μ-Opioids activate tyrosine kinase focal adhesion kinase and regulate cortical cytoskeleton proteins cortactin and vinculin in chick embryonic neurons

Journal of Neuroscience Research

Volumn 50, Issue 3, 1997, Pages 391-401

  Mangoura, Dimitra ^a,b  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

Chick embryo; Cortactin; FAK; G protein; Neuronal cultures; Opioid peptides; Src; Tyrosine kinases; Tyrosine phosphorylation; Vinculin

Indexed keywords

METENKEPHALIN; MU OPIATE RECEPTOR; PROTEIN TYROSINE KINASE; VINCULIN;

ANIMAL CELL; ARTICLE; BRAIN CORTEX; CELL ADHESION; CHICK EMBRYO; CYTOSKELETON; EMBRYO DEVELOPMENT; ENZYME ACTIVATION; ENZYME SUBSTRATE; NERVE CELL CULTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALS; CELL ADHESION MOLECULES; CELLS, CULTURED; CEREBRAL CORTEX; CHICK EMBRYO; CORTACTIN; CYTOSKELETAL PROTEINS; ENKEPHALIN, METHIONINE; ENZYME ACTIVATION; FOCAL ADHESION PROTEIN-TYROSINE KINASES; KINETICS; MICROFILAMENT PROTEINS; NEURONS; PHOSPHORYLATION; PHOSPHOTYROSINE; PROTEIN-TYROSINE KINASES; RECEPTORS, OPIOID, MU; VINCULIN;

EID: 0030708692     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4547(19971101)50:3<391::AID-JNR5>3.0.CO;2-D     Document Type: Article

References (73)

1. Alexandropoulos K, Baltimore D (1996): Coordinate activation of c-Src by SH3-and SH2-binding sites on a novel p130cas-related protein. Sin. Genes Dev 10:1341-1355.
2. Bennett V (1990): Spectrin-based membrane skeleton: A multipotential adapter between plasma membrane and cytoplasm. Annu Rev Biochem 54:273-304.
3. Bentley DB, O'Connor TP (1994): Cytoskeletal events in growth cone steering. Curr Opin Neurobiol 4:43-48.
4. Bishop J (1985): Viral oncogenes. Cell 42:23-28.
5. Bixby JL, Jhabvala P (1993): Tyrosine phosphorylation in early embryonic growth cones. J Neurosci 13:3421-3432.
6. Bockholt SM, Burridge K (1993): Cell spreading on extracellular matrix proteins induces tyrosine phosphorylation of tensin. J Biol Chem 268:14565-14567.
7. Burridge K, Turner CE, Romer LH (1992): Tyrosine phosphorylation of paxillin and pp125FAK accompanies cell adhesion to extracellular matrix: A role in cytoskeletal assembly. J Cell Biol 1059-1068.
8. Busquets X, Escriba PV, Sastre M, Garcia-Sevilla JA (1995) Loss of protein kinase C-αβ in brain of heroin addicts and morphine dependent rats. J Neurochem 64:247-252.
9. Calalb MB, Polte TR, Hanks SK (1995): Tyrosine phosphorylation of focal adhesion kinase at sites in the catalytic domain regulates kinase activity: A role for Src family kinases. Mol Cell Biol 15:954-963.
10. Chen Y, Mestek A, Liu J, Hurley JA, Yu L (1993): Molecular cloning and functional expression of a μ-opioid receptor from rat brain. Mol Pharmacol 44:8-12.
11. Chen YH, Pouyssegur J, Courtneidge S, Van Obberghen-Schilling E (1994): Activation of Src family kinase activity by the G protein-coupled thrombin receptor in growth-responsive fibroblasts. J Biol Chem 269:27372-27377.
12. Chen YH, Grall D, Salcini AE, Pelicci PG, Pouyssegur J, Van Obberghen-Schilling E (1996): Shc adaptor proteins are key transducers of mitogenic signaling mediated by the G protein-coupled thrombin receptor. EMBO 15:1037-1044.
13. Clark A, Brugge JS(1995): Integrins and signal transduction pathways: The road taken. Science 268:233-239.
14. FAK. Mol Cell Biol 14:147-155.
15. Cooper JA, Hunter T (1981): Changes in protein phosphorylation in Rous sarcoma virus-transformed chicken embryo cells. Mol Cell Biol 1:165-178.
16. Cypher C, Letourneau PC (1991): Identification of cytoskeletal focal adhesion and cell protein in growth cone particles isolated from developing chick brain. J Neurosci Res 30:259-265.
17. Depasquale JA, Izzard CS (1987): Evidence for an actin containing cytoplasmic precursors of the focal contact and the timing of incorporation of vinculin at the focal contact. J Cell Biol 105:2803-2809.
18. Fang KS, Sabe H, Saito H, Hanafusa H (1994): Comparative study of three protein-tyrosine phosphatases. J Biol Chem 269:20194-20200.
19. Force T, Kyriakis JM, Avruch J, Bonventre JV (1991): Endothelin vasopressin and angiotensin II enhance tyrosine phosphorylation hy protein kinase C-dependent and -independent pathways in glomerular mesangial cells. J Biol Chem 266:6650-6656.
20. Geiger B, Solomon D, Takechi M, Hynes RL (1992): A chimeric N cadherin beta-1 integrin receptor which localizes to both cell-cell and cell-matrix adhesions. J Cell Sci 103:943-951.
21. Geladopoulos T, Sakellaridis N, Vernadakis A (1988): Differential maturation of μ and δ opioid receptors in the chick embryonic-brain. Neurochem Res 12:279-288.
22. Gomez TM, Roche FK, Letourneau PC (1996): Chick sensory neuronal growth cones distinguish fibronectin from laminin by making substratum contacts that resemble focal contacts. J Neurobiol 29:18-34.
23. Grant SGN, Karl KA, Kiebler MA, Kandel ER (1995): Focal adhesion kinase in the brain: Novel subcellular localization and specific regulations by Fyn tyrosine kinase in mutant mice. Genes Dev 9:1909-1921.
24. Guan JL, Shalloway D (1992): Regulation of focal adhesion-associated protein tyrosine kinase by both cellular adhesion and oncogenic transformation. Nature 358:690-692.
25. Hamaguchi M, Grandori C, Hanafusa H (1988): Phosphorylation of cellular proteins in Rous sarcoma virus-infected cells: Analysis by use of anti-phosphotyrosine antibodies. Mol Cell Biol 8:3035-3042.
26. Hanks SK, Calalb MB, Harper MC, Patel SK (1992): Focal adhesion protein-tyrosine kinase phosphorylated in response to cell attachment to fibronectin. Proc Natl Acad Sci USA 89:8487-8491.
27. Hartwig JH, Thelen M, Rosen A, Nairn AC, Aderem A (1992): MARCKS is an actin filament crosslinking protein regulated by PKC and calcium-calmodulin. Nature 356:618-622.
28. Hausdorff WP, Pitcher JA, Luttrell DK, Linder ME, Kurose H, Parsons SJ, Caron MG, Lefkowitz RJ (1992): Tyrosine phosphorylation of G protein alpha subunits by pp60c-Src. Proc Natl Acad Sci USA 89:5720-5724.
29. Hauser K, Mangoura D (1997): Diversity of the endogenous opioid system in development: Novel signal transduction translates multiple extracellular signals into neural cell growth and differentiation. Perspect Dev Neurobiol (in press).
30. Hayashi Y, Mangoura D, Refetoff S (1996): Inhibition of thyroid hormone action by somatic gene transfer of a dominant negative mutant thyroid hormone. Receptor Mol Endocr 10:100-106.
31. Hennig A, Mangoura D, Schwartz NB (1993): Expression of large chondroitin sulfate proteoglycan in developing chick embryo telencephalon in ovo and in culture: Possible functional role. Brain Res 73:261-272.
32. Huckle WR, Prokop CA, Dy RC, Herman B, Earp S (1990): Angiotensin II stimulates protein-tyrosine phosphorylation in a calcium-dependent manner. Mol Cell Biol 10:6290-6298.
33. Hundle B, McMahon T, Dadgar J, Messing RO (1995): Overexpression of PKC-ε enhances nerve growth factor-induced phosphorylation of mitogen-activated protein kinases and neurite outgrowth. J Biol Chem 260:30134-30140.
34. Hunter T, Sefton BM (1980): Transforming gene product of Rous sarcoma virus phosphorylates tyrosine. Proc Natl Acad Sci USA 77:1311-1315.
35. Ignelzi MA, Miller DR, Soriano P, Maness PF (1994): Impaired neurite outgrowth of Src-minus cerebellar neurons on the cell adhesion molecule L1. Neuron 12:873-884.
36. Jiang H, Alexandropoulos K, Song J, Foster DA (1994): Evidence that v-Src-induced phospholipase D activity is mediated by a G protein. Mol Cell Biol 14:3676-3682.
37. 3 stimulates phospholipase C-γ in rat colonocytes: Role of c-src in PLC-γ activation. J Gastroenterol (in press).
38. FAK and paxillin are substrates for bradykinin-stimulated tyrosine phosphorylation in Swiss 3T3 cells. J Biol Chem 269:24328-24334.
39. Letourneau P, Shattuck TA (1989): Distribution and possible interactions of actin associated proteins and cell adhesion molecules of nerve growth cones. Development 105:505-519.
40. Levy JB, Dorai T, Wang L-H, Brugge JS (1987): The structurally distinct form of pp60Src detected in neuronal cells is encoded by a unique c-Src mRNA. Mol Cel Biol 7:4142-4145.
41. Lipfert L, Haimovich B, Schaller MD, Cobb BS, Parsons T, Brugge JS (1992): Integrin-dependent phosphorylation and activation of the protein tyrosine kinase pp125 in platelets. J Cell Biol 199:905-912.
42. Maher PA (1988): Nerve growth factor induces protein tyrosine phosphorylation. Proc Natl Acad Sci USA 85:6788-6791.
43. Maher PA, Pasquale EB, Wang JY, Singer SJ (1985): Phosphotyrosine-containing proteins are concentrated in focal adhesions and intercellular junctions in normal cells. Proc Natl Acad Sci USA 82:6576-6580.
44. Meiri KF, Gordon-Weeks PR (1990): GAP-43 in growth cones is associated with areas of membrane that are tightly bound to substrate and it is a component of a membrane skeleton subcellular fraction. J Neurosci 10:256-266.
45. Mangoura D (1994): Novel opioid receptor signal transduction pathways and regulation of neuronal plasticity. Neuropsychopharmacology Suppl 1 Plenary Lectures and Invited Symposia Abstracts CINP XIX Congress 818S S-191.
46. FAK and stimulate tyrosine phosphorylation of vinculin in chick embryonic neurons. J Neurochem S:45B.
47. Mangoura D, Dawson G (1991): Chronic opioid attenuates carbachol-mediated polyphosphoinositide hydrolysis in chick embryo neuronal culture. Brain Res 548:273-278.
48. Mangoura D, Dawson G (1993): Opioid peptides activate phospholipase D and protein kinase C-ε in chick embryo neuronal cultures. Proc Natl Acad Sci USA 90:2915-2919.
49. Mangoura D, Vernadakis A (1988): GABAergic neurons in cultures derived from three six-or eight-day-old chick embryos: A biochemical and immunocytochemical study. Dev Brain Res 40:37-46.
50. Mangoura D, Sakellaridis N, Vernadakis A (1988): Cholinergic neurons in cultures derived from three six-or eight-day-old chick embryos: A biochemical and immunocytochemical study. Dev Brain Res 40:25-36.
51. Mangoura D, Sogos V, Dawson G (1993): Protein kinase C-ε is a developmentally regulated neuronal isoform in the chick embryo central nervous system. J Neurosci Res 35:488-498.
52. Mangoura D, Sogos V, Dawson G (1995): Phorbol ester and PKC signaling regulate proliferation vimentin cytoskeleton assembly and glutamine synthetase activity of chick embryo cerebrum astrocytes in culture. Brain Res 87:1-11.
53. Meiri KF, Gordon-Weeks PR (1990): GAP-43 in growth cones is associated with areas of membrane that are tightly bound to substrate and it is a component of a membrane skeleton subcellular fraction. J Neurosci 10:256-266.
54. Nada S, Okada M, MacAuley A, Cooper JA, Nakagawa H (1991): Cloning of a complementary DNA for a protein-tyrosine kinase that specifically phosphorylates a negative regulatory site of p60c-src. Nature 351:69-72.
55. Rodriguez-Fernandez JL, Geiger B, Salomon D, Ben-Ze'ev A (1993): Suppression of vinculin expression by antisense transfectin confers changes in cell morphology motility and anchorage-dependent growth of 3T3 cells. J Cell Biol 122:1285-1294.
56. Sakellaridis N, Vernadakis A (1986): An unconventional response of adenylate cyclase to morphine and naloxone in the chicken during early development. Proc Natl Acad Sci USA 83:2738-2742.
57. Sakellaridis N, Mangoura D, Vernadakis A (1986): Effects of opiates on the growth of neuron-enriched cultures from chick embryonic brain. Int J Dev Neurosci 4:293-303.
58. Schaller MD, Borgman CA, Cobb BS, Vines RR, Reynolds AB, Parsons JT (1992): pp125FAKA structurally distinctive protein-tyrosine kinase associated with focal adhesions. Proc Natl Acad Sci USA 89:5192-5196.
59. Sefton BM, Hunter T, Ball EH, Singer SJ (1981): Vinculin: A cytoskeletal target of the transforming protein of Rous sarcoma virus. Cell 24:165-174.
60. FAK in platelets requires coordinated signalling through integrin and agonist receptors. J Biol Chem 269:14738-14745.
61. Simonson MS, Herman WH (1993): Protein kinase C and protein tyrosine kinase activity contribute to mitogenic signaling by endothelin-1. Cross-talk between G protein-coupled receptors and pp60c-Src. J Biol Chem 268:9347-9357.
62. Smart D, Lambert DG (1996): The stimulatory effects of opioids and their possible role in the development of tolerance. TIPS 17:264-269.
63. Sorge LK, Levy BT, Maness PF (1984): pp60c-Src is developmentally regulated in the neural retina. Cell 36:249-257.
64. Stephens RM, Loeb DM, Copeland TD, Pawson T, Greene LA, Kaplan DR (1994): Trk receptors use redundant signal transduction pathways involving SHC and PLC-gamma 1 to mediate NGF responses. Neuron 12:691-705.
65. Tsu RC, Chan JSC, Wong YH (1995): Regulation of multiple effectors by the cloned δ-opioid receptor: stimulation of phospholipase C and type II adenylyl cyclase. J Neurochem 64:2700-2707.
66. Turner CE (1993): Paxillin: A cytoskeletal target for tyrosine kinases. BioEssays 16:47-52.
67. FAK during development: Relation to paxillin. J Cell Sci 105:637-645.
68. Varnum-Finney B, Reichardt LF (1994): Vinculin-dependent PC 12 cell lines extend unstable lamellipodia and filopodia and have a reduced rate of neurite outgrowth. J Cell Biol 127:1071-1084.
69. Vernadakis A, Sakellaridis N, Geladopoulos T, Mangoura D (1990): Function of opioids early in embryogenesis. Ann NY Acad Sci 579:109-22.
70. Src substrate. Mol Cell Biol 11:5113-5124.
71. Xu W, Harrison SC, Eck M (1997): Three-dimensional structure of the tyrosine kinase c-src. Nature 385:595-602.
72. Zachary I, Sinnett-Smith J, Turner CE, Rozengurt E (1993): Bombesin vasopressin and endothelin rapidly stimulate tyrosine phosphorylation of the focal adhesion-associated protein paxillin in Swiss 3T3 cells. J Biol Chem 268:22060-22065.
73. Zhan X, Plourde C, Hu X, Friesel R, Maciag T (1994): Association of tibroblast growth factor receptor-1 with c-Src correlates with association between c-Src and cortactin. J Biol Chem 269:20221-20224.