The long lifespan and low turnover of human islet beta cells estimated by mathematical modeling of lipofuscin accumulation

Diabetologia

Volumn 53, Issue 2, 2010, Pages 321-330

  Cnop, M ^a   Hughes, S J ^b   Igoillo Esteve, M ^a   Hoppa, M B ^b   Sayyed, F ^b,f   Van De Laar, L ^b,g   Gunter, J H ^b,h   De Koning, E J P ^b,i   Walls, G V ^b   Gray, D W G ^b   Johnson , P R V ^b   Hansen , B C ^c   Morris, J F ^d   Pipeleers Marichal, M ^e   Cnop, I ^e   Clark, A ^b  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b CHURCHILL HOSPITAL   (United Kingdom)

^c UNIVERSITY OF SOUTH FLORIDA   (United States)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^f LEICESTER ROYAL INFIRMARY   (United Kingdom)

^g ERASMUS UNIVERSITY ROTTERDAM   (Netherlands)

^h UNIVERSITY OF QUEENSLAND   (Australia)

ⁱ LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

LIPOFUSCIN;

ADULT; AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; GENETIC MARKER; HALF LIFE TIME; HUMAN; HUMAN TISSUE; INSULINOMA; LIFESPAN; MATHEMATICAL MODEL; NERVE CELL; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PANCREAS ISLET ALPHA CELL; PANCREAS ISLET BETA CELL; PATHOGENESIS; PRIMATE; PRIORITY JOURNAL; RODENT;

ADULT; AGE DISTRIBUTION; AGING; ANIMALS; BIOLOGICAL MARKERS; CAUSE OF DEATH; CELL DIVISION; DIABETES MELLITUS, TYPE 2; HUMANS; INSULIN-SECRETING CELLS; LIPOFUSCIN; MACACA MULATTA; MICE; MICE, INBRED C57BL; MODELS, THEORETICAL; PANCREAS; TISSUE DONORS;

EID: 77949289481     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-009-1562-x     Document Type: Article

References (50)

1. McCarthy MI, Hattersley AT (2008) Learning from molecular genetics: novel insights arising from the definition of genes for monogenic and type 2 diabetes. Diabetes 57:2889-2898
2. Meier JJ (2009) Linking the genetics of type 2 diabetes with low birth weight: a role for prenatal islet maldevelopment? Diabetes 58:1255-1256
3. Freathy RM, Bennett AJ, Ring SM et al (2009) Type 2 diabetes risk alleles are associated with reduced size at birth. Diabetes 58:1428-1433
4. Butler AE, Janson J, Bonner-Weir S, Ritzel R, Rizza RA, Butler PC (2003) Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes 52:102-110
5. Weir GC, Bonner-Weir S (2004) Five stages of evolving beta-cell dysfunction during progression to diabetes. Diabetes 53(Suppl 3): S16-S21
6. Ritzel RA, Butler AE, Rizza RA, Veldhuis JD, Butler PC (2006) Relationship between beta-cell mass and fasting blood glucose concentration in humans. Diabetes Care 29:717-718
7. Dor Y, Brown J, Martinez OI, Melton DA (2004) Adult pancreatic beta-cells are formed by self-duplication rather than stem-cell differentiation. Nature 429:41-46
8. Bonner-Weir S (2001) Beta-cell turnover: its assessment and implications. Diabetes 50(Suppl 1):S20-S24
9. Finegood DT, Scaglia L, Bonner-Weir S (1995) Dynamics of betacell mass in the growing rat pancreas. Estimation with a simple mathematical model. Diabetes 44:249-256
10. Bock T, Pakkenberg B, Buschard K (2003) Increased islet volume but unchanged islet number in ob/ob mice. Diabetes 52:1716-1722
11. Butler PC, Meier JJ, Butler AE, Bhushan A (2007) The replication of beta cells in normal physiology, in disease and for therapy. Nat Clin Pract Endocrinol Metab 3:758-768
12. Rahier J, Guiot Y, Goebbels RM, Sempoux C, Henquin JC (2008) Pancreatic beta cell mass in European subjects with type 2 diabetes. Diabetes, Obesity and Metabolism 10:32-42
13. Meier JJ, Butler AE, Saisho Y et al (2008) Beta-cell replication is the primary mechanism subserving the postnatal expansion of beta-cell mass in humans. Diabetes 57:1584-1594
14. Teta M, Long SY, Wartschow LM, Rankin MM, Kushner JA (2005) Very slow turnover of beta-cells in aged adult mice. Diabetes 54:2557-2567
15. Xu X, D'Hoker J, Stange G et al (2008) Beta cells can be generated from endogenous progenitors in injured adult mouse pancreas. Cell 132:197-207
16. Basu R, Breda E, Oberg AL et al (2003) Mechanisms of the ageassociated deterioration in glucose tolerance: contribution of alterations in insulin secretion, action, and clearance. Diabetes 52:1738-1748
17. Gems D, Partridge L (2008) Stress-response hormesis and aging: "that which does not kill us makes us stronger". Cell Metab 7: 200-203
18. Harman D (1956) Aging: a theory based on free radical and radiation chemistry. J Gerontol 11:298-300
19. Bonawitz ND, Shadel GS (2007) Rethinking the mitochondrial theory of aging: the role of mitochondrial gene expression in lifespan determination. Cell Cycle 6:1574-1578
20. Hastie ND, Dempster M, Dunlop MG, Thompson AM, Green DK, Allshire RC (1990) Telomere reduction in human colorectal carcinoma and with ageing. Nature 346:866-868
21. Takubo K, Nakamura K, Izumiyama N et al (2000) Telomere shortening with aging in human liver. J Gerontol A Biol Sci Med Sci 55:B533-B536
22. Spalding KL, Bhardwaj RD, Buchholz BA, Druid H, Frisen J (2005) Retrospective birth dating of cells in humans. Cell 122: 133-143
23. Benavides SH, Monserrat AJ, Farina S, Porta EA (2002) Sequential histochemical studies of neuronal lipofuscin in human cerebral cortex from the first to the ninth decade of life. Arch Gerontol Geriatr 34:219-231
24. Schmucker DL, Sachs H (2002) Quantifying dense bodies and lipofuscin during aging: a morphologist's perspective. Arch Gerontol Geriatr 34:249-261
25. Terman A, Dalen H, Eaton JW, Neuzil J, Brunk UT (2004) Aging of cardiac myocytes in culture: oxidative stress, lipofuscin accumulation, and mitochondrial turnover. Ann N YAcad Sci 1019:70-77
26. Cnop M, Grupping A, Hoorens A, Bouwens L, Pipeleers-Marichal M, Pipeleers D (2000) Endocytosis of low-density lipoprotein by human pancreatic beta cells and uptake in lipid-storing vesicles, which increase with age. Am J Pathol 156:237-244
27. Denk W, Horstmann H (2004) Serial block-face scanning electron microscopy to reconstruct three-dimensional tissue nanostructure. PLoS Biol 2:e329
28. De Duve C, Pressman BC, Gianetto R, Wattiaux R, Appelmans F (1955) Tissue fractionation studies. 6. Intracellular distribution patterns of enzymes in rat-liver tissue. Biochem J 60:604-617
29. Mann DM, Yates PO, Stamp JE (1978) The relationship between lipofuscin pigment and ageing in the human nervous system. J Neurol Sci 37:83-93
30. Sulzer D, Mosharov E, Talloczy Z, Zucca FA, Simon JD, Zecca L (2008) Neuronal pigmented autophagic vacuoles: lipofuscin, neuromelanin, and ceroid as macroautophagic responses during aging and disease. J Neurochem 106:24-36
31. Savitha S, Naveen B, Panneerselvam C (2007) Carnitine and lipoate ameliorates lipofuscin accumulation and monoamine oxidase activity in aged rat heart. Eur J Pharmacol 574:61-65
32. Porta E, Llesuy S, Monserrat AJ, Benavides S, Travacio M (1995) Changes in cathepsin B and lipofuscin during development and aging in rat brain and heart. Gerontology 41(Suppl 2):81-93
33. Seehafer SS, Pearce DA (2006) You say lipofuscin, we say ceroid: defining autofluorescent storage material. Neurobiol Aging 27: 576-588
34. Kurz T, Terman A, Brunk UT (2007) Autophagy, ageing and apoptosis: the role of oxidative stress and lysosomal iron. Arch Biochem Biophys 462:220-230
35. Borg LA, Schnell AH (1986) Lysosomes and pancreatic islet function: intracellular insulin degradation and lysosomal transformations. Diabetes Res 3:277-285
36. Grupping AY, Cnop M, Van Schravendijk CF, Hannaert JC, Van Berkel TJ, Pipeleers DG (1997) Low density lipoprotein binding and uptake by human and rat islet beta cells. Endocrinology 138:4064-4068
37. Scharfmann R (2008) Expanding human beta cells. Diabetologia 51:692-693
38. Parnaud G, Bosco D, Berney T et al (2008) Proliferation of sorted human and rat beta cells. Diabetologia 51:91-100
39. Rankin MM, Kushner JA (2009) Adaptive beta-cell proliferation is severely restricted with advanced age. Diabetes 58:1365-1372
40. Menge BA, Tannapfel A, Belyaev O et al (2008) Partial pancreatectomy in adult humans does not provoke beta-cell regeneration. Diabetes 57:142-149
41. Peshavaria M, Larmie BL, Lausier J et al (2006) Regulation of pancreatic beta-cell regeneration in the normoglycemic 60% partial-pancreatectomy mouse. Diabetes 55:3289-3298
42. Tschen SI, Dhawan S, Gurlo T, Bhushan A (2009) Age-dependent decline in beta-cell proliferation restricts the capacity of beta-cell regeneration in mice. Diabetes 58:1312-1320
43. Maedler K, Schumann DM, Schulthess F et al (2006) Aging correlates with decreased beta-cell proliferative capacity and enhanced sensitivity to apoptosis: a potential role for Fas and pancreatic duodenal homeobox-1. Diabetes 55:2455-2462
44. Yoon KH, Ko SH, Cho JH et al (2003) Selective beta-cell loss and alpha-cell expansion in patients with type 2 diabetes mellitus in Korea. J Clin Endocrinol Metab 88:2300-2308
45. Parsons JA, Brelje TC, Sorenson RL (1992) Adaptation of islets of Langerhans to pregnancy: increased islet cell proliferation and insulin secretion correlates with the onset of placental lactogen secretion. Endocrinology 130:1459-1466
46. Bouwens L, Rooman I (2005) Regulation of pancreatic beta-cell mass. Physiol Rev 85:1255-1270
47. Bonner-Weir S, Weir GC (2005) New sources of pancreatic betacells. Nat Biotechnol 23:857-861
48. Reers C, Erbel S, Esposito I et al (2009) Impaired islet turnover in human donor pancreata with aging. Eur J Endocrinol 160:185-191
49. Terman A, Brunk UT (2006) Oxidative stress, accumulation of biological 'garbage', and aging. Antioxid Redox Signal 8: 197-204
50. Ihm SH, Matsumoto I, Sawada T et al (2006) Effect of donor age on function of isolated human islets. Diabetes 55:1361-1368