The structure, molecular interactions and bioactivities of proinsulin C-peptide correlate with a tripartite molecule

Biomolecular Concepts

Volumn 5, Issue 2, 2014, Pages 109-118

  Landreh, Michael ^a   Johansson, Jan ^a,b   Wahren, John ^a   Jörnvall, Hans ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

Author keywords

amyloid formation; diabetes; membrane binding; protein folding; receptor interactions

Indexed keywords

C PEPTIDE; G PROTEIN COUPLED RECEPTOR; INSULIN; PROINSULIN;

AMINO ACID SEQUENCE; ANIMAL; BINDING SITE; CHEMISTRY; DIABETES MELLITUS; HUMAN; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; C-PEPTIDE; CONSERVED SEQUENCE; DIABETES MELLITUS; HUMANS; INSULIN; MOLECULAR SEQUENCE DATA; PROINSULIN; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, G-PROTEIN-COUPLED;

EID: 84900449998     PISSN: 18685021     EISSN: 1868503X     Source Type: Journal    
DOI: 10.1515/bmc-2014-0005     Document Type: Review

References (64)

1. Steiner DF, Cunningham D, Spigelman L, Aten B. Insulin biosynthesis: evidence for a precursor. Science 1967; 157: 697-700.
2. Varandani PT, Shroyer LA. Degradation of proinsulin and isolated C-peptide by rat kidney neutral metallo-endopeptidase. Biochim Biophys Acta 1981; 661: 182-90.
3. Melles E, Jörnvall H, Tryggvason S, Danielsson KG, Ekberg K, Tryggvason K, Wahren J, Bergman T. Degradation of proinsulin C-peptide in kidney and placenta extracts by a specific endoprotease activity. Cell Mol Life Sci 2004; 61: 2979-82.
4. 2 incorporation. Cell Mol Life Sci 2003; 60: 1019-25.
5. Oran PE, Jarvis JW, Borges CR, Nelson RW. C-peptide microheterogeneity in type 2 diabetes populations. Proteom Clin Appl 2010; 4: 106-11.
6. Henriksson M, Nordling E, Melles E, Shafqat J, Ståhlberg M, Ekberg K, Persson B, Bergman T, Wahren J, Johansson J, Jörnvall H. Separate functional features of proinsulin C-peptide. Cell Mol Life Sci 2005; 62: 1772-8.
7. Kwok SC, Chan SJ, Steiner DF. Cloning and nucleotide sequence analysis of the dog insulin gene. Coded amino acid sequence of canine preproinsulin predicts an additional C-peptide fragment. J Biol Chem 1983; 258: 2357-63.
8. Nerelius C, Lindahl E, Landreh M, Jörnvall H. Peptide interactions of proinsulin C-peptide. New York: Springer, 2012.
9. Xie L, Tsou CL. Comparison of secondary structures of insulin and proinsulin by FTIR. J Prot Chem 1993; 12: 483-7.
10. Steiner DF. Cocrystallization of proinsulin and insulin. Nature 1973; 243: 528-30.
11. Yang Y, Hua QX, Liu J, Shimizu EH, Choquette MH, Mackin RB, Weiss MA. Solution structure of proinsulin: connecting domain flexibility and prohormone processing. J Biol Chem 2010; 285: 7847-51.
12. Ido Y, Vindigni A, Chang K, Stramm L, Chance R, Heath WF, DiMarchi RD, Di Cera E, Williamson JR. Prevention of vascular and neural dysfunction in diabetic rats by C-peptide. Science 1997; 277: 563-6.
13. Mares-Guia TR, Maigret B, Martins NF, Maia AL, Vilela L, Ramos CH, Neto LJ, Juliano MA, dos Mares-Guia ML, Santoro MM. Molecular dynamics and circular dichroism studies of human and rat C-peptides. J Molec Graph Model 2006; 25: 532-42.
14. Munte CE, Vilela L, Kalbitzer HR, Garratt RC. Solution structure of human proinsulin C-peptide. FEBS J 2005; 272: 4284-93.
15. Unnerståle S, Mäler L. pH-Dependent interaction between C-peptide and phospholipid bicelles. J Biophys 2012; 2012: 185-907.
16. Chen LM, Yang XW, Tang JG. Acidic residues on the N-terminus of proinsulin C-peptide are important for the folding of insulin precursor. J Biochem 2002; 131: 855-9.
17. Qiao ZS, Min CY, Hua QX, Weiss MA, Feng YM. In vitro refolding of human proinsulin. Kinetic intermediates, putative disulfideforming pathway folding initiation site, and potential role of C-peptide in folding process. J Biol Chem 2003; 278: 17800-9.
18. Min CY, Qiao ZS, Feng YM. Unfolding of human proinsulin. Intermediates and possible role of its C-peptide in folding/unfolding. Eur J Biochem 2004; 271: 1737-47.
19. Wang S, Wei W, Zheng Y, Hou J, Dou Y, Zhang S, Luo X, Cai X. The role of insulin C-peptide in the coevolution analyses of the insulin signaling pathway: a hint for its functions. Plos ONE 2012; 7: e528-47.
20. Brunner Y, Coute Y, Iezzi M, Foti M, Fukuda M, Hochstrasser DF, Wollheim CB, Sanchez JC. Proteomics analysis of insulin secretory granules. Mol Cell Proteom 2007; 6: 1007-17.
21. Foster MC, Leapman RD, Li MX, Atwater I. Elemental composition of secretory granules in pancreatic islets of Langerhans. Biophys J 1993; 64: 525-32.
22. Davidson HW, Rhodes CJ, Hutton JC. Intraorganellar calcium and pH control proinsulin cleavage in the pancreatic beta cell via two distinct site-specific endopeptidases. Nature 1988; 333: 93-6.
23. Michael DJ, Ritzel RA, Haataja L, Chow RH. Pancreatic beta-cells secrete insulin in fast- and slow-release forms. Diabetes 2006; 55: 600-7.
24. Westermark P, Li ZC, Westermark GT, Leckström A, Steiner DF. Effects of beta cell granule components on human islet amyloid polypeptide fibril formation. FEBS Lett 1996; 379: 203-6.
25. Nettleton EJ, Tito P, Sunde M, Bouchard M, Dobson CM, Robinson CV. Characterization of the oligomeric states of insulin in self-assembly and amyloid fibril formation by mass spectrometry. Biophys J 2000; 79: 1053-65.
26. Shafqat J, Melles E, Sigmundsson K, Johansson BL, Ekberg K, Alvelius G, Henriksson M, Johansson J, Wahren J, Jörnvall H. Proinsulin C-peptide elicits disaggregation of insulin resulting in enhanced physiological insulin effects. Cell Mol Life Sci 2006; 63: 1805-11.
27. Nerelius C, Alvelius G, Jörnvall H. N-terminal segment of proinsulin C-peptide active in insulin interaction/desaggregation. Biochem Biophys Res Commun 2010; 403: 462-7.
28. Landreh M, Alvelius G, Willander H, Stukenborg JB, Söder O, Johansson J, Jörnvall H. Insulin solubility transitions by pH-dependent interactions with proinsulin C-peptide. FEBS J 2012; 279: 4589-97.
29. Landreh M, Johansson J, Jörnvall H. C-peptide: a molecule balancing insulin states in secretion and diabetes-associated depository conditions. Horm Metab Res 2013; 45: 769-73.
30. Hayden MR, Tyagi SC, Kerklo MM, Nicolls MR. Type 2 diabetes mellitus as a conformational disease. J Pancreas 2005; 6: 287-302.
31. Dische FE, Wernstedt C, Westermark GT, Westermark P, Pepys MB, Rennie JA, Gilbey SG, Watkins PJ. Insulin as an amyloid-fibril protein at sites of repeated insulin injections in a diabetic patient. Diabetologia 1988; 31: 158-61.
32. Ivanova MI, Sievers SA, Sawaya MR, Wall JS, Eisenberg D. Molecular basis for insulin fibril assembly. Proc Natl Acad Sci USA 2009; 106: 18990-5.
33. Ahmad A, Uversky VN, Hong D, Fink AL. Early events in the fibrillation of monomeric insulin. J Biol Chem 2005; 280: 42669-75.
34. Landreh M, Stukenborg JB, Willander H, Söder O, Johansson J, Jörnvall H. Proinsulin C-peptide interferes with insulin fibril formation. Biochem Biophys Res Commun 2012; 418: 489-93.
35. Westermark P, Andersson A, Westermark GT. Islet amyloid polypeptide, islet amyloid, and diabetes mellitus. Physiol Rev 2011; 91: 795-826.
36. Janciauskiene S, Eriksson S, Carlemalm E, Ahrén B. B cell granule peptides affect human islet amyloid polypeptide (IAPP) fibril formation in vitro. Biochem Biophys Res Commun 1997; 236: 580-5.
37. Landreh M, Alvelius G, Johansson J, Jörnvall H. Insulin, islet amyloid polypeptide and C-peptide interactions evaluated by mass spectrometric analysis. Rapid Commun Mass Spectrom 2014; 28: 178-84.
38. Wiltzius JJ, Sievers SA, Sawaya MR, Eisenberg D. Atomic structures of IAPP (amylin) fusions suggest a mechanism for fibrillation and the role of insulin in the process. Protein Sci 2009; 18: 1521-30.
39. Brange J, Andersen L, Laursen ED, Meyn G, Rasmussen E. Toward understanding insulin fibrillation. J Pharm Sci 1997; 86: 517-25.
40. Kubota M, Sato Y, Khookhor O, Ekberg K, Chibalin AV, Wahren J. Enhanced insulin action following subcutaneous co-administration of insulin and C-peptide in rats. Diabetes Metab Res Rev 2014; 30: 124-31.
41. Jörnvall H, Lindahl E, Astorga-Wells J, Lind J, Holmlund A, Melles E, Alvelius G, Nerelius C, Mäler L, Johansson J. Oligomerization and insulin interactions of proinsulin C-peptide: threefold relationships to properties of insulin. Biochem Biophys Res Commun 2010; 391: 1561-6.
42. Lind J, Lindahl E, Peralvarez-Marin A, Holmlund A, Jörnvall H, Mäler L. Structural features of proinsulin C-peptide oligomeric and amyloid states. FEBS J 2010; 277: 3759-68.
43. Keltner Z, Meyer JA, Johnson EM, Palumbo AM, Spence DM, Reid GE. Mass spectrometric characterization and activity of zinc-activated proinsulin C-peptide and C-peptide mutants. Analyst 2010; 135: 278-88.
44. Biancalana M, Koide S. Molecular mechanism of Thioflavin-T binding to amyloid fibrils. Biochim Biophys Acta 2010; 1804: 1405-12.
45. Marx N, Walcher D, Raichle C, Aleksic M, Bach H, Grub M, Hombach V, Libby P, Zieske A, Homma S, Strong J. C-peptide colocalizes with macrophages in early arteriosclerotic lesions of diabetic subjects and induces monocyte chemotaxis in vitro. Arterioscl Thromb Vasc Biol 2004; 24: 540-5.
46. Wahren J, Ekberg K, Jörnvall H. C-peptide is a bioactive peptide. Diabetologia 2007; 50: 503-9.
47. Lindahl E, Nyman U, Melles E, Sigmundsson K, Ståhlberg M, Wahren J, Obrink B, Shafqat J, Joseph B, Jörnvall H. Cellular internalization of proinsulin C-peptide. Cell Mol Life Sci 2007; 64: 479-86.
48. Henriksson M, Shafqat J, Liepinsh E, Tally M, Wahren J, Jörnvall H, Johansson J. Unordered structured of proinsulin C-peptide in aqueous solution and in the presence of lipid vesicles. Cell Mol Life Sci 2000; 57: 337-42.
49. Luppi P, Geng X, Cifarelli V, Drain P, Trucco M. C-peptide is internalised in human endothelial and vascular smooth muscle cells via early endosomes. Diabetologia 2009; 52: 2218-28.
50. Ohtomo Y, Aperia A, Sahlgren B, Johansson BL, Wahren J. C-peptide stimulates rat renal tubular Na+, K(+)-ATPase activity in synergism with neuropeptide Y. Diabetologia 1996; 39: 199-205.
51. Ohtomo Y, Bergman T, Johansson BL, Jörnvall H, Wahren J. Differential effects of proinsulin C-peptide fragments on Na+, K+-ATPase activity of renal tubule segments. Diabetologia 1998; 41: 287-91.
52. Rigler R, Pramanik A, Jonasson P, Kratz G, Jansson OT, Nygren P, Stahl S, Ekberg K, Johansson B, Uhlén S, Uhlén M, Jörnvall H, Wahren J. Specific binding of proinsulin C-peptide to human cell membranes. Proc Natl Acad Sci USA 1999; 96: 13318-23.
53. Zhong Z, Davidescu A, Ehren I, Ekberg K, Jörnvall H, Wahren J, Chibalin AV. C-peptide stimulates ERK1/2 and JNK MAP kinases via activation of protein kinase C in human renal tubular cells. Diabetologia 2005; 48: 187-97.
54. Pramanik A, Ekberg K, Zhong Z, Shafqat J, Henriksson M, Jansson O, Tibell A, Tally M, Wahren J, Jörnvall H, Rigler R, Johansson J. C-peptide binding to human cell membranes: importance of Glu27. Biochem Biophys Res Commun 2001; 284: 94-8.
55. Sato Y, Oshida Y, Han YQ, Morishita Y, Li L, Ekberg K, Jörnvall H, Wahren J. C-peptide fragments stimulate glucose utilization in diabetic rats. Cell Mol Life Sci 2004; 61: 727-32.
56. Katritch V, Cherezov V, Stevens RC. Structure-function of the G protein-coupled receptor superfamily. Ann Rev Pharmacol Toxicol 2013; 53: 531-56.
57. Granier S, Kobilka B. A new era of GPCR structural and chemical biology. Nat Chem Biol 2012; 8: 670-3.
58. Hollenstein K, de Graaf C, Bortolato A, Wang MW, Marshall FH, Stevens RC. Insights into the structure of class B GPCRs. Trends Pharm Sci 2014; 35: 12-22.
59. Wahren J, Shafqat J, Johansson J, Chibalin A, Ekberg K, Jörnvall H. Molecular and cellular effects of C-peptide - new perspectives on an old peptide. Exp Diabesity Res 2004; 5: 15-23.
60. Yosten GL, Kolar GR, Redlinger LJ, Samson WK. Evidence for an interaction between proinsulin C-peptide and GPR146. J Endocrinol 2013; 218: B1-8.
61. Siu FY, He M, de Graaf C, Han GW, Yang D, Zhang Z, Zhou C, Xu Q, Wacker D, Joseph JS, Liu W, Lau J, Cherezov V, Katritch V, Wang MW, Stevens RC. Structure of the human glucagon class B G-protein-coupled receptor. Nature 2013; 499: 444-9.
62. White JF, Noinaj N, Shibata Y, Love J, Kloss B, Xu F, Gvozdenovic-Jeremic J, Shah P, Shiloach J, Tate CG, Grisshammer R. Structure of the agonist-bound neurotensin receptor. Nature 2012; 490: 508-13.
63. Authier F, Desbuquois B. Glucagon receptors. Cell Mol Life Sci 2008; 65: 1880-99.
64. Lovell SC, Robertson DL. An integrated view of molecular coevolution in protein-protein interactions. Mol Biol Evol 2010; 27: 2567-75.