TGN38 Recycles Basolaterally in Polarized Madin-Darby Canine Kidney Cells

Overview

Journal Mol Biol Cell

Specialties Cell Biology
Molecular Biology

Date 1994 Oct 1

PMID 7865877

Citations 25

Authors

A K Rajasekaran

J S Humphrey

M Wagner

G Miesenbock

A Le Bivic

J S Bonifacino

E Rodriguez-Boulan

Affiliations

Soon will be listed here.

Abstract

Sorting of newly synthesized plasma membrane proteins to the apical or basolateral surface domains of polarized cells is currently thought to take place within the trans-Golgi network (TGN). To explore the relationship between protein localization to the TGN and sorting to the plasma membrane in polarized epithelial cells, we have expressed constructs encoding the TGN marker, TGN38, in Madin-Darby canine kidney (MDCK) cells. We report that TGN38 is predominantly localized to the TGN of these cells and recycles via the basolateral membrane. Analyses of the distribution of Tac-TGN38 chimeric proteins in MDCK cells suggest that the cytoplasmic domain of TGN38 has information leading to both TGN localization and cycling through the basolateral surface. Mutations of the cytoplasmic domain that disrupt TGN localization also lead to nonpolarized delivery of the chimeric proteins to both surface domains. These results demonstrate an apparent equivalence of basolateral and TGN localization determinants and support an evolutionary relationship between TGN and plasma membrane sorting processes.

Citing Articles

Sorting of secretory proteins at the -Golgi network by human TGN46.

Lujan P, Garcia-Cabau C, Wakana Y, Lillo J, Rodilla-Ramirez C, Sugiura H Elife. 2024; 12.

PMID: 38466628 PMC: 10928510. DOI: 10.7554/eLife.91708.

Protein sorting from endosomes to the TGN.

Buser D, Spang A Front Cell Dev Biol. 2023; 11:1140605.

PMID: 36895788 PMC: 9988951. DOI: 10.3389/fcell.2023.1140605.

HHV-7 U21 exploits Golgi quality control carriers to reroute class I MHC molecules to lysosomes.

Dirck A, Whyte M, Hudson A Mol Biol Cell. 2019; 31(3):196-208.

PMID: 31851583 PMC: 7001482. DOI: 10.1091/mbc.E19-07-0363.

A recurrent missense variant in SLC9A7 causes nonsyndromic X-linked intellectual disability with alteration of Golgi acidification and aberrant glycosylation.

Khayat W, Hackett A, Shaw M, Ilie A, Dudding-Byth T, Kalscheuer V Hum Mol Genet. 2018; 28(4):598-614.

PMID: 30335141 PMC: 6360272. DOI: 10.1093/hmg/ddy371.

A novel tribasic Golgi export signal directs cargo protein interaction with activated Rab11 and AP-1-dependent Golgi-plasma membrane trafficking.

Parmar H, Duncan R Mol Biol Cell. 2016; 27(8):1320-31.

PMID: 26941330 PMC: 4831885. DOI: 10.1091/mbc.E15-12-0845.

References

McGraw T, Dunn K, Maxfield F . Isolation of a temperature-sensitive variant Chinese hamster ovary cell line with a morphologically altered endocytic recycling compartment. J Cell Physiol. 1993; 155(3):579-94. DOI: 10.1002/jcp.1041550316. View

Colley K, Lee E, Paulson J . The signal anchor and stem regions of the beta-galactoside alpha 2,6-sialyltransferase may each act to localize the enzyme to the Golgi apparatus. J Biol Chem. 1992; 267(11):7784-93. View

Peters C, Braun M, Weber B, Wendland M, Schmidt B, Pohlmann R . Targeting of a lysosomal membrane protein: a tyrosine-containing endocytosis signal in the cytoplasmic tail of lysosomal acid phosphatase is necessary and sufficient for targeting to lysosomes. EMBO J. 1990; 9(11):3497-506. PMC: 552098. DOI: 10.1002/j.1460-2075.1990.tb07558.x. View

Huttner W, Tooze S . Biosynthetic protein transport in the secretory pathway. Curr Opin Cell Biol. 1989; 1(4):648-54. DOI: 10.1016/0955-0674(89)90029-x. View

Sabatini D, Kreibich G, Morimoto T, Adesnik M . Mechanisms for the incorporation of proteins in membranes and organelles. J Cell Biol. 1982; 92(1):1-22. PMC: 2112015. DOI: 10.1083/jcb.92.1.1. View

Matter K, Hunziker W, Mellman I . Basolateral sorting of LDL receptor in MDCK cells: the cytoplasmic domain contains two tyrosine-dependent targeting determinants. Cell. 1992; 71(5):741-53. DOI: 10.1016/0092-8674(92)90551-m. View

Mellman I, Simons K . The Golgi complex: in vitro veritas?. Cell. 1992; 68(5):829-40. PMC: 7133332. DOI: 10.1016/0092-8674(92)90027-a. View

Trowbridge I . Endocytosis and signals for internalization. Curr Opin Cell Biol. 1991; 3(4):634-41. DOI: 10.1016/0955-0674(91)90034-v. View

Hunziker W, Harter C, Matter K, Mellman I . Basolateral sorting in MDCK cells requires a distinct cytoplasmic domain determinant. Cell. 1991; 66(5):907-20. DOI: 10.1016/0092-8674(91)90437-4. View

10.

Evan G, LEWIS G, Ramsay G, Bishop J . Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol Cell Biol. 1985; 5(12):3610-6. PMC: 369192. DOI: 10.1128/mcb.5.12.3610-3616.1985. View

11.

Sargiacomo M, Lisanti M, Graeve L, Le Bivic A, Rodriguez-Boulan E . Integral and peripheral protein composition of the apical and basolateral membrane domains in MDCK cells. J Membr Biol. 1989; 107(3):277-86. DOI: 10.1007/BF01871942. View

12.

Kornfeld S, Mellman I . The biogenesis of lysosomes. Annu Rev Cell Biol. 1989; 5:483-525. DOI: 10.1146/annurev.cb.05.110189.002411. View

13.

Rothman J, Orci L . Molecular dissection of the secretory pathway. Nature. 1992; 355(6359):409-15. DOI: 10.1038/355409a0. View

14.

Humphrey J, Peters P, Yuan L, Bonifacino J . Localization of TGN38 to the trans-Golgi network: involvement of a cytoplasmic tyrosine-containing sequence. J Cell Biol. 1993; 120(5):1123-35. PMC: 2119736. DOI: 10.1083/jcb.120.5.1123. View

15.

van Meer G, van t Hof W . Epithelial sphingolipid sorting is insensitive to reorganization of the Golgi by nocodazole, but is abolished by monensin in MDCK cells and by brefeldin A in Caco-2 cells. J Cell Sci. 1993; 104 ( Pt 3):833-42. DOI: 10.1242/jcs.104.3.833. View

16.

Brewer C, Roth M . A single amino acid change in the cytoplasmic domain alters the polarized delivery of influenza virus hemagglutinin. J Cell Biol. 1991; 114(3):413-21. PMC: 2289095. DOI: 10.1083/jcb.114.3.413. View

17.

Rodriguez-Boulan E . Polarized assembly of enveloped viruses from cultured epithelial cells. Methods Enzymol. 1983; 98:486-501. DOI: 10.1016/0076-6879(83)98176-4. View

18.

Griffiths G, Simons K . The trans Golgi network: sorting at the exit site of the Golgi complex. Science. 1986; 234(4775):438-43. DOI: 10.1126/science.2945253. View

19.

Ladinsky M, Howell K . The trans-Golgi network can be dissected structurally and functionally from the cisternae of the Golgi complex by brefeldin A. Eur J Cell Biol. 1992; 59(1):92-105. View

20.

Rodriguez-Boulan E, Powell S . Polarity of epithelial and neuronal cells. Annu Rev Cell Biol. 1992; 8:395-427. DOI: 10.1146/annurev.cb.08.110192.002143. View