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Cellular and Molecular Neurobiology

, Volume 27, Issue 6, pp 791–804 | Cite as

Pituicyte Stellation is Prevented by RhoA-or Cdc42-Dependent Actin Polymerization

  • Lia Rosso
  • Patricia M. Pierson
  • Claire Golfier
  • Brigitta Peteri-Brunbäck
  • Christophe Deroanne
  • Ellen Van Obberghen-Schilling
  • Jean-Marc Mienville
Original Paper

Abstract

Our aim was to shed light on different steps leading from metabotropic receptor activation to changes in cell shape, such as those that characterize the morphological plasticity of neurohypophysial astrocytes (pituicytes). Using explant cultures of adult rat pituicytes, we have previously established that adenosine A1 receptor activation induces stellation via inhibition of RhoA monomeric GTPase and subsequent disruption of actin stress fibers. Here, we rule out RhoA phosphorylation as a mechanism for that inhibition. Rather, our results are more consistent with involvement of a GTPase-activating protein (GAP). siRNA and pull-down experiments suggest that a step downstream of RhoA might involve Cdc42, another GTPase of the Rho family. However, RhoA activation, e.g., in the presence of serum, induces stress fibers, whereas direct Cdc42 activation appears to confine actin within a submembrane—i.e., cortical—network, which also prevents stellation. Therefore, we propose that RhoA may activate Cdc42 in parallel with an effector, such as p160Rho-kinase, that induces and maintains actin stress fibers in a dominant fashion. Rac1 is not involved in the stellation process per se but appears to induce a dendritogenic effect. Ultimately, it may be stated that pituicyte stellation is inducible upon mere actin depolymerization, and preventable upon actin organization, be it in the form of stress fibers or in a cortical configuration.

Keywords

Neurohypophysis Small GTPases Stress fibers Cortical actin Adenosine 

Notes

Acknowledgements

We are grateful to Anne-Sophie Coldefy for her help with western blot analysis. We thank Pierre Roux for giving us the Cdc42 and Rac1 mutants, and Gervaise Loirand and Pierre Chardin for the gift of RhoA mutants.

References

  1. Abe K, Saito H (1998) Adenosine stimulates stellation of cultured rat cortical astrocytes. Brain Res 804:63–71PubMedCrossRefGoogle Scholar
  2. Deroanne CF, Hamelryckx D, Ho TT, Lambert CA, Catroux P, Lapiere CM, Nusgens BV (2005) Cdc42 downregulates MMP-1 expression by inhibiting the ERK1/2 pathway. J Cell Sci 118:1173–1183PubMedCrossRefGoogle Scholar
  3. Ellerbroek SM, Wennerberg K, Burridge K (2003) Serine phosphorylation negatively regulates RhoA in vivo. J Biol Chem 278:19023–19031PubMedCrossRefGoogle Scholar
  4. Feoktistov I, Goldstein AE, Biaggioni I (2000) Cyclic AMP and protein kinase A stimulate Cdc42: role of A(2) adenosine receptors in human mast cells. Mol Pharmacol 58:903–910PubMedGoogle Scholar
  5. Fincham VJ, Chudleigh A, Frame MC (1999) Regulation of p190 Rho-GAP by v-Src is linked to cytoskeletal disruption during transformation. J Cell Sci 112:947–956PubMedGoogle Scholar
  6. Gadea G, Lapasset L, Gauthier-Rouviere C, Roux P (2002) Regulation of Cdc42-mediated morphological effects: a novel function for p53. EMBO J 21:2373–2382PubMedCrossRefGoogle Scholar
  7. Gasman S, Chasserot-Golaz S, Malacombe M, Way M, Bader MF (2004) Regulated exocytosis in neuroendocrine cells: a role for subplasmalemmal Cdc42/N-WASP-induced actin filaments. Mol Biol Cell 15:520–531PubMedCrossRefGoogle Scholar
  8. Gratzl M, Torp-Pedersen C, Daertt D, Treiman M, Thorn NA (1980) Isolation and characterization of secretory vesicles from bovine neurohypophyses. Hoppe Seylers Z Physiol Chem 361:1615–1628PubMedGoogle Scholar
  9. Hall A (1998) Rho GTPases and the actin cytoskeleton. Science 279:509–514PubMedCrossRefGoogle Scholar
  10. Harrington EO, Newton J, Morin N, Rounds S (2004) Barrier dysfunction and RhoA activation are blunted by homocysteine and adenosine in pulmonary endothelium. Am J Physiol Lung Cell Mol Physiol 287:L1091–1097PubMedCrossRefGoogle Scholar
  11. Hatton GI (1999) Astroglial modulation of neurotransmitter/peptide release from the neurohypophysis: present status. J Chem Neuroanat 16:203–222PubMedCrossRefGoogle Scholar
  12. Kreienbühl P, Keller H, Niggli V (1992) Protein phosphatase inhibitors okadaic acid and calyculin A alter cell shape and F-actin distribution and inhibit stimulus-dependent increases in cytoskeletal actin of human neutrophils. Blood 80:2911–2919PubMedGoogle Scholar
  13. Lang P, Gesbert F, Delespine-Carmagnat M, Stancou R, Pouchelet M, Bertoglio J (1996) Protein kinase A phosphorylation of RhoA mediates the morphological and functional effects of cyclic AMP in cytotoxic lymphocytes. EMBO J 15:510–519PubMedGoogle Scholar
  14. Miyata S, Furuya K, Nakai S, Bun H, Kiyohara T (1999) Morphological plasticity and rearrangement of cytoskeletons in pituicytes cultured from adult rat neurohypophysis. Neurosci Res 33:299–306PubMedCrossRefGoogle Scholar
  15. Morris JF, Pow DV, Shaw FD (1988) Release of neuropeptides from magnocellular neurons: does anatomical compartmentalization have a functional significance? In: Pickering BT, Wakerley JB, Summerlee AJS (eds), Neurosecretion: Cellular aspects of the production and release of neuropeptides, Plenum Press, New York, pp. 113–122Google Scholar
  16. Narumi S, Kimelberg HK, Bourke RS (1978) Effects of norepinephrine on the morphology and some enzyme activities of primary monolayer cultures from rat brain. J Neurochem 31:1479–1490PubMedCrossRefGoogle Scholar
  17. Patterson RL, van Rossum DB, Gill DL (1999) Store-operated Ca2+ entry: evidence for a secretion-like coupling model. Cell 98:487–499PubMedCrossRefGoogle Scholar
  18. Ramakers GJA, Moolenaar WH (1998) Regulation of astrocyte morphology by RhoA and lysophosphatidic acid. Exp Cell Res 245:252–262PubMedCrossRefGoogle Scholar
  19. Ramsell KD, Cobbett P (1997) Serum uncouples elevation of cyclic adenosine monophosphate concentration from cyclic adenosine monophosphate dependent morphological changes exhibited by cultured pituicytes. Neurosci Lett 226:41–44PubMedCrossRefGoogle Scholar
  20. Rolli-Derkinderen M, Sauzeau V, Boyer L, Lemichez E, Baron C, Henrion D, Loirand G, Pacaud P (2005) Phosphorylation of serine 188 protects RhoA from ubiquitin/proteasome-mediated degradation in vascular smooth muscle cells. Circ Res 96:1152–1160PubMedCrossRefGoogle Scholar
  21. Rosso L, Peteri-Brunbäck B, Vouret-Craviari V, Deroanne C, Troadec J-D, Thirion S, Van Obberghen-Schilling E, Mienville J-M. (2002a) RhoA inhibition is a key step in pituicyte stellation induced by A1-type adenosine receptor activation. Glia 38:351–362PubMedCrossRefGoogle Scholar
  22. Rosso L, Peteri-Brunbäck B, Vouret-Craviari V, Deroanne C, Van Obberghen-Schilling E, Mienville J-M. (2002b) Vasopressin and oxytocin reverse adenosine-induced pituicyte stellation via calcium-dependent activation of Cdc42. Eur J Neurosci 16:2324–2332PubMedCrossRefGoogle Scholar
  23. Roux P, Gauthier-Rouvière C, Doucet-Brutin S, Fort P (1997) The small GTPases Cdc42Hs, Rac1 and RhoG delineate Raf-independent pathways that cooperate to transform NIH3T3 cells. Curr Biol 7:629–637PubMedCrossRefGoogle Scholar
  24. Theodosis DT, Macvicar B (1996) Neurone-glia interactions in the hypothalamus and pituitary. Trends Neurosci 19:363–367PubMedCrossRefGoogle Scholar
  25. Vouret-Craviari V, Boulter E, Grall D, Matthews C, Van Obberghen-Schilling E (2004) ILK is required for the assembly of matrix-forming adhesions and capillary morphogenesis in endothelial cells. J Cell Sci 117:4559–4569PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • Lia Rosso
    • 1
    • 2
  • Patricia M. Pierson
    • 1
  • Claire Golfier
    • 1
  • Brigitta Peteri-Brunbäck
    • 1
  • Christophe Deroanne
    • 3
    • 4
  • Ellen Van Obberghen-Schilling
    • 3
  • Jean-Marc Mienville
    • 1
  1. 1.CNRS UMR 6548, Laboratoire de Physiologie Cellulaire et Moléculaire Faculté des SciencesUniversité de Nice-Sophia AntipolisNice Cedex 2France
  2. 2.Centre Intégratif de GénomiqueUniversité de LausanneLausanneSwitzerland
  3. 3.CNRS UMR 6543, Centre Antoine LacassagneUniversité de Nice-Sophia AntipolisNiceFrance
  4. 4.Laboratoire de Biologie des Tissus ConjonctifsSart-Tilman, Liège 1Belgium

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