urmjУральский медицинский журналUral Medical Journal2949-4389Ural State Medical University10.52420/2071-5943-2023-22-2-56-64urmj-1228Research ArticleОригинальные статьи | Original articlesOriginal articlesПрогностическое значение макрофагальной васкулоподобной мимикрии в оценке прогрессирования увеальной меланомыPrognostic value of macrophage vasculiform mimicry in the evaluation of uveal melanoma progressionhttps://orcid.org/0000-0002-9280-0608ШамановаА. Ю.ShamanovaA. Y.

Анна Юрьевна Шаманова − кандидат медицинских наук

Челябинск

Anna Yu. Shamanova – Ph.D. in medicine

Chelyabinsk

anna-sha@bk.ruhttps://orcid.org/0000-0002-4512-3421КазачковЕ. Л.KazachkovE. L.

Евгений Леонидович Казачков − доктор медицинских наук, профессор

Челябинск

Evgenij L. Kazachkov – Doctor of Science (Medicine), Professor

Chelyabinsk

doctorkel@mail.ruПановаИ. Е.PanovaI. E.

Ирина Евгеньевна Панова − доктор медицинских наук, профессор

Санкт-Петербург

Irina E. Panova – Doctor of Science (Medicine), Professor

St. Petersburg

eyeren@mail.ruСаевецВ. В.SaevetsV. V.

Валерия Владимировна Саевец – кандидат медицинских наук

Челябинск

Valeriya V. Saevets – Ph.D. in medicine

Chelyabinsk

lalili2013@mail.ruhttps://orcid.org/0000-0002-5162-525XЯринаЛ. В.YarinaL. V.

Любовь Владимировна Ярина – ординатор

Челябинск

Lyubov’ V. Yarina – Ph.D. in pedagogical

Chelyabinsk

yarina.lubov98@gmail.comhttps://orcid.org/0000-0001-6327-2685ШамаеваТ. Н.ShamaevaT. N.

Татьяна Николаевна Шамаева – кандидат педагогических наук

Челябинск

Tat’yana N. Shamaeva – Ph.D. in medicine

Chelyabinsk

shamtan@mail.ruhttps://orcid.org/0000-0001-5550-4466ВласоваВ. М.VlasovaV. M.

Вероника Михайловна Власова – студент

Челябинск

Veronika M. Vlasova – Student

Chelyabinsk

vvlasova02@mail.ruЮжно-Уральский государственный медицинский университет; Челябинский областной клинический центр онкологии и ядерной медициныРоссияSouth-Ural State Medical University; Chelyabinsk regional clinical center of Oncology and nuclear medicineRussian FederationЮжно-Уральский государственный медицинский университетРоссияSouth-Ural State Medical UniversityRussian FederationСПб филиал НМИЦ МНТК «Микрохирургия глаза» им. акад. С.Н. ФедороваРоссияSt. Petersburg branch of S.N. Fyodorov Eye Microsurgery ClinicRussian Federation2023290420232225664Copyright © Шаманова А.Ю., Казачков Е.Л., Панова И.Е., Саевец В.В., Ярина Л.В., Шамаева Т.Н., Власова В.М., 20232023Шаманова А.Ю., Казачков Е.Л., Панова И.Е., Саевец В.В., Ярина Л.В., Шамаева Т.Н., Власова В.М.Shamanova A.Y., Kazachkov E.L., Panova I.E., Saevets V.V., Yarina L.V., Shamaeva T.N., Vlasova V.M.Данная работа распространяется под лицензией Creative Commons Attribution 4.0.This work is licensed under a Creative Commons Attribution 4.0 License.https://www.umjusmu.ru/jour/article/view/1228Введение

Введение. Увеальная меланома (УМ) – злокачественное новообразование сосудистого тракта глаза, склонное к гематогенному метастазированию вне зависимости от вида проведенного лечения. Прогнозирование и предотвращение метастазирования УМ является одной из главных задач онкоофтальмологии. Описан альтернативный способ кровоснабжения опухоли за счет процесса васкулоподобной мимикрии (ВМ) с формированием псевдососудистых структур клетками опухоли. При этом участие микроокружения опухоли в процессах ВМ и метастазирования на сегодняшний день является дискуссионным и актуальным.

Цель работы − оценить прогностическую роль макрофагальной васкулоподобной мимикрии в прогрессировании меланомы хориоидеи на основе гистологической и иммуногистохимической характеристики операционного материала.

Материалы и методы

Материалы и методы. Исследован операционный материал меланомы хориоидеи после энуклеации за период 2013-2018 гг. Проведено гистологическое, гистохимическое (PAS-реакция) и иммуногистохимическое исследование с использованием маркеров CD68 (Macrophage), СD 34, СD31, D2-40 с целью качественной и количественной оценки макрофагов в строме опухоли, кровеносных сосудов и псевдососудов в опухоли.

Результаты

Результаты. Обнаружена и описана способность макрофагов к формированию васкулоподобных пространств в меланоме хориоидеи. В опухоли с метастазами статистически значимо больше представительство макрофагов, чем в тканевых образцах неметастазирующей меланомы. Между объемной плотностью сосудов и количеством макрофагов была зарегистрирована обратная средняя по силе корреляционная связь. В группе исследования с метастазами статистически значимо больше преобладает объемная плотность псевдососудистых пространств и количества макрофагов.

Обсуждение

Обсуждение. Макрофагальное микроокружение в опухоли может играть двойственную роль: противоопухолевую и проопухолевую. Описана способность макрофагов к васкулоподобной мимикрии в меланомах хориоидеи. Результаты нашего исследования подтверждают проопухолевую активность макрофагов и важную роль в метастазировании опухоли.

Заключение

Заключение. Углубленное исследование путей формирования псевдососудистых пространств не только клетками самой опухоли, но и её микроокружением, помогает открыть новые направления в исследовании предикторов метастазирования УМ и наметить подходы к разработке новых направлений противоопухолевой терапии.

Introduction Uveal melanoma (UM) is a malignant neoplasm of the vascular tract of the eye, prone to hematogenous metastasis, regardless of the type of treatment performed. Prediction and probability of UM metastasis is one of the main tasks of onco-ophthalmology. We decribed an alternative method of tumor blood supply due to the process of vasculo-like mimicry (VM) with the formation of pseudovascular structures of tumor cells is described. At the same time, the participation of the microenvironment in the processes of VM and metastasis is currently debatable and relevant.

Purpose of the work was to evaluate the prognostic role of macrophage vasculiform mimicry in the progression of chorioid melanoma based on the histological and immunohistochemical characteristics of surgical material.

Materials and methods The surgical material of choroidal melanoma after enucleation for the period 2013-2018 was studied. Histological, histochemical (PAS reaction) and immunohistochemical studies were carried out using markers CD68 (macrophages), CD 34, CD31, D2-40 for the purpose of qualitative and quantitative assessment of macrophages in the stroma of tumors, large vessels and pseudovessels in the tumor.

Results The ability of macrophages to form vasculo-like spaces in choroidal melanoma has been discovered and described. In growth with macrometastases, more phage representatives are recorded than in tissue samples of non-metastasizing melanoma. the volume of the macroscopic mass of the ulcer and the growth rate of phages were registered as the inverse average in terms of the strength of the correlation. In group studies with metastases, an increase in the volume of pseudovascular volumes and the number of phages is recorded.

Discussion The macrophage microenvironment in a tumor can play a dual role: antitumor and protumor. The ability of macrophages for VM in UM has been described. The results of our macrostudy confirm the protumor activity of phages and their important role in tumor metastasis.

Conclusion In-depth study of the ways of pseudovascular space formation not only by the cells of the tumor itself, but also by its microenvironment, helps to open new directions in the study of predictors of UM metastasis and outline approaches to the development of new directions of anti-tumortherapy.

меланома хориоидеимакрофагальная васкулоподобная мимикриямакрофагиchoroid melanomamacrophage vasculature-like mimicrymacrophagesReferencesGrossniklaus HE, Eberhart CG, Kivela TT. WHO Classification of tumours of the eye. 4th edition. Lyon : IARC; 2018 pp. 87−93.Grossniklaus HE, Eberhart CG, Kivela TT. WHO Classification of tumours of the eye. 4th edition. Lyon : IARC; 2018 pp. 87−93.Folberg R, Rummelt V, Parys-Van Ginderdeuren R et al. The prognostic value of tumor blood vessel morphology in primary uveal melanoma. Ophthalmology 1993;100(9):1389–1398. https://doi.org/10.1016/s0161-6420(93)31470-3.Folberg R, Rummelt V, Parys-Van Ginderdeuren R et al. The prognostic value of tumor blood vessel morphology in primary uveal melanoma. Ophthalmology 1993;100(9):1389–1398. https://doi.org/10.1016/s0161-6420(93)31470-3.Mäkitie T, Summanen P, Tarkkanen A, Kivelä T. Microvascular loops and networks as prognostic indicators in choroidal and ciliary body melanomas. J Natl Cancer Inst 1999; 91(4):359−367. https://doi.org/10.1093/jnci/91.4.359.Mäkitie T, Summanen P, Tarkkanen A, Kivelä T. Microvascular loops and networks as prognostic indicators in choroidal and ciliary body melanomas. J Natl Cancer Inst 1999; 91(4):359−367. https://doi.org/10.1093/jnci/91.4.359.Mäkitie T, Summanen P, Tarkkanen A, Kivelä T. Microvascular density in predicting survival of patients with choroidal and ciliary body melanoma. Invest Ophthalmol Vis Sci 1999;40(11):2471−2480.Mäkitie T, Summanen P, Tarkkanen A, Kivelä T. Microvascular density in predicting survival of patients with choroidal and ciliary body melanoma. Invest Ophthalmol Vis Sci 1999;40(11):2471−2480.Chen X, Maniotis AJ, Majumdar D et al. Uveal melanoma cell staining for CD34 and assessment of tumor vascularity. Invest Ophthalmol Vis Sci 2002;43(8):2533−2539.Chen X, Maniotis AJ, Majumdar D et al. Uveal melanoma cell staining for CD34 and assessment of tumor vascularity. Invest Ophthalmol Vis Sci 2002;43(8):2533−2539.Foss AJ, Alexander RA, Jefferies LW et al. Microvessel count predicts survival in uveal melanoma. Cancer Res 1996;56(13):2900−2903.Foss AJ, Alexander RA, Jefferies LW et al. Microvessel count predicts survival in uveal melanoma. Cancer Res 1996;56(13):2900−2903.Sun W, Shen ZY, Zhang H et al. Overexpression of HIF-1α in primary gallbladder carcinoma and its relation to vasculogenic mimicry and unfavourable prognosis. Oncol Rep 2012;27(6):1990–2002. https://doi.org/10.3892/or.2012.1746.Sun W, Shen ZY, Zhang H et al. Overexpression of HIF-1α in primary gallbladder carcinoma and its relation to vasculogenic mimicry and unfavourable prognosis. Oncol Rep 2012;27(6):1990–2002. https://doi.org/10.3892/or.2012.1746.Liu K, Sun B, Zhao X et al. Hypoxia induced epithelial-mesenchymal transition and vasculogenic mimicry formation by promoting Bcl-2/Twist1 cooperation. Exp Mol Pathol 2015;99(2):383−391. https://doi.org/10.1016/j.yexmp.2015.08.009.Liu K, Sun B, Zhao X et al. Hypoxia induced epithelial-mesenchymal transition and vasculogenic mimicry formation by promoting Bcl-2/Twist1 cooperation. Exp Mol Pathol 2015;99(2):383−391. https://doi.org/10.1016/j.yexmp.2015.08.009.Zhou TJ, Huang XH, Gong L, Xiang L. Vasculogenic mimicry and hypoxia-inducible factor-1alpha expression in cervical squamous cell carcinoma. Genet Mol Res 2016;15(1):15017396. https://doi.org/10.4238/gmr.15017396.Zhou TJ, Huang XH, Gong L, Xiang L. Vasculogenic mimicry and hypoxia-inducible factor-1alpha expression in cervical squamous cell carcinoma. Genet Mol Res 2016;15(1):15017396. https://doi.org/10.4238/gmr.15017396.Lim D, Do Y, Kwon BS et al. Angiogenesis and vasculogenic mimicry as therapeutic targets in ovarian cancer. BMB reports. 2020;53(6):291−298. https://doi.org/10.5483/BMBRep.2020.53.6.060.Lim D, Do Y, Kwon BS et al. Angiogenesis and vasculogenic mimicry as therapeutic targets in ovarian cancer. BMB reports. 2020;53(6):291−298. https://doi.org/10.5483/BMBRep.2020.53.6.060.Park Y, Kim J. Regulation of IL-6 signaling by miR-125a and let-7e in endothelial cells controls vasculogenic mimicry formation of breast cancer cells. BMB Rep 2019;52(3):214−219. https://doi.org/10.5483/BMBRep.2019.52.3.308.Park Y, Kim J. Regulation of IL-6 signaling by miR-125a and let-7e in endothelial cells controls vasculogenic mimicry formation of breast cancer cells. BMB Rep 2019;52(3):214−219. https://doi.org/10.5483/BMBRep.2019.52.3.308.Williamson SC, Metcalf RL, Trapani F et al. Vasculogenic mimicry in small cell lung cancer. Nat Commun 2016;7:13322. https://doi.org/10.1038/ncomms13322.Williamson SC, Metcalf RL, Trapani F et al. Vasculogenic mimicry in small cell lung cancer. Nat Commun 2016;7:13322. https://doi.org/10.1038/ncomms13322.Cong R, Sun Q, Yang L et al. Effect of Genistein on vasculogenic mimicry formation by human uveal melanoma cells. J Exp Clin Cancer Res 2009;28(1):124. https://doi.org/10.1186/1756-9966-28-124.Cong R, Sun Q, Yang L et al. Effect of Genistein on vasculogenic mimicry formation by human uveal melanoma cells. J Exp Clin Cancer Res 2009;28(1):124. https://doi.org/10.1186/1756-9966-28-124.Maniotis AJ, Folberg R, Hess A et al. Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am J Pathol 1999;155(3):739−752. https://doi.org/10.1016/S0002-9440(10)65173-5.Maniotis AJ, Folberg R, Hess A et al. Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am J Pathol 1999;155(3):739−752. https://doi.org/10.1016/S0002-9440(10)65173-5.Райхлин Н.Т., Букаева И.А., Смирнова Е.А. с соавт. Пролиферативная активность, степень злокачественности и прогноз при карциноидных опухолях легких. Вестник РОНЦ им. Н. Н. Блохина РАМН. 2012;23(4):17–24.Rajhlin NT, Bukaeva IA, Smirnova EA et al. Proliferative activity, degree of malig-nancy and prognosis in lung carcinoid tumors. Bulletin of the N. N. Blokhin Russian Research Center of the Russian Academy of Sciences = Vestnik RONC im. N. N. Blohina RAMN 2012;23(4):17–24. (In Russ.).Черданцева Т.М., Бобров И.П., Климачев В.В. Патоморфология перитуморозной зоны при раке почки разной степени злокачественности. Медицина в Кузбассе 2012;11(1):27–31.Cherdanceva TM, Bobrov IP, Klimachev VV. Pathomorphology of the peritumorous zone in kidney cancer of varying degrees of malignancy. Medicine in Kuzbass = Medicina v Kuzbasse 2012;11(1):27–31. (In Russ.).Stei MM, Loeffler KU, Kurts C et al. Impact of macrophages on tumor growth characteristics in a murine ocular tumor model. Exp Eye Res 2016;151:9–18. https://doi.org/10.1016/j.exer.2016.07.008.Stei MM, Loeffler KU, Kurts C et al. Impact of macrophages on tumor growth characteristics in a murine ocular tumor model. Exp Eye Res 2016;151:9–18. https://doi.org/10.1016/j.exer.2016.07.008.Makitie T, Summanen P, Tarkkanen A, Kivelä T. Tumor-infiltrating macrophages (CD68(+) cells) and prognosis in malignant uveal melanoma. Invest Ophthalmol Vis Sci 2001;42(7):1414−1421.Makitie T, Summanen P, Tarkkanen A, Kivelä T. Tumor-infiltrating macrophages (CD68(+) cells) and prognosis in malignant uveal melanoma. Invest Ophthalmol Vis Sci 2001;42(7):1414−1421.Barnett FH, Rosenfeld М, Wood М et al. Macrophages form functional vascular mimicry channels in vivo. Sci Rep 2016;6:36659. https://doi.org/10.1038/srep36659.Barnett FH, Rosenfeld М, Wood М et al. Macrophages form functional vascular mimicry channels in vivo. Sci Rep 2016;6:36659. https://doi.org/10.1038/srep36659.Foss AJ, Alexander RA, Hungerford JL et al. Reassessment of the PAS patterns in uveal melanoma. Br J Ophthalmol 1997;81(3):240–248. https://doi.org/10.1136/bjo.81.3.240.Foss AJ, Alexander RA, Hungerford JL et al. Reassessment of the PAS patterns in uveal melanoma. Br J Ophthalmol 1997;81(3):240–248. https://doi.org/10.1136/bjo.81.3.240.Bouck N, Stellmach V, Hsu SC. How tumors become angiogenic. Adv Cancer Res 1996;69:135−174. https://doi.org/10.1016/s0065-230x(08)60862-3.Bouck N, Stellmach V, Hsu SC. How tumors become angiogenic. Adv Cancer Res 1996;69:135−174. https://doi.org/10.1016/s0065-230x(08)60862-3.Folkman J, Watson K, Ingber D, Hanahan D. Induction of angiogenesis during the transition from hyperplasia to neoplasia. Nature 1989;339(6219):58–61. https://doi.org/10.1038/339058a0.Folkman J, Watson K, Ingber D, Hanahan D. Induction of angiogenesis during the transition from hyperplasia to neoplasia. Nature 1989;339(6219):58–61. https://doi.org/10.1038/339058a0.Hanahan D, Folkman J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 1996;86(3):353–364. https://doi.org/10.1016/s0092-8674(00)80108-7.Hanahan D, Folkman J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 1996;86(3):353–364. https://doi.org/10.1016/s0092-8674(00)80108-7.Folberg R, Mehaffey M, Gardner LM et al. The microcirculation of choroidal and ciliary body melanomas. Eye 1997;11(2):227–238. https://doi.org/10.1038/eye.1997.57.Folberg R, Mehaffey M, Gardner LM et al. The microcirculation of choroidal and ciliary body melanomas. Eye 1997;11(2):227–238. https://doi.org/10.1038/eye.1997.57.De Palma M, Biziato D, Petrova TV. Microenvironmental regulation of tumour angiogenesis. Nat Rev Cancer 2017;17:457−474. https://doi.org/10.1038/nrc.2017.51.De Palma M, Biziato D, Petrova TV. Microenvironmental regulation of tumour angiogenesis. Nat Rev Cancer 2017;17:457−474. https://doi.org/10.1038/nrc.2017.51.Shibuya M. Vascular endothelial growth factor-dependent and independent regulation of angiogenesis. BMB Rep 2008;41(4):278−286. https://doi.org/10.5483/bmbrep.2008.41.4.278.Shibuya M. Vascular endothelial growth factor-dependent and independent regulation of angiogenesis. BMB Rep 2008;41(4):278−286. https://doi.org/10.5483/bmbrep.2008.41.4.278.Ribatti D, Annese T, Ruggieri S et al. Limitations of anti-angiogenic treatment of tumors. Transl Oncol 2019;12(7):981−986. https://doi.org/10.1016/j.tranon.2019.04.022.Ribatti D, Annese T, Ruggieri S et al. Limitations of anti-angiogenic treatment of tumors. Transl Oncol 2019;12(7):981−986. https://doi.org/10.1016/j.tranon.2019.04.022.Dunleavey JM, Dudley AC. Vascular mimicry: concepts and implications for anti-angiogenic therapy. Curr Angiogenes 2012;1(2):133–138. https://doi.org/10.2174/2211552811201020133.Dunleavey JM, Dudley AC. Vascular mimicry: concepts and implications for anti-angiogenic therapy. Curr Angiogenes 2012;1(2):133–138. https://doi.org/10.2174/2211552811201020133.Maniotis AJ, Folberg R, Hess A et al. Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am J Pathol 1999;155(3):739−752. https://doi.org/10.1016/S0002-9440(10)65173-5.Maniotis AJ, Folberg R, Hess A et al. Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am J Pathol 1999;155(3):739−752. https://doi.org/10.1016/S0002-9440(10)65173-5.Sierra JR, Corso S, Caione L et al. Tumor angiogenesis and progression are enhanced by Sema4D produced by tumorassociated macrophages. J Exp Med 2008;205(7):1673−1685. https://doi.org/10.1084/jem.20072602.Sierra JR, Corso S, Caione L et al. Tumor angiogenesis and progression are enhanced by Sema4D produced by tumorassociated macrophages. J Exp Med 2008;205(7):1673−1685. https://doi.org/10.1084/jem.20072602.Chen P, Huang Y, Bong R et al. Tumor-associated macrophages promote angiogenesis and melanoma growth via adrenomedullin in a paracrine and autocrine manner. Clin Cancer Res 2011;17(23):7230−7239. https://doi.org/10.1158/1078-0432.CCR-11-1354.Chen P, Huang Y, Bong R et al. Tumor-associated macrophages promote angiogenesis and melanoma growth via adrenomedullin in a paracrine and autocrine manner. Clin Cancer Res 2011;17(23):7230−7239. https://doi.org/10.1158/1078-0432.CCR-11-1354.Torisu H, Ono M, Kiryu H et al. Macrophage infiltration correlates with tumor stage and angiogenesis in human malignant melanoma: possible involvement of TNFalpha and IL-1alpha. Int J Cancer 2000;85(2):182–188.Torisu H, Ono M, Kiryu H et al. Macrophage infiltration correlates with tumor stage and angiogenesis in human malignant melanoma: possible involvement of TNFalpha and IL-1alpha. Int J Cancer 2000;85(2):182–188.Hong TM, Teng LJ, Shun CT et al. Induced interleukin-8 expression in gliomas by tumor-associated macrophages. J Neurooncol 2009;93(3):289−301. https://doi.org/10.1007/s11060-008-9786-z.Hong TM, Teng LJ, Shun CT et al. Induced interleukin-8 expression in gliomas by tumor-associated macrophages. J Neurooncol 2009;93(3):289−301. https://doi.org/10.1007/s11060-008-9786-z.Cao Z, Bao M, Miele L et al. Tumour vasculogenic mimicry is associated with poor prognosis of human cancer patients: a systemic review and meta-analysis. Eur J Cancer 2013;49(18):3914–3923. https://doi.org/10.1016/j.ejca.2013.07.148.Cao Z, Bao M, Miele L et al. Tumour vasculogenic mimicry is associated with poor prognosis of human cancer patients: a systemic review and meta-analysis. Eur J Cancer 2013;49(18):3914–3923. https://doi.org/10.1016/j.ejca.2013.07.148.Cao Z, Shang B, Zhang G et al. Tumor cell-mediated neovascularization and lymphangiogenesis contrive tumor progression and cancer metastasis. Biochim Biophys Acta 2013;1836(2):273−286. https://doi.org/10.1016/j.bbcan.2013.08.001.Cao Z, Shang B, Zhang G et al. Tumor cell-mediated neovascularization and lymphangiogenesis contrive tumor progression and cancer metastasis. Biochim Biophys Acta 2013;1836(2):273−286. https://doi.org/10.1016/j.bbcan.2013.08.001.Angara K, Borin TF, Arbab AS. Vascular mimicry: A novel neovascularization mechanism driving anti-angiogenic therapy (AAT) resistance in glioblastoma. Transl Oncol 2017;10(4):650−660. https://doi.org/10.1016/j.tranon.2017.04.007.Angara K, Borin TF, Arbab AS. Vascular mimicry: A novel neovascularization mechanism driving anti-angiogenic therapy (AAT) resistance in glioblastoma. Transl Oncol 2017;10(4):650−660. https://doi.org/10.1016/j.tranon.2017.04.007.Liu Q, Qiao L, Liang N et al. The relationship between vasculogenic mimicry and epithelial-mesenchymal transitions. J Cell Mol Med 2016;20(9):1761-1769. https://doi.org/10.1111/jcmm.12851.Liu Q, Qiao L, Liang N et al. The relationship between vasculogenic mimicry and epithelial-mesenchymal transitions. J Cell Mol Med 2016;20(9):1761-1769. https://doi.org/10.1111/jcmm.12851.Sun H, Yao N, Cheng S et al. Cancer stem-like cells directly participate in vasculogenic mimicry channels in triple-negative breast cancer. Cancer Biol Med 2019;16(2):299−311. https://doi.org/10.20892/j.issn.2095-3941.2018.0209.Sun H, Yao N, Cheng S et al. Cancer stem-like cells directly participate in vasculogenic mimicry channels in triple-negative breast cancer. Cancer Biol Med 2019;16(2):299−311. https://doi.org/10.20892/j.issn.2095-3941.2018.0209.Delgado-Bellido D, Serrano-Saenz S, Fernández-Cortés M, Oliver FJ. Vasculogenic mimicry signaling revisited: focus on non-vascular VE-cadherin. Mol Cancer 2017;16(1):65. https://doi.org/10.1186/s12943-017-0631-x.Delgado-Bellido D, Serrano-Saenz S, Fernández-Cortés M, Oliver FJ. Vasculogenic mimicry signaling revisited: focus on non-vascular VE-cadherin. Mol Cancer 2017;16(1):65. https://doi.org/10.1186/s12943-017-0631-x.Denton AE, Roberts EW, Fearon DT. Stromal Cells in the Tumor Microenvironment. Adv Exp Med Biol 2018;1060:99−114. https://doi.org/10.1007/978-3-319-78127-3_6.Denton AE, Roberts EW, Fearon DT. Stromal Cells in the Tumor Microenvironment. Adv Exp Med Biol 2018;1060:99−114. https://doi.org/10.1007/978-3-319-78127-3_6.Tsai YM, Wu KL, Liu YW et al. Cooperation Between Cancer and Fibroblasts in Vascular Mimicry and N2-Type Neutrophil Recruitment via Notch2-Jagged1 Interaction in Lung Cancer. Front Oncol 2021;11:696931. https://doi.org/10.3389/fonc.2021.696931.Tsai YM, Wu KL, Liu YW et al. Cooperation Between Cancer and Fibroblasts in Vascular Mimicry and N2-Type Neutrophil Recruitment via Notch2-Jagged1 Interaction in Lung Cancer. Front Oncol 2021;11:696931. https://doi.org/10.3389/fonc.2021.696931.Jager MJ, Ly LV, El Filali M, Madigan MC. Macrophages in uveal melanoma and in experimental ocular tumor models: Friends or foes? Prog Retin Eye Res 2011;30(2):129−146. https://doi.org/10.1016/j.preteyeres.2010.11.004.Jager MJ, Ly LV, El Filali M, Madigan MC. Macrophages in uveal melanoma and in experimental ocular tumor models: Friends or foes? Prog Retin Eye Res 2011;30(2):129−146. https://doi.org/10.1016/j.preteyeres.2010.11.004.Sun H, Zhang D, Yao Z et al. Anti-angiogenic treatment promotes triple-negative breast cancer invasion via vasculogenic mimicry. Cancer Biol Ther 2017;18(4):205−213. https://doi.org/10.1080/15384047.2017.1294288.Sun H, Zhang D, Yao Z et al. Anti-angiogenic treatment promotes triple-negative breast cancer invasion via vasculogenic mimicry. Cancer Biol Ther 2017;18(4):205−213. https://doi.org/10.1080/15384047.2017.1294288.Silvestri VL, Henriet E, Linville RM et al. A Tissue-Engineered 3D Microvessel Model Reveals the Dynamics of Mosaic Vessel Formation in Breast Cancer. Cancer Res 2020;80:4288–4301. https://doi.org/10.1158/0008-5472.CAN-19-1564.Silvestri VL, Henriet E, Linville RM et al. A Tissue-Engineered 3D Microvessel Model Reveals the Dynamics of Mosaic Vessel Formation in Breast Cancer. Cancer Res 2020;80:4288–4301. https://doi.org/10.1158/0008-5472.CAN-19-1564.Xu Y, Li Q, Li XY et al. Short-term anti-vascular endothelial growth factor treatment elicits vasculogenic mimicry formation of tumors to accelerate metastasis. J Exp Clin Cancer Res 2012;31(1):16. https://doi.org/10.1186/1756-9966-31-16.Xu Y, Li Q, Li XY et al. Short-term anti-vascular endothelial growth factor treatment elicits vasculogenic mimicry formation of tumors to accelerate metastasis. J Exp Clin Cancer Res 2012;31(1):16. https://doi.org/10.1186/1756-9966-31-16.

The authors declare that there are no conflicts of interest present.