Skip to main content
SpringerLink
Log in

Cell-type-specific pathways of neurotensin endocytosis

  • Regular Article
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

The neurotensin receptor subtype 1 (NTS1) is a G-protein-coupled receptor (GPCR) mediating a large number of central and peripheral effects of neurotensin. Upon stimulation, NTS1 is rapidly internalized and targeted to lysosomes. This process depends on the interaction of the phosphorylated receptor with β–arrestin. Little is known about other accessory endocytic proteins potentially involved. Here, we investigated the involvement of dynamin, amphiphysin, and intersectin in the internalization of NTS1 receptor-ligand complexes in transfected COS-7 and HEK 293 cells, by using the transferrin receptor as an internal control for the constitutive endocytic pathway. We found that NTS1 endocytosis was not only arrestin–dependent, but also dynamin–dependent in both COS-7 and HEK 293 cells, whereas internalization of the transferrin receptor was independent of arrestin but required dynamin. Overexpression of the SH3 domain of amphiphysin II had no effect on receptor internalization in either cell type. By contrast, overexpression of full-length intersectin or of its SH3 domain (but not of its EH domain) inhibited NTS1 internalization in COS-7 but not in HEK 293 cells. This difference between COS-7 and HEK 293 cells was not attributable to differences in endogenous intersectin levels between the two cell lines. Indeed, the same constructs inhibited transferrin endocytosis equally well in COS-7 and HEK 293 cells. However, immunogold electron microscopy revealed that internalized NTS1 receptors were associated with clathrin-coated pits in COS-7 cells but with smooth vesicles in HEK 293 cells, suggesting that NTS1 internalization proceeds via different endocytic pathways in these two cell types.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

References

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Carraway R, Leeman SE (1973) The isolation of a new hypotensive peptide, neurotensin, from bovine hypothalami. J Biol Chem 248:6854–6861

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Faure MP, Nouel D, Beaudet A (1995c) Axonal and dendritic transport of internalized neurotensin in rat mesostriatal dopaminergic neurons. Neuroscience 68:519–529

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Ferguson SS (2001) Evolving concepts in G protein-coupled receptor endocytosis: the role in receptor desensitization and signaling. Pharmacol Rev 53:1–24

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Gaudriault G, Vincent JP (1992) Selective labeling of alpha– or epsilon–amino groups in peptides by the Bolton–Hunter reagent. Peptides 13:1187–1192

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hermans E, Octave JN, Maloteaux JM (1994) Receptor mediated internalization of neurotensin in transfected Chinese hamster ovary cells. Biochem Pharmacol 47:89–91

    Article  PubMed  CAS  Google Scholar 

  • Hermans E, Maloteaux JM (1998) Mechanisms of regulation of neurotensin receptors. Pharmacol Ther 79:89–104

    Article  PubMed  CAS  Google Scholar 

  • Herskovits JS, Burgess CC, Obar RA, Vallee RB (1993) Effects of mutant rat dynamin on endocytosis. J Cell Biol 122:565–578

    Article  PubMed  CAS  Google Scholar 

  • Hunyady L (1999) Molecular mechanisms of angiotensin II receptor internalization. J Am Soc Nephrol 10 Suppl 11:S47–S56

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Koenig JA, Edwardson JM (1997) Endocytosis and recycling of G protein-coupled receptors. Trends Pharmacol Sci 18:276–287

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Marsh M, McMahon HT (1999) The structural era of endocytosis. Science 285:215–220

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • McDonald PH, Lefkowitz RJ (2001) Beta-arrestins: new roles in regulating heptahelical receptors’ functions. Cell Signal 13:683–689

    Article  PubMed  CAS  Google Scholar 

  • McPherson PS (1999) Regulatory role of SH3 domain-mediated protein-protein interactions in synaptic vesicle endocytosis. Cell Signal 11:229–238

    Article  PubMed  CAS  Google Scholar 

  • McPherson PS (2002) The endocytic machinery at an interface with the actin cytoskeleton: a dynamic, hip intersection. Trends Cell Biol 12:312–315

    Article  PubMed  CAS  Google Scholar 

  • McPherson PS, Kay BK, Hussain NK (2001) Signaling on the endocytic pathway. Traffic 2:375–384

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • O’Bryan JP, Mohney RP, Oldham CE (2001) Mitogenesis and endocytosis: what’s at the intersection? Oncogene 20:6300–6308

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Perry SJ, Lefkowitz RJ (2002) Arresting developments in heptahelical receptor signaling and regulation. Trends Cell Biol 12:130–138

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Rothberg KG, Ying 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Santolini E, Salcini AE, Kay BK, Yamabhai M, Di Fiore PP (1999) The EH network. Exp Cell Res 253:186–209

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Schlador ML, Grubbs RD, Nathanson NM (2000) Multiple topological domains mediate subtype-specific internalization of the M2 muscarinic acetylcholine receptor. J Biol Chem 275:23295–23302

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Sever S, Damke H, Schmid SL (2000) Garrotes, springs, ratchets, and whips: putting dynamin models to the test. Traffic 1:385–392

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Tanaka K, Masu M, Nakanishi S (1990) Structure and functional expression of the cloned rat neurotensin receptor. Neuron 4:847–854

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Wigge P, McMahon HT (1998) The amphiphysin family of proteins and their role in endocytosis at the synapse. Trends Neurosci 21:339–344

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Wigge P, Vallis Y, McMahon HT (1997b) Inhibition of receptor-mediated endocytosis by the amphiphysin SH3 domain. Curr Biol 7:554–560

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank Mariette Lavallée and Clélia Tommi for excellent technical assistance. The EGFP-tagged amphiphysin II and intersectin 1 constructs and the antibodies against amphiphysin II, dynamin II, and intersectin 1 were kindly supplied by Dr. Peter S. McPherson, Montreal Neurological Institute.

Author information

Authors and Affiliations

  1. Department of Neurology and Neurosurgery, Montreal Neurological Institute, McGill University, 3801 University Street, Montréal, Québec, H3A 2B4, Canada

    Cheryl Savdie, Alain Beaudet & Thomas Stroh

  2. Robarts Research Institute, Department of Physiology and Pharmacology, University of Western Ontario, London, Ontario, Canada

    Stephen S. G. Ferguson

  3. Institut de Pharmacologie Moléculaire et Cellulaire, CNRS, UMR 6097, Université de Nice Sophia-Antipolis, 06560, Valbonne, France

    J.– P. Vincent

Authors
  1. Cheryl Savdie
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stephen S. G. Ferguson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J.– P. Vincent
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alain Beaudet
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Thomas Stroh
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Thomas Stroh.

Additional information

This work was supported by grants to A.B. from CIHR and FRSQ.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Savdie, C., Ferguson, S.S.G., Vincent, J.P. et al. Cell-type-specific pathways of neurotensin endocytosis. Cell Tissue Res 324, 69–85 (2006). https://doi.org/10.1007/s00441-005-0102-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-005-0102-3

Keywords

Search

Navigation