Ultrastructural Morphometry Points to a New Role for LAMTOR2 in Regulating the Endo/Lysosomal System

Traffic

Volumn 16, Issue 6, 2015, Pages 617-634

  Vogel, Georg F ^a   Ebner, Hannes L ^a   de Araujo, Mariana E G ^a   Schmiedinger, Thomas ^a   Eiter, Oliver ^a   Pircher, Haymo ^b   Gutleben, Karin ^a   Witting, Barbara ^a   Teis, David ^a   Huber, Lukas A ^a   Hess, Michael W ^a  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^b UNIVERSITY OF INNSBRUCK   (Austria)

Author keywords

Electron tomography; Endosome; High pressure freezing; Immuno gold; LAMTOR; MAPK; mTOR; MVB; P14; Ragulator

Indexed keywords

ADAPTOR PROTEIN; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; LATE ENDOSOMAL ADAPTOR PROTEIN 2; TRANSFERRIN RECEPTOR; UNCLASSIFIED DRUG; LAMTOR2 PROTEIN, MOUSE; PROTEIN;

ANIMAL CELL; ARTICLE; CELL MIGRATION; CELL ORGANELLE; CELL ULTRASTRUCTURE; CONTROLLED STUDY; ENDOSOME; FIBROBLAST; HOMEOSTASIS; LYSOSOME; MOUSE; MULTIVESICULAR BODY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN STRUCTURE; ANIMAL; CELL LINE; GENETICS; METABOLISM; PROTEIN TRANSPORT; ULTRASTRUCTURE;

ANIMALS; CELL LINE; ENDOSOMES; FIBROBLASTS; LYSOSOMES; MICE; MULTIVESICULAR BODIES; PROTEIN TRANSPORT; PROTEINS;

EID: 84929285803     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/tra.12271     Document Type: Article

References (96)

1. Dunn WA, Hubbard AL. Receptor-mediated endocytosis of epidermal growth factor by hepatocytes in the perfused rat liver: ligand and receptor dynamics. J Cell Biol 1984;98:2148-2159.
2. Mellman I. Endocytosis and molecular sorting. Annu Rev Cell Dev Biol 1996;12:575-625.
3. Gruenberg J, Griffiths G, Howell KE. Characterization of the early endosome and putative endocytic carrier vesicles in vivo and with an assay of vesicle fusion in vitro. J Cell Biol 1989;108:1301-1316.
4. Maxfield FR, McGraw TE. Endocytic recycling. Nat Rev Mol Cell Biol 2004;5:121-132.
5. Huotari J, Helenius A. Endosome maturation. EMBO J 2011;30:3481-3500.
6. Grimes ML, Zhou J, Beattie EC, Yuen EC, Hall DE, Valletta JS, Topp KS, LaVail JH, Bunnett NW, Mobley WC. Endocytosis of activated TrkA: evidence that nerve growth factor induces formation of signaling endosomes. J Neurosci 1996;16:7950-7964.
7. Howe CL, Mobley WC. Signaling endosome hypothesis: a cellular mechanism for long distance communication. J Neurobiol 2004;58:207-216.
8. Settembre C, Zoncu R, Medina DL, Vetrini F, Erdin S, Erdin S, Huynh T, Ferron M, Karsenty G, Vellard MC, Facchinetti V, Sabatini DM, Ballabio A. A lysosome-to-nucleus signalling mechanism senses and regulates the lysosome via mTOR and TFEB. EMBO J 2012;31:1095-1108.
9. McPherson PS, Kay BK, Hussain NK. Signaling on the endocytic pathway. Traffic (Copenhagen, Denmark) 2001;2:375-384.
10. Sorkin A, Von Zastrow M. Signal transduction and endocytosis: close encounters of many kinds. Nat Rev Mol Cell Biol 2002;3:600-614.
11. Seto ES, Bellen HJ, Lloyd TE. When cell biology meets development: endocytic regulation of signaling pathways. Genes Dev 2002;16:1314-1336.
12. Settembre C, Fraldi A, Medina DL, Ballabio A. Signals from the lysosome: a control centre for cellular clearance and energy metabolism. Nat Rev Mol Cell Biol 2013;14:283-296.
13. Pawson T, Scott JD. Signaling through scaffold, anchoring, and adaptor proteins. Science 1997;278:2075-2080.
14. Teis D, Huber LA. The odd couple: signal transduction and endocytosis. Cell Mol Life Sci 2003;60:2020-2033.
15. Schaeffer HJ, Catling AD, Eblen ST, Collier LS, Krauss A, Weber MJ. MP1: a MEK binding partner that enhances enzymatic activation of the MAP kinase cascade. Science 1998;281:1668-1671.
16. Wunderlich W, Fialka I, Teis D, Alpi A, Pfeifer A, Parton RG, Lottspeich F, Huber LA. A novel 14-kilodalton protein interacts with the mitogen-activated protein kinase scaffold mp1 on a late endosomal/lysosomal compartment. J Cell Biol 2001;152:765-776.
17. Teis D, Wunderlich W, Huber LA. Localization of the MP1-MAPK scaffold complex to endosomes is mediated by p14 and required for signal transduction. Dev Cell 2002;3:803-814.
18. Teis D, Taub N, Kurzbauer R, Hilber D, de Araujo ME, Erlacher M, Offterdinger M, Villunger A, Geley S, Bohn G, Klein C, Hess MW, Huber LA. p14-MP1-MEK1 signaling regulates endosomal traffic and cellular proliferation during tissue homeostasis. J Cell Biol 2006;175:861-868.
19. Nada S, Hondo A, Kasai A, Koike M, Saito K, Uchiyama Y, Okada M. The novel lipid raft adaptor p18 controls endosome dynamics by anchoring the MEK-ERK pathway to late endosomes. EMBO J 2009;28:477-489.
20. Bar-Peled L, Schweitzer LD, Zoncu R, Sabatini DM. Ragulator is a GEF for the rag GTPases that signal amino acid levels to mTORC1. Cell 2012;150:1196-1208.
21. Rebsamen M, Pochini L, Stasyk T, de Araujo ME, Galluccio M, Kandasamy RK, Snijder B, Fauster A, Rudashevskaya EL, Bruckner M, Scorzoni S, Filipek PA, Huber KV, Bigenzahn JW, Heinz LX, et al. SLC38A9 is a component of the lysosomal amino acid sensing machinery that controls mTORC1. Nature 2015; doi:10.1038/nature14107.
22. Sancak Y, Bar-Peled L, Zoncu R, Markhard AL, Nada S, Sabatini DM. Ragulator-Rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids. Cell 2010;141:290-303.
23. Zoncu R, Bar-Peled L, Efeyan A, Wang S, Sancak Y, Sabatini DM. mTORC1 senses lysosomal amino acids through an inside-out mechanism that requires the vacuolar H(+)-ATPase. Science 2011;334:678-683.
24. de Araujo ME, Stasyk T, Taub N, Ebner HL, Furst B, Filipek P, Weys SR, Hess MW, Lindner H, Kremser L, Huber LA. Stability of the endosomal scaffold protein LAMTOR3 depends on heterodimer assembly and proteasomal degradation. J Biol Chem 2013;288:18228-18242.
25. Sparber F, Scheffler JM, Amberg N, Tripp CH, Heib V, Hermann M, Zahner SP, Clausen BE, Reizis B, Huber LA, Stoitzner P, Romani N. The late endosomal adaptor molecule p14 (LAMTOR2) represents a novel regulator of Langerhans cell homeostasis. Blood 2014;123:217-227.
26. Pullikuth A, McKinnon E, Schaeffer HJ, Catling AD. The MEK1 scaffolding protein MP1 regulates cell spreading by integrating PAK1 and Rho signals. Mol Cell Biol 2005;25:5119-5133.
27. Park YE, Hayashi YK, Bonne G, Arimura T, Noguchi S, Nonaka I, Nishino I. Autophagic degradation of nuclear components in mammalian cells. Autophagy 2009;5:795-804.
28. Schiefermeier N, Scheffler JM, de Araujo ME, Stasyk T, Yordanov T, Ebner HL, Offterdinger M, Munck S, Hess MW, Wickstrom SA, Lange A, Wunderlich W, Fassler R, Teis D, Huber LA. The late endosomal p14-MP1 (LAMTOR2/3) complex regulates focal adhesion dynamics during cell migration. J Cell Biol 2014;205:525-540.
29. Sancak Y, Peterson TR, Shaul YD, Lindquist RA, Thoreen CC, Bar-Peled L, Sabatini DM. The Rag GTPases bind raptor and mediate amino acid signaling to mTORC1. Science 2008;320:1496-1501.
30. Lamming DW, Ye L, Katajisto P, Goncalves MD, Saitoh M, Stevens DM, Davis JG, Salmon AB, Richardson A, Ahima RS, Guertin DA, Sabatini DM, Baur JA. Rapamycin-induced insulin resistance is mediated by mTORC2 loss and uncoupled from longevity. Science 2012;335:1638-1643.
31. Bar-Peled L, Sabatini DM. Regulation of mTORC1 by amino acids. Trends Cell Biol 2014;24:400-406.
32. Taub N, Nairz M, Hilber D, Hess MW, Weiss G, Huber LA. The late endosomal adaptor p14 is a macrophage host-defense factor against Salmonella infection. J Cell Sci 2012;125(Pt 11):2698-2708.
33. Bohn G, Allroth A, Brandes G, Thiel J, Glocker E, Schaffer AA, Rathinam C, Taub N, Teis D, Zeidler C, Dewey RA, Geffers R, Buer J, Huber LA, Welte K, et al. A novel human primary immunodeficiency syndrome caused by deficiency of the endosomal adaptor protein p14. Nat Med 2007;13:38-45.
34. Eppenberger-Eberhardt M, Riesinger I, Messerli M, Schwarb P, Muller M, Eppenberger HM, Wallimann T. Adult rat cardiomyocytes cultured in creatine-deficient medium display large mitochondria with paracrystalline inclusions, enriched for creatine kinase. J Cell Biol 1991;113:289-302.
35. Schmiedinger T, Vogel GF, Eiter O, Pfaller K, Kaufmann WA, Florl A, Gutleben K, Schonherr S, Witting B, Lechleitner TW, Ebner HL, Seppi T, Hess MW. Cryo-immunoelectron microscopy of adherent cells improved by the use of electrospun cell culture substrates. Traffic (Copenhagen, Denmark) 2013;14:886-894.
36. Moor H, Riehle U. Snap-freezing under high pressure: a new fixation technique for freeze etching. In: Bocciarelli DA, editor. Electron Microscopy 1968 Pre-Congress Abstracts of Papers Presented at the Fourth European Regional Conference, Rome, September 1-7. Tipografia Poliglotta Vaticana; 1968, pp. 33-34.
37. Humbel B, Müller M. Freeze substitution and low temperature embedding. In: Müller M, Becker RP, Wolosewick JJ, editors. The Science of Biological Specimen Preparation 1985. Chicago, IL: SEM Inc. AMF O'Hare; 1986, pp. 175-183.
38. Stasyk T, Holzmann J, Stumberger S, Ebner HL, Hess MW, Bonn GK, Mechtler K, Huber LA. Proteomic analysis of endosomes from genetically modified p14/MP1 mouse embryonic fibroblasts. Proteomics 2010;10:4117-4127.
39. Futter CE, Pearse A, Hewlett LJ, Hopkins CR. Multivesicular endosomes containing internalized EGF-EGF receptor complexes mature and then fuse directly with lysosomes. J Cell Biol 1996;132:1011-1023.
40. Kleijmeer MJ, Morkowski S, Griffith JM, Rudensky AY, Geuze HJ. Major histocompatibility complex class II compartments in human and mouse B lymphoblasts represent conventional endocytic compartments. J Cell Biol 1997;139:639-649.
41. Mobius W, van Donselaar E, Ohno-Iwashita Y, Shimada Y, Heijnen HF, Slot JW, Geuze HJ. Recycling compartments and the internal vesicles of multivesicular bodies harbor most of the cholesterol found in the endocytic pathway. Traffic (Copenhagen, Denmark) 2003;4:222-231.
42. Klumperman J, Raposo G. The Complex Ultrastructure of the Endolysosomal System. Cold Spring Harb Perspect Biol 2014;6:a016857.
43. Holtzman E, Dominitz R. Cytochemical studies of lysosomes, golgi apparatus and endoplasmic reticulum in secretion and protein uptake by adrenal medulla cells of the rat. J Histochem Cytochem 1968;16:320-336.
44. Sachse M, Urbe S, Oorschot V, Strous GJ, Klumperman J. Bilayered clathrin coats on endosomal vacuoles are involved in protein sorting toward lysosomes. Mol Biol Cell 2002;13:1313-1328.
45. Berg TO, Fengsrud M, Stromhaug PE, Berg T, Seglen PO. Isolation and characterization of rat liver amphisomes. Evidence for fusion of autophagosomes with both early and late endosomes. J Biol Chem 1998;273:21883-21892.
46. Eskelinen EL, Illert AL, Tanaka Y, Schwarzmann G, Blanz J, Von Figura K, Saftig P. Role of LAMP-2 in lysosome biogenesis and autophagy. Mol Biol Cell 2002;13:3355-3368.
47. Saftig P, Klumperman J. Lysosome biogenesis and lysosomal membrane proteins: trafficking meets function. Nat Rev Mol Cell Biol 2009;10:623-635.
48. Liou W, Geuze HJ, Geelen MJ, Slot JW. The autophagic and endocytic pathways converge at the nascent autophagic vacuoles. J Cell Biol 1997;136:61-70.
49. Tokuyasu KT. A technique for ultracryotomy of cell suspensions and tissues. J Cell Biol 1973;57:551-565.
50. van Donselaar E, Posthuma G, Zeuschner D, Humbel BM, Slot JW. Immunogold labeling of cryosections from high-pressure frozen cells. Traffic (Copenhagen, Denmark) 2007;8:471-485.
51. Ripper D, Schwarz H, Stierhof YD. Cryo-section immunolabelling of difficult to preserve specimens: advantages of cryofixation, freeze-substitution and rehydration. Biol Cell 2008;100:109-123.
52. Ludwig T, Griffiths G, Hoflack B. Distribution of newly synthesized lysosomal enzymes in the endocytic pathway of normal rat kidney cells. J Cell Biol 1991;115:1561-1572.
53. Kobayashi T, Stang E, Fang KS, de Moerloose P, Parton RG, Gruenberg J. A lipid associated with the antiphospholipid syndrome regulates endosome structure and function. Nature 1998;392:193-197.
54. Myromslien FD, Grovdal LM, Raiborg C, Stenmark H, Madshus IH, Stang E. Both clathrin-positive and -negative coats are involved in endosomal sorting of the EGF receptor. Exp Cell Res 2006;312:3036-3048.
55. Komada M, Masaki R, Yamamoto A, Kitamura N. Hrs, a tyrosine kinase substrate with a conserved double zinc finger domain, is localized to the cytoplasmic surface of early endosomes. J Biol Chem 1997;272:20538-20544.
56. Ackerson CJ, Powell RD, Hainfeld JF. Site-specific biomolecule labeling with gold clusters. Methods Enzymol 2010;481:195-230.
57. He W, Ladinsky MS, Huey-Tubman KE, Jensen GJ, McIntosh JR, Bjorkman PJ. FcRn-mediated antibody transport across epithelial cells revealed by electron tomography. Nature 2008;455:542-546.
58. Driskell OJ, Mironov A, Allan VJ, Woodman PG. Dynein is required for receptor sorting and the morphogenesis of early endosomes. Nat Cell Biol 2007;9:113-120.
59. Peden AA, Oorschot V, Hesser BA, Austin CD, Scheller RH, Klumperman J. Localization of the AP-3 adaptor complex defines a novel endosomal exit site for lysosomal membrane proteins. J Cell Biol 2004;164:1065-1076.
60. van Weering JR, Verkade P, Cullen PJ. SNX-BAR-mediated endosome tubulation is co-ordinated with endosome maturation. Traffic (Copenhagen, Denmark) 2012;13:94-107.
61. Murk JL, Posthuma G, Koster AJ, Geuze HJ, Verkleij AJ, Kleijmeer MJ, Humbel BM. Influence of aldehyde fixation on the morphology of endosomes and lysosomes: quantitative analysis and electron tomography. J Microsc 2003;212(Pt 1):81-90.
62. Perret E, Lakkaraju A, Deborde S, Schreiner R, Rodriguez-Boulan E. Evolving endosomes: how many varieties and why? Curr Opin Cell Biol 2005;17:423-434.
63. van Deurs B, Holm PK, Kayser L, Sandvig K, Hansen SH. Multivesicular bodies in HEp-2 cells are maturing endosomes. Eur J Cell Biol 1993;61:208-224.
64. Gruenberg J, Stenmark H. The biogenesis of multivesicular endosomes. Nat Rev Mol Cell Biol 2004;5:317-323.
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. Lakadamyali M, Rust MJ, Zhuang X. Ligands for clathrin-mediated endocytosis are differentially sorted into distinct populations of early endosomes. Cell 2006;124:997-1009.
67. Woodman PG, Futter CE. Multivesicular bodies: co-ordinated progression to maturity. Curr Opin Cell Biol 2008;20:408-414.
68. Scott CC, Vacca F, Gruenberg J. Endosome maturation, transport and functions. Semin Cell Dev Biol 2014;31:2-10.
69. Malek M, Guillaumot P, Huber AL, Lebeau J, Petrilli V, Kfoury A, Mikaelian I, Renno T, Manie SN. LAMTOR1 depletion induces p53-dependent apoptosis via aberrant lysosomal activation. Cell Death Dis 2012;3:e300.
70. Takahashi Y, Nada S, Mori S, Soma-Nagae T, Oneyama C, Okada M. The late endosome/lysosome-anchored p18-mTORC1 pathway controls terminal maturation of lysosomes. Biochem Biophys Res Commun 2012;417:1151-1157.
71. Soma-Nagae T, Nada S, Kitagawa M, Takahashi Y, Mori S, Oneyama C, Okada M. The lysosomal signaling anchor p18/LAMTOR1 controls epidermal development by regulating lysosome-mediated catabolic processes. J Cell Sci 2013;126(Pt 16):3575-3584.
72. Nada S, Mori S, Takahashi Y, Okada M. p18/LAMTOR1: a late endosome/lysosome-specific anchor protein for the mTORC1/MAPK signaling pathway. Methods Enzymol 2014;535:249-263.
73. Settembre C, Di Malta C, Polito VA, Garcia Arencibia M, Vetrini F, Erdin S, Erdin SU, Huynh T, Medina D, Colella P, Sardiello M, Rubinsztein DC, Ballabio A. TFEB links autophagy to lysosomal biogenesis. Science 2011;332:1429-1433.
74. de Wit H, Lichtenstein Y, Kelly RB, Geuze HJ, Klumperman J, van der Sluijs P. Rab4 regulates formation of synaptic-like microvesicles from early endosomes in PC12 cells. Mol Biol Cell 2001;12:3703-3715.
75. Mari M, Bujny MV, Zeuschner D, Geerts WJ, Griffith J, Petersen CM, Cullen PJ, Klumperman J, Geuze HJ. SNX1 defines an early endosomal recycling exit for sortilin and mannose 6-phosphate receptors. Traffic (Copenhagen, Denmark) 2008;9:380-393.
76. Pols MS, van Meel E, Oorschot V, ten Brink C, Fukuda M, Swetha MG, Mayor S, Klumperman J. hVps41 and VAMP7 function in direct TGN to late endosome transport of lysosomal membrane proteins. Nat Commun 2013;4:1361.
77. Seaman MN. The retromer complex - endosomal protein recycling and beyond. J Cell Sci 2012;125(Pt 20):4693-4702.
78. Heiligenstein X, Heiligenstein J, Delevoye C, Hurbain I, Bardin S, Paul-Gilloteaux P, Sengmanivong L, Regnier G, Salamero J, Antony C, Raposo G. The CryoCapsule: simplifying correlative light to electron microscopy. Traffic (Copenhagen, Denmark) 2014;15:700-716.
79. Chichger H, Duong H, Braza J, Harrington EO. p18, a novel adaptor protein, regulates pulmonary endothelial barrier function via enhanced endocytic recycling of VE-cadherin. FASEB J 2014; Nov 17. pii: fj.14-257212.
80. Kurzbauer R, Teis D, de Araujo ME, Maurer-Stroh S, Eisenhaber F, Bourenkov GP, Bartunik HD, Hekman M, Rapp UR, Huber LA, Clausen T. Crystal structure of the p14/MP1 scaffolding complex: how a twin couple attaches mitogen-activated protein kinase signaling to late endosomes. Proc Natl Acad Sci USA 2004;101:10984-10989.
81. Obexer P, Geiger K, Ambros PF, Meister B, Ausserlechner MJ. FKHRL1-mediated expression of Noxa and Bim induces apoptosis via the mitochondria in neuroblastoma cells. Cell Death Differ 2007;14:534-547.
82. Hess MW, Muller M, Debbage PL, Vetterlein M, Pavelka M. Cryopreparation provides new insight into the effects of brefeldin A on the structure of the HepG2 Golgi apparatus. J Struct Biol 2000;130:63-72.
83. Hess MW, Pfaller K, Ebner HL, Beer B, Hekl D, Seppi T. 3D versus 2D cell culture implications for electron microscopy. Methods Cell Biol 2010;96:649-670.
84. Studer D, Michel M, Muller M. High pressure freezing comes of age. Scanning Microsc Suppl 1989;3:253-268; discussion 268-269.
85. Walther P, Ziegler A. Freeze substitution of high-pressure frozen samples: the visibility of biological membranes is improved when the substitution medium contains water. J Microsc 2002;208(Pt 1):3-10.
86. Robinson JM, Karnovsky MJ. Rapid-freezing cytochemistry: preservation of tubular lysosomes and enzyme activity. J Histochem Cytochem 1991;39:787-792.
87. Kirkham M, Fujita A, Chadda R, Nixon SJ, Kurzchalia TV, Sharma DK, Pagano RE, Hancock JF, Mayor S, Parton RG. Ultrastructural identification of uncoated caveolin-independent early endocytic vehicles. J Cell Biol 2005;168:465-476.
88. Ellinger A, Vetterlein M, Weiss C, Meisslitzer-Ruppitsch C, Neumuller J, Pavelka M. High-pressure freezing combined with in vivo-DAB-cytochemistry: a novel approach for studies of endocytic compartments. J Struct Biol 2010;169:286-293.
89. Berod A, Hartman BK, Pujol JF. Importance of fixation in immunohistochemistry: use of formaldehyde solutions at variable pH for the localization of tyrosine hydroxylase. J Histochem Cytochem 1981;29:844-850.
90. Liou W, Geuze HJ, Slot JW. Improving structural integrity of cryosections for immunogold labeling. Histochem Cell Biol 1996;106:41-58.
91. Griffiths G. Fine Structure Immunocytochemistry. Berlin: Springer; 1993.
92. Adell MA, Vogel GF, Pakdel M, Muller M, Lindner H, Hess MW, Teis D. Coordinated binding of Vps4 to ESCRT-III drives membrane neck constriction during MVB vesicle formation. J Cell Biol 2014;205:33-49.
93. He W, Fernandez JJ. Electron tomography. In: Zheng YX, editor. Encyclopedia of Life Sciences (ELS). Chichester: John Wiley & Sons; 2010. http://onlinelibrarywileycom/doi/101002/9780470015902a0021877/abstract.
94. Komada M, Kitamura N. Growth factor-induced tyrosine phosphorylation of Hrs, a novel 115-kilodalton protein with a structurally conserved putative zinc finger domain. Mol Cell Biol 1995;15:6213-6221.
95. Pohlmann R, Boeker MW, von Figura K. The two mannose 6-phosphate receptors transport distinct complements of lysosomal proteins. J Biol Chem 1995;270:27311-27318.
96. White S, Miller K, Hopkins C, Trowbridge IS. Monoclonal antibodies against defined epitopes of the human transferrin receptor cytoplasmic tail. Biochim Biophys Acta 1992;1136:28-34.