Substrate-Favored lysosomal and proteasomal pathways participate in the normal balance control of insulin precursor maturation and disposal in β-Cells

PLoS ONE

Volumn 6, Issue 11, 2011, Pages

  Zhang, Xiaoping ^a   Yuan, Qingxin ^a,b   Tang, Wei ^a,b   Gu, Jingyu ^a,b   Osei, Kwame ^a   Wang, Jie ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b THE FIRST AFFILIATED HOSPITAL OF NANJING MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; PROINSULIN; PROTEASOME; INSULIN;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; CONTROLLED STUDY; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; LYSOSOME; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PROTEIN PROCESSING; ANIMAL; ENZYME IMMUNOASSAY; IMMUNOPRECIPITATION; METABOLISM; PROTEIN SYNTHESIS; WESTERN BLOTTING;

ANIMALS; AUTOPHAGY; BLOTTING, WESTERN; GLUCOSE; IMMUNOENZYME TECHNIQUES; IMMUNOPRECIPITATION; INSULIN; INSULIN-SECRETING CELLS; LYSOSOMES; MICE; PROINSULIN; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BIOSYNTHESIS;

EID: 80755126045     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0027647     Document Type: Article

References (46)

1. Wang J, Chen Y, Yuan Q, Tang W, Zhang X, et al. (2011) Control of Precursor Maturation and Disposal Is an Early Regulative Mechanism in the Normal Insulin Production of Pancreatic β-Cells. PLoS ONE 6 (4): e19446.
2. Wang J, Takeuchi T, Tanaka S, Kubo SK, Kayo T, et al. (1999) A mutation in the insulin 2 gene induces diabetes with severe pancreatic beta-cell dysfunction in the Mody mouse. J Clin Invest 103: 27-37.
3. Stoy J, Edghill EL, Flanagan SE, Ye H, Paz VP, et al. (2007) Insulin gene mutations as a cause of permanent neonatal diabetes. Proc Natl Acad Sci U S A 104: 15040-15044.
4. Edghill EL, Flanagan SE, Patch AM, Boustred C, Parrish A, et al. (2008) Insulin mutation screening in 1,044 patients with diabetes: mutations in the INS gene are a common cause of neonatal diabetes but a rare cause of diabetes diagnosed in childhood or adulthood. Diabetes 57: 1034-1042.
5. Brodsky JL, Wojcikiewicz RJ, (2009) Substrate-specific mediators of ER associated degradation (ERAD). Curr Opin Cell Biol 21 (4): 516-21.
6. Hirsch C, Gauss R, Horn SC, Neuber O, Sommer T, (2009) The ubiquitylation machinery of the endoplasmic reticulum. Nature 458 (7237): 453-60.
7. Cuervo AM, (2004) Autophagy. in sickness and in health. Trends Cell Biol 14 (2): 70-7.
8. Levine B, Kroemer G, (2008) Autophagy in the pathogenesis of disease. Cell 132 (1): 27-42.
9. Vogiatzi T, Xilouri M, Vekrellis K, Stefanis L, (2008) Wild type alpha-synuclein is degraded by chaperone-mediated autophagy and macroautophagy in neuronal cells. J Biol Chem 283 (35): 23542-56.
10. Webb JL, Ravikumar B, Atkins J, Skepper JN, Rubinsztein DC, (2003) Alpha-Synuclein is degraded by both autophagy and the proteasome. J Biol Chem 278: 25009-13.
11. Anelli T, Sitia R, (2008) Protein quality control in the early secretory pathway. Embo J 27 (2): 315-27.
12. Scheuner D, Kaufman RJ, (2008) The unfolded protein response. a pathway that links insulin demand with beta-cell failure and diabetes. Endocr Rev 29 (3): 317-33.
13. Bernales S, Schuck S, Walter P, (2007) ER-phagy: selective autophagy of the endoplasmic reticulum. Autophagy 3 (3): 285-7.
14. Yorimitsu T, Klionsky DJ, (2007) Eating the endoplasmic reticulum. quality control by autophagy. Trends Cell Biol 17 (6): 279-85.
15. Hegde RS, Kang SW, (2008) The concept of translocational regulation. J Cell Biol 182 (2): 225-32.
16. Oyadomari S, Yun C, Fisher EA, Kreglinger N, Kreibich G, et al. (2006) Cotranslocational degradation protects the stressed endoplasmic reticulum from protein overload. Cell 126: 727-739.
17. Schubert U, Anton LC, Gibbs J, Norbury CC, Yewdell JW, et al. (2000) Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature 404: 770-774.
18. Steiner DF, Bell GI, Rubenstein AH, Chan SJ, (2001) Chemistry and biosynthesis of the islet hormones: insulin, islet amyloid polypeptide (amylin), glucogon, somatostatin, and pancreatic polypeptide. In: DeGroot LJ, Jameson JL, editors. Endocrinology Philadelphia Saunders pp. 667-696.
19. Goodge KA, Hutton JC, (2000) Translational regulation of proinsulin biosynthesis and proinsulin conversion in the pancreatic beta-cell. Semin Cell Dev Biol 11 (4): 235-42.
20. Huang XF, Arvan P, (1995) Intracellular transport of proinsulin in pancreatic beta-cells. Structural maturation probed by disulfide accessibility. J Biol Chem 270: 20417-20423.
21. Ohkuma S, Poole B, (1978) Fluorescence probe measurement of the intralysosomal pH in living cells and the perturbation of pH by various agents. Proc Natl Acad Sci U S A 75 (7): 3327-31.
22. Perry CN, Kyoi S, Hariharan N, Takagi H, Sadoshima J, et al. (2009) Novel methods for measuring cardiac autophagy in vivo. Methods Enzymol 453: 325-42.
23. Orci L, Perrelet A, Ravazzola M, Wieland FT, Schekman R, et al. (1993) "BFA bodies": a subcompartment of the endoplasmic reticulum. Proc Natl Acad Sci U S A 90 (23): 11089-93.
24. Nozaki J, Kubota H, Yoshida H, Naitoh M, Goji J, et al. (2004) The endoplasmic reticulum stress response is stimulated through the continuous activation of transcription factors ATF6 and XBP1 in Ins2+/Akita pancreatic beta cells. Genes Cells 9: 261-270.
25. Franklin JL, Johnson EM, (1998) Control of neuronal size homeostasis by trophic factor-mediated coupling of protein degradation to protein synthesis. J Cell Biol 142 (5): 1313-24.
26. Kuliawat R, Arvan P, (1994) Distinct molecular mechanisms for protein sorting within immature secretory granules of pancreatic beta-cells. J Cell Biol 126 (1): 77-86.
27. Marzban L, Rhodes CJ, Steiner DF, Haataja L, Halban PA, et al. (2006) Impaired NH2-terminal processing of human proislet amyloid polypeptide by the prohormone convertase PC2 leads to amyloid formation and cell death. Diabetes 55 (8): 2192-201.
28. Nagamatsu S, Nishi M, Steiner DF, (1991) Biosynthesis of islet amyloid polypeptide. Elevated expression in mouse beta TC3 cells. J Biol Chem 266 (21): 13737-41.
29. Rapoport TA, (2007) Protein translocation across the eukaryotic endoplasmic reticulum and bacterial plasma membranes. Nature 450 (7170): 663-9.
30. Albert SG, Permutt MA, (1979) Proinsulin precursors in catfish pancreatic islets. J Biol Chem 254 (9): 3483-92.
31. Eskridge EM, Shields D, (1983) Cell-free processing and segregation of insulin precursors. J Biol Chem 258 (19): 11487-91.
32. Okun MM, Eskridge EM, Shields D, (1990) Truncations of a secretory protein define minimum lengths required for binding to signal recognition particle and translocation across the endoplasmic reticulum membrane. J Biol Chem 265 (13): 7478-84.
33. Patzelt C, Labrecque AD, Duguid JR, Carroll RJ, Keim, PS, et al. (1978) Detection and kinetic behavior of preproinsulin in pancreatic islets. Proc Natl Acad Sci U S A 75 (3): 1260-4.
34. Manchester KL, (1969) Interference of various antibiotics and other compounds with protein synthesis in muscle and their influence on metabolic regulation. Nature 221 (5176): 188-90.
35. Seglen PO, Gordon PB, (1982) 3-Methyladenine: specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc Natl Acad Sci U S A 79: 1889-1892.
36. Yamamoto A, Tagawa Y, Yoshimori T, Moriyama Y, Masaki R, et al. (1998) Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells. Cell Struct Funct 23: 33-42.
37. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, et al. (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 19: 5720-5728.
38. Fujimoto K, Hanson PT, Tran H, Ford EL, Han Z, et al. (2009) Autophagy regulates pancreatic beta cell death in response to Pdx1 deficiency and nutrient deprivation. J Biol Chem 284: 27664-27673.
39. Ebato C, Uchida T, Arakawa M, Komatsu M, Ueno T, et al. (2008) Autophagy is important in islet homeostasis and compensatory increase of beta cell mass in response to high-fat diet. Cell Metab 8 (4): 325-32.
40. Jung HS, Chung KW, Won Kim J, Kim J, Komatsu M, et al. (2008) Loss of autophagy diminishes pancreatic beta cell mass and function with resultant hyperglycemia. Cell Metab 8 (4): 318-24.
41. Lopez-Avalos MD, Duvivier-Kali VF, Xu G, Bonner-Weir S, Sharma A, et al. (2006) Evidence for a role of the ubiquitin-proteasome pathway in pancreatic islets. Diabetes 55 (5): 1223-31.
42. Kitiphongspattana K, Mathews CE, Leiter EH, Gaskins HR, (2005) Proteasome inhibition alters glucose-stimulated (pro)insulin secretion and turnover in pancreatic {beta}-cells. J Biol Chem 280 (16): 15727-34.
43. Kawaguchi M, Minami K, Nagashima K, Seino S, (2006) Essential role of ubiquitin-proteasome system in normal regulation of insulin secretion. J Biol Chem 281 (19): 13015-20.
44. Steiner DF, Clark JL, (1968) The spontaneous reoxidation of reduced beef and rat proinsulins. Proc Natl Acad Sci U S A 60: 622-629.
45. Orci L, Ravazzola M, Amherdt M, Yanaihara C, Yanaihara N, et al. (1984) Insulin, not C-peptide (proinsulin), is present in crinophagic bodies of the pancreatic B-cell. J Cell Biol 98 (1): 222-8.
46. Anfinsen CB, (1973) Principles that govern the folding of protein chains. Science 181 (96): 223-30.