Ca2+-dependent regulation of Rho GTPases triggers turning of nerve growth cones

Journal of Neuroscience

Volumn 25, Issue 9, 2005, Pages 2338-2347

  Jin, Ming ^a,b   Guan, Chen Bing ^a,b   Jiang, Yun Ai ^a,b   Chen, Gang ^a,b   Zhao, Chun Tao ^a,b   Cui, Kai ^a,b   Song, Yuan Quan ^a,d   Wu, Chien Ping ^a   Poo, Mu Ming ^a,c   Yuan, Xiao Bing ^a  

^a Shanghai Jiao Tong University Affiliated Sixth People s Hospital   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Axon guidance; Calcium; CaMKII; Growth cone; PKC; Rho GTPases

Indexed keywords

CALCIUM ION; CHEMOATTRACTANT; CYTOSKELETON PROTEIN; PROTEIN CDC42; PROTEIN KINASE (CALCIUM,CALMODULIN) II; PROTEIN KINASE C; RAC PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; RYANODINE; 1,2-BIS(2-AMINOPHENOXY)ETHANE-N,N,N',N'-TETRAACETIC ACID; BACTERIAL PROTEIN; BACTERIAL TOXIN; BRAIN DERIVED NEUROTROPHIC FACTOR; CALCIUM; CHELATING AGENT; DRUG DERIVATIVE; EGTAZIC ACID; ENZYME INHIBITOR; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; GREEN FLUORESCENT PROTEIN; NERVE GROWTH FACTOR; NETRIN 1; NETRIN-1; THAPSIGARGIN; TOXB PROTEIN, CLOSTRIDIUM DIFFICILE; TUMOR SUPPRESSOR PROTEIN;

ANIMAL CELL; ARTICLE; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL CULTURE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; ENZYME ACTIVITY; GRANULE CELL; GROWTH CONE; HUMAN; HUMAN CELL; NERVE FIBER; NERVE GROWTH; NONHUMAN; PRIORITY JOURNAL; SPINAL CORD NERVE CELL; UPREGULATION; XENOPUS; ANIMAL; ANIMAL EMBRYO; CELL LINE; COMPARATIVE STUDY; CYTOLOGY; DIAGNOSTIC IMAGING; DOSE RESPONSE; DRUG EFFECT; DRUG INTERACTION; GENETIC TRANSFECTION; METABOLISM; METHODOLOGY; NERVE CELL; PHYSIOLOGY; SPINAL CORD; TIME; WESTERN BLOTTING;

ANIMALS; BACTERIAL PROTEINS; BACTERIAL TOXINS; BLOTTING, WESTERN; BRAIN-DERIVED NEUROTROPHIC FACTOR; CALCIUM; CDC42 GTP-BINDING PROTEIN; CELL LINE; CHELATING AGENTS; DIAGNOSTIC IMAGING; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; EGTAZIC ACID; EMBRYO, NONMAMMALIAN; ENZYME ACTIVATION; ENZYME INHIBITORS; GREEN FLUORESCENT PROTEINS; GROWTH CONES; HUMANS; NERVE GROWTH FACTORS; NEURONS; RHO GTP-BINDING PROTEINS; RYANODINE; SPINAL CORD; THAPSIGARGIN; TIME FACTORS; TRANSFECTION; TUMOR SUPPRESSOR PROTEINS; XENOPUS;

EID: 14644404254     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4889-04.2005     Document Type: Article

References (49)

1. Akasaki T, Koga H, Sumimoto H (1999) Phosphoinositide 3-kinase-dependent and -independent activation of the small GTPase Rac2 in human neutrophils. J Biol Chem 274:18055-18059.
2. Alder J, Kanki H, Valtorta F, Greengard P, Poo MM (1995) Overexpression of synaptophysin enhances neurotransmitter secretion at Xenopus neuromuscular synapses. J Neurosci 15:511-519.
3. Aurandt J, Vikis HG, Gutkind JS, Ahn N, Guan KL (2002) The semaphorin receptor plexin-B1 signals through a direct interaction with the Rho-specific nucleotide exchange factor, LARG. Proc Natl Acad Sci USA 99:12085-12091.
4. Cau J, Faure S, Comps M, Delsert C, Morin N (2001) A novel p21-activated kinase binds the actin and microtubule networks and induces microtu-bule stabilization. J Cell Biol 155:1029-1042.
5. Chadborn N, Eickholt B, Doherty P, Bolsover S (2002) Direct measurement of local raised subplasmalemmal calcium concentrations in growth cones advancing on an N-cadherin substrate. Eur J Neurosci 15:1891-1898.
6. Costello PS, Walters AE, Mee PJ, Turner M, Reynolds LF, Frisco A, Sarner N, Zamoyska R, Tybulewicz VL (1999) The Rho-family GTP exchange factor Vav is a critical transducer of T cell receptor signals to the calcium, ERK, and NF-κB pathways. Proc Natl Acad Sci USA 96:3035-3040.
7. 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.
8. Dickson BJ (2001) Rho GTPases in growth cone guidance. Curr Opin Neurobiol 11:103-110.
9. Dickson BJ (2002) Molecular mechanisms of axon guidance. Science 298:959-964.
10. Djouder N, Prepens U, Aktories K, Cavalie A (2000) Inhibition of calcium release-activated calcium current by Rac/Cdc42-inactivating clostridial cytotoxins in RBL cells. J Biol Chem 275:18732-18738.
11. Etienne-Manneville S, Hall A (2002) Rho GTPases in cell biology. Nature 420:629-635.
12. 2+/calmodulin-dependent protein kinase II are involved in platelet-derived growth factor-induced phosphorylation of Tiam1. FEBS Lett 429:229-233.
13. 2+/calmodulin-dependent protein kinase II regulates Tiam1 by reversible protein phosphorylation. J Biol Chem 274:12753-12758.
14. Fu WM, Tang YB, Lee KF (1997) Turning of nerve growth cones induced by the activation of protein kinase C. NeuroReport 8:2005-2009.
15. Gomez TM, Rubles E, Poo MM, Spitzer NC (2001) Filopodial calcium transients promote substrate-dependent growth cone turning. Science 291:1983-1987.
16. 2+ signals. Trends Cell Biol 14:320-330.
17. Hong K, Nishiyama M, Henley J, Tessier-Lavigne M, Poo MM (2000) Calcium signaling in the guidance of nerve growth by netrin-1. Nature 403:93-98.
18. Kater SB, Davenport RW, Guthrie PB (1994) Filopodia as detectors of environmental cues: signal integration through changes in growth cone calcium levels. Prog Brain Res 102:49-60.
19. Levchenko A, Iglesias PA (2002) Models of eukaryotic gradient sensing: application to chemotaxis of amoebae and neutrophils. Biophys J 82:50-63.
20. Li X, Saint-Cyr-Proulx E, Aktories K, Lamarche-Vane N (2002) Rac1 and Cdc42 but not RhoA or Rho kinase activities are required for neurite outgrowth induced by the Netrin-1 receptor DCC (deleted in colorectal cancer) in NIE-115 neuroblastoma cells. J Biol Chem 277:15207-15214.
21. Lohof AM, Quillan M, Dan Y, Poo MM (1992) Asymmetric modulation of cytosolic cAMP activity induces growth cone turning. J Neurosci 12:1253-1261.
22. Mackay DJ, Hall A (1998) Rho GTPases. J Biol Chem 14:20685-20688.
23. Ming G, Henley J, Tessier-Lavigne M, Song H, Poo MM (2001) Electrical activity modulates growth cone guidance by diffusible factors. Neuron 29:441-452.
24. Ng J, Nardine T, Harms M, Tzu J, Goldstein A, Sun Y, Dietzl G, Dickson BJ, Luo L (2002) Rac GTPases control axon growth, guidance and branching. Nature 416:442-447.
25. Perrot V, Vazquez-Prado J, Gutkind JS (2002) Plexin B regulates Rho through the guanine nucleotide exchange factors leukemia-associated Rho GEF (LARG) and PDZ-RhoGEF. J Biol Chem 277:43115-43120.
26. Powell EM, Mercado ML, Calle-Patino Y, Geller HM (2001) Protein kinase C mediates neurite guidance at an astrocyte boundary. Glia 33:288-297.
27. Price LS, Langeslag M, ten Klooster JP, Hordijk PL, Jalink K, Collard JG (2003) Calcium signaling regulates translocation and activation of Rac. J Biol Chem 278:39413-39421.
28. Ren XD, Kiosses WB, Schwartz MA (1999) Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. EMBO J 18:578-585.
29. Servant G, Weiner OD, Herzmark P, Balla T, Sedat JW, Bourne HR (2000) Polarization of chemoattractant receptor signaling during neutrophil chemotaxis. Science 287:1037-1040.
30. Shen Y, Mani S, Donovan SL, Schwob JE, Meiri KF (2002) Growth-associated protein-43 is required for commissural axon guidance in the developing vertebrate nervous system. J Neurosci 22:239-247.
31. 2+ signaling during hyaluronan (HA)-induced endothelial cell migration. Cell Motil Cytoskeleton 53:293-316.
32. Song HJ, Poo MM (1999) Signal transduction underlying growth cone guidance by diffusible factors. Curr Opin Neurobiol 9:355-363.
33. Song HJ, Poo MM (2001) The cell biology of neuronal navigation. Nat Cell Biol 3:E81-E88.
34. Steven R, Kubiseski TJ, Zheng H, Kulkarni S, Mancillas J, Ruiz Morales A, Hogue CW, Pawson T, Culotti J (1998) UNC-73 activates the Rac GT-Pase and is required for cell and growth cone migrations in C. elegans. Cell 92:785-795.
35. Swiercz JM, Kuner R, Behrens J, Offermanns S (2002) Plexin-B1 directly interacts with PDZ-RhoGEF/LARG to regulate RhoA and growth cone morphology. Neuron 35:51-63.
36. Wahl S, Barth H, Ciossek T, Aktories K, Mueller BK (2000) Ephrin-A5 induces collapse of growth cones by activating Rho and Rho kinase. J Cell Biol 149:263-270.
37. Wang KC, Kim JA, Sivasankaran R, Segal R, He Z (2002) P75 interacts with the Nogo receptor as a co-receptor for Nogo, MAG and OMgp. Nature 420:74-78.
38. Wang X, Berninger B, Poo MM (1998) Localized synaptic actions of neurotrophin-4. J Neurosci 18:4985-4992.
39. (2+)-dependent growth cone guidance. Neuron 43:835-846.
40. Whitford KL, Ghosh A (2001) Plexin signaling via off-track and rho family GTPases. Neuron 32:1-3.
41. Wilk-Blaszczak MA, Singer WD, Quill T, Miller B, Frost JA, Sternweis PC, Belardetti F (1997) The monomeric G-proteins Rac1 and/or Cdc42 are required for the inhibition of voltage-dependent calcium current by bradykinin. J Neurosci 17:4094-4100.
42. Wong K, Ren XR, Huang YZ, Xie Y, Liu G, Saito H, Tang H, Wen L, Brady-Kalnay SM, Mei L, Wu JY, Xiong WC, Rao Y (2001) Signal transduction in neuronal migration: roles of GTPase activating proteins and the small GTPase Cdc42 in the Slit-Robo pathway. Cell 107:209-221.
43. Wong ST, Henley JR, Kanning KC, Huang KH, Bothwell M, Poo MM (2002) A p75(NTR) and nogo receptor complex mediates repulsive signalling by myelin-associated glycoprotein. Nat Neurosci 5:1302-1308.
44. Yuan XB, Jing M, Xu X, Song YQ, Wu CP, Poo MM, Duan S (2003) Signalling and crosstalk of Rho GTPases in mediating axon guidance. Nat Cell Biol 5:38-45.
45. Zhang F, Lu C, Severin C, Sretavan DW (2000) GAP-43 mediates retinal axon interaction with lateral diencephalon cells during optic tract formation. Development 127:969-980.
46. 2+ concentration. Nature 403:89-93.
47. Zheng JQ, Felder M, Connor JA, Poo MM (1994) Turning of nerve growth cones induced by neurotransmitters. Nature 368:140-144.
48. Zheng JQ, Wan JJ, Poo MM (1996) Essential role of filopodia in chemotropic turning of nerve growth cone induced by a glutamate gradient. J Neurosci 16:1140-1149.
49. Zucchi R, Ronca-Testoni S (1997) The sarcoplasmic reticulum calcium channel/ryanodine receptor: modulation by endogenous effectors, drugs and disease states. Pharmacol Rev 49:1-51.