Cell-type-specific pathways of neurotensin endocytosis

Cell and Tissue Research

Volumn 324, Issue 1, 2006, Pages 69-85

  Savdie, Cheryl ^a   Ferguson, Stephen S G ^b   Vincent, Jean Pierre ^c   Beaudet, Alain ^a   Stroh, Thomas ^a  

^a MCGILL UNIVERSITY   (Canada)

^b ROBARTS RESEARCH INSTITUTE   (Canada)

^c INSTITUT DE PHARMACOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

arrestin; Amphiphysin; COS 7 green monkey kidney cell; Dynamin; HEK 293 human embryonic kidney cell; Immunoelectron microscopy; Internalization; Intersectin; Neurotensin receptor subtype 1 (NTS1)

Indexed keywords

AMPHIPHYSIN; BETA ARRESTIN; CLATHRIN; COMPLEMENTARY DNA; DYNAMIN; INTERSECTIN; NEUROTENSIN 1 RECEPTOR; NEUROTENSIN RECEPTOR; PROTEIN SH3; RECEPTOR SUBTYPE; RETINA S ANTIGEN; TRANSFERRIN RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL FUNCTION; CELL LINE; CELL STRAIN COS7; CELL STRAIN HEK293; CELL TYPE; CELL VACUOLE; COATED PIT; CONTROLLED STUDY; EMBRYO; ENDOCYTOSIS; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOGOLD ELECTRON MICROSCOPY; INTERNALIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; ARRESTINS; CERCOPITHECUS AETHIOPS; COS CELLS; DYNAMINS; ENDOCYTOSIS; GREEN FLUORESCENT PROTEINS; HUMANS; MUTATION; NERVE TISSUE PROTEINS; NEUROTENSIN; ORGAN SPECIFICITY; PROTEIN TRANSPORT; RECEPTORS, NEUROTENSIN; SIGNAL TRANSDUCTION; TRANSFECTION;

ANIMALIA; CERCOPITHECUS AETHIOPS;

EID: 33644614406     PISSN: 0302766X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00441-005-0102-3     Document Type: Article

References (85)

1. Barlic J, Khandaker MH, Mahon E, Andrews J, DeVries ME, Mitchell GB, Rahimpour R, Tan CM, Ferguson SS, Kelvin DJ (1999) Beta-arrestins regulate interleukin-8-induced CXCR1 internalization. J Biol Chem 274:16287-16294
2. Bliek AM van der, Redelmeier TE, Damke H, Tisdale EJ, Meyerowitz EM, Schmid SL (1993) Mutations in human dynamin block an intermediate stage in coated vesicle formation. J Cell Biol 122:553-563
3. Botto JM, Chabry J, Sarret P, Vincent JP, Mazella J (1998) Stable expression of the mouse levocabastine-sensitive neurotensin receptor in HEK 293 cell line: binding properties, photoaffinity labeling, and internalization mechanism. Biochem Biophys Res Commun 243:585-590
4. Bremnes T, Paasche JD, Mehlum A, Sandberg C, Bremnes B, Attramadal H (2000) Regulation and intracellular trafficking pathways of the endothelin receptors. J Biol Chem 275:17596-17604
5. Carraway R, Leeman SE (1973) The isolation of a new hypotensive peptide, neurotensin, from bovine hypothalami. J Biol Chem 248:6854-6861
6. Chabry J, Labbé-Jullié C, Gully D, Kitabgi P, Vincent JP, Mazella J (1994) Stable expression of the cloned rat brain neurotensin receptor into fibroblasts: binding properties, photoaffinity labeling, transduction mechanisms, and internalization. J Neurochem 63:19-27
7. Chalon P, Vita N, Kaghad M, Guillemot M, Bonnin J, Delpech B, Le Fur G, Ferrara P, Caput D (1996) Molecular cloning of a levocabastine-sensitive neurotensin binding site. FEBS Lett 386:91-94
8. Chen H, Fre S, Slepnev VI, Capua MR, Takei K, Butler MH, Di Fiore PP, De Camilli P (1998) Epsin is an EH-domain-binding protein implicated in clathrin-mediated endocytosis. Nature 394:793-797
9. Damke H, Baba T, Warnock DE, Schmid SL (1994) Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J Cell Biol 127:915-934
10. Daro E, Sluijs P van der, Galli T, Mellman I (1996) Rab4 and cellubrevin define different early endosome populations on the pathway of transferrin receptor recycling. Proc Natl Acad Sci USA 93:9559-9564
11. David C, McPherson PS, Mundigl O, De Camilli P (1996) A role of amphiphysin in synaptic vesicle endocytosis suggested by its binding to dynamin in nerve terminals. Proc Natl Acad Sci USA 93:331-335
12. DeGraff JL, Gagnon AW, Benovic JL, Orsini MJ (1999) Role of arrestins in endocytosis and signaling of alpha2-adrenergic receptor subtypes. J Biol Chem 274:11253-11259
13. Delaney KA, Murph MM, Brown LM, Radhakrishna H (2002) Transfer of M2 muscarinic acetylcholine receptors to clathrin-derived early endosomes following clathrin-independent endocytosis. J Biol Chem 277:33439-33446
14. Faure MP, Alonso A, Nouel D, Gaudriault G, Dennis M, Vincent JP, Beaudet A (1995a) Somatodendritic internalization and perinuclear targeting of neurotensin in the mammalian brain. J Neurosci 15:4140-4147
15. Faure MP, Labbé-Jullié C, Cashman N, Kitabgi P, Beaudet A (1995b) Binding and internalization of neurotensin in hybrid cells derived from septal cholinergic neurons. Synapse 20:106-116
16. Faure MP, Nouel D, Beaudet A (1995c) Axonal and dendritic transport of internalized neurotensin in rat mesostriatal dopaminergic neurons. Neuroscience 68:519-529
17. Ferguson SS, Downey WE, 3rd, Colapietro AM, Barak LS, Menard L, Caron MG (1996) Role of beta-arrestin in mediating agonist-promoted G protein-coupled receptor internalization. Science 271:363-366
18. Ferguson SS (2001) Evolving concepts in G protein-coupled receptor endocytosis: the role in receptor desensitization and signaling. Pharmacol Rev 53:1-24
19. Gáborik Z, Szaszak M, Szidonya L, Balla B, Paku S, Catt KJ, Clark AJ, Hunyady L (2001) Beta-arrestin- and dynamin-dependent endocytosis of the AT1 angiotensin receptor. Mol Pharmacol 59:239-247
20. Gaudriault G, Vincent JP (1992) Selective labeling of alpha- or epsilon-amino groups in peptides by the Bolton-Hunter reagent. Peptides 13:1187-1192
21. Guipponi M, Scott HS, Chen H, Schebesta A, Rossier C, Antonarakis SE (1998) Two isoforms of a human intersectin (ITSN) protein are produced by brain-specific alternative splicing in a stop codon. Genomics 53:369-376
22. Hermans E, Octave JN, Maloteaux JM (1994) Receptor mediated internalization of neurotensin in transfected Chinese hamster ovary cells. Biochem Pharmacol 47:89-91
23. Hermans E, Maloteaux JM (1998) Mechanisms of regulation of neurotensin receptors. Pharmacol Ther 79:89-104
24. Herskovits JS, Burgess CC, Obar RA, Vallee RB (1993) Effects of mutant rat dynamin on endocytosis. J Cell Biol 122:565-578
25. Hunyady L (1999) Molecular mechanisms of angiotensin II receptor internalization. J Am Soc Nephrol 10 Suppl 11:S47-S56
26. Hussain NK, Yamabhai M, Ramjaun AR, Guy AM, Baranes D, O'Bryan JP, Der CJ, Kay BK, McPherson PS (1999) Splice variants of intersectin are components of the endocytic machinery in neurons and nonneuronal cells. J Biol Chem 274:15671-15677
27. Jin Y, Kim KY, Soung NK, Shin EY, Kim EG, Kim SR (2001) Production and characterization of monoclonal antibodies against amphiphysins. Exp Mol Med 33:69-75
28. Kim KM, Valenzano KJ, Robinson SR, Yao WD, Barak LS, Caron MG (2001) Differential regulation of the dopamine D2 and D3 receptors by G protein-coupled receptor kinases and beta-arrestins. J Biol Chem 276:37409-37414
29. Koenig JA, Edwardson JM (1997) Endocytosis and recycling of G protein-coupled receptors. Trends Pharmacol Sci 18:276-287
30. Lenkei Z, Beaudet A, Chartrel N, De Mota N, Irinopoulou T, Braun B, Vaudry H, Llorens-Cortès C (2000) A highly sensitive quantitative cytosensor technique for the identification of receptor ligands in tissue extracts. J Histochem Cytochem 48:1553-1564
31. Lin FT, Daaka Y, Lefkowitz RJ (1998) Beta-arrestins regulate mitogenic signaling and clathrin-mediated endocytosis of the insulin-like growth factor I receptor. J Biol Chem 273:31640-31643
32. Marsh M, McMahon HT (1999) The structural era of endocytosis. Science 285:215-220
33. Mazella J, Leonard K, Chabry J, Kitabgi P, Vincent JP, Beaudet A (1991) Binding and internalization of iodinated neurotensin in neuronal cultures from embryonic mouse brain. Brain Res 564:249-255
34. Mazella J, Botto JM, Guillemare E, Coppola T, Sarret P, Vincent JP (1996) Structure, functional expression, and cerebral localization of the levocabastine-sensitive neurotensin/neuromedin N receptor from mouse brain. J Neurosci 16:5613-5620
35. Mazella J, Zsurger N, Navarro V, Chabry J, Kaghad M, Caput D, Ferrara P, Vita N, Gully D, Maffrand JP, Vincent JP (1998) The 100-kDa neurotensin receptor is gp95/sortilin, a non-G-protein-coupled receptor. J Biol Chem 273:26273-26276
36. McDonald PH, Lefkowitz RJ (2001) Beta-arrestins: new roles in regulating heptahelical receptors' functions. Cell Signal 13:683-689
37. McPherson PS (1999) Regulatory role of SH3 domain-mediated protein-protein interactions in synaptic vesicle endocytosis. Cell Signal 11:229-238
38. McPherson PS (2002) The endocytic machinery at an interface with the actin cytoskeleton: a dynamic, hip intersection. Trends Cell Biol 12:312-315
39. McPherson PS, Kay BK, Hussain NK (2001) Signaling on the endocytic pathway. Traffic 2:375-384
40. Menard L, Ferguson SS, Zhang J, Lin FT, Lefkowitz RJ, Caron MG, Barak LS (1997) Synergistic regulation of beta2-adrenergic receptor sequestration: intracellular complement of beta-adrenergic receptor kinase and beta-arrestin determine kinetics of internalization. Mol Pharmacol 51:800-808
41. Nouel D, Gaudriault G, Houle M, Reisine T, Vincent JP, Mazella J, Beaudet A (1997) Differential internalization of somatostatin in COS-7 cells transfected with SST1 and SST2 receptor subtypes: a confocal microscopic study using novel fluorescent somatostatin derivatives. Endocrinology 138:296-306
42. O'Bryan JP, Mohney RP, Oldham CE (2001) Mitogenesis and endocytosis: what's at the intersection? Oncogene 20:6300-6308
43. Oakley RH, Laporte SA, Holt JA, Caron MG, Barak LS (2000) Differential affinities of visual arrestin, beta arrestin1, and beta arrestin2 for G protein-coupled receptors delineate two major classes of receptors. J Biol Chem 275:17201-17210
44. Oakley RH, Laporte SA, Holt JA, Barak LS, Caron MG (2001) Molecular determinants underlying the formation of stable intracellular G protein-coupled receptor-beta-arrestin complexes after receptor endocytosis. J Biol Chem 276:19452-19460
45. Okamoto M, Schoch S, Südhof TC (1999) EHSH1/intersectin, a protein that contains EH and SH3 domains and binds to dynamin and SNAP-25. A protein connection between exocytosis and endocytosis? J Biol Chem 274:18446-18454
46. Pals-Rylaarsdam R, Gurevich VV, Lee KB, Ptasienski JA, Benovic JL, Hosey MM (1997) Internalization of the m2 muscarinic acetylcholine receptor. Arrestin-independent and -dependent pathways. J Biol Chem 272:23682-23689
47. Perry SJ, Lefkowitz RJ (2002) Arresting developments in heptahelical receptor signaling and regulation. Trends Cell Biol 12:130-138
48. Petersen CM, Nielsen MS, Nykjaer A, Jacobsen L, Tommerup N, Rasmussen HH, Roigaard H, Gliemann J, Madsen P, Moestrup SK (1997) Molecular identification of a novel candidate sorting receptor purified from human brain by receptor-associated protein affinity chromatography. J Biol Chem 272:3599-3605
49. Predescu SA, Predescu DN, Timblin BK, Stan RV, Malik AB (2003) Intersectin regulates fission and internalization of caveolae in endothelial cells. Mol Biol Cell 14:4997-5010
50. Pucharcos C, Estivill X, Luna S de la (2000) Intersectin 2, a new multimodular protein involved in clathrin-mediated endocytosis. FEBS Lett 478:43-51
51. Pucharcos C, Casas C, Nadal M, Estivill X, Luna S de la (2001) The human intersectin genes and their spliced variants are differentially expressed. Biochim Biophys Acta 1521:1-11
52. Ramjaun AR, Micheva KD, Bouchelet I, McPherson PS (1997) Identification and characterization of a nerve terminal-enriched amphiphysin isoform. J Biol Chem 272:16700-16706
53. Ramjaun AR, McPherson PS (1998) Multiple amphiphysin II splice variants display differential clathrin binding: identification of two distinct clathrin-binding sites. J Neurochem 70:2369-2376
54. Ramjaun AR, Philie J, Heuvel E de, McPherson PS (1999) The N terminus of amphiphysin II mediates dimerization and plasma membrane targeting. J Biol Chem 274:19785-19791
55. Roos J, Kelly RB (1998) Dap160, a neural-specific Eps15 homology and multiple SH3 domain-containing protein that interacts with Drosophila dynamin. J Biol Chem 273:19108-19119
56. Roseberry AG, Hosey MM (2001) Internalization of the M2 muscarinic acetylcholine receptor proceeds through an atypical pathway in HEK293 cells that is independent of clathrin and caveolae. J Cell Sci 114:739-746
57. Rothberg KG, Ting Y-S, Kamen BA, Anderson RGW (1990) Cholesterol controls the clustering of glycophospholipid-anchored membrane receptor for 5-methyltetrahydrofolate. J Cell Biol 111:2931-2938
58. Rothberg KG, Heuser JE, Donzell WC, Ying Y-S, Glenney JR, Anderson RGW (1992) Caveolin, a protein component of caveolae membrane coats. Cell 68:673-682
59. Santolini E, Salcini AE, Kay BK, Yamabhai M, Di Fiore PP (1999) The EH network. Exp Cell Res 253:186-209
60. Sarret P, Beaudet A (2003) Neurotensin receptors in the central nervous system. In: Quirion RB, Björklund A, Hökfelt, T (ed) Handbook of chemical neuroanatomy, vol 20. Peptide receptors, part II. Elsevier, Amsterdam, pp 323-400
61. Sarret P, Esdaile MJ, McPherson PS, Schonbrunn A, Kreienkamp HJ, Beaudet A (2004) Role of amphiphysin II in somatostatin receptor trafficking in neuroendocrine cells. J Biol Chem 279:8029-8037
62. Schlador ML, Grubbs RD, Nathanson NM (2000) Multiple topological domains mediate subtype-specific internalization of the M2 muscarinic acetylcholine receptor. J Biol Chem 275:23 295-23 302
63. Schramm NL, Limbird LE (1999) Stimulation of mitogen-activated protein kinase by G protein-coupled alpha(2)-adrenergic receptors does not require agonist-elicited endocytosis. J Biol Chem 274:24935-24940
64. Sengar AS, Wang W, Bishay J, Cohen S, Egan SE (1999) The EH and SH3 domain Ese proteins regulate endocytosis by linking to dynamin and Eps15. Embo J 18:1159-1171
65. Sever S, Damke H, Schmid SL (2000) Garrotes, springs, ratchets, and whips: putting dynamin models to the test. Traffic 1:385-392
66. Shupliakov O, Löw P, Grabs D, Gad H, Chen H, David C, Takei K, De Camilli P, Brodin L (1997) Synaptic vesicle endocytosis impaired by disruption of dynamin-SH3 domain interactions. Science 276:259-263
67. Simpson F, Hussain NK, Qualmann B, Kelly RB, Kay BK, McPherson PS, Schmid SL (1999) SH3-domain-containing proteins function at distinct steps in clathrin-coated vesicle formation. Nat Cell Biol 1:119-120
68. Souazé F, Rostène W, Forgez P (1997) Neurotensin agonist induces differential regulation of neurotensin receptor mRNA. Identification of distinct transcriptional and post-transcriptional mechanisms. J Biol Chem 272:10087-10094
69. Szaszak M, Gáborik Z, Turu G, McPherson PS, Clark AJ, Catt KJ, Hunyady L (2002) Role of the proline-rich domain of dynamin-2 and its interactions with Src homology 3 domains during endocytosis of the AT1 angiotensin receptor. J Biol Chem 277:21650-21656
70. Tanaka K, Masu M, Nakanishi S (1990) Structure and functional expression of the cloned rat neurotensin receptor. Neuron 4:847-854
71. Toy-Miou-Leong M, Cortès CL, Beaudet A, Rostène W, Forgez P (2004) Receptor trafficking via the perinuclear recycling compartment accompanied by cell division is necessary for permanent neurotensin cell sensitization and leads to chronic mitogen-activated protein kinase activation. J Biol Chem 279:12636-12646
72. Tsutsui K, Maeda Y, Seki S, Tokunaga A (1997) cDNA cloning of a novel amphiphysin isoform and tissue-specific expression of its multiple splice variants. Biochem Biophys Res Commun 236:178-183
73. Vandenbulcke F, Nouel D, Vincent JP, Mazella J, Beaudet A (2000) Ligand-induced internalization of neurotensin in transfected COS-7 cells: differential intracellular trafficking of ligand and receptor. J Cell Sci 113:2963-2975
74. Vickery RG, Zastrow M von (1999) Distinct dynamin-dependent and -independent mechanisms target structurally homologous dopamine receptors to different endocytic membranes. J Cell Biol 144:31-43
75. Vita N, Laurent P, Lefort S, Chalon P, Dumont X, Kaghad M, Gully D, Le Fur G, Ferrara P, Caput D (1993) Cloning and expression of a complementary DNA encoding a high affinity human neurotensin receptor. FEBS Lett 317:139-142
76. Volchuk A, Narine S, Foster LJ, Grabs D, De Camilli P, Klip A (1998) Perturbation of dynamin II with an amphiphysin SH3 domain increases GLUT4 glucose transporters at the plasma membrane in 3T3-L1 adipocytes. Dynamin II participates in GLUT4 endocytosis. J Biol Chem 273:8169-8176
77. Vögler O, Bogatkewitsch GS, Wriske C, Krummenerl P, Jakobs KH, Koppen CJ van (1998) Receptor subtype-specific regulation of muscarinic acetylcholine receptor sequestration by dynamin. Distinct sequestration of m2 receptors. J Biol Chem 273:12155-12160
78. Walker JK, Premont RT, Barak LS, Caron MG, Shetzline MA (1999) Properties of secretin receptor internalization differ from those of the beta(2)-adrenergic receptor. J Biol Chem 274:31515-31523
79. Werbonat Y, Kleutges N, Jakobs KH, Koppen CJ van (2000) Essential role of dynamin in internalization of M2 muscarinic acetylcholine and angiotensin AT1A receptors. J Biol Chem 275:21969-21974
80. Wigge P, McMahon HT (1998) The amphiphysin family of proteins and their role in endocytosis at the synapse. Trends Neurosci 21:339-344
81. Wigge P, Köhler K, Vallis Y, Doyle CA, Owen D, Hunt SP, McMahon HT (1997a) Amphiphysin heterodimers: potential role in clathrin-mediated endocytosis. Mol Biol Cell 8:2003-2015
82. Wigge P, Vallis Y, McMahon HT (1997b) Inhibition of receptor-mediated endocytosis by the amphiphysin SH3 domain. Curr Biol 7:554-560
83. Yamabhai M, Hoffman NG, Hardison NL, McPherson PS, Castagnoli L, Cesareni G, Kay BK (1998) Intersectin, a novel adaptor protein with two Eps15 homology and five Src homology 3 domains. J Biol Chem 273:31401-31407
84. Zhang J, Ferguson SS, Barak LS, Menard L, Caron MG (1996) Dynamin and beta-arrestin reveal distinct mechanisms for G protein-coupled receptor internalization. J Biol Chem 271:18302-18305
85. Zhang J, Barak LS, Anborgh PH, Laporte SA, Caron MG, Ferguson SS (1999) Cellular trafficking of G protein-coupled receptor/beta-arrestin endocytic complexes. J Biol Chem 274:10999-11006