Quantitative-proteomic comparison of alpha and beta cells to uncover novel targets for lineage reprogramming

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Choudhary, Amit ^a,b   He, Kaihui Hu ^b   Mertins, Philipp ^b   Udeshi, Namrata D ^b   Dančík, Vlado ^b   Fomina Yadlin, Dina ^b,c,f   Kubicek, Stefan ^b,g   Clemons, Paul A ^b   Schreiber, Stuart L ^b,d,e   Carr, Steven A ^b   Wagner, Bridget K ^b  

^a HARVARD UNIVERSITY   (United States)

^b BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^c HARVARD UNIVERSITY   (United States)

^d HARVARD UNIVERSITY   (United States)

^e HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^f AMGEN INC   (United States)

^g ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

INSULIN; PROTEIN KINASE; PROTEIN KINASE BRSK1; PROTEIN KINASE CAMKK2; UNCLASSIFIED DRUG; BRSK1 PROTEIN, HUMAN; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE KINASE; CAMKK2 PROTEIN, MOUSE; PROTEIN SERINE THREONINE KINASE; SIGNAL PEPTIDE;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL LINEAGE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME REPRESSION; GENE SILENCING; GLYCOLYSIS; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PANCREAS ISLET ALPHA CELL; PANCREAS ISLET BETA CELL; PHENOTYPE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; PROTEOMICS; TRANSCRIPTOMICS; ANIMAL; CELL LINE; METABOLISM; PHOSPHORYLATION; PROCEDURES;

ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE KINASE; CELL LINE; GLUCAGON-SECRETING CELLS; INSULIN-SECRETING CELLS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTEOMICS;

EID: 84899769809     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0095194     Document Type: Article

References (53)

1. Gepts W (1965) Pathologic anatomy of the pancreas in juvenile diabetes mellitus. Diabetes 14: 619-633.
2. van Belle TL, Coppieters KT, von Herrath MG (2011) Type 1 diabetes: etiology, immunology, and therapeutic strategies. Physiol Rev 91: 79-118.
3. Hirsch IB, Farkas-Hirsch R, Skyler JS (1990) Intensive insulin therapy for treatment of type I diabetes. Diabetes Care 13: 1265-1283.
4. Rajab A (2010) Islet transplantation: alternative sites. Curr Diab Rep 10: 332-337.
5. de Kort H, de Koning EJ, Rabelink TJ, Bruijn JA, Bajema IM (2011) Islet transplantation in type 1 diabetes. BMJ 342: d217.
6. Chatenoud L (2008) Chemical immunosuppression in islet transplantation - friend or foe? N Engl J Med 358: 1192-1193.
7. Johnson JD, Ao Z, Ao P, Li H, Dai LJ, et al. (2009) Different effects of FK506, rapamycin, and mycophenolate mofetil on glucose-stimulated insulin release and apoptosis in human islets. Cell Transplant 18: 833-845.
8. Borowiak M, Melton DA (2009) How to make β cells? Curr Opin Cell Biol 21: 727-732.
9. Yechoor V, Chan L (2010) Minireview: beta-cell replacement therapy for diabetes in the 21st century: manipulation of cell fate by directed differentiation. Mol Endocrinol 24: 1501-1511.
10. Collombat P, Xu X, Ravassard P, Sosa-Pineda B, Dussaud S, et al. (2009) The ectopic expression of Pax4 in the mouse pancreas converts progenitor cells into alpha and subsequently beta cells. Cell 138: 449-462.
11. Wagner BK (2010) Grand challenge commentary: Chemical transdifferentiation and regenerative medicine. Nat Chem Biol 6: 877-879.
12. Fomina-Yadlin D, Kubicek S, Walpita D, Dancik V, Hecksher-Sorensen J, et al. (2010) Small-molecule inducers of insulin expression in pancreatic alpha-cells. Proc Natl Acad Sci U S A 107: 15099-15104.
13. Fomina-Yadlin D, Kubicek S, Vetere A, He KH, Schreiber SL, et al. (2012) GW8510 Increases Insulin Expression in Pancreatic Alpha Cells through Activation of p53 Transcriptional Activity. PLoS One 7: e28808.
14. Kubicek S, Gilbert JC, Fomina-Yadlin D, Gitlin AD, Yuan Y, et al. (2012) Chromatin-targeting small molecules cause class-specific transcriptional changes in pancreatic endocrine cells. Proc Natl Acad Sci U S A: 5364-5369.
15. GENE-E software application:http://www.broadinstitute.org/cancer/ software/GENE-E.Accessed 2014 March 27.
16. Mertins P, Udeshi ND, Clauser KR, Mani DR, Patel J, et al. (2012) iTRAQ labeling is superior to mTRAQ for quantitative global proteomics and phosphoproteomics. Molecular & cellular proteomics: MCP 11: M111.014423.
17. Rappsilber J, Mann M, Ishihama Y (2007) Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat Protocols 2: 1896-1906. (Pubitemid 47308128)
18. Mertins P, Udeshi ND, Clauser KR, Mani DR, Patel J, et al. (2012) iTRAQ Labeling is Superior to mTRAQ for Quantitative Global Proteomics and Phosphoproteomics. Mol Cell Proteomics 11.
19. Ong SE, Mann M (2005) Mass spectrometry-based proteomics turns quantitative. Nat Chem Biol 1: 252-262.
20. Ong SE, Mann M (2006) A practical recipe for stable isotope labeling by amino acids in cell culture (SILAC). Nat Protoc 1: 2650-2660.
21. Ong SE, Mann M (2007) Stable isotope labeling by amino acids in cell culture for quantitative proteomics. Methods Mol Biol 359: 37-52.
22. Dorrell C, Schug J, Lin CF, Canaday PS, Fox AJ, et al. (2011) Transcriptomes of the major human pancreatic cell types. Diabetologia 54: 2832-2844.
23. Reich M, Liefeld T, Gould J, Lerner J, Tamayo P, et al. (2006) GenePattern 2.0. Nat Genet 38: 500-501.
24. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, et al. (2005) Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A 102: 15545-15550. (Pubitemid 41528093)
25. Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, et al. (2003) PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 34: 267-273. (Pubitemid 36792858)
26. Brand MD, Nicholls DG (2011) Assessing mitochondrial dysfunction in cells. Biochem J 435: 297-312.
27. Affourtit C, Brand MD (2008) Uncoupling protein-2 contributes significantly to high mitochondrial proton leak in INS-1E insulinoma cells and attenuates glucose-stimulated insulin secretion. Biochem J 409: 199-204.
28. Thorrez L, Laudadio I, Deun KV, Quintens R, Hendrickx N, et al. (2011) Tissue-specific disallowance of housekeeping genes: The other face of cell differentiation. Genome Res 21: 95-105.
29. Sekine N, Cirulli V, Regazzi R, Brown LJ, Gine E, et al. (1994) Low lactate dehydrogenase and high mitochondrial glycerol phosphate dehydrogenase in pancreatic beta-cells. Potential role in nutrient sensing. J Biol Chem 269: 4895-4902.
30. Schuit F, De Vos A, Farfari S, Moens K, Pipeleers D, et al. (1997) Metabolic Fate of Glucose in Purified Islet Cells: GLUCOSE-REGULATED ANAPLEROSIS IN β CELLS. J Biol Chem 272: 18572-18579. (Pubitemid 27318196)
31. Cox J, Matic I, Hilger M, Nagaraj N, Selbach M, et al. (2009) A practical guide to the MaxQuant computational platform for SILAC-based quantitative proteomics. Nat Prot 4: 698-705.
32. Cox J, Mann M (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotech 26: 1367-1372.
33. Skoglund G, Gross R, Ahrén B, Loubatières-Mariani M-M (1993) Different mechanisms are involved in neuropeptide Y-induced pancreatic vasoconstriction and inhibition of insulin secretion. Eur Jour Pharm 236: 69-74. (Pubitemid 23146852)
34. Moltz JH, McDonald JK (1985) Neuropeptide Y: Direct and indirect action on insulin secretion in the rat. Peptides 6: 1155-1159. (Pubitemid 16166869)
35. Strowski MZ, Parmar RM, Blake AD, Schaeffer JM (2000) Somatostatin Inhibits Insulin and Glucagon Secretion via Two Receptor Subtypes: An in Vitro Study of Pancreatic Islets from Somatostatin Receptor 2 Knockout Mice. Endocrinology 141: 111-117. (Pubitemid 32260349)
36. Zhou G, Wang h, Liu S-H, Shahi KM, Lin X, et al. (2013) p38 MAP kinase interacts with and stabilizes pancreatic and duodenal homeobox-1. Curr Mol Med 13: 377-386.
37. Guo S, Vanderford NL, Stein R (2010) Phosphorylation within the MafA N Terminus Regulates C-terminal Dimerization and DNA Binding. J Biol Chem 285: 12655-12661.
38. Sii-Felice K, Pouponnot C, Gillet S, Lecoin L, Girault J-A, et al. (2005) MafA transcription factor is phosphorylated by p38 MAP kinase. FEBS Lett 579: 3547-3554. (Pubitemid 40897689)
39. Bora RS, Gupta D, Mukkur TK, Saini KS (2012) RNA interference therapeutics for cancer: challenges and opportunities (review). Mol Med Report 6: 9-15.
40. Iype T, Francis J, Garmey JC, Schisler JC, Nesher R, et al. (2005) Mechanism of insulin gene regulation by the pancreatic transcription factor Pdx-1: application of pre-mRNA analysis and chromatin immunoprecipitation to assess formation of functional transcriptional complexes. J Biol Chem 280: 16798-16807. (Pubitemid 41389138)
41. Dalgin G, Ward AB, Hao LT, Beattie CE, Nechiporuk A, et al. (2011) Zebrafish mnx1 controls cell fate choice in the developing endocrine pancreas. Development 138: 4597-4608.
42. Kishi M, Pan YA, Crump JG, Sanes JR (2005) Mammalian SAD kinases are required for neuronal polarization. Science 307: 929-932. (Pubitemid 40229230)
43. Barnes AP, Lilley BN, Pan YA, Plummer LJ, Powell AW, et al. (2007) LKB1 and SAD kinases define a pathway required for the polarization of cortical neurons. Cell 129: 549-563. (Pubitemid 46660970)
44. Bright NJ, Carling D, Thornton C (2008) Investigating the regulation of brain-specific kinases 1 and 2 by phosphorylation. J Biol Chem 283: 14946-14954.
45. Lizcano JM, Goransson O, Toth R, Deak M, Morrice NA, et al. (2004) LKB1 is a master kinase that activates 13 kinases of the AMPK subfamily, including MARK/PAR-1. EMBO J 23: 833-843. (Pubitemid 38418750)
46. Shaw RJ, Lamia KA, Vasquez D, Koo SH, Bardeesy N, et al. (2005) The kinase LKB1 mediates glucose homeostasis in liver and therapeutic effects of metformin. Science 310: 1642-1646. (Pubitemid 41780780)
47. Fu A, Ng AC, Depatie C, Wijesekara N, He Y, et al. (2009) Loss of Lkb1 in adult beta cells increases beta cell mass and enhances glucose tolerance in mice. Cell Metab 10: 285-295.
48. Woods A, Dickerson K, Heath R, Hong SP, Momcilovic M, et al. (2005) Ca2+/ calmodulin-dependent protein kinase kinase-beta acts upstream of AMP-activated protein kinase in mammalian cells. Cell Metab 2: 21-33. (Pubitemid 43239822)
49. Hawley SA, Pan DA, Mustard KJ, Ross L, Bain J, et al. (2005) Calmodulin-dependent protein kinase kinase-beta is an alternative upstream kinase for AMPactivated protein kinase. Cell Metab 2: 9-19. (Pubitemid 43239821)
50. Soderling TR (1999) The Ca-calmodulin-dependent protein kinase cascade. Trends Biochem Sci 24: 232-236.
51. Anderson KA, Ribar TJ, Lin F, Noeldner PK, Green MF, et al. (2008) Hypothalamic CaMKK2 contributes to the regulation of energy balance. Cell Metab 7: 377-388. (Pubitemid 351598022)
52. Cao W, Sohail M, Liu G, Koumbadinga GA, Lobo VG, et al. (2011) Differential effects of PKA-controlled CaMKK2 variants on neuronal differentiation. RNA Biol 8: 1061-1072.
53. Cary RL, Waddell S, Racioppi Li, Long F, Novack DV, et al. (2013) Inhibition of Ca2+/Calmodulin-Dependent Protein Kinase Kinase 2 Stimulates Osteoblast Formation and Inhibits Osteoclast Differentiation. J Bone Miner Res 28: 1599-1610.