Profilin isoforms modulate astrocytic morphology and the motility of astrocytic processes

PLoS ONE

Volumn 10, Issue 1, 2015, Pages

  Schweinhuber, Stefanie K ^a   Meβerschmidt, Tania ^a   Hänsch, Robert ^a   Korte, Martin ^a   Rothkegel, Martin ^a  

^a TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FORSKOLIN; PROFILIN; PROFILIN 1; PROFILIN 2A; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; ISOPROTEIN; SMALL INTERFERING RNA;

ANIMAL CELL; ARTICLE; ASTROCYTE; ASTROCYTE CULTURE; CELL MOTILITY; CELL STRUCTURE; CONTROLLED STUDY; DOWN REGULATION; ENZYME REGULATION; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; MOUSE; NONHUMAN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; ANIMAL; CELL CULTURE; CELL MOTION; CELL SHAPE; CYTOLOGY; DRUG EFFECTS; GENETICS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY;

MURINAE;

ANIMALS; ASTROCYTES; CELL MOVEMENT; CELL SHAPE; CELLS, CULTURED; COLFORSIN; DOWN-REGULATION; MICE; PHOSPHORYLATION; PROFILINS; PROTEIN ISOFORMS; RNA, SMALL INTERFERING;

EID: 84929144036     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0117244     Document Type: Article

References (69)

1. Perea G, Navarrete M, Araque A (2009) Tripartite synapses: astrocytes process and control synaptic information. Trends Neurosci 32: 421-431. doi: 10.1016/j.tins.2009.05.001 PMID: 19615761
2. Reichenbach A, Derouiche A, Kirchhoff F (2010) Morphology and dynamics of perisynaptic glia. Brain Res Rev 63: 11-25. doi: 10.1016/j.brainresrev.2010.02.003 PMID: 20176054
3. Oliet SH, Piet R, Poulain DA (2001) Control of glutamate clearance and synaptic efficacy by glial coverage of neurons. Science 292: 923-926. PMID: 11340204
4. Panatier A, Theodosis DT, Mothet JP, Touquet B, Pollegioni L, et al. (2006) Glia-derived D-serine controls NMDA receptor activity and synaptic memory. Cell 125: 775-784. PMID: 16713567
5. Jourdain P, Bergersen LH, Bhaukaurally K, Bezzi P, Santello M, et al. (2007) Glutamate exocytosis from astrocytes controls synaptic strength. Nat Neurosci 10: 331-339. PMID: 17310248
6. Genoud C, Quairiaux C, Steiner P, Hirling H, Welker E, et al. (2006) Plasticity of astrocytic coverage and glutamate transporter expression in adult mouse cortex. PLoS Biol 4: e343. PMID: 17048987
7. Haber M, Zhou L, Murai KK (2006) Cooperative astrocyte and dendritic spine dynamics at hippocampal excitatory synapses. J Neurosci 26: 8881-8891. PMID: 16943543
8. Goldman JE, Abramson B (1990) Cyclic AMP-induced shape changes of astrocytes are accompanied by rapid depolymerization of actin. Brain Res 528: 189-196. PMID: 1980224
9. Hatten ME (1985) Neuronal regulation of astroglial morphology and proliferation in vitro. J Cell Biol 100: 384-396. PMID: 3881455
10. Baorto DM, Mellado W, Shelanski ML (1992) Astrocyte process growth induction by actin breakdown. J Cell Biol 117: 357-367. PMID: 1313815
11. Racchetti G, D'Alessandro R, Meldolesi J (2012) Astrocyte stellation, a process dependent on Rac1 is sustained by the regulated exocytosis of enlargeosomes. Glia 60: 465-475. doi: 10.1002/glia.22280 PMID: 22144092
12. Ramakers GJ, Moolenaar WH (1998) Regulation of astrocyte morphology by RhoA and lysophosphatidic acid. Exp Cell Res 245: 252-262. PMID: 9851865
13. Jockusch BM, Murk K, RothkegelM (2007) The profile of profilins. Rev Physiol Biochem Pharmacol 159: 131-149. PMID: 17682948
14. Grantham J, Lassing I, Karlsson R (2012) Controlling the cortical actin motor. Protoplasma 249: 1001-1015. PMID: 22526202
15. WitkeW(2004) The role of profilin complexes in cell motility and other cellular processes. Trends Cell Biol 14: 461-469. PMID: 15308213
16. Ding Z, Bae YH, Roy P (2012) Molecular insights on context-specific role of profilin-1 in cell migration. Cell Adh Migr 6: 442-449. doi: 10.4161/cam.21832 PMID: 23076048
17. Polet D, Lambrechts A, Vandepoele K, Vandekerckhove J, Ampe C (2007) On the origin and evolution of vertebrate and viral profilins. FEBS Lett 581: 211-217. PMID: 17187785
18. Witke W, Sutherland JD, Sharpe A, Arai M, Kwiatkowski DJ (2001) Profilin I is essential for cell survival and cell division in early mouse development. Proc Natl Acad Sci U S A 98: 3832-3836. PMID: 11274401
19. Di Nardo A, Gareus R, Kwiatkowski D, WitkeW(2000) Alternative splicing of the mouse profilin II gene generates functionally different profilin isoforms. J Cell Sci 113 Pt 21: 3795-3803. PMID: 11034907
20. Lambrechts A, Braun A, Jonckheere V, Aszodi A, Lanier LM, et al. (2000) Profilin II is alternatively spliced, resulting in profilin isoforms that are differentially expressed and have distinct biochemical properties. Mol Cell Biol 20: 8209-8219. PMID: 11027290
21. Hu E, Chen Z, Fredrickson T, Zhu Y (2001) Molecular cloning and characterization of profilin-3: a novel cytoskeleton-associated gene expressed in rat kidney and testes. Exp Nephrol 9: 265-274. PMID: 11423726
22. Obermann H, Raabe I, Balvers M, Brunswig B, Schulze W, et al. (2005) Novel testis-expressed profilin IV associated with acrosome biogenesis and spermatid elongation. Mol Hum Reprod 11: 53-64.PMID: 15591451
23. Kullmann JA, Neumeyer A, Wickertsheim I, Bottcher RT, Costell M, et al. (2012) Purkinje cell loss and motor coordination defects in profilin1 mutant mice. Neuroscience 223: 355-364. doi: 10.1016/j. neuroscience.2012.07.055 PMID: 22864186
24. Pilo Boyl P, Di Nardo A, Mulle C, Sassoe-Pognetto M, Panzanelli P, et al. (2007) Profilin2 contributes to synaptic vesicle exocytosis, neuronal excitability, and novelty-seeking behavior. EMBO J 26: 2991-3002. PMID: 17541406
25. Neuhoff H, Sassoe-Pognetto M, Panzanelli P, Maas C, Witke W, et al. (2005) The actin-binding protein profilin I is localized at synaptic sites in an activity-regulated manner. Eur J Neurosci 21: 15-25. PMID: 15654839
26. Ackermann M, Matus A (2003) Activity-induced targeting of profilin and stabilization of dendritic spine morphology. Nat Neurosci 6: 1194-1200. PMID: 14555951
27. Murk K, Wittenmayer N, Michaelsen-Preusse K, Dresbach T, Schoenenberger CA, et al. (2012) Neuronal profilin isoforms are addressed by different signalling pathways. PLoS One 7: e34167. doi: 10. 1371/journal.pone.0034167 PMID: 22470532
28. Michaelsen K, Murk K, Zagrebelsky M, Dreznjak A, Jockusch BM, et al. (2010) Fine-tuning of neuronal architecture requires two profilin isoforms. Proc Natl Acad Sci U S A 107: 15780-15785. doi: 10.1073/ pnas.1004406107 PMID: 20798032
29. Molotkov D, Zobova S, Arcas JM, Khiroug L (2013) Calcium-induced outgrowth of astrocytic peripheral processes requires actin binding by Profilin-1. Cell Calcium 53: 338-348. doi: 10.1016/j.ceca.2013.03.001 PMID: 23578580
30. Kullmann JA, Neumeyer A, Gurniak CB, Friauf E, Witke W, et al. (2012) Profilin1 is required for glial cell adhesion and radial migration of cerebellar granule neurons. EMBO Rep 13: 75-82. doi: 10.1038/ embor.2011.211 PMID: 22081137
31. Witke W, Podtelejnikov AV, Di Nardo A, Sutherland JD, Gurniak CB, et al. (1998) In mouse brain profilin I and profilin II associate with regulators of the endocytic pathway and actin assembly. EMBO J 17: 967-976. PMID: 9463375
32. Murk K, Buchmeier S, Jockusch BM, Rothkegel M (2009) In birds, profilin-2a is ubiquitously expressed and contributes to actin-based motility. J Cell Sci 122: 957-964. doi: 10.1242/jcs.041715 PMID: 19258389
33. Gorlich A, Zimmermann AM, Schober D, Bottcher RT, Sassoe-Pognetto M, et al. (2012) Preserved morphology and physiology of excitatory synapses in profilin1-deficient mice. PLoS One 7: e30068.doi: 10.1371/journal.pone.0030068 PMID: 22253883
34. Murk K, Blanco Suarez EM, Cockbill LM, Banks P, Hanley JG (2013) The antagonistic modulation of Arp2/3 activity by N-WASP, WAVE2 and PICK1 defines dynamic changes in astrocyte morphology. J Cell Sci 126: 3873-3883. doi: 10.1242/jcs.125146 PMID: 23843614
35. Kase H, Iwahashi K, Nakanishi S, Matsuda Y, Yamada K, et al. (1987) K-252 compounds, novel and potent inhibitors of protein kinase C and cyclic nucleotide-dependent protein kinases. Biochem Biophys Res Commun 142: 436-440. PMID: 3028414
36. Nolle A, Zeug A, van Bergeijk J, Tonges L, Gerhard R, et al. (2011) The spinal muscular atrophy disease protein SMN is linked to the Rho-kinase pathway via profilin. Hum Mol Genet 20: 4865-4878. doi: 10.1093/hmg/ddr425 PMID: 21920940
37. Da Silva JS, Medina M, Zuliani C, Di Nardo A, Witke W, et al. (2003) RhoA/ROCK regulation of neuritogenesis via profilin IIa-mediated control of actin stability. J Cell Biol 162: 1267-1279. PMID: 14517206
38. Mayboroda O, Schluter K, Jockusch BM (1997) Differential colocalization of profilin with microfilaments in PtK2 cells. Cell Motil Cytoskeleton 37: 166-177. PMID: 9186014
39. Stuven T, Hartmann E, Gorlich D (2003) Exportin 6: a novel nuclear export receptor that is specific for profilin. actin complexes. EMBO J 22: 5928-5940. PMID: 14592989
40. Skare P, Kreivi JP, Bergstrom A, Karlsson R (2003) Profilin I colocalizes with speckles and Cajal bodies: a possible role in pre-mRNA splicing. Exp Cell Res 286: 12-21. PMID: 12729790
41. Rawe VY, Payne C, Schatten G (2006) Profilin and actin-related proteins regulate microfilament dynamics during early mammalian embryogenesis. Hum Reprod 21: 1143-1153. PMID: 16428331
42. Cho SY, Klemke RL (2002) Purification of pseudopodia from polarized cells reveals redistribution and activation of Rac through assembly of a CAS/Crk scaffold. J Cell Biol 156: 725-736. PMID: 11839772
43. Thomsen R, Lade Nielsen A (2011) A Boyden chamber-based method for characterization of astrocyte protrusion localized RNA and protein. Glia 59: 1782-1792. doi: 10.1002/glia.21223 PMID: 21858875
44. Star EN, Kwiatkowski DJ, Murthy VN (2002) Rapid turnover of actin in dendritic spines and its regulation by activity. Nat Neurosci 5: 239-246. PMID: 11850630
45. Cahoy JD, Emery B, Kaushal A, Foo LC, Zamanian JL, et al. (2008) A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J Neurosci 28: 264-278. doi: 10.1523/JNEUROSCI.4178-07.2008 PMID: 18171944
46. Lovatt D, Sonnewald U, Waagepetersen HS, Schousboe A, HeW, et al. (2007) The transcriptome and metabolic gene signature of protoplasmic astrocytes in the adult murine cortex. J Neurosci 27: 12255-12266. PMID: 17989291
47. Doyle JP, Dougherty JD, Heiman M, Schmidt EF, Stevens TR, et al. (2008) Application of a translational profiling approach for the comparative analysis of CNS cell types. Cell 135: 749-762. doi: 10.1016/j. cell.2008.10.029 PMID: 19013282
48. Seamon KB, Padgett W, Daly JW (1981) Forskolin: unique diterpene activator of adenylate cyclase in membranes and in intact cells. Proc Natl Acad Sci U S A 78: 3363-3367. PMID: 6267587
49. Perez V, Bouschet T, Fernandez C, Bockaert J, Journot L (2005) Dynamic reorganization of the astrocyte actin cytoskeleton elicited by cAMP and PACAP: a role for phosphatidylInositol 3-kinase inhibition. Eur J Neurosci 21: 26-32. PMID: 15654840
50. Murray AJ (2008) Pharmacological PKA inhibition: all may not be what it seems. Sci Signal 1: re4. doi: 10.1126/scisignal.122re4 PMID: 18523239
51. Won CL, Oh YS (2000) cAMP-induced stellation in primary astrocyte cultures with regional heterogeneity. Brain Res 887: 250-258. PMID: 11134613
52. Fang KM, Liu YY, Lin CH, Fan SS, Tsai CH, et al. (2012) Mps one binder 2 gene upregulation in the stellation of astrocytes induced by cAMP-dependent pathway. J Cell Biochem 113: 3019-3028. doi: 10.1002/jcb.24180 PMID: 22566124
53. Sathish K, Padma B, Munugalavadla V, Bhargavi V, Radhika KVN, et al. (2004) Phosphorylation of profilin regulates its interaction with actin and poly (L-proline). Cellular Signalling 16: 589-596. PMID: 14751544
54. Vemuri B, Singh SS (2001) Protein kinase C isozyme-specific phosphorylation of profilin. Cell Signal 13: 433-439. PMID: 11384842
55. Shao J, Welch WJ, Diprospero NA, Diamond MI (2008) Phosphorylation of profilin by ROCK1 regulates polyglutamine aggregation. Mol Cell Biol 28: 5196-5208. doi: 10.1128/MCB.00079-08 PMID: 18573880
56. Minichiello L (2009) TrkB signalling pathways in LTP and learning. Nat Rev Neurosci 10: 850-860. doi: 10.1038/nrn2738 PMID: 19927149
57. Grandoch M, Roscioni SS, Schmidt M (2010) The role of Epac proteins, novel cAMP mediators, in the regulation of immune, lung and neuronal function. Br J Pharmacol 159: 265-284. doi: 10.1111/j.1476- 5381.2009.00458.x PMID: 19912228
58. Treisman R (2013) Shedding light on nuclear actin dynamics and function. Trends Biochem Sci 38: 376-377. doi: 10.1016/j.tibs.2013.06.004 PMID: 23810602
59. Sands WA, Palmer TM (2008) Regulating gene transcription in response to cyclic AMP elevation. Cell Signal 20: 460-466. PMID: 17993258
60. Miki T, Okawa K, Sekimoto T, Yoneda Y, Watanabe S, et al. (2009) mDia2 shuttles between the nucleus and the cytoplasm through the importin-{alpha}/{beta}- and CRM1-mediated nuclear transport mechanism. J Biol Chem 284: 5753-5762. doi: 10.1074/jbc.M806191200 PMID: 19117945
61. Lorente G, Syriani E, Morales M (2014) Actin filaments at the leading edge of cancer cells are characterized by a high mobile fraction and turnover regulation by profilin I. PLoS One 9: e85817. doi: 10. 1371/journal.pone.0085817 PMID: 24465723
62. Ventura R, Harris KM (1999) Three-dimensional relationships between hippocampal synapses and astrocytes. J Neurosci 19: 6897-6906. PMID: 10436047
63. Bernardinelli Y, Randall J, Janett E, Nikonenko I, Konig S, et al. (2014) Activity-dependent structural plasticity of perisynaptic astrocytic domains promotes excitatory synapse stability. Curr Biol 24: 1679-1688. doi: 10.1016/j.cub.2014.06.025 PMID: 25042585
64. Robel S, Bardehle S, Lepier A, Brakebusch C, Gotz M (2011) Genetic deletion of cdc42 reveals a crucial role for astrocyte recruitment to the injury site in vitro and in vivo. J Neurosci 31: 12471-12482. doi: 10.1523/JNEUROSCI.2696-11.2011 PMID: 21880909
65. Stoppini L, Buchs PA, Muller D (1991) A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 37: 173-182. PMID: 1715499
66. Zufferey R, Nagy D, Mandel RJ, Naldini L, Trono D (1997) Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo. Nat Biotechnol 15: 871-875. PMID: 9306402
67. Naldini L, Blomer U, Gallay P, Ory D, Mulligan R, et al. (1996) In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272: 263-267. PMID: 8602510
68. Phair RD, Gorski SA, Misteli T (2004) Measurement of dynamic protein binding to chromatin in vivo, using photobleaching microscopy. Methods Enzymol 375: 393-414. PMID: 14870680
69. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, et al. (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9: 676-682. doi: 10.1038/nmeth.2019 PMID: 22743772