Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1995 Feb 1;128(3):415–431. doi: 10.1083/jcb.128.3.415

LAR tyrosine phosphatase receptor: alternative splicing is preferential to the nervous system, coordinated with cell growth and generates novel isoforms containing extensive CAG repeats

PMCID: PMC2120354  PMID: 7844155

Abstract

Receptor-linked tyrosine phosphatases regulate cell growth by dephosphorylating proteins involved in tyrosine kinase signal transduction. The leukocyte common antigen-related (LAR) tyrosine phosphatase receptor has sequence similarity to the neural cell adhesion molecule N-CAM and is located in a chromosomal region (1p32- 33) frequently altered in neuroectodermal tumors. To understand the function of receptor-linked tyrosine phosphatases in neural development, we sought to identify LAR isoforms preferentially expressed in the nervous system and cellular processes regulating LAR alternative splicing. We report here the isolation of a series of rat LAR cDNA clones arising from complex combinatorial alternative splicing, not previously demonstrated for the tyrosine phosphatase- receptor gene family in general. Isoforms included: (a) deletions of the fourth, sixth and seventh fibronectin type III-like domains; (b) an alternatively spliced novel cassette exon in the fifth fibronectin type III-like domain; (c) two alternatively spliced novel cassette exons in the juxtamembrane region; (d) a retained intron in the extracellular region with in-frame stop codons predicting a secreted LAR isoform; and (e) an LAR transcript including an alternative 3' untranslated region containing multiple stretches of tandem CAG repeats up to 21 repeats in length. This number of repeats was in the range found in normal alleles of genes in which expansions of repeats are associated with neurodegenerative disease and the genetic phenomenon of anticipation. RT-PCR and Northern analysis demonstrated that LAR alternative splicing occurred preferentially in neuromuscular tissue in vivo and in neurons compared to astrocytes in vitro and was developmentally regulated. Alternative splicing was also regulated in PC12 cells by NGF, in 3T3 fibroblasts by cell confluence and in sciatic nerve and muscle subsequent to nerve transection. Western blot analysis demonstrated that alternatively spliced cassette exons result in the presence of corresponding amino acid segments of LAR protein in vivo. These studies suggest specialized functions of LAR isoforms in the nervous system and support our hypothesis that LAR-like tyrosine phosphatase receptors play a role in neural development and regeneration.

Full Text

The Full Text of this article is available as a PDF (3.3 MB).

Selected References

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

  1. Andrew S. E., Goldberg Y. P., Kremer B., Telenius H., Theilmann J., Adam S., Starr E., Squitieri F., Lin B., Kalchman M. A. The relationship between trinucleotide (CAG) repeat length and clinical features of Huntington's disease. Nat Genet. 1993 Aug;4(4):398–403. doi: 10.1038/ng0893-398. [DOI] [PubMed] [Google Scholar]
  2. Bauskin A. R., Alkalay I., Ben-Neriah Y. Redox regulation of a protein tyrosine kinase in the endoplasmic reticulum. Cell. 1991 Aug 23;66(4):685–696. doi: 10.1016/0092-8674(91)90114-e. [DOI] [PubMed] [Google Scholar]
  3. Brady-Kalnay S. M., Flint A. J., Tonks N. K. Homophilic binding of PTP mu, a receptor-type protein tyrosine phosphatase, can mediate cell-cell aggregation. J Cell Biol. 1993 Aug;122(4):961–972. doi: 10.1083/jcb.122.4.961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chao M. V. Neurotrophin receptors: a window into neuronal differentiation. Neuron. 1992 Oct;9(4):583–593. doi: 10.1016/0896-6273(92)90023-7. [DOI] [PubMed] [Google Scholar]
  5. Charbonneau H., Tonks N. K. 1002 protein phosphatases? Annu Rev Cell Biol. 1992;8:463–493. doi: 10.1146/annurev.cb.08.110192.002335. [DOI] [PubMed] [Google Scholar]
  6. Charbonneau H., Tonks N. K., Walsh K. A., Fischer E. H. The leukocyte common antigen (CD45): a putative receptor-linked protein tyrosine phosphatase. Proc Natl Acad Sci U S A. 1988 Oct;85(19):7182–7186. doi: 10.1073/pnas.85.19.7182. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cross M., Dexter T. M. Growth factors in development, transformation, and tumorigenesis. Cell. 1991 Jan 25;64(2):271–280. doi: 10.1016/0092-8674(91)90638-f. [DOI] [PubMed] [Google Scholar]
  8. Danielson P. E., Forss-Petter S., Brow M. A., Calavetta L., Douglass J., Milner R. J., Sutcliffe J. G. p1B15: a cDNA clone of the rat mRNA encoding cyclophilin. DNA. 1988 May;7(4):261–267. doi: 10.1089/dna.1988.7.261. [DOI] [PubMed] [Google Scholar]
  9. Dianzani U., Redoglia V., Malavasi F., Bragardo M., Pileri A., Janeway C. A., Jr, Bottomly K. Isoform-specific associations of CD45 with accessory molecules in human T lymphocytes. Eur J Immunol. 1992 Feb;22(2):365–371. doi: 10.1002/eji.1830220212. [DOI] [PubMed] [Google Scholar]
  10. Doherty P., Moolenaar C. E., Ashton S. V., Michalides R. J., Walsh F. S. The VASE exon downregulates the neurite growth-promoting activity of NCAM 140. Nature. 1992 Apr 30;356(6372):791–793. doi: 10.1038/356791a0. [DOI] [PubMed] [Google Scholar]
  11. Doherty P., Walsh F. S. Signal transduction events underlying neurite outgrowth stimulated by cell adhesion molecules. Curr Opin Neurobiol. 1994 Feb;4(1):49–55. doi: 10.1016/0959-4388(94)90031-0. [DOI] [PubMed] [Google Scholar]
  12. Edelman G. M., Crossin K. L. Cell adhesion molecules: implications for a molecular histology. Annu Rev Biochem. 1991;60:155–190. doi: 10.1146/annurev.bi.60.070191.001103. [DOI] [PubMed] [Google Scholar]
  13. Fischer E. H., Charbonneau H., Tonks N. K. Protein tyrosine phosphatases: a diverse family of intracellular and transmembrane enzymes. Science. 1991 Jul 26;253(5018):401–406. doi: 10.1126/science.1650499. [DOI] [PubMed] [Google Scholar]
  14. Foley K. P., Leonard M. W., Engel J. D. Quantitation of RNA using the polymerase chain reaction. Trends Genet. 1993 Nov;9(11):380–385. doi: 10.1016/0168-9525(93)90137-7. [DOI] [PubMed] [Google Scholar]
  15. Frei T., von Bohlen und Halbach F., Wille W., Schachner M. Different extracellular domains of the neural cell adhesion molecule (N-CAM) are involved in different functions. J Cell Biol. 1992 Jul;118(1):177–194. doi: 10.1083/jcb.118.1.177. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gebbink M. F., Zondag G. C., Wubbolts R. W., Beijersbergen R. L., van Etten I., Moolenaar W. H. Cell-cell adhesion mediated by a receptor-like protein tyrosine phosphatase. J Biol Chem. 1993 Aug 5;268(22):16101–16104. [PubMed] [Google Scholar]
  17. Gebbink M. F., van Etten I., Hateboer G., Suijkerbuijk R., Beijersbergen R. L., Geurts van Kessel A., Moolenaar W. H. Cloning, expression and chromosomal localization of a new putative receptor-like protein tyrosine phosphatase. FEBS Lett. 1991 Sep 23;290(1-2):123–130. doi: 10.1016/0014-5793(91)81241-y. [DOI] [PubMed] [Google Scholar]
  18. Genuardi M., Tsihira H., Anderson D. E., Saunders G. F. Distal deletion of chromosome Ip in ductal carcinoma of the breast. Am J Hum Genet. 1989 Jul;45(1):73–82. [PMC free article] [PubMed] [Google Scholar]
  19. Gilliland G., Perrin S., Blanchard K., Bunn H. F. Analysis of cytokine mRNA and DNA: detection and quantitation by competitive polymerase chain reaction. Proc Natl Acad Sci U S A. 1990 Apr;87(7):2725–2729. doi: 10.1073/pnas.87.7.2725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Goldberg Y. P., Andrew S. E., Clarke L. A., Hayden M. R. A PCR method for accurate assessment of trinucleotide repeat expansion in Huntington disease. Hum Mol Genet. 1993 Jun;2(6):635–636. doi: 10.1093/hmg/2.6.635. [DOI] [PubMed] [Google Scholar]
  21. Gower H. J., Barton C. H., Elsom V. L., Thompson J., Moore S. E., Dickson G., Walsh F. S. Alternative splicing generates a secreted form of N-CAM in muscle and brain. Cell. 1988 Dec 23;55(6):955–964. doi: 10.1016/0092-8674(88)90241-3. [DOI] [PubMed] [Google Scholar]
  22. Ignelzi M. A., Jr, Miller D. R., Soriano P., Maness P. F. Impaired neurite outgrowth of src-minus cerebellar neurons on the cell adhesion molecule L1. Neuron. 1994 Apr;12(4):873–884. doi: 10.1016/0896-6273(94)90339-5. [DOI] [PubMed] [Google Scholar]
  23. Ip N. Y., Ibáez C. F., Nye S. H., McClain J., Jones P. F., Gies D. R., Belluscio L., Le Beau M. M., Espinosa R., 3rd, Squinto S. P. Mammalian neurotrophin-4: structure, chromosomal localization, tissue distribution, and receptor specificity. Proc Natl Acad Sci U S A. 1992 Apr 1;89(7):3060–3064. doi: 10.1073/pnas.89.7.3060. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Jansen G., Mahadevan M., Amemiya C., Wormskamp N., Segers B., Hendriks W., O'Hoy K., Baird S., Sabourin L., Lennon G. Characterization of the myotonic dystrophy region predicts multiple protein isoform-encoding mRNAs. Nat Genet. 1992 Jul;1(4):261–266. doi: 10.1038/ng0792-261. [DOI] [PubMed] [Google Scholar]
  25. Jiang Y. P., Wang H., D'Eustachio P., Musacchio J. M., Schlessinger J., Sap J. Cloning and characterization of R-PTP-kappa, a new member of the receptor protein tyrosine phosphatase family with a proteolytically cleaved cellular adhesion molecule-like extracellular region. Mol Cell Biol. 1993 May;13(5):2942–2951. doi: 10.1128/mcb.13.5.2942. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Jirik F. R., Harder K. W., Melhado I. G., Anderson L. L., Duncan A. M. The gene for leukocyte antigen-related tyrosine phosphatase (LAR) is localized to human chromosome 1p32, a region frequently deleted in tumors of neuroectodermal origin. Cytogenet Cell Genet. 1992;61(4):266–268. doi: 10.1159/000133418. [DOI] [PubMed] [Google Scholar]
  27. Kimmel D. W., O'Fallon J. R., Scheithauer B. W., Kelly P. J., Dewald G. W., Jenkins R. B. Prognostic value of cytogenetic analysis in human cerebral astrocytomas. Ann Neurol. 1992 May;31(5):534–542. doi: 10.1002/ana.410310512. [DOI] [PubMed] [Google Scholar]
  28. Krueger N. X., Streuli M., Saito H. Structural diversity and evolution of human receptor-like protein tyrosine phosphatases. EMBO J. 1990 Oct;9(10):3241–3252. doi: 10.1002/j.1460-2075.1990.tb07523.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Li S. H., McInnis M. G., Margolis R. L., Antonarakis S. E., Ross C. A. Novel triplet repeat containing genes in human brain: cloning, expression, and length polymorphisms. Genomics. 1993 Jun;16(3):572–579. doi: 10.1006/geno.1993.1232. [DOI] [PubMed] [Google Scholar]
  30. Longo F. M., Martignetti J. A., Le Beau J. M., Zhang J. S., Barnes J. P., Brosius J. Leukocyte common antigen-related receptor-linked tyrosine phosphatase. Regulation of mRNA expression. J Biol Chem. 1993 Dec 15;268(35):26503–26511. [PubMed] [Google Scholar]
  31. Luna E. J., Hitt A. L. Cytoskeleton--plasma membrane interactions. Science. 1992 Nov 6;258(5084):955–964. doi: 10.1126/science.1439807. [DOI] [PubMed] [Google Scholar]
  32. Magal E., Burnham P., Varon S. Effect of CNTF on low-affinity NGF receptor expression by cultured neurons from different rat brain regions. J Neurosci Res. 1991 Nov;30(3):560–566. doi: 10.1002/jnr.490300314. [DOI] [PubMed] [Google Scholar]
  33. Maher P. A. Activation of phosphotyrosine phosphatase activity by reduction of cell-substrate adhesion. Proc Natl Acad Sci U S A. 1993 Dec 1;90(23):11177–11181. doi: 10.1073/pnas.90.23.11177. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Martin J. B. Molecular genetics of neurological diseases. Science. 1993 Oct 29;262(5134):674–676. doi: 10.1126/science.8235586. [DOI] [PubMed] [Google Scholar]
  35. Mathew C. G., Smith B. A., Thorpe K., Wong Z., Royle N. J., Jeffreys A. J., Ponder B. A. Deletion of genes on chromosome 1 in endocrine neoplasia. Nature. 1987 Aug 6;328(6130):524–526. doi: 10.1038/328524a0. [DOI] [PubMed] [Google Scholar]
  36. Matten W. T., Aubry M., West J., Maness P. F. Tubulin is phosphorylated at tyrosine by pp60c-src in nerve growth cone membranes. J Cell Biol. 1990 Nov;111(5 Pt 1):1959–1970. doi: 10.1083/jcb.111.5.1959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Michie C. A., McLean A., Alcock C., Beverley P. C. Lifespan of human lymphocyte subsets defined by CD45 isoforms. Nature. 1992 Nov 19;360(6401):264–265. doi: 10.1038/360264a0. [DOI] [PubMed] [Google Scholar]
  38. Mizuno K., Hasegawa K., Katagiri T., Ogimoto M., Ichikawa T., Yakura H. MPTP delta, a putative murine homolog of HPTP delta, is expressed in specialized regions of the brain and in the B-cell lineage. Mol Cell Biol. 1993 Sep;13(9):5513–5523. doi: 10.1128/mcb.13.9.5513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Mobley W. C., Rutkowski J. L., Tennekoon G. I., Gemski J., Buchanan K., Johnston M. V. Nerve growth factor increases choline acetyltransferase activity in developing basal forebrain neurons. Brain Res. 1986 Jul;387(1):53–62. doi: 10.1016/0169-328x(86)90020-3. [DOI] [PubMed] [Google Scholar]
  40. Moley J. F., Brother M. B., Fong C. T., White P. S., Baylin S. B., Nelkin B., Wells S. A., Brodeur G. M. Consistent association of 1p loss of heterozygosity with pheochromocytomas from patients with multiple endocrine neoplasia type 2 syndromes. Cancer Res. 1992 Feb 15;52(4):770–774. [PubMed] [Google Scholar]
  41. Nieke J., Schachner M. Expression of the neural cell adhesion molecules L1 and N-CAM and their common carbohydrate epitope L2/HNK-1 during development and after transection of the mouse sciatic nerve. Differentiation. 1985;30(2):141–151. doi: 10.1111/j.1432-0436.1985.tb00525.x. [DOI] [PubMed] [Google Scholar]
  42. O'Grady P., Krueger N. X., Streuli M., Saito H. Genomic organization of the human LAR protein tyrosine phosphatase gene and alternative splicing in the extracellular fibronectin type-III domains. J Biol Chem. 1994 Oct 7;269(40):25193–25199. [PubMed] [Google Scholar]
  43. Pallen C. J., Tong P. H. Elevation of membrane tyrosine phosphatase activity in density-dependent growth-arrested fibroblasts. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):6996–7000. doi: 10.1073/pnas.88.16.6996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Pan M. G., Rim C., Lu K. P., Florio T., Stork P. J. Cloning and expression of two structurally distinct receptor-linked protein-tyrosine phosphatases generated by RNA processing from a single gene. J Biol Chem. 1993 Sep 15;268(26):19284–19291. [PubMed] [Google Scholar]
  45. Patthy L. Homology of a domain of the growth hormone/prolactin receptor family with type III modules of fibronectin. Cell. 1990 Apr 6;61(1):13–14. doi: 10.1016/0092-8674(90)90208-v. [DOI] [PubMed] [Google Scholar]
  46. Penninger J. M., Wallace V. A., Kishihara K., Mak T. W. The role of p56lck and p59fyn tyrosine kinases and CD45 protein tyrosine phosphatase in T-cell development and clonal selection. Immunol Rev. 1993 Oct;135:183–214. doi: 10.1111/j.1600-065x.1993.tb00649.x. [DOI] [PubMed] [Google Scholar]
  47. Pot D. A., Woodford T. A., Remboutsika E., Haun R. S., Dixon J. E. Cloning, bacterial expression, purification, and characterization of the cytoplasmic domain of rat LAR, a receptor-like protein tyrosine phosphatase. J Biol Chem. 1991 Oct 15;266(29):19688–19696. [PubMed] [Google Scholar]
  48. 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]
  49. Richards R. I., Sutherland G. R. Dynamic mutations: a new class of mutations causing human disease. Cell. 1992 Sep 4;70(5):709–712. doi: 10.1016/0092-8674(92)90302-s. [DOI] [PubMed] [Google Scholar]
  50. Richards R. I., Sutherland G. R. Simple repeat DNA is not replicated simply. Nat Genet. 1994 Feb;6(2):114–116. doi: 10.1038/ng0294-114. [DOI] [PubMed] [Google Scholar]
  51. Riggins G. J., Lokey L. K., Chastain J. L., Leiner H. A., Sherman S. L., Wilkinson K. D., Warren S. T. Human genes containing polymorphic trinucleotide repeats. Nat Genet. 1992 Nov;2(3):186–191. doi: 10.1038/ng1192-186. [DOI] [PubMed] [Google Scholar]
  52. Ritke M. K., Shah R., Valentine M., Douglass E. C., Tereba A. Molecular analysis of chromosome 1 abnormalities in neuroblastoma. Cytogenet Cell Genet. 1989;50(2-3):84–90. doi: 10.1159/000132729. [DOI] [PubMed] [Google Scholar]
  53. Rutishauser U. Adhesion molecules of the nervous system. Curr Opin Neurobiol. 1993 Oct;3(5):709–715. doi: 10.1016/0959-4388(93)90142-l. [DOI] [PubMed] [Google Scholar]
  54. Sahin M., Hockfield S. Protein tyrosine phosphatases expressed in the developing rat brain. J Neurosci. 1993 Nov;13(11):4968–4978. doi: 10.1523/JNEUROSCI.13-11-04968.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Sap J., Jiang Y. P., Friedlander D., Grumet M., Schlessinger J. Receptor tyrosine phosphatase R-PTP-kappa mediates homophilic binding. Mol Cell Biol. 1994 Jan;14(1):1–9. doi: 10.1128/mcb.14.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Satterwhite L. L., Lohka M. J., Wilson K. L., Scherson T. Y., Cisek L. J., Corden J. L., Pollard T. D. Phosphorylation of myosin-II regulatory light chain by cyclin-p34cdc2: a mechanism for the timing of cytokinesis. J Cell Biol. 1992 Aug;118(3):595–605. doi: 10.1083/jcb.118.3.595. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Schraven B., Samstag Y., Altevogt P., Meuer S. C. Association of CD2 and CD45 on human T lymphocytes. Nature. 1990 May 3;345(6270):71–74. doi: 10.1038/345071a0. [DOI] [PubMed] [Google Scholar]
  58. Schubert D., Heinemann S., Kidokoro Y. Cholinergic metabolism and synapse formation by a rat nerve cell line. Proc Natl Acad Sci U S A. 1977 Jun;74(6):2579–2583. doi: 10.1073/pnas.74.6.2579. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Small S. J., Akeson R. Expression of the unique NCAM VASE exon is independently regulated in distinct tissues during development. J Cell Biol. 1990 Nov;111(5 Pt 1):2089–2096. doi: 10.1083/jcb.111.5.2089. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Smith C. W., Patton J. G., Nadal-Ginard B. Alternative splicing in the control of gene expression. Annu Rev Genet. 1989;23:527–577. doi: 10.1146/annurev.ge.23.120189.002523. [DOI] [PubMed] [Google Scholar]
  61. Streuli M., Krueger N. X., Ariniello P. D., Tang M., Munro J. M., Blattler W. A., Adler D. A., Disteche C. M., Saito H. Expression of the receptor-linked protein tyrosine phosphatase LAR: proteolytic cleavage and shedding of the CAM-like extracellular region. EMBO J. 1992 Mar;11(3):897–907. doi: 10.1002/j.1460-2075.1992.tb05128.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Streuli M., Krueger N. X., Hall L. R., Schlossman S. F., Saito H. A new member of the immunoglobulin superfamily that has a cytoplasmic region homologous to the leukocyte common antigen. J Exp Med. 1988 Nov 1;168(5):1523–1530. doi: 10.1084/jem.168.5.1523. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Tian S. S., Tsoulfas P., Zinn K. Three receptor-linked protein-tyrosine phosphatases are selectively expressed on central nervous system axons in the Drosophila embryo. Cell. 1991 Nov 15;67(4):675–685. doi: 10.1016/0092-8674(91)90063-5. [DOI] [PubMed] [Google Scholar]
  64. Vogel W., Lammers R., Huang J., Ullrich A. Activation of a phosphotyrosine phosphatase by tyrosine phosphorylation. Science. 1993 Mar 12;259(5101):1611–1614. doi: 10.1126/science.7681217. [DOI] [PubMed] [Google Scholar]
  65. Walton K. M., Dixon J. E. Protein tyrosine phosphatases. Annu Rev Biochem. 1993;62:101–120. doi: 10.1146/annurev.bi.62.070193.000533. [DOI] [PubMed] [Google Scholar]
  66. Walton K. M., Martell K. J., Kwak S. P., Dixon J. E., Largent B. L. A novel receptor-type protein tyrosine phosphatase is expressed during neurogenesis in the olfactory neuroepithelium. Neuron. 1993 Aug;11(2):387–400. doi: 10.1016/0896-6273(93)90193-u. [DOI] [PubMed] [Google Scholar]
  67. Wang A. M., Doyle M. V., Mark D. F. Quantitation of mRNA by the polymerase chain reaction. Proc Natl Acad Sci U S A. 1989 Dec;86(24):9717–9721. doi: 10.1073/pnas.86.24.9717. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Yan H., Grossman A., Wang H., D'Eustachio P., Mossie K., Musacchio J. M., Silvennoinen O., Schlessinger J. A novel receptor tyrosine phosphatase-sigma that is highly expressed in the nervous system. J Biol Chem. 1993 Nov 25;268(33):24880–24886. [PubMed] [Google Scholar]
  69. Yu Q., Lenardo T., Weinberg R. A. The N-terminal and C-terminal domains of a receptor tyrosine phosphatase are associated by non-covalent linkage. Oncogene. 1992 Jun;7(6):1051–1057. [PubMed] [Google Scholar]
  70. Zhang W. R., Goldstein B. J. Identification of skeletal muscle protein-tyrosine phosphatases by amplification of conserved cDNA sequences. Biochem Biophys Res Commun. 1991 Aug 15;178(3):1291–1297. doi: 10.1016/0006-291x(91)91034-a. [DOI] [PubMed] [Google Scholar]
  71. Zheng C. J., Byers B., Moolgavkar S. H. Allelic instability in mitosis: a unified model for dominant disorders. Proc Natl Acad Sci U S A. 1993 Nov 1;90(21):10178–10182. doi: 10.1073/pnas.90.21.10178. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Zisch A. H., D'Alessandri L., Ranscht B., Falchetto R., Winterhalter K. H., Vaughan L. Neuronal cell adhesion molecule contactin/F11 binds to tenascin via its immunoglobulin-like domains. J Cell Biol. 1992 Oct;119(1):203–213. doi: 10.1083/jcb.119.1.203. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES