CoChat
Sign Up
Cited by 146

The DOI matches its Crossref record; 12 of the 12 references it cites were found in a registry or an index.

Vascular normalisation as the stepping stone into tumour microenvironment transformation

Magnussen, Anette L., Mills, Ian G.·2021·British Journal of Cancer
DOI 10.1038/s41416-021-01330-zPMC PMC8329166
Open this paper in CoChat — free account

Abstract

A functional vascular system is indispensable for drug delivery and fundamental for responsiveness of the tumour microenvironment to such medication. At the same time, the progression of a tumour is defined by the interactions of the cancer cells with their surrounding environment, including neovessels, and the vascular network continues to be the major route for the dissemination of tumour cells in cancer, facilitating metastasis. So how can this apparent conflict be reconciled? Vessel normalisation—in which redundant structures are pruned and the abnormal vasculature is stabilised and remodelled—is generally considered to be beneficial in the course of anti-cancer treatments. A causality between normalised vasculature and improved response to medication and treatment is observed. For this reason, it is important to discern the consequence of vessel normalisation on the tumour microenvironment and to modulate the vasculature advantageously. This article will highlight the challenges of controlled neovascular remodelling and outline how vascular normalisation can shape disease management.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1038/s41416-021-01330-z

Cites

12 of 12 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Flagged first, then by citations

Show all 12 references

Research works printed but not linked: 136

  1. Franses, J. W. & Edelman, E. R. The evolution of endothelial regulatory paradigms in cancer biology and vascular repair. Cancer Res. 71, 7339 (2011). · DOI
  2. Harvey, W. An anatomical disquisition on the motion of the heart and blood in animals*. Ann. Noninvasive Electrocardiol. 5, 196–203 (2020). · DOI
  3. Meyer, J. Über die Neubildung von Blutgefäßen in plastischen Exudaten serösen Membranen und in Hautwunden. Ann Charité 4, 41–140 (1852).
  4. Clark, E. R. & Clark, E. L. Observations on changes in blood vascular endothelium in the living animal. Am. J. Anat. 57, 385–438 (1935). · DOI
  5. Clark, E. R. & Clark, E. L. Microscopic observations on the growth of blood capillaries in the living mammal. Am. J. Anat. 64, 251–301 (1939). · DOI
  6. Ribatti, D., Nico, B. & Crivellato, E. The development of the vascular system: a historical overview. in Vascular Morphogenesis: Methods and Protocols (ed. Ribatti, D.) 1–14 (Springer New York, 2015). · DOI
  7. Patan, S. Vasculogenesis and angiogenesis. Cancer Treat. Res. 117, 3–32 (2004). · DOI
  8. Patan, S. Vasculogenesis and angiogenesis as mechanisms of vascular network formation, growth and remodeling. J. Neurooncol. 50, 1–15 (2000). · DOI
  9. Chen, Q., Jiang, L., Li, C., Hu, D., Bu, J.-W., Cai, D. et al. Haemodynamics-driven developmental pruning of brain vasculature in zebrafish. PLoS Biol. 10, e1001374 (2012). · DOI
  10. Asahara, T., Murohara, T., Sullivan, A., Silver, M., van der Zee, R., Li, T. et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science 275, 964–967 (1997). · DOI · Paper page
  11. Rafii, S. & Lyden, D. Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat. Med. 9, 702–712 (2003). · DOI
  12. Larrivée, B., Niessen, K., Pollet, I., Corbel, S. Y., Long, M., Rossi, F. M. et al. Minimal contribution of marrow-derived endothelial precursors to tumor vasculature. J. Immunol. 175, 2890 (2005). · DOI
  13. Marçola, M. & Rodrigues, C. E. Endothelial progenitor cells in tumor angiogenesis: another brick in the wall. Stem Cells Int. 2015, 832649 (2015). · DOI
  14. Moschetta, M., Mishima, Y., Sahin, I., Manier, S., Glavey, S., Vacca, A. et al. Role of endothelial progenitor cells in cancer progression. Biochimica et Biophysica Acta 1846, 26–39 (2014).
  15. Tanaka, S., Ueno, T., Ishiguro, H., Morita, S. & Toi, M. The lack of increases in circulating endothelial progenitor cell as a negative predictor for pathological response to neoadjuvant chemotherapy in breast cancer patients. npj Precis. Oncol. 1, 6 (2017). · DOI
  16. Mentzer, S. J. & Konerding, M. A. Intussusceptive angiogenesis: expansion and remodeling of microvascular networks. Angiogenesis 17, 499–509 (2014). · DOI
  17. Burri, P. H. & Djonov, V. Intussusceptive angiogenesis–the alternative to capillary sprouting. Mol. Aspects Med. 23, S1–S27 (2002). · DOI
  18. Burri, P. H., Hlushchuk, R. & Djonov, V. Intussusceptive angiogenesis: its emergence, its characteristics, and its significance. Dev. Dyn. 231, 474–488 (2004). · DOI
  19. Algire, G. H. C. & Vascular, H. W. reactions of normal and malignant tissues in vivo. J. Natl Cancer Inst. 6, 73 (1945). · DOI
  20. Tannock, I. F. The relation between cell proliferation and the vascular system in a transplanted mouse mammary tumour. Br. J. Cancer 22, 258–273 (1968). · DOI · Paper page
  21. Folkman, J., Merler, E., Abernathy, C. & Williams, G. Isolation of a tumor factor responsible for angiogenesis. J. Exp. Med. 133, 275–288 (1971). · DOI · Paper page
  22. Leung, D. W., Cachianes, G., Kuang, W. J., Goeddel, D. V. & Ferrara, N. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 246, 1306–1309 (1989). · DOI
  23. Plouët, J., Schilling, J. & Gospodarowicz, D. Isolation and characterization of a newly identified endothelial cell mitogen produced by AtT-20 cells. EMBO J. 8, 3801–3806 (1989). · DOI
  24. Senger, D. R., Galli, S. J., Dvorak, A. M., Perruzzi, C. A., Harvey, V. S. & Dvorak, H. F. Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 219, 983–985 (1983). · DOI
  25. Kerbel, R. S. Tumor angiogenesis. New Engl. J. Med. 358, 2039–2049 (2008). · DOI
  26. Sennino, B. & McDonald, D. M. Controlling escape from angiogenesis inhibitors. Nat. Rev. Cancer 12, 699–709 (2012). · DOI
  27. Overgaard, J. & Horsman, M. R. Modification of hypoxia-induced radioresistance in tumors by the use of oxygen and sensitizers. Semin. Radiat. Oncol. 6, 10–21 (1996). · DOI
  28. Krzywinska, E. & Stockmann, C. Hypoxia, metabolism and immune cell function. Biomedicines 6, 56 (2018). · DOI
  29. Ohga, N., Ishikawa, S., Maishi, N., Akiyama, K., Hida, Y., Kawamoto, T. et al. Heterogeneity of tumor endothelial cells: comparison between tumor endothelial cells isolated from high- and low-metastatic tumors. Am. J. Pathol. 180, 1294–1307 (2012). · DOI
  30. Matsumoto, S., Batra, S., Saito, K., Yasui, H., Choudhuri, R., Gadisetti, C. et al. Antiangiogenic agent sunitinib transiently increases tumor oxygenation and suppresses cycling hypoxia. Cancer Res. 71, 6350–6359 (2011). · DOI
  31. Morikawa, S., Baluk, P., Kaidoh, T., Haskell, A., Jain, R. K. & McDonald, D. M. Abnormalities in pericytes on blood vessels and endothelial sprouts in tumors. Am. J. Pathol. 160, 985–1000 (2002). · DOI
  32. Claffey, K. P., Brown, L. F., del Aguila, L. F., Tognazzi, K., Yeo, K. T., Manseau, E. J. et al. Expression of vascular permeability factor/vascular endothelial growth factor by melanoma cells increases tumor growth, angiogenesis, and experimental metastasis. Cancer Res. 56, 172–181 (1996).
  33. Baluk, P., Morikawa, S., Haskell, A., Mancuso, M. & McDonald, D. M. Abnormalities of basement membrane on blood vessels and endothelial sprouts in tumors. Am. J. Pathol. 163, 1801–1815 (2003). · DOI · Paper page
  34. Nina Kristine, R., Aphirak, J., Tore, L. & Catharina de Lange, D. Macromolecular diffusion in the extracellular matrix measured by fluorescence correlation spectroscopy. J. Biomed. Optics 13, 1–9 (2008).
  35. Ariffin, A. B., Forde, P. F., Jahangeer, S., Soden, D. M. & Hinchion, J. Releasing pressure in tumors: what do we know so far and where do we go from here? A review. Cancer Res. 74, 2655–2662 (2014). · DOI
  36. Le Serve, A. W. & Hellmann, K. Metastases and the normalization of tumour blood vessels by ICRF 159: a new type of drug action. Br. Med. J. 1, 597–601 (1972). · DOI
  37. Rybak, S. M., Sanovich, E., Hollingshead, M. G., Borgel, S. D., Newton, D. L., Melillo, G. et al. “Vasocrine” formation of tumor cell-lined vascular spaces: implications for rational design of antiangiogenic therapies. Cancer Res. 63, 2812–2819 (2003).
  38. Jain, R. K. Molecular regulation of vessel maturation. Nat. Med. 9, 685–693 (2003). · DOI
  39. Carmeliet, P. & Jain, R. K. Principles and mechanisms of vessel normalization for cancer and other angiogenic diseases. Nat. Rev. Drug Discov. 10, 417–427 (2011). · DOI
  40. Jain, R. K. Normalizing tumor vasculature with anti-angiogenic therapy: a new paradigm for combination therapy. Nat. Med. 7, 987–989 (2001). · DOI · Paper page
  41. Schwartz, M. A., Vestweber, D. & Simons, M. A unifying concept in vascular health and disease. Science 360, 270–271 (2018). · DOI
  42. Schreiter, J., Meyer, S., Schmidt, C., Schulz, R. M. & Langer, S. Dorsal skinfold chamber models in mice. GMS Interdiscip Plast. Reconstr. Surg. DGPW 6, Doc10, https://doi.org/10.3205/iprs000112 (2017). · DOI
  43. Tong, R. T., Boucher, Y., Kozin, S. V., Winkler, F., Hicklin, D. J. & Jain, R. K. Vascular normalization by vascular endothelial growth factor receptor 2 blockade induces a pressure gradient across the vasculature and improves drug penetration in tumors. Cancer Res. 64, 3731 (2004). · DOI · Paper page
  44. Yang, J., Liao, C., Liu, Y., Yang, G., Ke, T., Ding, Y. et al. MR imaging biomarkers evaluating vascular normalization window after anti-vessel treatment. Oncotarget 9, 11964–11976 (2017). · DOI
  45. Bohndiek, S. E., Sasportas, L. S., Machtaler, S., Jokerst, J. V., Hori, S. & Gambhir, S. S. Photoacoustic tomography detects early vessel regression and normalization during ovarian tumor response to the antiangiogenic therapy trebananib. J. Nucl. Med. 56, 1942–1947 (2015). · DOI
  46. Goel, S., Duda, D. G., Xu, L., Munn, L. L., Boucher, Y., Fukumura, D. et al. Normalization of the vasculature for treatment of cancer and other diseases. Physiol. Rev. 91, 1071–1121 (2011). · DOI · Paper page
  47. Winkler, F., Kozin, S. V., Tong, R. T., Chae, S.-S., Booth, M. F., Garkavtsev, I. et al. Kinetics of vascular normalization by VEGFR2 blockade governs brain tumor response to radiation: Role of oxygenation, angiopoietin-1, and matrix metalloproteinases. Cancer Cell 6, 553–563 (2004).
  48. Willett, C. G., Kozin, S. V., Duda, D. G., di Tomaso, E., Kozak, K. R., Boucher, Y. et al. Combined vascular endothelial growth factor-targeted therapy and radiotherapy for rectal cancer: theory and clinical practice. Semin. Oncol. 33, S35–S40 (2006). · DOI
  49. Collet, G., Lamerant-Fayel, N., Tertil, M., El Hafny-Rahbi, B., Stepniewski, J., Guichard, A. et al. Hypoxia-regulated overexpression of soluble VEGFR2 controls angiogenesis and inhibits tumor growth. Mol. Cancer Ther. 13, 165–178 (2014). · DOI
  50. Boudria, A., Abou Faycal, C., Jia, T., Gout, S., Keramidas, M., Didier, C. et al. VEGF165b, a splice variant of VEGF-A, promotes lung tumor progression and escape from anti-angiogenic therapies through a β1 integrin/VEGFR autocrine loop. Oncogene 38, 1050–1066 (2019). · DOI · Paper page
  51. Woolard, J., Wang, W. Y., Bevan, H. S., Qiu, Y., Morbidelli, L., Pritchard-Jones, R. O. et al. VEGF165b, an inhibitory vascular endothelial growth factor splice variant: mechanism of action, in vivo effect on angiogenesis and endogenous protein expression. Cancer Res. 64, 7822–7835 (2004). · DOI · Paper page
  52. Nowak, D. G., Woolard, J., Amin, E. M., Konopatskaya, O., Saleem, M. A., Churchill, A. J. et al. Expression of pro- and anti-angiogenic isoforms of VEGF is differentially regulated by splicing and growth factors. J. Cell Sci. 121, 3487 (2008). · DOI
  53. Mavrou, A. & Oltean, S. SRPK1 inhibition in prostate cancer: A novel anti-angiogenic treatment through modulation of VEGF alternative splicing. Pharmacol Res. 107, 276–281 (2016). · DOI
  54. Magnussen, A. L., Rennel, E. S., Hua, J., Bevan, H. S., Beazley Long, N., Lehrling, C. et al. VEGF-A165b is cytoprotective and antiangiogenic in the retina. Investig. Ophthalmol. Vis. Sci. 51, 4273–4281 (2010). · DOI
  55. Liu, J., Liao, S., Diop-Frimpong, B., Chen, W., Goel, S., Naxerova, K. et al. TGF-β blockade improves the distribution and efficacy of therapeutics in breast carcinoma by normalizing the tumor stroma. Proc. Natl Acad. Sci. USA 109, 16618–16623 (2012). · DOI
  56. Dieterich, L. C., Mellberg, S., Langenkamp, E., Zhang, L., Zieba, A., Salomäki, H. et al. Transcriptional profiling of human glioblastoma vessels indicates a key role of VEGF-A and TGFβ2 in vascular abnormalization. J. Pathol. 228, 378–390 (2012). · DOI
  57. Qayum, N., Muschel, R. J., Im, J. H., Balathasan, L., Koch, C. J., Patel, S. et al. Tumor vascular changes mediated by inhibition of oncogenic signaling. Cancer Res. 69, 6347–6354 (2009). · DOI
  58. Sawada, J., Urakami, T., Li, F., Urakami, A., Zhu, W., Fukuda, M. et al. Small GTPase R-Ras regulates integrity and functionality of tumor blood vessels. Cancer Cell 22, 235–249 (2012). · DOI
  59. Hida, K., Maishi, N., Annan, D. A. & Hida, Y. Contribution of tumor endothelial cells in cancer progression. Int. J. Mol. Sci. 19, 1272 (2018). · DOI
  60. Hamzah, J., Jugold, M., Kiessling, F., Rigby, P., Manzur, M., Marti, H. H. et al. Vascular normalization in Rgs5-deficient tumours promotes immune destruction. Nature 453, 410–414 (2008). · DOI
  61. Cox, D. B., Platt, R. J. & Zhang, F. Therapeutic genome editing: prospects and challenges. Nat. Med. 21, 121–131 (2015). · DOI · Paper page
  62. Falcón, B. L., Hashizume, H., Koumoutsakos, P., Chou, J., Bready, J. V., Coxon, A. et al. Contrasting actions of selective inhibitors of angiopoietin-1 and angiopoietin-2 on the normalization of tumor blood vessels. Am. J. Pathol. 175, 2159–2170 (2009). · DOI
  63. Alto, L. T. & Terman, J. R. Semaphorins and their signaling mechanisms. Methods Mol. Biol. 1493, 1–25 (2017). · DOI
  64. Casazza, A., Fu, X., Johansson, I., Capparuccia, L., Andersson, F., Giustacchini, A. et al. Systemic and targeted delivery of semaphorin 3A inhibits tumor angiogenesis and progression in mouse tumor models. Arterioscler. Thromb. Vasc. Biol. 31, 741–749 (2011). · DOI
  65. Serini, G., Bussolino, F., Maione, F. & Giraudo, E. Class 3 semaphorins: physiological vascular normalizing agents for anti-cancer therapy. J. Intern. Med. 273, 138–155 (2013). · DOI
  66. Fogal, V., Sugahara, K. N., Ruoslahti, E. & Christian, S. Cell surface nucleolin antagonist causes endothelial cell apoptosis and normalization of tumor vasculature. Angiogenesis 12, 91–100 (2009). · DOI
  67. Baron, M. An overview of the Notch signalling pathway. Semin. Cell Dev. Biol. 14, 113–119 (2003). · DOI
  68. Hellstrom, M., Phng, L. K., Hofmann, J. J., Wallgard, E., Coultas, L., Lindblom, P. et al. Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature 445, 776–780 (2007). · DOI · Paper page
  69. Phng, L. K. & Gerhardt, H. Angiogenesis: a team effort coordinated by notch. Dev. Cell 16, 196–208 (2009). · DOI
  70. Maes, H., Kuchnio, A., Peric, A., Moens, S., Nys, K., De Bock, K. et al. Tumor vessel normalization by chloroquine independent of autophagy. Cancer Cell 26, 190–206 (2014). · DOI
  71. Trindade, A., Djokovic, D., Gigante, J., Mendonça, L. & Duarte, A. Endothelial Dll4 overexpression reduces vascular response and inhibits tumor growth and metastasization in vivo. BMC Cancer 17, 189- (2017). · DOI
  72. Polet, F. & Feron, O. Endothelial cell metabolism and tumour angiogenesis: glucose and glutamine as essential fuels and lactate as the driving force. J. Intern. Med. 273, 156–165 (2013). · DOI
  73. Zhang, L., Li, S., Li, L., Chen, Z. & Yang, Y. COX‑2 inhibition in the endothelium induces glucose metabolism normalization and impairs tumor progression. Mol. Med. Rep. 17, 2937–2944 (2018).
  74. Cantelmo, A. R., Conradi, L. C., Brajic, A., Goveia, J., Kalucka, J., Pircher, A. et al. Inhibition of the glycolytic activator PFKFB3 in endothelium induces tumor vessel normalization, impairs metastasis, and improves chemotherapy. Cancer Cell 30, 968–985 (2016). · DOI · Paper page
  75. Kocher, M., Treuer, H., Voges, J., Hoevels, M., Sturm, V. & Muller, R. P. Computer simulation of cytotoxic and vascular effects of radiosurgery in solid and necrotic brain metastases. Radiother. Oncol. 54, 149–156 (2000). · DOI
  76. Potiron, V. A., Abderrahmani, R., Clément-Colmou, K., Marionneau-Lambot, S., Oullier, T., Paris, F. et al. Improved functionality of the vasculature during conventionally fractionated radiation therapy of prostate cancer. PLoS ONE 8, e84076 (2013). · DOI
  77. Koelwyn, G. J., Quail, D. F., Zhang, X., White, R. M. & Jones, L. W. Exercise-dependent regulation of the tumour microenvironment. Nat. Rev. Cancer 17, 620 (2017). · DOI
  78. Di Francescomarino, S., Sciartilli, A., Di Valerio, V., Di Baldassarre, A. & Gallina, S. The effect of physical exercise on endothelial function. Sports Med. 39, 797–812 (2009). · DOI
  79. Resnick, N., Yahav, H., Shay-Salit, A., Shushy, M., Schubert, S., Zilberman, L. C. et al. Fluid shear stress and the vascular endothelium: for better and for worse. Prog. Biophys. Mol. Biol. 81, 177–199 (2003). · DOI
  80. Schadler, K. L., Thomas, N. J., Galie, P. A., Bhang, D. H., Roby, K. C., Addai, P. et al. Tumor vessel normalization after aerobic exercise enhances chemotherapeutic efficacy. Oncotarget 7, 65429–65440 (2016). · DOI · Paper page
  81. McCarthy, M. Antiangiogenesis drug promising for metastatic colorectal cancer. Lancet 361, 1959 (2003). · DOI
  82. Gonzalez, H., Hagerling, C. & Werb, Z. Roles of the immune system in cancer: from tumor initiation to metastatic progression. Genes Dev. 32, 1267–1284 (2018). · DOI · Paper page
  83. Al-Soudi, A., Kaaij, M. H. & Tas, S. W. Endothelial cells: from innocent bystanders to active participants in immune responses. Autoimmun. Rev. 16, 951–962 (2017). · DOI
  84. Funaro, A., Ferrero, E., Mehta, K. & Malavasi, F. Schematic portrait of human CD38 and related molecules. Chem. Immunol. 75, 256–273 (2000).
  85. Rothermel, A. L., Wang, Y., Schechner, J., Mook-Kanamori, B., Aird, W. C., Pober, J. S. et al. Endothelial cells present antigens in vivo. BMC Immunol. 5, 5 (2004). · DOI
  86. Mai, J., Virtue, A., Shen, J., Wang, H. & Yang, X.-F. An evolving new paradigm: endothelial cells—conditional innate immune cells. J. Hematol. Oncol. 6, 61 (2013). · DOI
  87. Masopust, D. & Schenkel, J. M. The integration of T cell migration, differentiation and function. Nat. Rev. Immunol. 13, 309–320 (2013). · DOI
  88. Huang, Y., Kim, B. Y. S., Chan, C. K., Hahn, S. M., Weissman, I. L. & Jiang, W. Improving immune–vascular crosstalk for cancer immunotherapy. Nat. Rev. Immunol. 18, 195 (2018). · DOI · Paper page
  89. Barzilai, S., Yadav, S. K., Morrell, S., Roncato, F., Klein, E., Stoler-Barak, L. et al. Leukocytes breach endothelial barriers by insertion of nuclear lobes and disassembly of endothelial actin filaments. Cell Rep. 18, 685–699 (2017). · DOI
  90. Dvorak, H. F. Tumors: wounds that do not heal—a historical perspective with a focus on the fundamental roles of increased vascular permeability and clotting. Semin. Thromb. Hemost. 45, 576–592 (2019). · DOI
  91. Mpekris, F., Voutouri, C., Baish, J. W., Duda, D. G., Munn, L. L., Stylianopoulos, T. et al. Combining microenvironment normalization strategies to improve cancer immunotherapy. Proc. Natl Acad. Sci. USA 117, 3728 (2020). · DOI
  92. Noman, M. Z., Hasmim, M., Messai, Y., Terry, S., Kieda, C., Janji, B. et al. Hypoxia: a key player in antitumor immune response. A Review in the theme: cellular responses to hypoxia. Am. J. Physiol. Cell Physiol. 309, C569–C579 (2015). · DOI
  93. Doedens, A. L., Stockmann, C., Rubinstein, M. P., Liao, D., Zhang, N., DeNardo, D. G. et al. Macrophage expression of hypoxia-inducible factor-1 alpha suppresses T-cell function and promotes tumor progression. Cancer Res. 70, 7465–7475 (2010). · DOI · Paper page
  94. McEver, R. P. & Zhu, C. Rolling cell adhesion. Annu. Rev. Cell Dev. Biol. 26, 363–396 (2010). · DOI
  95. Huang, H., Langenkamp, E., Georganaki, M., Loskog, A., Fuchs, P. F., Dieterich, L. C. et al. VEGF suppresses T-lymphocyte infiltration in the tumor microenvironment through inhibition of NF-kappaB-induced endothelial activation. Faseb J. 29, 227–238 (2015). · DOI
  96. Pardoll, D. M. The blockade of immune checkpoints in cancer immunotherapy. Nat. Rev. Cancer 12, 252–264 (2012). · DOI · Paper page
  97. Li, Y., Li, F., Jiang, F., Lv, X., Zhang, R., Lu, A. et al. A mini-review for cancer immunotherapy: molecular understanding of PD-1/PD-L1 pathway: translational blockade of immune checkpoints. Int. J. Mol. Sci. 17, 1151 (2016). · DOI
  98. Carter, T., Shaw, H., Cohn-Brown, D., Chester, K. & Mulholland, P. Ipilimumab and bevacizumab in glioblastoma. Clin. Oncol. 28, 622–626 (2016). · DOI
  99. Wu, X., Li, J., Connolly, E. M., Liao, X., Ouyang, J., Giobbie-Hurder, A. et al. Combined anti-VEGF and anti-CTLA-4 therapy elicits humoral immunity to galectin-1 which is associated with favorable clinical outcomes. Cancer Immunol. Res. 5, 446–454 (2017). · DOI
  100. Di Tacchio, M., Macas, J., Weissenberger, J., Sommer, K., Bähr, O., Steinbach, J. P. et al. Tumor vessel normalization, immuno-stimulatory reprogramming, and improved survival in glioblastoma with combined inhibition of PD-1, angiopoietin-2, and VEGF. Cancer Immunol. Res. 7, 1910–1927 (2019). · DOI
  101. Davis, B. P. & Rothenberg, M. E. Eosinophils and cancer. Cancer Immunol. Res. 2, 1–8 (2014). · DOI
  102. Carretero, R., Sektioglu, I. M., Garbi, N., Salgado, O. C., Beckhove, P. & Hämmerling, G. J. Eosinophils orchestrate cancer rejection by normalizing tumor vessels and enhancing infiltration of CD8+ T cells. Nat. Immunol. 16, 609 (2015). · DOI · Paper page
  103. Sanchez, L. R., Borriello, L., Entenberg, D., Condeelis, J. S., Oktay, M. H. & Karagiannis, G. S. The emerging roles of macrophages in cancer metastasis and response to chemotherapy. J. Leukoc. Biol. 106, 259–274 (2019). · DOI
  104. Arwert, E. N., Harney, A. S., Entenberg, D., Wang, Y., Sahai, E., Pollard, J. W. et al. A unidirectional transition from migratory to perivascular macrophage is required for tumor cell intravasation. Cell Rep. 23, 1239–1248 (2018). · DOI
  105. Harney, A. S., Karagiannis, G. S., Pignatelli, J., Smith, B. D., Kadioglu, E., Wise, S. C. et al. The selective Tie2 inhibitor rebastinib blocks recruitment and function of Tie2(Hi) macrophages in breast cancer and pancreatic neuroendocrine tumors. Mol. Cancer Ther. 16, 2486–2501 (2017). · DOI
  106. Nishide, S., Matsunaga, S., Shiota, M., Yamaguchi, T., Kitajima, S., Maekawa, Y. et al. Controlling the phenotype of tumor-infiltrating macrophages via the PHD-HIF axis inhibits tumor growth in a mouse model. iScience 19, 940–954 (2019). · DOI
  107. Sato, N., Nariuchi, H., Tsuruoka, N., Nishihara, T., Beitz, J. G., Calabresi, P. et al. Actions of TNF and IFN-gamma on angiogenesis in vitro. J. Investig. Dermatol. 95, 85s–89ss (1990). · DOI
  108. Sun, T., Yang, Y., Luo, X., Cheng, Y., Zhang, M., Wang, K. et al. Inhibition of tumor angiogenesis by interferon-gamma by suppression of tumor-associated macrophage differentiation. Oncol. Res. 21, 227–235 (2014). · DOI
  109. Kwee, B. J., Seo, B. R., Najibi, A. J., Li, A. W., Shih, T.-Y., White, D. et al. Treating ischemia via recruitment of antigen-specific T cells. Sci. Adv. 5, eaav6313 (2019). · DOI
  110. Johansson-Percival, A., He, B. & Ganss, R. Immunomodulation of tumor vessels: it takes two to tango. Trends Immunol. 39, 801–814 (2018). · DOI
  111. Batchelor, T. T., Sorensen, A. G., di Tomaso, E., Zhang, W.-T., Duda, D. G., Cohen, K. S. et al. AZD2171, a pan-VEGF receptor tyrosine kinase inhibitor, normalizes tumor vasculature and alleviates edema in glioblastoma patients. Cancer Cell 11, 83–95 (2007). · DOI · Paper page
  112. Sorensen, A. G., Batchelor, T. T., Zhang, W.-T., Chen, P.-J., Yeo, P., Wang, M. et al. A “vascular normalization index” as potential mechanistic biomarker to predict survival after a single dose of cediranib in recurrent glioblastoma patients. Cancer Res. 69, 5296–5300 (2009). · DOI
  113. Batchelor, T. T., Gerstner, E. R., Emblem, K. E., Duda, D. G., Kalpathy-Cramer, J., Snuderl, M. et al. Improved tumor oxygenation and survival in glioblastoma patients who show increased blood perfusion after cediranib and chemoradiation. Proc. Natl Acad. Sci. USA 110, 19059–19064 (2013). · DOI
  114. von Baumgarten, L., Brucker, D., Tirniceru, A., Kienast, Y., Grau, S., Burgold, S. et al. Bevacizumab has differential and dose-dependent effects on glioma blood vessels and tumor cells. Clin. Cancer Res. 17, 6192–6205 (2011). · DOI
  115. Keunen, O., Johansson, M., Oudin, A., Sanzey, M., Rahim, S. A., Fack, F. et al. Anti-VEGF treatment reduces blood supply and increases tumor cell invasion in glioblastoma. Proc. Natl Acad. Sci. USA 108, 3749–3754 (2011). · DOI
  116. Li, Y., Ali, S., Clarke, J. & Cha, S. Bevacizumab in recurrent glioma: patterns of treatment failure and implications. Brain Tumor Res. Treat. 5, 1–9 (2017). · DOI
  117. Claes, A., Wesseling, P., Jeuken, J., Maass, C., Heerschap, A. & Leenders, W. P. Antiangiogenic compounds interfere with chemotherapy of brain tumors due to vessel normalization. Mol. Cancer Ther. 7, 71–78 (2008). · DOI
  118. Boujelben, A., Watson, M., McDougall, S., Yen, Y.-F., Gerstner, E. R., Catana, C. et al. Multimodality imaging and mathematical modelling of drug delivery to glioblastomas. Interface Focus 6, 20160039 (2016). · DOI
  119. Donnem, T., Reynolds, A. R., Kuczynski, E. A., Gatter, K., Vermeulen, P. B., Kerbel, R. S. et al. Non-angiogenic tumours and their influence on cancer biology. Nat. Rev. Cancer 18, 323–336 (2018). · DOI
  120. García-Gómez, P. & Valiente, M. Vascular co-option in brain metastasis. Angiogenesis 23, 3–8 (2020). · DOI
  121. Holash, J., Maisonpierre, P. C., Compton, D., Boland, P., Alexander, C. R., Zagzag, D. et al. Vessel cooption, regression, and growth in tumors mediated by angiopoietins and VEGF. Science 284, 1994 (1999). · DOI
  122. Reymond, N., Im, J. H., Garg, R., Vega, F. M., Borda d’Agua, B., Riou, P. et al. Cdc42 promotes transendothelial migration of cancer cells through β1 integrin. J. Cell Biol. 199, 653–668 (2012). · DOI
  123. Watkins, S., Robel, S., Kimbrough, I. F., Robert, S. M., Ellis-Davies, G. & Sontheimer, H. Disruption of astrocyte-vascular coupling and the blood-brain barrier by invading glioma cells. Nat. Commun. 5, 4196 (2014). · DOI
  124. Jezzard, P., Matthews, P. M. & Smith, S. M. Functional Magnetic Resonance Imaging: An Introduction to Methods (Oxford University Press, 2001). · DOI
  125. Yang, J., Zhang, G., Li, Q., Liao, C., Huang, L., Ke, T. et al. Photoacoustic imaging for the evaluation of early tumor response to antivascular treatment. Quant. Imaging Med. Surg. 9, 160–170 (2019). · DOI
  126. Brown, E., Brunker, J. & Bohndiek, S. E. Photoacoustic imaging as a tool to probe the tumour microenvironment. Dis. Model. Mech. 12, dmm039636 (2019). · DOI
  127. Matsumoto, S., Saito, K., Takakusagi, Y., Matsuo, M., Munasinghe, J. P., Morris, H. D. et al. In vivo imaging of tumor physiological, metabolic, and redox changes in response to the anti-angiogenic agent sunitinib: longitudinal assessment to identify transient vascular renormalization. Antioxid. Redox Signal 21, 1145–1155 (2014). · DOI
  128. Xu, S., Han, P., Huang, M., Wu, J. C., Chang, C., Tsao, P. S. et al. In vivo, ex vivo, and in vitro studies on apelin’s effect on myocardial glucose uptake. Peptides 37, 320–326 (2012). · DOI
  129. Cox, C. M., D’Agostino, S. L., Miller, M. K., Heimark, R. L. & Krieg, P. A. Apelin, the ligand for the endothelial G-protein-coupled receptor, APJ, is a potent angiogenic factor required for normal vascular development of the frog embryo. Dev. Biol. 296, 177–189 (2006). · DOI
  130. Eyries, M., Siegfried, G., Ciumas, M., Montagne, K., Agrapart, M., Lebrin, F. et al. Hypoxia-induced apelin expression regulates endothelial cell proliferation and regenerative angiogenesis. Circ Res. 103, 432–440 (2008). · DOI
  131. Zhang, L., Takara, K., Yamakawa, D., Kidoya, H. & Takakura, N. Apelin as a marker for monitoring the tumor vessel normalization window during antiangiogenic therapy. Cancer Sci. 107, 36–44 (2016). · DOI
  132. Yamakawa, D., Jia, W., Kidoya, H., Hosojima, S., Torigata, M., Zhang, L. et al. Visualization of proliferative vascular endothelial cells in tumors in vivo by imaging their partner of Sld5-1 promoter activity. Am. J. Pathol. 188, 1300–1314 (2018). · DOI
  133. Boumahdi, S. & de Sauvage, F. J. The great escape: tumour cell plasticity in resistance to targeted therapy. Nat Rev. Drug Discov. 19, 39–56 (2020). · DOI
  134. Standring, S., Standring, S. & Gray, H. Gray’s Anatomy E-Book: The Anatomical Basis of Clinical Practice (Elsevier, 2015).
  135. Aird, W. C. Endothelial cell heterogeneity. Cold Spring Harb. Perspect. Med. 2, a006429 (2012). · DOI
  136. Hida, K., Hida, Y., Amin, D. N., Flint, A. F., Panigrahy, D., Morton, C. C. et al. Tumor-associated endothelial cells with cytogenetic abnormalities. Cancer Res. 64, 8249 (2004). · DOI

Cited by

Sorted by citations

See all 146

Metadata

Authors
Magnussen, A. L., & Mills, I. G.
Venue
British Journal of Cancer
Publisher
Springer Science and Business Media LLC
Published
2021-04-07
Volume
125
Issue
3
Pages
324-336
ISSN
  • 0007-0920
  • 1532-1827
DOI
10.1038/s41416-021-01330-z
PMC
PMC8329166
Cited by
146
References
12
Language
en
Licence

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review