The Role of Microtubule-Associated Protein 2c in the Reorganization of Microtubules and Lamellipodia during Neurite Initiation

Journal of Neuroscience

Volumn 23, Issue 29, 2003, Pages 9479-9490

  Dehmelt, Leif ^a   Smart, Fiona M ^a   Ozer, Rachel S ^a,b   Halpain, Shelley ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b STANFORD UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Actin; Cell motility; Growth cone; Lamellipodia; MAP2; Microtubule associated proteins; Microtubules; Neurite

Indexed keywords

ACTIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; F ACTIN; MICROTUBULE ASSOCIATED PROTEIN 2; MICROTUBULE ASSOCIATED PROTEIN 2C; MUTANT PROTEIN; PACLITAXEL; UNCLASSIFIED DRUG; HYBRID PROTEIN; MAP2 PROTEIN, HUMAN; MICROTUBULE ASSOCIATED PROTEIN; MTAP2 PROTEIN, MOUSE; MTAP2 PROTEIN, RAT;

ARTICLE; CELL MOTILITY; CONTROLLED STUDY; CYTOSKELETON; GROWTH CONE; HIPPOCAMPUS; HUMAN; HUMAN CELL; LAMELLIPODIUM; MICROTUBULE; MICROTUBULE ORGANIZING CENTER; NERVE FIBER GROWTH; NEURITE; NEUROBLASTOMA CELL; PERIKARYON; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; ANIMAL; CELL DIFFERENTIATION; CELL LINE; CYTOLOGY; DOMINANT GENE; DRUG EFFECT; GENETIC TRANSFECTION; GENETICS; METABOLISM; MICROSCOPY; MOUSE; NERVE CELL; PHYSIOLOGY; PSEUDOPODIUM; RAT; ULTRASTRUCTURE;

ACTINS; ANIMALS; CELL DIFFERENTIATION; CELL LINE; CYCLIC AMP-DEPENDENT PROTEIN KINASES; GENES, DOMINANT; HIPPOCAMPUS; HUMANS; MICE; MICROSCOPY, VIDEO; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; NEURITES; NEURONS; PSEUDOPODIA; RATS; RECOMBINANT FUSION PROTEINS; TRANSFECTION;

EID: 0142182060     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-29-09479.2003     Document Type: Article

References (54)

1. Bernhardt R, Matus A (1984) Light and electron microscopic studies of the distribution of microtubule-associated protein 2 in rat brain: a difference between dendritic and axonal cytoskeleton. J Comp Neurol 226:203-221.
2. Bubb MR, Spector I, Beyer BB, Fosen KM (2000) Effects of jasplakinolide on the kinetics of actin polymerization: an explanation for certain in vivo observations. J Biol Chem 275:5163-5170.
3. Burgin KE, Ludin B, Ferralli J, Matus A (1994) Bundling of microtubules in transfected cells does not involve an autonomous dimerization site on the MAP2 molecule. Mol Biol Cell 5:511-517.
4. Caceres A, Banker GA, Binder L (1986) Immunocytochemical localization of tubulin and microtubule-associated protein 2 during the development of hippocampal neurons in culture. J Neurosci 6:714-722.
5. Caceres A, Mautino J, Kosik KS (1992) Suppression of MAP2 in cultured cerebellar macroneurons inhibits minor neurite formation. Neuron 9:607-618.
6. Condeelis J (1993) Life at the leading edge: the formation of cell protrusions. Annu Rev Cell Biol 9:411-444.
7. Cooper JA (1987) Effects of cytochalasin and phalloidin on actin. J Cell Biol 105:1473-1478.
8. Correas I, Padilla R, Avila J (1990) The tubulin-binding sequence of brain microtubule-associated proteins, tau and MAP-2, is also involved in actin binding. Biochem J 269:61-64.
9. Cunningham CC, LeClerc N, Flanagan LA, Lu M, Janmey PA, Kosik KS (1997) Microtubule-associated protein 2c reorganizes both microtubules and microfilaments into distinct cytological structures in an actin-binding protein-280-deficient melanoma cell line. J Cell Biol 136:845-857.
10. da Silva JS, Dotti CG (2002) Breaking the neuronal sphere: regulation of the actin cytoskeleton in neuritogenesis. Nat Rev Neurosci 3:694-704.
11. Daub H, Gevaert K, Vandekerckhove J, Sobel A, Hall A (2001) Rac/Cdc42 and p65PAK regulate the microtubule-destabilizing protein stathmin through phosphorylation at serine 16. J Biol Chem 276:1677-1680.
12. Dent EW, Kalil K (2001) Axon branching requires interactions between dynamic microtubules and actin filaments. J Neurosci 21:9757-9769.
13. DeTure MA, Zhang EY, Bubb MR, Purich DL (1996) In vitro polymerization of embryonic MAP-2c and fragments of the MAP-2 microtubule binding region into structures resembling paired helical filaments. J Biol Chem 271:32702-32706.
14. Dotti CG, Sullivan CA, Banker GA (1988) The establishment of polarity by hippocampal neurons in culture. J Neurosci 8:1454-1468.
15. Edson K, Weisshaar B, Matus A (1993) Actin depolymerisation induces process formation on MAP2-transfected non-neuronal cells. Development 117:689-700.
16. Ferralli J, Doll T, Matus A (1994) Sequence analysis of MAP2 function in living cells. J Cell Sci 107:3115-3125.
17. Fischer I, Shea TB, Sapirstein VS, Kosik KS (1986) Expression and distribution of microtubule-associated protein 2 (MAP2) in neuroblastoma and primary neuronal cells. Brain Res 390:99-109.
18. Fukata M, Watanabe T, Noritake J, Nakagawa M, Yamaga M, Kuroda S, Matsuura Y, Iwamatsu A, Perez F, Kaibuchi K (2002) Rac1 and Cdc42 capture microtubules through IQGAP1 and CLIP-170. Cell 109:873-885.
19. Goslin K, Asmussen H, Banker GA (1998) Rat hippocampal neurons in low density culture. In: Culturing nerve cells (Banker GA, Goslin K, eds), pp 339-370. Cambridge, MA: MIT.
20. Griffin CG, Letourneau PC (1980) Rapid retraction of neurites by sensory neurons in response to increased concentrations of nerve growth factor. J Cell Biol 86:156-161.
21. Harada A, Teng J, Takei Y, Oguchi K, Hirokawa N (2002) MAP2 is required for dendrite elongation, PKA anchoring in dendrites, and proper PKA signal transduction. J Cell Biol 158:541-549.
22. Jay DG (2000) The clutch hypothesis revisited: ascribing the roles of actin-associated proteins in filopodial protrusion in the nerve growth cone. J Neurobiol 44:114-125.
23. Kim H, Binder LI, Rosenbaum JL (1979) The periodic association of MAP2 with brain microtubules in vitro. J Cell Biol 80:266-276.
24. Kohrmann M, Haubensak W, Hemraj I, Kaether C, Lessmann VJ, Kiebler MA (1999) Fast, convenient, and effective method to transiently transfect primary hippocampal neurons. J Neurosci Res 58:831-835.
25. LeClerc N, Kosik KS, Cowan N, Pienkowski TP, Baas PW (1993) Process formation in Sf9 cells induced by the expression of a microtubule-associated protein 2C-like construct. Proc Natl Acad Sci USA 90:6223-6227.
26. Letourneau PC (1996) The cytoskeleton in nerve growth cone motility and axonal pathfinding. Perspect Dev Neurobiol 4:111-123.
27. 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.
28. Lewis SA, Ivanov IE, Lee G-H, Cowan NJ (1989) Organization of microtubules in dendrites and axons is determined by a short hydrophobic zipper in microtubule-associated proteins MAP2 and tau. Nature 342:498-505.
29. Luo L (2002) Actin cytoskeleton regulation in neuronal morphogenesis and structural plasticity. Annu Rev Cell Dev Biol 18:601-635.
30. Marsden KM, Doll T, Ferralli J, Botteri F, Matus A (1996) Transgenic expression of embryonic MAP2 in adult mouse brain: implications for neuronal polarization. J Neurosci 16:3265-3273.
31. Mitchison T, Kirschner M (1988) Cytoskeletal dynamics and nerve growth. Neuron 1:761-772.
32. Morales M, Fifkova E (1989) Distribution of MAP2 in dendritic spines and its colocalization with actin. Cell Tissue Res 256:447-456.
33. Ozer RS, Halpain S (2000) Phosphorylation-dependent localization of microtubule-associated protein MAP2c to the actin cytoskeleton. Mol Biol Cell 11:3573-3587.
34. Rotsch C, Radmacher M (2000) Drug-induced changes of cytoskeletal structure and mechanics in fibroblasts: an atomic force microscopy study. Biophys J 78:520-535.
35. Ruthel G, Hollenbeck PJ (2000) Growth cones are not required for initial establishment of polarity or differential axon branch growth in cultured hippocampal neurons. J Neurosci 20:2266-2274.
36. Salmon WC, Adams MC, Waterman-Storer CM (2002) Dual-wavelength fluorescent speckle microscopy reveals coupling of microtubule and actin movements in migrating cells. J Cell Biol 158:31-37.
37. Sattilaro W (1986) Interaction of microtubule-associated protein 2 with actin filaments. Biochemistry 25:2003-2009.
38. Schaefer AW, Kabir N, Forscher P (2002) Filopodia and actin arcs guide the assembly and transport of two populations of microtubules with unique dynamic parameters in neuronal growth cones. J Cell Biol 158:139-152.
39. Selden SC, Pollard TD (1983) Phosphorylation of microtubule-associated proteins regulates their interaction with actin filaments. J Biol Chem 258:7064-7071.
40. Selden SC, Pollard TD (1986) Interaction of actin filaments with microtubules is mediated by microtubule-associated proteins and regulated by phosphorylation. Ann NY Acad Sci 466:803-12:803-812.
41. Shea TB, Fischer I, Sapirstein VS (1985) Effect of retinoic acid on growth and morphological differentiation of mouse NB2a neuroblastoma cells in culture. Brain Res 353:307-314.
42. Spector I, Shocet NR, Blasberger D, Kashman Y (1989) Latrunculins-novel marine macrolides that disrupt microfilament organization and affect cell growth: I. Comparison with cytochalasin D. Cell Motil Cytoskeleton 13:127-144.
43. Suter DM, Forscher P (2000) Substrate-cytoskeletal coupling as a mechanism for the regulation of growth cone motility and guidance. J Neurobiol 44:97-113.
44. Takemura R, Okabe S, Umeyama T, Hirokawa N (1995) Polarity orientation and assembly process of microtubule bundles in nocodazole-treated, MAP2c-transfected COS cells. Mol Biol Cell 6:981-996.
45. Tang D, Goldberg DJ (2000) Bundling of microtubules in the growth cone induced by laminin. Mol Cell Neurosci 15:303-313.
46. 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.
47. Vijayaraghavan S, Liberty GA, Mohan J, Winfrey VP, Olson GE, Carr DW (1999) Isolation and molecular characterization of AKAP110, a novel, sperm-specific protein kinase A-anchoring protein. Mol Endocrinol 13:705-717.
48. Waterman-Storer CM, Salmon ED (1997) Actomyosin-based retrograde flow of microtubules in the lamella of migrating epithelial cells influences microtubule dynamic instability and turnover and is associated with microtubule breakage and treadmilling. J Cell Biol 139:417-434.
49. Waterman-Storer CM, Worthylake RA, Liu BP, Burridge K, Salmon ED (1999) Microtubule growth activates Rac1 to promote lamellipodial protrusion in fibroblasts. Nat Cell Biol 1:45-50.
50. Wille H, Mandelkow EM, Mandelkow E (1992) The juvenile microtubule-associated protein MAP2c is a rod-like molecule that forms antiparallel dimers. J Biol Chem 267:10737-10742.
51. Wittmann T, Waterman-Storer CM (2001) Cell motility: can Rho GTPases and microtubules point the way? J Cell Sci 114:3795-3803.
52. Wu G, Fang Y, Lu ZH, Ledeen RW (1998) Induction of axon-like and dendrite-like processes in neuroblastoma cells. J Neurocytol 27:1-14.
53. Yu W, Ling C, Baas PW (2001) Microtubule reconfiguration during axogenesis. J Neurocytol 30:861-875.
54. Zhou FQ, Waterman-Storer CM, Cohan CS (2002) Focal loss of actin bundles causes microtubule redistribution and growth cone turning. J Cell Biol 157:839-849.