Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Original Paper
  • Published:

ELF a β-spectrin is a neuronal precursor cell marker in developing mammalian brain; structure and organization of the elf/β-G spectrin gene

Oncogene volume 21, pages 5255–5267 (2002)Cite this article

Abstract

Spectrins play a pivotal role in axonal transport, neurite extension, the organization of synaptic vesicles, as well as for protein sorting in the Golgi apparatus and cell membrane. Among spectrins there is great variability in sequence composition, tissue distribution, and function, with two known genes encoding the α-chain, and at least five encoding the β-chain. It remains unclear as to whether novel β-spectrins such as elf1-4are distinct genes or β-G-spectrin isoforms. The role for ELF in the developing nervous system has not been identified to date. In this study we demonstrate the genomic structure of elf-3, as well as the expression of ELF in the developing mouse brain using a peptide specific antibody against its distinctive amino-terminal end. Full genomic structural analyses reveal that elf-3is composed of 31 exons spanning ∼67˜kb, and confirm that elfand mouse brain β-G-spectrin share multiple exons, with a complex form of exon/intron usage. In embryonic stages, E9–12, anti-ELF localized to the primary brain vesicular cells that also labeled strongly with anti-nestin but not anti-vimentin. At E12–14, anti-ELF localized to axonal sprouts in the developing neuroblasts of cortex and purkinje cell layer of the cerebellum, as well as in cell bodies in the diencephalon and metencephalon. Double labeling identified significant co-localization of anti-ELF, nestin and dystrophin in sub ventricular zone cells and in stellate-like cells of the developing forebrain. These studies define clearly the expression of ELF, a new isoform of β-G-spectrin in the developing brain. Based on its expression pattern, ELF may have a role in neural stem cell development and is a marker of axonal sprouting in mid stages of embryonic development.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Similar content being viewed by others

References

  • Altschul SF, Gish W . 1996 Methods Enzymol. 266: 460–480

  • Altschul SF, Madden TI, Schaffer AA, Zhang J, Miller W, Lipman DJ . 1997 Nucleic Acids Res. 25: 3389–3402

  • Beck KA, Nelson WJ . 1998 Biochem. Biophys. Acta 1404: 153–160

  • Bennett V, Davis J, Fowler WE . 1982 Nature 299: 126–131

  • Bennett V, Gilligan DM . 1993 Annu. Rev. Cell. Biol. 9: 27–66

  • Birkenmeier CS, McFarland-Starr EC, Barker JE . 1988 Proc. Natl. Acad. Sci. USA 85: 8121–8125

  • Black JD, Koury ST, Bankert RB, Repasky EA . 1988 J. Cell Biol. 106: 97–109

  • Blakeslee D . 1977 J. Immunol. Methods 17: 361–364

  • Bloch RJ, Morrow JS . 1989 J. Cell Biol. 108: 481–493

  • Bloom ML, Birkenmeier CS, Barker JE . 1993 Blood 82: 2906–2914

  • Bulfield G, Siller WG, Wight PA, Moore KJ . 1984 Proc. Natl. Acad. Sci. USA 81: 1189–1192

  • Chen Y, Yu P, Lu D, Tagle DA, Cai T . 2001 J. Mol. Neurosci. 17: 59–70

  • Craig SW, Pardo JV . 1983 Cell Motil. 3: 449–462

  • Dahlstrand J, Lardelli M, Lendahl U . 1995 Brain Res. Dev. Brain Res. 84: 109–129

  • Davis J, Bennett V . 1983 J. Biol. Chem. 258: 7757–7766

  • De Matteis MA, Morrow JS . 2000 J. Cell. Sci. 113: 2331–2343

  • Devarajan P, Morrow JS . 1996 Membrane Protein-Cytoskeleton Complexes; Protein Interactions, Distributions and Functions Vol. 43: Nelson WJ (ed) New York: Academic Press pp. 97–128

    Book  Google Scholar 

  • Devarajan P, Stabach PR, De Matteis MA, Morrow JS . 1997 Proc. Natl. Acad. Sci. USA 94: 10711–10716

  • Devarajan P, Stabach PR, Mann AS, Ardito T, Kashgarian M, Morrow JS . 1996 J. Cell Biol. 133: 819–830

  • Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A . 1997 J. Neurosci. 17: 5046–5061

  • Dubowitz V, Crome L . 1969 Brain 92: 805–808

  • Dubreuil RR, Wang P, Dahl S, Lee J, Goldstein LS . 2000 J. Cell Biol. 149: 647–656

  • Emery AH (ed) . 1988 Duchenne Muscular Dystrophy New York: Oxford University Press

    Google Scholar 

  • Fath KR, Trimbur GM, Burgess DR . 1997 J. Cell Biol 139: 1169–1181

  • Gallagher PG, Forget BG . 1993 Semin. Hematol. 30: 4–20

  • Gallagher PG, Sabatino DE, Romana M, Cline AP, Garrett LJ, Bodine DM, Forget BG . 1999 J. Biol. Chem. 274: 6062–6073

  • Gallagher PG, Tse WT, Scarpa AL, Lux SE, Forget BG . 1997 J. Biol. Chem. 272: 19220–19228

  • Glenney Jr JR, Glenney P, Weber K . 1983 J. Cell Biol. 96: 1491–1496

  • Goodman SR, Zimmer WE, Clark MB, Zagon IS, Barker JE, Bloom ML . 1995 Brain Res. Bull. 36: 593–606

  • Hammarlund M, Davis WS, Jorgensena EM . 2000 J. Cell Biol. 149: 931–942

  • Hayes NV, Scott C, Heerkens E, Ohanian V, Maggs AM, Pinder JC, Kordeli E, Baines AJ . 2000 J. Cell Sci. 113: 2023–2034

  • Hu RJ, Moorthy S, Bennett V . 1995 J. Cell Biol. 128: 1069–1080

  • Hu RJ, Watanabe M, Bennett V . 1992 J. Biol. Chem. 267: 18715–18722

  • Joosten EA, Gribnau AA . 1989 Neuroscience 31: 439–452

  • Jung D, Pons F, Leger JJ, Aunis D, Rendon A . 1991 Neurosci. Lett. 124: 87–91

  • Kadonaga JT, Tjian R . 1986 Proc. Natl. Acad. Sci. USA 83: 5889–5893

  • Kageyama R, Pastan I . 1989 Cell 59: 815–825

  • Kordeli E, Davis J, Trapp B, Bennett V . 1990 J. Cell Biol. 110: 1341–1352

  • Kordeli E, Lambert S, Bennett V . 1995 J. Biol. Chem. 270: 2352–2359

  • Kunimoto M, Adachi T, Ishido M . 1998 J. Neurochem. 71: 2585–9252

  • Leid M, Kastner P, Chambon P . 1992 Trends Biochem. Sci. 17: 427–433

  • Levine J, Willard M . 1981 J. Cell Biol. 90: 631–642

  • Lidov HG, Byers TJ, Watkins SC, Kunkel LM . 1990 Nature 348: 725–728

  • Lux SE, Palek J . 1995 Blood. Handin RI, Lambert S and Stossel TP (ed) Philadelphia: JB Lippincott pp. 1701–1816

    Google Scholar 

  • Ma Y, Zimmer WE, Riederer BM, Bloom ML, Barker JE, Goodman SR . 1993 Mol. Brain Res. 18: 87–99

  • Malchiodi-Albedi F, Ceccarini M, Winkelmann JC, Morrow JS, Petruci TC . 1993 J. Cell Sci. 106: 67–78

  • Marin-Padilla M . 1985 J. Comp. Neurol. 235: 82–96

  • Mishra L, Cai T, Levine A, Weng D, Mezey E, Mishra B, Gearhart J . 1998 Int. J. Dev. Biol. 42: 221–224

  • Mishra L, Cai T, Yu P, Monga SP, Mishra B . 1999 Oncogene 18: 353–364

  • Mishra L, Tully RE, Monga SP, Yu P, Cai T, Makalowski W, Mezey E, Pavan WJ, Mishra B . 1997 Oncogene 15: 2361–2368

  • Moon RT, McMahon AP . 1987 Bioessays 7: 159–164

  • Moorthy S, Chen L, Bennett V . 2000 J. Cell Biol. 149: 915–930

  • Morrow JS, Rimm DL, Kennedy SP, Ciancia CD, Sinard JH, Weed SA . 1997 Handbook of Physiology. Jamieson J (ed) Oxford: Oxford University Press pp. 485–540

    Google Scholar 

  • Nelson WJ, Hammerton RW . 1989 J. Cell Biol. 108: 893–902

  • Nelson WJ, Veshnock PJ . 1987a J. Cell Biol. 104: 1527–1537

  • Nelson WJ, Veshnock PJ . 1987b Nature 328: 533–536

  • Ohara O, Ohara R, Yamakawa H, Nakajima D, Nakayama M . 1998 Brain Res. Mol. Brain Res. 57: 181–192

  • Pinder JC, Baines AJ . 2000 Nature 406: 253–254

  • Riederer BM, Zagon IS, Goodman SR . 1986 J. Cell Biol. 102: 2088–2097

  • Roesler WJ, Vandenbark GR, Hanson RW . 1989 J. Biol. Chem. 264: 9657–9664

  • Sakaguchi G, Orita S, Naito A, Maeda M, Igarashi H, Sasaki T, Takal Y . 1998 Biochem. Biophys. Res. Commun. 248: 846–851

  • Sambrook J, Fritsch EF, Manlatis T (ed) . 1989 Molecular Cloning Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press

    Google Scholar 

  • Sanger F, Nicklen S, Coulson AR . 1977 Proc. Natl. Acad. Sci. USA 74: 5463–5467

  • Scotland P, Zhou D, Benveniste H, Bennett V . 1998 J. Cell Biol. 143: 1305–1315

  • Sihag RK, Shea TB, Wang F-S . 1996 J. Neurosci. Res. 44: 430–437

  • Sikorski AF, Sangerman J, Goodman SR, Critz SD . 2000 Brain Research 852: 161–166

  • Sikorski AF, Terlecki G, Zagon IS, Goodman SR . 1991 J. Cell Biol. 114: 313–318

  • Siman R, Ahdoot M, Lynch G . 1987 J. Neurosci. 7: 55–64

  • Sobue K . 1990 Neurosci. Res. 13: Suppl S80–S91

  • Sobue K, Kanda K . 1989 Neuron 3: 311–319

  • Srinivasan Y, Lewallen M, Angelides KJ . 1992 J. Biol. Chem. 267: 7483–7489

  • Stabach PR, Morrow JS . 2000 J. Biol. Chem. 275: 21385–21395

  • Stankewich MC, Tse WT, Peters LL, Ch'ng Y, John KM, Stabach PR, Devarajan P, Morrow JS, Lux SE . 1998 Proc. Natl. Acad. Sci. USA 95: 14158–14163

  • Takashima S, Becker LE, Armstrong DL, Chan F . 1981 Brain Res. 225: 1–21

  • Thomas G . 2000 Nat. Cell Biol. 2: E71–E72

  • Thomas GS, Kiehart DP . 1994 Development 120: 2039–2050

  • Wechsler A, Teichberg VI . 1998 EMBO J. 17: 3931–3939

  • Whittaker PA, Southern EM . 1986 Gene 41: 129–134

  • Winkelman JC, Leto TL, Watkins PC, Eddy R, Shows TB, Linnenbach AJ, Sahr KE, Kathuria N, Marchesi VT, Forget BG . 1988 Blood 72: 328–334

  • Yu P, Cai T, Monga SP, Mishra B, Mishra L . 1999 Mamm. Genome 10: 62–67

  • Zagon IS, Higbee R, Riederer BM, Goodman SR . 1986 J. Neurosci. 6: 2977–2986

  • Zarnescu DC, Thomas GH . 1999 J. Cell Biol. 146: 1075–1086

  • Zhou D, Lambert S, Malen PL, Carpenter S, Boland LM, Bennett V . 1998 J. Cell Biol. 143: 1295–1304

  • Ziemnicka-Kotula D, Xu J, Gu H, Potempska A, Kim KS, Jenkins EC, Trenkner E, Kotula L . 1998 J. Biol. Chem. 273: 13681–13692

  • Zimmer WE, Ma YP, Goodman SR . 1991 Brain Res. Bull. 27: 187–193

Download references

Author information

Authors and Affiliations

  1. Laboratory of Development Molecular Biology, DVAMC, Washington, 20422, District of Columbia, DC, USA

    Yi Tang, Varalakshmi Katuri, Sohail Iqbal, Robert S Lu & Lopa Mishra

  2. Fels Institute for Cancer Research and Molecular Biology, Temple University, Philadelphia, Pennsylvania, USA

    Yi Tang, Varalakshmi Katuri, Sohail Iqbal, Robert S Lu & Lopa Mishra

  3. Temple University School of Medicine, Philadelphia, Pennsylvania, USA

    Tina Narayan

  4. Children's Hospital, Philadelphia, Pennsylvania, USA

    Zhili Wang

  5. Clinical Gene Therapy Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, Maryland, USA

    Bibhuti Mishra

  6. Georgetown University, Washington, District of Columbia, USA

    Bibhuti Mishra

Authors
  1. Yi Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Varalakshmi Katuri
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sohail Iqbal
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tina Narayan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zhili Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Robert S Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Lopa Mishra
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Bibhuti Mishra
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bibhuti Mishra.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tang, Y., Katuri, V., Iqbal, S. et al. ELF a β-spectrin is a neuronal precursor cell marker in developing mammalian brain; structure and organization of the elf/β-G spectrin gene. Oncogene 21, 5255–5267 (2002). https://doi.org/10.1038/sj.onc.1205548

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/sj.onc.1205548

Keywords

This article is cited by

Search

Advanced search

Quick links