Signaling Endosome Hypothesis: A Cellular Mechanism for Long Distance Communication

Journal of Neurobiology

Volumn 58, Issue 2, 2004, Pages 207-216

  Howe, Charles L ^a   Mobley, William C ^b  

^a MAYO CLINIC   (United States)

^b STANFORD UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Axon; Calcium; Clathrin coated vesicle; Diffusion; Early endosome; Inositol 1,4,5 trisphosphate; Neuron; Neurotrophic factor hypothsesis; Neurotrophin; Retrograde transport; Signaling endosome hypothesis

Indexed keywords

CALCIUM; CLATHRIN; INOSITOL 1,4,5 TRISPHOSPHATE; NEUROTROPHIN;

CELL COMMUNICATION; CELL FUNCTION; CELL INTERACTION; CELL TYPE; DIFFUSION; ENDOSOME; HYPOTHESIS; NERVE FIBER TRANSPORT; NONHUMAN; PRIORITY JOURNAL; RETROGRADE NERVE FIBER TRANSPORT; REVIEW; SIGNAL TRANSDUCTION; SIGNALING ENDOSOME HYPOTHESIS;

ANIMALS; AXONAL TRANSPORT; CELL COMMUNICATION; ENDOSOMES; KINETICS; MODELS, BIOLOGICAL; NERVE GROWTH FACTOR;

EID: 0842333853     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/neu.10323     Document Type: Review

References (62)

1. Allbritton NL, Meyer T, Stryer L. 1992. Range of messenger action of calcium ion and inositol 1,4,5-trisphosphate. Science 258:1812-1815.
2. Beattie EC, Howe CL, Wilde A, Brodsky FM, Mobley WC. 2000. NGF signals through TrkA to increase clathrin at the plasma membrane and enhance clathrin-mediated membrane trafficking. J Neurosci 20:7325-7333.
3. Beattie EC, Zhou J, Grimes ML, Bunnett NW, Howe CL, Mobley WC. 1996. A signaling endosome hypothesis to explain NGF actions: potential implications for neurodegeneration. Cold Spring Harb Symp Quant Biol 61:389-406.
4. Beguinot L, Lyall RM, Willingham MC, Pastan I. 1984. Down-regulation of the epidermal growth factor receptor in KB cells is due to receptor internalization and subsequent degradation in lysosomes. Proc Natl Acad Sci USA 81:2384-2388.
5. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE. 2000. The Protein Data Bank. Nucleic Acids Res 28:235-242.
6. Berridge MJ. 1998. Neuronal calcium signaling. Neuron 21:13-26.
7. Bhattacharyya A, Watson FL, Bradlee TA, Pomeroy SL, Stiles CD, Segal RA. 1997. Trk receptors function as rapid retrograde signal carriers in the adult nervous system. J Neurosci 17:7007-7016.
8. Bhattacharyya A, Watson FL, Pomeroy SL, Zhang YZ, Stiles CD, Segal RA. 2002. High-resolution imaging demonstrates dynein-based vesicular transport of activated Trk receptors. J Neurobiol 51:302-312.
9. Blaustein MP, Golovina VA. 2001. Structural complexity and functional diversity of endoplasmic reticulum Ca(2+) stores. Trends Neurosci 24:602-608.
10. Campenot RB. 1994. NGF and the local control of nerve terminal growth. J Neurobiol 25:599-611.
11. Canagarajah BJ, Khokhlatchev A, Cobb MH, Goldsmith EJ. 1997. Activation mechanism of the MAP kinase ERK2 by dual phosphorylation. Cell 90:859-869.
12. Claude P, Hawrot E, Dunis DA, Campenot RB. 1982. Binding, internalization, and retrograde transport of 1251-nerve growth factor in cultured rat sympathetic neurons. J Neurosci 2:431-442,
13. Crank J. 1979. The Mathematics of Diffusion. Oxford: Clarendon. 414 p.
14. Delcroix JD, Valletta JS, Wu C, Hunt SV, Kowal AS, Mobley WC. 2003. NGF Signaling in sensory neurons: evidence that early endosomes carry NGF retrograde signals. Neuron 39:69-84.
15. DiStefano PS, Friedman B, Radziejewski C, Alexander C, Boland P, Schick CM, Lindsay RM, Wiegand SJ. 1992. The neurotrophins BDNF, NT-3, and NGF display distinct patterns of retrograde axonal transport in peripheral and central neurons. Neuron 8:983-993.
16. Ehlers MD, Kaplan DR, Price DL, Koliatsos VE. 1995. NGF-stimulated retrograde transport of trkA in the mammalian nervous system. J Cell Biol 130:149-156.
17. Fitzsimonds RM, Poo MM. 1998. Retrograde signaling in the development and modification of synapses. Physiol Rev 78:143-170.
18. Ginty DD, Bonni A, Greenberg ME. 1994. Nerve growth factor activates a Ras-dependent protein kinase that stimulates c-fos transcription via phosphorylation of CREB. Cell 77:713-725.
19. Ginty DD, Segal RA. 2002. Retrograde neurotrophin signaling: Trk-ing along the axon. Curr Opin Neurobiol 12:268-274.
20. Grimes ML, Zhou J, Beattie EC, Yuen EC, Hall DE, Valletta JS, Topp KS, LaVail JH, Bunnett NW, Mobley WC. 1996. Endocytosis of activated TrkA: evidence that nerve growth factor induces formation of signaling endosomes. J Neurosci 16:7950-7964.
21. Haak RA, Kleinhans FW, Ochs S. 1976. The viscosity of mammalian nerve axoplasm measured by electron spin resonance. J Physiol 263:115-137.
22. Hendry IA, Crouch M. 1993. Synergy, retrograde transport, and cell death. In: Loughlin SE, Fallon JH, editors. Neurotrophic Factors. Boston: Academic, p 51-88.
23. Hendry IA, Stockel K, Thoenen H, Iversen LL. 1974. The retrograde axonal transport of nerve growth factor. Brain Res 68:103-121.
24. Heumann R, Schwab M, Thoenen H. 1981. A second messenger required for nerve growth factor biological activity? Nature 292:838-840.
25. Hosang M, Shooter EM. 1987. The internalization of nerve growth factor by high-affinity receptors on pheochromocytoma PC12 cells. Embo J 6:1197-1202.
26. Howe CL, Mobley WC. 2001. Nerve Growth Factor Effects on Cholinergic Modulation of Hippocampal and Cortical Plasticity. In: Mocchetti I, editor. Neurobiology of the Neurotrophins. Johnson City, TN: F.P. Graham Publishing, p 255-307.
27. Howe CL, Valletta JS, Rusnak AS, Mobley WC. 2001. NGF signaling from clathrin-coated vesicles: evidence that signaling endosomes serve as a platform for the Ras-MAPK pathway. Neuron 32:801-814.
28. Johanson SO, Crouch MF, Hendry IA. 1995. Retrograde axonal transport of signal transduction proteins in rat sciatic nerve. Brain Res 690:55-63.
29. Johenning FW, Zochowski M, Conway SJ, Holmes AB, Koulen P, Ehrlich BE. 2002. Distinct intracellular calcium transients in neurites and somata integrate neuronal signals. J Neurosci 22:5344-5353,
30. Johnson EM Jr, Andres RY, Bradshaw RA. 1978. Characterization of the retrograde transport of nerve growth factor (NGF) using high specific activity [125I] NGF. Brain Res 150:319-331.
31. Johnson EM Jr, Taniuchi M, Clark HB, Springer JE, Koh S, Tayrien MW, Loy R. 1987. Demonstration of the retrograde transport of nerve growth factor receptor in the peripheral and central nervous system. J Neurosci 7:923-929.
32. Kelley GG, Reks SE, Ondrako JM, Smrcka AV. 2001. Phospholipase C(epsilon): a novel Ras effector. Embo J 20:743-754.
33. Korsching S. 1993. The neurotrophic factor concept: a reexamination. J Neurosci 13:2739-2748.
34. Korsching S, Thoenen H. 1983a. Nerve growth factor in sympathetic ganglia and corresponding target organs of the rat: correlation with density of sympathetic innervation. Proc Natl Acad Sci USA 80:3513-3516.
35. Korsching S, Thoenen H. 1983b. Quantitative demonstration of the retrograde axonal transport of endogenous nerve growth factor. Neurosci Lett 39:1-4.
36. Kuruvilla R, Ye H, Ginty DD. 2000. Spatially and functionally distinct roles of the PI3-K effector pathway during NGF signaling in sympathetic neurons. Neuron 27:499-512.
37. Layer PG, Shooter EM. 1983, Binding and degradation of nerve growth factor by PC12 pheochromocytoma cells. J Biol Chem 258:3012-3018.
38. Lopez I, Mak EC, Ding J, Hamm HE, Lomasney JW. 2001, A novel bifunctional phospholipase c that is regulated by Galpha 12 and stimulates the Ras/mitogen-activated protein kinase pathway. J Biol Chem 276:2758-2765,
39. MacInnis BL, Campenot RB. 2002. Retrograde support of neuronal survival without retrograde transport of nerve growth factor. Science 295:1536-1539.
40. Mahadeo D, Kaplan L, Chao MV, Hempstead BL. 1994. High affinity nerve growth factor binding displays a faster rate of association than p140trk binding. Implications for multi-subunit polypeptide receptors. J Biol Chem 269:6884-6891.
41. Nguyen T, Chin WC, Verdugo P. 1998. Role of Ca2+/K+ ion exchange in intracellular storage and release of Ca2+. Nature 395:908-912.
42. Nichols BJ, Lippincott-Schwartz J. 2001. Endocytosis without clathrin coats. Trends Cell Biol 11:406-412.
43. Riccio A, Pierchala BA, Ciarallo CL, Ginty DD. 1997. An NGF-TrkA-mediated retrograde signal to transcription factor CREB in sympathetic neurons. Science 277:1097-1100.
44. Richardson PM, Riopelle RJ. 1984. Uptake of nerve growth factor along peripheral and spinal axons of primary sensory neurons. J Neurosci 4:1683-1689.
45. Senger DL, Campenot RB. 1997. Rapid retrograde tyrosine phosphorylation of trkA and other proteins in rat sympathetic neurons in compartmented cultures. J Cell Biol 138:411-421.
46. Shao Y, Akmentin W, Toledo-Aral JJ, Rosenbaum J, Valdez G, Cabot JB, Hilbush BS, Halegoua S. 2002. Pincher, a pinocytic chaperone for nerve growth factor/TrkA signaling endosomes. J Cell Biol 157:679-691.
47. Sofroniew MV, Howe CL, Mobley WC. 2001. Nerve growth factor signaling, neuroprotection, and neural repair. Annu Rev Neurosci 24:1217-1281.
48. Song C, Hu CD, Masago M, Kariyai K, Yamawaki-Kataoka Y, Shibatohge M, Wu D, Satoh T, Kataoka T. 2001. Regulation of a novel human phospholipase C, PLCepsilon, through membrane targeting by Ras. J Biol Chem 276:2752-2757.
49. Sorkin A, Carpenter G. 1993. Interaction of activated EGF receptors with coated pit adaptins. Science 261:612-615.
50. Stoeckel K, Guroff G, Schwab M, Thoenen H. 1976. The significance of retrograde axonal transport for the accumulation of systemically administered nerve growth factor (NGF) in the rat superior cervical ganglion. Brain Res 109:271-284.
51. Stoeckel K, Schwab M, Thoenen H. 1975a. Comparison between the retrograde axonal transport of nerve growth factor and tetanus toxin in motor, sensory and adrenergic neurons. Brain Res 99:1-16.
52. Stoeckel K, Schwab M, Thoenen H. 1975b. Specificity of retrograde transport of nerve growth factor (NGF) in sensory neurons: a biochemical and morphological study. Brain Res 89:1-14.
53. Stoscheck CM, Carpenter G. 1984. Down regulation of epidermal growth factor receptors: direct demonstration of receptor degradation in human fibroblasts. J Cell Biol 98:1048-1053.
54. Tsien RW, Tsien RY. 1990. Calcium channels, stores, and oscillations. Annu Rev Cell Biol 6:715-760.
55. Tsui-Pierchala BA, Ginty DD. 1999. Characterization of an NGF-P-TrkA retrograde-signaling complex and age-dependent regulation of TrkA phosphorylation in sympathetic neurons. J Neurosci 19:8207-8218.
56. Ure DR, Campenot RB. 1997. Retrograde transport and steady-state distribution of 125I-nerve growth factor in rat sympathetic neurons in compartmented cultures. J Neurosci 17:1282-1290.
57. Watson FL, Heerssen HM, Bhattacharyya A, Klesse L, Lin MZ, Segal RA. 2001. Neurotrophins use the Erk5 pathway to mediate a retrograde survival response. Nat Neurosci 4:981-988.
58. Watson FL, Heerssen HM, Moheban DB, Lin MZ, Sauvageot CM, Bhattacharyya A, Pomeroy SL, Segal RA. 1999, Rapid nuclear responses to target-derived neurotrophins require retrograde transport of ligand-receptor complex. J Neurosci 19:7889-7900.
59. Wu C, Lai CF, Mobley WC. 2001. Nerve growth factor activates persistent Rap1 signaling in endosomes. J Neurosci 21:5406-5416.
60. Ye H, Kuruvilla R, Zweifel LS, Ginty DD. 2003. Evidence in support of signaling endosome-based retrograde survival of sympathetic neurons. Neuron 39:57-68.
61. Yip HK, Johnson EM Jr. 1986. Comparative dynamics of retrograde transport of nerve growth factor and horseradish peroxidase in rat lumbar dorsal root ganglia. J Neurocytol 15:789-798.
62. Zhou J, Valletta JS, Grimes ML, Mobley WC. 1995. Multiple levels for regulation of TrkA in PC12 cells by nerve growth factor. J Neurochem 65:1146-1156.