Inhaled insulin forms toxic pulmonary amyloid aggregates

Endocrinology

Volumn 151, Issue 10, 2010, Pages 4717-4724

  Lasagna Reeves, Cristian A ^a   Clos, Audra L ^a   Midoro Hiriuti, Terumi ^a   Goldblum, Randall M ^a   Jackson, George R ^a   Kayed, Rakez ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID; CASPASE 9; RECOMBINANT HUMAN INSULIN; GLUCOSE BLOOD LEVEL; INSULIN; RECOMBINANT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIABETES MELLITUS; DRUG DELIVERY SYSTEM; IMMUNOHISTOCHEMISTRY; INHALER; LUNG CAPACITY; LUNG DISEASE; LUNG PARENCHYMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; RESPIRATORY AIRFLOW; ANIMAL; C57BL MOUSE; CELL LINE; CHEMICALLY INDUCED; DRUG EFFECTS; DRUG SCREENING; ENZYME ACTIVATION; GLUCOSE BLOOD LEVEL; HUMAN; INHALATIONAL DRUG ADMINISTRATION; METABOLISM; PHYSIOLOGY; PRECIPITATION; PROTEIN MULTIMERIZATION; PROTEOSTASIS DEFICIENCY; TOXICITY;

ADMINISTRATION, INHALATION; AMYLOID; ANIMALS; BLOOD GLUCOSE; CASPASE 9; CELL LINE; CHEMICAL PRECIPITATION; DIABETES COMPLICATIONS; DRUG EVALUATION, PRECLINICAL; ENZYME ACTIVATION; HUMANS; INSULIN; LUNG DISEASES; MICE; MICE, INBRED C57BL; PROTEIN MULTIMERIZATION; PROTEOSTASIS DEFICIENCIES; RECOMBINANT PROTEINS;

EID: 77957288054     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2010-0457     Document Type: Article

References (48)

1. Campbell RK 2009 Type 2 diabetes: where we are today: an overview of disease burden, current treatments, and treatment strategies. J Am Pharm Assoc 49(Suppl 1):S3-S9
2. Cleveringa FG, Welsing PM, van den Donk M, Gorter KJ, Niessen LW, Rutten GE, Redekop WK 2010 Cost-effectiveness of the diabetes care protocol, a multifaceted computerized decision support diabetes management intervention that reduces cardiovascular risk. Diabetes Care 33:258-263
3. Shaw JE, Sicree RA, Zimmet PZ 2010 Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Res Clin Pract 87:4-14
4. Swinnen SG, Hoekstra JB, DeVries JH 2009 Insulin therapy for type 2 diabetes. Diabetes Care 32(Suppl 2):S253-S259
5. Richardson T, Kerr D 2003 Skin-related complications of insulin therapy: epidemiology and emerging management strategies. Am J Clin Dermatol 4:661-667
6. Fineberg SE 2006 Diabetes therapy trials with inhaled insulin. Expert Opin Investig Drugs 15:743-762
7. Arnolds S, Heise T 2007 Inhaled insulin. Best Pract Res Clin Endocrinol Metab 21:555-571
8. Szymborska-Kajanek A, Wrobel M, Grzeszczak W, Strojek K 2007 Inhaled insulin-the breakthrough in the treatment of diabetes?. Pol Arch Med Wewn 117:415-419
9. Pham DQ, Cohen H, Chu V 2007 Inhaled human [rDNA origin] insulin, a novel formulation for diabetes mellitus. J Clin Pharmacol 47:890-903
10. Barnett AH, Lange P, Dreyer M, Serdarevic-Pehar M 2007 Longterm tolerability of inhaled human insulin (Exubera) in patients with poorly controlled type 2 diabetes. Int J Clin Pract 61:1614-1625
11. Skyler JS, Hollander PA, Jovanovic L, Klioze S, Krasner A, Riese RJ, Reis J, Schwartz P, Duggan W 2008 Safety and efficacy of inhaled human insulin (Exubera) during discontinuation and readministration of therapy in adults with type 1 diabetes: a 3-year randomized controlled trial. Diabetes Res Clin Pract 82:238-246
12. White NH, Quattrin T, St Aubin LB, Duggan WT, England RD, Fryburg JS 2008 Efficacy and safety of inhaled human insulin (Exubera) compared to subcutaneous insulin in children ages 6 to 11 years with type 1 diabetes mellitus: results of a 3-month, randomized, parallel trial. J Pediatr Endocrinol Metab 21:555-568
13. Ceglia L, Lau J, Pittas AG 2006 Meta-analysis: efficacy and safety of inhaled insulin therapy in adults with diabetes mellitus. Ann Intern Med 145:665-675
14. Mauro M, Craparo EF, Podestà A, Bulone D, Carrotta R, Martorana V, Tiana G, San Biagio PL 2007 Kinetics of different processes in human insulin amyloid formation. J Mol Biol 366:258-274
15. Podestà A, Tiana G, Milani P, Manno M 2006 Early events in insulin fibrillization studied by time-lapse atomic force microscopy. Biophys J 90:589-597
16. Murali J, Koteeswari D, Rifkind JM, Jayakumar R 2003 Amyloid insulin interaction with erythrocytes. Biochem Cell Biol 81:51-59
17. Malisauskas M, Weise C, Yanamandra K, Wolf-Watz M, Morozova-Roche L 2010 Lability landscape and protease resistance of human insulin amyloid: a new insight into its molecular properties. J Mol Biol 396:60-74
18. Ivanova MI, Sievers SA, Sawaya MR, Wall JS, Eisenberg D 2009 Molecular basis for insulin fibril assembly. Proc Natl Acad Sci USA 106:18990-18995
19. Wilhelm KR, Yanamandra K, Gruden MA, Zamotin V, Malisauskas M, Casaite V, Darinskas A, Forsgren L, Morozova-Roche LA 2007 Immune reactivity towards insulin, its amyloid and protein S100B in blood sera of Parkinson's disease patients. Eur J Neurol 14:327-334
20. Swift B 2002 Examination of insulin injection sites: an unexpected finding of localized amyloidosis. Diabet Med 19:881-882
21. Yumlu S, Barany R, Eriksson M, Röcken C 2009 Localized insulinderived amyloidosis in patients with diabetes mellitus: a case report. Hum Pathol 40:1655-1660
22. Sie MP, van der Wiel HE, Smedts FM, de Boer AC 2010 Human recombinant insulin and amyloidosis: an unexpected association. Neth J Med 68:138-140
23. Teeter JG, Riese RJ 2006 Dissociation of lung function changes with humoral immunity during inhaled human insulin therapy. Am J Respir Crit Care Med 173:1194-1200
24. Papagianni M, Hatziefthimiou A, Chachami G, Gourgoulianis K, Molyvdas PA, Paraskeva E 2009 Inhaled insulin does not trigger lung inflammation and airway remodelling. Eur Respir J 33:444-445
25. Cefalu WT, Bohannon NJ, Fineberg SE, Teeter JG, Schwartz PF, Reis JM, Krasner AS 2008 Assessment of long-term immunological and pulmonary safety of inhaled human insulin with up to 24 months of continuous therapy. Curr Med Res Opin 24:3073-3083
26. LiuMC, Riese RJ, Van Gundy K, NorwoodP, Sullivan BE, Schwartz PF, Teeter JG 2008 Effects of inhaledhumaninsulin on airway lining fluid composition in adults with diabetes. Eur Respir J 32:180-188
27. Papagianni M, Hatziefthimiou A, Chachami G, Gourgoulianis K, Molyvdas PA, Paraskeva E 2007 Insulin causes a transient induction of proliferation via activation of the PI3-kinase pathway in airway smooth muscle cells. Exp Clin Endocrinol Diabetes 115:118-123
28. Jiang D, Dinh KL, Ruthenburg TC, Zhang Y, Su L, Land DP, Zhou F 2009 A kinetic model for β-amyloid adsorption at the air/solution interface and its implication to the β-amyloid aggregation process. J Phys Chem B 113:3160-3168
29. Zhao X, Pan F, Lu JR 2009 Interfacial assembly of proteins and peptides: recent examples studied by neutron reflection. J R Soc Interface 6(Suppl 5):S659-S670
30. Han X, Hristova K, Wimley WC 2008 Protein folding in membranes: insights from neutron diffraction studies of a membrane β-sheet oligomer. Biophys J 94:492-505
31. Knecht V 2008 β-Hairpin folding by a model amyloid peptide in solution and at an interface. J Phys Chem B 112:9476-9483
32. Muenter AH, Hentschel J, Börner HG, Brezesinski G 2008 Characterization of peptide-guided polymer assembly at the air/water interface. Langmuir 24:3306-3316
33. Renault A, Rioux-Dubé JF, Lefèvre T, Pezennec S, Beaufils S, Vié V, Tremblay M, Pézolet M 2009 Surface properties and conformation of Nephila clavipes spider recombinant silk proteins at the air-water interface. Langmuir 25:8170-8180
34. Nichols MR, Moss MA, Reed DK, Hoh JH, Rosenberry TL 2005 Amyloid-β aggregates formed at polar-nonpolar interfaces differ from amyloid-β protofibrils produced in aqueous buffers. Microsc Res Tech 67:164-174
35. Kayed R, Head E, Sarsoza F, Saing T, Cotman CW, Necula M, Margol L, Wu J, Breydo L, Thompson JL, Rasool S, Gurlo T, Butler P, Glabe CG 2007 Fibril specific, conformation dependent antibodies recognize a generic epitope common to amyloid fibrils and fibrillar oligomers that is absent in prefibrillar oligomers. Mol Neurodegener 2:18
36. Kayed R, Head E, Thompson JL, McIntire TM, Milton SC, Cotman CW, Glabe CG 2003 Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300: 486-489
37. Meier JJ, Kayed R, Lin CY, Gurlo T, Haataja L, Jayasinghe S, Langen R, Glabe CG, Butler PC 2006 Inhibition of human IAPP fibril formation does not prevent β-cell death: evidence for distinct actions of oligomers and fibrils of human IAPP. Am J Physiol Endocrinol Metab 291:E1317-E1324
38. Castro SM, Guerrero-Plata A, Suarez-Real G, Adegboyega PA, Colasurdo GN, Khan AM, Garofalo RP, Casola A 2006 Antioxidant treatment ameliorates respiratory syncytial virus-induced disease and lung inflammation.AmJ Respir Crit Care Med 174:1361-1369
39. Hegewald M, Crapo RO, Jensen RL 2007 Pulmonary function changes related to acute and chronic administration of inhaled insulin. Diabetes Technol Ther 9(Suppl 1):S93-S101
40. Sharp JS, Forrest JA, Jones RA 2002 Surface denaturation and amyloid fibril formation of insulin at model lipid-water interfaces. Biochemistry 41:15810-15819
41. Haass C, Selkoe DJ 2007 Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid β-peptide. Nat Rev Mol Cell Biol 8:101-112
42. Ashkenazi A, Dixit VM 1999 Apoptosis control by death and decoy receptors. Curr Opin Cell Biol 11:255-260
43. García-Suárez Mdel M, Flórez N, Astudillo A, Vázquez F, Villaverde R, Fabrizio K, Pirofski LA, Méndez FJ 2007 The role of pneumolysin in mediating lung damage in a lethal pneumococcal pneumonia murine model. Respir Res 8:3
44. Hashimoto M, Rockenstein E, Crews L, Masliah E 2003 Role of protein aggregation in mitochondrial dysfunction and neurodegeneration in Alzheimer's and Parkinson's diseases. Neuromolecular Med 4:21-36
45. Chiti F, Dobson CM 2006 Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem 75:333-366
46. Stefani M, Dobson CM 2003 Protein aggregation and aggregate toxicity: new insights into protein folding, misfolding diseases and biological evolution. J Mol Med 81:678-699
47. Yang Y, Petkova A, Huang K, Xu B, Hua QX, Ye IJ, Chu YC, Hu SQ, Phillips NB, Whittaker J, Ismail-Beigi F, Mackin RB, Katsoyannis PG, Tycko R, Weiss MA An Achilles' heel in an amyloidogenic protein and its repair: insulin fibrillation and therapeutic design. J Biol Chem 285: 10806-10821.
48. Cherepanov DA, Feniouk BA, Junge W, Mulkidjanian AY 2003 Low dielectric permittivity of water at the membrane interface: effect on the energy coupling mechanism in biological membranes. Biophys J 85:1307-1316