Noninvasive in vivo imaging of embryonic β-cell development in the anterior chamber of the eye

References

• Sandovici I, Hammerle CM, Ozanne SE, Constancia M. Developmental and environmental epigenetic programming of the endocrine pancreas: consequences for type 2 diabetes. Cell Mol Life Sci 2013; 70:1575-95; PMID:23463236; http://dx.doi.org/10.1007/s00018-013-1297-1
   Google Scholar
• Dor Y, Brown J, Martinez OI, Melton DA. Adult pancreatic beta-cells are formed by self-duplication rather than stem-cell differentiation. Nature 2004; 429:41-6; PMID:15129273; http://dx.doi.org/10.1038/natu-re02520
   Google Scholar
• Lango H, Consortium UKTDG, Palmer CN, Morris AD, Zeggini E, Hattersley AT, McCarthy MI, Frayling TM, Weedon MN. Assessing the combined impact of 18 common genetic variants of modest effect sizes on type 2 diabetes risk. Diabetes 2008; 57:3129-35; PMID:18591388; http://dx.doi.org/10.2337/db08-0504
   Google Scholar
• Morris AP, Voight BF, Teslovich TM, Ferreira T, Segre AV, Steinthorsdottir V, Strawbridge RJ, Khan H, Grallert H, Mahajan A, et al. Large-scale association analysis provides insights into the genetic architecture and pathophysiology of type 2 diabetes. Nat Gen 2012; 44:981-90; PMID:22885922; http://dx.doi.org/10.1038/ng.2383
   Google Scholar
• Hellerström C, Swenne I. Functional maturation and proliferation of fetal pancreatic beta-cells. Diabetes 1991; 40(Suppl 2):89-93; PMID:1748274; http://dx.doi.org/10.2337/diab.40.2.S89
   Google Scholar
• Berney DM, Desai M, Palmer DJ, Greenwald S, Brown A, Hales CN, Berry CL. The effects of maternal protein deprivation on the fetal rat pancreas: major structural changes and their recuperation. J Pathol 1997; 183:109-15; PMID:9370956; http://dx.doi.org/10.1002/(SICI)1096-9896(199709)183:1%3c109::AID-PATH1091%3e3.0.CO;2-B
   Google Scholar
• Dahri S, Snoeck A, Reusens-Billen B, Remacle C, Hoet JJ. Islet function in offspring of mothers on low-protein diet during gestation. Diabetes 1991; 40(Suppl 2):115-20; PMID:1748239; http://dx.doi.org/10.2337/diab.40.2.S115
   Google Scholar
• Dahri S, Reusens B, Remacle C, Hoet JJ. Nutritional influences on pancreatic development and potential links with non-insulin-dependent diabetes. Proc Nutr Soc 1995; 54:345-56; PMID:8524881; http://dx.doi.org/10.1079/PNS19950003
   Google Scholar
• Aldoretta PW, Carver TD, Hay WW. Maturation of glucose-stimulated insulin secretion in fetal sheep. Biol Neonate 1998; 73:375-86; PMID:9618055; http://dx.doi.org/10.1159/000014000
   Google Scholar
• Carver TD, Anderson SM, Aldoretta PW, Hay WW. Effect of low-level basal plus marked “pulsatile” hyperglycemia on insulin secretion in fetal sheep. Am J Physiol 1996; 271:E865-71; PMID:8944673
   Google Scholar
• Ozanne SE, Hales CN. The long-term consequences of intra-uterine protein malnutrition for glucose metabolism. Proc Nutr Soc 1999; 58:615-9; PMID:10604194; http://dx.doi.org/10.1017/S0029665199000804
   Google Scholar
• Petrik J, Reusens B, Arany E, Remacle C, Coelho C, Hoet JJ, Hill DJ. A low protein diet alters the balance of islet cell replication and apoptosis in the fetal and neonatal rat and is associated with a reduced pancreatic expression of insulin-like growth factor-II. Endocrinology 1999; 140:4861-73; PMID:10499546
   Google Scholar
• Snoeck A, Remacle C, Reusens B, Hoet JJ. Effect of a low protein diet during pregnancy on the fetal rat endocrine pancreas. Biol Neonate 1990; 57:107-18; PMID:2178691; http://dx.doi.org/10.1159/000243170
   Google Scholar
• Carver TD, Anderson SM, Aldoretta PA, Esler AL, Hay WW. Glucose suppression of insulin secretion in chronically hyperglycemic fetal sheep. Pediatr Res 1995; 38:754-62; PMID:8552445; http://dx.doi.org/10.1203/00006450-199511000-00020
   Google Scholar
• Van Assche FA, De Prins F, Aerts L, Verjans M. The endocrine pancreas in small-for-dates infants. Br J Obst Gynaecol 1977; 84:751-3; PMID:336076; http://dx.doi.org/10.1111/j.1471-0528.1977.tb12486.x
   Google Scholar
• Dumortier O, Blondeau B, Duvillié B, Reusens B, Bréant B, Remacle C. Different mechanisms operating during different critical time-windows reduce rat fetal beta cell mass due to a maternal low-protein or low-energy diet. Diabetologia 2007; 50:2495-503; PMID:17882398; http://dx.doi.org/10.1007/s00125-007-0811-0
   Google Scholar
• Garofano A, Czernichow P, Breant B. In utero undernutrition impairs rat beta-cell development. Diabetologia 1997; 40:1231-4; PMID:9349607; http://dx.doi.org/10.1007/s001250050812
   Google Scholar
• Winick M. Cellular growth in intrauterine malnutrition. Pediatr Clin North Am 1970; 17:69-78; PMID:5419110
   Google Scholar
• Garofano A, Czernichow P, Bréant B. Effect of ageing on beta-cell mass and function in rats malnourished during the perinatal period. Diabetologia 1999; 42:711-8; PMID:10382591; http://dx.doi.org/10.1007/s00125005-1219
   Google Scholar
• Stanger BZ, Tanaka AJ, Melton DA. Organ size is limited by the number of embryonic progenitor cells in the pancreas but not the liver. Nature 2007; 445:886-91; PMID:17259975; http://dx.doi.org/10.1038/nature05537
   Google Scholar
• Alejandro EU, Gregg B, Wallen T, Kumusoglu D, Meister D, Chen A, Merrins MJ, Satin LS, Liu M, Arvan P, et al. Maternal diet-induced microRNAs and mTOR underlie beta cell dysfunction in offspring. J Clin Invest 2014; 124:4395-410; PMID:25180600; http://dx.doi.org/10.1172/JCI74237
   Google Scholar
• Miralles F, Serup P, Cluzeaud F, Vandewalle A, Czernichow P, Scharfmann R. Characterization of beta cells developed in vitro from rat embryonic pancreatic epithelium. Dev Dyn 1999; 214:116-26; PMID:10030591; http://dx.doi.org/10.1002/(SICI)1097-0177(199902)214:2%3c116::AID-AJA2%3e3.0.CO;2-M
   Google Scholar
• Miralles F, Czernichow P, Scharfmann R. Follistatin regulates the relative proportions of endocrine versus exocrine tissue during pancreatic development. Development 1998; 125:1017-24; PMID:9463348
   Google Scholar
• Bhushan A, Itoh N, Kato S, Thiery J, Czernichow P, Bellusci S, Scharfmann R. Fgf10 is essential for maintaining the proliferative capacity of epithelial progenitor cells during early pancreatic organogenesis. Development 2001; 128:5109-17; PMID:11748146
   Google Scholar
• Huotari M, Miettinen P, Palgi J, Koivisto T, Ustinov J, Harari D, Yarden Y, Otonkoski T. ErbB signaling regulates lineage determination of developing pancreatic islet cells in embryonic organ culture. Endocrinology 2002; 143:4437-46; PMID:12399441; http://dx.doi.org/10.1210/en.2002-220382
   Google Scholar
• Duvillié B, Attali M, Aiello V, Quemeneur E, Scharfmann R. Label-retaining cells in the rat pancreas: location and differentiation potential in vitro. Diabetes 2003; 52:2035-42; PMID:12882920; http://dx.doi.org/10.2337/diabetes.52.8.2035
   Google Scholar
• Speier S, Nyqvist D, Köhler M, Caicedo A, Leibiger IB, Berggren P-O. Noninvasive high-resolution in vivo imaging of cell biology in the anterior chamber of the mouse eye. Nature protocols 2008; 3:1278-86; PMID:18714296; http://dx.doi.org/10.1038/nprot.2008.118
   Google Scholar
• Adeghate E. Host-graft circulation and vascular morphology in pancreatic tissue transplants in rats. Anat Rec 1998; 251:448-59; PMID:9713983; http://dx.doi.org/10.1002/(SICI)1097-0185(199808)251:4%3c448::AID-AR4%3e3.0.CO;2-O
   Google Scholar
• Adeghate E, Ponery AS, Ahmed I, Donáth T. Comparative morphology and biochemistry of pancreatic tissue fragments transplanted into the anterior eye chamber and subcutaneous regions of the rat. Eur J Morphol 2001; 39:257-68; PMID:12221507; http://dx.doi.org/10.1076/ejom.39.5.0257
   Google Scholar
• Speier S, Nyqvist D, Cabrera O, Yu J, Molano RD, Pileggi A, Moede T, Köhler M, Wilbertz J, Leibiger B, et al. Noninvasive in vivo imaging of pancreatic islet cell biology. Nat Med 2008; 14:574-8; PMID:18327249; http://dx.doi.org/10.1038/nm1701
   Google Scholar
• Herrera P-L. Adult insulin- and glucagon-producing cells differentiate from two independent cell lineages. Development 2000; 127:2317-22; PMID:10804174
   Google Scholar
• Madisen L, Zwingman TA, Sunkin SM, Oh SW, Zariwala HA, Gu H, Ng LL, Palmiter RD, Hawrylycz MJ, Jones AR, et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat Neurosci 2010; 13:133-40; PMID:20023653; http://dx.doi.org/10.1038/nn.2467
   Google Scholar
• Cras-Méneur C, Li L, Kopan R, Permutt MA. Presenilins, Notch dose control the fate of pancreatic endocrine progenitors during a narrow developmental window. Genes Dev 2009; 23:2088-101; PMID:19723764; http://dx.doi.org/10.1101/gad.1800209
   Google Scholar
• Forster B, Van De Ville D, Berent J, Sage D, Unser M. Complex wavelets for extended depth-of-field: a new method for the fusion of multichannel microscopy images. Microsc Res Tech 2004; 65:33-42; PMID:15570586; http://dx.doi.org/10.1002/jemt.20092
   Google Scholar
• Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 2012; 9:671-5; PMID:22930834; http://dx.doi.org/10.1038/nmeth.2089
   Google Scholar
• Mojibian M, Harder B, Hurlburt A, Bruin JE, Asadi A, Kieffer TJ. Implanted islets in the anterior chamber of the eye are prone to autoimmune attack in a mouse model of diabetes. Diabetologia 2013; 56:2213-21. PMID:23933952
   Google Scholar
• Ahlgren U, Jonsson J, Edlund H. The morphogenesis of the pancreatic mesenchyme is uncoupled from that of the pancreatic epithelium in IPF1/PDX1-deficient mice. Development 1996; 122:1409-16; PMID:8625829
   Google Scholar
• Ahlgren U, Pfaff SL, Jessell TM, Edlund T, Edlund H. Independent requirement for ISL1 in formation of pancreatic mesenchyme and islet cells. Nature 1997; 385:257-60; PMID:9000074; http://dx.doi.org/10.1038/385257a0
   Google Scholar
• Dudley AT, Godin RE, Robertson EJ. Interaction between FGF and BMP signaling pathways regulates development of metanephric mesenchyme. Gen Dev 1999; 13:1601-13; PMID:10385628; http://dx.doi.org/10.1101/gad.13.12.1601
   Google Scholar
• Scharfmann R. Control of early development of the pancreas in rodents and humans: implications of signals from the mesenchyme. Diabetologia 2000; 43:1083-92; PMID:11043853; http://dx.doi.org/10.1007/s00125005-1498
   Google Scholar
• Guo T, Landsman L, Li N, Hebrok M. Factors expressed by murine embryonic pancreatic mesenchyme enhance generation of insulin-producing cells from hESCs. Diabetes 2013; 62(5):1581-92; PMID:23305648
   Google Scholar
• Hörnblad A, Eriksson AU, Sock E, Hill RE, Ahlgren U. Impaired spleen formation perturbs morphogenesis of the gastric lobe of the pancreas. PloS One 2011; 6:e21753; PMID:21738788; http://dx.doi.org/10.1371/journal.po-ne.0021753
   Google Scholar
• Duvillié B, Attali M, Bounacer A, Ravassard P, Basmaciogullari A, Scharfmann R. The mesenchyme controls the timing of pancreatic {beta}-cell differentiation. Diabetes 2006; 55:582-9; PMID:16505219; http://dx.doi.org/10.2337/diabetes.55.03.06.db05-0839
   Google Scholar
• Landsman L, Nijagal A, Whitchurch TJ, VanderLaan RL, Zimmer WE, MacKenzie TC, Hebrok M. Pancreatic mesenchyme regulates epithelial organogenesis throughout development. PLoS biology 2011; 9:e1001143; PMID:21909240; http://dx.doi.org/10.1371/journal.pbio.1001143
   Google Scholar
• Sneddon JB, Borowiak M, Melton DA. Self-renewal of embryonic-stem-cell-derived progenitors by organ-matched mesenchyme. Nature 2012; 491:765-8. PMID:23041930
   Google Scholar
• Hecksher-Sorensen J, Watson RP, Lettice LA, Serup P, Eley L, De Angelis C, Ahlgren U, Hill RE. The splanchnic mesodermal plate directs spleen and pancreatic laterality, and is regulated by Bapx1/Nkx3.2. Development 2004; 131:4665-75; PMID:15329346; http://dx.doi.org/10.1242/dev.01364
   Google Scholar
• Asayesh A, Sharpe J, Watson RP, Hecksher-Sorensen J, Hastie ND, Hill RE, Ahlgren U. Spleen versus pancreas: strict control of organ interrelationship revealed by analyses of Bapx1−/− mice. Gen Dev 2006; 20:2208-13; PMID:16912273; http://dx.doi.org/10.1101/gad.381906
   Google Scholar
• Cras-Méneur C, Elghazi L, Czernichow P, Scharfmann R. Epidermal growth factor increases undifferentiated pancreatic embryonic cells in vitro: a balance between proliferation and differentiation. Diabetes 2001; 50:1571-9; PMID:11423478; http://dx.doi.org/10.2337/diabetes.50.7.1571
   Google Scholar
• Zhou Q, Law AC, Rajagopal J, Anderson WJ, Gray PA, Melton DA. A multipotent progenitor domain guides pancreatic organogenesis. Dev Cell 2007; 13:103-14; PMID:17609113; http://dx.doi.org/10.1016/j.devcel.2007.06.001
   Google Scholar
• Chen Y, Chen J, Chen H, Hong Z, Zhu X, Zhuo S, Chen Y, Chen J. Multiphoton microscopy as a diagnostic imaging modality for pancreatic neoplasms without hematoxylin and eosin stains. J Biomed Opt 2014; 19:96008; PMID:25216027; http://dx.doi.org/10.1117/1.JBO.19.9.096008
   Google Scholar
• Elghazi L, Cras-Méneur C, Czernichow P, Scharfmann R. Role for FGFR2IIIb-mediated signals in controlling pancreatic endocrine progenitor cell proliferation. Proc Natl Acad Sci U S A 2002; 99:3884-9; PMID:11891329; http://dx.doi.org/10.1073/pnas.062321799
   Google Scholar
• Ilegems E, Dicker A, Speier S, Sharma A, Bahow A, Edlund PK, Leibiger IB, Berggren PO. Reporter islets in the eye reveal the plasticity of the endocrine pancreas. Proceedings of the National Academy of Sciences of the United States of America 2013; 110:20581-6. PMID:24248353
   Google Scholar
• Gittes GK, Galante PE, Hanahan D, Rutter WJ, Debase HT. Lineage-specific morphogenesis in the developing pancreas: role of mesenchymal factors. JPEN J Parenter Enteral Nutr 1996; 122:439-47; PMID:8625795
   Google Scholar
• Puri S, Hebrok M. Dynamics of embryonic pancreas development using real-time imaging. Dev Biol 2007; 306:82-93; PMID:17448459; http://dx.doi.org/10.1016/j.ydbio.2007.03.003
   Google Scholar
• Guillemain G, Filhoulaud G, Da Silva Xavier G, Rutter GA, Scharfmann R. Glucose is necessary for embryonic pancreatic endocrine cell differentiation. J Biol Chem 2007; 282:15228-37; PMID:17376780; http://dx.doi.org/10.1074/jbc.M610986200
   Google Scholar
• Murtaugh LC. Pancreas and beta-cell development: from the actual to the possible. JPEN J Parenter Enteral Nutr 2007; 134:427-38; PMID:17185316
   Google Scholar
• Abdulreda MH, Faleo G, Molano RD, Lopez-Cabezas M, Molina J, Tan Y, Echeverria OA, Zahr-Akrawi E, Rodriguez-Diaz R, Edlund PK, et al. High-resolution, noninvasive longitudinal live imaging of immune responses. Proc Natl Acad Sci U S A 2011; 108:12863-8; PMID:21768391; http://dx.doi.org/10.1073/pnas.1105002108
   Google Scholar