The pH-dependent client release from the collagen-specific chaperone HSP47 is triggered by a tandem histidine pair

Journal of Biological Chemistry

Volumn 291, Issue 24, 2016, Pages 12612-12626

  Oecal, Sinan ^a   Socher, Eileen ^b   Uthoff, Matthias ^a   Ernst, Corvin ^a   Zaucke, Frank ^a   Sticht, Heinrich ^b   Baumann, Ulrich ^a   Gebauer, Jan M ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BINS; CELL MEMBRANES; INTERFACE STATES;

BINDING AND RELEASE; COLLAGEN TRIPLE HELIX; ENDOPLASMIC RETICULUM; FOLDED CONFORMATION; GOLGI COMPARTMENTS; HEAT SHOCK PROTEIN; HISTIDINE RESIDUES; NUCLEOTIDE EXCHANGE;

COLLAGEN;

ARGININE; ASPARTIC ACID; HEAT SHOCK PROTEIN 47; HISTIDINE; CHAPERONE; COLLAGEN; PROTEIN BINDING;

ARTICLE; BINDING SITE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DISSOCIATION CONSTANT; INTERFEROMETRY; MOLECULAR DYNAMICS; MOLECULAR PHYLOGENY; MOLECULAR RECOGNITION; PH MEASUREMENT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN SECRETION; PROTON TRANSPORT; RESIDUE ANALYSIS; SITE DIRECTED MUTAGENESIS; AMINO ACID REPEAT; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; CIRCULAR DICHROISM; CLASSIFICATION; DOG; ENDOPLASMIC RETICULUM; GENETICS; GOLGI COMPLEX; KINETICS; METABOLISM; MOLECULAR MODEL; MUTATION; PH; PHYLOGENY; PROTEIN DENATURATION; PROTEIN DOMAIN; PROTEIN SECONDARY STRUCTURE; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANIMALS; CIRCULAR DICHROISM; COLLAGEN; DOGS; ENDOPLASMIC RETICULUM; GOLGI APPARATUS; HISTIDINE; HSP47 HEAT-SHOCK PROTEINS; HYDROGEN-ION CONCENTRATION; KINETICS; MODELS, MOLECULAR; MOLECULAR CHAPERONES; MUTATION; PHYLOGENY; PROTEIN BINDING; PROTEIN DENATURATION; PROTEIN DOMAINS; PROTEIN STRUCTURE, SECONDARY; REPETITIVE SEQUENCES, AMINO ACID; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84974625208     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.706069     Document Type: Article

References (36)

1. Kadler, K. E., Baldock, C., Bella, J., and Boot-Handford, R. P. (2007) Collagens at a glance. J. Cell Sci. 120, 1955-1958
2. Ricard-Blum, S. (2011) The collagen family. Cold Spring Harb. Perspect. Biol. 3, a004978
3. Shoulders, M. D., and Raines, R. T. (2009) Collagen structure and stability. Annu. Rev. Biochem. 78, 929-958
4. Koide, T., Nagata, K., Asada, S., Takahara, Y., Nishikawa, Y., and Kitagawa, K. (2005) in Collagen: Topics in Current Chemistry (Brinckmann, J., Notbohm, H., and Müller, P. K., eds) pp. 85-114, Springer, Berlin
5. Hirayoshi, K., Kudo, H., Takechi, H., Nakai, A., Iwamatsu, A., Yamada, K. M., and Nagata, K. (1991) HSP47: a tissue-specific, transformation-sensitive, collagen-binding heat shock protein of chicken embryo fibroblasts. Mol. Cell. Biol. 11, 4036-4044
6. Ishida, Y., and Nagata, K. (2011) Hsp47 as a collagen-specific molecular chaperone. Methods Enzymol. 499, 167-182
7. Ishida, Y., Kubota, H., Yamamoto, A., Kitamura, A., Bächinger, H. P., and Nagata, K. (2006) Type I collagen in Hsp47-null cells is aggregated in endoplasmic reticulum and deficient in N-propeptide processing and fibrillogenesis. Mol. Biol. Cell 17, 2346-2355
8. Nagai, N., Hosokawa, M., Itohara, S., Adachi, E., Matsushita, T., Hosokawa, N., and Nagata, K. (2000) Embryonic lethality of molecular chaperone hsp47 knockout mice is associated with defects in collagen biosynthesis. J. Cell Biol. 150, 1499-1506
9. Christiansen, H. E., Schwarze, U., Pyott, S. M., AlSwaid, A., Al Balwi, M., Alrasheed, S., Pepin, M. G., Weis, M. A., Eyre, D. R., and Byers, P. H. (2010) Homozygosity for a missense mutation in SERPINH1, which encodes the collagen chaperone protein HSP47, results in severe recessive osteogenesis imperfecta. Am. J. Hum. Genet. 86, 389-398
10. Drögemüller, C., Becker, D., Brunner, A., Haase, B., Kircher, P., Seeliger, F., Fehr, M., Baumann, U., Lindblad-Toh, K.,and Leeb, T. (2009) A missense mutation in the SERPINH1 gene in Dachshunds with osteogenesis imperfecta. PLoS Genet. 5, e1000579
11. Ono, T., Miyazaki, T., Ishida, Y., Uehata, M., and Nagata, K. (2012) Direct in vitro and in vivo evidence for interaction between Hsp47 protein and collagen triple helix. J. Biol. Chem. 287, 6810-6818
12. Paroutis, P., Touret, N., and Grinstein, S. (2004) The pH of the secretory pathway: measurement, determinants, and regulation. Physiology 19, 207-215
13. Wu, M. M., Llopis, J., Adams, S., McCaffery, J. M., Kulomaa, M. S., Machen, T. E., Moore, H. P., and Tsien, R. Y. (2000) Organelle pH studies using targeted avidin and fluorescein-biotin. Chem. Biol. 7, 197-209
14. Whisstock, J. C., Silverman, G. A., Bird, P. I., Bottomley, S. P., Kaiserman, D., Luke, C. J., Pak, S. C., Reichhart, J.-M., and Huntington, J. A. (2010) Serpins flex their muscle: II. structural insights into target peptidase recognition, polymerization, and transport functions. J. Biol. Chem. 285, 24307-24312
15. El-Thaher, T. S. H., Drake, A. F., Yokota, S., Nakai, A., Nagata, K., and Miller, A. D. (1996) The pH-dependent, ATP-independent interaction of collagen specific serpin/stress protein HSP47. Protein Pept. Lett. 3, 1-8
16. Thomson, C. A., and Ananthanarayanan, V. S. (2000) Structure-function studies on hsp47: pH-dependent inhibition of collagen fibril formation in vitro. Biochem. J. 349, 877-883
17. Widmer, C., Gebauer, J. M., Brunstein, E., Rosenbaum, S., Zaucke, F., Drögemüller, C., Leeb, T., and Baumann, U. (2012) Molecular basis for the action of the collagen-specific chaperone Hsp47/SERPINH1 and its structure-specific client recognition. Proc. Natl. Acad. Sci. U.S.A. 109, 13243-13247
18. Abdul-Wahab, M. F., Homma, T., Wright, M., Olerenshaw, D., Dafforn, T. R., Nagata, K., and Miller, A. D. (2013) The pH sensitivity of murine heat shock protein 47 (HSP47) binding to collagen is affected by mutations in the breach histidine cluster. J. Biol. Chem. 288, 4452-4461
19. Fiser, A., Do, R. K., and Sali, A. (2000) Modeling of loops in protein structures. Protein Sci. 9, 1753-1773
20. Fiser, A., and Sali, A. (2003) ModLoop: automated modeling of loops in protein structures. Bioinformatics 19, 2500-2501
21. Mongan, J., Case, D. A., and McCammon, J. A. (2004) Constant pH molecular dynamics in generalized Born implicit solvent. J. Comput. Chem. 25, 2038-2048
22. Case, D. A., Darden, T. A., Cheatham, T. E., Simmerling, C. L., Wang, J., Duke, R. E., Luo, R., Walker, R. C., Zhang, W., Merz, K. M., Roberts, B., Hayik, S., Roitberg, A., Seabra, G., Swails, J., et al. (2012) AMBER 12, University of California, San Francisco
23. Wang, J., Cieplak, P., and Kollman, P. A. (2000) How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules. J. Comput. Chem. 21, 1049-1074
24. Onufriev, A., Bashford, D., and Case, D. A. (2004) Exploring protein native states and large-scale conformational changes with a modified generalized Born model. Proteins 55, 383-394
25. Socher, E., and Sticht, H. (2016) Mimicking titration experiments with MD simulations: a protocol for the investigation of pH-dependent effects on proteins. Sci. Rep. 6, 22523
26. Zheng, L., Baumann, U., and Reymond, J. L. (2004) An efficient one-step site-directed and site-saturation mutagenesis protocol. Nucleic Acids Res. 32, e115
27. Du, C., Wang, M., Liu, J., Pan, M., Cai, Y., and Yao, J. (2008) Improvement of thermostability of recombinant collagen-like protein by incorporating a foldon sequence. Appl. Microbiol. Biotechnol. 79, 195-202
28. McIlvaine, T. C. (1921) A buffer solution for colorimetric comparison. J. Biol. Chem. 49, 183-186
29. Findlay, J. W., and Dillard, R. F. (2007) Appropriate calibration curve fitting in ligand binding assays. AAPS J. 9, E260-E267
30. Sreerama, N., and Woody, R. W. (2000) Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal. Biochem. 287, 252-260
31. Provencher, S. W., and Glöckner, J. (1981) Estimation of globular protein secondary structure from circular dichroism. Biochemistry 20, 33-37
32. Macdonald, J. R., and Bächinger, H. P. (2001) HSP47 binds cooperatively to triple helical type I collagen but has little effect on the thermal stability or rate of refolding. J. Biol. Chem. 276, 25399-25403
33. a of histidine side-chains correlates with burial within proteins. Proteins 49, 1-6
34. Gebauer, J. M., Kobbe, B., Paulsson, M., and Wagener, R. (2016) Structure, evolution and expression of collagen XXVIII: lessons from the zebrafish. Matrix Biol. 49, 106-119
35. Meyer, A., and Schartl, M. (1999) Gene and genome duplications in vertebrates: the one-to-four (-to-eight in fish) rule and the evolution of novel gene functions. Curr. Opin. Cell Biol. 11, 699-704
36. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF Chimera: a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612