A novel cross-talk between endothelin and ErbB receptors controlling glutamate transporter expression in astrocytes

Journal of Neurochemistry

Volumn 122, Issue 4, 2012, Pages 844-855

  Glisic, Darko ^a   Lehmann, Claudia ^a   Figiel, MacIej ^b   Ödemis, Veysel ^a   Lindner, Ricco ^a   Engele, Jürgen ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b INSTITUTE OF BIOORGANIC CHEMISTRY   (Poland)

Author keywords

astrocytes; EGF; endothelins; GLT 1 EAAT 2; receptor internalization

Indexed keywords

ABELSON KINASE; ENDOTHELIN; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; GLUTAMATE TRANSPORTER; VESICULAR GLUTAMATE TRANSPORTER 1;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL SURFACE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; GENE SEQUENCE; INTERNALIZATION; INTRACELLULAR SIGNALING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT;

EID: 84864119773     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2012.07819.x     Document Type: Article

References (63)

1. Attwell D., Buchan A. M., Charpak S., Lauritzen M., Macvicar B. A., and, Newman E. A., (2010) Glial and neuronal control of brain blood flow. Nature 468, 232-243.
2. Bagnato A., and, Rosanò L., (2008) The endothelin axis in cancer. Int. J. Biochem. Cell Biol. 40, 1443-1451.
3. Barbieri M. A., Ramkumar T. P., Fernadez-Pol S., Chen P. I., and, Stahl P. D., (2004) Receptor tyrosine kinase signaling and trafficking - paradigms revisited. Curr. Top. Microbiol. Immunol. 286, 1-20.
4. Beart P. M., and, O'Shea R. D., (2007) Transporters for L-glutamate: an update on their molecular pharmacology and pathological involvement. Br. J. Pharmacol. 150, 5-17.
5. Buchdunger E., Zimmermann J., Mett H., Meyer T., Müller M., Druker B. J., and, Lydon N. B., (1996) Inhibition of the Abl protein-tyrosine kinase in vitro and in vivo by a 2-phenylaminopyrimidine derivative. Cancer Res. 56, 100-104.
6. Cabrita M. A., and, Christofori G., (2008) Sprouty proteins, masterminds of receptor tyrosine kinase signaling. Angiogenesis 11, 53-62.
7. Chung K. Y., and, Walker J. W., (2007) Interaction and inhibitory cross-talk between endothelin and ErbB receptors in the adult heart. Mol. Pharmacol. 71, 1494-1502.
8. Citri A., Skaria K. B., and, Yarden Y., (2003) The deaf and the dumb: the biology of ErbB-2 and ErbB-3. Exp. Cell Res. 284, 54-65.
9. Daub H., Weiss F. U., Wallasch C., and, Ullrich A., (1996) Role of transactivation of the EGF receptor in signalling by G-protein-coupled receptors. Nature 379, 557-560.
10. Davenport A. P., and, Maguire J. J., (2006) Endothelin Handb. Exp. Pharmacol. 176, 295-329.
11. Ferguson K. M., (2008) Structure-based view of epidermal growth factor receptor regulation. Ann. Rev. Biophys. 37, 353-373.
12. Figiel M., Maucher T., Rozyczka J., Bayatti N., and, Engele J., (2003) Regulation of glial glutamate transporter expression by growth factors. Exp. Neurol. 183, 124-135.
13. Gadea A., Schinelli S., and, Gallo V., (2008) Endothelin-1 regulates astrocyte proliferation and reactive gliosis via a JNK/c-Jun signaling pathway. J. Neurosci. 28, 2394-2408.
14. González-González I. M., García-Tardõn N., Giménez C., and, Zafra F., (2008) PKC-dependent endocytosis of the GLT1 glutamate transporter depends on ubiquitylation of lysines located in a C-terminal cluster. Glia 56, 963-974.
15. Gur G., Rubin C., Katz M., et al. (2004) LRIG1 restricts growth factor signaling by enhancing receptor ubiquitylation and degradation. EMBO J. 23, 3270-3281.
16. Halassa M. M., Fellin T., and, Haydon G., (2007) The tripartite synapse: roles for gliotransmission in health and disease. Trends Mol. Med. 13, 54-63.
17. Haslekås C., Breen K., Pedersen K. W., Johannessen L. E., Stang E., and, Madshus I. H., (2005) The inhibitory effect of ErbB2 on epidermal growth factor-induced formation of clathrin-coated pits correlates with retention of epidermal growth factor receptor-ErbB2 oligomeric complexes at the plasma membrane. Mol. Biol. Cell 16, 5832-5842.
18. Hasselblatt M., Lewczuk P., Löffler B. M., Kamrowski-Kruck H., von Ahsen N., Sirén A. L., and, Ehrenreich H., (2003) Effect of endothelin-1 on astrocytic protein content. Glia 42, 390-397.
19. Hsu J. M., Chen C. T., Chou C. K., et al. (2011) Crosstalk between Arg 1175 methylation and Tyr 1173 phosphorylation negatively modulates EGFR-mediated ERK activation. Nat. Cell Biol. 13, 174-181.
20. Johannessen L. E., Haugen K. E., Ostvold A. C., Stang E., and, Madshus I. H., (2001) Heterodimerization of the epidermal-growth-factor (EGF) receptor and ErbB2 and the affinity of EGF binding are regulated by different mechanisms. Biochem. J. 356, 87-96.
21. Jones R. B., Gordus A., Krall J. A., and, MacBeath G., (2006) A quantitative protein interaction network for the ErbB receptors using protein microarrays. Nature 439, 168-174.
22. Kallakuri S., Kreipke C. W., Schafer P. C., Schafer S. M., and, Rafols J. A., (2010) Brain cellular localization of endothelin receptors A and B in a rodent model of diffuse traumatic brain injury. Neuroscience 168, 820-830.
23. Kario E., Marmor M. D., Adamsky K., Citri A., Amit I., Amariglio N., Rechavi G., and, Yarden Y., (2005) Suppressors of cytokine signaling 4 and 5 regulate epidermal growth factor receptor signaling. J. Biol. Chem. 280, 7038-7048.
24. Kesarwala A. H., Samrakandi M. M., and, Piwnica-Worms D., (2009) Proteasome inhibition blocks ligand-induced dynamic processing and internalization of epidermal growth factor receptor via altered receptor ubiquitination and phosphorylation. Cancer Res. 69, 976-983.
25. Kreipke C. W., Reynolds C. A., Schafer P. C., Schafer S., Pirooz R., and, Rafols J. A., (2011) Endothelin receptors A and B are expressed in distinct cellular compartments of rat hippocampus following global ischemia: an immunocytochemical study. Neurol. Res. 33, 162-168.
26. Kuwaki T., Kurihara H., Cao W. H., Kurihara Y., Unekawa M., Yazaki Y., and, Kumada M., (1997) Physiological role of brain endothelin in the central autonomic control: from neuron to knockout mouse. Prog. Neurobiol. 51, 545-579.
27. Laux I., Jain A., Singh S., and, Agus D. B., (2006) Epidermal growth factor receptor dimerization status determines skin toxicity to HER-kinase targeted therapies. Br. J. Cancer 94, 85-92.
28. Lehmann C., Eisner F., and, Engele J., (2008) Role of endothelins as mediators of injury-induced alterations of glial glutamate turnover. J. Neurosci. Res. 86, 660-667.
29. Lehmann C., Bette S., and, Engele J., (2009) High extracellular glutamate modulates expression of glutamate transporters and glutamine synthetase in cultured astrocytes. Brain Res. 1297, 1-8.
30. Li N., Hill K. S., and, Elferink L. A., (2008) Analysis of receptor tyrosine kinase internalization using flow cytometry. Methods Mol. Biol. 457, 305-317.
31. Liebmann C., (2011) EGF receptor activation by GPCRs: an universal pathway reveals different versions. Mol. Cell. Endocrinol. 331, 222-231.
32. Liu B., and, Neufeld A. H., (2007) Activation of epidermal growth factor receptors in astrocytes: from development to neural injury. J. Neurosci. Res. 85, 3523-3529.
33. Liu B., Chen H., Johns T. G., and, Neufeld A. H., (2006) Epidermal growth factor receptor activation: an upstream signal for transition of quiescent astrocytes into reactive astrocytes after neural injury. J. Neurosci. 26, 7532-7540.
34. Longva K. E., Blystad F. D., Stang E., Larsen A. M., Johannessen L. E., and, Madshus I. H., (2002) Ubiquitination and proteasomal activity is required for transport of the EGF receptor to inner membranes of multivesicular bodies. J. Cell Biol. 156, 843-854.
35. Melikova M. S., Kondratov K. A., and, Kornilova E. S., (2006) Two different stages of epidermal growth factor (EGF) receptor endocytosis are sensitive to free ubiquitin depletion produced by proteasome inhibitor MG132. Cell Biol. Int. 30, 31-43.
36. Nicholson S. E., Metcalf D., Sprigg N. S., et al. (2005) Suppressor of cytokine signaling (SOCS)-5 is a potential negative regulator of epidermal growth factor signaling. Proc. Natl Acad. Sci. USA 102, 2328-2333.
37. Normanno N., De Luca A., Bianco C., Strizzi L., Mancino M., Maiello M. R., Carotenuto A., De Feo G., Caponigro F., and, Salomon D. S., (2006) Epidermal growth factor receptor (EGFR) signaling in cancer. Gene 366, 2-16.
38. Offterdinger M., and, Bastiaens P. I., (2008) Prolonged EGFR signalling by ERBB2-mediated sequestration at the plasma membrane. Traffic 9, 147-155.
39. Ohtsu H., Dempsey P. J., and, Eguchi S., (2006) ADAMs as mediators of EGF receptor transactivation by G protein-coupled receptors. Am. J. Physiol. Cell Physiol. 291, C1-C10.
40. Prasanna G., Krishnamoorthy R., and, Yorio T., (2011) Endothelin, astrocytes and glaucoma. Exp. Eye Res. 93, 170-177.
41. Roepstorff K., Grøvdal L., Grandal M., Lerdrup M., and, van Deurs B., (2008) Endocytic downregulation of ErbB receptors: mechanisms and relevance in cancer. Histochem. Cell Biol. 129, 563-578.
42. Rozengurt E., (2007) Mitogenic signaling pathways induced by G protein-coupled receptors. J. Cell. Physiol. 213, 589-602.
43. Rozyczka J., Figiel M., and, Engele J., (2004) Endothelins negatively regulate glial glutamate transporter expression. Brain Pathol. 14, 406-414.
44. Sadowski L., Pilecka I., and, Miaczynska M., (2009) Signaling from endosomes: location makes a difference. Exp. Cell Res. 315, 1601-1609.
45. Schinelli S., (2006) Pharmacology and physiopathology of the brain endothelin system: an overview. Curr. Med. Chem. 13, 627-638.
46. Schinelli S., Zanassi P., Paolillo M., Wang H., Feliciello A., and, Gallo V., (2001) Stimulation of endothelin B receptors in astrocytes induces cAMP response element-binding protein phosphorylation and c-fos expression via multiple mitogen-activated protein kinase signaling pathways. J. Neurosci. 21, 8842-8853.
47. Sharif A., and, Prevot V., (2010) ErbB receptor signaling in astrocytes: a mediator of neuron-glia communication in the mature central nervous system. Neurochem. Int. 57, 344-358.
48. Sheldon A. L., and, Robinson M. B., (2007) The role of glutamate transporters in neurodegenerative diseases and potential opportunities for intervention. Neurochem. Int. 51, 333-355.
49. Sheldon A. L., González M. I., Krizman-Genda E. N., Susarla B. T., and, Robinson M. B., (2008) Ubiquitination-mediated internalization and degradation of the astroglial glutamate transporter, GLT-1. Neurochem. Int. 53, 296-308.
50. Sirvent A., Benistant C., and, Roche S., (2008) Cytoplasmic signalling by the c-Abl tyrosine kinase in normal and cancer cells. Biol. Cell 100, 617-631.
51. Sofroniew M. V., and, Vinters H. V., (2010) Astrocytes: biology and pathology. Acta Neuropathol. 119, 7-35.
52. Sorkin A., and, Goh L. K., (2009) Endocytosis and intracellular trafficking of ErbBs. Exp. Cell Res. 315, 683-696.
53. Sweeney C., and, Carraway K. L. III, (2000) Ligand discrimination by ErbB receptors: differential signaling through differential phosphorylation site usage. Oncogene 19, 5568-5573.
54. Tanos B., and, Pendergast A. M., (2006) Abl tyrosine kinase regulates endocytosis of the epidermal growth factor receptor. J. Biol. Chem. 281, 32714-32723.
55. Unger T., Bette S., Zhang J., Theis M., and, Engele J., (2012) Connexin-deficiency affects expression levels of glial glutamate transporters within the cerebrum. Neurosci. Lett. 506, 12-16.
56. Wang Z., Zhang L., Yeung T. K., and, Chen X., (1999) Endocytosis deficiency of epidermal growth factor (EGF) receptor-ErbB2 heterodimers in response to EGF stimulation. Mol. Biol. Cell 10, 1621-1636.
57. Wang Q., Zhu F., and, Wang Z., (2007) Identification of EGF receptor C-terminal sequences 1005-1017 and di-leucine motif 1010LL1011 as essential in EGF receptor endocytosis. Exp. Cell Res. 313, 3349-3363.
58. Wu V. W., and, Schwartz J. P., (1998) Cell culture models for reactive gliosis: new perspectives. J. Neurosci. Res. 51, 675-681.
59. Yamazaki T., Zaal K., Hailey D., Presley J., Lippincott-Schwartz J., and, Samelson L. E., (2002) Role of Grb2 in EGF-stimulated EGFR internalization. J. Cell Sci. 115, 1791-1802.
60. Yi J. H., and, Hazell A. S., (2006) Excitotoxic mechanisms and the role of astrocytic glutamate transporters in traumatic brain injury. Neurochem. Int. 48, 394-403.
61. Yool A. J., (2007) Aquaporins: multiple roles in the central nervous system. Neuroscientist 13, 470-485.
62. von Zastrow M., and, Sorkin A., (2007) Signaling on the endocytic pathway. Curr. Opin. Cell Biol. 19, 436-445.
63. Zelenaia O., Schlag B. D., Gochenauer G. E., Ganel R., Song W., Beesley J. S., Grinspan J. B., Rothstein J. D., and, Robinson M. B., (2000) Epidermal growth factor receptor agonists increase expression of glutamate transporter GLT-1 in astrocytes through pathways dependent on phosphatidylinositol 3-kinase and transcription factor NF-kappaB. Mol. Pharmacol. 57, 667-678.