Short overview on metabolomics approach to study pathophysiology of oxidative stress in cancer

Redox Biology

Volumn 14, Issue , 2018, Pages 47-58

  Andrisic, Luka ^a,b   Dudzik, Danuta ^a   Barbas, Coral ^a   Milkovic, Lidija ^b   Grune, Tilman ^c   Zarkovic, Neven ^b  

^a UNIVERSIDAD SAN PABLO CEU   (Spain)

^b RUDER BO KOVI INSTITUTE   (Croatia)

^c GERMAN INSTITUTE OF HUMAN NUTRITION   (Germany)

Author keywords

4 hydroxynonenal; Biomarkers; Cancer; Carcinogenesis; Glutathione; Immunochemistry; Lipid peroxidation; Metabolomics; Omics science; Oxidative stress

Indexed keywords

ANTIOXIDANT; GLUTATHIONE; REACTIVE OXYGEN METABOLITE; TUMOR MARKER;

ADAPTATION; CARCINOGENESIS; HUMAN; IMMUNOHISTOCHEMISTRY; LIPID PEROXIDATION; MALIGNANT NEOPLASM; METABOLISM; METABOLOMICS; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PATHOPHYSIOLOGY; PERSONALIZED MEDICINE; PRIORITY JOURNAL; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; REVIEW; CHEMISTRY; NEOPLASM;

BIOMARKERS, TUMOR; GLUTATHIONE; HUMANS; METABOLIC NETWORKS AND PATHWAYS; METABOLOMICS; NEOPLASMS; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES;

EID: 85028551316     PISSN: 22132317     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.redox.2017.08.009     Document Type: Review

References (113)

1. Hanahan, D., Weinberg, R.A., The hallmarks of cancer. Cell 100 (2000), 57–70.
2. Milkovic, L., Siems, W., Siems, R., Zarkovic, N., Oxidative stress and antioxidants in carcinogenesis and integrative therapy of cancer. Curr. Pharm. Des. 20 (2014), 6529–6542.
3. Stepanic, V., Gasparovic, A.C., Troselj, K.G., Amic, D., Zarkovic, N., Selected attributes of polyphenols in targeting oxidative stress in cancer. Curr. Top. Med. Chem. 15 (2015), 496–509.
4. Bauer, G., Zarkovic, N., Revealing mechanisms of selective, concentration-dependent potentials of 4-hydroxy-2-nonenal to induce apoptosis in cancer cells through inactivation of membrane-associated catalase. Free Radic. Biol. Med. 81 (2015), 128–144.
5. Milkovic, L., Zarkovic, N., Saso, L., Controversy about pharmacological modulation of Nrf2 for cancer therapy. Redox Biol. 12 (2017), 727–732.
6. Meacham, C.E., Morrison, S.J., Tumour heterogeneity and cancer cell plasticity. Nature 501 (2013), 328–337.
7. Floegel, A., Stefan, N., Yu, Z., Mühlenbruch, K., Drogan, D., Joost, H.G., et al. Identification of serum metabolites associated with risk of type 2 diabetes using a targeted metabolomic approach. Diabetes 62 (2013), 639–648.
8. Dudzik, D., Zorawski, M., Skotnicki, M., Zarzycki, W., García, A., Angulo, S., et al. GC–MS based Gestational Diabetes Mellitus longitudinal study: identification of 2-and 3-hydroxybutyrate as potential prognostic biomarkers. J. Pharm. Biomed. Anal., 2017.
9. Laborde, C.M., Mourino-Alvarez, L., Posada-Ayala, M., Alvarez-Llamas, G., Serranillos-Reus, M.G., Moreu, J., et al. Plasma metabolomics reveals a potential panel of biomarkers for early diagnosis in acute coronary syndrome. Metabolomics 10 (2014), 414–424.
10. Reinke, S.N., Gallart-Ayala, H., Gómez, C., Checa, A., Fauland, A., Naz, S., et al. Metabolomics analysis identifies different metabotypes of asthma severity. Eur. Respir. J., 49, 2017, 1601740.
11. González-Domínguez, R., García-Barrera, T., Gómez-Ariza, J.L., Metabolite profiling for the identification of altered metabolic pathways in Alzheimer's disease. J. Pharm. Biomed. Anal. 107 (2015), 75–81.
12. Armitage, E.G., Barbas, C., Metabolomics in cancer biomarker discovery: current trends and future perspectives. J. Pharm. Biomed. Anal. 87 (2014), 1–11.
13. Nicholson, J.K., Lindon, J.C., Systems biology: metabonomics. Nature 455 (2008), 1054–1056.
14. Vuckovic, D., Current trends and challenges in sample preparation for global metabolomics using liquid chromatography-mass spectrometry. Anal. Bioanal. Chem. 403 (2012), 1523–1548.
15. Wishart, D.S., Tzur, D., Knox, C., Eisner, R., Guo, A.C., Young, N., et al. HMDB: the human metabolome database. Nucleic Acids Res. 35 (2007), D521–D526.
16. Dunn, W.B., Broadhurst, D.I., Atherton, H.J., Goodacre, R., Griffin, J.L., Systems level studies of mammalian metabolomes: the roles of mass spectrometry and nuclear magnetic resonance spectroscopy. Chem. Soc. Rev. 40 (2011), 387–426.
17. Alonso, A., Marsal, S., Julià, A., Analytical methods in untargeted metabolomics: state of the art in 2015. Front. Bioeng. Biotechnol., 3, 2015, 23.
18. Cornett, D.S., Reyzer, M.L., Chaurand, P., Caprioli, R.M., MALDI imaging mass spectrometry: molecular snapshots of biochemical systems. Nat. Methods 4 (2007), 828–833.
19. Lee, R.F.S., Theiner, S., Meibom, A., Koellensperger, G., Keppler, B.K., Dyson, P.J., Application of imaging mass spectrometry approaches to facilitate metal-based anticancer drug research. Metallomics 9 (2017), 365–381.
20. Eberlin, L.S., Liu, X., Ferreira, C.R., Santagata, S., Agar, N.Y.R., Cooks, R.G., Desorption electrospray ionization then MALDI mass spectrometry imaging of lipid and protein distributions in single tissue sections. Anal. Chem. 83 (2011), 8366–8371.
21. Greving, M.P., Patti, G.J., Siuzdak, G., Nanostructure-initiator mass spectrometry metabolite analysis and imaging. Anal. Chem. 83 (2011), 2–7.
22. Hernandes, V.V., Barbas, C., Dudzik, D., A review of blood sample handling and pre-processing for metabolomics studies. Electrophoresis, 2017.
23. Want, E.J., Masson, P., Michopoulos, F., Wilson, I.D., Theodoridis, G., Plumb, R.S., et al. Global metabolic profiling of animal and human tissues via UPLC-MS. Nat. Protoc. 8 (2013), 17–32.
24. Schieber, M., Chandel, N.S., ROS function in redox signaling and oxidative stress. Curr. Biol. 24 (2014), R453–R462.
25. Birben, E., Sahiner, U.M., Sackesen, C., Erzurum, S., Kalayci, O., Oxidative stress and antioxidant defense. World Allergy Organ. J. 5 (2012), 9–19.
26. Halliwell, B., Biochemistry of oxidative stress: figure 1. Biochem. Soc. Trans. 35 (2007), 1147–1150.
27. Antoncic-Svetina, M., Sentija, D., Cipak, A., Milicic, D., Meinitzer, A., Tatzber, F., et al. Ergometry induces systemic oxidative stress in healthy human subjects. Tohoku J. Exp. Med. 221 (2010), 43–48.
28. Reuter, S., Gupta, S.C., Chaturvedi, M.M., Aggarwal, B.B., Oxidative stress, inflammation, and cancer: how are they linked?. Free Radic. Biol. Med. 49 (2010), 1603–1616.
29. Di Meo, S., Reed, T.T., Venditti, P., Victor, V.M., Role of ROS and RNS sources in physiological and pathological conditions. Oxid. Med. Cell. Longev., 2016, 2016, 1245049.
30. Trachootham, D., Lu, W., Ogasawara, M. a., Nilsa, R.-D.V., Huang, P., Redox regulation of cell survival. Antioxid. Redox Signal. 10 (2008), 1343–1374.
31. Willcox, J.K., Ash, S.L., Catignani, G.L., Antioxidants and prevention of chronic disease. Crit. Rev. Food Sci. Nutr. 44 (2004), 275–295.
32. Lobo, V., Patil, A., Phatak, A., Chandra, N., Free radicals, antioxidants and functional foods: impact on human health. Pharmacogn. Rev. 4 (2010), 118–126.
33. Kovacic, P., Jacintho, J.D., Mechanisms of carcinogenesis: focus on oxidative stress and electron transfer. Curr. Med. Chem. 8 (2001), 773–796.
34. Sohal, R.S., Weindruch, R., Oxidative stress, caloric restriction, and aging. Science 273 (1996), 59–63.
35. A.D. Romano, G. Serviddio, A. de Matthaeis, F. Bellanti, G. Vendemiale, Oxidative stress and aging., J. Nephrol. 23 Suppl 15 (n.d.)S29–S36.
36. Jaganjac, M., Čačev, T., Čipak, A., Kapitanović, S., Gall Trošelj, K., Zarković, N., Even stressed cells are individuals: second messengers of free radicals in pathophysiology of cancer. Croat. Med. J. 53 (2012), 304–309.
37. Cipak Gasparovic, A., Zarkovic, N., Zarkovic, K., Semen, K., Kaminskyy, D., Yelisyeyeva, O., et al. Biomarkers of oxidative and nitro-oxidative stress: conventional and novel approaches. Br. J. Pharmacol. 174 (2017), 1771–1783.
38. Frijhoff, J., Winyard, P.G., Zarkovic, N., Davies, S.S., Stocker, R., Cheng, D., et al. Clinical relevance of biomarkers of oxidative stress., 23, 2015.
39. Egea, J., Fabregat, I., Frapart, Y.M., Ghezzi, P., Görlach, A., Kietzmann, T., et al. European contribution to the study of ROS: a summary of the findings and prospects for the future from the COST action BM1203 (EU-ROS). Redox Biol. 13 (2017), 94–162.
40. Toyokuni, S., The origin and future of oxidative stress pathology: from the recognition of carcinogenesis as an iron addiction with ferroptosis-resistance to non-thermal plasma therapy. Pathol. Int. 66 (2016), 245–259.
41. Ho, E., Karimi Galougahi, K., Liu, C.-C., Bhindi, R., Figtree, G.A., Biological markers of oxidative stress: applications to cardiovascular research and practice. Redox Biol. 1 (2013), 483–491.
42. Somogyi, A., Rosta, K., Pusztai, P., Tulassay, Z., Nagy, G., Antioxidant measurements. Physiol. Meas. 28 (2007), R41–R55.
43. Sadikovic, B., Al-Romaih, K., Squire, J.A., Zielenska, M., Cause and consequences of genetic and epigenetic alterations in human cancer. Curr. Genom. 9 (2008), 394–408.
44. Klaunig, J.E., Kamendulis, L.M., Hocevar, B.A., Oxidative stress and oxidative damage in carcinogenesis. Toxicol. Pathol. 38 (2010), 96–109.
45. Sosa, V., Moliné, T., Somoza, R., Paciucci, R., Kondoh, H., LLeonart, M.E., Oxidative stress and cancer: an overview. Ageing Res. Rev. 12 (2013), 376–390.
46. Zheng, L., Cardaci, S., Jerby, L., MacKenzie, E.D., Sciacovelli, M., Johnson, T.I., et al. Fumarate induces redox-dependent senescence by modifying glutathione metabolism. Nat. Commun., 6, 2015, 6001.
47. Vander Heiden, M.G., Exploiting tumor metabolism: challenges for clinical translation. J. Clin. Invest. 123 (2013), 3648–3651.
48. Yuneva, M.O., Fan, T.W.M., Allen, T.D., Higashi, R.M., Ferraris, D.V., Tsukamoto, T., et al. The metabolic profile of tumors depends on both the responsible genetic lesion and tissue type. Cell Metab. 15 (2012), 157–170.
49. Yun, J., Rago, C., Cheong, I., Pagliarini, R., Angenendt, P., Rajagopalan, H., et al. Glucose deprivation contributes to the development of KRAS pathway mutations in tumor cells. (80-.). (325) Science, 2009, 1555–1559.
50. Metallo, C.M., Gameiro, P.A., Bell, E.L., Mattaini, K.R., Yang, J., Hiller, K., et al. Reductive glutamine metabolism by IDH1 mediates lipogenesis under hypoxia. Nature 481 (2011), 380–384.
51. Sotgia, F., Martinez-Outschoorn, U.E., Howell, A., Pestell, R.G., Pavlides, S., Lisanti, M.P., Caveolin-1 and cancer metabolism in the tumor microenvironment: markers, models, and mechanisms. Annu. Rev. Pathol. Mech. Dis. 7 (2012), 423–467.
52. Kim, J.-w., Dang, C.V., Cancer's molecular sweet tooth and the Warburg effect. Cancer Res. 66 (2006), 8927–8930.
53. Vaughn, A.E., Deshmukh, M., Glucose metabolism inhibits apoptosis in neurons and cancer cells by redox inactivation of cytochrome c. Nat. Cell Biol. 10 (2008), 1477–1483.
54. Kondoh, H., Lleonart, M.E., Gil, J., Wang, J., Degan, P., Peters, G., et al. Glycolytic enzymes can modulate cellular life span. Cancer Res. 65 (2005), 177–185.
55. Kondoh, H., Lleonart, M.E., Bernard, D., Gil, J., Protection from oxidative stress by enhanced glycolysis; a possible mechanism of cellular immortalization. Histol. Histopathol. 22 (2007), 85–90.
56. Weinberg, F., Chandel, N.S., Mitochondrial metabolism and cancer. Ann. N. Y. Acad. Sci. 1177 (2009), 66–73.
57. Kondoh, H., Lleonart, M.E., Nakashima, Y., Yokode, M., Tanaka, M., Bernard, D., et al. A high glycolytic flux supports the proliferative potential of murine embryonic stem cells. Antioxid. Redox Signal. 9 (2007), 293–299.
58. Gatenby, R.A., Gillies, R.J., Why do cancers have high aerobic glycolysis?. Nat. Rev. Cancer 4 (2004), 891–899.
59. Smolková, K., Bellance, N., Scandurra, F., Génot, E., Gnaiger, E., Plecitá-Hlavatá, L., et al. Mitochondrial bioenergetic adaptations of breast cancer cells to aglycemia and hypoxia. J. Bioenerg. Biomembr. 42 (2010), 55–67.
60. Rossignol, R., Gilkerson, R., Aggeler, R., Yamagata, K., Remington, S.J., Capaldi, R.A., Energy substrate modulates mitochondrial structure and oxidative capacity in cancer cells. Cancer Res. 64 (2004), 985–993.
61. Zhong, H., Xiao, M., Zarkovic, K., Zhu, M., Sa, R., Lu, J., et al. Mitochondrial control of apoptosis through modulation of cardiolipin oxidation in hepatocellular carcinoma: a novel link between oxidative stress and cancer. Free Radic. Biol. Med. 102 (2017), 67–76.
62. Živković, N.P., Petrovečki, M., Lončarić, T., Nikolić, I., Waeg, G., Jaganjac, M., et al. Positron emission tomography-computed tomography and 4-hydroxynonenal-histidine immunohistochemistry reveal differential onset of lipid peroxidation in primary lung cancer and in pulmonary metastasis of remote malignancies. Redox Biol. 11 (2017), 600–605.
63. Zarkovic, N., Cipak, A., Jaganjac, M., Borovic, S., Zarkovic, K., Pathophysiological relevance of aldehydic protein modifications. J. Proteom. 92 (2013), 239–247.
64. Beloribi-Djefaflia, S., Vasseur, S., Guillaumond, F., Lipid metabolic reprogramming in cancer cells. Oncogenesis, 5, 2016, e189.
65. N. Zarkovic, 4-hydroxynonenal as a bioactive marker of pathophysiological processes., Mol. Aspects Med. 24 (n.d.) 281–291.
66. Zarkovic, K., Jakovcevic, A., Zarkovic, N., Contribution of the HNE-immunohistochemistry to modern pathological concepts of major human diseases. Free Radic. Biol. Med. 111 (2017), 110–126.
67. Aquilano, K., Baldelli, S., Ciriolo, M.R., Glutathione: new roles in redox signaling for an old antioxidant. Front. Pharmacol., 5, 2014, 196.
68. Sentellas, S., Morales-Ibanez, O., Zanuy, M., Albertí, J.J., GSSG/GSH ratios in cryopreserved rat and human hepatocytes as a biomarker for drug induced oxidative stress. Toxicol. Vitr. 28 (2014), 1006–1015.
69. Wang, N., Wei, J., Liu, Y., Pei, D., Hu, Q., Wang, Y., et al. Discovery of biomarkers for oxidative stress based on cellular metabolomics. Biomarkers 21 (2016), 449–457.
70. Shaw, A.T., Winslow, M.M., Magendantz, M., Ouyang, C., Dowdle, J., Subramanian, A., et al. Selective killing of K-RAS mutant cancer cells by small molecule inducers of oxidative stress. Proc. Natl. Acad. Sci. 108 (2011), 8773–8778.
71. Brunelli, L., Caiola, E., Marabese, M., Broggini, M., Pastorelli, R., Capturing the metabolomic diversity of KRAS mutants in non-small-cell lung cancer cells. Oncotarget 5 (2014), 4722–4731.
72. Willmann, L., Schlimpert, M., Hirschfeld, M., Erbes, T., Neubauer, H., Stickeler, E., et al. Alterations of the exo- and endometabolite profiles in breast cancer cell lines: a mass spectrometry-based metabolomics approach. Anal. Chim. Acta 925 (2016), 34–42.
73. Yeh, C.-C., Hou, M.-F., Tsai, S.-M., Lin, S.-K., Hsiao, J.-K., Huang, J.-C., et al. Superoxide anion radical, lipid peroxides and antioxidant status in the blood of patients with breast cancer. Clin. Chim. Acta 361 (2005), 104–111.
74. King, A., Selak, M.A., Gottlieb, E., Succinate dehydrogenase and fumarate hydratase: linking mitochondrial dysfunction and cancer. Oncogene 25 (2006), 4675–4682.
75. Chesler, L., Weiss, W.A., Genetically engineered murine models – contribution to our understanding of the genetics, molecular pathology and therapeutic targeting of neuroblastoma. Semin. Cancer Biol. 21 (2011), 245–255.
76. Carter, D.R., Sutton, S.K., Pajic, M., Murray, J., Sekyere, E.O., Fletcher, J., et al. Glutathione biosynthesis is upregulated at the initiation of MYCN-driven neuroblastoma tumorigenesis. Mol. Oncol. 10 (2016), 866–878.
77. Emmett, M., Acetaminophen toxicity and 5-oxoproline (pyroglutamic acid): a tale of two cycles, one an ATP-depleting futile cycle and the other a useful cycle. Clin. J. Am. Soc. Nephrol. 9 (2014), 191–200.
78. Ganti, S., Taylor, S.L., Abu Aboud, O., Yang, J., Evans, C., Osier, M.V., et al. Kidney tumor biomarkers revealed by simultaneous multiple matrix metabolomics analysis. Cancer Res. 72 (2012), 3471–3479.
79. Ishikawa, S., Sugimoto, M., Kitabatake, K., Sugano, A., Nakamura, M., Kaneko, M., et al. Identification of salivary metabolomic biomarkers for oral cancer screening. Sci. Rep., 6, 2016, 31520.
80. Somashekar, B.S., Kamarajan, P., Danciu, T., Kapila, Y.L., Chinnaiyan, A.M., Rajendiran, T.M., et al. Magic angle spinning NMR-based metabolic profiling of head and neck squamous cell carcinoma tissues. J. Proteome Res. 10 (2011), 5232–5241.
81. Tang, X., Lin, C.-C., Spasojevic, I., Iversen, E.S., Chi, J.-T., Marks, J.R., A joint analysis of metabolomics and genetics of breast cancer. Breast Cancer Res., 16, 2014, 415.
82. Gao, R., Cheng, J., Fan, C., Shi, X., Cao, Y., Sun, B., et al. Serum metabolomics to identify the liver disease-specific biomarkers for the progression of hepatitis to hepatocellular carcinoma. Sci. Rep., 5, 2016, 18175.
83. Qiu, Y., Cai, G., Zhou, B., Li, D., Zhao, A., Xie, G., et al. A distinct metabolic signature of human colorectal cancer with prognostic potential. Clin. Cancer Res. 20 (2014), 2136–2146.
84. Soga, T., Baran, R., Suematsu, M., Ueno, Y., Ikeda, S., Sakurakawa, T., et al. Differential metabolomics reveals ophthalmic acid as an oxidative stress biomarker indicating hepatic glutathione consumption. J. Biol. Chem. 281 (2006), 16768–16776.
85. Davis, V.W., Schiller, D.E., Eurich, D., Sawyer, M.B., Urinary metabolomic signature of esophageal cancer and Barrett's esophagus. World J. Surg. Oncol., 10, 2012, 271.
86. Fong, M.Y., McDunn, J., Kakar, S.S., Identification of metabolites in the normal ovary and their transformation in primary and metastatic ovarian cancer. PLoS One, 6, 2011, e19963.
87. Soga, T., Sugimoto, M., Honma, M., Mori, M., Igarashi, K., Kashikura, K., et al. Serum metabolomics reveals γ-glutamyl dipeptides as biomarkers for discrimination among different forms of liver disease. J. Hepatol. 55 (2011), 896–905.
88. Fitian, A.I., Nelson, D.R., Liu, C., Xu, Y., Ararat, M., Cabrera, R., Integrated metabolomic profiling of hepatocellular carcinoma in hepatitis C cirrhosis through GC/MS and UPLC/MS-MS. Liver Int. 34 (2014), 1428–1444.
89. Björkblom, B., Wibom, C., Jonsson, P., Mörén, L., Andersson, U., Børge Johannesen, T., et al. Metabolomic screening of pre-diagnostic serum samples identifies association between α- and γ-tocopherols and glioblastoma risk. Oncotarget 7 (2016), 37043–37053.
90. Zarkovic, K., Juric, G., Waeg, G., Kolenc, D., Zarkovic, N., Immunohistochemical appearance of HNE-protein conjugates in human astrocytomas. Biofactors 24 (2005), 33–40.
91. G. Juric-Sekhar, K. Zarkovic, G. Waeg, A. Cipak, N. Zarkovic, Distribution of 4-hydroxynonenal-protein conjugates as a marker of lipid peroxidation and parameter of malignancy in astrocytic and ependymal tumors of the brain., Tumori. 95 (n.d.) 762–768.
92. Rizvi, S., Raza, S.T., Ahmed, F., Ahmad, A., Abbas, S., Mahdi, F., The role of vitamin e in human health and some diseases. Sultan Qaboos Univ. Med. J. 14 (2014), e157–65.
93. Jin, H., Qiao, F., Chen, L., Lu, C., Xu, L., Gao, X., Serum metabolomic signatures of lymph node metastasis of esophageal squamous cell carcinoma. J. Proteome Res. 13 (2014), 4091–4103.
94. Wikoff, W.R., Grapov, D., Fahrmann, J.F., DeFelice, B., Rom, W.N., Pass, H.I., et al. Metabolomic markers of altered nucleotide metabolism in early stage adenocarcinoma. Cancer Prev. Res. 8 (2015), 410–418.
95. Ke, C., Li, A., Hou, Y., Sun, M., Yang, K., Cheng, J., et al. Metabolic phenotyping for monitoring ovarian cancer patients. Sci. Rep., 6, 2016, 23334.
96. Hwang, I.K., Yoo, K.-Y., Li, H., Park, O.K., Lee, C.H., Choi, J.H., et al. Indole-3-propionic acid attenuates neuronal damage and oxidative stress in the ischemic hippocampus. J. Neurosci. Res. 87 (2009), 2126–2137.
97. Sihvo, E.I., Ruohtula, T., Auvinen, M.I., Koivistoinen, A., Harjula, A.L., Salo, J.A., Simultaneous progression of oxidative stress and angiogenesis in malignant transformation of Barrett esophagus. J. Thorac. Cardiovasc. Surg. 126 (2003), 1952–1957.
98. Wang, Q., Liu, D., Song, P., Zou, M.-H., Tryptophan-kynurenine pathway is dysregulated in inflammation, and immune activation. Front. Biosci. (Landmark Ed.) 20 (2015), 1116–1143.
99. Song, H., Park, H., Kim, Y.-S., Kim, K.D., Lee, H.-K., Cho, D.-H., et al. L-Kynurenine-induced apoptosis in human NK cells is mediated by reactive oxygen species. Int. Immunopharmacol. 11 (2011), 932–938.
100. Buczko, P., Zalewska, A., Szarmach, I., Saliva and oxidative stress in oral cavity and in some systemic disorders. J. Physiol. Pharmacol. 66 (2015), 3–9.
101. Maiuolo, J., Oppedisano, F., Gratteri, S., Muscoli, C., Mollace, V., Regulation of uric acid metabolism and excretion. Int. J. Cardiol. 213 (2016), 8–14.
102. Gu, J., Hu, X., Shao, W., Ji, T., Yang, W., Zhuo, H., et al. Metabolomic analysis reveals altered metabolic pathways in a rat model of gastric carcinogenesis. Oncotarget 7 (2016), 60053–60073.
103. Abaffy, T., Möller, M.G., Riemer, D.D., Milikowski, C., DeFazio, R.A., Comparative analysis of volatile metabolomics signals from melanoma and benign skin: a pilot study. Metabolomics 9 (2013), 998–1008.
104. Kalluri, U., Naiker, M., Myers, M.A., Cell culture metabolomics in the diagnosis of lung cancer—the influence of cell culture conditions. J. Breath. Res., 8, 2014, 027109.
105. Li, F., Patterson, A.D., Krausz, K.W., Jiang, C., Bi, H., Sowers, A.L., et al. Metabolomics reveals that tumor xenografts induce liver dysfunction. Mol. Cell. Proteom. 12 (2013), 2126–2135.
106. Jones, C.M., Monge, M.E., Kim, J., Matzuk, M.M., Fernández, F.M., Metabolomic serum profiling detects early-stage high-grade serous ovarian cancer in a mouse model. J. Proteome Res. 14 (2015), 917–927.
107. Negre-Salvayre, A., Auge, N., Ayala, V., Basaga, H., Boada, J., Brenke, R., et al. Pathological aspects of lipid peroxidation. Free Radic. Res. 44 (2010), 1125–1171.
108. Gęgotek, A., Nikliński, J., Žarković, N., Žarković, K., Waeg, G., Łuczaj, W., et al. Lipid mediators involved in the oxidative stress and antioxidant defence of human lung cancer cells. Redox Biol. 9 (2016), 210–219.
109. Gasparovic, A.C., Milkovic, L., Sunjic, S.B., Zarkovic, N., Cancer growth regulation by 4-hydroxynonenal. Free Radic. Biol. Med., 2017, 0–1.
110. Fedorova, M., Zarkovic, N., Preface to the special issue on 4-hydroxynonenal and related lipid oxidation products. Free Radic. Biol. Med., 111, 2017, 1.
111. Poli, G., Zarkovic, N., Editorial introduction to the special issue on 4-hydroxynonenal and related lipid oxidation products. Free Radic. Biol. Med. 111 (2017), 2–5.
112. Shannon, P., Markiel, A., Ozier, O., Baliga, N.S., Wang, J.T., Ramage, D., et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13 (2003), 2498–2504.
113. Xia, J., Sinelnikov, I.V., Han, B., Wishart, D.S., MetaboAnalyst 3.0-making metabolomics more meaningful. Nucleic Acids Res. 43 (2015), W251–W257.