TMTC1 and TMTC2 are novel endoplasmic reticulum Tetratricopeptide repeat-containing adapter proteins involved in calcium homeostasis

Journal of Biological Chemistry

Volumn 289, Issue 23, 2014, Pages 16085-16099

  Sunryd, Johan C ^a   Cheon, Banyoon ^a   Graham, Jill B ^a   Giorda, Kristina M ^a   Fissore, Rafael A ^a   Hebert, Daniel N ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CELL MEMBRANES; PHYSIOLOGY;

CALCIUM HOMEOSTASIS; CO-IMMUNOPRECIPITATIONS; ENDOPLASMIC RETICULUM; INTEGRAL MEMBRANE PROTEINS; POLYTOPIC MEMBRANE PROTEINS; PROTEIN STRUCTURAL MOTIFS; PROTEIN-PROTEIN INTERACTIONS; TETRATRICOPEPTIDE REPEATS;

PROTEINS;

CALNEXIN; MEMBRANE PROTEIN; REGULATOR PROTEIN; SERCA2B PROTEIN; TETRATRICOPEPTIDE REPEAT PROTEIN; TMTC1 PROTEIN; TMTC2 PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BIOASSAY; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CALCIUM TRANSPORT; CONTROLLED STUDY; DNA SEQUENCE; EMBRYO; ENDOPLASMIC RETICULUM; HUMAN; HUMAN CELL; HUMAN TISSUE; HYDROPHOBICITY; IMMUNOPRECIPITATION; INTRACELLULAR SIGNALING; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; PROTEOMICS; REDOX STRESS; SEQUENCE HOMOLOGY; TETRATRICOPEPTIDE REPEAT; UPREGULATION;

CALCIUM; CALCIUM INTRACELLULAR RELEASE; CELL BIOLOGY; ENDOPLASMIC RETICULUM (ER); MEMBRANE PROTEIN;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; BASE SEQUENCE; CALCIUM; CARRIER PROTEINS; CERCOPITHECUS AETHIOPS; COS CELLS; CYTOPLASM; DNA PRIMERS; DNA, COMPLEMENTARY; ENDOPLASMIC RETICULUM; HEK293 CELLS; HOMEOSTASIS; HUMANS; MEMBRANE PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84902125445     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.554071     Document Type: Article

References (44)

1. Voeltz, G. K., Rolls, M. M., and Rapoport, T. A. (2002) Structural organization of the endoplasmic reticulum. EMBO Rep. 3, 944-950
2. Levine, T., and Rabouille, C. (2005) Endoplasmic reticulum: one continuous network compartmentalized by extrinsic cues. Curr. Opin. Cell Biol. 17, 362-368
3. Carvalho, P., Goder, V., and Rapoport, T. A. (2006) Distinct ubiquitinligase complexes define convergent pathways for the degradation of ER proteins. Cell 126, 361-373
4. Mueller, B., Klemm, E. J., Spooner, E., Claessen, J. H., and Ploegh, H. L. (2008) SEL1L nucleates a protein complex required for dislocation of misfolded glycoproteins. Proc. Natl. Acad. Sci. U. S. A. 105, 12325-12330
5. Christianson, J. C., Shaler, T. A., Tyler, R. E., and Kopito, R. R. (2008) OS-9 and GRP94 deliver mutant α1-antitrypsin to the Hrd1-SEL1L ubiquitin ligase complex for ERAD. Nat. Cell Biol. 10, 272-282
6. Hebert, D. N., and Molinari, M. (2007) In and out of the ER: protein folding, quality control, degradation, and related human diseases. Physiol. Rev. 87, 1377-1408
7. English, A. R., Zurek, N., and Voeltz, G. K. (2009) Peripheral ER structure and function. Curr. Opin. Cell Biol. 21, 596-602
8. Lynes, E. M., Raturi, A., Shenkman, M., Ortiz Sandoval, C., Yap, M. C., Wu, J., Janowicz, A., Myhill, N., Benson, M. D., Campbell, R. E., Berthiaume, L. G., Lederkremer, G. Z., and Simmen, T. (2013) Palmitoylation is the switch that assigns calnexin to quality control or ER calcium signaling. J. Cell Sci. 126, 3893-3903
9. D'Andrea, L. D., and Regan, L. (2003) TPR proteins: the versatile helix. Trends Biochem. Sci. 28, 655-662
10. Das, A. K., Cohen, P. W., and Barford, D. (1998) The structure of the tetratricopeptide repeats of protein phosphatase 5: implications for TPRmediated protein-protein interactions. EMBO J. 17, 1192-1199
11. Scheufler, C., Brinker, A., Bourenkov, G., Pegoraro, S., Moroder, L., Bartunik, H., Hartl, F. U., and Moarefi, I. (2000) Structure of TPR domainpeptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell 101, 199-210
12. Chang, H. C., Nathan, D. F., and Lindquist, S. (1997) In vivo analysis of the Hsp90 cochaperone Sti1 (p60). Mol. Cell. Biol. 17, 318-325
13. Lazarus, M. B., Nam, Y., Jiang, J., Sliz, P., and Walker, S. (2011) Structure of human O-GlcNAc transferase and its complex with a peptide substrate. Nature 469, 564-567
14. Wu, Y., and Sha, B. (2006) Crystal structure of yeast mitochondrial outer membrane translocon member Tom70p. Nat. Struct. Mol. Biol. 13, 589-593
15. Rutkowski, D. T., Kang, S. W., Goodman, A. G., Garrison, J. L., Taunton, J., Katze, M. G., Kaufman, R. J., and Hegde, R. S. (2007) The role of p58IPK in protecting the stressed endoplasmic reticulum. Mol. Biol. Cell 18, 3681-3691
16. Petrova, K., Oyadomari, S., Hendershot, L. M., and Ron, D. (2008) Regulated association of misfolded endoplasmic reticulum lumenal proteins with p58/DNAJc3. EMBO J. 27, 2862-2872
17. UniProt Consortium (2013) Update on activities at the Universal Protein Resource (UniProt) in 2013. Nucleic Acids Res. 41, D43-D47
18. Karpenahalli, M. R., Lupas, A. N., and Söding, J. (2007) TPRpred: a tool for prediction of TPR-, PPR-, and SEL1-like repeats from protein sequences. BMC Bioinformatics 8, 2
19. Hessa, T., Meindl-Beinker, N. M., Bernsel, A., Kim, H., Sato, Y., Lerch-Bader, M., Nilsson, I., White, S. H., and von Heijne, G. (2007) Molecular code for transmembrane-helix recognition by the Sec61 translocon. Nature 450, 1026-1030
20. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. (1990) Basic local alignment search tool. J. Mol. Biol. 215, 403-410
21. Sievers, F., Wilm, A., Dineen, D., Gibson, T. J., Karplus, K., Li, W., Lopez, R., McWilliam, H., Remmert, M., Söding, J., Thompson, J. D., and Higgins, D. G. (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539
22. Svedine, S., Wang, T., Halaban, R., and Hebert, D. N. (2004) Carbohydrates act as sorting determinants in ER-associated degradation of tyrosinase. J. Cell Sci. 117, 2937-2949
23. Tamura, T., Cormier, J. H., and Hebert, D. N. (2011) Characterization of early EDEM1 protein maturation events and their functional implications. J. Biol. Chem. 286, 24906-24915
24. Pfaffl, M. W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45
25. Letunic, I., Doerks, T., and Bork, P. (2012) SMART7: recent updates to the protein domain annotation resource. Nucleic Acids Res. 40, D302-D305
26. Magliery, T. J., and Regan, L. (2005) Sequence variation in ligand binding sites in proteins. BMC Bioinformatics 6, 240
27. Bendtsen, J. D., Nielsen, H., von Heijne, G., and Brunak, S. (2004) Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340, 783-795
28. Ota, T., Suzuki, Y., Nishikawa, T., Otsuki, T., Sugiyama, T., Irie, R., Wakamatsu, A., Hayashi, K., Sato, H., Nagai, K., Kimura, K., Makita, H., Sekine, M., Obayashi, M., Nishi, T., Shibahara, T., Tanaka, T., Ishii, S., Yamamoto, J., Saito, K., Kawai, Y., Isono, Y., Nakamura, Y., Nagahari, K., Murakami, K., Yasuda, T., Iwayanagi, T., Wagatsuma, M., Shiratori, A., Sudo, H., Hosoiri, T., Kaku, Y., Kodaira, H., Kondo, H., Sugawara, M., Takahashi, M., Kanda, K., Yokoi, T., Furuya, T., Kikkawa, E., Omura, Y., Abe, K., Kamihara, K., Katsuta, N., Sato, K., Tanikawa, M., Yamazaki, M., Ninomiya, K., Ishibashi, T., Yamashita, H., Murakawa, K., Fujimori, K., Tanai, H., Kimata, M., Watanabe, M., Hiraoka, S., Chiba, Y., Ishida, S., Ono, Y., Takiguchi, S., Watanabe, S., Yosida, M., Hotuta, T., Kusano, J., Kanehori, K., Takahashi-Fujii, A., Hara, H., Tanase, T. O., Nomura, Y., Togiya, S., Komai, F., Hara, R., Takeuchi, K., Arita, M., Imose, N., Musashino, K., Yuuki, H., Oshima, A., Sasaki, N., Aotsuka, S., Yoshikawa, Y., Matsunawa, H., Ichihara, T., Shiohata, N., Sano, S., Moriya, S., Momiyama, H., Satoh, N., Takami, S., Terashima, Y., Suzuki, O., Nakagawa, S., Senoh, A., Mizoguchi, H., Goto, Y., Shimizu, F., Wakebe, H., Hishigaki, H., Watanabe, T., Sugiyama, A., Takemoto, M., Kawakami, B., Yamazaki, M., Watanabe, K., Kumagai, A., Itakura, S., Fukuzumi, Y., Fujimori, Y., Komiyama, M., Tashiro, H., Tanigami, A., Fujiwara, T., Ono, T., Yamada, K., Fujii, Y., Ozaki, K., Hirao, M., Ohmori, Y., Kawabata, A., Hikiji, T., Kobatake, N., Inagaki, H., Ikema, Y., Okamoto, S., Okitani, R., Kawakami, T., Noguchi, S., Itoh, T., Shigeta, K., Senba, T., Matsumura, K., Nakajima, Y., Mizuno, T., Morinaga, M., Sasaki, M., Togashi, T., Oyama, M., Hata, H., Watanabe, M., Komatsu, T., Mizushima-Sugano, J., Satoh, T., Shirai, Y., Takahashi, Y., Nakagawa, K., Okumura, K., Nagase, T., Nomura, N., Kikuchi, H., Masuho, Y., Yamashita, R., Nakai, K., Yada, T., Nakamura, Y., Ohara, O., Isogai, T., and Sugano, S. (2004) Complete sequencing and characterization of 21, 243 full-length human cDNAs. Nat. Genet. 36, 40-45
29. Gerhard, D. S., Wagner, L., Feingold, E. A., Shenmen, C. M., Grouse, L. H., Schuler, G., Klein, S. L., Old, S., Rasooly, R., Good, P., Guyer, M., Peck, A. M., Derge, J. G., Lipman, D., Collins, F. S., Jang, W., Sherry, S., Feolo, M., Misquitta, L., Lee, E., Rotmistrovsky, K., Greenhut, S. F., Schaefer, C. F., Buetow, K., Bonner, T. I., Haussler, D., Kent, J., Kiekhaus, M., Furey, T., Brent, M., Prange, C., Schreiber, K., Shapiro, N., Bhat, N. K., Hopkins, R. F., Hsie, F., Driscoll, T., Soares, M. B., Casavant, T. L., Scheetz, T. E., Brownstein, M. J., Usdin, T. B., Toshiyuki, S., Carninci, P., Piao, Y., Dudekula, D. B., Ko, M. S., Kawakami, K., Suzuki, Y., Sugano, S., Gruber, C. E., Smith, M. R., Simmons, B., Moore, T., Waterman, R., Johnson, S. L., Ruan, Y., Wei, C. L., Mathavan, S., Gunaratne, P. H., Wu, J., Garcia, A. M., Hulyk, S. W., Fuh, E., Yuan, Y., Sneed, A., Kowis, C., Hodgson, A., Muzny, D. M., McPherson, J., Gibbs, R. A., Fahey, J., Helton, E., Ketteman, M., Madan, A., Rodrigues, S., Sanchez, A., Whiting, M., Madari, A., Young, A. C., Wetherby, K. D., Granite, S. J., Kwong, P. N., Brinkley, C. P., Pearson, R. L., Bouffard, G. G., Blakesly, R. W., Green, E. D., Dickson, M. C., Rodriguez, A. C., Grimwood, J., Schmutz, J., Myers, R. M., Butterfield, Y. S., Griffith, M., Griffith, O. L., Krzywinski, M. I., Liao, N., Morin, R., Palmquist, D., Petrescu, A. S., Skalska, U., Smailus, D. E., Stott, J. M., Schnerch, A., Schein, J. E., Jones, S. J., Holt, R. A., Baross, A., Marra, M. A., Clifton, S., Makowski, K. A., Bosak, S., Malek, J., and M. G. C. Project Team (2004) The status, quality, and expansion of the NIH full-length cDNA project: the Mammalian Gene Collection (MGC). Genome Res. 14, 2121-2127
30. Sayers, E. W., Barrett, T., Benson, D. A., Bryant, S. H., Canese, K., Chetvernin, V., Church, D. M., DiCuccio, M., Edgar, R., Federhen, S., Feolo, M., Geer, L. Y., Helmberg, W., Kapustin, Y., Landsman, D., Lipman, D. J., Madden, T. L., Maglott, D. R., Miller, V., Mizrachi, I., Ostell, J., Pruitt, K. D., Schuler, G. D., Sequeira, E., Sherry, S. T., Shumway, M., Sirotkin, K., Souvorov, A., Starchenko, G., Tatusova, T. A., Wagner, L., Yaschenko, E., and Ye, J. (2009) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 37, D5-D15
31. Walter, P., and Ron, D. (2011) The unfolded protein response: from stress pathway to homeostatic regulation. Science 334, 1081-1086
32. Mostov, K. E., DeFoor, P., Fleischer, S., and Blobel, G. (1981) Co-translational membrane integration of calcium pump protein without signal sequence cleavage. Nature 292, 87-88
33. Giorda, K. M., Raghava, S., and Hebert, D. N. (2012) The simian virus 40 late viral protein VP4 disrupts the nuclear envelope for viral release. J. Virol. 86, 3180-3192
34. Pearse, B. R., and Hebert, D. N. (2010) Lectin chaperones help direct the maturation of glycoproteins in the endoplasmic reticulum. Biochim. Biophys. Acta 1803, 684-693
35. Luo, D., Broad, L. M., Bird, G. S., and Putney, J. W., Jr. (2001) Signaling pathways underlying muscarinic receptor-induced [Ca2]i oscillations in HEK293 cells. J. Biol. Chem. 276, 5613-5621
36. Wu, X., Babnigg, G., Zagranichnaya, T., and Villereal, M. L. (2002) The role of endogenous human Trp4 in regulating carbachol-induced calcium oscillations in HEK-293 cells. J. Biol. Chem. 277, 13597-13608
37. Brini, M., and Carafoli, E. (2009) Calcium pumps in health and disease. Physiol. Rev. 89, 1341-1378
38. Wu, C., Macleod, I., and Su, A. I. (2013) BioGPS and MyGene.info: organizing online, gene-centric information. Nucleic Acids Res. 41, D561-D565
39. Nilsson, I. M., and von Heijne, G. (1993) Determination of the distance between the oligosaccharyltransferase active site and the endoplasmic reticulum membrane. J. Biol. Chem. 268, 5798-5801
40. Zeytuni, N., and Zarivach, R. (2012) Structural and functional discussion of the tetra-trico-peptide repeat, a protein interaction module. Structure 20, 397-405
41. Swanton, E., High, S., and Woodman, P. (2003) Role of calnexin in the glycan-independent quality control of proteolipid protein. EMBO J. 22, 2948-2958
42. Roderick, H. L., Lechleiter, J. D., and Camacho, P. (2000) Cytosolic phosphorylation of calnexin controls intracellular Ca2 oscillations via an interaction with SERCA2b. J. Cell Biol. 149, 1235-1248
43. Simpson, J. C., Joggerst, B., Laketa, V., Verissimo, F., Cetin, C., Erfle, H., Bexiga, M. G., Singan, V. R., Hériché, J. K., Neumann, B., Mateos, A., Blake, J., Bechtel, S., Benes, V., Wiemann, S., Ellenberg, J., and Pepperkok, R. (2012) Genome-wide RNAi screening identifies human proteins with a regulatory function in the early secretory pathway. Nat Cell Biol. 14, 764-774
44. Landry, J. J., Pyl, P. T., Rausch, T., Zichner, T., Tekkedil, M. M., Stütz, A. M., Jauch, A., Aiyar, R. S., Pau, G., Delhomme, N., Gagneur, J., Korbel, J. O., Huber, W., and Steinmetz, L. M. (2013) The genomic and transcriptomic landscape of a HeLa cell line. G3 3, 1213-1224