Rab11 and its effector rab coupling protein contribute to the trafficking of β1 integrins during axon growth in adult dorsal root ganglion neurons and PC12 cells

Journal of Neuroscience

Volumn 30, Issue 35, 2010, Pages 11654-11669

  Eva, Richard ^a   Dassie, Elisa ^a   Caswell, Patrick T ^b   Dick, Gunnar ^a   Ffrench Constant, Charles ^c   Norman, Jim C ^b   Fawcett, James W ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b BEATSON INSTITUTE FOR CANCER RESEARCH   (United Kingdom)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTEGRIN; BETA1 INTEGRIN; BINDING PROTEIN; INTEGRIN ALPHA9; RAB COUPLING PROTEIN; RAB11 PROTEIN; TENASCIN; UNCLASSIFIED DRUG; MEMBRANE PROTEIN; RAB PROTEIN; RAB11FIP1 PROTEIN, HUMAN; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ANIMAL CELL; ARTICLE; CELL COMPARTMENTALIZATION; CELL STRAIN; CONTROLLED STUDY; ENDOCYTOSIS; GROWTH CONE; MALE; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; RAT; SPINAL GANGLION; AGE; ANIMAL; CELL CULTURE; COMPARATIVE STUDY; CYTOLOGY; HUMAN; METABOLISM; NERVE CELL; NERVE FIBER; PC12 CELL LINE; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AGE FACTORS; ANIMALS; ANTIGENS, CD29; AXONS; CELLS, CULTURED; GANGLIA, SPINAL; GROWTH CONES; HUMANS; MALE; MEMBRANE PROTEINS; NEURONS; PC12 CELLS; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 77956257696     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2425-10.2010     Document Type: Article

References (56)

1. Allen J, Chilton JK (2009) The specific targeting of guidance receptors within neurons: who directs the directors? Dev Biol 327:4-11.
2. Andrews MR, Czvitkovich S, Dassie E, Vogelaar CF, Faissner A, Blits B, Gage FH, ffrench-Constant C, Fawcett JW (2009) α9 integrin promotes neurite outgrowth on tenascin-C and enhances sensory axon regeneration. J Neurosci 29:5546-5557.
3. Ascaño M, Richmond A, Borden P, Kuruvilla R (2009) Axonal targeting of Trk receptors via transcytosis regulates sensitivity to neurotrophin responses. J Neurosci 29:11674-11685.
4. Bolte S, Cordelières FP (2006) A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 224:213-232. (Pubitemid 46010930)
5. Bomsel M, Parton R, Kuznetsov SA, Schroer TA, Gruenberg J (1990) Microtubule- and motor-dependent fusion in vitro between apical and basolateral endocytic vesicles from MDCK cells. Cell 62:719-731. (Pubitemid 20275712)
6. Brakebusch C, Fässler R (2005) beta 1 integrin function in vivo: adhesion, migration and more. Cancer Metastasis Rev 24:403-411. (Pubitemid 41569980)
7. Brown TC, Correia SS, Petrok CN, Esteban JA (2007) Functional compartmentalization of endosomal trafficking for the synaptic delivery of AMPA receptors during long-term potentiation. J Neurosci 27:13311-13315.
8. Caswell PT, Chan M, Lindsay AJ, McCaffrey MW, Boettiger D, Norman JC (2008) Rab-coupling protein coordinates recycling of alpha5beta1 integrin and EGFR1 to promote cell migration in 3D microenvironments. J Cell Biol 183:143-155.
9. Choe EA, Liao L, Zhou JY, Cheng D, Duong DM, Jin P, Tsai LH, Peng J (2007) Neuronal morphogenesis is regulated by the interplay between cyclin-dependent kinase 5 and the ubiquitin ligase mind bomb 1. J Neurosci 27:9503-9512. (Pubitemid 47358202)
10. Cingolani LA, Thalhammer A, Yu LM, Catalano M, Ramos T, Colicos MA, Goda Y (2008) Activity-dependent regulation of synaptic AMPA receptor composition and abundance by beta3 integrins. Neuron 58:749-762. (Pubitemid 351778467)
11. Correia SS, Bassani S, Brown TC, Lisé MF, Backos DS, El-Husseini A, Passafaro M, Esteban JA (2008) Motor protein-dependent transport of AMPA receptors into spines during long-term potentiation. Nat Neurosci 11:457-466. (Pubitemid 351441879)
12. Damiani MT, Pavarotti M, Leiva N, Lindsay AJ, McCaffrey MW, Colombo MI (2004) Rab coupling protein associates with phagosomes and regulates recycling from the phagosomal compartment. Traffic 5:785-797. (Pubitemid 39307262)
13. Deinhardt K, Salinas S, Verastegui C, Watson R, Worth D, Hanrahan S, Bucci C, Schiavo G (2006) Rab5 and Rab7 control endocytic sorting along the axonal retrograde transport pathway. Neuron 52:293-305. (Pubitemid 44548343)
14. Fabbri M, Di Meglio S, Gagliani MC, Consonni E, Molteni R, Bender JR, Tacchetti C, Pardi R (2005) Dynamic partitioning into lipid rafts controls the endo-exocytic cycle of the alphaL/beta2 integrin, LFA-1, during leukocyte chemotaxis. Mol Biol Cell 16:5793-5803. (Pubitemid 41752227)
15. Fache MP, Moussif A, Fernandes F, Giraud P, Garrido JJ, Dargent B (2004) Endocytotic elimination and domain-selective tethering constitute a potential mechanism of protein segregation at the axonal initial segment. J Cell Biol 166:571-578. (Pubitemid 39097176)
16. Gardiner NJ, Fernyhough P, Tomlinson DR, Mayer U, von der Mark H, Streuli CH (2005) Alpha7 integrin mediates neurite outgrowth of distinct populations of adult sensory neurons. Mol Cell Neurosci 28:229-240. (Pubitemid 40202585)
17. Gardiner NJ, Moffatt S, Fernyhough P, Humphries MJ, Streuli CH, Tomlinson DR (2007) Preconditioning injury-induced neurite outgrowth of adult rat sensory neurons on fibronectin is mediated by mobilisation of axonal alpha5 integrin. Mol Cell Neurosci 35:249-260. (Pubitemid 46843563)
18. Gorvel JP, Chavrier P, Zerial M, Gruenberg J (1991) rab5 controls early endosome fusion in vitro. Cell 64:915-925. (Pubitemid 121001179)
19. Hémar A, Olivo JC, Williamson E, Saffrich R, Dotti CG (1997) Dendroaxonal transcytosis of transferrin in cultured hippocampal and sympathetic neurons. J Neurosci 17:9026-9034. (Pubitemid 27498430)
20. Hollis ER 2nd, Jamshidi P, Löw K, Blesch A, Tuszynski MH (2009) Induction of corticospinal regeneration by lentiviral trkB-induced Erk activation. Proc Natl Acad Sci U S A 106:7215-7220.
21. Hu F, Strittmatter SM (2008) The N-terminal domain of Nogo-A inhibits cell adhesion and axonal outgrowth by an integrin-specific mechanism. J Neurosci 28:1262-1269. (Pubitemid 351186346)
22. Joester A, Faissner A (2001) The structure and function of tenascins in the nervous system. Matrix Biol 20:13-22. (Pubitemid 32178103)
23. Kamiguchi H (2003) The mechanism of axon growth: what we have learned from the cell adhesion molecule L1. Mol Neurobiol 28:219-228.
24. Kamiguchi H, Lemmon V (2000) Recycling of the cell adhesion molecule L1 in axonal growth cones. J Neurosci 20:3676-3686. (Pubitemid 30266230)
25. Koprivica V, Cho KS, Park JB, Yiu G, Atwal J, Gore B, Kim JA, Lin E, Tessier-Lavigne M, Chen DF, He Z (2005) EGFR activation mediates inhibition of axon regeneration by myelin and chondroitin sulfate proteoglycans. Science 310:106-110.
26. Laukaitis CM, Webb DJ, Donais K, Horwitz AF (2001) Differential dynamics of alpha 5 integrin, paxillin, and alpha-actinin during formation and disassembly of adhesions in migrating cells. J Cell Biol 153:1427-1440. (Pubitemid 34286127)
27. Leterrier C, Lainé J, Darmon M, Boudin H, Rossier J, Lenkei Z (2006) Constitutive activation drives compartment-selective endocytosis and axonal targeting of type 1 cannabinoid receptors. J Neurosci 26:3141-3153.
28. Lindsay AJ, McCaffrey MW (2004) Characterisation of the Rab binding properties of Rab coupling protein (RCP) by site-directed mutagenesis. FEBS Lett 571:86-92.
29. Lindsay AJ, Hendrick AG, Cantalupo G, Senic-Matuglia F, Goud B, Bucci C, McCaffrey MW (2002) Rab coupling protein (RCP), a novel Rab4 and Rab11 effector protein. J Biol Chem 277:12190-12199. (Pubitemid 34952785)
30. Lisé MF, Wong TP, Trinh A, Hines RM, Liu L, Kang R, Hines DJ, Lu J, Goldenring JR, Wang YT, El-Husseini A (2006) Involvement of myosin Vb in glutamate receptor trafficking. J Biol Chem 281:3669-3678. (Pubitemid 43845985)
31. McDonald NA, Henstridge CM, Connolly CN, Irving AJ (2007) An essential role for constitutive endocytosis, but not activity, in the axonal targeting of the CB1 cannabinoid receptor. Mol Pharmacol 71:976-984. (Pubitemid 46457002)
32. Milner R, ffrench-Constant C (1994) A developmental analysis of oligodendroglial integrins in primary cells: changes in alpha v-associated beta subunits during differentiation. Development 120:3497-3506.
33. Moser M, Bauer M, Schmid S, Ruppert R, Schmidt S, Sixt M, Wang HV, Sperandio M, Fässler R (2009) Kindlin-3 is required for beta2 integrin-mediated leukocyte adhesion to endothelial cells. Nat Med 15:300-305.
34. Muller PA, Caswell PT, Doyle B, Iwanicki MP, Tan EH, Karim S, Lukashchuk N, Gillespie DA, Ludwig RL, Gosselin P, Cromer A, Brugge JS, Sansom OJ, Norman JC, Vousden KH (2009) Mutant p53 drives invasion by promoting integrin recycling. Cell 139:1327-1341.
35. Park M, Penick EC, Edwards JG, Kauer JA, Ehlers MD (2004) Recycling endosomes supply AMPA receptors for LTP. Science 305:1972-1975. (Pubitemid 39287999)
36. Pazyra-Murphy MF, Segal RA (2008) Preparation and maintenance of dorsal root ganglia neurons in compartmented cultures. J Vis Exp pii:951.
37. Peden AA, Schonteich E, Chun J, Junutula JR, Scheller RH, Prekeris R (2004) The RCP-Rab11 complex regulates endocytic protein sorting. Mol Biol Cell 15:3530-3541. (Pubitemid 38989694)
38. Pellinen T, Ivaska J (2006) Integrin traffic. J Cell Sci 119:3723-3731.
39. Plantman S, Patarroyo M, Fried K, Domogatskaya A, Tryggvason K, Hammarberg H, Cullheim S (2008) Integrin-laminin interactions controlling neurite outgrowth from adult DRG neurons in vitro. Mol Cell Neurosci 39:50-62.
40. Powelka AM, Sun J, Li J, Gao M, Shaw LM, Sonnenberg A, Hsu VW (2004) Stimulation-dependent recycling of integrin beta1 regulated by ARF6 and Rab11. Traffic 5:20-36. (Pubitemid 38159401)
41. Pozzi A, Wary KK, Giancotti FG, Gardner HA (1998) Integrin alpha1beta1 mediates a unique collagen-dependent proliferation pathway in vivo. J Cell Biol 142:587-594. (Pubitemid 28361562)
42. Rigato F, Garwood J, Calco V, Heck N, Faivre-Sarrailh C, Faissner A (2002) Tenascin-C promotes neurite outgrowth of embryonic hippocampal neurons through the alternatively spliced fibronectin type III BD domains via activation of the cell adhesion molecule F3/contactin. J Neurosci 22:6596-6609. (Pubitemid 35386416)
43. Rink J, Ghigo E, Kalaidzidis Y, Zerial M (2005) Rab conversion as a mechanism of progression from early to late endosomes. Cell 122:735-749. (Pubitemid 41242638)
44. Sampo B, Kaech S, Kunz S, Banker G (2003) Two distinct mechanisms target membrane proteins to the axonal surface. Neuron 37:611-624. (Pubitemid 36262983)
45. Skalski M, Coppolino MG (2005) SNARE-mediated trafficking of alpha5beta1 integrin is required for spreading in CHO cells. Biochem Biophys Res Commun 335:1199-1210.
46. Sönnichsen B, De Renzis S, Nielsen E, Rietdorf J, Zerial M (2000) Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11. J Cell Biol 149:901-914.
47. Ullrich O, Reinsch S, Urbé S, Zerial M, Parton RG (1996) Rab11 regulates recycling through the pericentriolar recycling endosome. J Cell Biol 135:913-924.
48. Vaudry D, Stork PJ, Lazarovici P, Eiden LE (2002) Signaling pathways for PC12 cell differentiation: making the right connections. Science 296:1648-1649. (Pubitemid 34579153)
49. Wang Z, Edwards JG, Riley N, Provance DW Jr, Karcher R, Li XD, Davison IG, Ikebe M, Mercer JA, Kauer JA, Ehlers MD (2008) Myosin Vb mobilizes recycling endosomes and AMPA receptors for postsynaptic plasticity. Cell 135:535-548.
50. Webb DJ, Zhang H, Majumdar D, Horwitz AF (2007) alpha5 integrin signaling regulates the formation of spines and synapses in hippocampal neurons. J Biol Chem 282:6929-6935. (Pubitemid 47093674)
51. Werner A, Willem M, Jones LL, Kreutzberg GW, Mayer U, Raivich G (2000) Impaired axonal regeneration in α7 integrin-deficient mice. J Neurosci 20:1822-1830. (Pubitemid 30220379)
52. Winckler B (2004) Scientiae forum/models and speculations pathways for axonal targeting of membrane proteins. Biol Cell 96:669-674.
53. Wisco D, Anderson ED, Chang MC, Norden C, Boiko T, Fölsch H, Winckler B (2003) Uncovering multiple axonal targeting pathways in hippocampal neurons. J Cell Biol 162:1317-1328. (Pubitemid 37210887)
54. Yap CC, Wisco D, Kujala P, Lasiecka ZM, Cannon JT, Chang MC, Hirling H, Klumperman J, Winckler B (2008a) The somatodendritic endosomal regulator NEEP21 facilitates axonal targeting of L1/NgCAM. J Cell Biol 180:827-842. (Pubitemid 351397781)
55. Yap CC, Nokes RL, Wisco D, Anderson E, Fölsch H, Winckler B (2008b) Pathway selection to the axon depends on multiple targeting signals in NgCAM. J Cell Sci 121:1514-1525.
56. Yoon SO, Shin S, Mercurio AM (2005) Hypoxia stimulates carcinoma invasion by stabilizing microtubules and promoting the Rab11 trafficking of the alpha6beta4 integrin. Cancer Res 65:2761-2769.