DOI: 10.1002/jcb.240230111. Sorting and recycling of cell surface receptors and endocytosed ligands: The asialoglycoprotein and transferrin receptors

Sorting and recycling of cell surface receptors and endocytosed ligands: The asialoglycoprotein and transferrin receptors

10.1002/jcb.240230111

Crossref journal-article

Wiley

Journal of Cellular Biochemistry (311)

Abstract

AbstractWith few exceptions, receptor‐mediated endocytosis of specific ligands is mediated through clustering of receptor‐ligand complexes in coated pits on the cell surface, followed by internalizalion of the complex into endocytic vesicles. During this process, ligand‐receptor dissociation occurs, most probably in a low pH prelysosomal compartment. In most cases the ligand is ultimately directed to the lysosomes, wherein it is degraded, while the receptor recycles to the cell surface.We have studied the kinetics of internalization and recycling of both the asialoglycoprotein receptor and the transferrin receptor in a human hepatoma cell line. By employing both biochemical and morphological/immunocytochemical approaches, we have gained some insight into the complex mechanisms which govern receptor recycling as well as ligand sorting and targeting. We can, in particular, explain why transferrin is exocytosed intact from the cells, while asialoglycoprotcins are degraded in lysosomes. We have also localized the intra‐cellular site at which endocylosed receptor and ligand dissociate.

Bibliography

Ciechanover, A., Schwartz, A. L., & Lodish, H. F. (1983). Sorting and recycling of cell surface receptors and endocytosed ligands: The asialoglycoprotein and transferrin receptors. Journal of Cellular Biochemistry, 23(1â4), 107â130. Portico.

Authors 3

Aaron Ciechanover (first)
Alan L. Schwartz (additional)
Harvey F. Lodish (additional)

References 67 Referenced 116

10.1016/0092-8674(78)90336-7
10.1182/blood.V47.1.133.133
10.1083/jcb.92.3.865
10.1038/279679a0
10.1016/0092-8674(83)90518-4
10.1016/S0021-9258(18)32848-5 / J Biol Chem by Harford J (1983)
10.1083/jcb.92.3.634
10.1016/S0021-9258(18)34710-0
10.1101/SQB.1982.046.01.068
10.1016/0092-8674(83)90052-1
10.1126/science.6170111
10.1146/annurev.ph.43.030181.001323
10.1016/S0021-9258(17)34164-9
10.1016/0006-2952(79)90586-0
10.1016/S0021-9258(19)85843-X
10.1016/S0021-9258(19)70520-1
10.1083/jcb.85.3.839
10.1016/0092-8674(80)90402-X
10.1016/0092-8674(80)90232-9
10.1016/S0021-9258(19)68423-1 / J Biol Chem by Marshall S (1981)
10.1083/jcb.92.1.34
10.1016/0092-8674(82)90219-7
10.1002/9780470122860.ch3
10.1016/S0021-9258(17)34768-3 / J Biol Chem by Basu SK (1978)
10.1016/S0021-9258(17)34799-3 / J Biol Chem by Posner BI (1978)
10.1016/S0021-9258(17)44551-0
10.1083/jcb.97.6.1762
10.1073/pnas.79.20.6186
10.1016/0092-8674(83)90078-8
10.1073/pnas.80.5.1300
10.1016/S0021-9258(18)32581-X
10.1016/S0021-9258(19)69536-0
10.1146/annurev.bi.51.070182.002531
10.1083/jcb.83.1.47
10.1016/0092-8674(80)90371-2
10.1016/S0021-9258(19)70522-5 / J Biol Chem by Schwartz AL (1980)
10.1016/S0021-9258(20)79761-9
10.1073/pnas.78.6.3348
10.1083/jcb.90.3.687
10.1016/0304-4165(77)90230-6
10.1126/science.6248960
10.1016/S0021-9258(19)52477-2
10.1177/31.1.6300218
10.1016/0092-8674(83)90517-2
10.1083/jcb.89.3.653
10.1146/annurev.bi.49.070180.002041
10.1016/0005-2736(77)90293-0
10.1073/pnas.78.7.4222
10.1073/pnas.78.5.3039
10.1016/0014-4827(69)90232-8
10.1073/pnas.80.8.2258
10.1016/S0021-9258(18)32481-5
10.1073/pnas.80.8.2263
10.1172/JCI104718
10.1016/S0021-9258(18)33171-5 / J Biol Chem by Nunez M‐T (1983)
10.1016/0167-4889(83)90122-2
10.1016/0006-291X(83)91776-X
10.1016/S0021-9258(18)34022-5
10.1016/S0021-9258(18)32120-3 / J Biol Chem by Lamb JE (1983)
10.1016/S0021-9258(19)69597-9
10.1073/pnas.75.7.3327
10.1083/jcb.95.2.676
{'key': 'e_1_2_1_64_2', 'first-page': '1842', 'volume': '42', 'author': 'Klausner RD', 'year': '1983', 'journal-title': 'Fed Proc'} / Fed Proc by Klausner RD (1983)
10.1016/S0021-9258(19)42341-7
10.1016/0092-8674(81)90340-8
10.1083/jcb.92.2.417
10.1098/rstb.1982.0169

Dates

Type	When
Created	20 years, 8 months ago (Dec. 30, 2004, 2:23 a.m.)
Deposited	2 years ago (Aug. 31, 2023, 1:05 a.m.)
Indexed	4 weeks, 2 days ago (Aug. 7, 2025, 4:23 p.m.)
Issued	42 years, 8 months ago (Jan. 1, 1983)
Published	42 years, 8 months ago (Jan. 1, 1983)
Published Online	21 years, 6 months ago (Feb. 19, 2004)
Published Print	42 years, 8 months ago (Jan. 1, 1983)

Funders 0

None

BibTeX

@article{Ciechanover_1983, title={Sorting and recycling of cell surface receptors and endocytosed ligands: The asialoglycoprotein and transferrin receptors}, volume={23}, ISSN={1097-4644}, url={http://dx.doi.org/10.1002/jcb.240230111}, DOI={10.1002/jcb.240230111}, number={1–4}, journal={Journal of Cellular Biochemistry}, publisher={Wiley}, author={Ciechanover, Aaron and Schwartz, Alan L. and Lodish, Harvey F.}, year={1983}, month=jan, pages={107–130} }

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      "URL": "https://onlinelibrary.wiley.com/doi/10.1002/jcb.240230111"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1983,
        1
      ]
    ]
  },
  "references-count": 67,
  "journal-issue": {
    "issue": "1-4",
    "published-print": {
      "date-parts": [
        [
          1983,
          1
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      ]
    }
  },
  "alternative-id": [
    "10.1002/jcb.240230111"
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  "URL": "http://dx.doi.org/10.1002/jcb.240230111",
  "relation": {},
  "ISSN": [
    "0730-2312",
    "1097-4644"
  ],
  "subject": [],
  "container-title-short": "J of Cellular Biochemistry",
  "published": {
    "date-parts": [
      [
        1983,
        1
      ]
    ]
  }
}