Home LiteratureArticle Details
PMID: 9236215 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Identification of a somatodendritic targeting signal in the cytoplasmic domain of the transferrin receptor.

West AE, Neve RL, Buckley KM

Abstract

Neurons are highly polarized cells that must sort proteins synthesized in the cell body for transport into the axon or the dendrites. Given the amount of time and energy needed to deliver proteins to the distal processes, neurons must have high fidelity mechanisms that ensure proper polarized protein trafficking. Although a variety of proteins are localized either to the somatodendritic domain or to the axon (), the question of whether there are signal-dependent mechanisms that sort proteins to distinct neuronal domains is only beginning to be addressed. To determine sequence requirements for the polarized sorting of transmembrane proteins into dendrites, we expressed mutant transferrin receptors in cultured rat hippocampal neurons, using a defective herpes virus vector. Wild-type human transferrin receptor colocalized with the endogenous protein in dendritic endosomes and was strictly excluded from axons, despite overexpression. Polarized targeting was abolished by deletion of cytoplasmic amino acids 7-10, 11-14, or 19-28, but not 29-42 or 43-58. These deletions also increased the appearance of transferrin receptor on the plasma membrane, implying that endocytosis and dendritic targeting are mediated by overlapping signals and similar molecular mechanisms. In addition, we have characterized a specialized para-Golgi endosome poised to play a critical role in the polarized recycling of transmembrane proteins.

MeSH Terms
Animals Cell Polarity/physiology Cells, Cultured Cytoplasm/chemistry,metabolism Dendrites/chemistry,physiology,ultrastructure Endocytosis/physiology Endosomes/chemistry,metabolism Fluorescent Antibody Technique Hippocampus/cytology Humans Mutagenesis/physiology Neurons/chemistry,cytology,ultrastructure Protein Structure, Tertiary Rats Rats, Sprague-Dawley Receptors, Transferrin/chemistry,genetics Signal Transduction/physiology
Chemicals
Receptors, Transferrin
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
West A E
Department of Neurobiology, Harvard Medical School, Boston, Massachusetts 02115, USA.
Neve R L
Buckley K M
References (62)
62 references, click to expand
  1. Segregation of transferrin to a mildly acidic (pH 6.5) para-Golgi compartment in the recycling pathway.
    Cell. 1984 Jul;37(3):789-800 PMID: 6204769
  2. Neuronal polarity.
    Annu Rev Neurosci. 1994;17:267-310 PMID: 8210176
  3. Lateral diffusion of proteins in membranes.
    Annu Rev Physiol. 1987;49:163-75 PMID: 3551795
  4. Rat hippocampal neurons in dispersed cell culture.
    Brain Res. 1977 May 13;126(3):397-42 PMID: 861729
  5. A novel adaptor-related protein complex.
    J Cell Biol. 1996 May;133(4):749-60 PMID: 8666661
  6. Intracellular trafficking of lysosomal membrane proteins.
    Bioessays. 1996 May;18(5):379-89 PMID: 8639161
  7. Apical and basolateral endocytosis in Madin-Darby canine kidney (MDCK) cells grown on nitrocellulose filters.
    EMBO J. 1985 Nov;4(11):2781-92 PMID: 4065093
  8. The internalization signal and the phosphorylation site of transferrin receptor are distinct from the main basolateral sorting information.
    EMBO J. 1993 Apr;12(4):1713-21 PMID: 8467813
  9. PCR-ligation-PCR mutagenesis: a protocol for creating gene fusions and mutations.
    Biotechniques. 1995 May;18(5):746-50 PMID: 7619468
  10. Axonal and dendritic endocytic pathways in cultured neurons.
    J Cell Biol. 1992 Oct;119(1):123-37 PMID: 1527164
  11. Analysis of the signals for polarized transport of influenza virus (A/WSN/33) neuraminidase and human transferrin receptor, type II transmembrane proteins.
    J Virol. 1994 Mar;68(3):1812-8 PMID: 8107243
  12. In migrating fibroblasts, recycling receptors are concentrated in narrow tubules in the pericentriolar area, and then routed to the plasma membrane of the leading lamella.
    J Cell Biol. 1994 Jun;125(6):1265-74 PMID: 7515888
  13. A targeting signal in VAMP regulating transport to synaptic vesicles.
    Cell. 1995 May 19;81(4):581-9 PMID: 7758112
  14. Receptor-mediated transcytosis of IgA in MDCK cells is via apical recycling endosomes.
    J Cell Biol. 1994 Apr;125(1):67-86 PMID: 8138576
  15. Apical and basolateral endosomes of MDCK cells are interconnected and contain a polarized sorting mechanism.
    J Cell Biol. 1996 Oct;135(1):139-52 PMID: 8858169
  16. Assembly and intracellular transport of MHC class I and class II molecules.
    Cold Spring Harb Symp Quant Biol. 1995;60:249-61 PMID: 8824398
  17. A novel class of clathrin-coated vesicles budding from endosomes.
    J Cell Biol. 1996 Jan;132(1-2):21-33 PMID: 8567724
  18. Evidence that the herpes simplex virus immediate early protein ICP27 acts post-transcriptionally during infection to regulate gene expression.
    Virology. 1992 Jan;186(1):74-86 PMID: 1309283
  19. Ubiquitous cell-surface glycoprotein on tumor cells is proliferation-associated receptor for transferrin.
    Proc Natl Acad Sci U S A. 1981 Jul;78(7):4515-9 PMID: 6270680
  20. A defective HSV-1 vector expresses Escherichia coli beta-galactosidase in cultured peripheral neurons.
    Science. 1988 Sep 23;241(4873):1667-9 PMID: 2843986
  21. Membrane protein trafficking through the common apical endosome compartment of polarized Caco-2 cells.
    Mol Biol Cell. 1995 May;6(5):597-610 PMID: 7545032
  22. In vitro binding of clathrin adaptors to sorting signals correlates with endocytosis and basolateral sorting.
    EMBO J. 1996 Jun 3;15(11):2893-9 PMID: 8654387
  23. Clathrin, adaptors, and sorting.
    Annu Rev Cell Biol. 1990;6:151-71 PMID: 2177341
  24. Common signals control low density lipoprotein receptor sorting in endosomes and the Golgi complex of MDCK cells.
    Cell. 1993 Sep 24;74(6):1053-64 PMID: 8402881
  25. Basolateral sorting of LDL receptor in MDCK cells: the cytoplasmic domain contains two tyrosine-dependent targeting determinants.
    Cell. 1992 Nov 27;71(5):741-53 PMID: 1423629
  26. Transferrin receptor polarity and recycling accuracy in "tight" and "leaky" strains of Madin-Darby canine kidney cells.
    J Cell Biol. 1986 Nov;103(5):1767-79 PMID: 2877994
  27. Coats and vesicle budding.
    Trends Cell Biol. 1997 Mar;7(3):99-102 PMID: 17708916
  28. A casein kinase II phosphorylation site in the cytoplasmic domain of the cation-dependent mannose 6-phosphate receptor determines the high affinity interaction of the AP-1 Golgi assembly proteins with membranes.
    J Biol Chem. 1996 Jan 26;271(4):2171-8 PMID: 8567675
  29. Generation of high-titer defective HSV-1 vectors using an IE 2 deletion mutant and quantitative study of expression in cultured cortical cells.
    Biotechniques. 1996 Mar;20(3):460-9 PMID: 8679207
  30. Amplicon-based herpes simplex virus vectors.
    Methods Cell Biol. 1994;43 Pt A:191-210 PMID: 7823862
  31. Interaction of tyrosine-based sorting signals with clathrin-associated proteins.
    Science. 1995 Sep 29;269(5232):1872-5 PMID: 7569928
  32. Targeting of membrane proteins to endosomes and lysosomes.
    Trends Cell Biol. 1994 Aug;4(8):292-7 PMID: 14731593
  33. MAP2 is localized to the dendrites of hippocampal neurons which develop in culture.
    Brain Res. 1984 Apr;315(2):314-8 PMID: 6722593
  34. The herpes simplex virus amplicon: a new eucaryotic defective-virus cloning-amplifying vector.
    Cell. 1982 Aug;30(1):295-304 PMID: 6290080
  35. pH and the recycling of transferrin during receptor-mediated endocytosis.
    Proc Natl Acad Sci U S A. 1983 Apr;80(8):2258-62 PMID: 6300903
  36. Sorting of membrane components from endosomes and subsequent recycling to the cell surface occurs by a bulk flow process.
    J Cell Biol. 1993 Jun;121(6):1257-69 PMID: 8509447
  37. Mutational analysis of the cytoplasmic tail of the human transferrin receptor. Identification of a sub-domain that is required for rapid endocytosis.
    J Biol Chem. 1991 Oct 5;266(28):19006-12 PMID: 1918016
  38. Lipid diffusion in neurons.
    Nature. 1993 Mar 11;362(6416):119 PMID: 8450884
  39. Mutagenesis of the human transferrin receptor: two cytoplasmic phenylalanines are required for efficient internalization and a second-site mutation is capable of reverting an internalization-defective phenotype.
    J Cell Biol. 1991 Mar;112(5):853-61 PMID: 1900298
  40. Herpes simplex virus type 1 ICP27 deletion mutants exhibit altered patterns of transcription and are DNA deficient.
    J Virol. 1989 Jan;63(1):18-27 PMID: 2535723
  41. Molecular analysis of neuronal physiology by gene transfer into neurons with herpes simplex virus vectors.
    Trends Neurosci. 1991 Oct;14(10):428-32 PMID: 1722360
  42. The basolateral targeting signal in the cytoplasmic domain of glycoprotein G from vesicular stomatitis virus resembles a variety of intracellular targeting motifs related by primary sequence but having diverse targeting activities.
    J Biol Chem. 1994 Jun 3;269(22):15732-9 PMID: 8195226
  43. Barriers for lateral diffusion of transferrin receptor in the plasma membrane as characterized by receptor dragging by laser tweezers: fence versus tether.
    J Cell Biol. 1995 Jun;129(6):1559-74 PMID: 7790354
  44. Receptor-mediated endocytosis: concepts emerging from the LDL receptor system.
    Annu Rev Cell Biol. 1985;1:1-39 PMID: 2881559
  45. YTRF is the conserved internalization signal of the transferrin receptor, and a second YTRF signal at position 31-34 enhances endocytosis.
    J Biol Chem. 1993 Oct 15;268(29):21686-92 PMID: 8408022
  46. Long-term increases in neurotransmitter release from neuronal cells expressing a constitutively active adenylate cyclase from a herpes simplex virus type 1 vector.
    Proc Natl Acad Sci U S A. 1993 Aug 15;90(16):7603-7 PMID: 8102799
  47. Compartmentalized structure of the plasma membrane for receptor movements as revealed by a nanometer-level motion analysis.
    J Cell Biol. 1994 Jun;125(6):1251-64 PMID: 8207056
  48. Transferrin receptor internalization sequence YXRF implicates a tight turn as the structural recognition motif for endocytosis.
    Cell. 1990 Nov 30;63(5):1061-72 PMID: 2257624
  49. A vital stain for the Golgi apparatus.
    Science. 1985 May 10;228(4700):745-7 PMID: 2581316
  50. Transport into and out of the Golgi complex studied by transfecting cells with cDNAs encoding horseradish peroxidase.
    J Cell Biol. 1994 Nov;127(3):641-52 PMID: 7962049
  51. Identification of a consensus motif for retention of transmembrane proteins in the endoplasmic reticulum.
    EMBO J. 1990 Oct;9(10):3153-62 PMID: 2120038
  52. The distribution of synapsin I and synaptophysin in hippocampal neurons developing in culture.
    J Neurosci. 1991 Jun;11(6):1617-26 PMID: 1904480
  53. Membrane transport in the endocytic pathway.
    Curr Opin Cell Biol. 1995 Aug;7(4):552-63 PMID: 7495576
  54. Protein sorting by tyrosine-based signals: adapting to the Ys and wherefores.
    Trends Cell Biol. 1997 Mar;7(3):124-8 PMID: 17708922
  55. The establishment of polarity by hippocampal neurons in culture.
    J Neurosci. 1988 Apr;8(4):1454-68 PMID: 3282038
  56. The human transferrin receptor gene: genomic organization, and the complete primary structure of the receptor deduced from a cDNA sequence.
    Cell. 1984 Dec;39(2 Pt 1):267-74 PMID: 6094009
  57. Role of the human transferrin receptor cytoplasmic domain in endocytosis: localization of a specific signal sequence for internalization.
    J Cell Biol. 1990 Feb;110(2):283-94 PMID: 2298808
  58. Mechanisms of cell polarity: sorting and transport in epithelial cells.
    Curr Opin Cell Biol. 1994 Aug;6(4):545-54 PMID: 7986532
  59. Colocalization of synaptophysin with transferrin receptors: implications for synaptic vesicle biogenesis.
    J Cell Biol. 1991 Oct;115(1):151-64 PMID: 1918133
  60. Expression of exogenous proteins in mammalian cells with the Semliki Forest virus vector.
    Methods Cell Biol. 1994;43 Pt A:43-53 PMID: 7529866
  61. Intracellular routing of wild-type and mutated polymeric immunoglobulin receptor in hippocampal neurons in culture.
    J Cell Biol. 1995 Sep;130(6):1447-59 PMID: 7559765
  62. Lateral diffusion of rhodopsin in the photoreceptor membrane.
    Nature. 1974 Feb 15;247(5441):438-41 PMID: 4818543
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
0270-6474
Published
1997-08-15
Pages
6038-47
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6568350
Subset
IM
Grants
NINDS NIH HHS · 2 T32 NS07009-21 · United States
NINDS NIH HHS · NS27536 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com