Васкулогенная мимикрия при меланоме: молекулярные механизмы и клиническое значение
https://doi.org/10.17650/1726-9784-2019-18-1-16-24
Аннотация
Концепция васкулогенной мимикрии (ВМ) была введена для описания уникальной способности высокоагрессивных опухолевых клеток формировать капиллярно-подобные структуры и богатую матрицами структурированную сеть в трехмерной культуре, которая имитирует эмбриональную васкулогенную сеть. Сообщалось о ВМ в нескольких агрессивных опухолях, включая рак яичников, молочной железы, печени, легких, саркому, глиобластому. Следует отметить, что ВМ в меланоцитарных опухолях наиболее распространена и является наиболее изученной. Хотя большое внимание уделялось факторам, которые стимулируют или подавляют образование сосудистых каналов опухолевыми клетками, молекулярные механизмы, лежащие в основе этого явления, остаются загадочными. Этот обзор будет посвящен молекулярным детерминантам и ключевым сигнальным путям, участвующим в опухолевой ВМ. Исследование лекарственных препаратов, нацеленных на молекулярные сигнальные пути в ВМ, является областью проблем и надежд. Исследования на ВМ увеличат наши знания о молекулярных событиях, дающих агрессивным опухолевым клеткам пластичность, что приводит к их способности имитировать сосудистую систему. На сегодняшний день существует мало функциональных данных, которые показывают, как каналы, связанные с опухолевыми клетками, способствуют общей выживаемости опухоли. Однако даже среди исследователей, которые поставили под сомнение концепцию ВМ как важнейшей системы кровообращения, в целом существует консенсус о том, что прогностическое значение PAS-положительных паттернов важно.
Об авторах
Д. Л. Ротин
Государственная Израильская больница «Шиба» (Тель ха-Шомер)
Израиль
Израиль, 52621 Рамат-Ган, Дорога Шиба, 2;
Израиль
Израиль, 52621 Рамат-Ган, Дорога Шиба, 2;
К. С. Титов
ГБУЗ «Московский клинический научный центр им. А.С. Логинова» Департамента здравоохранения г. Москвы
Россия
111123 Москва, ш. Энтузиастов, 86
Россия
111123 Москва, ш. Энтузиастов, 86
А. М. Казаков
ФГБУ «НМИЦ онкологии им. Н.Н. Блохина» Минздрава России
Россия
115478 Москва, Каширское ш., 24
Россия
115478 Москва, Каширское ш., 24
Список литературы
1. Jain R.K., Carmeliet P. SnapShot: Tumor angiogenesis. Cell 2012;149(6):1408–1408.е1. DOI: 10.1016/j.cell.2012.05.025. PMID: 22682256.
2. Hilen F., Griffioen A.W. Tumour vascularization: sprouting angiogenesis and beyond. Cancer Metastasis Rev 2007;26(3–4):489–502. DOI: 10.1007/s10555-007-9094-7. PMID: 17717633.
3. Seftor R.E., Hess A.R., Seftor E.A. et al. Tumor cell vasculogenic mimicry: from controversy to therapeutic promise. Am J Pathol 2012;181(4):1115–25. DOI: 10.1016/j.ajpath.2012.07.013. PMID: 22944600.
4. Kirschmann D.A., Seftor E.A., Hardy K.M. et al. Molecular pathways: vasculogenic mimicry in tumor cells: diagnostic and therapeutic implications. Clin Cancer Res 2012;18(10):2726–32. DOI: 10.1158/1078-0432.CCR-11-3237. PMID: 22474319.
5. Qiao L., Liang N., Zhang J. et al. Advanced research on vasculogenic mimicry in cancer. J Cell Mol Med 2015;19(2):315–26. DOI: 10.1111/jcmm.12496. PMID: 25598425.
6. Chung H.J., Mahalingam M. Angiogenesis, vasculogenic mimicry and vascular invasion in cutaneous malignant melanoma – implications for therapeutic strategies and targeted therapies. Expert Rev Anticancer Ther 2014;14(5):621–39. DOI: 10.1586/14737140.2014.883281. PMID: 24506089.
7. Maniotis A.J., 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):739–52. DOI: 10.1016/S0002-9440(10)65173-5. PMID: 10487832.
8. Folberg R., Hendrix M.J., Maniotis A.J. Vasculogenic mimicry and tumor angiogenesis. Am J Pathol 2000;156(2):361–81. DOI: 10.1016/S0002-9440(10)64739-6. PMID: 10666364.
9. Clarijs R., van Dijk M., Ruiter D.J., de Waal R.M. Functional and morphologic analysis of the fluid-conducting meshwork in xenografted cutaneous and primary uveal melanoma. Invest Ophthalmol Vis Sci 2015;46(9):3013–20. DOI: 10.1167/iovs.04-0876. PMID: 16123395.
10. Frenkel S., Barzel I., Levy J. et al. Demonstrating circulation in vasculogenic mimicry patterns of uveal melanoma by confocal indocyanine green angiography. Eye (Lond) 2008;22(7):948–52. DOI: 10.1038/sj.eye.6702783. PMID: 17363922.
11. van Beurden A., Schmitz R.F., van Dijk C.M., Baeten C.I. Periodic acid Schiff loops and blood lakes associated with metastasis in cutaneous melanoma. Melanoma Res 2012;22(6):424–9. DOI: 10.1097/CMR.0b013e328358b355. PMID: 23010821.
12. Chang Y.S., di Tomaso E., McDonald D.M. et al. Mosaic blood vessels in tumors: frequency of cancer cells in contact with flowing blood. Proc Natl Acad Sci USA 2000;97(26):14608–13. DOI: 10.1073/pnas.97.26.14608. PMID: 11121063.
13. di Tomaso E., Capen D., Haskell A. et al. Mosaic tumor vessels: cellular basis and ultrastructure of focal regions lacking endothelial cell markers. Cancer Res 2005;65(13):5740–9. DOI: 10.1158/0008-5472.CAN-04-4552. PMID: 15994949.
14. Chen L., Zhang S., Li X. et al. A pilot study of vasculogenic mimicry immunohistochemical expression in intraocular melanoma model. Oncol Rep 2009;21(4):989–99. PMID: 19287998.
15. Maniotis A.J., Chen X., Garcia C. et al. Control of melanoma morphogenesis, endothelial survival, and perfusion by extracellular matrix. Lab Invest 2012;82(8):1031–43. PMID: 12177242.
16. Clarijs R., Otte-Holler I., Ruiter D.J., de Waal R.M. Presence of a fluidconducting meshwork in xenografted cutaneous and primary human uveal melanoma. Invest Ophthalmol Vis Sci 2002;43(4):912–8. PMID: 11923228.
17. Mueller A.J., Bartsch D.U., Folberg R. et al. Imaging the microvasculature of choroidal melanomas with confocal indocyanine green scanning laser ophthalmoscopy. Arch Ophthalmol 1998;116(1):31–9. PMID: 9445206.
18. Ruf W., Seftor E.A., Petrovan R.J. et al. Differential role of tissue factor pathway inhibitors 1 and 2 in melanoma vasculogenic mimicry. Cancer Res 2003;63(17):5381–9. PMID: 14500372.
19. Hess A.R., Seftor E.A., Gardner L.M. et al. Molecular regulation of tumor cell vasculogenic mimicry by tyrosine phosphorylation: role of epithelial cell kinase (Eck/EphA2). Cancer Res 2001;61(8):3250–5. PMID: 11309274.
20. Girouard S.D., Murphy G.F. Melanoma stem cells: not rare, but well done. Lab Invest 2011;91(5):647–64. DOI: 10.1038/labinvest.2011.50. PMID: 21445060.
21. Sajithlal G.B., McGuire T.F., Lu J. et al. Endothelial-like cells derived directly from human tumor xenografts. Int J Cancer 2010;127(10):2268–78. DOI: 10.1002/ijc.25251. PMID: 20162569.
22. Dunleavey J.M., Dudley A.C. Vascular mimicry: concepts and implications for anti-angiogenic therapy. Curr Angiogenes 2012;1(2):133–8. DOI: 10.2174/2211552811201020133. PMID: 24729954.
23. Seftor E.A., Meltzer P.S., Schatteman G.C. et al. Expression of multiple molecular phenotypes by aggressive melanoma tumor cells: role in vasculogenic mimicry. Crit Rev Oncol Hematol 2002;44(1):17–27. PMID: 12398997.
24. McAllister J.C., Zhan Q., Weishaupt C. et al. The embryonic morphogen, Nodal, is associated with channel-like structures in human malignant melanoma xenografts. J Cutan Pathol 2010;37(Suppl 1):19–25. DOI: 10.1111/j.1600-0560.2010.01503.x. PMID: 20482672.
25. Khalkhali-Ellis Z., Kirschmann D.A., Seftor E.A. et al. Divergence(s) in Nodal signaling between aggressive melanoma and embryonic stem cells. Int J Cancer 2015;136(5):E242–51. DOI: 10.1002/ijc.29198. PMID: 25204799.
26. Frank N.Y., Schatton T., Kim S. et al. VEGFR-1 expressed by malignant melanoma-initiating cells is required for tumor growth. Cancer Res 2011;71(4):1474–85. DOI: 10.1158/0008-5472.CAN-10-1660. PMID: 21212411.
27. Murphy G.F., Wilson B.J., Girouard S.D. et al. Stem cells and targeted approaches to melanoma cure. Mol Aspects Med 2014;39:33–49. DOI: 10.1016/j.mam.2013.10.003. PMID: 24145241.
28. Lai C.Y., Schwartz B.E., Hsu M.Y. CD133+ melanoma subpopulations contribute to perivascular niche morphogenesis and tumorigenicity through vasculogenic mimicry. Cancer Res 2012;72(19):5111–8. DOI: 10.1158/0008-5472.CAN-12-0624. PMID: 22865455.
29. Valyi-Nagy K., Kormos B., Ali M. et al. Stem cell marker CD271 is expressed by vasculogenic mimicry-forming uveal melanoma cells in three-dimensional cultures. Mol Vis 2012;18:588–92. PMID: 22419851.
30. Demou Z.N., Hendrix M.J. Microgenomics profile the endogenous angiogenic phenotype in subpopulations of aggressive melanoma. J Cell Biochem 2008;105(2):562–73. DOI: 10.1002/ jcb.21855. PMID: 18655191.
31. Bittner M., Meltzer P., Chen Y. et al. Molecular classification of cutaneous malignant melanoma by gene expression profiling. Nature 2000;406(6795): 536–40. DOI: 10.1038/35020115. PMID: 10952317.
32. Hess A.R., Margaryan N.V., Seftor E.A., Hendrix M.J. Deciphering the signaling events that promote melanoma tumor cell vasculogenic mimicry and their link to embryonic vasculogenesis: role of the Eph receptors. Dev Dyn 2007;236(12):3283–96. DOI: 10.1002/dvdy.21190. PMID: 17557303.
33. Margaryan N.V., Strizzi L., Abbott D.E. et al. EphA2 as a promoter of melanoma tumorigenicity. Cancer Biol Ther 2009;8(3):279–88. PMID: 19223760.
34. Hendrix M.J., Seftor E.A., Meltzer P.S. et al. Expression and functional significance of VE-cadherin in aggressive human melanoma cells: role in vasculogenic mimicry. Proc Natl Acad Sci USA 2001;98(14):8018–23. DOI: 10.1073/pnas.131209798. PMID: 11416160.
35. 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;28:124. DOI: 10.1186/1756-996628-124. PMID: 19735546.
36. Liu R., Cao Z., Tu J. et al. Lycorine hydrochloride inhibits metastatic melanoma cell-dominant vasculogenic mimicry. Pigment Cell Melanoma Res 2012;25(5):630–8. DOI: 10.1111/ j.1755-148X.2012.01036.x. PMID: 22781316.
37. Hess A.R., Seftor E.A., Gruman L.M. et al. VE-cadherin regulates EphA2 in aggressive melanoma cells through a novel signaling pathway: implications. Cancer Biol Ther 2006;5(2):228–33. PMID: 16481735.
38. Hess A.R., Postovit L.M., Margaryan N.V. et al. Focal adhesion kinase promotes the aggressive melanoma phenotype. Cancer Res 2005;65(21):9851–60. DOI: 10.1158/0008-5472.CAN-05-2172. PMID: 16267008.
39. Hess A.R., Hendrix M.J. Focal adhesion kinase signaling and the aggressive melanoma phenotype. Cell Cycle 2006;5(5):478–80. DOI: 10.4161/cc.5.5.2518. PMID: 16552181.
40. Lissitzky J.C., Parriaux D., Ristorcelli E. et al. Cyclic AMP signaling as a mediator of vasculogenic mimicry in aggressive human melanoma cells in vitro. Cancer Res 2009;69(3):802–9. DOI: 10.1158/0008-5472.CAN-08-2391. PMID: 19176384.
41. Chen L.X., He Y.J., Zhao S.Z. et al. Inhibition of tumor growth and vasculogenic mimicry by curcumin through down-regulation of the EphA2/ PI3K/MMP pathway in a murine choroidal melanoma model. Cancer Biol Ther 2011;11(2):229–35. PMID: 21084858.
42. Seftor R.E., Seftor E.A., Koshikawa N. et al. Cooperative interactions of laminin 5 γ2 chain, matrix metalloproteinase-2, and membrane type-1-matrix/ metalloproteinase are required for mimicry of embryonic vasculogenesis by aggressive melanoma. Cancer Res 2011;61(17):6322–7. PMID: 11522618.
43. Seftor E.A., Meltzer P.S., Kirschmann D.A. et al. The epigenetic reprogramming of poorly aggressive melanoma cells by a metastatic microenvironment. J Cell Mol Med 2006;10(1):174–96. PMID: 16563230.
44. Hess A.R., Seftor E.A., Seftor R.E., Hendrix M.J. Phosphoinositide 3-kinase regulates membrane type 1-matrix metalloproteinase (MMP) and MMP-2 activity during melanoma cell vasculogenic mimicry. Cancer Res 2003;63(16):4757–62. PMID: 12941789.
45. Zhang S., Li M., Gu Y. et al. Thalidomide influences growth and vasculogenic mimicry channel formation in melanoma. J Exp Clin Cancer Res 2008;27:60. DOI: 10.1186/1756-996627-60. PMID: 18983651.
46. Zhang S., Zhang D., Sun B. Vasculogenic mimicry: current status and future prospects. Cancer Lett 2007;254(2):157–64. DOI: 10.1016/j.canlet.2006.12.036. PMID: 17306454.
47. Seftor R.E., Seftor E.A., Kirschman D.A., Hendrix M.J. Targeting the tumor microenvironment with chemically modified tetracyclines: inhibition of laminin 5 γ2 chain promigratory fragments and vasculogenic mimicry. Mol Cancer Ther 2002;1(13): 1173–9. PMID: 12479698.
48. Zhao L., Marshall E.S., Kelland L.R., Baguley B.C. Evidence for the involvement of p38 MAP kinase in the action of the vascular disrupting agent 5,6-dimethylxanthenone-4-acetic acid (DMXAA). Invest New Drugs 2007;25(3):271–6. DOI: 10.1007/s10637-006-9029-0. PMID: 17203401.
49. Hardy K.M., Kirschmann D.A., Seftor E.A. et al. Regulation of the embryonic morphogen Nodal by Notch4 facilitates manifestation of the aggressive melanoma phenotype. Cancer Res 2010;70(24):10340–50. DOI: 10.1158/0008-5472.CAN-10-0705. PMID: 21159651.
50. Strizzi L., Postovit L.M., Margaryan N.V. et al. Nodal as a biomarker for melanoma progression and a new therapeutic target for clinical intervention. Expert Rev Dermatol 2009;4(1):67–78. DOI: 10.1586/17469872.4.1.67. PMID: 19885369.
51. Sun B., Zhang D., Zhang S. et al. Hypoxia influences vasculogenic mimicry channel formation and tumor invasion-related protein expression in melanoma. Cancer Lett 2007;249(2):188–97. DOI: 10.1016/j.canlet.2006.08.016. PMID: 16997457.
52. Zhao N., Sun B.C., Sun T. et al. Hypoxia-induced vasculogenic mimicry formation via VE-cadherin regulation by Bcl-2. Med Oncol 2012;29(5):3599–607. DOI: 10.1007/s12032-012-0245-5. PMID: 22562824.
53. Comito G., Calvani M., Giannoni E. et al. HIF-1α stabilization by mitochondrial ROS promotes MET-dependent invasive growth and vasculogenic mimicry in melanoma cells. Free Radic Biol Med 2011;51(4):893–904. DOI: 10.1016/j.freeradbiomed.
54. 05.042. PMID: 21703345. 54. Wu S., Singh R.K. Resistance to chemotherapy and molecularly targeted therapies: rationale for combination therapy in malignant melanoma. Curr Mol Med 2011;11(7):553–63. PMID: 21707515.
55. Benazzi C., Al-Dissi A., Chau C.H. et al. Angiogenesis in spontaneous tumors and implications for comparative tumor biology. Scientific World Journal 2014;2014:919570. DOI: 10.1155/2014/919570. PMID: 24563633.
56. Schnegg C.I., Yang M.H., Ghosh S.K., Hsu M.Y. Induction of vasculogenic mimicry overrides VEGF-A silencing and enriches stem-like cancer cells in melanoma. Cancer Res 2015;75(8):1682–90. DOI: 10.1158/0008-5472.CAN-14-1855. PMID: 25769726.
57. Vartanian A.A., Burova O.S., Stepanova E.V. et al. Melanoma vasculogenic mimicry is strongly related to reactive oxygen species level. Melanoma Res 2007;17(6):370–9. DOI: 10.1097/CMR.0b013e3282f1d2ec. PMID: 17992120.
58. van der Schaft D.W., Seftor R.E., Seftor E.A. et al. Effects of angiogenesis inhibitors on vascular network formation by human endothelial and melanoma cells. J Natl Cancer Inst 2004;96(19):1473–7. DOI: 10.1093/jnci/ djh267. PMID: 15467037.
59. Spinella F., Caprara V., Di Castro V. et al. Endothelin-1 induces the transactivation of vascular endothelial growth factor receptor-3 and modulates cell migration and vasculogenic mimicry in melanoma cells. J Mol Med (Berl) 2013;91(3):395–405. DOI: 10.1007/s00109-012-0956-2. PMID: 22965194.
60. Orgaz J.L., Ladhani O., Hoek K.S. et al. Loss of pigment epithelium derived factor enables migration, invasion and metastatic spread of human melanoma. Oncogene 2008;28(47):4147–61. DOI: 10.1038/onc.2009.284. PMID: 19767774.
61. Rothhammer T., Bataille F., Spruss T. et al. Functional implication of BMP4 expression on angiogenesis in malignant melanoma. Oncogene 2007;26(28):4158–70. DOI: 10.1038/sj.onc.1210182. PMID: 17173062.
62. Su F., Li B., Wang J. et al. Molecular regulation of vasculogenic mimicry in human uveal melanoma cells: role of helix-loop-helix ID2. Graefes Arch Clin Exp Ophthalmol 2009;247(3):411–9. DOI: 10.1007/s00417-008-1008-z. PMID: 19043732.
63. Liu Y.R., Sun B., Zhao X.L. et al. Basal caspase-3 activity promotes migration, invasion, and vasculogenic mimicry formation of melanoma cells. Melanoma Res 2013;23(4):243–53. DOI: 10.1097/CMR.0b013e3283625498. PMID: 23695439.
64. Vartanian A.A., Burova O.S., Stepanova E.V., Baryshnikov A.Y. The involvement of apoptosis in melanoma vasculogenic mimicry. Melanoma Res 2007;17(1):1–8. DOI: 10.1097/ CMR.0b013e3280112b76. PMID: 17235236.
65. Mourad-Zeidan A.A., Melnikova V.O., Wang H. et al. Expression profiling of galectin-3-depleted melanoma cells reveals its major role in melanoma cell plasticity and vasculogenic mimicry. Am J Pathol 2008;173(6):1839–52. DOI: 10.2353/ajpath.2008.080380. PMID: 18988806.
66. Makitie T., Summanen P., Tarkkanen A., Kivela T. Microvascular loops and networks as prognostic indicators in choroidal and ciliary body melanomas. J Natl Cancer Inst 1999;91(4):359–67. PMID: 10050870.
67. 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):1389–98. PMID: 8371929.
68. Warso M.A., Maniotis A.J., Chen X. et al. Prognostic significance of periodic acid-Schiff-positive patterns in primary cutaneous melanoma. Clin Cancer Res 2001;7(3):473–7. PMID: 11297236.
69. 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):3914–23. DOI: 10.1016/j.ejca.2013.07.148. PMID: 23992642.
70. Einspahr J.G., Thomas T.L., Saboda K. et al. Expression of vascular endothelial growth factor in early cutaneous melanocytic lesion progression. Cancer 2007;110(11):2519–27. DOI: 10.1002/cncr.23076. PMID: 17932890.
71. Modlin R.L., Gottlieb B., Taylor C., Rea T.H. Identification of cells lining pseudovascular spaces of benign pigmented nevi. Am J Dermatopathol 1984;6 Suppl:25–9. PMID: 6084957.
72. Lee K.H., Han Y.W., Park C.J. Three cases of melanocytic nevi with pseudovascular spaces. Korean J Dermatol 2007;45(1):90–3.
73. Demitsu T., Kakurai M., Yamada T. et al. The vascular space-like structure in melanocytic nevus is not an injection artifact: report of a case and an experimental study. J Dermatol 1998;25(3):143–9. PMID: 9575674.
74. Goldstein A.M., Tucker M.A. Dysplastic nevi and melanoma. Cancer Epidemiol Biomarkers Prev 2013;22(4):528–32. DOI: 10.1158/1055-9965.EPI-12-1346. PMID: 23549396.
75. Coupland S.E., Lake S.L., Zeschnigk M., Damato B.E. Molecular pathology of uveal melanoma. Eye 2013;27(2):230–42. DOI: 10.1038/eye.2012.255. PMID: 23222563.
76. Chang S.H., Worley L.A., Onken M.D., Harbour J.W. Prognostic biomarkers in uveal melanoma: evidence for a stem cell-like phenotype associated with metastasis. Melanoma Res 2008;18(3):191–200. DOI: 10.1097/ CMR.0b013e3283005270. PMID: 18477893.
77. Gould Rothberg B.E., Bracken M.B., Rimm D.L. Tissue biomarkers for prognosis in cutaneous melanoma: a systematic review and meta-analysis. J Natl Cancer Inst 2009;101(7):452–74. DOI: 10.1093/jnci/djp038. PMID: 19318635.
Рецензия
Для цитирования:
Ротин Д.Л., Титов К.С., Казаков А.М. Васкулогенная мимикрия при меланоме: молекулярные механизмы и клиническое значение. Российский биотерапевтический журнал. 2019;18(1):16-24. https://doi.org/10.17650/1726-9784-2019-18-1-16-24
For citation:
Rotin D.L., Titov K.S., Kazakov A.M. Vasculogenic mimicry in melanoma: molecular mechanisms and clinical significance. Russian Journal of Biotherapy. 2019;18(1):16-24. (In Russ.) https://doi.org/10.17650/1726-9784-2019-18-1-16-24
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