Skip to main content
Biochemical Journal logoLink to Biochemical Journal
. 1991 Apr 15;275(Pt 2):427–433. doi: 10.1042/bj2750427

Molecular structure of the human muscle-specific enolase gene (ENO3).

M Peshavaria 1, I N Day 1
PMCID: PMC1150071  PMID: 1840492

Abstract

The single human gene for muscle-specific enolase was isolated and its structure was characterized, from which the mature mRNA transcript and encoded protein were also deduced. The gene contains 12 exons, spans approx. 6 kb and encodes a protein of 433 residues. The gene structure is similar to that found for the rat neuron-specific enolase gene, and the deduced protein aligns precisely with other enolase sequences, including the sequence of the only published crystallized enolase, yeast eno-1. The 5' boundary of the gene includes a 5' non-coding exon and is characterized by an upstream TATA-like box and CpG-rich region. This region contains potential recognition motifs for general transcriptional regulation involving Sp1, activator protein 1 and 2, CCAAT box transcription factor/nuclear factor I and cyclic AMP, and for muscle-specific transcriptional regulation involving a CC(A + T-rich)6GG box, M-CAT-box CAATCCT and two myocyte-specific enhancer-binding factor 1 boxes.

Full text

PDF
427

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anderson S. Shotgun DNA sequencing using cloned DNase I-generated fragments. Nucleic Acids Res. 1981 Jul 10;9(13):3015–3027. doi: 10.1093/nar/9.13.3015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Batke J., Nazaryan K. B., Karapetian N. H. Complex of brain D-phosphoglycerate mutase and gamma enolase and its reactivation by D-glycerate 2,3-bisphosphate. Arch Biochem Biophys. 1988 Aug 1;264(2):510–518. doi: 10.1016/0003-9861(88)90316-5. [DOI] [PubMed] [Google Scholar]
  3. Brady S. T., Lasek R. J. Nerve-specific enolase and creatine phosphokinase in axonal transport: soluble proteins and the axoplasmic matrix. Cell. 1981 Feb;23(2):515–523. doi: 10.1016/0092-8674(81)90147-1. [DOI] [PubMed] [Google Scholar]
  4. Braun T., Bober E., Winter B., Rosenthal N., Arnold H. H. Myf-6, a new member of the human gene family of myogenic determination factors: evidence for a gene cluster on chromosome 12. EMBO J. 1990 Mar;9(3):821–831. doi: 10.1002/j.1460-2075.1990.tb08179.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Buskin J. N., Hauschka S. D. Identification of a myocyte nuclear factor that binds to the muscle-specific enhancer of the mouse muscle creatine kinase gene. Mol Cell Biol. 1989 Jun;9(6):2627–2640. doi: 10.1128/mcb.9.6.2627. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Calzone F. J., Britten R. J., Davidson E. H. Mapping of gene transcripts by nuclease protection assays and cDNA primer extension. Methods Enzymol. 1987;152:611–632. doi: 10.1016/0076-6879(87)52069-9. [DOI] [PubMed] [Google Scholar]
  7. Calì L., Feo S., Oliva D., Giallongo A. Nucleotide sequence of a cDNA encoding the human muscle-specific enolase (MSE). Nucleic Acids Res. 1990 Apr 11;18(7):1893–1893. doi: 10.1093/nar/18.7.1893. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cohen R., Holland J. P., Yokoi T., Holland M. J. Identification of a regulatory region that mediates glucose-dependent induction of the Saccharomyces cerevisiae enolase gene ENO2. Mol Cell Biol. 1986 Jul;6(7):2287–2297. doi: 10.1128/mcb.6.7.2287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Day I. N., Hinks L. J., Thompson R. J. The structure of the human gene encoding protein gene product 9.5 (PGP9.5), a neuron-specific ubiquitin C-terminal hydrolase. Biochem J. 1990 Jun 1;268(2):521–524. doi: 10.1042/bj2680521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Delort J., Dumas J. B., Darmon M. C., Mallet J. An efficient strategy for cloning 5' extremities of rare transcripts permits isolation of multiple 5'-untranslated regions of rat tryptophan hydroxylase mRNA. Nucleic Acids Res. 1989 Aug 25;17(16):6439–6448. doi: 10.1093/nar/17.16.6439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Devlin B. H., Wefald F. C., Kraus W. E., Bernard T. S., Williams R. S. Identification of a muscle-specific enhancer within the 5'-flanking region of the human myoglobin gene. J Biol Chem. 1989 Aug 15;264(23):13896–13901. [PubMed] [Google Scholar]
  12. Fink J. S., Verhave M., Kasper S., Tsukada T., Mandel G., Goodman R. H. The CGTCA sequence motif is essential for biological activity of the vasoactive intestinal peptide gene cAMP-regulated enhancer. Proc Natl Acad Sci U S A. 1988 Sep;85(18):6662–6666. doi: 10.1073/pnas.85.18.6662. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Forss-Petter S., Danielson P., Sutcliffe J. G. Neuron-specific enolase: complete structure of rat mRNA, multiple transcriptional start sites, and evidence suggesting post-transcriptional control. J Neurosci Res. 1986;16(1):141–156. doi: 10.1002/jnr.490160114. [DOI] [PubMed] [Google Scholar]
  14. Gardiner-Garden M., Frommer M. CpG islands in vertebrate genomes. J Mol Biol. 1987 Jul 20;196(2):261–282. doi: 10.1016/0022-2836(87)90689-9. [DOI] [PubMed] [Google Scholar]
  15. Giallongo A., Feo S., Moore R., Croce C. M., Showe L. C. Molecular cloning and nucleotide sequence of a full-length cDNA for human alpha enolase. Proc Natl Acad Sci U S A. 1986 Sep;83(18):6741–6745. doi: 10.1073/pnas.83.18.6741. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gustafson T. A., Kedes L. Identification of multiple proteins that interact with functional regions of the human cardiac alpha-actin promoter. Mol Cell Biol. 1989 Aug;9(8):3269–3283. doi: 10.1128/mcb.9.8.3269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hattori M., Sakaki Y. Dideoxy sequencing method using denatured plasmid templates. Anal Biochem. 1986 Feb 1;152(2):232–238. doi: 10.1016/0003-2697(86)90403-3. [DOI] [PubMed] [Google Scholar]
  18. Hawkins J. D. A survey on intron and exon lengths. Nucleic Acids Res. 1988 Nov 11;16(21):9893–9908. doi: 10.1093/nar/16.21.9893. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Horlick R. A., Benfield P. A. The upstream muscle-specific enhancer of the rat muscle creatine kinase gene is composed of multiple elements. Mol Cell Biol. 1989 Jun;9(6):2396–2413. doi: 10.1128/mcb.9.6.2396. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kozak M. An analysis of 5'-noncoding sequences from 699 vertebrate messenger RNAs. Nucleic Acids Res. 1987 Oct 26;15(20):8125–8148. doi: 10.1093/nar/15.20.8125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lamandé N., Mazo A. M., Lucas M., Montarras D., Pinset C., Gros F., Legault-Demare L., Lazar M. Murine muscle-specific enolase: cDNA cloning, sequence, and developmental expression. Proc Natl Acad Sci U S A. 1989 Jun;86(12):4445–4449. doi: 10.1073/pnas.86.12.4445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lassar A. B., Buskin J. N., Lockshon D., Davis R. L., Apone S., Hauschka S. D., Weintraub H. MyoD is a sequence-specific DNA binding protein requiring a region of myc homology to bind to the muscle creatine kinase enhancer. Cell. 1989 Sep 8;58(5):823–831. doi: 10.1016/0092-8674(89)90935-5. [DOI] [PubMed] [Google Scholar]
  23. Lathe R. Synthetic oligonucleotide probes deduced from amino acid sequence data. Theoretical and practical considerations. J Mol Biol. 1985 May 5;183(1):1–12. doi: 10.1016/0022-2836(85)90276-1. [DOI] [PubMed] [Google Scholar]
  24. Mar J. H., Ordahl C. P. A conserved CATTCCT motif is required for skeletal muscle-specific activity of the cardiac troponin T gene promoter. Proc Natl Acad Sci U S A. 1988 Sep;85(17):6404–6408. doi: 10.1073/pnas.85.17.6404. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Mar J. H., Ordahl C. P. M-CAT binding factor, a novel trans-acting factor governing muscle-specific transcription. Mol Cell Biol. 1990 Aug;10(8):4271–4283. doi: 10.1128/mcb.10.8.4271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Marangos P. J., Parma A. M., Goodwin F. K. Functional properties of neuronal and glial isoenzymes of brain enolase. J Neurochem. 1978 Sep;31(3):727–732. doi: 10.1111/j.1471-4159.1978.tb07847.x. [DOI] [PubMed] [Google Scholar]
  27. Marangos P. J., Zis A. P., Clark R. L., Goodwin F. K. Neuronal, non-neuronal and hybrid forms of enolase in brain: structural, immunological and functional comparisons. Brain Res. 1978 Jul 7;150(1):117–133. doi: 10.1016/0006-8993(78)90657-1. [DOI] [PubMed] [Google Scholar]
  28. Matsushita H., Yamada S., Satoh T., Kato K., Adachi M. Muscle-specific beta-enolase concentrations after cross- and random innervation of soleus and extensor digitorum longus in rats. Exp Neurol. 1986 Jul;93(1):84–91. doi: 10.1016/0014-4886(86)90147-0. [DOI] [PubMed] [Google Scholar]
  29. McAleese S. M., Dunbar B., Fothergill J. E., Hinks L. J., Day I. N. Complete amino acid sequence of the neurone-specific gamma isozyme of enolase (NSE) from human brain and comparison with the non-neuronal alpha form (NNE). Eur J Biochem. 1988 Dec 15;178(2):413–417. doi: 10.1111/j.1432-1033.1988.tb14465.x. [DOI] [PubMed] [Google Scholar]
  30. Miner J. H., Wold B. Herculin, a fourth member of the MyoD family of myogenic regulatory genes. Proc Natl Acad Sci U S A. 1990 Feb;87(3):1089–1093. doi: 10.1073/pnas.87.3.1089. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Ng S. Y., Gunning P., Liu S. H., Leavitt J., Kedes L. Regulation of the human beta-actin promoter by upstream and intron domains. Nucleic Acids Res. 1989 Jan 25;17(2):601–615. doi: 10.1093/nar/17.2.601. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Ohshima Y., Mitsui H., Takayama Y., Kushiya E., Sakimura K., Takahashi Y. cDNA cloning and nucleotide sequence of rat muscle-specific enolase (beta beta enolase). FEBS Lett. 1989 Jan 2;242(2):425–430. doi: 10.1016/0014-5793(89)80515-0. [DOI] [PubMed] [Google Scholar]
  33. Oliva D., Barba G., Barbieri G., Giallongo A., Feo S. Cloning, expression and sequence homologies of cDNA for human gamma enolase. Gene. 1989 Jul 15;79(2):355–360. doi: 10.1016/0378-1119(89)90217-5. [DOI] [PubMed] [Google Scholar]
  34. Pagliaro L., Kerr K., Taylor D. L. Enolase exists in the fluid phase of cytoplasm in 3T3 cells. J Cell Sci. 1989 Oct;94(Pt 2):333–342. doi: 10.1242/jcs.94.2.333. [DOI] [PubMed] [Google Scholar]
  35. Pearce J. M., Edwards Y. H., Harris H. Human enolase isozymes: electrophoretic and biochemical evidence for three loci. Ann Hum Genet. 1976 Jan;39(3):263–276. doi: 10.1111/j.1469-1809.1976.tb00130.x. [DOI] [PubMed] [Google Scholar]
  36. Penotti F. E. Human DNA TATA boxes and transcription initiation sites. A statistical study. J Mol Biol. 1990 May 5;213(1):37–52. doi: 10.1016/S0022-2836(05)80120-2. [DOI] [PubMed] [Google Scholar]
  37. Peshavaria M., Hinks L. J., Day I. N. Structure of human muscle (beta) enolase mRNA and protein deduced from a genomic clone. Nucleic Acids Res. 1989 Nov 11;17(21):8862–8862. doi: 10.1093/nar/17.21.8862. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Peshavaria M., Quinn G. B., Reeves I., Hinks L. J., Day I. N. Molecular biology of the human enolase gene family: nerve (gamma), muscle (beta) and general (alpha) isoforms. Biochem Soc Trans. 1990 Apr;18(2):254–255. doi: 10.1042/bst0180254. [DOI] [PubMed] [Google Scholar]
  39. Russell G. A., Dunbar B., Fothergill-Gilmore L. A. The complete amino acid sequence of chicken skeletal-muscle enolase. Biochem J. 1986 May 15;236(1):115–126. doi: 10.1042/bj2360115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. SWARTZ M. N., TRAUTNER T. A., KORNBERG A. Enzymatic synthesis of deoxyribonucleic acid. XI. Further studies on nearest neighbor base sequences in deoxyribonucleic acids. J Biol Chem. 1962 Jun;237:1961–1967. [PubMed] [Google Scholar]
  41. Sakimura K., Kushiya E., Obinata M., Odani S., Takahashi Y. Molecular cloning and the nucleotide sequence of cDNA for neuron-specific enolase messenger RNA of rat brain. Proc Natl Acad Sci U S A. 1985 Nov;82(21):7453–7457. doi: 10.1073/pnas.82.21.7453. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Sakimura K., Kushiya E., Obinata M., Takahashi Y. Molecular cloning and the nucleotide sequence of cDNA to mRNA for non-neuronal enolase (alpha alpha enolase) of rat brain and liver. Nucleic Acids Res. 1985 Jun 25;13(12):4365–4378. doi: 10.1093/nar/13.12.4365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Sakimura K., Kushiya E., Takahashi Y., Suzuki Y. The structure and expression of neuron-specific enolase gene. Gene. 1987;60(1):103–113. doi: 10.1016/0378-1119(87)90218-6. [DOI] [PubMed] [Google Scholar]
  44. Sawyer L., Fothergill-Gilmore L. A., Russell G. A. The predicted secondary structure of enolase. Biochem J. 1986 May 15;236(1):127–130. doi: 10.1042/bj2360127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Shapiro M. B., Senapathy P. RNA splice junctions of different classes of eukaryotes: sequence statistics and functional implications in gene expression. Nucleic Acids Res. 1987 Sep 11;15(17):7155–7174. doi: 10.1093/nar/15.17.7155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Spoerel N. A., Kafatos F. C. Isolation of full-length genes: walking the chromosome. Methods Enzymol. 1987;152:598–603. doi: 10.1016/0076-6879(87)52067-5. [DOI] [PubMed] [Google Scholar]
  47. Stec B., Lebioda L. Refined structure of yeast apo-enolase at 2.25 A resolution. J Mol Biol. 1990 Jan 5;211(1):235–248. doi: 10.1016/0022-2836(90)90023-F. [DOI] [PubMed] [Google Scholar]
  48. Tanaka M., Sugisaki K., Nakashima K. Switching in levels of translatable mRNAs for enolase isozymes during development of chicken skeletal muscle. Biochem Biophys Res Commun. 1985 Dec 31;133(3):868–872. doi: 10.1016/0006-291x(85)91215-x. [DOI] [PubMed] [Google Scholar]
  49. Tapscott S. J., Davis R. L., Thayer M. J., Cheng P. F., Weintraub H., Lassar A. B. MyoD1: a nuclear phosphoprotein requiring a Myc homology region to convert fibroblasts to myoblasts. Science. 1988 Oct 21;242(4877):405–411. doi: 10.1126/science.3175662. [DOI] [PubMed] [Google Scholar]
  50. Tolan D. R., Niclas J., Bruce B. D., Lebo R. V. Evolutionary implications of the human aldolase-A, -B, -C, and -pseudogene chromosome locations. Am J Hum Genet. 1987 Nov;41(5):907–924. [PMC free article] [PubMed] [Google Scholar]
  51. Wingender E. Compilation of transcription regulating proteins. Nucleic Acids Res. 1988 Mar 25;16(5):1879–1902. doi: 10.1093/nar/16.5.1879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Wistow G., Piatigorsky J. Recruitment of enzymes as lens structural proteins. Science. 1987 Jun 19;236(4808):1554–1556. doi: 10.1126/science.3589669. [DOI] [PubMed] [Google Scholar]
  53. Wright W. E., Sassoon D. A., Lin V. K. Myogenin, a factor regulating myogenesis, has a domain homologous to MyoD. Cell. 1989 Feb 24;56(4):607–617. doi: 10.1016/0092-8674(89)90583-7. [DOI] [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES