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Published in: Journal of Gastrointestinal Cancer 3/2020

01-09-2020 | Probiotics | Review Article

Importance of the Microbiota Inhibitory Mechanism on the Warburg Effect in Colorectal Cancer Cells

Authors: Majid Eslami, Sina Sadrifar, Mohsen Karbalaei, Masoud Keikha, Nazarii M. Kobyliak, Bahman Yousefi

Published in: Journal of Gastrointestinal Cancer | Issue 3/2020

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Abstract

Methods and Results

Colorectal cancer (CRC) is the third most common cancer in the world. Genetic backgrounds, lifestyle, and diet play an important role in CRC risk. The human gut microbiota has an influence on many features of human physiology such as metabolism, nutrient absorption, and immune function. Imbalance of the microbiota has been implicated in many disorders including CRC. It seems Warburg effect hypothesis corresponds to the early beginning of carcinogenesis because of eventual failure in the synthesis of a pyruvate dehydrogenase complex in cooperation with a supply of glucose in carbohydrates rich diets.
From investigation among previous publications, we attempted to make it clear importance of Warburg effect in tumors; it also discusses the mechanisms of probiotics in inhibiting tumor progression and reverse Warburg effect of probiotics in modulating the microbiota and CRC therapies. These effects were observed in some clinical trials, the application of probiotics as a therapeutic agent against CRC still requirements further investigation.

Conclusion

Fiber is fermented by colonic bacteria into SCFAs such as butyrate/acetate, which may play a vital role in normal homeostasis by promoting turnover of the colonic epithelium. Butyrate enters the nucleus and functions as a histone deacetylase inhibitor (HDACi). Because cancerous colonocytes undertake the Warburg effect pathway, their favored energy source is glucose instead of butyrate. Therefore, accumulation of moderate concentrations of butyrate in cancerous colonocytes and role as HDACi. Probiotics have been shown to play a protective role against cancer development by modulating intestinal microbiota and immune response.
Literature
1.
2.
go back to reference Liemburg-Apers DC, et al. Quantitative glucose and ATP sensing in mammalian cells. Pharm Res. 2011;28(11):2745.PubMedCrossRef Liemburg-Apers DC, et al. Quantitative glucose and ATP sensing in mammalian cells. Pharm Res. 2011;28(11):2745.PubMedCrossRef
3.
go back to reference Winkler BS, Arnold MJ, Brassell MA, Sliter DR. Glucose dependence of glycolysis, hexose monophosphate shunt activity, energy status, and the polyol pathway in retinas isolated from normal (nondiabetic) rats. Invest Ophthalmol Vis Sci. 1997;38(1):62–71.PubMed Winkler BS, Arnold MJ, Brassell MA, Sliter DR. Glucose dependence of glycolysis, hexose monophosphate shunt activity, energy status, and the polyol pathway in retinas isolated from normal (nondiabetic) rats. Invest Ophthalmol Vis Sci. 1997;38(1):62–71.PubMed
4.
go back to reference Pike LS, et al. Inhibition of fatty acid oxidation by etomoxir impairs NADPH production and increases reactive oxygen species resulting in ATP depletion and cell death in human glioblastoma cells. Biochim Biophys Acta (BBA)-Bioenergenet. 2011;1807(6):726–34.CrossRef Pike LS, et al. Inhibition of fatty acid oxidation by etomoxir impairs NADPH production and increases reactive oxygen species resulting in ATP depletion and cell death in human glioblastoma cells. Biochim Biophys Acta (BBA)-Bioenergenet. 2011;1807(6):726–34.CrossRef
5.
go back to reference Nemoto S, Takeda K, Yu ZX, Ferrans VJ, Finkel T. Role for mitochondrial oxidants as regulators of cellular metabolism. Mol Cell Biol. 2000;20(19):7311–8.PubMedPubMedCentralCrossRef Nemoto S, Takeda K, Yu ZX, Ferrans VJ, Finkel T. Role for mitochondrial oxidants as regulators of cellular metabolism. Mol Cell Biol. 2000;20(19):7311–8.PubMedPubMedCentralCrossRef
6.
go back to reference Lam TK, Gutierrez-Juarez R, Pocai A, Rossetti L. Regulation of blood glucose by hypothalamic pyruvate metabolism. Science. 2005;309(5736):943–7.PubMedCrossRef Lam TK, Gutierrez-Juarez R, Pocai A, Rossetti L. Regulation of blood glucose by hypothalamic pyruvate metabolism. Science. 2005;309(5736):943–7.PubMedCrossRef
7.
go back to reference Lunt SY, Vander Heiden MG. Aerobic glycolysis: meeting the metabolic requirements of cell proliferation. Annu Rev Cell Dev Biol. 2011;27:441–64.PubMedCrossRef Lunt SY, Vander Heiden MG. Aerobic glycolysis: meeting the metabolic requirements of cell proliferation. Annu Rev Cell Dev Biol. 2011;27:441–64.PubMedCrossRef
8.
go back to reference Koppenol WH, Bounds PL, Dang CV. Otto Warburg’s contributions to current concepts of cancer metabolism. Nat Rev Cancer. 2011;11(5):325.PubMedCrossRef Koppenol WH, Bounds PL, Dang CV. Otto Warburg’s contributions to current concepts of cancer metabolism. Nat Rev Cancer. 2011;11(5):325.PubMedCrossRef
11.
go back to reference Haber RS, Rathan A, Weiser KR, Pritsker A, Itzkowitz SH, Bodian C, et al. GLUT1 glucose transporter expression in colorectal carcinoma: a marker for poor prognosis. Cancer. 1998;83(1):34–40.PubMedCrossRef Haber RS, Rathan A, Weiser KR, Pritsker A, Itzkowitz SH, Bodian C, et al. GLUT1 glucose transporter expression in colorectal carcinoma: a marker for poor prognosis. Cancer. 1998;83(1):34–40.PubMedCrossRef
12.
13.
go back to reference Mathupala SP, Ko YH, Pedersen PL. The pivotal roles of mitochondria in cancer: Warburg and beyond and encouraging prospects for effective therapies. Biochim Biophys Acta (BBA)-Bioenergenet. 2010;1797(6-7):1225–30.CrossRef Mathupala SP, Ko YH, Pedersen PL. The pivotal roles of mitochondria in cancer: Warburg and beyond and encouraging prospects for effective therapies. Biochim Biophys Acta (BBA)-Bioenergenet. 2010;1797(6-7):1225–30.CrossRef
14.
go back to reference Chiche J, Brahimi-Horn MC, Pouysségur J. Tumour hypoxia induces a metabolic shift causing acidosis: a common feature in cancer. J Cell Mol Med. 2010;14(4):771–94.PubMedCrossRef Chiche J, Brahimi-Horn MC, Pouysségur J. Tumour hypoxia induces a metabolic shift causing acidosis: a common feature in cancer. J Cell Mol Med. 2010;14(4):771–94.PubMedCrossRef
15.
go back to reference Puglisi MA, Tesori V, Lattanzi W, Gasbarrini GB, Gasbarrini A. Colon cancer stem cells: controversies and perspectives. World J Gastroenterol. 2013;19(20):2997–3006.PubMedPubMedCentralCrossRef Puglisi MA, Tesori V, Lattanzi W, Gasbarrini GB, Gasbarrini A. Colon cancer stem cells: controversies and perspectives. World J Gastroenterol. 2013;19(20):2997–3006.PubMedPubMedCentralCrossRef
16.
go back to reference Kim J-w, Dang CV. Cancer's molecular sweet tooth and the Warburg effect. Cancer Res. 2006;66(18):8927–30.PubMedCrossRef Kim J-w, Dang CV. Cancer's molecular sweet tooth and the Warburg effect. Cancer Res. 2006;66(18):8927–30.PubMedCrossRef
17.
go back to reference Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61(2):69–90.PubMedCrossRef Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61(2):69–90.PubMedCrossRef
19.
go back to reference Haas P, et al. Effectiveness of whole grain consumption in the prevention of colorectal cancer: Meta-analysis of cohort studies. Int J Food Sci Nutr. 2009;60(sup6):1–13.PubMedCrossRef Haas P, et al. Effectiveness of whole grain consumption in the prevention of colorectal cancer: Meta-analysis of cohort studies. Int J Food Sci Nutr. 2009;60(sup6):1–13.PubMedCrossRef
20.
go back to reference Donovan MG, et al. Mediterranean diet: prevention of colorectal cancer. Front Nutri. 2017;4:59.CrossRef Donovan MG, et al. Mediterranean diet: prevention of colorectal cancer. Front Nutri. 2017;4:59.CrossRef
21.
go back to reference Aune D, et al. Dietary fibre, whole grains, and risk of colorectal cancer: systematic review and dose-response meta-analysis of prospective studies. Bmj. 2011;343:d6617.PubMedPubMedCentralCrossRef Aune D, et al. Dietary fibre, whole grains, and risk of colorectal cancer: systematic review and dose-response meta-analysis of prospective studies. Bmj. 2011;343:d6617.PubMedPubMedCentralCrossRef
22.
go back to reference Yousefi B, Eslami M, Ghasemian A, Kokhaei P, Salek Farrokhi A, Darabi N. Probiotics importance and their immunomodulatory properties. J Cell Physiol. 2019;234(6):8008–18.PubMedCrossRef Yousefi B, Eslami M, Ghasemian A, Kokhaei P, Salek Farrokhi A, Darabi N. Probiotics importance and their immunomodulatory properties. J Cell Physiol. 2019;234(6):8008–18.PubMedCrossRef
23.
go back to reference Eslami M, et al. Are probiotics useful for therapy of Helicobacter pylori diseases? Comp Immunol Microbiol Infect Dis. 2019;64:99–108.PubMedCrossRef Eslami M, et al. Are probiotics useful for therapy of Helicobacter pylori diseases? Comp Immunol Microbiol Infect Dis. 2019;64:99–108.PubMedCrossRef
24.
go back to reference Salek Farrokhi A, et al. Is it true that gut microbiota is considered as panacea in cancer therapy? J Cell Physiol. 2019;234(9):14941–50.CrossRef Salek Farrokhi A, et al. Is it true that gut microbiota is considered as panacea in cancer therapy? J Cell Physiol. 2019;234(9):14941–50.CrossRef
25.
go back to reference Kobyliak N, et al. Probiotics for experimental obesity prevention: focus on strain dependence and viability of composition. Endokrynologia Polska. 2017;68(6):659–67.PubMed Kobyliak N, et al. Probiotics for experimental obesity prevention: focus on strain dependence and viability of composition. Endokrynologia Polska. 2017;68(6):659–67.PubMed
26.
go back to reference Kobyliak N, Abenavoli L, Falalyeyeva T, Beregova T. Efficacy of probiotics and smectite in rats with non-alcoholic fatty liver disease. Ann Hepatol. 2018;17(1):153–61.PubMedCrossRef Kobyliak N, Abenavoli L, Falalyeyeva T, Beregova T. Efficacy of probiotics and smectite in rats with non-alcoholic fatty liver disease. Ann Hepatol. 2018;17(1):153–61.PubMedCrossRef
27.
go back to reference Kobyliak N, Falalyeyeva T, Bodnar P, Beregova T. Probiotics supplemented with omega-3 fatty acids are more effective for hepatic steatosis reduction in an animal model of obesity. Probiot Antimicrobial Proteins. 2017;9(2):123–30.CrossRef Kobyliak N, Falalyeyeva T, Bodnar P, Beregova T. Probiotics supplemented with omega-3 fatty acids are more effective for hepatic steatosis reduction in an animal model of obesity. Probiot Antimicrobial Proteins. 2017;9(2):123–30.CrossRef
28.
go back to reference Eslami M, et al. Importance of probiotics in the prevention and treatment of colorectal cancer. J Cell Physiol. 2019. Eslami M, et al. Importance of probiotics in the prevention and treatment of colorectal cancer. J Cell Physiol. 2019.
29.
go back to reference Yousefi, B., et al. Probiotics can really cure an autoimmune disease? Gene Reports, 2019: p. 100364. Yousefi, B., et al. Probiotics can really cure an autoimmune disease? Gene Reports, 2019: p. 100364.
30.
go back to reference Ghasemian A, et al. Probiotics and their increasing importance in human health and infection control. Rev Med Microbiol. 2018;29(4):153–8.CrossRef Ghasemian A, et al. Probiotics and their increasing importance in human health and infection control. Rev Med Microbiol. 2018;29(4):153–8.CrossRef
32.
go back to reference Cines DB, Pollak ES, Buck CA, Loscalzo J, Zimmerman GA, McEver R, et al. Endothelial cells in physiology and in the pathophysiology of vascular disorders. Blood. 1998;91(10):3527–61.PubMed Cines DB, Pollak ES, Buck CA, Loscalzo J, Zimmerman GA, McEver R, et al. Endothelial cells in physiology and in the pathophysiology of vascular disorders. Blood. 1998;91(10):3527–61.PubMed
33.
34.
go back to reference Bergers G, Benjamin LE. Angiogenesis: tumorigenesis and the angiogenic switch. Nat Rev Cancer. 2003;3(6):401–10.PubMedCrossRef Bergers G, Benjamin LE. Angiogenesis: tumorigenesis and the angiogenic switch. Nat Rev Cancer. 2003;3(6):401–10.PubMedCrossRef
36.
go back to reference Ouyang W, et al. An essential role of the Forkhead-box transcription factor Foxo1 in control of T cell homeostasis and tolerance. Immunity. 2009;30(3):358–71.PubMedPubMedCentralCrossRef Ouyang W, et al. An essential role of the Forkhead-box transcription factor Foxo1 in control of T cell homeostasis and tolerance. Immunity. 2009;30(3):358–71.PubMedPubMedCentralCrossRef
37.
go back to reference Milisav I, Poljšak B, Ribarič S. Reduced risk of apoptosis: mechanisms of stress responses. Apoptosis. 2017;22(2):265–83.PubMedCrossRef Milisav I, Poljšak B, Ribarič S. Reduced risk of apoptosis: mechanisms of stress responses. Apoptosis. 2017;22(2):265–83.PubMedCrossRef
39.
go back to reference Kroemer G, Pouyssegur J. Tumor cell metabolism: cancer’s Achilles’ heel. Cancer Cell. 2008;13(6):472–82.PubMedCrossRef Kroemer G, Pouyssegur J. Tumor cell metabolism: cancer’s Achilles’ heel. Cancer Cell. 2008;13(6):472–82.PubMedCrossRef
40.
go back to reference Cairns RA, Harris IS, Mak TW. Regulation of cancer cell metabolism. Nat Rev Cancer. 2011;11(2):85–95.PubMedCrossRef Cairns RA, Harris IS, Mak TW. Regulation of cancer cell metabolism. Nat Rev Cancer. 2011;11(2):85–95.PubMedCrossRef
41.
go back to reference Yuan J, Glazer PM. Mutagenesis induced by the tumor microenvironment. Mutation Res/Fund Mol Mech Mutagen. 1998;400(1-2):439–46.CrossRef Yuan J, Glazer PM. Mutagenesis induced by the tumor microenvironment. Mutation Res/Fund Mol Mech Mutagen. 1998;400(1-2):439–46.CrossRef
42.
go back to reference Goda N, Kanai M. Hypoxia-inducible factors and their roles in energy metabolism. Int J Hematol. 2012;95(5):457–63.PubMedCrossRef Goda N, Kanai M. Hypoxia-inducible factors and their roles in energy metabolism. Int J Hematol. 2012;95(5):457–63.PubMedCrossRef
43.
go back to reference Vander Heiden MG. Targeting cancer metabolism: a therapeutic window opens. Nat Rev Drug Discov. 2011;10(9):671–84.PubMedCrossRef Vander Heiden MG. Targeting cancer metabolism: a therapeutic window opens. Nat Rev Drug Discov. 2011;10(9):671–84.PubMedCrossRef
44.
go back to reference Makeeva EN, Makeev AM, Rodziller ID. Metabolism of monocarbon compounds during biological purification of sewage waters. Prikl Biokhim Mikrobiol. 1975;11(3):367–73.PubMed Makeeva EN, Makeev AM, Rodziller ID. Metabolism of monocarbon compounds during biological purification of sewage waters. Prikl Biokhim Mikrobiol. 1975;11(3):367–73.PubMed
45.
go back to reference Clare CE, et al. One-carbon metabolism: linking nutritional biochemistry to epigenetic programming of long-term development. Ann Rev Anim Biosci. 2019;7(1):263–87.CrossRef Clare CE, et al. One-carbon metabolism: linking nutritional biochemistry to epigenetic programming of long-term development. Ann Rev Anim Biosci. 2019;7(1):263–87.CrossRef
46.
47.
go back to reference Innocenti F, Ratain M. Update on pharmacogenetics in cancer chemotherapy. Eur J Cancer. 2002;38(5):639–44.PubMedCrossRef Innocenti F, Ratain M. Update on pharmacogenetics in cancer chemotherapy. Eur J Cancer. 2002;38(5):639–44.PubMedCrossRef
48.
go back to reference Schirch V, Szebenyi DM. Serine hydroxymethyltransferase revisited. Curr Opin Chem Biol. 2005;9(5):482–7.PubMedCrossRef Schirch V, Szebenyi DM. Serine hydroxymethyltransferase revisited. Curr Opin Chem Biol. 2005;9(5):482–7.PubMedCrossRef
49.
go back to reference Yablokov VY, et al. Studies of the rates of thermal decomposition of glycine, alanine, and serine. Russ J Gen Chem. 2009;79(8):1704–6.CrossRef Yablokov VY, et al. Studies of the rates of thermal decomposition of glycine, alanine, and serine. Russ J Gen Chem. 2009;79(8):1704–6.CrossRef
51.
52.
go back to reference Newsholme P, Procopio J, Lima MM, Pithon-Curi TC, Curi R. Glutamine and glutamate—their central role in cell metabolism and function. Cell Biochem Funct. 2003;21(1):1–9.PubMedCrossRef Newsholme P, Procopio J, Lima MM, Pithon-Curi TC, Curi R. Glutamine and glutamate—their central role in cell metabolism and function. Cell Biochem Funct. 2003;21(1):1–9.PubMedCrossRef
53.
go back to reference Newsholme P, Lima MM, Procopio J, Pithon-Curi TC, Doi SQ, Bazotte RB, et al. Glutamine and glutamate as vital metabolites. Braz J Med Biol Res. 2003;36(2):153–63.PubMedCrossRef Newsholme P, Lima MM, Procopio J, Pithon-Curi TC, Doi SQ, Bazotte RB, et al. Glutamine and glutamate as vital metabolites. Braz J Med Biol Res. 2003;36(2):153–63.PubMedCrossRef
55.
go back to reference Innocenti F, Iyer L, Ratain MJ. Pharmacogenomics of chemotherapeutic agents in cancer treatment. In: Licinio W, editor. Pharmacogenomics: the Search for Individualized Therapies. Weinheim: Wiley-VCH Verlag GmbH; 2002. Innocenti F, Iyer L, Ratain MJ. Pharmacogenomics of chemotherapeutic agents in cancer treatment. In: Licinio W, editor. Pharmacogenomics: the Search for Individualized Therapies. Weinheim: Wiley-VCH Verlag GmbH; 2002.
56.
go back to reference Maddocks OD, Berkers CR, Mason SM, Zheng L, Blyth K, Gottlieb E, et al. Serine starvation induces stress and p53-dependent metabolic remodelling in cancer cells. Nature. 2013;493(7433):542–6.PubMedCrossRef Maddocks OD, Berkers CR, Mason SM, Zheng L, Blyth K, Gottlieb E, et al. Serine starvation induces stress and p53-dependent metabolic remodelling in cancer cells. Nature. 2013;493(7433):542–6.PubMedCrossRef
57.
go back to reference Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science. 2009;324(5930):1029–33.PubMedPubMedCentralCrossRef Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science. 2009;324(5930):1029–33.PubMedPubMedCentralCrossRef
61.
go back to reference Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: integrating immunity’s roles in cancer suppression and promotion. Science. 2011;331(6024):1565–70.PubMedCrossRef Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: integrating immunity’s roles in cancer suppression and promotion. Science. 2011;331(6024):1565–70.PubMedCrossRef
62.
go back to reference Chang C-H, Curtis JD, Maggi LB Jr, Faubert B, Villarino AV, O'Sullivan D, et al. Posttranscriptional control of T cell effector function by aerobic glycolysis. Cell. 2013;153(6):1239–51.PubMedPubMedCentralCrossRef Chang C-H, Curtis JD, Maggi LB Jr, Faubert B, Villarino AV, O'Sullivan D, et al. Posttranscriptional control of T cell effector function by aerobic glycolysis. Cell. 2013;153(6):1239–51.PubMedPubMedCentralCrossRef
63.
go back to reference Brand A, et al. LDHA-associated lactic acid production blunts tumor immunosurveillance by T and NK cells. Cell Metab. 2016;24(5):657–71.PubMedCrossRef Brand A, et al. LDHA-associated lactic acid production blunts tumor immunosurveillance by T and NK cells. Cell Metab. 2016;24(5):657–71.PubMedCrossRef
65.
go back to reference Berdasco M, Esteller M. Aberrant epigenetic landscape in cancer: how cellular identity goes awry. Dev Cell. 2010;19(5):698–711.PubMedCrossRef Berdasco M, Esteller M. Aberrant epigenetic landscape in cancer: how cellular identity goes awry. Dev Cell. 2010;19(5):698–711.PubMedCrossRef
66.
go back to reference Scott KP, Gratz SW, Sheridan PO, Flint HJ, Duncan SH. The influence of diet on the gut microbiota. Pharmacol Res. 2013;69(1):52–60.PubMedCrossRef Scott KP, Gratz SW, Sheridan PO, Flint HJ, Duncan SH. The influence of diet on the gut microbiota. Pharmacol Res. 2013;69(1):52–60.PubMedCrossRef
68.
go back to reference Gonçalves P, Martel F. Butyrate and colorectal cancer: the role of butyrate transport. Curr Drug Metab. 2013;14(9):994–1008.PubMedCrossRef Gonçalves P, Martel F. Butyrate and colorectal cancer: the role of butyrate transport. Curr Drug Metab. 2013;14(9):994–1008.PubMedCrossRef
69.
go back to reference Galluzzi L, Kepp O, Vander Heiden MG, Kroemer G. Metabolic targets for cancer therapy. Nat Rev Drug Discov. 2013;12(11):829–46.PubMedCrossRef Galluzzi L, Kepp O, Vander Heiden MG, Kroemer G. Metabolic targets for cancer therapy. Nat Rev Drug Discov. 2013;12(11):829–46.PubMedCrossRef
70.
go back to reference Donohoe DR, Collins LB, Wali A, Bigler R, Sun W, Bultman SJ. The Warburg effect dictates the mechanism of butyrate-mediated histone acetylation and cell proliferation. Mol Cell. 2012;48(4):612–26.PubMedPubMedCentralCrossRef Donohoe DR, Collins LB, Wali A, Bigler R, Sun W, Bultman SJ. The Warburg effect dictates the mechanism of butyrate-mediated histone acetylation and cell proliferation. Mol Cell. 2012;48(4):612–26.PubMedPubMedCentralCrossRef
71.
go back to reference Forte A, de Sanctis R, Leonetti G, Manfredelli S, Urbano V, Bezzi M. Dietary chemoprevention of colorectal cancer. Ann Ital Chir. 2008;79(4):261–7.PubMed Forte A, de Sanctis R, Leonetti G, Manfredelli S, Urbano V, Bezzi M. Dietary chemoprevention of colorectal cancer. Ann Ital Chir. 2008;79(4):261–7.PubMed
72.
go back to reference Kennedy KM, Dewhirst MW. Tumor metabolism of lactate: the influence and therapeutic potential for MCT and CD147 regulation. Future Oncol. 2010;6(1):127–48.PubMedCrossRef Kennedy KM, Dewhirst MW. Tumor metabolism of lactate: the influence and therapeutic potential for MCT and CD147 regulation. Future Oncol. 2010;6(1):127–48.PubMedCrossRef
73.
go back to reference Encarnação J, et al. Revisit dietary fiber on colorectal cancer: butyrate and its role on prevention and treatment. Cancer Metastasis Rev. 2015;34(3):465–78.PubMedCrossRef Encarnação J, et al. Revisit dietary fiber on colorectal cancer: butyrate and its role on prevention and treatment. Cancer Metastasis Rev. 2015;34(3):465–78.PubMedCrossRef
74.
go back to reference Garcia-Ramirez M, Rocchini C, Ausio J. Modulation of chromatin folding by histone acetylation. J Biol Chem. 1995;270(30):17923–8.PubMedCrossRef Garcia-Ramirez M, Rocchini C, Ausio J. Modulation of chromatin folding by histone acetylation. J Biol Chem. 1995;270(30):17923–8.PubMedCrossRef
75.
go back to reference Medina V, Edmonds B, Young GP, James R, Appleton S, Zalewski PD. Induction of caspase-3 protease activity and apoptosis by butyrate and trichostatin A (inhibitors of histone deacetylase): dependence on protein synthesis and synergy with a mitochondrial/cytochrome c-dependent pathway. Cancer Res. 1997;57(17):3697–707.PubMed Medina V, Edmonds B, Young GP, James R, Appleton S, Zalewski PD. Induction of caspase-3 protease activity and apoptosis by butyrate and trichostatin A (inhibitors of histone deacetylase): dependence on protein synthesis and synergy with a mitochondrial/cytochrome c-dependent pathway. Cancer Res. 1997;57(17):3697–707.PubMed
76.
go back to reference Minucci S, Pelicci PG. Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer. Nat Rev Cancer. 2006;6(1):38–51.PubMedCrossRef Minucci S, Pelicci PG. Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer. Nat Rev Cancer. 2006;6(1):38–51.PubMedCrossRef
77.
go back to reference Itzkowitz SH, Yio X. Inflammation and cancer IV. Colorectal cancer in inflammatory bowel disease: the role of inflammation. Am J Physiol-Gastrointest Liver Physiol. 2004;287(1):G7–G17.PubMedCrossRef Itzkowitz SH, Yio X. Inflammation and cancer IV. Colorectal cancer in inflammatory bowel disease: the role of inflammation. Am J Physiol-Gastrointest Liver Physiol. 2004;287(1):G7–G17.PubMedCrossRef
78.
go back to reference Wächtershäuser A, Stein J. Rationale for the luminal provision of butyrate in intestinal diseases. Eur J Nutr. 2000;39(4):164–71.PubMedCrossRef Wächtershäuser A, Stein J. Rationale for the luminal provision of butyrate in intestinal diseases. Eur J Nutr. 2000;39(4):164–71.PubMedCrossRef
79.
go back to reference Kaisar MM, et al. Butyrate conditions human dendritic cells to prime type 1 regulatory T cells via both histone deacetylase inhibition and G protein-coupled receptor 109A signaling. Front Immunol. 2017;8:1429.PubMedPubMedCentralCrossRef Kaisar MM, et al. Butyrate conditions human dendritic cells to prime type 1 regulatory T cells via both histone deacetylase inhibition and G protein-coupled receptor 109A signaling. Front Immunol. 2017;8:1429.PubMedPubMedCentralCrossRef
80.
go back to reference Walker AW, et al. High-throughput clone library analysis of the mucosa-associated microbiota reveals dysbiosis and differences between inflamed and non-inflamed regions of the intestine in inflammatory bowel disease. BMC Microbiol. 2011;11(1):7.PubMedPubMedCentralCrossRef Walker AW, et al. High-throughput clone library analysis of the mucosa-associated microbiota reveals dysbiosis and differences between inflamed and non-inflamed regions of the intestine in inflammatory bowel disease. BMC Microbiol. 2011;11(1):7.PubMedPubMedCentralCrossRef
81.
go back to reference Greenhalgh K, Meyer KM, Aagaard KM, Wilmes P. The human gut microbiome in health: establishment and resilience of microbiota over a lifetime. Environ Microbiol. 2016;18(7):2103–16.PubMedPubMedCentralCrossRef Greenhalgh K, Meyer KM, Aagaard KM, Wilmes P. The human gut microbiome in health: establishment and resilience of microbiota over a lifetime. Environ Microbiol. 2016;18(7):2103–16.PubMedPubMedCentralCrossRef
82.
83.
go back to reference den Besten G, et al. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J Lipid Res. 2013;54(9):2325–40.CrossRef den Besten G, et al. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J Lipid Res. 2013;54(9):2325–40.CrossRef
84.
go back to reference Bultman SJ. Molecular pathways: gene–environment interactions regulating dietary fiber induction of proliferation and apoptosis via butyrate for cancer prevention. Clin Cancer Res. 2014;20(4):799–803.PubMedCrossRef Bultman SJ. Molecular pathways: gene–environment interactions regulating dietary fiber induction of proliferation and apoptosis via butyrate for cancer prevention. Clin Cancer Res. 2014;20(4):799–803.PubMedCrossRef
85.
go back to reference Hamer HM, Jonkers D, Venema K, Vanhoutvin S, Troost FJ, Brummer RJ. The role of butyrate on colonic function. Aliment Pharmacol Ther. 2008;27(2):104–19.PubMedCrossRef Hamer HM, Jonkers D, Venema K, Vanhoutvin S, Troost FJ, Brummer RJ. The role of butyrate on colonic function. Aliment Pharmacol Ther. 2008;27(2):104–19.PubMedCrossRef
87.
go back to reference Canani RB, Di Costanzo M, Leone L. The epigenetic effects of butyrate: potential therapeutic implications for clinical practice. Clin Epigenetics. 2012;4(1):4.CrossRef Canani RB, Di Costanzo M, Leone L. The epigenetic effects of butyrate: potential therapeutic implications for clinical practice. Clin Epigenetics. 2012;4(1):4.CrossRef
88.
go back to reference Yagi A, Yu BP. Immune modulation by microbiota sources: effects of aloe vera gel and butyrate. J Gastroenterol Hepatol Res. 2018;7(5):2681–9.CrossRef Yagi A, Yu BP. Immune modulation by microbiota sources: effects of aloe vera gel and butyrate. J Gastroenterol Hepatol Res. 2018;7(5):2681–9.CrossRef
Metadata
Title
Importance of the Microbiota Inhibitory Mechanism on the Warburg Effect in Colorectal Cancer Cells
Authors
Majid Eslami
Sina Sadrifar
Mohsen Karbalaei
Masoud Keikha
Nazarii M. Kobyliak
Bahman Yousefi
Publication date
01-09-2020
Publisher
Springer US
Published in
Journal of Gastrointestinal Cancer / Issue 3/2020
Print ISSN: 1941-6628
Electronic ISSN: 1941-6636
DOI
https://doi.org/10.1007/s12029-019-00329-3

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