Neurotrophin signaling endosomes: Biogenesis, regulation, and functions

Current Opinion in Neurobiology

Volumn 39, Issue , 2016, Pages 139-145

  Yamashita, Naoya ^a   Kuruvilla, Rejji ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROTROPHIN; PROTEIN TYROSINE KINASE; NERVE GROWTH FACTOR;

BIOGENESIS; CELL COMPARTMENTALIZATION; CELL MIGRATION; DEVELOPMENTAL DISORDER; ENDOSOME; HUMAN; MOLECULAR MECHANICS; NERVE FIBER; NEUROLOGIC DISEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN TRANSPORT; REVIEW; SIGNAL TRANSDUCTION; METABOLISM; NERVE CELL; PHYSIOLOGY;

ENDOSOMES; HUMANS; NERVE GROWTH FACTORS; NEURONS; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

EID: 84974666995     PISSN: 09594388     EISSN: 18736882     Source Type: Journal    
DOI: 10.1016/j.conb.2016.06.004     Document Type: Review

References (50)

1. Chao M.V. Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat Rev Neurosci 2003, 4:299-309.
2. Huang E.J., Reichardt L.F. Trk receptors: roles in neuronal signal transduction. Annu Rev Biochem 2003, 72:609-642.
3. Cosker K.E., Segal R.A. Neuronal signaling through endocytosis. Cold Spring Harb Perspect Biol 2014, 6.
4. Harrington A.W., Ginty D.D. Long-distance retrograde neurotrophic factor signalling in neurons. Nat Rev Neurosci 2013, 14:177-187.
5. Ascano M., Bodmer D., Kuruvilla R. Endocytic trafficking of neurotrophins in neural development. Trends Cell Biol 2012, 22:266-273.
6. Howe C.L., Valletta J.S., Rusnak A.S., Mobley W.C. NGF signaling from clathrin-coated vesicles: evidence that signaling endosomes serve as a platform for the Ras-MAPK pathway. Neuron 2001, 32:801-814.
7. Shao Y., Akmentin W., Toledo-Aral J.J., Rosenbaum J., Valdez G., Cabot J.B., Hilbush B.S., Halegoua S. Pincher, a pinocytic chaperone for nerve growth factor/TrkA signaling endosomes. J Cell Biol 2002, 157:679-691.
8. 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.
9. Beattie E.C., Howe C.L., Wilde A., Brodsky F.M., Mobley W.C. NGF signals through TrkA to increase clathrin at the plasma membrane and enhance clathrin-mediated membrane trafficking. J Neurosci 2000, 20:7325-7333.
10. Bodmer D., Ascano M., Kuruvilla R. Isoform-specific dephosphorylation of dynamin1 by calcineurin couples neurotrophin receptor endocytosis to axonal growth. Neuron 2011, 70:1085-1099.
11. Harrington A.W., St Hillaire C., Zweifel L.S., Glebova N.O., Philippidou P., Halegoua S., Ginty D.D. Recruitment of actin modifiers to TrkA endosomes governs retrograde NGF signaling and survival. Cell 2011, 146:421-434.
12. Kuruvilla R., Ye H., Ginty D.D. Spatially and functionally distinct roles of the PI3-K effector pathway during NGF signaling in sympathetic neurons. Neuron 2000, 27:499-512.
13. Ure D.R., Campenot R.B. Retrograde transport and steady state distribution of 125-NGF in rat sympathetic neurons in compartmentalized cultures. J Neurosci 1997, 17:1282-1290.
14. Tsui-Pierchala B.A., Ginty D.D. Characterization of an NGF-P-TrkA retrograde signaling complex and age-dependent regulation of TrkA phosphorylation in sympathetic neurons. J Neurosci 1999, 19:8207-8218.
15. Arevalo J.C., Waite J., Rajagopal R., Beyna M., Chen Z.Y., Lee F.S., Chao M.V. Cell survival through Trk neurotrophin receptors is differentially regulated by ubiquitination. Neuron 2006, 50:549-559.
16. Yu T., Calvo L., Anta B., Lopez-Benito S., Southon E., Chao M.V., Tessarollo L., Arevalo J.C. Regulation of trafficking of activated TrkA is critical for NGF-mediated functions. Traffic 2011, 12:521-534.
17. Sigismund S., Argenzio E., Tosoni D., Cavallaro E., Polo S., Di Fiore P.P. Clathrin-mediated internalization is essential for sustained EGFR signaling but dispensable for degradation. Dev Cell 2008, 15:209-219.
18. Belliveau D.J., Krivko I., Kohn J., Lachance C., Pozniak C., Rusakov D., Kaplan D., Miller F.D. NGF and neurotrophin-3 both activate TrkA on sympathetic neurons but differentially regulate survival and neuritogenesis. J Cell Biol 1997, 136:375-388.
19. Kuruvilla R., Zweifel L.S., Glebova N.O., Lonze B.E., Valdez G., Ye H., Ginty D.D. A neurotrophin signaling cascade coordinates sympathetic neuron development through differential control of TrkA trafficking and retrograde signaling. Cell 2004, 118:243-255.
20. Heerssen H.M., Pazyra M.F., Segal R.A. Dynein motors transport activated Trks to promote survival of target-dependent neurons. Nat Neurosci 2004, 7:596-604.
21. Moughamian A.J., Osborn G.E., Lazarus J.E., Maday S., Holzbaur E.L. Ordered recruitment of dynactin to the microtubule plus-end is required for efficient initiation of retrograde axonal transport. J Neurosci 2013, 33:13190-13203.
22. Lee H.S., Komarova Y.A., Nadezhdina E.S., Anjum R., Peloquin J.G., Schober J.M., Danciu O., van Haren J., Galjart N., Gygi S.P., et al. Phosphorylation controls autoinhibition of cytoplasmic linker protein-170. Mol Biol Cell 2010, 21:2661-2673.
23. Kardon J.R., Vale R.D. Regulators of the cytoplasmic dynein motor. Nat Rev Mol Cell Biol 2009, 10:854-865.
24. Ha J., Lo K.W., Myers K.R., Carr T.M., Humsi M.K., Rasoul B.A., Segal R.A., Pfister K.K. A neuron-specific cytoplasmic dynein isoform preferentially transports TrkB signaling endosomes. J Cell Biol 2008, 181:1027-1039.
25. Yano H., Lee F.S., Kong H., Chuang J., Arevalo J., Perez P., Sung C., Chao M.V. Association of Trk neurotrophin receptors with components of the cytoplasmic dynein motor. J Neurosci 2001, 21:RC125.
26. Zhou B., Cai Q., Xie Y., Sheng Z.H. Snapin recruits dynein to BDNF-TrkB signaling endosomes for retrograde axonal transport and is essential for dendrite growth of cortical neurons. Cell Rep 2012, 2:42-51.
27. Mitchell D.J., Blasier K.R., Jeffery E.D., Ross M.W., Pullikuth A.K., Suo D., Park J., Smiley W.R., Lo K.W., Shabanowitz J., et al. Trk activation of the ERK1/2 kinase pathway stimulates intermediate chain phosphorylation and recruits cytoplasmic dynein to signaling endosomes for retrograde axonal transport. J Neurosci 2012, 32:15495-15510.
28. Bhattacharyya A., Watson F.L., Pomeroy S.L., Zhang Y.Z., Stiles C.D., Segal R.A. High-resolution imaging demonstrates dynein-based vesicular transport of activated Trk receptors. J Neurobiol 2002, 51:302-312.
29. Delcroix J.D., Valletta J.S., Wu C., Hunt S.J., Kowal A.S., Mobley W.C. NGF signaling in sensory neurons: evidence that early endosomes carry NGF retrograde signals. Neuron 2003, 39:69-84.
30. 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.
31. Watson F.L., Heerssen H.M., Bhattacharyya A., Klesse L., Lin M.Z., Segal R.A. Neurotrophins use the Erk5 pathway to mediate a retrograde survival response. Nat Neurosci 2001, 4:981-988.
32. Riccio A., Pierchala B., Ciarallo C., Ginty D.D. An NGF-TrkA-mediated retrograde signal to transcription factor CREB in sympathetic neurons. Science 1997, 227:1097-1100.
33. Pazyra-Murphy M.F., Hans A., Courchesne S.L., Karch C., Cosker K.E., Heerssen H.M., Watson F.L., Kim T., Greenberg M.E., Segal R.A. A retrograde neuronal survival response: target-derived neurotrophins regulate MEF2D and bcl-w. J Neurosci 2009, 29:6700-6709.
34. Wickramasinghe S.R., Alvania R.S., Ramanan N., Wood J.N., Mandai K., Ginty D.D. Serum response factor mediates NGF-dependent target innervation by embryonic DRG sensory neurons. Neuron 2008, 58:532-545.
35. Graef I.A., Wang F., Charron F., Chen L., Neilson J., Tessier-Lavigne M., Crabtree G.R. Neurotrophins and netrins require calcineurin/NFAT signaling to stimulate outgrowth of embryonic axons. Cell 2003, 113:657-670.
36. Deppmann C.D., Mihalas S., Sharma N., Lonze B.E., Niebur E., Ginty D.D. A model for neuronal competition during development. Science 2008, 320:369-373.
37. Mandai K., Guo T., St Hillaire C., Meabon J.S., Kanning K.C., Bothwell M., Ginty D.D. LIG family receptor tyrosine kinase-associated proteins modulate growth factor signals during neural development. Neuron 2009, 63:614-627.
38. Suo D., Park J., Harrington A.W., Zweifel L.S., Mihalas S., Deppmann C.D. Coronin-1 is a neurotrophin endosomal effector that is required for developmental competition for survival. Nat Neurosci 2014, 17:36-45.
39. Terenzio M., Golding M., Russell M.R., Wicher K.B., Rosewell I., Spencer-Dene B., Ish-Horowicz D., Schiavo G. Bicaudal-D1 regulates the intracellular sorting and signalling of neurotrophin receptors. EMBO J 2014, 33:1582-1598.
40. Sharma N., Deppmann C.D., Harrington A.W., St Hillaire C., Chen Z.Y., Lee F.S., Ginty D.D. Long-distance control of synapse assembly by target-derived NGF. Neuron 2010, 67:422-434.
41. Lazo O.M., Gonzalez A., Ascano M., Kuruvilla R., Couve A., Bronfman F.C. BDNF regulates Rab11-mediated recycling endosome dynamics to induce dendritic branching. J Neurosci 2013, 33:6112-6122.
42. Song M., Giza J., Proenca C.C., Jing D., Elliott M., Dincheva I., Shmelkov S.V., Kim J., Schreiner R., Huang S.H., et al. Slitrk5 mediates BDNF-dependent TrkB receptor trafficking and signaling. Dev Cell 2015, 33:690-702.
43. Salehi A., Delcroix J.D., Mobley W.C. Traffic at the intersection of neurotrophic factor signaling and neurodegeneration. Trends Neurosci 2003, 26:73-80.
44. Bronfman F.C., Escudero C.A., Weis J., Kruttgen A. Endosomal transport of neurotrophins: roles in signaling and neurodegenerative diseases. Dev Neurobiol 2007, 67:1183-1203.
45. Yap C.C., Winckler B. Acid indigestion in the endosome: linking signaling dysregulation to neurodevelopmental disorders. Neuron 2013, 80:4-6.
46. Patel A., Yamashita N., Ascano M., Bodmer D., Boehm E., Bodkin-Clarke C., Ryu Y.K., Kuruvilla R. RCAN1 links impaired neurotrophin trafficking to aberrant development of the sympathetic nervous system in Down syndrome. Nat Commun 2015, 6:10119.
47. Salehi A., Delcroix J.D., Belichenko P.V., Zhan K., Wu C., Valletta J.S., Takimoto-Kimura R., Kleschevnikov A.M., Sambamurti K., Chung P.P., et al. Increased App expression in a mouse model of Down's syndrome disrupts NGF transport and causes cholinergic neuron degeneration. Neuron 2006, 51:29-42.
48. Keating D.J., Chen C., Pritchard M.A. Alzheimer's disease and endocytic dysfunction: clues from the Down syndrome-related proteins, DSCR1 and ITSN1. Ageing Res Rev 2006, 5:388-401.
49. Ouyang Q., Lizarraga S.B., Schmidt M., Yang U., Gong J., Ellisor D., Kauer J.A., Morrow E.M. Christianson syndrome protein NHE6 modulates TrkB endosomal signaling required for neuronal circuit development. Neuron 2013, 80:97-112.
50. Sardiello M., Palmieri M., di Ronza A., Medina D.L., Valenza M., Gennarino V.A., Di Malta C., Donaudy F., Embrione V., Polishchuk R.S., et al. A gene network regulating lysosomal biogenesis and function. Science 2009, 325:473-477.