<italic style="font-style: italic">Aspongopus chinensis</italic>-derived cytochrome c delivered <italic style="font-style: italic">via</italic> lentivirus-like particles induces mitochondrial apoptosis to inhibit HER2-positive breast cancer

Li Xiping; Jia Bentao; Yang Xiaotong; Hou Zeyu; Dai Peifang; Qiu Mei; Liu Qing; Qi Ling; Shi Xiuli; Chen Shasha; Wang Min; Peng Li

doi:10.16016/j.2097-0927.202604068

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Aspongopus chinensis-derived cytochrome c delivered via lentivirus-like particles induces mitochondrial apoptosis to inhibit HER2-positive breast cancer

Monographic Reports | 更新时间：2026-10-01

- Aspongopus chinensis-derived cytochrome c delivered via lentivirus-like particles induces mitochondrial apoptosis to inhibit HER2-positive breast cancer
- Journal of Army Medical University Vol. 48, Issue 18, Pages: 2578-2592(2026)
- 作者机构：
  
  1.贵州中医药大学第二临床医学院，贵州贵阳
  2.贵州中医药大学第一附属医院，急诊科，贵州贵阳
  4.贵州中医药大学第一附属医院，党委办公室，贵州贵阳
  7.贵州中医药大学第一附属医院，重症医学科，贵州贵阳
  3.贵州医科大学附属医院重症医学科，贵州贵阳
  5.遵义医科大学附属医院甲乳外科，贵州遵义
  6.黑龙江中医药大学护理学院，黑龙江哈尔滨
  8.贵州中医药大学第二附属医院心血管内科，贵州贵阳
- 作者简介：
  
  Wang Min， E-mail： wangmin@stu.gzy.edu.cn；
  Peng Li， E-mail： dr_pengli@126.com
- 基金信息：
- DOI：10.16016/j.2097-0927.202604068
  CLC： R285.5;R730.23;R737.9
- Received：19 April 2026，
  
  Revised：2026-06-15，
  
  Accepted：20 June 2026，
  
  Published：30 September 2026
- 稿件说明：
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李习平，贾本涛，杨晓彤，等.通过慢病毒样颗粒载体递送九香虫来源细胞色素c基因诱导线粒体凋亡抑制HER2阳性乳腺癌［J］.陆军军医大学学报，2026，48（18）：2578-2592.DOI：10.16016/j.2097-0927.202604068.

Li X P，Jia B T，Yang X T，et al.Aspongopus chinensis-derived cytochrome c delivered via lentivirus-like particles induces mitochondrial apoptosis to inhibit HER2-positive breast cancer［J］.J Army Med Univ，2026，48（18）：2578-2592.DOI：10.16016/j.2097-0927.202604068.
李习平，贾本涛，杨晓彤，等.通过慢病毒样颗粒载体递送九香虫来源细胞色素c基因诱导线粒体凋亡抑制HER2阳性乳腺癌［J］.陆军军医大学学报，2026，48（18）：2578-2592.DOI：10.16016/j.2097-0927.202604068. DOI：

Li X P，Jia B T，Yang X T，et al.Aspongopus chinensis-derived cytochrome c delivered via lentivirus-like particles induces mitochondrial apoptosis to inhibit HER2-positive breast cancer［J］.J Army Med Univ，2026，48（18）：2578-2592.DOI：10.16016/j.2097-0927.202604068. DOI：

摘要

目的

HER2阳性乳腺癌约占全部乳腺癌的20%，其持续激活的HER2/PI3K/AKT信号通路可通过上调Bcl-2/Bcl-xL并抑制内源性细胞色素c（cytochrome c， Cyt c）释放，从而逃避线粒体凋亡。九香虫（

Aspongopus chinensis Dallas

）来源Cyt c具有潜在线粒体促凋亡活性。本研究构建递送九香虫来源Cyt c的慢病毒样颗粒（lentivirus-like particles，VLPs），并系统评价其对HER2阳性乳腺癌的抗肿瘤作用及相关机制。

方法

从九香虫组织中扩增Cyt c完整编码序列，并克隆至含mCherry报告基因的慢病毒载体pWSLV中，重组质粒与包装质粒共转染HEK293T细胞，构建mCherry-Cyt c-VLPs（滴度≥1×10

TU/mL），采用P24蛋白进行Western blot实验及测序验证包装是否成功。采用改良组织块法分离HER2阳性乳腺癌患者原代细胞，通过MUC1、Ki67、HER2、ER及PR免疫荧光进行表型鉴定。体外实验设PBS组、mCherry-VLP组和mCherry-Cyt c-VLP组（MOI=100）。①RT-qPCR和Western blot检测Cyt c递送效率；②MTT法（24 h和48 h）和Transwell实验（24 h）分别检测细胞活力与迁移能力；③流式细胞术分析细胞周期，并以Western blot检测CDK2和Cyclin A表达；④Annexin V-FITC/PI双染检测细胞凋亡，并检测Bcl-2、Bcl-xL、Bax、胞质Cyt c、cleaved Caspase-9及cleaved Caspase-3蛋白表达。建立HER2阳性乳腺癌患者来源异种移植（patient-derived xenograft model，PDX）模型（

=3），肿瘤内注射给药（50 μg/kg，20 μL/次，每2天1次，共20 d），记录肿瘤体积及体质量变化，并通过HE染色、Western blot、血常规及肝肾功能指标评价体内抗肿瘤作用与初步安全性。

结果

成功构建mCherry-Cyt c-VLPs，P24

蛋白表达阳性，提示病毒样颗粒包装完整。分离的原代乳腺癌细胞呈典型上皮样铺路石状形态，MUC1、Ki67、HER2、ER 及 PR 均呈阳性，确认为HER2阳性管腔B型乳腺癌原代细胞。体外实验结果：①基因递送验证：与 PBS 组及 mCherry-VLP组相比，mCherry-Cyt c-VLP组Cyt c mRNA（

0.000 1）和蛋白水平（

0.000 1）均显著升高，证实递送成功。②抗增殖与抗迁移：mCherry-Cyt c-VLP组细胞活力（

0.05）和迁移细胞数（

0.000 1）显著降低，mCherry-VLP组无显著影响（

0.05）。③细胞周期阻滞：mCherry-Cyt c-VLP 组流式检测显示G1期细胞比例显著增加、S期比例显著降低（

0.05），Western blot显示CDK2和Cyclin A蛋白水平显著下调（

0.000 1）。④凋亡诱导：mCherry-Cyt c-VLP组凋亡率约20%（

0.000 1），Bcl-2和Bcl-xL显著下调（

0.000 1），Bax、细胞质Cyt c、cleaved Caspase-9及cleaved Caspase-3均显著上调（

0.000 1），提示外源Cyt c表达激活了胞质caspase级联反应，线粒体凋亡通路被激活。体内PDX实验：mCherry-Cyt c-VLP 组肿瘤体积和质量均显著低于PBS组（

0.01），瘤组织HE染色示细胞密度降低、结构紊乱，瘤组织线粒体凋亡相关蛋白变化规律与体外一致，各组小鼠体质量及血液学、肝肾功能指标无显著差异（

0.05）。

结论

mCherry-Cyt c-VLPs 递送的九香虫来源Cyt c在HER2阳性乳腺癌细胞内持续表达，直接激活Caspase-9/3级联反应，导致肿瘤细胞增殖受抑和凋亡，体内外初步研究未见明显系统毒性。

Abstract

Objective

Human epidermal growth factor receptor 2 (HER2)-positive breast cancer accounts for approximately 20% of all breast cancer cases. Persistent activation of the HER2/PI3K/AKT signaling pathway enables tumor cells to evade mitochondrial apoptosis through upregulation of Bcl-2/Bcl-xL and suppression of endogenous cytochrome c (Cyt c) release. Cyt c derived from

Aspongopus chinensis

(

A.chinensis

) Dallas exhibits potential pro-apoptotic activity targeting mitochondria. This study aims to construct lentivirus-like particles (VLPs) delivering the

A. chinensis

-derived Cyt c and systematically evaluate their anti-tumor effects and underlying mechanisms in HER2-positive breast cancer.

Methods

The full-length coding sequence of Cyt c was amplified from

A. chinensis

tissu

es and cloned into the lentiviral vector pWSLV containing mCherry reporter. Recombinant plasmids were co-transfected with packaging plasmids into HEK293T cells to construct mCherry-Cyt c-VLPs (titer ≥1×10

TU/mL). P24 protein was detected with Western blotting and sequencing to confirm successful packaging. Primary cells isolated from HER2-positive breast cancer tissues using a modified tissue block culture method were phenotypically characterized by immunofluorescence staining for MUC1

Ki67

HER2

estrogen receptor (ER)

and progesterone receptor (PR).

In vitro

experiments included a PBS group

an mCherry-VLP group

and an mCherry-Cyt c-VLP group (MOI=100). ① RT-qPCR and Western blotting were used to evaluate Cyt c delivery efficiency; ② cell viability and migration were assessed by MTT assay (24 h and 48 h) and Transwell assay (24 h)

respectively; ③ cell cycle distribution was analyzed by flow cytometry

and CDK2 and Cyclin A expression levels were detected by Western blotting; ④ apoptosis was detected using Annexin V-FITC/PI double staining

and the expression levels of Bcl-2

Bcl-xL

Bax

cytosolic Cyt c

cleaved Caspase-9

and cleaved Caspase-3 were determined by Western blotting. A HER2-positive patient-derived xenograft (PDX) model was further established (

=3 per group). The mice received intratumoral injections (50 μg/kg

20 μL per injection

once every 2 days for 20 d). Tumor volume and body weight were recorded

and HE staining

Western blotting

blood routine test

and liver and kidney function tests were applied to evaluate

in vivo

antitumor efficacy and preliminary safety. Statistical analyses were performed using one-way ANOVA and Tukey's post hoc test

with

0.05 considered statistically significant.

Results

mCherry-Cyt c-VLPs were successfully constructed

and positive P24 protein expression confirmed intact VLP viral particle packaging. The isolated primary breast cancer cells exhi

bited typical epithelial cobblestone morphology and positive expression of MUC1

Ki67

HER2

and PR

confirming them as HER2-positive luminal B primary breast cancer cells.

In vitro

results: ① Gene delivery: compared with the PBS and mCherry-VLP groups

mCherry-Cyt c-VLP treatment significantly increased Cyt c at both mRNA (

0.0001) and protein levels (

0.000 1)

confirming successful delivery. ②Anti-proliferation and anti-migration: mCherry-Cyt c-VLP treatment significantly reduced cell viability (

0.05) and the number of migrated cells (

0.000 1)

whereas the empty-particle group showed no significant effect (

0.05). ③ Cell cycle arrest: flow cytometry revealed a significantly increased proportion of cells in G1 phase and a decreased proportion in S phase in the mCherry-Cyt c-VLP group (

0.05)

and Western blotting showed significantly downregulated CDK2 and Cyclin A protein levels (

0.000 1). ④Apoptosis induction: the mCherry-Cyt c-VLP group exhibited approximately 20% apoptosis rate (

0.000 1)

with significant downregulation of Bcl-2 and Bcl-xL (

0.000 1) and significant upregulation of Bax

cytosolic Cyt c

cleaved Caspase-9 and cleaved Caspase-3 (

0.000 1)

indicating that exogenous Cyt c expression activated the cytosolic Caspase cascade and thereby the mitochondrial apoptotic pathway.

In vivo

PDX experiments: the tumor volume and weight in the mCherry-Cyt c-VLP group were significantly lower than those in the control groups (

0.01). HE staining of tumor tissues showed decreased cell density and disordered architecture

with mitochondrial apoptosis-related protein changes in tumor tissue consistent with

in vitro

results. No significant differences were found across groups in mouse body weight or in hematological

liver and k

idney function indicators (

0.05).

Conclusion

The

A. chinensis

-derived Cyt c delivered by mCherry-Cyt c-VLPs is sustainably expressed in HER2-positive breast cancer cells and directly activates the Caspase-9/3 cascade

leading to suppressed proliferation and apoptosis of tumor cells. No obvious systemic toxicity is observed in either

in vitro

in vivo

experiments.

关键词

Keywords

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Aspongopus chinensis-derived cytochrome c delivered via lentivirus-like particles induces mitochondrial apoptosis to inhibit HER2-positive breast cancer

DOI：10.16016/j.2097-0927.202604068

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