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Изменения метаболомного профиля плазмы крови у пациентов с лимфомами в ходе полихимиотерапии - Журнал Терапевтический архив №11 Инфекционные болезни 2025
Изменения метаболомного профиля плазмы крови у пациентов с лимфомами в ходе полихимиотерапии
Варзиева В.Г., Болдин А.А., Шестакова К.М., Басханова С.Н., Самойлов В.М., Ильгисонис И.С., Кириченко Ю.Ю., Каримов Р.Р., Смолярчук Е.А., Кудлай Д.А., Тарасов В.В., Беленков Ю.Н., Апполонова С.А. Изменения метаболомного профиля плазмы крови у пациентов с лимфомами в ходе полихимиотерапии. Терапевтический архив. 2025;97(11):908–919. DOI: 10.26442/00403660.2025.11.203491
© ООО «КОНСИЛИУМ МЕДИКУМ», 2025 г.
© ООО «КОНСИЛИУМ МЕДИКУМ», 2025 г.
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Аннотация
Обоснование. Метаболомные исследования в онкологии позволяют глубже понять биохимические процессы, сопровождающие опухолевый рост и ответ организма на лечение. При лимфомах системные метаболические изменения остаются малоизученными, несмотря на высокую клиническую значимость.
Цель. Оценить изменения метаболомного профиля плазмы крови у пациентов с лимфомами на различных этапах полихимиотерапии (ПХТ) и сравнить их с показателями здоровых добровольцев.
Материалы и методы. В исследование включены 18 пациентов с лимфомами, у которых кровь отбирали до начала лечения, после 1 и 3-го курсов ПХТ. Контрольную группу составили 30 здоровых добровольцев. Анализ выполняли методом высокоэффективной жидкостной хроматографии с тандемной масс-спектрометрией (ВЭЖХ–МС/МС), включая аминокислоты, производные триптофана, аргинина и ацилкарнитины. Статистическую обработку проводили с использованием дисперсионного анализа и метода главных компонент.
Результаты. До терапии у пациентов выявлены характерные нарушения обмена веществ: активация кинуренинового пути метаболизма триптофана, снижение уровня аргинина и увеличение его метилированных производных, сдвиги в аминокислотном и ацилкарнитиновом профилях. На фоне ПХТ наблюдали частичную нормализацию приведенных показателей, особенно в отношении серотонин-мелатонинового каскада и кинурениновых метаболитов.
Заключение. Метаболомный анализ позволил выявить характерные биохимические изменения при лимфомах и их динамику в ходе лечения. Полученные данные подчеркивают потенциал метаболомики как инструмента мониторинга эффективности лечения и состояния пациента в онкологии.
Ключевые слова: лимфома, метаболомика, полихимиотерапия, аминокислоты, триптофан, ацилкарнитин
Aim. To evaluate changes in the metabolomic profile of blood plasma in patients with lymphoma at various stages of polychemotherapy (PCT) and compare them to those of healthy volunteers.
Materials and methods. The study included 18 patients with lymphoma from whom blood was collected before treatment and after the first and third courses of PCT. The control group included 30 healthy volunteers. The analysis was performed by high-performance liquid chromatography with tandem mass spectrometry (HPLC-MS/MS) and included measurements of amino acids, tryptophan and arginine derivatives, and acylcarnitines. Statistical processing was performed using analysis of variance and principal component analysis.
Results. Prior to therapy, patients showed characteristic metabolic disorders: activation of the kynurenine pathway of tryptophan metabolism, a decrease in arginine, and an increase in its methylated derivatives, as well as shifts in the amino acid and acylcarnitine profiles. During PCT, partial normalization of these indicators was observed, especially for the serotonin-melatonin cascade and kynurenine metabolites.
Conclusion. Metabolomics analysis revealed characteristic biochemical changes in patients with lymphoma and their changes over time during treatment. The data obtained emphasize the potential of metabolomics as a tool for monitoring treatment effectiveness and patient condition in oncology.
Keywords: lymphoma, metabolomics, polychemotherapy, aminoacids, tryptophan, acylcarnitin
Цель. Оценить изменения метаболомного профиля плазмы крови у пациентов с лимфомами на различных этапах полихимиотерапии (ПХТ) и сравнить их с показателями здоровых добровольцев.
Материалы и методы. В исследование включены 18 пациентов с лимфомами, у которых кровь отбирали до начала лечения, после 1 и 3-го курсов ПХТ. Контрольную группу составили 30 здоровых добровольцев. Анализ выполняли методом высокоэффективной жидкостной хроматографии с тандемной масс-спектрометрией (ВЭЖХ–МС/МС), включая аминокислоты, производные триптофана, аргинина и ацилкарнитины. Статистическую обработку проводили с использованием дисперсионного анализа и метода главных компонент.
Результаты. До терапии у пациентов выявлены характерные нарушения обмена веществ: активация кинуренинового пути метаболизма триптофана, снижение уровня аргинина и увеличение его метилированных производных, сдвиги в аминокислотном и ацилкарнитиновом профилях. На фоне ПХТ наблюдали частичную нормализацию приведенных показателей, особенно в отношении серотонин-мелатонинового каскада и кинурениновых метаболитов.
Заключение. Метаболомный анализ позволил выявить характерные биохимические изменения при лимфомах и их динамику в ходе лечения. Полученные данные подчеркивают потенциал метаболомики как инструмента мониторинга эффективности лечения и состояния пациента в онкологии.
Ключевые слова: лимфома, метаболомика, полихимиотерапия, аминокислоты, триптофан, ацилкарнитин
________________________________________________
Aim. To evaluate changes in the metabolomic profile of blood plasma in patients with lymphoma at various stages of polychemotherapy (PCT) and compare them to those of healthy volunteers.
Materials and methods. The study included 18 patients with lymphoma from whom blood was collected before treatment and after the first and third courses of PCT. The control group included 30 healthy volunteers. The analysis was performed by high-performance liquid chromatography with tandem mass spectrometry (HPLC-MS/MS) and included measurements of amino acids, tryptophan and arginine derivatives, and acylcarnitines. Statistical processing was performed using analysis of variance and principal component analysis.
Results. Prior to therapy, patients showed characteristic metabolic disorders: activation of the kynurenine pathway of tryptophan metabolism, a decrease in arginine, and an increase in its methylated derivatives, as well as shifts in the amino acid and acylcarnitine profiles. During PCT, partial normalization of these indicators was observed, especially for the serotonin-melatonin cascade and kynurenine metabolites.
Conclusion. Metabolomics analysis revealed characteristic biochemical changes in patients with lymphoma and their changes over time during treatment. The data obtained emphasize the potential of metabolomics as a tool for monitoring treatment effectiveness and patient condition in oncology.
Keywords: lymphoma, metabolomics, polychemotherapy, aminoacids, tryptophan, acylcarnitin
Полный текст
Список литературы
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2. Ansell SM. Hodgkin lymphoma: 2025 update on diagnosis, risk-stratification, and management. Am J Hematol. 2024;99(12):2367-78. DOI:10.1002/ajh.27470
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65. Choe CU, Lezius S, Cordts K, et al. Low homoarginine/SDMA ratio is associated with poor short- and long-term outcome after stroke in two prospective studies. Neurol Sci. 2020;41(1):149-53. DOI:10.1007/s10072-019-04058-0
66. Rodionov RN, Beyer-Westendorf J, Bode-Böger SM, et al. Homoarginine and methylarginines independently predict long-term outcome in patients presenting with suspicion of venous thromboembolism. Sci Rep. 2021;11(1):9569. DOI:10.1038/s41598-021-88986-y
2. Ansell SM. Hodgkin lymphoma: 2025 update on diagnosis, risk-stratification, and management. Am J Hematol. 2024;99(12):2367-78. DOI:10.1002/ajh.27470
3. Ansell SM. Non-Hodgkin Lymphoma: Diagnosis and Treatment. Mayo Clin Proc. 2015;90(8):1152-63. DOI:10.1016/j.mayocp.2015.04.025
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6. Alfaifi A, Refai MY, Alsaadi M, et al. Metabolomics: A New Era in the Diagnosis or Prognosis of B-Cell Non-Hodgkin's Lymphoma. Diagnostics (Basel). 2023;13(5):861. DOI:10.3390/diagnostics13050861
7. Moskaleva NE, Shestakova KM, Kukharenko AV, et al. Target Metabolome Profiling-Based Machine Learning as a Diagnostic Approach for Cardiovascular Diseases in Adults. Metabolites. 2022;12(12):1185. DOI:10.3390/metabo12121185
8. Shestakova KM, Moskaleva NE, Boldin AA, et al. Targeted metabolomic profiling as a tool for diagnostics of patients with non-small-cell lung cancer. Sci Rep. 2023;13(1):11072. DOI:10.1038/s41598-023-38140-7
9. Musaeva LM, Shestakova KM, Baskhanova SN, et al. Evaluating treatment responsiveness in rheumatoid arthritis through predictive metabolomic profiling: A systematic review of studies examining methotrexate, TNF, and IL-6 inhibitors as therapeutic interventions. Clin Rheumatol. 2025;44(3):923-52. DOI:10.1007/s10067-025-07355-6
10. Barberini L, Noto A, Fattuoni C, et al. The Metabolomic Profile of Lymphoma Subtypes: A Pilot Study. Molecules. 2019;24(13):2367. DOI:10.3390/molecules24132367
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14. Banoei MM, Mahé E, Mansoor A, et al. NMR-based metabolomic profiling can differentiate follicular lymphoma from benign lymph node tissues and may be predictive of outcome. Sci Rep. 2022;12(1):8294. DOI:10.1038/s41598-022-12445-5
15. Stenson M, Pedersen A, Hasselblom S, et al. Serum nuclear magnetic resonance-based metabolomics and outcome in diffuse large B-cell lymphoma patients – a pilot study. Leuk Lymphoma. 2016;57(8):1814-22. DOI:10.3109/10428194.2016.1140164
16. Pera B, Krumsiek J, Assouline SE, et al. Metabolomic Profiling Reveals Cellular Reprogramming of B-Cell Lymphoma by a Lysine Deacetylase Inhibitor through the Choline Pathway. EBioMedicine. 2018;28:80-9. DOI:10.1016/j.ebiom.2018.01.014
17. Xiong J, Bian J, Wang L, et al. Dysregulated choline metabolism in T-cell lymphoma: role of choline kinase-α and therapeutic targeting. Blood Cancer J. 2015;5(3):287. DOI:10.1038/bcj.2015.10
18. Zheng M, Zhou X, Wang Q, et al. Metabolomic approach to characterize the metabolic phenotypes and varied response to ouabain of diffuse large B-cell lymphoma cells. Leuk Lymphoma. 2021;62(7):1597-608. DOI:10.1080/10428194.2021.1881513
19. Mi M, Liu Z, Zheng X, et al. Serum metabolomic profiling based on GC/MS helped to discriminate Diffuse Large B-cell Lymphoma patients with different prognosis. Leuk Res. 2021;111:106693. DOI:10.1016/j.leukres.2021.106693
20. Fei F, Zheng M, Xu Z, et al. Plasma Metabolites Forecast Occurrence and Prognosis for Patients With Diffuse Large B-Cell Lymphoma. Front Oncol. 2022;12:894891. DOI:10.3389/fonc.2022.894891
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24. Фолликулярная лимфома. Клинические рекомендации. 2024. Режим доступа: https://cr.minzdrav.gov.ru/view-cr/151_2. Ссылка активна на 08.06.2025 [Follikuliarnaia limfoma. Klinicheskie rekomendatsii. 2024. Available at: https://cr.minzdrav.gov.ru/view-cr/151_2. Accessed: 08.06.2025 (in Russian)].
25. Лимфома Ходжкина. Клинические рекомендации. 2024. Режим доступа: https://cr.minzdrav.gov.ru/view-cr/139_2. Ссылка активна на 08.06.2025 Limfoma Khodzhkina. Klinicheskie rekomendatsii. 2024. Available at: https://cr.minzdrav.gov.ru/view-cr/139_2. Accessed: 08.06.2025 (in Russian)].
26. Агрессивные нефолликулярные лимфомы – диффузная В-клеточная крупноклеточная лимфома, В-клеточная лимфома высокой степени злокачественности с перестройкой генов c-MYC и BCL2/BCL6, первичная медиастинальная В-клеточная лимфома, медиастинальная лимфома серой зоны, лимфома Беркитта, плазмобластная лимфома. Клинические рекомендации. 2024. Режим доступа: https://cr.minzdrav.gov.ru/view-cr/129_3. Ссылка активна на 08.06.2025 [Agressivnye nefollikuliarnye limfomy – diffuznaia V-kletochnaia krupnokletochnaia limfoma, V-kletochnaia limfoma vysokoi stepeni zlokachestvennosti s perestroikoi genov c-MYC i BCL2/BCL6, pervichnaia mediastinal'naia V-kletochnaia limfoma, mediastinal'naia limfoma seroi zony, limfoma Berkitta, plazmoblastnaia limfoma. Klinicheskie rekomendatsii. 2024. Available at: https://cr.minzdrav.gov.ru/view-cr/129_3. Accessed: 08.06.2025 (in Russian)].
27. Лимфома из клеток мантии. Клинические рекомендации. 2024. Режим доступа: https://cr.minzdrav.gov.ru/view-cr/136_2. Ссылка активна на 08.06.2025 [Limfoma iz kletok mantii. Klinicheskie rekomendatsii. 2024. Available at: https://cr.minzdrav.gov.ru/view-cr/136_2. Accessed: 08.06.2025 (in Russian)].
28. Baskhanova SN, Moskaleva NE, Shestakova KM, et al. Targeted metabolomics for cardiovascular disease: Validation of a high-throughput HPLC-MS/MS assay. J Chromatogr B Analyt Technol Biomed Life Sci. 2025;1264:124732. DOI:10.1016/j.jchromb.2025.124732
29. Kim M, Tomek P. Tryptophan: A Rheostat of Cancer Immune Escape Mediated by Immunosuppressive Enzymes IDO1 and TDO. Front Immunol. 2021;12:636081. DOI:10.3389/fimmu.2021.636081
30. Lu Z, Zhang C, Zhang J, et al. The Kynurenine Pathway and Indole Pathway in Tryptophan Metabolism Influence Tumor Progression. Cancer Med. 2025;14(6):e70703. DOI:10.1002/cam4.70703
31. Sordillo PP, Sordillo LA, Helson L. The Kynurenine Pathway: A Primary Resistance Mechanism in Patients with Glioblastoma. Anticancer Res. 2017;37(5):2159-71. DOI:10.21873/anticanres.11551
32. Basson C, Serem JC, Hlophe YN, Bipath P. The tryptophan-kynurenine pathway in immunomodulation and cancer metastasis. Cancer Med. 2023;12(18):18691-801. DOI:10.1002/cam4.6484
33. León-Letelier RA, Dou R, Vykoukal J, et al. The kynurenine pathway presents multi-faceted metabolic vulnerabilities in cancer. Front Oncol. 2023;13:1256769. DOI:10.3389/fonc.2023.1256769
34. Gouasmi R, Ferraro-Peyret C, Nancey S, et al. The Kynurenine Pathway and Cancer: Why Keep It Simple When You Can Make It Complicated. Cancers (Basel). 2022;14(11):2793. DOI:10.3390/cancers14112793
35. Sahm F, Oezen I, Opitz CA, et al. The endogenous tryptophan metabolite and NAD+ precursor quinolinic acid confers resistance of gliomas to oxidative stress. Cancer Res. 2013;73(11):3225-34. DOI:10.1158/0008-5472.CAN-12-3831
36. Navas LE, Carnero A. NAD(+) metabolism, stemness, the immune response, and cancer. Signal Transduct Target Ther. 2021;6(1):2. DOI:10.1038/s41392-020-00354-w
37. Ghanem MS, Caffa I, Monacelli F, Nencioni A. Inhibitors of NAD(+) Production in Cancer Treatment: State of the Art and Perspectives. Int J Mol Sci. 2024;25(4):2092. DOI:10.3390/ijms25042092
38. De Santo C, Booth S, Vardon A, et al. The arginine metabolome in acute lymphoblastic leukemia can be targeted by the pegylated-recombinant arginase I BCT-100. Int J Cancer. 2018;142(7):1490-502. DOI:10.1002/ijc.31170
39. Delage B, Luong P, Maharaj L, et al. Promoter methylation of argininosuccinate synthetase-1 sensitises lymphomas to arginine deiminase treatment, autophagy and caspase-dependent apoptosis. Cell Death Dis. 2012;3(7):e342. DOI:10.1038/cddis.2012.83
40. Ren Y, Fan L, Wang L, et al. SSRP1/SLC3A2 Axis in Arginine Transport: A New Target for Overcoming Immune Evasion and Tumor Progression in Peripheral T-Cell Lymphoma. Adv Sci (Weinh). 2025;12(21):e2415698. DOI:10.1002/advs.202415698
41. Puglisi F, Padella A, Parrinello NL, et al. Dissecting the Adaptive Response to Arginine Deprivation in Hodgkin Lymphoma. Blood. 2021;138(Suppl. 1):4497-47. DOI:10.1182/blood-2021-151006
42. Chung J, Karkhanis V, Baiocchi RA, Sif S. Protein arginine methyltransferase 5 (PRMT5) promotes survival of lymphoma cells via activation of WNT/β-catenin and AKT/GSK3β proliferative signaling. J Biol Chem. 2019;294(19):7692-710. DOI:10.1074/jbc.RA119.007640
43. Sauter C, Simonet J, Guidez F, et al. Protein Arginine Methyltransferases as Therapeutic Targets in Hematological Malignancies. Cancers (Basel). 2022;14(21):5443. DOI:10.3390/cancers14215443
44. Yao N, Li W, Xu G, et al. Choline metabolism and its implications in cancer. Front Oncol. 2023;13:1234887. DOI:10.3389/fonc.2023.1234887
45. Glunde K, Bhujwalla ZM, Ronen SM. Choline metabolism in malignant transformation. Nat Rev Cancer. 2011;11(12):835-48. DOI:10.1038/nrc3162
46. Glunde K, Ackerstaff E, Mori N, et al. Choline phospholipid metabolism in cancer: consequences for molecular pharmaceutical interventions. Mol Pharm. 2006;3(5):496-506. DOI:10.1021/mp060067e
47. Dobrijević D, Pastor K, Nastić N, et al. Betaine as a Functional Ingredient: Metabolism, Health-Promoting Attributes, Food Sources, Applications and Analysis Methods. Molecules. 2023;28(12):4824. DOI:10.3390/molecules28124824
48. Zhou C, Basnet R, Zhen C, et al. Trimethylamine N-oxide promotes the proliferation and migration of hepatocellular carcinoma cell through the MAPK pathway. Discov Oncol. 2024;15(1):346. DOI:10.1007/s12672-024-01178-8
49. Xie H, Zhang K, Wei Y, et al. The association of serum betaine concentrations with the risk of new-onset cancers: results from two independent nested case-control studies. Nutr Metab (Lond). 2023;20(1):46. DOI:10.1186/s12986-023-00755-y
50. Ninomiya S, Narala N, Huye L, et al. Tumor indoleamine 2,3-dioxygenase (IDO) inhibits CD19-CAR T cells and is downregulated by lymphodepleting drugs. Blood. 2015;125(25):3905-16. DOI:10.1182/blood-2015-01-621474
51. Zhang N, Huang Y, Wang G, et al. Metabolomics assisted by transcriptomics analysis to reveal metabolic characteristics and potential biomarkers associated with treatment response of neoadjuvant therapy with TCbHP regimen in HER2 + breast cancer. Breast Cancer Res. 2024;26(1):64. DOI:10.1186/s13058-024-01813-w
52. Yoneyama T, Abdul-Hadi K, Brown A, et al. A Citrulline-Based Translational Population System Toxicology Model for Gastrointestinal-Related Adverse Events Associated With Anticancer Treatments. CPT Pharmacometrics Syst Pharmacol. 2019;8(12):951-61. DOI:10.1002/psp4.12475
53. Zezulová M, Bartoušková M, Hlídková E, et al. Citrulline as a biomarker of gastrointestinal toxicity in patients with rectal carcinoma treated with chemoradiation. Clin Chem Lab Med. 2016;54(2):305-14. DOI:10.1515/cclm-2015-0326
54. Mehdizadeh A, Bonyadi M, Darabi M, et al. Common chemotherapeutic agents modulate fatty acid distribution in human hepatocellular carcinoma and colorectal cancer cells. Bioimpacts. 2017;7(1):31-9. DOI:10.15171/bi.2017.05
55. Dambrova M, Makrecka-Kuka M, Kuka J, et al. Acylcarnitines: Nomenclature, Biomarkers, Therapeutic Potential, Drug Targets, and Clinical Trials. Pharmacol Rev. 2022;74(3):506-51. DOI:10.1124/pharmrev.121.000408
56. Nowak C, Hetty S, Salihovic S, et al. Glucose challenge metabolomics implicates medium-chain acylcarnitines in insulin resistance. Sci Rep. 2018;8(1):8691. DOI:10.1038/s41598-018-26701-0
57. Davies A, Wenzl FA, Li XS, et al. Short and medium chain acylcarnitines as markers of outcome in diabetic and non-diabetic subjects with acute coronary syndromes. Int J Cardiol. 2023;389:131261. DOI:10.1016/j.ijcard.2023.131261
58. Koves TR, Zhang GF, Davidson MT, et al. Pyruvate-supported flux through medium-chain ketothiolase promotes mitochondrial lipid tolerance in cardiac and skeletal muscles. Cell Metab. 2023;35(6):1038-1056.e8. DOI:10.1016/j.cmet.2023.03.016
59. Fiamoncini J, Lima TM, Hirabara SM, et al. Medium-chain dicarboxylic acylcarnitines as markers of n-3 PUFA-induced peroxisomal oxidation of fatty acids. Mol Nutr Food Res. 2015;59(8):1573-83. DOI:10.1002/mnfr.201400743
60. Cheng M, Bhujwalla ZM, Glunde K. Abstract 2120: Distinct molecular effects of chemotherapeutic agents on choline phospholipid metabolism of triple-negative breast cancer cells. Cancer Research. 2017;77(13_Supplement):2120-10. DOI:10.1158/1538-7445.am2017-2120
61. Bagnoli M, Granata A, Nicoletti R, et al. Choline Metabolism Alteration: A Focus on Ovarian Cancer. Front Oncol. 2016;6:153. DOI:10.3389/fonc.2016.00153
62. Glunde K, Penet MF, Jiang L, et al. Choline metabolism-based molecular diagnosis of cancer: an update. Expert Rev Mol Diagn. 2015;15(6):735-47. DOI:10.1586/14737159.2015.1039515
63. Wang X, Zhang J, Zheng K, et al. Discovering metabolic vulnerability using spatially resolved metabolomics for antitumor small molecule-drug conjugates development as a precise cancer therapy strategy. J Pharm Anal. 2023;13(7):776-87. DOI:10.1016/j.jpha.2023.02.010
64. Liu C, Liu D, Wang F, et al. Construction of a novel choline metabolism-related signature to predict prognosis, immune landscape, and chemotherapy response in colon adenocarcinoma. Front Immunol. 2022;13:1038927. DOI:10.3389/fimmu.2022.1038927
65. Choe CU, Lezius S, Cordts K, et al. Low homoarginine/SDMA ratio is associated with poor short- and long-term outcome after stroke in two prospective studies. Neurol Sci. 2020;41(1):149-53. DOI:10.1007/s10072-019-04058-0
66. Rodionov RN, Beyer-Westendorf J, Bode-Böger SM, et al. Homoarginine and methylarginines independently predict long-term outcome in patients presenting with suspicion of venous thromboembolism. Sci Rep. 2021;11(1):9569. DOI:10.1038/s41598-021-88986-y
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22. Khronicheskii limfotsitarnyi leikoz / limfoma iz malykh limfotsitov. Klinicheskie rekomendatsii. 2024. Available at: https://cr.minzdrav.gov.ru/view-cr/134_2. Accessed: 08.06.2025 (in Russian).
23. Limfoma marginal'noi zony. Klinicheskie rekomendatsii. 2023. Available at: https://cr.minzdrav.gov.ru/view-cr/137_2. Accessed: 08.06.2025 (in Russian).
24. Follikuliarnaia limfoma. Klinicheskie rekomendatsii. 2024. Available at: https://cr.minzdrav.gov.ru/view-cr/151_2. Accessed: 08.06.2025 (in Russian).
25. Limfoma Khodzhkina. Klinicheskie rekomendatsii. 2024. Available at: https://cr.minzdrav.gov.ru/view-cr/139_2. Accessed: 08.06.2025 (in Russian).
26. Agressivnye nefollikuliarnye limfomy – diffuznaia V-kletochnaia krupnokletochnaia limfoma, V-kletochnaia limfoma vysokoi stepeni zlokachestvennosti s perestroikoi genov c-MYC i BCL2/BCL6, pervichnaia mediastinal'naia V-kletochnaia limfoma, mediastinal'naia limfoma seroi zony, limfoma Berkitta, plazmoblastnaia limfoma. Klinicheskie rekomendatsii. 2024. Available at: https://cr.minzdrav.gov.ru/view-cr/129_3. Accessed: 08.06.2025 (in Russian).
27. Limfoma iz kletok mantii. Klinicheskie rekomendatsii. 2024. Available at: https://cr.minzdrav.gov.ru/view-cr/136_2. Accessed: 08.06.2025 (in Russian).
28. Baskhanova SN, Moskaleva NE, Shestakova KM, et al. Targeted metabolomics for cardiovascular disease: Validation of a high-throughput HPLC-MS/MS assay. J Chromatogr B Analyt Technol Biomed Life Sci. 2025;1264:124732. DOI:10.1016/j.jchromb.2025.124732
29. Kim M, Tomek P. Tryptophan: A Rheostat of Cancer Immune Escape Mediated by Immunosuppressive Enzymes IDO1 and TDO. Front Immunol. 2021;12:636081. DOI:10.3389/fimmu.2021.636081
30. Lu Z, Zhang C, Zhang J, et al. The Kynurenine Pathway and Indole Pathway in Tryptophan Metabolism Influence Tumor Progression. Cancer Med. 2025;14(6):e70703. DOI:10.1002/cam4.70703
31. Sordillo PP, Sordillo LA, Helson L. The Kynurenine Pathway: A Primary Resistance Mechanism in Patients with Glioblastoma. Anticancer Res. 2017;37(5):2159-71. DOI:10.21873/anticanres.11551
32. Basson C, Serem JC, Hlophe YN, Bipath P. The tryptophan-kynurenine pathway in immunomodulation and cancer metastasis. Cancer Med. 2023;12(18):18691-801. DOI:10.1002/cam4.6484
33. León-Letelier RA, Dou R, Vykoukal J, et al. The kynurenine pathway presents multi-faceted metabolic vulnerabilities in cancer. Front Oncol. 2023;13:1256769. DOI:10.3389/fonc.2023.1256769
34. Gouasmi R, Ferraro-Peyret C, Nancey S, et al. The Kynurenine Pathway and Cancer: Why Keep It Simple When You Can Make It Complicated. Cancers (Basel). 2022;14(11):2793. DOI:10.3390/cancers14112793
35. Sahm F, Oezen I, Opitz CA, et al. The endogenous tryptophan metabolite and NAD+ precursor quinolinic acid confers resistance of gliomas to oxidative stress. Cancer Res. 2013;73(11):3225-34. DOI:10.1158/0008-5472.CAN-12-3831
36. Navas LE, Carnero A. NAD(+) metabolism, stemness, the immune response, and cancer. Signal Transduct Target Ther. 2021;6(1):2. DOI:10.1038/s41392-020-00354-w
37. Ghanem MS, Caffa I, Monacelli F, Nencioni A. Inhibitors of NAD(+) Production in Cancer Treatment: State of the Art and Perspectives. Int J Mol Sci. 2024;25(4):2092. DOI:10.3390/ijms25042092
38. De Santo C, Booth S, Vardon A, et al. The arginine metabolome in acute lymphoblastic leukemia can be targeted by the pegylated-recombinant arginase I BCT-100. Int J Cancer. 2018;142(7):1490-502. DOI:10.1002/ijc.31170
39. Delage B, Luong P, Maharaj L, et al. Promoter methylation of argininosuccinate synthetase-1 sensitises lymphomas to arginine deiminase treatment, autophagy and caspase-dependent apoptosis. Cell Death Dis. 2012;3(7):e342. DOI:10.1038/cddis.2012.83
40. Ren Y, Fan L, Wang L, et al. SSRP1/SLC3A2 Axis in Arginine Transport: A New Target for Overcoming Immune Evasion and Tumor Progression in Peripheral T-Cell Lymphoma. Adv Sci (Weinh). 2025;12(21):e2415698. DOI:10.1002/advs.202415698
41. Puglisi F, Padella A, Parrinello NL, et al. Dissecting the Adaptive Response to Arginine Deprivation in Hodgkin Lymphoma. Blood. 2021;138(Suppl. 1):4497-47. DOI:10.1182/blood-2021-151006
42. Chung J, Karkhanis V, Baiocchi RA, Sif S. Protein arginine methyltransferase 5 (PRMT5) promotes survival of lymphoma cells via activation of WNT/β-catenin and AKT/GSK3β proliferative signaling. J Biol Chem. 2019;294(19):7692-710. DOI:10.1074/jbc.RA119.007640
43. Sauter C, Simonet J, Guidez F, et al. Protein Arginine Methyltransferases as Therapeutic Targets in Hematological Malignancies. Cancers (Basel). 2022;14(21):5443. DOI:10.3390/cancers14215443
44. Yao N, Li W, Xu G, et al. Choline metabolism and its implications in cancer. Front Oncol. 2023;13:1234887. DOI:10.3389/fonc.2023.1234887
45. Glunde K, Bhujwalla ZM, Ronen SM. Choline metabolism in malignant transformation. Nat Rev Cancer. 2011;11(12):835-48. DOI:10.1038/nrc3162
46. Glunde K, Ackerstaff E, Mori N, et al. Choline phospholipid metabolism in cancer: consequences for molecular pharmaceutical interventions. Mol Pharm. 2006;3(5):496-506. DOI:10.1021/mp060067e
47. Dobrijević D, Pastor K, Nastić N, et al. Betaine as a Functional Ingredient: Metabolism, Health-Promoting Attributes, Food Sources, Applications and Analysis Methods. Molecules. 2023;28(12):4824. DOI:10.3390/molecules28124824
48. Zhou C, Basnet R, Zhen C, et al. Trimethylamine N-oxide promotes the proliferation and migration of hepatocellular carcinoma cell through the MAPK pathway. Discov Oncol. 2024;15(1):346. DOI:10.1007/s12672-024-01178-8
49. Xie H, Zhang K, Wei Y, et al. The association of serum betaine concentrations with the risk of new-onset cancers: results from two independent nested case-control studies. Nutr Metab (Lond). 2023;20(1):46. DOI:10.1186/s12986-023-00755-y
50. Ninomiya S, Narala N, Huye L, et al. Tumor indoleamine 2,3-dioxygenase (IDO) inhibits CD19-CAR T cells and is downregulated by lymphodepleting drugs. Blood. 2015;125(25):3905-16. DOI:10.1182/blood-2015-01-621474
51. Zhang N, Huang Y, Wang G, et al. Metabolomics assisted by transcriptomics analysis to reveal metabolic characteristics and potential biomarkers associated with treatment response of neoadjuvant therapy with TCbHP regimen in HER2 + breast cancer. Breast Cancer Res. 2024;26(1):64. DOI:10.1186/s13058-024-01813-w
52. Yoneyama T, Abdul-Hadi K, Brown A, et al. A Citrulline-Based Translational Population System Toxicology Model for Gastrointestinal-Related Adverse Events Associated With Anticancer Treatments. CPT Pharmacometrics Syst Pharmacol. 2019;8(12):951-61. DOI:10.1002/psp4.12475
53. Zezulová M, Bartoušková M, Hlídková E, et al. Citrulline as a biomarker of gastrointestinal toxicity in patients with rectal carcinoma treated with chemoradiation. Clin Chem Lab Med. 2016;54(2):305-14. DOI:10.1515/cclm-2015-0326
54. Mehdizadeh A, Bonyadi M, Darabi M, et al. Common chemotherapeutic agents modulate fatty acid distribution in human hepatocellular carcinoma and colorectal cancer cells. Bioimpacts. 2017;7(1):31-9. DOI:10.15171/bi.2017.05
55. Dambrova M, Makrecka-Kuka M, Kuka J, et al. Acylcarnitines: Nomenclature, Biomarkers, Therapeutic Potential, Drug Targets, and Clinical Trials. Pharmacol Rev. 2022;74(3):506-51. DOI:10.1124/pharmrev.121.000408
56. Nowak C, Hetty S, Salihovic S, et al. Glucose challenge metabolomics implicates medium-chain acylcarnitines in insulin resistance. Sci Rep. 2018;8(1):8691. DOI:10.1038/s41598-018-26701-0
57. Davies A, Wenzl FA, Li XS, et al. Short and medium chain acylcarnitines as markers of outcome in diabetic and non-diabetic subjects with acute coronary syndromes. Int J Cardiol. 2023;389:131261. DOI:10.1016/j.ijcard.2023.131261
58. Koves TR, Zhang GF, Davidson MT, et al. Pyruvate-supported flux through medium-chain ketothiolase promotes mitochondrial lipid tolerance in cardiac and skeletal muscles. Cell Metab. 2023;35(6):1038-1056.e8. DOI:10.1016/j.cmet.2023.03.016
59. Fiamoncini J, Lima TM, Hirabara SM, et al. Medium-chain dicarboxylic acylcarnitines as markers of n-3 PUFA-induced peroxisomal oxidation of fatty acids. Mol Nutr Food Res. 2015;59(8):1573-83. DOI:10.1002/mnfr.201400743
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Авторы
В.Г. Варзиева*1, А.А. Болдин1, К.М. Шестакова1, С.Н. Басханова1, В.М. Самойлов1, И.С. Ильгисонис1, Ю.Ю. Кириченко1, Р.Р. Каримов1, Е.А. Смолярчук1, Д.А. Кудлай1–3, В.В. Тарасов1, Ю.Н. Беленков1, С.А. Апполонова1
1ФГАОУ ВО «Первый Московский государственный медицинский университет им. И.М. Сеченова» Минздрава России (Сеченовский Университет), Москва, Россия;
2ФГБОУ ВО «Московский государственный университет им. М.В. Ломоносова», Москва, Россия;
3ФГБУ «ГНЦ Институт иммунологии» Федерального медико-биологического агентства России, Москва, Россия
*varzieva.valeria@gmail.com
1Sechenov First Moscow State Medical University (Sechenov University), Moscow, Russia;
2Lomonosov Moscow State Univesity, Moscow, Russia;
3State Research Center Institute of Immunology, Moscow, Russia
*varzieva.valeria@gmail.com
1ФГАОУ ВО «Первый Московский государственный медицинский университет им. И.М. Сеченова» Минздрава России (Сеченовский Университет), Москва, Россия;
2ФГБОУ ВО «Московский государственный университет им. М.В. Ломоносова», Москва, Россия;
3ФГБУ «ГНЦ Институт иммунологии» Федерального медико-биологического агентства России, Москва, Россия
*varzieva.valeria@gmail.com
________________________________________________
1Sechenov First Moscow State Medical University (Sechenov University), Moscow, Russia;
2Lomonosov Moscow State Univesity, Moscow, Russia;
3State Research Center Institute of Immunology, Moscow, Russia
*varzieva.valeria@gmail.com
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