Accepted Manuscript. Innate immune cells regulate oncoimmunity and cancer development. Ai-Ping Bai, Yuan Guo

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1 Accepted Manuscript Innate immune cells regulate oncoimmunity and cancer development Ai-Ping Bai, Yuan Guo PII: S (18) DOI: /j.gastro Reference: YGAST To appear in: Gastroenterology Accepted Date: 17 August 2018 Please cite this article as: Bai A-P, Guo Y, Innate immune cells regulate oncoimmunity and cancer development, Gastroenterology (2018), doi: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

2 Innate immune cells regulate oncoimmunity and cancer development Dear Editors, We read with high interest the recently published article titled Gut microbiota promotes tumor growth in mice by modulating immune response. Sethi and colleagues 1 reported that gut microbiome depletion by combination of multiple antibiotics suppressed tumor growth and metastasis in wild-type mice, but not in RAG1 -/- mice, the T cell and B cell deficient strain. They further observed significant increase of interferon (IFN)γ producing T cells with decrease of interleukin (IL)-17 producing T cells in wild-type mice post gut microbiome depletion. They then concluded that gut microbiome promoted tumor development through modulation of adaptive immune responses, i.e., IFNγ and IL-17 related responses. 1 Given the significant induction of T helper cell type 1 (Th1)/IFNγ + immune cells as seen in wild-type mice treated by antibiotics, neutralization of IFNγ responses using the blocking antibodies would be much helpful to explore the pivotal roles of Th1/IFNγ in tumor development, at least in the tumor cell grafted models as depicted in the article. We have two concerns. First, existence of commensal microbiota is associated with innate immune cell functions in local tissues of gut, particularly plasmacytoid dendritic cells (pdc) and other phagocytes. 2 Responses of pdc and other potential innate immune cells may become altered after antibiotics treatment. Considering the important roles of pdc in regulation of immune responses, e.g., IFN responses as well as T cell differentiation inclusive of Th1 and

3 regulatory T cells (Treg), 3 studies on innate immune responses including pdc in gut and tumor tissues after gut microbiome depletion are requisite. At this end, to minimize the impacts of innate immune system on tumor development using the tumor cell grafted models, application of the innate immune deficient mice, such as NSG mice, should be the optimal option. Indeed, innate immune system has been considered to contribute to tumor development. 4 Colon cancer can be induced during the progression of chronic colitis, and antibiotics can reduce the incidence of colitis associated cancer, through inhibition of recruitment of neutrophils and other phagocytes. 5 In addition, exposure of RAG -/- mice to some bacterial strains in gut induces colitis and later on cancer, 6 providing the direct evidence of innate immune responses in mediating bacteria triggered inflammation and tumor progression. Second, as Sethi et al 1 reported, bacterial translocation to peripheral tissues inclusive of tumor, i.e., metastatic liver, was common in wild-type mice, and treatment with antibiotics significantly decreased bacterial translocation and load in metastatic liver. In RAG1 -/- mice, a strain lack of mucosal IgA and insufficient intestinal barrier, 7 more bacterial translocation to local tissues including lympho nodes and liver, or/and systemic blood, is postulated, which results in activation of local and systemic innate immune cells. Upon activation by translocated bacterial components such as lipopolysaccharide (LPS), those innate immune cells release amount of cytokines including tumor necrosis factor (TNF). Thus, elevated TNF levels in systemic blood or/and local tumor tissues are proposed. Conversely, treatment with antibiotics may limit bacterial translocation, and thereby dampen innate immune cell activation as well as cytokine productions

4 inclusive of TNF. The putative roles of TNF in cancer development have been noted. 8 TNF is a typical cytokine mainly released by innate immune cells, and intriguingly, TNF levels in tumor tissues are upregulated. Meanwhile, long term exposure to TNF at low doses facilitates tumor cell growth, migration, and metastasis. Moreover, severity of inflammation derived cancer is associated with sustained TNF productions and infiltration of innate immune cells such as macrophages and neutrophils. 8 In contrast, inhibition of TNF signals using either TNF receptor deficient mice or TNF specific antagonist abrogates the progression of inflammation associated colon carcinogenesis. 8 Current evidence indicates that, innate immune system inclusive of macrophages and neutrophils, which can be activated by TNF cytokines or translocation of bacteria, is associated with and also contribute to the progression of tumors. Collectively, Sethi et al provided the novel findings that adaptive immune responses in association with gut microbiome contribute to tumor growth, whereas the putative roles of innate immune system need to be considered. AI-PING BAI YUAN GUO Department of Gastroenterology The First Affiliated Hospital of Nanchang University, Nanchang, China

5 Conflicts of interest All other authors have no conflicts of interest to disclose. Funding This research was funded by the National Natural Science Foundation of China (No and ), and the Principle Investigator Program of Jiangxi Province (No BCB22010).

6 References 1. Sethi V, et al. Gastroenterology.2018; 155: Geva-Zatorsky N, et al. Cell. 2017; 168: Swiecki M, et al. Nat Rev Immunol. 2015; 15: Hagerling C, et al. Trends Cell Biol. 2015; 25: Tanaka Y, et al. Sci Rep. 2016; 6: Boulard O, et al. J Exp Med. 2012; 209: Bergstrom KS, et al. Infect Immun. 2008; 76: Popivanova BK, et al. J Clin Invest. 2008; 118:

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