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Cancer Prevention Research
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Research Article

Plasma Metabolomic Profiles of Breast Cancer Patients after Short-term Limonene Intervention

Jessica A. Miller, Kirk Pappan, Patricia A. Thompson, Elizabeth J. Want, Alexandros P. Siskos, Hector C. Keun, Jacob Wulff, Chengcheng Hu, Julie E. Lang and H.-H. Sherry Chow
Jessica A. Miller
1University of Arizona Cancer Center, Tucson, Arizona.
2Department of Nutritional Sciences, University of Arizona, Tucson, Arizona.
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  • For correspondence: jam1@email.arizona.edu
Kirk Pappan
3Metabolon, Inc., Durham, North Carolina.
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Patricia A. Thompson
4Department of Pathology, Stony Brook University, Stony Brook, New York.
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Elizabeth J. Want
5Department of Surgery and Cancer, Imperial College, London.
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Alexandros P. Siskos
5Department of Surgery and Cancer, Imperial College, London.
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Hector C. Keun
5Department of Surgery and Cancer, Imperial College, London.
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Jacob Wulff
3Metabolon, Inc., Durham, North Carolina.
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Chengcheng Hu
6College of Public Health, University of Arizona, Tucson, Arizona.
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Julie E. Lang
7Norris Comprehensive Cancer Center, University of Southern California, Los Angeles, California.
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H.-H. Sherry Chow
1University of Arizona Cancer Center, Tucson, Arizona.
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DOI: 10.1158/1940-6207.CAPR-14-0100 Published January 2015
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    Figure 1.

    Metabolites that changed significantly from pre- to postintervention are in bold with their fold change and P value indicated. The pattern of changes supports restricted entry or usage of glucose-derived carbons with preferential incorporation of fatty acids into the TCA cycle.

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    Figure 2.

    The up and down arrows indicate observed changes with limonene intervention. Bold arrows indicate the hypothesized chain of events; limonene causes apoptosis in multiple cells types and is known to deposit in adipose tissue (top box), this leads to the hypothesized altered metabolism in the liver (bottom box) and may explain the observed changes in metabolites in circulation (middle box). Gly, glycine; Ala, alanine.

Tables

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  • Table 1.

    Metabolites that changed after 2 to 6 weeks daily limonene intervention (72 metabolites P ≤ 0.05; 39 metabolites Q ≤ 0.10)

    Fold changePQ
    Adrenal steroids
     Androsterone-S0.75<0.001<0.001
     Epiandosterone-S0.79<0.001<0.001
     Pregnendiol disulfate0.82<0.0010.01
     4-androsten-3β,17β diol disulfate 20.900.010.06
     DHEA-S0.930.020.12
    Secondary bile acids
     Glycodeoxycholate2.30<0.010.02
     Glycoursodeoxycholate3.60<0.010.03
     Taurodeoxycholate3.50<0.010.03
     Taurocholate3.40<0.010.03
     Taurocholenate sulfate0.900.010.06
     Glychochenodeoxycholate2.500.010.92
     Glycocholate2.600.020.10
     Taurochenodeoxycholate2.000.020.12
     Deoxycholate1.700.050.18
    Glucose/energy metabolism
     Glucuronate1.83<0.010.03
     Pyruvate1.66<0.010.03
     Acetylcarnitine0.89<0.010.03
     3-hydroxybutyrate (BHBA)1.090.010.06
     Fructose1.560.020.10
     Mannitol4.870.030.14
     Citrate0.940.040.17
     Malate1.380.040.17
    Collagen breakdown products
     Glycine1.380.010.01
     Proline1.20<0.0010.01
     Trans-4-hydroxyproline1.70<0.0010.01
     Pro-hydroxy-pro1.400.020.11
    Amino acids and metabolites
     Indolepropionate2.60<0.001<0.001
     Alanine1.21<0.0010.02
     3-phenylpropionate (hydrocinnamate)1.95<0.0010.01
     3-(4-hydroxyphenyl)lactate0.87<0.010.03
     Kynurenate0.87<0.010.04
     Phenylacetate2.080.010.06
     γ-glutamylisoleucine0.910.010.07
     α-hydroxybutyrate (AHB)0.900.010.08
     Phenylalanyltryptophan0.920.010.08
     Aspartate0.930.020.12
     N-acetylglycine1.410.030.13
     γ-glutamylalanine1.150.030.13
     α-hydroxyisovalerate0.930.030.13
     Aspartylphenylalanine1.090.030.13
     Isoleucylvaline1.470.030.15
     Phenylalanine0.950.040.13
     Isobutyrylcarnitine1.480.050.18
    Fatty acids
     Tetradecanedioate0.84<0.0010.01
     Hexadecanedioate0.82<0.0010.02
     Tetradecanedioate0.84<0.0010.01
     10-undecenoate (11:1n1)0.86<0.010.03
     5-dodecenoate (12:1n7)0.91<0.010.04
     Myristate (14:0)0.940.010.09
     Myristoleate (14:1n5)1.210.010.09
     3-hydroxydecanoate0.930.010.09
     Pentadecanoate (15:0)0.940.020.10
     Octadecanedioate0.940.020.11
     Eicosenoate (20:1n9 or 11)1.060.040.17
     Palmitoleate (16:1n7)1.130.040.17
     Eicosapentaenoate (EPA; 20:5n3)0.970.050.18
    Lysolipids
     2-myristoylglycerophosphocholine2.300.010.06
     1-oleoylglycerophosphoethanolamine1.630.020.11
     1-heptadecanoylglycerophosphocholine3.630.020.12
     2-stearoylglycerophosphocholine2.800.030.14
     1-eicosadienoylglycerophosphocholine2.680.040.17
     2-palmitoylglycerophosphocholine3.780.050.18
    Other
     Homostachydrine1.50<0.010.04
     Trigonelline (N′-methylnicotinate)1.200.010.05
     N4-acetylcytidine0.890.010.06
     1-methylxanthine1.610.010.09
     Hypoxanthine0.910.010.10
     5-acetyl-2-pyridinecarboxylic acid0.920.020.10
     Ascorbate15.230.020.12
     D-Histidyl-D-tryptophyl-D-α-glutamyl-L-seryl-L-alanyl-L-serylleucylleucine (HWESASXX)0.940.020.12
     L-urobilin1.020.020.12
     Inositol 1-phosphate (I1P)1.440.040.17
  • Table 2.

    Metabolites whose change is significantly correlated to the change in tissue Cyclin D1 expression (47 metabolites P ≤ 0.05; 23 metabolites Q ≤ 0.10)

    PQR2
    Lysolipids
     1-Palmitoylglycerophosphocholine<0.0010.010.62
     1-Palmitoleoylglycerophosphocholine<0.0010.020.59
     1-Stearoylglycerophosphocholine<0.0010.010.61
     2-Stearoylglycerophosphocholine<0.0010.010.61
     1-Oleoylglycerophosphocholine<0.0010.010.62
     1-Eicosadienoylglycerophosphocholine<0.0010.010.63
     2-Oleoylglycerophosphocholine<0.010.050.55
     2-Linoleoylglycerophosphocholine0.010.090.51
     1-Eicosatrienoylglycerophosphocholine0.010.090.50
     1-Heptadecanoylglycerophosphocholine0.010.090.49
     1-Palmitoylplasmenylethanolamine0.020.140.42
    Acylcarnitines
     Palmitoylcarnitine<0.0010.010.63
     Oleoylcarnitine<0.0010.020.59
     Decanoylcarnitine0.010.100.47
     Butyrylcarnitine0.020.140.43
     Acetylcarnitine0.020.140.43
    Amino acids and metabolites
     Indolelactate0.010.090.49
     Kynurenine0.010.100.47
     α-hydroxyisocaproate0.010.100.47
     Phenylalanylserine0.010.100.47
     Serine0.010.110.46
     Phenol sulfate0.020.120.45
     3-indoxyl sulfate0.020.140.43
     Alanine0.020.140.43
     Asparagine0.030.160.41
     Aspartate0.040.170.39
     γ-glutamylvaline0.040.170.39
     Symmetric and asymmetric dimethylarginine (SDMA + ADMA)0.040.180.39
    Glucose/energy metabolism
     1,5-Anhydroglucitol (1,5-AG)0.010.090.50
    Fatty acids
     3-Carboxy-4-methyl-5-propyl-2-furanpropanoate (CMPF)0.010.030.57
     15-Methylpalmitate0.010.100.48
     cis-Vaccenate (18:1n7)0.020.120.45
     Palmitoyl sphingomyelin0.020.140.42
     Adrenate (22:4n6)0.030.160.41
     17-Methylstearate0.030.170.40
     Palmitate, methyl ester0.040.170.39
     Oleate (18:1n9)0.040.190.38
    Other
     Bilirubin (E,E)<0.0010.010.65
     N1-Methyladenosine<0.010.050.53
     Quinate0.010.090.49
     2-Ethylhexanoate0.020.140.43
     Pregnendiol disulfate0.020.150.42
     Erythritol0.030.160.41
     Bilirubin (Z,Z)0.030.170.40
     Urate0.040.170.39
     Cholesterol0.040.190.38
     α-Tocopherol0.040.190.38
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Cancer Prevention Research: 8 (1)
January 2015
Volume 8, Issue 1
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Plasma Metabolomic Profiles of Breast Cancer Patients after Short-term Limonene Intervention
Jessica A. Miller, Kirk Pappan, Patricia A. Thompson, Elizabeth J. Want, Alexandros P. Siskos, Hector C. Keun, Jacob Wulff, Chengcheng Hu, Julie E. Lang and H.-H. Sherry Chow
Cancer Prev Res January 1 2015 (8) (1) 86-93; DOI: 10.1158/1940-6207.CAPR-14-0100

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Plasma Metabolomic Profiles of Breast Cancer Patients after Short-term Limonene Intervention
Jessica A. Miller, Kirk Pappan, Patricia A. Thompson, Elizabeth J. Want, Alexandros P. Siskos, Hector C. Keun, Jacob Wulff, Chengcheng Hu, Julie E. Lang and H.-H. Sherry Chow
Cancer Prev Res January 1 2015 (8) (1) 86-93; DOI: 10.1158/1940-6207.CAPR-14-0100
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