Skip to main content
NCBI home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1996 Nov 2;135(4):1071–1083. doi: 10.1083/jcb.135.4.1071

Ventricular zone gene-1 (vzg-1) encodes a lysophosphatidic acid receptor expressed in neurogenic regions of the developing cerebral cortex

PMCID: PMC2133395  PMID: 8922387

Abstract

Neocortical neuroblast cell lines were used to clone G-protein-coupled receptor (GPCR) genes to study signaling mechanisms regulating cortical neurogenesis. One putative GPCR gene displayed an in situ expression pattern enriched in cortical neurogenic regions and was therefore named ventricular zone gene-1 (vzg-1). The vzg-1 cDNA hybridized to a 3.8-kb mRNA transcript and encoded a protein with a predicted molecular mass of 41-42 kD, confirmed by Western blot analysis. To assess its function, vzg-1 was overexpressed in a cell line from which it was cloned, inducing serum-dependent "cell rounding." Lysophosphatidic acid (LPA), a bioactive lipid present in high concentrations in serum, reproduced the effect seen with serum alone. Morphological responses to other related phospholipids or to thrombin, another agent that induces cell rounding through a GPCR, were not observed in vzg-1 overexpressing cells. Vzg-1 overexpression decreased the EC50 of both cell rounding and Gi activation in response to LPA. Pertussis toxin treatment inhibited vzg-1-dependent LPA-mediated Gi activation, but had no effect on cell rounding. Membrane binding studies indicated that vzg-1 overexpression increased specific LPA binding. These analyses identify the vzg-1 gene product as a receptor for LPA, suggesting the operation of LPA signaling mechanisms in cortical neurogenesis. Vzg-1 therefore provides a link between extracellular LPA and the activation of LPA- mediated signaling pathways through a single receptor and will allow new investigations into LPA signaling both in neural and nonneural systems.

Full Text

The Full Text of this article is available as a PDF (4.2 MB).

Selected References

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

  1. Allen L. F., Lefkowitz R. J., Caron M. G., Cotecchia S. G-protein-coupled receptor genes as protooncogenes: constitutively activating mutation of the alpha 1B-adrenergic receptor enhances mitogenesis and tumorigenicity. Proc Natl Acad Sci U S A. 1991 Dec 15;88(24):11354–11358. doi: 10.1073/pnas.88.24.11354. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Barbacid M. Neurotrophic factors and their receptors. Curr Opin Cell Biol. 1995 Apr;7(2):148–155. doi: 10.1016/0955-0674(95)80022-0. [DOI] [PubMed] [Google Scholar]
  3. Berry M., Rogers A. W. The migration of neuroblasts in the developing cerebral cortex. J Anat. 1965 Oct;99(Pt 4):691–709. [PMC free article] [PubMed] [Google Scholar]
  4. Blaschke A. J., Staley K., Chun J. Widespread programmed cell death in proliferative and postmitotic regions of the fetal cerebral cortex. Development. 1996 Apr;122(4):1165–1174. doi: 10.1242/dev.122.4.1165. [DOI] [PubMed] [Google Scholar]
  5. Buck L., Axel R. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell. 1991 Apr 5;65(1):175–187. doi: 10.1016/0092-8674(91)90418-x. [DOI] [PubMed] [Google Scholar]
  6. Cattaneo E., McKay R. Proliferation and differentiation of neuronal stem cells regulated by nerve growth factor. Nature. 1990 Oct 25;347(6295):762–765. doi: 10.1038/347762a0. [DOI] [PubMed] [Google Scholar]
  7. Caviness V. S., Jr Neocortical histogenesis in normal and reeler mice: a developmental study based upon [3H]thymidine autoradiography. Brain Res. 1982 Jul;256(3):293–302. doi: 10.1016/0165-3806(82)90141-9. [DOI] [PubMed] [Google Scholar]
  8. Caviness V. S., Jr Time of neuron origin in the hippocampus and dentate gyrus of normal and reeler mutant mice: an autoradiographic analysis. J Comp Neurol. 1973 Sep 15;151(2):113–120. doi: 10.1002/cne.901510203. [DOI] [PubMed] [Google Scholar]
  9. Checovich W. J., Mosher D. F. Lysophosphatidic acid enhances fibronectin binding to adherent cells. Arterioscler Thromb. 1993 Nov;13(11):1662–1667. doi: 10.1161/01.atv.13.11.1662. [DOI] [PubMed] [Google Scholar]
  10. Chen C., Okayama H. High-efficiency transformation of mammalian cells by plasmid DNA. Mol Cell Biol. 1987 Aug;7(8):2745–2752. doi: 10.1128/mcb.7.8.2745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Chenn A., McConnell S. K. Cleavage orientation and the asymmetric inheritance of Notch1 immunoreactivity in mammalian neurogenesis. Cell. 1995 Aug 25;82(4):631–641. doi: 10.1016/0092-8674(95)90035-7. [DOI] [PubMed] [Google Scholar]
  12. Chun J. J., Schatz D. G., Oettinger M. A., Jaenisch R., Baltimore D. The recombination activating gene-1 (RAG-1) transcript is present in the murine central nervous system. Cell. 1991 Jan 11;64(1):189–200. doi: 10.1016/0092-8674(91)90220-s. [DOI] [PubMed] [Google Scholar]
  13. Chun J. J., Shatz C. J. A fibronectin-like molecule is present in the developing cat cerebral cortex and is correlated with subplate neurons. J Cell Biol. 1988 Mar;106(3):857–872. doi: 10.1083/jcb.106.3.857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Chun J. J., Shatz C. J. Interstitial cells of the adult neocortical white matter are the remnant of the early generated subplate neuron population. J Comp Neurol. 1989 Apr 22;282(4):555–569. doi: 10.1002/cne.902820407. [DOI] [PubMed] [Google Scholar]
  15. Chun J. J., Shatz C. J. Redistribution of synaptic vesicle antigens is correlated with the disappearance of a transient synaptic zone in the developing cerebral cortex. Neuron. 1988 Jun;1(4):297–310. doi: 10.1016/0896-6273(88)90078-5. [DOI] [PubMed] [Google Scholar]
  16. Chun J. J., Shatz C. J. The earliest-generated neurons of the cat cerebral cortex: characterization by MAP2 and neurotransmitter immunohistochemistry during fetal life. J Neurosci. 1989 May;9(5):1648–1667. doi: 10.1523/JNEUROSCI.09-05-01648.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Chun J., Jaenisch R. Clonal cell lines produced by infection of neocortical neuroblasts using multiple oncogenes transduced by retroviruses. Mol Cell Neurosci. 1996 Apr;7(4):304–321. doi: 10.1006/mcne.1996.0023. [DOI] [PubMed] [Google Scholar]
  18. Crespo P., Xu N., Simonds W. F., Gutkind J. S. Ras-dependent activation of MAP kinase pathway mediated by G-protein beta gamma subunits. Nature. 1994 Jun 2;369(6479):418–420. doi: 10.1038/369418a0. [DOI] [PubMed] [Google Scholar]
  19. Das G. D. Gliogenesis and ependymogenesis during embryonic development of the rat. An autoradiographic study. J Neurol Sci. 1979 Oct;43(2):193–204. doi: 10.1016/0022-510x(79)90115-1. [DOI] [PubMed] [Google Scholar]
  20. Desarnaud F., Labbe O., Eggerickx D., Vassart G., Parmentier M. Molecular cloning, functional expression and pharmacological characterization of a mouse melanocortin receptor gene. Biochem J. 1994 Apr 15;299(Pt 2):367–373. doi: 10.1042/bj2990367. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Dohlman H. G., Bouvier M., Benovic J. L., Caron M. G., Lefkowitz R. J. The multiple membrane spanning topography of the beta 2-adrenergic receptor. Localization of the sites of binding, glycosylation, and regulatory phosphorylation by limited proteolysis. J Biol Chem. 1987 Oct 15;262(29):14282–14288. [PubMed] [Google Scholar]
  22. Donnelly J. J., Martinez D., Jansen K. U., Ellis R. W., Montgomery D. L., Liu M. A. Protection against papillomavirus with a polynucleotide vaccine. J Infect Dis. 1996 Feb;173(2):314–320. doi: 10.1093/infdis/173.2.314. [DOI] [PubMed] [Google Scholar]
  23. Eichholtz T., Jalink K., Fahrenfort I., Moolenaar W. H. The bioactive phospholipid lysophosphatidic acid is released from activated platelets. Biochem J. 1993 May 1;291(Pt 3):677–680. doi: 10.1042/bj2910677. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Erba H. P., Eddy R., Shows T., Kedes L., Gunning P. Structure, chromosome location, and expression of the human gamma-actin gene: differential evolution, location, and expression of the cytoskeletal beta- and gamma-actin genes. Mol Cell Biol. 1988 Apr;8(4):1775–1789. doi: 10.1128/mcb.8.4.1775. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Fourcade O., Simon M. F., Viodé C., Rugani N., Leballe F., Ragab A., Fournié B., Sarda L., Chap H. Secretory phospholipase A2 generates the novel lipid mediator lysophosphatidic acid in membrane microvesicles shed from activated cells. Cell. 1995 Mar 24;80(6):919–927. doi: 10.1016/0092-8674(95)90295-3. [DOI] [PubMed] [Google Scholar]
  26. Ghosh A., Greenberg M. E. Distinct roles for bFGF and NT-3 in the regulation of cortical neurogenesis. Neuron. 1995 Jul;15(1):89–103. doi: 10.1016/0896-6273(95)90067-5. [DOI] [PubMed] [Google Scholar]
  27. Hausdorff W. P., Caron M. G., Lefkowitz R. J. Turning off the signal: desensitization of beta-adrenergic receptor function. FASEB J. 1990 Aug;4(11):2881–2889. [PubMed] [Google Scholar]
  28. Hicks S. P., D'Amato C. J. Cell migrations to the isocortex in the rat. Anat Rec. 1968 Mar;160(3):619–634. doi: 10.1002/ar.1091600311. [DOI] [PubMed] [Google Scholar]
  29. Hill C. S., Oh S. Y., Schmidt S. A., Clark K. J., Murray A. W. Lysophosphatidic acid inhibits gap-junctional communication and stimulates phosphorylation of connexin-43 in WB cells: possible involvement of the mitogen-activated protein kinase cascade. Biochem J. 1994 Oct 15;303(Pt 2):475–479. doi: 10.1042/bj3030475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Hill C. S., Treisman R. Differential activation of c-fos promoter elements by serum, lysophosphatidic acid, G proteins and polypeptide growth factors. EMBO J. 1995 Oct 16;14(20):5037–5047. doi: 10.1002/j.1460-2075.1995.tb00186.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Hill C. S., Wynne J., Treisman R. The Rho family GTPases RhoA, Rac1, and CDC42Hs regulate transcriptional activation by SRF. Cell. 1995 Jun 30;81(7):1159–1170. doi: 10.1016/s0092-8674(05)80020-0. [DOI] [PubMed] [Google Scholar]
  32. Hla T., Maciag T. An abundant transcript induced in differentiating human endothelial cells encodes a polypeptide with structural similarities to G-protein-coupled receptors. J Biol Chem. 1990 Jun 5;265(16):9308–9313. [PubMed] [Google Scholar]
  33. Ishii K., Hein L., Kobilka B., Coughlin S. R. Kinetics of thrombin receptor cleavage on intact cells. Relation to signaling. J Biol Chem. 1993 May 5;268(13):9780–9786. [PubMed] [Google Scholar]
  34. Jalink K., Eichholtz T., Postma F. R., van Corven E. J., Moolenaar W. H. Lysophosphatidic acid induces neuronal shape changes via a novel, receptor-mediated signaling pathway: similarity to thrombin action. Cell Growth Differ. 1993 Apr;4(4):247–255. [PubMed] [Google Scholar]
  35. Jalink K., Moolenaar W. H. Thrombin receptor activation causes rapid neural cell rounding and neurite retraction independent of classic second messengers. J Cell Biol. 1992 Jul;118(2):411–419. doi: 10.1083/jcb.118.2.411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Jalink K., van Corven E. J., Hengeveld T., Morii N., Narumiya S., Moolenaar W. H. Inhibition of lysophosphatidate- and thrombin-induced neurite retraction and neuronal cell rounding by ADP ribosylation of the small GTP-binding protein Rho. J Cell Biol. 1994 Aug;126(3):801–810. doi: 10.1083/jcb.126.3.801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Julius D., Livelli T. J., Jessell T. M., Axel R. Ectopic expression of the serotonin 1c receptor and the triggering of malignant transformation. Science. 1989 Jun 2;244(4908):1057–1062. doi: 10.1126/science.2727693. [DOI] [PubMed] [Google Scholar]
  38. Karnik S. S., Khorana H. G. Assembly of functional rhodopsin requires a disulfide bond between cysteine residues 110 and 187. J Biol Chem. 1990 Oct 15;265(29):17520–17524. [PubMed] [Google Scholar]
  39. Kilpatrick T. J., Bartlett P. F. Cloned multipotential precursors from the mouse cerebrum require FGF-2, whereas glial restricted precursors are stimulated with either FGF-2 or EGF. J Neurosci. 1995 May;15(5 Pt 1):3653–3661. doi: 10.1523/JNEUROSCI.15-05-03653.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Kilpatrick T. J., Bartlett P. F. Cloning and growth of multipotential neural precursors: requirements for proliferation and differentiation. Neuron. 1993 Feb;10(2):255–265. doi: 10.1016/0896-6273(93)90316-j. [DOI] [PubMed] [Google Scholar]
  41. Klein R. Role of neurotrophins in mouse neuronal development. FASEB J. 1994 Jul;8(10):738–744. doi: 10.1096/fasebj.8.10.8050673. [DOI] [PubMed] [Google Scholar]
  42. 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]
  43. Lauener R., Shen Y., Duronio V., Salari H. Selective inhibition of phosphatidylinositol 3-kinase by phosphatidic acid and related lipids. Biochem Biophys Res Commun. 1995 Oct 4;215(1):8–14. doi: 10.1006/bbrc.1995.2427. [DOI] [PubMed] [Google Scholar]
  44. Libert F., Parmentier M., Lefort A., Dinsart C., Van Sande J., Maenhaut C., Simons M. J., Dumont J. E., Vassart G. Selective amplification and cloning of four new members of the G protein-coupled receptor family. Science. 1989 May 5;244(4904):569–572. doi: 10.1126/science.2541503. [DOI] [PubMed] [Google Scholar]
  45. Lo Turco J. J., Kriegstein A. R. Clusters of coupled neuroblasts in embryonic neocortex. Science. 1991 Apr 26;252(5005):563–566. doi: 10.1126/science.1850552. [DOI] [PubMed] [Google Scholar]
  46. Luttrell L. M., Hawes B. E., Touhara K., van Biesen T., Koch W. J., Lefkowitz R. J. Effect of cellular expression of pleckstrin homology domains on Gi-coupled receptor signaling. J Biol Chem. 1995 Jun 2;270(22):12984–12989. doi: 10.1074/jbc.270.22.12984. [DOI] [PubMed] [Google Scholar]
  47. Luttrell L. M., van Biesen T., Hawes B. E., Koch W. J., Touhara K., Lefkowitz R. J. G beta gamma subunits mediate mitogen-activated protein kinase activation by the tyrosine kinase insulin-like growth factor 1 receptor. J Biol Chem. 1995 Jul 14;270(28):16495–16498. doi: 10.1074/jbc.270.28.16495. [DOI] [PubMed] [Google Scholar]
  48. Matsuda L. A., Lolait S. J., Brownstein M. J., Young A. C., Bonner T. I. Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature. 1990 Aug 9;346(6284):561–564. doi: 10.1038/346561a0. [DOI] [PubMed] [Google Scholar]
  49. Mead D. A., Pey N. K., Herrnstadt C., Marcil R. A., Smith L. M. A universal method for the direct cloning of PCR amplified nucleic acid. Biotechnology (N Y) 1991 Jul;9(7):657–663. doi: 10.1038/nbt0791-657. [DOI] [PubMed] [Google Scholar]
  50. Moolenaar W. H. Lysophosphatidic acid signalling. Curr Opin Cell Biol. 1995 Apr;7(2):203–210. doi: 10.1016/0955-0674(95)80029-8. [DOI] [PubMed] [Google Scholar]
  51. Post S. R., Jacobson J. P., Insel P. A. P2 purinergic receptor agonists enhance cAMP production in Madin-Darby canine kidney epithelial cells via an autocrine/paracrine mechanism. J Biol Chem. 1996 Jan 26;271(4):2029–2032. doi: 10.1074/jbc.271.4.2029. [DOI] [PubMed] [Google Scholar]
  52. Probst W. C., Snyder L. A., Schuster D. I., Brosius J., Sealfon S. C. Sequence alignment of the G-protein coupled receptor superfamily. DNA Cell Biol. 1992 Jan-Feb;11(1):1–20. doi: 10.1089/dna.1992.11.1. [DOI] [PubMed] [Google Scholar]
  53. Rakic P. Specification of cerebral cortical areas. Science. 1988 Jul 8;241(4862):170–176. doi: 10.1126/science.3291116. [DOI] [PubMed] [Google Scholar]
  54. Rands E., Candelore M. R., Cheung A. H., Hill W. S., Strader C. D., Dixon R. A. Mutational analysis of beta-adrenergic receptor glycosylation. J Biol Chem. 1990 Jun 25;265(18):10759–10764. [PubMed] [Google Scholar]
  55. Raz E., Carson D. A., Parker S. E., Parr T. B., Abai A. M., Aichinger G., Gromkowski S. H., Singh M., Lew D., Yankauckas M. A. Intradermal gene immunization: the possible role of DNA uptake in the induction of cellular immunity to viruses. Proc Natl Acad Sci U S A. 1994 Sep 27;91(20):9519–9523. doi: 10.1073/pnas.91.20.9519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Ridley A. J., Hall A. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell. 1992 Aug 7;70(3):389–399. doi: 10.1016/0092-8674(92)90163-7. [DOI] [PubMed] [Google Scholar]
  57. SIDMAN R. L., MIALE I. L., FEDER N. Cell proliferation and migration in the primitive ependymal zone: an autoradiographic study of histogenesis in the nervous system. Exp Neurol. 1959 Oct;1:322–333. doi: 10.1016/0014-4886(59)90024-x. [DOI] [PubMed] [Google Scholar]
  58. Seymour R. M., Berry M. Scanning and transmission electron microscope studies of interkinetic nuclear migration in the cerebral vesicles of the rat. J Comp Neurol. 1975 Mar 1;160(1):105–125. doi: 10.1002/cne.901600107. [DOI] [PubMed] [Google Scholar]
  59. Stewart G. R., Pearlman A. L. Fibronectin-like immunoreactivity in the developing cerebral cortex. J Neurosci. 1987 Oct;7(10):3325–3333. doi: 10.1523/JNEUROSCI.07-10-03325.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Suidan H. S., Stone S. R., Hemmings B. A., Monard D. Thrombin causes neurite retraction in neuronal cells through activation of cell surface receptors. Neuron. 1992 Feb;8(2):363–375. doi: 10.1016/0896-6273(92)90302-t. [DOI] [PubMed] [Google Scholar]
  61. Takahashi T., Nowakowski R. S., Caviness V. S., Jr Cell cycle parameters and patterns of nuclear movement in the neocortical proliferative zone of the fetal mouse. J Neurosci. 1993 Feb;13(2):820–833. doi: 10.1523/JNEUROSCI.13-02-00820.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Takahashi T., Nowakowski R. S., Caviness V. S., Jr The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall. J Neurosci. 1995 Sep;15(9):6046–6057. doi: 10.1523/JNEUROSCI.15-09-06046.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Temple S., Davis A. A. Isolated rat cortical progenitor cells are maintained in division in vitro by membrane-associated factors. Development. 1994 Apr;120(4):999–1008. doi: 10.1242/dev.120.4.999. [DOI] [PubMed] [Google Scholar]
  64. Temple S., Qian X. bFGF, neurotrophins, and the control or cortical neurogenesis. Neuron. 1995 Aug;15(2):249–252. doi: 10.1016/0896-6273(95)90030-6. [DOI] [PubMed] [Google Scholar]
  65. Thomson F. J., Perkins L., Ahern D., Clark M. Identification and characterization of a lysophosphatidic acid receptor. Mol Pharmacol. 1994 Apr;45(4):718–723. [PubMed] [Google Scholar]
  66. Tokumura A., Iimori M., Nishioka Y., Kitahara M., Sakashita M., Tanaka S. Lysophosphatidic acids induce proliferation of cultured vascular smooth muscle cells from rat aorta. Am J Physiol. 1994 Jul;267(1 Pt 1):C204–C210. doi: 10.1152/ajpcell.1994.267.1.C204. [DOI] [PubMed] [Google Scholar]
  67. Turka L. A., Schatz D. G., Oettinger M. A., Chun J. J., Gorka C., Lee K., McCormack W. T., Thompson C. B. Thymocyte expression of RAG-1 and RAG-2: termination by T cell receptor cross-linking. Science. 1991 Aug 16;253(5021):778–781. doi: 10.1126/science.1831564. [DOI] [PubMed] [Google Scholar]
  68. Vara J. A., Portela A., Ortín J., Jiménez A. Expression in mammalian cells of a gene from Streptomyces alboniger conferring puromycin resistance. Nucleic Acids Res. 1986 Jun 11;14(11):4617–4624. doi: 10.1093/nar/14.11.4617. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Xu Y., Casey G., Mills G. B. Effect of lysophospholipids on signaling in the human Jurkat T cell line. J Cell Physiol. 1995 Jun;163(3):441–450. doi: 10.1002/jcp.1041630303. [DOI] [PubMed] [Google Scholar]
  70. Yoshida S., Fujisawa-Sehara A., Taki T., Arai K., Nabeshima Y. Lysophosphatidic acid and bFGF control different modes in proliferating myoblasts. J Cell Biol. 1996 Jan;132(1-2):181–193. doi: 10.1083/jcb.132.1.181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Zhang Q., Checovich W. J., Peters D. M., Albrecht R. M., Mosher D. F. Modulation of cell surface fibronectin assembly sites by lysophosphatidic acid. J Cell Biol. 1994 Dec;127(5):1447–1459. doi: 10.1083/jcb.127.5.1447. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. van Corven E. J., Groenink A., Jalink K., Eichholtz T., Moolenaar W. H. Lysophosphatidate-induced cell proliferation: identification and dissection of signaling pathways mediated by G proteins. Cell. 1989 Oct 6;59(1):45–54. doi: 10.1016/0092-8674(89)90868-4. [DOI] [PubMed] [Google Scholar]
  73. van Corven E. J., Hordijk P. L., Medema R. H., Bos J. L., Moolenaar W. H. Pertussis toxin-sensitive activation of p21ras by G protein-coupled receptor agonists in fibroblasts. Proc Natl Acad Sci U S A. 1993 Feb 15;90(4):1257–1261. doi: 10.1073/pnas.90.4.1257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. van Corven E. J., van Rijswijk A., Jalink K., van der Bend R. L., van Blitterswijk W. J., Moolenaar W. H. Mitogenic action of lysophosphatidic acid and phosphatidic acid on fibroblasts. Dependence on acyl-chain length and inhibition by suramin. Biochem J. 1992 Jan 1;281(Pt 1):163–169. doi: 10.1042/bj2810163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. van der Bend R. L., Brunner J., Jalink K., van Corven E. J., Moolenaar W. H., van Blitterswijk W. J. Identification of a putative membrane receptor for the bioactive phospholipid, lysophosphatidic acid. EMBO J. 1992 Jul;11(7):2495–2501. doi: 10.1002/j.1460-2075.1992.tb05314.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. van der Geer P., Hunter T., Lindberg R. A. Receptor protein-tyrosine kinases and their signal transduction pathways. Annu Rev Cell Biol. 1994;10:251–337. doi: 10.1146/annurev.cb.10.110194.001343. [DOI] [PubMed] [Google Scholar]

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

RESOURCES