Islet autoimmunity identifies a unique pattern of impaired pancreatic beta-cell function, markedly reduced pancreatic beta cell mass and insulin resistance in clinically diagnosed type 2 diabetes

PLoS ONE

Volumn 9, Issue 9, 2014, Pages

  Subauste, Angela ^b,d   Gianani, Roberto ^a,b   Chang, Annette M ^b   Plunkett, Cynthia ^b   Pietropaolo, Susan L ^a,b   Zhang, Ying Jian ^b   Barinas Mitchell, Emma ^c   Kuller, Lewis H ^c   Galecki, Andrzej ^b   Halter, Jeffrey B ^b   Pietropaolo, Massimo ^a,b  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

^d UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; PANCREAS ISLET CELL ANTIBODY; AUTOANTIBODY; BIOLOGICAL MARKER; C PEPTIDE; GLUCOSE BLOOD LEVEL; HLA DR ANTIGEN; INSULIN;

ADULT; AGED; ANTIBODY DETECTION; ARTICLE; AUTOIMMUNITY; CELL DESTRUCTION; CELLULAR PARAMETERS; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE DURATION; FAT FREE MASS; FAT MASS; FEMALE; GLUCOSE CLAMP TECHNIQUE; HUMAN; HUMAN TISSUE; INSULIN RELEASE; INSULIN RESISTANCE; LATENT AUTOIMMUNE DIABETES IN ADULT; MALE; METABOLIC RATE; NON INSULIN DEPENDENT DIABETES MELLITUS; PANCREAS ISLET BETA CELL; PANCREAS ISLET BETA CELL MASS; PANCREAS ISLET CELL FUNCTION; ALLELE; BODY COMPOSITION; CELL SIZE; DONOR; GENETICS; GLUCOSE BLOOD LEVEL; IMMUNOLOGY; METABOLISM; MIDDLE AGED; PATHOLOGY; SECRETION (PROCESS);

ADULT; AGED; ALLELES; AUTOANTIBODIES; AUTOIMMUNITY; BIOLOGICAL MARKERS; BLOOD GLUCOSE; BODY COMPOSITION; C-PEPTIDE; CELL SIZE; DIABETES MELLITUS, TYPE 2; FEMALE; HLA-DR ANTIGENS; HUMANS; INSULIN; INSULIN RESISTANCE; INSULIN-SECRETING CELLS; MALE; MIDDLE AGED; TISSUE DONORS;

EID: 84907190403     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0106537     Document Type: Article

References (50)

1. Polonsky KS, Sturis J, Bell GI (1996) Non-insulin-dependent diabetes mellitus - a genetically programmed failure of the beta cell to compensate for insulin resistance. Seminars in Medicine of the Beth Israel Hospital, Boston. N Engl J Med 334: 777-783.
2. Ward WK, Bolgiano DC, McKnight B, Halter JB, Porte D Jr (1984) Diminished B cell secretory capacity in patients with noninsulin-dependent diabetes mellitus. J Clin Invest 74: 1318-1328.
3. Taylor SI (1992) Lilly Lecture: molecular mechanisms of insulin resistance. Lessons from patients with mutations in the insulin-receptor gene. Diabetes 41: 1473-1490.
4. Kahn CR (1994) Insulin action, diabetogenes and the cause of type II diabetes. Banting Lecture. Diabetes 43: 1066-1084.
5. Huang CJ, Haataja L, Gurlo T, Butler AE, Wu X, et al. (2007) Induction of endoplasmic reticulum stress-induced beta-cell apoptosis and accumulation of polyubiquitinated proteins by human islet amyloid polypeptide. Am J Physiol Endocrinol Metab 293: E1656-E1662. 00318.2007 [pii];10.1152/ajpendo.00318.2007 [doi].
6. Turner R, Stratton I, Horton V, Manley S, Zimmet P, et al. (1997) UKPDS 25: autoantibodies to islet-cell cytoplasm and glutamic acid decarboxylase for prediction of insulin requirement in type 2 diabetes. Lancet 350: 1288-1293.
7. Pietropaolo M, Barinas-Mitchell E, Pietropaolo SL, Kuller LH, Trucco M (2000) Evidence of islet cell autoimmunity in elderly patients with Type 2 diabetes mellitus. Diabetes 49: 32-38.
8. Pietropaolo M, Barinas-Mitchell E, Kuller LH (2007) The heterogeneity of diabetes: unraveling a dispute: is systemic inflammation related to islet autoimmunity? Diabetes 56: 1189-1197.
9. Hotamisligil GS (2010) Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 140: 900-917. S0092-8674(10)00187-X [pii];10.1016/j.cell.2010.02.034 [doi].
10. Brooks-Worrell B, Palmer JP (2012) Immunology in the Clinic Review Series; focus on metabolic diseases: development of islet autoimmune disease in type 2. diabetes patients: potential sequelae of chronic inflammation. Clin Exp Immunol 167: 40-46. 10.1111/j.1365-2249.2011.04501.x [doi].
11. Tuomi T, Groop LC, Zimmet PZ, Rowley MJ, Knowles WJ, et al. (1993) Antibodies to glutamic acid decarboxylase reveal latent autoimmune diabetes in adults with a non-insulin-dependent onset of diabetes. Diabetes 42: 359-362.
12. Barinas-Mitchell E, Pietropaolo S, Zhang YJ, Henderson T, Trucco M, Kuller LH, et al. (2004) Islet cell autoimmunity in a triethnic adult population of the National Health and Nutrition Examination Survey (NHANES) III. Diabetes 53: 1293-1302.
13. Maioli M, Tonolo G, Bekris L, Schranz D, Cossu E, et al. Study Group for the Genetics of Diabetes in Sardina (SGGDS). (2002) GAD65 and IA-2 autoantibodies are common in a subset of siblings of Sardinian Type 2 diabetes families. Diabetes Res Clin Pract 56: 41-47.
14. Barinas-Mitchell E, Kuller LH, Pietropaolo S, Zhang YJ, Henderson T, et al. (2006) The prevalence of the 65-kilodalton isoform of glutamic acid decarboxylase autoantibodies by glucose tolerance status in elderly patients from the cardiovascular health study. J Clin Endocrinol Metab 91: 2871-2877. jc.2005-2667 [pii];10.1210/jc.2005-2667 [doi].
15. Leslie RD, Williams R, Pozzilli P (2006) Clinical review: Type 1 diabetes and latent autoimmune diabetes in adults: one end of the rainbow. J Clin Endocrinol Metab 91: 1654-1659.
16. Uibo R, Lernmark A (2008) GAD65 autoimmunity-clinical studies. Adv Immunol 100: 39-78. S0065-2776(08)00803-1 [pii];10.1016/S0065-2776(08)00803-1 [doi].
17. Palmer JP, Hirsch IB (2003) What's in a Name: Latent autoimmune diabetes of adults, type 1.5, adult-onset, and type 1 diabetes. Diabetes Care 26: 536-538.
18. Leslie RD, Kolb H, Schloot NC, Buzzetti R, Mauricio D, et al. (2008) Diabetes classification: grey zones, sound and smoke: Action LADA 1. Diabetes Metab Res Rev 24: 511-519. 10.1002/dmrr.877 [doi].
19. Hawa MI, Kolb H, Schloot N, Beyan H, Paschou SA, et al. (2013) Adult-onset autoimmune diabetes in Europe is prevalent with a broad clinical phenotype: Action LADA 7. Diabetes Care 36: 908-913. dc12-0931 [pii];10.2337/dc12-0931 [doi].
20. Tuomi T, Santoro N, Caprio S, Cai M, Weng J, et al. (2013) The many faces of diabetes: a disease with increasing heterogeneity. Lancet. S0140-6736(13)62219-9 [pii];10.1016/S0140-6736(13)62219-9 [doi].
21. Gottsater A, Landin-Olsson M, Lernmark A, Fernlund P, Sundkvist G (1994) Islet cell antibodies are associated with beta-cell failure also in obese adult onset diabetic patients. Acta Diabetol 31: 226-231.
22. Naik RG, Brooks-Worrell BM, Palmer JP (2009) Latent autoimmune diabetes in adults. J Clin Endocrinol Metab 94: 4635-4644. jc.2009-1120 [pii];10.1210/jc.2009-1120 [doi].
23. Gianani R, Campbell-Thompson M, Sarkar SA, Wasserfall C, Pugliese A, at al. (2010) Dimorphic histopathology of long-standing childhood-onset diabetes. Diabetologia 53:690-8.
24. National Diabetes Data Group (1979) Classification and diagnosis of diabetes mellitus and other categories of glucose intolerance. Diabetes 28: 1039-1057.
25. Pugliese A, Yang M, Kusmarteva I, Heiple T, Vendrame F, et al. (2014) The Juvenile Diabetes Research Foundation Network for Pancreatic Organ Donors with Diabetes (nPOD) Program: goals, operational model and emerging findings. Pediatr Diabetes 15: 1-9. 10.1111/pedi.12097 [doi].
26. Campbell-Thompson ML, Atkinson MA, Butler AE, Chapman NM, Frisk G, et al. (2013) The diagnosis of insulitis in human type 1 diabetes. Diabetologia 56: 2541-2543. 10.1007/s00125-013-3043-5 [doi].
27. Rakotoambinina B, Timsit J, Deschamps I, Laborde K, Gautier D, et al. (1997) Insulin responses to intravenous glucose, intravenous arginine and a hyperglycaemic clamp in ICA-positive subjects with different degrees of glucose tolerance. Diabetes Metab 23: 43-50.
28. Kahn SE, Prigeon RL, McCulloch DK, Boyko EJ, Bergman RN, et al. (1993) Quantification of the relationship between insulin sensitivity and beta-cell function in human subjects. Diabetes 42: 1663-1662.
29. Simoneau JA, Veerkamp JH, Turcotte LP, Kelley DE (1999) Markers of capacity to utilize fatty acids in human skeletal muscle: relation to insulin resistance and obesity and effects of weight loss. FASEB J 13: 2051-2060.
30. American Diabetes Association (2014) Diagnosis and Classification of Diabetes Mellitus. Diabetes Care 37: S81-S90.
31. Hu FB, Manson JE, Stampfer MJ, Colditz G, Liu S, et al. (2001) Diet, lifestyle, and the risk of type 2 diabetes mellitus in women. N Engl J Med 345: 790-797. 10.1056/NEJMoa010492 [doi].
32. Pietropaolo M, Towns R, Eisenbarth GS (2012) Humoral autoimmunity in type 1 diabetes: prediction, significance, and detection of distinct disease subtypes. Cold Spring Harb Perspect Med 2. cshperspect.a012831 [pii];10.1101/cshperspect.a012831 [doi].
33. Hawa MI, Thivolet C, Mauricio D, Alemanno I, Cipponeri E, et al. (2009) Metabolic syndrome and autoimmune diabetes: action LADA 3. Diabetes Care 32: 160-164.
34. Grant SF, Hakonarson H, Schwartz S (2010) Can the genetics of type 1 and type 2 diabetes shed light on the genetics of latent autoimmune diabetes in adults? Endocr Rev 31: 183-193. er.2009-0029 [pii];10.1210/er.2009-0029 [doi].
35. Cervin C, Lyssenko V, Bakhtadze E, Lindholm E, Nilsson P, et al. (2008) Genetic similarities between latent autoimmune diabetes in adults, type 1 diabetes, and type 2 diabetes. Diabetes 57: 1433-1437. db07-0299 [pii]; 10.2337/db07-0299 [doi].
36. Liu F, Liu J, Zheng TS, Li Q, Wang C, et al. (2012) The -1123G>C variant of PTPN22 gene promoter is associated with latent autoimmune diabetes in adult Chinese Hans. Cell Biochem Biophys 62: 273-279. 10.1007/s12013-011-9291-4 [doi].
37. Brooks-Worrell BM, Reichow JL, Goel A, Ismail H, Palmer JP (2011) Identification of autoantibody-negative autoimmune type 2 diabetic patients. Diabetes Care 34: 168-173. dc10-0579 [pii];10.2337/dc10-0579 [doi].
38. Olsson L, Ahlbom A, Grill V, Midthjell K, Carlsson S (2012) Sleep disturbances and low psychological well-being are associated with an increased risk of autoimmune diabetes in adults. Results from the Nord-Trondelag Health Study. Diabetes Res Clin Pract 98: 302-311. S0168-8227(12)00315-4 [pii];10.1016/j.diabres.2012.09.011 [doi].
39. Zinman B, Kahn SE, Haffner SM, O'Neill MC, Heise MA, et al. (2004) Phenotypic characteristics of GAD antibody-positive recently diagnosed patients with type 2 diabetes in North America and Europe. Diabetes 53: 3193-3200.
40. Dandona P, Aljada A, Bandyopadhyay A (2004) Inflammation: the link between insulin resistance, obesity and diabetes. Trends Immunol 25: 4-7.
41. Wellen KE, Hotamisligil GS (2005) Inflammation, stress, and diabetes. J Clin Invest 115: 1111-1119.
42. Pickup JC (2004) Inflammation and activated innate immunity in the pathogenesis of Type 2 diabetes. Diabetes Care 27: 813-823.
43. Lee CC, Adler AI, Sandhu MS, Sharp SJ, Forouhi NG, et al. (2009) Association of C-reactive protein with type 2 diabetes: prospective analysis and meta-analysis. Diabetologia 52: 1040-1047. 10.1007/s00125-009-1338-3 [doi].
44. Pereira RI, Snell-Bergeon JK, Erickson C, Schauer IE, Bergman BC, et al. (2012) Adiponectin dysregulation and insulin resistance in type 1 diabetes. J Clin Endocrinol Metab 97: E642-E647. jc.2011-2542 [pii];10.1210/jc.2011-2542 [doi].
45. Bergman BC, Howard D, Schauer IE, Maahs DM, Snell-Bergeon JK, et al. (2012) Features of hepatic and skeletal muscle insulin resistance unique to type 1 diabetes. J Clin Endocrinol Metab 97: 1663-1672. jc.2011-3172 [pii];10.1210/jc.2011-3172 [doi].
46. Monnier L, Colette C, Owens DR (2008) Type 2 diabetes: a well-characterised but suboptimally controlled disease. Can we bridge the divide? Diabetes Metab 34: 207-216. S1262-3636(08)00062-1 [pii];10.1016/j.diabet.2008.01.011 [doi].
47. Cassese A, Esposito I, Fiory F, Barbagallo AP, Paturzo F, et al. (2008) In skeletal muscle advanced glycation end products (AGEs) inhibit insulin action and induce the formation of multimolecular complexes including the receptor for AGEs. J Biol Chem 283: 36088-36099. M801698200 [pii];10.1074/jbc.M801698200 [doi].
48. Schmitz-Peiffer C, Biden TJ (2008) Protein kinase C function in muscle, liver, and beta-cells and its therapeutic implications for type 2 diabetes. Diabetes 57:1774-1783. 57/7/1774 [pii];10.2337/db07-1769 [doi].
49. Evans JL, Goldfine ID, Maddux BA, Grodsky GM (2003) Are oxidative stress-activated signaling pathways mediators of insulin resistance and beta-cell dysfunction? Diabetes 52: 1-8.
50. Ceriello A, Esposito K, Piconi L, Ihnat MA, Thorpe JE, et al. (2008) Oscillating glucose is more deleterious to endothelial function and oxidative stress than mean glucose in normal and type 2 diabetic patients. Diabetes 57: 1349-1354. db08-0063 [pii];10.2337/db08-0063 [doi]