Endocytosis and Endosomes at the Crossroads of Regulating Trafficking of Axon Outgrowth-Modifying Receptors

Traffic

Volumn 12, Issue 9, 2011, Pages 1099-1108

  Winckler, Bettina ^a   Choo Yap, Chan ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Axon outgrowth; Axonal trafficking; EHD4 Pincher; Endocytosis; Endosomes; L1 NgCAM; Nogo A; Transcytosis; Trk

Indexed keywords

CELL PROTEIN; EHD4 PROTEIN; MEMBRANE PROTEIN; NERVE CELL ADHESION MOLECULE L1; NEUROTROPHIN; NGCAM PROTEIN; PINCHER PROTEIN; PROTEIN NOGO A; PROTEIN TYROSINE KINASE A; UNCLASSIFIED DRUG;

ANTEROGRADE TRANSPORT; CELL GROWTH; CELL MIGRATION; CELL POLARITY; CELL SELECTION; CELL SURFACE; CELL TRANSPORT; ENDOCYTOSIS; ENDOSOME; HUMAN; NERVE FIBER GROWTH; NERVE FIBER TRANSPORT; NONHUMAN; PERIKARYON; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN TRANSPORT; RETINA CONE; RETROGRADE TRANSPORT; REVIEW; SIGNAL TRANSDUCTION; TRANS GOLGI NETWORK; TRANSCYTOSIS;

ANIMALS; AXONS; CELL ADHESION MOLECULES, NEURON-GLIA; ENDOCYTOSIS; ENDOSOMES; GROWTH CONES; MYELIN PROTEINS; NERVE REGENERATION; NERVE TISSUE PROTEINS; NEURONS; PROTEIN TRANSPORT; RECEPTOR, TRKA; SIGNAL TRANSDUCTION;

EID: 80051665982     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2011.01213.x     Document Type: Review

References (102)

1. Winckler B, Mellman I. Trafficking guidance receptors. Cold Spring Harb Perspect Biol 2010;2:a001826. pp. 1-18.
2. Aridor M, Hannan LA. Traffic jam: a compendium of human diseases that affect intracellular transport processes. Traffic 2000;1:836-851.
3. Wisco D, Anderson ED, Chang MC, Norden C, Boiko T, Folsch H, Winckler B. Uncovering multiple axonal targeting pathways in hippocampal neurons. J Cell Biol 2003;162:1317-1328.
4. Leterrier C, Laine J, Darmon M, Boudin H, Rossier J, Lenkei Z. Constitutive activation drives compartment-selective endocytosis and axonal targeting of type 1 cannabinoid receptors. J Neurosci 2006;26:3141-3153.
5. Bel C, Oguievetskaia K, Pitaval C, Goutebroze L, Faivre-Sarrailh C. Axonal targeting of Caspr2 in hippocampal neurons via selective somatodendritic endocytosis. J Cell Sci 2009;122:3403-3413.
6. Eva R, Dassie E, Caswell PT, Dick G, ffrench-Constant C, Norman JC, Fawcett JW. Rab11 and its effector Rab coupling protein contribute to the trafficking of beta 1 integrins during axon growth in adult dorsal root ganglion neurons and PC12 cells. J Neurosci 2010; 30:11654-11669.
7. Ascano M, Richmond A, Borden P, Kuruvilla R. Axonal targeting of Trk receptors via transcytosis regulates sensitivity to neurotrophin responses. J Neurosci 2009;29:11674-11685.
8. Rosenthal A, Jouet M, Kenwrick S. Aberrant splicing of neural cell adhesion molecule L1 mRNA in a family with X-linked hydrocephalus. Nat Genet 1992;2:107-112.
9. Van Camp G, Vits L, Coucke P, Lyonnet S, Schrander-Stumpel C, Darby J, Holden J, Munnich A, Willems PJ. A duplication in the L1CAM gene associated with X-linked hydrocephalus. Nat Genet 1993;4:421-425.
10. Kamiguchi H, Hlavin ML, Yamasaki M, Lemmon V. Adhesion molecules and inherited diseases of the human nervous system. Annu Rev Neurosci 1998;21:97-125.
11. Grumet M, Edelman GM. Neuron-glia cell adhesion molecule interacts with neurons and astroglia via different binding mechanisms. J Cell Biol 1988;106:487-503.
12. Lemmon V, Farr KL, Lagenaur C. L1-mediated axon outgrowth occurs via a homophilic binding mechanism. Neuron 1989;2: 1597-1603.
13. Yip PM, Zhao X, Montgomery AM, Siu CH. The Arg-Gly-Asp motif in the cell adhesion molecule L1 promotes neurite outgrowth via interaction with the alphavbeta3 integrin. Mol Biol Cell 1998;9:277-290.
14. Kamiguchi H, Long KE, Pendergast M, Schaefer AW, Rapoport I, Kirchhausen T, Lemmon V. The neural cell adhesion molecule L1 interacts with the AP-2 adaptor and is endocytosed via the clathrin-mediated pathway. J Neurosci 1998;18:5311-5321.
15. Davis JQ, McLaughlin T, Bennett V. Ankyrin-binding proteins related to nervous system cell adhesion molecules: candidates to provide transmembrane and intercellular connections in adult brain. J Cell Biol 1993;121:121-133.
16. Garver TD, Ren Q, Tuvia S, Bennett V. Tyrosine phosphorylation at a site highly conserved in the L1 family of cell adhesion molecules abolishes ankyrin binding and increases lateral mobility of neurofascin. J Cell Biol 1997;137:703-714.
17. Dickson TC, Mintz CD, Benson DL, Salton SR. Functional binding interaction identified between the axonal CAM L1 and members of the ERM family. J Cell Biol 2002;157:1105-1112.
18. Nakamura Y, Lee S, Haddox CL, Weaver EJ, Lemmon VP. Role of the cytoplasmic domain of the L1 cell adhesion molecule in brain development. J Comp Neurol 2010;518:1113-1132.
19. Yap CC, Wisco D, Kujala P, Lasiecka ZM, Cannon JT, Chang MC, Hirling H, Klumperman J, Winckler B. The somatodendritic endosomal regulator NEEP21 facilitates axonal targeting of L1/NgCAM. J Cell Biol 2008;180:827-842.
20. Kamiguchi H, Lemmon V. A neuronal form of the cell adhesion molecule L1 contains a tyrosine-based signal required for sorting to the axonal growth cone. J Neurosci 1998;18:3749-3756.
21. Yap CC, Nokes RL, Wisco D, Anderson E, Folsch H, Winckler B. Pathway selection to the axon depends on multiple targeting signals in NgCAM. J Cell Sci 2008;121:1514-1525.
22. Sampo B, Kaech S, Kunz S, Banker G. Two distinct mechanisms target membrane proteins to the axonal surface. Neuron 2003;37:611-624.
23. Schaefer AW, Kamei Y, Kamiguchi H, Wong EV, Rapoport I, Kirchhausen T, Beach CM, Landreth G, Lemmon SK, Lemmon V. L1 endocytosis is controlled by a phosphorylation-dephosphorylation cycle stimulated by outside-in signaling by L1. J Cell Biol 2002;157:1223-1232.
24. Reichardt LF. Neurotrophin-regulated signalling pathways. Philos Trans R Soc Lond B Biol Sci 2006;361:1545-1564.
25. Chao MV. Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat Rev Neurosci 2003;4:299-309.
26. Huang EJ, Reichardt LF. Trk receptors: roles in neuronal signal transduction. Annu Rev Biochem 2003;72:609-642.
27. Ginty DD, Segal RA. Retrograde neurotrophin signaling: Trk-ing along the axon. Curr Opin Neurobiol 2002;12:268-274.
28. Teng KK, Felice S, Kim T, Hempstead BL. Understanding proneurotrophin actions: recent advances and challenges. Dev Neurobiol 2010;70:350-359.
29. Schecterson LC, Bothwell M. Neurotrophin receptors: old friends with new partners. Dev Neurobiol 2010;70:332-338.
30. Segal RA. Selectivity in neurotrophin signaling: theme and variations. Annu Rev Neurosci 2003;26:299-330.
31. Arimura N, Kimura T, Nakamuta S, Taya S, Funahashi Y, Hattori A, Shimada A, Menager C, Kawabata S, Fujii K, Iwamatsu A, Segal RA, Fukuda M, Kaibuchi K. Anterograde transport of TrkB in axons is mediated by direct interaction with Slp1 and Rab27. Dev Cell 2009;16:675-686.
32. Vaegter CB, Jansen P, Fjorback AW, Glerup S, Skeldal S, Kjolby M, Richner M, Erdmann B, Nyengaard JR, Tessarollo L, Lewin GR, Willnow TE, Chao MV, Nykjaer A. Sortilin associates with Trk receptors to enhance anterograde transport and neurotrophin signaling. Nat Neurosci 2011;14:54-61.
33. Yap CC, Lasiecka ZM, Caplan S, Winckler B. Alterations of EHD1/ EHD4 protein levels interfere with L1/NgCAM endocytosis in neurons and disrupt axonal targeting. J Neurosci 2010;30:6646-6657.
34. Grant BD, Caplan S. Mechanisms of EHD/RME-1 protein function in endocytic transport. Traffic 2008;9:2043-2052.
35. Rotem-Yehudar R, Galperin E, Horowitz M. Association of insulin-like growth factor 1 receptor with EHD1 and SNAP29. J Biol Chem 2001;276:33054-33060.
36. Shao Y, Akmentin W, Toledo-Aral JJ, Rosenbaum J, Valdez G, Cabot JB, Hilbush BS, Halegoua S. Pincher, a pinocytic chaperone for nerve growth factor/TrkA signaling endosomes. J Cell Biol 2002;157:679-691.
37. Sharma M, Naslavsky N, Caplan S. A role for EHD4 in the regulation of early endosomal transport. Traffic 2008;9:995-1018.
38. Long KE, Asou H, Snider MD, Lemmon V. The role of endocytosis in regulating L1-mediated adhesion. J Biol Chem 2001;276:1285-1290.
39. Smith CA, Dho SE, Donaldson J, Tepass U, McGlade CJ. The cell fate determinant numb interacts with EHD/Rme-1 family proteins and has a role in endocytic recycling. Mol Biol Cell 2004;15:3698-3708.
40. Steiner P, Sarria JC, Glauser L, Magnin S, Catsicas S, Hirling H. Modulation of receptor cycling by neuron-enriched endosomal protein of 21 kD. J Cell Biol 2002;157:1197-1209.
41. Steiner P, Alberi S, Kulangara K, Yersin A, Sarria JC, Regulier E, Kasas S, Dietler G, Muller D, Catsicas S, Hirling H. Interactions between NEEP21, GRIP1 and GluR2 regulate sorting and recycling of the glutamate receptor subunit GluR2. EMBO J 2005;24:2873-2884.
42. Debaigt C, Hirling H, Steiner P, Vincent JP, Mazella J. Crucial role of neuron-enriched endosomal protein of 21 kDa in sorting between degradation and recycling of internalized G-protein-coupled receptors. J Biol Chem 2004;279:35687-35691.
43. Norstrom EM, Zhang C, Tanzi R, Sisodia SS. Identification of NEEP21 as a beta-amyloid precursor protein-interacting protein in vivo that modulates amyloidogenic processing in vitro. J Neurosci 2010;30:15677-15685.
44. Valdez G, Akmentin W, Philippidou P, Kuruvilla R, Ginty DD, Halegoua S. Pincher-mediated macroendocytosis underlies retrograde signaling by neurotrophin receptors. J Neurosci 2005;25:5236-5247.
45. Joset A, Dodd DA, Halegoua S, Schwab ME. Pincher-generated Nogo-A endosomes mediate growth cone collapse and retrograde signaling. J Cell Biol 2010;188:271-285.
46. Long KE, Lemmon V. Dynamic regulation of cell adhesion molecules during axon outgrowth. J Neurobiol 2000;44:230-245.
47. Schmid RS, Pruitt WM, Maness PF. A MAP kinase-signaling pathway mediates neurite outgrowth on L1 and requires Src-dependent endocytosis. J Neurosci 2000;20:4177-4188.
48. Kamiguchi H, Lemmon V. Recycling of the cell adhesion molecule L1 in axonal growth cones. J Neurosci 2000;20:3676-3686.
49. Kamiguchi H. The mechanism of axon growth: what we have learned from the cell adhesion molecule L1. Mol Neurobiol 2003;28:219-228.
50. Nishimura T, Fukata Y, Kato K, Yamaguchi T, Matsuura Y, Kamiguchi H, Kaibuchi K. CRMP-2 regulates polarized Numb-mediated endocytosis for axon growth. Nat Cell Biol 2003;5:819-826.
51. Miaczynska M, Pelkmans L, Zerial M. Not just a sink: endosomes in control of signal transduction. Curr Opin Cell Biol 2004;16:400-406.
52. Le Roy C, Wrana JL. Clathrin- and non-clathrin-mediated endocytic regulation of cell signalling. Nat Rev Mol Cell Biol 2005;6:112-126.
53. Deinhardt K, Reversi A, Berninghausen O, Hopkins CR, Schiavo G. Neurotrophins redirect p75NTR from a clathrin-independent to a clathrin-dependent endocytic pathway coupled to axonal transport. Traffic 2007;8:1736-1749.
54. Nakata A, Kamiguchi H. Serine phosphorylation by casein kinase II controls endocytic L1 trafficking and axon growth. J Neurosci Res 2007;85:723-734.
55. Zoncu R, Perera RM, Balkin DM, Pirruccello M, Toomre D, De Camilli P. A phosphoinositide switch controls the maturation and signaling properties of APPL endosomes. Cell 2009;136:1110-1121.
56. Bilderback TR, Gazula VR, Lisanti MP, Dobrowsky RT. Caveolin interacts with Trk A and p75(NTR) and regulates neurotrophin signaling pathways. J Biol Chem 1999;274:257-263.
57. Huang CS, Zhou J, Feng AK, Lynch CC, Klumperman J, DeArmond SJ, Mobley WC. Nerve growth factor signaling in caveolae-like domains at the plasma membrane. J Biol Chem 1999;274: 36707-36714.
58. Valdez G, Philippidou P, Rosenbaum J, Akmentin W, Shao Y, Halegoua S. Trk-signaling endosomes are generated by Rac-dependent macroendocytosis. Proc Natl Acad Sci U S A 2007;104:12270-12275.
59. Howe CL, Valletta JS, Rusnak AS, Mobley WC. NGF signaling from clathrin-coated vesicles: evidence that signaling endosomes serve as a platform for the Ras-MAPK pathway. Neuron 2001;32:801-814.
60. Varsano T, Dong MQ, Niesman I, Gacula H, Lou X, Ma T, Testa JR, Yates JR III, Farquhar MG. GIPC is recruited by APPL to peripheral TrkA endosomes and regulates TrkA trafficking and signaling. Mol Cell Biol 2006;26:8942-8952.
61. Lin DC, Quevedo C, Brewer NE, Bell A, Testa JR, Grimes ML, Miller FD, Kaplan DR. APPL1 associates with TrkA and GIPC1 and is required for nerve growth factor-mediated signal transduction. Mol Cell Biol 2006;26:8928-8941.
62. Wu C, Cui B, He L, Chen L, Mobley WC. The coming of age of axonal neurotrophin signaling endosomes. J Proteomics 2009;72:46-55.
63. Wu C, Lai CF, Mobley WC. Nerve growth factor activates persistent Rap1 signaling in endosomes. J Neurosci 2001;21:5406-5416.
64. Liu J, Lamb D, Chou MM, Liu YJ, Li G. Nerve growth factor-mediated neurite outgrowth via regulation of Rab5. Mol Biol Cell 2007;18:1375-1384.
65. Rink J, Ghigo E, Kalaidzidis Y, Zerial M. Rab conversion as a mechanism of progression from early to late endosomes. Cell 2005;122:735-749.
66. Philippidou P, Valdez G, Akmentin W, Bowers WJ, Federoff HJ, Halegoua S. Trk retrograde signaling requires persistent, pincher-directed endosomes. Proc Natl Acad Sci U S A 2011;108:852-857.
67. Deinhardt K, Salinas S, Verastegui C, Watson R, Worth D, Hanrahan S, Bucci C, Schiavo G. Rab5 and Rab7 control endocytic sorting along the axonal retrograde transport pathway. Neuron 2006;52:293-305.
68. Lalli G, Schiavo G. Analysis of retrograde transport in motor neurons reveals common endocytic carriers for tetanus toxin and neurotrophin receptor p75NTR. J Cell Biol 2002;156:233-239.
69. Bronfman FC, Escudero CA, Weis J, Kruttgen A. Endosomal transport of neurotrophins: roles in signaling and neurodegenerative diseases. Dev Neurobiol 2007;67:1183-1203.
70. Bronfman FC, Tcherpakov M, Jovin TM, Fainzilber M. Ligand-induced internalization of the p75 neurotrophin receptor: a slow route to the signaling endosome. J Neurosci 2003;23:3209-3220.
71. Hibbert AP, Kramer BM, Miller FD, Kaplan DR. The localization, trafficking and retrograde transport of BDNF bound to p75NTR in sympathetic neurons. Mol Cell Neurosci 2006;32:387-402.
72. Ibanez CF. Message in a bottle: long-range retrograde signaling in the nervous system. Trends Cell Biol 2007;17:519-528.
73. van de Velde HJ, Roebroek AJ, Senden NH, Ramaekers FC, Van de Ven WJ. NSP-encoded reticulons, neuroendocrine proteins of a novel gene family associated with membranes of the endoplasmic reticulum. J Cell Sci 1994;107:2403-2416.
74. GrandPre T, Nakamura F, Vartanian T, Strittmatter SM. Identification of the Nogo inhibitor of axon regeneration as a reticulon protein. Nature 2000;403:439-444.
75. Oertle T, Schwab ME. Nogo and its paRTNers. Trends Cell Biol 2003;13:187-194.
76. Oertle T, Klinger M, Stuermer CA, Schwab ME. A reticular rhapsody: phylogenic evolution and nomenclature of the RTN/Nogo gene family. FASEB J 2003;17:1238-1247.
77. Huber AB, Weinmann O, Brosamle C, Oertle T, Schwab ME. Patterns of Nogo mRNA and protein expression in the developing and adult rat and after CNS lesions. J Neurosci 2002;22:3553-3567.
78. Oertle T, van der Haar ME, Bandtlow CE, Robeva A, Burfeind P, Buss A, Huber AB, Simonen M, Schnell L, Brosamle C, Kaupmann K, Vallon R, Schwab ME. Nogo-A inhibits neurite outgrowth and cell spreading with three discrete regions. J Neurosci 2003;23:5393-5406.
79. Schweigreiter R, Bandtlow CE. Nogo in the injured spinal cord. J Neurotrauma 2006;23:384-396.
80. McKerracher L, Higuchi H. Targeting Rho to stimulate repair after spinal cord injury. J Neurotrauma 2006;23:309-317.
81. Hu F, Strittmatter SM. The N-terminal domain of Nogo-A inhibits cell adhesion and axonal outgrowth by an integrin-specific mechanism. J Neurosci 2008;28:1262-1269.
82. Fournier AE, GrandPre T, Strittmatter SM. Identification of a receptor mediating Nogo-66 inhibition of axonal regeneration. Nature 2001;409:341-346.
83. Atwal JK, Pinkston-Gosse J, Syken J, Stawicki S, Wu Y, Shatz C, Tessier-Lavigne M. PirB is a functional receptor for myelin inhibitors of axonal regeneration. Science 2008;322:967-970.
84. Mi S, Lee X, Shao Z, Thill G, Ji B, Relton J, Levesque M, Allaire N, Perrin S, Sands B, Crowell T, Cate RL, McCoy JM, Pepinsky RB. LINGO-1 is a component of the Nogo-66 receptor/p75 signaling complex. Nat Neurosci 2004;7:221-228.
85. Park JB, Yiu G, Kaneko S, Wang J, Chang J, He XL, Garcia KC, He Z. A TNF receptor family member, TROY, is a coreceptor with Nogo receptor in mediating the inhibitory activity of myelin inhibitors. Neuron 2005;45:345-351.
86. Shao Z, Browning JL, Lee X, Scott ML, Shulga-Morskaya S, Allaire N, Thill G, Levesque M, Sah D, McCoy JM, Murray B, Jung V, Pepinsky RB, Mi S. TAJ/TROY, an orphan TNF receptor family member, binds Nogo-66 receptor 1 and regulates axonal regeneration. Neuron 2005;45:353-359.
87. Domeniconi M, Cao Z, Spencer T, Sivasankaran R, Wang K, Nikulina E, Kimura N, Cai H, Deng K, Gao Y, He Z, Filbin M. Myelin-associated glycoprotein interacts with the Nogo66 receptor to inhibit neurite outgrowth. Neuron 2002;35:283-290.
88. Wang KC, Koprivica V, Kim JA, Sivasankaran R, Guo Y, Neve RL, He Z. Oligodendrocyte-myelin glycoprotein is a Nogo receptor ligand that inhibits neurite outgrowth. Nature 2002;417:941-944.
89. Zheng B, Ho C, Li S, Keirstead H, Steward O, Tessier-Lavigne M. Lack of enhanced spinal regeneration in Nogo-deficient mice. Neuron 2003;38:213-224.
90. Freund P, Schmidlin E, Wannier T, Bloch J, Mir A, Schwab ME, Rouiller EM. Nogo-A-specific antibody treatment enhances sprouting and functional recovery after cervical lesion in adult primates. Nat Med 2006;12:790-792.
91. Thallmair M, Metz GA, Z'Graggen WJ, Raineteau O, Kartje GL, Schwab ME. Neurite growth inhibitors restrict plasticity and functional recovery following corticospinal tract lesions. Nat Neurosci 1998;1:124-131.
92. Carcea I, Ma'ayan A, Mesias R, Sepulveda B, Salton SR, Benson DL. Flotillin-mediated endocytic events dictate cell type-specific responses to semaphorin 3A. J Neurosci 2010;30:15317-15329.
93. Harvey PA, Lee DH, Qian F, Weinreb PH, Frank E. Blockade of Nogo receptor ligands promotes functional regeneration of sensory axons after dorsal root crush. J Neurosci 2009;29:6285-6295.
94. Foscarin S, Gianola S, Carulli D, Fazzari P, Mi S, Tamagnone L, Rossi F. Overexpression of GAP-43 modifies the distribution of the receptors for myelin-associated growth-inhibitory proteins in injured Purkinje axons. Eur J Neurosci 2009;30:1837-1848.
95. Cai D, Shen Y, De Bellard M, Tang S, Filbin MT. Prior exposure to neurotrophins blocks inhibition of axonal regeneration by MAG and myelin via a cAMP-dependent mechanism. Neuron 1999;22:89-101.
96. Gao Y, Nikulina E, Mellado W, Filbin MT. Neurotrophins elevate cAMP to reach a threshold required to overcome inhibition by MAG through extracellular signal-regulated kinase-dependent inhibition of phosphodiesterase. J Neurosci 2003;23:11770-11777.
97. Roonprapunt C, Huang W, Grill R, Friedlander D, Grumet M, Chen S, Schachner M, Young W. Soluble cell adhesion molecule L1-Fc promotes locomotor recovery in rats after spinal cord injury. J Neurotrauma 2003;20:871-882.
98. Chen J, Wu J, Apostolova I, Skup M, Irintchev A, Kugler S, Schachner M. Adeno-associated virus-mediated L1 expression promotes functional recovery after spinal cord injury. Brain 2007;130:954-969.
99. Gao Y, Deng K, Hou J, Bryson JB, Barco A, Nikulina E, Spencer T, Mellado W, Kandel ER, Filbin MT. Activated CREB is sufficient to overcome inhibitors in myelin and promote spinal axon regeneration in vivo. Neuron 2004;44:609-621.
100. DeBellard ME, Tang S, Mukhopadhyay G, Shen YJ, Filbin MT. Myelin-associated glycoprotein inhibits axonal regeneration from a variety of neurons via interaction with a sialoglycoprotein. Mol Cell Neurosci 1996;7:89-101.
101. Song HJ, Ming GL, Poo MM. cAMP-induced switching in turning direction of nerve growth cones. Nature 1997;388:275-279.
102. Wang Q, Zheng JQ. cAMP-mediated regulation of neurotrophin-induced collapse of nerve growth cones. J Neurosci 1998;18: 4973-4984.