Interaction between PKD1L3 and PKD2L1 through their transmembrane domains is required for localization of PKD2L1 at taste pores in taste cells of circumvallate and foliate papillae

FASEB Journal

Volumn 24, Issue 10, 2010, Pages 4058-4067

  Ishimaru, Yoshiro ^a,b   Katano, Yuka ^a   Yamamoto, Kurumi ^a   Akiba, Masato ^a   Misaka, Takumi ^a   Roberts, Richard W ^b   Asakura, Tomiko ^a   Matsunami, Hiroaki ^b   Abe, Keiko ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Association; Polycystic kidney disease; Sour taste receptor; Trafficking

Indexed keywords

MEMBRANE PROTEIN; PROTEIN POLYCYSTIC KIDNEY DISEASE 1 LIKE 3; PROTEIN POLYCYSTIC KIDNEY DISEASE 2 LIKE 1; UNCLASSIFIED DRUG; CALCIUM CHANNEL; CELL SURFACE RECEPTOR; ION CHANNEL; PKD1L3 PROTEIN, HUMAN; PKD2L1 PROTEIN, HUMAN; PROTEIN BINDING;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL SURFACE; CIRCUMVALLATE; DELETION MUTANT; FOLIATE PAPILLAE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; TASTE BUD; TASTE CELL; TONGUE; CELL LINE; CHEMISTRY; HUMAN; IMMUNOPRECIPITATION; IN SITU HYBRIDIZATION; METABOLISM;

MAMMALIA; MUS;

CALCIUM CHANNELS; CELL LINE; HUMANS; IMMUNOPRECIPITATION; IN SITU HYBRIDIZATION; ION CHANNELS; MEMBRANE PROTEINS; PROTEIN BINDING; RECEPTORS, CELL SURFACE; TASTE BUDS;

EID: 77957841185     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.10-162925     Document Type: Article

References (41)

1. Delmas, P., Padilla, F., Osorio, N., Coste, B., Raoux, M. and Crest, M. (2004) Polycystins, calcium signaling, and human diseases. Biochem. Biophys. Res. Commun. 322, 1374-1383 (Pubitemid 39164667)
2. Huang, A. L., Chen, X., Hoon, M. A., Chandrashekar, J., Guo, W., Trankner, D., Ryba, N. J. and Zuker, C. S. (2006) The cells and logic for mammalian sour taste detection. Nature 442, 934-938 (Pubitemid 44285950)
3. 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. U. S. A. 103, 12569-12574 (Pubitemid 44267299)
4. Kataoka, S., Yang, R., Ishimaru, Y., Matsunami, H., Sevigny, J., Kinnamon, J. C. and Finger, T. E. (2008) The candidate sour taste receptor, PKD2L1, is expressed by type III taste cells in the mouse. Chem. Senses 33, 243-254
5. LopezJimenez, N. D., Cavenagh, M. M., Sainz, E., Cruz-Ithier, M. A., Battey, J. F. and Sullivan, S. L. (2006) Two members of the TRPP family of ion channels, Pkd1l3 and Pkd2l1, are coexpressed in a subset of taste receptor cells. J. Neurochem. 98, 68-77
6. Miyoshi, M. A., Abe, K. and Emori, Y. (2001) IP(3) receptor type 3 and PLCbeta2 are co-expressed with taste receptors T1R and T2R in rat taste bud cells. Chem. Senses 26, 259-265 (Pubitemid 32318376)
7. Hoon, M. A., Adler, E., Lindemeier, J., Battey, J. F., Ryba, N. J. and Zuker, C. S. (1999) Putative mammalian taste receptors: a class of taste-specific GPCRs with distinct topographic selectivity. Cell 96, 541-551 (Pubitemid 29106841)
8. Zhang, Y., Hoon, M. A., Chandrashekar, J., Mueller, K. L., Cook, B., Wu, D., Zuker, C. S. and Ryba, N. J. (2003) Coding of sweet, bitter, and umami tastes: different receptor cells sharing similar signaling pathways. Cell 112, 293-301 (Pubitemid 36183651)
9. Clapp, T. R., Stone, L. M., Margolskee, R. F. and Kinnamon, S. C. (2001) Immunocytochemical evidence for co-expression of Type III IP3 receptor with signaling components of bitter taste transduction. BMC Neurosci. 2, 6
10. Perez, C. A., Huang, L., Rong, M., Kozak, J. A., Preuss, A. K., Zhang, H., Max, M. and Margolskee, R. F. (2002) A transient receptor potential channel expressed in taste receptor cells. Nat. Neurosci. 5, 1169-1176
11. Inada, H., Kawabata, F., Ishimaru, Y., Fushiki, T., Matsunami, H. and Tominaga, M. (2008) Off-response property of an acid-activated cation channel complex PKD1L3-PKD2L1. EMBO Rep. 9, 690-697 (Pubitemid 351927691)
12. Kawaguchi, H., Yamanaka, A., Uchida, K., Shibasaki, K., Sokabe, T., Maruyama, Y., Yanagawa, Y., Murakami, S. and Tominaga, M. (2010) Activation of polycystic kidney disease-2-like 1 (PKD2L1)/PKD1L3 complex by acid in mouse taste cells. J. Biol. Chem. 285, 17277-17281
13. Ishimaru, Y. and Matsunami, H. (2009) Transient receptor potential (TRP) channels and taste sensation. J. Dent. Res. 88, 212-218
14. Ishimaru, Y. (2009) Molecular mechanisms of taste transduction in vertebrates. Odontology 97, 1-7
15. Yarmolinsky, D. A., Zuker, C. S. and Ryba, N. J. (2009) Common sense about taste: from mammals to insects. Cell 139, 234-244
16. Nauli, S. M. and Zhou, J. (2004) Polycystins and mechanosensation in renal and nodal cilia. Bioessays 26, 844-856
17. Qian, F., Germino, F. J., Cai, Y., Zhang, X., Somlo, S. and Germino, G. G. (1997) PKD1 interacts with PKD2 through a probable coiled-coil domain. Nat. Genet. 16, 179-183
18. Tsiokas, L., Kim, E., Arnould, T., Sukhatme, V. P. and Walz, G. (1997) Homo- and heterodimeric interactions between the gene products of PKD1 and PKD2. Proc. Natl. Acad. Sci. U. S. A. 94, 6965-6970 (Pubitemid 27281974)
19. Casuscelli, J., Schmidt, S., DeGray, B., Petri, E. T., Celic, A., Folta-Stogniew, E., Ehrlich, B. E. and Boggon, T. J. (2009) Analysis of the cytoplasmic interaction between polycystin-1 and polycystin-2. Am. J. Physiol. Renal Physiol. 297, F1310-F1315
20. Hanaoka, K., Qian, F., Boletta, A., Bhunia, A. K., Piontek, K., Tsiokas, L., Sukhatme, V. P., Guggino, W. B. and Germino, G. G. (2000) Co-assembly of polycystin-1 and -2 produces unique cation-permeable currents. Nature 408, 990-994
21. Nauli, S. M., Alenghat, F. J., Luo, Y., Williams, E., Vassilev, P., Li, X., Elia, A. E., Lu, W., Brown, E. M., Quinn, S. J., Ingber, D. E. and Zhou, J. (2003) Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells. Nat. Genet. 33, 129-137
22. Nauli, S. M., Kawanabe, Y., Kaminski, J. J., Pearce, W. J., Ingber, D. E. and Zhou, J. (2008) Endothelial cilia are fluid shear sensors that regulate calcium signaling and nitric oxide production through polycystin-1. Circulation 117, 1161-1171 (Pubitemid 351544064)
23. Sharif-Naeini, R., Folgering, J. H., Bichet, D., Duprat, F., Lauritzen, I., Arhatte, M., Jodar, M., Dedman, A., Chatelain, F. C., Schulte, U., Retailleau, K., Loufrani, L., Patel, A., Sachs, F., Delmas, P., Peters, D. J. and Honore, E. (2009) Polycystin-1 and -2 dosage regulates pressure sensing. Cell 139, 587-596
24. Li, A., Tian, X., Sung, S. W. and Somlo, S. (2003) Identification of two novel polycystic kidney disease-1-like genes in human and mouse genomes. Genomics 81, 596-608 (Pubitemid 36637015)
25. Nomura, H., Turco, A. E., Pei, Y., Kalaydjieva, L., Schiavello, T., Weremowicz, S., Ji, W., Morton, C. C., Meisler, M., Reeders, S. T. and Zhou, J. (1998) Identification of PKDL, a novel polycystic kidney disease 2-like gene whose murine homologue is deleted in mice with kidney and retinal defects. J. Biol. Chem. 273, 25967-25973
26. Saito, H., Kubota, M., Roberts, R. W., Chi, Q. and Matsunami, H. (2004) RTP family members induce functional expression of mammalian odorant receptors. Cell 119, 679-691 (Pubitemid 39535755)
27. Ishii, S., Misaka, T., Kishi, M., Kaga, T., Ishimaru, Y. and Abe, K. (2009) Acetic acid activates PKD1L3-PKD2L1 channel-a candidate sour taste receptor. Biochem. Biophys. Res. Commun. 385, 346-350
28. Bunting, M., Bernstein, K. E., Greer, J. M., Capecchi, M. R. and Thomas, K. R. (1999) Targeting genes for self-excision in the germ line. Genes Dev. 13, 1524-1528
29. Gao, N., Lu, M., Echeverri, F., Laita, B., Kalabat, D., Williams, M. E., Hevezi, P., Zlotnik, A. and Moyer, B. D. (2009) Voltage-gated sodium channels in taste bud cells. BMC Neurosci. 10, 20
30. Hughes, J., Ward, C. J., Aspinwall, R., Butler, R. and Harris, P. C. (1999) Identification of a human homologue of the sea urchin receptor for egg jelly: a polycystic kidney disease-like protein. Hum. Mol. Genet. 8, 543-549
31. Murakami, M., Ohba, T., Xu, F., Shida, S., Satoh, E., Ono, K., Miyoshi, I., Watanabe, H., Ito, H. and Iijima, T. (2005) Genomic organization and functional analysis of murine PKD2L1. J. Biol. Chem. 280, 5626-5635
32. Montell, C. (2005) The TRP superfamily of cation channels. Sci. STKE 2005, re3
33. Erler, I., Al-Ansary, D. M., Wissenbach, U., Wagner, T. F., Flockerzi, V. and Niemeyer, B. A. (2006) Trafficking and assembly of the cold-sensitive TRPM8 channel. J. Biol. Chem. 281, 38396-38404
34. Tsuruda PR, Julius, D. and Minor DL, Jr. (2006) Coiled coils direct assembly of a cold-activated TRP channel. Neuron 51, 201-212 (Pubitemid 44041868)
35. Phelps, C. B. and Gaudet, R. (2007) The role of the N terminus and transmembrane domain of TRPM8 in channel localization and tetramerization. J. Biol. Chem. 282, 36474-36480
36. Dai, X. Q., Karpinski, E. and Chen, X. Z. (2006) Permeation and inhibition of polycystin-L channel by monovalent organic cations. Biochim. Biophys. Acta 1758, 197-205
37. Shimizu, T., Janssens, A., Voets, T. and Nilius, B. (2009) Regulation of the murine TRPP3 channel by voltage, pH, and changes in cell volume. Pflügers Arch. 457, 795-807
38. Chen, X. Z., Vassilev, P. M., Basora, N., Peng, J. B., Nomura, H., Segal, Y., Brown, E. M., Reeders, S. T., Hediger, M. A. and Zhou, J. (1999) Polycystin-L is a calcium-regulated cation channel permeable to calcium ions. Nature 401, 383-386
39. Dai, X. Q., Ramji, A., Liu, Y., Li, Q., Karpinski, E. and Chen, X. Z. (2007) Inhibition of TRPP3 channel by amiloride and analogs. Mol. Pharmacol. 72, 1576-1585
40. Li, Q., Dai, X. Q., Shen, P. Y., Wu, Y., Long, W., Chen, C. X., Hussain, Z., Wang, S. and Chen, X. Z. (2007) Direct binding of alpha-actinin enhances TRPP3 channel activity. J. Neurochem. 103, 2391-2400
41. Li, Q., Liu, Y., Zhao, W. and Chen, X. Z. (2002) The calcium-binding EF-hand in polycystin-L is not a domain for channel activation and ensuing inactivation. FEBS Lett. 516, 270-278