Single pancreatic beta cells co-express multiple islet hormone genes in mice

Diabetologia

Volumn 53, Issue 1, 2010, Pages 128-138

  Katsuta, H ^a   Akashi, T ^a   Katsuta, R ^a   Nagaya, M ^a   Kim, D ^a   Arinobu, Y ^b   Hara, M ^c   Bonner Weir, S ^a   Sharma, A J ^a   Akashi, K ^b   Weir, G C ^a  

^a JOSLIN DIABETES CENTER   (United States)

^b DANA FARBER CANCER INSTITUTE   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

Heterogeneity; Pancreatic beta cell; Single cell nested RT PCR

Indexed keywords

GREEN FLUORESCENT PROTEIN; INSULIN DERIVATIVE; PANCREAS HORMONE; PANCREAS POLYPEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL FATE; CELL FUNCTION; CELL HETEROGENEITY; CELL LINEAGE; CONTROLLED STUDY; EMBRYO; EMBRYO CELL; FETUS; GENE CASSETTE; GENE EXPRESSION; LOXP SITE; MOUSE; NEWBORN; NONHUMAN; PANCREAS ISLET; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEM CELL; TRANSGENIC MOUSE;

AGING; ANIMALS; ANIMALS, NEWBORN; B-LYMPHOCYTES; CELL DIFFERENTIATION; CELL SIZE; CELL SURVIVAL; COLLAGENASES; GENE EXPRESSION REGULATION; GENES, REPORTER; GLUCAGON; GREEN FLUORESCENT PROTEINS; INSULIN; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; MICE; PANCREATIC POLYPEPTIDE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SOMATOSTATIN;

EID: 72449156523     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-009-1570-x     Document Type: Article

References (48)

1. D Salomon P Meda 1986 Heterogeneity and contact-dependent regulation of hormone secretion by individual B cells Exp Cell Res 162 507 520 10.1016/0014-4827(86)90354-X 1:CAS:528:DyaL28Xht1emt70%3D 3510882
2. Y Stefan P Meda M Neufeld L Orci 1987 Stimulation of insulin secretion reveals heterogeneity of pancreatic B cells in vivo J Clin Invest 80 175 183 10.1172/JCI113045 1:CAS:528:DyaL2sXkslWhsLg%3D 3110211
3. FC Schuit PA In 't Veld DG Pipeleers 1988 Glucose stimulates proinsulin biosynthesis by a dose-dependent recruitment of pancreatic beta cells Proc Natl Acad Sci U S A 85 3865 3869 10.1073/pnas.85.11.3865 1:CAS:528:DyaL1cXktlamsrY%3D 3287379 (Pubitemid 18160635)
4. R Kiekens P In 't Veld T Mahler F Schuit M van de Winkel D Pipeleers 1992 Differences in glucose recognition by individual rat pancreatic β cells are associated with intercellular differences in glucose-induced biosynthetic activity J Clin Invest 89 117 125 10.1172/JCI115551 1:CAS:528: DyaK38Xns1yjsg%3D%3D 1729264
5. H Heimberg A de Vos A Vandercammen E Schaftingen D Pipeleers F Schuit 1993 Heterogeneity in glucose sensitivity among pancreatic β-cells is correlated to differences in glucose phosphorylation rather than glucose transport EMBO J 12 2873 2879 1:CAS:528:DyaK3sXkvFajs7c%3D 8335003
6. YM Leung I Ahmed L Sheu, et al. 2005 Electrophysiological characterization of pancreatic islet cells in the mouse insulin promoter-green fluorescent protein mouse Endocrinology 146 4766 4775 10.1210/en.2005-0803 1:CAS:528:DC%2BD2MXhtFGqur%2FF 16109783 (Pubitemid 41446614)
7. Z Ling Q Wang G Stange P In 't Veld D Pipeleers 2006 Glibenclamide treatment recruits beta-cell subpopulation into elevated and sustained basal insulin synthetic activity Diabetes 55 78 85 10.2337/diabetes.55.01.06.db05-0820 1:CAS:528:DC%2BD28XlvVSmuw%3D%3D 16380479
8. S Alpert D Hanahan G Teitelman 1988 Hybrid insulin genes reveal a developmental lineage for pancreatic endocrine cells and imply a relationship with neurons Cell 53 295 308 10.1016/0092-8674(88)90391-1 1:CAS:528: DyaL1cXktFyisL4%3D 3282675 (Pubitemid 18139066)
9. RR de Krijger HJ Aanstoot G Kranenburg M Reinhard WJ Visser GJ Bruining 1992 The midgestational human fetal pancreas contains cells coexpressing islet hormones Dev Biol 153 368 375 10.1016/0012-1606(92)90121-V 1356859
10. G Teitelman S Alpert JM Polak A Martinez D Hanahan 1993 Precursor cells of mouse endocrine pancreas coexpress insulin, glucagon and the neuronal proteins tyrosine hydroxylase and neuropeptide Y but not pancreatic polypeptide Development 118 1031 1039 1:CAS:528:DyaK2cXht1Gmsb0%3D 7903631
11. KH Yoon RR Quickel K Tatarkiewicz, et al. 1999 Differentiation and expansion of beta cell mass in porcine neonatal pancreatic cell clusters transplanted into nude mice Cell Transplant 8 673 689 1:STN:280: DC%2BD3c7mtlCgsw%3D%3D 10701496
12. S Bonner-Weir M Taneja GC Weir, et al. 2000 In vitro cultivation of human islets from expanded ductal tissue Proc Natl Acad Sci U S A 97 7999 8004 10.1073/pnas.97.14.7999 1:CAS:528:DC%2BD3cXkvFCmsr4%3D 10884429 (Pubitemid 30460762)
13. MK Chiang DA Melton 2003 Single-cell transcript analysis of pancreas development Dev Cell 4 383 393 10.1016/S1534-5807(03)00035-2 1:CAS:528:DC%2BD3sXisVekur0%3D 12636919 (Pubitemid 36342363)
14. Y Guz I Nasir G Teitelman 2001 Regeneration of pancreatic beta cells from intra-islet precursor cells in an experimental model of diabetes Endocrinology 142 4956 4968 10.1210/en.142.11.4956 1:CAS:528:DC%2BD3MXnslGqu7Y%3D 11606464 (Pubitemid 33022372)
15. M van de Winkle E Maes D Pipeleers 1982 Islet cell analysis and purification by light scatter and autofluorescence Biochem Biophys Res Commun 107 525 532 10.1016/0006-291X(82)91523-6 6751329
16. DJ Fletcher WM Grogan E Barras GC Weir 1983 Hormone release by islet B cell-enriched and A and D cell-enriched populations prepared by flow cytometry Endocrinology 113 1791 1798 10.1210/endo-113-5-1791 1:CAS:528:DyaL3sXmtVKks7s%3D 6194980
17. C Bernard-Kargar N Kassis MF Berthault W Pralong A Ktorza 2001 Sialylated form of the neural cell adhesion molecule (NCAM): a new tool for the identification and sorting of beta-cell subpopulations with different functional activity Diabetes 50 Suppl 1 S125 S130 10.2337/diabetes.50.2007.S125 1:CAS:528:DC%2BD3MXhtVOgtLw%3D 11272170
18. C Meyer R Grosmann A Mitrakou, et al. 1998 Effects of autonomic neuropathy on counterregulation and awareness of hypoglycemia in type 1 diabetic patients Diabetes Care 21 1960 1966 10.2337/diacare.21.11.1960 1:STN:280:DyaK1M%2FhslOmsw%3D%3D 9802751 (Pubitemid 28478301)
19. M Hara X Wang T Kawamura, et al. 2003 Transgenic mice with green fluorescent protein-labeled pancreatic beta-cells Am J Physiol Endocrinol Metab 284 E177 E183 1:CAS:528:DC%2BD3sXntVShug%3D%3D 12388130
20. F Kamme R Salunga J Yu, et al. 2003 Single-cell microarray analysis in hippocampus CA1: demonstration and validation of cellular heterogeneity J Neurosci 23 3607 3615 1:CAS:528:DC%2BD3sXjslGntbg%3D 12736331
21. I Tietjen JM Rihel Y Cao G Koentges L Zakhary C Dulac 2003 Single-cell transcriptional analysis of neuronal progenitors Neuron 38 161 175 10.1016/S0896-6273(03)00229-0 1:CAS:528:DC%2BD3sXjslOkt7c%3D 12718852 (Pubitemid 36555644)
22. G Baier D Telford E Gulbins N Yamada T Kawakami A Altman 1993 Improved specificity of RT-PCR amplifications using nested cDNA primers Nucleic Acids Res 21 1329 1330 10.1093/nar/21.5.1329 1:CAS:528:DyaK3sXitVKiu74%3D 7681946
23. B Sauer N Henderson 1988 Site-specific DNA recombination in mammalian cells by the Cre recombinase of bacteriophage P1 Proc Natl Acad Sci U S A 85 5166 5170 10.1073/pnas.85.14.5166 1:CAS:528:DyaL1cXltVGrtro%3D 2839833
24. M Gannon C Shiota C Postic CV Wright M Magnuson 2000 Analysis of the Cre-mediated recombination driven by rat insulin promoter in embryonic and adult mouse pancreas Genesis 26 139 142 10.1002/(SICI)1526-968X(200002)26:2<139:: AID-GENE12>3.0.CO;2-7 1:CAS:528:DC%2BD3cXitVCjt7o%3D 10686610 (Pubitemid 30158100)
25. X Mao Y Fujiwara A Chapdelaine H Yang SH Orkin 2001 Activation of EGFP expression by Cre-mediated excision in a new ROSA26 reporter mouse strain Blood 97 324 326 10.1182/blood.V97.1.324 1:CAS:528:DC%2BD3MXis1Cgsg%3D%3D 11133778 (Pubitemid 32061277)
26. M Gotoh T Maki T Kiyoizumi S Satomi AP Monaco 1985 An improved method for isolation of mouse pancreatic islets Transplantation 40 437 438 10.1097/00007890-198510000-00018 1:STN:280:DyaL28%2FitVWnsQ%3D%3D 2996187 (Pubitemid 16215266)
27. T Miyamoto H Iwasaki B Reizis, et al. 2002 Myeloid or lymphoid promiscuity as a critical step in hematopoietic lineage commitment Dev Cell 3 137 147 10.1016/S1534-5807(02)00201-0 1:CAS:528:DC%2BD38XlsFSmsLo%3D 12110174 (Pubitemid 34778402)
28. L Leroux P Desbois L Lamotte, et al. 2001 Compensatory responses in mice carrying a null mutation for Ins1 or Ins2 Diabetes 50 Suppl 1 S150 S153 10.2337/diabetes.50.2007.S150 1:CAS:528:DC%2BD3MXhtVOgtb8%3D 11272179
29. SU Devaskar BS Singh LR Carnaghi PA Rajakumar SJ Giddings 1993 Insulin II gene expression in rat central nervous system Regul Pept 48 55 63 10.1016/0167-0115(93)90335-6 1:CAS:528:DyaK2cXhtVWq 8265817
30. C Alarcon J Serna B Perez-Villamil F de Pablo 1998 Synthesis and differentially regulated processing of proinsulin in developing chick pancreas, liver and neuroretina FEBS Lett 436 361 366 10.1016/S0014-5793(98)01168-5 1:CAS:528:DyaK1cXmvFOltL0%3D 9801149 (Pubitemid 28482962)
31. D Hanahan 1998 Peripheral-antigen-expressing cells in thymic medulla: factors in self-tolerance and autoimmunity Curr Opin Immunol 10 656 662 10.1016/S0952-7915(98)80085-X 1:CAS:528:DyaK1MXhtlGn 9914224 (Pubitemid 28558580)
32. N Blume JS Petersen LC Andersen, et al. 1992 Immature transformed rat islet beta-cells differentially express C-peptides derived from the genes coding for insulin I and II as well as a transfected human insulin gene Mol Endocrinol 6 299 307 10.1210/me.6.2.299 1:CAS:528:DyaK38XitVyitbk%3D 1569972
33. G Xu DA Stoffers JF Habener S Bonner-Weir 1999 Exendin-4 stimulates both β-cell replication and neogenesis, resulting in increased β-cell mass and improved glucose tolerance in diabetic rats Diabetes 48 2270 2276 10.2337/diabetes.48.12.2270 1:CAS:528:DyaK1MXnslOqtro%3D 10580413
34. P Itkin-Ansari E Marcora I Geron, et al. 2005 NeuroD1 in the endocrine pancreas: localization and dual function as an activator and repressor Dev Dyn 233 946 953 10.1002/dvdy.20443 1:CAS:528:DC%2BD2MXmtFKgsLk%3D 15906379 (Pubitemid 40853470)
35. G Gradwohl A Dierich M LeMeur F Guillemot 2000 Neurogenin3 is required for the development of the four endocrine cell lineages of the pancreas Proc Natl Acad Sci U S A 97 1607 1611 10.1073/pnas.97.4.1607 1:CAS:528: DC%2BD3cXhsFCrsLk%3D 10677506 (Pubitemid 30118489)
36. B Sosa-Pineda K Chowdhury M Torres G Oliver P Gruss 1997 The Pax4 gene is essential for differentiation of insulin-producing -cells in the mammalian pancreas Nature 386 399 402 10.1038/386399a0 1:CAS:528:DyaK2sXit1WrsLs%3D 9121556 (Pubitemid 27154480)
37. DG Pipeleers 1992 Heterogeneity in pancreatic b-cell population Diabetes 41 777 781 10.2337/diabetes.41.7.777 1:CAS:528:DyaK38Xks1eju74%3D 1612191
38. D Bosco P Meda B Thorens WJ Malaisse 1995 Heterogeneous secretion of individual B cells in response to D-gluclose and to nonglucidic nutrient secretagogues Am J Physiol 268 C611 C618 1:CAS:528:DyaK2MXkslKit7k%3D 7900769
39. FC Jonkers JC Henquin 2001 Measurements of cytoplasmic Ca2+ in islet cell clusters show that glucose rapidly recruits b-cells and gradually increases the individual cell response Diabetes 50 540 550 10.2337/diabetes.50.3.540 1:CAS:528:DC%2BD3MXhslGhu7g%3D 11246873
40. CR Bliss GW Sharp 1992 Glucose-induced insulin release in islets of young rats: time-dependent potentiation and effects of 2-bromostearate Am J Physiol 263 E890 E896 1:CAS:528:DyaK3sXlt1yiug%3D%3D 1443122
41. T Cheng H Shen D Giokas J Gere DG Tenen DT Scadden 1996 Temporal mapping of gene expression levels during the differentiation of individual primary hematopoietic cells Proc Natl Acad Sci U S A 93 13158 13163 10.1073/pnas.93.23. 13158 1:CAS:528:DyaK28XmvV2qt78%3D 8917561 (Pubitemid 26382786)
42. M Hu D Krause M Greaves, et al. 1997 Multilineage gene expression precedes commitment in the hemopoietic system Genes Dev 11 774 785 10.1101/gad.11.6.774 1:CAS:528:DyaK2sXisVGjtL0%3D 9087431
43. S Delassus I Titley T Enver 1999 Functional and molecular analysis of hematopoietic progenitors derived from the aorta-gonad-mesonephros region of the mouse embryo Blood 94 1495 1503 1:CAS:528:DyaK1MXmtVaiurY%3D 10477673
44. K Akashi X He J Chen, et al. 2003 Transcriptional accessibility for genes of multiple tissues and hematopoietic lineages is hierarchically controlled during early hematopoiesis Blood 101 383 389 10.1182/blood-2002-06-1780 1:CAS:528:DC%2BD3sXkvVWmug%3D%3D 12393558 (Pubitemid 36077553)
45. PL Herrera J Huarte R Zufferey, et al. 1994 Ablation of islet endocrine cells by targeted expression of hormone-promoter-driven toxigenes Proc Natl Acad Sci U S A 91 12999 13003 10.1073/pnas.91.26.12999 1:CAS:528:DyaK2MXivVCqsbc%3D 7809163
46. PL Herrera J Huarte F Sanvito P Meda L Orci JD Vassalli 1991 Embryogenesis of the murine endocrine pancreas; early expression of pancreatic polypeptide gene Development 113 1257 1265 1:CAS:528:DyaK38Xhs1Klurk%3D 1811941
47. PL Herrera 2000 Adult insulin- and glucagon-producing cells differentiate from two independent cell lineages Development 127 2317 2322 1:CAS:528:DC%2BD3cXksVKmsrg%3D 10804174
48. PL Herrera V Nepote A Delacour 2002 Pancreatic cell lineage analyses in mice Endocrine 19 267 278 10.1385/ENDO:19:3:267 1:CAS:528:DC%2BD2cXhsFKitbo%3D 12624426 (Pubitemid 36250306)