Molecular mechanisms and clinical applications of tumor budding in hepatocellular carcinoma

ZHANG Hongbin, TAN Kai, YANG Zhenyu, JIA Shengxiong, DU Xilin

PDF(546 KB)
PDF(546 KB)
Journal of Clinical Hepatol ›› 2025, Vol. 41 ›› Issue (05) : 963-967. DOI: 10.12449/JCH250524
Review

Molecular mechanisms and clinical applications of tumor budding in hepatocellular carcinoma

Author information +
History +

Abstract

Tumor budding is a distinct pathomorphological feature observed in various types of solid tumor. In recent years，tumor budding has been recognized as an important biological feature associated with tumor invasion and metastasis，and it has become a new focus in the research on tumor progression. Although studies have explored the role of tumor budding in different types of tumor，there are studies in the field of hepatocellular carcinoma （HCC）. This article systematically reviews the research advances in tumor budding in HCC，with a focus on the mechanism of tumor budding，the association between tumor budding and tumor progression，and the potential application of tumor budding in prognostic assessment，in order to provide new insights and strategies for the early diagnosis and treatment of HCC.

Key words

Carcinoma，Hepatocellular / Tumor Budding / Prognosis

Cite this article

EndNote

Ris (Procite)

Bibtex

Download Citations
ZHANG Hongbin , TAN Kai , YANG Zhenyu , et al . Molecular mechanisms and clinical applications of tumor budding in hepatocellular carcinoma. Journal of Clinical Hepatol. 2025, 41(05): 963-967 https://doi.org/10.12449/JCH250524

References

List( Publishing order | Descend order by publishing year | Descend order by cited within ) Chart analysis
[1]
BRAY F, LAVERSANNE M, SUNG H, et al. Global cancer statistics 2022: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries[J]. CA Cancer J Clin, 2024, 74(3): 229-263. DOI: 10.3322/caac.21834.
本文引用 [1]
[2]
PRASAD D, NGUYEN MH. Epidemiology, pathogenesis, diagnosis, surveillance, and management of hepatocellular carcinoma associated with vascular liver disease[J]. Kaohsiung J Med Sci, 2021, 37(5): 355-360. DOI: 10.1002/kjm2.12368.
本文引用 [1]
[3]
TÜMEN D, HEUMANN P, GÜLOW K, et al. Pathogenesis and current treatment strategies of hepatocellular carcinoma[J]. Biomedicines, 2022, 10(12): 3202. DOI: 10.3390/biomedicines10123202.
本文引用 [2]
[4]
TURAJLIC S, SWANTON C. Metastasis as an evolutionary process[J]. Science, 2016, 352(6282): 169-175. DOI: 10.1126/science.aaf2784.
本文引用 [1]
[5]
LUGLI A, ZLOBEC I, BERGER MD, et al. Tumour budding in solid cancers[J]. Nat Rev Clin Oncol, 2021, 18(2): 101-115. DOI: 10.1038/s41571-020-0422-y.
本文引用 [1]
[6]
HASE K, SHATNEY C, JOHNSON D, et al. Prognostic value of tumor “budding” in patients with colorectal cancer[J]. Dis Colon Rectum, 1993, 36(7): 627-635. DOI: 10.1007/BF02238588.
本文引用 [1]
[7]
REGMI SM, REGMI P, PAUDYAL A, et al. Tumor budding is associated with poor prognosis and clinicopathologic factors in esophageal carcinoma: A meta-analysis[J]. Eur J Surg Oncol, 2024, 50(12): 108668. DOI: 10.1016/j.ejso.2024.108668.
本文引用 [1]
[8]
OKCU O, ÖZTÜRK Ç, ŞEN B, et al. Tumor Budding is a reliable predictor for death and metastasis in invasive ductal breast cancer and correlates with other prognostic clinicopathological parameters[J]. Ann Diagn Pathol, 2021, 54: 151792. DOI: 10.1016/j.anndiagpath.2021.151792.
本文引用 [1]
[9]
GÜRÇAY N, ACAR LN, ÜNAL TDK, et al. High grade tumor budding is associated with poor survival in pathologic stage I lung adenocarcinoma[J]. Ann Diagn Pathol, 2023, 66: 152188. DOI: 10.1016/j.anndiagpath.2023.152188.
本文引用 [2]
[10]
KARAMITOPOULOU E, GLOOR B. Tumour budding is a strong and independent prognostic factor in pancreatic cancer. Reply to comment[J]. Eur J Cancer, 2013, 49(10): 2458-2459. DOI: 10.1016/j.ejca.2013.03.028.
本文引用 [1]
[11]
KEMI N, ESKURI M, IKÄLÄINEN J, et al. Tumor budding and prognosis in gastric adenocarcinoma[J]. Am J Surg Pathol, 2019, 43(2): 229-234. DOI: 10.1097/PAS.0000000000001181.
本文引用 [1]
[12]
KAIRALUOMA V, KEMI N, POHJANEN VM, et al. Tumour budding and tumour-stroma ratio in hepatocellular carcinoma[J]. Br J Cancer, 2020, 123(1): 38-45. DOI: 10.1038/s41416-020-0847-1.
本文引用 [2]
[13]
JIANG D, XU SS, ZHANG CP, et al. Association between the expression levels of ADAMTS16 and BMP2 and tumor budding in hepatocellular carcinoma[J]. Oncol Lett, 2023, 25(6): 256. DOI: 10.3892/ol.2023.13842.
本文引用 [5]
[14]
BERG KB, SCHAEFFER DF. Tumor budding as a standardized parameter in gastrointestinal carcinomas: More than just the colon[J]. Mod Pathol, 2018, 31(6): 862-872. DOI: 10.1038/s41379-018-0028-4.
本文引用 [1]
[15]
ALMANGUSH A, SALO T, HAGSTRÖM J, et al. Tumour budding in head and neck squamous cell carcinoma - a systematic review[J]. Histopathology, 2014, 65(5): 587-594. DOI: 10.1111/his.12471.
本文引用 [1]
[16]
ZLOBEC I, LUGLI A. Tumour budding in colorectal cancer: Molecular rationale for clinical translation[J]. Nat Rev Cancer, 2018, 18(4): 203-204. DOI: 10.1038/nrc.2018.1.
本文引用 [1]
[17]
NIRANJAN KC, RAJ M, HALLIKERI K. Prognostic evaluation of tumour budding in oral squamous cell carcinoma: Evidenced by CD44 expression as a cancer stem cell marker[J]. Pathol Res Pract, 2023, 251: 154883. DOI: 10.1016/j.prp.2023.154883.
本文引用 [1]
[18]
ALMAYOUF F. Tumor budding in upper gastrointestinal carcinomas: A systematic review and meta-analysis[J]. Cureus, 2024, 16(9): e70422. DOI: 10.7759/cureus.70422.
本文引用 [1]
[19]
KOVEITYPOUR Z, PANAHI F, VAKILIAN M, et al. Signaling pathways involved in colorectal cancer progression[J]. Cell Biosci, 2019, 9: 97. DOI: 10.1186/s13578-019-0361-4.
本文引用 [1]
[20]
SUN JY, YIN C, LI J. Research progress on pathways related to proliferation and metastasis of hepatocellular carcinoma[J]. Clin J Med Offic, 2024, 52(9): 982-985. DOI: 10.16680/j.1671-3826.2024.09.29.
孙嘉钰, 尹畅, 李京. 肝细胞癌增殖与转移相关通路研究进展[J]. 临床军医杂志, 2024, 52(9): 982-985. DOI: 10.16680/j.1671-3826.2024.09.29.
本文引用 [1]
[21]
HADDAD TS, van den DOBBELSTEEN L, ÖZTÜRK SK, et al. Pseudobudding: Ruptured glands do not represent true tumor buds[J]. J Pathol, 2023, 261(1): 19-27. DOI: 10.1002/path.6146.
本文引用 [2]
[22]
SHAKHPAZYAN N, MIKHALEVA L, BEDZHANYAN A, et al. Cellular and molecular mechanisms of the tumor stroma in colorectal cancer: Insights into disease progression and therapeutic targets[J]. Biomedicines, 2023, 11(9): 2361. DOI: 10.3390/biomedicines11092361.
本文引用 [1]
[23]
ROGERS AC, WINTER DC, HEENEY A, et al. Systematic review and meta-analysis of the impact of tumour budding in colorectal cancer[J]. Br J Cancer, 2016, 115(7): 831-840. DOI: 10.1038/bjc.2016.274.
本文引用 [1]
[24]
BOSCH SL, TEERENSTRA S, de WILT JH, et al. Predicting lymph node metastasis in pT1 colorectal cancer: A systematic review of risk factors providing rationale for therapy decisions[J]. Endoscopy, 2013, 45(10): 827-834. DOI: 10.1055/s-0033-1344238.
本文引用 [1]
[25]
KAUNDIYAL S, CHANDRA S, ARORA A. Study of tumor budding and its association with clinicopathological parameters in breast carcinoma[J]. Rev Assoc Med Bras (1992), 2024, 70(7): e20240173. DOI: 10.1590/1806-9282.20240173.
本文引用 [1]
[26]
VASUDEVAN S, KANNAN K, RAGHAVAN AV, et al. Analyzing tumor budding scores in invasive breast carcinoma: A tertiary care center study in south India[J]. J Pharm Bioallied Sci, 2024, 16(Suppl 2): S1850-S1853. DOI: 10.4103/jpbs.jpbs_910_23.
本文引用 [1]
[27]
YAAGOUBI S EL, ZARYOUHI M, BENMAAMAR S, et al. Prognostic impact of tumor budding on Moroccan gastric cancer patients[J]. Clin Pathol, 2023, 16: 2632010X231184329. DOI: 10.1177/2632010X231184329.
本文引用 [1]
[28]
RATHOD GB, DESAI KN, SHRIVASTAVA A, et al. Correlation of tumor budding with known clinicopathological, histomorphological and hormonal receptor status in patients with invasive breast carcinoma[J]. Cureus, 2022, 14(9): e29637. DOI: 10.7759/cureus.29637.
本文引用 [1]
[29]
KUMARGURU BN, RAMASWAMY AS, SHAIK S, et al. Tumor budding in invasive breast cancer - An indispensable budding touchstone[J]. Indian J Pathol Microbiol, 2020, 63(Supplement): S117-S122. DOI: 10.4103/IJPM.IJPM_731_18.
本文引用 [1]
[30]
de ASSIS EM, RODRIGUES M, VIEIRA JC, et al. Lymphatic vascular density, the expression of podoplanin and tumor budding in oral squamous cell carcinoma[J]. Head Neck Pathol, 2023, 17(2): 371-382. DOI: 10.1007/s12105-022-01511-z.
本文引用 [1]
[31]
ASSIS EM, RODRIGUES M, VIEIRA JC, et al. Microvascular density and tumor budding in oral squamous cell carcinoma[J]. Med Oral Patol Oral Cir Bucal, 2023, 28(2): e174-e182. DOI: 10.4317/medoral.25640.
本文引用 [1]
[32]
MAYER P, HAUSEN A, STEINLE V, et al. The radiomorphological appearance of the invasive margin in pancreatic cancer is associated with tumor budding[J]. Langenbeck’s Arch Surg, 2024, 409(1): 167. DOI: 10.1007/s00423-024-03355-3.
本文引用 [1]
[33]
WEI L, DELIN Z, KEFEI Y, et al. A classification based on tumor budding and immune score for patients with hepatocellular carcinoma[J]. Oncoimmunology, 2019, 9(1): 1672495. DOI: 10.1080/2162402X.2019.1672495.
本文引用 [2]
[34]
ZHOU B, ZONG S, ZHONG W, et al. Interaction between laminin-5γ2 and integrin β1 promotes the tumor budding of colorectal cancer via the activation of Yes-associated proteins[J]. Oncogene, 2020, 39(7): 1527-1542. DOI: 10.1038/s41388-019-1082-1.
本文引用 [1]
[35]
UNAL B, CELIK MY, GEDIK EO, et al. Tumor budding as a potential prognostic marker in determining the behavior of primary liver cancers[J]. World J Hepatol, 2023, 15(6): 775-785. DOI: 10.4254/wjh.v15.i6.775.
本文引用 [1]
[36]
SHAFIQ AM, TAHA NA, ZAKY AH, et al. Prognostic significance of the tumor budding and tumor-infiltrating lymphocytes in survival of hepatocellular carcinoma patients[J]. Int J Health Sci (Qassim), 2024, 18(6): 10-19.
本文引用 [1]
[37]
MONDAL S, ADHIKARI N, BANERJEE S, et al. Matrix metalloproteinase-9 (MMP-9) and its inhibitors in cancer: A minireview[J]. Eur J Med Chem, 2020, 194: 112260. DOI: 10.1016/j.ejmech.2020.112260.
本文引用 [1]
[38]
FUERST R, CHOI JY, KNAPINSKA AM, et al. Development of a putative Zn2+-chelating but highly selective MMP-13 inhibitor[J]. Bioorg Med Chem Lett, 2022, 76: 129014. DOI: 10.1016/j.bmcl.2022.129014.
本文引用 [1]
[39]
SANYAL S, AMIN SA, BANERJEE P, et al. A review of MMP-2 structures and binding mode analysis of its inhibitors to strategize structure-based drug design[J]. Bioorg Med Chem, 2022, 74: 117044. DOI: 10.1016/j.bmc.2022.117044.
本文引用 [1]
[40]
CHEN C, ZHAO SJ, KARNAD A, et al. The biology and role of CD44 in cancer progression: Therapeutic implications[J]. J Hematol Oncol, 2018, 11(1): 64. DOI: 10.1186/s13045-018-0605-5.
本文引用 [1]
[41]
MA ZL, GUO DL, WANG QX, et al. Lgr5-mediated p53 Repression through PDCD5 leads to doxorubicin resistance in hepatocellular carcinoma[J]. Theranostics, 2019, 9(10): 2967-2983. DOI: 10.7150/thno.30562.
本文引用 [1]
[42]
XIA LZ, OYANG L, LIN JG, et al. The cancer metabolic reprogramming and immune response[J]. Mol Cancer, 2021, 20(1): 28. DOI: 10.1186/s12943-021-01316-8.
本文引用 [1]
[43]
LI ZZ, SUN CJ, QIN ZH. Metabolic reprogramming of cancer-associated fibroblasts and its effect on cancer cell reprogramming[J]. Theranostics, 2021, 11(17): 8322-8336. DOI: 10.7150/thno.62378.
本文引用 [1]
[44]
ALAWYIA B, CONSTANTINOU C. Hepatocellular carcinoma: A narrative review on current knowledge and future prospects[J]. Curr Treat Options Oncol, 2023, 24(7): 711-724. DOI: 10.1007/s11864-023-01098-9.
本文引用 [1]

张宏斌负责确定选题，资料分析，撰写论文；谭凯、杨振宇参与文章审阅，修改论文；贾生雄负责文献检索，收集资料；杜锡林负责拟定写作思路，指导撰写文章并最后定稿。

Funding

The Science and Technology Project of Xi’an(23YXYJ0154)
Tangdu Hospital Discipline Promotion Project(2024JSYX019)

Comments

PDF(546 KB)

Accesses

Citation

Detail
Sections
Recommended
Copyright © Journal of Clinical Hepatol, All Rights Reserved.
Powered by Beijing Magtech Co. Ltd.

/

〈 〉