Structure of human insulin-like peptide 5 and characterization of conserved hydrogen bonds and electrostatic interactions within the relaxin framework

Biochemical Journal

Volumn 419, Issue 3, 2009, Pages 619-627

  Haugaard Jönsson, Linda M ^a   Hossain, Mohammed Akhter ^b   Daly, Norelle L ^b   Craik, David J ^b   Wade, John D ^b,c   Rosengren, K Johan ^a  

^a LINNAEUS UNIVERSITY   (Sweden)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Insulin like peptide 5 (INSL5); NMR; Peptide hormone; Relaxin; Relaxin family peptide receptor (RXFP); Solution state structure

Indexed keywords

INSULIN-LIKE PEPTIDE 5 (INSL5); NMR; PEPTIDE HORMONE; RELAXIN; RELAXIN FAMILY PEPTIDE RECEPTOR (RXFP);

BINDING ENERGY; BINDING SITES; ELECTROSTATICS; HYDROGEN; HYDROGEN BONDS; INSULIN; NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PEPTIDES;

AMINES;

ARGININE; RELAXIN; RELAXIN 3; RELAXIN 5; SYNTHETIC PEPTIDE; TRYPTOPHAN; UNCLASSIFIED DRUG; G PROTEIN COUPLED RECEPTOR; INSULIN; LEYDIG INSULIN LIKE PROTEIN; LEYDIG INSULIN-LIKE PROTEIN; PEPTIDE; PROTEIN; RECEPTOR; RXFP3 PROTEIN, HUMAN; RXFP4 PROTEIN, HUMAN;

ARTICLE; BETA CHAIN; BINDING SITE; ELECTROSTATIC PROTEIN INTERACTION; HUMAN; HYDROGEN BOND; HYDROPHOBICITY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PEPTIDE SYNTHESIS; PH; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; RECEPTOR BINDING; TEMPERATURE; TITRIMETRY; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; MOLECULAR GENETICS; PROTEIN BINDING; PROTEIN SECONDARY STRUCTURE; SOLUTION AND SOLUBILITY; STATIC ELECTRICITY; SYNTHESIS;

AMINO ACID SEQUENCE; HUMANS; HYDROGEN BONDING; HYDROGEN-ION CONCENTRATION; INSULIN; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEINS; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, PEPTIDE; RELAXIN; SOLUTIONS; STATIC ELECTRICITY; TEMPERATURE; TITRIMETRY;

EID: 64849117347     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20082353     Document Type: Article

References (39)

1. Hudson, P., Haley, J., John, M., Cronk, M., Crawford, R., Haralambidis, J., Tregear, G., Shine, J. and Niall, H. (1983) Structure of a genomic clone encoding biologically active human relaxin. Nature 301, 628-631
2. Hudson, P., John, M., Crawford, R., Haralambidis, J., Scanlon, D., Gorman, J., Tregear, G., Shine, J. and Niall, H. (1984) Relaxin gene expression in human ovaries and the predicted structure of a human preprorelaxin by analysis of cDNA clones. EMBO J. 3, 2333-2339
3. Bathgate, R. A., Samuel, C. S., Burazin, T. C., Layfield, S., Claasz, A. A., Reytomas, I. G., Dawson, N. F., Zhao, C., Bond, C., Summers, R. J. et al. (2002) Human relaxin gene 3 (H3) and the equivalent mouse relaxin (M3) gene: novel members of the relaxin peptide family. J. Biol. Chem. 277, 1148-1157
4. Burkhardt, E., Adham, I. M., Hobohm, U., Murphy, D., Sander, C. and Engel, W. (1994) A human cDNA coding for the Leydig insulin-like peptide (Ley I-L). Hum. Genet. 94, 91-94
5. Chassin, D., Laurent, A., Janneau, J. L., Berger, R. and Bellet, D. (1995) Cloning of a new member of the insulin gene superfamily (INSL4) expressed in human placenta. Genomics 29, 465-470
6. Conklin, D., Lofton-Day, C. E., Haldeman, B. A., Ching, A., Whitmore, T. E., Lok, S. and Jaspers, S. (1999) Identification of INSL5, a new member of the insulin superfamily. Genomics 60, 50-56
7. Lok, S., Johnston, D. S., Conklin, D., Lofton-Day, C. E., Adams, R. L., Jelmberg, A. C., Whitmore, T. E., Schrader, S., Griswold, M. D. and Jaspers, S. R. (2000) Identification of INSL6, a new member of the insulin family that is expressed in the testis of the human and rat. Biol. Reprod. 62, 1593-1599
8. Schwabe, C. and McDonald, J. K. (1977) Relaxin: a disulfide homolog of insulin. Science 197, 914-915
9. Liu, C., Kuei, C., Sutton, S., Chen, J., Bonaventure, P., Wu, J., Nepomuceno, D., Kamme, F., Tran, D. T., Zhu, J. et al. (2005) INSL5 is a high affinity specific agonist for GPCR142 (GPR100). J. Biol. Chem. 280, 292-300
10. Hsu, S. Y. (1999) Cloning of two novel mammalian paralogs of relaxin/ insulin family proteins and their expression in testis and kidney. Mol. Endocrinol. 13, 2163-2174
11. Dun, S. L., Brailoiu, E., Wang, Y., Brailoiu, G. C., Liu-Chen, L. Y., Yang, J., Chang, J. K. and Dun, N. J. (2006) Insulin-like peptide 5: expression in the mouse brain and mobilization of calcium. Endocrinology 147, 3243-3248
12. Hossain, M. A., Bathgate, R. A., Kong, C. K., Shabanpoor, F., Zhang, S., Haugaard-Jönsson, L. M., Rosengren, K. J., Tregear, G. W. and Wade, J. D. (2008) Synthesis, conformation, and activity of human insulin-like peptide 5 (INSL5). Chembiochem 9, 1816-1822
13. Hsu, S. Y., Nakabayashi, K., Nishi, S., Kumagai, J., Kudo, M., Sherwood, O. D. and Hsueh, A. J. (2002) Activation of orphan receptors by the hormone relaxin. Science 295, 671-674
14. Kumagai, J., Hsu, S. Y., Matsumi, H., Roh, J. S., Fu, P., Wade, J. D., Bathgate, R. A. and Hsueh, A. J. (2002) INSL3/Leydig insulin-like peptide activates the LGR8 receptor important in testis descent. J. Biol. Chem. 277, 31283-31286
15. Liu, C., Eriste, E., Sutton, S., Chen, J., Roland, B., Kuei, C., Farmer, N., Jornvall, H., Sillard, R. and Lovenberg, T. W. (2003) Identification of relaxin-3/INSL7 as an endogenous ligand for the orphan G-protein-coupled receptor GPCR135. J. Biol. Chem. 278, 50754-50764
16. Wilkinson, T. N., Speed, T. P., Tregear, G. W. and Bathgate, R. A. (2005) Evolution of the relaxin-like peptide family. BMC Evol. Biol. 5, 14
17. Sudo, S., Kumagai, J., Nishi, S., Layfield, S., Ferraro, T., Bathgate, R. A. and Hsueh, A. J. (2003) H3 relaxin is a specific ligand for LGR7 and activates the receptor by interacting with both the ectodomain and the exoloop 2. J. Biol. Chem. 278, 7855-7862
18. Liu, C., Chen, J., Sutton, S., Roland, B., Kuei, C., Farmer, N., Sillard, R. and Lovenberg, T. W. (2003) Identification of relaxin-3/ INSL7 as a ligand for GPCR142. J. Biol. Chem. 278, 50765-50770
19. Eigenbrot, C., Randal, M., Quan, C., Burnier, J., O'Connell, L., Rinderknecht, E. and Kossiakoff, A. A. (1991) X-ray structure of human relaxin at 1.5Å: comparison to insulin and implications for receptor binding determinants. J. Mol. Biol. 221, 15-21
20. Rosengren, K. J., Lin, F., Bathgate, R. A., Tregear, G. W., Daly, N. L., Wade, J. D. and Craik, D. J. (2006) Solution structure and novel insights into the determinants of the receptor specificity of human relaxin-3. J. Biol. Chem. 281, 5845-5851
21. Rosengren, K. J., Zhang, S., Lin, F., Daly, N. L., Scott, D. J., Hughes, R. A., Bathgate, R. A., Craik, D. J. and Wade, J. D. (2006) Solution structure and characterization of the LGR8 receptor binding surface of insulin-like peptide 3. J. Biol. Chem. 281, 28287-28295
22. Haugaard-Jönsson, L. M., Hossain, M. A., Daly, N. L., Bathgate, R. A., Wade, J. D., Craik, D. J. and Rosengren, K. J. (2008) Structure of the R3/I5 chimeric relaxin peptide, a selective GPCR135 and GPCR142 agonist. J. Biol. Chem. 283, 23811-23818
23. Hossain, M. A., Rosengren, K. J., Haugaard-Jönsson, L. M., Zhang, S., Layfield, S., Ferraro, T., Daly, N. L., Tregear, G. W., Wade, J. D. and Bathgate, R. A. (2008) The A-chain of human relaxin family peptides has distinct roles in the binding and activation of the different relaxin family peptide receptors. J. Biol. Chem. 283, 17287-17297
24. Park, J. I., Semyonov, J., Yi, W., Chang, C. L. and Hsu, S. Y. (2008) Regulation of receptor signaling by relaxin A chain motifs: derivation of pan-specific and LGR7-specific human relaxin analogs. J. Biol. Chem. 283, 32099-32109
25. Büllesbach, E. E., Yang, S. and Schwabe, C. (1992) The receptor-binding site of human relaxin II. A dual prong-binding mechanism. J. Biol. Chem. 267, 22957-22960
26. Kuei, C., Sutton, S., Bonaventure, P., Pudiak, C., Shelton, J., Zhu, J., Nepomuceno, D., Wu, J., Chen, J., Kamme, F. et al. (2007) R3(B23-27)R/I5 chimeric peptide, a selective antagonist for GPCR135 and GPCR142 over relaxin receptor LGR7: in vitro and in vivo characterization. J. Biol. Chem. 282, 25425-25435
27. Keller, R. L. J. (2004) The Computer Aided Resonance Assignment Tutorial, CANTINA Verlag, Goldau, Switzerland
28. uthrich, K. (1997) Torsion angle dynamics for NMR structure calculation with the new program DYANA. J. Mol. Biol. 273, 283-298
29. Wagner, G. (1990) NMR investigations of protein-structure. Prog. Nucl. Magn. Reson. Spectrosc. 22, 101-139
30. Brunger, A. T. (2007) Version 1.2 of the Crystallography and NMR system. Nat. Protoc. 2, 2728-2733
31. Nederveen, A. J., Doreleijers, J. F., Vranken, W., Miller, Z., Spronk, C. A., Nabuurs, S. B., Guntert, P., Livny, M., Markley, J. L., Nilges, M. et al. (2005) RECOORD: a recalculated coordinate database of 500+ proteins from the PDB using restraints from the BioMagResBank. Proteins 59, 662-672
32. Laskowski, R. A., Rullmannn, J. A., MacArthur, M. W., Kaptein, R. and Thornton, J. M. (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 8, 477-486
33. uthrich, K. (1996) MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graphics 14, 51-55
34. Wüthrich, K. (1986) NMR of proteins and nucleic acids. John Wiley and Sons, New York
35. Cierpicki, T. and Otlewski, J. (2001) Amide proton temperature coefficients as hydrogen bond indicators in proteins. J. Biomol. NMR 21, 249-261
36. Andersen, N. H., Neidigh, J. W., Harris, S. M., Lee, G. M., Liu, Z. H. and Tong, H. (1997) Extracting information from the temperature gradients of polypeptide NH chemical shifts. 1. The importance of conformational averaging. J. Am. Chem. Soc. 119, 8547-8561
37. Matthew, J. B., Gurd, F. R. N., Garciamoreno, E. B., Flanagan, M. A., March, K. L. and Shire, S. J. (1985) Ph-dependent processes in proteins. CRC Crit. Rev. Biochem. 18, 91-197
38. Jorgensen, A. M. M., Olsen, H. B., Balschmidt, P. and Led, J. J. (1996) Solution structure of the superactive monomeric Des-[Phe(BP5)] human insulin mutant: elucidation of the structural basis for the monomerization of Des-[Phe(B25)] insulin and the dimerization of native insulin. J. Mol. Biol. 257, 684-699
39. Keller, D., Clausen, R., Josefsen, K. and Led, J. J. (2001) Flexibility and bioactivity of insulin: an NMR investigation of the solution structure and folding of an unusually flexible human insulin mutant with increased biological activity. Biochemistry 40, 10732-10740