Proline in transmembrane domain of type II protein DPP-IV governs its translocation behavior through endoplasmic reticulum

Biochemistry

Volumn 50, Issue 37, 2011, Pages 7909-7918

  Chung, Kuei Min ^a   Huang, Chih Hsiang ^a   Cheng, Jai Hong ^a   Tsai, Cheng Han ^a   Suen, Ching Shu ^b   Hwang, Ming Jing ^b   Chen, Xin ^a  

^a NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^b INSTITUTE OF BIOMEDICAL SCIENCES   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CONFORMATIONAL CHANGE; DIPEPTIDYL PEPTIDASE; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM MEMBRANES; HYDROPHOBIC RESIDUES; IN-VITRO; MAMMALIAN CELLS; MEMBRANE PROTEASE; MEMBRANE PROTEINS; N-TERMINALS; PROLINE RESIDUES; PROTEIN TRANSLOCATION; RELATIVE POSITIONS; SIGNAL SEQUENCE; TRANS-MEMBRANE DOMAINS; TRANSMEMBRANE DOMAIN; TYPE II;

ACTIVATION ANALYSIS; BIOLOGICAL MEMBRANES; DEFECTS; HYDROPHOBICITY; INTEGRATION; MAMMALS; MEMBRANES; PROTEINS;

AMINO ACIDS;

AMINO ACID; DIPEPTIDYL PEPTIDASE IV; MEMBRANE PROTEIN; MUTANT PROTEIN; PROLINE;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; FEMALE; HYDROPHOBICITY; IN VITRO STUDY; MAMMAL CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN TARGETING; PROTEIN TRANSPORT;

AMINO ACID SEQUENCE; ANIMALS; CHO CELLS; CRICETINAE; CRICETULUS; DIPEPTIDYL PEPTIDASE 4; DOGS; ENDOPLASMIC RETICULUM; HEK293 CELLS; HUMANS; MOLECULAR SEQUENCE DATA; PROLINE; PROTEIN TRANSPORT;

MAMMALIA;

EID: 80052746513     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi200605h     Document Type: Article

References (43)

1. Rapoport, T. A. (2007) Protein translocation across the eukaryotic endoplasmic reticulum and bacterial plasma membranes. Nature 450, 663-669. (Pubitemid 350207698)
2. Osborne, A. R., Rapoport, T. A., and van den Berg, B. (2005) Protein translocation by the Sec61/SecY channel. Annu. Rev. Cell Dev. Biol. 21, 529-550. (Pubitemid 41740645)
3. Cannon, K. S., Or, E., Clemons, W. M. Jr., Shibata, Y., and Rapoport, T. A. (2005) Disulfide bridge formation between SecY and a translocating polypeptide localizes the translocation pore to the center of SecY. J. Cell Biol. 169, 219-225. (Pubitemid 40656559)
4. Heinrich, S. U., Mothes, W., Brunner, J., and Rapoport, T. A. (2000) The Sec61p complex mediates the integration of a membrane protein by allowing lipid partitioning of the transmembrane domain. Cell 102, 233-244.
5. Mothes, W., Heinrich, S. U., Graf, R., Nilsson, I., von Heijne, G., Brunner, J., and Rapoport, T. A. (1997) Molecular mechanism of membrane protein integration into the endoplasmic reticulum. Cell 89, 523-533. (Pubitemid 27511763)
6. Plath, K., Mothes, W., Wilkinson, B. M., Stirling, C. J., and Rapoport, T. A. (1998) Signal sequence recognition in posttranslational protein transport across the yeast ER membrane. Cell 94, 795- 807. (Pubitemid 28436011)
7. Wimley, W. C., Creamer, T. P., and White, S. H. (1996) Solvation energies of amino acid side chains and backbone in a family of host-guest pentapeptides. Biochemistry 35, 5109-5124.
8. Wimley, W. C., Gawrisch, K., Creamer, T. P., and White, S. H. (1996) Direct measurement of salt-bridge solvation energies using a peptide model system: implications for protein stability. Proc. Natl. Acad. Sci. U. S. A. 93, 2985-2990. (Pubitemid 26114350)
9. Wimley, W. C., and White, S. H. (1996) Experimentally determined hydrophobicity scale for proteins at membrane interfaces. Nat. Struct. Biol. 3, 842-848. (Pubitemid 26330634)
10. Jayasinghe, S., Hristova, K., and White, S. H. (2001) Energetics, stability, and prediction of transmembrane helices. J. Mol. Biol. 312, 927-934. (Pubitemid 32980315)
11. Hessa, T., Kim, H., Bihlmaier, K., Lundin, C., Boekel, J., Andersson, H., Nilsson, I., White, S. H., and von Heijne, G. (2005) Recognition of transmembrane helices by the endoplasmic reticulum translocon. Nature 433, 377-381. (Pubitemid 40203311)
12. 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. (Pubitemid 350273612)
13. White, S. H., and von Heijne, G. (2008) How translocons select transmembrane helices. Annu. Rev. Biophys. 37, 23-42.
14. Brandl, C. J., and Deber, C. M. (1986) Hypothesis about the function of membrane-buried proline residues in transport proteins. Proc. Natl. Acad. Sci. U. S. A. 83, 917-921. (Pubitemid 16086388)
15. Senes, A., Engel, D. E., and DeGrado, W. F. (2004) Folding of helical membrane proteins: the role of polar, GxxxG-like and proline motifs. Curr. Opin. Struct. Biol. 14, 465-479. (Pubitemid 39094354)
16. Presta, L. G., and Rose, G. D. (1988) Helix signals in proteins. Science 240, 1632-1641.
17. Richardson, J. S., and Richardson, D. C. (1988) Amino acid preferences for specific locations at the ends of alpha helices. Science 240, 1648-1652.
18. Lundin, C., Kim, H., Nilsson, I., White, S. H., and von Heijne, G. (2008) Molecular code for protein insertion in the endoplasmic reticulum membrane is similar for Nin-Cout and Nout-Cin transmembrane helices. Proc. Natl. Acad. Sci. U. S. A., .
19. Yohannan, S., Yang, D., Faham, S., Boulting, G., Whitelegge, J., and Bowie, J. U. (2004) Proline substitutions are not easily accommodated in a membrane protein. J. Mol. Biol. 341, 1-6. (Pubitemid 39090629)
20. Deacon, C. F., Ahren, B., and Holst, J. J. (2004) Inhibitors of dipeptidyl peptidase IV: a novel approach for the prevention and treatment of Type 2 diabetes. Expert Opin. Investig. Drugs 13, 1091- 1102. (Pubitemid 39242733)
21. Hong, W. J., and Doyle, D. (1988) Membrane orientation of rat gp110 as studied by in vitro translation. J. Biol. Chem. 263, 16892- 16898. (Pubitemid 18268872)
22. Low, S. H., Tang, B. L., Wong, S. H., and Hong, W. (1994) Golgi retardation in Madin-Darby canine kidney and Chinese hamster ovary cells of a transmembrane chimera of two surface proteins. J. Biol. Chem. 269, 1985-1994. (Pubitemid 24035404)
23. Munro, S. (1991) Sequences within and adjacent to the transmembrane segment of alpha-2,6-sialyltransferase specify Golgi retention. EMBO J. 10, 3577-3588. (Pubitemid 21905383)
24. Hong, W. J., and Doyle, D. (1990) Molecular dissection of the NH2-terminal signal/anchor sequence of rat dipeptidyl peptidase IV. J. Cell Biol. 111, 323-328.
25. Chien, C. H., Huang, L. H., Chou, C. Y., Chen, Y. S., Han, Y. S., Chang, G. G., Liang, P. H., and Chen, X. (2004) One site mutation disrupts dimer formation in human DPP-IV proteins. J. Biol. Chem. 279, 52338-52345. (Pubitemid 39656609)
26. Chien, C. H., Tsai, C. H., Lin, C. H., Chou, C. Y., and Chen, X. (2006) Identification of hydrophobic residues critical for DPP-IV dimerization. Biochemistry 45, 7006-7012. (Pubitemid 43877389)
27. Conarello, S. L. (2003) Mice lacking dipeptidyl peptidase IV are protected against obesity and insulin resistance. Proc. Natl. Acad. Sci. U. S. A. 100, 6825-6830. (Pubitemid 36666664)
28. Chung, K.-M., Cheng, J.-H., Suen, C.-S., Huang, C.-H., Tsai, C.-H., Huang, L.-H., Chen, Y.-R., Wang, A. H. J., Jiaang, W.-T., Hwang, M.-J., and Chen, X. (2010) The dimeric transmembrane domain of prolyl dipeptidase DPP-IV contributes to its quaternary structure and enzymatic activities. Protein Sci. 19, 1627-1638.
29. Pacheco, R. (2005) CD26, adenosine deaminase, and adenosine receptors mediate costimulatory signals in the immunological synapse. Proc. Natl. Acad. Sci. U. S. A. 102, 9583-9588. (Pubitemid 40981724)
30. Dong, R. P., and Morimoto, C. (1996) Role of CD26 for CD4 memory T cell function and activation. Hum. Cell 9, 153-162.
31. Lee, H. J., Chen, Y. S., Chou, C. Y., Chien, C. H., Lin, C. H., Chang, G. G., and Chen, X. (2006) Investigation of the Dimer Interface and Substrate Specificity of Prolyl Dipeptidase DPP8. J. Biol. Chem. 281, 38653-38662. (Pubitemid 46041990)
32. Chen, X., Wen, S., Fukuda, M. N., Gavva, N. R., Hsu, D., Akama, T. O., Yang-Feng, T., and Shen, C. K. (2001) Human ITCH is a coregulator of the hematopoietic transcription factor NF-E2. Genomics 73, 238-241. (Pubitemid 32411361)
33. Hurley, W. L., and Finkelstein, E. (1990) Identification of leukocyte surface proteins. Methods Enzymol. 184, 429-433. (Pubitemid 20219774)
34. Bourd-Boittin, K., Le Pabic, H., Bonnier, D., L'Helgoualc'h, A., and Theret, N. (2008) RACK1, a new ADAM12 interacting protein. Contribution to liver fibrogenesis. J. Biol. Chem. 283, 26000-26009.
35. Fazio, S., Horie, Y., Weisgraber, K. H., Havekes, L. M., and Rall, S. C. Jr. (1993) Preferential association of apolipoprotein E Leiden with very low density lipoproteins of human plasma. J. Lipid Res. 34, 447-453. (Pubitemid 23095371)
36. Tang, H. K., Tang, H. Y., Hsu, S. C., Chu, Y. R., Chien, C. H., Shu, C. H., and Chen, X. (2009) Biochemical properties and expression profile of human prolyl dipeptidase DPP9. Arch. Biochem. Biophys. 485, 120-127.
37. He, M., and Taussig, M. J. (1997) Antibody-ribosome-mRNA (ARM) complexes as efficient selection particles for in vitro display and evolution of antibody combining sites. Nucleic Acids Res. 25, 5132-5134. (Pubitemid 28022282)
38. Ballesteros, J. A., Deupi, X., Olivella, M., Haaksma, E. E., and Pardo, L. (2000) Serine and threonine residues bend alpha-helices in the chi(1) = g(-) conformation. Biophys. J. 79, 2754-2760.
39. Deupi, X., Olivella, M., Govaerts, C., Ballesteros, J. A., Campillo, M., and Pardo, L. (2004) Ser and Thr residues modulate the conformation of pro-kinked transmembrane alpha-helices. Biophys. J. 86, 105-115. (Pubitemid 38067440)
40. Senes, A., Engel, D. E., and DeGrado, W. F. (2004) Folding of helical membrane proteins: the role of polar, GxxxG-like and proline motifs. Curr. Opin. Struct. Biol. 14, 465-479. (Pubitemid 39094354)
41. Cordes, F. S., Bright, J. N., and Sansom, M. S. P. (2002) Proline-induced Distortions of Transmembrane Helices. J. Mol. Biol. 323, 951-960. (Pubitemid 35341067)
42. Nilsson, I., Saaf, A., Whitley, P., Gafvelin, G., Waller, C., and von Heijne, G. (1998) Proline-induced disruption of a transmembrane alpha-helix in its natural environment. J. Mol. Biol. 284, 1165-1175. (Pubitemid 28558564)
43. Nilsson, I., and von Heijne, G. (1998) Breaking the camel's back: proline-induced turns in a model transmembrane helix. J. Mol. Biol. 284, 1185-1189. (Pubitemid 28558566)