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The Microbiome-Immunity-Cancer Axis in Cancers
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The Microbiome-Immunity-Cancer Axis in Cancers

A special issue of Cancers (ISSN 2072-6694). This special issue belongs to the section "Infectious Agents and Cancer".

Deadline for manuscript submissions: closed (31 May 2023) | Viewed by 18119

Special Issue Editors

Dr. Anquan Shang

E-Mail Website
Guest Editor
Tongji Hospital, School of Medicine, Tongji University, Shanghai 200065, China
Interests: tumor micro-ecology; tumor microenvironment; tumor immunity; cancer and anticancer drug resistance; liquid biopsy; biomarkers; bioinformatics
Special Issues, Collections and Topics in MDPI journals
Dr. William Cho

grade E-Mail Website
Guest Editor
Department of Clinical Oncology, Queen Elizabeth Hospital, 30 Gascoigne Road, Hong Kong, China
Interests: cancer biomarker; evidence-based medicine; extracellular vesicles; genomics; microRNA; molecular diagnostics; non-coding RNAs; nasopharyngeal carcinoma; next-generation sequencing; non-small cell lung cancer; proteomics; drug repurposing and bioinformatics
Special Issues, Collections and Topics in MDPI journals
Dr. Zongxin Ling

E-Mail Website
Guest Editor
Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, National Clinical Research Center for Infectious Diseases, The First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou 310003, China
Interests: infection micro-ecology; infectious diseases; tumor-associated bacteria; gut microbiota; oncogene; oncogenesis

Special Issue Information

Dear Colleagues,

Tumors and their surroundings are closely related and constantly interact. The tumor microenvironment (TME), a complex biological ecosystem for cancer cells to survive and develop, refers to the surrounding circumstances of cancer cells, including surrounding blood vessels, immune cells, fibroblasts, bone marrow inflammatory cells, various signaling molecules, extracellular matrix (ECM), and the balance of the microbiome.

The immune cells and their regulation mode in TME have tumor-antagonizing or tumor-promoting functions. The TME has been gradually recognized as a key contributor to cancer progression and drug resistance, with cellular components in the TME able to enhance tumor resistance by recruiting and secreting multiple protective cytokines. The acellular components of the TME can mediate drug resistance by building physical barriers, affecting tumor cell growth and metabolism, etc.

Trillions of microbes inhabit human body surfaces and cavities and interact with the host constantly. Recently, it came to light that the microbiota is a critical regulator of pro-tumorigenic inflammation that has long been suspected to play a significant role in cancer development. On one hand, pathogenic bacteria can contribute to cancer progression via inducing a variety of tumor-promoting inflammatory responses and initiating a pro-tumorigenic microenvironment. On the other hand, beneficial commensals prevent inflammation and stimulate the host anti-cancer immunity. Thus, a delicate balance between the microbiomes and the immune system plays a critical role in the development or prevention of cancer. Despite our understanding of the molecular mechanisms underlying the pathogenesis of these microbes, key questions remain regarding the impact of oncomicrobe-induced alterations on microbiota–immune interactions and how these interactions impact tumorigenesis, anti-tumor immunosurveillance, and responses to immunotherapy. Additionally, much remains to be learned about the consequences of immunotherapy on microbial communities and microbe–immune cell interactions.

Therefore, the scope of this topic is to contribute to the understanding of the mechanisms that govern how oncomicrobes influence the microbiota and shape the immune system to affect anti-tumor immunity, cancer immunosurveillance, and response to immunotherapies. Advances in all those fields greatly enable the discovery of novel biomarkers for diagnosis and prognosis, as well as expedite the design of novel microbiome-manipulating strategies to prevent, abort, and treat cancers.

We currently face new challenges for the evaluation of effective treatment strategies to accelerate the clinical translation of combination treatments that can improve patient outcomes. In this research topic, we encourage the submission of original research, reviews and perspective articles on the interactions between microbiome, cancer, and the immune system, the underlying mechanistic bases, as well as method articles that innovate the way of study in this field. We aim to provide a comprehensive overview of the current knowledge of new microbe-based immuno-therapies for cancer. Articles focusing on, but not limited to, the following subtopics are welcome:

  • Cell types and functions in the TME of cancer.
  • The metabolism of immune cells in cancers.
  • The single-cell analysis of cancers.
  • Regulated cell death in cancers.
  • Cell aging and carcinogenesis.
  • Inflammation, hypoxia, and pH in cancers.
  • Treatment options for cancers.
  • TME and resistance to therapy in cancers.
  • TME in immune escape in cancers.
  • The microbiota in cancer.
  • The molecular basis of interactions between microbes, cancer, and the immune system.
  • Novel molecules and signaling pathways involved in microbiome-mediated pro-inflammatory or anti-cancer immune responses.
  • The identification of individual microbial species that influence cancer and immune responses.
  • The impact of the microbiome on inflammation and the tumor microenvironment.
  • Impact of the microbiome on cancer immune surveillance and cancer immunity.
  • Impact of the microbiome on the efficacy of cancer therapies.
  • Interactions between the microbiome, immune system, and other systems to affect cancer.
  • Innovative strategies and novel therapies to influence the microbiome to enhance the therapeutic response to cancer.
  • Development of new biomarkers for cancer diagnosis and prognosis.
  • New technologies, methods, and strategies to stimulate studies in this field.

Dr. Anquan Shang
Dr. William Cho
Dr. Zongxin Ling
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Cancers is an international peer-reviewed open access semimonthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2900 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • tumor microenvironment (TME)
  • tumor immunity
  • tumor therapy
  • bioinformatics
  • predict and prognosis model
  • microbiome
  • tumor-associated bacteria
  • cellular metabolism
  • tumor biomarkers

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Published Papers (6 papers)

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Research

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16 pages, 4215 KiB  
Article
Tumor Colonization and Therapy by Escherichia coli Nissle 1917 Strain in Syngeneic Tumor-Bearing Mice Is Strongly Affected by the Gut Microbiome
by Ivaylo Gentschev, Ivan Petrov, Mingyu Ye, Lina Kafuri Cifuentes, Romy Toews, Alexander Cecil, Tobias A. Oelschaeger and Aladar A. Szalay
Cancers 2022, 14(24), 6033; https://doi.org/10.3390/cancers14246033 - 7 Dec 2022
Cited by 6 | Viewed by 3387
Abstract
In the past, different bacterial species have been tested for cancer therapy in preclinical and clinical studies. The success of bacterial cancer therapy is mainly dependent on the ability of the utilized bacteria to overcome the host immune defense system to colonize the [...] Read more.
In the past, different bacterial species have been tested for cancer therapy in preclinical and clinical studies. The success of bacterial cancer therapy is mainly dependent on the ability of the utilized bacteria to overcome the host immune defense system to colonize the tumors and to initiate tumor-specific immunity. In recent years, several groups have demonstrated that the gut microbiome plays an important role of modulation of the host immune response and has an impact on therapeutic responses in murine models and in cohorts of human cancer patients. Here we analyzed the impact of the gut microbiome on tumor colonization and tumor therapy by the Escherichia coli Nissle 1917 (EcN) strain. This EcN strain is a promising cancer therapy candidate with probiotic properties. In our study, we observed significantly better tumor colonization by EcN after antibiotic-induced temporal depletion of the gut microbiome and after two intranasal applications of the EcN derivate (EcN/pMUT-gfp Knr) in 4T1 tumor-bearing syngeneic BALB/c mice. In addition, we demonstrated significant reduction in tumor growth and extended survival of the EcN-treated mice in contrast to phosphate-buffered saline (PBS)-treated tumor-bearing control animals. Multispectral imaging of immune cells revealed that depletion of the gut microbiome led to significantly lower infiltration of cytotoxic and helper T cells (CD4 and CD8 cells) in PBS tumors of mice pretreated with antibiotics in comparison with antibiotic untreated PBS—or EcN treated mice. These findings may help in the future advancement of cancer treatment strategies using E. coli Nissle 1917. Full article
(This article belongs to the Special Issue The Microbiome-Immunity-Cancer Axis in Cancers)
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11 pages, 1441 KiB  
Article
Postoperative Chemoradiotherapy versus Radiotherapy Alone in Major Salivary Gland Cancers: A Stratified Study Based on the External Validation of the Distant Metastasis Risk Score Model
by Wenbin Yan, Lili Huang, Jianyun Jiang, Chunying Shen, Xiaomin Ou and Chaosu Hu
Cancers 2022, 14(22), 5583; https://doi.org/10.3390/cancers14225583 - 14 Nov 2022
Viewed by 1388
Abstract
Background: The role of additional chemoradiotherapy (CRT) for distant metastasis (DM) on the resected malignancy of the major salivary gland (SGM) remained unknown. We conducted this study to externally validate a recently reported DM risk score model and compare the survival outcome between [...] Read more.
Background: The role of additional chemoradiotherapy (CRT) for distant metastasis (DM) on the resected malignancy of the major salivary gland (SGM) remained unknown. We conducted this study to externally validate a recently reported DM risk score model and compare the survival outcome between adjuvant CRT and RT alone. Materials: We retrospectively reviewed the patients with SGM following postoperative radiotherapy (PORT). The cumulative incidence of DM was assessed using a competing risk method. Multivariate analysis was performed with Cox proportional-hazards regression to identify significant predictors for DM. Patients were classified as high- and low-risk subgroups with the cutoff value of the DM risk score model. The inverse probability of treatment weighting (IPTW) was conducted to minimize the bias of the groups. Results: A total of 586 eligible patients were analyzed and 67 cases underwent adjuvant CRT. The 5-year incidence of DM was 19.5% (95% CI 16.0–23.0%). The model reasonably discriminated the DM risk between the high- and low-risk subgroup in our cohort, and the c-index was 0.75. No survival benefit was observed for the CRT group compared with RT alone in the entire cohort after IPTW (p = 0.095). After subgroup analysis, increased mortality was identified with the administration of CRT in the low-risk subset (p = 0.002) while no significant difference in OS was illustrated in the high-risk subgroup (p = 0.98). Conclusions: This external validation provides further exploration of the DM risk score model in major SGM. Our results demonstrated no support for the utility of additional chemotherapy to PORT in the major SGM, especially in the low-risk subgroup of patients with DM. Full article
(This article belongs to the Special Issue The Microbiome-Immunity-Cancer Axis in Cancers)
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16 pages, 2645 KiB  
Article
Endogenous Propionibacterium acnes Promotes Ovarian Cancer Progression via Regulating Hedgehog Signalling Pathway
by Qifa Huang, Xin Wei, Wenyu Li, Yanbing Ma, Guanxiang Chen, Lu Zhao, Ying Jiang, Siqi Xie, Qi Chen and Tingtao Chen
Cancers 2022, 14(21), 5178; https://doi.org/10.3390/cancers14215178 - 22 Oct 2022
Cited by 16 | Viewed by 2259 | Correction
Abstract
Background: The oncogenesis and progression of epithelial ovarian cancer (EOC) is a complicated process involving several key molecules and factors, yet whether microbiota are present in EOC, and their role in the development of EOC, remains greatly unknown. Methods: In this study, 30 [...] Read more.
Background: The oncogenesis and progression of epithelial ovarian cancer (EOC) is a complicated process involving several key molecules and factors, yet whether microbiota are present in EOC, and their role in the development of EOC, remains greatly unknown. Methods: In this study, 30 patients were enrolled to compare the similarities and differences of intratumour microbiota among patients with epithelial benign ovarian tumours (EBOTs) and patients with EOC based on the high-throughput sequencing method. Subsequently, we further isolated the specific EOC-related bacteria and defined Propionibacterium acnes as a key strain in facilitating EOC progression. More importantly, we constructed a mouse EOC model to evaluate the effect of the P. acnes strain on EOC using immunohistochemistry, Western blotting, and RT-qPCR. Results: The high-throughput sequencing showed that the intratumour microbiota in EOC tissues had a higher microbial diversity and richness compared to EBOT tissues. The abundance of previously considered pathogens, Actinomycetales, Acinetobacter, Streptococcus, Ochrobacterium, and Pseudomonadaceae Pseudomonas, was increased in the EOC tissues. Meanwhile, we discovered the facilitating role of the P. acnes strain in the progression of EOC, which may be partially associated with the increased inflammatory response to activate the hedgehog (Hh) signalling pathway. This microbial-induced EOC progression mechanism is further confirmed using the inhibitor GANT61. Conclusions: This study profiled the intratumour microbiota of EBOT and EOC tissues and demonstrated that the diversity and composition of the intratumour microbiota were significantly different. Furthermore, through in vivo and in vitro experiments, we confirmed the molecular mechanism of intratumour microbiota promotion of EOC progression in mice, which induces inflammation to activate the Hh signalling pathway. This could provide us clues for improving EOC treatment. Full article
(This article belongs to the Special Issue The Microbiome-Immunity-Cancer Axis in Cancers)
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16 pages, 4740 KiB  
Article
Pancreatic Cancer Cell-Derived Exosomes Promote Lymphangiogenesis by Downregulating ABHD11-AS1 Expression
by Xulin Zhou, Fengyun Zhong, Yongmin Yan, Sihui Wu, Huizhi Wang, Junqiang Liu, Feifan Li, Dawei Cui and Min Xu
Cancers 2022, 14(19), 4612; https://doi.org/10.3390/cancers14194612 - 23 Sep 2022
Cited by 11 | Viewed by 2111
Abstract
Research on pancreatic cancer microbiomes has attracted attention in recent years. The current view is that enriched microbial communities in pancreatic cancer tissues may affect pancreatic cancer metastasis, including lymph node (LN) metastasis. Similar to carriers of genetic information between cells, such as [...] Read more.
Research on pancreatic cancer microbiomes has attracted attention in recent years. The current view is that enriched microbial communities in pancreatic cancer tissues may affect pancreatic cancer metastasis, including lymph node (LN) metastasis. Similar to carriers of genetic information between cells, such as DNA, mRNA, protein, and non-coding RNA, exosomes are of great importance in early LN metastasis in tumors, including pancreatic cancer. Our previous study showed that the long non-coding RNA ABHD11-AS1 was highly expressed in tissues of patients with pancreatic cancer, and was correlated with patient survival time. However, the role of ABHD11-AS1 in pancreatic cancer LN metastasis has rarely been studied. Hence, in this paper we confirmed that exosomes derived from pancreatic cancer cells could promote lymphangiogenesis in vitro and in vivo, and that the mechanism was related to the downregulation of ABHD11-AS1 expression in lymphatic endothelial cells, and to the enhancement of their ability to proliferate, migrate, and form tubes. These findings preliminarily show a new mechanism by which pancreatic cancer cells regulate peripheral lymphangiogenesis, providing a new therapeutic strategy for inhibiting LN metastasis in pancreatic cancer. Full article
(This article belongs to the Special Issue The Microbiome-Immunity-Cancer Axis in Cancers)
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Review

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26 pages, 649 KiB  
Review
The Role of the Gut Microbiome in Cancer Immunotherapy: Current Knowledge and Future Directions
by Despoina E. Kiousi, Antonia Z. Kouroutzidou, Konstantinos Neanidis, Emmanuel Karavanis, Dimitrios Matthaios, Aglaia Pappa and Alex Galanis
Cancers 2023, 15(7), 2101; https://doi.org/10.3390/cancers15072101 - 31 Mar 2023
Cited by 9 | Viewed by 4573
Abstract
Cancer immunotherapy is a treatment modality that aims to stimulate the anti-tumor immunity of the host to elicit favorable clinical outcomes. Immune checkpoint inhibitors (ICIs) gained traction due to the lasting effects and better tolerance in patients carrying solid tumors in comparison to [...] Read more.
Cancer immunotherapy is a treatment modality that aims to stimulate the anti-tumor immunity of the host to elicit favorable clinical outcomes. Immune checkpoint inhibitors (ICIs) gained traction due to the lasting effects and better tolerance in patients carrying solid tumors in comparison to conventional treatment. However, a significant portion of patients may present primary or acquired resistance (non-responders), and thus, they may have limited therapeutic outcomes. Resistance to ICIs can be derived from host-related, tumor-intrinsic, or environmental factors. Recent studies suggest a correlation of gut microbiota with resistance and response to immunotherapy as well as with the incidence of adverse events. Currently, preclinical and clinical studies aim to elucidate the unique microbial signatures related to ICI response and anti-tumor immunity, employing metagenomics and/or multi-omics. Decoding this complex relationship can provide the basis for manipulating the malleable structure of the gut microbiota to enhance therapeutic success. Here, we delve into the factors affecting resistance to ICIs, focusing on the intricate gut microbiome–immunity interplay. Additionally, we review clinical studies and discuss future trends and directions in this promising field. Full article
(This article belongs to the Special Issue The Microbiome-Immunity-Cancer Axis in Cancers)
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18 pages, 2095 KiB  
Review
The Function and Molecular Mechanism of Commensal Microbiome in Promoting Malignant Progression of Lung Cancer
by Haiyang Wang, Jiayi Hu, Junlu Wu, Ping Ji, Anquan Shang and Dong Li
Cancers 2022, 14(21), 5394; https://doi.org/10.3390/cancers14215394 - 2 Nov 2022
Cited by 3 | Viewed by 2417
Abstract
The human commensal microbiome existing in an internal environment is relatively consistent with that of the host. The presence of bacterial dysbiosis, on the other hand, promptly results in the termination of this symbiotic association. The altered microbial structure in the lung may [...] Read more.
The human commensal microbiome existing in an internal environment is relatively consistent with that of the host. The presence of bacterial dysbiosis, on the other hand, promptly results in the termination of this symbiotic association. The altered microbial structure in the lung may be responsible for the development of lung cancer by controlling the host’s inflammatory response and influencing a variety of immunological pathways. More and more studies have pointed to the fact that the commensal microbiota plays a vital role in both the development of tumors and the body’s response to lung cancer treatment. Microbiome dysbiosis, genotoxicity, virulence effect, and epigenetic dysregulations are some of the potential mechanisms that may lie behind the process of tumorigenesis that is mediated by microbiome. Other potential mechanisms include regulating host immune activity through a variety of pathogenic factors, dysregulating host metabolism as a result of microbiome alterations, and microbiome dysbiosis. In this historical overview, we go through some of the more recent mechanistic discoveries into the biological processes that are involved in lung cancer that are caused by bacteria. Without a question, obtaining a greater knowledge of the dynamic link between the lung microbiome and lung cancer has the potential to inspire the development of innovative early detection and customized treatment methods for lung cancer. Full article
(This article belongs to the Special Issue The Microbiome-Immunity-Cancer Axis in Cancers)
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