Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1993 Oct 2;123(2):443–454. doi: 10.1083/jcb.123.2.443

A myelin proteolipid protein-LacZ fusion protein is developmentally regulated and targeted to the myelin membrane in transgenic mice

PMCID: PMC2119842  PMID: 8408224

Abstract

Transgenic mice were generated with a fusion gene carrying a portion of the murine myelin proteolipid protein (PLP) gene, including the first intron, fused to the E. coli LacZ gene. Three transgenic lines were derived and all lines expressed the transgene in central nervous system white matter as measured by a histochemical assay for the detection of beta-galactosidase activity. PLP-LacZ transgene expression was regulated in both a spatial and temporal manner, consistent with endogenous PLP expression. Moreover, the transgene was expressed specifically in oligodendrocytes from primary mixed glial cultures prepared from transgenic mouse brains and appeared to be developmentally regulated in vitro as well. Transgene expression occurred in embryos, presumably in pre- or nonmyelinating cells, rather extensively throughout the peripheral nervous system and within very discrete regions of the central nervous system. Surprisingly, beta- galactosidase activity was localized predominantly in the myelin in these transgenic animals, suggesting that the NH2-terminal 13 amino acids of PLP, which were present in the PLP-LacZ gene product, were sufficient to target the protein to the myelin membrane. Thus, the first half of the PLP gene contains sequences sufficient to direct both spatial and temporal gene regulation and to encode amino acids important in targeting the protein to the myelin membrane.

Full Text

The Full Text of this article is available as a PDF (4.6 MB).

Selected References

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

  1. Agrawal H. C., Agrawal D. Proteolipid protein and DM-20 are synthesized by Schwann cells, present in myelin membrane, but they are not fatty acylated. Neurochem Res. 1991 Aug;16(8):855–858. doi: 10.1007/BF00965533. [DOI] [PubMed] [Google Scholar]
  2. Aronow B., Lattier D., Silbiger R., Dusing M., Hutton J., Jones G., Stock J., McNeish J., Potter S., Witte D. Evidence for a complex regulatory array in the first intron of the human adenosine deaminase gene. Genes Dev. 1989 Sep;3(9):1384–1400. doi: 10.1101/gad.3.9.1384. [DOI] [PubMed] [Google Scholar]
  3. Asotra K., Macklin W. B. Protein kinase C activity modulates myelin gene expression in enriched oligodendrocytes. J Neurosci Res. 1993 Apr 1;34(5):571–588. doi: 10.1002/jnr.490340509. [DOI] [PubMed] [Google Scholar]
  4. Banerji J., Olson L., Schaffner W. A lymphocyte-specific cellular enhancer is located downstream of the joining region in immunoglobulin heavy chain genes. Cell. 1983 Jul;33(3):729–740. doi: 10.1016/0092-8674(83)90015-6. [DOI] [PubMed] [Google Scholar]
  5. Berndt J. A., Kim J. G., Hudson L. D. Identification of cis-regulatory elements in the myelin proteolipid protein (PLP) gene. J Biol Chem. 1992 Jul 25;267(21):14730–14737. [PubMed] [Google Scholar]
  6. Bornstein P., McKay J., Morishima J. K., Devarayalu S., Gelinas R. E. Regulatory elements in the first intron contribute to transcriptional control of the human alpha 1(I) collagen gene. Proc Natl Acad Sci U S A. 1987 Dec;84(24):8869–8873. doi: 10.1073/pnas.84.24.8869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brinster R. L., Allen J. M., Behringer R. R., Gelinas R. E., Palmiter R. D. Introns increase transcriptional efficiency in transgenic mice. Proc Natl Acad Sci U S A. 1988 Feb;85(3):836–840. doi: 10.1073/pnas.85.3.836. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Brooks A. R., Blackhart B. D., Haubold K., Levy-Wilson B. Characterization of tissue-specific enhancer elements in the second intron of the human apolipoprotein B gene. J Biol Chem. 1991 Apr 25;266(12):7848–7859. [PubMed] [Google Scholar]
  9. Burbelo P. D., Bruggeman L. A., Gabriel G. C., Klotman P. E., Yamada Y. Characterization of a cis-acting element required for efficient transcriptional activation of the collagen IV enhancer. J Biol Chem. 1991 Nov 25;266(33):22297–22302. [PubMed] [Google Scholar]
  10. Campagnoni A. T., Macklin W. B. Cellular and molecular aspects of myelin protein gene expression. Mol Neurobiol. 1988 Spring;2(1):41–89. doi: 10.1007/BF02935632. [DOI] [PubMed] [Google Scholar]
  11. Campagnoni A. T. Molecular biology of myelin proteins from the central nervous system. J Neurochem. 1988 Jul;51(1):1–14. doi: 10.1111/j.1471-4159.1988.tb04827.x. [DOI] [PubMed] [Google Scholar]
  12. Campagnoni C. W., Garbay B., Micevych P., Pribyl T., Kampf K., Handley V. W., Campagnoni A. T. DM20 mRNA splice product of the myelin proteolipid protein gene is expressed in the murine heart. J Neurosci Res. 1992 Sep;33(1):148–155. doi: 10.1002/jnr.490330119. [DOI] [PubMed] [Google Scholar]
  13. Choi T., Huang M., Gorman C., Jaenisch R. A generic intron increases gene expression in transgenic mice. Mol Cell Biol. 1991 Jun;11(6):3070–3074. doi: 10.1128/mcb.11.6.3070. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  15. Colman D. R., Kreibich G., Frey A. B., Sabatini D. D. Synthesis and incorporation of myelin polypeptides into CNS myelin. J Cell Biol. 1982 Nov;95(2 Pt 1):598–608. doi: 10.1083/jcb.95.2.598. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Cook J. L., Irias-Donaghey S., Deininger P. L. Regulation of rodent myelin proteolipid protein gene expression. Neurosci Lett. 1992 Mar 16;137(1):56–60. doi: 10.1016/0304-3940(92)90297-k. [DOI] [PubMed] [Google Scholar]
  17. Diehl H. J., Schaich M., Budzinski R. M., Stoffel W. Individual exons encode the integral membrane domains of human myelin proteolipid protein. Proc Natl Acad Sci U S A. 1986 Dec;83(24):9807–9811. doi: 10.1073/pnas.83.24.9807. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Dubois-Dalcq M., Behar T., Hudson L., Lazzarini R. A. Emergence of three myelin proteins in oligodendrocytes cultured without neurons. J Cell Biol. 1986 Feb;102(2):384–392. doi: 10.1083/jcb.102.2.384. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Edmond J., Robbins R. A., Bergstrom J. D., Cole R. A., de Vellis J. Capacity for substrate utilization in oxidative metabolism by neurons, astrocytes, and oligodendrocytes from developing brain in primary culture. J Neurosci Res. 1987;18(4):551–561. doi: 10.1002/jnr.490180407. [DOI] [PubMed] [Google Scholar]
  20. Eng L. F., Chao F. C., Gerstl B., Pratt D., Tavaststjerna M. G. The maturation of human white matter myelin. Fractionation of the myelin membrane proteins. Biochemistry. 1968 Dec;7(12):4455–4465. doi: 10.1021/bi00852a042. [DOI] [PubMed] [Google Scholar]
  21. Franklin G. C., Donovan M., Adam G. I., Holmgren L., Pfeifer-Ohlsson S., Ohlsson R. Expression of the human PDGF-B gene is regulated by both positively and negatively acting cell type-specific regulatory elements located in the first intron. EMBO J. 1991 Jun;10(6):1365–1373. doi: 10.1002/j.1460-2075.1991.tb07656.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Gardinier M. V., Macklin W. B., Diniak A. J., Deininger P. L. Characterization of myelin proteolipid mRNAs in normal and jimpy mice. Mol Cell Biol. 1986 Nov;6(11):3755–3762. doi: 10.1128/mcb.6.11.3755. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Gardinier M. V., Macklin W. B. Myelin proteolipid protein gene expression in jimpy and jimpy(msd) mice. J Neurochem. 1988 Aug;51(2):360–369. doi: 10.1111/j.1471-4159.1988.tb01047.x. [DOI] [PubMed] [Google Scholar]
  24. Gillies S. D., Morrison S. L., Oi V. T., Tonegawa S. A tissue-specific transcription enhancer element is located in the major intron of a rearranged immunoglobulin heavy chain gene. Cell. 1983 Jul;33(3):717–728. doi: 10.1016/0092-8674(83)90014-4. [DOI] [PubMed] [Google Scholar]
  25. Gow A., Friedrich V. L., Jr, Lazzarini R. A. Myelin basic protein gene contains separate enhancers for oligodendrocyte and Schwann cell expression. J Cell Biol. 1992 Nov;119(3):605–616. doi: 10.1083/jcb.119.3.605. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Griffiths I. R., Mitchell L. S., McPhilemy K., Morrison S., Kyriakides E., Barrie J. A. Expression of myelin protein genes in Schwann cells. J Neurocytol. 1989 Jun;18(3):345–352. doi: 10.1007/BF01190837. [DOI] [PubMed] [Google Scholar]
  27. Gupta S. K., Pringle J., Poduslo J. F., Mezei C. Levels of proteolipid protein mRNAs in peripheral nerve are not under stringent axonal control. J Neurochem. 1991 May;56(5):1754–1762. doi: 10.1111/j.1471-4159.1991.tb02077.x. [DOI] [PubMed] [Google Scholar]
  28. Harpold M. M., Evans R. M., Salditt-Georgieff M., Darnell J. E. Production of mRNA in Chinese hamster cells: relationship of the rate of synthesis to the cytoplasmic concentration of nine specific mRNA sequences. Cell. 1979 Aug;17(4):1025–1035. doi: 10.1016/0092-8674(79)90341-6. [DOI] [PubMed] [Google Scholar]
  29. Horton W., Miyashita T., Kohno K., Hassell J. R., Yamada Y. Identification of a phenotype-specific enhancer in the first intron of the rat collagen II gene. Proc Natl Acad Sci U S A. 1987 Dec;84(24):8864–8868. doi: 10.1073/pnas.84.24.8864. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Hurt E. C., Pesold-Hurt B., Suda K., Oppliger W., Schatz G. The first twelve amino acids (less than half of the pre-sequence) of an imported mitochondrial protein can direct mouse cytosolic dihydrofolate reductase into the yeast mitochondrial matrix. EMBO J. 1985 Aug;4(8):2061–2068. doi: 10.1002/j.1460-2075.1985.tb03892.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Huxley A. F., Stämpfli R. Evidence for saltatory conduction in peripheral myelinated nerve fibres. J Physiol. 1949 May 15;108(3):315–339. [PMC free article] [PubMed] [Google Scholar]
  32. Ikenaka K., Fujino I., Morita N., Iwasaki Y., Miura M., Kagawa T., Nakahira K., Mikoshiba K. Reliable transient promoter assay using fluorescein-di-beta-D-galactopyranoside substrate. DNA Cell Biol. 1990 May;9(4):279–286. doi: 10.1089/dna.1990.9.279. [DOI] [PubMed] [Google Scholar]
  33. Ikenaka K., Furuichi T., Iwasaki Y., Moriguchi A., Okano H., Mikoshiba K. Myelin proteolipid protein gene structure and its regulation of expression in normal and jimpy mutant mice. J Mol Biol. 1988 Feb 20;199(4):587–596. doi: 10.1016/0022-2836(88)90303-8. [DOI] [PubMed] [Google Scholar]
  34. Ikenaka K., Kagawa T., Mikoshiba K. Selective expression of DM-20, an alternatively spliced myelin proteolipid protein gene product, in developing nervous system and in nonglial cells. J Neurochem. 1992 Jun;58(6):2248–2253. doi: 10.1111/j.1471-4159.1992.tb10970.x. [DOI] [PubMed] [Google Scholar]
  35. Kaiser C. A., Preuss D., Grisafi P., Botstein D. Many random sequences functionally replace the secretion signal sequence of yeast invertase. Science. 1987 Jan 16;235(4786):312–317. doi: 10.1126/science.3541205. [DOI] [PubMed] [Google Scholar]
  36. Kamholz J., Sessa M., Scherer S., Vogelbacker H., Mokuno K., Baron P., Wrabetz L., Shy M., Pleasure D. Structure and expression of proteolipid protein in the peripheral nervous system. J Neurosci Res. 1992 Feb;31(2):231–244. doi: 10.1002/jnr.490310204. [DOI] [PubMed] [Google Scholar]
  37. Kronquist K. E., Crandall B. F., Macklin W. B., Campagnoni A. T. Expression of myelin proteins in the developing human spinal cord: cloning and sequencing of human proteolipid protein cDNA. J Neurosci Res. 1987;18(3):395–401. doi: 10.1002/jnr.490180303. [DOI] [PubMed] [Google Scholar]
  38. LeVine S. M., Wong D., Macklin W. B. Developmental expression of proteolipid protein and DM20 mRNAs and proteins in the rat brain. Dev Neurosci. 1990;12(4-5):235–250. doi: 10.1159/000111853. [DOI] [PubMed] [Google Scholar]
  39. Letourneur F., Klausner R. D. A novel di-leucine motif and a tyrosine-based motif independently mediate lysosomal targeting and endocytosis of CD3 chains. Cell. 1992 Jun 26;69(7):1143–1157. doi: 10.1016/0092-8674(92)90636-q. [DOI] [PubMed] [Google Scholar]
  40. Lim K., Chae C. B. A simple assay for DNA transfection by incubation of the cells in culture dishes with substrates for beta-galactosidase. Biotechniques. 1989 Jun;7(6):576–579. [PubMed] [Google Scholar]
  41. Liu Y. C., Chapman E. R., Storm D. R. Targeting of neuromodulin (GAP-43) fusion proteins to growth cones in cultured rat embryonic neurons. Neuron. 1991 Mar;6(3):411–420. doi: 10.1016/0896-6273(91)90249-y. [DOI] [PubMed] [Google Scholar]
  42. Loewy A. D., Bridgman P. C., Mettenleiter T. C. beta-Galactosidase expressing recombinant pseudorabies virus for light and electron microscopic study of transneuronally labeled CNS neurons. Brain Res. 1991 Aug 2;555(2):346–352. doi: 10.1016/0006-8993(91)90364-2. [DOI] [PubMed] [Google Scholar]
  43. Lozano G., Levine A. J. Tissue-specific expression of p53 in transgenic mice is regulated by intron sequences. Mol Carcinog. 1991;4(1):3–9. doi: 10.1002/mc.2940040103. [DOI] [PubMed] [Google Scholar]
  44. Macklin W. B., Campagnoni C. W., Deininger P. L., Gardinier M. V. Structure and expression of the mouse myelin proteolipid protein gene. J Neurosci Res. 1987;18(3):383–394. doi: 10.1002/jnr.490180302. [DOI] [PubMed] [Google Scholar]
  45. Macklin W. B., Gardinier M. V., Obeso Z. O., King K. D., Wight P. A. Mutations in the myelin proteolipid protein gene alter oligodendrocyte gene expression in jimpy and jimpymsd mice. J Neurochem. 1991 Jan;56(1):163–171. doi: 10.1111/j.1471-4159.1991.tb02576.x. [DOI] [PubMed] [Google Scholar]
  46. Magram J., Niederreither K., Costantini F. Beta-globin enhancers target expression of a heterologous gene to erythroid tissues of transgenic mice. Mol Cell Biol. 1989 Oct;9(10):4581–4584. doi: 10.1128/mcb.9.10.4581. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Mattei M. G., Alliel P. M., Dautigny A., Passage E., Pham-Dinh D., Mattei J. F., Jollès P. The gene encoding for the major brain proteolipid (PLP) maps on the q-22 band of the human X chromosome. Hum Genet. 1986 Apr;72(4):352–353. doi: 10.1007/BF00290964. [DOI] [PubMed] [Google Scholar]
  48. Matter K., Hunziker W., Mellman I. Basolateral sorting of LDL receptor in MDCK cells: the cytoplasmic domain contains two tyrosine-dependent targeting determinants. Cell. 1992 Nov 27;71(5):741–753. doi: 10.1016/0092-8674(92)90551-m. [DOI] [PubMed] [Google Scholar]
  49. Mikoshiba K., Okano H., Tamura T., Ikenaka K. Structure and function of myelin protein genes. Annu Rev Neurosci. 1991;14:201–217. doi: 10.1146/annurev.ne.14.030191.001221. [DOI] [PubMed] [Google Scholar]
  50. Milner R. J., Lai C., Nave K. A., Lenoir D., Ogata J., Sutcliffe J. G. Nucleotide sequences of two mRNAs for rat brain myelin proteolipid protein. Cell. 1985 Oct;42(3):931–939. doi: 10.1016/0092-8674(85)90289-2. [DOI] [PubMed] [Google Scholar]
  51. Mitoma J., Ito A. The carboxy-terminal 10 amino acid residues of cytochrome b5 are necessary for its targeting to the endoplasmic reticulum. EMBO J. 1992 Nov;11(11):4197–4203. doi: 10.1002/j.1460-2075.1992.tb05513.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Nave K. A., Lai C., Bloom F. E., Milner R. J. Splice site selection in the proteolipid protein (PLP) gene transcript and primary structure of the DM-20 protein of central nervous system myelin. Proc Natl Acad Sci U S A. 1987 Aug;84(16):5665–5669. doi: 10.1073/pnas.84.16.5665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Nave K. A., Lemke G. Induction of the myelin proteolipid protein (PLP) gene in C6 glioblastoma cells: functional analysis of the PLP promotor. J Neurosci. 1991 Oct;11(10):3060–3069. doi: 10.1523/JNEUROSCI.11-10-03060.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Norton W. T., Poduslo S. E. Myelination in rat brain: changes in myelin composition during brain maturation. J Neurochem. 1973 Oct;21(4):759–773. doi: 10.1111/j.1471-4159.1973.tb07520.x. [DOI] [PubMed] [Google Scholar]
  55. Palmiter R. D., Sandgren E. P., Avarbock M. R., Allen D. D., Brinster R. L. Heterologous introns can enhance expression of transgenes in mice. Proc Natl Acad Sci U S A. 1991 Jan 15;88(2):478–482. doi: 10.1073/pnas.88.2.478. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Pellman D., Garber E. A., Cross F. R., Hanafusa H. An N-terminal peptide from p60src can direct myristylation and plasma membrane localization when fused to heterologous proteins. 1985 Mar 28-Apr 3Nature. 314(6009):374–377. doi: 10.1038/314374a0. [DOI] [PubMed] [Google Scholar]
  57. Pham-Dinh D., Birling M. C., Roussel G., Dautigny A., Nussbaum J. L. Proteolipid DM-20 predominates over PLP in peripheral nervous system. Neuroreport. 1991 Feb;2(2):89–92. doi: 10.1097/00001756-199102000-00006. [DOI] [PubMed] [Google Scholar]
  58. Picard D., Schaffner W. A lymphocyte-specific enhancer in the mouse immunoglobulin kappa gene. Nature. 1984 Jan 5;307(5946):80–82. doi: 10.1038/307080a0. [DOI] [PubMed] [Google Scholar]
  59. Pierce J. W., Gifford A. M., Baltimore D. Silencing of the expression of the immunoglobulin kappa gene in non-B cells. Mol Cell Biol. 1991 Mar;11(3):1431–1437. doi: 10.1128/mcb.11.3.1431. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Puckett C., Hudson L., Ono K., Friedrich V., Benecke J., Dubois-Dalcq M., Lazzarini R. A. Myelin-specific proteolipid protein is expressed in myelinating Schwann cells but is not incorporated into myelin sheaths. J Neurosci Res. 1987;18(4):511–518. doi: 10.1002/jnr.490180402. [DOI] [PubMed] [Google Scholar]
  61. Queen C., Baltimore D. Immunoglobulin gene transcription is activated by downstream sequence elements. Cell. 1983 Jul;33(3):741–748. doi: 10.1016/0092-8674(83)90016-8. [DOI] [PubMed] [Google Scholar]
  62. Raff M. C., Miller R. H., Noble M. A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium. Nature. 1983 Jun 2;303(5916):390–396. doi: 10.1038/303390a0. [DOI] [PubMed] [Google Scholar]
  63. Ranscht B., Clapshaw P. A., Price J., Noble M., Seifert W. Development of oligodendrocytes and Schwann cells studied with a monoclonal antibody against galactocerebroside. Proc Natl Acad Sci U S A. 1982 Apr;79(8):2709–2713. doi: 10.1073/pnas.79.8.2709. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Readhead C., Popko B., Takahashi N., Shine H. D., Saavedra R. A., Sidman R. L., Hood L. Expression of a myelin basic protein gene in transgenic shiverer mice: correction of the dysmyelinating phenotype. Cell. 1987 Feb 27;48(4):703–712. doi: 10.1016/0092-8674(87)90248-0. [DOI] [PubMed] [Google Scholar]
  65. Sanes J. R., Rubenstein J. L., Nicolas J. F. Use of a recombinant retrovirus to study post-implantation cell lineage in mouse embryos. EMBO J. 1986 Dec 1;5(12):3133–3142. doi: 10.1002/j.1460-2075.1986.tb04620.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Sarkar S., Cowan N. J. Intragenic sequences affect the expression of the gene encoding glial fibrillary acidic protein. J Neurochem. 1991 Aug;57(2):675–684. doi: 10.1111/j.1471-4159.1991.tb03799.x. [DOI] [PubMed] [Google Scholar]
  67. Schindler P., Luu B., Sorokine O., Trifilieff E., Van Dorsselaer A. Developmental study of proteolipids in bovine brain: a novel proteolipid and DM-20 appear before proteolipid protein (PLP) during myelination. J Neurochem. 1990 Dec;55(6):2079–2085. doi: 10.1111/j.1471-4159.1990.tb05798.x. [DOI] [PubMed] [Google Scholar]
  68. Simons R., Alon N., Riordan J. R. Human myelin DM-20 proteolipid protein deletion defined by cDNA sequence. Biochem Biophys Res Commun. 1987 Jul 31;146(2):666–671. doi: 10.1016/0006-291x(87)90580-8. [DOI] [PubMed] [Google Scholar]
  69. Stahl N., Harry J., Popko B. Quantitative analysis of myelin protein gene expression during development in the rat sciatic nerve. Brain Res Mol Brain Res. 1990 Aug;8(3):209–212. doi: 10.1016/0169-328x(90)90018-9. [DOI] [PubMed] [Google Scholar]
  70. Timsit S. G., Bally-Cuif L., Colman D. R., Zalc B. DM-20 mRNA is expressed during the embryonic development of the nervous system of the mouse. J Neurochem. 1992 Mar;58(3):1172–1175. doi: 10.1111/j.1471-4159.1992.tb09378.x. [DOI] [PubMed] [Google Scholar]
  71. Timsit S., Sinoway M. P., Levy L., Allinquant B., Stempak J., Staugaitis S. M., Colman D. R. The DM20 protein of myelin: intracellular and surface expression patterns in transfectants. J Neurochem. 1992 May;58(5):1936–1942. doi: 10.1111/j.1471-4159.1992.tb10072.x. [DOI] [PubMed] [Google Scholar]
  72. Verrall S., Hall Z. W. The N-terminal domains of acetylcholine receptor subunits contain recognition signals for the initial steps of receptor assembly. Cell. 1992 Jan 10;68(1):23–31. doi: 10.1016/0092-8674(92)90203-o. [DOI] [PubMed] [Google Scholar]
  73. Vidal M., Morris R., Grosveld F., Spanopoulou E. Tissue-specific control elements of the Thy-1 gene. EMBO J. 1990 Mar;9(3):833–840. doi: 10.1002/j.1460-2075.1990.tb08180.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Weimbs T., Stoffel W. Proteolipid protein (PLP) of CNS myelin: positions of free, disulfide-bonded, and fatty acid thioester-linked cysteine residues and implications for the membrane topology of PLP. Biochemistry. 1992 Dec 15;31(49):12289–12296. doi: 10.1021/bi00164a002. [DOI] [PubMed] [Google Scholar]
  75. Willard H. F., Riordan J. R. Assignment of the gene for myelin proteolipid protein to the X chromosome: implications for X-linked myelin disorders. Science. 1985 Nov 22;230(4728):940–942. doi: 10.1126/science.3840606. [DOI] [PubMed] [Google Scholar]
  76. Zuber M. X., Strittmatter S. M., Fishman M. C. A membrane-targeting signal in the amino terminus of the neuronal protein GAP-43. Nature. 1989 Sep 28;341(6240):345–348. doi: 10.1038/341345a0. [DOI] [PubMed] [Google Scholar]

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

RESOURCES