Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1992 Sep 1;118(5):1259–1270. doi: 10.1083/jcb.118.5.1259

Bravo/Nr-CAM is closely related to the cell adhesion molecules L1 and Ng-CAM and has a similar heterodimer structure

PMCID: PMC2289593  PMID: 1512296

Abstract

Diverse cell-surface molecules of the nervous system play an important role in specifying cell interactions during development. Using a method designed to generate mAbs against neural surface molecules of defined molecular weight, we have previously reported on the surface protein, Bravo, found in the developing avian retinotectal system. Bravo is immunologically detected on developing optic fibers in the retina, but absent from distal regions of the same fibers in the tectum. We have isolated cDNA clones encompassing the entire coding region of Bravo, including clones containing five alternative sequences of cDNA. These putative alternatively spliced sequences encode stretches of polypeptide ranging in length from 10-93 amino acids and are predicted to be both extra- and intracellular. The deduced primary structure of Bravo reveals that, like the cell adhesion molecules (CAMs) chicken Ng- CAM and mouse L1, Bravo is composed of six Ig-like domains, five fibronectin type III repeats, a transmembrane domain, and a short cytoplasmic region. Recently, the cDNA sequence of a related molecule, Nr-CAM, was reported and its possible identity with Bravo discussed (Grumet, M., V. Mauro, M. P. Burgoon, G. E. Edelman, and B. A. Cunningham. 1991. J. Cell Biol. 113:1399-1412). Here we confirm this identity and moreover show that Bravo is found on Muller glial processes and end-feet in the developing retina. In contrast to the single polypeptide chain structure of Nr-CAM reported previously, we show that Bravo has a heterodimer structure composed of an alpha chain of M(r) 140/130 and a beta chain of 60-80 kD. As with L1 and Ng-CAM, the two chains of Bravo are generated from an intact polypeptide by cleavage at identical locations and conserved sites within all three molecules (Ser-Arg/Lys-Arg). The similar domain composition and heterodimer structure, as well as the 40% amino acid sequence identity of these molecules, defines them as an evolutionarily related subgroup of CAMs. The relationship of Bravo to molecules known to be involved in cell adhesion and process outgrowth, combined with its pattern of expression and numerous potential isoforms, suggests a complex role for this molecule in cell interactions during neural development.

Full Text

The Full Text of this article is available as a PDF (1.9 MB).

Selected References

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

  1. Ansorge W. Fast and sensitive detection of protein and DNA bands by treatment with potassium permanganate. J Biochem Biophys Methods. 1985 May;11(1):13–20. doi: 10.1016/0165-022x(85)90037-5. [DOI] [PubMed] [Google Scholar]
  2. Becker J. W., Erickson H. P., Hoffman S., Cunningham B. A., Edelman G. M. Topology of cell adhesion molecules. Proc Natl Acad Sci U S A. 1989 Feb;86(3):1088–1092. doi: 10.1073/pnas.86.3.1088. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bieber A. J., Snow P. M., Hortsch M., Patel N. H., Jacobs J. R., Traquina Z. R., Schilling J., Goodman C. S. Drosophila neuroglian: a member of the immunoglobulin superfamily with extensive homology to the vertebrate neural adhesion molecule L1. Cell. 1989 Nov 3;59(3):447–460. doi: 10.1016/0092-8674(89)90029-9. [DOI] [PubMed] [Google Scholar]
  4. Bork P. Shuffled domains in extracellular proteins. FEBS Lett. 1991 Jul 29;286(1-2):47–54. doi: 10.1016/0014-5793(91)80937-x. [DOI] [PubMed] [Google Scholar]
  5. Brümmendorf T., Wolff J. M., Frank R., Rathjen F. G. Neural cell recognition molecule F11: homology with fibronectin type III and immunoglobulin type C domains. Neuron. 1989 Apr;2(4):1351–1361. doi: 10.1016/0896-6273(89)90073-1. [DOI] [PubMed] [Google Scholar]
  6. Burgoon M. P., Grumet M., Mauro V., Edelman G. M., Cunningham B. A. Structure of the chicken neuron-glia cell adhesion molecule, Ng-CAM: origin of the polypeptides and relation to the Ig superfamily. J Cell Biol. 1991 Mar;112(5):1017–1029. doi: 10.1083/jcb.112.5.1017. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chang S., Rathjen F. G., Raper J. A. Extension of neurites on axons is impaired by antibodies against specific neural cell surface glycoproteins. J Cell Biol. 1987 Feb;104(2):355–362. doi: 10.1083/jcb.104.2.355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chuong C. M., Edelman G. M. Expression of cell-adhesion molecules in embryonic induction. II. Morphogenesis of adult feathers. J Cell Biol. 1985 Sep;101(3):1027–1043. doi: 10.1083/jcb.101.3.1027. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cole G. J., Schachner M. Localization of the L2 monoclonal antibody binding site on chicken neural cell adhesion molecule (NCAM) and evidence for its role in NCAM-mediated cell adhesion. Neurosci Lett. 1987 Jul 22;78(2):227–232. doi: 10.1016/0304-3940(87)90638-0. [DOI] [PubMed] [Google Scholar]
  10. Crossin K. L., Chuong C. M., Edelman G. M. Expression sequences of cell adhesion molecules. Proc Natl Acad Sci U S A. 1985 Oct;82(20):6942–6946. doi: 10.1073/pnas.82.20.6942. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Crossland W. J., Cowan W. M., Rogers L. A. Studies on the development of the chick optic tectum. IV. An autoradiographic study of the development of retino-tectal connections. Brain Res. 1975 Jun 20;91(1):1–23. doi: 10.1016/0006-8993(75)90463-1. [DOI] [PubMed] [Google Scholar]
  12. Cunningham B. A., Hemperly J. J., Murray B. A., Prediger E. A., Brackenbury R., Edelman G. M. Neural cell adhesion molecule: structure, immunoglobulin-like domains, cell surface modulation, and alternative RNA splicing. Science. 1987 May 15;236(4803):799–806. doi: 10.1126/science.3576199. [DOI] [PubMed] [Google Scholar]
  13. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Dodd J., Morton S. B., Karagogeos D., Yamamoto M., Jessell T. M. Spatial regulation of axonal glycoprotein expression on subsets of embryonic spinal neurons. Neuron. 1988 Apr;1(2):105–116. doi: 10.1016/0896-6273(88)90194-8. [DOI] [PubMed] [Google Scholar]
  15. Ebina Y., Ellis L., Jarnagin K., Edery M., Graf L., Clauser E., Ou J. H., Masiarz F., Kan Y. W., Goldfine I. D. The human insulin receptor cDNA: the structural basis for hormone-activated transmembrane signalling. Cell. 1985 Apr;40(4):747–758. doi: 10.1016/0092-8674(85)90334-4. [DOI] [PubMed] [Google Scholar]
  16. Edelman G. M. CAMs and Igs: cell adhesion and the evolutionary origins of immunity. Immunol Rev. 1987 Dec;100:11–45. doi: 10.1111/j.1600-065x.1987.tb00526.x. [DOI] [PubMed] [Google Scholar]
  17. Edelman G. M. Cell adhesion molecules in neural histogenesis. Annu Rev Physiol. 1986;48:417–430. doi: 10.1146/annurev.ph.48.030186.002221. [DOI] [PubMed] [Google Scholar]
  18. Engel J. Domains in proteins and proteoglycans of the extracellular matrix with functions in assembly and cellular activities. Int J Biol Macromol. 1991 Jun;13(3):147–151. doi: 10.1016/0141-8130(91)90039-w. [DOI] [PubMed] [Google Scholar]
  19. Faissner A., Teplow D. B., Kübler D., Keilhauer G., Kinzel V., Schachner M. Biosynthesis and membrane topography of the neural cell adhesion molecule L1. EMBO J. 1985 Dec 1;4(12):3105–3113. doi: 10.1002/j.1460-2075.1985.tb04052.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Feinberg A. P., Vogelstein B. "A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity". Addendum. Anal Biochem. 1984 Feb;137(1):266–267. doi: 10.1016/0003-2697(84)90381-6. [DOI] [PubMed] [Google Scholar]
  21. Fischer G., Künemund V., Schachner M. Neurite outgrowth patterns in cerebellar microexplant cultures are affected by antibodies to the cell surface glycoprotein L1. J Neurosci. 1986 Feb;6(2):605–612. doi: 10.1523/JNEUROSCI.06-02-00605.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Furley A. J., Morton S. B., Manalo D., Karagogeos D., Dodd J., Jessell T. M. The axonal glycoprotein TAG-1 is an immunoglobulin superfamily member with neurite outgrowth-promoting activity. Cell. 1990 Apr 6;61(1):157–170. doi: 10.1016/0092-8674(90)90223-2. [DOI] [PubMed] [Google Scholar]
  23. Gennarini G., Rougon G., Vitiello F., Corsi P., Di Benedetta C., Goridis C. Identification and cDNA cloning of a new member of the L2/HNK-1 family of neural surface glycoproteins. J Neurosci Res. 1989 Jan;22(1):1–12. doi: 10.1002/jnr.490220102. [DOI] [PubMed] [Google Scholar]
  24. Glass D. B., el-Maghrabi M. R., Pilkis S. J. Synthetic peptides corresponding to the site phosphorylated in 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase as substrates of cyclic nucleotide-dependent protein kinases. J Biol Chem. 1986 Feb 25;261(6):2987–2993. [PubMed] [Google Scholar]
  25. Grumet M., Edelman G. M. Heterotypic binding between neuronal membrane vesicles and glial cells is mediated by a specific cell adhesion molecule. J Cell Biol. 1984 May;98(5):1746–1756. doi: 10.1083/jcb.98.5.1746. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Grumet M., Edelman G. M. Neuron-glia cell adhesion molecule interacts with neurons and astroglia via different binding mechanisms. J Cell Biol. 1988 Feb;106(2):487–503. doi: 10.1083/jcb.106.2.487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Grumet M., Hoffman S., Chuong C. M., Edelman G. M. Polypeptide components and binding functions of neuron-glia cell adhesion molecules. Proc Natl Acad Sci U S A. 1984 Dec;81(24):7989–7993. doi: 10.1073/pnas.81.24.7989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Grumet M., Mauro V., Burgoon M. P., Edelman G. M., Cunningham B. A. Structure of a new nervous system glycoprotein, Nr-CAM, and its relationship to subgroups of neural cell adhesion molecules. J Cell Biol. 1991 Jun;113(6):1399–1412. doi: 10.1083/jcb.113.6.1399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Gubler U., Hoffman B. J. A simple and very efficient method for generating cDNA libraries. Gene. 1983 Nov;25(2-3):263–269. doi: 10.1016/0378-1119(83)90230-5. [DOI] [PubMed] [Google Scholar]
  30. Harrelson A. L., Goodman C. S. Growth cone guidance in insects: fasciclin II is a member of the immunoglobulin superfamily. Science. 1988 Nov 4;242(4879):700–708. doi: 10.1126/science.3187519. [DOI] [PubMed] [Google Scholar]
  31. Hortsch M., Bieber A. J. Sticky molecules in not-so-sticky cells. Trends Biochem Sci. 1991 Aug;16(8):283–287. doi: 10.1016/0968-0004(91)90116-d. [DOI] [PubMed] [Google Scholar]
  32. Huhtala P., Chow L. T., Tryggvason K. Structure of the human type IV collagenase gene. J Biol Chem. 1990 Jul 5;265(19):11077–11082. [PubMed] [Google Scholar]
  33. Inuzuka H., Miyatani S., Takeichi M. R-cadherin: a novel Ca(2+)-dependent cell-cell adhesion molecule expressed in the retina. Neuron. 1991 Jul;7(1):69–79. doi: 10.1016/0896-6273(91)90075-b. [DOI] [PubMed] [Google Scholar]
  34. Jessell T. M. Adhesion molecules and the hierarchy of neural development. Neuron. 1988 Mar;1(1):3–13. doi: 10.1016/0896-6273(88)90204-8. [DOI] [PubMed] [Google Scholar]
  35. Kadmon G., Kowitz A., Altevogt P., Schachner M. Functional cooperation between the neural adhesion molecules L1 and N-CAM is carbohydrate dependent. J Cell Biol. 1990 Jan;110(1):209–218. doi: 10.1083/jcb.110.1.209. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Kimizuka F., Ohdate Y., Kawase Y., Shimojo T., Taguchi Y., Hashino K., Goto S., Hashi H., Kato I., Sekiguchi K. Role of type III homology repeats in cell adhesive function within the cell-binding domain of fibronectin. J Biol Chem. 1991 Feb 15;266(5):3045–3051. [PubMed] [Google Scholar]
  37. Kobayashi M., Miura M., Asou H., Uyemura K. Molecular cloning of cell adhesion molecule L1 from human nervous tissue: a comparison of the primary sequences of L1 molecules of different origin. Biochim Biophys Acta. 1991 Oct 8;1090(2):238–240. doi: 10.1016/0167-4781(91)90108-x. [DOI] [PubMed] [Google Scholar]
  38. Komoriya A., Green L. J., Mervic M., Yamada S. S., Yamada K. M., Humphries M. J. The minimal essential sequence for a major cell type-specific adhesion site (CS1) within the alternatively spliced type III connecting segment domain of fibronectin is leucine-aspartic acid-valine. J Biol Chem. 1991 Aug 15;266(23):15075–15079. [PubMed] [Google Scholar]
  39. Kruse J., Mailhammer R., Wernecke H., Faissner A., Sommer I., Goridis C., Schachner M. Neural cell adhesion molecules and myelin-associated glycoprotein share a common carbohydrate moiety recognized by monoclonal antibodies L2 and HNK-1. Nature. 1984 Sep 13;311(5982):153–155. doi: 10.1038/311153a0. [DOI] [PubMed] [Google Scholar]
  40. Kuenzel E. A., Mulligan J. A., Sommercorn J., Krebs E. G. Substrate specificity determinants for casein kinase II as deduced from studies with synthetic peptides. J Biol Chem. 1987 Jul 5;262(19):9136–9140. [PubMed] [Google Scholar]
  41. Kyte J., Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. doi: 10.1016/0022-2836(82)90515-0. [DOI] [PubMed] [Google Scholar]
  42. Künemund V., Jungalwala F. B., Fischer G., Chou D. K., Keilhauer G., Schachner M. The L2/HNK-1 carbohydrate of neural cell adhesion molecules is involved in cell interactions. J Cell Biol. 1988 Jan;106(1):213–223. doi: 10.1083/jcb.106.1.213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  44. Lagenaur C., Lemmon V. An L1-like molecule, the 8D9 antigen, is a potent substrate for neurite extension. Proc Natl Acad Sci U S A. 1987 Nov;84(21):7753–7757. doi: 10.1073/pnas.84.21.7753. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Lee M. K., Lander A. D. Analysis of affinity and structural selectivity in the binding of proteins to glycosaminoglycans: development of a sensitive electrophoretic approach. Proc Natl Acad Sci U S A. 1991 Apr 1;88(7):2768–2772. doi: 10.1073/pnas.88.7.2768. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Lemmon V., Farr K. L., Lagenaur C. L1-mediated axon outgrowth occurs via a homophilic binding mechanism. Neuron. 1989 Jun;2(6):1597–1603. doi: 10.1016/0896-6273(89)90048-2. [DOI] [PubMed] [Google Scholar]
  47. Lemmon V., McLoon S. C. The appearance of an L1-like molecule in the chick primary visual pathway. J Neurosci. 1986 Oct;6(10):2987–2994. doi: 10.1523/JNEUROSCI.06-10-02987.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Matsudaira P. Sequence from picomole quantities of proteins electroblotted onto polyvinylidene difluoride membranes. J Biol Chem. 1987 Jul 25;262(21):10035–10038. [PubMed] [Google Scholar]
  49. Miura M., Kobayashi M., Asou H., Uyemura K. Molecular cloning of cDNA encoding the rat neural cell adhesion molecule L1. Two L1 isoforms in the cytoplasmic region are produced by differential splicing. FEBS Lett. 1991 Sep 2;289(1):91–95. doi: 10.1016/0014-5793(91)80915-p. [DOI] [PubMed] [Google Scholar]
  50. Moos M., Tacke R., Scherer H., Teplow D., Früh K., Schachner M. Neural adhesion molecule L1 as a member of the immunoglobulin superfamily with binding domains similar to fibronectin. Nature. 1988 Aug 25;334(6184):701–703. doi: 10.1038/334701a0. [DOI] [PubMed] [Google Scholar]
  51. Pearson W. R., Lipman D. J. Improved tools for biological sequence comparison. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2444–2448. doi: 10.1073/pnas.85.8.2444. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Prince J. T., Milona N., Stallcup W. B. Characterization of a partial cDNA clone for the NILE glycoprotein and identification of the encoded polypeptide domain. J Neurosci. 1989 Mar;9(3):876–883. doi: 10.1523/JNEUROSCI.09-03-00876.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Ranscht B. Sequence of contactin, a 130-kD glycoprotein concentrated in areas of interneuronal contact, defines a new member of the immunoglobulin supergene family in the nervous system. J Cell Biol. 1988 Oct;107(4):1561–1573. doi: 10.1083/jcb.107.4.1561. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Rathjen F. G., Wolff J. M., Frank R., Bonhoeffer F., Rutishauser U. Membrane glycoproteins involved in neurite fasciculation. J Cell Biol. 1987 Feb;104(2):343–353. doi: 10.1083/jcb.104.2.343. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Reichardt L. F., Tomaselli K. J. Extracellular matrix molecules and their receptors: functions in neural development. Annu Rev Neurosci. 1991;14:531–570. doi: 10.1146/annurev.ne.14.030191.002531. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Rice C. M., Strauss J. H. Nucleotide sequence of the 26S mRNA of Sindbis virus and deduced sequence of the encoded virus structural proteins. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2062–2066. doi: 10.1073/pnas.78.4.2062. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Sadoul K., Sadoul R., Faissner A., Schachner M. Biochemical characterization of different molecular forms of the neural cell adhesion molecule L1. J Neurochem. 1988 Feb;50(2):510–521. doi: 10.1111/j.1471-4159.1988.tb02941.x. [DOI] [PubMed] [Google Scholar]
  58. Sadoul R., Kirchhoff F., Schachner M. A protein kinase activity is associated with and specifically phosphorylates the neural cell adhesion molecule L1. J Neurochem. 1989 Nov;53(5):1471–1478. doi: 10.1111/j.1471-4159.1989.tb08540.x. [DOI] [PubMed] [Google Scholar]
  59. Salzer J. L., Colman D. R. Mechanisms of cell adhesion in the nervous system: role of the immunoglobulin gene superfamily. Dev Neurosci. 1989;11(6):377–390. doi: 10.1159/000111914. [DOI] [PubMed] [Google Scholar]
  60. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Santoni M. J., Barthels D., Barbas J. A., Hirsch M. R., Steinmetz M., Goridis C., Wille W. Analysis of cDNA clones that code for the transmembrane forms of the mouse neural cell adhesion molecule (NCAM) and are generated by alternative RNA splicing. Nucleic Acids Res. 1987 Nov 11;15(21):8621–8641. doi: 10.1093/nar/15.21.8621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Schuch U., Lohse M. J., Schachner M. Neural cell adhesion molecules influence second messenger systems. Neuron. 1989 Jul;3(1):13–20. doi: 10.1016/0896-6273(89)90111-6. [DOI] [PubMed] [Google Scholar]
  63. Siri A., Carnemolla B., Saginati M., Leprini A., Casari G., Baralle F., Zardi L. Human tenascin: primary structure, pre-mRNA splicing patterns and localization of the epitopes recognized by two monoclonal antibodies. Nucleic Acids Res. 1991 Feb 11;19(3):525–531. doi: 10.1093/nar/19.3.525. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Stallcup W. B., Beasley L. Involvement of the nerve growth factor-inducible large external glycoprotein (NILE) in neurite fasciculation in primary cultures of rat brain. Proc Natl Acad Sci U S A. 1985 Feb;82(4):1276–1280. doi: 10.1073/pnas.82.4.1276. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Strathmann M., Hamilton B. A., Mayeda C. A., Simon M. I., Meyerowitz E. M., Palazzolo M. J. Transposon-facilitated DNA sequencing. Proc Natl Acad Sci U S A. 1991 Feb 15;88(4):1247–1250. doi: 10.1073/pnas.88.4.1247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Takeichi M. Cadherin cell adhesion receptors as a morphogenetic regulator. Science. 1991 Mar 22;251(5000):1451–1455. doi: 10.1126/science.2006419. [DOI] [PubMed] [Google Scholar]
  67. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Updyke T. V., Nicolson G. L. Immunoaffinity isolation of membrane antigens with biotinylated monoclonal antibodies and immobilized streptavidin matrices. J Immunol Methods. 1984 Oct 12;73(1):83–95. doi: 10.1016/0022-1759(84)90034-6. [DOI] [PubMed] [Google Scholar]
  69. Weller A., Beck S., Ekblom P. Amino acid sequence of mouse tenascin and differential expression of two tenascin isoforms during embryogenesis. J Cell Biol. 1991 Jan;112(2):355–362. doi: 10.1083/jcb.112.2.355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Williams A. F., Barclay A. N. The immunoglobulin superfamily--domains for cell surface recognition. Annu Rev Immunol. 1988;6:381–405. doi: 10.1146/annurev.iy.06.040188.002121. [DOI] [PubMed] [Google Scholar]
  71. Young R. A., Davis R. W. Yeast RNA polymerase II genes: isolation with antibody probes. Science. 1983 Nov 18;222(4625):778–782. doi: 10.1126/science.6356359. [DOI] [PubMed] [Google Scholar]
  72. de la Rosa E. J., Kayyem J. F., Roman J. M., Stierhof Y. D., Dreyer W. J., Schwarz U. Topologically restricted appearance in the developing chick retinotectal system of Bravo, a neural surface protein: experimental modulation by environmental cues. J Cell Biol. 1990 Dec;111(6 Pt 2):3087–3096. doi: 10.1083/jcb.111.6.3087. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES