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Strong evolutionary conservation of broadly expressed protein isoforms in the troponin I gene family and other vertebrate gene families

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Abstract

It is well established that different protein classes undergo molecular evolution at different rates, presumably reflecting differing functional constraints. However, it is also the case that different isoforms of the “same” protein, encoded by a multigene family, may evolve at different rates. Here I report a relationship within gene families between isoform evolutionary rate and gene expression profile: Broadly expressed isoforms show stronger sequence conservation than do narrowly expressed isoforms. This observation emerged initially from cDNA cloning and sequencing studies, described here, of a vertebrate gene family encoding three differentially expressed isoforms of the muscle protein troponin I. However, the expression breadth/sequence conservation relationship applies to vertebrate gene families in general. In a broad and arbitrary survey sampling of sequence data on well-characterized vertebrate gene families, I found that in 14/15 families the most strongly conserved isoform was the most broadly expressed isoform, or one of several similarly broadly expressed isoforms. Broadly expressed isoforms are presumably subjected to greater negative selection pressure because they must function in a more diverse biochemical environment than do narrowly expressed isoforms. The expression breadth/evolutionary rate relationship has several interesting implications regarding the overall process of gene family evolution by duplication/divergence from ancestral genes.

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References

  • Auerbach S, Brinster RL (1967) Lactate dehydrogenase isozymes in the early mouse embryo. Exp Cell Res 46:89–92

    Article  CAS  PubMed  Google Scholar 

  • Ausoni S, De Nardi C, Moretti P, Gorza L, Schiaffino S (1991) Developmental expression of rat cardiac troponin I mRNA. Development 112:1041–1051

    CAS  PubMed  Google Scholar 

  • Ausoni S, Campione M, Picard A, Moretti P, Vitadello M, De Nardi C, Schiaffino S (1994) Structure and regulation of the mouse cardiac troponin I gene. J Biol Chem 269:339–346

    CAS  PubMed  Google Scholar 

  • Baldwin AS Jr, Kittler ELW, Emerson CP Jr (1985) Structure, evolution, and regulation of a fast skeletal muscle troponin I gene. Proc Natl Acad Sci USA 82:8080–8084

    CAS  PubMed  Google Scholar 

  • Bandman E (1992) Contractile protein isoforms in muscle development. Dev Biol 154:273–283

    Article  CAS  PubMed  Google Scholar 

  • Barker PA, Shooter EM (1994) Disruption of NGF binding to the low affinity neurotrophin receptor p75LNTR reduces NGF binding to TrkA on PC12 cells. Neuron 13:203–215

    Article  CAS  PubMed  Google Scholar 

  • Beyer EC (1993) Gap junctions. Int Rev Cytol 137C:1–35

    CAS  PubMed  Google Scholar 

  • Bradshaw KD, Waterman MR, Couch RT, Simpson ER, Zuber MX (1987) Characterization of complementary deoxyribonucleic acid for human adrenocortical 17α-hydroxylase: a probe for analysis of 17α-hydroxylase deficiency. Mol Endocrinol 1:348–354

    CAS  PubMed  Google Scholar 

  • Campbell AM, Kessler PD, Sagara Y, Inesi G, Fambrough DM (1991) Nucleotide sequences of avian cardiac and brain SR/ER Ca2+-ATPases and functional comparisons with fast twitch Ca2+-ATPase. J Biol Chem 266:16050–16055

    CAS  PubMed  Google Scholar 

  • Collins JH (1991) Myosin light chains and troponin C: structural and evolutionary relationships revealed by amino acid sequence comparisons. J Muscle Res Cell Motil 12:3–25

    Article  CAS  PubMed  Google Scholar 

  • Corin SJ, Juhasz O, Zhu L, Conley P, Kedes L, Wade R (1994) Structure and expression of the human slow twitch skeletal muscle troponin I gene. J Biol Chem 269:10651–10659

    CAS  PubMed  Google Scholar 

  • Davies AM, Lee KF, Jaenisch R (1993) p75-deficient trigeminal sensory neurons have an altered response to NGF but not to other neurotrophins. Neuron 11:565–574

    Article  CAS  PubMed  Google Scholar 

  • Day INM (1992) Enolases and PGP9.5 as tissue-specific markers. Biochem Soc Trans 20:637–642

    CAS  PubMed  Google Scholar 

  • Drysdale TA, Tonissen AF, Patterson KD, Crawford MJ, Krieg PA (1994) Cardiac troponin I is a heart-specific marker in theXenopus embryo: expression during abnormal heart morphogenesis. Dev Biol 165:432–441

    Article  CAS  PubMed  Google Scholar 

  • Ebendal T (1992) Function and evolution of the NGF family and its receptors. J Neurosci Res 32:461–470

    Article  CAS  PubMed  Google Scholar 

  • Evans CT, Ledesma DB, Shulz TZ, Simpson ER, Mendelson CR (1986) Isolation and characterization of a complementary DNA specific for human aromatase-system cytochrome P-450 mRNA. Proc Natl Acad Sci USA 83:6387–6391

    CAS  PubMed  Google Scholar 

  • Feinberg AP, Vogelstein B (1984) Addendum: a technique for radio-labeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 137:266–267

    CAS  PubMed  Google Scholar 

  • Geleibter J (1987) Dideoxynucleotide sequencing of RNA and uncloned cDNA. Focus (Bethesda Research Laboratories, Inc) 9:5–8

    Google Scholar 

  • Gorza L, Ausoni S, Merciai N, Hastings KEM, Schiaffino S (1993) Regional differences in troponin I isoform switching during rat heart development. Dev Biol 156:253–264

    Article  CAS  PubMed  Google Scholar 

  • Guénet J-L, Simon-Chazottes D, Gravel M, Hastings KEM, Schiaffino S (1996) Cardiac and skeletal muscle troponin I isoforms are encoded by a dispersed gene family on mouse chromosomes 1 and 7. Mamm Genome 7:13–15

    PubMed  Google Scholar 

  • Gunning P, Hardeman E (1991) Multiple mechanisms regulate muscle fiber diversity. FASEB J 5:3064–3070

    CAS  PubMed  Google Scholar 

  • Hastings KEM, Emerson CP Jr (1982) cDNA clone analysis of six co-regulated mRNAs encoding skeletal muscle contractile proteins. Proc Natl Acad Sci USA 79:1553–1557

    CAS  PubMed  Google Scholar 

  • Hastings KEM, Koppe RI, Marmor E, Bader D, Shimada Y, Toyota N (1991) Structure and developmental regulation of troponin I isoforms. cDNA clone analysis of avian cardiac troponin I mRNA. J Biol Chem 266:19659–19665

    CAS  PubMed  Google Scholar 

  • Hide WA, Chan L, Li W-H (1992) Structure and evolution of the lipase superfamily. J Lipid Res 33:167–178

    CAS  PubMed  Google Scholar 

  • Karin NJ, Kaprelian Z, Fambrough DM (1989) Expression of avian Ca2+-ATPase in cultured mouse myogenic cells. Mol Cell Biol 9:1978–1986

    CAS  PubMed  Google Scholar 

  • Kobayashi T, Takagi T, Konishi K, Wnuk W (1989) Amino acid sequences of the two major isoforms of troponin C from crayfish. J Biol Chem 264:18247–18259

    CAS  PubMed  Google Scholar 

  • Konigsberg IR (1979) Skeletal myoblasts in culture. Methods Enzymol 58:511–542

    CAS  PubMed  Google Scholar 

  • Koppe RI, Hallauer PL, Karpati GK, Hastings KEM (1989) cDNA clone and expression analysis of rodent fast and slow skeletal muscle troponin I mRNAs. J Biol Chem 264:14327–14333

    CAS  PubMed  Google Scholar 

  • Kuma K, Iwabe N, Miyata T (1995) Functional constraints against variation on molecules from the tissue level: slowly evolving brain-specific genes demonstrated by protein kinase and immunoglobulin supergene families. Mol Biol Evol 12:123–130

    CAS  PubMed  Google Scholar 

  • Le Novère N, Changeux JP (1995) Molecular evolution of the nicotinic acetylcholine receptor: an example of multigene family in excitable cells. J Mol Evol 40:155–172

    PubMed  Google Scholar 

  • Lindsay DT (1963) Isozymic patterns and properties of lactate dehydrogenase from developing tissues of the chicken. J Exp Zool 152: 75–89

    Article  CAS  PubMed  Google Scholar 

  • Lompré A-M, Anger M, Levitsky D (1994) Sarco(endo)plasmic reticulum calcium pumps in the cardiovascular system: function and gene expression. J Mol Cell Cardiol 26:1109–1121

    Article  PubMed  Google Scholar 

  • Ludueña RF (1993) Are tubulin isotypes functionally significant? Mol Biol Cell 4:445–457

    PubMed  Google Scholar 

  • Markert CL, Shaklee JB, Whitt GS (1975) Evolution of a gene. Science 189:102–114

    CAS  PubMed  Google Scholar 

  • Markert CL, Ursprung H (1962) The ontogeny of isozyme patterns of lactate dehydrogenase in the mouse. Dev Biol 5:363–381

    Article  CAS  Google Scholar 

  • Martin AF, Orlowski J (1991) Molecular cloning and developmental expression of the rat cardiac-specific isoform of troponin I. J Mol Cell Cardiol 23:583–588

    Article  CAS  PubMed  Google Scholar 

  • Moncrief ND, Kretsinger RH, Goodman M (1990) Evolution of the EF-hand calcium-modulated proteins. I. Relationships based on amino acid sequences. J Mol Evol 30:522–562

    Article  CAS  PubMed  Google Scholar 

  • Moore LA, Tidyman WE, Arrizubietta MJ, Bandman E (1993) The evolutionary relationship of avian and mammalian myosin heavy-chain genes. J Mol Evol 36:21–30

    CAS  PubMed  Google Scholar 

  • Mühlebach SM, Gross M, Wirz T, Wallimann T, Perriard J-C, Wyss M (1994) Sequence homology and structure predictions of the creatine kinase isozymes. Mol Cell Biochem 133(134):245–262

    PubMed  Google Scholar 

  • Murphy AM, Jones L, Sims HF, Strauss AW (1991) Molecular cloning of rat cardiac troponin I and analysis of troponin I isoform expression in developing rat heart. Biochemistry 30:707–712

    CAS  PubMed  Google Scholar 

  • Nelson DR, Kamataki T, Waxman DJ, Guengerich FP, Estabrook RW, Feyerseisen R, Gonzales FJ, Coon MJ, Gunsalus IC, Gotoh O, Okuda K, Nebert DW (1993) The P450 superfamily: update on new sequences, gene mapping, accession numbers, early trivial names of enzymes, and nomenclature. DNA Cell Biol 12:1–51

    CAS  PubMed  Google Scholar 

  • Ohno S (1970) Evolution by gene duplication. Springer-Verlag, Heidelberg

    Google Scholar 

  • Ohta T (1989) Role of gene duplication in evolution. Genome 31:304–310

    CAS  PubMed  Google Scholar 

  • Perry SV (1994) Activation of the contractile mechanism by calcium. In: Engel AG, Franzini-Armstrong L (eds) Myology: basic and clinical, 2nd ed, vol 1. McGraw-Hill, New York, pp 529–552

    Google Scholar 

  • Pette D, Staron RS (1990) Cellular and molecular diversities of mammalian skeletal muscle fibers. Rev Physiol Biochem Pharmacol 116:1–76

    CAS  PubMed  Google Scholar 

  • Sabry MA, Dhoot GK (1989) Identification and pattern of expression of a developmental isoform of troponin 1 in chicken and rat cardiac muscle. J Muscle Res Cell Motil 10:85–91

    Article  CAS  PubMed  Google Scholar 

  • Saggin L, Gorza L, Ausoni S, Schiaffino S (1990) Troponin I switching in the developing heart. J Biol Chem 264:16299–16302

    Google Scholar 

  • Sargent PB (1993) The diversity of neuronal nicotinic acetylcholine receptors. Annu Rev Neurosci 16:403–443

    Article  CAS  PubMed  Google Scholar 

  • Stewart AFR, Camoretti-Mercado B, Perlman D, Gupta M, Jakoveic S, Zak R (1991) Structural and phylogenetic analysis of the chicken ventricular myosin heavy chain rod. J Mol Evol 33:357–366

    Article  CAS  PubMed  Google Scholar 

  • Sullivan KF (1988) Structure and utilization of tubulin isotypes. Annu Rev Cell Biol 4:687–716

    Article  CAS  PubMed  Google Scholar 

  • Sutherland CJ, Elsom VL, Gordon ML, Dunwoodie SL, Hardeman EC (1991) Coordination of skeletal muscle gene expression occurs late in mammalian development. Dev Biol 146:167–178

    Article  CAS  PubMed  Google Scholar 

  • Thomas PS (1980) Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc Natl Acad Sci USA 77:5201–5205

    CAS  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties, and weight matrix choice. Nucleic Acids Res 22:4673–4680

    CAS  PubMed  Google Scholar 

  • Tsuji S, Qureshi MA, Hou EW, Fitch WM, Li SS-L (1994) Evolutionary relationships of lactate dehydrogenases (LDHs) from mammals, birds, an amphibian, fish, barley, and bacteria: LDH cDNA sequences fromXenopus, pig, and rat. Proc Natl Acad Sci USA 91:9392–9396

    CAS  PubMed  Google Scholar 

  • Vallins WJ, Brand NJ, Dabhade N, Butler-Browne G, Yacoub MH, Barton PJR (1990) Molecular cloning of human cardiac troponin I using polymerase chain reaction. FEBS Lett 270:57–61

    Article  CAS  PubMed  Google Scholar 

  • Wallimann T, Hemmer W (1994) Creatine kinase in non-muscle tissues and cells. Mol Cell Biochem 133(134):193–220

    PubMed  Google Scholar 

  • Wilkinson JM, Grand RJA (1978) Comparison of amino acid sequences of troponin I from different striated muscles. Nature 271: 31–35

    CAS  PubMed  Google Scholar 

  • Wilson AC, Carlson SS, White TJ (1977) Biochemical evolution. Annu Rev Biochem 46:573–639

    Article  CAS  PubMed  Google Scholar 

  • Zhu L, Perez-Alvarado G, Wade R (1994) Sequencing of a cDNA encoding the human fast-twitch skeletal muscle isoform of troponin I. Biochim Biophys Acta 1217:338–340

    CAS  PubMed  Google Scholar 

  • Zhu L, Lyons GE, Juhasz O, Joya JE, Hardeman EC, Wade R (1995) Developmental regulation of troponin I isoform genes in striated muscles of transgenic mice. Dev Biol 169:487–503

    Article  CAS  PubMed  Google Scholar 

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  1. Montreal Neurological Institute and Departments of Neurology/Neurosurgery and Biology, McGill University, 3801 University St., H3A 2134, Montreal, Quebec, Canada

    Kenneth E. M. Hastings

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  1. Kenneth E. M. Hastings
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The nucleotide/amino acid sequence reported in this paper has been submitted to GenBank (accession number U37118)

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Hastings, K.E.M. Strong evolutionary conservation of broadly expressed protein isoforms in the troponin I gene family and other vertebrate gene families. J Mol Evol 42, 631–640 (1996). https://doi.org/10.1007/BF02338796

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  • DOI: https://doi.org/10.1007/BF02338796

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