Role of the Microtubule Destabilizing Proteins SCG10 and Stathmin in Neuronal Growth

Journal of Neurobiology

Volumn 58, Issue 1, 2004, Pages 60-69

  Grenningloh, Gabriele ^a   Soehrman, Sophia ^a   Bondallaz, Percy ^a   Ruchti, Evelyne ^a   Cadas, Hugues ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

Growth cone; Microtubule dynamics; Neurite outgrowth; SCG10; Stathmin

Indexed keywords

CYTOSKELETON PROTEIN; MICROTUBULE DESTABILIZING PROTEIN SCG10; STATHMIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; CELLULAR DISTRIBUTION; CYTOSOL; DYNAMICS; GROWTH CONE; HUMAN; MICROTUBULE; NERVE CELL GROWTH; NERVE FIBER GROWTH; NERVE REGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; MICROTUBULE PROTEINS; MICROTUBULES; NERVE GROWTH FACTORS; NEURITES; PHOSPHOPROTEINS; STATHMIN;

EID: 0346750741     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/neu.10279     Document Type: Review

References (56)

1. Ahmad FJ, Pienkowski TP, Baas PW. 1993. Regional differences in microtubule dynamics in the axon. J Neurosci 13:856-866.
2. Antonsson B, Kassel DB, Di Paolo G, Lutjens R, Riederer BM, Grenningloh G. 1998. Identification of in vitro phosphorylation sites in the growth cone protein SCG10. Effect of phosphorylation site mutants on microtubule-destabilizing activity. J Biol Chem 273:8439-8446.
3. Baas PW, Deitch JS, Black MM, Banker GA. 1988. Polarity orientation of microtubules in hippocampal neurons: uniformity in the axon and nonuniformity in the dendrite. Proc Natl Acad Sci USA 85:8335-8339.
4. Baas PW, White LA, Heidemann SR. 1987. Microtubule polarity reversal accompanies regrowth of amputated neurites. Proc Natl Acad Sci USA 84:5272-5276.
5. Belmont L, Mitchison TJ. 1996. Identification of a protein that interacts with tubulin dimers and increases the catastrophe rate of microtubules. Cell 84:623-631.
6. Challacombe JF, Snow DM, Letourneau PC. 1997. Dynamic microtubule ends are required for growth cone turning to avoid an inhibitory guidance cue. J Neurosci 17:3085-3095.
7. Charbaut E, Curmi PA, Ozon S, Lachkar S, Redeker V, Sobel A. 2001. Stathmin family proteins display specific molecular and tubulin binding properties. J Biol Chem 276:16146-16154.
8. Chneiweiss H, Beretta L, Cordier J, Boutterin MC, Glowinski J, Sobel A. 1989. Stathmin is a major phosphoprotein and cyclic AMP-dependent protein kinase substrate in mouse brain neurons but not in astrocytes in culture: regulation during ontogenesis. J Neurochem 53:856-863.
9. Desai A, Mitchison TJ. 1997. Microtubule polymerization dynamics. Annu Rev Cell Dev Biol 13:83-117.
10. Desai A, Verma S, Mitchison TJ, Walczak CE. 1999. Kin I kinesins are microtubule-destabilizing enzymes. Cell 96:69-78.
11. Di Paolo G, Antonsson B, Kassel D, Riederer BM, Grenningloh G. 1997a. Phosphorylation regulates the microtubule-destabilizing activity of stathmin and its interaction with tubulin. FEBS Lett 416:149-152.
12. Di Paolo G, Lutjens R, Osen-Sand A, Sobel A, Catsicas S, Grenningloh G. 1997b. Differential distribution of stathmin and SCG10 in developing neurons in culture. J Neurosci Res 50:1000-1009.
13. Di Paolo G, Lutjens R, Pellier V, Stimpson SA, Beuchat MH, Catsicas S, Grenningloh G. 1997c. Targeting of SCG10 to the area of the Golgi complex is mediated by its NH2-terminal region. J Biol Chem 272:5175-5182.
14. Di Paolo G, Pellier V, Catsicas M, Antonsson B, Catsicas S, Grenningloh G. 1996. The phosphoprotein stathmin is essential for nerve growth factor-stimulated differentiation. J Cell Biol 133:1383-1390.
15. DiTella MC, Feiguin F, Carri N, Kosik KS, Caceres A. 1996. MAP-1B/TAU functional redundancy during laminin-enhanced axonal growth. J Cell Sci 109:467-477.
16. Fleury D, Grenningloh G, Lafanechere L, Antonsson B, Job D, Cohen-Addad C. 2000. Preliminary crystallographic study of a complex formed between the alpha/beta-tubulin heterodimer and the neuronal growth-associated protein SCG10. J Struct Biol 131:156-158.
17. Fukunaga K, Miyamoto E. 1998. Role of MAP kinase in neurons. Mol Neurobiol 16:79-95.
18. Glick JL, Meigs TE, Miron A, Casey PJ. 1998. RGSZ1, a Gz-selective regulator of G protein signaling whose action is sensitive to the phosphorylation state of Gzalpha. J Biol Chem 273:26008-26013.
19. Gonzalez-Billault C, Owen R, Gordon-Weeks PR, Avila J. 2002. Microtubule-associated protein 1B is involved in the initial stages of axonogenesis in peripheral nervous system cultured neurons. Brain Res 943:56-67.
20. Gordon-Weeks PR. 1991. Evidence for microtubule capture by filopodial actin filaments in growth cones. NeuroReport 2:573-576.
21. Heidemann SR, Landers JM, Hamborg MA. 1981. Polarity orientation of axonal microtubules. J Cell Biol 91:661-665.
22. Hirokawa N. 1994. Microtubule organization and dynamics dependent on microtubule-associated proteins. Curr Opin Cell Biol 6:74-81.
23. Holmfeldt P, Larsson N, Segerman B, Howell B, Morabito J, Cassimeris L, Gullberg M. 2001. The catastrophe-promoting activity of ectopic Op18/stathmin is required for disruption of mitotic spindles but not interphase microtubules. Mol Biol Cell 12:73-83.
24. Howell B, Larsson N, Gullberg M, Cassimeris L. 1999. Dissociation of the tubulin-sequestering and microtubule catastrophe-promoting activities of oncoprotein 18/stathmin. Mol Biol Cell 10:105-118.
25. Igarashi M, Tagaya M, Komiya Y. 1997. The soluble N-ethylmaleimide-sensitive factor attached protein receptor complex in growth cones: molecular aspects of the axon terminal development. J Neurosci 17:1460-1470.
26. Jourdain L, Curmi P, Sobel A, Pantaloni D, Carlier MF. 1997. Stathmin: a tubulin-sequestering protein which forms a ternary T2S complex with two tubulin molecules. Biochemistry 36:10817-10821.
27. Letourneau PC. 1996. The cytoskeleton in nerve growth cone motility and axonal pathfinding. Perspect Dev Neurobiol 4:111-123.
28. Letourneau PC, Ressler AH. 1984. Inhibition of neurite initiation and growth by taxol. J Cell Biol 98:1355-1362.
29. Liedtke W, Leman EE, Fyffe RE, Raine CS, Schubart UK. 2002. Stathmin-deficient mice develop an age-dependent axonopathy of the central and peripheral nervous systems. Am J Pathol 160:469-480.
30. Liu Z, Chatterjee TK, Fisher RA. 2002. RGS6 interacts with SCG10 and promotes neuronal differentiation. 2002. Role of the G gamma subunit-like (GGL) domain of RGS6. J Biol Chem 277:37832-37839.
31. Lutjens R, Igarashi M, Pellier-Monnin V, Blasey H, Di Paolo G, Ruchti E, Pfulg C, Staple J, Catsicas S, Grenningloh G. 2000. Localization and targeting of SCG10 to the trans Golgi apparatus and to growth cone vesicles. Eur J Neurosci 12:2224-2234.
32. Manceau V, Gavet O, Curmi P, Sobel A. 1999. Stathmin interaction with HSC70 family proteins. Electrophoresis 20:409-417.
33. Mason MR, Lieberman AR, Grenningloh G, Anderson PN. 2002. Transcriptional upregulation of SCG10 and CAP-23 is correlated with regeneration of the axons of peripheral and central neurons in vivo. Mol Cell Neurosci 20:595-615.
34. Matus A. 1988. Microtubule-associated proteins: their potential role in determining neuronal morphology. Annu Rev Neurosci 11:29-44.
35. Maucuer A, Camonis JH, Sobel A. 1995. Stathmin interaction with a putative kinase and coiled-coil-forming protein domains. Proc Natl Acad Sci USA 92:3100-3104.
36. Mistry SJ, Atweh GF. 2002. Role of stathmin in the regulation of the mitotic spindle: potential applications in cancer therapy. Mt Sinai J Med 69:299-304.
37. Mitchison T, Kirschner MW. 1984. Dynamic instability of microtubule growth. Nature 312:237-242.
38. Morishima-Kawashima M, Kosik KS. 1996. The pool of map kinase associated with microtubules is small but constitutively active. Mol Biol Cell 7:893-905.
39. Neidhart S, Antonsson B, Gillieron C, Vilbois F, Grenningloh G, Arkinstall S. 2001. c-Jun N-terminal kinase-3 (JNK3)/stress-activated protein kinase-beta (SAPKbeta) binds and phosphorylates the neuronal microtubule regulator SCG10. FEBS Lett 508:259-264.
40. Nixon AB, Grenningloh G, Casey PJ. 2002. The interaction of RGSZI with SCG10 attenuates the ability of SCG10 to promote microtubule disassembly. J Biol Chem 277:18127-18133.
41. Ozon S, El Mestikawy S, Sobel A. 1999. Differential, regional, and cellular expression of the stathmin family transcripts in the adult rat brain. J Neurosci Res 56:553-564.
42. Pellier-Monnin V, Astic L, Bichet S, Riederer BM, Grenningloh G. 2001. Expression of SCG10 and stathmin proteins in the rat olfactory system during development and axonal regeneration. J Comp Neurol 433:239-254.
43. Pfenninger KH, Ellis L, Johnson MP, Friedman LB, Somlo S. 1983. Nerve growth cones isolated from fetal rat brain: subcellular fractionation and characterization. Cell 35:573-584.
44. Pigino G, Paglini G, Ulloa L, Avila J, Caceres A. 1997. Analysis of the expression, distribution and function of cyclin dependent kinase 5 (cdk5) in developing cerebellar macroneurons. J Cell Sci 110:257-270.
45. Riederer BM, Pellier V, Antonsson B, Di Paolo G, Stimpson SA, Lutjens R, Catsicas S, Grenningloh G. 1997. Regulation of microtubule dynamics by the neuronal growth-associated protein SCG10. Proc Natl Acad Sci USA 94:741-745.
46. Rochlin MW, Wickline KM, Bridgman PC. 1996. Microtubule stability decreases axon elongation but not axoplasm production. J Neurosci 16:3236-3246.
47. Schubart UK, Yu J, Amat JA, Wang Z, Hoffmann MK, Edelmann W. 1996. Normal development of mice lacking metablastin (P19), a phosphoprotein implicated in cell cycle regulation. J Biol Chem 271:14062-14066.
48. Sobel A. 1991. Stathmin: a relay phosphoprotein for multiple signal transduction? Trends Biochem Sci 16:301-305.
49. Stein R, Mori N, Matthews K, Lo LC, Anderson DJ. 1988. The NGF-inducible SCG10 mRNA encodes a novel membrane-bound protein present in growth cones and abundant in developing neurons. Neuron 1:463-476.
50. Takei Y, Kondo S, Harada A, Inomata S, Noda T, Hirokawa N. 1997. Delayed development of nervous system in mice homozygous for disrupted microtubule-associated protein 1B (MAP1B) gene. J Cell Biol 137:1615-1626.
51. Takei Y, Teng J, Harada A, Hirokawa N. 2000. Defects in axonal elongation and neuronal migration in mice with disrupted tau and maplb genes. J Cell Biol 150:989-1000.
52. Tanaka E, Sabry J. 1995. Making the connection: cytoskeletal rearrangements during growth cone guidance. Cell 83:171-176.
53. Tanaka EM, Kirschner MW. 1991. Microtubule behavior in the growth cones of living neurons during axon elongation. J Cell Biol 115:345-363.
54. Tessier-Lavigne M, Goodman CS. 1996. The molecular biology of axon guidance. Science 274:1123-1133.
55. Walker RA, O'Brien ET, Pryer NK, Soboeiro MF, Voter WA, Erickson HP, Salmon ED. 1988. Dynamic instability of individual microtubules analyzed by video light microscopy: rate constants and transition frequencies. J Cell Biol 107:1437-1448.
56. Williamson T, Gordon-Weeks PR, Schachner M, Taylor J. 1996. Microtubule reorganization is obligatory for growth cone turning. Proc Natl Acad Sci USA 93:15221-15226.