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Pathophysiology

Gene Expression Profile in Skeletal Muscle of Type 2 Diabetes and the Effect of Insulin Treatment

  1. Raghavakaimal Sreekumar,
  2. Panagiotis Halvatsiotis,
  3. Jill Coenen Schimke and
  4. K. Sreekumaran Nair
  1. From the Endocrinology Division, Mayo Clinic, Rochester, Minnesota
    Diabetes 2002 Jun; 51(6): 1913-1920. https://doi.org/10.2337/diabetes.51.6.1913
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      FIG. 1.

      Real-time PCR data (mRNA levels) of GLUT4, IGFBP5, SOD2, UCP-3, and MHC-I in D2− patients (▪) and D2+ patients (□) (mean ± SE percent change from control subjects). The P values were significant for three genes (GLUT4, SOD2, and MHC-I) in the control versus D2− comparison and also for GLUT4 and IGFBP5 in the control versus D2+ comparison. *P < 0.01; #P < 0.05.

    Tables

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    • TABLE 1

      Characteristics of subjects

      Study populationAge (years)BMI (kg/m2)Average glucose (mg/dl)Insulin level (μU/ml)SI (minimum model)
      Control52.4 ± 4.129.2 ± 1.590.0 ± 2.95.2 ± 0.15.96 ± 1.04*
      Diabetic Patients (D2−)52.8 ± 3.529.1 ± 1.4224.0 ± 26.2*5.8 ± 0.61.82 ± 0.62
      Diabetic Patients (D2+)52.8 ± 3.529.1 ± 1.498.8 ± 6.413.5 ± 2.9†2.37 ± 0.8
      • Data are means ± SE.

      • *

        * P < 0.001;

      • †

        † P < 0.05 vs. other two groups. Five subjects were studied in each group (two men and three women).

    • TABLE 2

      Differences in gene transcript levels of type 2 diabetic patients (D2−) and insulin-treated type 2 diabetic patients (D2+) in comparison with control subjects

      Probe setFold Δ
      Gene name
      AB
      Structural/contractile
       HG2743-HT2846↑3.3*(↑1.5)†Caldesmon 1
       HG1862-HT1897↑2.0‡(↑2.9)§Calmodulin type I
       HG2175-HT2245↓4.9*(↓1.4)†Myosin heavy chain polypeptide
       HG2260-HT2349↓3.9‖(↓1.4)†Duchenne Muscular Dystrophy protein
       M21984↓3.2*(↓1.7)†Troponin-T
       M21665↓3.1*(↓1.7)†MHC-I
       HG3514-HT3708↓2.5*(↓1.2)†Tropomyosin (cytoskeletal)
       X04201↓2.4*(↓1.9)*Tropomyosin (1.3 kb)
       X66276↓2.4*(↓2.0)§Skeletal muscle C-protein
       L21715↓2.3‖(↓2.1)§Troponin-I fast-twitch
       J04760↓2.2*(↓2.0)*Troponin-I slow-twitch
       M20642↓2.1‡(↓1.4)†Myosin light chain
       M20543↓2.0‖(↓1.5)†Skeletal muscle α-actin
       U35637↓2.0‡(↓1.5)†Nebulin
       X13839↓1.9‡(↓1.8)†Smooth muscle α-actin
       M33772↓1.9†(↓2.1)*Troponin-C fast-twitch
      Mitochondrial maintenance/chaperone
       X93511↓2.4*(↓1.3)†Telomeric DNA binding protein
       X83416↓2.4§(↓1.4)†PrP
       V00594↓2.2‡(↓1.6)†MT
       X82200↓2.2‖(↓1.8)†Staf50
       X65965↓2.2‖(↓1.2)†SOD2
       HG2855-HT2995↑2.0*(↑3.2)*Heat shock protein, 70 kDa
      Growth factors/tissue development/maintenance
       L27560↑2.5*(↑2.9)*IGFBP-5
       M55210↓3.9*(↓1.7)†Laminin B2 chain
       L08246↓3.4‡(↓2.2)§MCL1
       AB000897↓2.8‖(↓2.1)§Cadherin FIB3
      Insulin signaling/signal transduction/glucose metabolism
       HG2702-HT2798↓5.6‖(↓1.4)†Serine/threonine kinase
       D23673↓2.8*(↓1.3)†IRS-1
       L10717↑2.9‡(↓1.3)†T-cell–specific tyrosine kinase
       L33881↓3.1†(↓1.4)†Protein kinase C-ι
       K03515↑2.3‡(↓1.4)†Neuroleukin
       J04501↓2.4‖(↓1.6)†Muscle glycogen synthase
       U27460↓2.3*(↓1.2)†UDP-glucose pyrophosphorylase
       M91463↓2.1§(↓1.3)†GLUT4
       M32598↓2.0*(↓1.2)†Muscle glycogen phosphorylase
      Energy metabolism
       D16480↑3.1*(↑1.6)†Mitochondrial enoyl-CoA hydratase
       D10523↑2.3‖(↑1.2)†2-Oxoglutarate dehydrogenase
       AF001787↓2.7§(↓1.4)†UCP-3
       X13794↓2.7‡(↓1.4)†Lactate dehydrogenase B
       M83186↓2.5‖(↓1.7)†COX VIIa
       M19483↓2.4‖(↓1.4)†ATP synthase β subunit
       U65579↓2.3‡(↓2.0)‡NADH dehydrogenase-ubiquinone
       X69433↓2.2‖(↓1.2)†Mitochondrial isocitrate dehydrogenase
       U94586↓2.2‖(↑1.2)†NADH-ubiquinone oxidoreductase
       HG4747-HT5195↓2.1*(↓1.1)†NADH-ubiquinone oxidoreductase MLRQ
       M22760↓2.1‡(↓1.3)†COX Va
       U09813↓2.0§(↑1.2)†ATP synthase subunit 9
       X83218↓2.0§(↓1.1)†ATP synthase
       U17886↓2.0§(↓1.2)†Succinate dehydrogenase (SDHB)
       L32977↓1.9§(↑1.4)†Ubiquinol cytochrome C reductase
      Transcription factors/protein metabolism
       HG1428-HT1428↓2.1‡(↓1.4)†Globin-β
       HG3635-HT3845↓3.8*(↓1.6)†Zinc finger protein, krupple
       X69116↓3.7*(↓1.7)†Zinc finger protein
       X16064↓2.2*(↓1.5)†Translationally controlled tumor protein
       U37690↓2.0‖(↓1.3)†RNA polymerase II subunit
       U95040↓2.1‡(↓1.2)†hKAP1/TIF1B
       U65928↓1.9*(↓1.1)†Jun activation domain binding protein
       HG3214-HT3391↑2.9*(↓1.8)†Metallopanstimulin 1
       U73379↑2.3‡(↓1.3)†Cyclin-selective ubiquitin carrier
       X03689↑2.3‡(↓1.4)†Elongation factor TU
       M17886↓2.1*(↓1.7)†Acidic ribosomal phosphoprotein P1
       U49869↓2.1*(↓1.5)†Ubiquitin
       Z21507↓2.0‡(↓1.5)†Elongation factor-1 Δ
       U14968↓1.9‡(↑1.5)†Ribosomal protein L27a
       U14973↓1.9‡(↓1.4)†Ribosomal protein S29
      • A, control versus D2− patients; B, control versus D2+ patients.

      • *

        * P < 0.01,

      • †

        † P > 0.05,

      • ‡

        ‡ P < 0.05,

      • §

        § P < 0.0001,

      • ‖

        ‖ P < 0.001, with P values calculated from t test on the average difference between control subjects and D2− (A) or D2+ (B) patients.

    • TABLE 3

      Additional genes altered in type 2 diabetes (D2− and D2+)

      Probe setFold Δ
      Gene nameClass/function
      AB
      HG2239-HT2324↑11*(↑1.3)†Potassium channel proteinIon channel
      U90546↑5.8*(↑1.7)†Butyrophilin 4Immune system
      X89267↑3.6*(↑1.5)†Uroporphyrinogen decarboxylaseHeme biosynthesis
      L24564↑3.2‡(↑1.8)†RadRas-oncogene associated with diabetes
      D43951↑3.1§(↑1.3)†KIAA0099Unknown
      D79986↑2.3§(↑1.3)†KIAA0164Unknown
      J02611↑2.1‡(↑1.8)†Apolipoprotein DLipid transport
      L11238↓3.2§(↓1.6)†Platelet membrane glycoprotein VHomeostasis
      X59405↓3.0‖(↓1.5)†Membrane cofactor proteinRegulatory glycoprotein
      X63575↓2.8‡(↓1.5)†Calcium ATPaseCalcium homeostasis
      M16714↓2.6§(↓1.6)†MHC I lymphocyte antigenImmune system
      X00371↓2.5*(↓1.8)†MyoglobinOxygen transport
      X91103↓2.5§(↓1.2)†Hr44Immune system
      X01060↓2.4‡(↓1.6)†Transferrin receptorIron uptake
      U90313↓2.3§(↓1.4)†Glutathione-S-transferaseGlutathione metabolism
      X75755↓2.3‡(↓1.3)†PR264Unknown
      U33286↓2.2§(↓1.2)†Chromosome segregation gene CASCell proliferation/apoptosis
      X15729↓2.1§(↓1.5)†Nuclear p68 proteinCell poliferation
      X06700↓2.1§(↓1.7)†Pro-α (III) collagenExtracellular matrix protein
      AB000220↓1.9*(↓1.4)†Semaphorin EImmune system
      • A, control versus D2− patients; B, control versus D2+ patients.

      • *

        * P < 0.05,

      • †

        † P > 0.05,

      • ‡

        ‡ P < 0.001,

      • §

        § P < 0.01,

      • ‖

        ‖ P < 0.0001, with P values calculated from t test on the average difference between control subjects and D2− (A) or D2+ (B) patients.

    • TABLE 4

      Gene transcripts remain unaltered by 10 days of insulin treatment in type 2 diabetic patients

      Fold ΔGene name
      Structural/contractile genes
       ↑2.9*Calmodulin Type I
       ↓2.1*Troponin I fast-twitch
       ↓2.1†Troponin C fast-twitch
       ↓2.0*Skeletal muscle C-protein
       ↓2.0†Troponin I slow-twitch
       ↓1.9†Tropomyosin
      Stress response/energy metabolism
       ↑3.2†Heat shock protein, 70 kDa
       ↓2.0‡NADH dehydrogenase-ubiquinone
      Growth factor/tissue development
       ↑2.9†IGFBP-5
       ↓2.2*MCL1
       ↓2.1*Cadherin FIB3
      • *

        * P < 0.0001,

      • †

        † P < 0.01,

      • ‡

        ‡ P < 0.05, with P values calculated from t test on the average difference between control and D2+ subjects.

    • TABLE 5

      Gene transcripts altered (which was normal in D2−) with 10 days of insulin treatment in type 2 diabetic patients

      Fold ΔGene name
      Structural/Contractile/ Growth factor
       ↑2.2*ACTN3
       ↑2.1*CO-029
       ↓2.7†SM22
       ↓2.6*Sarcolipin
       ↓2.2*β-Tropomyosin
       ↓1.9‡Cytoskeletal gamma-actin
       ↑1.9*IGF-II
      Protein metabolism/Signal transduction
       ↑2.0*eIF-4C
       ↑1.9*Ribosomal protein L21
       ↓2.6†Ubiquitin carboxyl terminal hydrolase
       ↓2.3*Ribosomal protein L37a
       ↓2.0*Elongation factor 1 alpha-2
       ↑2.3*AMP-activated protein kinase
       ↑2.1*Protein tyrosine phosphatase, alpha
       ↓2.7†Tyrosine kinase receptor
       ↓2.5†Adenylyl cyclase
      Immune system/energy metabolism/cell adhesion
       ↑2.1*Class II histocompatibility antigen DC-α-chain
       ↑2.3†HK1
       ↓1.9*NDUFV3
       ↓3.8*Fibronectin
       ↓2.4†HSPG2
      Tissue development/fatty acid metabolism
       ↑2.1†Cadherin FIB2
       ↓2.4*Fatty acid binding protein
      Transposition/extracellular matrix/unknown
       ↑2.0*Transposon-like element
       ↓2.3*Tenascin-X
       ↑3.0†GOS2
       ↑2.6*H4 Histone
       ↓2.1*SCAMP1
       ↓2.0†Phosphodieaterase 3B
      • *

        * P < 0.01,

      • †

        † P < 0.0001,

      • ‡

        ‡ P < 0.05; P values were calculated from t test on the average difference between control and D2+ subjects. Metallopanstimulin 1 (↓1.8) was the only gene that showed <1.9-fold alteration in gene expression in D2− or D2+ patients compared with the control subjects, with a statistical significance in the above t test (P = 0.04).

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    Gene Expression Profile in Skeletal Muscle of Type 2 Diabetes and the Effect of Insulin Treatment
    Raghavakaimal Sreekumar, Panagiotis Halvatsiotis, Jill Coenen Schimke, K. Sreekumaran Nair
    Diabetes Jun 2002, 51 (6) 1913-1920; DOI: 10.2337/diabetes.51.6.1913

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    Gene Expression Profile in Skeletal Muscle of Type 2 Diabetes and the Effect of Insulin Treatment
    Raghavakaimal Sreekumar, Panagiotis Halvatsiotis, Jill Coenen Schimke, K. Sreekumaran Nair
    Diabetes Jun 2002, 51 (6) 1913-1920; DOI: 10.2337/diabetes.51.6.1913
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