Probiotic Bacteria: A Promising Tool in Cancer Prevention and Therapy

Agata Górska, Dawid Przystupski, Magdalena J Niemczura, Julita Kulbacka, Agata Górska, Dawid Przystupski, Magdalena J Niemczura, Julita Kulbacka

Abstract

Gut microbiota is widely considered to be one of the most important components to maintain balanced homeostasis. Looking forward, probiotic bacteria have been shown to play a significant role in immunomodulation and display antitumour properties. Bacterial strains could be responsible for detection and degradation of potential carcinogens and production of short-chain fatty acids, which affect cell death and proliferation and are known as signaling molecules in the immune system. Lactic acid bacteria present in the gut has been shown to have a role in regression of carcinogenesis due to their influence on immunomodulation, which can stand as a proof of interaction between bacterial metabolites and immune and epithelial cells. Probiotic bacteria have the ability to both increase and decrease the production of anti-inflammatory cytokines which play an important role in prevention of carcinogenesis. They are also capable of activating phagocytes in order to eliminate early-stage cancer cells. Application of heat-killed probiotic bacteria coupled with radiation had a positive influence on enhancing immunological recognition of cancer cells. In the absence of active microbiota, murine immunity to carcinogens has been decreased. There are numerous cohort studies showing the correlation between ingestion of dairy products and the risk of colon and colorectal cancer. An idea of using probiotic bacteria as vectors to administer drugs has emerged lately as several papers presenting successful results have been revealed. Within the next few years, probiotic bacteria as well as gut microbiota are likely to become an important component in cancer prevention and treatment.

Conflict of interest statement

The authors declare that they have no conflict of interest.

Figures

Fig. 1
Fig. 1
Summary of the possible applications of probiotic bacteria in the treatment and prevention of cancer. Figure summaries most significant findings from studies in vitro and in vivo mentioned in text [–114]. This figure was prepared using Servier Medical Art, available from www.servier.com/Powerpoint-image-bank. Legend: downwards arrow decrease, upwards arrow increase ACF aberrant crypt foci, MPL multiple plaque lesions

References

    1. Goldin BR, Gorbach SL. Effect of Lactobacillus acidophilus dietary supplements on 1,2-dimethylhydrazine dihydrochloride-induced intestinal cancer in rats. J Natl Cancer Inst. 1980;64:263–265.
    1. Kim Y, Lee D, Kim D, et al. Inhibition of proliferation in colon cancer cell lines and harmful enzyme activity of colon bacteria by Bifidobacterium adolescentis SPM0212. Arch Pharm Res. 2008;31:468–473.
    1. Thirabunyanon M, Boonprasom P, Niamsup P. Probiotic potential of lactic acid bacteria isolated from fermented dairy milks on antiproliferation of colon cancer cells. Biotechnol Lett. 2009;31:571–576.
    1. Altonsy MO, Andrews SC, Tuohy KM. Differential induction of apoptosis in human colonic carcinoma cells (Caco-2) by Atopobium, and commensal, probiotic and enteropathogenic bacteria: mediation by the mitochondrial pathway. Int J Food Microbiol. 2010;137:190–203.
    1. Ma EL, Choi YJ, Choi J, et al. The anticancer effect of probiotic Bacillus polyfermenticus on human colon cancer cells is mediated through ErbB2 and ErbB3 inhibition. Int J Cancer. 2010;127:780–790.
    1. Orlando A, Refolo MG, Messa C, et al. Antiproliferative and proapoptotic effects of viable or heat-killed Lactobacillus paracasei IMPC2.1 and Lactobacillus rhamnosus GG in HGC-27 gastric and DLD-1 colon cell lines. Nutr Cancer. 2012;64:1103–1111.
    1. Thirabunyanon M, Hongwittayakorn P. Potential probiotic lactic acid bacteria of human origin induce antiproliferation of colon cancer cells via synergic actions in adhesion to cancer cells and short-chain fatty acid bioproduction. Appl Biochem Biotechnol. 2013;169:511–525.
    1. Sadeghi-Aliabadi H, Mohammadi F, Fazeli H, Mirlohi M. Effects of Lactobacillus plantarum A7 with probiotic potential on colon cancer and normal cells proliferation in comparison with a commercial strain. Iran J Basic Med Sci. 2014;17:815–819.
    1. Chen Z-F, Ai L-Y, Wang J-L, et al. Probiotics Clostridium butyricum and Bacillus subtilis ameliorate intestinal tumorigenesis. Future Microbiol. 2015;10:1433–1445.
    1. Lee NK, Son SH, Jeon EB, et al. The prophylactic effect of probiotic Bacillus polyfermenticus KU3 against cancer cells. J Funct Foods. 2015;14:513–518.
    1. Han KJ, Lee NK, Park H, Paik HD. Anticancer and anti-inflammatory activity of probiotic Lactococcus lactis nk34. J Microbiol Biotechnol. 2015;25:1697–1701.
    1. Tiptiri-Kourpeti A, Spyridopoulou K, Santarmaki V, et al. Lactobacillus casei exerts anti-proliferative effects accompanied by apoptotic cell death and up-regulation of TRAIL in colon carcinoma cells. PLoS ONE. 2016
    1. Saxami G, Karapetsas A, Lamprianidou E, et al. Two potential probiotic lactobacillus strains isolated from olive microbiota exhibit adhesion and anti-proliferative effects in cancer cell lines. J Funct Foods. 2016;24:461–471.
    1. Arvind Singh NK, Sinha PR. Inhibition of 1,2 dimethylhydrazine induced genotoxicity in rats by the administration of probiotic curd. Int J Probiotics Prebiotics. 2009;4:201–203.
    1. Kim SW, Kim HM, Yang KM, et al. Bifidobacterium lactis inhibits NF-κB in intestinal epithelial cells and prevents acute colitis and colitis-associated colon cancer in mice. Inflamm Bowel Dis. 2010;16:1514–1525.
    1. Appleyard CB, Cruz ML, Isidro AA, et al. Pretreatment with the probiotic VSL#3 delays transition from inflammation to dysplasia in a rat model of colitis-associated cancer. Am J Physiol Liver Physiol. 2011;301:G1004–G1013.
    1. Verma A, Shukla G. Synbiotic (Lactobacillus rhamnosus + Lactobacillus acidophilus + inulin) attenuates oxidative stress and colonic damage in 1,2 dimethylhydrazine dihydrochloride-induced colon carcinogenesis in Sprague’ Dawley rats: a long-term study. Eur J Cancer Prev. 2014;23:550–559.
    1. Lee HA, Kim H, Lee K-W, Park K-Y. Dead nano-sized Lactobacillus plantarum inhibits azoxymethane/dextran sulfate sodium-induced colon cancer in Balb/c mice. J Med Food. 2015;18:1400–1405.
    1. Hu J, Wang C, Ye L, et al. Anti-tumour immune effect of oral administration of Lactobacillus plantarum to CT26 tumour-bearing mice. J Biosci. 2015;40:269–279.
    1. Talero E, Bolivar S, Ávila-Román J, et al. Inhibition of chronic ulcerative colitis-associated adenocarcinoma development in mice by VSL#3. Inflamm Bowel Dis. 2015;21:1027–1037.
    1. Walia S, Kamal R, Kanwar SS, Dhawan DK. Cyclooxygenase as a target in chemoprevention by probiotics during 1,2-dimethylhydrazine induced colon carcinogenesis in rats. Nutr Cancer. 2015;67:603–611.
    1. Zhang M, Fan X, Fang B, et al. Effects of Lactobacillus salivarius Ren on cancer prevention and intestinal microbiota in 1, 2-dimethylhydrazine-induced rat model. J Microbiol. 2015;53:398–405.
    1. Kuugbee ED, Shang X, Gamallat Y, et al. Structural change in microbiota by a probiotic cocktail enhances the gut barrier and reduces cancer via TLR2 signaling in a rat model of colon cancer. Dig Dis Sci. 2016;61:2908–2920.
    1. Gamallat Y, Meyiah A, Kuugbee ED, et al. Lactobacillus rhamnosus induced epithelial cell apoptosis, ameliorates inflammation and prevents colon cancer development in an animal model. Biomed Pharmacother. 2016;83:536–541.
    1. Dubey V, Ghosh AR, Bishayee K, Khuda-Bukhsh AR. Appraisal of the anti-cancer potential of probiotic Pediococcus pentosaceus GS4 against colon cancer: in vitro and in vivo approaches. J Funct Foods. 2016;23:66–79.
    1. Lenoir M, del Carmen S, Cortes-Perez NG, et al. Lactobacillus casei BL23 regulates Tregand Th17 T-cell populations and reduces DMH-associated colorectal cancer. J Gastroenterol. 2016;51:862–873.
    1. Jia W, Xie G, Jia W. Bile acid–microbiota crosstalk in gastrointestinal inflammation and carcinogenesis. Nat Rev Gastroenterol Hepatol. 2017
    1. Bernstein H, Bernstein C, Payne CM, et al. Bile acids as carcinogens in human gastrointestinal cancers. Mutat Res. 2005;589:47–65.
    1. Biasco G, Paganelli GM, Brandi G, et al. Effect of Lactobacillus acidophilus and Bifidobacterium bifidum on rectal cell kinetics and fecal pH. Ital J Gastroenterol. 1991;23:142.
    1. Lidbeck A, Allinger UG, Orrhage KM, et al. Impact of Lactobacillus acidophilus supplements on the faecal microflora and soluble faecal bile acids in colon cancer patients. Microb Ecol Health Dis. 1991;4:81–88.
    1. Goldin B, Gorbach SL. Alterations in fecal microflora enzymes related to diet, age, lactobacillus supplements, and dimethylhydrazine. Cancer. 1977;40:2421–2426.
    1. Kim DHDH, Jin YHYH. Intestinal bacterial beta-glucuronidase activity of patients with colon cancer. Arch Pharm Res. 2001;24:564–567.
    1. Goldin BR, Swenson L, Dwyer J, et al. Effect of diet and Lactobacillus acidophilus supplements on human fecal bacterial enzymes. J Natl Cancer Inst. 1980;64:255–261.
    1. Gorbach SL. The relationship between diet and rat fecal bacterial enzymes implicated in colon cancer. J Natl Cancer Inst. 1976;57:371–375.
    1. Goldin BR, Gorbach SL. Alterations of the intestinal microflora by diet, oral antibiotics, and lactobacillus: decreased production of free amines from aromatic nitro compounds, azo dyes, and glucuronides. J Natl Cancer Inst. 1984;73:689–695.
    1. Kulkarni N, Reddy BS. Inhibitory effect of Bifidobacterium iongum cultures on the azoxymethane-induced aberrant crypt foci formation and fecal bacterial -glucuronidase. Exp Biol Med. 1994;207:278–283.
    1. Rowland IR, Rumney CJ, Coutts JT, Lievense LC. Effect of Bifidobacterium longum and inulin on gut bacterial metabolism and carcinogen-induced aberrant crypt foci in rats. Carcinogenesis. 1998;19:281–285.
    1. Singh J, Rivenson A, Tomita M, et al. Bifidobacterium longum, a lactic acid-producing intestinal bacterium inhibits colon cancer and modulates the intermediate biomarkers of colon carcinogenesis. Carcinogenesis. 1997;18:833–841.
    1. Hirayama K, Rafter J. The role of probiotic bacteria in cancer prevention. Microbes Infect. 2000;2:681–686.
    1. Lidbeck A, Övervik E, Rafter J, et al. Effect of Lactobacillus acidophilus supplements on mutagen excretion in faeces and urine in humans. Microb Ecol Health Dis. 1992;5:59–67.
    1. Hayatsu H, Hayatsu T. Suppressing effect of Lactobacillus casei administration on the urinary mutagenicity arising from ingestion of fried ground beef in the human. Cancer Lett. 1993;73:173–179.
    1. Orrhage KM, Annas A, Nord CE, et al. Effects of lactic acid bacteria on the uptake and distribution of the food mutagen Trp-P-2 in mice. Scand J Gastroenterol. 2002;37:215–221.
    1. Nowak A, Kuberski S, Libudzisz Z. Probiotic lactic acid bacteria detoxify N-nitrosodimethylamine. Food Addit Contam Part A. 2014;31:1678–1687.
    1. Faridnia F, Hussin ASM, Saari N, et al. In vitro binding of mutagenic heterocyclic aromatic amines by Bifidobacterium pseudocatenulatum G4. Benef Microbes. 2010;1:149–154.
    1. Stidl R, Sontag G, Koller V, Knasmüller S. Binding of heterocyclic aromatic amines by lactic acid bacteria: results of a comprehensive screening trial. Mol Nutr Food Res. 2008;52:322–329.
    1. Orrhage K, Sillerström E, Gustafsson JÅ, et al. Binding of mutagenic heterocyclic amines by intestinal and lactic acid bacteria. Mutat Res Regul Pap. 1994;311:239–248.
    1. Nowak A, Libudzisz Z. Ability of probiotic Lactobacillus casei DN 114001 to bind or/and metabolise heterocyclic aromatic amines in vitro. Eur J Nutr. 2009;48:419–427.
    1. Peltonen KD, El-Nezami HS, Salminen SJ, Ahokas JT. Binding of aflatoxin B1 by probiotic bacteria. J Sci Food Agric. 2000;80:1942–1945.
    1. Duangjitcharoen Y, Kantachote D, Prasitpuripreecha C, et al. Selection and characterization of probiotic lactic acid bacteria with heterocyclic amine binding and nitrosamine degradation properties. J Appl Pharm Sci. 2014;4:14–23.
    1. Nowak A, Czyżowska A, Stańczyk M. Protective activity of probiotic bacteria against 2-amino-3-methyl-3H-imidazo[4,5-f]quinoline (IQ) and 2-amino-1-methyl-6-phenyl-1H-imidazo[4,5-b]pyridine (PhIP) – an in vitro study. Food Addit Contam. 2015;32:1927–1938.
    1. Nowak A, Ślizewska K, Błasiak J, Libudzisz Z. The influence of Lactobacillus casei DN 114 001 on the activity of faecal enzymes and genotoxicity of faecal water in the presence of heterocyclic aromatic amines. Anaerobe. 2014;30:129–136.
    1. Lili Z, Junyan W, Hongfei Z, et al. Detoxification of cancerogenic compounds by lactic acid bacteria strains. Crit Rev Food Sci Nutr. 2017;0:1–16.
    1. Commane D, Hughes R, Shortt C, Rowland I. The potential mechanisms involved in the anti-carcinogenic action of probiotics. Mutat Res. 2005;591:276–289.
    1. Garret WS. Cancer and the microbiota. Science. 2015;348:80–86.
    1. Requena T, Martinez-Cuesta MC, Peláez C. Diet and microbiota linked in health and disease. Food Funct. 2018
    1. LeBlanc JG, Chain F, Martín R, et al. Beneficial effects on host energy metabolism of short-chain fatty acids and vitamins produced by commensal and probiotic bacteria. Cell Fact: Microb; 2017. p. 16.
    1. Fotiadis CI, Stoidis CN, Spyropoulos BG, Zografos ED. Role of probiotics, prebiotics and synbiotics in chemoprevention for colorectal cancer. World J Gastroenterol. 2008;14:6453–6457.
    1. Dos Reis SA, da Conceição LL, Siqueira NP, et al. Review of the mechanisms of probiotic actions in the prevention of colorectal cancer. Nutr Res. 2017;37:1–19.
    1. Ohkawara S, Furuya H, Nagashima K, et al. Oral administration of Butyrivibrio fibrisolvens, a butyrate-producing bacterium, decreases the formation of aberrant crypt foci in the colon and rectum of mice. J Nutr. 2005;135:2878–2883.
    1. Le Leu RK, Hu Y, Brown IL, et al. Synbiotic intervention of Bifidobacterium lactis and resistant starch protects against colorectal cancer development in rats. Carcinogenesis. 2010;31:246–251.
    1. Ivanov II, Honda K. Intestinal commensal microbes as immune modulators. Cell Host Microbe. 2012;12:496–508.
    1. Delcenserie V, Martel D, Lamoureux M, et al. Immunomodulatory effects of probiotics in the intestinal tract. Curr Issues Mol Biol. 2008;10:37–54.
    1. Pitt JM, Vétizou M, Waldschmitt N, et al. Fine-tuning cancer immunotherapy: optimizing the gut microbiome. Cancer Res. 2016;76:4602–4607.
    1. Honda K, Littman DR. The microbiota in adaptive immune homeostasis and disease. Nature. 2016;535:75–84.
    1. Kuo CH, Kuo CH, Wang SSW, et al. Long-term use of probiotic-containing yogurts is a safe way to prevent Helicobacter pylori: based on a Mongolian Gerbil’s model. Biochem Res Int. 2013
    1. Chen X, Liu XM, Tian F, et al. Antagonistic activities of Lactobacilli against Helicobacter pylori growth and infection in human gastric epithelial cells. J Food Sci. 2012;77:9–14.
    1. Oh Y, Osato MS, Han X, et al. Folk yoghurt kills Helicobacter pylori. J Appl Microbiol. 2002;93:1083–1088.
    1. Verhoeven V, Renard N, Makar A, et al. Probiotics enhance the clearance of human papillomavirus-related cervical lesions: a prospective controlled pilot study. Eur J Cancer Prev. 2013;22:46–51.
    1. Okawa T, Niibe H, Arai T, et al. Effect of LC9018 combined with radiation therapy on carcinoma of the uterine cervix. A phase III, multicenter, randomized, controlled study. Cancer. 1993;72:1949–1954.
    1. Bassaganya-Riera J, Viladomiu M, Pedragosa M, et al. Immunoregulatory mechanisms underlying prevention of colitis-associated colorectal cancer by probiotic bacteria. PLoS ONE. 2012;7:e34676.
    1. Mi H, Dong Y, Zhang B, et al. Bifidobacterium infantis ameliorates chemotherapy-induced intestinal mucositis via regulating T cell immunity in colorectal cancer rats. Cell Physiol Biochem. 2017;42:2330–2341.
    1. Viaud S, Saccheri F, Mignot G, et al. The intestinal microbiota modulates the anticancer immune effects of cyclophosphamide. Science. 2013;342:971–976.
    1. Iida N, Dzutsev A, Stewart CA, et al. Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science. 2013;342:967–970.
    1. Poutahidis T, Kleinewietfeld M, Erdman SE. Gut microbiota and the paradox of cancer immunotherapy. Front Immunol. 2014;5:157.
    1. West NR, Powrie F. Immunotherapy not working? Check your microbiota. Cancer Cell. 2015;28:687–689.
    1. Wan MLY, El-Nezami H. Targeting gut microbiota in hepatocellular carcinoma: probiotics as a novel therapy. Hepatobiliary Surg Nutr. 2018;7:11–20.
    1. Sivan A, Corrales L, Hubert N, et al. Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy. Science. 2015;350:1084–1089.
    1. Vétizou M, Pitt JM, Daillère R, et al. Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science. 2015;350(6264):1079–1084.
    1. Järvinen R, Knekt P, Hakulinen T, Aromaa A. Prospective study on milk products, calcium and cancers of the colon and rectum. Eur J Clin Nutr. 2001;55:1000–1007.
    1. van’t Veer P, Goldbohm RA, van den Brandt PA, van’t Veer P. Fermented dairy products, calcium, and colorectal cancer in the Netherlands Cohort Study. Cancer Res. 1994;54:3186–3190.
    1. Kearney J, Giovannucci E, Rimm EB, et al. Calcium, vitamin D, and dairy foods and the occurrence of colon cancer in men. Am J Epidemiol. 1996;143:907–917.
    1. Pietinen P, Malila N, Virtanen M, et al. Diet and risk of colorectal cancer in a cohort of Finnish men. Cancer Causes Control. 1999;10:387–396.
    1. Lin J, Zhang SM, Cook NR, et al. Intakes of calcium and vitamin D and risk of colorectal cancer in women. Am J Epidemiol. 2005;161:755–764.
    1. Larsson SC, Bergkvist L, Rutegård J, et al. Calcium and dairy food intakes are inversely associated with colorectal cancer risk in the Cohort of Swedish Men. Am J Clin Nutr. 2006;83:667–673.
    1. Aune D, Lau R, Chan DSM, et al. Dairy products and colorectal cancer risk: a systematic review and meta-analysis of cohort studies. Ann Oncol. 2012;23:37–45.
    1. Yang B, McCullough ML, Gapstur SM, et al. Calcium, vitamin D, dairy products, and mortality among colorectal cancer survivors: the cancer prevention study-II nutrition cohort. J Clin Oncol. 2014;32:2335–2343.
    1. Narisawa T, Reddy BS, Weisburger JH. Effect of bile acids and dietary fat on large bowel carcinogenesis in animal models. Gastroenterol Jpn. 1978;13:206–212.
    1. Pala V, Sieri S, Berrino F, et al. Yogurt consumption and risk of colorectal cancer in the Italian European prospective investigation into cancer and nutrition cohort. Int J Cancer. 2011;129:2712–2719.
    1. Sleator RD, Hill C. Battle of the bugs. Science. 2008;321:1294–1295.
    1. Wells J. Mucosal vaccination and therapy with genetically modified lactic acid bacteria. Annu Rev Food Sci Technol. 2011;2:423–445.
    1. Amalaradjou MAR, Bhunia AK. Bioengineered probiotics, a strategic approach to control enteric infections. Bioengineered. 2013;4:379–387.
    1. Steidler L, Hans W, Schotte L, et al. Treatment of murine colitis by Lactococcus lactis secreting interleukin-10. Science. 2000;289:1352–1355.
    1. Zhuang Z, Wu Z-G, Chen M, Wang PG. Secretion of human interferon-beta 1b by recombinant Lactococcus lactis. Biotechnol Lett. 2008;30:1819–1823.
    1. Pang Q, Ji Y, Li Y, et al. Intragastric administration with recombinant Lactococcus lactis producing heme oxygenase-1 prevents lipopolysaccharide-induced endotoxemia in rats. FEMS Microbiol Lett. 2008;283:62–68.
    1. LeBlanc ADM, LeBlanc JG, Perdigón G, et al. Oral administration of a catalase-producing Lactococcus lactis can prevent a chemically induced colon cancer in mice. J Med Microbiol. 2008;57:100–105.
    1. del Carmen S, de LeBlanc ADM, Levit R, et al. Anti-cancer effect of lactic acid bacteria expressing antioxidant enzymes or IL-10 in a colorectal cancer mouse model. Int Immunopharmacol. 2017;42:122–129.
    1. Kajikawa A, Masuda K, Katoh M, Igimi S. Adjuvant effects for oral immunization provided by recombinant Lactobacillus casei secreting biologically active murine interleukin-1β. Clin Vaccine Immunol. 2010;17:43–48.
    1. Fredriksen L, Kleiveland CR, Hult LTO, et al. Surface display of N-terminally anchored invasin by Lactobacillus plantarum activates NF-κB in monocytes. Appl Environ Microbiol. 2012;78:5864–5871.
    1. Wang Z, Yu Q, Gao J, Yang Q. Mucosal and systemic immune responses induced by recombinant Lactobacillus spp. expressing the hemagglutinin of the avian influenza virus H5N1. Clin Vaccine Immunol. 2012;19:174–179.
    1. Benbouziane B, Ribelles P, Aubry C, et al. Development of a stress-inducible controlled expression (SICE) system in Lactococcus lactis for the production and delivery of therapeutic molecules at mucosal surfaces. J Biotechnol. 2013;168:120–129.
    1. Bermudez-Humaran LG, Cortes-Perez NG, Lefevre F, et al. A novel mucosal vaccine based on live lactococci expressing E7 antigen and IL-12 induces systemic and mucosal immune responses and protects mice against human papillomavirus type 16-induced tumors. J Immunol. 2005;175:7297–7302.
    1. Li Y, Li X, Liu H, et al. Intranasal immunization with recombinant lactococci carrying human papillomavirus E7 protein and mouse interleukin-12 DNA induces E7-specific antitumor effects in C57BL/6 mice. Oncol Lett. 2014;7:576–582.
    1. Cortes-Perez NG, Bermúdez-Humarán LG, Le Loir Y, et al. Mice immunization with live lactococci displaying a surface anchored HPV-16 E7 oncoprotein. FEMS Microbiol Lett. 2003;229:37–42.
    1. Rangel-Colmenero BR, Gomez-Gutierrez JG, Villatoro-Hernández J, et al. Enhancement of Ad-CRT/E7-mediated antitumor effect by preimmunization with L. lactis expressing HPV-16 E7. Viral Immunol. 2014;27:463–467.
    1. Kitagawa K, Oda T, Saito H, et al. Development of oral cancer vaccine using recombinant Bifidobacterium displaying Wilms’ tumor 1 protein. Cancer Immunol Immunother. 2017;66:787–798.
    1. Kimura NT, Taniguchi SI, Aoki K, Baba T. Selective localization and growth of Bifidobacterium bifidum in mouse tumors following intravenous administration. Cancer Res. 1980;40:2061–2068.
    1. Yazawa K, Fujimori M, Nakamura T, et al. Bifidobacterium longum as a delivery system for gene therapy of chemically induced rat mammary tumors. Breast Cancer Res Treat. 2001;69:256.
    1. Fujimori M, Amano J, Taniguchi S. The genus Bifidobacterium for cancer gene therapy. Curr Opin Drug Discov Dev. 2002;5:200–203.
    1. Sasaki T, Fujimori M, Hamaji Y, et al. Genetically engineered Bifidobacterium longum for tumor-targeting enzyme-prodrug therapy of autochthonous mammary tumors in rats. Cancer Sci. 2006;97:649–657.
    1. Fujimori M. Genetically engineered bifidobacterium as a drug delivery system for systemic therapy of metastatic breast cancer patients. Breast cancer. 2006;13:27–31.
    1. Wei C, Xun AY, Wei XX, et al. Bifidobacteria expressing tumstatin protein for antitumor therapy in tumor-bearing mice. Technol Cancer Res Treat. 2015;15:498–508.
    1. Fu G-F, Li X, Hou Y-Y, et al. Bifidobacterium longum as an oral delivery system of endostatin for gene therapy on solid liver cancer. Cancer Gene Ther. 2005;12:133–140.
    1. Wang C, Ma Y, Hu Q, et al. Bifidobacterial recombinant thymidine kinase-ganciclovir gene therapy system induces FasL and TNFR2 mediated antitumor apoptosis in solid tumors. BMC Cancer. 2016;16:545.
    1. Cano-Garrido O, Seras-Franzoso J, Garcia-Fruitós E. Lactic acid bacteria: reviewing the potential of a promising delivery live vector for biomedical purposes. Microb Cell Fact. 2015;14:1–12.
    1. Li W, Li C-B. Effect of oral Lactococcus lactis containing endostatin on 1, 2-dimethylhydrazine-induced colon tumor in rats. World J Gastroenterol. 2005;11:7242–7247.
    1. Yi C, Huang Y, Guo Z, Wang S. Antitumor effect of cytosine deaminase/5-fluorocytosine suicide gene therapy system mediated by Bifidobacterium infantis on melanoma. Acta Pharmacol Sin. 2005;26:629–634.

Source: PubMed

3
订阅