Exclusion of integrins from CNS axons is regulated by Arf6 activation and the AIS

Journal of Neuroscience

Volumn 35, Issue 21, 2015, Pages 8359-8375

  Franssen, Elske H P ^a   Zhao, Rong Rong ^a   Koseki, Hiroaki ^a   Kanamarlapudi, Venkateswarlu ^b   Hoogenraad, Casper C ^c   Eva, Richard ^a   Fawcett, James W ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b SWANSEA UNIVERSITY   (United Kingdom)

^c UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Arf6; Axon initial segment; Axonal transport; Integrin; Trafficking

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; ADENOVIRUS VECTOR; ALPHA5 INTEGRIN; ALPHA9 INTEGRIN; BETA1 INTEGRIN; CD51 ANTIGEN; DIMETHYL SULFOXIDE; ENHANCED GREEN FLUORESCENT PROTEIN; INTEGRIN; LATRUNCULIN A; PACLITAXEL; PHALLOIDIN; PROTEIN P50; SHORT HAIRPIN RNA; TENASCIN; TRANSCRIPTION FACTOR AP 1; TRICHOSTATIN A; TUBULIN; UNCLASSIFIED DRUG; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; ADP-RIBOSYLATION FACTOR 6;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AXON INITIAL SEGMENT; BRAIN CELL; CELL MATURATION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DENDRITE; GENE OVEREXPRESSION; GENE SILENCING; GENETIC TRANSFECTION; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE MICROSCOPY; NERVE CELL CULTURE; NERVE FIBER GROWTH; NERVE FIBER MEMBRANE POTENTIAL; NERVE FIBER REGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ACETYLATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN TRANSPORT; RAT; RETROGRADE NERVE FIBER TRANSPORT; UPREGULATION; ANIMAL; BRAIN CORTEX; CELL CULTURE; CYTOLOGY; DEFICIENCY; EMBRYOLOGY; METABOLISM; NERVE FIBER; PHYSIOLOGY; REGENERATION;

ADP-RIBOSYLATION FACTORS; ANIMALS; AXONS; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; CEREBRAL CORTEX; INTEGRINS; RATS; REGENERATION;

EID: 84930255291     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2850-14.2015     Document Type: Article

References (80)

1. Andrews MR, Czvitkovich S, Dassie E, Vogelaar CF, Faissner A, Blits B, Gage FH, ffrench-Constant C, Fawcett JW (2009) Alpha9 integrin promotes neurite outgrowth on tenascin-C and enhances sensory axon regeneration. J Neurosci 29:5546–5557. CrossRef Medline
2. Arjonen A, Kaukonen R, Ivaska J (2011) Filopodia and adhesion in cancer cell motility. Cell Adh Migr 5:421–430. CrossRef Medline
3. Arnold DB (2009) Actin and microtubule-based cytoskeletal cues direct polarized targeting of proteins in neurons. Sci Signal 2:pe49. Medline
4. Bi X, Lynch G, Zhou J, Gall CM (2001) Polarized distribution of integrin alpha5 in dendrites of hippocampal and cortical neurons. J Comp Neurol 435:184–193. CrossRef Medline
5. Blackmore MG, Wang Z, Lerch JK, Motti D, Zhang YP, Shields CB, Lee JK, Goldberg JL, Lemmon VP, Bixby JL (2012) Kruppel-like Factor 7 engineered for transcriptional activation promotes axon regeneration in the adult corticospinal tract. Proc Natl Acad Sci U S A 109:7517–7522. CrossRef Medline
6. Bonifacino JS, Traub LM (2003) Signals for sorting of transmembrane pro teins to endosomes and lysosomes. Annu Rev Biochem 72:395–447. CrossRef Medline
7. Bouschet T, Martin S, Kanamarlapudi V, Mundell S, Henley JM (2007) The calcium-sensing receptor changes cell shape via a β-arrestin-1–ARNO– Arf6–ELMO protein network. J Cell Sci 120:2489–2497. CrossRef Medline
8. Bradke F, Dotti CG (2000) Changes in membrane trafficking and actin dynamics during axon formation in cultured hippocampal neurons. Microsc Res Tech 48:3–11. CrossRef Medline
9. Burkhardt JK, Echeverri CJ, Nilsson T, Vallee RB (1997) Overexpression of the dynamitin (p50) subunit of the dynactin complex disrupts dynein-dependent maintenance of membrane organelle distribution. J Cell Biol 139:469–484. CrossRef Medline
10. Caster AH, Sztul E, Kahn RA (2013) A role for cargo in the activation of ADP-ribosylation factors (Arf) and adaptor recruitment. J Biol Chem 288:14788–14804. CrossRef Medline
11. Cheah M, Andrews MR, Verhaagen J, Fassler R, Faissner A, Fawcett JW 2013 Alpha9 integrin activation in neurite outgrowth and axon regeneration. Soc Neurosci Abstr 39:341.17. CrossRef Medline
12. Chisholm AD (2013) Cytoskeletal dynamics in Caenorhabditis elegans axon regeneration. Annu Rev Cell Dev Biol 29:271–297. CrossRef Medline
13. Conde C, Cáceres A (2009) Microtubule assembly, organization and dynamics in axons and dendrites. Nat Rev Neurosci 10:319–332. CrossRef Medline
14. Donaldson JG, Jackson CL (2011) ARF family G proteins and their regulators, roles in membrane transport, development and disease. Nat Rev Mol Cell Biol 12:362–375. CrossRef Medline
15. Dotti CG, Poo MM (2003) Neuronal polarization, building fences for molecular segregation. Nat Cell Biol 5:591–594. Medline
16. Eva R, Dassie E, Caswell PT, Dick G, ffrench-Constant C, Norman JC, Fawcett JW (2010) 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. J Neurosci 30:11654–11669. CrossRef Medline
17. Eva R, Crisp S, Marland JR, Norman JC, Kanamarlapudi V, ffrench-Constant C, Fawcett JW (2012) Arf6 directs axon transport and traffic of integrins and regulates axon growth in adult DRG neurons. J Neurosci 32:10352– 10364. CrossRef Medline
18. Farías GG, Cuitino L, Guo X, Ren X, Jarnik M, Mattera R, Bonifacino JS (2012) Signal-mediated., AP-1/clathrin-dependent sorting of transmembrane receptors to the somatodendritic domain of hippocampal neurons. Neuron 75:810–823. CrossRef Medline
19. Fawcett JW (1992) Axon growth and regeneration: intrinsic neuronal effects. Trends Neurosci 15:5–8. CrossRef Medline
20. 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. CrossRef Medline
21. Gumy LF, Yeo GS, Tung YC, Zivraj KH, Willis D, Coppola G, Lam BY, Twiss JL, Holt CE, Fawcett JW (2011) Transcriptome analysis of embryonic and adult sensory axons reveals changes in mRNA repertoire localization. RNA 17:85–98. CrossRef Medline
22. Gumy LF, Chew DJ, Tortosa E, Katrukha EA, Kapitein LC, Tolkovsky AM, Hoogenraad CC, Fawcett JW (2013) The kinesin-2 family member KIF3C regulates microtubule dynamics and is required for axon growth and regeneration. J Neurosci 33:11329–11345. CrossRef Medline
23. Hammond JW, Huang CF, Kaech S, Jacobson C, Banker G, Verhey KJ (2010) Posttranslational modifications of tubulin and the polarized transport of kinesin-1 in neurons. Mol Biol Cell 21:572–583. CrossRef Medline
24. Hedstrom KL, Xu X, Ogawa Y, Frischknecht R, Seidenbecher CI, Shrager P, Rasband MN (2007) Neurofascin assembles a specialized extra-cellular matrix at the AIS. J Cell Biol 178:875–886. CrossRef Medline
25. Hedstrom KL, Ogawa Y, Rasband MN (2008) AnkyrinG is required for maintenance of the AIS and neuronal polarity. J Cell Biol 183:635–640. CrossRef Medline
26. Heintz TG, Heller JP, Zhao R, Caceres A, Eva R, Fawcett JW (2014) Kinesin KIF4A transports integrin beta1 in developing axons of cortical neurons. Mol Cell Neurosci 63:60–71. CrossRef Medline
27. Hellal F, Hurtado A, Ruschel J, Flynn KC, Laskowski CJ, Umlauf M, Kapitein LC, Strikis D, Lemmon V, Bixby J, Hoogenraad CC, Bradke F (2011) Microtubule stabilization reduces scarring and causes axon regeneration after spinal cord injury. Science 331, 928–931. CrossRef Medline
28. Hernández-Deviez DJ, Wilson JM (2005) Functional assay of ARNO and Arf6 in neurite elongation and branching. Methods Enzymol 404:242– 252. CrossRef Medline
29. Hernández-Deviez DJ, Roth MG, Casanova JE, Wilson JM (2004) ARNO and Arf6 regulate axonal elongation and branching through downstream activation of phosphatidylinositol 4-phosphate 5-kinase alpha. Mol Biol Cell 15:111–120. Medline
30. Hernández-Deviez D, Mackay-Sim A, Wilson JM (2007) A role for Arf6 and ARNO in the regulation of endosomal dynamics in neurons. Traffic 8:1750–1764. CrossRef Medline
31. Hirokawa N, Noda Y, Tanaka Y, Niwa S (2009) Kinesin superfamily motor proteins and intracellular transport. Nat Rev Mol Cell Biol 10:682–696. Medline
32. Hollis ER2nd, 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. CrossRef Medline
33. Hoogenraad CC, Akhmanova A, Howell SA, Dortland BR, De Zeeuw CI, Willemsen R, Visser P, Grosveld F, Galjart N (2001) Mammalian golgi-associated bicaudal-D2 functions in the dynein-dynactin pathway by interacting with these complexes. EMBO J 20:4041–4054. CrossRef Medline
34. Huang CF, Banker G (2012) The translocation selectivity of the kinesins that mediate neuronal organelle transport. Traffic 13:549–564. Medline
35. Huang Z, Shimazu K, Woo NH, Zang K, Müller U, Lu B, Reichardt LF (2006) Distinct roles of the beta 1-class integrins at the developing and the mature hippocampal excitatory synapse. J Neurosci 26:11208–11219. CrossRef Medline
36. Isabet T, Montagnac G, Regazzoni K, Raynal B, El Khadali F, England P, Franco M, Chavrier P, Houdusse A, Ménétrey J (2009) The structural basis of Arf effector specificity, the crystal structure of Arf6 in a complex with JIP4. EMBO J 28:2835–2845. CrossRef Medline
37. Janke C, Bulinski JC (2011) Post-translational regulation of the microtubule cytoskeleton, mechanisms and functions. Nat Rev Mol Cell Biol 12:773–786. CrossRef Medline
38. Kapitein LC, Schlager MA, van der Zwan WA, Wulf PS, Keijzer N, Hoogenraad CC (2010) Probing intracellular motor protein activity using an inducible cargo trafficking assay. Biophys J 99:2143–2152. CrossRef Medline
39. Kee HL, Dishinger JF, Blasius TL, Liu CJ, Margolis B, Verhey KJ (2012) A size-exclusion permeability barrier and nucleoporins characterize a ciliary pore complex that regulates transport into cilia. Nat Cell Biol 14:431– 437. CrossRef Medline
40. Kobayashi T, Storrie B, Simons K, Dotti CG (1992) A functional barrier to movement of lipids in polarized neurons. Nature 359:647–650. CrossRef Medline
41. Lasiecka ZM, Winckler B (2011) Mechanisms of polarized membrane trafficking in neurons–focusing in on endosomes. Mol Cell Neurosci 48:278– 287. CrossRef Medline
42. Laummonerie C, Mutterer J (2003) RGB Profiler ImageJ Plugin. Available from: http://rsbweb.nih.gov/ij/plugins/download/RGB_Profiler.java. Accessed May 8, 2015.
43. Legate KR, Fässler R (2009) Mechanisms that regulate adaptor binding to beta-integrin cytoplasmic tails. J Cell Sci 122:187–198. CrossRef Medline
44. Lewis TL Jr, Mao T, Svoboda K, Arnold DB (2009) Myosin-dependent targeting of transmembrane proteins to neuronal dendrites. Nat Neurosci 12:568–576. CrossRef Medline
45. Li J, Ballif BA, Powelka AM, Dai J, Gygi SP, Hsu VW (2005) Phosphorylation of ACAP1 by Akt regulates the stimulation-dependent recycling of integrin beta1 to control cell migration. Dev Cell 9:663–673. CrossRef Medline
46. Li J, Peters PJ, Bai M, Dai J, Bos E, Kirchhausen T, Kandror KV, Hsu VW (2007) An ACAP1-containing clathrin coat complex for endocytic recycling. J Cell Biol 178:453–464. CrossRef Medline
47. Mansfield SG, Gordon-Weeks PR (1991) Dynamic post-translational modification of tubulin in rat cerebral cortical neurons extending neurites in culture: effects of taxol. J Neurocytol 20:654–666. CrossRef Medline
48. Margadant C, Monsuur HN, Norman JC, Sonnenberg A (2011) Mechanisms of integrin activation and trafficking. Curr Opin Cell Biol 23:607– 614. CrossRef Medline
49. Margadant C, Kreft M, de Groot DJ, Norman JC, Sonnenberg A (2012) Distinct roles of talin and kindlin in regulating integrin α5β1 function and trafficking. Curr Biol 22:1554–1563. CrossRef Medline
50. Margeta MA, Wang GJ, Shen K (2009) Clathrin adaptor AP-1 complex excludes multiple postsynaptic receptors from axons in C. elegans. Proc Natl Acad Sci U S A 106:1632–1637. CrossRef Medline
51. McGeachie AB, Cingolani LA, Goda Y (2011) A stabilising influence: Integrins in regulation of synaptic plasticity. Neurosci Res 70:24–29. CrossRef Medline
52. Melkonian KA, Maier KC, Godfrey JE, Rodgers M, Schroer TA (2007) Mechanism of dynamitin-mediated disruption of dynactin. J Biol Chem 282:19355–19364. CrossRef Medline
53. Mo J, Choi S, Ahn PG, Sun W, Lee HW, Kim H (2012) PDZ-scaffold protein, Tamalin promotes dendritic outgrowth and arborization in rat hippocampal neuron. Biochem Biophys Res Commun 422:250–255. CrossRef Medline
54. Montagnac G, de Forges H, Smythe E, Gueudry C, Romao M, Salamero J, Chavrier P (2011) Decoupling of activation and effector binding underlies Arf6 priming of fast endocytic recycling. Curr Biol 21:574–579. CrossRef Medline
55. Morse EM, Brahme NN, Calderwood DA (2014) Integrin cytoplasmic tail interactions. Biochemistry 53:810–820. CrossRef Medline
56. Mortillo S, Elste A, Ge Y, Patil SB, Hsiao K, Huntley GW, Davis RL, Benson DL (2012) Compensatory redistribution of neuroligins and N-cadherin following deletion of synaptic β1-integrin. J Comp Neurol 520:2041– 2052. CrossRef Medline
57. Myers JP, Santiago-Medina M, Gomez TM (2011) Regulation of axonal outgrowth and pathfinding by integrin-ECM interactions. Dev Neurobiol 71:901–923. CrossRef Medline
58. Nakata T, Hirokawa N (2003) Microtubules provide directional cues for polarized axonal transport through interaction with kinesin motor head. J Cell Biol 162:1045–1055. CrossRef Medline
59. Nakata T, Niwa S, Okada Y, Perez F, Hirokawa N (2011) Preferential binding of a kinesin-1 motor to GTP-tubulin-rich microtubules underlies polarized vesicle transport. J Cell Biol 194:245–255. CrossRef Medline
60. Oku Y, Huganir RL (2013) AGAP3 and Arf6 regulate trafficking of AMPA receptors and synaptic plasticity. J Neurosci 33:12586–12598. CrossRef Medline
61. Petersen JD, Kaech S, Banker G (2014) Selective microtubule-based transport of dendritic membrane proteins arises in concert with axon specification. J Neurosci 34:4135–4147. CrossRef Medline
62. 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. CrossRef Medline
63. R Development Core Team (2008) R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. CrossRef Medline
64. Rasband MN (2010) The AIS and the maintenance of neuronal polarity. Nat Rev Neurosci 11:552–562. CrossRef Medline
65. Ren X, Farías GG, Canagarajah BJ, Bonifacino JS, Hurley JH (2013) Structural basis for recruitment and activation of the AP-1 clathrin adaptor complex by Arf1. Cell 152:755–767. CrossRef Medline
66. Sakagami H, Suzuki H, Kamata A, Owada Y, Fukunaga K, Mayanagi H, Kondo H (2006) Distinct spatiotemporal expression of EFA6D, a guanine nucleotide exchange factor for Arf6, among the EFA6 family in mouse brain. Brain Res 1093:1–11. CrossRef Medline
67. Scholz R, Berberich S, Rathgeber L, Kolleker A, Köhr G, Kornau HC (2010) AMPA receptor signaling through BRAG2 and Arf6 critical for long-term synaptic depression. Neuron 66:768–780. CrossRef Medline
68. Song AH, Wang D, Chen G, Li Y, Luo J, Duan S, Poo MM (2009) A selective filter for cytoplasmic transport at the AIS. Cell 136:1148–1160. CrossRef Medline
69. Steinberg F, Heesom KJ, Bass MD, Cullen PJ (2012) SNX17 protects integrins from degradation by sorting between lysosomal and recycling pathways. J Cell Biol 197:219–230. CrossRef Medline
70. Suzuki A, Arikawa C, Kuwahara Y, Itoh K, Watanabe M, Watanabe H, Suzuki T, Funakoshi Y, Hasegawa H, Kanaho Y (2010) The scaffold protein JIP3 functions as a downstream effector of the small GTPase Arf6 to regulate neurite morphogenesis of cortical neurons. FEBS Lett 584:2801– 2806. CrossRef Medline
71. Tan CL, Andrews MR, Kwok JC, Heintz TG, Gumy LF, Fässler R, Fawcett JW (2012) Kindlin-1 enhances axon growth on inhibitory chondroitin sulfate proteoglycans and promotes sensory axon regeneration. J Neurosci 32:7325–7335. CrossRef Medline
72. Torii T, Miyamoto Y, Sanbe A, Nishimura K, Yamauchi J, Tanoue A (2010) Cytohesin-2/ARNO, through its interaction with focal adhesion adaptor protein paxillin, regulates preadipocyte migration via the downstream activation of Arf6. J Biol Chem 285:24270–24281. CrossRef Medline
73. Venkateswarlu K, Cullen PJ (2000) Signalling via ADP-ribosylation factor 6 lies downstream of phosphatidylinositide 3-kinase. Biochem J 345:719– 724. CrossRef Medline
74. Verma P, Chierzi S, Codd AM, Campbell DS, Meyer RL, Holt CE, Fawcett JW (2005) Axonal protein synthesis and degradation are necessary for efficient growth cone regeneration. J Neurosci 25:331–342. CrossRef Medline
75. Vogelezang MG, Liu Z, Relvas JB, Raivich G, Scherer SS, ffrench-Constant C (2001) α4 integrin is expressed during peripheral nerve regeneration and enhances neurite outgrowth. J Neurosci 21:6732–6744. Medline
76. Vogelezang M, Forster UB, Han J, Ginsberg MH, ffrench-Constant C (2007) Neurite outgrowth on a fibronectin isoform expressed during peripheral nerve regeneration is mediated by the interaction of paxillin with alpha4beta1 integrins. BMC Neurosci 8:44. CrossRef Medline
77. Werner A, Willem M, Jones LL, Kreutzberg GW, Mayer U, Raivich G (2000) Impaired axonal regeneration in 7 integrin-deficient mice. J Neurosci 20:1822–1830. Medline
78. White DT, McShea KM, Attar MA, Santy LC (2010) GRASP and IPCEF promote ARF-to-Rac signaling and cell migration by coordinating the association of ARNO/cytohesin 2 with Dock180. Mol Biol Cell 21:562– 571. CrossRef Medline
79. Winckler B, Forscher P, Mellman I (1999) A diffusion barrier maintains distribution of membrane proteins in polarized neurons. Nature 397: 698–701. CrossRef Medline
80. Zou Y, Chiu H, Zinovyeva A, Ambros V, Chuang CF, Chang C (2013) Developmental decline in neuronal regeneration by the progressive change of two intrinsic timers. Science 340:372–376. CrossRef Medline