Metabolomics of human cerebrospinal fluid identifies signatures of malignant glioma

Molecular and Cellular Proteomics

Volumn 11, Issue 6, 2012, Pages

  Locasale, Jason W ^a,b   Melman, Tamar ^a   Song, Susan ^a   Yang, Xuemei ^a   Swanson, Kenneth D ^a   Cantley, Lewis C ^a,b   Wong, Eric T ^a   Asara, John M ^b  

^a BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRYPTOPHAN; TUMOR MARKER;

ADULT; AGED; ARTICLE; CEREBROSPINAL FLUID ANALYSIS; CITRIC ACID CYCLE; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; GLIOBLASTOMA; HUMAN; INFLAMMATION; MALE; MASS SPECTROMETRY; METABOLITE; METABOLOMICS; PRIORITY JOURNAL; SAMPLE SIZE; STATISTICAL ANALYSIS; TRYPTOPHAN METABOLISM; BRAIN TUMOR; CASE CONTROL STUDY; CEREBROSPINAL FLUID; CLUSTER ANALYSIS; METABOLOME; MIDDLE AGED; MONTE CARLO METHOD; PATHOLOGY; PRINCIPAL COMPONENT ANALYSIS; SENSITIVITY AND SPECIFICITY; TANDEM MASS SPECTROMETRY; TUMOR VOLUME;

ADULT; AGED; BRAIN NEOPLASMS; CASE-CONTROL STUDIES; CLUSTER ANALYSIS; FEMALE; GLIOBLASTOMA; HUMANS; MALE; METABOLOME; METABOLOMICS; MIDDLE AGED; MONTE CARLO METHOD; PRINCIPAL COMPONENT ANALYSIS; SENSITIVITY AND SPECIFICITY; TANDEM MASS SPECTROMETRY; TUMOR BURDEN; TUMOR MARKERS, BIOLOGICAL;

EID: 84862329697     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M111.014688     Document Type: Article

References (52)

1. Stupp, R., Hegi, M. E., Mason, W. P., van den Bent, M. J., Taphoorn, M. J. B., Janzer, R. C., Ludwin, S. K., Allgeier, A., Fisher, B., Belanger, K., Hau, P., Brandes, A. A., Gijtenbeek, J., Marosi, C., Vecht, C. J., Mokhtari, K., Wesseling, P., Villa, S., Eisenhauer, E., Gorlia, T., Weller, M., Lacombe, D., Cairncross, J. G., Mirimanoff, R. O., European Org, R., Treatment; Canc Brain Tumour Grp; Radiat Oncol, G., and Natl Canc Inst Canada Clin, T. (2009) Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol. 10, 459-466
2. Cairncross, G., Berkey, B., Shaw, E., Jenkins, R., Scheithauer, B., Brachman, D., Buckner, J., Fink, K., Souhami, L., Laperierre, N., Mehta, M., and Curran, W. (2006) Phase III trial of chemotherapy plus radiotherapy compared with radiotherapy alone for pure and mixed anaplastic oligodendroglioma: Intergroup Radiation Therapy Oncology Group Trial 9402. J. Clin. Oncol. 24, 2707-2714 (Pubitemid 46630566)
3. Louis, D. N., Holland, E. C., and Cairncross, J. G. (2001) Glioma classification - A molecular reappraisal. Am. J. Pathol. 159, 779-786
4. Chandrasoma, P. T., Smith, M. M., and Apuzzo, M. L. J. (1989) Stereotactic biopsy in the diagnosis of brain masses - Comparison of results of biopsy and resected surgical specimen. Neurosurgery 24, 160-165 (Pubitemid 19044578)
5. Glantz, M. J., Burger, P. C., Herndon, J. E., 2nd, Friedman, A. H., Cairncross, J. G., Vick, N. A., and Schold, S. C., Jr. (1991) Influence of the type of surgery on the histologic diagnosis in patients with anaplastic gliomas. Neurology 41, 1741-1744
6. Swanson, K., Lok, E., Song, S., Dessain, J., and Wong, E. T. (2009) Cerebrospinal fluid (CSF) Biomarkers for breast cancer (BC) brain metastases. Ann. Neurol. 66, S58
7. Lehtinen, M. K., Zappaterra, M. W., Chen, X., Yang, Y. J., Hill, A. D., Lun, M. L., Maynard, T., Gonzalez, D., Kim, S., Ye, P., D'Ercole, A. J., Wong, E. T., LaMantia, A. S., and Walsh, C. A. (2010) The cerebrospinal fluid provides a proliferative niche for neural progenitor cells. Neuron 69, 893-905
8. Locasale, J. W., Cantley, L. C., and Vander Heiden, M. G. (2009) Cancer's insatiable appetite. Nat. Biotechnol. 27, 916-917
9. Luo, J., Solimini, N. L., and Elledge, S. J. (2009) Principles of Cancer Therapy: Oncogene and Non-oncogene Addiction. Cell 136, 823-837
10. Vander Heiden, M. G., Cantley, L. C., and Thompson, C. B. (2009) Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324, 1029-1033
11. Michelakis ED, S. G., Dromparis P, Webster L, Haromy A, Niven E, Maguire C, Gammer TL, Mackey JR, Fulton D, Abdulkarim B, McMurtry MS, Petruk KC. (2010) Metabolic modulation of glioblastoma with dichloroacetate. Sci. Translation Med. 2, 31-34
12. Tlsty, T. D., and Coussens, L. M. (2006) Tumor stroma and regulation of cancer development. Annu. Rev. Pathol.-Mech. Dis. 1, 119-150
13. Sreekumar, A., Poisson, L. M., Rajendiran, T. M., Khan, A. P., Cao, Q., Yu, J., Laxman, B., Mehra, R., Lonigro, R. J., Li, Y., Nyati, M. K., Ahsan, A., Kalyana-Sundaram, S., Han, B., Cao, X. H., Byun, J., Omenn, G. S., Ghosh, D., Pennathur, S., Alexander, D. C., Berger, A., Shuster, J. R., Wei, J. T., Varambally, S., Beecher, C., and Chinnaiyan, A. M. (2009) Metabolomic profiles delineate potential role for sarcosine in prostate cancer progression. Nature 457, 910-914
14. Lin, L., Huang, Z. Z., Gao, Y., Yan, X. M., Xing, J. C., and Hang, W. (2011) LC-MS based serum metabonomic analysis for renal cell carcinoma diagnosis, staging, and biomarker discovery. J. Proteome Res. 10, 1396-1405
15. Parsons, D. W., Jones, S., Zhang, X., Lin, J. C., Leary, R. J., Angenendt, P., Mankoo, P., Carter, H., Siu, I. M., Gallia, G. L., Olivi, A., McLendon, R., Rasheed, B. A., Keir, S., Nikolskaya, T., Nikolsky, Y., Busam, D. A., Tekleab, H., Diaz, L. A., Hartigan, J., Smith, D. R., Strausberg, R. L., Marie, S. K. N., Shinjo, S. M., Yan, H., Riggins, G. J., Bigner, D. D., Karchin, R., Papadopoulos, N., Parmigiani, G., Vogelstein, B., Velculescu, V. E., and Kinzler, K. W. (2008) An integrated genomic analysis of human glioblastoma Multiforme. Science 321, 1807-1812
16. Deberardinis, R. J., Lum, J. J., Hatzivassiliou, G., and Thompson, C. B. (2008) The biology of cancer: metabolic reprogramming fuels cell growth and proliferation. Cell Metab 7, 11-20
17. Dang, L., White, D. W., Gross, S., Bennett, B. D., Bittinger, M. A., Driggers, E. M., Fantin, V. R., Jang, H. G., Jin, S., Keenan, M. C., Marks, K. M., Prins, R. M., Ward, P. S., Yen, K. E., Liau, L. M., Rabinowitz, J. D., Cantley, L. C., Thompson, C. B., Heiden, M. G. V., and Su, S. M. (2009) Cancer-associated IDH1 mutations produce 2-hydroxyglutarate. Nature 462, 739-744
18. Wuolikainen, A., Moritz, T., Marklund, S. L., Antti, H., and Andersen, P. M. Disease-related changes in the cerebrospinal fluid metabolome in amyotrophic lateral sclerosis detected by GC/TOFMS. PLoS One 6, e17947
19. Rosenling, T., Slim, C. L., Christin, C., Coulier, L., Shi, S., Stoop, M. P., Bosman, J., Suits, F., Horvatovich, P. L., Stockhofe-Zurwieden, N., Vreeken, R., Hankemeier, T., van Gool, A. J., Luider, T. M., and Bischoff, R. (2009) The effect of preanalytical factors on stability of the proteome and selected metabolites in cerebrospinal fluid (CSF). J. Proteome Res. 8, 5511-5522
20. Wishart, D. S., Lewis, M. J., Morrissey, J. A., Flegel, M. D., Jeroncic, K., Xiong, Y. P., Cheng, D., Eisner, R., Gautam, B., Tzur, D., Sawhney, S., Bamforth, F., Greiner, R., and Li, L. (2008) The human cerebrospinal fluid metabolome. J. Chromatogr. B 871, 164-173
21. Crews, B., Wikoff, W. R., Patti, G. J., Woo, H. K., Kalisiak, E., Heideker, J., and Siuzdak, G. (2009) Variability analysis of human plasma and cerebral spinal fluid reveals statistical significance of changes in mass spectrometry-based metabolomics data. Anal. Chem. 81, 8538-8544
22. Stoop, M. P., Coulier, L., Rosenling, T., Shi, S., Smolinska, A. M., Buydens, L., Ampt, K., Stingl, C., Dane, A., Muilwijk, B., Luitwieler, R. L., Sillevis Smitt, P. A., Hintzen, R. Q., Bischoff, R., Wijmenga, S. S., Hankemeier, T., van Gool, A. J., and Luider, T. M. (2010) Quantitative proteomics and metabolomics analysis of normal human cerebrospinal fluid samples. Mol. Cell. Proteomics 9, 2063-2075
23. Rosenling, T., Stoop, M. P., Smolinska, A., Muilwijk, B., Coulier, L., Shi, S., Dane, A., Christin, C., Suits, F., Horvatovich, P. L., Wijmenga, S. S., Buydens, L. M., Vreeken, R., Hankemeier, T., van Gool, A. J., Luider, T. M., and Bischoff, R. The impact of delayed storage on the measured proteome and metabolome of human cerebrospinal fluid. Clin. Chem. 57, 1703-1711
24. Holmes, E., Tsang, T. M., Huang, J. T. J., Leweke, F. M., Koethe, D., Gerth, C. W., Nolden, B. M., Gross, S., Schreiber, D., Nicholson, J. K., and Bahn, S. (2006) Metabolic profiling of CSF: Evidence that early intervention may impact on disease progression and outcome in schizophrenia. PLos Med. 3, 1420
25. Wikoff, W. R., Pendyala, G., Siuzdak, G., and Fox, H. S. (2008) Metabolomic analysis of the cerebrospinal fluid reveals changes in phospholipase expression in the CNS of SIV-infected macaques. J. Clin. Invest. 2661-2669 Page.
26. Yuan, M., Breitkopf, S. B., Yang, X., and Asara, J. M. (2012) A Positive/Negative Switching Targeted Mass Spectrometry Based Metabolomics Platform for Bodily Fluids, Cells, Fresh and Fixed Tissue. Nature Protocols In press
27. Kelly, A. D., Breitkopf, S. B., Yuan, M., Goldsmith, J., Spentzos, D., and Asara, J. M. Metabolomic Profiling from Formalin-Fixed, Paraffin-Embedded Tumor Tissue Using Targeted LC/MS/MS: Application in Sarcoma. PLoS One 6, e25357
28. Locasale, J. W., Grassian, A. R., Melman, T., Lyssiotis, C. A., Mattaini, K. R., Bass, A. J., Heffron, G., Metallo, C. M., Muranen, T., Sharfi, H., Sasaki, A. T., Anastasiou, D., Mullarky, E., Vokes, N. I., Sasaki, M., Beroukhim, R., Stephanopoulos, G., Ligon, A. H., Meyerson, M., Richardson, A. L., Chin, L., Wagner, G., Asara, J. M., Brugge, J. S., Cantley, L. C., and Vander Heiden, M. G. Phosphoglycerate dehydrogenase diverts glycolytic flux and contributes to oncogenesis. Nat. Genet. 43, 869-874
29. Anastasiou, D., Poulogiannis, G., Asara, J. M., Boxer, M. B., Jiang, J. K., Shen, M., Bellinger, G., Sasaki, A. T., Locasale, J. W., Auld, D. S., Thomas, C. J., Vander Heiden, M. G., and Cantley, L. C. Inhibition of pyruvate kinase M2 by reactive oxygen species contributes to cellular antioxidant responses. Science 334, 1278-1283
30. Yi, C. H., Pan, H., Seebacher, J., Jang, I. H., Hyberts, S. G., Heffron, G. J., Vander Heiden, M. G., Yang, R., Li, F., Locasale, J. W., Sharfi, H., Zhai, B., Rodriguez-Mias, R., Luithardt, H., Cantley, L. C., Daley, G. Q., Asara, J. M., Gygi, S. P., Wagner, G., Liu, C. F., and Yuan, J. Metabolic regulation of protein N-alpha-acetylation by Bcl-xL promotes cell survival. Cell 146, 607-620
31. Bajad, S. U., Lu, W. Y., Kimball, E. H., Yuan, J., Peterson, C., and Rabinowitz, J. D. (2006) Separation and quantitation of water soluble cellular metabolites by hydrophilic interaction chromatography-tandem mass spectrometry. J. Chromatogr. A 1125, 76-88 (Pubitemid 44144585)
32. Lu, W., Bennett, B. D., and Rabinowitz, J. D. (2008) Analytical strategies for LC-MS-based targeted metabolomics. J. Chromatogr. B 871, 236-242
33. Xia, J., and Wishart, D. S. Metabolomic data processing, analysis, and interpretation using MetaboAnalyst. Curr. Protoc. Bioinformatics Chapter 14, Unit 14 10
34. Ward, J. H. (1963) Hierarchical grouping to optimize an objective function. J. Am. Stat. Assoc. 58, 236
35. Quackenbush, J. (2001) Computational analysis of microarray data. Nat. Rev. Genet. 2, 418-427
36. Sorlie, T., Perou, C. M., Tibshirani, R., Aas, T., Geisler, S., Johnsen, H., Hastie, T., Eisen, M. B., van de Rijn, M., Jeffrey, S. S., Thorsen, T., Quist, H., Matese, J. C., Brown, P. O., Botstein, D., Lonning, P. E., and Borresen-Dale, A. L. (2001) Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc. Natl. Acad. Sci. U. S. A. 98, 10869-10874 (Pubitemid 32878711)
37. Sorlie, T., Tibshirani, R., Parker, J., Hastie, T., Marron, J. S., Nobel, A., Deng, S., Johnsen, H., Pesich, R., Geisler, S., Demeter, J., Perou, C. M., Lonning, P. E., Brown, P. O., Borresen-Dale, A. L., and Botstein, D. (2003) Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc. Natl. Acad. Sci. U. S. A. 100, 8418-8423 (Pubitemid 36842560)
38. Collisson, E. A., Sadanandam, A., Olson, P., Gibb, W. J., Truitt, M., Gu, S. D., Cooc, J., Weinkle, J., Kim, G. E., Jakkula, L., Feiler, H. S., Ko, A. H., Olshen, A. B., Danenberg, K. L., Tempero, M. A., Spellman, P. T., Hanahan, D., and Gray, J. W. (2011) Subtypes of pancreatic ductal adenocarcinoma and their differing responses to therapy. Nat. Med. 17, 500-503
39. Zhu, C. Q., Ding, K. Y., Strumpf, D., Weir, B. A., Meyerson, M., Pennell, N., Thomas, R. K., Naoki, K., Ladd-Acosta, C., Liu, N., Pintilie, M., Der, S., Seymour, L., Jurisica, I., Shepherd, F. A., and Tsao, M. S. (2010) Prognostic and predictive gene signature for adjuvant chemotherapy in resected non-small-cell lung cancer. J. Clin. Oncol. 28, 4417-4424
40. Ringnér, M. (2008) What is principal component analysis? Nat. Biotechnol. 26, 303-304
41. Munn, D. H., Zhou, M., Attwood, J. T., Bondarev, I., Conway, S. J., Marshall, B., Brown, C., and Mellor, A. L. (1998) Prevention of allogeneic fetal rejection by tryptophan catabolism. Science 281, 1191-1193 (Pubitemid 28406294)
42. Dantzer, R., O'Connor, J. C., Freund, G. G., Johnson, R. W., and Kelley, K. W. (2008) From inflammation to sickness and depression: when the immune system subjugates the brain. Nat. Rev. Neurosci. 9, 46-56 (Pubitemid 350295688)
43. Lacroix, M., Abi-Said, D., Fourney, D. R., Gokaslan, Z. L., Shi, W. M., DeMonte, F., Lang, F. F., McCutcheon, I. E., Hassenbusch, S. J., Holland, E., Hess, K., Michael, C., Miller, D., and Sawaya, R. (2001) A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival. J. Neurosurg. 95, 190-198 (Pubitemid 32799739)
44. Gerber, J., Tumani, H., Kolenda, H., and Nau, R. (1998) Lumbar and ventricular CSF protein, leukocytes, and lactate in suspected bacterial CNS infections. Neurology 51, 1710-1714 (Pubitemid 28565258)
45. Bralten, L. B. C., Kloosterhof, N. K., Balvers, R., Sacchetti, A., Lapre, L., Lamfers, M., Leenstra, S., de Jonge, H., Kros, J. M., Jansen, E. E. W., Struys, E. A., Jakobs, C., Salomons, G. S., Diks, S. H., Peppelenbosch, M., Kremer, A., Hoogenraad, C. C., Smitt, P., and French, P. J. (2011) IDH1 R132H decreases proliferation of glioma cell lines in vitro and in vivo. Ann. Neurol. 69, 455-463
46. Kallenberg, K., Bock, H. C., Helms, G., Jung, K., Wrede, A., Buhk, J. H., Giese, A., Frahm, J., Strik, H., Dechent, P., and Knauth, M. (2009) Untreated glioblastoma multiforme: increased myo-inositol and glutamine levels in the contralateral cerebral hemisphere at proton MR spectroscopy. Radiology 253, 805-812
47. Castillo, M., Smith, J. K., and Kwock, L. (2000) Correlation of myo-inositol levels and grading of cerebral astrocytomas. Am. J. Neuroradiol. 21, 1645-1649
48. Strott, C. A., and Higashi, Y. (2003) Cholesterol sulfate in human physiology: what's it all about? J. Lipid Res. 44, 1268-1278 (Pubitemid 37279607)
49. Rearick, J. I., Stoner, G. D., George, M. A., and Jetten, A. M. (1988) Cholesterol sulfate accumulation in tumorigenic and nontumorigenic rat esophageal epithelial cells: evidence for defective differentiation control in tumorigenic cells. Cancer Res. 48, 5289-5295
50. Romani, L., Fallarino, F., De Luca, A., Montagnoli, C., D'Angelo, C., Zelante, T., Vacca, C., Bistoni, F., Fioretti, M. C., Grohmann, U., Segal, B. H., and Puccetti, P. (2008) Defective tryptophan catabolism underlies inflammation in mouse chronic granulomatous disease. Nature 451, 211-215
51. Grivennikov, S. I., Greten, F. R., and Karin, M. (2010) Immunity, Inflammation, and Cancer. Cell 140, 883-899
52. Wong, E. T. (2006) Tumor growth, invasion, and angiogenesis in malignant gliomas. J. Neuro-Oncol. 77, 295-296