand domains that were precursors to the congruent eight and to calpain and to SARC.

The rates of evolution of the EF-hand domains are slower following formation of the subfamilies and establishment of their functions. Subfamilies are not readily classified by patterns of calcium coordination, interdomain linker stability, and glycine and proline distribution. There are many homoplasies indicating that similar variants of the EF-hand evolved by independent pathways.

Key words

EF-hand Calcium binding protein Gene duplication Congruence Domain transposition Calmodulin Troponin C Light chains of myosin Parvalbumin S100 Calpain 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Arimura C, Suzuki T, Yanagisawa M, Imamura M, Hamada Y, Masaki T (1988) Primary structure of chicken skeletal muscle and fibroblast α-actinins deduced from cDNA sequences. Eur J Biochem 177:649–655Google Scholar
  2. Arnold H-H, Lohse P, Seidel U, Bober E (1988) A novel human myosin alkali light chain is developmentally regulated. Expression in fatal cardiac and skeletal muscle and in adult atria. Eur J Biochem 178:53–60Google Scholar
  3. Baba ML, Goodman M, Berger-Cohn J, Demaille JG, Matsuda G (1984) The early adaptive evolution of calmodulin. Mol Biol Evol 1:442–455Google Scholar
  4. Babu YS, Sack JS, Greenbough TC, Bugg CE, Means AR, Cook WJ (1985) Three-dimensional structure of calmodulin. Nature 315:37–40Google Scholar
  5. Babu YS, Bugg CE, Cook WJ (1988) Structure of calmodulin refined at 2.2 Å resolution. J Mol Biol 204:191–204Google Scholar
  6. Barnett MJ, Long SR (1990) Nucleotide sequence of an alfalfa calmodulin cDNA. Nucleic Acids Res 18:3395–3395Google Scholar
  7. Berchtold MW (1988) Structural organization of the human parvalbumin gene. In: Hidaka H (ed) Ca2+ protein signaling. Plenum, New York, pp 251–256Google Scholar
  8. Berchtold MW (1989) Parvalbumin genes from human and rat are identical in intron/exon organization and contain highly homologous regulatory elements and coding sequences. J Mol Biol 210:417–427Google Scholar
  9. Boyhan A, Casimir CM, French JK, Teahan CG, Segal AW (1992) Molecular cloning and characterization of grancalcin, a novel EF-hand calcium-binding protein abundant in neutrophils and monocytes. SubmittedGoogle Scholar
  10. Braam J, Davis RW (1990) Rain-, wind-, and touch-induced expression of calmodulin and calmodulin-related genes in Arabidopsis. Cell 60:357–364Google Scholar
  11. Brewer JM, Wunderlich JK, Kim D-H, Carr MY, Beach GG, Ragland WL (1989) Avian thymic hormone (ATH) is a parvalbumin. Biochem Biophys Res Commun 160:1155–1161Google Scholar
  12. Brewer JM, Wunderlich JK, Ragland WL (1990) The amino acid sequence of avian thymic hormone, a parvalbumin. Biochimie 72:653–660Google Scholar
  13. Collins JH, Theibert JL, Francois J-M, Ashley CC, Potter JD (1991) Amino acid sequences and Ca+-binding properties of two isoforms of barnacle troponin C. Biochemistry 30:702–707Google Scholar
  14. Deka N, Wong E, Matera AG, Kraft R, Leinwand LA, Schmid CW (1988) Repetitive nucleotide sequence insertions into a novel calmodulin-related gene and its processed pseudogene. Gene 71:123–134Google Scholar
  15. Dizhoor AM, Ray S, Kumar S, Niemi G, Spencer M, Brolley D, Walsh KA, Philipov PP, Hurley JB, Stryer L (1991) Recoverin: a calcium sensitive activator of retinal rod guanylate cyclase. Science 251:915–918Google Scholar
  16. Engman DM, Krause K-H, Blumin JH, Kim KS, Kirchhoff LV, Donelson JE (1989) A novel flagellar Ca2+-binding protein in Trypanosomes. J Biol Chem 264:18627–18631Google Scholar
  17. Fairbridge RW, Jablonski D (1979) In: The encyclopedia of paleontology. In: Fairbridge RW, Jablonski D (eds) Encyclopedia of earth sciences, vol VII. Dowden, Hutchinson and Ross, Stroudsburg PA, 886 ppGoogle Scholar
  18. Fasman GD (1989) Protein conformational prediction. Trends Biochem Sci 14:295–299Google Scholar
  19. Filipek A, Gerke V, Weber K, Kuźnicki J (1991) Characterization of the cell-cycle-regulated protein calcyclin from Ehrlich ascites tumor cells. Identification of two binding proteins obtained by Ca2+-dependent affinity chromatography. Eur J Biochem 195:795–800Google Scholar
  20. Francois J-M et al. (1991) The amino acid sequence of troponin C from eel skeletal muscle. A single tryptophan containing protein. FEBS Lett (in press)Google Scholar
  21. Glenney JR, Kindy MS, Zokas L (1989) Isolation of a new member of the S100 protein family: amino acid sequence, tissue, and subcellular distribution. J Cell Biol 108:569–578Google Scholar
  22. Gonzalez A, Lerner TJ, Huecas M, Sosa-Pineda B, Nogueira N, Lizardi PM (1985) Apparent generation of a segmented mRNA from two separate tandem gene families in Trypanosoma cruzi. Nucleic Acids Res 13:5789–5804Google Scholar
  23. Grant JW, Taubman MB, Church SL, Johnson RL, Nadal-Ginard B (1990a) Mammalian nonsarcomeric myosin regulatory light chains are encoded by two differentially regulated and linked genes. J Cell Biol 111:1127–1135Google Scholar
  24. Grant JW, Zhong RQ, McEwen PM, Church SL (1990b) Human nonsarcomeric 20,000 Da myosin regulatory light chain cDNA. Nucleic Acids Res 18:5892–5892Google Scholar
  25. Guerini D, Krinks MH, Sikela JM, Hahn WE, Klee CB (1989) Isolation and sequence of a cDNA clone for human calcineurin B, the Ca2+-binding subunit of the Ca2+/calmodulin-stimulated protein phosphatase. DNA 8:675–682Google Scholar
  26. Hailstones DL, Gunning PW (1990) Characterization of human myosin light chains 1 sa and 3nm: implications for isoform evolution and function. Mol Cell Biol 10:1095–1104Google Scholar
  27. Hardin PE, Klein WH (1987) Unusual sequence conservation in the 5′ and 3′ untranslated regions of the sea urchin spec mRNAs. J Mol Evol 25:126–133Google Scholar
  28. Hardy DO, Bender PK, Kretsinger RH (1988) Two calmodulin genes are expressed in Arbacia punctulata. An ancient gene duplication is indicated. J Mol Biol 199:223–227Google Scholar
  29. Harper JF, Sussman MR, Schaller GE, Putnam-Evans C, Charbonneau H, Harmon AC (1991) A calcium-dependent protein kinase with a regulatory domain similar to calmodulin. Science 252:951–954Google Scholar
  30. Heidorn DB, Trewhella J (1988) Comparison of the crystal and solution structures of calmodulin and troponin C. Biochemistry 27:909–915Google Scholar
  31. Herzberg O, James MNG (1985) Structure of the calcium regulatory muscle protein troponin-C at 2.8 Å resolution. Nature 313:653–659Google Scholar
  32. Herzberg O, James MNG (1988) Refined crystal structure of troponin C from turkey skeletal muscle at 2.0 Å resolution. J Mol Biol 203:761–779Google Scholar
  33. Hosoya H, Takagi T, Mabuchi I, Iwaasa H, Sakai H, Hiramoto Y, Konishi K (1988) The amino acid sequence, immunofluorescence and microinjection studies on the 15 kDa calcium-binding protein from sea urchin egg. Cell Struct Funct 13:525–532Google Scholar
  34. Hunt DF, Yates JR III, Shabanowitz J, Bruns ME, Bruns DE (1989) Amino acid sequence analysis of two mouse calbindin-D9k isoforms by tandem mass spectrometry. Protein modification by internal insertion of a single amino acid. J Biol Chem 264:6580–6586Google Scholar
  35. Jena PK, Reddy ASN, Poovaiah BW (1989) Molecular cloning and sequencing of a cDNA for plant calmodulin: signal-induced changes in the expression of calmodulin. Proc Natl Acad Sci USA 86:3644–3648Google Scholar
  36. Karess RE, Chang X-J, Edwards KA, Kulkarni S, Aguilera I, Kiehart DP (1991) The regulatory light chain of nonmuscle myosin is encoded by spaghetti-squash, a gene required for cytokinesis in Drosophila. Cell 65:1177–1189Google Scholar
  37. Kobayashi T, Kagami O, Takagi T, Konishi K (1989) Amino acid sequence of horseshoe crab, Tachypleus tridentatus, striated muscle troponin C. J Biochem 105:823–828Google Scholar
  38. Koller M, Schnyder B, Strehler EE (1990) Structural organization of the human CaMIII calmodulin gene. Biochim Biophys Acta 1087:180–189Google Scholar
  39. Koller M, Baumer A, Strehler EE (1991) Characterization of two novel human retropseudogenes related to the calmodulin-encoding gene, CaMII. Gene 97:245–251Google Scholar
  40. Kretsinger RH, Rudnick SE, Weissman LJ (1986) Crystal structure of calmodulin. J Inorg Biochem 28:289–302Google Scholar
  41. Kretsinger RH, Tolbert D, Nakayama S, Pearson W (1991) The EF-hand, homologs and analogs. In: Heizmann C (ed) Novel calcium binding proteins. Springer-Verlag, New York, pp 17–38Google Scholar
  42. Kumar CC, Mohan SR, Zavodny PJ, Narula SK, Leibowitz PJ (1989) Characterization and differential expression of human vascular smooth muscle myosin light chain 2 isoform in non-muscle cells. Biochemistry 28:4027–4035Google Scholar
  43. Kurabayashi M, Komuro I, Tsuchimori H, Takaku F, Yazaki Y (1988) Molecular cloning and characterization of human atrial and ventricular myosin alkali light chain cDNA clones. J Biol Chem 263:13930–13936Google Scholar
  44. Kuster T. Staudemann W, Hughes GJ, Heizmann CW (1991) Parvalbumin-isoforms in chicken muscle and thymus. Amino acid sequence analysis of muscle parvalbumin by tandem mass spectrometry. Biochemistry 30:8812–8816Google Scholar
  45. Laroche A, Lemieux G, Pallotta D (1989) The nucleotide sequence of a developmentally regulated cDNA from Physarum polycephalum. Nucleic Acids Res 17:10502–10502Google Scholar
  46. Lee MG-S, Chen J, Ho AWM, D'Alesandro PA, Van der Ploeg LHT (1990) A putative flagellar Ca2+-binding protein of the flagellum of trypanosomatid protozoan parasites. Nucleic Acids Res 18:4252–4252Google Scholar
  47. Lefort A, Lecocq R, Libert F, Lamy F, Swillens S, Vassart G, Dumont JE (1989) Cloning and sequencing of a calcium-binding protein regulated by cyclic AMP in the thyroid. EMBO J 8:111–116Google Scholar
  48. LeJohn HB (1989) Structure and expression of fungal calmodulin gene. J Biol Chem 264:19366–19372Google Scholar
  49. Lenz S, Lohse P, Seidel U, Arnold H-H (1989) The alkali light chains of human smooth and nonmuscle myosins are encoded by a single gene. Tissue-specific expression by alternative splicing pathways. J Biol Chem 264:9009–9015Google Scholar
  50. Libera LD, Hoffmann E, Floroff M, Jackowski G (1989) Isolation and nucleotide sequence of the cDNA encoding human ventricular myosin light chain 2. Nucleic Acids Res 17:2360–2360Google Scholar
  51. Ling V, Zielinski RE (1989) Cloning of cDNA sequences encoding the calcium-binding protein, calmodulin, from barley (Hodeum vulgare L.). Plant Physiol 90:714–719Google Scholar
  52. Maeda N, Zhu D, FitchWM (1984) Amino acid sequences of lower vertebrate parvalbumins and their evolution: parvalbumins of boa, turtle, and salamander. Mol Biol Evol 1:473–488Google Scholar
  53. Maeda K, Müller-Gerhardt E, Wittinghofer A (1990) Sequence of two isoforms of myosin light chain 2 isolated from a rabbit fast skeletal muscle lambda library. Nucleic Acids Res 22:6687–6687Google Scholar
  54. Matsushima N, Izumi Y, Masuo T, Yoshino Y, Ueki T, Miyake YJ (1989) Binding of both Ca+ and mastoparan to calmodulin induces a large change in the tertiary structure. Biochemistry (Tokyo) 105:883–887Google Scholar
  55. McNally EM, Buttrick PM, Leinwand LA (1989) Ventricular myosin light chain 1 is developmentally regulated and does not change in hypertension. Nucleic Acids Res 17:2753–2767Google Scholar
  56. Moncrief ND, Kretsinger RH, Goodman M (1990) Evolution of EF-hand calcium-modulated proteins. I. Relationships based on amino acid sequences. J Mol Evol 30:522–562Google Scholar
  57. Palmisano WA, Henzl MT (1990) Partial nucleotide sequence of the parvalbumin from chicken thymus designated “avian thymic hormone.” Biochem Biophys Res Commun 167:1286–1293Google Scholar
  58. Parker VP, Falkenthal S, Davidson N (1985) Characterization of the myosin light-chain-2 gene of Drosophila melanogaster. Mol Cell Biol 5:3058–3068Google Scholar
  59. Parmacek MS, Leiden JM (1989) Structure and expression of the murine slow/cardiac troponin C gene. J Biol Chem 264:13217–13225Google Scholar
  60. Parmacek MS, Bengur AR, Vora AJ, Leiden JM (1990) The structure and regulation of expression of the murine fast skeletal troponin C gene. Identification of a developmentally regulated, muscle-specific transcriptional enhancer. J Biol Chem 265:15970–15976Google Scholar
  61. Periasamy M, Wadgaonkar R, Kumar C, Martin BJ, Siddiqui MAQ (1989) Characterization of a rat myosin alkali light chain gene expressed in ventricular and slow twitch skeletal muscles. Nucleic Acids Res 17:7723–7734Google Scholar
  62. Permyakov EA, Shnyrov VL, Kalinichenko LP, Orlov NY (1985) Effects of cation binding on the thermal transitions in calmodulin. Biochim Biophys Acta 830:288–295Google Scholar
  63. Persechini A, Kretsinger RH (1988) The central helix of calmodulin functions as a flexible tether. J Biol Chem 263:12175–12178Google Scholar
  64. Putkey JA, Carroll SL, Means AR (1987) The nontranscribed chicken calmodulin pseudogene cross-hybridizes with mRNA from the slow-muscle troponin C gene. Mol Cell Biol 7:1549–1553Google Scholar
  65. Raghunathan S, Chandross R, Cheng B-P, Persechini A, Sobottka SE, Kretsinger RH (1992) The crystal structure of desGlu84 calmodulin has an unexpected bend at Thr-79. SubmittedGoogle Scholar
  66. Rasmussen CD, Means RL, Lu KP, May GS, Means AR (1990) Characterization and expression of the unique calmodulin gene of Aspergillus nidulans. J Biol Chem 265:13767–13775Google Scholar
  67. Roquet F, Declercq J-P, Tinant B, Rambaud J, Parello J (1992) Crystal structure of the unique parvalbumin component from the muscle of leopard shark (Triakis semifasciata): the first x-ray study of an alpha parvalbumin. SubmittedGoogle Scholar
  68. Rovner AS, McNally EM, Leinwand LA (1990) Complete cDNA sequence of rat atrial myosin light chain 1: patterns of expression during development and with hypertension. Nucleic Acids Res 18:1581–1586Google Scholar
  69. Sakane F, Yamada K, Kanoh H, Yokoyama C, Tanabe T (1990) Porcine diacylglycerol kinase sequence has zinc finger and E-F hand motifs. Nature 344:345–348Google Scholar
  70. Sankoff D, Cedergren R (1983) Simultaneous comparison of three or more sequences related by a tree. In: Sankoff D, Kruskal JB (eds) Time warps, string edits, and macromolecules: the theory and practice of sequence comparison. Addison-Wesley, London, pp 253–263Google Scholar
  71. Schaap D, de Widt J, van der Wal J, Vandekerckhove J, van Damme J, Gussow D, Ploegh HL, van Blitterwijk WJ, van der Bend RL (1990) Purification, cDNA-cloning and expression of human diacylglycerol kinase. FEBS Lett 275:151–158Google Scholar
  72. Seharaseyon J, Bober E, Hsieh C-L, Fodor WL, Francke U, Arnold H-H, Vanin EF (1990) Human embryonic/atrial myosin alkali light chain gene: characterization, sequence, and chromosomal location. Genomics 7:289–293Google Scholar
  73. Sen Gupta B, Detera-Wadleigh SD, McBride OW, Friedberg F (1989) A calmodulin pseudogene on human chromosome 17. Nucleic Acids Res 17:2868–2868Google Scholar
  74. Sorimachi H, Imajoh-Ohmi S, Emori Y, Kawasaki H, Ohno S, Minami Y, Suzuki K (1989) Molecular cloning of a novel mammalian calcium-dependent protease distinct from both m- and µ-types. Specific expression of the mRNA in skeletal muscle. J Biol Chem 264:20106–20111Google Scholar
  75. Sundaralingam M, Bergstrom R, Strasburg G, Rao ST, Roychowdhury P, Greaser M, Wang BC (1985) Molecular structure of troponin C from chicken skeletal muscle at 3-Angstrom resolution. Science 227:945–948Google Scholar
  76. Takagi T, Cox JA (1990) Amino acid sequences of four isoforms of Amphioxus sarcoplasmic calcium-binding proteins. Eur J Biochem 192:387–399Google Scholar
  77. Takemasa T, Ohnishi K, Kobayashi T, Takagi T, Konishi K, Watanabe Y (1989) Cloning and sequencing of the gene for Tetrahymena calcium-binding protein 25-kDa protein (TCBP-25). J Biol Chem 264:19293–19301Google Scholar
  78. Takemasa T, Takagi T, Kobayashi T, Konishi K, Watanabe Y (1990) The third calmodulin family protein in Tetrahymena. Cloning of the cDNA for Tetrahymena calcium-binding protein of 23 kDa (TCBP-23). J Biol Chem 265:2514–2517Google Scholar
  79. Taubman MB, Grant JW, Nadal-Ginard B (1987) Cloning and characterization of mammalian myosin regulatory light chain (RLC) cDNA: the RLC gene is expressed in smooth, sarcomeric, and nonmuscle tissues. J Cell Biol 104:1505–1513Google Scholar
  80. Todoroki H, Kobayashi R, Watanabe M, Minami H, Hidaka H (1991) Purification, characterization, and partial sequence analysis of a newly identified EF-hand type 13-kDa Ca2+ binding protein from smooth muscle and non-muscle tissues. J Biol Chem 266:18668–18673Google Scholar
  81. Wong S, Kretsinger RH, Campbell DA (1992) Identification of a new EF-hand superfamily member from Trypanosoma brucei. Molec Gen Genet (in press)Google Scholar
  82. Xiang M, Ge T, Tomlinson CR, Klein WH (1991) Structure and promoter activity of the LpS 1 genes of Lytechinus pictus. Duplicated exons account for LpS 1 proteins with eight calcium binding domains. J Biol Chem 266:10524–10533Google Scholar
  83. Yamagata K, Goto K, Kuo C-H, Kondo H, Miki N (1990) Visinin: a novel calcium binding protein expressed in retinal cone cells. Neuron 4:469–476Google Scholar
  84. Zhu D, Maeda N, Fitch WM (1985) Amino acid sequences of two parvalbumins from electric eel (Electrophorus electricus). Sci Sin B 28:926–941Google Scholar
  85. Zimmermann K, Starzinski-Powitz A (1989) A novel isoform of myosin alkali light chain isolated from human muscle cells. Nucleic Acids Res 17:10496–10496Google Scholar
  86. Zimmermann K, Kautz S, Hajdu G, Winter C, Whalen RG, Starzinski-Powitz A (1990) Heterogenic mRNAs with an identical protein-coding region of the human embryonic myosin alkali light chain in skeletal muscle cells. J Mol Biol 211:505–513Google Scholar
  87. Zühlke C, Schöfll F, Jockusch H, Simon D, Guénet J-L (1989) cDNA sequence and chromosomal localization of the mouse parvalbumin gene, Pva. Genet Res 54:37–43Google Scholar

Copyright information

© Springer-Verlag New York Inc 1992

Authors and Affiliations

  • Susumu Nakayama
    • 1
  • Nancy D. Moncrief
    • 2
  • Robert H. Kretsinger
    • 1
  1. 1.Department of BiologyUniversity of VirginiaCharlottesvilleUSA
  2. 2.Department of MammalogyVirginia Museum of Natural HistoryMartinsvilleUSA

Personalised recommendations