STAM and Hrs down-regulate ciliary TRP receptors

Molecular Biology of the Cell

Volumn 18, Issue 9, 2007, Pages 3277-3289

  Hu, Jinghua ^a   Wittekind, Samuel G ^b   Barr, Maureen M ^a,c  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; HEPATOCYTE GROWTH FACTOR REGULATED TYROSINE KINASE SUBSTRATE HRS; MEMBRANE RECEPTOR; POLYCYSTIN 1; PROTEIN LOV1; PROTEIN TYROSINE KINASE; SCATTER FACTOR; SIGNAL TRANSDUCTION ADAPTOR MOLECULE 1A; TRANSIENT RECEPTOR POLYCYSTIN 2 CHANNEL; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CAENORHABDITIS ELEGANS; COMPLEX FORMATION; CONTROLLED STUDY; DOWN REGULATION; ENDOSOME; EUKARYOTIC FLAGELLUM; FEMALE; GENE; LYSOSOME; MALE; MECHANORECEPTOR; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; STAM 1 GENE; YEAST;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CILIA; DENDRITES; DOWN-REGULATION; ENDOSOMES; LYSOSOMES; MALE; MODELS, BIOLOGICAL; NEURONS, AFFERENT; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN TRANSPORT; RAB5 GTP-BINDING PROTEINS; TRPP CATION CHANNELS; UBIQUITIN;

CAENORHABDITIS ELEGANS; MAMMALIA;

EID: 34548515061     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E07-03-0239     Document Type: Article

References (93)

1. Aguiari, G., Campanella, M., Manzati, E., Pinton, P., Banzi, M., Moretti, S., Piva, R., Rizzuto, R., and del Senno, L. (2003). Expression of polycystin-1 C-terminal fragment enhances the ATP-induced Ca(2+) release in human kidney cells. Biochem. Biophys. Res. Commun. 301(3), 657-664.
2. Asao, H., Sasaki, Y., Arita, T., Tanaka, N., Endo, K., Kasai, H., Takeshita, T., Endo, Y., Fujita, T., and Sugamura, K. (1997). Hrs is associated with STAM, a signal-transducing adaptor molecule. Its suppressive effect on cytokine-induced cell growth. J. Biol. Chem. 272(52), 32785-32791.
3. Bache, K. G., Raiborg, C., Mehlum, A., and Stenmark, H. (2003). STAM and Hrs are subunits of a multivalent ubiquitin-binding complex on early endosomes. J. Biol. Chem. 278(14), 12513-12521.
4. Badano, J. L., Mitsuma, N., Beales, P. L., and Katsanis, N. (2006) The ciliopathies: an emerging class of human genetic disorders. Annu. Rev. Genomics Hum. Genet. 7, 125-148.
5. Bae, Y. K., Qin, H., Knobel, K. M., Hu, J., Rosenbaum, J. L., and Barr, M. M. (2006). General and cell-type specific mechanisms target TRPP2/PKD-2 to cilia. Development 133(19), 3859-3870.
6. Barr, M. M. (2005). Caenorhabditis elegans as a model to study renal development and disease: sexy cilia. J. Am. Soc. Nephrol. 16(2), 305-312.
7. Barr, M. M., DeModena, J., Braun, D., Nguyen, C. Q., Hall, D. H., and Sternberg, P. W. (2001). The Caenorhabditis elegans autosomal dominant polycystic kidney disease gene homologs lov-1 and pkd-2 act in the same pathway. Curr. Biol. 11(17), 1341-1346.
8. Barr, M. M., and Sternberg, P. W. (1999). A polycystic kidney-disease gene homologue required for male mating behaviour in C. elegans. Nature 401(6751), 386-389.
9. Bilodeau, P. S., Urbanowski, J. L., Winistorfer, S. C., and Piper, R. C. (2002). The Vps27p Hse1p complex binds ubiquitin and mediates endosomal protein sorting. Nat. Cell Biol. 4(7), 534-539.
10. Bilodeau, P. S., Winistorfer, S. C., Kearney, W. R., Robertson, A. D., and Piper, R. C. (2003). Vps27-Hse1 and ESCRT-I complexes cooperate to increase efficiency of sorting ubiquitinated proteins at the endosome. J. Cell Biol. 163(2), 237-243.
11. Brailov, I., Bancila, M., Brisorgueil, M. J., Miquel, M. C., Hamon, M., and Verge, D. (2000). Localization of 5-HT(6) receptors at the plasma membrane of neuronal cilia in the rat brain. Brain Res. 872(1-2), 271-275.
12. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77(1), 71-94.
13. Buck, L., and Axel, R. (1991). A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65(1), 175-187.
14. Burbea, M., Dreier, L., Dittman, J. S., Grunwald, M. E., and Kaplan, J. M. (2002). Ubiquitin and AP180 regulate the abundance of GLR-1 glutamate receptors at postsynaptic elements in C. elegans. Neuron 35(1), 107-120.
15. Cai, Y. et al. (2004). Calcium dependence of polycystin-2 channel activity is modulated by phosphorylation at Ser812. J. Biol. Chem. 279(19), 19987-19995.
16. Chauvet, V. et al. (2004). Mechanical stimuli induce cleavage and nuclear translocation of the polycystin-1 C terminus. J. Clin. Invest. 114(10), 1433-1443.
17. Chen, L., and Davis, N. G. (2002). Ubiquitin-independent entry into the yeast recycling pathway. Traffic 3(2), 110-123.
18. Chin, L. S., Raynor, M. C., Wei, X., Chen, H. Q., and Li, L. (2001). Hrs interacts with sorting nexin 1 and regulates degradation of epidermal growth factor receptor. J. Biol. Chem. 276(10), 7069-7078.
19. Clapham, D. E. (2003). TRP channels as cellular sensors. Nature 426(6966), 517-524.
20. Delmas, P. (2004). Polycystins: from mechanosensation to gene regulation. Cell 118(2), 145-148.
21. Delmas, P. (2005). Polycystins: polymodal receptor/ion-channel cellular sensors. Pfluegers Arch. 451(1), 264-276.
22. Dunn, R., and Hicke, L. (2001). Multiple roles for Rsp5p-dependent ubiquitination at the internalization step of endocytosis. J. Biol. Chem. 276(28), 25974-25981.
23. Dwyer, N. D., Adler, C. E., Crump, J. G., L'Etoile, N. D., and Bargmann, C. I. (2001). Polarized dendritic transport and the AP-1 mu1 clathrin adaptor UNC-101 localize odorant receptors to olfactory cilia. Neuron 31(2), 277-287.
24. Fraser, A. G., Kamath, R. S., Zipperlen, P., Martinez-Campos, M., Sohrmann, M., and Ahringer, J. (2000). Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature 408(6810), 325-330.
25. Fisher, R. D., Wang, B., Alam, S. L., Higginson, D. S., Robinson, H., Sundquist, W. I., and Hill, C. P. (2003). Structure and ubiquitin binding of the ubiquitin-interacting motif. J. Biol. Chem. 278(31), 28976-28984.
26. Govindan, J. A., Cheng, H., Harris, J. E., and Greenstein, D. (2006). Galphao/i and Galphas signaling function in parallel with the MSP/Eph receptor to control meiotic diapause in C. elegans. Curr. Biol. 16(13), 1257-1268.
27. Govers, R., ten Broeke, T., van Kerkhof, P., Schwartz, A. L., and Strous, G. J. (1999). Identification of a novel ubiquitin conjugation motif, required for ligand-induced internalization of the growth hormone receptor. EMBO J. 18(1), 28-36.
28. Granato M, Schnabel H, and Schnabel R. (1994). pha-1, a selectable marker for gene transfer in C. elegans. Nucleic Acids Res. 22(9), 1762-1763.
29. Hicke, L., and Dunn, R. (2003). Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu. Rev. Cell Dev. Biol. 19, 141-172.
30. Hodgkin, J. (1983). Male phenotypes and mating efficiency in Caenorhabditis elegans. Genetics 103, 43-64.
31. Hooper, K. M., Unwin, R. J., and Sutters, M. (2003). The isolated C-terminus of polycystin-1 promotes increased ATP-stimulated chloride secretion in a collecting duct cell line. Clin. Sci. (Lond.) 104(3), 217-221.
32. Hu, J., Bae, Y. K., Knobel, K. M., and Barr, M. M. (2006). Casein kinase II and calcineurin modulate TRPP function and ciliary localization. Mol. Biol. Cell 17(5), 2200-2211.
33. Hu, J., and Barr, M. M. (2005). ATP-2 interacts with the PLAT domain of LOV-1 and is involved in Caenorhabditis elegans polycystin signaling. Mol. Biol. Cell 16(2), 458-469.
34. Huangfu, D., and Anderson, K. V. (2006). Signaling from Smo to Ci/Gli: conservation and divergence of Hedgehog pathways from Drosophila to vertebrates. Development 133(1), 3-14.
35. Igarashi, P., and Somlo, S. (2002). Genetics and pathogenesis of polycystic kidney disease. J. Am. Soc. Nephrol. 13(9), 2384-2398.
36. Ishimaru, Y., Inada, H., Kubota, M., Zhuang, H., Tominaga, M., and Matsunami, H. (2006). Transient receptor potential family members PKD1L3 and PKD2L1 form a candidate sour taste receptor. Proc. Natl. Acad. Sci. USA 103(33), 12569-12574.
37. Kanazawa, C., Morita, E., Yamada, M., Ishii, N., Miura, S., Asao, H., Yoshimori, T., and Sugamura, K. (2003). Effects of deficiencies of STAMs and Hrs, mammalian class E Vps proteins, on receptor downregulation. Biochem. Biophys. Res. Commun. 309(4), 848-56.
38. Katzmann, D. J., Odorizzi, G., and Emr, S. D. (2002). Receptor downregulation and multivesicular-body sorting. Nat. Rev. Mol. Cell Biol. 3(12), 893-905.
39. Kim, H., Jeong, W., Ahn, K., Ahn, C., and Kang, S. (2004). Siah-1 interacts with the intracellular region of polycystin-1 and affects its stability via the ubiquitin-proteasome pathway. J. Am. Soc. Nephrol. 15(8), 2042-2049.
40. Kim, J. et al. (2003). A TRPV family ion channel required for hearing in Drosophila. Nature 424(6944), 81-84.
41. Komada, M., and Kitamura, N. (2005). The Hrs/STAM Complex in the Downregulation of receptor tyrosine kinases. J. Biochem. (Tokyo) 137(1), 1-8.
42. Komada, M., Masaki, R., Yamamoto, A., and Kitamura, N. (1997). Hrs, a tyrosine kinase substrate with a conserved double zinc finger domain, is localized to the cytoplasmic surface of early endosomes. J. Biol. Chem. 272(33), 20538-20544.
43. Kottgen, M. et al. (2005). Trafficking of TRPP2 by PACS proteins represents a novel mechanism of ion channel regulation. EMBO J. 24(4), 705-716.
44. Koushika, S. P., Schaefer, A. M., Vincent, R., Willis, J. H., Bowerman, B., and Nonet, M. L. (2004). Mutations in Caenorhabditis elegans cytoplasmic dynein components reveal specificity of neuronal retrograde cargo. J. Neurosci. 24(16), 3907-16.
45. Lee, J., Jongeward, G. D., and Sternberg, P. W. (1994). unc-101, a gene required for many aspects of Caenorhabditis elegans development and behavior, encodes a clathrin-associated protein. Genes Dev. 8(1), 60-73.
46. Levkowitz, G., Waterman, H., Zamir, E., Kam, Z., Oved, S., Langdon, W. Y., Beguinot, L., Geiger, B., and Yarden, Y. (1998). c-Cbl/Sli-1 regulates endocytic sorting and ubiquitination of the epidermal growth factor receptor. Genes Dev. 12(23), 3663-3674.
47. Liu, K. S., and Sternberg, P. W. (1995). Sensory regulation of male mating behavior in Caenorhabditis elegans. Neuron 14(1), 79-89.
48. Liu, Q., Tan, G., Levenkova, N., Li, T., Pugh, E. N. Jr., Rux, J., Speicher, D.W., and Pierce, E. A. (2007) The proteome of the mouse photoreceptor sensory cilium complex. Mol. Cell Proteomics Epub ahead of print.
49. Lloyd, T. E., Atkinson, R., Wu, M. N., Zhou, Y., Pennetta, G., and Bellen, H. J. (2002). Hrs regulates endosome membrane invagination and tyrosine kinase receptor signaling in Drosophila. Cell 108(2), 261-269.
50. Ma, R., Li, W. P., Rundle, D., Kong, J., Akbarali, H. I., and Tsiokas, L. (2005). PKD2 functions as an epidermal growth factor-activated plasma membrane channel. Mol. Cell. Biol. 25(18), 8285-8298.
51. Marchese, A., Raiborg, C., Santini, F., Keen, J. H., Stenmark, H., and Benovic, J. L. (2003). The E3 ubiquitin ligase AIP4 mediates ubiquitination and sorting of the G protein-coupled receptor CXCR4. Dev. Cell 5(5), 709-722.
52. Marshall, W. F., and Nonaka, S. (2006). Cilia: tuning in to the cell's antenna. Curr. Biol. 16(15), R604-R614.
53. Marszalek, J. R., Liu, X., Roberts, E. A., Chui, D., Marth, J. D., Williams, D. S., and Goldstein, L. S. (2000). Genetic evidence for selective transport of opsin and arrestin by kinesin-II in mammalian photoreceptors. Cell 102(2), 175-187.
54. May, S. R., Ashique, A. M., Karlen, M., Wang, B., Shen, Y., Zarbalis, K., Reiter, J., Ericson, J., and Peterson, A. S. (2005). Loss of the retrograde motor for IFT disrupts localization of Smo to cilia and prevents the expression of both activator and repressor functions of Gli. Dev. Biol. 287(2), 378-389.
55. Mello, C., and Fire, A. (1995). DNA transformation. Methods Cell Biol. 48, 451-482.
56. Mizuno, E., Kawahata, K., Kato, M., Kitamura, N., and Komada, M. (2003). STAM proteins bind ubiquitinated proteins on the early endosome via the VHS domain and ubiquitin-interacting motif. Mol. Biol. Cell 14(9), 3675-3689.
57. Mochizuki, T. et al. (1996). PKD2, a gene for polycystic kidney disease that encodes an integral membrane protein. Science 272(5266), 1339-1342.
58. Nauli, S. M. et al. (2003). Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells. Nat. Genet. 33(2), 129-137.
59. Nauli, S. M., and Zhou, J. (2004). Polycystins and mechanosensation in renal and nodal cilia. Bioessays 26(8), 844-856.
60. Neill, A. T., Moy, G. W., and Vacquier, V. D. (2004). Polycystin-2 associates with the polycystin-1 homolog, suREJ3, and localizes to the acrosomal region of sea urchin spermatozoa. Reprod. Dev. 67(4), 472-477.
61. Nickel, C., Benzing, T., Sellin, L., Gerke, P., Karihaloo, A., Liu, Z. X., Cantley, L. G., and Walz, G. (2002). The polycystin-1 C-terminal fragment triggers branching morphogenesis and migration of tubular kidney epithelial cells. J. Clin. Invest. 109(4), 481-489.
62. Oldham, C. E., Mohney, R. P., Miller, S. L., Hanes, R. N., and O'Bryan, J. P. (2002). The ubiquitin-interacting motifs target the endocytic adaptor protein epsin for ubiquitination. Curr. Biol. 12(13), 1112-1116.
63. Pazour, G. J., Agrin, N., Leszyk, J., and Witman, G. B. (2005). Proteomic analysis of a eukaryotic cilium. J. Cell Biol. 170(1), 103-113.
64. Pazour, G. J., and Rosenbaum, J. L. (2002). Intraflagellar transport and cilia-dependent diseases. Trends Cell Biol. 12(12), 551-555.
65. Pazour, G. J., San Agustin, J. T., Follit, J. A., Rosenbaum, J. L., and Witman, G. B. (2002). Polycystin-2 localizes to kidney cilia and the ciliary level is elevated in orpk mice with polycystic kidney disease. Curr. Biol. 12, R378-R380.
66. Petiot, A., Faure, J., Stenmark, H., and Gmenberg, J. (2003). PI3P signaling regulates receptor sorting but not transport in the endosomal pathway. J. Cell Biol. 162(6), 971-979.
67. Polo, S., Sigismund, S., Faretta, M., Guidi, M., Capua, M. R., Bossi, G., Chen, H., De Camilli, P., and Di Fiore, P. P. (2002). A single motif responsible for ubiquitin recognition and monoubiquitination in endocytic proteins. Nature 416(6879), 451-455.
68. Raiborg, C., Bache, K. G., Gillooly, D. J., Madshus, I. H., Stang, E., and Stenmark, H. (2002). Hrs sorts ubiquitinated proteins into clathrin-coated microdomains of early endosomes. Nat. Cell Biol. 4(5), 394-398.
69. Raiborg, C., Rusten, T. E., and Stenmark, H. (2003). Protein sorting into multivesicular endosomes. Curr. Opin. Cell Biol. 15(4), 446-455.
70. Rosenbaum, J. L., and Witman, G. B. (2002). Intraflagellar transport. Nat. Rev. Mol. Cell Biol. 3(11), 813-825.
71. Roudier, N., Lefebvre, C., and Legouis, R. (2005). CeVPS-27 is an endosomal protein required for the molting and the endocytic trafficking of the low-density lipoprotein receptor-related protein 1 in Caenorhabditis elegans. Traffic 6(8), 695-705.
72. Sato, M., Sato, K., Fonarev, P., Huang, C. J., Liou, W., and Grant, B. D. (2005). Caenorhabditis elegans RME-6 is a novel regulator of RAB-5 at the clathrin-coated pit. Nat. Cell Biol. 7(6), 559-569.
73. Schlessinger, J. (2000). Cell signaling by receptor tyrosine kinases. Cell 103(2), 211-225.
74. Schneider, L., Clement, C. A., Teilmann, S. C., Pazour, G. J., Hoffmann, E. K., Satir, P., and Christensen, S. T. (2005). PDGFRalphaalpha signaling is regulated through the primary cilium in fibroblasts. Curr. Biol. 15(20), 1861-1866.
75. Scholey, J. M., and Anderson, K. V. (2006). Intraflagellar transport and cilium-based signaling. Cell 125(3), 439-442.
76. Shih, S. C., Katzmann, D. J., Schnell, J. D., Sutanto, M., Emr, S. D., and Hicke, L. (2002). Epsins and Vps27p/Hrs contain ubiquitin-binding domains that function in receptor endocytosis. Nat. Cell Biol. 4(5), 389-393.
77. Signor, D., Wedaman, K. P., Orozco, J. T., Dwyer, N. D., Bargmann, C. I., Rose, L. S., and Scholey, J. M. (1999). Role of a class DHC1b dynein in retrograde transport of IFT motors and IFT raft particles along cilia, but not dendrites, in chemosensory neurons of living Caenorhabditis elegans. J. Cell Biol. 147(3), 519-530.
78. Singla, V., and Reiter, J. F. (2006). The primary cilium as the cell's antenna: signaling at a sensory organelle. Science 313(5787), 629-633.
79. Sonnichsen, B. et al. (2005). RNAi profiling of early embryogenesis in Caenorhabditis elegans. Nature 434(7032), 462-469.
80. Staub, O., and Rotin, D. (2006). Role of ubiquitylation in cellular membrane transport. Physiol. Rev. 86(2), 669-707.
81. Sulston, J. E., Albertson, D. G., and Thomson, J. N. (1980). The Caenorhabditis elegans male: postembryonic development of nongonadal structures. Dev. Biol. 78(2), 542-576.
82. Sutton, K. A., Jungnickel, M. K., Ward, C. J., Harris, P. C., and Florman, H. M. (2006). Functional characterization of PKDREJ, a male germ cell-restricted polycystic J. Cell. Physiol. 209(2), 493-500.
83. Swanson, K. A., Kang, R. S., Stamenova, S. D., Hicke, L., and Radhakrishnan, I. (2003). Solution structure of Vps27 UIM-ubiquitin complex important for endosomal sorting and receptor downregulation. EMBO J. 22(18), 4597-4606.
84. Takata, H., Kato, M., Denda, K., Kitamura, N. (2000). A hrs binding protein having a Src homology 3 domain is involved in intracellular degradation of growth factors and their receptors. Genes Cells 5(1), 57-69.
85. Thien, C. B., Walker, F., and Langdon, W. Y. (2001). RING finger mutations that abolish c-Cbl-directed polyubiquitination and downregulation of the EGF receptor are insufficient for cell transformation. Mol. Cell 7(2), 355-365.
86. Thrower, J. S., Hoffman, L., Rechsteiner, M., and Pickart, C. M. (2000). Recognition of the polyubiquitin proteolytic signal. EMBO J. 19(1), 94-102.
87. Tobin, D., Madsen, D., Kahn-Kirby, A., Peckol, E., Moulder, G., Barstead, R., Maricq, A., and Bargmann, C. (2002). Combinatorial expression of TRPV channel proteins defines their sensory functions and subcellular localization in C. elegans neurons. Neuron 35(2), 307-318.
88. Urbe, S., Sachse, M., Row, P. E., Preisinger, C., Barr, F. A., Strous, G., Klumperman, J., and Clague, M. J. (2003) The UIM domain of Hrs couples receptor sorting to vesicle formation. J. Cell Sci. 116(Pt 20), 4169-4179.
89. Vandorpe, D. H., Chernova, M. N., Jiang, L., Sellin, L. K., Wilhelm, S., Stuart-Tilley, A. K., Walz, G., and Alper, S. L. (2001). The cytoplasmic C-terminal fragment of polycystin-1 regulates a Ca2+- permeable cation channel. J. Biol. Chem. 276(6), 4093-4101.
90. Wegierski, T., Hill, K., Schaefer, M., and Walz, G. (2006). The HECT ubiquitin ligase AIP4 regulates the cell surface expression of select TRP channels. EMBO J. 25(24), 5659-5669.
91. Whitfield, J. F. (2004). The neuronal primary cilium - an extrasynaptic signaling device. Cell Signal 16(7), 763-767.
92. Wicks, S. R., de Vries, C. J., van Luenen, H. G., and Plasterk, R. H. (2000). CHE-3, a cytosolic dynein heavy chain, is required for sensory cilia structure and function in Caenorhabditis elegans. Dev. Biol. 221(2), 295-307.
93. Yoder, B. K., Hou, X., and Guay-Woodford, L. M. (2002). The polycystic kidney disease proteins, polycystin-1, polycystin-2, polaris, and cystin, are co-localized in renal cilia. J. Am. Soc. Nephrol. 13(10), 2508-2516.