Advertisement

Journal of Gastrointestinal Cancer

, Volume 44, Issue 2, pp 121–131 | Cite as

RETRACTED ARTICLE: Intestinal Microbiota, Probiotics and Human Gastrointestinal Cancers

  • Antonella Orlando
  • Francesco Russo
Review Article

Abstract

Introduction

Cancers of the gastrointestinal tract account for 25 % of all cancers and for 9 % of all causes of cancer death in the world, so gastrointestinal cancers represent a major health problem. In the past decades, an emerging role has been attributed to the interactions between the gastrointestinal content and the onset of neoplasia.

Methods

Thus, exogenous microbial administration of peculiar bacterial strains (probiotics) has been suggested as having a profound influence on multiple processes associated with a change in cancer risk. Probiotics are mono or mixed cultures of live microorganisms that might beneficially affect the host by improving the characteristics of indigenous microflora. Although the effects of probiotic administration has been intensively investigated in vitro, in animal models, in healthy volunteers, and in some human gastrointestinal diseases, very little is still known about the possible cross-interactions among probiotic administration, changes of intestinal flora, and the neoplastic transformation of gastrointestinal mucosa.

Results

Theoretically, probiotics are able to reduce cancer risk by a number of mechanisms: (a) binding and degradation of potential carcinogens; (b) quantitative, qualitative and metabolic alterations of the intestinal microflora; (c) production of anti-tumorigenic or anti-mutagenic compounds; (d) competitive action towards pathogenic bacteria; (e) enhancement of the host’s immune response; (f) direct effects on cell proliferation.

Conclusion

This review will attempt to highlight the literature on the most widely recognized effects of probiotics against neoplastic transformation of gastrointestinal mucosa and in particular on their effects on cell proliferation.

Keywords

Probiotics Gastric cancer Colorectal cancer Pancreatic cancer Microbiota 

Abbreviations

GI

Gastrointestinal

LAB

Lactic acid bacteria

IBD

Inflammatory bowel disease

H. pylori

Helicobacter pylori

GC

Gastric cancer

MALT

Mucosa-associated lymphoid tissue

CRC

Colorectal cancer

IBS

Irritable bowel syndrome

ACF

Aberrant crypt foci

L. GG

Lactobacillus rhamnosus GG

ODC

Ornithine decarboxylase

IL-1β

Interleukin 1β

TNF-α

Tumor necrosis factor-alpha

SMO

Spermine oxidase

PAO

Polyamine oxidase

SSAT

Spermidine/spermine N1-acetyltransferase

SAMDC

S-Adenosylmethionine decarboxylase

Notes

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Bazuro GE, Torino F, Gasparini G, Capurso L. Chemoprevention in gastrointestinal adenocarcinoma: for few but not for all? Minerva Gastroenterol Dietol. 2009;54(4):429–44.Google Scholar
  2. 2.
    Tlaskalová-Hogenová H, Stěpánková R, Kozáková H, Hudcovic T, Vannucci L, Tučková L, Rossmann P, Hrnčíř T, Kverka M, Zákostelská Z, Klimešová K, Přibylová J, Bártová J, Sanchez D, Fundová P, Borovská D, Srůtková D, Zídek Z, Schwarzer M, Drastich P, Funda DP. The role of gut microbiota (commensal bacteria) and the mucosal barrier in the pathogenesis of inflammatory and autoimmune diseases and cancer: contribution of germ-free and gnotobiotic animal models of human diseases. Cell Mol Immunol. 2011;8(2):110–20. doi: 10.1038/cmi.2010.67.PubMedCrossRefGoogle Scholar
  3. 3.
    Guarner F. Enteric flora in health and disease. Digestion. 2006;73(1):5–12. doi: 10.1159/000089775.PubMedCrossRefGoogle Scholar
  4. 4.
    Report of a Joint FAO/WHO Expert Consultation on Evaluation of Health and Nutritional Properties of Probiotics in Food Including Powder Milk with Live Lactic Acid Bacteria (October 2001). Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. Food and Agriculture Organization of the United Nations, World Health Organization. Retrieved 2009-11-04.Google Scholar
  5. 5.
    Ciorba MA. A Gastroenterologist's guide to probiotics. Clin Gastroenterol Hepatol. 2012;10(9):960–8. doi: 10.1016/j.cgh.2012.03.024.PubMedCrossRefGoogle Scholar
  6. 6.
    Goossens DA, Jonkers DM, Russel MG, Stobberingh EE, Stockbrügger RW. The effect of a probiotic drink with Lactobacillus plantarum 299v on the bacterial composition in faeces and mucosal biopsies of rectum and ascending colon. Aliment Pharmacol Ther. 2006;23:255–63. doi: 10.1111/j.1365-2036.2006.02749.x.PubMedCrossRefGoogle Scholar
  7. 7.
    Bhandari A, Crowe SE. Helicobacter pylori in gastric malignancies. Curr Gastroenterol Rep. 2012;14(6):489v96. doi: 10.1007/s11894-012-0296-y.CrossRefGoogle Scholar
  8. 8.
    Thiel A, Ristimäki A. Gastric cancer: basic aspects. Helicobacter. 2012;17(1):26–9. doi: 10.1111/j.1523-5378.2011.00879.x.PubMedCrossRefGoogle Scholar
  9. 9.
    Wroblewski LE, Richard M, Peek Jr RM, Wilson KT. Helicobacter pylori and gastric cancer: factors that modulate disease risk. Clin Microbiol Rev. 2010;23(4):713–39. doi: 10.1128/CMR.00011-10.PubMedCrossRefGoogle Scholar
  10. 10.
    Eslick GD. Helicobacter pylori infection causes gastric cancer? A review of the epidemiological, meta-analytic, and experimental evidence. World J Gastroenterol. 2006;12(19):2991–9.PubMedGoogle Scholar
  11. 11.
    De Vries AC, Van Driel HF, Richardus JH, Ouwendijk M, Van Vuuren AJ, De Man RA, Kuipers EJ. Migrant communities constitute a possible target population for primary prevention of Helicobacter pylori-related complications in low incidence countries. Scand J Gastroenterol. 2008;43:403–9. doi: 10.1080/00365520701814077.PubMedCrossRefGoogle Scholar
  12. 12.
    Kokkola A, Valle J, Haapiainen R, Sipponen P, Kivilaakso E, Puokallainen P. Helicobacter pylori infection in young patients with gastric carcinoma. Scand J Gastroenterol. 1996;31:643–7. doi: 10.1056/NEJM199110173251603.PubMedCrossRefGoogle Scholar
  13. 13.
    Gisbert JP, Calvet X. Review article: common misconceptions in the management of Helicobacter pylori-associated gastric MALT-lymphoma. Aliment Pharmacol Ther. 2011;34(9):1047–62. doi: 10.1111/j.1365-2036.2011.04839.x.PubMedCrossRefGoogle Scholar
  14. 14.
    Romano M, Ricci V, Zarrilli R. Mechanisms of disease: Helicobacter pylori-related gastric carcinogenesis—implications for chemoprevention. Nat Clin Pract Gastroenterol Hepatol. 2006;3(11):622–32. doi: 10.1038/ncpgasthep0634.PubMedCrossRefGoogle Scholar
  15. 15.
    Ngoan LT, Mizoue T, Fujino Y, Tokui N, Yoshimura T. Dietary factors and stomach cancer mortality. Br J Cancer. 2002;87:37–42. doi: 10.1038/sj.bjc.6600415.PubMedCrossRefGoogle Scholar
  16. 16.
    Joossens JV, Hill MJ, Elliott P, Stamler R, Lesaffre E, Dyer A, Nichols R, Kesteloot H. Dietary salt, nitrate and stomach cancer mortality in 24 countries. European Cancer Prevention (ECP) and the INTERSALT Cooperative Research Group. Int J Epidemiol. 1996;25:494–504. doi: 10.1093/ije/25.3.494.PubMedCrossRefGoogle Scholar
  17. 17.
    Fox JG, Dangler CA, Taylor NS, King A, Koh TJ, Wang TC. High-salt diet induces gastric epithelial hyperplasia and parietal cell loss, and enhances Helicobacter pylori colonization in C57BL/6 mice. Cancer Res. 1999;59:4823–8.PubMedGoogle Scholar
  18. 18.
    Sinha R, Rothman N, Brown ED, Mark SD, Hoover RN, Caporaso NE, Levander OA, Knize MG, Lang NP, Kadlubar FF. Pan-fried meat containing high levels of heterocyclic aromatic amines but low levels of polycyclic aromatic hydrocarbons induces cytochrome P4501A2 activity in humans. Cancer Res. 1994;54:6154–9.PubMedGoogle Scholar
  19. 19.
    You WC, Zhao L, Chang YS, Blot WJ, Fraumeni Jr JF. Progression of precancerous gastric lesions. Lancet. 1995;345:866–7. doi: 10.1016/S0140-6736(95)93006-X.PubMedCrossRefGoogle Scholar
  20. 20.
    Zhang ZW, Abdullahi M, Farthing MJ. Effect of physiological concentrations of vitamin C on gastric cancer cells and Helicobacter pylori. Gut. 2002;50:165–9. doi: 10.1136/gut.50.2.165.PubMedCrossRefGoogle Scholar
  21. 21.
    Gouma DJ, Busch ORC, van Gulik TM. Treatment of pancreatic adenocarcinoma: a European perspective. Surg Oncol Clin North Am. 2008;17(3):569–86. doi: 10.1016/j.soc.2008.02.005.CrossRefGoogle Scholar
  22. 22.
    Van Santvoort HC, Besselink MG, Timmerman HM, et al. Probiotics in surgery. Surgery. 2008;143:1–7. doi: 10.1016/j.surg.2007.06.009.PubMedCrossRefGoogle Scholar
  23. 23.
    Burn J, Mathers J, Bishop DT. Genetics, inheritance and strategies for prevention in populations at high risk of colorectal cancer (CRC). Recent Results Canc Res. 2012;191:157–83. doi: 10.1007/978-3-642-30331-9_9.CrossRefGoogle Scholar
  24. 24.
    Castells A, Castellvi-Bel S, Balaguer F. Concepts in familial colorectal cancer: where do we stand and what is the future? Gastroenterology. 2009;137:404–9. doi: 10.1053/j.gastro.2009.06.015.PubMedCrossRefGoogle Scholar
  25. 25.
    Johnson IT, Lund EK. Review article: nutrition, obesity and colorectal cancer. Aliment Pharmacol Ther. 2007;26:161–81. doi: 10.1111/j.1365-2036.2007.03371.x.PubMedCrossRefGoogle Scholar
  26. 26.
    Marshall JR. Prevention of colorectal cancer: diet, chemoprevention, and lifestyle. Gastroenterol Clin North Am. 2008;37:73–82. doi: 10.1016/j.gtc.2007.12.008.PubMedCrossRefGoogle Scholar
  27. 27.
    Austin GL, Adair LS, Galanko JA, Martin CF, Satia JA, Sandler RS. A diet high in fruits and low in meats reduces the risk of colorectal adenomas. J Nutr. 2007;137:999–1004.PubMedGoogle Scholar
  28. 28.
    Randi G, Edefonti V, Ferraroni M, La Vecchia C, Decarli A. Dietary patterns and the risk of colorectal cancer and adenomas. Nutr Rev. 2010;68:389–408. doi: 10.1111/j.1753-4887.2010.00299.x.PubMedCrossRefGoogle Scholar
  29. 29.
    Andersen V, Halfvarson J, Vogel U. Colorectal cancer in patients with inflammatory bowel disease: can we predict risk? World J Gastroenterol. 2012;18(31):4091–4. doi: 10.3748/wjg.v18.i31.4091.PubMedCrossRefGoogle Scholar
  30. 30.
    Sobhani I, Tap J, Roudot-Thoraval F, Roperch JP, Letulle S, Langella P, Corthier G, Van Nhieu JT, Furet JP. Microbial dysbiosis in colorectal cancer (CRC) patients. PLoS One. 2011;6(1):e16393. doi: 10.1371/journal.pone.0016393.PubMedCrossRefGoogle Scholar
  31. 31.
    Shen XJ, Rawls JF, Randall T, Burcal L, Mpande CN, Jenkins N, Jovov B, Abdo Z, Sandler RS, Keku TO. Molecular characterization of mucosal adherent bacteria and associations with colorectal adenomas. Gut Microbes. 2010;1:138–47. doi: 10.4161/gmic.1.3.12360.PubMedCrossRefGoogle Scholar
  32. 32.
    Jeffery IB, Claesson MJ, O'Toole PW, Shanahan F. Categorization of the gut microbiota: enterotypes or gradients? Nat Rev Microbiol. 2012;10(9):591–2. doi: 10.1038/nrmicro2859.PubMedCrossRefGoogle Scholar
  33. 33.
    Lagier JC, Armougom F, Million M, Hugon P, Pagnier I, Robert C, Bittar F, Fournous G, Gimenez G, Maraninchi M, Trape JF, Koonin EV, La Scola B, Raoult D. Microbial culturomics: paradigm shift in the human gut microbiome study. Clin Microbiol Infect Sep. 2012;4. doi: 10.1111/1469-0691.12023.
  34. 34.
    Shen D, Liu C, Xu R, Zhang F. Human gut microbiota: dysbiosis and manipulation. Front Cell Infect Microbiol. 2012;2:123. doi: 10.3389/fcimb.2012.00123.PubMedCrossRefGoogle Scholar
  35. 35.
    Ley RE, Peterson DA, Gordon JI. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell. 2006;124:837–48. doi: 10.1016/j.cell.2006.02.017.PubMedCrossRefGoogle Scholar
  36. 36.
    Salminen S, Isolauri E. Intestinal colonization, microbiota and probiotics. J Pediatr. 2006;149:115–20. doi: 10.1016/j.jpeds.2006.06.062.CrossRefGoogle Scholar
  37. 37.
    Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R. Diversity, stability and resilience of the human gut microbiota. Nature. 2012;489(7415):220–30. doi: 10.1038/nature11550.PubMedCrossRefGoogle Scholar
  38. 38.
    Ohland CL, Macnaughton WK. Probiotic bacteria and intestinal epithelial barrier function. Am J Physiol Gastrointest Liver Physiol. 2010;298(6):G807–19. doi: 10.1152/ajpgi.00243.2009.PubMedCrossRefGoogle Scholar
  39. 39.
    Mason KL, Huffnagle GB, Noverr MC, Kao JY (2008) Overview of gut immunology. In: Huffnagle GB, Noverr MC, (ed) GI microbiota and regulation of the immune system. Landes Bioscience and Springer Science Business Media: Austin, TX. pp 1–14.Google Scholar
  40. 40.
    Bischoff SC. Gut health: a new objective in medicine? BMC Med. 2011;9:24. doi: 10.1186/1741-7015-9-24.PubMedCrossRefGoogle Scholar
  41. 41.
    Preidis GA, Versalovic J. Targeting the human microbiome with antibiotics, probiotics, and prebiotics: gastroenterology enters the metagenomics era. Gastroenterology. 2009;136:2015–31. doi: 10.1053/j.gastro.2009.01.072.PubMedCrossRefGoogle Scholar
  42. 42.
    Round JL, Mazmanian SK. The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol. 2009;9:313–23. doi: 10.1038/nri2515.PubMedCrossRefGoogle Scholar
  43. 43.
    Jones BV, Begley M, Hill C, Gahan CG, Marchesi JR. Functional and comparative metagenomic analysis of bile salt hydrolase activity in the human gut microbiome. Proc Natl Acad Sci USA. 2008;105:13580–5. doi: 10.1073/pnas.0804437105.PubMedCrossRefGoogle Scholar
  44. 44.
    Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444:1027–31. doi: 10.1038/nature05414.PubMedCrossRefGoogle Scholar
  45. 45.
    Lilly DM, Stillwell RH. Probiotics growth promoting factors produced by microorganisms. Science. 1965;147:747–8. doi: 10.1126/science.147.3659.747.PubMedCrossRefGoogle Scholar
  46. 46.
    Ng SC, Hart AL, Kamm MA, Stagg AJ, Knight SC. Mechanisms of action of probiotics: recent advances. Inflamm Bowel Dis. 2009;15(2):300–10. doi: 10.1002/ibd.20602.PubMedCrossRefGoogle Scholar
  47. 47.
    Zuccotti GV, Meneghin F, Raimondi C, Dilillo D, Agostoni C, Riva E, Giovannini M. Probiotics in clinical practice: an overview. J Int Med Res. 2008;36(1):1–53. doi: 10.1038/sj.ejcn.1602718.CrossRefGoogle Scholar
  48. 48.
    De Preter V, Hamer HM, Windey K, Verbeke K. The impact of pre- and/or probiotics on human colonic metabolism: does it affect human health? Mol Nutr Food Res. 2011;55:46–57. doi: 10.1002/mnfr.201000451.PubMedCrossRefGoogle Scholar
  49. 49.
    Kumar M, Kumar A, Nagpal R, Mohania D, Behare P, et al. Cancer-preventing attributes of probiotics: an update. Int J Food Sci Nutr. 2010;61:473–96. doi: 10.3109/09637480903455971.PubMedCrossRefGoogle Scholar
  50. 50.
    Fotiadis CI, Stoidis CN, Spyropoulos BG, Zografos ED. Role of probiotics, prebiotics and synbiotics in chemoprevention for colorectal cancer. World J Gastroenterol. 2008;14:6453–7. doi: 10.3748/wjg.14.6453.PubMedCrossRefGoogle Scholar
  51. 51.
    van Zanten GC, Knudsen A, Röytiö H, Forssten S, Lawther M, et al. The effect of selected synbiotics on microbial composition and short-chain fatty acid production in a model system of the human colon. PLoS One. 2012;7(10):e47212. doi: 10.1371/journal.pone.0047212.PubMedCrossRefGoogle Scholar
  52. 52.
    Knackstedt RW, Moseley VR, Wargovich MJ (2012) Epigenetic mechanisms underlying diet-sourced compounds in the prevention and treatment of gastrointestinal cancer. Anticancer Agents Med Chem Aug 23.Google Scholar
  53. 53.
    Verghese M, Walker LT, Shackelford L, Chawan CB. Inhibitory effects of nondigestible carbohydrates of different chain lengths on azoxymethane-induced aberrant crypt foci in Fisher 344 rats. Nutr Res. 2005;25:859–68. doi: 10.1016/j.nutres.2005.09.007.CrossRefGoogle Scholar
  54. 54.
    Roller M, Femia AP, Caderni G, Rechkemmer G, Watzl B. Intestinal immunity of rats with colon cancer is modulated by oligofructose-enriched inulin combined with Lactobacillus rhamnosus and Bifidobacterium lactis. Brit J Nutr. 2004;92:931–8. doi: 10.1079/BJN20041289.PubMedCrossRefGoogle Scholar
  55. 55.
    Uronis JM, Muhlbauer M, Herfarth HH, Rubinas TC, Jones GS, Jobin C. Modulation of the intestinal microbiota alters colitis-associated colorectal cancer susceptibility. PLoS One. 2009;4:e6026. doi: 10.1371/journal.pone.0006026.PubMedCrossRefGoogle Scholar
  56. 56.
    Kasmi G, Andoni R, Mano V, Kraja D, Muço E, Kasmi I. Streptococcus bovis isolated in haemoculture a signal of malignant lesion of the colon. Clin Lab. 2011;57(11–12):1007–9.PubMedGoogle Scholar
  57. 57.
    Nakamura J, Kubota Y, Miyaoka M, Saitoh T, Mizuno F, Benno Y. Comparison of four microbial enzymes in Clostridia and Bacteroides isolated from human feces. Microbiol Immunol. 2002;46:487–90.PubMedGoogle Scholar
  58. 58.
    Strofilas A, Lagoudianakis EE, Seretis C, Pappas A, Koronakis N, Keramidaris D, Koukoutsis I, Chrysikos I, Manouras I, Manouras A. Association of Helicobacter pylori infection and colon cancer. J Clin Med Res. 2012;4(3):172–6. doi: 10.4021/jocmr880w.PubMedGoogle Scholar
  59. 59.
    Chang JH, Shim YY, Cha SK, Reaney MJ, Chee KM. Effect of Lactobacillus acidophilus KFRI342 on the development of chemically induced precancerous growths in the rat colon. J Med Microbiol. 2012;61(3):361–8. doi: 10.1099/jmm.0.035154-0.PubMedCrossRefGoogle Scholar
  60. 60.
    Foo NP, Ou Yang H, Chiu HH, Chan HY, Liao CC, Yu CK, Wang YJ. Probiotics prevent the development of 1,2-dimethylhydrazine (DMH)-induced colonictumorigenesis through suppressed colonic mucosa cellular proliferation and increased stimulation of macrophages. J Agric Food Chem. 2011;59(24):13337–45. doi: 10.1021/jf203444d.PubMedCrossRefGoogle Scholar
  61. 61.
    Rafter J, Bennett M, Caderni G, et al. Dietary synbiotics reduce cancer risk factors in polypectomized and colon cancer patients. Am J Clin Nutr. 2007;85:488–96.PubMedGoogle Scholar
  62. 62.
    De Vuyst L, Leroy F. Bacteriocins from lactic acid bacteria: production, purification, and food applications. J Mol Microbiol Biotechnol. 2007;13(4):194–9. doi: 10.1159/000104752.PubMedCrossRefGoogle Scholar
  63. 63.
    Kim Y, Lee D, Kim D, Cho J, Yang J, Chung M, Kim K, Ha N. Inhibition of proliferation in colon cancer cell lines and harmful enzyme activity of colon bacteria by Bifidobacterium adolescentis SPM0212. Arch Pharm Res. 2008;31(4):468–73. doi: 10.1007/s12272-001-1180-y.PubMedCrossRefGoogle Scholar
  64. 64.
    Baricault L, Denariaz G, Houri JJ, Bouley C, Sapin C, Trugnan G. Use of HT-29, a cultured human colon cancer cell line, to study the effect of fermented milks on colon cancer cell growth and differentiation. Carcinogenesis. 1995;16:245–52. doi: 10.1093/carcin/16.2.245.PubMedCrossRefGoogle Scholar
  65. 65.
    Biffi A, Coradini D, Larsen R, Riva L, Di Fronzo G. Antiproliferative effect of fermented milk on the growth of a human breast cancer cell line. Nutr Canc. 1997;28:93–9. doi: 10.1080/01635589709514558.CrossRefGoogle Scholar
  66. 66.
    Arimochi H, Kinouchi T, Kataoka K, Kuwahara T, Ohnishi Y. Effect of intestinal bacteria on formation of azoxymethane-induced aberrant crypt foci in the rat colon. Biochem Biophys Res Commun. 1997;238:753–7. doi: 10.1006/bbrc.1997.7384.PubMedCrossRefGoogle Scholar
  67. 67.
    Reddy BS. Prevention of colon cancer by pre- and probiotics: evidence from laboratory studies. Br J Nutr. 1998;80:219–23.Google Scholar
  68. 68.
    Azcarate Peril MA, Tallon R, Klaenhammer TR. Temporal gene expression and probiotic attributes of Lactobacillus acidophilus during growth in milk. J Dairy Sci. 2009;92:870–86. doi: 10.3168/jds.2008-1457.PubMedCrossRefGoogle Scholar
  69. 69.
    Khalil R. Evidence for probiotic potential of a capsular-producing Streptococcus thermophilus CHCC 3534 strain. Pol J Microbiol. 2009;58:49–55.PubMedCrossRefGoogle Scholar
  70. 70.
    Tallon R, Arias S, Bressollier P, Urdaci MC. Strain and matrix dependent adhesion of Lactobacillus plantarum is mediated by proteinaceous bacterial compounds. J Appl Microbiol. 2007;102:442–51. doi: 10.1111/j.1365-2672.2006.03086.x.PubMedCrossRefGoogle Scholar
  71. 71.
    Servin AL, Coconnier MH. Adhesion of probiotic strains to the intestinal mucosa and interaction with pathogens. Best Pract Res Clin Gastroenterol. 2003;17:741–54. doi: 10.1016/S1521-6918(03)00052-0.PubMedCrossRefGoogle Scholar
  72. 72.
    Lievin LE, Moal V, Servin AL. The front line of enteric host defense against unwelcome intrusion of harmful microorganisms: mucins, antimicrobial peptides, and microbiota. Clin Microbiol Rev. 2006;19:315–37. doi: 10.1128/CMR.19.2.315-337.2006.CrossRefGoogle Scholar
  73. 73.
    Candela M, Perna F, Carnevali P, Vitali B, Ciati R, Gionchetti P, Rizzello F, Campieri M, Brigidi P. Interaction of probiotic Lactobacillus and Bifidobacterium strains with human intestinal epithelial cells: adhesion properties, competition against enteropathogens and modulation of IL-8 production. Int J Food Microbiol. 2008;125:286–92. doi: 10.1016/j.ijfoodmicro.2008.04.012.PubMedCrossRefGoogle Scholar
  74. 74.
    Collado MC, Isolauri E, Salminen S. Specific probiotic strains and their combinations counteract adhesion of Enterobacter sakazakii to intestinal mucus. FEMS Microbiol Lett. 2008;285:58–64. doi: 10.1111/j.1574-6968.2008.01211.x.PubMedCrossRefGoogle Scholar
  75. 75.
    Ruas-Madiedo P, Gueimonde M, Margolles A, de los Reyes-Gavilan CG, Salminen S. Exopolysaccharides produced by probiotic strains modify the adhesion of probiotics and enteropathogens to human intestinal mucus. J Food Prot. 2006;69:2011–5.PubMedGoogle Scholar
  76. 76.
    Sekine K, Toida T, Saito M, Kuboyama M, Kawashima T, Hashimoto Y. A new morphologically characterized cell wall preparation (whole peptidoglycan) from Bifidobacterium infantis with a higher efficacy on the regression of an established tumor in mice. Cancer Res. 1985;45:1300–7.PubMedGoogle Scholar
  77. 77.
    Matsuzaki T. Immunomodulation by treatment with Lactobacillus casei strain Shirota. Int J Food Microbiol. 1998;41:133–40. doi: 10.1016/S0168-1605(98)00046-4.PubMedCrossRefGoogle Scholar
  78. 78.
    Lee JW, Shin JG, Kim EH, Kang HE, Yim IB, Kim JY, Joo HG, Woo HJ. Immunomodulatory and antitumor effects in vivo by the cytoplasmic fraction of Lactobacillus casei and Bifidobacterium longum. J Vet Sci. 2004;5:41–8.PubMedGoogle Scholar
  79. 79.
    Sun J, Shi YH, Le GW, Ma XY. Distinct immune response induced by peptidoglycan derived from Lactobacillus sp. World J Gastroenterol. 2005;11:6330–7.PubMedGoogle Scholar
  80. 80.
    Ghoneum M, Hamilton J, Brown J, Gollapudi S. Human squamous cell carcinoma of the tongue and colon undergoes apoptosis upon phagocytosis of Saccharomyces cerevisiae, the baker's yeast, in vitro. Anticancer Res. 2005;25:981–9.PubMedGoogle Scholar
  81. 81.
    Ghoneum M, Gollapudi S. Induction of apoptosis in breast cancer cells by Saccharomyces cerevisiae, the baker's yeast, in vitro. Anticancer Res. 2004;24:1455–63.PubMedGoogle Scholar
  82. 82.
    Liong MT. Roles of probiotics and prebiotics in colon cancer prevention: Postulated mechanisms and in-vivo evidence. Int J Mol Sci. 2008;9:854–63. doi: 10.3390/ijms9050854.PubMedCrossRefGoogle Scholar
  83. 83.
    Guengerich FP. Cytochromes P450, drugs, and diseases. Mol Interv. 2003;3:194–204. doi: 10.1124/mi.3.4.194.PubMedCrossRefGoogle Scholar
  84. 84.
    Linsalata M, Notarnicola M, Tutino V, Bifulco M, Santoro A, Laezza C, Messa C, Orlando A, Caruso MG. Effects of anandamide on polyamine levels and cell growth in human colon cancer cells. Anticancer Res. 2010;30(7):2583–9.PubMedGoogle Scholar
  85. 85.
    Linsalata M, Russo F, Cavallini A, Berloco P, Di Leo A. Polyamines, diamine oxidase, and ornithine decarboxylase activity in colorectal cancer and in normal surrounding mucosa. Dis Colon Rectum. 1993;36(7):662–7. doi: 10.1007/BF02238593.PubMedCrossRefGoogle Scholar
  86. 86.
    Linsalata M, Russo F, Berloco P, Valentini AM, Caruso ML, et al. Effects of probiotic bacteria (VSL#3) on the polyamine biosynthesis and cell proliferation of normal colonic mucosa of rats. In Vivo. 2005;19:989–95.PubMedGoogle Scholar
  87. 87.
    Orlando A, Messa C, Linsalata M, Cavallini A, Russo F. Effects of Lactobacillus rhamnosus GG on proliferation and polyamine metabolism in HGC-27 human gastric and DLD-1 colonic cancer cell lines. Immunopharmacol Immunotoxicol. 2009;31:108–16. doi: 10.1080/08923970802443631.PubMedCrossRefGoogle Scholar
  88. 88.
    Linsalata M, Cavallini A, Messa C, Orlando A, Refolo MG, et al. Lactobacillus rhamnosus GG influences polyamine metabolism in HGC-27 gastric cancer cell line: a strategy toward nutritional approach to chemoprevention of gastric cancer. Curr Pharm Des. 2010;16:847–53. doi: 10.2174/138161210790883598.PubMedCrossRefGoogle Scholar
  89. 89.
    Ouyang L, Shi Z, Zhao S, Wang FT, Zhou TT, Liu B, Bao JK. Programmed cell death pathways in cancer: a review of apoptosis, autophagy and programmed necrosis. Cell Prolif Oct. 2012;3. doi: 10.1111/j.1365-2184.2012.00845.x.
  90. 90.
    Call JA, Eckhardt SG, Camidge DR. Targeted manipulation of apoptosis in cancer treatment. Lancet Oncol. 2008;9(10):1002–11. doi: 10.1016/S1470-2045(08)70209-2.PubMedCrossRefGoogle Scholar
  91. 91.
    Pagnini C, Corleto VD, Hoang SB, Saeed R, Cominelli F, Delle Fave G. Commensal bacteria and "Oncologic Surveillance" suggestions from an experimental model. J Clin Gastroenterol. 2008;42(3):193–6. doi: 10.1097/MCG.0b013e31817f1284.CrossRefGoogle Scholar
  92. 92.
    Orlando A, Refolo MG, Messa C, Amati L, Lavermicocca P, Guerra V, Russo F. 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 Canc. 2012;64(7):1103–11. doi: 10.1080/01635581.2012.717676.CrossRefGoogle Scholar
  93. 93.
    Lee NK, Park JS, Park E, Paik HD. Adherence and anticarcinogenic effects of Bacillus polyfermenticus SCD in the large intestine. Lett Appl Microbiol. 2007;44:274–8. doi: 10.1111/j.1472-765X.2006.02078.x.PubMedCrossRefGoogle Scholar
  94. 94.
    Kim Y, Lee D, Kim D, Cho J, Yang J, Chung M, Kim K, Ha N. Inhibition of proliferation in colon cancer cell lines and harmful enzyme activity of colon bacteria by Bifidobacterium adolescentis SPM0212. Arch Pharm Res. 2008;31:467–8. doi: 10.1007/s12272-001-1180-y.Google Scholar
  95. 95.
    Linsalata M, Russo F, Berloco P, Caruso ML, Di Matteo G, et al. The influence of Lactobacillus brevis on ornithine decarboxylase activity and polyamine profiles in Helicobacter pylori-infected gastric mucosa. Helicobacter. 2004;9:165–72. doi: 10.1111/j.1083-4389.2004.00214.x.PubMedCrossRefGoogle Scholar
  96. 96.
    Park SK, Park DI, Choi JS, Kang MS, Park JH, et al. The effect of probiotics on Helicobacter pylori eradication. Hepatogastroenterology. 2007;54:2032–6. doi: 10.1016/S0016-5085(10)61543-0.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2012

Authors and Affiliations

  1. 1.Laboratory of Experimental Biochemistry, National Institute for Digestive Diseases, I.R.C.C.S. “S. de Bellis”Castellana GrotteItaly

Personalised recommendations