Differential effects on β-cell mass by disruption of Bardet-Biedl syndrome or Alstrom syndrome genes

Human Molecular Genetics

Volumn 25, Issue 1, 2016, Pages 57-68

  Lodh, Sukanya ^a   Hostelley, Timothy L ^a   Leitch, Carmen C ^a   O'Hare, Elizabeth A ^a   Zaghloul, Norann A ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALSTROM SYNDROME; ANIMAL CELL; ARTICLE; BARDET BIEDL SYNDROME; BETA CELL MASS; CELL COUNT; CELL CULTURE; CELL DEATH; CELL DIFFERENTIATION; CELL PROLIFERATION; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; DISEASE ASSOCIATION; EMBRYO; ENDOCRINE CELL; GENE DISRUPTION; GENETIC REGULATION; GENETIC SUSCEPTIBILITY; GLUCOSE HOMEOSTASIS; IN SITU HYBRIDIZATION; LONG TERM EXPOSURE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROMOTER REGION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RISK FACTOR; WESTERN BLOTTING; ZEBRA FISH; ANIMAL; DISEASE MODEL; GENETICS; HYPERGLYCEMIA; PATHOLOGY;

BBS1 PROTEIN, ZEBRAFISH; BBS4 PROTEIN, ZEBRAFISH; GLUCOSE; MICROTUBULE ASSOCIATED PROTEIN; MORPHOLINO OLIGONUCLEOTIDE; ZEBRAFISH PROTEIN;

ALSTROM SYNDROME; ANIMALS; BARDET-BIEDL SYNDROME; CELL DEATH; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; GLUCOSE; HYPERGLYCEMIA; INSULIN-SECRETING CELLS; MICROTUBULE-ASSOCIATED PROTEINS; MORPHOLINOS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84962184413     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddv447     Document Type: Article

References (45)

1. Krishnamurthy, J., Ramsey, M.R., Ligon, K.L., Torrice, C., Koh, A., Bonner-Weir, S. and Sharpless, N.E. (2006) p16(INK4a) induces an age-dependent decline in islet regenerative potential. Nature, 443, 453-457
2. Rosen, E.D., Kulkarni, R.N., Sarraf, P., Ozcan, U., Okada, T., Hsu, C.H., Eisenman, D., Magnuson, M.A., Gonzalez, F.J., Kahn, C.R. et al. (2003) Targeted elimination of peroxisome proliferator-activated receptor gamma in beta cells leads to abnormalities in islet mass without compromising glucose homeostasis. Mol. Cell Biol., 23, 7222-7229
3. SosaPineda, B., Chowdhury, K., Torres, M., Oliver, G. and Gruss, P. (1997) The Pax4 gene is essential for differentiation of insulin-producing beta cells in the mammalian pancreas. Nature, 386, 399-402
4. Stoffers, D.A., Ferrer, J., Clarke, W.L. and Habener, J.F. (1997) Early-onset type-II diabetes mellitus (MODY4) linked to IPF1. Nat. Genet., 17, 138-139
5. Stoffers, D.A., Stanojevic, V. and Habener, J.F. (1998) Insulin promoter factor-1 gene mutation linked to early-onset type 2 diabetes mellitus directs expression of a dominant negative isoprotein. J. Clin. Invest., 102, 232-241
6. Yamagata, K., Nammo, T., Moriwaki, M., Ihara, A., Iizuka, K., Yang, Q., Satoh, T., Li, M., Uenaka, R., Okita, K. et al. (2002) Overexpression of dominant-negative mutant hepatocyte nuclear factor-1 alpha in pancreatic beta-cells causes abnormal islet architecture with decreased expression of E-cadherin, reduced beta-cell proliferation, and diabetes. Diabetes, 51, 114-123
7. Adams, M., Smith, U.M., Logan, C.V. and Johnson, C.A. (2008) Recent advances in the molecular pathology, cell biology and genetics of ciliopathies. J. Med. Genet., 45, 257-267
8. Badano, J.L., Mitsuma, N., Beales, P.L. and Katsanis, N. (2006) The ciliopathies: an emerging class of human genetic disorders. Annu. Rev. Genomics Hum. Genet., 7, 125-148
9. Baker, K. and Beales, P.L. (2009) Making sense of cilia in disease: the human cilioplathies. Am. J. Med. Genet. C Semin. Med. Genet., 151C, 281-295
10. Cardenas-Rodriguez, M. and Badano, J.L. (2009) Ciliary biology: understanding the cellular and genetic basis of human cillopathies. Am. J. Med. Genet. C Semin. Med. Genet., 151C, 263-280
11. Muller, J., Stoetzel, C., Vincent, M.C., Leitch, C.C., Laurier, V., Danse, J.M., Helle, S., Marion, V., Bennouna-Greene, V., Vicaire, S. et al. (2010) Identification of 28 novel mutations in the Bardet-Biedl syndrome genes: the burden of private mutations in an extensively heterogeneous disease. Hum. Genet., 127, 583-593
12. Bettini, V., Maffei, P., Pagano, C., Romano, S., Milan, G., Favaretto, F., Marshall, J.D., Paisey, R., Scolari, F., Greggio, N. A. et al. (2012) The progression from obesity to type 2 diabetes in Alstrom syndrome. Pediatr. Diabetes, 13, 59-67
13. Forsythe, E. and Beales, P.L. (2013) Bardet-Biedl syndrome. Eur. J. Hum. Genet., 21, 8-13
14. Girard, D. and Petrovsky, N. (2011) Alstrom syndrome: insights into the pathogenesis of metabolic disorders. Nat. Rev. Endocrinol., 7, 77-88
15. Beales, P.L., Elcioglu, N., Woolf, A.S., Parker, D. and Flinter, F.A. (1999) New criteria for improved diagnosis of Bardet-Biedl syndrome: results of a population survey. J. Med. Genet., 36, 437-446
16. Feuillan, P.P., Ng, D., Han, J.C., Sapp, J.C., Wetsch, K., Spaulding, E., Zheng, Y.C., Caruso, R.C., Brooks, B.P., Johnston, J.J. et al. (2011) Patients with Bardet-Biedl Syndrome have hyperleptinemia suggestive of leptin resistance. J. Clin. Endocrinol. Metab., 96, E528-E535
17. Grace, C., Beales, P., Summerbell, C., Jebb, S.A., Wright, A., Parker, D. and Kopelman, P. (2003) Energy metabolism in Bardet-Biedl syndrome. Int. J. Obes. Relat. Metab. Disord., 27, 1319-1324
18. Marshall, J.D., Bronson, R.T., Collin, G.B., Nordstrom, A.D., Maffei, P., Paisey, R.B., Carey, C., MacDermott, S., Russell-Eggitt, I., Shea, S.E. et al. (2005) New Alstrom syndrome phenotypes based on the evaluation of 182 cases. Arch. Intern. Med., 165, 675-683
19. Marshall, J.D., Maffei, P., Collin, G.B. and Naggert, J.K. (2011) Alstrom Syndrome: Genetics and Clinical Overview. Curr. Genomics, 12, 225-235
20. Minton, J.A.L., Owen, K.R., Ricketts, C.J., Crabtree, N., Shaikh, G., Ehtisham, S., Porter, J.R., Carey, C., Hodge, D., Paisey, R. et al. (2006) Syndromic obesity and diabetes: changes in body composition with age and mutation analysis of ALMS1 in 12 United Kingdom kindreds with Alstrom syndrome. J. Clin. Endocrinol. Metab., 91, 3110-3116
21. Argenton, F., Zecchin, E. and Bortolussi, M. (1999) Early appearance of pancreatic hormone-expressing cells in the zebrafish embryo. Mech. Dev., 87, 217-221
22. Biemar, F., Argenton, F., Schmidtke, R., Epperlein, S., Peers, B. and Driever, W. (2001) Pancreas development in zebrafish: early dispersed appearance of endocrine hormone expressing cells and their convergence to form the definitive islet. Dev. Biol., 230, 189-203
23. Lin, J.W., Biankin, A.V., Horb, M.E., Ghosh, B., Prasad, N.B., Yee, N.S., Park, M.A. and Leach, S.D. (2004) Differential requirement for ptf1a in endocrine and exocrine lineages of developing zebrafish pancreas. Dev. Biol., 270, 474-486
24. Yee, N.S., Yusuff, S. and Pack, M. (2001) Zebrafish pdx1 morphant displays defects in pancreas development and digestive organ chirality, and potentially identifies a multipotent pancreas progenitor cell. Genesis, 30, 137-140
25. Zecchin, E., Mavropoulos, A., Devos, N., Filippi, A., Tiso, N., Meyer, D., Peers, B., Bortolussi, M. and Argenton, F. (2004) Evolutionary conserved role of ptf1a in the specification of exocrine pancreatic fates. Dev. Biol., 268, 174-184
26. Leitch, C.C., Lodh, S., Prieto-Echaguee, V., Badano, J.L. and Zaghloul, N.A. (2014) Basal body proteins regulate Notch signaling through endosomal trafficking. J. Cell Sci., 127, 2407-2419
27. Pisharath, H., Rhee, J.M., Swanson, M.A., Leach, S.D. and Parsons, M.J. (2007) Targeted ablation of beta cells in the embryonic zebrafish pancreas using E. coli nitroreductase. Mech. Dev., 124, 218-229
28. Tiso, N., Moro, E. and Argenton, F. (2009) Zebrafish pancreas development. Mol. Cell. Endocrinol., 312, 24-30
29. Parsons, M.J., Pisharath, H., Yusuff, S., Moore, J.C., Siekmann, A.F., Lawson, N. and Leach, S.D. (2009) Notch-responsive cells initiate the secondary transition in larval zebrafish pancreas. Mech. Dev., 126, 898-912
30. Robu, M.E., Larson, J.D., Nasevicius, A., Beiraghi, S., Brenner, C., Farber, S.A. and Ekker, S.C. (2007) p53 activation by knockdown technologies. PLoS Genet., 3, 787-801
31. Hwang, W.Y., Fu, Y., Reyon, D., Maeder, M.L., Tsai, S.Q., Sander, J.D., Peterson, R.T., Yeh, J.R.J. and Joung, J.K. (2013) Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat. Biotechnol., 31, 227-229
32. Hwang, W.Y., Fu, Y., Reyon, D., Maeder, M.L., Tsai, S.Q., Sander, J.D., Peterson, R.T., Yeh, J.R.J. and Joung, J.K. (2013) Efficient in vivo genome editing using RNA-guided nucleases. Nat. Biotechnol., 31, 227-229
33. Maddison, L.A. and Chen, W. (2012) Nutrient excess stimulates beta-cell neogenesis in zebrafish. Diabetes, 61, 2517-2524
34. Lee, B.H., Liu, J., Wong, D., Srinivasan, S. and Ashrafi, K. (2011) Hyperactive neuroendocrine secretion causes size, feeding, and metabolic defects of C. elegans Bardet-Biedl syndrome mutants. PLoS Biol., 9, e1001219
35. Gerdes, J.M., Christou-Savina, S., Xiong, Y., Moede, T., Moruzzi, N., Karlsson-Edlund, P., Leibiger, B., Leibiger, I.B., Ostenson, C.-G., Beales, P.L. et al. (2014) Ciliary dysfunction impairs beta-cell insulin secretion and promotes development of type 2 diabetes in rodents. Nat. Commun., 5, doi: 10.1038/ncomms6308
36. Meier, J.J. and Bonadonna, R.C. (2013) Role of reduced beta-cell mass versus impaired beta-cell function in the pathogenesis of type 2 diabetes. Diabetes Care, 36, S113-S119
37. Gerdes, J.M., Liu, Y., Zaghloul, N.A., Leitch, C.C., Lawson, S.S., Kato, M., Beachy, P.A., Beales, P.L., Demartino, G.N., Fisher, S. et al. (2007) Disruption of the basal body compromises proteasomal function and perturbs intracellular Wnt response. Nat. Genet., 39, 1350-1360
38. Goetz, S.C. and Anderson, K.V. (2010) The primary cilium: a signalling centre during vertebrate development. Nat. Rev. Genet., 11, 331-344
39. Ocbina, P. and Anderson, K. (2008) Intraflagellar transport, cilia, and mammalian Hedgehog signaling: analysis in mouse embryonic fibroblasts. Dev. Dyn., 237, 2030-2038
40. Rohatgi, R., Milenkovic, L. and Scott, M. (2007) Patched1 regulates hedgehog signaling at the primary cilium. Science, 317, 372-376
41. Boehlke, C., Kotsis, F., Patel, V., Braeg, S., Voelker, H., Bredt, S., Beyer, T., Janusch, H., Hamann, C., Goedel, M. et al. (2010) Primary cilia regulate mTORC1 activity and cell size through Lkb1. Nat. Cell Biol., 12, 1115.-1126
42. Granot, Z., Swisa, A., Magenheim, J., Stolovich-Rain, M., Fujimoto, W., Manduchi, E., Miki, T., Lennerz, J.K., Stoeckert, C.J. Jr, Meyuhas, O. et al. (2009) LKB1 regulates pancreatic beta cell size, polarity, and function. Cell Metab., 10, 296-308
43. Zhu, D., Shi, S., Wang, H. and Liao, K. (2009) Growth arrest induces primary-cilium formation and sensitizes IGF-1-receptor signaling during differentiation induction of 3T3-L1 preadipocytes. J. Cell Sci., 122, 2760-2768
44. Thisse, C. and Thisse, B. (2008) High-resolution in situ hybridization to whole-mount zebrafish embryos. Nat. Protoc., 3, 59-69
45. Varshney, G.K., Pei, W., LaFave, M.C., Idol, J., Xu, L., Gallardo, V., Carrington, B., Bishop, K., Jones, M., Li, M. et al. (2015) Highthroughput gene targeting and phenotyping in zebrafish using CRISPR/Cas9. Genome Res., 25, 1030-1042