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Intestinal Microbiota in the Carcinogenesis and Treatment of Colorectal Cancers

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Intestinal Microbiota in the Carcinogenesis and Treatment of Colorectal Cancers · 76 · Journal of Nutritional Oncology, May 15, 2018, Volume 3, Number 2 Intestinal Microbiota in the Carcinogenesis and Treatment of Colorectal Cancers Shao Hua Ge, Yi Ba Tianjin Medical University Cancer Institute and Hospital, National Clinical Research Center for Cancer, Tianjin’s Clinical Research Center for Cancer, Key Laboratory of Cancer Prevention and Therapy, Tianjin Medical University, Tianjin 300060, China Abstract: The term “intestinal microbiota” mainly refers to the bacteria colonizing the gut. They are divided into different enterotypes, which have different distributions and functions. Dysbiosis of the intestinal microbiota may cause a variety of diseases, including colorectal cancers. Besides carcinogenesis, they are also related to the efficacy and side effects of antitumor therapies, as well as the prognosis of patients. There are two theoretical explanations for how microbiota is involved in carcinogenesis: the “alpha-bughypothesis” and the “driver-passenger” model. These theories explain the course of carcinogenesis related to intestinal microbiota. However, the relationship between the intestinal microbiota and colonic epithelial cells is excessively emphasized under both of these theories, and other factors related to carcinogenesis are neglected. Pathogenic microbiota may be associated with colorectal cancer through different mechanisms, and may act singly or in combination. With regard to treatment, some intestinal microbiota may exert chemopreventive effects and improve the dysbiosis besides anti-inflammatory drugs. Most importantly, the intestinal microbiota may affect the anticancer effects of chemotherapy and immunotherapy. For example, it has been shown that some probiotics can promote the antitumor effects of immune checkpoint inhibitors. Intestinal microbiota may also influence the effects of oxaliplatin and the incidence and grade of diarrhea associated with irinotecan. There are new clinical trials that have been initiated to further investigate the effects of intestinal microbiota on the efficacy and side effects of antitumor therapy. In addition, new targets for the prevention and treatment of colorectal cancers associated with intestinal microbiota are under investigation. Key Words: Intestinal microbiota; Colorectal cancer; Carcinogenesis; Antitumor treatment; Prognosis Introduction nutrient metabolism and absorption, to stimulate the The term “intestinal microbiota” refers to the immune function, etc. [3-5]. There is enormous diversity bacteria, viruses, fungi, archaea and protozoa present in in the human intestinal microbiota, and most bacterial the intestine. Most studies on gut microbiota have species and their functions are still unknown under both focused on the bacteria in the small intestine, colon and physiological and pathological conditions. rectum. It has been reported that there are more than 1014 In order to obtain a better understanding of the bacteria in the gut of an adult, and the density in the intestinal microbiota, the different categories should be large intestine (~1012 cells per ml) is much higher than defined. The human intestinal microbiota is currently that in small intestine (~102 cells per ml). The stratified into different enterotypes, but this stratification composition of the bacteria is reasonably stable is sometimes controversial [6]. The recurrent throughout adult life, although there are short-term compositional patterns in the intestinal microbiota have variations and variations among individuals [1]. These previously been examined using sequencing bacteria play an important role in maintaining the technologies (Illumina, 454 and Sanger), as well as 16S dynamic balance of the intestinal environment and rRNA gene profiling. The enterotype is described as human health through interactions with intestinal “densely populated areas in a multidimensional space of epithelial pattern recognition receptors (PRRs) [2]. The community composition”. It has been proposed that intestinal microbiota is essential to maintain the there are at least three enterotypes [7]: enterotype 1 is intestinal barrier, to ensure the correct balance between represented by Bacteroides; enterotype 2 by Prevotella, pathogenic and nonpathogenic organisms, to regulate whose abundance is inversely correlated with Bacteroides; and enterotype 3 is comprised primarily by Firmicutes, most prominently Ruminococcus. These Corresponding Authors: Yi Ba, MD, PhD, Tianjin Medical University classifications are independent of geography and the Cancer Institute and Hospital, National Clinical Research Center for cultural background, age and gender of the individual. Cancer, Tianjin’s Clinical Research Center for Cancer, Key Laboratory This suggests that different compositions of bacteria of Cancer Prevention and Therapy, Tianjin Medical University, Tianjin within these enterotypes may act differently in terms of 300060, China; Tel: +86 22 2334 0123; Email: [email protected] their functions and ecological properties [8]. Journal of Nutritional Oncology, May 15, 2018, Volume 3, Number 2 · 77 · Abnormities of intestinal microbiota may cause research on colorectal cancer. dysbiosis, which may be related to many diseases not only of the colorectum, but also other parts of the gut. In The Intestinal Microbiota Is Related to the the intestine, dysbiosis is associated with inflammatory Carcinogenesis of Colorectal Cancers bowel diseases, Crohn’s disease, ulcerative colitis and Due to the many functions of the intestinal colorectal cancers [5,9,10]. The microbiota can also have microbiota in the colorectum, dysbiosis may promote effects on other organs, including the liver, pancreas, carcinogenesis [20]. There is increasing evidence adipose tissue, cardiovascular system, lungs, and even showing that the intestinal microbiota is related to the the brain. As a result, the intestinal microbiota is carcinogenesis of colorectal cancer [21-25]. There are involved in metabolic syndrome, obesity, diabetes several hypotheses regarding the mechanisms by which mellitus, non-alcoholic fatty liver disease, and dysbiosis may lead to colorectal cancers. The most malnutrition, as well as other diseases affecting various important of these are the “alpha-bug hypothesis” and systems [11-13]. With regard to colorectal cancers, the “driver-passenger” model. The “alpha-bug hypothesis” intestinal microbiota is involved in many processes from was proposed by Sears CL et al. [26]. The hypothesis carcinogenesis to determining the prognosis. Some suggests that microbes and microbiome communities are bacteria, such as Lactobacilli and Bifidobacteria, may associated with colon carcinogenesis similar to the antagonize carcinogenesis [14-16]. On the contrary, relationship between Helicobacter pylori and gastric some can function as cancer-promoters, such as cancer, hepatitis virus B or C and liver cancer, or human Bacteroides fragilis, Spirochetes, Firmicutes, and papilloma virus (HPV) and cervical cancer. It considers Fusobacteria [17-19]. Therefore, the intestinal that the immune response to bacteria serves as the driver microbiota deserves more attention, especially in of colon epithelial cell transformation, and then the Figure 1 How colorectal carcinogenesis may be related to intestinal microbiota A. The “alpha-bughypothesis” described by Sears CL and Pardoll DM [26]. It is considered that there are interactions among the intestinal microbiota, mucosal immune system, and colonic epithelial cells. B. The “driver-passenger” model developed by Tjalsma H et al. [27]. Bacterial drivers may be pro•carcinogens and may cause a series of changes, in collaboration with bacterial passengers, to induce carcinogenesis. C. An ideal model for the carcinogenesis of colorectal cancer involving the intestinal microbiota, immune system and other factors, including dietary factors. · 78 · Journal of Nutritional Oncology, May 15, 2018, Volume 3, Number 2 cancer originates through a series of exposures to prebiotics) [34-36], pharmacological factors (including pro-inflammatory cytokines. This hypothesis simplifies antibiotics) [37,38], lifestyle [39], and environmental the relationship between the intestinal microbiota and and other carcinogens. A prospective cohort study on colorectal cancer, and mainly concerns the interactions 137,217 nurses and health professionals showed that the among the intestinal microbiota, the host immune system risk of colorectal cancer was strongly influenced by diet, and colonic epithelial cells (Figure 1A). even in patients with other similar risk factors [35]. For The “driver-passenger” model was subsequently F.nucleatum-positive cancers, a “prudent” diet score was proposed by Tjalsma H et al. in 2012 [27]. This associated with a lower risk (P = 0.003 for the trend; hypothesis refers to the patterns of “driver-passenger” multivariable hazard ratio = 0.43; 95% CI, 0.25 - 0.72, gene mutations and combined this with the “alpha­bug” for the highest vs. the lowest score quartile). This hypothesis. The driver mutations in tumor suppressor explains why the risk of colorectal cancer differs even in genes or oncogenes can result in carcinogenesis, while individuals with similar intestinal microbiota. That is to the other numerous mutations in passenger genes may say, the diet affects the cancer risk, and may exert an not change the tumorigenesis process [28]. In this model, equally or more important influence on cancer the bacterial drivers are defined as pro•carcinogens that development as the factors in the “alpha-bug hypothesis”.
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