Feb 2024, Volume 44 Issue 2
    

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  • REVIEW
    Xianjie Jiang, Qiu Peng, Mingjing Peng, Linda Oyang, Honghan Wang, Qiang Liu, Xuemeng Xu, Nayiyuan Wu, Shiming Tan, Wenjuan Yang, Yaqian Han, Jinguan Lin, Longzheng Xia, Yanyan Tang, Xia Luo, Jie Dai, Yujuan Zhou, Qianjin Liao
    2024, 44(2): 185-204. https://doi.org/10.1002/cac2.12519
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    Cellular metabolism is the fundamental process by which cells maintain growth and self-renewal. It produces energy, furnishes raw materials, and intermediates for biomolecule synthesis, and modulates enzyme activity to sustain normal cellular functions. Cellular metabolism is the foundation of cellular life processes and plays a regulatory role in various biological functions, including programmed cell death. Ferroptosis is a recently discovered form of iron-dependent programmed cell death. The inhibition of ferroptosis plays a crucial role in tumorigenesis and tumor progression. However, the role of cellular metabolism, particularly glucose and amino acid metabolism, in cancer ferroptosis is not well understood. Here, we reviewed glucose, lipid, amino acid, iron and selenium metabolism involvement in cancer cell ferroptosis to elucidate the impact of different metabolic pathways on this process. Additionally, we provided a detailed overview of agents used to induce cancer ferroptosis. We explained that the metabolism of tumor cells plays a crucial role in maintaining intracellular redox homeostasis and that disrupting the normal metabolic processes in these cells renders them more susceptible to iron-induced cell death, resulting in enhanced tumor cell killing. The combination of ferroptosis inducers and cellular metabolism inhibitors may be a novel approach to future cancer therapy and an important strategy to advance the development of treatments.

  • REVIEW
    Ming-Kun Chen, Zi-Xian Chen, Mao-Ping Cai, Hong Chen, Zhuang-Fei Chen, Shan-Chao Zhao
    2024, 44(2): 205-225. https://doi.org/10.1002/cac2.12518
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    Targeted delivery of anti-tumor drugs and overcoming drug resistance in malignant tumor cells remain significant clinical challenges. However, there are only few effective methods to address these issues. Extracellular vesicles (EVs), actively secreted by cells, play a crucial role in intercellular information transmission and cargo transportation. Recent studies have demonstrated that engineered EVs can serve as drug delivery carriers and showed promising application prospects. Nevertheless, there is an urgent need for further improvements in the isolation and purification of EVs, surface modification techniques, drug assembly processes, and precise recognition of tumor cells for targeted drug delivery purposes. In this review, we summarize the applications of engineered EVs in cancer treatment and overcoming drug resistance, and current challenges associated with engineered EVs are also discussed. This review aims to provide new insights and potential directions for utilizing engineered EVs as targeted delivery systems for anti-tumor drugs and overcoming drug resistance in the near future.

  • ORIGINAL ARTICLE
    Weiren Liu, Huqiang Wang, Qianfu Zhao, Chenyang Tao, Weifeng Qu, Yushan Hou, Run Huang, Zimei Sun, Guiqi Zhu, Xifei Jiang, Yuan Fang, Jun Gao, Xiaoling Wu, Zhixiang Yang, Rongyu Ping, Jiafeng Chen, Rui Yang, Tianhao Chu, Jian Zhou, Jia Fan, Zheng Tang, Dong Yang, Yinghong Shi
    2024, 44(2): 226-250. https://doi.org/10.1002/cac2.12513
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    Background: Intrahepatic cholangiocarcinoma (iCCA) is a highly heterogeneous and lethal hepatobiliary tumor with few therapeutic strategies. The metabolic reprogramming of tumor cells plays an essential role in the development of tumors, while the metabolic molecular classification of iCCA is largely unknown. Here, we performed an integrated multiomics analysis and metabolic classification to depict differences in metabolic characteristics of iCCA patients, hoping to provide a novel perspective to understand and treat iCCA.

    Methods: We performed integrated multiomics analysis in 116 iCCA samples, including whole-exome sequencing, bulk RNA-sequencing and proteome analysis. Based on the non-negative matrix factorization method and the protein abundance of metabolic genes in human genome-scale metabolic models, the metabolic subtype of iCCA was determined. Survival and prognostic gene analyses were used to compare overall survival (OS) differences between metabolic subtypes. Cell proliferation analysis, 5-ethynyl-2'-deoxyuridine (EdU) assay, colony formation assay, RNA-sequencing and Western blotting were performed to investigate the molecular mechanisms of diacylglycerol kinase α (DGKA) in iCCA cells.

    Results: Three metabolic subtypes (S1-S3) with subtype-specific biomarkers of iCCA were identified. These metabolic subtypes presented with distinct prognoses, metabolic features, immune microenvironments, and genetic alterations. The S2 subtype with the worst survival showed the activation of some special metabolic processes, immune-suppressed microenvironment and Kirsten rat sarcoma viral oncogene homolog (KRAS)/AT-rich interactive domain 1A (ARID1A) mutations. Among the S2 subtype-specific upregulated proteins, DGKA was further identified as a potential drug target for iCCA, which promoted cell proliferation by enhancing phosphatidic acid (PA) metabolism and activating mitogen-activated protein kinase (MAPK) signaling.

    Conclusion: Via multiomics analyses, we identified three metabolic subtypes of iCCA, revealing that the S2 subtype exhibited the poorest survival outcomes. We further identified DGKA as a potential target for the S2 subtype.

  • ORIGINAL ARTICLE
    Yue Yao, Yi Xu, Liang Yu, Ting-Mao Xue, Zhi-Jie Xiao, Pui-Chi Tin, Hiu-Ling Fung, Hoi-Tang Ma, Jing-Ping Yun, Judy Wai Ping Yam
    2024, 44(2): 251-272. https://doi.org/10.1002/cac2.12515
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    Background: Small extracellular vesicles (sEVs) mediate intercellular communication that contributes to hepatocellular carcinoma (HCC) progression via multifaceted pathways. The success of cell entry determines the effect of sEV on recipient cells. Here, we aimed to delineate the mechanisms underlying the uptake of sEV in HCC.

    Methods: Macropinocytosis was examined by the ability of cells to internalize dextran and sEV. Macropinocytosis was analyzed in Na(+)/H(+) exchanger 7 (NHE7)-knockdown and -overexpressing cells. The properties of cells were studied using functional assays. pH biosensor was used to evaluate the intracellular and endosomal pH. The expression of NHE7 in patients’ liver tissues was examined by immunofluorescent staining. Inducible silencing of NHE7 in established tumors was performed to reveal the therapeutic potential of targeting NHE7.

    Results: The data revealed that macropinocytosis controlled the internalization of sEVs and their oncogenic effect on recipient cells. It was found that metastatic HCC cells exhibited the highest efficiency of sEV uptake relative to normal liver cells and non-metastatic HCC cells. Attenuation of macropinocytic activity by 5-(N-ethyl-N-isopropyl)-amiloride (EIPA) limited the entry of sEVs and compromised cell aggressiveness. Mechanistically, we delineated that high level of NHE7, a sodium-hydrogen exchanger, alkalized intracellular pH and acidized endosomal pH, leading to the maturation of macropinosomes. Inducible inhibition of NHE7 in established tumors developed in mice delayed tumor development and suppressed lung metastasis. Clinically, NHE7 expression was upregulated and linked to dismal prognosis of HCC.

    Conclusions: This study advances the understanding that NHE7 enhances sEV uptake by macropinocytosis to promote the malignant properties of HCC cells. Inhibition of sEV uptake via macropinocytosis can be exploited as a treatment alone or in combination with conventional therapeutic approaches for HCC.

  • LETTER TO THE EDITOR
    Mi-Jeong Kim, Ji Young Kim, Ji Hye Shin, Juhee Son, Yeeun Kang, Soo-Kyung Jeong, Duk-Hwan Kim, Kyun-Hwan Kim, Eunyoung Chun, Ki-Young Lee
    2024, 44(2): 273-277. https://doi.org/10.1002/cac2.12485
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  • LETTER TO THE EDITOR
    Tiantian Guo, Yue Zhou, Fei Liang, Zezhou Wang, Vincent Bourbonne, Lukas Käsmann, Nora Sundahl, Abraham Jing-Ching Wu, Jianjiao Ni, Zhengfei Zhu
    2024, 44(2): 278-281. https://doi.org/10.1002/cac2.12512
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  • LETTER TO THE EDITOR
    Bianca Cesaro, Alessia Iaiza, Fabio Piscopo, Marco Tarullo, Eleonora Cesari, Dante Rotili, Antonello Mai, Alberto Diana, Michela Londero, Luca Del Giacco, Riccardo Masetti, Alba Di Leone, Chiara Naro, Silvia Masciarelli, Giulia Fontemaggi, Claudio Sette, Francesco Fazi, Alessandro Fatica
    2024, 44(2): 282-286. https://doi.org/10.1002/cac2.12509
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  • LETTER TO THE EDITOR
    Kouya Shiraishi, Atsushi Takahashi, Yukihide Momozawa, Yataro Daigo, Syuzo Kaneko, Takahisa Kawaguchi, Hideo Kunitoh, Shingo Matsumoto, Hidehito Horinouchi, Akiteru Goto, Takayuki Honda, Kimihiro Shimizu, Masahiro Torasawa, Daisuke Takayanagi, Motonobu Saito, Akira Saito, Yuichiro Ohe, Shun-ichi Watanabe, Koichi Goto, Masahiro Tsuboi, Katsuya Tsuchihara, Sadaaki Takata, Tomomi Aoi, Atsushi Takano, Masashi Kobayashi, Yohei Miyagi, Kazumi Tanaka, Hiroyuki Suzuki, Daichi Maeda, Takumi Yamaura, Maiko Matsuda, Yoko Shimada, Takaaki Mizuno, Hiromi Sakamoto, Teruhiko Yoshida, Yasushi Goto, Tatsuya Yoshida, Taiki Yamaji, Makoto Sonobe, Shinichi Toyooka, Kazue Yoneda, Katsuhiro Masago, Fumihiro Tanaka, Megumi Hara, Nobuo Fuse, Satoshi S. Nishizuka, Noriko Motoi, Norie Sawada, Yuichiro Nishida, Kazuki Kumada, Kenji Takeuchi, Kozo Tanno, Yasushi Yatabe, Kuniko Sunami, Tomoyuki Hishida, Yasunari Miyazaki, Hidemi Ito, Mitsuhiro Amemiya, Hirohiko Totsuka, Haruhiko Nakayama, Tomoyuki Yokose, Kazuyoshi Ishigaki, Toshiteru Nagashima, Yoichi Ohtaki, Kazuhiro Imai, Ken Takasawa, Yoshihiro Minamiya, Kazuma Kobayashi, Kenichi Okubo, Kenji Wakai, Atsushi Shimizu, Masayuki Yamamoto, Motoki Iwasaki, Koichi Matsuda, Johji Inazawa, Yuichi Shiraishi, Hiroyoshi Nishikawa, Yoshinori Murakami, Michiaki Kubo, Fumihiko Matsuda, Yoichiro Kamatani, Ryuji Hamamoto, Keitaro Matsuo, Takashi Kohno
    2024, 44(2): 287-293. https://doi.org/10.1002/cac2.12498
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