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收稿日期:
2024-03-19
接受日期:
2024-05-14
出版日期:
2024-12-20
发布日期:
2024-12-20
通讯作者:
赵丽艳
E-mail:zhaoliy@jlu.edu.cn
作者简介:
沈忠军(2000-),男,安徽省阜阳市人,在读硕士研究生,主要从事肿瘤与血栓形成机制方面的研究。
基金资助:
Zhongjun SHEN1,Yao ZHAO2,Mingbo JIA1,Liyan ZHAO1()
Received:
2024-03-19
Accepted:
2024-05-14
Online:
2024-12-20
Published:
2024-12-20
Contact:
Liyan ZHAO
E-mail:zhaoliy@jlu.edu.cn
摘要:
上皮-间质转化(EMT)是包括神经胶质瘤在内的各种癌症发展的关键过程。在神经胶质瘤细胞中,缺氧诱导因子(HIF)的活化可以影响胶质瘤细胞发生EMT,促进细胞迁移和侵袭。现就HIF在胶质瘤细胞EMT过程中的作用进行综述,旨在探讨HIF对细胞迁移和侵袭的影响,包括对血管生成、代谢重编程、糖酵解及微环境免疫系统的调控,并总结HIF在Wnt/β-catenin、Notch和TGF-β等EMT相关信号通路中的作用,为深入理解HIF在胶质瘤细胞EMT过程中的机制研究提供新的思路和方向。
中图分类号:
沈忠军, 赵钥, 贾茗博, 赵丽艳. 缺氧诱导因子在胶质瘤细胞上皮-间质转化过程中对细胞迁移和侵袭影响的研究进展[J]. 吉林大学学报(医学版), 2024, (): 1-10.
Zhongjun SHEN, Yao ZHAO, Mingbo JIA, Liyan ZHAO. Research progress in effects of hypoxia-inducible factors on cell migration and invasion during epithelial-mesenchymal transition in glioma cells[J]. Journal of Jilin University(Medicine Edition), 2024, (): 1-10.
1 | TAN H X, CAO Z B, HE T T, et al. TGFβ1 is essential for MSCs-CAFs differentiation and promotes HCT116 cells migration and invasion via JAK/STAT3 signaling[J]. Onco Targets Ther, 2019, 12: 5323-5334. |
2 | YIN J H, WANG L, WANG Y, et al. Curcumin reverses oxaliplatin resistance in human colorectal cancer via regulation of TGF-β/Smad2/3 signaling pathway[J]. Onco Targets Ther, 2019, 12: 3893-3903. |
3 | ZHU L H, CHEN W, LI G Q, et al. Upregulated RACK1 attenuates gastric cancer cell growth and epithelial-mesenchymal transition via suppressing Wnt/β-catenin signaling[J]. Onco Targets Ther, 2019, 12: 4795-4805. |
4 | MAHASE S, RATTENNI R N, WESSELING P, et al. Hypoxia-mediated mechanisms associated with antiangiogenic treatment resistance in glioblastomas[J]. Am J Pathol, 2017, 187(5): 940-953. |
5 | KUSAMA K, FUKUSHIMA Y, YOSHIDA K, et al. Endometrial epithelial-mesenchymal transition (EMT) by menstruation-related inflammatory factors during hypoxia[J]. Mol Hum Reprod, 2021, 27(6): gaab036. |
6 | LIN J C, TSAI J T, CHAO T Y, et al. The STAT3/slug axis enhances radiation-induced tumor invasion and cancer stem-like properties in radioresistant glioblastoma[J]. Cancers, 2018, 10(12): 512. |
7 | KAHLERT U D, MACIACZYK D, DOOSTKAM S, et al. Activation of canonical WNT/β-catenin signaling enhances in vitro motility of glioblastoma cells by activation of ZEB1 and other activators of epithelial-to-mesenchymal transition[J]. Cancer Lett, 2012, 325(1): 42-53. |
8 | KONG D J, WANG Z W, SARKAR S H, et al. Platelet-derived growth factor-D overexpression contributes to epithelial-mesenchymal transition of PC3 prostate cancer cells[J]. Stem Cells, 2008, 26(6): 1425-1435. |
9 | LU Z M, GHOSH S, WANG Z Y, et al. Downregulation of caveolin-1 function by EGF leads to the loss of E-cadherin, increased transcriptional activity of beta-catenin, and enhanced tumor cell invasion[J]. Cancer Cell, 2003, 4(6): 499-515. |
10 | ZHANG J, CAI H Q, SUN L X, et al. LGR5, a novel functional glioma stem cell marker, promotes EMT by activating the Wnt/β-catenin pathway and predicts poor survival of glioma patients[J]. J Exp Clin Cancer Res, 2018, 37(1): 225. |
11 | ZHAO L, LI X Q, SU J, et al. STAT1 determines aggressiveness of glioblastoma both in vivo and in vitro through Wnt/β-catenin signalling pathway[J]. Cell Biochem Funct, 2020, 38(5): 630-641. |
12 | CHI D P, ZHANG W, JIA Y L, et al. Spalt-like transcription factor 1 (SALL1) gene expression inhibits cell proliferation and cell migration of human glioma cells through the Wnt/β-catenin signaling pathway[J]. Med Sci Monit Basic Res, 2019, 25: 128-138. |
13 | LIU Z J, LIU H L, ZHOU H C, et al. TIPE2 inhibits hypoxia-induced Wnt/β-catenin pathway activation and EMT in glioma cells[J]. Oncol Res, 2016, 24(4): 255-261. |
14 | LIANG Y K, VOSHART D, PARIDAEN J T M L, et al. CD146 increases stemness and aggressiveness in glioblastoma and activates YAP signaling[J]. Cell Mol Life Sci, 2022, 79(8): 398. |
15 | PU B, ZHANG X, YAN T F, et al. Mical2 promotes proliferation and migration of glioblastoma cells through TGF-β/p-Smad2/EMT-Like signaling pathway[J]. Front Oncol, 2021, 11: 735180. |
16 | SUN E Y, LI Z, CAI H H, et al. HOXC6 regulates the epithelial-mesenchymal transition through the TGF-β/smad signaling pathway and predicts a poor prognosis in glioblastoma[J]. J Oncol, 2022, 2022: 8016102. |
17 | GAO Y, ZHENG H, LI L D, et al. KIF3C promotes proliferation, migration, and invasion of glioma cells by activating the PI3K/AKT pathway and inducing EMT[J]. Biomed Res Int, 2020, 2020: 6349312. |
18 | GAO K, JI Z W, SHE K, et al. Long non-coding RNA ZFAS1 is an unfavourable prognostic factor and promotes glioma cell progression by activation of the Notch signaling pathway[J]. Biomedecine Pharmacother, 2017, 87: 555-560. |
19 | WANG Y R, SONG W, KAN P C, et al. Overexpression of Epsin3 enhances migration and invasion of glioma cells by inducing epithelial-mesenchymal transition[J]. Oncol Rep, 2018, 40(5): 3049-3059. |
20 | LEI J J, MA J G, MA Q Y, et al. Hedgehog signaling regulates hypoxia induced epithelial to mesenchymal transition and invasion in pancreatic cancer cells via a ligand-independent manner[J]. Mol Cancer, 2013, 12: 66. |
21 | SHI J, CHEN J, SERRADJI N, et al. PMS1077 sensitizes TNF-α induced apoptosis in human prostate cancer cells by blocking NF-κB signaling pathway[J]. PLoS One, 2013, 8(4): e61132. |
22 | ZHANG L, ZHANG W, LI Y, et al. SHP-2-upregulated ZEB1 is important for PDGFRα-driven glioma epithelial-mesenchymal transition and invasion in mice and humans[J]. Oncogene, 2016, 35(43): 5641-5652. |
23 | LV F, DU Q, LI L, et al. Eriodictyol inhibits glioblastoma migration and invasion by reversing EMT via downregulation of the P38 MAPK/GSK-3β/ZEB1 pathway[J]. Eur J Pharmacol, 2021, 900: 174069. |
24 | CHEN B, LI X L, WU L H, et al. Quercetin suppresses human glioblastoma migration and invasion via GSK3β/β-catenin/ZEB1 signaling pathway [J]. Front Pharmacol, 2022, 13: 963614. |
25 | YANG W, WU P F, MA J X, et al. Sortilin promotes glioblastoma invasion and mesenchymal transition through GSK-3β/β-catenin/twist pathway[J]. Cell Death Dis, 2019, 10(3): 208. |
26 | YANG L Q, LIN C Y, WANG L, et al. Hypoxia and hypoxia-inducible factors in glioblastoma multiforme progression and therapeutic implications[J]. Exp Cell Res, 2012, 318(19): 2417-2426. |
27 | JOCHMANOVÁ I, ZELINKA T, WIDIMSKÝ J Jr, et al. HIF signaling pathway in pheochromocytoma and other neuroendocrine tumors[J]. Physiol Res, 2014, 63(): S251-S262. |
28 | GORT E H, GROOT A J, VAN DER WALL E, et al. Hypoxic regulation of metastasis via hypoxia-inducible factors[J]. Curr Mol Med, 2008, 8(1): 60-67. |
29 | SEMENZA G L. Oxygen sensing, hypoxia-inducible factors, and disease pathophysiology[J]. Annu Rev Pathol, 2014, 9: 47-71. |
30 | PERSANO L, PISTOLLATO F, RAMPAZZO E, et al. BMP2 sensitizes glioblastoma stem-like cells to Temozolomide by affecting HIF-1α stability and MGMT expression[J]. Cell Death Dis, 2012, 3(10): e412. |
31 | MALEKAN M, EBRAHIMZADEH M A, SHEIDA F. The role of Hypoxia-Inducible Factor-1alpha and its signaling in melanoma[J]. Biomed Pharmacother, 2021, 141: 111873. |
32 | LU N, PIAO M H, FENG C S, et al. Isoflurane promotes epithelial-to-mesenchymal transition and metastasis of bladder cancer cells through HIF-1α-β-catenin/ Notch1 pathways[J]. Life Sci, 2020, 258: 118154. |
33 | WEI M, MA R, HUANG S L, et al. Oroxylin A increases the sensitivity of temozolomide on glioma cells by hypoxia-inducible factor 1α/hedgehog pathway under hypoxia[J]. J Cell Physiol, 2019, 234(10): 17392-17404. |
34 | HUANG W Y, DING X P, YE H B, et al. Hypoxia enhances the migration and invasion of human glioblastoma U87 cells through PI3K/Akt/mTOR/HIF-1α pathway[J]. Neuroreport, 2018, 29(18): 1578-1585. |
35 | XIA P, XU X Y. PI3K/Akt/mTOR signaling pathway in cancer stem cells: from basic research to clinical application[J]. Am J Cancer Res, 2015, 5(5): 1602-1609. |
36 | LIN Y H, GUO L. GLI1 is involved in HIF-1α-induced migration, invasion, and epithelial-mesenchymal transition in glioma cells[J]. Folia Histochem Cytobiol, 2022, 60(2): 156-166. |
37 | WANG T C, LUO S J, LIN C L, et al. Modulation of p75 neurotrophin receptor under hypoxic conditions induces migration and invasion of C6 glioma cells[J]. Clin Exp Metastasis, 2015, 32(1): 73-81. |
38 | TONG B, PANTAZOPOULOU V, JOHANSSON E, et al. The p75 neurotrophin receptor enhances HIF-dependent signaling in glioma[J]. Exp Cell Res, 2018, 371(1): 122-129. |
39 | KIM K Y, PERKINS G A, SHIM M S, et al. DRP1 inhibition rescues retinal ganglion cells and their axons by preserving mitochondrial integrity in a mouse model of glaucoma[J]. Cell Death Dis, 2015, 6(8): e1839. |
40 | ZHANG B, CHEN Y, SHI X L, et al. Regulation of branched-chain amino acid metabolism by hypoxia-inducible factor in glioblastoma[J]. Cell Mol Life Sci, 2021, 78(1): 195-206. |
41 | ZHANG B, CHEN Y, BAO L, et al. GPT2 is induced by hypoxia-inducible factor (HIF)-2 and promotes glioblastoma growth[J]. Cells, 2022, 11(16): 2597. |
42 | WANG Q, ZHANG C, ZHU J L, et al. Crucial role of RLIP76 in promoting glycolysis and tumorigenesis by stabilization of HIF-1α in glioma cells under hypoxia[J]. Mol Neurobiol, 2022, 59(11): 6724-6739. |
43 | ZHANG G, TAO X, JI B W, et al. Hypoxia-driven M2-polarized macrophages facilitate cancer aggressiveness and temozolomide resistance in glioblastoma[J]. Oxid Med Cell Longev, 2022, 2022: 1614336. |
44 | ZHANG P C, LIU X, LI M M, et al. AT-533, a novel Hsp90 inhibitor, inhibits breast cancer growth and HIF-1α/VEGF/VEGFR-2-mediated angiogenesis in vitro and in vivo[J]. Biochem Pharmacol, 2020, 172: 113771. |
45 | SRIVASTAVA C, IRSHAD K, DIKSHIT B, et al. FAT1 modulates EMT and stemness genes expression in hypoxic glioblastoma[J]. Int J Cancer, 2018, 142(4): 805-812. |
46 | ZHANG S Y, WANG W W, LIU G X, et al. Long non-coding RNA HOTTIP promotes hypoxia-induced epithelial-mesenchymal transition of malignant glioma by regulating the miR-101/ZEB1 axis[J]. Biomedecine Pharmacother, 2017, 95: 711-720. |
47 | DEPNER C, BUTTEL HZUM, BÖĞÜRCÜ N, et al. EphrinB2 repression through ZEB2 mediates tumour invasion and anti-angiogenic resistance[J]. Nat Commun, 2016, 7: 12329. |
48 | LIU H, CHEN C J, ZENG J H, et al. MicroRNA-210-3p is transcriptionally upregulated by hypoxia induction and thus promoting EMT and chemoresistance in glioma cells[J]. PLoS One, 2021, 16(7): e0253522. |
49 | SONG Y, ZHENG S H, WANG J Z, et al. Hypoxia-induced PLOD2 promotes proliferation, migration and invasion via PI3K/Akt signaling in glioma [J]. Oncotarget, 2017, 8(26): 41947-41962. |
50 | KAR R, JHA N K, JHA S K, et al. A “NOTCH” deeper into the epithelial-to-mesenchymal transition (EMT) program in breast cancer[J]. Genes, 2019, 10(12): 961. |
51 | DE CRAENE B, BERX G. Regulatory networks defining EMT during cancer initiation and progression[J]. Nat Rev Cancer, 2013, 13(2): 97-110. |
52 | LOH C Y, CHAI J Y, TANG T F, et al. The E-cadherin and N-cadherin switch in epithelial-to-mesenchymal transition: signaling, therapeutic implications, and challenges[J]. Cells, 2019, 8(10): 1118. |
53 | LIU T J, ZHAO X L, ZHENG X, et al. The EMT transcription factor, Twist1, as a novel therapeutic target for pulmonary sarcomatoid carcinomas[J]. Int J Oncol, 2020, 56(3): 750-760. |
54 | TRAN D D, CORSA C A, BISWAS H, et al. Temporal and spatial cooperation of Snail1 and Twist1 during epithelial-mesenchymal transition predicts for human breast cancer recurrence[J]. Mol Cancer Res, 2011, 9(12): 1644-1657. |
55 | ZHANG W J, SHI X P, PENG Y, et al. HIF-1α promotes epithelial-mesenchymal transition and metastasis through direct regulation of ZEB1 in colorectal cancer[J]. PLoS One, 2015, 10(6): e0129603. |
56 | JOSEPH J V, CONROY S, PAVLOV K, et al. Hypoxia enhances migration and invasion in glioblastoma by promoting a mesenchymal shift mediated by the HIF1α-ZEB1 axis[J]. Cancer Lett, 2015, 359(1): 107-116. |
57 | CHEN Z M, MOU L, PAN Y H, et al. CXCL8 promotes glioma progression by activating the JAK/STAT1/HIF-1α/snail signaling axis[J]. Onco Targets Ther, 2019, 12: 8125-8138. |
58 | NOPPARAT J, ZHANG J, LU J P, et al. δ-Catenin, a Wnt/β-catenin modulator, reveals inducible mutagenesis promoting cancer cell survival adaptation and metabolic reprogramming[J]. Oncogene, 2015, 34(12): 1542-1552. |
59 | LIU H, YIN J, WANG H S, et al. FOXO3a modulates WNT/β-catenin signaling and suppresses epithelial-to-mesenchymal transition in prostate cancer cells[J]. Cell Signal, 2015, 27(3): 510-518. |
60 | TIAN Q, XUE Y, ZHENG W, et al. Overexpression of hypoxia-inducible factor 1α induces migration and invasion through Notch signaling[J]. Int J Oncol, 2015, 47(2): 728-738. |
61 | QIANG L, WU T, ZHANG H W, et al. HIF-1α is critical for hypoxia-mediated maintenance of glioblastoma stem cells by activating Notch signaling pathway[J]. Cell Death Differ, 2012, 19(2): 284-294. |
62 | SU X S, YANG Y H, GUO C F, et al. NOX4-derived ROS mediates TGF-β1-induced metabolic reprogramming during epithelial-mesenchymal transition through the PI3K/AKT/HIF-1α pathway in glioblastoma[J]. Oxid Med Cell Longev, 2021, 2021: 5549047. |
63 | ONISHI H, KAI M, ODATE S, et al. Hypoxia activates the hedgehog signaling pathway in a ligand-independent manner by upregulation of Smo transcription in pancreatic cancer[J]. Cancer Sci, 2011, 102(6): 1144-1150. |
64 | BHURIA V, XING J, SCHOLTA T, et al. Hypoxia induced Sonic Hedgehog signaling regulates cancer stemness, epithelial-to-mesenchymal transition and invasion in cholangiocarcinoma[J]. Exp Cell Res, 2019, 385(2): 111671. |
65 | LIU J H, GAO L, ZHAN N, et al. Hypoxia induced ferritin light chain (FTL) promoted epithelia mesenchymal transition and chemoresistance of glioma[J]. J Exp Clin Cancer Res, 2020, 39(1): 137. |
66 | ZHANG L, CAO Y Y, GUO X X, et al. Hypoxia-induced ROS aggravate tumor progression through HIF-1α-SERPINE1 signaling in glioblastoma[J]. J Zhejiang Univ Sci B, 2023, 24(1): 32-49. |
67 | QIU W J, SONG S B, CHEN W, et al. Hypoxia-induced EPHB2 promotes invasive potential of glioblastoma[J]. Int J Clin Exp Pathol, 2019, 12(2): 539-548. |
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