Endocytic control of growth factor signalling: Multivesicular bodies as signalling organelles

Nature Reviews Molecular Cell Biology

Volumn 13, Issue 1, 2012, Pages 53-60

  Dobrowolski, Radek ^a   De Robertis, Edward M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESCRT PROTEIN; GLYCOGEN SYNTHASE KINASE 3; GROWTH FACTOR; WNT PROTEIN;

BIOGENESIS; CELL ORGANELLE; CELLULAR DISTRIBUTION; CYTOSOL; DEGRADATION KINETICS; DOWN REGULATION; ENDOCYTOSIS; ENDOSOME; HUMAN; LYSOSOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN STABILITY; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; ENDOCYTOSIS; GLYCOGEN SYNTHASE KINASE 3; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LYSOSOMES; MULTIVESICULAR BODIES; RATS; SIGNAL TRANSDUCTION; WNT SIGNALING PATHWAY;

EID: 84355162786     PISSN: 14710072     EISSN: 14710080     Source Type: Journal    
DOI: 10.1038/nrm3244     Document Type: Review

References (85)

1. Katzmann, D. J., Odorizzi, G. & Emr, S. D. Receptor downregulation and multivesicular-body sorting. Nature Rev. Mol. Cell Biol. 12, 893-905 (2002). (Pubitemid 35477368)
2. Piper, R. C. & Katzmann, D. J. Biogenesis and function of multivesicular bodies. Annu. Rev. Cell Dev. Biol. 23, 519-547 (2007).
3. McKanna, J. A., Haigler, H. T. & Cohen, S. Hormone receptor topology and dynamics: morphological analysis using ferritin-labeled epidermal growth factor. Proc. Natl Acad. Sci. USA 76, 5689-5693 (1979). (Pubitemid 10168672)
4. Hurley, J. H. ESCRT complexes and the biogenesis of multivesicular bodies. Curr. Opin. Cell Biol. 20, 4-11 (2008).
5. Raiborg, C. & Stenmark, H. The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature 458, 445-452 (2009).
6. Sorkin, A. & von Zastrow, M. Endocytosis and signalling: intertwining molecular networks. Nature Rev. Mol. Cell Biol. 10, 609-622 (2009).
7. 2- Rab11a interaction. Mol. Biol. Cell 19, 4188-4200 (2008).
8. Grimes, M. L. et al. Endocytosis of activated TrkA: evidence that nerve growth factor induces formation of signaling endosomes. J. Neurosci. 16, 7950-7964 (1996). (Pubitemid 26405058)
9. Watson, F. L. et al. Neurotrophins use the Erk5 pathway to mediate a retrograde survival response. Nature Neurosci. 4, 981-988 (2001). (Pubitemid 32924137)
10. Tsukazaki, T., Chiang, T. A., Davison, A. F., Attisano, L. & Wrana, J. L. SARA, a FYVE domain protein that recruits Smad2 to the TGFβ receptor. Cell 95, 779-791 (1998). (Pubitemid 29014458)
11. Hayes, S., Chawla, A. & Corvera, S. TGFβ receptor internalization into EEA1-enriched early endosomes: role in signaling to Smad2. J. Cell Biol. 158, 1239-1249 (2002).
12. Taelman, V. F. et al. Wnt signaling requires sequestration of glycogen synthase kinase 3 inside multivesicular endosomes. Cell 143, 1136-1148 (2010).
13. Bilic, J. et al. Wnt induces LRP6 signalosomes and promotes Dishevelled-dependent LRP6 phosphorylation. Science 316, 1619-1622 (2007). (Pubitemid 46982035)
14. Zeng, X. et al. Initiation of Wnt signaling: control of Wnt coreceptor Lrp6 phosphorylation/activation via Frizzled, Dishevelled and Axin functions. Development 135, 367-375 (2008). (Pubitemid 351228428)
15. Metcalfe, C., Mendoza-Topaz, C., Mieszczanek, J. & Bienz, M. Stability elements in the LRP6 cytoplasmic tail confer efficient signalling upon DIX-dependent polymerization. J. Cell Sci. 123, 1588-1599 (2010).
16. Mi, K., Dolan, P. J. & Johnson, G. V. W. The low density lipoprotein receptor-related protein 6 interacts with glycogen synthase kinase 3 and attenuates activity. J. Biol. Chem. 281, 4787-4794 (2006). (Pubitemid 43847740)
17. Cselenyi, C. S. et al. LRP6 transduces a canonical Wnt signal independently of Axin degradation by inhibiting GSK3's phosphorylation of β-catenin. Proc. Natl Acad. Sci. USA 105, 8032-8037 (2008). (Pubitemid 351904702)
18. Piao, S. et al. Direct inhibition of GSK3β by the phosphorylated cytoplasmic domain of LRP6 in Wnt/β-catenin signaling. PLoS ONE 3, e4046 (2008).
19. Wu, G., Huang, H., Garcia Abreu, J. & He, X. Inhibition of GSK3 phosphorylation of β-catenin via phosphorylated PPPSPXS motifs of Wnt coreceptor LRP6. PLoS ONE 4, e4926 (2009).
20. Ding, V. W., Chen, R. H. & McCormick, F. Differential regulation of glycogen synthase kinase 3β by insulin and Wnt signaling. J. Biol. Chem. 275, 32475-32481 (2000).
21. Blitzer, J. T. & Nusse, R. A critical role for endocytosis in Wnt signaling. BMC Cell Biol. 7, 28 (2006).
22. Platta, H. W. & Stenmark, H. Endocytosis and signaling. Curr. Opin. Cell. Biol. 23, 393-403 (2011).
23. Kleijmeer, M. et al. Reorganization of multivesicular bodies regulates MHC class II antigen presentation by dendritic cells. J. Cell Biol. 155, 53-63 (2001). (Pubitemid 34286207)
24. Cohen, P. & Frame, S. The renaissance of GSK3. Nature Rev. Mol. Cell Biol. 2, 769-776 (2001). (Pubitemid 33679839)
25. Logan, C. Y. & Nusse, R. The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20, 781-810 (2004). (Pubitemid 39488658)
26. Clevers, H. Wnt/β-catenin signaling in development and disease. Cell 127, 469-480 (2006).
27. Yamamoto, H., Komekado, H. & Kikuchi, A. Caveolin is necessary for Wnt-3a-dependent internalization of LRP6 and accumulation of β-catenin. Dev. Cell 11, 213-223 (2006). (Pubitemid 44138502)
28. Wegener, C. S. et al. Ultrastructural characterization of giant endosomes induced by GTPase-deficient Rab5. Histochem. Cell Biol. 133, 41-55 (2010).
29. Jékely, G. & Rørth, P. Hrs mediates downregulation of multiple signalling receptors in Drosophila. EMBO Rep. 4, 1163-1168 (2003). (Pubitemid 38088411)
30. Stern, K. A. et al. Epidermal growth factor receptor fate is controlled by Hrs tyrosine phosphorylation sites that regulate Hrs degradation. Mol. Cell. Biol. 27, 888-898 (2007). (Pubitemid 46174554)
31. Malerød, L., Stuffers, S., Brech, A. & Stenmark, H. Vps22/EAP30 in ESCRT-II mediates endosomal sorting of growth factor and chemokine receptors destined for lysosomal degradation. Traffic 8, 1617-1629 (2007). (Pubitemid 47578365)
32. Bache, K. G. et al. The ESCRT-III subunit hVps24 is required for degradation but not silencing of the epidermal growth factor receptor. Mol. Biol. Cell 17, 2513-2523 (2006). (Pubitemid 43825490)
33. Chanut-Delalande, H. et al. The Hrs/Stam complex acts as a positive and negative regulator of RTK signaling during Drosophila development. PLoS ONE 5, e10245 (2010).
34. Toyoshima, M. et al. Inhibition of tumor growth and metastasis by depletion of vesicular sorting protein Hrs: its regulatory role on E-cadherin and β-catenin. Cancer Res. 67, 5162-5171 (2007). (Pubitemid 46997253)
35. Falguières, T., Luyet, P. P. & Gruenberg, J. Molecular assemblies and membrane domains in multivesicular endosome dynamics. J. Exp. Cell Res. 315, 1567-1573 (2009).
36. Von Bartheld, C. S. & Altick, A. L. Multivesicular bodies in neurons: distribution, protein content, and trafficking functions. Prog. Neurobiol. 93, 313-340 (2011).
37. Fuentealba, L. C. et al. Integrating patterning signals: Wnt/GSK3 regulates the duration of the BMP/Smad1 signal. Cell 131, 980-993 (2007). (Pubitemid 350138081)
38. Eivers, E., Demagny, H., Choi, R. H. & De Robertis, E. M. A molecular competition between wingless and BMP signaling controlled by mad phosphorylations. Sci. Signal. 4, ra68 (2011).
39. Wu, D. & Pan, W. GSK3: a multifaceted kinase in Wnt signaling. Trends Biochem. Sci. 35, 161-168 (2010).
40. Jope, R. S. & Johnson, G. V. The glamour and gloom of glycogen synthase kinase-3. Trends Biochem. Sci. 29, 95-102 (2004). (Pubitemid 38186580)
41. Kim, N. G., Xu, C. & Gumbiner, B. M. Identification of targets of the Wnt pathway destruction complex in addition to β-catenin. Proc. Natl Acad. Sci. USA 106, 5165-5170 (2009).
42. Huang, H. R., Chen, Z. J., Kunes, S., Chang, G. D. & Maniatis, T. Endocytic pathway is required for Drosophila Toll innate immune signaling. Proc. Natl Acad. Sci. USA 107, 8322-8327 (2010).
43. Luttrell, L. M. et al. β-arrestin-dependent formation of β2 adrenergic receptor-Src protein kinase complexes. Science 283, 655-661 (1999).
44. Ahn, S., Maudsley, S., Luttrell, L. M., Lefkowitz, R. J. & Daaka, Y. Src-mediated tyrosine phosphorylation of dynamin is required for β2-adrenergic receptor internalization and mitogen-activated protein kinase signaling. J. Biol. Chem. 274, 1185-1188 (1999).
45. Hanyaloglu, A. C., McCullagh, E. & von Zastrow, M. Essential role of Hrs in a recycling mechanism mediating functional resensitization of cell signaling. EMBO J. 24, 2265-2283 (2005). (Pubitemid 41032580)
46. Devergne, O., Ghiglione, C. & Noselli, S. The endocytic control of JAK/STAT signalling in Drosophila. J. Cell Sci. 120, 3457-3464 (2007). (Pubitemid 350028353)
47. Vidal, O. M., Stec, W., Bausek, N., Smythe, E. & Zeidler, M. P. Negative regulation of Drosophila JAK-STAT signalling by endocytic trafficking. J. Cell Sci. 123, 3457-3466 (2010).
48. Coumailleau, F., Fürthauer, M., Knoblich, J. A. & González-Gaitán, M. Directional Delta and Notch trafficking in Sara endosomes during asymmetric cell division. Nature 458, 1051-1055 (2009).
49. Wilkin, M. et al. Drosophila HOPS and AP-3 complex genes are required for a Deltex-regulated activation of notch in the endosomal trafficking pathway. Dev. Cell 15, 762-772 (2008).
50. Fürthauer, M. & González-Gaitán, M. Endocytic regulation of notch signalling during development. Traffic 10, 792-802 (2009).
51. Rowning, B. A. et al. Microtubule-mediated transport of organelles and localization of β-catenin to the future dorsal side of Xenopus eggs. Proc. Natl Acad. Sci. USA 94, 1224-1229 (1997).
52. Weaver, C. & Kimelman, D. Move it or lose it: axis specification in Xenopus. Development 131, 3491-3499 (2004). (Pubitemid 39199362)
53. Nieuwkoop, P. D. Origin and establishment of embryonic polar axes in amphibian development. Curr. Top. Dev. Biol. 11, 115-132 (1977).
54. Black, S. D. & Gerhart, J. C. High-frequency twinning of Xenopus laevis embryos from eggs centrifuged before first cleavage. Dev. Biol. 11 6, 228-240 (1986). (Pubitemid 16041543)
55. McMahon, A. P. & Moon, R. T. Ectopic expression of the proto-oncogene int-1 in Xenopus embryos leads to duplication of the embryonic axis. Cell 58, 1075-1084 (1989). (Pubitemid 19238185)
56. De Robertis, E. M. Spemann's organizer and self-regulation in amphibian embryos. Nature Rev. Mol. Cell Biol. 7, 296-302 (2006).
57. Leyns, L., Bouwmeester, T., Kim, S. H., Piccolo, S. & De Robertis, E. M. Frzb-1 is a secreted antagonist of Wnt signaling expressed in the Spemann organizer. Cell 88, 747-756 (1997). (Pubitemid 27164263)
58. Opresko, L., Wiley, H. S. & Wallace, R. A. Differential postendocytotic compartmentation in Xenopus oocytes is mediated by a specifically bound ligand. Cell 22, 47-57 (1980). (Pubitemid 11226427)
59. Balinsky, B. I. Changes in the ultrastructure of amphibian eggs following fertilization. Acta Embryol. Morphol. Exp. 9, 132-154 (1966).
60. Miller, J. R. et al. Establishment of the dorsal-ventral axis in Xenopus embryos coincides with the dorsal enrichment of Dishevelled that is dependent on cortical rotation. J. Cell Biol. 146, 427-437 (1999). (Pubitemid 29369778)
61. Tao, Q. et al. Maternal Wnt11 activates the canonical Wnt signaling pathway required for axis formation in Xenopus embryos. Cell 120, 857-871 (2005). (Pubitemid 40575651)
62. Sotelo, J. R. & Porter, K. R. An electron microscope study of the rat ovum. J. Biophys. Biochem. Cytol. 5, 327-342 (1959).
63. Young, T. W. et al. Up-regulation of tumor susceptibility gene 101 conveys poor prognosis through suppression of p21 expression in ovarian cancer. Clin. Cancer Res. 13, 3848-3854 (2007). (Pubitemid 47037590)
64. Oh, K. B., Stanton, M. J., West, W. W., Todd, G. L. & Wagner, K. U. Tsg101 is upregulated in a subset of invasive human breast cancers and its targeted overexpression in transgenic mice reveals weak oncogenic properties for mammary cancer initiation. Oncogene 26, 5950-5959 (2007).
65. Liu, R. T. et al. Overexpression of tumor susceptibility gene TSG101 in human papillary thyroid carcinomas. Oncogene 21, 4830-4837 (2002).
66. Vaccari, T. & Bilder, D. The Drosophila tumor suppressor vps25 prevents nonautonomous overproliferation by regulating notch trafficking. Dev. Cell 9, 687-698 (2005). (Pubitemid 41555150)
67. Thompson, B. J. et al. Tumor suppressor properties of the ESCRT-II complex component Vps25 in Drosophila. Dev. Cell 9, 711-720 (2005). (Pubitemid 41555152)
68. Li, J., Belogortseva, N., Porter, D. & Park, M. Chmp1A functions as a novel tumor suppressor gene in human embryonic kidney and ductal pancreatic tumor cells. Cell Cycle 7, 2886-2893 (2008).
69. Wilson, E. M., Oh, Y., Hwa, V. & Rosenfeld, R. G. Interaction of IGF-binding protein-related protein 1 with a novel protein, neuroendocrine differentiation factor, results in neuroendocrine differentiation of prostate cancer cells. J. Clin. Endocrinol. Metab. 86, 4504-4511 (2001). (Pubitemid 32848581)
70. Babst, M. A protein's final ESCRT. Traffic 6, 2-9 (2005).
71. Babst, M., Wendland, B., Estepa, E. J. & Emr, S. D. The Vps4p AAA ATPase regulates membrane association of a Vps protein complex required for normal endosome function. EMBO J. 17, 2982-2993 (1998). (Pubitemid 28254371)
72. Fernandez-Borja. et al. Multivesicular body morphogenesis requires phosphatidyl-inositol 3-kinase activity. Curr. Biol. 9, 55-58 (1999). (Pubitemid 29045796)
73. Stoorvogel, W., Strous, G. J., Geuze, H. J., Oorschot, V. & Schwartz, A. L. Late endosomes derive from early endosomes by maturation. Cell 65, 417-427 (1991). (Pubitemid 121002051)
74. Ohashi, M., Miwako, I., Yamamoto, A. & Nagayama, K. Arrested maturing multivesicular endosomes observed in a Chinese hamster ovary cell mutant, LEX2, isolated by repeated flow-cytometric cell sorting. J. Cell Sci. 113, 2187-2205 (2000). (Pubitemid 30426834)
75. Maxfield, F. R. & McGraw, T. E. Endocytic recycling. Nature Rev. Mol. Cell Biol. 5, 121-132 (2004). (Pubitemid 38160255)
76. Woodman, P. G. & Futter, C. E. Multivesicular bodies: co-ordinated progression to maturity. Curr. Opin. Cell Biol. 20, 408-414 (2008).
77. Raiborg, C., Rusten, T. E. & Stenmark, H. Protein sorting into multivesicular endosomes. Curr. Opin. Cell Biol. 15, 446-455 (2003). (Pubitemid 36928047)
78. Gruenberg, J. & Stenmark, H. The biogenesis of multivesicular endosomes. Nature Rev. Mol. Cell Biol. 5, 317-323 (2004). (Pubitemid 38480612)
79. Harding, C., Heuser, J. & Stahl, P. Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes. J. Cell Biol. 97, 329-339 (1983).
80. Denzer, K., Kleijmeer, M. J., Heijnen, H. F., Stoorvogel, W. & Geuze, H. J. Exosome: from internal vesicle of the multivesicular body to intercellular signaling device. J. Cell Sci. 11 3, 3365-3374 (2000).
81. Février, B. & Raposo, G. Exosomes: endosomal-derived vesicles shipping extracellular messages. Curr. Opin. Cell Biol. 16, 415-421 (2004). (Pubitemid 38903148)
82. Murk, J. L., Stoorvogel, W., Kleijmeer, M. J. & Geuze, H. J. The plasticity of multivesicular bodies and the regulation of antigen presentation. Semin. Cell Dev. Biol. 13, 303-311 (2002). (Pubitemid 35304516)
83. Sahu, R. et al. Microautophagy of cytosolic proteins by late endosomes. Dev. Cell 20, 131-139 (2011).
84. +-ATPase-mediated acidification for Wnt signaling. Science 327, 459-463 (2010).
85. MacDonald, B. T., Tamai, K. & He, X. Wnt/β-catenin signaling: components, mechanisms, and diseases. Dev. Cell 17, 9-26 (2009).