Значение ангиогенеза и лимфангиогенеза при раке желудка

   Проведен литературный поиск в базе данных PubMed для изучения работ, посвященных результатам исследований особенностей кровеносной и лимфатической васкуляризации рака желудка (РЖ). Гемангиогенез и лимфангиогенез в любой опухоли, в том числе и при РЖ, абсолютно необходимы для роста, инвазии и метастатического распространения. Опухолевый ангиогенез активируется гипоксией клеточных элементов, соответственно, в тканях РЖ возрастает содержание факторов, как индуцируемых гипоксией, так и связанных с ростом сосудов. Кроме того, некоторые лейкоциты, инфильтрирующие опухоль, принимают активное участие в ангиогенезе, также способствуя развитию и прогрессированию РЖ. Рост сосудов запускается не только в опухоли, но и в других отделах желудка. Ингибиторы ангиогенеза и роста лимфатических сосудов способствуют замедлению роста опухоли и подавляют метастазирование. К сожалению, остается неисследованным состояние сосудистого русла близлежащих органов, тогда как проангиогенные факторы распространяются по уже имеющимся кровеносным и лимфатическим сосудам и должны влиять на ангиогенез, как минимум, в печени и регионарных лимфатических узлах.

1. Bray F., Laversanne M., Sung H., Ferlay J., Siegel R.L., Soerjomataram I., Jemal A. Global cancer statistics 2022: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 2024;74(3):229–263. doi: 10.3322/caac.21834

2. Злокачественные новообразования в России в 2023 году (заболеваемость и смертность). Ред. А.Д. Каприн, В.В. Старинский, А.О. Шахзадова. М.: МНИОИ им. П.А. Герцена, 2024. 276 с.

3. van Cutsem E., Sagaert X., Topal B., Haustermans K., Prenen H. Gastric cancer. Lancet. 2016;388(10060):2654–2664. doi: 10.1016/S0140-6736(16)30354-3

4. Lott P.C., Carvajal-Carmona L.G. Resolving gastric cancer aetiology: an update in genetic predisposition. Lancet Gastroenterol. Hepatol. 2018;3(12):874–883. doi: 10.1016/S2468-1253(18)30237-1

5. Russo A.E., Strong V.E. Gastric cancer etiology and management in Asia and the West. Annu. Rev. Med. 2019;70:353–367. doi: 10.1146/annurev-med-081117-043436

6. Shi D.B., Ma R.R., Zhang H., Hou F., Guo X.Y., Gao P. GAGE7B promotes tumor metastasis and growth via activating the p38δ/pMAPKAPK2/pHSP27 pathway in gastric cancer. J. Exp. Clin. Cancer Res. 2019;38(1):124. doi: 10.1186/s13046-019-1125-z

7. Xue L., Chu W., Wan F., Wu P., Zhao X., Ma L., She Y., Li C., Li Y. YKL-39 is an independent prognostic factor in gastric adenocarcinoma and is associated with tumor-associated macrophage infiltration and angiogenesis. World J. Surg. Oncol. 2022;20(1):362. doi: 10.1186/s12957-022-02830-9

8. Qiu Y., Lu G., Li N., Hu Y., Tan H., Jiang C. Exosome-mediated communication between gastric cancer cells and macrophages: implications for tumor microenvironment. Front. Immunol. 2024;15:1327281. doi: 10.3389/fimmu.2024.1327281

9. Майбородин И.В., Гончаров М.А., Шевела А.И., Красильников С.Э., Шумейкина А.О., Майбородина В.И. Ангиогенез при раке эндометрия: клиническое и биологическое значение. Сиб. онкол. ж. 2024;23(4):172–185. doi: 10.21294/1814-4861-2024-23-4-172-185

10. Macedo F., Ladeira K., Longatto-Filho A., Martins S.F. Gastric cancer and angiogenesis: is VEGF a useful biomarker to assess progression and remission? J. Gastric Cancer. 2017;17(1):1–10. doi: 10.5230/jgc.2017.17.e1

11. Li N., Wang H.X., Qin C., Wang X.H., Han F.Y. Relationship between clinicopathological features and HIF-2α in gastric adenocarcinoma. Genet. Mol. Res. 2015;14(1):1404–1413. doi: 10.4238/2015.February.13.19

12. Ozmen M.M., Ozmen F., Zulfikaroglu B. Lymph nodes in gastric cancer. J. Surg. Oncol. 2008;98(6):476–481. doi: 10.1002/jso.21134

13. Mantovani A., Allavena P., Sica A., Balkwill F. Cancer-related inflammation. Nature. 2008; 454(7203):436–444. doi: 10.1038/nature07205

14. Hanahan D., Coussens L.M. Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell. 2012;21(3):309–322. doi: 10.1016/j.ccr.2012.02.022

15. Galdiero M.R., Garlanda C., Jaillon S., Marone G., Mantovani A. Tumor associated macrophages and neutrophils in tumor progression. J. Cell. Physiol. 2013;228(7):1404–1412. doi: 10.1002/jcp.24260

16. Varricchi G., Galdiero M.R., Marone G., Granata F., Borriello F., Marone G. Controversial role of mast cells in skin cancers. Exp. Dermatol. 2017;26(1):11–17. doi: 10.1111/exd.13107

17. Zhang L.X., Wei Z.J., Xu A.M., Zang J.H. Can the neutrophil-lymphocyte ratio and platelet-lymphocyte ratio be beneficial in predicting lymph node metastasis and promising prognostic markers of gastric cancer patients? Tumor maker retrospective study. Int. J. Surg. 2018;56:320–327. doi: 10.1016/j.ijsu.2018.06.037

18. Стадников А.А., Сеньчукова М.А., Шевлюк Н.Н., Боков Д.А. Морфологическая характеристика сосудов подслизистой основы желудка на участках, прилежащих к опухоли. Морфология. 2011;140(4):18–22.

19. Hafez N.H., Tahoun N.S. Expression of cyclooxygenase 2 and vascular endothelial growth factor in gastric carcinoma: Relationship with clinico-pathological parameters. J. Egypt. Natl. Canc. Inst. 2016;28(3):149–156. doi: 10.1016/j.jnci.2016.05.005

20. Ikeda K., Oki E., Saeki H., Ando K., Morita M., Oda Y., Imamura M., Kakeji Y., Maehara Y. Intratumoral lymphangiogenesis and prognostic significance of VEGFC expression in gastric cancer. Anticancer Res. 2014;34(8):3911–3915.

21. Li F., Meng G., Tan B., Chen Z., Ji Q., Wang X., Liu C., Niu S., Li Y., Liu Y. Relationship between HER2 expression and tumor interstitial angiogenesis in primary gastric cancer and its effect on prognosis. Pathol. Res. Pract. 2021;217:153280. doi: 10.1016/j.prp.2020.153280

22. Fan Z., Li Y., Zhao Q., Fan L., Tan B., Zuo J., Hua K., Ji Q. Highly expressed granulocyte colony-stimulating factor (G-CSF) and granulocyte colony-stimulating factor receptor (G-CSFR) in human gastric cancer leads to poor survival. Med. Sci. Monit. 2018;24:1701–1711. doi: 10.12659/msm.909128

23. Gao L.M., Wang F., Zheng Y., Fu Z.Z., Zheng L., Chen L.L. Roles of fibroblast activation protein and hepatocyte growth factor expressions in angiogenesis and metastasis of gastric cancer. Pathol. Oncol. Res. 2019;25(1):369–376. doi: 10.1007/s12253-017-0359-3

24. Yan Z., Yan Q., Song Y., Wang L. TMSB10, a potential prognosis prediction biomarker, promotes the invasion and angiogenesis of gastric cancer. J. Gastroenterol. Hepatol. 2021;36(11):3102–3112. doi: 10.1111/jgh.15576

25. Cao H., Li Y., Huang L., Bai B., Xu Z. Clinicopathological significance of neuropilin 1 expression in gastric cancer: a meta-analysis. Dis. Markers. 2020;2020:4763492. doi: 10.1155/2020/4763492

26. Tao X., Cheng L., Li Y., Ci H., Xu J., Wu S., Tao Y. Expression of CRYAB with the angiogenesis and poor prognosis for human gastric cancer. Medicine (Baltimore). 2019;98(45):e17799. doi: 10.1097/MD.0000000000017799

27. Liu W., Zhang Q., Zhang Y., Sun L., Xiao H., Luo B. Epstein–Barr virus regulates endothelin-1 expression through the ERK/FOXO1 pathway in EBV-associated gastric cancer. Microbiol. Spectr. 2023;11(1):e0089822. doi: 10.1128/spectrum.00898-22

28. Pak K.H., Park K.C., Cheong J.H. VEGF-C induced by TGF- β1 signaling in gastric cancer enhances tumor-induced lymphangiogenesis. BMC Cancer. 2019;19(1):799. doi: 10.1186/s12885-019-5972-y

29. Xia Y.J., Jiang X.T., Jiang S.B., He X.J., Luo J.G., Liu Z.C., Wang L., Tao H.Q., Chen J.Z. PHD3 affects gastric cancer progression by negatively regulating HIF1A. Mol. Med. Rep. 2017;16(5):6882–6889. doi: 10.3892/mmr.2017.7455

30. Ma C., Luo C., Yin H., Zhang Y., Xiong W., Zhang T., Gao T., Wang X., Che D., Fang Z., … Yang X. Kallistatin inhibits lymphangiogenesis and lymphatic metastasis of gastric cancer by downregulating VEGF-C expression and secretion. Gastric Cancer. 2018;21(4):617–631. doi: 10.1007/s10120-017-0787-5

31. Park J.Y., Sung J.Y., Lee J., Park Y.K., Kim Y.W., Kim G.Y., Won K.Y., Lim S.J. Polarized CD163+ tumor-associated macrophages are associated with increased angiogenesis and CXCL12 expression in gastric cancer. Clin. Res. Hepatol. Gastroenterol. 2016;40(3):357–365. doi: 10.1016/j.clinre.2015.09.005

32. Wu H., Xu J.B., He Y.L., Peng J.J., Zhang X.H., Chen C.Q., Li W., Cai S.R. Tumor-associated macrophages promote angiogenesis and lymphangiogenesis of gastric cancer. J. Surg. Oncol. 2012;106(4):462–468. doi: 10.1002/jso.23110

33. Hiramatsu S., Tanaka H., Nishimura J., Sakimura C., Tamura T., Toyokawa T., Muguruma K., Yashiro M., Hirakawa K., Ohira M. Neutrophils in primary gastric tumors are correlated with neutrophil infiltration in tumor-draining lymph nodes and the systemic inflammatory response. BMC Immunol. 2018;19(1):13. doi: 10.1186/s12865-018-0251-2

34. Ammendola M., Sacco R., Donato G., Zuccalà V., Russo E., Luposella M., Vescio G., Rizzuto A., Patruno R., de Sarro G., … Ranieri G. Mast cell positivity to tryptase correlates with metastatic lymph nodes in gastrointestinal cancer patients treated surgically. Oncology. 2013;85(2):111–116. doi: 10.1159/000351145

35. Ammendola M., Sacco R., Zuccalà V., Luposella M., Patruno R., Gadaleta P., Zizzo N., Gadaleta C.D., de Sarro G., Sammarco G., Oltean M., Ranieri G. Mast cells density positive to tryptase correlate with microvascular density in both primary gastric cancer tissue and loco-regional lymph node metastases from patients that have undergone radical surgery. Int. J. Mol. Sci. 2016;17(11):1905. doi: 10.3390/ijms17111905

36. Lotfi-Emran S., Ward B.R., Le Q.T., Pozez A.L., Manjili M.H., Woodfolk J.A., Schwartz L.B. Human mast cells present antigen to autologous CD4+ T cells. J. Allergy Clin. Immunol. 2018;141(1):311–321.e10. doi: 10.1016/j.jaci.2017.02.048

37. Kritikou E., van der Heijden T., Swart M., van Duijn J., Slütter B., Wezel A., Smeets H.J., Maffia P., Kuiper J., Bot I. Hypercholesterolemia induces a mast Cell-CD4+ T cell interaction in atherosclerosis. J. Immunol. 2019;202(5):1531–1539. doi: 10.4049/jimmunol.1800648

38. Dawson M.A., Kouzarides T., Huntly B.J. Targeting epigenetic readers in cancer. N. Engl. J. Med. 2012;367(7):647–657. doi: 10.1056/NEJMra1112635

39. Yao J., Da M., Guo T., Duan Y., Zhang Y. RNAi-mediated gene silencing of vascular endothelial growth factor-C inhibits tumor lymphangiogenesis and growth of gastric cancer in vivo in mice. Tumour Biol. 2013;34(3):1493–1501. doi: 10.1007/s13277-013-0674-6

40. Liu P., Ding P., Yang J., Wu H., Wu J., Guo H., Yang P., Tian Y., Meng L., Zhao Q. MicroRNA-431-5p inhibits angiogenesis, lymphangiogenesis, and lymph node metastasis by affecting TGF-β1/SMAD2/3 signaling via ZEB1 in gastric cancer. Mol. Carcinog. 2024;63(7):1378–1391. doi: 10.1002/mc.23731

41. Liu H.T., Ma R.R., Lv B.B., Zhang H., Shi D.B., Guo X.Y., Zhang G.H., Gao P. LncRNA-HNF1A-AS1 functions as a competing endogenous RNA to activate PI3K/AKT signalling pathway by sponging miR-30b-3p in gastric cancer. Br. J. Cancer. 2020;122(12):1825–1836. doi: 10.1038/s41416-020-0836-4

42. Sammarco G., Varricchi G., Ferraro V., Ammendola M., de Fazio M., Altomare D.F., Luposella M., Maltese L., Currò G., Marone G., Ranieri G., Memeo R. Mast cells, angiogenesis and lymphangiogenesis in human gastric cancer. Int. J. Mol. Sci. 2019;20(9):2106. doi: 10.3390/ijms20092106

43. Tapia O., Riquelme I., Leal P., Sandoval A., Aedo S., Weber H., Letelier P., Bellolio E., Villaseca M., Garcia P., Roa J.C. The PI3K/AKT/mTOR pathway is activated in gastric cancer with potential prognostic and predictive significance. Virchows Arch. 2014;465(1):25–33. doi: 10.1007/s00428-014-1588-4

44. Xing X., Zhang L., Wen X., Wang X., Cheng X., Du H., Hu Y., Li L., Dong B., Li Z., Ji J. PP242 suppresses cell proliferation, metastasis, and angiogenesis of gastric cancer through inhibition of the PI3K/AKT/mTOR pathway. Anticancer Drugs. 2014;25(10):1129–1140. doi: 10.1097/CAD.0000000000000148

45. Ma J., Yao S., Li X.S., Kang H.R., Yao F.F., Du N. Neoadjuvant therapy of DOF regimen plus bevacizumab can increase surgical resection ratein locally advanced gastric cancer: a randomized, controlled study. Medicine (Baltimore). 2015;94(42):e1489. doi: 10.1097/MD.0000000000001489

46. Takeuchi T., Yuasa Y., Okitsu H., Maki H., Tsuneki T., Matsuo Y., Edagawa H., Mori O., Miyamoto N., Eto S. … Ishikura H. Effectiveness of ramucirumab therapy for advanced gastric cancer after stent placement for esophagogastric junction carcinoma obstruction-a case report. Gan To Kagaku Ryoho. 2019;46(6):1057–1059.

47. Mori K., Aoyama T., Morita J., Maezawa Y., Amano S., Sawazaki S., Numata M., Tamagawa H., Sato T., Oshima T., … Rino Y. Gastrectomy for bleeding gastric cancer during ramucirumab plus paclitaxel therapy – a case report. Gan To Kagaku Ryoho. 2019;46(3):586–588.

48. Kurihara M., Sawazaki S., Kawabe T., Minowa K., Akimoto N., Tsuchiya K., Kato A., Higuchi A., Rino Y., Matsukawa H., Saeki H. A case of perforation of the diverticulum of the appendix during chemotherapy with ramucirumab plus nab-paclitaxel for gastric cancer. Gan To Kagaku Ryoho. 2021;48(10):1293–1295.

49. Wang J., Dong X., Li D., Fang Z., Wan X, Liu J. Fucoxanthin inhibits gastric cancer lymphangiogenesis and metastasis by regulating Ran expression. Phytomedicine. 2023;118:154926. doi: 10.1016/j.phymed.2023.154926