Skip to main content

Some NLM-NCBI services and products are experiencing heavy traffic, which may affect performance and availability. We apologize for the inconvenience and appreciate your patience. For assistance, please contact our Help Desk at info@ncbi.nlm.nih.gov.

Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1990 Sep;10(9):4770–4777. doi: 10.1128/mcb.10.9.4770

Characterization and cDNA cloning of phospholipase C-gamma, a major substrate for heparin-binding growth factor 1 (acidic fibroblast growth factor)-activated tyrosine kinase.

W H Burgess 1, C A Dionne 1, J Kaplow 1, R Mudd 1, R Friesel 1, A Zilberstein 1, J Schlessinger 1, M Jaye 1
PMCID: PMC361079  PMID: 2167438

Abstract

Heparin-binding growth factors (HBGFs) bind to high-affinity cell surface receptors which possess intrinsic tyrosine kinase activity. A Mr 150,000 protein phosphorylated on tyrosine in response to class 1 HBGF (HBGF-1) was purified and partially sequenced. On the basis of this sequence, cDNA clones were isolated from a human endothelial cell library and identified as encoding phospholipase C-gamma. Phosphorylation of phospholipase C-gamma in intact cells treated with HBGF-1 was directly demonstrated by using antiphospholipase C-gamma antibodies. Thus, HBGF-1 joins epidermal growth factor and platelet-derived growth factor, whose receptor activation leads to tyrosine phosphorylation and probable activation of phospholipase C-gamma.

Full text

PDF
4770

Images in this article

Selected References

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

  1. Brown K. D., Blakeley D. M., Brigstock D. R. Stimulation of polyphosphoinositide hydrolysis in Swiss 3T3 cells by recombinant fibroblast growth factors. FEBS Lett. 1989 Apr 24;247(2):227–231. doi: 10.1016/0014-5793(89)81340-7. [DOI] [PubMed] [Google Scholar]
  2. Burgess W. H., Maciag T. The heparin-binding (fibroblast) growth factor family of proteins. Annu Rev Biochem. 1989;58:575–606. doi: 10.1146/annurev.bi.58.070189.003043. [DOI] [PubMed] [Google Scholar]
  3. Burgess W. H., Mehlman T., Marshak D. R., Fraser B. A., Maciag T. Structural evidence that endothelial cell growth factor beta is the precursor of both endothelial cell growth factor alpha and acidic fibroblast growth factor. Proc Natl Acad Sci U S A. 1986 Oct;83(19):7216–7220. doi: 10.1073/pnas.83.19.7216. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Coughlin S. R., Barr P. J., Cousens L. S., Fretto L. J., Williams L. T. Acidic and basic fibroblast growth factors stimulate tyrosine kinase activity in vivo. J Biol Chem. 1988 Jan 15;263(2):988–993. [PubMed] [Google Scholar]
  5. Doctrow S. R., Folkman J. Protein kinase C activators suppress stimulation of capillary endothelial cell growth by angiogenic endothelial mitogens. J Cell Biol. 1987 Mar;104(3):679–687. doi: 10.1083/jcb.104.3.679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Downing J. R., Margolis B. L., Zilberstein A., Ashmun R. A., Ullrich A., Sherr C. J., Schlessinger J. Phospholipase C-gamma, a substrate for PDGF receptor kinase, is not phosphorylated on tyrosine during the mitogenic response to CSF-1. EMBO J. 1989 Nov;8(11):3345–3350. doi: 10.1002/j.1460-2075.1989.tb08496.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Friesel R., Burgess W. H., Maciag T. Heparin-binding growth factor 1 stimulates tyrosine phosphorylation in NIH 3T3 cells. Mol Cell Biol. 1989 May;9(5):1857–1865. doi: 10.1128/mcb.9.5.1857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Huang S. S., Huang J. S. Association of bovine brain-derived growth factor receptor with protein tyrosine kinase activity. J Biol Chem. 1986 Jul 25;261(21):9568–9571. [PubMed] [Google Scholar]
  9. Hunkapiller M. W., Lujan E., Ostrander F., Hood L. E. Isolation of microgram quantities of proteins from polyacrylamide gels for amino acid sequence analysis. Methods Enzymol. 1983;91:227–236. doi: 10.1016/s0076-6879(83)91019-4. [DOI] [PubMed] [Google Scholar]
  10. Jaye M., Burgess W. H., Shaw A. B., Drohan W. N. Biological equivalence of natural bovine and recombinant human alpha-endothelial cell growth factors. J Biol Chem. 1987 Dec 5;262(34):16612–16617. [PubMed] [Google Scholar]
  11. Jaye M., Howk R., Burgess W., Ricca G. A., Chiu I. M., Ravera M. W., O'Brien S. J., Modi W. S., Maciag T., Drohan W. N. Human endothelial cell growth factor: cloning, nucleotide sequence, and chromosome localization. Science. 1986 Aug 1;233(4763):541–545. doi: 10.1126/science.3523756. [DOI] [PubMed] [Google Scholar]
  12. Kaibuchi K., Tsuda T., Kikuchi A., Tanimoto T., Yamashita T., Takai Y. Possible involvement of protein kinase C and calcium ion in growth factor-induced expression of c-myc oncogene in Swiss 3T3 fibroblasts. J Biol Chem. 1986 Jan 25;261(3):1187–1192. [PubMed] [Google Scholar]
  13. Karn J., Brenner S., Barnett L., Cesareni G. Novel bacteriophage lambda cloning vector. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5172–5176. doi: 10.1073/pnas.77.9.5172. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Konigsberg W. H., Henderson L. Removal of sodium dodecyl sulfate from proteins by ion-pair extraction. Methods Enzymol. 1983;91:254–259. doi: 10.1016/s0076-6879(83)91022-4. [DOI] [PubMed] [Google Scholar]
  15. Kornbluth S., Paulson K. E., Hanafusa H. Novel tyrosine kinase identified by phosphotyrosine antibody screening of cDNA libraries. Mol Cell Biol. 1988 Dec;8(12):5541–5544. doi: 10.1128/mcb.8.12.5541. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Lee P. L., Johnson D. E., Cousens L. S., Fried V. A., Williams L. T. Purification and complementary DNA cloning of a receptor for basic fibroblast growth factor. Science. 1989 Jul 7;245(4913):57–60. doi: 10.1126/science.2544996. [DOI] [PubMed] [Google Scholar]
  18. Magnaldo I., L'Allemain G., Chambard J. C., Moenner M., Barritault D., Pouysségur J. The mitogenic signaling pathway of fibroblast growth factor is not mediated through polyphosphoinositide hydrolysis and protein kinase C activation in hamster fibroblasts. J Biol Chem. 1986 Dec 25;261(36):16916–16922. [PubMed] [Google Scholar]
  19. Mansukhani A., Moscatelli D., Talarico D., Levytska V., Basilico C. A murine fibroblast growth factor (FGF) receptor expressed in CHO cells is activated by basic FGF and Kaposi FGF. Proc Natl Acad Sci U S A. 1990 Jun;87(11):4378–4382. doi: 10.1073/pnas.87.11.4378. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Margolis B., Rhee S. G., Felder S., Mervic M., Lyall R., Levitzki A., Ullrich A., Zilberstein A., Schlessinger J. EGF induces tyrosine phosphorylation of phospholipase C-II: a potential mechanism for EGF receptor signaling. Cell. 1989 Jun 30;57(7):1101–1107. doi: 10.1016/0092-8674(89)90047-0. [DOI] [PubMed] [Google Scholar]
  21. Margolis B., Zilberstein A., Franks C., Felder S., Kremer S., Ullrich A., Rhee S. G., Skorecki K., Schlessinger J. Effect of phospholipase C-gamma overexpression on PDGF-induced second messengers and mitogenesis. Science. 1990 May 4;248(4955):607–610. doi: 10.1126/science.2333512. [DOI] [PubMed] [Google Scholar]
  22. Meisenhelder J., Suh P. G., Rhee S. G., Hunter T. Phospholipase C-gamma is a substrate for the PDGF and EGF receptor protein-tyrosine kinases in vivo and in vitro. Cell. 1989 Jun 30;57(7):1109–1122. doi: 10.1016/0092-8674(89)90048-2. [DOI] [PubMed] [Google Scholar]
  23. Moenner M., Magnaldo I., L'Allemain G., Barritault D., Pouysségur J. Early and late mitogenic events induced by FGF on bovine epithelial lens cells are not triggered by hydrolysis of polyphosphoinositides. Biochem Biophys Res Commun. 1987 Jul 15;146(1):32–40. doi: 10.1016/0006-291x(87)90686-3. [DOI] [PubMed] [Google Scholar]
  24. Moolenaar W. H., Bierman A. J., Tilly B. C., Verlaan I., Defize L. H., Honegger A. M., Ullrich A., Schlessinger J. A point mutation at the ATP-binding site of the EGF-receptor abolishes signal transduction. EMBO J. 1988 Mar;7(3):707–710. doi: 10.1002/j.1460-2075.1988.tb02866.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Paris S., Chambard J. C., Pouysségur J. Tyrosine kinase-activating growth factors potentiate thrombin- and AIF4- -induced phosphoinositide breakdown in hamster fibroblasts. Evidence for positive cross-talk between the two mitogenic signaling pathways. J Biol Chem. 1988 Sep 15;263(26):12893–12900. [PubMed] [Google Scholar]
  26. Pasquale E. B., Singer S. J. Identification of a developmentally regulated protein-tyrosine kinase by using anti-phosphotyrosine antibodies to screen a cDNA expression library. Proc Natl Acad Sci U S A. 1989 Jul;86(14):5449–5453. doi: 10.1073/pnas.86.14.5449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Presta M., Maier J. A., Ragnotti G. The mitogenic signaling pathway but not the plasminogen activator-inducing pathway of basic fibroblast growth factor is mediated through protein kinase C in fetal bovine aortic endothelial cells. J Cell Biol. 1989 Oct;109(4 Pt 1):1877–1884. doi: 10.1083/jcb.109.4.1877. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Reid H. H., Wilks A. F., Bernard O. Two forms of the basic fibroblast growth factor receptor-like mRNA are expressed in the developing mouse brain. Proc Natl Acad Sci U S A. 1990 Feb;87(4):1596–1600. doi: 10.1073/pnas.87.4.1596. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Rhee S. G., Suh P. G., Ryu S. H., Lee S. Y. Studies of inositol phospholipid-specific phospholipase C. Science. 1989 May 5;244(4904):546–550. doi: 10.1126/science.2541501. [DOI] [PubMed] [Google Scholar]
  30. Ruta M., Burgess W., Givol D., Epstein J., Neiger N., Kaplow J., Crumley G., Dionne C., Jaye M., Schlessinger J. Receptor for acidic fibroblast growth factor is related to the tyrosine kinase encoded by the fms-like gene (FLG). Proc Natl Acad Sci U S A. 1989 Nov;86(22):8722–8726. doi: 10.1073/pnas.86.22.8722. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Saiki R. K., Gelfand D. H., Stoffel S., Scharf S. J., Higuchi R., Horn G. T., Mullis K. B., Erlich H. A. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 1988 Jan 29;239(4839):487–491. doi: 10.1126/science.2448875. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. Sherr C. J., Rettenmier C. W., Sacca R., Roussel M. F., Look A. T., Stanley E. R. The c-fms proto-oncogene product is related to the receptor for the mononuclear phagocyte growth factor, CSF-1. Cell. 1985 Jul;41(3):665–676. doi: 10.1016/s0092-8674(85)80047-7. [DOI] [PubMed] [Google Scholar]
  34. Stahl M. L., Ferenz C. R., Kelleher K. L., Kriz R. W., Knopf J. L. Sequence similarity of phospholipase C with the non-catalytic region of src. Nature. 1988 Mar 17;332(6161):269–272. doi: 10.1038/332269a0. [DOI] [PubMed] [Google Scholar]
  35. Suh P. G., Ryu S. H., Moon K. H., Suh H. W., Rhee S. G. Inositol phospholipid-specific phospholipase C: complete cDNA and protein sequences and sequence homology to tyrosine kinase-related oncogene products. Proc Natl Acad Sci U S A. 1988 Aug;85(15):5419–5423. doi: 10.1073/pnas.85.15.5419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Tsuda T., Kaibuchi K., Kawahara Y., Fukuzaki H., Takai Y. Induction of protein kinase C activation and Ca2+ mobilization by fibroblast growth factor in Swiss 3T3 cells. FEBS Lett. 1985 Oct 28;191(2):205–210. doi: 10.1016/0014-5793(85)80009-0. [DOI] [PubMed] [Google Scholar]
  37. Wahl M. I., Daniel T. O., Carpenter G. Antiphosphotyrosine recovery of phospholipase C activity after EGF treatment of A-431 cells. Science. 1988 Aug 19;241(4868):968–970. doi: 10.1126/science.2457254. [DOI] [PubMed] [Google Scholar]
  38. Wahl M. I., Nishibe S., Suh P. G., Rhee S. G., Carpenter G. Epidermal growth factor stimulates tyrosine phosphorylation of phospholipase C-II independently of receptor internalization and extracellular calcium. Proc Natl Acad Sci U S A. 1989 Mar;86(5):1568–1572. doi: 10.1073/pnas.86.5.1568. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Yamamoto T., Tsuda T., Hamamori Y., Nishimura N., Takai Y. Inhibition of DNA synthesis by protein kinase C-activating phorbol esters in NIH/3T3 cells. J Biochem. 1988 Jul;104(1):53–56. doi: 10.1093/oxfordjournals.jbchem.a122422. [DOI] [PubMed] [Google Scholar]
  40. Yarden Y., Escobedo J. A., Kuang W. J., Yang-Feng T. L., Daniel T. O., Tremble P. M., Chen E. Y., Ando M. E., Harkins R. N., Francke U. Structure of the receptor for platelet-derived growth factor helps define a family of closely related growth factor receptors. Nature. 1986 Sep 18;323(6085):226–232. doi: 10.1038/323226a0. [DOI] [PubMed] [Google Scholar]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES