The HSP90 inhibitor geldanamycin perturbs endosomal structure and drives recycling ErbB2 and transferrin to modified MVBs/lysosomal compartments

Molecular Biology of the Cell

Volumn 24, Issue 2, 2013, Pages 129-144

  Cortese, Katia ^a,b   Howes, Mark T ^a   Lundmark, Richard ^c   Tagliatti, Erica ^b   Bagnato, Paola ^b   Petrelli, Annalisa ^d   Bono, Maria ^b   McMahon, Harvey T ^e   Parton, Robert G ^a   Tacchetti, Carlo ^b,f  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF GENOA   (Italy)

^c UMEÅ UNIVERSITY   (Sweden)

^d UNIVERSITY OF TURIN   (Italy)

^e MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^f SAN RAFFAELE HOSPITAL   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CLATHRIN; EPIDERMAL GROWTH FACTOR RECEPTOR 2; GELDANAMYCIN; HEAT SHOCK PROTEIN 90 INHIBITOR; TRANSFERRIN;

ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL COMPARTMENTALIZATION; CELL SELECTION; CELL STRUCTURE; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; HUMAN; HUMAN CELL; INTERNALIZATION; LYSOSOME; MICROSCOPY; MODIFIED MULTIVESICULAR ENDOSOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION;

ANIMALS; ANTINEOPLASTIC AGENTS; BENZOQUINONES; CELL LINE, TUMOR; CERCOPITHECUS AETHIOPS; CLATHRIN; CLATHRIN-COATED VESICLES; COS CELLS; DYNAMINS; ELECTRON MICROSCOPE TOMOGRAPHY; ENDOCYTOSIS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; LACTAMS, MACROCYCLIC; LYSOSOMES; MICE; MICROSCOPY, FLUORESCENCE; MULTIVESICULAR BODIES; PROTEIN TRANSPORT; RECEPTOR, ERBB-2; SINGLE-CELL ANALYSIS; TRANSFERRIN;

EID: 84872350755     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E12-04-0282     Document Type: Article

References (71)

1. Abella JV, Park M (2009). Breakdown of endocytosis in the oncogenic activation of receptor tyrosine kinases. Am J Physiol Endocrinol Metab 296, E973-E984.
2. Austin CD, De Maziere AM, Pisacane PI, van Dijk SM, Eigenbrot C, Sliwkowski MX, Klumperman J, Scheller RH (2004). Endocytosis and sorting of ErbB2 and the site of action of cancer therapeutics trastuzumab and geldanamycin. Mol Biol Cell 15, 5268-5282.
3. Barr DJ, Ostermeyer-Fay AG, Matundan RA, Brown DA (2008). Clathrin-independent endocytosis of ErbB2 in geldanamycin-treated human breast cancer cells. J Cell Sci 121, 3155-3166.
4. Ben-Kasus T, Schechter B, Lavi S, Yarden Y, Sela M (2009). Persistent elimination of ErbB-2/HER2-overexpressing tumors using combinations of monoclonal antibodies: relevance of receptor endocytosis. Proc Natl Acad Sci USA 106, 3294-3299.
5. Chen CY, Balch WE (2006). The Hsp90 chaperone complex regulates GDI-dependent Rab recycling. Mol Biol Cell 17, 3494-3507.
6. Chen CY, Sakisaka T, Balch WE (2005). Use of Hsp90 inhibitors to disrupt GDI-dependent Rab recycling. Methods Enzymol 403, 339-347.
7. Citri A, Alroy I, Lavi S, Rubin C, Xu W, Grammatikakis N, Patterson C, Neckers L, Fry DW, Yarden Y (2002). Drug-induced ubiquitylation and degradation of ErbB receptor tyrosine kinases: implications for cancer therapy. EMBO J 21, 2407-2417.
8. Citri A, Gan J, Mosesson Y, Vereb G, Szollosi J, Yarden Y (2004). Hsp90 restrains ErbB-2/HER2 signalling by limiting heterodimer formation. EMBO Rep 5, 1165-1170.
9. Citri A, Yarden Y (2006). EGF-ERBB signalling: towards the systems level. Nat Rev Mol Cell Biol 7, 505-516.
10. Corso S, Migliore C, Ghiso E, De Rosa G, Comoglio PM, Giordano S (2008). Silencing the MET oncogene leads to regression of experimental tumors and metastases. Oncogene 27, 684-693.
11. Doherty GJ, Ahlund MK, Howes MT, Moren B, Parton RG, McMahon HT, Lundmark R (2011). The endocytic protein GRAF1 is directed to cell-matrix adhesion sites and regulates cell spreading. Mol Biol Cell 22, 4380-4389.
12. Doherty GJ, Lundmark R (2009). GRAF1-dependent endocytosis. Biochem Soc Trans 37, 1061-1065.
13. Falguieres T, Castle D, Gruenberg J (2012). Regulation of the MVB pathway by SCAMP3. Traffic 13, 131-142.
14. Falguieres T, Luyet PP, Gruenberg J (2009). Molecular assemblies and membrane domains in multivesicular endosome dynamics. Exp Cell Res 315, 1567-1573.
15. Frick M, Bright NA, Riento K, Bray A, Merrified C, Nichols BJ (2007). Coassembly of flotillins induces formation of membrane microdomains, membrane curvature, and vesicle budding. Curr Biol 17, 1151-1156.
16. Fukuyo Y, Hunt CR, Horikoshi N (2010). Geldanamycin and its anti-cancer activities. Cancer Lett 290, 24-35.
17. Glebov OO, Bright NA, Nichols BJ (2006). Flotillin-1 defines a clathrin-independent endocytic pathway in mammalian cells. Nat Cell Biol 8, 46-54.
18. Gomez TS, Gorman JA, Artal-Martinez de Narvajas A, Koenig AO, Billadeau DD (2012). Trafficking defects in WASH knockout fibroblasts originate from collapsed endosomal and lysosomal networks. Mol Biol Cell 16, 3215-3228.
19. Gruenberg J, Stenmark H (2004). The biogenesis of multivesicular endosomes. Nat Rev Mol Cell Biol 5, 317-323.
20. Haslekas C, Breen K, Pedersen KW, Johannessen LE, Stang E, Madshus IH (2005). The inhibitory effect of ErbB2 on epidermal growth factor-induced formation of clathrin-coated pits correlates with retention of epidermal growth factor receptor-ErbB2 oligomeric complexes at the plasma membrane. Mol Biol Cell 16, 5832-5842.
21. Hommelgaard AM, Lerdrup M, van Deurs B (2004). Association with membrane protrusions makes ErbB2 an internalization-resistant receptor. Mol Biol Cell 15, 1557-1567.
22. Howes MT et al. (2010). Clathrin-independent carriers form a high capacity endocytic sorting system at the leading edge of migrating cells. J Cell Biol 190, 675-691.
23. Hynes NE, MacDonald G (2009). ErbB receptors and signaling pathways in cancer. Curr Opin Cell Biol 21, 177-184.
24. Jones KL, Buzdar AU (2009). Evolving novel anti-HER2 strategies. Lancet Oncol 10, 1179-1187.
25. Kalia M, Kumari S, Chadda R, Hill MM, Parton RG, Mayor S (2006). Arf6-independent GPI-anchored protein-enriched early endosomal compartments fuse with sorting endosomes via a Rab5/phosphatidylinositol-32-kinase-dependent machinery. Mol Biol Cell 17, 3689-3704.
26. Kirkham M, Fujita A, Chadda R, Nixon SJ, Kurzchalia TV, Sharma DK, Pagano RE, Hancock JF, Mayor S, Parton RG (2005). Ultrastructural identification of uncoated caveolin-independent early endocytic vehicles. J Cell Biol 168, 465-476.
27. Kirkham M, Parton RG (2005). Clathrin-independent endocytosis: new insights into caveolae and non-caveolar lipid raft carriers. Biochim Biophys Acta 1746, 349-363.
28. Kleijmeer MJ, Morkowski S, Griffith JM, Rudensky AY, Geuze HJ (1997). Major histocompatibility complex class II compartments in human and mouse B lymphoblasts represent conventional endocytic compartments. J Cell Biol 139, 639-649.
29. Klumperman J, Hille A, Veenendaal T, Oorschot V, Stoorvogel W, von Figura K, Geuze HJ (1993). Differences in the endosomal distributions of the two mannose 6-phosphate receptors. J Cell Biol 5, 997-1010.
30. Kremer JR, Mastronarde DN, McIntosh JR (1996). Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116, 71-76.
31. Lanzetti L, Di Fiore PP (2008). Endocytosis and cancer: an "insider" network with dangerous liaisons. Traffic 9, 2011-2021.
32. Lerdrup M, Bruun S, Grandal MV, Roepstorff K, Kristensen MM, Hommelgaard AM, van Deurs B (2007). Endocytic down-regulation of ErbB2 is stimulated by cleavage of its C-terminus. Mol Biol Cell 18, 3656-3666.
33. Lerdrup M, Hommelgaard AM, Grandal M, van Deurs B (2006). Geldanamycin stimulates internalization of ErbB2 in a proteasome-dependent way. J Cell Sci 119, 85-95.
34. Liu J, Bressan M, Hassel D, Huisken J, Staudt D, Kikuchi K, Poss KD, Mikawa T, Stainier DY (2010). A dual role for ErbB2 signaling in cardiac trabeculation. Development 137, 3867-3875.
35. Liu J, Zhang JP, Shi M, Quinn T, Bradner J, Beyer R, Chen S, Zhang J (2009). Rab11a and HSP90 regulate recycling of extracellular α-synuclein. J Neurosci 29, 1480-1485.
36. Longva KE, Pedersen NM, Haslekas C, Stang E, Madshus IH (2005). Herceptin-induced inhibition of ErbB2 signaling involves reduced phosphorylation of Akt but not endocytic down-regulation of ErbB2. Int J Cancer 116, 359-367.
37. Lundmark R, Doherty GJ, Howes MT, Cortese K, Vallis Y, Parton RG, McMahon HT (2008). The GTPase-activating protein GRAF1 regulates the CLIC/GEEC endocytic pathway. Curr Biol 18, 1802-1808.
38. Mari M, Bujny MV, Zeuschner D, Geerts WJ, Griffith J, Petersen CM, Cullen PJ, Klumperman J, Geuze HJ (2007). SNX1 defines an early endosomal recycling exit for sortilin and mannose 6-phosphate receptors. Traffic 3, 380-393.
39. Marone R, Hess D, Dankort D, Muller WJ, Hynes NE, Badache A (2004). Memo mediates ErbB2-driven cell motility. Nat Cell Biol 6, 515-522.
40. Matsui T, Itoh T, Fukuda M (2011). Small GTPase Rab12 regulates constitutive degradation of transferrin receptor. Traffic 10, 1432-1443.
41. Mayor S, Pagano RE (2007). Pathways of clathrin-independent endocytosis. Nat Rev Mol Cell Biol 8, 603-612.
42. Mettlen M, Loerke D, Yarar D, Danuser G, Schmid SL (2010). Cargo- and adaptor-specific mechanisms regulate clathrin-mediated endocytosis. J Cell Biol 188, 919-933.
43. Mosesson Y, Mills GB, Yarden Y (2008). Derailed endocytosis: an emerging feature of cancer. Nat Rev Cancer 8, 835-850.
44. Murk JL, Posthuma G, Koster AJ, Geuze HJ, Verkleij AJ, Kleijmeer MJ, Humbel BM (2003). Influence of aldehyde fixation on the morphology of endosomes and lysosomes: quantitative analysis and electron tomography. J Microsc 212, 81-90.
45. Otto GP, Nichols BJ (2011). The roles of flotillin microdomains - endocytosis and beyond. J Cell Sci 124, 3933-3940.
46. Pedersen NM, Breen K, Rodland MS, Haslekas C, Stang E, Madshus IH (2009). Expression of epidermal growth factor receptor or ErbB3 facilitates geldanamycin-induced down-regulation of ErbB2. Mol Cancer Res 7, 275-284.
47. Pedersen NM, Madshus IH, Haslekas C, Stang E (2008). Geldanamycin-induced down-regulation of ErbB2 from the plasma membrane is clathrin dependent but proteasomal activity independent. Mol Cancer Res 6, 491-500.
48. Pelkmans L, Fava E, Grabner H, Hannus M, Habermann B, Krausz E, Zerial M (2005). Genome-wide analysis of human kinases in clathrin- and caveolae/raft-mediated endocytosis. Nature 436, 78-86.
49. Puri C, Tosoni D, Comai R, Rabellino A, Segat D, Caneva F, Luzzi P, Di Fiore PP, Tacchetti C (2005). Relationships between EGFR signaling-competent and endocytosis-competent membrane microdomains. Mol Biol Cell 16, 2704-2718.
50. Puthenveedu MA, Lauffer B, Temkin P, Vistein R, Carlton P, Thorn K, Taunton J, Weiner OD, Parton RG, von Zastrow M (2010). Sequence-dependent sorting of recycling proteins by actin-stabilized endosomal microdomains. Cell 143, 761-773.
51. Raja SM et al. (2008). A combination of trastuzumab and 17-AAG induces enhanced ubiquitinylation and lysosomal pathway-dependent ErbB2 degradation and cytotoxicity in ErbB2-overexpressing breast cancer cells. Cancer Biol Ther 7, 1630-1640.
52. Rink J, Ghigo E, Kalaidzidis Y, Zerial M (2005). Rab conversion as a mechanism of progression from early to late endosomes. Cell 122, 735-749.
53. Roepstorff K, Grovdal L, Grandal M, Lerdrup M, van Deurs B (2008). Endocytic downregulation of ErbB receptors: mechanisms and relevance in cancer. Histochem Cell Biol 129, 563-578.
54. Romer W et al. (2007). Shiga toxin induces tubular membrane invaginations for its uptake into cells. Nature 450, 670-675.
55. Sabharanjak S, Sharma P, Parton RG, Mayor S (2002). GPI-anchored proteins are delivered to recycling endosomes via a distinct cdc42-regulated, clathrin-independent pinocytic pathway. Dev Cell 2, 411-423.
56. Saftig P, Klumperman J (2009). Lysosome biogenesis and lysosomal membrane proteins: trafficking meets function. Nat Rev Mol Cell Biol 10, 623-635.
57. Sandvig K, Torgersen ML, Raa HA, van Deurs B (2008). Clathrin-independent endocytosis: from nonexisting to an extreme degree of complexity. Histochem Cell Biol 129, 267-276.
58. Scita G, Di Fiore PP (2010). The endocytic matrix. Nature 463, 464-473.
59. Sorkin A, Di Fiore PP, Carpenter G (1993). The carboxyl terminus of epidermal growth factor receptor/erbB-2 chimerae is internalization impaired. Oncogene 8, 3021-3028.
60. Sorkin A, Goh LK (2008). Endocytosis and intracellular trafficking of ErbBs. Exp Cell Res 314, 3093-3106.
61. Taiyab A, Rao ChM (2011). HSP90 modulates actin dynamics: inhibition of HSP90 leads to decreased cell motility and impairs invasion. Biochim Biophys Acta 1813, 213-221.
62. Tikhomirov O, Carpenter G (2000). Geldanamycin induces ErbB-2 degradation by proteolytic fragmentation. J Biol Chem 275, 26625-26631.
63. Tikhomirov O, Carpenter G (2003). Identification of ErbB-2 kinase domain motifs required for geldanamycin-induced degradation. Cancer Res 63, 39-43.
64. Tosoni D, Puri C, Confalonieri S, Salcini AE, De Camilli P, Tacchetti C, Di Fiore PP (2005). TTP specifically regulates the internalization of the transferrin receptor. Cell 123, 875-888.
65. Wang Z, Zhang L, Yeung TK, Chen X (1999). Endocytosis deficiency of epidermal growth factor (EGF) receptor-ErbB2 heterodimers in response to EGF stimulation. Mol Biol Cell 10, 1621-1636.
66. Vaccari T, Bilder D (2009). At the crossroads of polarity, proliferation and apoptosis: the use of Drosophila to unravel the multifaceted role of endocytosis in tumor suppression. Mol Oncol 3, 354-365.
67. van Weering JRT, Verkade P, Cullen PJ (2012). SNX-BAR-mediated endosome tubulation is co-ordinated with endosome maturation. Traffic 13, 94-107.
68. Vigna E, Naldini L (2000). Lentiviral vectors: excellent tools for experimental gene transfer and promising candidates for gene therapy. J Gene Med 2, 308-316.
69. Xu W, Marcu M, Yuan X, Mimnaugh E, Patterson C, Neckers L (2002). Chaperone-dependent E3 ubiquitin ligase CHIP mediates a degradative pathway for c-ErbB2/Neu. Proc Natl Acad Sci USA 99, 12847-12852.
70. Zhou P, Fernandes N, Dodge IL, Reddi AL, Rao N, Safran H, DiPetrillo TA, Wazer DE, Band V, Band H (2003). ErbB2 degradation mediated by the co-chaperone protein CHIP. J Biol Chem 278, 13829-13837.
71. Zsebik B, Citri A, Isola J, Yarden Y, Szollosi J, Vereb G (2006). Hsp90 inhibitor 17-AAG reduces ErbB2 levels and inhibits proliferation of the trastuzumab resistant breast tumor cell line JIMT-1. Immunol Lett 104, 146-155.