Bifidobacterially produced, C18:3 and C18:4 conjugated fatty acids exhibit in vitro anti-carcinogenic and anti-microbial activity

European Journal of Lipid Science and Technology

Volumn 118, Issue 11, 2016, Pages 1743-1758

  Hennessy, Alan A ^a,b   Ross, Paul ^a   Devery, Rosaleen ^b   Stanton, Catherine ^a  

^a TEAGASC FOOD RESEARCH CENTRE   (Ireland)

^b DUBLIN CITY UNIVERSITY   (Ireland)

Author keywords

ALA; Anti microbial; Cancer; Conjugated; GLA

Indexed keywords

EID: 84961266439     PISSN: 14387697     EISSN: 14389312     Source Type: Journal    
DOI: 10.1002/ejlt.201500424     Document Type: Article

References (82)

1. Stanton, C., Murphy, J., Mcgrath, E., Devery, R., in: Sebedio, J. L., Christie, W. W., Adlof, R., (Eds.), Animal Feeding Strategies for Conjugated Linoleic Acid Enrichment of Milk, in Advances in Conjugated Linoleic Acid Research, AOCS Press, Champaign, IL 2003, p. 123–145.
2. Dhiman, T. R., Nam, S. H., Ure, A. L., Factors affecting conjugated linoleic acid content in milk and meat. Crit. Rev. Food Sci. Nutr. 2005, 45, 463–482.
3. Hennessy, A. A., Devery, R., Ross, R. P., Stanton, C., The health promoting properties of the conjugated isomers of a-linolenic acid. Lipids 2011, 46, 105–119.
4. Wise, M. L., Hamberg, M., Gerwick, W. H., Biosynthesis of conjugated triene-containing fatty acids by a novel isomerase from the red marine alga Ptilota filicina. Biochemistry 1994, 33, 15223–15232.
5. Lopez, A., Gerwick, W. H., Two new icosapentaenoic acids from the temperate red seaweed Ptilota filicina J. Agardh. Lipids 1987, 22, 190–194.
6. Burgess, J. R., de la Rossa, R. I., Jacobs, R. S., Butler, A., A new eicosapentaenoic acid formed from arachidonic acid in cralline red algae Bossiella orbigniana. Lipids 1991, 26, 162–165.
7. Mikhailova, M. V., Bemis, D. L., Wise, M. L., Gerwick, W. H., et al., Structure and biosynthesis of novel conjugated polyene fatty acids from the marine green alga Anadyomene stellata. Lipids 1995, 30, 583–589.
8. Hennessy, A. A., Ross, R. P., Stanton, C., Devery, R., in: Saarela, M. (Eds.), Development of dairy based functional foods enriched in conjugated linoleic acid with special reference to rumenic acid, in Functional Dairy Products, Woodhead Publishing Limit ed, Cambridge, England 2007, p. 443–495.
9. Sieber, R., Collomb, M., Aeschlimann, A., Jelen, P., Eyer, H., Impact of microbial cultures on conjugated linoleic acid in dairy products—A review. Int. Dairy J. 2004, 14, 1–15.
10. Coakley, M., Banni, S., Johnson, M. C., Mills, S., et al., Inhibitory effect of conjugated α-linolenic acid (CALA) from bifidobacteria of intestinal origin on SW480 cancer cells. Lipids 2009, 44, 249–256.
11. Hennessy, A. A., Barrett, E., Ross, R. P., Fitzgerald, G. F., et al., The production of conjugated alpha-linolenic, gamma-linolenic and stearidonic acids by strains of bifidobacteria and propionibacteria. Lipids 2012, 47, 313–327.
12. Kishino, S., Ogawa, J., Ando, A., Yokozeki, K., Shimizu, S., Microbial production of conjugated gamma-linolenic acid from gamma-linolenic acid by Lactobacillus plantarum AKU 1009a. J. Appl. Microbiol. 2009, 108, 2012–2018.
13. Ogawa, J., Kishino, S., Ando, A., Sugimoto, S., et al., Production of conjugated fatty acids by lactic acid bacteria. J. Biosci. Bioeng. 2005, 100, 355–364.
14. Bhattacharya, A., Banu, J., Rahman, M., Causey, J., Fernandes, G., Biological effects of conjugated linoleic acids in health and disease. J. Nutr. Biochem. 2006, 17, 789–810.
15. Wahle, K. W., Heys, S. D., Rotondo, D., Conjugated linoleic acids: Are they beneficial or detrimental to health? Prog. Lipid Res. 2004, 43, 553–587.
16. Tanaka, T., Effect of diet on human carcinogenesis. Crit. Rev. Oncol. Hematol. 1997, 25, 73–95.
17. Shike, M., Winawer, S. J., Greenwald, P. H., Bloch, A., et al., Primary prevention of colorectal cancer. The WHO collaborating centre for the prevention of colorectal cancer. Bull. World Health Organ. 1990, 68, 377–385.
18. Beppu, F., Hosokawa, M., Tanaka, L., Kohno, H., et al., Potent inhibitory effect of trans 9, trans 11 isomer of conjugated linoleic acid on the growth of human colon cancer cells. J. Nutr. Biochem. 2006, 17, 830–836.
19. Kohno, H., Suzuki, R., Yasui, Y., Hosokawa, M., et al., Pomegranate seed oil rich in conjugated linolenic acid suppresses chemically induced colon carcinogenesis in rats. Cancer Sci. 2004, 95, 481–486.
20. Ewaschuk, J. B., Walker, J. W., Diaz, H., Madsen, K. L., Bioproduction of conjugated linoleic acid by probiotic bacteria occurs in vitro and in vivo in mice. J.Nutr. 2006, 136, 1483–1487.
21. Coakley, M., Ross, R. P., Nordgren, M., Fitzgerald, G., et al., Conjugated linoleic acid biosynthesis by human-derived Bifidobacterium species. J. Appl. Microbiol. 2003, 94, 138–145.
22. Barrett, E., Ross, R. P., Fitzgerald, G. F., Stanton, C., Rapid screening method for analyzing the conjugated linoleic acid production capabilities of bacterial cultures. Appl. Environ. Microbiol. 2007, 73, 2333–2337.
23. Oh, D. K., Hong, G. H., Lee, Y., Min, S., et al., Production of conjugated linoleic acid by isolated Bifidobacterium strains. World J. Microbiol. Biotechnol. 2003, 19, 907–912.
24. Wall, R., Ross, R. P., Shanahan, F., O'Mahony, L., et al., The metabolic activity of the enteric microbiota influences the fatty acid composition of murine and porcine liver and adipose tissues. Am. J. Clin. Nutr. 2009, 89, 1393–1401.
25. Kodicek, E., The effect of unsaturated fatty acids on gram-positive bacteria. Soc. Exp. Biol. Symp. 1949, 3, 217–232.
26. Sun, C. Q., O'Connor, C. J., Roberton, A. M., Antibacterial actions of fatty acids and monoglycerides against Helicobacter pylori. FEMS Immunol. Med. Microbiol. 2003, 36, 9–17.
27. Lee, J. Y., Kim, Y. S., Shin, D. H., Antimicrobial synergistic effect of linolenic acid and monoglyceride against Bacillus cereus and Staphylococcus aureus. J. Agric. Food Chem. 2002, 50, 2193–2199.
28. Giamarellos-Bourboulis, E. J., Grecka, P., Dionyssiou-Asteriou, A., Giamarellou, H., In-vitro inhibitory activity of gamma-linolenic acid on Escherichia coli strains and its influence on their susceptibilities to various antimicrobial agents. J. Antimicrob. Chemother. 1995, 36, 327–334.
29. Knapp, H. R., Melly, M. A., Bactericidal effects of polyunsaturated fatty acids. J. Infect. Dis. 1986, 154, 84–94.
30. Greenway, D. L., Dyke, K. G., Mechanism of the inhibitory action of linoleic acid on the growth of Staphylococcus aureus. J. Gen. Microbiol. 1979, 115, 233–245.
31. Kenny, J. G., Ward, D., Josefsson, E., Jonsson, I. M., et al., The Staphylococcus aureus response to unsaturated long chain free fatty acids: Survival mechanisms and virulence implications. PLoS ONE 2009, 4, e4344.
32. Chajès, V., Sattler, W., Stranzl, A., Kostner, G. M., Influence of n-3 fatty acids on the growth of human breast cancer cells in vitro: Relationship to peroxides and Vitamin-E. Breast Cancer Res. Treat. 1995, 34, 199–212.
33. Durgam, V. R., Fernandes, G., The growth inhibitory effect of conjugated linoleic acid on MCF-7 cells is related to estrogen response system. Cancer Lett. 1997, 116, 121–130.
34. Igarashi, M., Miyazawa, T., Do conjugated eicosapentaenoic acid and conjugated docosahexaenoic acid induce apoptosis via lipid peroxidation in cultured human tumor cells? Biochem. Biophys. Res. Commun. 2000, 270, 649–656.
35. Folch, J., Lees, M., Sloane Stanley, G. H., A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 1957, 226, 497–509.
36. Bondia-Pons, I., Morera-Pons, S., Castellote, A. I., Lopez-Sabater, M. C., Determination of phospholipid fatty acids in biological samples by solid-phase extraction and fast gas chromatography. J. Chromatogr. A. 2006, 1116, 204–208.
37. Park, P. W., Goins, R. E., In situ preparation of fatty acid methyl esters for analysis of fatty acid composition in foods. J. Food Sci. 1994, 59, 1262–1266.
38. Childs, S., Hennessy, A. A., Sreenan, J. M., Wathes, D. C., et al., Effect of level of dietary n-3 polyunsaturated fatty acid supplementation on systemic and tissue fatty acid concentrations and on selected reproductive variables in cattle. Theriogenology 2008, 70, 595–611.
39. Lacey, R. W., Lord, V. L., Sensitivity of staphylococci to fatty acids: Novel inactivation of linolenic acid by serum. J. Med. Microbiol. 1981, 14, 41–49.
40. Das, U. N., Gamma-linolenic acid therapy of human glioma—A review of in vitro, in vivo, and clinical studies. Med. Sci. Monit. 2007, 13, RA119–RA131.
41. Hrelia, S., Pession, A., Buda, R., Lorenzini, A., et al., Concentration- and time-dependent effects of gamma-linolenic acid supplementation to tumor cells in culture. Prostaglandins Leukot. Essent. Fatty Acids 1999, 60, 235–241.
42. Hrelia, S., Bordoni, A., Biagi, P., Rossi, C. A., et al., Gamma-Linolenic acid supplementation can affect cancer cell proliferation via modification of fatty acid composition. Biochem. Biophys. Res. Commun. 1996, 225, 441–447.
43. Kong, X., Ge, H., Hou, L., Shi, L., Liu, Z., Induction of apoptosis in K562/ADM cells by gamma-linolenic acid involves lipid peroxidation and activation of caspase-3. Chem. Biol. Interact. 2006, 162, 140–148.
44. Das, U. N., From bench to the clinic: Gamma-linolenic acid therapy of human gliomas. Prostaglandins Leukot. Essent. Fatty Acids 2004, 70, 539–552.
45. Petrik, M. B., McEntee, M. F., Johnson, B. T., Obukowicz, M. G., Whelan, J., Highly unsaturated (n-3) fatty acids, but not alpha-linolenic, conjugated linoleic or gamma-linolenic acids, reduce tumorigenesis in Apc(Min/+) mice. J. Nutr. 2000, 130, 2434–2443.
46. Cantrill, R. C., Huang, Y. S., Ells, G. W., Horrobin, D. F., Comparison of the metabolism of alpha-linolenic acid and its delta 6 desaturation product, stearidonic acid, in cultured NIH-3T3 cells. Lipids 1993, 28, 163–166.
47. Whelan, J., Dietary stearidonic acid is a long chain (n-3) polyunsaturated fatty acid with potential health benefits. J. Nutr. 2009, 139, 5–10.
48. Shimizu, M., Deguchi, A., Lim, J. T., Moriwaki, H., et al., (−)—Epigallocatechin gallate and polyphenon E inhibit growth and activation of the epidermal growth factor receptor and human epidermal growth factor receptor-2 signaling pathways in human colon cancer cells. Clin. Cancer Res. 2005, 11, 2735–2746.
49. Yasui, Y., Hosokawa, M., Kohno, H., Tanaka, T., Miyashita, K., Troglitazone and 9cis,11trans,13trans-conjugated linolenic acid: Comparison of their antiproliferative and apoptosis-inducing effects on different colon cancer cell lines. Chemotherapy 2006, 52, 220–225.
50. Cai, F., Dupertuis, Y. M., Pichard, C., Role of polyunsaturated fatty acids and lipid peroxidation on colorectal cancer risk and treatments. Curr. Opin. Clin. Nutr. Metab. Care 2012, 15, 99–106.
51. Suzuki, R., Noguchi, R., Ota, T., Abe, M., et al., Cytotoxic effect of conjugated trienoic fatty acids on mouse tumor and human monocytic leukemia cells. Lipids 2001, 36, 477–482.
52. Bagga, D., Capone, S., Wang, H. J., Heber, D., et al., Dietary modulation of omega-3/omega-6 polyunsaturated fatty acid ratios in patients with breast cancer. J. Natl. Cancer Inst. 1997, 89, 1123–1131.
53. Aronson, W. J., Glaspy, J. A., Reddy, S. T., Reese, D., et al., Modulation of omega-3/omega-6 polyunsaturated ratios with dietary fish oils in men with prostate cancer. Urology 2001, 58, 283–288.
54. Karmali, R. A., Eicosanoids in neoplasia. Prev. Med. 1987, 16, 493–502.
55. Lupulescu, A., Prostaglandins, their inhibitors and cancer. Prostaglandins Leukot. Essent. Fatty Acids 1996, 54, 83–94.
56. Tsuzuki, T., Kambe, T., Shibata, A., Kawakami, Y., et al., Conjugated EPA activates mutant p53 via lipid peroxidation and induces p53-dependent apoptosis in DLD-1 colorectal adenocarcinoma human cells. Biochim. Biophys. Acta. 2007, 1771, 20–30.
57. Tsuzuki, T., Igarashi, M., Miyazawa, T., Conjugated eicosapentaenoic acid (EPA) inhibits transplanted tumor growth via membrane lipid peroxidation in nude mice. J. Nutr. 2004, 134, 1162–1166.
58. Tsuzuki, T., Tokuyama, Y., Igarashi, M., Miyazawa, T., Tumor growth suppression by alpha-eleostearic acid, a linolenic acid isomer with a conjugated triene system, via lipid peroxidation. Carcinogenesis 2004, 25, 1417–1425.
59. Yasui, Y., Hosokawa, M., Sahara, T., Suzuki, R., et al., Bitter gourd seed fatty acid rich in 9c,11t,13t-conjugated linolenic acid induces apoptosis and up-regulates the GADD45, p53 and PPARgamma in human colon cancer Caco-2 cells. Prostaglandins Leukot. Essent. Fatty Acids 2005, 73, 113–119.
60. Yasui, Y., Hosokawa, M., Kohno, H., Tanaka, T., Miyashita, K., Growth inhibition and apoptosis induction by all-trans-conjugated linolenic acids on human colon cancer cells. Anticancer Res. 2006, 26, 1855–1860.
61. Miller, A., Stanton Devery, C. R., Cis 9, trans 11- and trans 10, cis 12-conjugated linoleic acid isomers induce apoptosis in cultured SW480 cells. Anticancer Res. 2002, 22, 3879–3887.
62. Reed, J. C., Bcl-2 and the regulation of programmed cell death. J. Cell. Biol. 1994, 124, 1–6.
63. Russell, D. A., Ross, R. P., Fitzgerald, G. F., Stanton, C., Metabolic activities and probiotic potential of bifidobacteria. Int. J. Food Microbiol. 2011, 149, 88–105.
64. O'Shea, E. F., Cotter, P. D., Stanton, C., Ross, R. P., Hill, C., Production of bioactive substances by intestinal bacteria as a basis for explaining probiotic mechanisms: Bacteriocins and conjugated linoleic acid. Int. J. Food Microbiol. 2011, 152, 189–205.
65. Morelli, L., Postnatal development of intestinal microflora as influenced by infant nutrition. J. Nutr. 2008, 138, 1791S–1795S.
66. Lesniewska, V., Rowland, I., Laerke, H. N., Grant, G., Naughton, P. J., Relationship between dietary-induced changes in intestinal commensal microflora and duodenojejunal myoelectric activity monitored by radiotelemetry in the rat in vivo. Exp. Physiol. 2006, 91, 229–237.
67. McCormick, J. K., Yarwood, J. M., Schlievert, P. M., Toxic shock syndrome and bacterial superantigens: An update. Annu. Rev. Microbiol. 2001, 55, 77–104.
68. Fischetti, V., Gram Positive Pathogens. ASM Press, Washington, DC 2000. p. 307–470.
69. Karchmer, A. W., Nosocomial bloodstream infections: Organisms, risk factors, and implications. Clin. Infect. Dis. 2000, 31, S139–S143.
70. EARSS, EARSS Annual Report 2006. European Antimicrobial Resistance Surveillance System. 54–58.
71. Kelsey, J. A., Bayles, K. W., Shafii, B., McGuire, M. A., Fatty acids and monoacylglycerols inhibit growth of Staphylococcus aureus. Lipids 2006, 41, 951–961.
72. Chamberlain, N. R., Mehrtens, B. G., Xiong, Z., Kapral, F. A., et al. Correlation of carotenoid production, decreased membrane fluidity, and resistance to oleic acid killing in Staphylococcus aureus 18Z. Infect. Immun. 1991, 59, 4332–4337.
73. Pande, S. V., Mead, J. F., Inhibition of enzyme activities by free fatty acids. J. Biol. Chem. 1968, 243, 6180–6185.
74. Sievert, D. M., Rudrik, J. T., Patel, J. B., McDonald, L. C., et al., Vancomycin-resistant Staphylococcus aureus in the United States, 2002–2006. Clin. Infect. Dis. 2008, 46, 668–674.
75. Fusillo, M. H., Pulaski, E. J., Reiss, E., Kuhns, D. M., Staphylococcus aureus simultaneously resistant to penicillin and the broad spectrum antibiotics. Surg. Forum. 1953, 38, 241–245.
76. Plourde, M., Sergiel, J. P., Chardigny, J. M., Gregoire, S., et al., Absorption and metabolism of conjugated alpha-linolenic acid given as free fatty acids or triacylglycerols in rats. Nutr. Metab. (Lond) 2006, 3, 8.
77. Tsuzuki, T., Kawakami, Y., Abe, R., Nakagawa, K., et al., Conjugated linolenic acid is slowly absorbed in rat intestine, but quickly converted to conjugated linoleic acid. J. Nutr. 2006, 136, 2153–2159.
78. Burdge, G. C., Calder, P. C., Conversion of alpha-linolenic acid to longer-chain polyunsaturated fatty acids in human adults. Reprod. Nutr. Dev. 2005, 45, 581–597.
79. Venkateshwari, A., Krishnaveni, D., Venugopal, S., Shashikumar, P., et al., Helicobacter pylori infection in relation to gastric cancer progression. Indian J. Cancer 2011, 48, 94–98.
80. Wroblewski, L. E., Peek, R. M., Jr., Wilson, K. T., Helicobacter pylori and gastric cancer: Factors that modulate disease risk. Clin. Microbiol. Rev. 2010, 23, 713–739.
81. Xu, S., Boylston, T. D., Glatz, B. A., Effect of lipid source on probiotic bacteria and conjugated linoleic acid formation in milk model systems. J. Am. Oil Chem. Soc. 2004, 81, 589–595.
82. Xu, S., Boylston, T. D., Glatz, B. A., Conjugated linoleic acid content and organoleptic attributes of fermented milk products produced with probiotic bacteria. J. Agric. Food Chem. 2005, 53, 9064–9072.