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






Images in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]