Spectraplakins promote microtubule-mediated axonal growth by functioning as structural microtubule-associated proteins and EB1-dependent + TIPs (tip interacting proteins)

Journal of Neuroscience

Volumn 32, Issue 27, 2012, Pages 9143-9158

  Alves Silva, Juliana ^a   Sánchez Soriano, Natalia ^a   Beaven, Robin ^a   Klein, Melanie ^a   Parkin, Jill ^a   Millard, Thomas H ^a   Bellen, Hugo J ^b   Venken, Koen J T ^b   Ballestrem, Christoph ^a   Kammerer, Richard A ^a,c   Prokop, Andreas ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c PAUL SCHERRER INSTITUTE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CYTOSKELETON PROTEIN; DROSOPHILA PROTEIN; END BINDING PROTEIN 1; FASCICLIN II; MICROTUBULE ASSOCIATED PROTEIN; SHOT PROTEIN; SPECTRAPLAKIN; TIP INTERACTING PROTEIN; TUBULIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DROSOPHILA; EMBRYO; FEMALE; FIBROBLAST; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MALE; MICROTUBULE ASSEMBLY; MOUSE; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; SEQUENCE ANALYSIS; WESTERN BLOTTING;

ACTINS; AMINO ACID MOTIFS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; AXONS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCKOUT TECHNIQUES; GROWTH CONES; MALE; MICE; MICROFILAMENT PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; MUTATION; NERVE TISSUE PROTEINS; NIH 3T3 CELLS; PRIMARY CELL CULTURE;

EID: 84863452328     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0416-12.2012     Document Type: Article

References (57)

1. Ahmad FJ, He Y, Myers KA, Hasaka TP, Francis F, Black MM, Baas PW (2006) Effects of dynactin disruption and dynein depletion on axonalmicrotubules. Traffic 7:524-537.
2. Akhmanova A, Steinmetz MO (2008) Tracking the ends: a dynamic protein network controls the fate of microtubule tips. Nat Rev Mol Cell Biol 9:309-322.
3. Alves-Silva J, Hahn I, Huber O, Mende M, Reissaus A, Prokop A (2008) Prominent actin fibre arrays in Drosophila tendon cells represent architectural elements different from stress fibres. Mol Biol Cell 19:4287-4297.
4. Applewhite DA, Grode KD, Keller D, Zadeh AD, Slep KC, Rogers SL (2010) The Spectraplakin Short stop is an actin-microtubule cross-linker that contributes to organization of the microtubule network. Mol Biol Cell 21:1714-1724.
5. Bielas SL, Serneo FF, Chechlacz M, Deerinck TJ, Perkins GA, Allen PB, Ellisman MH, Gleeson JG (2007) Spinophilin facilitates dephosphorylation of doublecortin by PP1 to mediate microtubule bundling at the axonal wrist. Cell 129:579-591.
6. Bottenberg W, Sánchez-Soriano N, Alves-Silva J, Hahn I, Mende M, Prokop A (2009) Context-specific requirements of functional domains of the Spectraplakin Short stop in vivo. Mech Dev 126:489-502.
7. Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401-415.
8. Campos-Ortega JA, Hartenstein V (1997) The embryonic development of Drosophila melanogaster. Berlin: Springer.
9. Chilton J, Gordon-Weeks P (2007) Role of microtubules and MAPs during neuritogenesis. In: Intracellular mechanisms for neuritogenesis (de Curtis I, ed), pp 57-88. New York: Springer.
10. Conde C, Cáceres A (2009) Microtubule assembly, organization and dynamics in axons and dendrites. Nat Rev Neurosci 10:319-332.
11. Dent EW, Gupton SL, Gertler FB (2011) The growth cone cytoskeleton in axon outgrowth and guidance. Cold Spring Harb Perspect Biol 3:pii: a001800.
12. Elliott SL, Cullen CF, Wrobel N, Kernan MJ, Ohkura H (2005) EB1 is essential during Drosophila development and plays a crucial role in the integrity of chordotonal mechanosensory organs. Mol Biol Cell 16:891-901.
13. Geraldo S, Khanzada UK, Parsons M, Chilton JK, Gordon-Weeks PR (2008) Targeting of the F-actin-binding protein drebrin by the microtubule plus-tip protein EB3 is required for neuritogenesis. Nat Cell Biol 10:1181-1189.
14. Gonçalves-Pimentel C, Gombos R, Mihály J, Sánchez-Soriano N, Prokop A (2011) Dissecting regulatory networks of filopodia formation in a Drosophila growth cone model. PLoS One 6:e18340.
15. Goriounov D, Leung CL, Liem RK (2003) Protein products of human Gas2-related genes on chromosomes 17 and 22 (hGAR17 and hGAR22) associate with both microfilaments and microtubules. J Cell Sci 116:1045-1058.
16. Goryunov D, He CZ, Lin CS, Leung CL, Liem RK (2010) Nervous-tissuespecific elimination of microtubule-actin crosslinking factor 1a results in multiple developmental defects in the mouse brain. Mol Cell Neurosci 44:1-14.
17. Gouveia SM, Akhmanova A (2010) Cell and molecular biology of microtubule plus end tracking proteins: end binding proteins and their partners. Int Rev Cell Mol Biol 285:1-74.
18. Grabham PW, Seale GE, Bennecib M, Goldberg DJ, Vallee RB (2007) Cytoplasmic dynein and LIS1 are required for microtubule advance during growth cone remodeling and fast axonal outgrowth. J Neurosci 27:5823-5834.
19. Groth AC, Olivares EC, Thyagarajan B, Calos MP (2000) A phage integrase directs efficient site-specific integration in human cells. Proc Natl Acad Sci U S A 97:5995-6000.
20. Honnappa S, Gouveia SM, Weisbrich A, Damberger FF, Bhavesh NS, Jawhari H, Grigoriev I, van Rijssel FJ, Buey RM, Lawera A, Jelesarov I, Winkler FK, Wuthrich K, Akhmanova A, Steinmetz MO (2009) An EB1-binding motif acts as a microtubule tip localization signal. Cell 138:366-376.
21. Hur EM, Saijilafu, Lee BD, Kim SJ, Xu WL, Zhou FQ (2011) GSK3 controls axon growth via CLASP-mediated regulation of growth cone microtubules. Genes Dev 25:1968-1981.
22. Janke C, Kneussel M (2010) Tubulin post-translational modifications: encoding functions on the neuronal microtubule cytoskeleton. Trends Neurosci 33:362-372.
23. Kodama A, Karakesisoglou I, Wong E, Vaezi A, Fuchs E (2003) ACF7. An essential integrator of microtubule dynamics. Cell 115:343-354.
24. Kuppers-Munther B, Letzkus JJ, Luer K, Technau G, Schmidt H, Prokop A (2004) A new culturing strategy optimises Drosophila primary cell cultures for structural and functional analyses. Dev Biol 269:459-478.
25. Lee S, Kolodziej PA (2002) Short stop provides an essential link between F-actin and microtubules during axon extension. Development 129:1195-1204.
26. Lee T, Luo L (1999) Mosaic analysis with a repressible neurotechnique cell marker for studies of gene function in neuronal morphogenesis. Neuron 22:451-461.
27. Letourneau PC (2009) Actin in axons: stable scaffolds and dynamic filaments. Results Probl Cell Differ 48:65-90.
28. Letourneau PC, Shattuck TA, Ressler AH (1987) "Pull" and "push" in neurite elongation: observations on the effects of different concentrations of cytochalasin B and taxol. Cell Motil Cytoskeleton 8:193-209.
29. Luo L, Liao YJ, Jan LY, Jan YN (1994) Distinct morphogenetic functions of similar small GTPases: Drosophila Drac1 is involved in axonal outgrowth and myoblast fusion. Genes Dev 8:1787-1802.
30. Morris M, Maeda S, Vossel K, Mucke L (2011) The many faces of tau. Neuron 70:410-426.
31. Prokop A, Uhler J, Roote J, Bate M (1998) The kakapo mutation affects terminal arborisation and central dendritic sprouting of Drosophila motorneurons. J Cell Biol 143:1283-1294.
32. Purro SA, Ciani L, Hoyos-Flight M, Stamatakou E, Siomou E, Salinas PC (2008) Wnt regulates axon behavior through changes in microtubule growth directionality: a new role for adenomatous polyposis coli. J Neurosci 28:8644-8654.
33. Qiang L, Yu W, Andreadis A, Luo M, Baas PW (2006) Tau protects microtubules in the axon from severing by katanin. J Neurosci 26:3120-3129.
34. Riederer BM (2007) Microtubule-associated protein 1B, a growthassociated and phosphorylated scaffold protein. Brain Res Bull 71:541-558.
35. Rogers SL, Rogers GC, Sharp DJ, Vale RD (2002) Drosophila EB1 is important for proper assembly, dynamics, and positioning of the mitotic spindle. J Cell Biol 158:873-884.
36. Röper K, Gregory SL, Brown NH (2002) The 'Spectraplakins': cytoskeletal giants with characteristics of both spectrin and plakin families. J Cell Sci 115:4215-4225.
37. Sánchez-Soriano N, Prokop A (2005) The influence of pioneer neurons on a growing motor nerve in Drosophila requires the neural cell adhesion molecule homolog FasciclinII. J Neurosci 25:78-87.
38. Sánchez-Soriano N, Travis M, Dajas-Bailador F, Gonçalves-Pimentel C, Whitmarsh AJ, Prokop A (2009) Mouse ACF7 and Drosophila Short stop modulate filopodia formation and microtubule organisation during neuronal growth. J Cell Sci 122:2534-2542.
39. Sánchez-Soriano N, Gonçalves-Pimentel C, Beaven R, Haessler U, Ofner-Ziegenfuss L, Ballestrem C, Prokop A (2010) Drosophila growth cones: a genetically tractable platform for the analysis of axonal growth dynamics. Dev Neurobiol 70:58-71.
40. Schneider I (1964) Differentiation of larval Drosophila eye-antennal discs in vitro. J Exp Zool 156:91-103.
41. Slep KC, Rogers SL, Elliott SL, Ohkura H, Kolodziej PA, Vale RD (2005) Structural determinants for EB1-mediated recruitment of APC and spectraplakins to the microtubule plus end. J Cell Biol 168:587-598.
42. Sonnenberg A, Liem RK (2007) Plakins in development and disease. Exp Cell Res 313:2189-2203.
43. Stroud MJ, Kammerer RA, Ballestrem C (2011) Characterization of G2L3 (GAS2-like 3), a new microtubule- and actin-binding protein related to spectraplakins. J Biol Chem 286:24987-24995.
44. Strumpf D, Volk T (1998) Kakapo, a novel Drosophila protein, is essential for the restricted localization of the neuregulin-like factor, Vein, at the muscle-tendon junctional site. J Cell Biol 143:1259-1270.
45. Subramanian A, Prokop A, Yamamoto M, Sugimura K, Uemura T, Betschinger J, Knoblich JA, Volk T (2003) Short stop recruits EB1/APC1 and promotes microtubule assembly at the muscle-tendon junction. Curr Biol 13:1086-1095.
46. Sun D, Leung CL, Liem RK (2001) Characterization of the microtubule binding domain of microtubule actin crosslinking factor (MACF): identification of a novel group of microtubule associated proteins. J Cell Sci 114:161-172.
47. Takei Y, Teng J, Harada A, Hirokawa N (2000) Defects in axonal elongation and neuronal migration in mice with disrupted tau and map1b genes. J Cell Biol 150:989-1000.
48. Teng J, Takei Y, Harada A, Nakata T, Chen J, Hirokawa N (2001) Synergistic effects of MAP2 and MAP1B knockout in neuronal migration, dendritic outgrowth, and microtubule organization. J Cell Biol 155:65-76.
49. Tymanskyj SR, Scales TM, Gordon-Weeks PR (2012) MAP1B enhances microtubule assembly rates and axon extension rates in developing neurons. Mol Cell Neurosci 49:110-119.
50. Venken KJ, He Y, Hoskins RA, Bellen HJ (2006) P[acman]: a BAC transgenic platform for targeted insertion of large DNA fragments in D. melanogaster. Science 314:1747-1751.
51. Viñals J, Kolinski A, Skolnick J (2002) Numerical study of the entropy loss of dimerization and the folding thermodynamics of the GCN4 leucine zipper. Biophys J 83:2801-2811.
52. Warming S, Costantino N, Court DL, Jenkins NA, Copeland NG (2005) Simple and highly efficient BAC recombineering using galK selection. Nucleic Acids Res 33:e36.
53. Wild J, Hradecna Z, Szybalski W (2002) Conditionally amplifiable BACs: switching from single-copy to high-copy vectors and genomic clones. Genome Res 12:1434-1444.
54. Wolff J (1998) Promotion of microtubule assembly by oligocations: cooperativity between charged groups. Biochemistry 37:10722-10729.
55. Wu X, Kodama A, Fuchs E (2008) ACF7 regulates cytoskeletal-focal adhesion dynamics and migration and has ATPase activity. Cell 135:137-148.
56. Wu X, Shen QT, Oristian DS, Lu CP, Zheng Q, Wang HW, Fuchs E (2011) Skin stem cells orchestrate directional migration by regulating microtubule-ACF7 connections through GSK3beta. Cell 144:341-352.
57. Yang Y, Bauer C, Strasser G, Wollman R, Julien JP, Fuchs E (1999) Integrators of the cytoskeleton that stabilize microtubules. Cell 98:229-238.