A Novel Cytoplasmic Tail MXXXL Motif Mediates the Internalization of Prostate-specific Membrane Antigen

Molecular Biology of the Cell

Volumn 14, Issue 12, 2003, Pages 4835-4845

  Rajasekaran, Sigrid A ^a   Anilkumar, Gopalakrishnapillai ^a   Oshima, Eri ^a   Bowie, James U ^b   Liu, He ^c   Heston, Warren ^d   Bander, Neil H ^c   Rajasekaran, Ayyappan K ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

^d LERNER RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; ALANINE; CHIMERIC PROTEIN; CLATHRIN; INTERLEUKIN 2 RECEPTOR; PROSTATE SPECIFIC MEMBRANE ANTIGEN;

ALPHA CHAIN; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOPLASM; ENDOCYTOSIS; GENE DELETION; GENETIC TRANSFECTION; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN MOTIF;

ADAPTOR PROTEIN COMPLEX 2; AMINO ACID MOTIFS; ANIMALS; ANTIGENS, SURFACE; CERCOPITHECUS AETHIOPS; CLATHRIN; COS CELLS; ENDOCYTOSIS; GLUTAMATE CARBOXYPEPTIDASE II; HELA CELLS; HUMANS; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; MODELS, MOLECULAR; MUTATION; PLASMIDS; PROTEIN BINDING; RECEPTORS, INTERLEUKIN-2;

ANIMALIA;

EID: 0345306595     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E02-11-0731     Document Type: Article

References (56)

1. Anilkumar, G., Rajasekaran, S.A., Wang, S., Hankinson, O., Bander, N.H., and Rajasekaran, A.K. (2003). Prostate-specific membrane antigen association with filamin A modulates its internalization and NAALADase activity. Cancer Res. 63, 2645-2648.
2. Bello, V., Goding, J.W., Greengrass, V., Sali, A., Dubljevic, V., Lenoir, C., Trugnan, G., and Maurice, M. (2001). Characterization of a di-leucine-based signal in the cytoplasmic tail of the nucleotide-pyrophosphatase NPP1 that mediates basolateral targeting but not endocytosis. Mol. Biol. Cell 12, 3004-3015.
3. Boll, W., Rapoport I., Brunner, C., Modis, Y., Prehn, S., and Kirchhausen, T. (2002). The mu2 subunit of the clathrin adaptor AP-2 binds to FDNPVY and YppO sorting signals at distinct sites. Traffic 3, 590-600.
4. Bonifacino, J.S., and Dell'Angelica, E.C. (1999). Molecular bases for the recognition of tyrosine-based sorting signals. J. Cell Biol. 145, 923-926.
5. Bonifacino, J.S., and Traub, L.M. (2003). Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu. Rev. Biochem. 72, 395-447.
6. Carter, R.E., Feldman, A.R., and Coyle, J.T. (1996). Prostate-specific membrane antigen is a hydrolase with substrate and pharmacologic characteristics of a neuropeptidase. Proc. Natl. Acad. Sci. USA 93, 749-753.
7. Chang, S.S., Bander, N.H., and Heston, W.D. (1999a). Monoclonal antibodies: will they become an integral part of the evaluation and treatment of prostate cancer-focus on prostate-specific membrane antigen? Curr. Opin. Urol. 9, 391-395.
8. Chang, S.S., O'Keefe, D.S., Bacich, D.J., Reuter, V.E., Heston, W.D., and Gaudin, P.B. (1999b). Prostate-specific membrane antigen is produced in tumor-associated neovasculature. Clin. Cancer Res. 5, 2674-2681.
9. Chang, S.S., Reuter, V.E., Heston, W.D., Bander, N.H., Grauer, L.S., and Gaudin, P.B. (1999c). Five different anti-prostate-specific membrane antigen (PSMA) antibodies confirm PSMA expression in tumor-associated neovasculature. Cancer Res. 59, 3192-3198.
10. Chen, H.J., Yuan, J., and Lobel, P. (1997). Systematic mutational analysis of the cation-independent mannose 6-phosphate/insulin-like growth factor II receptor cytoplasmic domain. An acidic cluster containing a key aspartate is important for function in lysosomal enzyme sorting. J. Biol. Chem. 272, 7003-7012.
11. Christiansen, J.J., Rajasekaran, S.A., Moy, P., Butch, A., Goodglick, L., Gu, Z., Reiter, R.E., Bander, N.H., and Rajasekaran, A.K. (2003). Polarity of prostate specific membrane antigen, prostate stem cell antigen, and prostate specific antigen in prostate tissue and in a cultured epithelial cell line. Prostate 55, 9-19.
12. Coyle, J.T. (1997). The nagging question of the function of N-acetylaspartyl-glutamate. Neurobiol. Dis. 4, 231-238.
13. El Nemer, W., Colin, Y., Bauvy, C., Codogno, P., Fraser, R.H., Cartron, J.P., and Le Van Kim, C.L. (1999). Isoforms of the Lutheran/basal cell adhesion molecule glycoprotein are differentially delivered in polarized epithelial cells. Mapping of the basolateral sorting signal to a cytoplasmic di-leucine motif. J. Biol. Chem. 274, 31903-31908.
14. Halsted, C.H., Ling, E.H., Luthi-Carter, R., Villanueva, J.A., Gardner, J.M., and Coyle, J.T. (1998). Folylpoly-gamma-glutamate carboxypeptidase from pig jejunum. Molecular characterization and relation to glutamate carboxypeptidase II. J. Biol. Chem. 273, 20417-20424.
15. Herskovits, J.S., Burgess, C.C., Obar, R.A., and Vallee, R.B. (1993). Effects of mutant rat dynamin on endocytosis. J. Cell Biol. 122, 565-578.
16. Hirst, J., and Robinson, M.S. (1998). Clathrin and adaptors. Biochim. Biophys. Acta 1404, 173-193.
17. Hofmann, M.W., Honing, S., Rodionov, D., Dobberstein, B., von Figura, K., and Bakke, O. (1999). The leucine-based sorting motifs in the cytoplasmic domain of the invariant chain are recognized by the clathrin adaptors AP1 and AP2 and their medium chains. J. Biol. Chem. 274, 36153-36158.
18. Honing, S., Griffith, J., Geuze, H.J., and Hunziker, W. (1996). The tyrosine-based lysosomal targeting signal in lamp-1 mediates sorting into Golgi-derived clathrin-coated vesicles. EMBO J. 15, 5230-5239.
19. Horoszewicz, J.S., Kawinski, E., and Murphy, G.P. (1987). Monoclonal antibodies to a new antigenic marker in epithelial prostatic cells and serum of prostatic cancer patients. Anticancer Res. 7, 927-935.
20. Israeli, R.S., Powell, C.T., Fair, W.R., and Heston, W.D. (1993). Molecular cloning of a complementary DNA encoding a prostate-specific membrane antigen. Cancer Res. 53, 227-230.
21. Johnson, K.F., and Kornfeld, S. (1992). The cytoplasmic tail of the mannose 6-phosphate/insulin-like growth factor-II receptor has two signals for lysosomal enzyme sorting in the Golgi. J. Cell Biol. 119, 249-257.
22. Kawabata, H., Yang, R., Hirama, T., Vuong, P.T., Kawano, S., Gombart, A.F., and Koeffler, H.P. (1999). Molecular cloning of transferrin receptor 2. A new member of the transferrin receptor-like family. J. Biol. Chem. 274, 20826-20832.
23. Kirchhausen, T. (1999). Adaptors for clathrin-mediated traffic. Annu. Rev. Cell Dev. Biol. 15, 705-732.
24. Kirchhausen, T., Bonifacino, J.S., and Riezman, H. (1997). Linking cargo to vesicle formation: receptor tail interactions with coat proteins. Curr. Opin. Cell Biol. 9, 488-495.
25. Lazarovits, J., and Roth, M. (1988). A single amino acid change in the cytoplasmic domain allows the influenza virus hemagglutinin to be endocytosed through coated pits. Cell 53, 743-752,
26. Leonard, et al. (1984). Molecular cloning and expression of cDNAs for the human interleukin-2 receptor. Nature 311, 626-631.
27. Letourneur, F., and Klausner, R.D. (1992). A novel di-leucine motif and a tyrosine-based motif independently mediate lysosomal targeting and endocytosis of CD3 chains. Cell 69, 1143-1157.
28. Liu, H., Moy, P., Kim, S., Xia, Y., Rajasekaran, A., Navarro, V., Knudsen, B., and Bander, N.H. (1997). Monoclonal antibodies to the extracellular domain of prostate-specific membrane antigen also react with tumor vascular endothelium. Cancer Res. 57, 3629-3634.
29. Liu, H., Rajasekaran, A.K., Moy, P., Xia, Y., Kim, S., Navarro, V., Rahmati, R., and Bander, N.H. (1998). Constitutive and antibody-induced internalization of prostate-specific membrane antigen. Cancer Res. 58, 4055-4060.
30. Luthi-Carter, R., Barczak, A.K., Speno, H., and Coyle, J.T. (1998). Molecular characterization of human brain N-acetylated alpha-linked acidic dipeptidase (NAALADase). J. Pharmacol. Exp. Ther. 286, 1020-1025.
31. Marks, M.S., Ohno, H., Kirchhausen, T., and Bonifacino, J.S. (1997). Protein sorting by tyrosine-based signals: adapting to the Ys and wherefores. Trends Cell Biol. 7, 124-128.
32. McDevitt, M.R., et al. (2001). Tumor therapy with targeted atomic nanogenerators. Science 294, 1537-1540.
33. Mellman, I. (1996). Endocytosis and molecular sorting. Annu. Rev. Cell Dev. Biol. 12, 575-625.
34. Mukherjee, S., Ghosh, R.N., and Maxfield, F.R. (1997). Endocytosis. Physiol. Rev. 77, 759-803.
35. Nesterov, A., Carter, R.E., Sorkina, T., Gill, G.N., and Sorkin, A. (1999). Inhibition of the receptor-binding function of clathrin adaptor protein AP-2 by dominant-negative mutant mu2 subunit and its effects on endocytosis. EMBO J. 18, 2489-2499.
36. Ohno, H., Stewart, J., Fournier, M.C., Bosshart, H., Rhee, I., Miyatake, S., Saito, T., Gallusser, A., Kirchhausen, T., and Bonifacino, J.S. (1995). Interaction of tyrosine-based sorting signals with clathrin-associated proteins. Science 269, 1872-1875.
37. Owen, D.J., and Evans, P.R. (1998). A structural explanation for the recognition of tyrosine-based endocytotic signals. Science 282, 1327-1332.
38. Owen, D.J., and Luzio, J.P. (2000). Structural insights into clathrin-mediated endocytosis. Curr. Opin. Cell Biol. 12, 467-474.
39. Pastan, I.H., and Willingham, M.C. (1981). Receptor-mediated endocytosis of hormones in cultured cells. Annu. Rev. Physiol. 43, 239-250.
40. Pinto, J.T., Suffoletto, B.P., Berzin, T.M., Qiao, C.H., Lin, S., Tong, W.P., May, F., Mukherjee, B., and Heston, W.D. (1996). Prostate-specific membrane antigen: a novel folate hydrolase in human prostatic carcinoma cells. Clin. Cancer Res. 2, 1445-1451.
41. Pond, L., Kuhn, L.A., Teyton, L., Schutze, M.P., Tainer, J.A., Jackson, M.R., and Peterson, P.A. (1995). A role for acidic residues in di-leucine motif-based targeting to the endocytic pathway. J. Biol. Chem. 270, 19989-19997.
42. Rajasekaran, A.K., Humphrey, J.S., Wagner, M., Miesenbock, G., Le Bivic, A., Bonifacino, J.S., and Rodriguez-Boulan, E. (1994). TGN38 recycles basolaterally in polarized Madin-Darby canine kidney cells. Mol. Biol. Cell 5, 1093-1103.
43. Rinker-Schaeffer, C.W., Hawkins, A.L., Su, S.L., Israeli, R.S., Griffin, C.A., Isaacs, J.T., and Heston, W.D. (1995). Localization and physical mapping of the prostate-specific membrane antigen (PSM) gene to human chromosome 11. Genomics 30, 105-108.
44. Rubin, L.A., Kurman, C.C., Biddison, W.E., Goldman, N.D., and Nelson, D.L. (1985). A monoclonal antibody 7G7/B6, binds to an epitope on the human interleukin-2 (IL-2) receptor that is distinct from that recognized by IL-2 or anti-Tac. Hybridoma 4, 91-102.
45. Sandoval, I.V., and Bakke, O. (1994). Targeting of membrane proteins to endosomes and lysosomes. Trends Cell Biol. 4, 292-297.
46. Sandoval, I.V., Martinez-Arca, S., Valdueza, J., Palacios, S., and Holman, G.D. (2000). Distinct reading of different structural determinants modulates the dileucine-mediated transport steps of the lysosomal membrane protein LIM-PII and the insulin-sensitive glucose transporter GLUT4. J. Biol. Chem. 275, 39874-39885.
47. Sekiguchi, M., Okamoto, K., and Sakai, Y. (1989). Release of endogenous N-acetylaspartylglutamate (NAAG) and uptake of [3H]NAAG in guinea pig cerebellar slices. Brain Res. 482, 78-86.
48. Sheikh, H., and Isacke, C.M. (1996). A di-hydrophobic Leu-Val motif regulates the basolateral localization of CD44 in polarized Madin-Darby canine kidney epithelial cells. J. Biol. Chem. 271, 12185-12190.
49. Silver, D.A., Pellicer, I., Fair, W.R., Heston, W.D., and Cordon-Cardo, C. (1997). Prostate-specific membrane antigen expression in normal and malignant human tissues. Clin. Cancer Res. 3, 81-85.
50. Slusher, B.S., et al. (1999). Selective inhibition of NAALADase, which converts NAAG to glutamate, reduces ischemic brain injury. Nat. Med. 5, 1396-1402.
51. Smith-Jones, P.M., Vallabhajosula, S., Navarro, V., Bastidas, D., Goldsmith, S.J., and Bander, N.H. (2003). Radiolabeled monoclonal antibodies specific to the extracellular domain of prostate-specific membrane antigen: preclinical studies in nude mice bearing LNCaP human prostate tumor. J. Nucl. Med. 44, 610-617.
52. Speno, H.S., Luthi-Carter, R., Macias, W.L., Valentine, S.L., Joshi, A.R., and Coyle, J.T. (1999). Site-directed mutagenesis of predicted active site residues in glutamate carboxypeptidase II. Mol. Pharmacol. 55, 179-185.
53. Trowbridge, I.S., Collawn, J.F., and Hopkins, C.R. (1993). Signal-dependent membrane protein trafficking in the endocytic pathway. Annu. Rev. Cell Biol. 9, 129-161.
54. van der Bliek, A.M., Redelmeier, T.E., Damke, H., Tisdale, E.J., Meyerowitz, E.M., and Schmid, S.L. (1993). Mutations in human dynamin block an intermediate stage in coated vesicle formation. J. Cell Biol. 122, 553-563.
55. von Heijne, G. (1988). Transcending the impenetrable: how proteins come to terms with membranes. Biochim. Biophys. Acta 947, 307-333.
56. Wright, G.L., Jr., Grob, B.M., Haley, C., Grossman, K., Newhall, K., Petrylak, D., Troyer, J., Konchuba, A., Schellhammer, P.F., and Moriarty, R. (1996). Upregulation of prostate-specific membrane antigen after androgen-deprivation therapy. Urology 48, 326-334.