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KramerMass SpectrometryBottom-up proteomicsNot availableRatLcmseDiabetesPancreasLabel free quantitationhttp://www.ebi.ac.uk/pride/archive/projects/PXD001577PancreasNeonatal endocrine aggregate-enriched preparations were collected by gradient centrifugation rather than handpicking of islets in 10w-old rats: collagenase-digested pancreas was density-centrifuged first over a Ficoll layer (1.10 g/ml) to separate exocrine from endocrine cells; the endocrine-enriched interphase was collected (ii) and trypsinized to single cells, additionally purified over a Percoll (1.04 g/ml) layer to separate viable from damaged cells prior to FACS-sorting. While the 10w-old beta cells are mainly discriminated from other islet endocrine cell types by their higher cell size (forward scatter, FSC) in combination with higher endogenous fluorescence due to oxidized flavin cofactors (FAD/FMN) (Fig.1C) (Van De Winkel & Pipeleers 1983), flavin fluorescence is lower in neonatal beta cells and a combination of FSC and cellular complexity/granulation (Side Scatter, SSC) is used to separate beta cells from a less granulated cell population; the latter SSClow population contains not only exocrine duct cells but also endothelial and mesenchymal cells and a very small fraction of insulin-positive cells. Protein extraction and trypsinization Cells were washed 3 times with PBS (4°C) and soluble protein was extracted in 50 µl 0.5% (w/v) RapiGest detergent in 50 mM ammonium bicarbonate (Waters Corporation, Milford, MA.) in the presence of Complete Protease Inhibitor Cocktail (F. Hoffmann–La Roche Ltd, Basel, Switserland) and bovine DNAse II (Boehringer Ingelheim GmbH, Ingelheim am Rhein, Germany, 2 µg/mL) solution, followed by centrifugation (10,000 x g, 10 min) to remove cellular debris. 25 µl protein extract was reduced with 2.5 µl 100 mM dithiothreitol (DTT) at room temperature for 60 min, followed by 3 subsequent washes with 400 µl 50 mM ammonium bicarbonate and 4 µl 100 mM DTT using a 5 KDa cut-off membrane filter. This step removes protease inhibitors and most of reduced insulin molecules. Proteins were denatured by heating at 80 °C for 15 min, followed by 30 min at 60°C after addition of 2.5 µl 100 mM DTT and another 30 min at ambient temperature in the dark after addition of 2.5 µl 200 mM iodoacetamide. Trypsinization was carried out overnight at 37°C (1:25 w/w trypsin ratio) in final volume of 100 µl. Finally, RapiGest detergent was removed by acidifying digest to pH = 2 with trifluoroacetic acid and incubation for 15 min at 37°C. LC-MS configuration Nanoscale LC separation of the tryptic peptides was performed with a NanoAcquity system (Waters). Samples were loaded on to a Symmetry C18 5 μm, 2 cm×180 μm trap column (Waters) at a flow rate of 5 μl/min prior to separation on a Bridged Ethyl Hybrid C18 1.7 μm, 25 cm×75 μm analytical reversed-phase column (Waters) by application of a 90 min gradient from 1% ACN and 0.1% formic acid to 40% ACN and 0.1% formic acid at a column flow rate of 0.25 μl/min. The column temperature was maintained at 35ºC. Analysis of the eluted tryptic peptides was performed using a Synapt G2 Q-TOF (quadrupole time-of-flight) mass spectrometer (Waters) equipped with a nanolockspray source (Waters) fitted with a pico-tip emitter (New Objective) operated at a capillary voltage of approximately 3 kV. For all measurements, the mass spectrometer was operated in v-mode with a typical resolution of at least 20,000 full width at half maximum. All analyses were performed in positive mode ESI. The time-of-flight analyzer of the mass spectrometer was externally calibrated with a NaI mixture from m/z 50 to 1990. The collision gas used was argon, maintained at a constant pressure of 2.0×10−3 mbar (1 bar=100 kPa) in the collision cell. The lock mass, [Glu1]fibrinopeptide B, was delivered from the auxiliary pump of the NanoAcquity system with a concentration of 100 fmol/μl at 0.5 μl/min to the reference sprayer of the nanolockspray source. The data were post-acquisition lock-mass corrected using the monoisotopic mass of the doubly charged precursor of [Glu1]fibrinopeptide B, delivered through the reference sprayer, which was sampled every 120 s. Accurate mass precursor and fragment ion LC-MS data were collected in data independent, alternate scanning (LC-MSE) mode of acquisition (13;14)PrideMS1 intensity based label-free quantification methodiodoacetamide derivatized residuemonohydroxylated residueLC-MS data processing and protein identification Continuum LC-MS data were processed and searched using ProteinLynx GlobalSERVER v2.5 (Waters Corporation). Protein identifications were obtained by searching databases of Rattus norvegicus databases (v15.12, 7,449 entries). Sequence information of Alcohol dehydrogenase Saccharomyces cerevisiae was added to the databases to afford the ability to normalize the data sets and to estimate amounts and concentration [11] and that of known contaminant proteins (e.g. serum albumin Bos taurus and trypsin Sus scrofa). A decoy was generated on the fly with every database search experiment conducted to estimate the protein false positive rate of identification [43]. Data independent scanning protein identifications were accepted when more than three fragment ions per peptide, seven fragment ions per protein and more than 2 peptides per protein were identified, in at least one technical replicate per sample. Protein quantitation was only reported when the protein was detected in at least 2 out of 3 technical replicate of at least one biological replicate. Typical search criteria used for protein identification included automatic peptide and fragment ion tolerance settings (approximately 10 and 25 ppm, respectively), 1 allowed missed cleavage, fixed carbamidomethyl-cysteine modification and variable methionine oxidation. Raw data were expressed as ‘relative molar amount units’ calculated by dividing the determined molar amount for a given protein by the summed determined amount for all identified proteins as this accounts for both technical and biological variations (10;14;15).ProteomicsMultiomicsJ.M.F.G AertsSynapt G2 MSPARTIALClinical proteomics facility, Medical Biochemistry, Academic Medical Center, University of AmstedamRattus Norvegicus (rat)24049066 Martens GA, Motté E, Kramer G, Stangé G, Gaarn LW, Hellemans K, Nielsen JH, Aerts JM, Ling Z, Pipeleers D; Functional characteristics of neonatal rat β cells with distinct markers., J Mol Endocrinol, 2014 Feb, 52, 1, 11-28, 10.1530/JME-13-0106gertjan.kramer@dkfz-heidelberg.deBiologicalProteomics of Stem Cells and Cancer.University Clinic Heidelberg.German Cancer Research Center.Im Neuenheimer Feld 581Heidelberg, Germany.GermanyNeonatal β cells are considered developmentally immature and hence less glucose responsive. To study the acquisition of mature glucose responsiveness, we compared glucose-regulated redox state, insulin synthesis, and secretion of β cells purified from neonatal or 10-week-old rats with their transcriptomes and proteomes measured by oligonucleotide and LC-MS/MS profiling. Lower glucose responsiveness of neonatal β cells was explained by two distinct properties: higher activity at low glucose and lower activity at high glucose. Basal hyperactivity was associated with higher NAD(P)H, a higher fraction of neonatal β cells actively incorporating (3)H-tyrosine, and persistently increased insulin secretion below 5 mM glucose. Neonatal β cells lacked the steep glucose-responsive NAD(P)H rise between 5 and 10 mM glucose characteristic for adult β cells and accumulated less NAD(P)H at high glucose. They had twofold lower expression of malate/aspartate-NADH shuttle and most glycolytic enzymes. Genome-wide profiling situated neonatal β cells at a developmental crossroad: they showed advanced endocrine differentiation when specifically analyzed for their mRNA/protein level of classical neuroendocrine markers. On the other hand, discrete neonatal β cell subpopulations still expressed mRNAs/proteins typical for developing/proliferating tissues. One example, delta-like 1 homolog (DLK1) was used to investigate whether neonatal β cells with basal hyperactivity corresponded to a more immature subset with high DLK1, but no association was found. In conclusion, the current study supports the importance of glycolytic NADH-shuttling in stimulus function coupling, presents basal hyperactivity as novel property of neonatal β cells, and provides potential markers to recognize intercellular developmental differences in the endocrine pancreas.Functional characteristics of neonatal rat β cells with distinct markers.Martens G A GA, Motté E E, Kramer G G, Stangé G G, Gaarn L W LW, Hellemans K K, Nielsen J H JH, Aerts J M JM, Ling Z Z, Pipeleers D Dsodium salt, Soluble, HB-6, dairy cow, Rat, BBE, ammonium formate, bar-h1, 13C-labeled, FEZL, insuline humaine, magnesium formate, Apaf-1, Norway Rats, zinc salt, 8-dihydroxy-3-carboxyl-9, dmTAF[[II]]230, rat, tumour of pancreas, Grp1, B1, 1, HRR-1, 2, 3, 4, progressive systemic sclerosis, 5-dihydroxy-9, 9, WMS, Virion-associated nuclear shuttling protein, nup154, (R*, C79325, kus, Endocrine, beta1tub, exocrine gland duct, hac-1, cel, systemic scleroderma, weight-weight percentage, burnett Schwartz Berberian syndrome, T, cell sheath, ABIN1, endocrine, LACS1, density, e, FMN, decreased, Peptidohydrolase Inhibitor, g/ml, beta1Tub, desatF-alpha, D1, Acn, Acs, CT, Acz, nickel salt, SGS, size of cell, insulinum humanum, Atrophodermia reticulata symmetrica faciei, dTAF[[II]]230, HRR1, cobalt (+2) salt, MSE., Ct, anon-53Fa, breast sarcoma, tip, Regular Insulin, ACMICD, BEST:SD05462, sodium (4:1:1) salt, magnesium salt, anon-WO0118547.726, BH1, tumor of the pancreas, FLOWERING TIME CONTROL PROTEIN FCA ALPHA, anon-WO0118547.730, hrr1, CG32315, dark/hac-1/dapaf-1, A20-binding inhibitor of NF-kappa-B activation 1, CG11628, formate, hedolit, beta1-tub, desat-2, Desat1, ulerythema ophryogenes with multiple congenital anomalies, Desat2, tumour of the pancreas, Taf250, nip40-1, DL4180C, Cells, ammonium (4:1) salt, GSD13, Peptide Peptidohydrolase Inhibitor, PSS (progressive systemic sclerosis), tlp, Specbeta, 6-dinitrophenol, HH, breadth, NEOPL PANCREATIC, l(1)VE614, GRP1/cytohesin 1, BELLRINGER, Endopeptidase Inhibitors, Neoplasms, CG5887, Cell Volume, number, precursor, R*)-, body system, CG7826, mass-to-charge ratio, Hh, CG11633, Rats, B-spec, CG7835, Gene Products, system, foetal AEDS, FA-D2, School-Age Populations, 10-dioxo-2-anthracenecarboxylic acid, anatomical systems, dTAF[[II]]250, BLR, Acinus, thallium (+1) salt, cell, homopolymer, rubidium salt, pk18, DmelCG11940, Population, Antagonist, MBR, anon-EST:fe1B3, acinusL, dTAF250, Scleroderma syndrome, Insulin recombinant, Protease Antagonists, acinusS, xfor, Nef, amelogenesis imperfecta, PTBR, Peptide Peptidohydrolase Inhibitors, peptidos, CG5870, Cell Volumes, LD, l(3)dre1, PTHB1, Acas1, dark/dapaf-1/hac-1, cow, pancreatic neoplasm, 2-phospho-D-glycerate hydro-lyase, copper (+2) salt, i168, mKIAA0670, S182, dTAF230, APAF1, native protein, Temperatures, DmelCG5529, Hac-1, hVAN, C18, cupric formate, chemical analysis, barH1, Insulin A Chain, BEL1-LIKE HOMEODOMAIN 9, MFS1, Sodium, domestic cattle, aluminum formate, NAF1, ami, AU015151, Cleland's, Taf[[II]]250, AU020952, FXR, VAAMANA, pancreatic cancer, CG4579, b spectrin, School Age Populations, Tub, DmelCG7923, hypoplastic-hypomaturation, CG7615, quotient, Peptide Hydrolase Inhibitors, quantitative, Pancreas Neoplasms, 6-dinitro-2-cresol, ADRB2R, reversed, SSc, Insulin B Chain, Systemic, DmelCG6829, zinc formate, LACS 1, lead salt, protein, Bar H1, peptide, School-Age, Cut, BETA2AR, Facl2, ammonium tetraformate, Atrophodermia vermiculata, anon-WO0134654.19, peptido, DmelCG4637, l(1)7Ba, l(1)7Bb, Atrophodermia reticulata, Volume, Apaf1, Progressive systemic sclerosis, protein aggregate, Hydrolase Inhibitors, PIST, systemic, neoplasm of pancreas, ducts, kDa, peptides, BRCC2, TACHD, 2610036I19Rik, membrane region, Bos bovis, hypoplasia, arc, PSS - Progressive systemic sclerosis, mAPC, IBP, BcDNA:LP01106, ark, SO, T1, keratosis pilaris atrophicans facies, insulin human, lithium salt, Sputolysin, l(2)k08110, domestic cow, blood capillary, Bladder pain syndrome, GPHYSD2, ammonium (2:1) salt, So, REPLUMLESS, BETA 56D, D-Apaf-1, rip14, ZC2HC5, lamina, detergent, Dmel_CG7826, Th, HTATIP1, TAFII-250, 7-11HD, membranous organ component, TAF250/230, Mus norvegicus, TAFII250, DmelCG5925, Cleland, School Age, BcDNA:GH10590, nickel (+2) salt, Dmel_CG7835, Acetic acid, MNB, PS-1, beta-tub, ammonium salt, Painful Bladder Syndrome, Step, endocrinocyte, cobaltous formate, FCAALL.331, 3-Butanediol, beta56D, DmelCG9277, AW124434, CG17603, TAF[[II]], 10-dihydro-4, beta-Tub, apaf-1, fetal AEDS, Fad, copper salt, Antiproteases, Fibrinopeptide B, GARD:0000632, Bladder Pain Syndrome, Nip40-1, VAN, fad, Dapaf-1/HAC-1, barium salt, cesium salt, dTAFII250, electron, cytohesin/GRP1, Argon 40, Hac1, Bar-H1, polypeptide chain, dmTAF1, subnumerary, ECTOL1, betaspec, integral component of membrane, 14C-labeled, Protease Antagonist, tiny, 6-dinitro-o-cresol, TAF250, l(2)10432, Rattus norvegicus, betatub(56D), layer, dapaf-1, l(2)SH2 0323, dapaf, calcium formate, Systemic sclerosis (disorder), Iletin, Neural-specific protein-tyrosine phosphatase, SPEC8, region of membrane, l(2)01501, TAF, 2-iodo-, KPA, HIV-1 Nef-interacting protein, small, Decidual protein induced by progesterone, Neonatal, Spec-beta, membrane, DYRK1, TAF[[II]]250, ABIN-1, protein complex, Tubulin, l(3)84Ab, strontium salt, count in organism, Sodium Insulin, p230, CAL, whole membrane, gram per millilitre, Dyrk1, Dark, connected anatomical system, b-Spec, LARSON, CYH1, 2410150O07Rik, diffuse sclerosis, jog, l(1)G0074, transmembrane, nup32D, Exubera, TAF[[II]]230, negatron, Nef-associated factor 1, INS, CC1, Tripcellim, Pancreatic Neoplasms, dApaf-1/DARK/HAC-1, chromic formate, incised, Protein Gene Products, DmelCG17603, Pressures, concentration, Acas, SSKS, calcium salt, layer of cells, Bar, l(3)62Ba, Spec, dAPAF-1, Enolase 3, TAF1, presence or absence in organism, Size, PLIP, cadmium salt, Laboratory, bar, 4-dinitro-o-cresol, ulerythema ophryogenesis, CG5925, Type 2A-interacting protein, Trifluoroacetate, Polypeptides, protein polypeptide chains, cobalt(II) formate dihydrate, Protease Inhibitor, GRP1, Barh1, HTATIP, ASD2, Endocrine Cell, CG11940, TFIID TAF250, sarcoma of breast, CG9277, PTPSTEP, keratosis pilaris, AI844555, beta-particle, proteins, PNCA2, AI047805, Pico, Bos Tauurus, Fmn, oxen, e-, column, cPLA2, ACN, fetal antiepileptic drug syndrome, AD3, Argon-40, honeycomb atrophy, RIP14, T7H20_80, TIP, GPH, B2AR, NEWBORN (0-27 DAYS), DMT1, Regular, BZRP, T7H20.80, familial, TAF200, Volumes, integral to membrane, l(2)SH0173, ANAC091, CG4637, PBS, PBR, Fibrinopeptides B, Putative MAPK-activating protein PM10, insulin (recombinant), soluble, Dm1, Hydrolase Inhibitor, Sizes, PANCREATIC NEOPL, Pancreatic, TIP60, 2-methyl-4, Soluble Insulin, CG6829, Acid, neoplasm of the pancreas, Antagonists, Skeletal muscle enolase, Dlt, alpha-D-Glucopyranoside, proportionality, insulina humana, fmol, rate, cromium (+3), Striatum-enriched protein-tyrosine phosphatase, 5-dihydroxyanthraquinone-2-carboxylic acid, rats, beta Trypsin, Pancreas, w/w, beta(-), DTB2, Fibrinogen beta chain, Painful bladder syndrome, i6, School-Age Population, Endopeptidase, beta-Tub56D, bovine, lead (+2) salt, TIP41, TAF230, hg, BPBS, Cleland Reagent, nickel formate dihydrate, GLM3, lead formate, sarcoma of the breast, Sclerosis, aluminum salt, e(-), 4-dimercapto-, pancreas, ABIN, protein-containing complex, thomson, CG5529, ESA1, Scleroderma (& [systemic sclerosis]), RNF47, TOF, Insulin, CG42273, Peptide Hydrolase, ZNF312, Interphases, Chain, Cesium Trifluoroacetate, DmelCG7615, proportion, desatF, Elektron, CG7923, beta-Trypsin, beta1t, dre1, SS - Systemic sclerosis, systemic Scleroderma, methanoic acid, ESI, kf, keratosis pilaris atrophicans, Nramp2, Solution, DmelCG4579, ms(2)zk, FANCB, bar-3, FANCD, ld, Drl, beta-tubulin56D, ds2, ds1, mKIAA0559, constant, Dmbeta1, mass percentage, diffuse, dApaf-1, BcDNA:LD21772, barh1, Proteins, Clelands Reagent, stepk, BG:DS00004.13, potassium formate, Mischung, backward, Pancreas Neoplasm, Cell, mk, Mdu, polypeptide, hrr-1, DmelCG5887, mda, Bos primigenius taurus, Laboratory Rats, Neoplasm, TAF[[II]]250/230, resting phase, Novolin, Systemic sclerosis, DmelCG32315, Naf1, X-linked 2, DmelCG5870, pancreatic tumor, lithium formate, underdeveloped, beta[[1]]-tubulin, med, foetal antiepileptic drug syndrome, flavin, Dark/Dapaf-1/HAC1, beta1, Peptidohydrolase Inhibitors, Muscle-specific enolase, mDRC, Scleroderma, beta, DmelCG11628, ME-IV, Cleland's Reagent, fxr, Cell Sizes, Gene Proteins, Peptidase, ZFP312, ox, Antiprotease, anon-WO0182946.19, sheath of cells, BETA, Newborn, Norway, Hac-1/Dark, Nup32D, Endopeptidase Inhibitor, determination, Peptide Hydrolase Inhibitor, DELTA AND GAMMA, Norway Rat, exocrine duct, betaTub1, PNY, CG11121, l(3)04276, B1t, old, BANF, dJ69E11.3, human insulin, Detergents, Min, Inhibitors, Norway rat, BROVCA2, Mir, present in fewer numbers in organism, ARK, DmelCG42273, pancreas tumour, insulin, FAD1, FAD2, PENNYWISE, FACS, 2610510L13Rik, min, analyzer, copper, tumor of pancreas, anatomical duct, CG11387, DEPP, Laboratory Rat, 1t, fSAP152, fad2, DNAse, trifluoro-, Fseg, desat, dApaf1, FACD, pancreatic tumour, pancreas neoplasm, ratio, pancreas tumor, Alzheimer disease, AU018810, Peptidase Inhibitor, PS1, Rattus, Peptide Peptidohydrolase, beta-D-fructofuranosyl, Fasting-induced gene protein, BLH9, l(1)G0108, ADRBR, bar3, 3.1.3.48, XRCC11, GOPC1, folliculitis ulerythematosa reticulata, Mnb, parent ion, Populations, membrane of organ, l(3)neo56, Beta <eudicots>, l(3)neo57, DNOC cpd, Trifluoroacetic, hac1, MASS, FA4, karyostasis, FAC sorting, organ system, dapaf-1S, Peptidase Inhibitors, dapaf-1L, FAD, precursor ion, Cesium, STEP, SR3-5, Acetamide, Polypeptide, Inhibitor, betaTub, beta1-Tubulin, Van, DCT1, d230, norvegicus, Reagent, FBN, Eno-3, Gene, Protease, Insulin B, ACINUS, EfW1, 2210402P09Rik, presence, formic acid, Dark/Hac-1/dApaf1, van, potassium salt, Dark/Hac-1/dApaf-1, reduced, DmelCG11121, cattle, Taf230, Arabidopsis NAC domain containing protein 91, zk, ulerythema ophryogenes, FANCD1, CG1977, desat2/Fad, 4.2.1.11, brown rat, PANCREAS NEOPL, Taf200, mVAN, hormones, somda, BB137857, lead(2+) salt, Mrt, beta[[1]] tubulin, uniform, Taf1p, dark, decreased number, OCTD, diffuse Scleroderma, DmelCG11387, DARK, 10-anthraquinone, cromium (+3) salt, l(3)S028813, School Age Population, dArk, Dapaf-1, FEZ, sodium formate, dipropionyl rhein, 6-dinitro-ortho-cresol, l(3)hh, data, nickel formate, DBI, strontium formate, apaf1, pancreas neoplasm (disease), Peptide, LSN, capillary vessel, natural protein, PKBS, Protein, 5-dinitro-2-hydroxytoluene, TFIID, betaSpec, l(2)SH0323, Dark/Apaf-I, WMS2, VSD1, l(1)G0198, systemic sclerosis, TAF[II]250, Thibierge-Weissenbach syndrome, dJ94G16.2, Trypure, FIG, beta-spec, Liver regeneration-related protein LRRG036|LRRG043|LRRG189, TCV-interacting protein, Peptid, BAR, assay, folliculitis ulerythematosa, SCH, BarHI, DNOCNEWBORN (0-27 DAYS), Neonatal, Rat, dTAF[[II]]230, TAF[[II]]250, d230, norvegicus, Laboratory, TAF200, Norway Rat, l(3)84Ab, dTAFII250, Rattus, BG:DS00004.13, TAFII-250, TAF250/230, EfW1, Norway Rats, Cell, dTAF230, dmTAF[[II]]230, rat, Mus norvegicus, TAFII250, Rats, dmTAF1, Taf230, p230, Laboratory Rats, TAF[[II]]250/230, TFIID, Norway rat, TAF250, brown rat, Taf[[II]]250, distinct., Taf200, Rattus norvegicus, dTAF[[II]]250, TAF[[II]]230, TFIID TAF250, cel, cell, Taf1p, TAF[II]250, CG17603, rats, TAF[[II]], Laboratory Rat, dTAF250, DmelCG17603, Taf250, SR3-5, Newborn, Norway, TAF, TAF230, TAF1Boars, ALCOHOL DEHYDROGENASE, TAPETUM 1, dairy cow, Bru, Cysteine Hydrochloride, 2-amino-4-(methylsulfanyl)butanoic acid, ion, Raw, False, Dehydrogenase, Sus scrofa domestica, Brewer's, cleavage, L Isomer, baker's yeast, Gene, protein, Serum, protein-containing complex, Saccharomyces italicus, peptide, Polypeptides, protein polypeptide chains, rat, Rattus sp. strain Wistar, L-Isomer Methionine, Drug Tolerance, Methionine, TAPETUM1, ClvPrd, peptido, polypeptide chain, biological_replicate, cattle, Alcohol:NAD+ oxidoreductase, Gene Products, technical_replicate, L-Methionine, Norway rat, wild boar, Del(8)44H, Rattus rattiscus, Half-Cystine, protein aggregate, Alcohol-NAD+, Pedameth, brown rat, Boar, Svc, Domestic Pig, proportion, Oxidoreductase, F, peptides, iones, L Cysteine, M, Bos bovis, beta-Trypsin, ASD, proteins, Baker, Domestic, Saccharomyces uvarum var. melibiosus, ions, Domestic Pigs, Alcohol Dehydrogenase I, S. cerevisiae, Bos Tauurus, TA1, S cerevisiae, oxen, data processing, Candida robusta, 2-amino-4-(methylthio)butanoic acid, Alcohol-NAD+ Oxidoreductase, 10^[-6], Saccharomyces capensis, ppm, sample, Pig, swine, Baker's, peptidos, Mycoderma cerevisiae, domestic cow, Half Cystine, brewer's yeast, rat <Rattus norvegicus>, rats <Rattus norvegicus>, Wild Boars, metionina, Racemethionine, Yeast Alcohol, drug tolerance, Alcohol NAD+ Oxidoreductase, Rattus norvegicus8, ratio, data, Alcohol, cow, Alcohol Dehydrogenase, Saccharomyces cerevisiae 'var. diastaticus', Zinc Cysteinate, DL-Methionine, Molars, protein complex, immune system tolerance, T5E21.12, pig, molar, Proteins, Wild Boar, pigs, 2-Amino-4-(methylthio)butyric acid, Sus scrofus, L-Isomer, Alcohol Dehydrogenase (NAD+), Peptide, Yeast Alcohol Dehydrogenase, Plasma Albumin, Baker's Yeasts, polypeptide, Alcohol Dehydrogenase II, Mus norvegicus, pigs <Sus scrofa>, Experiment, native protein, Rattus norwegicus, Immune Tolerance, natural protein, Ionen, dens molaris, Saccharomyces diastaticus, Bos primigenius taurus, Protein, sequence, Immunologic Tolerance, Methionin, domestic cattle, methionine, Hmet, fixed, Data Base, Met, T5E21_12, Saccharomyces oviformis, Yeast, Wild, technical replicate, Col4a-1, Protein., Sus scrofa domesticus, proportionality, Tripcellim, rate, L-Cysteine, rats, beta Trypsin, primary structure of sequence macromolecule, sample population, Protein Gene Products, Pigs, Gene Proteins, Trypure, data analysis, biological replicate, Self Tolerance, Albumin, Tolerance, ox, Ion, concentration, quotient, alpha-amino-gamma-methylmercaptobutyric acid, Peptid, Polypeptide, Baker's Yeast, variable, bovine, Liquimeth, Brewer's Yeast, Baker Yeast, Gunn rats, Immunological Toleranceliquid chromatography tandem mass spectroscopy, Rat, para Tyrosine, beta cell of pancreatic islet, delta, Activity, Laboratory, Ass-1, Glukose, adult stage, basophil cell of anterior lobe of hypophysis, DELTA AND GAMMA, Monohydrate, Norway Rat, pancreatic beta-cell, protein, SCP1, (DL)-Isomer, betaTub1, Norway Rats, CG11121, hydroxybutanedioic acid, UCRBP, dmTAF[[II]]230, YIN-YANG-1, rat, protein polypeptide chains, B1t, old, forelimb autopod, 0926/11, Associations, AA408052, Dextrose, fold, Norway rat, protein aggregate, adult, beta cell islet, beta cell, increased, D, me75, DELTA, DLK-1, LCMSMS, kus, beta1tub, TFIID TAF250, enzymes, CG9277, Genomes, cel, HAND, C1, 2-amino-3-(4-hydroxyphenyl)propanoic acid, 3-(p-Hydroxyphenyl)alanine, Tissue, Delta1, T, beta-particle, Bodily, bHLHa28, proteins, Y, SO, D17Mit170, DL-glucose, T1, 2-hydroxybutanedioate, Laboratory Rat, endocrine, hand, DELTA1, ASS, glucose, 1t, e, Secretion, e-, beta1Tub, Secretions, Tyr, malate anion, delta D1, pancreatic B-cell, Delta, associated, CG3619, So, islet beta cell, accumulated, forefoot of quadruped, LC-MS2, NEWBORN (0-27 DAYS), dTAF[[II]]230, BETA 56D, wide/broad, DL, 1053/14, islets of Langerhans part of pancreas, external secretion, LC-MS/MS, 2-Amino-3-(p-hydroxyphenyl)propionic acid, TAF200, pref-1, Rattus, terminal segment of free upper limb, para-Tyrosine, TAFII-250, TAF250/230, Oligonucleotide, Tl3, Tl2, Tyrosine, insulin-secreting cell, exocrine gland fluid/secretion, Bodily Secretion, TAFII250, Mus norvegicus, l(1)G0108, DL1, NF-E1, malate dianion, precocious, FLOWERING TIME CONTROL PROTEIN FCA ALPHA, secretion, (alpha-D)-Isomer, Adults, tyrosine, D-Glucose, DLK, beta-tub, adults, Beta <eudicots>, protein_coding_transcript, DmelCG3619, L-isomer, FCAALL.331, FA1, beta56D, DmelCG9277, 1304/03, CG17603, TAF[[II]], rats, CT12133, early, beta1-tub, beta(-), L isomer, DTB2, pancreatic beta cell, beta-Tub, PREF1, wide, Taf250, D Glucose, SR3-5, liquid chromatography-tandem mass spectroscopy, hand region, i6, DL4180C, Biocatalyst, fore paw, L-Tyrosine, l(3)92Ab, beta-Tub56D, Glucose Monohydrate, forefoot, exocrine gland secretion, Proteomes, betaTub, Specbeta, TAF230, accessory, beta1-Tubulin, gluco-hexose, AW742678, forelimb autopodium, l(3)j8C3, d230, advanced, exocrine gland fluid, norvegicus, Glucose, exocrine gland fluid or secretion, Biocatalysts, anon-WO0118547.269, e(-), Gene, dTAFII250, electron, broad, protein-containing complex, EfW1, supernumerary, LC-MS-MS, Rats, B-spec, polypeptide chain, dmTAF1, DmelCG11121, Taf230, betaspec, Insulin, LC-MSMS, CG18144, Gene Products, type B enteroendocrine cell, Low, pG2, TAF250, brown rat, study, Taf200, hormones, somda, betatub(56D), dTAF[[II]]250, Rattus norvegicus, pituitary beta cell, 1119/09, cell, Ly107, Elektron, beta[[1]] tubulin, dHand, INO80S, beta1t, aspartate(2-), messenger RNA, Taf1p, mal, Dhand, anon-EST:fe1B3, dTAF250, secreted substance, template RNA, Enzyme, hand-C, bodily secretion, L Tyrosine, LMPY, SPEC8, dHAND, dmDelta, CG5870, Tyrosin, TAF, Anhydrous, Drl, Neonatal, beta-tubulin56D, Spec-beta, Dmbeta1, TAF[[II]]250, cou, (beta-D)-Isomer, l(3)05151, protein complex, Proteins, 1440/11, pars endocrina pancreatis, Tubulin, l(3)84Ab, enzyme activity, BG:DS00004.13, function, i168, aspartate, Cell, Mdu, dTAF230, insulin cell, Peg9, endocrine pancreas, LC/MS/MS, Lr, pancreatic islet core, native protein, natural protein, tirosina, mda, p230, fore-paw, Laboratory Rats, Protein, 0495/20, endocrine part of pancreas., TAF[[II]]250/230, INSDC_feature:mRNA, betaSpec, TFIID, malate, Zog, ZOG, aspartic acid dianion, forefeet, b-Spec, ami, 2-aminosuccinate, Taf[[II]]250, DmelCG5870, l(1)G0074, pancreatic B cell, DlkI, l(1)G0198, TAF[[II]]230, negatron, distinct, underdeveloped, mRNA, beta[[1]]-tubulin, med, increased number, 1423/11, DmelCG18144, 2-aminobutanedioate, b spectrin, beta1, TAF[II]250, ion(2-), E(ls)2, beta, Anhydrous Dextrose, Pref-1, Tub, Hands, pancreatic islet beta cell, Protein Gene Products, present in greater numbers in organism, B-cell of pancreatic islet, Gene Proteins, DmelCG17603, 1485/04, beta-spec, fore foot, BETA, Bra, forepaw, liquid chromatography tandem mass spectrometry, Newborn, Norway, responsive, General activity, Spec, TAF1, Glcliquid chromatography tandem mass spectroscopy, Rat, para Tyrosine, delta, Activity, Laboratory, Glukose, adult stage, Monohydrate, Norway Rat, protein, SCP1, (DL)-Isomer, Norway Rats, CG11121, hydroxybutanedioic acid, UCRBP, dmTAF[[II]]230, YIN-YANG-1, rat, protein polypeptide chains, old, forelimb autopod, 0926/11, Associations, Dextrose, Norway rat, protein aggregate, adult, increased, D, me75, DELTA, DLK-1, LCMSMS, TFIID TAF250, enzymes, Genomes, cel, HAND, C1, 2-amino-3-(4-hydroxyphenyl)propanoic acid, 3-(p-Hydroxyphenyl)alanine, Tissue, Delta1, Bodily, bHLHa28, proteins, Y, SO, D17Mit170, DL-glucose, T1, 2-hydroxybutanedioate, Laboratory Rat, endocrine, hand, DELTA1, glucose, Secretion, Secretions, Tyr, malate anion, delta D1, Delta, associated, CG3619, So, accumulated, forefoot of quadruped, LC-MS2, NEWBORN (0-27 DAYS), dTAF[[II]]230, wide/broad, DL, 1053/14, islets of Langerhans part of pancreas, external secretion, LC-MS/MS, 2-Amino-3-(p-hydroxyphenyl)propionic acid, TAF200, pref-1, Rattus, terminal segment of free upper limb, para-Tyrosine, TAFII-250, TAF250/230, Oligonucleotide, Tl3, Tl2, Tyrosine, exocrine gland fluid/secretion, Bodily Secretion, TAFII250, Mus norvegicus, DL1, NF-E1, malate dianion, precocious, secretion, (alpha-D)-Isomer, Adults, tyrosine, D-Glucose, DLK, adults, protein_coding_transcript, DmelCG3619, L-isomer, FA1, 1304/03, CG17603, TAF[[II]], rats, CT12133, early, L isomer, PREF1, wide, Taf250, D Glucose, SR3-5, liquid chromatography-tandem mass spectroscopy, hand region, Biocatalyst, fore paw, L-Tyrosine, l(3)92Ab, Glucose Monohydrate, forefoot, exocrine gland secretion, Proteomes, TAF230, accessory, gluco-hexose, AW742678, forelimb autopodium, l(3)j8C3, d230, advanced, exocrine gland fluid, norvegicus, Glucose, exocrine gland fluid or secretion, Biocatalysts, anon-WO0118547.269, Gene, dTAFII250, broad, protein-containing complex, EfW1, supernumerary, LC-MS-MS, Rats, polypeptide chain, dmTAF1, DmelCG11121, Taf230, Insulin, LC-MSMS, CG18144, Gene Products, Low, pG2, TAF250, brown rat, study, Taf200, hormones, somda, dTAF[[II]]250, Rattus norvegicus, 1119/09, cell, Ly107, dHand, INO80S, aspartate(2-), messenger RNA, Taf1p, mal, Dhand, dTAF250, secreted substance, template RNA, Enzyme, hand-C, bodily secretion, L Tyrosine, LMPY, dHAND, dmDelta, Tyrosin, TAF, Anhydrous, Drl, Neonatal, TAF[[II]]250, cou, (beta-D)-Isomer, l(3)05151, protein complex, Proteins, 1440/11, pars endocrina pancreatis, l(3)84Ab, enzyme activity, BG:DS00004.13, function, aspartate, Cell, Mdu, dTAF230, Peg9, endocrine pancreas, LC/MS/MS, Lr, native protein, natural protein, tirosina, mda, p230, fore-paw, Laboratory Rats, Protein, 0495/20, endocrine part of pancreas., TAF[[II]]250/230, INSDC_feature:mRNA, TFIID, malate, Zog, ZOG, aspartic acid dianion, forefeet, ami, 2-aminosuccinate, Taf[[II]]250, DlkI, TAF[[II]]230, distinct, underdeveloped, mRNA, med, increased number, 1423/11, DmelCG18144, 2-aminobutanedioate, TAF[II]250, ion(2-), E(ls)2, Anhydrous Dextrose, Pref-1, Hands, Protein Gene Products, present in greater numbers in organism, Gene Proteins, DmelCG17603, 1485/04, fore foot, Bra, forepaw, liquid chromatography tandem mass spectrometry, Newborn, Norway, responsive, General activity, TAF1, GlcRat, d230, norvegicus, Laboratory, e(-), DELTA AND GAMMA, Norway Rat, dTAFII250, electron, betaTub1, EfW1, Norway Rats, dmTAF[[II]]230, rat, B1t, Rats, B-spec, dmTAF1, Taf230, betaspec, Norway rat, TAF250, brown rat, Taf200, Rattus norvegicus, betatub(56D), dTAF[[II]]250, kus, beta1tub, TFIID TAF250, CG9277, cel, cell, Elektron, beta[[1]] tubulin, beta1t, T, beta-particle, Taf1p, Laboratory Rat, anon-EST:fe1B3, dTAF250, 1t, e, e-, beta1Tub, SPEC8, CG5870, TAF, NEWBORN (0-27 DAYS), Neonatal, beta-tubulin56D, Spec-beta, Dmbeta1, dTAF[[II]]230, TAF[[II]]250, BETA 56D, TAF200, Tubulin, l(3)84Ab, Rattus, BG:DS00004.13, TAFII-250, i168, TAF250/230, Cell, dTAF230, Mus norvegicus, TAFII250, l(1)G0108, p230, Laboratory Rats, TAF[[II]]250/230, betaSpec, TFIID, FLOWERING TIME CONTROL PROTEIN FCA ALPHA, b-Spec, Taf[[II]]250, distinct., beta-tub, DmelCG5870, l(1)G0074, l(1)G0198, TAF[[II]]230, Beta <eudicots>, negatron, beta[[1]]-tubulin, b spectrin, FCAALL.331, beta1, TAF[II]250, beta56D, DmelCG9277, CG17603, rats, TAF[[II]], beta, beta1-tub, beta(-), DTB2, Tub, beta-Tub, DmelCG17603, Taf250, beta-spec, SR3-5, i6, DL4180C, BETA, Newborn, Norway, beta-Tub56D, Spec, betaTub, Specbeta, TAF230, beta1-Tubulin, TAF1408trueFunctional characteristics of neonatal rat beta cells With distinct markersNeonatal beta cells are considered developmentally immature and hence less glucose-responsive. To study the acquisition of mature glucose-responsiveness, we compared glucose-regulated redox state, insulin synthesis and secretion of beta cells purified from neonatal or 10-weeks old rats to their transcriptomes and proteomes measured by oligonucleotide and LC-MS/MS profiling. Lower glucose-responsiveness of neonatal beta cells was explained by two distinct properties: higher activity at low glucose and lower activity at high glucose. Basal hyperactivity was associated with higher NAD(P)H, a higher fraction of neonatal beta cells actively incorporating 3H-Tyrosine, and persistently increased insulin secretion below 5 mM glucose. Neonatal beta cells lacked the steep glucose-responsive NAD(P)H rise between 5-10 mM glucose characteristic for adult beta cells, and accumulated less NAD(P)H at high glucose. They had 2-fold lower expression of malate/aspartate-NADH shuttle and most glycolytic enzymes. Genome-wide profiling situated neonatal beta cells at a developmental crossroad: they showed advanced endocrine differentiation when specifically analyzed for their mRNA/protein level of classical neuroendocrine markers. On the other hand, discrete neonatal beta cell subpopulations still expressed mRNAs/proteins typical for developing/proliferating tissues. One example, Delta-like 1 homolog (DLK1) was used to investigate if neonatal beta cells with basal hyperactivity corresponded to a more immature subset with high DLK1, but no association was found. In conclusion, the current study supports the importance of glycolytic NADH-shuttling in stimulus-function coupling, presents basal hyperactivity as novel property of neonatal beta cells, and provides potential markers to recognize intercellular developmental differences in the endocrine pancreas.2014-12-122014-12-05PXD00157728065516460991804982953585111454224942024527872842188090368093270429330845811363336351524260119834300662758385NCBITaxon:128068888561896111430118726355557114526236493461364031952065126957366649274670738538836411354615821582310665688954762721123294422291180992323122586365458333460792519365914320597129386558195851149315242592637371250232NCBITaxon:127211195774818661488584310430024513586722175543740816918045426683429531945305861266835149822505814963674452158554528113208147956410039237514636942049433208964208963445974137979138712728384400667453293529367156759388036478434716052165994048321659721659545501315282693042165915627161696833218321729204277944762376454317203094980197525556978159509439843948840479NCBITaxon:2157525338551531051067439899037122857759515205968762262311210884555588845587077918178081736309431794571698936160488409859NCBITaxon:3716210478267940150590714836432042106132049138169363035554320466326333119945654535110254111032174592161292642012886764100264203694569410167634102107612773515248671316582392547279334281461358430141729876091746334577444916754760489321287356756840301350621917265181301941119294393671104113102393202555986325827883965910475934749516049016529983552566317585439801102432608663102459808757417555183201964471452680457966313670190832331156114155355104219325552113834397634981812359871069955529NCBITaxon:4751850298335476113615741465477180066556484337677299767982510216998238976484074137351155711089725482444474153NCBITaxon:505578996984410003646534933414714749354801946751299114359741276473137086326547876565893639835322159589366983819201110677577271034819852348780265554479464098609958615718717668599191572951372211711012929210768783497419860202809148840633424923423515233598598865597464998703920211107294331171139363527215987419085037117082711708284182350241451139692931902197822474636046147123749402375939723287581722532566489050794526591972211915853101774208588596NCBITaxon:615750521028307989515586411051989972375059576131720002634196102641088878176179212190659407121906772275885815689964975151950582873757244NCBITaxon:22023717NCBITaxon:17036122019998570506050617476792745062724915961533355418400524643213686150596487844612286662941786661347515363291018194301086731018510184NCBITaxon:1763573039635586331492862876705801321650852718481865368595105135553482260710185687294296110091416333NCBITaxon:619184023210007348824123363630710470058127187878645159812894555663577553470951451225786425011260704NCBITaxon:13356262607052607076584574054163677483167233150561007133705654195NCBITaxon:305550445791399878168119011928752829126806315327341478281055524NCBITaxon:9606135858469008111167815022830519302836728593008529005NCBITaxon:569382688306401794699151011849943525875913151590144824283811139442258441604193704759272370860423281677285035158199011951953267386370137024924053608838581622488186156227748817562615835583715333760572671193501998086119350216787910857913711371272407190650371475917262981288057125627457572709030903113335503728142433747924910078711082NCBITaxon:96157243359463318586260799141262200298492670NCBITaxon:126371928124921252830385683856959116926610065813735237561275045426662551519788135663837506442233600941293497905463224535247214012575151164990851515143899237453747445446415243235937605920222887051580595536555088157932716029385157811497863389229382894535936479437NCBITaxon:68544127542251177529915901090134167387158955210129661030612967158515845158493765939343271591002263767338899046142345128768959119833296646704146479293657616428034116022164133159928038280353690910891768814989462181214108034817939228788929502711313329528282944568617493468191126526997227321890382107601247190400727159736997828114311402064119810871355477436581424507229533796982042321242231291632180334708714537209164573321535815754699287770202060328114319338293550833291292211486437457252649997283035739087183087267271037908550717629970767892683704155737292140532941281607839563924314262654898227377561155962073220865958827355516936053307972551811354914321371597495350261159556143213840607258781414471509493349194963401614334728005936046316461046603815184547448500356709747777195124017484185560133575554792042741580536076994688103762014887100594120037582890931643542826885007123038399001389464940838283594144242322197857742171598921409212205853939621157781154756929793244704749906604162103591905158114452749907312987779913112273170187546991103589915NCBITaxon:37296103609833418710491130798133679531640729946710340157865826453033373306383011306413992530642363650591169654788546981121162034317652616103372861299404458620734011535711195296526117455311147161338654131316634305521323120179836025323731276125523299351299385057316317642619794011513458445772678728623219334151346186208621160791392227983516811961255228149539322323116761757312108077213487999948861856962814084341033517787996321849620994887321392488209711533820961153392095330439375569927612686266447NCBITaxon:269704933986243694110312195883205092029061013068599975864445882864324995252972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