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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.
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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]
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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
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Items 201–300 of 849
Fu, R., Li, Y., Jiang, N., Ren, B., Zang, C.-Z., Liu, L., Lv, W., Li, H., Weiss, S. J., Li, Z., et al. (2020) · Journal of Clinical Investigation · doi:10.1172/jci131507 · Cited by 60
Reprogramming Tumor Blood Vessels for Enhancing Immunotherapy
Schmittnaegel, M., & Palma, M. D. (2017) · Trends in cancer · doi:10.1016/j.trecan.2017.10.002 · Cited by 56
Immunotherapy resistance in non-small cell lung cancer: from mechanisms to therapeutic opportunities
Wang, H., Niu, X., Jin, Z., Zhang, S., Fan, R., Xiao, H., & Hu, S. (2025) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-025-03519-z · Cited by 72
Self-citationGao, L., Yang, X., Cheng, Y., & Zhu, H. (2019) · Frontiers in Pharmacology · doi:10.3389/fphar.2019.01173 · Cited by 57
Targeting miR-27a/VE-cadherin interactions rescues cerebral cavernous malformations in mice
Li, J., Zhao, Y., Choi, J. P., Ting, K. K., Coleman, P. R., Chen, J., Cogger, V. C., Wan, L., Shi, Z., Møller, T., et al. (2020) · PLoS Biology · doi:10.1371/journal.pbio.3000734 · Cited by 52
Stoltzfus, C. R., Sivakumar, R., Kunz, L., Olin, B. E., Menietti, E., Speziale, D., Adelfio, R., Bacac, M., Colombetti, S., Perro, M., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.726492 · Cited by 52
Angiogenesis and targeted therapy in the tumour microenvironment: From basic to clinical practice
Yang, S., Fang, Y., Ma, Y., Wang, F., Wang, Y., Jia, J., Yang, Y., Sun, W., Zhou, Q., & Li, Z. (2025) · Clinical and Translational Medicine · doi:10.1002/ctm2.70313 · Cited by 61
CD4 + T Cell Activation and Vascular Normalization: Two Sides of the Same Coin?
Palma, M. D., & Jain, R. K. (2017) · Immunity · doi:10.1016/j.immuni.2017.04.015 · Cited by 53
Jin, F., Zheng, X., Yang, Y., Yao, G., Ye, L., Doeppner, T. R., Hermann, D. M., Wang, H., & Dai, Y. (2019) · Aging · doi:10.18632/aging.101726 · Cited by 52
Self-citationQiao, M., Jiang, T., Ren, S., & Zhou, C. (2017) · Clinical Lung Cancer · doi:10.1016/j.cllc.2017.06.005 · Cited by 53
Xu, Y., Huang, Z., Lu, H., Yu, X., Li, Y., Li, W., Chen, J., Chen, M., Gong, L., Chen, K., et al. (2019) · British Journal of Cancer · doi:10.1038/s41416-019-0583-6 · Cited by 49
Apatinib enhanced anti-PD-1 therapy for colon cancer in mice via promoting PD-L1 expression
Cai, X., Wei, B., Li, L., Chen, X., Liu, W., Cui, J. T., Lin, Y., Sun, Y., Xu, Q., Guo, W., et al. (2020) · International Immunopharmacology · doi:10.1016/j.intimp.2020.106858 · Cited by 52
Li, Q., Cheng, X., Zhou, C., Tang, Y., Li, F., Zhang, B., Huang, T., Wang, J., & Tu, S. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.841977 · Cited by 50
Yang, F., Xu, G., Huang, J., Yin, Y., Xiang, W., Zhong, B., Li, W.-C., Shen, J., Zhang, S., Yang, J., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.847601 · Cited by 50
Pircher, A., Wolf, D. G. F., Heidenreich, A., Hilbe, W., Pichler, R., & Heidegger, I. M. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18112291 · Cited by 49
DLL1 orchestrates CD8 + T cells to induce long-term vascular normalization and tumor regression
Zhang, N., Yin, R., Zhou, P., Liu, X., Fan, P., Qian, L., Li, D., Zhang, C., Zheng, X., Deng, S., et al. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2020057118 · Cited by 50
Normalization in tumor ecosystem: Opportunities and challenges
Mortezaee, K. (2021) · Cell Biology International · doi:10.1002/cbin.11655 · Cited by 49
Boucher, Y., Kumar, A. S., Posada, J. M., Gjini, E., Pfaff, K. L., Lipschitz, M., Lako, A., Duda, D. G., Rodig, S. J., Hodi, F. S., et al. (2021) · npj Precision Oncology · doi:10.1038/s41698-021-00197-w · Cited by 49
Vessels that encapsulate tumour clusters vascular pattern in hepatocellular carcinoma
Liu, K., Dennis, C. V., Prince, D. S., Marsh‐Wakefield, F., Santhakumar, C., Gamble, J. R., Strasser, S. I., & McCaughan, G. W. (2023) · JHEP Reports · doi:10.1016/j.jhepr.2023.100792 · Cited by 48
Duan, J., Wang, Y., & Jiao, S. (2018) · Cancer Medicine · doi:10.1002/cam4.1722 · Cited by 47
Zheng, W., Qian, C., Tang, Y., Yang, C., Zhou, Y., Shen, P., Chen, W., Yu, S., Wei, Z., Wang, A., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.1035323 · Cited by 50
Hypoxia: Turning vessels into vassals of cancer immunotolerance
Schito, L., & Rey, S. (2020) · Cancer Letters · doi:10.1016/j.canlet.2020.05.015 · Cited by 49
Tumor Vessel Normalization: A Window to Enhancing Cancer Immunotherapy
Li, S., Zhang, Q., & Hong, Y. (2020) · Technology in Cancer Research & Treatment · doi:10.1177/1533033820980116 · Cited by 52
Xiao, Y., Zhu, T., Zeng, Q., Tan, Q., Jiang, G., & Huang, X. (2022) · Acta Biomaterialia · doi:10.1016/j.actbio.2022.11.043 · Cited by 45
Immune microenvironment of cholangiocarcinoma: Biological concepts and treatment strategies
Yu, X., Zhu, L., Wang, T., & Chen, J. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1037945 · Cited by 45
Eino, D., Tsukada, Y., Naito, H., Kanemura, Y., Iba, T., Wakabayashi, T., Muramatsu, F., Kidoya, H., Arita, H., Kagawa, N., et al. (2018) · Cancer Research · doi:10.1158/0008-5472.can-18-0498 · Cited by 45
Anti-angiogenesis: Opening a new window for immunotherapy
Guo, F., & Cui, J. (2020) · Life Sciences · doi:10.1016/j.lfs.2020.118163 · Cited by 46
The impact of hypoxia on tumor-mediated bypassing anti-PD-(L)1 therapy
Mortezaee, K., Majidpoor, J., & Kharazinejad, E. (2023) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2023.114646 · Cited by 45
Taleb, M., Atabakhshi‐Kashi, M., Wang, Y., Alanagh, H. R., Sabet, Z. F., Li, F., Cheng, K., Li, C., Qi, Y., Nie, G., et al. (2021) · Advanced Healthcare Materials · doi:10.1002/adhm.202100051 · Cited by 44
Fan, P., Qiang, H., Liu, Z., Zhao, Q., Wang, Y., Liu, T., Wang, X., Chu, T., Huang, Y., Xu, W., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.937924 · Cited by 41
Anti‐angiogenic therapy enhances cancer immunotherapy: Mechanism and clinical application
Li, A., & Fang, J. (2024) · Interdisciplinary medicine · doi:10.1002/inmd.20230025 · Cited by 46
Jiang, Z., Xiong, H., Yang, S., Lü, Y., Deng, Y., Yao, J., & Yao, J. (2020) · Advanced Healthcare Materials · doi:10.1002/adhm.202000075 · Cited by 42
A Window of Opportunity: Targeting Cancer Endothelium to Enhance Immunotherapy
Duru, G., van Egmond, M., & Heemskerk, N. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.584723 · Cited by 44
Current Advances in PD-1/PD-L1 Blockade in Recurrent Epithelial Ovarian Cancer
Zhang, Y., Cui, Q., Xu, M., Liu, D., Yao, S., & Chen, M. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.901772 · Cited by 45
Shen, R., Peng, L., Zhou, W., Wang, D., Jiang, Q., Ji, J., Hu, F., & Yuan, H. (2022) · Journal of Controlled Release · doi:10.1016/j.jconrel.2022.07.015 · Cited by 43
Wang, C., Cui, A., Bukenya, M., Aung, A., Pradhan, D., Whittaker, C. A., Agarwal, Y., Thomas, A., Liang, S., Amlashi, P., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.110021 · Cited by 43
The tumour immune microenvironment in oesophageal cancer
Davern, M., Donlon, N. E., Power, R. F., Hayes, C., King, R., Dunne, M. R., & Reynolds, J. V. (2021) · British Journal of Cancer · doi:10.1038/s41416-021-01331-y · Cited by 45
Jancewicz, I., Szarkowska, J., Konopiński, R., Stachowiak, M., Swiatek, M., Błachnio, K., Kubala, S., Oksinska, P., Cwiek, P., Rusetska, N., et al. (2021) · Cancers · doi:10.3390/cancers13164148 · Cited by 42
Panagi, M., Mpekris, F., Voutouri, C., Hadjigeorgiou, A. G., Symeonidou, C., Porfyriou, E., Michael, C., Stylianou, A., Martin, J. D., Cabral, H., et al. (2024) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-24-0246 · Cited by 47
Toward Normalization of the Tumor Microenvironment for Cancer Therapy
Zheng, J., & Gao, P. (2019) · Integrative Cancer Therapies · doi:10.1177/1534735419862352 · Cited by 42
Nano drug delivery system reconstruct tumour vasculature for the tumour vascular normalisation
Liang, Q., Zhou, L., Li, Y., Liu, J., & Liu, Y. (2021) · Journal of drug targeting · doi:10.1080/1061186x.2021.1927056 · Cited by 43
Zhu, L., Yu, X., Wang, L., Liu, J., Qu, Z., Zhang, H., Li, L., Chen, J., & Zhou, Q. (2021) · Oncogenesis · doi:10.1038/s41389-021-00335-w · Cited by 45
Yan, X., Xie, Y., Yang, F., Hua, Y., Zeng, T., Sun, C., Yang, M., Huang, X., Wu, H., Fu, Z., et al. (2021) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-021-01949-z · Cited by 41
New approaches to first-line treatment of advanced renal cell carcinoma
George, D. J., Lee, C., & Heng, D. Y. C. (2021) · Therapeutic Advances in Medical Oncology · doi:10.1177/17588359211034708 · Cited by 41
Choi, S. H., Yoo, S. S., Lee, S. Y., & Park, J. Y. (2022) · Archives of Pharmacal Research · doi:10.1007/s12272-022-01382-6 · Cited by 40
Deciphering the complexities of cancer cell immune evasion: Mechanisms and therapeutic implications
Gupta, I., Hussein, O., Sastry, K. S., Bougarn, S., Gopinath, N., Chin-Smith, E. C., Sinha, Y., Korashy, H. M., & Maccalli, C. (2023) · Advances in Cancer Biology - Metastasis · doi:10.1016/j.adcanc.2023.100107 · Cited by 39
Ai, D., Hao, S., Shen, W., Wu, Q., Zhang, S., Chen, Y., Liu, Q., Deng, J., Zhu, H., Chen, K., et al. (2024) · EClinicalMedicine · doi:10.1016/j.eclinm.2024.102471 · Cited by 39
Su, X., Li, J., Xu, X., Ye, Y., Wang, C., Pang, G., Liu, W., Liu, A., Zhao, C., & Hao, X. (2024) · Journal of Translational Medicine · doi:10.1186/s12967-024-05552-6 · Cited by 45
Automatic microscopic detection of mycobacteria in sputum: a proof-of-concept
Zingué, D., Weber, P., Soltani, F., Raoult, D., & Drancourt, M. (2018) · Scientific Reports · doi:10.1038/s41598-018-29660-8 · Cited by 38
Management of patients with intermediate stage hepatocellular carcinoma
Prince, D. S., Liu, K., Xu, W., Chen, M., Sun, J., Lu, X., & Ji, J. (2020) · Therapeutic Advances in Medical Oncology · doi:10.1177/1758835920970840 · Cited by 38
Lee, T. W., Lai, A., Harms, J. K., Singleton, D. C., Dickson, B. D., Macann, A., Hay, M. P., & Jamieson, S. M. F. (2020) · Cancers · doi:10.3390/cancers12123743 · Cited by 38
He, Y., Zhan, L., Shi, J., Xiao, M., Zuo, R., Wang, C., Liu, Z., Gong, W., Chen, L., Luo, Y., et al. (2023) · Advanced Science · doi:10.1002/advs.202207650 · Cited by 39
Jie, C., Li, R., Cheng, Y., Wang, Z., Wu, Q., & Xie, C. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1122352 · Cited by 37
Yang, J., Guo, Z., Song, M., Pan, Q., Zhao, J., Huang, Y., Han, Y., Ouyang, D., Yang, C., Chen, H., et al. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1212577 · Cited by 38
Mane, M. M., Cohen, I., Ackerstaff, E., Shalaby, K., Ijoma, J. N., Ko, M. K., Maeda, M., Albeg, A. S., Vemuri, K., Satagopan, J. M., et al. (2020) · Molecular Therapy — Oncolytics · doi:10.1016/j.omto.2020.07.006 · Cited by 37
Kurebayashi, Y., Olkowski, C. P., Lane, K. C., Vasalatiy, O. V., Xu, B., Okada, R., Furusawa, A., Choyke, P. L., Kobayashi, H., & Sato, N. (2021) · Cancer Research · doi:10.1158/0008-5472.can-20-2673 · Cited by 38
Targeted and immuno-based therapies in sarcoma: mechanisms and advances in clinical trials
Tang, F., Tie, Y., Wei, Y.-Q., Tu, C., & Wei, X. (2021) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2021.188606 · Cited by 39
The Interplay of Tumor Vessels and Immune Cells Affects Immunotherapy of Glioblastoma
Ghosh, M., Lenkiewicz, A. M., & Kaminska, B. (2022) · Biomedicines · doi:10.3390/biomedicines10092292 · Cited by 37
Ou, D., Lin, Y., Hsu, C., Lin, Y., Chen, C., Yu, J.-S., Miaw, S., Hsu, P., Cheng, A., & Hsu, C. (2018) · Liver Cancer · doi:10.1159/000489318 · Cited by 35
Bai, Y., Wang, Y., Zhang, X., Fu, J., Xing, X., Wang, C., Gao, L., Liu, Y., & Shi, L. (2019) · International Journal of Pharmaceutics · doi:10.1016/j.ijpharm.2019.118636 · Cited by 36
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Ganß, R. (2020) · Vascular Biology · doi:10.1530/vb-19-0032 · Cited by 39
Tumor Vasculature as an Emerging Pharmacological Target to Promote Anti-Tumor Immunity
Tzeng, H., & Huang, Y.-J. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24054422 · Cited by 38
Avallone, A., Piccirillo, M. C., Nasti, G., Rosati, G., Carlomagno, C., Gennaro, E. D., Romano, C., Tatangelo, F., Granata, V., Cassata, A., et al. (2021) · JAMA Network Open · doi:10.1001/jamanetworkopen.2021.18475 · Cited by 37
Daam2 driven degradation of VHL promotes gliomagenesis
Zhu, W., Krishna, S., Garcia, C., Lin, C.-C. J., Mitchell, B. D., Scott, K. L., Mohila, C., Creighton, C. J., Yoo, S. H., Lee, H. K., et al. (2017) · eLife · doi:10.7554/elife.31926 · Cited by 33
Liu, Q., Zhang, D., Qian, H., Chu, Y., Yan, Y., Shao, J., Xu, Q., & Liu, B. (2020) · International Journal of Nanomedicine · doi:10.2147/ijn.s249174 · Cited by 34
Kurebayashi, Y., Kubota, N., & Sakamoto, M. (2020) · Hepatology Research · doi:10.1111/hepr.13539 · Cited by 35
Resistance Mechanisms of Anti-angiogenic Therapy and Exosomes-Mediated Revascularization in Cancer
Zeng, Y., & Fu, B. M. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.610661 · Cited by 35
Multimodal Molecular Imaging Detects Early Responses to Immune Checkpoint Blockade
Saida, Y., Brender, J., Yamamoto, K., Mitchell, J. B., Krishna, M. C., & Kishimoto, S. (2021) · Cancer Research · doi:10.1158/0008-5472.can-20-3182 · Cited by 38
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Martin, J. D., Miyazaki, T., & Cabral, H. (2021) · Wiley Interdisciplinary Reviews Nanomedicine and Nanobiotechnology · doi:10.1002/wnan.1730 · Cited by 35
Zeng, Z., Li, J., Zhang, J., Li, Y., Liu, X., Chen, J., Huang, Z., Wu, Q., Gong, Y. Q., & Xie, C. (2021) · Journal of Translational Medicine · doi:10.1186/s12967-021-03002-1 · Cited by 34
Li, X., Yang, Y., Huang, Q., Deng, Y., Guo, F., Wang, G., & Liu, M. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.738373 · Cited by 36
Wensink, G. E., Bond, M. J. G., Küçükköse, E., May, A. M., Vink, G. R., Koopman, M., Kranenburg, O., & Roodhart, J. M. L. (2021) · Cancer Treatment Reviews · doi:10.1016/j.ctrv.2021.102174 · Cited by 35
Hill, R. M., Rocha, S., & Parsons, J. L. (2022) · Cancers · doi:10.3390/cancers14174130 · Cited by 33
Tumor endothelial cell autophagy is a key vascular‐immune checkpoint in melanoma
Verhoeven, J., Jacobs, K., Rizzollo, F., Lodi, F., Hua, Y., Poźniak, J., Srinivasan, A. N., Houbaert, D., Shankar, G., More, S., et al. (2023) · EMBO Molecular Medicine · doi:10.15252/emmm.202318028 · Cited by 35
Shaikat, A. H., Azad, S. M. A. K., Tamim, M. A. R., Ullah, M. S., Amin, M. N., Sabbir, M. K., Tarun, M. T. I., Mostaq, M. S., Sabrin, S., Mahmud, M. Z., et al. (2025) · Cancer Pathogenesis and Therapy · doi:10.1016/j.cpt.2025.07.003 · Cited by 37
Du, S. M., Yu, Y., Xu, C., Xiong, H., Yang, S., & Yao, J. (2019) · Drug Discovery Today · doi:10.1016/j.drudis.2019.06.011 · Cited by 33
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Furukawa, N., Stearns, V., Santa-Maria, C. A., & Popel, A. S. (2022) · Expert Opinion on Therapeutic Targets · doi:10.1080/14728222.2022.2170779 · Cited by 31
Boydell, E., Marinari, E., Migliorini, D., Dietrich, P., Patrikidou, A., & Dutoit, V. (2019) · Cancers · doi:10.3390/cancers11040464 · Cited by 32
Popel, A. S. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2001050117 · Cited by 32
Zhu, Q. C., Li, J., Wu, Q., Cheng, Y., Zheng, H., Zhan, T., Wang, H., Yang, Y., Wang, H., Liu, Y., et al. (2020) · Biological Research · doi:10.1186/s40659-020-0273-0 · Cited by 32
Self-citationXu, X., Chen, M.-X., Lou, X.-F., Du, Y., Shu, G., Qi, J., Zhu, M., Ying, X., Lian, Y., Ji, J., et al. (2021) · Chemical Engineering Journal · doi:10.1016/j.cej.2021.128743 · Cited by 32
Disrupting cancer angiogenesis and immune checkpoint networks for improved tumor immunity
Anderson, T. S., McCormick, A. L., Piersall, S. L., Okpalanwaka, I. F., & Lowe, D. B. (2022) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2022.02.009 · Cited by 32
Portillo, A. L., Monteiro, J. K., Rojas, E. A. P., Ritchie, T. M., Gillgrass, A. E., & Ashkar, A. A. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1286750 · Cited by 32
STIM1 overexpression in hypoxia microenvironment contributes to pancreatic carcinoma progression
Jian, W., Junling, S., Kaili, Z., Jinmeng, H., Jiuxing, D., & Jianwei, S. (2019) · Cancer Biology and Medicine · doi:10.20892/j.issn.2095-3941.2018.0304 · Cited by 31
Li, M., Zhang, Y. L., Wu, J., & Wang, K. (2020) · Current Medical Science · doi:10.1007/s11596-020-2183-3 · Cited by 31
Dey, S., Mondal, A., DuHadaway, J. B., Sutanto‐Ward, E., Laury‐Kleintop, L. D., Thomas, S., Prendergast, G. C., Mandik‐Nayak, L., & Muller, A. J. (2021) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-20-0226 · Cited by 31
Granito, A., Marinelli, S., Forgione, A., Renzulli, M., Benevento, F., Piscaglia, F., & Tovoli, F. (2021) · Journal of Hepatocellular Carcinoma · doi:10.2147/jhc.s251729 · Cited by 31
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Zhao, Y., Ting, K. K., Coleman, P. R., Qi, Y., Chen, J., Vadas, M. A., & Gamble, J. R. (2021) · Cancers · doi:10.3390/cancers13071724 · Cited by 34
A tumor-on-a-chip for in vitro study of CAR-T cell immunotherapy in solid tumors
Liu, H., Noguera-Ortega, E., Dong, X., Lee, W. D., Chang, J., Aday, S., Li, Y., Shin, Y., Shi, X., Liousia, M., et al. (2025) · Nature Biotechnology · doi:10.1038/s41587-025-02845-z · Cited by 41
Molecular description of ANGPT2 associated colorectal carcinoma
Jary, M., Hasanova, R., Vienot, A., Asgarov, K., Loyon, R., Tirole, C., Bouard, A., Orillard, É., Klajer, É., Kim, S. C. H., et al. (2020) · International Journal of Cancer · doi:10.1002/ijc.32993 · Cited by 30
Cho, R., Sakurai, Y., Jones, H. S., Akita, H., Hisaka, A., & Hatakeyama, H. (2020) · Cancers · doi:10.3390/cancers12123630 · Cited by 31
Enhancing CAR T-cell therapies against solid tumors: Mechanisms and reversion of resistance
Qin, Y., & Xu, G. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.1053120 · Cited by 32
Changing landscape of anti-angiogenic therapy: Novel approaches and clinical perspectives
Gacche, R. N. (2023) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2023.189020 · Cited by 34
Qu, F., Zhou, Y., & Wu, S. (2023) · British Journal of Cancer · doi:10.1038/s41416-023-02482-w · Cited by 30
Sullivan, J. M., Bagnell, A. M., Alevy, J., Avila, E. M., Mihaljević, L., Saavedra-Rivera, P. C., Kong, L., Huh, J. S., McCray, B. A., Aisenberg, W. H., et al. (2024) · Science Translational Medicine · doi:10.1126/scitranslmed.adk1358 · Cited by 29
Immune microenvironment and immunotherapy in hepatocellular carcinoma: mechanisms and advances
Xie, D., Liu, Y., Xu, F., Dang, Z., Li, M., Zhang, Q., & Dang, Z. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1581098 · Cited by 35
ADAMTS1 protease is required for a balanced immune cell repertoire and tumour inflammatory response
Rodríguez‐Baena, F. J., Redondo-García, S., Peris-Torres, C., Martino‐Echarri, E., Fernández‐Rodríguez, R., Plaza‐Calonge, M. D. C., Anderson, P. O., & Rodríguez-Manzaneque, J. C. (2018) · Scientific Reports · doi:10.1038/s41598-018-31288-7 · Cited by 33
Huynh, H. T., Prawira, A., Le, T. B. U., Vu, T. C., Hao, H.-X., Huang, A., Wang, Y., & Porta, D. G. (2020) · Experimental & Molecular Medicine · doi:10.1038/s12276-020-00524-4 · Cited by 28
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
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