Yang Hua, Cheung Pak-Hin Hinson, Wu Li
Department of Microbiology and Immunology, Carver College of Medicine, The University of Iowa, Iowa City, Iowa, USA.
mBio. 2025 May 28:e0042525. doi: 10.1128/mbio.00425-25.
Sterile alpha motif (SAM) and histidine-aspartate (HD) domain-containing protein 1 (SAMHD1) inhibits HIV-1 replication in non-dividing cells by reducing the intracellular dNTP pool. While SAMHD1 is known to promote spontaneous apoptosis, its role in HIV-1-induced apoptosis and the underlying mechanisms remain unclear. In this study, we identify a novel mechanism by which SAMHD1 enhances HIV-1-induced apoptosis in monocytic cells via the mitochondrial pathway. We demonstrate that SAMHD1 enhances apoptosis induced by HIV-1 infection in dividing monocytic THP-1 and U937 cell lines, but not in differentiated macrophage-like cells. Mechanistically, SAMHD1 expression reduces mitochondrial membrane potential and promotes cytochrome c release in HIV-1-infected THP-1 cells, thereby augmenting the mitochondrial apoptotic pathway. Furthermore, SAMHD1-enhanced apoptosis is linked to elevated levels of the pro-apoptotic protein BCL-2-interacting killer (BIK) in cells, which contributes to enhanced apoptosis during HIV-1 infection. These findings reveal a previously unrecognized regulatory role of SAMHD1 in amplifying HIV-1-induced apoptosis in monocytic cells, highlighting its involvement in the mitochondrial apoptotic pathway.IMPORTANCESterile alpha motif (SAM) and histidine-aspartate (HD) domain-containing protein 1 (SAMHD1), a dNTP triphosphohydrolase, lowers intracellular dNTP levels and restricts HIV-1 replication in non-dividing cells. HIV-1 infection induces cell death mainly through apoptosis. While we have shown that endogenous SAMHD1 enhances spontaneous apoptosis in monocytic cells, its role in HIV-1-induced apoptosis and the underlying mechanisms remain unknown. In this study, we aim to bridge this knowledge gap by investigating the functional significance of SAMHD1 in regulating apoptosis during HIV-1 infection of immune cells. Our findings reveal a novel mechanism whereby SAMHD1 enhances HIV-1-induced apoptosis in monocytic cells through the mitochondrial pathway. This suggests a previously unrecognized role of SAMHD1 in modulating cellular responses to HIV-1 infection.
含无菌α基序(SAM)和组氨酸-天冬氨酸(HD)结构域蛋白1(SAMHD1)通过降低细胞内脱氧核苷三磷酸(dNTP)池来抑制HIV-1在非分裂细胞中的复制。虽然已知SAMHD1会促进自发性凋亡,但其在HIV-1诱导的凋亡中的作用及潜在机制仍不清楚。在本研究中,我们确定了一种新机制,通过该机制SAMHD1经由线粒体途径增强HIV-1在单核细胞中诱导的凋亡。我们证明,SAMHD1增强HIV-1感染在分裂的单核THP-1和U937细胞系中诱导的凋亡,但在分化的巨噬细胞样细胞中则不然。从机制上讲,SAMHD1的表达降低了HIV-1感染的THP-1细胞的线粒体膜电位并促进细胞色素c释放,从而增强线粒体凋亡途径。此外,SAMHD1增强的凋亡与细胞中促凋亡蛋白BCL-2相互作用杀手(BIK)水平升高有关,这有助于在HIV-1感染期间增强凋亡。这些发现揭示了SAMHD1在放大HIV-1在单核细胞中诱导的凋亡方面以前未被认识的调节作用,突出了其参与线粒体凋亡途径。重要性含无菌α基序(SAM)和组氨酸-天冬氨酸(HD)结构域蛋白1(SAMHD1)是一种dNTP三磷酸水解酶,可降低细胞内dNTP水平并限制HIV-1在非分裂细胞中的复制。HIV-1感染主要通过凋亡诱导细胞死亡。虽然我们已经表明内源性SAMHD1增强单核细胞中的自发性凋亡,但其在HIV-1诱导的凋亡中的作用及潜在机制仍然未知。在本研究中,我们旨在通过研究SAMHD1在免疫细胞HIV-1感染期间调节凋亡的功能意义来填补这一知识空白。我们的发现揭示了一种新机制,通过该机制SAMHD1通过线粒体途径增强HIV-1在单核细胞中诱导的凋亡。这表明SAMHD1在调节细胞对HIV-1感染的反应方面有以前未被认识的作用。