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Harnessing bacteria for tumor therapy:Current advances and challenges

Chinese Chemical Letters 2024年第2期35卷 97-106页

作者： Lina Guo Jinsong Ding wenhu zhou Xiangya School of Pharmaceutical Sciences Central South UniversityChangsha 410013China Changsha Medical University Academician WorkstationChangsha 410219China Key Laboratory of Biological Nanotechnology of National Health Commission Changsha 410008China

After a century of standstill,bacteria-based tumor therapy has resurged recently benefiting from the revolution of tumor immunotherapy,which provides unique solutions to tackle the obstacles of traditional tumor treatments.Obligate and facultative anaerobes with active tropism can selectively colonize at tumor sites and suppress tumor growth via different mechanisms,serving as attractive tools for tumor treatment either as a monotherapy or combining with other therapies for synergistic anti-tumor effects.In this critical review,we introduce the recent advances of bacteria-based tumor therapy from the following aspects.First,the general properties of bacteria are reviewed emphasizing on their structural components related to tumor immunotherapy,and the main bacteria that have been used in tumor therapy are listed.Then,the benefits of bacteria for tumor therapy are illustrated,such as tumor targetability,deep penetration,and facile genetic engineering for attenuation,enhanced efficacy,as well as bioimaging.Next,anti-tumor mechanisms of bacteria are summarized,which refer to intrinsic tumoricidal activities,immune activation,bacteria metabolism,and their capability to regulate gut microbiota homeostasis.Moreover,bacteria could act as carriers to deliver various types of therapeutics to achieve combination therapy with improved efficacy.In addition,several challenges for anti-tumor applications of bacteria are discussed regarding the delivery,efficacy and safety issues,and potential solutions are also provided.Finally,the possible improvements and perspectives are discussed in the end,which provide a guideline for the design of advanced bacteria-based tumor therapeutics in the future.

关键词： Bacteria Tumor targeting Immunotherapy Combination therapy Genetic engineering Surface decoration

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Recent progress of vaccines administration via microneedles for cancer immunotherapy

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Chinese Chemical Letters 2024年第3期35卷 96-103页

作者： Yuanzheng Chen Jiaojiao Zhu Jinsong Ding wenhu zhou Xiangya School of Pharmaceutical Sciences Central South UniversityChangsha 410013China Key Laboratory of Biological Nanotechnology of National Health Commission Changsha 410008China

Therapeutic cancer vaccines have undergone a resurgence in the past decade.Because of the high level of immune cell accumulation and abundant capillary lymphatic system in the dermis,percutaneous vaccination is considered to be an ideal treatment route.For convenient administration,the recent development of microneedles(MNs)provides a safe,painless,and low-cost transdermal delivery strategy,which could bypass the first-pass metabolism of vaccines for enhanced stability and bioavailability.However,the therapeutic effect of MNs-based cancer vaccines is not optimal,which is limited by the complex set of host,tumor,and environmental factors,as well as the limited vaccine loading capacity.Therefore,further improvements are still required to push their clinical translation.In this critical review,we deliberate on how to improve the therapeutic effect of MNs-based vaccines for cancer immunotherapy,summarize the recent advances in MNs-based cancer vaccination,and provide an overview of various design strategies and mechanisms for active or passive targeting delivery,aiming to develop safer,more effective,and more stable MNs-based cancer vaccines.Finally,we briefly describe the potential of vaccine platforms in combination with other therapies,suggest the need to design vaccines according to specific circumstances,and discuss the biosafety of repeated administration for enhancing clinical efficacy.

关键词： Transdermal delivery Microneedles Cancer vaccine Immunotherapy Nanoparticle Lymph node

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Mn-based cGAS-STING activation for tumor therapy

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Chinese Journal of Cancer Research 2023年第1期35卷 19-43页

作者： Aiping Huang wenhu zhou Xiangya School of Pharmaceutical Sciences Central South UniversityChangsha 410013China Changsha Medical University Academician WorkstationChangsha 410219China

Immunotherapy has efficiently revolutionized the treatment of human neoplastic diseases.However,the overall responsive rate of current immunotherapy is still unsatisfactory,benefiting only a small proportion of patients.Therefore,significant attention has been paid to the modulation of tumor microenvironment(TME)for the enhancement of immunotherapy.Interestingly,recent studies have shown that cyclic GMP-AMP synthasestimulator of interferon gene(cGAS-STING)was initially found as an innate immune sensor to recognize cytoplasmic DNA(such as bacterial,viral,micronuclei,and mitochondrial).It is a promising signaling pathway to activate antitumor immune responses via type I interferon production.Notably,Mn^(2+)was found to be a critical molecule to sensitize the activation of the cGAS-STING pathway for better immunotherapy.This activation led to the development of Mn^(2+)-based strategies for tumor immunotherapy via the activation of the cGAS-STING pathway.In this critical review,we aimed to summarize the recent progress of this field,focusing on the following three aspects.First,we briefly introduced the signaling pathway of cGAS-STING activation,and its regulation effect on the antitumor immunity cycle has been discussed.Along with this,several agonists of the cGAS-STING pathway were introduced with their potential as immunotherapeutic drugs.Then,the basic biological functions of Mn^(2+)have been illustrated,focusing on its critical roles in the cGAS-STING pathway activation.Next,we systematically reviewed the Mn^(2+)-based strategies for tumor immunotherapy,which can be classified by the methods based on Mn^(2+)alone or Mn^(2+)combined with other therapeutic modalities.We finally speculated the future perspectives of the field and provided rational suggestions to develop better Mn^(2+)-based therapeutics.

关键词： Tumor immunity metal ions combinatorial therapy targeting nanoparticles

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Converting bacteria into autologous tumor vaccine via surface biomineralization of calcium carbonate for enhanced immunotherapy

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Acta Pharmaceutica Sinica B 2023年第12期13卷 5074-5090页

作者： Lina Guo Jinsong Ding wenhu zhou Xiangya School of Pharmaceutical Sciences Central South UniversityChangsha 410013China Key Laboratory of Biological Nanotechnology of National Health Commission Xiangya HospitalChangsha 410008China

Autologous cancer vaccine that stimulates tumor-specific immune responses for personalized immunotherapy holds great potential for tumor therapy.However,its efficacy is still suboptimal due to the immunosuppressive tumor microenvironment(ITM).Here,we report a new type of bacteria-based autologous cancer vaccine by employing calcium carbonate(CaCO_(3))biomineralized Salmonella(Sal)as an in-situ cancer vaccine producer and systematical ITM regulator.CaCO_(3) can be facilely coated on the Sal surface with calcium ionophore A23187 co-loading,and such biomineralization did not affect the bioactivities of the bacteria.Upon intratumoral accumulation,the CaCO_(3) shell was decomposed at an acidic microenvironment to atenuate tumor acidity,accompanied by the release of Sal and Ca^(2+)/A23187.Specifically,Sal served as a cancer vaccine producer by inducing cancer cells'immunogenic cell death(ICD)and promoting the gap junction formation between tumor cells and dendritic cells(DCs)to promote antigen presentation.Ca^(2+),on the other hand,was intermalized into various types of immune cells with the aid of A23187 and synergized with Sal to systematically regulate the immune system,including DCs maturation,macrophages polarization,and T cells activation.As a result,such bio-vaccine achieved remarkable effcacy against both primary and metastatic tumors by eliciting potent anti-tumor immunity with full biocompatibility.This work demonstrated the potential of bioengineered bacteria as bio-active vaccines for enhanced tumor immunotherapy.

关键词： Bacteria-mediated cancer therapy Tumor microenvironment Calcium carbonate Mineralization Metalloimmunology Autologous tumor vaccine Immunotherapy Tumor metastasis

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Macrophage-targeted nanomedicine for chronic diseases immunotherapy

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Chinese Chemical Letters 2022年第2期33卷 597-612页

作者： Yuejia Song Yaqian Huang Fang zhou Jinsong Ding wenhu zhou Xiangya School of Pharmaceutical Sciences Central South UniversityChangsha 410013China Academician Workstation Changsha Medical UniversityChangsha 410219China Department of Pharmacy Southern University of Science and Technology HospitalShenzhen 518055China

Macrophage is the key innate immune effector in first-line defense against the pathogens, and can be polarized into different phenotypes to regulate a variety of immunological functions. However, the plasticity of macrophage is extraordinarily recruited, activated, and polarized under pathological conditions,playing paramount roles in occurrence, development, and prognosis of various chronic diseases, such as rheumatoid arthritis(RA), atherosclerosis(AS), and cancer. To this end, macrophage has become an important therapeutic target for etiological treatment of these diseases. Meanwhile, with the development of nanotechnology, various nano-drug delivery systems have been explored to target macrophages for disease modulation, displaying unique advantages to address both pharmaceutic and biopharmaceutic limitations of various drugs. This review aims to summarize the recent progress of macrophage-targeted nanomedicine for chronic diseases immunotherapy. First, the origin, polarization and biological functions of macrophages have been introduced, in which macrophages can differentiate into different phenotypes in response to physiological stimuli to play various immunological roles. Then, the macrophage disorder has been reviewed in related with various chronic diseases, and several representative diseases, including AS, RA, obesity, and cancer, have been discussed in detail to elucidate the pathological contributions of macrophages for disease progress. Next, strategies to regulate macrophages for diseases immunotherapy, such as macrophages depletion, macrophage reprograming, inhibition of macrophage recruitment,are summarized, and particular attention has been paid on bio-functional nanomaterials to engineer macrophages via different mechanisms. Further, methods for macrophage-targeting delivery nanosystems are discussed based on both passive and active targeting approaches. Finally, the perspective is speculated for potential clinical translation, and there still has significant room for the development of novel m

关键词： Nanoparticles Delivery Macrophages Polarization Immunotherapy

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Fenton metal nanomedicines for imaging-guided combinatorial chemodynamic therapy against cancer

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Asian Journal of Pharmaceutical Sciences 2022年第2期17卷 177-192页

作者： Peng Liu Ying Peng Jinsong Ding wenhu zhou Xiangya School of Pharmaceutical Sciences Central South UniversityChangsha 410013China Henan Key Laboratory of Biomolecular Recognition and Sensing Shangqiu Normal UniversityShangqiu 476000China

Chemodynamic therapy(CDT)is considered as a promising modality for selective cancer therapy,which is realized via Fenton reaction-mediated decomposition of endogenous H_(2)O_(2) to produce toxic hydroxyl radical(•OH)for tumor ablation.While extensive efforts have been made to develop CDT-based therapeutics,their in vivo efficacy is usually unsatisfactory due to poor catalytic activity limited by tumor microenvironment,such as anti-oxidative systems,insufficient H_(2)O_(2),and mild acidity.To mitigate these issues,we have witnessed a surge in the development of CDT-based combinatorial nanomedicines with complementary or synergistic mechanisms for enhanced tumor therapy.By virtue of their bio-imaging capabilities,Fenton metal nanomedicines(FMNs)are equipped with intrinsic properties of imaging-guided tumor therapies.In this critical review,we summarize recent progress of this field,focusing on FMNs for imaging-guided combinatorial tumor therapy.First,various Fenton metals with inherent catalytic performances and imaging properties,including Fe,Cu and Mn,were introduced to illustrate their possible applications for tumor theranostics.Then,CDT-based combinatorial systems were reviewed by incorporating many other treatment means,including chemotherapy,photodynamic therapy(PDT),sonodynamic therapy(SDT),photothermal therapy(PTT),starvation therapy and immunotherapy.Next,various imaging approaches based on Fenton metals were presented in detail.Finally,challenges are discussed,and future prospects are speculated in the field to pave way for future developments.

关键词： combinatorial medicines equipped

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Non-cytotoxic nanoparticles re-educating macrophages achieving both innate and adaptive immune responses for tumor therapy

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Asian Journal of Pharmaceutical Sciences 2022年第4期17卷 557-570页

作者： Shengmei Wang Xuanjun Liu Minghua Yang Linqi Ouyang Jinsong Ding Shengfeng Wang wenhu zhou Department of Pharmacy The Third Xiangya HospitalCentral South UniversityChangshaHunan410013China Xiangya School of Pharmaceutical Sciences Central South UniversityChangshaHunan410013China Postdoctoral Research Station of Clinical Medicine and Department of Pediatrics The Third Xiangya HospitalCentral South UniversityChangshaHunan410013China The First Hospital of Hunan University of Chinese Medicine ChangshaHunan410007China

Macrophages are important antigen-presenting cells to combat tumor via both innate and adaptive immunity,while they are programmed toM2 phenotype in established tumors and instead promote cancer development and metastasis.Here,we develop a nanomedicine that can re-educate M2 polarized macrophages to restore their anti-tumor activities.The nanomedicine has a core-shell structure to co-load IPI549,a PI3Kγinhibitor,and CpG,a Toll-like receptor 9 agonist.Specifically,the hydrophobic IPI549 is self-assembled into a pure drug nano-core,while MOF shell layer is coated for CpG encapsulation,achieving extra-high total drugs loading of 44%.Such nanosystem could facilitate intracellular delivery of the payloads but without any cytotoxicity,displaying excellent biocompatibility.After entering macrophages,the released IPI549 and CpG exert a synergistic effect to switch macrophages from M2 to M1 phenotype,which enables anti-tumor activities via directly engulfing tumor cells or excreting tumor killing cytokines.Moreover,tumor antigens released from the dying tumor cells could be effectively presented by the re-educated macrophages owing to the up-regulation of various antigen presenting mediators,resulting in infiltration and activation of cytotoxic T lymphocytes.As a result,the nanosystem triggers a robust antitumor immune response in combination with PD-L1 antibody to inhibit tumor growth and metastasis.This work provides a non-cytotoxic nanomedicine to modulate tumor immune microenvironment by reprograming macrophages.

关键词： Core-shell nanoparticles Metal-organic-framework CpG IPI549 Tumor immunotherapy

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Copper carbonate nanoparticles as an effective biomineralized carrier to load macromolecular drugs for multimodal therapy

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中国化学快报:英文版 2023年第9期34卷 204-209页

作者： Liping Dong Jinsong Ding Lemei Zhu Yujun Liu Xiang Gao wenhu zhou Changsha Medical University Academician WorkstationChangsha 410219China Xiangya School of Pharmaceutical Sciences Central South UniversityChangsha 410013China State Key Laboratory of Toxicology and Medical Countermeasures Institute of Pharmacology and ToxicologyBeijing 100850China Key Laboratory of Biological Nanotechnology of National Health Commission Changsha 410000China

Macromolecular drugs have attracted great interest as biotherapy to cure previously untreatable diseases.For clinical translation,biomacromolecules encounter several common druggability difficulties,such as in vivo instability and poor penetration to cross physiologic barriers,thus requiring sophisticated systems for drug delivery.Inspired by the natural biomineralization via interaction between inorganic ions and biomacromolecules,herein we rationally screened biocompatible transition metals to biomineralize with carbonate for macromolecules loading.Among the metal ions,Cu^(2+)was found to be the best candidate,and its superiority over the widely studied Ca^(2+)minerals was also demonstrated.Capitalized on this finding,copper carbonate nanoparticles were prepared via a simple mixing process to co-load glucose oxidase(GOx)and a HIF-αDNAzyme(DZ),achieving ultra-high loading capacity of 61%.Upon encapsulation into nanoparticles,enzymatic activity of both drugs was passivated to avoid potential side-effects during circulation,while the drugs could be rapidly released within 1 h in response to acidic p H to fully recover their activities.The nanoparticles could accumulate into tumor via intravenous injection,facilitate the cell membrane penetration,and release the payloads of GOx,DZ and Cu^(2+)inside cells to exert a series of anti-tumor effects.GOx caused tumor starvation by catalytic glucose consumption,and the concomitantly generated H_(2)O_(2)byproduct boosted the Cu^(2+)-mediated chemodynamic therapy(CDT).Meanwhile,the DZ silenced HIF-αexpression to sensitize both starvation therapy and CDT.As a result,a synergistic tumor growth inhibition was achieved.This work provides a simple method to prepare biomineralized nanoparticles,and offers a general approach for macromolecular drugs delivery via Cu^(2+)-based biomineralization.

关键词： Metal ions Biomineralization Drug delivery Nanomedicine Tumor therapy

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Smart drug delivery systems for precise cancer therapy

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Acta Pharmaceutica Sinica B 2022年第11期12卷 4098-4121页

作者： Xiaoyou Wang Chong Li Yiguang Wang Huabing Chen Xinxin Zhang Cong Luo wenhu zhou Lili Li Lesheng Teng Haijun Yu Jiancheng Wang College of Pharmaceutical Sciences Southwest UniversityChongqing 400715China Beijing Key Laboratory of Molecular Pharmaceutics and New Drug Delivery Systems State Key Laboratory of Natural and Biomimetic DrugsSchool of Pharmaceutical SciencesPeking UniversityBeijing 100191China School of Radiation Medicine and Protection Soochow UniversitySuzhou 215123China Shanghai Institute of Materia Medica Chinese Academy of SciencesShanghai 201203China Department of Pharmaceutics Wuya College of InnovationShenyang Pharmaceutical UniversityShenyang 110016China Xiangya School of Pharmaceutical Sciences Central South UniversityChangsha 410013China CAS Center for Excellence in Nanoscience CAS Key Laboratory for Biomedical Effects of Nanomaterials and NanosafetyNational Center for Nanoscience and TechnologyBeijing 100190China School of Life Sciences Jilin UniversityChangchun 130012China

Nano-drug delivery strategies have been highlighted in cancer treatment, and much effort has been made in the optimization of bioavailability, biocompatibility, pharmacokinetics profiles, and in vivo distributions of anticancer nano-drug delivery systems. However, problems still exist in the delicate balance between improved anticancer efficacy and reduced toxicity to normal tissues, and opportunities arise along with the development of smart stimuli-responsive delivery strategies. By on-demand responsiveness towards exogenous or endogenous stimulus, these smart delivery systems hold promise for advanced tumor-specificity as well as controllable release behavior in a spatial-temporal manner. Meanwhile, the blossom of nanotechnology, material sciences, and biomedical sciences has shed light on the diverse modern drug delivery systems with smart characteristics, versatile functions, and modification possibilities. This review summarizes the current progress in various strategies for smart drug delivery systems against malignancies and introduces the representative endogenous and exogenous stimuli-responsive smart delivery systems. It may provide references for researchers in the fields of drug delivery, biomaterials, and nanotechnology.

关键词： Pharmaceutics Smart drugdelivery system Stimuli-responsive Receptor-ligand-based delivery Nano-drug delivery systems Precise therapy Toxicity Cancer

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Salmonella-mediated blood-brain barrier penetration,tumor homing and tumor microenvironment regulation for enhanced chemo/bacterial glioma therapy

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Acta Pharmaceutica Sinica B 2023年第2期13卷 819-833页

作者： Ze Mi Qing Yao Yan Qi Jinhai Zheng Jiahao Liu Zhenguo Liu Hongpei Tan Xiaoqian Ma wenhu zhou Pengfei Rong Department of Radiology The Third Xiangya HospitalCentral South UniversityChangsha 410013China Xiangya School of Pharmaceutical Sciences Central South UniversityChangsha 410013China Department of Pathology Shihezi University School of Medicine and the First Affiliated Hospital to Shihezi University School of MedicineShihezi 832003China Key Laboratory of Biological Nanotechnology of National Health Commission Changsha 410082China School of Biomedical Sciences Hunan UniversityChangsha 410082China Department of Pathology Cangzhou Central Hospital&the Affiliated to Hebei Medical UniversityCangzhou 062650China

Chemotherapy is an important adjuvant treatment of glioma,while the efficacy is far from satisfactory,due not only to the biological barriers of blood-brain barrier(BBB)and blood-tumor barrier(BTB)but also to the intrinsic resistance of glioma cells via multiple survival mechanisms such as upregulation of P-glycoprotein(P-gp).To address these limitations,we report a bacteria-based drug delivery strategy for BBB/BTB transportation,glioma targeting,and chemo-sensitization.Bacteria selectively colonized into hypoxic tumor region and modulated tumor microenvironment,including macrophages repolarization and neutrophils infiltration.Specifically,tumor migration of neutrophils was employed as hitchhiking delivery of doxorubicin(DOX)-loaded bacterial outer membrane vesicles(OMVs/DOX).By virtue of the surface pathogen-associated molecular patterns derived from native bacteria,OMVs/DOX could be selectively recognized by neutrophils,thus facilitating glioma targeted delivery of drug with significantly enhanced tumor accumulation by 18-fold as compared to the classical passive targeting effect.Moreover,the P-gp expression on tumor cells was silenced by bacteria typeⅢsecretion effector to sensitize the efficacy of DOX,resulting in complete tumor eradication with 100%survival of all treated mice.In addition,the colonized bacteria were finally cleared by anti-bacterial activity of DOX to minimize the potential infection risk,and cardiotoxicity of DOX was also avoided,achieving excellent compatibility.This work provides an efficient trans-BBB/BTB drug delivery strategy via cell hitchhiking for enhanced glioma therapy.

关键词： Glioma Neutrophil hitchhiking Blood-brain barrier Chemo-sensitization Outer membrane vesicles Doxorubicin P-glycoprotein Salmonella

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