Structural features of proinsulin C-peptide oligomeric and amyloid states

FEBS Journal

Volumn 277, Issue 18, 2010, Pages 3759-3768

  Lind, Jesper ^a   Lindahl, Emma ^b   Perálvarez Marín, Alex ^a   Holmlund, Anna ^b   Jörnvall, Hans ^b   Mäler, Lena ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

C peptide; diabetes; oligomer; spectroscopy; structure

Indexed keywords

AMYLOID; C PEPTIDE; DODECYL SULFATE SODIUM; INSULIN; MONOMER; OLIGOMER; THIOFLAVINE;

AMINO ACID SEQUENCE; ARTICLE; BETA SHEET; CIRCULAR DICHROISM; FLUORESCENCE ANALYSIS; INFRARED SPECTROSCOPY; LIGHT SCATTERING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OLIGOMERIZATION; PEPTIDE SYNTHESIS; PH; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; STATIC ELECTRICITY;

AMYLOID; BIOTINYLATION; C-PEPTIDE; CATIONS, DIVALENT; CIRCULAR DICHROISM; ELECTROPHORESIS, POLYACRYLAMIDE GEL; HUMANS; INSULIN; NEPHELOMETRY AND TURBIDIMETRY; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; OSMOLAR CONCENTRATION; PROTEIN STRUCTURE, SECONDARY; SOLUBILITY; SPECTROMETRY, FLUORESCENCE; SPECTROPHOTOMETRY, INFRARED; SURFACE-ACTIVE AGENTS;

EID: 77956320980     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2010.07777.x     Document Type: Article

References (40)

1. Steiner DF (1967) Evidence for a precursor in the biosynthesis of insulin. Trans N Y Acad Sci 30, 60 68.
2. Dodson G Steiner D (1998) The role of assembly in insulin's biosynthesis. Curr Opin Struct Biol 8, 189 194.
3. Rigler R, Pramanik A, Jonasson P, Kratz G, Jansson OT, Nygren På, Ståhl S, Ekberg K, Johansson BL Uhlen S (1999) Specific binding of proinsulin C-peptide to human cell membranes. Proc Natl Acad Sci USA 96, 13318 13323.
4. 2+ increases in human renal tubular cells. Cell Mol Life Sci 59, 1185 1189.
5. Kitamura T, Kimura K, Jung BD, Makondo K, Okamoto S, Canas X, Sakane N, Yoshida T Saito M (2001) Proinsulin C-peptide rapidly stimulates mitogen-activated protein kinases in Swiss 3T3 fibroblasts: requirement of protein kinase C, phosphoinositide 3-kinase and pertussis toxin-sensitive G-protein. Biochem J 355, 123.
6. Zhong Z, Davidescu A, Ehrén I, Ekberg K, Jörnvall H, Wahren J Chibalin AV (2005) C-peptide stimulates ERK1/2 and JNK MAP kinases via activation of protein kinase C in human renal tubular cells. Diabetologia 48, 187 197.
7. Henriksson M, Nordling E, Melles E, Shafqat J, Ståhlberg M, Ekberg K, Persson B, Bergman T, Wahren J Johansson J (2005) Separate functional features of proinsulin C-peptide. Cell Mol Life Sci 62, 1772 1778.
8. Wahren J, Ekberg K Jörnvall H (2007) C-peptide is a bioactive peptide. Diabetologia 50, 503 509.
9. Luppi P, Geng X, Cifarelli V, Drain P Trucco M (2009) C-peptide is internalised in human endothelial and vascular smooth muscle cells via early endosomes. Diabetologia 52, 2218 2228.
10. Lindahl E, Nyman U, Melles E, Sigmundsson K, Stahlberg M, Wahren J, Obrink B, Shafqat J, Joseph B Jornvall H (2007) Cellular internalization of proinsulin C-peptide. Cell Mol Life Sci 64, 479 486.
11. Lindahl E, Nyman U, Zaman F, Palmberg C, Cascante A, Shafqat J, Takigawa M, Savendahl L, Jornvall H Joseph B (2010) Proinsulin C-peptide regulates ribosomal RNA expression. J Biol Chem 285, 3462 3469.
12. Shafqat J, Melles E, Sigmundsson K, Johansson BL, Ekberg K, Alvelius G, Henriksson M, Johansson J, Wahren J Jornvall H (2006) Proinsulin C-peptide elicits disaggregation of insulin resulting in enhanced physiological insulin effects. Cell Mol Life Sci 63, 1805 1811.
13. Jornvall H, Lindahl E, Astorga-Wells J, Lind J, Holmlund A, Melles E, Alvelius G, Nerelius C, Maler L Johansson J (2010) Oligomerization and insulin interactions of proinsulin C-peptide: threefold relationships to properties of insulin. Biochem Biophys Res Commun 391, 1561 1566.
14. Henriksson M, Shafqat J, Liepinsh E, Tally M, Wahren J, Jornvall H Johansson J (2000) Unordered structured of proinsulin C-peptide in aqueous solution and in the presence of lipid vesicles. Cell Mol Life Sci 57, 337 342.
15. Munte CE, Vilela L, Kalbitzer HR Garratt RC (2005) Solution structure of human proinsulin C-peptide. FEBS J 272, 4284 4293.
16. Mares-Guia TR, Maigret B, Martins NF, Maia AL, Vilela L, Ramos CH, Neto LJ, Juliano MA, dos Mares-Guia ML Santoro MM (2006) Molecular dynamics and circular dichroism studies of human and rat C-peptides. J Mol Graph Model 25, 532 542.
17. Dobson CM (1999) Protein misfolding, evolution and disease. Trends Biochem Sci 24, 329 332.
18. Dobson CM (2003) Protein folding and misfolding. Nature 426, 884 890.
19. Waugh DF, Wilhelmson DF, Commerford SL Sackler ML (1953) Studies of the nucleation and growth reactions of selected types of insulin fibrils. J Am Chem Soc 75, 2592 2600.
20. Pekar AH Frank BH (1972) Conformation of proinsulin. A comparison of insulin and proinsulin self-association at neutral pH. Biochemistry 11, 4013 4016.
21. Frank BH Veros AJ (1968) Physical studies on proinsulin-association behavior and conformation in solution. Biochem Biophys Res Commun 32, 155 160.
22. Nielsen L, Frokjaer S, Carpenter JF Brange J (2001) Studies of the structure of insulin fibrils by Fourier transform infrared (FTIR) spectroscopy and electron microscopy. J Pharm Sci 90, 29 37.
23. Huang K, Dong J, Phillips NB, Carey PR Weiss MA (2005) Proinsulin is refractory to protein fibrillation: topological protection of a precursor protein from cross-beta assembly. J Biol Chem 280, 42345 42355.
24. Wahlström A, Hugonin L, Perálvarez-Marín A, Jarvet J Gräslund A (2008) Secondary structure conversions of Alzheimer's Abeta (1-40) peptide induced by membrane-mimicking detergents. FEBS J 275, 5117 5128.
25. Hugonin L, Barth A, Gräslund A Perálvarez-Marín A (2008) Secondary structure transitions and aggregation induced in dynorphin neuropeptides by the detergent sodium dodecyl sulfate. Biochim Biophys Acta 1778, 2580 2587.
26. Damberg P, Jarvet J Graslund A (2001) Micellar systems as solvents in peptide and protein structure determination. Methods Enzymol 339, 271 285.
27. Meyer JA, Froelich JM, Reid GE, Karunarathne WK Spence DM (2008) Metal-activated C-peptide facilitates glucose clearance and the release of a nitric oxide stimulus via the GLUT1 transporter. Diabetologia 51, 175 182.
28. Danielsson J, Jarvet J, Damberg P Graslund A (2002). Translational diffusion measured by PFG-NMR on full length and fragments of the Alzheimer Aβ (1-40) peptide. Determination of hydrodynamic radii of random coil peptides of varying length. Magn Reson Chem 40, S89 S97.
29. Khurana R, Coleman C, Ionescu-Zanetti C, Carter SA, Krishna V, Grover RK, Roy R Singh S (2005) Mechanism of thioflavin T binding to amyloid fibrils. J Struct Biol 151, 229 238.
30. Decatur SM (2006) Elucidation of residue-level structure and dynamics of polypeptides via isotope-edited infrared spectroscopy. Acc Chem Res 39, 169 175.
31. Nilsson MR Dobson CM (2003) In vitro characterization of lactoferrin aggregation and amyloid formation. Biochemistry 42, 375 382.
32. Byler DM Susi H (1986) Examination of the secondary structure of proteins by deconvolved FTIR spectra. Biopolymers 25, 469 487.
33. Peralvarez-Marin A, Barth A Graslund A (2008) Time-resolved infrared spectroscopy of pH-induced aggregation of the Alzheimer Abeta(1-28) peptide. J Mol Biol 379, 589 596.
34. Waugh DF (1944) The linkage of corpuscular protein molecules. I. A fibrous modification of insulin. Am Chem Soc 66, 663 663.
35. Waugh DF (1946) A fibrous modification of insulin. I. The heat precipitate of insulin. J Am Chem Soc 68, 247 250.
36. Nettleton EJ, Tito P, Sunde M, Bouchard M, Dobson CM Robinson CV (2000) Characterization of the oligomeric states of insulin in self-assembly and amyloid fibril formation by mass spectrometry. Biophys J 79, 1053 1065.
37. Brange J, Andersen L, Laursen ED, Meyn G Rasmussen E (1997) Toward understanding insulin fibrillation. J Pharm Sci 86, 517 525.
38. Hwang TL Shaka AJ (1995) Water suppression that works. Excitation sculpting using arbitrary waveforms and pulsed field gradients. J Magn Reson 112, 275 279.
39. Stejskal EO Tanner JE (1965) Spin diffusion measurements: spin echoes in the presence of a time dependent field gradient. J Chem Phys 42, 288 292.
40. Gibbs SJ Johnson CS (1991) A PFG NMR experiment for accurate diffusion and flow studies in the presence of Eddy currents. J Magn Reson 93, 395 402.