Skip to main content
Biochemical Journal logoLink to Biochemical Journal
. 1995 Jan 15;305(Pt 2):499–504. doi: 10.1042/bj3050499

A novel receptor-type protein tyrosine phosphatase with a single catalytic domain is specifically expressed in mouse brain.

W Hendriks 1, J Schepens 1, C Brugman 1, P Zeeuwen 1, B Wieringa 1
PMCID: PMC1136390  PMID: 7832766

Abstract

Protein tyrosine phosphatases (PTPases) are important regulatory proteins that, together with protein tyrosine kinases, determine the phosphotyrosine levels in cell signalling proteins. By PCR amplification of mouse brain cDNA fragments encoding the catalytic domains of these enzymes, we identified three novel members of the PTPase gene family. Northern-blot analysis showed that two of these novel clones represent brain-specific PTPases, whereas the third originates from a large-sized mRNA that is more ubiquitously expressed. A full-length cDNA encoding one of the brain-specific PTPases, PTP-SL, was isolated. Sequence analysis revealed a transmembrane PTPase containing a single catalytic phosphatase domain that has 45% homology to a rat cytoplasmic brain-specific PTPase named STEP. This suggests a role for PTP-SL in cell-cell signalling processes in the brain.

Full text

PDF
503

Images in this article

Selected References

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

  1. Adachi M., Sekiya M., Arimura Y., Takekawa M., Itoh F., Hinoda Y., Imai K., Yachi A. Protein-tyrosine phosphatase expression in pre-B cell NALM-6. Cancer Res. 1992 Feb 1;52(3):737–740. [PubMed] [Google Scholar]
  2. Auffray C., Rougeon F. Purification of mouse immunoglobulin heavy-chain messenger RNAs from total myeloma tumor RNA. Eur J Biochem. 1980 Jun;107(2):303–314. doi: 10.1111/j.1432-1033.1980.tb06030.x. [DOI] [PubMed] [Google Scholar]
  3. Bliska J. B., Guan K. L., Dixon J. E., Falkow S. Tyrosine phosphate hydrolysis of host proteins by an essential Yersinia virulence determinant. Proc Natl Acad Sci U S A. 1991 Feb 15;88(4):1187–1191. doi: 10.1073/pnas.88.4.1187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1006/abio.1976.9999. [DOI] [PubMed] [Google Scholar]
  5. Brautigan D. L. Great expectations: protein tyrosine phosphatases in cell regulation. Biochim Biophys Acta. 1992 Sep 14;1114(1):63–77. doi: 10.1016/0304-419x(92)90007-l. [DOI] [PubMed] [Google Scholar]
  6. Cantley L. C., Auger K. R., Carpenter C., Duckworth B., Graziani A., Kapeller R., Soltoff S. Oncogenes and signal transduction. Cell. 1991 Jan 25;64(2):281–302. doi: 10.1016/0092-8674(91)90639-g. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Church G. M., Gilbert W. Genomic sequencing. Proc Natl Acad Sci U S A. 1984 Apr;81(7):1991–1995. doi: 10.1073/pnas.81.7.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Crowe J. S., Cooper H. J., Smith M. A., Sims M. J., Parker D., Gewert D. Improved cloning efficiency of polymerase chain reaction (PCR) products after proteinase K digestion. Nucleic Acids Res. 1991 Jan 11;19(1):184–184. doi: 10.1093/nar/19.1.184. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  12. Goldstein B. J., Zhang W. R., Hashimoto N., Kahn C. R. Approaches to the molecular cloning of protein-tyrosine phosphatases in insulin-sensitive tissues. Mol Cell Biochem. 1992 Feb 12;109(2):107–113. doi: 10.1007/BF00229763. [DOI] [PubMed] [Google Scholar]
  13. Gu M. X., York J. D., Warshawsky I., Majerus P. W. Identification, cloning, and expression of a cytosolic megakaryocyte protein-tyrosine-phosphatase with sequence homology to cytoskeletal protein 4.1. Proc Natl Acad Sci U S A. 1991 Jul 1;88(13):5867–5871. doi: 10.1073/pnas.88.13.5867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hall L. R., Streuli M., Schlossman S. F., Saito H. Complete exon-intron organization of the human leukocyte common antigen (CD45) gene. J Immunol. 1988 Oct 15;141(8):2781–2787. [PubMed] [Google Scholar]
  15. 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]
  16. Howard P. K., Sefton B. M., Firtel R. A. Analysis of a spatially regulated phosphotyrosine phosphatase identifies tyrosine phosphorylation as a key regulatory pathway in Dictyostelium. Cell. 1992 Nov 13;71(4):637–647. doi: 10.1016/0092-8674(92)90597-6. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. 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]
  19. Lin H. C., Lei S. P., Wilcox G. An improved DNA sequencing strategy. Anal Biochem. 1985 May 15;147(1):114–119. doi: 10.1016/0003-2697(85)90016-8. [DOI] [PubMed] [Google Scholar]
  20. Lombroso P. J., Murdoch G., Lerner M. Molecular characterization of a protein-tyrosine-phosphatase enriched in striatum. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):7242–7246. doi: 10.1073/pnas.88.16.7242. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lombroso P. J., Naegele J. R., Sharma E., Lerner M. A protein tyrosine phosphatase expressed within dopaminoceptive neurons of the basal ganglia and related structures. J Neurosci. 1993 Jul;13(7):3064–3074. doi: 10.1523/JNEUROSCI.13-07-03064.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Maeda T., Tsai A. Y., Saito H. Mutations in a protein tyrosine phosphatase gene (PTP2) and a protein serine/threonine phosphatase gene (PTC1) cause a synthetic growth defect in Saccharomyces cerevisiae. Mol Cell Biol. 1993 Sep;13(9):5408–5417. doi: 10.1128/mcb.13.9.5408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Maekawa K., Imagawa N., Nagamatsu M., Harada S. Molecular cloning of a novel protein-tyrosine phosphatase containing a membrane-binding domain and GLGF repeats. FEBS Lett. 1994 Jan 10;337(2):200–206. doi: 10.1016/0014-5793(94)80273-4. [DOI] [PubMed] [Google Scholar]
  25. Matthews R. J., Cahir E. D., Thomas M. L. Identification of an additional member of the protein-tyrosine-phosphatase family: evidence for alternative splicing in the tyrosine phosphatase domain. Proc Natl Acad Sci U S A. 1990 Jun;87(12):4444–4448. doi: 10.1073/pnas.87.12.4444. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Miyasaka H., Li S. S. The cDNA cloning, nucleotide sequence and expression of an intracellular protein tyrosine phosphatase from mouse testis. Biochem Biophys Res Commun. 1992 Jun 30;185(3):818–825. doi: 10.1016/0006-291x(92)91700-z. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. 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]
  29. Perkins L. A., Larsen I., Perrimon N. corkscrew encodes a putative protein tyrosine phosphatase that functions to transduce the terminal signal from the receptor tyrosine kinase torso. Cell. 1992 Jul 24;70(2):225–236. doi: 10.1016/0092-8674(92)90098-w. [DOI] [PubMed] [Google Scholar]
  30. Pot D. A., Dixon J. E. A thousand and two protein tyrosine phosphatases. Biochim Biophys Acta. 1992 Jul 22;1136(1):35–43. doi: 10.1016/0167-4889(92)90082-m. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. Ramalingam R., Shaw D. R., Ennis H. L. Cloning and functional expression of a Dictyostelium discoideum protein tyrosine phosphatase. J Biol Chem. 1993 Oct 25;268(30):22680–22685. [PubMed] [Google Scholar]
  33. Saga Y., Tung J. S., Shen F. W., Pancoast T. C., Boyse E. A. Organization of the Ly-5 gene. Mol Cell Biol. 1988 Nov;8(11):4889–4895. doi: 10.1128/mcb.8.11.4889. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. 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]
  35. Sap J., D'Eustachio P., Givol D., Schlessinger J. Cloning and expression of a widely expressed receptor tyrosine phosphatase. Proc Natl Acad Sci U S A. 1990 Aug;87(16):6112–6116. doi: 10.1073/pnas.87.16.6112. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Schepens J., Zeeuwen P., Wieringa B., Hendriks W. Identification and typing of members of the protein-tyrosine phosphatase gene family expressed in mouse brain. Mol Biol Rep. 1992 Sep;16(4):241–248. doi: 10.1007/BF00419663. [DOI] [PubMed] [Google Scholar]
  37. Shultz L. D., Schweitzer P. A., Rajan T. V., Yi T., Ihle J. N., Matthews R. J., Thomas M. L., Beier D. R. Mutations at the murine motheaten locus are within the hematopoietic cell protein-tyrosine phosphatase (Hcph) gene. Cell. 1993 Jul 2;73(7):1445–1454. doi: 10.1016/0092-8674(93)90369-2. [DOI] [PubMed] [Google Scholar]
  38. Smith D. B., Johnson K. S. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene. 1988 Jul 15;67(1):31–40. doi: 10.1016/0378-1119(88)90005-4. [DOI] [PubMed] [Google Scholar]
  39. Stahl N., Yancopoulos G. D. The alphas, betas, and kinases of cytokine receptor complexes. Cell. 1993 Aug 27;74(4):587–590. doi: 10.1016/0092-8674(93)90506-l. [DOI] [PubMed] [Google Scholar]
  40. 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]
  41. Tsui H. W., Siminovitch K. A., de Souza L., Tsui F. W. Motheaten and viable motheaten mice have mutations in the haematopoietic cell phosphatase gene. Nat Genet. 1993 Jun;4(2):124–129. doi: 10.1038/ng0693-124. [DOI] [PubMed] [Google Scholar]
  42. Ullrich A., Schlessinger J. Signal transduction by receptors with tyrosine kinase activity. Cell. 1990 Apr 20;61(2):203–212. doi: 10.1016/0092-8674(90)90801-k. [DOI] [PubMed] [Google Scholar]
  43. 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]
  44. 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]
  45. Yang Q., Tonks N. K. Isolation of a cDNA clone encoding a human protein-tyrosine phosphatase with homology to the cytoskeletal-associated proteins band 4.1, ezrin, and talin. Proc Natl Acad Sci U S A. 1991 Jul 15;88(14):5949–5953. doi: 10.1073/pnas.88.14.5949. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Yi T., Cleveland J. L., Ihle J. N. Identification of novel protein tyrosine phosphatases of hematopoietic cells by polymerase chain reaction amplification. Blood. 1991 Nov 1;78(9):2222–2228. [PubMed] [Google Scholar]
  47. von Heijne G. A new method for predicting signal sequence cleavage sites. Nucleic Acids Res. 1986 Jun 11;14(11):4683–4690. doi: 10.1093/nar/14.11.4683. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES