The DOI matches its Crossref record; 36 of the 36 references it cites were found in a registry or an index.
Mutual regulation of tumour vessel normalization and immunostimulatory reprogramming
Open accessAbstract
Blockade of angiogenesis can retard tumour growth, but may also paradoxically increase metastasis. This paradox may be resolved by vessel normalization, which involves increased pericyte coverage, improved tumour vessel perfusion, reduced vascular permeability, and consequently mitigated hypoxia. Although these processes alter tumour progression, their regulation is poorly understood. Here we show that type 1 T helper (T H 1) cells play a crucial role in vessel normalization. Bioinformatic analyses revealed that gene expression features related to vessel normalization correlate with immunostimulatory pathways, especially T lymphocyte infiltration or activity. To delineate the causal relationship, we used various mouse models with vessel normalization or T lymphocyte deficiencies. Although disruption of vessel normalization reduced T lymphocyte infiltration as expected, reciprocal depletion or inactivation of CD4+ T lymphocytes decreased vessel normalization, indicating a mutually regulatory loop. In addition, activation of CD4+ T lymphocytes by immune checkpoint blockade increased vessel normalization. T H 1 cells that secrete interferon-γ are a major population of cells associated with vessel normalization. Patient-derived xenograft tumours growing in immunodeficient mice exhibited enhanced hypoxia compared to the original tumours in immunocompetent humans, and hypoxia was reduced by adoptive T H 1 transfer. Our findings elucidate an unexpected role of T H 1 cells in vasculature and immune reprogramming. T H 1 cells may be a marker and a determinant of both immune checkpoint blockade and anti-angiogenesis efficacy.
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.
Integrity signals
Registry
Cites
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.
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?
In the citing paper
“We previously demonstrated that vascular normalization could increase immune cells’ infiltration into tumors, and multiple studies have confirmed these findings in several tumor models (15,17-19).”
In the citing paper
“An improved vascular network favors adaptive antitumor immunity by promoting trafficking and re-localization of tumor-infiltrating lymphocytes (TILs), leading to improved outcomes of various immunotherapies, including immune checkpoint blockade (ICB) (15-20).”
In the citing paper
“There is an association of IFNγ-secreting T cells and vessel normalization (18), and IFNγ promotes the enhanced expression of adhesion molecules in endothelial cells (65).”
In the citing paper
“Lack of perfusion, tumoral hypoxia, and T-cell exclusion are considered significant resistance mechanisms (15,17-19).”
In the citing paper
“ICB of cytotoxic T lymphocyte protein 4 (CTLA-4) and PD-1 can normalize blood vessels in multiple models of transplanted breast and other tumours105.”
From Enhancing cancer immunotherapy using antiangiogenics: opportunities and challenges (2018) · cites this paper as [105]
In the citing paper
“ICB can have vessel-normalizing effects in preclinical models of breast tumours105, although the kinetics of vascular normalization are unknown.”
From Enhancing cancer immunotherapy using antiangiogenics: opportunities and challenges (2018) · cites this paper as [105]
In the citing paper
“The vascular normalization effect observed in this study was attributed to increased CD4+ type 1 T helper (TH1) cell accumulation and anticancer activity105.”
From Enhancing cancer immunotherapy using antiangiogenics: opportunities and challenges (2018) · cites this paper as [105]
In the citing paper
“This observation contrasts with the vascular normalization induced by ICB in breast cancer models105 and suggests that the vascular effects are dependent on the tumour location and/or type — a possibility that needs to be further investigated.”
From Enhancing cancer immunotherapy using antiangiogenics: opportunities and challenges (2018) · cites this paper as [105]
In the citing paper
“although the generalizability of the reciprocal regulation of tumour vessel normalization and immunostimulatory reprogramming is supported by analyses of large transcriptomic databases in human tumours, the experimental studies were limited to breast cancer models105.”
From Enhancing cancer immunotherapy using antiangiogenics: opportunities and challenges (2018) · cites this paper as [105]
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
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
Love, M. I., Huber, W., & Anders, S. (2014) · Genome Biology · doi:10.1186/s13059-014-0550-8 · Cited by 95,106
Subramanian, A., Tamayo, P., Mootha, V. K., Mukherjee, S., Ebert, B. L., Gillette, M. A., Paulovich, A., Pomeroy, S. L., Golub, T. R., Lander, E. S., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506580102 · Cited by 53,625
STAR: ultrafast universal RNA-seq aligner
Dobin, A., Davis, C. A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M., & Gingeras, T. R. (2013) · Bioinformatics · doi:10.1093/bioinformatics/bts635 · Cited by 51,709
RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome
Li, B., & Dewey, C. N. (2011) · BMC Bioinformatics · doi:10.1186/1471-2105-12-323 · Cited by 22,179
Robust enumeration of cell subsets from tissue expression profiles
Newman, A. M., Liu, C. L., Green, M. R., Gentles, A. J., Feng, W., Xu, Y., Hoang, C. D., Diehn, M., & Alizadeh, A. A. (2015) · Nature Methods · doi:10.1038/nmeth.3337 · Cited by 13,224
REVIGO summarizes and visualizes long lists of gene ontology terms
Supek, F., Bošnjak, M., Škunca, N., & Šmuc, T. (2011) · PLoS ONE · doi:10.1371/journal.pone.0021800 · Cited by 6,264
The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups
METABRIC Group, Curtis, C., Shah, S. P., Chin, S.-F., Turashvili, G., Rueda, O. M., Dunning, M. J., Speed, D., Lynch, A. G., Samarajiwa, S., et al. (2012) · Nature · doi:10.1038/nature10983 · Cited by 6,097
Molecular mechanisms and clinical applications of angiogenesis
Carmeliet, P., & Jain, R. K. (2011) · Nature · doi:10.1038/nature10144 · Cited by 5,467
KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases
Xie, C., Mao, X., Huang, J., Ding, Y., Wu, J., Dong, S., Kong, L., Gao, G., Li, C., & Wei, L. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr483 · Cited by 5,078
Systematic RNA interference reveals that oncogenic KRAS-driven cancers require TBK1
Barbie, D. A., Tamayo, P., Boehm, J. S., Kim, S. Y., Moody, S. E., Dunn, I. F., Schinzel, A. C., Sandy, P., Meylan, E., Scholl, C., et al. (2009) · Nature · doi:10.1038/nature08460 · Cited by 3,922
Flagged first, then by citations
Cited by
Sorted by citations
The biology and management of non-small cell lung cancer
Herbst, R. S., Morgensztern, D., & Boshoff, C. (2018) · Nature · doi:10.1038/nature25183 · Cited by 4,891
Approaches to treat immune hot, altered and cold tumours with combination immunotherapies
Galon, J., & Bruni, D. (2019) · Nature Reviews Drug Discovery · doi:10.1038/s41573-018-0007-y · Cited by 3,520
Enhancing cancer immunotherapy using antiangiogenics: opportunities and challenges
Fukumura, D., Kloepper, J., Amoozgar, Z., Duda, D. G., & Jain, R. K. (2018) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2018.29 · Cited by 2,027
Microenvironmental regulation of tumour angiogenesis
De Palma, M., Biziato, D., & Petrova, T. V. (2017) · Nature Reviews Cancer · doi:10.1038/nrc.2017.51 · Cited by 1,847
Phenotype molding of stromal cells in the lung tumor microenvironment
Lambrechts, D., Wauters, E., Boeckx, B., Aibar, S., Nittner, D., Burton, O., Bassez, A., Decaluwé, H., Pircher, A., Van den Eynde, K., et al. (2018) · Nature Medicine · doi:10.1038/s41591-018-0096-5 · Cited by 1,648
IFNγ: signalling, epigenetics and roles in immunity, metabolism, disease and cancer immunotherapy
Ivashkiv, L. B. (2018) · Nature reviews. Immunology · doi:10.1038/s41577-018-0029-z · Cited by 1,418
Zeng, D., Li, M., Zhou, R., Zhang, J., Sun, H., Shi, M., Bin, J., Liao, Y., Rao, J., & Liao, W. (2019) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-18-0436 · Cited by 986
“These data offer mechanistic insights into the responses to immune-checkpoint blockade, suggesting that response to PD-L1 and PD-1 blockade is not only related to enhanced cytolytic activity, antigen processing, and IFNg pathway components (13, 75), but is also associated with inhibition of fibroblast activation, angi…”
BackgroundPancreatic cancer stroma: an update on therapeutic targeting strategies
Hosein, A. N., Brekken, R. A., & Maitra, A. (2020) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-020-0300-1 · Cited by 950
Regulatory mechanisms of PD-1/PD-L1 in cancers
Lin, X., Kang, K., Chen, P., Zeng, Z., Li, G., Xiong, W., Yi, M., & Xiang, B. (2024) · Molecular Cancer · doi:10.1186/s12943-024-02023-w · Cited by 909
Control of Metastasis by NK Cells
López‐Soto, A., Gonzalez, S. R., Smyth, M. J., & Galluzzi, L. (2017) · Cancer Cell · doi:10.1016/j.ccell.2017.06.009 · Cited by 744
Cold and hot tumors: from molecular mechanisms to targeted therapy
Wu, B., Zhang, B., Li, B., Wu, H., & Jiang, M. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-01979-x · Cited by 811
Lee, W. S., Yang, H., Chon, H. J., & Kim, C. (2020) · Experimental & Molecular Medicine · doi:10.1038/s12276-020-00500-y · Cited by 736
Improving cancer immunotherapy using nanomedicines: progress, opportunities and challenges
Martin, J. D., Cabral, H., Stylianopoulos, T., & Jain, R. K. (2020) · Nature Reviews Clinical Oncology · doi:10.1038/s41571-019-0308-z · Cited by 691
Improving immunotherapy outcomes with anti-angiogenic treatments and vice versa
Khan, K. A., & Kerbel, R. S. (2018) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2018.9 · Cited by 670
Defining the role of the tumor vasculature in antitumor immunity and immunotherapy
Schaaf, M. B., Garg, A. D., & Agostinis, P. (2018) · Cell Death & Disease · doi:10.1038/s41419-017-0061-0 · Cited by 629
Synergistic effect of immune checkpoint blockade and anti-angiogenesis in cancer treatment
Yi, M., Jiao, D., Qin, S., Chu, Q., Wu, K., & Li, A. (2019) · Molecular Cancer · doi:10.1186/s12943-019-0974-6 · Cited by 608
The hallmarks of successful anticancer immunotherapy
Galluzzi, L., Chan, T. A., Kroemer, G., Wolchok, J. D., & López-Soto, A. (2018) · Science Translational Medicine · doi:10.1126/scitranslmed.aat7807 · Cited by 575
Improving immune–vascular crosstalk for cancer immunotherapy
Huang, Y., Kim, B. Y. S., Chan, C. K., Hahn, S. M., Weissman, I. L., & Jiang, W. (2018) · Nature Reviews Immunology · doi:10.1038/nri.2017.145 · Cited by 563
Normalizing Function of Tumor Vessels: Progress, Opportunities, and Challenges
Martin, J. D., Seano, G., & Jain, R. K. (2019) · Annual Review of Physiology · doi:10.1146/annurev-physiol-020518-114700 · Cited by 530
Tumor Angiogenesis and Anti-Angiogenic Strategies for Cancer Treatment
Teleanu, R. I., Chircov, C., Grumezescu, A. M., & Teleanu, D. M. (2019) · Journal of Clinical Medicine · doi:10.3390/jcm9010084 · Cited by 523
Speiser, D. E., Chijioke, O., Schaeuble, K., & Münz, C. (2023) · Nature Cancer · doi:10.1038/s43018-023-00521-2 · Cited by 514
Predictive markers of anti-VEGF and emerging role of angiogenesis inhibitors as immunotherapeutics
Hegde, P. S., Wallin, J. J., & Mancao, C. (2017) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2017.12.002 · Cited by 455
Stromal cell diversity associated with immune evasion in human triple‐negative breast cancer
Wu, S. Z., Roden, D. L., Wang, C., Holliday, H., Harvey, K., Cazet, A., Murphy, K. J., Pereira, B., Al‐Eryani, G., Bartoniček, N., et al. (2020) · The EMBO Journal · doi:10.15252/embj.2019104063 · Cited by 454
Shigeta, K., Datta, M., Hato, T., Kitahara, S., Chen, I. X., Matsui, A., Kikuchi, H., Mamessier, É., Aoki, S., Ramjiawan, R. R., et al. (2019) · Hepatology · doi:10.1002/hep.30889 · Cited by 415
Perspective on Oncogenic Processes at the End of the Beginning of Cancer Genomics
Ding, L., Bailey, M. H., Porta-Pardo, E., Thorsson, V., Colaprico, A., Bertrand, D., Gibbs, D. L., Weerasinghe, A., Huang, K.-L., Tokheim, C., et al. (2018) · Cell · doi:10.1016/j.cell.2018.03.033 · Cited by 399
Huinen, Z. R., Huijbers, E. J. M., B, J. R. V. B., Nowak-Sliwinska, P. M., & Griffioen, A. W. (2021) · Nature Reviews Clinical Oncology · doi:10.1038/s41571-021-00496-y · Cited by 415
HIFs, angiogenesis, and metabolism: Elusive enemies in breast cancer
de Heer, E. C., Jalving, M., & Harris, A. L. (2020) · Journal of Clinical Investigation · doi:10.1172/jci137552 · Cited by 372
The Current Landscape of Immune Checkpoint Blockade in Hepatocellular Carcinoma
Pinter, M., Jain, R. K., & Duda, D. G. (2020) · JAMA Oncology · doi:10.1001/jamaoncol.2020.3381 · Cited by 352
Endothelial Cell Metabolism in Health and Disease
Rohlenová, K., Veys, K., Santos, I. M., Bock, K. D., & Carmeliet, P. (2017) · Trends in Cell Biology · doi:10.1016/j.tcb.2017.10.010 · Cited by 351
Kim, I. S., Gao, Y., Welte, T., Wang, H., Liu, J., Janghorban, M., Sheng, K., Niu, Y., Goldstein, A., Zhao, N., et al. (2019) · Nature Cell Biology · doi:10.1038/s41556-019-0373-7 · Cited by 340
Self-citationTumor-specific cytolytic CD4 T cells mediate immunity against human cancer
Cachot, A., Bilous, M., Liu, Y., Li, X., Saillard, M., Cenerenti, M., Rockinger, G. A., Wyss, T., Guillaume, P., Schmidt, J., et al. (2021) · Science Advances · doi:10.1126/sciadv.abe3348 · Cited by 340
Immunogenic chemotherapy: Dose and schedule dependence and combination with immunotherapy
Wu, J., & Waxman, D. J. (2018) · Cancer Letters · doi:10.1016/j.canlet.2018.01.050 · Cited by 329
Zhao, S., Ren, S., Jiang, T., Zhu, B., Li, X., Zhao, C., Jia, Y., Shi, J., Zhang, L., Liu, X., et al. (2019) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-17-0640 · Cited by 323
Innocenti, F., Ou, F.-S., Qu, X., Zemla, T. J., Niedzwiecki, D., Tam, R., Mahajan, S., Goldberg, R. M., Bertagnolli, M. M., Blanke, C. D., et al. (2019) · Journal of Clinical Oncology · doi:10.1200/jco.18.01798 · Cited by 317
STING activation reprograms tumor vasculatures and synergizes with VEGFR2 blockade
Yang, H., Lee, W. S., Kong, S. J., Kim, C. G., Kim, J. H., Chang, S. K., Kim, S., Kim, G., Chon, H. J., & Kim, C. (2019) · Journal of Clinical Investigation · doi:10.1172/jci125413 · Cited by 316
Metabolic interventions in the immune response to cancer
O’Sullivan, D., Sanin, D. E., Pearce, E. J., & Pearce, E. L. (2019) · Nature reviews. Immunology · doi:10.1038/s41577-019-0140-9 · Cited by 320
Immunity, Hypoxia, and Metabolism–the Ménage à Trois of Cancer: Implications for Immunotherapy
Riera-Domingo, C., Audigé, A., Granja, S., Cheng, W.-C., Ho, P.-C., Baltazar, F., Stockmann, C., & Mazzone, M. (2020) · Physiological Reviews · doi:10.1152/physrev.00018.2019 · Cited by 310
Integrin CD11b activation drives anti-tumor innate immunity
Schmid, M. C., Khan, S. Q., Kaneda, M. M., Pathria, P., Shepard, R. M., Louis, T. L., Anand, S., Woo, G., Leem, C. J., Faridi, M. H., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-07387-4 · Cited by 307
Combining microenvironment normalization strategies to improve cancer immunotherapy
Mpekris, F., Voutouri, C., Baish, J. W., Duda, D. G., Munn, L. L., Stylianopoulos, T., & Jain, R. K. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1919764117 · Cited by 297
Hack, S. P., Zhu, A. X., & Wang, Y. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.598877 · Cited by 286
Angiogenesis as a hallmark of solid tumors - clinical perspectives
Majidpoor, J., & Mortezaee, K. (2021) · Cellular Oncology · doi:10.1007/s13402-021-00602-3 · Cited by 276
Song, Y., Fu, Y., Xie, Q., Zhu, B., Wang, J., & Zhang, B. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01956 · Cited by 273
Immune Checkpoint Inhibitors in Non-Small Cell Lung Cancer: Progress, Challenges, and Prospects
Tang, S., Qin, C., Hu, H., Liu, T., He, Y., Guo, H., Yan, H., Zhang, J., Tang, S., & Zhou, H. (2022) · Cells · doi:10.3390/cells11030320 · Cited by 273
Metabolic reprogramming and therapeutic resistance in primary and metastatic breast cancer
Liu, S., Zhang, X., Wang, W., Li, X., Sun, X., Zhao, Y., Wang, Q., Li, Y., Hu, F., & Ren, H. (2024) · Molecular Cancer · doi:10.1186/s12943-024-02165-x · Cited by 300
Self-citationVisualizing Engrafted Human Cancer and Therapy Responses in Immunodeficient Zebrafish
Yan, C., Brunson, D. C., Tang, Q., Do, D., Iftimia, N. A., Moore, J. C., Hayes, M. N., Welker, A. M., Garcia, E. G., Dubash, T. D., et al. (2019) · Cell · doi:10.1016/j.cell.2019.04.004 · Cited by 242
Lenz, H.-J., Ou, F.-S., Venook, A. P., Hochster, H. S., Niedzwiecki, D., Goldberg, R. M., Mayer, R. J., Bertagnolli, M. M., Blanke, C. D., Zemla, T., et al. (2019) · Journal of Clinical Oncology · doi:10.1200/jco.18.02258 · Cited by 246
Increased vessel perfusion predicts the efficacy of immune checkpoint blockade
Zheng, X., Fang, Z., Liu, X., Deng, S., Zhou, P., Wang, X., Zhang, C., Yin, R., Hu, H., Chen, X., et al. (2018) · Journal of Clinical Investigation · doi:10.1172/jci96582 · Cited by 239
Autophagy in endothelial cells and tumor angiogenesis
Schaaf, M. B. E., Houbaert, D., Meçe, O., & Agostinis, P. (2019) · Cell Death and Differentiation · doi:10.1038/s41418-019-0287-8 · Cited by 234
Remodeling the Tumor Microenvironment with Emerging Nanotherapeutics
Chen, Q., Liu, G., Liu, S., Su, H., Wang, Y., Li, J., & Luo, C. (2017) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2017.10.009 · Cited by 228
Phase 1b Study of Sintilimab Plus Anlotinib as First-line Therapy in Patients With Advanced NSCLC
Chu, T., Zhong, R., Zhong, H., Zhang, B., Zhang, W., Shi, C., Qian, J., Zhang, Y., Chang, Q., Zhang, X., et al. (2021) · Journal of Thoracic Oncology · doi:10.1016/j.jtho.2020.11.026 · Cited by 227
Self-citationTertiary lymphoid structures in diseases: immune mechanisms and therapeutic advances
Zhao, L., Jin, S., Wang, S., Zhang, Z., Wang, X., Chen, Z., Wang, X., Huang, S., Zhang, D., & Wu, H. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-01947-5 · Cited by 261
Immune determinants of the pre-metastatic niche
Pătraș, L., Shaashua, L., Matei, I. R., & Lyden, D. C. (2023) · Cancer Cell · doi:10.1016/j.ccell.2023.02.018 · Cited by 229
Neutrophils and Snail Orchestrate the Establishment of a Pro-tumor Microenvironment in Lung Cancer
Faget, J., Groeneveld, S., Boivin, G., Sankar, M., Zangger, N., Garcia, M., Guex, N., Zlobec, I., Steiner, L., Piersigilli, A., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.11.052 · Cited by 225
Anti-Angiogenics: Current Situation and Future Perspectives
Zirlik, K., & Duyster, J. (2018) · Oncology Research and Treatment · doi:10.1159/000488087 · Cited by 218
Zhou, Y., Chen, X., Cao, J., & Gao, H. (2020) · Journal of Materials Chemistry B · doi:10.1039/d0tb00649a · Cited by 213
He, Z., & Zhang, S. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.741305 · Cited by 207
ten Hoorn, S., de Back, T. R., Sommeijer, D. W., & Vermeulen, L. (2022) · JNCI: Journal of the National Cancer Institute · doi:10.1093/jnci/djab106 · Cited by 203
Reshaping the Tumor Stroma for Treatment of Pancreatic Cancer
Vennin, C., Murphy, K. J., Morton, J. P., Cox, T. R., Pajic, M., & Timpson, P. (2017) · Gastroenterology · doi:10.1053/j.gastro.2017.11.280 · Cited by 207
Lan, Y., Moustafa, M., Knoll, M., Xu, C., Furkel, J., Lazorchak, A. S., Yeung, T.-L., Hasheminasab, S.-M., Jenkins, M. H., Meister, S., et al. (2021) · Cancer Cell · doi:10.1016/j.ccell.2021.08.008 · Cited by 211
Gao, S., Yang, D., Fang, Y., Lin, X., Jin, X., Wang, Q., Wang, X., Ke, L., & Shi, K. (2018) · Theranostics · doi:10.7150/thno.29431 · Cited by 200
Opposing Roles of Type I Interferons in Cancer Immunity
Boukhaled, G. M., Harding, S. M., & Brooks, D. G. (2020) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev-pathol-031920-093932 · Cited by 208
A nitric-oxide driven chemotactic nanomotor for enhanced immunotherapy of glioblastoma
Chen, H., Li, T., Liu, Z., Tang, S., Tong, J., Tao, Y., Zhao, Z., Li, N., Mao, C., Shen, J., et al. (2023) · Nature Communications · doi:10.1038/s41467-022-35709-0 · Cited by 198
Vascular regulation of antitumor immunity
Munn, L. L., & Jain, R. K. (2019) · Science · doi:10.1126/science.aaw7875 · Cited by 194
Targeting the tumour vasculature: from vessel destruction to promotion
Guelfi, S., Hodivala‐Dilke, K., & Bergers, G. (2024) · Nature reviews. Cancer · doi:10.1038/s41568-024-00736-0 · Cited by 216
Liu, S., Qin, T., Liu, Z., Wang, J., Jia, Y., Feng, Y., Gao, Y., & Li, K. (2020) · Cell Death and Disease · doi:10.1038/s41419-020-2511-3 · Cited by 192
TGF-β suppresses type 2 immunity to cancer
Liu, M., Kuo, F., Capistrano, K. J., Kang, D., Nixon, B. G., Shi, W., Chou, C., Do, M. H., Stamatiades, E. G., Gao, S., et al. (2020) · Nature · doi:10.1038/s41586-020-2836-1 · Cited by 193
Donlon, N., Power, R. F., Hayes, C., Reynolds, J. V., & Lysaght, J. (2021) · Cancer Letters · doi:10.1016/j.canlet.2020.12.045 · Cited by 199
Choi, Y., & Jung, K. (2023) · Experimental & Molecular Medicine · doi:10.1038/s12276-023-01114-w · Cited by 188
Gomes-Santos, I. L., Amoozgar, Z., Kumar, A. S., Ho, W. W., Roh, K., Talele, N. P., Curtis, H., Kawaguchi, K., Jain, R. K., & Fukumura, D. (2021) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-20-0499 · Cited by 181
The Reciprocity between Radiotherapy and Cancer Immunotherapy
Wang, Y., Liu, Z.-G., Yuan, H., Deng, W., Li, J., Huang, Y.-H., Kim, B. Y. S., Story, M. D., & Jiang, W. (2018) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-18-2581 · Cited by 184
Nagl, L., Horvath, L., Pircher, A., & Wolf, D. G. F. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00766 · Cited by 189
Tumor microenvironment and radioresistance
Suwa, T., Kobayashi, M., Nam, J., & Harada, H. (2021) · Experimental & Molecular Medicine · doi:10.1038/s12276-021-00640-9 · Cited by 186
Galectin-1–driven T cell exclusion in the tumor endothelium promotes immunotherapy resistance
Nambiar, D. K., Aguilera, T. A., Cao, H., Kwok, S., Kong, C. S., Bloomstein, J. D., Wang, Z., Rangan, V. S., Jiang, D., von Eyben, R., et al. (2019) · Journal of Clinical Investigation · doi:10.1172/jci129025 · Cited by 176
Multiscale Agent-Based and Hybrid Modeling of the Tumor Immune Microenvironment
Norton, K., Gong, C., Jamalian, S., & Popel, A. S. (2019) · Processes · doi:10.3390/pr7010037 · Cited by 178
Deng, H., Kan, A., Lyu, N., Mu, L., Han, Y., Liu, L., Zhang, Y., Duan, Y., Liao, S., Li, S., et al. (2020) · Liver Cancer · doi:10.1159/000505695 · Cited by 173
Meder, L., Schuldt, P., Thelen, M., Schmitt, A., Dietlein, F., Klein, S., Borchmann, S., Wennhold, K., Vlašić, I., Oberbeck, S., et al. (2018) · Cancer Research · doi:10.1158/0008-5472.can-17-2176 · Cited by 176
Pericytes augment glioblastoma cell resistance to temozolomide through CCL5-CCR5 paracrine signaling
Zhang, X., Yang, K., Chen, C., He, Z., Wang, Q., Feng, H., Lv, S., Wang, Y., Mao, M., Liu, Q., et al. (2021) · Cell Research · doi:10.1038/s41422-021-00528-3 · Cited by 173
Self-citationChafe, S. C., McDonald, P. C., Saberi, S., Nemirovsky, O., Venkateswaran, G., Burugu, S., Gao, D., Delaidelli, A., Kyle, A. H., Baker, J. H. E., et al. (2019) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-18-0657 · Cited by 168
Strategies to Improve the Antitumor Effect of Immunotherapy for Hepatocellular Carcinoma
Xing, R., Gao, J., Cui, Q., & Wang, Q. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.783236 · Cited by 172
The Era of Cytotoxic CD4 T Cells
Cenerenti, M., Saillard, M., Romero, P. J., & Jandus, C. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.867189 · Cited by 184
Platelet glycoprotein VI promotes metastasis through interaction with cancer cell-derived Galectin-3
Mammadova‐Bach, E., Gil‐Pulido, J., Sarukhanyan, E., Burkard, P., Shityakov, S., Schonhart, C., Stegner, D., Remer, K. A., Nurden, P., Nurden, A. T., et al. (2020) · Blood · doi:10.1182/blood.2019002649 · Cited by 165
Wang, Z., Li, Z., Sun, Z., Wang, S., Ali, Z., Zhu, S., Liu, S., Ren, Q., Sheng, F., Wang, B., et al. (2020) · Science Advances · doi:10.1126/sciadv.abc8733 · Cited by 164
Macrophage correlates with immunophenotype and predicts anti-PD-L1 response of urothelial cancer
Zeng, D., Ye, Z., Wu, J., Zhou, R., Fan, X., Wang, G., Huang, Y., Wu, J., Sun, H., Wang, M., et al. (2020) · Theranostics · doi:10.7150/thno.46176 · Cited by 157
Pericytes in the tumor microenvironment
Jiang, Z., Zhou, J., Li, L., Liao, S., He, J., Zhou, S., & Zhou, Y. (2023) · Cancer Letters · doi:10.1016/j.canlet.2023.216074 · Cited by 168
Microenvironmental Metabolism Regulates Antitumor Immunity
Ngwa, V. M., Edwards, D. N., Philip, M., & Chen, J. (2019) · Cancer Research · doi:10.1158/0008-5472.can-19-0617 · Cited by 156
Sun, Y., Chen, W., Torphy, R. J., Yao, S., Zhu, G., Lin, R., Lugano, R., Miller, E. N., Fujiwara, Y., Bian, L., et al. (2021) · Science Translational Medicine · doi:10.1126/scitranslmed.abc8922 · Cited by 165
Wang, H., Wang, Z., Zhang, Z., Liu, J., & Li, H. (2023) · Advances in Nutrition · doi:10.1016/j.advnut.2023.05.013 · Cited by 171
Self-citationEndothelial DGKG promotes tumor angiogenesis and immune evasion in hepatocellular carcinoma
Zhang, L., Xu, J., Zhou, S., Yao, F., Zhang, R., You, W., Dai, J., Yu, K., Zhang, Y., Baheti, T., et al. (2023) · Journal of Hepatology · doi:10.1016/j.jhep.2023.10.006 · Cited by 160
Low-Dose Anti-Angiogenic Therapy Sensitizes Breast Cancer to PD-1 Blockade
Li, Q., Wang, Y., Jia, W., Deng, H., Li, G., Deng, W., Chen, J., Kim, B. Y. S., Jiang, W., Liu, Q., et al. (2019) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-19-2179 · Cited by 156
Shigeta, K., Matsui, A., Kikuchi, H., Klein, S., Mamessier, É., Chen, I. X., Aoki, S., Kitahara, S., Inoue, K., Shigeta, A., et al. (2020) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2020-001435 · Cited by 148
Su, Y., Luo, B., Lu, Y., Wang, D., Yan, J. Y., Zheng, J., Xiao, J. H., Wang, Y., Xue, Z., Yin, J., et al. (2021) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-21-2241 · Cited by 153
Endothelial cells in tumor microenvironment: insights and perspectives
Leone, P., Malerba, E., Susca, N., Favoino, E., Perosa, F., Brunori, G., Prete, M., & Racanelli, V. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1367875 · Cited by 158
Chen, H., Shi, T., Wang, Y., Liu, Z., Liu, F., Zhang, H., Wang, X., Miao, Z., Liu, B., Wan, M., et al. (2021) · Journal of the American Chemical Society · doi:10.1021/jacs.1c03071 · Cited by 144
Immune regulation of metastasis: mechanistic insights and therapeutic opportunities
Blomberg, O. S., Spagnuolo, L., & de Visser, K. E. (2018) · Disease Models & Mechanisms · doi:10.1242/dmm.036236 · Cited by 145
Vascular normalisation as the stepping stone into tumour microenvironment transformation
Magnussen, A. L., & Mills, I. G. (2021) · British Journal of Cancer · doi:10.1038/s41416-021-01330-z · Cited by 146
Liu, L., Bai, H., Wang, C., Seery, S., Wang, Z., Duan, J., Li, S., Xue, P., Wang, G., Sun, Y., et al. (2021) · Journal of Thoracic Oncology · doi:10.1016/j.jtho.2021.03.016 · Cited by 140
Self-citationHypoxia‐Inducible Exosomes Facilitate Liver‐Tropic Premetastatic Niche in Colorectal Cancer
Sun, H., Meng, Q., Shi, C., Yang, H., Li, X., Wu, S., Familiari, G., Relucenti, M., Aschner, M., Wang, X., et al. (2021) · Hepatology · doi:10.1002/hep.32009 · Cited by 144
Hill, B. S., Sarnella, A., D’Avino, G., & Zannetti, A. (2019) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2019.07.028 · Cited by 142
Tyrosine kinase inhibitors and immunotherapy combinations in renal cell carcinoma
Rassy, E., Flippot, R., & Albiges, L. K. (2020) · Therapeutic Advances in Medical Oncology · doi:10.1177/1758835920907504 · Cited by 136
Ju, W., Xia, R., Zhu, D., Dou, S., Zhu, G., Dong, M., Wang, L., Sun, Q., Zhao, T., Zhou, Z., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-33080-8 · Cited by 143
Metadata
- Authors
- Tian, L., Goldstein, A., Wang, H., Ching Lo, H., Sun Kim, I., Welte, T., Sheng, K., Dobrolecki, L. E., Zhang, X., Putluri, N., Phung, T. L., Mani, S. A., Stossi, F., Sreekumar, A., Mancini, M. A., Decker, W. K., Zong, C., Lewis, M. T., & Zhang, X. H.-F.
- Affiliations
- Baylor College of Medicine (US)
- The University of Texas MD Anderson Cancer Center (US)
- Corresponding author
- Zhang, Xiaomei
- Zhang, Xiang H.-F.
- ORCID
- Venue
- Nature
- Published
- 2017-04
- Volume
- 544
- Issue
- 7649
- Pages
- 250-254
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC5788037
- OpenAlex
- W2601414401
- Cited by
- 841
- References
- 36
- Citations by year
- 2026: 88 · 2025: 98 · 2024: 98 · 2023: 100 · 2022: 92 · 2021: 129 · 2020: 97 · 2019: 63 · 2018: 51 · 2017: 25
- FWCI
- 26.46
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Institutes of Health (1s10od016167-01)
- National Cancer Institute (R00CA151293, R01CA220297, K99CA151293, R21CA185516, U01CA179674, R01CA183878, P30CA125123)
- National Institute of Allergy and Infectious Diseases (P30AI036211, R01AI127387)
- National Institute of Diabetes and Digestive and Kidney Diseases (P30DK056338)
- National Center for Research Resources (S10RR024574)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Health Sciences › Medicine › Oncology › Lymphatic System and Diseases
- Keywords
- tumor immunosuppression, pericyte coverage, tumor hypoxia, CD4+ T cells, Th1 cells, interferon-gamma, immune checkpoint blockade, anti-angiogenic therapy, T cell infiltration, endothelial cells, tumor vasculature, patient-derived xenografts, cancer immunotherapy
- MeSH terms
- Animals, Capillary Permeability, Female, Humans, Interferon-gamma, Mice, Inbred BALB C, Mice, Inbred C57BL, Neoplasms, Neovascularization, Pathologic, Prognosis, CD4-Positive T-Lymphocytes, Cell Hypoxia, Lymphocytes, Tumor-Infiltrating, Th1 Cells, Neovascularization, Physiologic, Adoptive Transfer, Pericytes, Xenograft Model Antitumor Assays, Endothelial Cells, Mice
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
