Zang Wenli, Geng Fengxue, Liu Junchao, Wang Zengxu, Zhang Shuwei, Li Yuchao, Lu Ze, Pan Yaping
Department of Periodontics, School and Hospital of Stomatology, China Medical University, Liaoning Provincial Key Laboratory of Oral Disease, Shenyang, China.
Department of Oral Maxillofacial-Head and Neck Surgery, School and Hospital of Stomatology, China Medical University, Liaoning Provincial Key Laboratory of Oral Disease, Shenyang, China.
Int J Oral Sci. 2025 Feb 28;17(1):15. doi: 10.1038/s41368-024-00342-8.
Cancer stem cells (CSCs) are widely acknowledged as primary mediators to the initiation and progression of tumors. The association between microbial infection and cancer stemness has garnered considerable scholarly interest in recent years. Porphyromonas gingivalis (P. gingivalis) is increasingly considered to be closely related to the development of oral squamous cell carcinoma (OSCC). Nevertheless, the role of P. gingivalis in the stemness of OSCC cells remains uncertain. Herein, we showed that P. gingivalis was positively correlated with CSC markers expression in human OSCC specimens, promoted the stemness and tumorigenicity of OSCC cells, and enhanced tumor formation in nude mice. Mechanistically, P. gingivalis increased lipid synthesis in OSCC cells by upregulating the expression of stearoyl-CoA desaturase 1 (SCD1) expression, a key enzyme involved in lipid metabolism, which ultimately resulted in enhanced acquisition of stemness. Moreover, SCD1 suppression attenuated P. gingivalis-induced stemness of OSCC cells, including CSCs markers expression, sphere formation ability, chemoresistance, and tumor growth, in OSCC cells both in vitro and in vivo. Additionally, upregulation of SCD1 in P. gingivalis-infected OSCC cells was associated with the expression of KLF5, and that was modulated by P. gingivalis-activated NOD1 signaling. Taken together, these findings highlight the importance of SCD1-dependent lipid synthesis in P. gingivalis-induced stemness acquisition in OSCC cells, suggest that the NOD1/KLF5 axis may play a key role in regulating SCD1 expression and provide a molecular basis for targeting SCD1 as a new option for attenuating OSCC cells stemness.
癌症干细胞(CSCs)被广泛认为是肿瘤发生和发展的主要介导因素。近年来,微生物感染与癌症干性之间的关联引起了学术界的广泛关注。牙龈卟啉单胞菌(P. gingivalis)越来越被认为与口腔鳞状细胞癌(OSCC)的发展密切相关。然而,牙龈卟啉单胞菌在OSCC细胞干性中的作用仍不确定。在此,我们表明牙龈卟啉单胞菌与人OSCC标本中CSC标志物的表达呈正相关,促进了OSCC细胞的干性和致瘤性,并增强了裸鼠体内的肿瘤形成。机制上,牙龈卟啉单胞菌通过上调硬脂酰辅酶A去饱和酶1(SCD1)的表达来增加OSCC细胞中的脂质合成,SCD1是参与脂质代谢的关键酶,最终导致干性获得增强。此外,SCD1抑制减弱了牙龈卟啉单胞菌诱导的OSCC细胞干性,包括CSC标志物表达、球体形成能力、化疗耐药性和肿瘤生长,无论是在体外还是体内的OSCC细胞中。此外,牙龈卟啉单胞菌感染的OSCC细胞中SCD1的上调与KLF5的表达相关,并且这是由牙龈卟啉单胞菌激活的NOD1信号通路调节的。综上所述,这些发现突出了SCD1依赖性脂质合成在牙龈卟啉单胞菌诱导的OSCC细胞干性获得中的重要性,表明NOD1/KLF5轴可能在调节SCD1表达中起关键作用,并为靶向SCD1作为减弱OSCC细胞干性的新选择提供了分子基础。