Diabetic pdx1-mutant zebrafish show conserved responses to nutrient overload and anti-glycemic treatment

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Kimmel, Robin A ^a   Dobler, Stefan ^a   Schmitner, Nicole ^a   Walsen, Tanja ^a,b   Freudenblum, Julia ^a   Meyer, Dirk ^a  

^a UNIVERSITY OF INNSBRUCK   (Austria)

^b INNSBRUCK MEDICAL UNIVERSITY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIDIABETIC AGENT; GLUCOSE; HOMEODOMAIN PROTEIN; PANCREATIC AND DUODENAL HOMEOBOX 1 PROTEIN; STOP CODON; TRANSACTIVATOR PROTEIN;

AMINO ACID SEQUENCE; ANIMAL; ANIMAL FOOD; BODY SIZE; CELL SURVIVAL; CHEMISTRY; DIABETES MELLITUS, TYPE 2; DISEASE MODEL; DRUG EFFECTS; GENE INACTIVATION; GENETICS; GENOTYPE; METABOLISM; MOLECULAR GENETICS; MUTATION; PANCREAS ISLET; PANCREAS ISLET BETA CELL; PATHOLOGY; SEQUENCE ALIGNMENT; STOP CODON; TRANSGENIC ANIMAL; ZEBRA FISH;

AMINO ACID SEQUENCE; ANIMAL FEED; ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BODY SIZE; CELL SURVIVAL; CODON, NONSENSE; DIABETES MELLITUS, TYPE 2; DISEASE MODELS, ANIMAL; GENE KNOCKOUT TECHNIQUES; GENOTYPE; GLUCOSE; HOMEODOMAIN PROTEINS; HYPOGLYCEMIC AGENTS; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; MOLECULAR SEQUENCE DATA; MUTATION; SEQUENCE ALIGNMENT; TRANS-ACTIVATORS; ZEBRAFISH;

EID: 84941992117     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep14241     Document Type: Article

References (69)

1. Doria, A., Patti, M. E. & Kahn, C. R. Te emerging genetic architecture of type 2 diabetes. Cell Metab 8, 186-200 (2008).
2. Ashcrof, F. M. & Rorsman, P. Diabetes mellitus and the beta cell: the last ten years. Cell 148, 1160-1171 (2012).
3. Klupa, T., Skupien, J. & Malecki, M. T. Monogenic models: what have the single gene disorders taught us? Curr Diab Rep 12, 659-666 (2012).
4. Naylor, R. N., Greeley, S. A., Bell, G. I. & Philipson, L. H. Genetics and pathophysiology of neonatal diabetes mellitus. J Diabetes Investig 2, 158-169 (2011).
5. Seth, A., Stemple, D. L. & Barroso, I. Te emerging use of zebrafsh to model metabolic disease. Dis Model Mech 6, 1080-1088 (2013).
6. Jorgens, K., Hillebrands, J. L., Hammes, H. P. & Kroll, J. Zebrafsh: a model for understanding diabetic complications. Exp Clin Endocrinol Diabetes 120, 186-187 (2012).
7. Dalgin, G. & Prince, V. E. Diferential levels of Neurod establish zebrafsh endocrine pancreas cell fates. Dev Biol 402, 81-97 (2015).
8. Gleeson, M., Connaughton, V. & Arneson, L. S. Induction of hyperglycaemia in zebrafsh (Danio rerio) leads to morphological changes in the retina. Acta Diabetol 44, 157-163 (2007).
9. Alvarez, Y. et al. Predominant cone photoreceptor dysfunction in a hyperglycaemic model of non-proliferative diabetic retinopathy. Dis Model Mech 3, 236-245 (2010).
10. Jorgens, K. et al. High tissue glucose alters intersomitic blood vessels in zebrafsh via methylglyoxal targeting the VEGF receptor signalling cascade. Diabetes 64, 213-25 (2015).
11. Olsen, A. S., Sarras, Jr. M. P. & Intine, R. V. Limb regeneration is impaired in an adult zebrafsh model of diabetes mellitus. Wound Repair Regen 18, 532-542 (2010).
12. Curado, S. et al. Conditional targeted cell ablation in zebrafsh: a new tool for regeneration studies. Dev Dyn 236, 1025-1035 (2007).
13. Moss, J. B. et al. Regeneration of the pancreas in adult zebrafsh. Diabetes 58, 1844-1851 (2009).
14. Ninov, N. et al. Metabolic regulation of cellular plasticity in the pancreas. Curr Biol 23, 1242-1250 (2013).
15. Pisharath, H., Rhee, J. M., Swanson, M. A., Leach, S. D. & Parsons, M. J. Targeted ablation of beta cells in the embryonic zebrafsh pancreas using E. coli nitroreductase. Mech Dev 124, 218-229 (2007).
16. Fujimoto, K. et al. Autophagy regulates pancreatic beta cell death in response to Pdx1 defciency and nutrient deprivation. J Biol Chem 284, 27664-27673 (2009).
17. Babu, D. A., Deering, T. G. & Mirmira, R. G. A feat of metabolic proportions: Pdx1 orchestrates islet development and function in the maintenance of glucose homeostasis. Mol Genet Metab 92, 43-55 (2007).
18. Hani, E. H. et al. Defective mutations in the insulin promoter factor-1 (IPF-1) gene in late-onset type 2 diabetes mellitus. J Clin Invest 104, R41-48 (1999).
19. Macfarlane, W. M. et al. Missense mutations in the insulin promoter factor-1 gene predispose to type 2 diabetes. J Clin Invest 104, R33-39 (1999).
20. Stofers, D. A., Ferrer, J., Clarke, W. L. & Habener, J. F. Early-onset type-II diabetes mellitus (MODY4) linked to IPF1. Nat Genet 17, 138-139 (1997).
21. Stofers, D. A., Zinkin, N. T., Stanojevic, V., Clarke, W. L. & Habener, J. F. Pancreatic agenesis attributable to a single nucleotide deletion in the human IPF1 gene coding sequence. Nat Genet 15, 106-110 (1997).
22. Nicolino, M. et al. A novel hypomorphic PDX1 mutation responsible for permanent neonatal diabetes with subclinical exocrine defciency. Diabetes 59, 733-740 (2010).
23. De Franco, E. et al. Biallelic PDX1 (insulin promoter factor 1) mutations causing neonatal diabetes without exocrine pancreatic insufciency. Diabet Med 30, e197-200 (2013).
24. Kimmel, R. A., Onder, L., Wilfnger, A., Ellertsdottir, E. & Meyer, D. Requirement for Pdx1 in specifcation of latent endocrine progenitors in zebrafsh. BMC biology 9, 75 (2011).
25. Jurczyk, A. et al. Dynamic glucoregulation and mammalian-like responses to metabolic and developmental disruption in zebrafsh. Gen Comp Endocrinol 170, 334-345 (2011).
26. Milewski, W. M., Duguay, S. J., Chan, S. J. & Steiner, D. F. Conservation of PDX-1 structure, function, and expression in zebrafsh. Endocrinology 139, 1440-1449 (1998).
27. Kettleborough, R. N. et al. A systematic genome-wide analysis of zebrafsh protein-coding gene function. Nature 496, 494-497 (2013).
28. Lawrence, C. Te husbandry of zebrafsh (Danio rerio): A review. Aquaculture 269, 1-20 (2007).
29. Ahlgren, U., Jonsson, J. & Edlund, H. Te morphogenesis of the pancreatic mesenchyme is uncoupled from that of the pancreatic epithelium in IPF1/PDX1-defcient mice. Development 122, 1409-1416 (1996).
30. Jonsson, J., Carlsson, L., Edlund, T. & Edlund, H. Insulin-promoter-factor 1 is required for pancreas development in mice. Nature 371, 606-609 (1994).
31. Ofeld, M. F. et al. PDX-1 is required for pancreatic outgrowth and diferentiation of the rostral duodenum. Development 122, 983-995 (1996).
32. Yee, N. S., Lorent, K. & Pack, M. Exocrine pancreas development in zebrafsh. Dev Biol 284, 84-101 (2005).
33. Kimmel, R. A. & Meyer, D. Molecular regulation of pancreas development in zebrafsh. Methods Cell Biol 100, 261-280 (2010).
34. Parsons, M. J. et al. Notch-responsive cells initiate the secondary transition in larval zebrafsh pancreas. Mech Dev 126, 898-912 (2009).
35. Wang, Y., Rovira, M., Yusuf, S. & Parsons, M. J. Genetic inducible fate mapping in larval zebrafsh reveals origins of adult insulin-producing {beta}-cells. Development 138, 609-617 (2011).
36. Obholzer, N. et al. Vesicular glutamate transporter 3 is required for synaptic transmission in zebrafsh hair cells. J Neurosci 28, 2110-2118 (2008).
37. Yang, Y. P., Torel, F., Boyer, D. F., Herrera, P. L. & Wright, C. V. Context-specifc alpha-to-beta-cell reprogramming by forced Pdx1 expression. Genes Dev 25, 1680-1685 (2011).
38. Gannon, M. et al. pdx-1 function is specifcally required in embryonic beta cells to generate appropriate numbers of endocrine cell types and maintain glucose homeostasis. Dev Biol 314, 406-417 (2008).
39. Ahlgren, U., Jonsson, J., Jonsson, L., Simu, K. & Edlund, H. beta-cell-specifc inactivation of the mouse Ipf1/Pdx1 gene results in loss of the beta-cell phenotype and maturity onset diabetes. Genes Dev 12, 1763-1768 (1998).
40. Gao, T. et al. Pdx1 maintains beta cell identity and function by repressing an alpha cell program. Cell Metab 19, 259-271 (2014).
41. Yee, N. S., Yusuf, S. & Pack, M. Zebrafsh pdx1 morphant displays defects in pancreas development and digestive organ chirality, and potentially identifes a multipotent pancreas progenitor cell. Genesis 30, 137-140 (2001).
42. Ninov, N., Borius, M. & Stainier, D. Y. Diferent levels of Notch signaling regulate quiescence, renewal and diferentiation in pancreatic endocrine progenitors. Development 139, 1557-1567 (2012).
43. Huang, W. et al. Retinoic acid plays an evolutionarily conserved and biphasic role in pancreas development. Dev Biol 394, 83-93 (2014).
44. Gut, P. et al. Whole-organism screening for gluconeogenesis identifes activators of fasting metabolism. Nat Chem Biol 9, 97-104 (2013).
45. Eames, S. C., Philipson, L. H., Prince, V. E. & Kinkel, M. D. Blood sugar measurement in zebrafsh reveals dynamics of glucose homeostasis. Zebrafsh 7, 205-213 (2010).
46. Dornhorst, A. Insulinotropic meglitinide analogues. Lancet 358, 1709-1716 (2001).
47. Rhodes, C. J. Type 2 diabetes-a matter of beta-cell life and death? Science 307, 380-384 (2005).
48. Oka, T. et al. Diet-induced obesity in zebrafsh shares common pathophysiological pathways with mammalian obesity. BMC Physiol 10, 21 (2010).
49. Tschen, S. I., Dhawan, S., Gurlo, T. & Bhushan, A. Age-dependent decline in beta-cell proliferation restricts the capacity of beta-cell regeneration in mice. Diabetes 58, 1312-1320 (2009).
50. Butler, A. E. et al. Beta-cell defcit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes 52, 102-110 (2003).
51. Halban, P. A. et al. beta-cell failure in type 2 diabetes: postulated mechanisms and prospects for prevention and treatment. J Clin Endocrinol Metab 99, 1983-1992 (2014).
52. Maddison, L. A. & Chen, W. Nutrient excess stimulates beta-cell neogenesis in zebrafsh. Diabetes 61, 2517-2524 (2012).
53. Brereton, M. F. et al. Reversible changes in pancreatic islet structure and function produced by elevated blood glucose. Nat Commun 5, 4639 (2014).
54. Weir, G. C., Aguayo-Mazzucato, C. & Bonner-Weir, S. beta-cell dediferentiation in diabetes is important, but what is it? Islets 5, 233-237 (2013).
55. Lancman, J. J. et al. Specifcation of hepatopancreas progenitors in zebrafsh by hnf1ba and wnt2bb. Development 140, 2669-2679 (2013).
56. Pan, F. C. & Wright, C. Pancreas organogenesis: from bud to plexus to gland. Dev Dyn 240, 530-565 (2011).
57. Wendik, B., Maier, E. & Meyer, D. Zebrafsh mnx genes in endocrine and exocrine pancreas formation. Dev Biol 268, 372-383 (2004).
58. Hale, M. A. et al. Te homeodomain protein PDX1 is required at mid-pancreatic development for the formation of the exocrine pancreas. Dev Biol 286, 225-237 (2005).
59. Tsuji, N. et al. Whole organism high content screening identifes stimulators of pancreatic beta-cell proliferation. PLoS ONE 9, e104112 (2014).
60. Fujimoto, K. & Polonsky, K. S. Pdx1 and other factors that regulate pancreatic beta-cell survival. Diabetes Obes Metab 11 Suppl 4, 30-37 (2009).
61. Ardestani, A. et al. MST1 is a key regulator of beta cell apoptosis and dysfunction in diabetes. Nat Med 20, 385-397 (2014).
62. Guo, S. et al. Inactivation of specifc beta cell transcription factors in type 2 diabetes. J Clin Invest 123, 3305-3316 (2013).
63. Workeneh, B. & Bajaj, M. Te regulation of muscle protein turnover in diabetes. Int J Biochem Cell Biol 45, 2239-2244 (2013).
64. Elo, B., Villano, C. M., Govorko, D. & White, L. A. Larval zebrafsh as a model for glucose metabolism: expression of phosphoenolpyruvate carboxykinase as a marker for exposure to anti-diabetic compounds. J Mol Endocrinol 38, 433-440 (2007).
65. Westerfeld, M. Te Zebrafsh Book. Eugene: University of Oregon Press (1995).
66. Parichy, D. M., Elizondo, M. R., Mills, M. G., Gordon, T. N. & Engeszer, R. E. Normal table of postembryonic zebrafsh development: staging by externally visible anatomy of the living fsh. Dev Dyn 238, 2975-3015 (2009).
67. Akhtar, T., Li, J., Olden, T. & Wallace, K. N. Use of phospholipase A2 for antigen retrieval in zebrafsh whole-mount immunohistochemistry. Zebrafsh 6, 223-227 (2009).
68. Forster, B., Van De Ville, D., Berent, J., Sage, D. & Unser, M. Complex wavelets for extended depth-of-feld: a new method for the fusion of multichannel microscopy images. Microsc Res Tech 65, 33-42 (2004).
69. Mutterer, J. & Zinck, E. Quick-and-clean article fgures with FigureJ. J Microsc 252, 89-91 (2013).