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Influence of SLC40A1 on Cytokine Interactions and Immune Infiltration in Glioblastoma

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Abstract

Numerous studies have explored the various functions of Slc40a1 in cancer development. However, the role of Slc40a1 in primary glioblastoma requires further investigation. Initially, we observed that GBM patients with high Slc40a1 expression had a more favorable prognosis than those with low Slc40a1 expression, as evidenced by an analysis of the TIMER database. Subsequent analysis using the cancer genome atlas (TCGA) database enabled us to identify potential underlying mechanisms involved. Further analyses, including GO, KEGG, GSEA, immune infiltration, and correlation analyses, revealed that Slc40a1 primarily affected cytokine interactions, particularly with Ccl14 and Il18, resulting in changes in the immune microenvironment and ultimately leading to a better prognosis in GBM patients. We validated our findings by examining a tissue microarray with 180 samples and confirmed that GBM patients with high SLC40A1 protein expression exhibited more favorable prognostic outcomes than those with low SLC40A1 protein expression. Immunofluorescence analysis also revealed a significant correlation between SLC40A1 protein expression and the protein expression of IL18 and CCL14. These findings suggest that Slc40a1 may play a role in GBM pathogenesis by modulating the tumor immune microenvironment through the regulation of Il18 and Ccl14. Hence, targeting Slc40a1 might offer potential benefits for immunotherapeutic interventions and prognostic assessments in GBM patients.

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Data Availability

TCGA and the single-cell portal are public databases. The patients whose samples are included in the databases have already provided informed consent. Users are permitted to download relevant data for free for research and to publish relevant articles. This study is based on open source data in public databases, and our tissue chip was provided by Shanghai Yan Tuo Biotechnology Co., Ltd.; therefore, ethics approval is unnecessary.

References

  • Appin, C. L., & Brat, D. J. (2015). Molecular pathways in gliomagenesis and their relevance to neuropathologic diagnosis. Advances in Anatomic Pathology, 22(1), 50–58. https://doi.org/10.1097/pap.0000000000000048FromNLM

    Article  CAS  PubMed  Google Scholar 

  • Aushev, V. N., Gopalakrishnan, K., Teitelbaum, S. L., ParadaJr, H., Santella, R. M., Gammon, M. D., & Chen, J. (2019). Tumor expression of environmental chemical-responsive genes and breast cancer mortality. Endocrine Related Cancer, 26(12), 843–851. https://doi.org/10.1530/erc-19-0357FromNLM

    Article  CAS  PubMed  Google Scholar 

  • Bauché, D., Joyce-Shaikh, B., Jain, R., Grein, J., Ku, K. S., Blumenschein, W. M., Ganal-Vonarburg, S. C., Wilson, D. C., McClanahan, T. K., Malefyt, R. W., Macpherson, A. J., Annamalai, L., Yearley, J. H., Cua, D. (2018). LAG3+ regulatory T Cells restrain interleukin-23-producing CX3CR1+ gut-resident macrophages during group 3 innate lymphoid cell-driven colitis.  Immunity,  49(2),  342–352. https://doi.org/10.1016/j.immuni.2018.07.007

    Article  CAS  Google Scholar 

  • Benyamin, B., Esko, T., Ried, J. S., Radhakrishnan, A., Vermeulen, S. H., Gögele, T., Anderson, D., Broer, L., Podmore, C., Luan, J., Kutalik, Z., Sanna, S., van der Meer, P., Tanaka, T., Wang, F., Westra, H-J., Franke, L., Mihailov, E., Milani, L., Hälldin, J., Winkelmann, J., Meitinger, T., Thiery, J., Peters, A., Waldenberger, M., Rendon, A., Jolley, J., Sambrook, J., Kiemeney, L., Sweep, F. C., Sala, C. F., Schwienbacher, C., Irene Pichler, I., Jennie Hui, J., Demirkan, A., Isaacs, A., Amin, N., Maristella Steri, M., Gérard Waeber, G., Verweij, N., Powell, J. E., Nyholt, D. R., Heath, A. C., Madden, P. A. F., Visscher, P. M., Wright, M. J., Montgomery, G. W., Martin, N. G., Hernandez, D., Bandinelli, S., van der Harst, P., Uda, M., Vollenweider, P., Scott, R. A., Langenberg, C., Wareham, N. J., Consortium, I., van Duijn, C., Beilby, J., Pramstaller, P. P., Hicks, A. A., Ouwehand, W. H., Oexle, K., Gieger, C., Metspalu, A., Camaschella, C., Toniolo, D., Swinkels, D. W., & Whitfield J. B. (2014). Novel loci affecting iron homeostasis and their effects in individuals at risk for hemochromatosis. Nature Communications, 5, 4926. https://doi.org/10.1038/ncomms5926FromNLM

  • Beroukhim, R., Getz, G., Nghiemphu, L., Barretina, J., Hsueh, T., Linhart, D., Vivanco, I., Lee, J. C., Huang, J. H., Alexander, S., Du, J., Kau, T., Thomas, R. K., Shah, K., Soto, H., Perner, S., Prensner, J., Debiasi, R. M., Demichelis, F., Hatton, C., Rubin, M. A., Garraway, L. A., Nelson, S. F., Liau, L., Mischel, P. S., Cloughesy, T. F., Meyerson, M., Golub, T. A., Lander, E. S., Mellinghoff, I. K., Sellers, W. R. (2007). Assessing the significance of chromosomal aberrations in cancer: Methodology and application to glioma. Proceedings of the National Academy of Sciences, 104(50), 20007–20012. https://doi.org/10.1073/pnas.0710052104FromNLM

  • Blain, K. Y., Kwiatkowski, W., Zhao, Q., La Fleur, D., Naik, C., Chun, T. W., Tsareva, T., Kanakaraj, P., Laird, M. W., Shah, R., George, L., Sanyal, I., Moore, P. A., Demeler, B., and Choe, C. (2007). Structural and functional characterization of CC chemokine CCL14. Biochemistry, 46(35), 10008–10015. https://doi.org/10.1021/bi700936wFromNLM

  • Bredel, M., Bredel, C., Juric, D., Harsh, G. R., Vogel, H., Recht, L. D., & Sikic, B. I. (2005). Functional network analysis reveals extended gliomagenesis pathway maps and three novel MYC-interacting genes in human gliomas. Cancer Research, 65(19), 8679–8689. https://doi.org/10.1158/0008-5472.Can-05-1204FromNLM

    Article  CAS  PubMed  Google Scholar 

  • Brissot, P., Pietrangelo, A., Adams, P. C., de Graaff, B., McLaren, C. E., & Loréal, O. (2018). Haemochromatosis. Nature Reviews Disease Primers, 4, 18016. https://doi.org/10.1038/nrdp.2018.16FromNLM

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen, X., Kang, R., Kroemer, G., & Tang, D. (2021). Broadening horizons: The role of ferroptosis in cancer. Nature Reviews Clinical Oncology, 18(5), 280–296. https://doi.org/10.1038/s41571-020-00462-0FromNLM

    Article  CAS  PubMed  Google Scholar 

  • Chong, W. P., Mattapallil, M. J., Raychaudhuri, K., Bing, S. J., Wu, S., Zhong, Y., Wang, W., Chen, Z., Silver, P. B., Jittayasothorn, Y., Chan C. C., Chen, J., Horai, R., Caspi, R. R. (2020). The cytokine IL-17A limits Th17 pathogenicity via a negative feedback loop driven by autocrine induction of IL-24.  Immunity, 53(2),  384-397. https://doi.org/10.1016/j.immuni.2020.06.022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Daubon, T., Hemadou, A., Romero Garmendia, I., & Saleh, M. (2020). Glioblastoma immune landscape and the potential of new immunotherapies. Frontiers in Immunology, 11, 585616. https://doi.org/10.3389/fimmu.2020.585616FromNLM

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deng, S., Zheng, Y., Mo, Y., Xu, X., Li, Y., Zhang, Y., Liu, J., Chen, J., Tian, Y., & Ke, Y. (2021). Ferroptosis suppressive genes correlate with immunosuppression in glioblastoma. World Neurosurg, 152, e436–e448. https://doi.org/10.1016/j.wneu.2021.05.098FromNLM

    Article  PubMed  Google Scholar 

  • Donovan, A., Lima, C. A., Pinkus, J. L., Pinkus, G. S., Zon, L. I., Robine, S., & Andrews, N. C. (2005). The iron exporter ferroportin/Slc40a1 is essential for iron homeostasis. Cell Metabolism, 1(3), 191–200. https://doi.org/10.1016/j.cmet.2005.01.003FromNLM

    Article  CAS  PubMed  Google Scholar 

  • Drakesmith, H., Nemeth, E., & Ganz, T. (2015). Ironing out ferroportin. Cell Metabolism, 22(5), 777–787. https://doi.org/10.1016/j.cmet.2015.09.006FromNLM

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fang, X., Huang, Z., Zhai, K., Huang, Q., Tao, W., Kim, L., Wu, Q., Almasan, A., Yu, J. S., Li, X., Strak, G. R., Rich, J. N., Bao, S. (2021). Inhibiting DNA-PK induces glioma stem cell differentiation and sensitizes glioblastoma to radiation in mice. Science Translational Medicine. https://doi.org/10.1126/scitranslmed.abc7275

  • Funakoshi, N., Chaze, I., Alary, A. S., Tachon, G., Cunat, S., Giansily-Blaizot, M., Bismuth, M., Larrey, D., Pageaux, G. P., Schved, J. F., Donnadieu-Rigole, H., Blanc, P., Aguilar-Martinez, P. (2016). The role of genetic factors in patients with hepatocellular carcinoma and iron overload—a prospective series of 234 patients. Liver International, 36(5), 746–754. https://doi.org/10.1111/liv.12984FromNLM

  • Herrmann, A., Lahtz, C., Nagao, T., Song, J. Y., Chan, W. C., Lee, H., Yue, C., Look, T., Mülfarth, R., Li, W., Jenkins, K., Williams, J., Budde, L. E., Forman, S., Kwak, L., Blankenstein, T., Yu, H. (2017). CTLA4 Promotes Tyk2-STAT3–Dependent B-cell Oncogenicity. Abstract Cancer Research, 77(18),  5118–5128. https://doi.org/10.1158/0008-5472.CAN-16-0342

    Article  CAS  Google Scholar 

  • Huang, Y. H., Zhu, C., Kondo, Y., Anderson, A. C., Gandhi, A., Russell, A., Dougan, S. K., Petersen, B. S., Melum, E., Pertel, T., Clayton, K. L., Raab, M., Chen, Q., Beauchemin, N., Yazaki, P. J., Pyzik, M., Ostrowski, M. A., Glickman, J. N., Rudd, C. E., Ploegh, H. L., Franke, A., Petsko, G. A., Kuchroo, V. K., Blumberg, R. S. (2015) CEACAM1 regulates TIM-3-mediated tolerance and exhaustion. Nature, 517(7534), 386–390. https://doi.org/10.1038/nature13848

    Article  CAS  Google Scholar 

  • Jagot, F., Gaston-Breton, R., Choi, A. J., Pascal, M., Bourhy, L., Dorado-Doncel, R., Conzelmann, K. K., Lledo, P. M., Lepousez, G., Eberl, G. (2023). The parabrachial nucleus elicits a vigorous corticosterone feedback response to the pro-inflammatory cytokine IL-1β. Neuron, 111(15), 2367–2382. https://doi.org/10.1016/j.neuron.2023.05.009

    Article  CAS  PubMed  Google Scholar 

  • Kahn, J., Hayman, T. J., Jamal, M., Rath, B. H., Kramp, T., Camphausen, K., & Tofilon, P. J. (2014). The mTORC1/mTORC2 inhibitor AZD2014 enhances the radiosensitivity of glioblastoma stem-like cells. Neuro-Oncology, 16(1), 29–37. https://doi.org/10.1093/neuonc/not139FromNLM

    Article  CAS  PubMed  Google Scholar 

  • Khasraw, M., & Lassman, A. B. (2010). Advances in the treatment of malignant gliomas. Current Oncology Reports, 12(1), 26–33. https://doi.org/10.1007/s11912-009-0077-4FromNLM

    Article  CAS  PubMed  Google Scholar 

  • Komohara, Y., Ohnishi, K., Kuratsu, J., & Takeya, M. (2008). Possible involvement of the M2 anti-inflammatory macrophage phenotype in growth of human gliomas. The Journal of Pathology, 216(1), 15–24. https://doi.org/10.1002/path.2370FromNLM

    Article  CAS  PubMed  Google Scholar 

  • Korur, S., Huber, R. M., Sivasankaran, B., Petrich, M., Morin, P., Jr., Hemmings, B. A., Merlo, A., & Lino, M. M. (2009). GSK3beta regulates differentiation and growth arrest in glioblastoma. PLoS ONE, 4(10), e7443. https://doi.org/10.1371/journal.pone.0007443FromNLM

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee, J., Kotliarova, S., Kotliarov, Y., Li, A., Su, Q., Donin, N. M., Pastorino, S., Purow, B. W., Christopher, N., Zhang, W., Park, J. K., Fine, H. A. (2006). Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell, 9(5), 391–403. https://doi.org/10.1016/j.ccr.2006.03.030FromNLM

  • Liang, B., Zhou, C., Cui, S., Lu, H., Xu, R., Xue, D., Zou, S., & He, X. (2021). Upregulation of miR-18a-5p promotes the proliferation of prostate cancer via inhibiting the expression of SLC40A1. Pathology, Research and Practice, 224, 153448. https://doi.org/10.1016/j.prp.2021.153448FromNLM

    Article  CAS  PubMed  Google Scholar 

  • Liang, Y., Diehn, M., Watson, N., Bollen, A. W., Aldape, K. D., Nicholas, M. K., Lamborn, K. R., Berger, M. S., Botstein, D., Brown, P. O., Israel, M. A. (2005). Gene expression profiling reveals molecularly and clinically distinct subtypes of glioblastoma multiforme. Proceedings of the National Academy of Sciences, 102(16), 5814–5819. https://doi.org/10.1073/pnas.0402870102FromNLM

  • Mattiola, I., Tomay, F., De Pizzol, M., Silva-Gomes, R., Savino, B., Gulic, T., Doni, A., Lonardi, S., Astrid Boutet, M., Nerviani, A.., Carriero, R., Molgora, M., Stravalaci,M., Morone, D., Shalova, I. N., Lee, Y., Biswas, S. K., Mantovani, G., Sironi, M., Pitzalis, C., Vermi, W., Bottazzi, B., Mantovani, A., & Locati, M. (2019). The macrophage tetraspan MS4A4A enhances dectin-1-dependent NK cell-mediated resistance to metastasis. Nature Immunology, 20(8), 1012–1022. https://doi.org/10.1038/s41590-019-0417-yFromNLM

  • Mora, J., Mertens, C., Meier, J. K., Fuhrmann, D. C., Brüne, B., & Jung, M. (2019). strategies to interfere with tumor metabolism through the interplay of innate and adaptive Immunity. Cells. https://doi.org/10.3390/cells8050445

    Article  PubMed  PubMed Central  Google Scholar 

  • Murat, A., Migliavacca, E., Gorlia, T., Lambiv, W. L., Shay, T., Hamou, M. F., de Tribolet, N., Regli, L., Wick, W., Kouwenhoven, M. C., Hainfellner, J. A., Heppner, F. l., Dietrich, P-Y., Zimmer, Y., Cairncross, J. G., Janzer, R-C., Domany, E., Delorenzi, M., Stupp, R., and Hegi, M. E. (2008). Stem cell-related “self-renewal” signature and high epidermal growth factor receptor expression associated with resistance to concomitant chemoradiotherapy in glioblastoma. Journal of Clinical Oncology, 26(18), 3015–3024. https://doi.org/10.1200/jco.2007.15.7164FromNLM

  • Nakanishi, K. (2018). Unique action of interleukin-18 on T cells and other immune cells. Frontiers in Immunology, 9, 763. https://doi.org/10.3389/fimmu.2018.00763FromNLM

    Article  PubMed  PubMed Central  Google Scholar 

  • Neftel, C., Laffy, J., Filbin, M. G., Hara, T., Shore, M. E., Rahme, G. J., Richman, A. R., Silverbush, D., Shaw, M. L., Hebert, C. M., Dewitt, J., Gritsch, S., Perez, E. M., Castro, L. N. G., Lan, X., Druck, N., Rodman, C., Dionne, D., Kaplan, A., Bertalan, M. S., Small, J., Pelton, K., Becker, S., Bonal, D., Nguyen, Q-D., Servis, R. L., Fung, J. M., Mylvaganam, R., Mayr, L., Gojo, J., Haberler, C., Geyeregger, R., Czech, T., Slavc, I., Nahed, B. V., Curry, W. T., Carter, B. S., Wakimoto, H., Brastianos, P. K., Batchelor, T. T., Stemmer-Rachamimov, A., Martinez-Lage, M., Frosch, M. P., Stamenkovic, I., Riggi, N., Rheinbay, E., Monje, M., Rozenblatt-Rosen, O., Cahill, D. P., Patel, A. P., Hunter, T., Verma, I. M., Ligon, K. L., Louis, D. N., Regev, A., Bernstein, B. E., Tirosh, I., and Suva, M. L. (2019). An integrative model of cellular states, plasticity, and genetics for glioblastoma. Cell, 178(4), 835-849.e821. https://doi.org/10.1016/j.cell.2019.06.024FromNLM

  • Oh, S., Yeom, J., Cho, H. J., Kim, J. H., Yoon, S. J., Kim, H., Sa, J. K., Ju, S., Lee, H., Oh, M. J., Lee, W., Kwon, Y., Li, H., Choi, S., Han, J. H., Chang, J. H., Choi, E., Kim, J., Her, N-G., Kim, S. H., Kang, S-G., Paek, E., Nam, D-H., Lee, C., & Kim, H. S. (2020). Integrated pharmaco-proteogenomics defines two subgroups in isocitrate dehydrogenase wild-type glioblastoma with prognostic and therapeutic opportunities. Nature Communications, 11(1), 3288. https://doi.org/10.1038/s41467-020-17139-yFromNLM

  • Patel, A. P., Tirosh, I., Trombetta, J. J., Shalek, A. K., Gillespie, S. M., Wakimoto, H., Cahill, D. P., Nahed, B. V., Curry, W. T., Martuza, R. L., Louis, D. N., Rozenblatt-Rosen, O., Suva, M. L., Regev, A., Bernstein, B. E. (2014). Single-cell RNA-seq highlights intratumoral heterogeneity in primary glioblastoma. Science, 344(6190), 1396–1401. https://doi.org/10.1126/science.1254257FromNLM

  • Perisé-Barrios, A. J., Gómez, R., Corbí, A. L., de la Mata, J., Domínguez-Soto, A., & Muñoz-Fernandez, M. A. (2015). Use of carbosilane dendrimer to switch macrophage polarization for the acquisition of antitumor functions. Nanoscale, 7(9), 3857–3866. https://doi.org/10.1039/c4nr04038dFromNLM

    Article  PubMed  Google Scholar 

  • Poff, A., Koutnik, A. P., Egan, K. M., Sahebjam, S., D’Agostino, D., & Kumar, N. B. (2019). Targeting the Warburg effect for cancer treatment: Ketogenic diets for management of glioma. Seminars in Cancer Biology, 56, 135–148. https://doi.org/10.1016/j.semcancer.2017.12.011FromNLM

    Article  CAS  PubMed  Google Scholar 

  • Pogribny, I. P. (2010). Ferroportin and hepcidin: A new hope in diagnosis, prognosis, and therapy for breast cancer. Breast Cancer Research, 12(5), 314. https://doi.org/10.1186/bcr2641FromNLM

    Article  PubMed  PubMed Central  Google Scholar 

  • Radio, F. C., Majore, S., Aurizi, C., Sorge, F., Biolcati, G., Bernabini, S., Giotti, I., Torricelli, F., Giannarelli, D., De Bernardo, C., Grammatico, P. (2015). Hereditary hemochromatosis type 1 phenotype modifiers in Italian patients. The controversial role of variants in HAMP, BMP2, FTL and SLC40A1 genes. Blood Cells Molecules and Diseases. https://doi.org/10.1016/j.bcmd.2015.04.001FromNLM

  • Reardon, D. A., Wen, P. Y., Wucherpfennig, K. W., & Sampson, J. H. (2017). Immunomodulation for glioblastoma. Current Opinion in Neurology, 30(3), 361–369. https://doi.org/10.1097/wco.0000000000000451FromNLM

    Article  CAS  PubMed  Google Scholar 

  • Sachamitr, P., Ho, J. C., Ciamponi, F. E., Ba-Alawi, W., Coutinho, F. J., Guilhamon, P., Kushida, M. M., Cavalli, F. M. G., Lee, L., Rastegar, N., Vu, V., Sánchez-Osuna, M., Coulombe-Huntington, J., Kanshin, E., Whetstone, H., Durand, M., Thibault, P., Hart, K., Mangos, M., Veyhl, J., Chen, W., Tran, N., Duong, B-C., Aman, A. M., Dirks, P. B. (2021). PRMT5 inhibition disrupts splicing and stemness in glioblastoma. Nature Communications, 12(1), 979. https://doi.org/10.1038/s41467-021-21204-5FromNLM

  • Sun, L., Hui, A. M., Su, Q., Vortmeyer, A., Kotliarov, Y., Pastorino, S., Passaniti, A., Menon, J., Walling, J., Bailey, R., Rosenblum, M., Mikkelsen, T., Fine, H. A. (2006). Neuronal and glioma-derived stem cell factor induces angiogenesis within the brain. Cancer Cell, 9(4), 287–300. https://doi.org/10.1016/j.ccr.2006.03.003FromNLM

  • Tao, W., Chu, C., Zhou, W., Huang, Z., Zhai, K., Fang, X., Huang, Q., Zhang, A., Wang, X., Yu, X., Huang, H., Wu, Q., Sloan, A. E., Yu, J. S., Li, X. Stark, G. R., Rich, J. N., & Bao, S. (2020). Dual Role of WISP1 in maintaining glioma stem cells and tumor-supportive macrophages in glioblastoma. Nature Communications, 11(1), 3015. https://doi.org/10.1038/s41467-020-16827-zFromNLM

  • Torti, S. V., & Torti, F. M. (2013). Iron and cancer: More ore to be mined. Nature Reviews Cancer, 13(5), 342–355. https://doi.org/10.1038/nrc3495FromNLM

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Meir, E. G., Hadjipanayis, C. G., Norden, A. D., Shu, H. K., Wen, P. Y., & Olson, J. J. (2010). Exciting new advances in neuro-oncology: The avenue to a cure for malignant glioma. CA: A Cancer Journal for Clinicians, 60(3), 166–193. https://doi.org/10.3322/caac.20069FromNLM

    Article  PubMed  Google Scholar 

  • Wessling-Resnick, M. (2015). Nramp1 and other transporters involved in metal withholding during infection. Journal of Biological Chemistry, 290(31), 18984–18990. https://doi.org/10.1074/jbc.R115.643973FromNLM

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu, J., Zhang, L., Wu, S., Yi, X., & Liu, Z. (2020). miR-194-5p inhibits SLC40A1 expression to induce cisplatin resistance in ovarian cancer. Pathology, Research and Practice, 216(7), 152979. https://doi.org/10.1016/j.prp.2020.152979FromNLM

    Article  CAS  PubMed  Google Scholar 

  • Wu, L., Xia, W., Hua, Y., Fan, K., Lu, Y., Wang, M., Jin, Y., Zhang, W., & Pan, S. (2023). Cellular crosstalk of macrophages and therapeutic implications in non-small cell lung cancer revealed by integrative inference of single-cell transcriptomics. Frontiers in Pharmacology, 14, 1295442. https://doi.org/10.3389/fphar.2023.1295442FromNLM

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yasuda, K., Nakanishi, K., & Tsutsui, H. (2019). Interleukin-18 in health and disease. International Journal of Molecular Sciences. https://doi.org/10.3390/ijms20030649

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang, Q., He, Y., Luo, N., Patel, S. J., Han, Y., Gao, R., Modak, M., Carotta, S., Haslinger, C., Kind, D., Peet, G. W., Zhong, G., Lu, S., Zhu, W., Mao, Y., Xiao, M., Bergmann, M., Hu, X., Kerkar, S. P., Vogt, A. B., Pflanz, S., Liu, K., Peng, J., Ren, X., and Zhang, Z. (2019). Landscape and dynamics of single immune cells in hepatocellular carcinoma. Cell, 179(4), 829-845.e820. https://doi.org/10.1016/j.cell.2019.10.003FromNLM

  • Zhang, Y., Yu, G., Chu, H., Wang, X., Xiong, L., Cai, G., Liu, R., Gao, H., Tao, B., Li, W., Li, G., Liang, J., Yang, W. (2018). Macrophage-associated PGK1 phosphorylation promotes aerobic glycolysis and tumorigenesis. Molecular Cell, 71(2), 201-215.e207. https://doi.org/10.1016/j.molcel.2018.06.023FromNLM

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Acknowledgements

We are grateful to TCGA, Oncomine, GEPIA2, TIMER2.0, CIBERSORT, EPIC, and single-cell portal databases for providing platforms for the analysis of public datasets.

Funding

This research was funded by the National Natural Science Foundation of China (No. 82171832 and No.82371839) and the Shanghai Science and Technology Development Foundation (No. 20Z11900100).

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Author notes

  1. Jiahao Jiang

    Present address: Tongji Hospital Affiliated with Tongji University, 389 Xincun Road, Putuo District, Shanghai, 200065, China

  2. Jiahao Jiang, Riquan Duan and Junle Zhu have been Contributed equally to this work.

Authors and Affiliations

  1. Department of Neurosurgery, Tongji Hospital, School of Medicine, Tongji University, Shanghai, China

    Jiahao Jiang, Riquan Duan, Junle Zhu, Junqing Yan, Jingliang Ye & Chun Luo

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Conceptualization, JH.J., RQ.D. and JL.Y.; methodology, JH.J., RQ.D., C.L. and JL.Y.; software, JH.J., RQ.D., JL.Z. and JQ.Y.; validation, JH.J., RQ.D. and JQ.Y.; formal analysis, JH.J., RQ.D., JL.Z. and JQ.Y.; investigation, JH.J. and JL.Y.; resources, C.L.; data curation, JH.J., RQ.D.; writing—original draft preparation, JH.J., RQ.D. and JL.Y.; writing—review and editing, JH.J., RQ.D. and JQ.Y.; visualization, C.L. and JL.Y.; supervision, C.L.; project administration, C.L. and JL.Y.; and funding acquisition, C.L. All authors have read and agreed to the published version of the manuscript.

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Correspondence to Jingliang Ye or Chun Luo.

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Jiang, J., Duan, R., Zhu, J. et al. Influence of SLC40A1 on Cytokine Interactions and Immune Infiltration in Glioblastoma. Neuromol Med 26, 21 (2024). https://doi.org/10.1007/s12017-024-08789-y

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