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The Journal of Neuroscience, April 15, 2000, 20(8):2774-2782

Muscarinic Receptor Activation Promotes the Membrane Association of Tubulin for the Regulation of Gq-Mediated Phospholipase C₁ Signaling

Juliana S. Popova¹ and Mark M. Rasenick^{1, 2}

Departments of ¹ Physiology and Biophysics, and ² Psychiatry, University of Illinois at Chicago, College of Medicine, Chicago, Illinois 60612-7342

The microtubule protein tubulin regulates adenylyl cyclase and phospholipase C₁ (PLC₁) signaling via transactivation of the G-protein subunits Gs, Gi1, and Gq. Because most tubulin is not membrane associated, this study investigates whether tubulin translocates to the membrane in response to an agonist so that it might regulate G-protein signaling. This was studied in SK-N-SH neuroblastoma cells, which possess a muscarinic receptor-regulated PLC₁-signaling pathway. Tubulin, at nanomolar concentrations, transactivated Gq by the direct transfer of a GTP analog and potentiated carbachol-activated PLC₁. A specific and time-dependent association of tubulin with plasma membranes was observed when SK-N-SH cells were treated with carbachol. The same phenomenon was observed with membranes from Sf9 cells, expressing a recombinant PLC₁ cascade. The time course of this event was concordant both with transactivation of Gq by the direct transfer of [³²P]P³(4-azidoanilido)-P¹-5'-GTP from tubulin as well as with the activation of PLC₁. In SK-N-SH cells, carbachol induced a rapid and transient translocation of tubulin to the plasma membrane, microtubule reorganization, and a change in cell shape as demonstrated by confocal immunofluorescence microscopy. These observations presented a spatial and temporal resolution of the sequence of events underlying receptor-evoked involvement of tubulin in G-protein-mediated signaling. It is suggested that G-protein-coupled receptors might modulate cytoskeletal dynamics, intracellular traffic, and cellular architecture.

Key words: tubulin; microtubules; cytoskeleton; G-protein; phospholipase C; muscarinic receptor

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Copyright © 2000 Society for Neuroscience  0270-6474/00/2082774-09$05.00/0

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