Basolateral sorting of transforming growth factor-α precursor in polarized epithelial cells: Characterization of cytoplasmic domain determinants

Experimental Cell Research

Volumn 285, Issue 2, 2003, Pages 159-174

  Dempsey, Peter J ^a,c   Meise, Katherine S ^a   Coffey, Robert J ^a,b  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^c PACIFIC NORTHWEST RESEARCH INSTITUTE   (United States)

Author keywords

Cell polarity; MDCK cells; Membrane anchored growth factor; TGF ; Trafficking

Indexed keywords

ALKALINE PHOSPHATASE PLACENTA ISOENZYME; BINDING PROTEIN; EPIDERMAL GROWTH FACTOR; MEMBRANE PROTEIN; NEUROTROPHIN; PROTEIN P75; TRANSFORMING GROWTH FACTOR ALPHA;

ANIMAL CELL; ARTICLE; CELL POLARITY; CHIMERA; CONTROLLED STUDY; CYTOPLASM; DELETION MUTANT; EPITHELIUM CELL; HUMAN; MUTAGENESIS; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN MOTIF; RAT; SECRETION;

EID: 0037403645     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0014-4827(03)00035-1     Document Type: Article

References (66)

1. Dempsey P.J., Coffey R.J. Basolateral targeting and efficient consumption of transforming growth factor-alpha when expressed in Madin-Darby canine kidney cells. J. Biol. Chem. 269:1994;16878-16889.
2. Aroeti B., Okhrimenko H., Reich V., Orzech E. Polarized trafficking of plasma membrane proteins emerging roles for coats, SNAREs, GTPases and their link to the cytoskeleton . Biochim. Biophys. Acta. 1376:1998;57-90.
3. Yeaman C., Grindstaff K.K., Nelson W.J. New perspectives on mechanisms involved in generating epithelial cell polarity. Physiol. Rev. 79:1999;73-98.
4. Mostov K.E., Verges M., Altschuler Y. Membrane traffic in polarized epithelial cells. Curr. Opin. Cell Biol. 12:2000;483-490.
5. Mays R.W., Siemers K.A., Fritz B.A., Lowe A.W., van Meer G., Nelson W.J. Hierarchy of mechanisms involved in generating Na/KATPase polarity in MDCK epithelial cells. J. Cell Biol. 130:1995;1105-1115.
6. Garner C.C., Nash J., Huganir R.L. PDZ domains in synapse assembly and signalling. Trends Cell Biol. 10:2000;274-280.
7. Carraway K.L. 3rd, Sweeney C. Localization and modulation of ErbB receptor tyrosine kinases. Curr. Opin. Cell Biol. 13:2001;125-130.
8. Bezprozvanny I., Maximov A. PDZ domains More than just a glue . Proc. Natl. Acad. Sci. USA. 98:2001;787-789.
9. Borg J.P., Marchetto S., Le Bivic A., Ollendorff V., Jaulin-Bastard F., Saito H., Fournier E., Adelaide J., Margolis B., Birnbaum D. ERBIN a basolateral PDZ protein that interacts with the mammalian ERBB2/HER2 receptor . Nat. Cell Biol. 2:2000;407-414.
10. Garcia R.A., Vasudevan K., Buonanno A. The neuregulin receptor ErbB-4 interacts with PDZ-containing proteins at neuronal synapses. Proc. Natl. Acad. Sci. USA. 97:2000;3596-3601.
11. Legouis R., Gansmuller A., Sookhareea S., Bosher J.M., Baillie D.L., Labouesse M. LET-413 is a basolateral protein required for the assembly of adherens junctions in Caenorhabditis elegans. Nat. Cell Biol. 2:2000;415-422.
12. Huang Y.Z., Won S., Ali D.W., Wang Q., Tanowitz M., Du Q.S., Pelkey K.A., Yang D.J., Xiong W.C., Salter M.W., Mei L. Regulation of neuregulin signaling by PSD-95 interacting with ErbB4 at CNS synapses. Neuron. 26:2000;443-455.
13. Rongo C., Whitfield C.W., Rodal A., Kim S.K., Kaplan J.M. LIN-10 is a shared component of the polarized protein localization pathways in neurons and epithelia. Cell. 94:1998;751-759.
14. Bilder D., Perrimon N. Localization of apical epithelial determinants by the basolateral PDZ protein Scribble. Nature. 403:2000;676-680.
15. Milewski M.I., Mickle J.E., Forrest J.K., Stafford D.M., Moyer B.D., Cheng J., Guggino W.B., Stanton B.A., Cutting G.R. A PDZ-binding motif is essential but not sufficient to localize the C terminus of CFTR to the apical membrane. J. Cell Sci. 114:2001;719-726.
16. Perego C., Vanoni C., Villa A., Longhi R., Kaech S.M., Frohli E., Hajnal A., Kim S.K., Pietrini G. PDZ-mediated interactions retain the epithelial GABA transporter on the basolateral surface of polarized epithelial cells. EMBO J. 18:1999;2384-2393.
17. Muth T.R., Ahn J., Caplan M.J. Identification of sorting determinants in the C-terminal cytoplasmic tails of the gamma-aminobutyric acid transporters GAT-2 and GAT-3. J. Biol. Chem. 273:1998;25616-25627.
18. Teuchert M., Maisner A., Herrler G. Importance of the carboxyl-terminal FTSL motif of membrane cofactor protein for basolateral sorting and endocytosis. Positive and negative modulation by signals inside and outside the cytoplasmic tail. J. Biol. Chem. 274:1999;19979-19984.
19. Cohen C.J., Gaetz J., Ohman T., Bergelson J.M. Multiple regions within the coxsackievirus and adenovirus receptor cytoplasmic domain are required for basolateral sorting. J. Biol Chem. 20:2001;20.
20. Hock B., Bohme B., Karn T., Yamamoto T., Kaibuchi K., Holtrich U., Holland S., Pawson T., Rubsamen-Waigmann H., Strebhardt K. PDZ-domain-mediated interaction of the Eph-related receptor tyrosine kinase EphB3 and the ras-binding protein AF6 depends on the kinase activity of the receptor. Proc. Natl. Acad. Sci. USA. 95:1998;9779-9784.
21. Torres R., Firestein B.L., Dong H., Staudinger J., Olson E.N., Huganir R.L., Bredt D.S., Gale N.W., Yancopoulos G.D. PDZ proteins bind, cluster, and synaptically colocalize with Eph receptors and their ephrin ligands. Neuron. 21:1998;1453-1463.
22. Lin D., Gish G.D., Songyang Z., Pawson T. The carboxyl terminus of B class ephrins constitutes a PDZ domain binding motif. J. Biol. Chem. 274:1999;3726-3733.
23. Simske J.S., Kaech S.M., Harp S.A., Kim S.K. LET-23 receptor localization by the cell junction protein LIN-7 during C. elegans vulval induction. Cell. 85:1996;195-204.
24. Kaech S.M., Whitfield C.W., Kim S.K. The LIN-2/LIN-7/LIN-10 complex mediates basolateral membrane localization of the C. elegans EGF receptor LET-23 in vulval epithelial cells. Cell. 94:1998;761-771.
25. Straight S.W., Chen L., Karnak D., Margolis B. Interaction with mLin-7 alters the targeting of endocytosed transmembrane proteins in mammalian epithelial cells. Mol. Biol. Cell. 12:2001;1329-1340.
26. Bilder D., Birnbaum D., Borg J.P., Bryant P., Huigbretse J., Jansen E., Kennedy M.B., Labouesse M., Legouis R., Mechler B., Perrimon N., Petit M., Sinha P. Collective nomenclature for LAP proteins. Nat. Cell Biol. 2:2000;E114.
27. Jaulin-Bastard F., Saito H., Le Bivic A., Ollendorff V., Marchetto S., Birnbaum D., Borg J.P. The erbb2/her2 receptor differentially interacts with erbin and pick1 psd-95/dlg/zo-1 domain proteins. J. Biol. Chem. 276:2001;15256-15263.
28. Buonanno A., Fischbach G.D. Neuregulin and ErbB receptor signaling pathways in the nervous system. Curr. Opin. Neurobiol. 11:2001;287-296.
29. Dillon C., Creer A., Kerr K., Kumin A., Dickson C. Basolateral targeting of ERBB2 is dependent on a novel bipartite juxtamembrane sorting signal but independent of the C-terminal ERBIN-binding domain. Mol. Cell. Biol. 22:2002;6553-6563.
30. Hobert M., Carlin C. Cytoplasmic juxtamembrane domain of the human EGF receptor is required for basolateral localization in MDCK cells. J. Cell. Physiol. 162:1995;434-446.
31. Hobert M.E., Kil S.J., Medof M.E., Carlin C.R. The cytoplasmic juxtamembrane domain of the epidermal growth factor receptor contains a novel autonomous basolateral sorting determinant. J. Biol. Chem. 272:1997;32901-32909.
32. He C., Hobert M., Friend L., Carlin C. The epidermal growth factor receptor juxtamembrane domain has multiple basolateral plasma membrane localization determinants, including a dominant signal with a polyproline core. J. Biol. Chem. 277:2002;38284-38293.
33. Hobert M.E., Friend L.A., Carlin C.R. Regulation of EGF signaling by cell polarity in MDCK kidney epithelial cells. J. Cell Physiol. 181:1999;330-341.
34. Kuwada S.K., Li X.F., Damstrup L., Dempsey P.J., Coffey R.J., Wiley H.S. The dynamic expression of the epidermal growth factor receptor and epidermal growth factor ligand family in a differentiating intestinal epithelial cell line. Growth Factors. 17:1999;139-153.
35. Kuwada S.K., Lund K.A., Li X.F., Cliften P., Amsler K., Opresko L.K., Wiley H.S. Differential signaling and regulation of apical vs. basolateral EGFR in polarized epithelial cells [see comments]. Am. J. Physiol. 275:1998;C1419-C1428.
36. Amsler K., Kuwada S.K. Membrane receptor location defines receptor interaction with signaling proteins in a polarized epithelium. Am. J. Physiol. 276:1999;C91-C101.
37. Damstrup L., Kuwada S.K., Dempsey P.J., Brown C.L., Hawkey C.J., Poulsen H.S., Wiley H.S., Coffey R.J. Amphiregulin acts as an autocrine growth factor in two human polarizing colon cancer lines that exhibit domain selective EGF receptor mitogenesis. Br. J. Cancer. 80:1999;1012-1019.
38. Dempsey P.J., Meise K.S., Yoshitake Y., Nishikawa K., Coffey R.J. Apical enrichment of human EGF precursor in Madin-Darby canine kidney cells involves preferential basolateral ectodomain cleavage sensitive to a metalloprotease inhibitor. J. Cell Biol. 138:1997;747-758.
39. Brown C.L., Coffey R.J., Dempsey P.J. ProAmphiregulin cytoplasmic domain is required for basolateral sorting but is not essential for constitutive or stimulus-induced processing in polarized MDCK cells. J. Biol. Chem. 29:2001;29538-29549.
40. Wiley H.S., Woolf M.F., Opresko L.K., Burke P.M., Will B., Morgan J.R., Lauffenburger D.A. Removal of the membrane-anchoring domain of epidermal growth factor leads to intracrine signaling and disruption of mammary epithelial cell organization. J. Cell Biol. 143:1998;1317-1328.
41. Dong J., Wiley H.S. Trafficking and proteolytic release of epidermal growth factor receptor ligands are modulated by their membrane-anchoring domains. J. Biol. Chem. 275:2000;557-564.
42. Shum L., Turck C.W., Derynck R. Cysteines 153 and 154 of transmembrane transforming growth factor-alpha are palmitoylated and mediate cytoplasmic protein association. J. Biol. Chem. 271:1996;28502-28508.
43. Fernandez-Larrea J., Merlos-Suarez A., Urena J.M., Baselga J., Arribas J. A role for a PDZ protein in the early secretory pathway for the targeting of proTGF-alpha to the cell surface. Mol. Cell. 3:1999;423-433.
44. Kuo A., Zhong C., Lane W.S., Derynck R. Transmembrane transforming growth factor-α tethers to the PDZ domain containing, Golgi membrane-associated protein p59/GRASP55. EMBO J. 19:2000;6427-6439.
45. Briley G.P., Hissong M.A., Chiu M.L., Lee D.C. The carboxyl-terminal valine residues of proTGF alpha are required for its efficient maturation and intracellular routing. Mol. Biol. Cell. 8:1997;1619-1631.
46. Urena J.M., Merlos-Suarez A., Baselga J., Arribas J. The cytoplasmic carboxy-terminal amino acid determines the subcellular localization of proTGF-(alpha) and membrane type matrix metalloprotease (MT1-MMP). J. Cell Sci. 112:1999;773-784.
47. Shum L., Reeves S.A., Kuo A.C., Fromer E.S., Derynck R. Association of the transmembrane TGF-alpha precursor with a protein kinase complex. J. Cell Biol. 125:1994;903-916.
48. Russell W.E., Dempsey P.J., Sitaric S., Peck A.J., Coffey R.J. Jr. Transforming growth factor-alpha (TGF alpha) concentrations increase in regenerating rat liver evidence for a delayed accumulation of mature TGF alpha . Endocrinology. 133:1993;1731-1738.
49. Bosenberg M.W., Pandiella A., Massague J. The cytoplasmic carboxy-terminal amino acid specifies cleavage of membrane TGF alpha into soluble growth factor. Cell. 71:1992;1157-1165.
50. Monlauzeur L., Rajasekaran A., Chao M., Rodriguez-Boulan E., Le Bivic A. A cytoplasmic tyrosine is essential for the basolateral localization of mutants of the human nerve growth factor receptor in Madin-Darby canine kidney cells. J. Biol. Chem. 270:1995;12219-12225.
51. Casanova J.E., Apodaca G., Mostov K.E. An autonomous signal for basolateral sorting in the cytoplasmic domain of the polymeric immunoglobulin receptor. Cell. 66:1991;65-75.
52. Brown C.L., Meise K.S., Plowman G.D., Coffey R.J., Dempsey P.J. Cell surface ectodomain cleavage of human amphiregulin precursor is sensitive to a metalloprotease inhibitor. Release of a predominant N-glycosylated 43-kDa soluble form. J. Biol. Chem. 273:1998;17258-17268.
53. Le Bivic A., Sambuy Y., Patzak A., Patil N., Chao M., Rodriguez-Boulan E. An internal deletion in the cytoplasmic tail reverses the apical localization of human NGF receptor in transfected MDCK cells. J. Cell Biol. 115:1991;607-618.
54. Yeaman C., Le Gall A.H., Baldwin A.N., Monlauzeur L., Le Bivic A., Rodriguez-Boulan E. The O-glycosylated stalk domain is required for apical sorting of neurotrophin receptors in polarized MDCK cells. J. Cell Biol. 139:1997;929-940.
55. Brown D.A., Crise B., Rose J.K. Mechanism of membrane anchoring affects polarized expression of two proteins in MDCK cells. Science. 245:1989;1499-1501.
56. Matter K., Hunziker W., Mellman I. Basolateral sorting of LDL receptor in MDCK cells the cytoplasmic domain contains two tyrosine-dependent targeting determinants . Cell. 71:1992;741-753.
57. Distel B., Bauer U., Le Borgne R., Hoflack B. Basolateral sorting of the cation-dependent mannose 6-phosphate receptor in Madin-Darby canine kidney cells. Identification of a basolateral determinant unrelated to clathrin-coated pit localization signals. J. Biol. Chem. 273:1998;186-193.
58. Geffen I., Fuhrer C., Leitinger B., Weiss M., Huggel K., Griffiths G., Spiess M. Related signals for endocytosis and basolateral sorting of the asialoglycoprotein receptor. J. Biol. Chem. 268:1993;20772-20777.
59. Rajasekaran A.K., Humphrey J.S., Wagner M., Miesenbock G., Le Bivic A., Bonifacino J.S., Rodriguez-Boulan E. TGN38 recycles basolaterally in polarized Madin-Darby canine kidney cells. Mol. Biol. Cell. 5:1994;1093-1103.
60. Le Gall A.H., Powell S.K., Yeaman C.A., Rodriguez-Boulan E. The neural cell adhesion molecule expresses a tyrosine-independent basolateral sorting signal. J. Biol. Chem. 272:1997;4559-4567.
61. Haass C., Koo E.H., Capell A., Teplow D.B., Selkoe D.J. Polarized sorting of beta-amyloid precursor protein and its proteolytic products in MDCK cells is regulated by two independent signals. J. Cell Biol. 128:1995;537-547.
62. Thomas D.C., Brewer C.B., Roth M.G. Vesicular stomatitis virus glycoprotein contains a dominant cytoplasmic basolateral sorting signal critically dependent upon a tyrosine. J. Biol. Chem. 268:1993;3313-3320.
63. Aroeti B., Kosen P.A., Kuntz I.D., Cohen F.E., Mostov K.E. Mutational and secondary structural analysis of the basolateral sorting signal of the polymeric immunoglobulin receptor. J. Cell Biol. 123:1993;1149-1160.
64. Folsch H., Ohno H., Bonifacino J.S., Mellman L. A novel clathrin adaptor complex mediates basolateral targeting in polarized epithelial cells. Cell. 99:1999;189-198.
65. Ohno H., Tomemori T., Nakatsu F., Okazaki Y., Aguilar R.C., Foelsch H., Mellman I., Saito T., Shirasawa T., Bonifacino J.S. Mu1B, a novel adaptor medium chain expressed in polarized epithelial cells. FEBS Lett. 449:1999;215-220.
66. Folsch H., Pypaert M., Schu P., Mellman I. Distribution and function of AP-1 clathrin adaptor complexes in polarized epithelial cells. J. Cell Biol. 152:2001;595-606.