Skip to main content

Advertisement

SpringerLink
Log in

1H NMR metabolomics study of metastatic melanoma in C57BL/6J mouse spleen

  • Original Article
  • Published:
Metabolomics Aims and scope Submit manuscript

Abstract

Melanoma is a malignant tumor of melanocytes. Although extensive investigations have been done to study metabolic changes in primary melanoma in vivo and in vitro, little effort has been devoted to metabolic profiling of metastatic tumors in organs other than lymph nodes. In this work, NMR-based metabolomics combined with multivariate data analysis is used to study metastatic B16-F10 melanoma in C57BL/6J mouse spleen. Principal component analysis, an unsupervised multivariate data analysis method, is used to detect possible outliers, while orthogonal projection to latent structure (OPLS), a supervised multivariate data analysis method, is employed to find important metabolites responsible for discriminating the control and the melanoma groups. Two different strategies, i.e. spectral binning and spectral deconvolution, are used to reduce the original spectral data before statistical analysis. Spectral deconvolution is found to be superior for identifying a set of discriminatory metabolites between the control and the melanoma groups, especially when the sample size is small. OPLS results show that the melanoma group can be well separated from its control group. It is found that taurine, glutamate, aspartate, O-phosphoethanolamine, niacinamide, ATP, lipids and glycerol derivatives are decreased statistically and significantly while alanine, malate, xanthine, histamine, dCTP, GTP, thymidine, 2′-deoxyguanosine are statistically and significantly elevated. These significantly changed metabolites are associated with multiple biological pathways and may be potential biomarkers for metastatic melanoma in spleen.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abaffy, T., Moller, M. G., Riemer, D. D., Milikowski, C., & DeFazio, R. A. (2013). Comparative analysis of volatile metabolomics signals from melanoma and benign skin: a pilot study. Metabolomics, 9(5), 998–1008. doi:10.1007/s11306-013-0523-z.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Akoh, C. C., & Min, D. B. (2008). Food Lipids: Chemistry, Nutrition, and Biotechnology (Food Science and Technology) (3rd ed.). Boca Raton: CRC Press.

    Book  Google Scholar 

  • Ali, K., Iqbal, M., Yuliana, N. D., Lee, Y. J., Park, S., Han, S., et al. (2013). Identification of bioactive metabolites against adenosine A1 receptor using NMR-based metabolomics. Metabolomics, 9(4), 778–785. doi:10.1007/s11306-013-0498-9.

    Article  CAS  Google Scholar 

  • Alizadeh, H., Howard, K., Mellon, J., Mayhew, E., Rusciano, D., & Niederkorn, J. Y. (2003). Reduction of liver metastasis of intraocular melanoma by interferon-beta gene transfer. Investigative Ophthalmology and Visual Science, 44(7), 3042–3051. doi:10.1167/Iovs.02-1147.

    Article  PubMed  Google Scholar 

  • An, Y. P., Xu, W. X., Li, H. H., Lei, H. H., Zhang, L. M., Hao, F. H., et al. (2013). High-fat diet induces dynamic metabolic alterations in multiple biological matrices of rats. Journal of Proteome Research, 12(8), 3755–3768. doi:10.1021/Pr400398b.

    Article  CAS  PubMed  Google Scholar 

  • Bailet, O., Fenouille, N., Abbe, P., Robert, G., Rocchi, S., Gonthier, N., et al. (2009). Spleen tyrosine kinase functions as a tumor suppressor in melanoma cells by inducing senescence-like growth arrest. Cancer Research, 69(7), 2748–2756.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beckonert, O., Keun, H. C., Ebbels, T. M. D., Bundy, J. G., Holmes, E., Lindon, J. C., et al. (2007). Metabolic profiling, metabolomic and metabonomic procedures for NMR spectroscopy of urine, plasma, serum and tissue extracts. Nature Protocols, 2(11), 2692–2703.

    Article  CAS  PubMed  Google Scholar 

  • Bernardo, S. G., Moskalenko, M., Pan, M., Shah, S., Sidhu, H. K., Sicular, S., et al. (2013). Elevated rates of transaminitis during ipilimumab therapy for metastatic melanoma. Melanoma Research, 23(1), 47–54. doi:10.1097/Cmr.0b013e32835c7e68.

    Article  CAS  PubMed  Google Scholar 

  • Bourne, R. M., Stanwell, P., Stretch, J. R., Scolyer, R. A., Thompson, J. F., Mountford, C. E., et al. (2005). In vivo and ex vivo proton MR spectroscopy of primary and secondary melanoma. European Journal of Radiology, 53(3), 506–513.

    Article  PubMed  Google Scholar 

  • Chiu, K. P., Ariyaratne, P., Xu, H., Tan, A., Ng, P., Liu, E. T. B., et al. (2007). Pathway aberrations of murine melanoma cells observed in paired-end diTag transcriptomes. BMC Cancer,. doi:10.1186/1471-2407-7-109.

    PubMed  PubMed Central  Google Scholar 

  • Choi, K. Y., Chang, K., Pickel, J. M., Badger, J. D., & Roche, K. W. (2011). Expression of the metabotropic glutamate receptor 5 (mGluR5) induces melanoma in transgenic mice. Proceedings of the National Academy of Sciences of the USA, 108(37), 15219–15224. doi:10.1073/pnas.1107304108.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cloarec, O., Dumas, M. E., Trygg, J., Craig, A., Barton, R. H., Lindon, J. C., et al. (2005). Evaluation of the orthogonal projection on latent structure model limitations caused by chemical shift variability and improved visualization of biomarker changes in H-1 NMR spectroscopic metabonomic studies. Analytical Chemistry, 77(2), 517–526.

    Article  CAS  PubMed  Google Scholar 

  • Constantinou, M. A., Papakonstantinou, E., Spraul, M., Sevastiadou, S., Costalos, C., Koupparis, M. A., et al. (2005). H-1 NMR-based metabonomics for the diagnosis of inborn errors of metabolism in urine. Analytica Chimica Acta, 542(2), 169–177. doi:10.1016/j.aca.2005.03.059.

    Article  CAS  Google Scholar 

  • Craig, A., Cloareo, O., Holmes, E., Nicholson, J. K., & Lindon, J. C. (2006). Scaling and normalization effects in NMR spectroscopic metabonomic data sets. Analytical Chemistry, 78(7), 2262–2267.

    Article  CAS  PubMed  Google Scholar 

  • Cybulska-Stopa, B., Skoczek, M., Ziobro, M., Switaj, T., Falkowski, S., Morysinski, T., et al. (2012). Results of systemic treatment of cutaneous melanoma in inoperable stage III and IV. Wspolczesna Onkologia (Contemporary Oncology), 16(6), 532–545. doi:10.5114/wo.2012.32487.

    Article  Google Scholar 

  • Davis, S. C., Clark, S., Hayes, J. R., Green, T. L., & Gruetter, C. A. (2011). Up-regulation of histidine decarboxylase expression and histamine content in B16F10 murine melanoma cells. Inflammation Research, 60(1), 55–61. doi:10.1007/s00011-010-0234-0.

    Article  CAS  PubMed  Google Scholar 

  • Dong, F. C., Zhang, L. L., Hao, F. H., Tang, H. R., & Wang, Y. L. (2013). Systemic responses of mice to dextran sulfate sodium-induced acute ulcerative colitis using H-1 NMR spectroscopy. Journal of Proteome Research, 12(6), 2958–2966. doi:10.1021/Pr4002383.

    Article  CAS  PubMed  Google Scholar 

  • Enot, D. P., & Draper, J. (2007). Statistical measures for validating plant genotype similarity assessments following multivariate analysis of metabolome fingerprint data. Metabolomics, 3(3), 349–355. doi:10.1007/s11306-007-0066-2.

    Article  CAS  Google Scholar 

  • Eriksson, L., Trygg, J., & Wold, S. (2008). CV-ANOVA for significance testing of PLS and OPLS (R) models. Journal of Chemometrics, 22(11–12), 594–600. doi:10.1002/Cem.1187.

    Article  CAS  Google Scholar 

  • Fages, A., Morvan, D., Schwartz, L., Steyaert, J. M., Stepien, G., & Demidem, A. (2010). Disturbance of metabolic pathways of glucose consumption by CENU treatment in B16 melanoma tumors: a NMR spectroscopy-based [1,2-13C]glucose fluxomics. Bulletin du Cancer, 97, S39–S40.

    Google Scholar 

  • Feng, J. I., Isern, N. G., Burton, S. D., & Hu, J. Z. (2013). Studies of secondary melanoma on C57BL/6J mouse liver using 1H NMR metabolomics. Metabolites, 3(4), 1011–1035.

    Article  PubMed  PubMed Central  Google Scholar 

  • Filipp, F. V., Ratnikov, B., De Ingeniis, J., Smith, J. W., Osterman, A. L., & Scott, D. A. (2012). Glutamine-fueled mitochondrial metabolism is decoupled from glycolysis in melanoma. Pigment Cell and Melanoma Research, 25(6), 732–739. doi:10.1111/Pcmr.12000.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frolkis, A., Knox, C., Lim, E., Jewison, T., Law, V., Hau, D. D., et al. (2010). SMPDB: The small molecule pathway database. Nucleic Acids Research, 38, D480–D487. doi:10.1093/Nar/Gkp1002.

    Article  CAS  PubMed  Google Scholar 

  • Gheorgheosu, D., Dehelean, C., Cristea, M., & Muntean, D. (2011). Development of the B16 murine melanoma model. Annals of RSCB, 2, 148–152.

    Google Scholar 

  • Gruetter, C. A., Davis, S. C., Clark, S. L., McKee, K. R., & Green, T. L. (2008). Comparative expression of histidine decarboxylase (HDC) protein in B16F10 melanoma cells and nontumorigenic melan-A melanocytes. FASEB Journal, 22, 898.

    Google Scholar 

  • Gruetter, C. A., Davis, S. C., Hayes, J. R., Clark, S. L., & Green, T. L. (2009). Comparison of histamine content in B16F10 melanoma cells and non-tumorigenic melan-A melanocytes. FASEB Journal, 16(1), 105.

    Google Scholar 

  • Guitera, P., Bourgeat, P., Stretch, J. R., Scolyer, R. A., Ourselin, S., Lean, C., et al. (2010). Diagnostic value of 8.5 T magnetic resonance spectroscopy of benign and malignant skin lesion biopsies. Melanoma Research, 20(4), 311–317.

    Article  PubMed  Google Scholar 

  • Hatse, S., De Clercq, E., & Balzarini, J. (1999). Role of antimetabolites of purine and pyrimidine nucleotide metabolism in tumor cell differentiation. Biochemical Pharmacology, 58(4), 539–555. doi:10.1016/S0006-2952(99)00035-0.

    Article  CAS  PubMed  Google Scholar 

  • Huang, R. Z., Gao, H. C., Ma, L. H., Wang, X., Jia, J. M., Wang, M. J., et al. (2014). Dynamic H-1 NMR-based extracellular metabonomic analysis of oligodendroglia cells infected with herpes simplex virus type 1. Metabolomics, 10(1), 33–41. doi:10.1007/s11306-013-0548-3.

    Article  CAS  Google Scholar 

  • Itzhaki, O., Greenberg, E., Shalmon, B., Kubi, A., Treves, A. J., Shapira-Frommer, R., et al. (2013). Nicotinamide inhibits vasculogenic mimicry, an alternative vascularization pathway observed in highly aggressive melanoma. PLoS ONE,. doi:10.1371/journal.pone.0057160.

    PubMed  PubMed Central  Google Scholar 

  • Iverson, S. J., Lang, S. L. C., & Cooper, M. H. (2001). Comparison of the Bligh and Dyer and Folch methods for total lipid determination in a broad range of marine tissue. Lipids, 36(11), 1283–1287.

    Article  CAS  PubMed  Google Scholar 

  • Jacobson, E. L., & Jacobson, M. K. (1993). A biomarker for the assessment of niacin nutriture as a potential preventive factor in carcinogenesis. Journal of Internal Medicine, 233(1), 59–62.

    Article  CAS  PubMed  Google Scholar 

  • Jiang, L. M., Huang, J., Wang, Y. L., & Tang, H. R. (2012). Metabonomic analysis reveals the CCl4-induced systems alterations for multiple rat organs. Journal of Proteome Research, 11(7), 3848–3859.

    Article  CAS  PubMed  Google Scholar 

  • Keun, H. C., Ebbels, T. M. D., Antti, H., Bollard, M. E., Beckonert, O., Schlotterbeck, G., et al. (2002). Analytical reproducibility in H-1 NMR-based metabonomic urinalysis. Chemical Research in Toxicology, 15(11), 1380–1386. doi:10.1021/Tx0255774.

    Article  CAS  PubMed  Google Scholar 

  • Kizaki, H., Williams, J. C., Morris, H. P., & Weber, G. (1980). Increased cytidine 5′-triphosphate synthetase activity in rat and human tumors. Cancer Research, 40(11), 3921–3927.

    CAS  PubMed  Google Scholar 

  • Kristensen, M., Savorani, F., Ravn-Haren, G., Poulsen, M., Markowski, J., Larsen, F. H., et al. (2010). NMR and interval PLS as reliable methods for determination of cholesterol in rodent lipoprotein fractions. Metabolomics, 6(1), 129–136. doi:10.1007/s11306-009-0181-3.

    Article  CAS  Google Scholar 

  • Lee, H. J., Wall, B. A., Wangari-Talbot, J., Shin, S. S., Rosenberg, S., Chan, J. L. K., et al. (2011). Glutamatergic pathway targeting in melanoma: Single-agent and combinatorial therapies. Clinical Cancer Research, 17(22), 7080–7092.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, W., Slominski, R., & Slominski, A. T. (2009). High-resolution magic angle spinning nuclear magnetic resonance analysis of metabolic changes in melanoma cells after induction of melanogenesis. Analytical Biochemistry, 386(2), 282–284.

    Article  CAS  PubMed  Google Scholar 

  • Lindon, J. C., Nicholson, J. K., & Everett, J. R. (1999). NMR spectroscopy of biofluids. Annual Reports on NMR Spectroscopy, 38(38), 1–88.

    Article  CAS  Google Scholar 

  • Lu, Y. H., Wang, C. M., Chen, Z. X., Zhao, H., Chen, J. Y., Liu, X. B., et al. (2012). Serum metabolomics for the diagnosis and classification of myasthenia gravis. Metabolomics, 8(4), 704–713. doi:10.1007/s11306-011-0364-6.

    Article  CAS  Google Scholar 

  • Maiese, K., Chong, Z. Z., Hou, J. L., & Shang, Y. C. (2009). The vitamin nicotinamide: Translating nutrition into clinical care. Molecules, 14(9), 3446–3485. doi:10.3390/molecules14093446.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maire, C., Vercambre-Darras, S., Devos, P., D’Herbomez, M., Dubucquoi, S., & Mortier, L. (2013). Metastatic melanoma: spontaneous occurrence of auto antibodies is a good prognosis factor in a prospective cohort. Journal of the European Academy of Dermatology and Venereology, 27(1), 92–96.

    Article  CAS  PubMed  Google Scholar 

  • Maniotis, A. J., Folberg, R., Hess, A., Seftor, E. A., Gardner, L. M. G., Pe’er, J., et al. (1999). Vascular channel formation by human melanoma cells in vivo and in vitro: Vasculogenic mimicry. American Journal of Pathology, 155(3), 739–752. doi:10.1016/S0002-9440(10)65173-5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin, F. P. J., Dumas, M. E., Wang, Y. L., Legido-Quigley, C., Yap, I. K. S., Tang, H. R., et al. (2007a). A top-down systems biology view of microbiome-mammalian metabolic interactions in a mouse model. Molecular Systems Biology, 3, 112.

    Article  PubMed  PubMed Central  Google Scholar 

  • Martin, F. P. J., Wang, Y. L., Sprenger, N., Holmes, E., Lindon, J. C., Kochhar, S., et al. (2007b). Effects of probiotic Lactobacillus paracasei treatment on the host gut tissue metabolic profiles probed via magic–angle–spinning NMR spectroscopy. Journal of Proteome Research, 6(4), 1471–1481.

    Article  CAS  PubMed  Google Scholar 

  • Massari, N. A., Medina, V. A., Cricco, G. P., Lamas, D. J. M., Sambuco, L., Pagotto, R., et al. (2013). Antitumor activity of histamine and clozapine in a mouse experimental model of human melanoma. Journal of Dermatological Science, 72(3), 252–262. doi:10.1016/j.jdermsci.2013.07.012.

    Article  CAS  PubMed  Google Scholar 

  • Mizuarai, S., Miki, S., Araki, H., Takahashi, K., & Kotani, H. (2005). Identification of dicarboxylate carrier Slc25a10 as malate transporter in de novo fatty acid synthesis. Journal of Biological Chemistry, 280(37), 32434–32441. doi:10.1074/jbc.M503152200.

    Article  CAS  PubMed  Google Scholar 

  • Morvan, D., Demidem, A., Guenin, S., & Madelmont, J. C. (2006). Methionine-dependence phenotype of tumors: Metabolite profiling in a melanoma model using l-[methyl-C-13]methionine and high-resolution magic angle spinning H-1-C-13 nuclear magnetic resonance spectroscopy. Magnetic Resonance in Medicine, 55(5), 984–996.

    Article  CAS  PubMed  Google Scholar 

  • Morvan, D., Demidem, A., Papon, J., De Latour, M., & Madelmont, J. C. (2002). Melanoma tumors acquire a new phospholipid metabolism phenotype under cystemustine as revealed by high-resolution magic angle spinning proton nuclear magnetic resonance spectroscopy of intact tumor sampled. Cancer Research, 62(6), 1890–1897.

    CAS  PubMed  Google Scholar 

  • Morvan, D., Demidem, A., Papon, J., & Madelmont, J. C. (2003). Quantitative HRMAS proton total correlation spectroscopy applied to cultured melanoma cells treated by chloroethyl nitrosourea: Demonstration of phospholipid metabolism alterations. Magnetic Resonance in Medicine, 49(2), 241–248.

    Article  CAS  PubMed  Google Scholar 

  • Mounet, F., Lemaire-Chamley, M., Maucourt, M., Cabasson, C., Giraudel, J. L., Deborde, C., et al. (2007). Quantitative metabolic profiles of tomato flesh and seeds during fruit development: Complementary analysis with ANN and PCA. Metabolomics, 3(3), 273–288. doi:10.1007/s11306-007-0059-1.

    Article  CAS  Google Scholar 

  • Namkoong, J., Shin, S. S., Lee, H. J., Marin, Y. E., Wall, B. A., Goydos, J. S., et al. (2007). Metabotropic glutamate receptor 1 and glutamate signaling in human melanoma. Cancer Research, 67(5), 2298–2305.

    Article  CAS  PubMed  Google Scholar 

  • Nicholson, J. K., Foxall, P. J. D., Spraul, M., Farrant, R. D., & Lindon, J. C. (1995). 750-Mhz H-1 and H-1-C-13 NMR-spectroscopy of human blood-plasma. Analytical Chemistry, 67(5), 793–811.

    Article  CAS  PubMed  Google Scholar 

  • Orlov, N. V., Weeraratna, A. T., Hewitt, S. M., Coletta, C. E., Delaney, J. D., Eckley, D., et al. (2012). Automatic detection of melanoma progression by histological analysis of secondary sites. Cytometry Part A, 81A(5), 364–373.

    Article  CAS  Google Scholar 

  • Patwardhan, G. A., & Liu, Y. Y. (2011). Sphingolipids and expression regulation of genes in cancer. Progress in Lipid Research, 50(1), 104–114. doi:10.1016/j.plipres.2010.10.003.

    Article  CAS  PubMed  Google Scholar 

  • Pontarin, G., Ferraro, P., Hakansson, P., Thelander, L., Reichard, P., & Bianchi, V. (2007). p53R2-dependent ribonucleotide reduction provides deoxyribonucleotides in quiescent human fibroblasts in the absence of induced DNA damage. Journal of Biological Chemistry, 282(23), 16820–16828. doi:10.1074/jbc.M701310200.

    Article  CAS  PubMed  Google Scholar 

  • Pos, Z., Safrany, G., Muller, K., Toth, R., Falus, A., & Hegyesi, H. (2005). Phenotypic profiling of engineered mouse melanomas with manipulated histamine production identifies histamine H2 receptor and Rho-C as histamine-regulated melanoma progression markers. Cancer Research, 65(10), 4458–4466. doi:10.1158/0008-5472.Can-05-0011.

    Article  CAS  PubMed  Google Scholar 

  • Qiu, Y., Rajagopalan, D., Connor, S. C., Damian, D., Zhu, L., Handzel, A., et al. (2008). Multivariate classification analysis of metabolomic data for candidate biomarker discovery in type 2 diabetes mellitus. Metabolomics, 4(4), 337–346. doi:10.1007/s11306-008-0123-5.

    Article  CAS  Google Scholar 

  • Rocha, C. M., Carrola, J., Barros, A. S., Gil, A. M., Goodfellow, B. J., Carreira, I. M., et al. (2011). Metabolic signatures of lung cancer in biofluids: NMR-based metabonomics of blood plasma. Journal of Proteome Research, 10(9), 4314–4324. doi:10.1021/Pr200550p.

    Article  CAS  PubMed  Google Scholar 

  • Roomi, M. W., Kalinovsky, T., Roomi, N. W., Ivanov, V., Rath, M., & Niedzwiecki, A. (2008). Suppression of growth and hepatic metastasis of murine B16FO melanoma cells by a novel nutrient mixture. Oncology Reports, 20(4), 809–817. doi:10.3892/or_00000078.

    CAS  PubMed  Google Scholar 

  • Rzeski, W., Turski, L., & Ikonomidou, C. (2001). Glutamate antagonists limit tumor growth. Proceedings of the National Academy of Sciences of the USA, 98(11), 6372–6377.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sato, A., Yoshikawa, N., Kubo, E., Kakuda, M., Nishiuchi, A., Kimoto, Y., et al. (2013). Inhibitory Effect of Cordycepin on Experimental Hepatic Metastasis of B16-F0 Mouse Melanoma Cells. Vivo, 27(6), 729–732.

    CAS  Google Scholar 

  • Sikora-Borgula, A., Slominska, M., Trzonkowski, P., Zielke, R., Mysliwski, A., Wegrzyn, G., et al. (2002). A role for the common GTP-binding protein in coupling of chromosome replication to cell growth and cell division. Biochemical and Biophysical Research Communications, 292(2), 333–338. doi:10.1006/bbrc.2002.6671.

    Article  CAS  PubMed  Google Scholar 

  • Song, Z. Q., He, C. D., Liu, J., Sun, C. K., Lu, P., Li, L. L., et al. (2012). Blocking glutamate-mediated signalling inhibits human melanoma growth and migration. Experimental Dermatology, 21(12), 926–931. doi:10.1111/Exd.12048.

    Article  CAS  PubMed  Google Scholar 

  • Stepulak, A., Sifringer, M., Rzeski, W., Endesfelder, S., Gratopp, A., Pohl, E. E., et al. (2005). NMDA antagonist inhibits the extracellular signal-regulated kinase pathway and suppresses cancer growth. Proceedings of the National Academy of Sciences of the USA, 102(43), 15605–15610.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stretch, J. R., Somorjai, R., Bourne, R., Hsiao, E., Scolyer, R. A., Dolenko, B., et al. (2005). Melanoma metastases in regional lymph nodes are accurately detected by proton magnetic resonance spectroscopy of fine-needle aspirate biopsy samples. Annals of Surgical Oncology, 12(11), 943–949.

    Article  PubMed  Google Scholar 

  • Szymanska, E., Saccenti, E., Smilde, A. K., & Westerhuis, J. A. (2012). Double-check: validation of diagnostic statistics for PLS-DA models in metabolomics studies. Metabolomics, 8(1), S3–S16. doi:10.1007/s11306-011-0330-3.

    Article  Google Scholar 

  • Triba, M. N., Starzec, A., Bouchemal, N., Guenin, E., Perret, G. Y., & Le Moyec, L. (2010). Metabolomic profiling with NMR discriminates between biphosphonate and doxorubicin effects on B16 melanoma cells. NMR in Biomedicine, 23(9), 1009–1016.

    Article  CAS  PubMed  Google Scholar 

  • Trygg, J., & Wold, S. (2002). Orthogonal projections to latent structures (O-PLS). Journal of Chemometrics, 16(3), 119–128. doi:10.1002/Cem.695.

    Article  CAS  Google Scholar 

  • Washburn, K. W. (1989). A modification of the Folch method of lipid extraction for poultry. Poultry Science, 68(11), 1425–1427.

    Article  Google Scholar 

  • Weljie, A. M., Dowlatabadi, R., Miller, B. J., Vogel, H. J., & Jirik, F. R. (2007). An inflammatory arthritis-associated metabolite biomarker pattern revealed by H-1 NMR Spectroscopy. Journal of Proteome Research, 6(9), 3456–3464. doi:10.1021/Pr070123j.

    Article  CAS  PubMed  Google Scholar 

  • Wiklund, S., Johansson, E., Sjostrom, L., Mellerowicz, E. J., Edlund, U., Shockcor, J. P., et al. (2008). Visualization of GC/TOF-MS-based metabolomics data for identification of biochemically interesting compounds using OPLS class models. Analytical Chemistry, 80(1), 115–122. doi:10.1021/Ac0713510.

    Article  CAS  PubMed  Google Scholar 

  • Wu, B. J., Li, W. P., Qian, C., Ding, W., Zhou, Z. W., & Jiang, H. (2013). Increased serum level of thymidine kinase 1 correlates with metastatic site in patients with malignant melanoma. Tumor Biology, 34(2), 643–648. doi:10.1007/s13277-012-0591-0.

    Article  CAS  PubMed  Google Scholar 

  • Xia, J. M., Wu, X. J., & Yuan, Y. J. (2007). Integration of wavelet transform with PCA and ANN for metabolomics data-mining. Metabolomics, 3(4), 531–537. doi:10.1007/s11306-007-0090-2.

    Article  CAS  Google Scholar 

  • Yu, J., & Kim, A. K. (2009). Effect of taurine on antioxidant enzyme system in B16F10 melanoma cells. Taurine, 7(643), 491–499. doi:10.1007/978-0-387-75681-3_51.

    Google Scholar 

Download references

Acknowledgments

Research reported in this publication was supported by the National Institute of Environmental Health Sciences of the National Institute of Health (NIH) under Award Numbers R01ES022176, and NIH/R01EB013231. All of the NMR experiments were performed in the Environmental Molecular Sciences Laboratory, a national scientific user facility sponsored by the DOE’s Office of Biological and Environmental Research, and located at PNNL. PNNL is a multi-program national laboratory operated for the DOE by Battelle Memorial Institute under Contract DE-AC06-76RLO 1830. And finally we thank Dr. Xihai Wang for his contributions in pathology and animal work.

Conflict of interest

The authors declare no conflict of interest.

Author information

Authors and Affiliations

  1. Pacific Northwest National Laboratory, Richland, WA, 99352, USA

    Xuan Wang, Mary Hu, Ju Feng & Jian Zhi Hu

  2. Wuhan Institute of Physics and Mathematics, The Chinese Academy of Sciences, Wuhan, 430071, People’s Republic of China

    Xuan Wang & Maili Liu

Authors
  1. Xuan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mary Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ju Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Maili Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jian Zhi Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jian Zhi Hu.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 936 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, X., Hu, M., Feng, J. et al. 1H NMR metabolomics study of metastatic melanoma in C57BL/6J mouse spleen. Metabolomics 10, 1129–1144 (2014). https://doi.org/10.1007/s11306-014-0652-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11306-014-0652-z

Keywords

Search

Navigation