Abstract
The use of probiotics, alone or in interaction with bile acids, is a modern strategy in the prevention and treatment of hypercholesterolemia. Numerous mechanisms for hypocholesterolemic effect of probiotics have been hypothesized, based mostly on in vitro evidence. Interaction with bile acids through reaction of deconjugation catalyzed by bile salt hydrolase enzymes (BSH) is considered as the main mechanism of cholesterol-lowering effects of probiotic bacteria, but it has been reported that microbial BSH activity could be potentially detrimental to the human host. There are several approaches for prevention of possible side effects associated with BSH activity, which at the same time increase the viability of probiotics in the intestines and also in food matrices. The aim of our study was to summarize present knowledge of probiotics—bile acids interactions, with special reference to cholesterol-lowering mechanisms of probiotics, and to report novel biotechnological approaches for increasing the pharmacological benefits of probiotics.
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References
Joint FAO/WHO Expert Consultation on evaluation of health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria, Geneva, 2001. Available from: http://www.who.int/foodsafety/publications/fs_management/en/probiotics.pdf. Accessed 24 August 2011.
Hezcko, P. B., Strus, M., & Kochan, P. (2006). Journal of Physiology and Pharmacology, 57, 5–12.
Brunser, O., & Gotteland, M. (2010). In: R. R. Watson, V. R. Preedy (Eds.), Bioactive foods in promoting health: probiotics and prebiotics (pp. 73–93). London: Elsevier
Iannitti, T., & Palmieri, B. (2010). Clinical Nutrition, 29(6), 701–725.
Wilson, M. (2005). In: M. Wilson (Ed.), Microbial inhabitants of humans: their ecology and role in health and disease (pp. 395–419). Cambridge: Cambridge University Press
Joint FAO/WHO Working Group report on drafting guidelines for the evaluation of probiotics in food. London, Ontario, Canada, 2002. Available from: http://www.who.int/foodsafety/fs_management/en/probiotic_guidelines.pdf. Accessed 24 August 2011.
Williams, N. T. (2010). American Journal of Health-System Pharmacy, 67(6), 449–458.
Goldin, B. R., & Gorbach, S. L. (2008). Clinical Infectious Diseases, 46, S96–S100.
Deshpande, G., Rao, S., & Patole, S. (2011). Current Opinion in Gastroenterology, 27(1), 13–18.
Mercenier, A., Pavan, S., & Pot, B. (2003). Current Pharmaceutical Design, 9(2), 175–191.
Mercenier, A., Lenoir-Wijnkoop, I., & Sanders, M. E. (2008). Bulletin of the International Dairy Federation, 429, 2–6.
Rijkers, G. T., Bengmark, S., Enck, P., Haller, D., Herz, U., Kalliomaki, M., et al. (2010). Journal of Nutrition, 140(3), 671S–676S.
Kaushik, J. K., Kumar, A., Duary, R. K., Mohanty, A. K., Grover, S., & Batish, V. K. (2009). PloS One, 4(12), e8099.
Land, M. H., Rouster-Stevens, K., Woods, C. R., Cannon, M. L., Cnota, J., & Shetty, A. K. (2005). Pediatrics, 115(1), 178–181.
Huys, G., D'Haene, K., & Swings, J. (2006). Antimicrobial Agents and Chemotherapy, 50(4), 1550–1551.
Al-Salami, H., Butt, G., Tucker, I., Golocorbin-Kon, S., & Mikov, M. (2011). European Journal of Drug Metabolism and Pharmacokinetics, doi: 10.1007/s13318-011-0060-y.
Al-Salami, H., Butt, G., Fawcet, J. P., Tucker, I., Golocorbin-Kon, S., & Mikov, M. (2008). European Journal of Drug Metabolism and Pharmacokinetics, 33(2), 101–106.
Pigeon, R. M., Cuesta, E. P., & Gillilliand, S. E. (2002). Journal of Dairy Science, 85(11), 2705–2710.
Mikov, M., Fawcett, J. P., Kuhajda, K., & Kevresan, S. (2007) In: M. Mikov, J. P. Fawcett (Eds.), Bile acids: chemistry, biosynthesis, analysis, chemical and metabolic transformations (pp. 179–203). Geneva: Mediset Publisher
Al-Salami, H., Butt, G., Tucker, I., & Mikov, M. (2008). Methods and Findings in Experimental and Clinical Pharmacology, 30, 107–113.
Begley, M., Hill, C., & Gahan, C. G. (2006). Applied and Environmental Microbiology, 72(3), 1729–1738.
Tanaka, H., Doesburg, K., Iwasaki, T., & Mierau, I. (1999). Journal of Dairy Science, 82, 2530–2535.
Schillinger, U., Guigas, C., & Holzapfel, W. H. (2005). International Dairy Journal, 15(12), 1289–1297.
Ridlon, J. M., Kang, D. J., & Hylemon, P. B. (2006). Journal of Lipid Research, 47(2), 241–259.
Patel, A. K., Singhania, R. R., Pandey, A., & Chincholkar, S. B. (2010). Applied Biochemistry and Biotechnology, 162(1), 166–180.
Kim, G. B., Miyamoto, C. M., Meighen, E. A., & Lee, B. H. (2004). Applied and Environmental Microbiology, 70(9), 5603–5612.
Tanaka, H., Hashiba, H., Kok, J., & Mierau, I. (2000). Applied and Environmental Microbiology, 66(6), 2502–2512.
Liong, M. T., & Shah, N. P. (2005). International Dairy Journal, 15(4), 391–398.
De Smet, I., Van Hoorde, L., Vande Woestyne, M., Christiaens, H., & Verstraete, W. (1995). Journal of Applied Bacteriology, 79(3), 292–301.
Kim, G. B., Yi, S. H., & Lee, B. H. (2004). Journal of Dairy Science, 87(2), 258–266.
Jiang, J., Hang, X., Zhang, M., Liu, X., Li, D., & Yang, H. (2010). Annals of Microbiology, 60, 81–88.
Moser, S. A., & Savage, D. C. (2001). Applied and Environmental Microbiology, 67(8), 3476–3480.
Rossocha, M., Schultz-Heienbrok, R., von Moeller, H., Coleman, J. P., & Saenger, W. (2005). Biochemistry, 44(15), 5739–5748.
McAuliffe, O., Cano, R. J., & Klaenhammer, T. R. (2005). Applied and Environmental Microbiology, 71(8), 4925–4929.
Lambert, J. M., Bongers, R. S., de Vos, W. M., & Kleerebezem, M. (2008). Applied and Environmental Microbiology, 74(15), 4719–4726.
Kim, G. B., & Lee, B. H. (2008). Journal of Applied Microbiology, 105(3), 778–790.
Elkins, C. A., Moser, S. A., & Savage, D. C. (2001). Microbiology, 147, 3403–3412.
Van Reenen, C. A., & Dicks, L. M. (2011). Archives of Microbiology, 193(3), 157–168.
Grill, J. P., Cayuela, C., Antoine, J. M., & Schneider, F. (2000). Journal of Applied Microbiology, 89(4), 553–563.
Minelli, E. B., Benini, A., Marzotto, M., Sbarbati, A., Ruzzenente, O., Ferrario, R., Hendriks, H., & Dellaglio, F. (2004). International Dairy Journal, 14(8), 723–736.
Dussurget, O., Cabanes, D., Dehoux, P., Lecuit, M., Buchrieser, C., Glaser, P., & Cossart, P. (2002). Molecular Microbiology, 45(4), 1095–1106.
Lee, B. H., & Kim, G. B. (2007). Agro Food Industry Hi-Tech, 18(3), 18–22.
McGarr, S. E., Ridlon, J. M., & Hylemon, P. B. (2005). Journal of Clinical Gastroenterology, 39(2), 98–109.
Takahashi, T., & Morotom, M. (1994). Journal of Dairy Science, 77(11), 3275–3286.
Ahn, Y. T., Kim, G. B., Lim, K. S., Baek, Y. T., & Kim, H. U. (2003). International Dairy Journal, 13, 303–311.
Jones, M. L., Chen, H., Ouyang, W., Metz, T., & Prakash, S. (2004). Journal of Biomedicine and Biotechnology, 2004(1), 61–69.
Ooi, L. G., & Liong, M. T. (2010). International Journal of Molecular Sciences, 11(6), 2499–2522.
Schuster, H. (2004). International Journal of Clinical Practice, 58(7), 689–694.
Kumar, R., Grover, S., & Batish, V. K. (2011). British Journal of Nutrition, 105(4), 561–573.
Roberts, M. S., Magnusson, B. M., Burczynski, F. J., & Weiss, M. (2002). Clinical Pharmacokinetics, 41(10), 751–790.
Russell, D. W. (2009). Journal of Lipid Research, 50, S120–S125.
Lye, H. S., Rahmat-Ali, G. R., & Liong, M. T. (2010). International Dairy Journal, 20(3), 169–175.
Wang, D. Q. (2003). Annals of Hepatology, 2(3), 113–121.
Ramasamy, K., Abdullah, N., Wong, M. C., Karuthan, C., & Ho, Y. W. (2010). Journal of the Science of Food and Agriculture, 90(1), 65–69.
Walker, D. K., & Gilliland, S. E. (1993). Journal of Dairy Science, 76(4), 956–961.
Usman, & Hosono, A. (1999). Journal of Dairy Science, 82(2), 243–248.
Noh, D. O., Kim, S. H., & Gilliland, S. E. (1997). Journal of Dairy Science, 80(12), 3107–3113.
Lye, H. S., Rusul, G., & Liong, M. T. (2010). Journal of Dairy Science, 93(4), 1383–1392.
Lye, H. S., Alias, K. A., Rusul, G., & Liong, M. T. (2012). Ultrasonics Sonochemistry, 19(3), 632–641.
Kurdi, P., Tanaka, H., van Veen, H. W., Asano, K., Tomita, F., & Yokota, A. (2003). Microbiology, 149, 2031–2037.
Klaver, F. A., & van der Meer, R. (1993). Applied and Environmental Microbiology, 59(4), 1120–1124.
Al-Saleh, A. A., Metwalli, A. A. M., & Abu-Tarboush, H. M. (2006). Journal of Saudi Society for Food and Nutrition, 1, 1–17.
Parvez, S., Kim, H. Y., Lee, H. C., & Kim, D. S. (2006). World Journal of Microbiology and Biotechnology, 22(5), 455–459.
Taranto, M. P., Sesma, F., Pesce de Ruiz Holgado, A., & de Valdez, G. F. (1997). Biotechnology Letters, 19(9), 845–847.
Li, G., Hang, X., Tan, J., Zhang, M., Liu, X., Li, D., & Yang, H. (2009). Annals of Microbiology, 59(3), 469–475.
Cardona, M. E., de Vanay, V., Midtvedt, T., & Norin, K. E. (2000). Microbial Ecology in Health and Disease, 12, 219–224.
Pereira, D. I., & Gibson, G. R. (2002). Critical Reviews in Biochemistry and Molecular Biology, 37(4), 259–281.
Wong, J. M., de Souza, R., Kendall, C. W., Emam, A., & Jenkins, D. J. (2006). Journal of Clinical Gastroenterology, 40(3), 235–243.
Yamashita, K., Kawai, K., & Itakura, M. (1984). Nutrition Research, 4(6), 961–966.
Lee, J., Kim, Y., Yun, H. S., Kim, J. G., Oh, S., & Kim, S. H. (2010). Applied and Environmental Microbiology, 76(14), 4829–4835.
Huang, Y., & Zheng, Y. (2010). British Journal of Nutrition, 103(4), 473–478.
Duval, C., Touche, V., Tailleux, A., Fruchart, J. C., Fievet, C., Clavey, V., Staels, B., & Lestavel, S. (2006). Biochemical and Biophysical Research Communications, 340(4), 1259–1263.
Mooradian, A. (2009). Nature Clinical Practice. Endocrinology & Metabolism, 5, 150–159.
Al-Salami, H., Butt, G., Skrbic, R., Golocorbin-Kon, S., & Mikov, M. (2008). Archives of Drug Information, 1, 35–41.
Miljkovic, D., Kuhajda, K., Mikov, M., Kevresan, S., & Sabo, S. (May 2000). Bile acids and their derivatives as glycoregulatory agents. Patent US 6060465.
Goldfine, A. B. (2008). Current Opinion in Cardiology, 23(5), 502–511.
Brinton, E. A. (2008). Diabetes, Obesity & Metabolism, 10(11), 1004–1011.
Yang, L., Zhang, H., Mikov, M., & Tucker, I. G. (2009). Molecular Pharmaceutics, 6(2), 448–456.
Krittaphol, W., McDowell, A., Thomson, C. D., Mikov, M., & Fawcett, J. P. (2011). Biological Trace Element Research, 139(2), 188–196.
Krittaphol, W., Wescombe, P. A., Thomson, C. D., McDowell, A., Tagg, J. R., & Fawcett, J. P. (2011). Biological Trace Element Research, 144(1–3), 1358–1369.
Mikov, M., Boni, N. S., Al-Salami, H., Kuhajda, K., Kevresan, S., Golocorbin-Kon, S., & Fawcett, J. P. (2007). European Journal of Drug Metabolism and Pharmacokinetics, 32, 7–12.
Mikov, M., Al-Salami, H., Golocorbin-Kon, S., Skrbic, R., Raskovic, A., & Fawcett, J. P. (2008). European Journal of Drug Metabolism and Pharmacokinetics, 33, 137–142.
Al-Salami, H., Butt, G., Tucker, I., & Mikov, M. (2008). Medical Hypotheses and Research, 4, 93–101.
Li, T., Matozel, M., Boehme, S., Kong, B., Nilsson, L. M., Guo, G., Ellis, E., & Chiang, J. Y. I. (2011). Hepatology, 53, 996–1006.
Zhang, Y., Lee, F. Y., Barrera, G., Lee, H., Vales, C., Gonzales, F. J., Willson, M., & Edwards, P. A. (2006). PNAS, 103, 1006–1011.
Pullinger, C. R., Eng, C., Salen, G., Shefer, S., Batta, A. K., Erickson, S. K., Verhagen, A., Rivera, C. R., Mulvihill, S. J., Malloy, M. J., & Kane, J. P. (2002). Journal of Clinical Investigations, 110, 109–117.
Li, T., Francl, J. M., Boehme, S., Ochoa, A., Zhang, Y., Klaassen, C. D., Erickson, S. K., & Chiang, J. Y. (2011). Journal of Biological Chemistry, doi:10.1074/jbc.M111.305789.
De Fabiani, E., Mitro, N., Gilardi, F., Galmozzi, A., Caruso, D., & Crestani, M. (2010). Nutrients, 2, 551–571.
Ha, C. G., Cho, J. K., Lee, C. H., Chai, Y. G., Ha, Y. A., & Shin, S. H. (2006). World Journal of Microbiology and Biotechnology, 16(8), 1201–1209.
Nguyen, T. D., Kang, J. H., & Lee, M. S. (2007). International Journal of Food Microbiology, 113(3), 358–361.
El-Shafie, H. A., Yahia, N. I., Ali, H. A., Khalil, F. A., El-Kady, E. M., & Moustafa, Y. A. (2009). Australian Journal of Basic and Applied Sciences, 3(1), 218–228.
Wang, Y., Xu, N., Xi, A., Ahmed, Z., Zhang, B., & Bai, X. (2009). Applied Microbiology and Biotechnology, 84(2), 341–347.
Xie, N., Cui, Y., Yin, Y. N., Zhao, X., Yang, J. W., Wang, Z. G., Fu, N., Tang, Y., Wang, X. H., Liu, X. W., Wang, C. L., & Lu, F. G. (2011). BMC Complementary and Alternative Medicine, 11, 53.
Tamura, M., Hori, S., & Nakagawa, H. (2009). Antonie Van Leeuwenhoek, 96(4), 621–626.
Huang, Y., Wang, J., Cheng, Y., & Zheng, Y. (2010). British Journal of Nutrition, 104(6), 807–812.
Anderson, J. W., & Gilliland, S. E. (1999). Journal of the American College of Nutrition, 18(1), 43–50.
Ahn, Y. T., Kim, B. H., & Kim, H. U. (2000). Korean Journal of Animal Science and Technology, 42, 223–234.
Schaarmann, G., Schneider, J., Zorn, A., Vilser, C., & Jahreis, G. (2001). American Journal of Clinical Nutrition, 73, 496S.
Sadrzadeh-Yeganeh, H., Elmadfa, I., Djazayery, A., Jalali, M., Heshmat, R., & Chamary, M. (2010). British Journal of Nutrition, 103(12), 1778–1783.
Ataie-Jafari, A., Larijani, B., Alavi Majd, H., & Tahbaz, F. (2009). Annals of Nutrition and Metabolism, 54(1), 22–27.
Simons, L. A., Amansec, S. G., & Conway, P. (2006). Nutrition, Metabolism, and Cardiovascular Diseases, 16(8), 531–535.
Hatakka, K., Mutanen, M., Holma, R., Saxelin, M., & Korpela, R. (2008). Journal of the American College of Nutrition, 27(4), 441–447.
Fung, W. Y., Lye, H. S., Lim, T. J., Kuan, C. Y., & Liong, M. T. (2011). In: M. T. Liong (Ed.), Microbiology monographs 21: probiotics—biology, genetics and health aspects (pp. 139–165). Heidelberg: Springer
Shane, A. L., Cabana, M. D., Vidry, S., Merenstein, D., Hummelen, R., Ellis, C. L., Heimbach, J. T., Hempel, S., Lynch, S. V., Sanders, M. E., & Tancredi, D. J. (2010). Gut Microbes, 1(4), 243–253.
Prakash, S., & Martoni, C. (2006). Applied Biochemistry and Biotechnology, 128(1), 1–22.
Borgogna, M., Bellich, B., Zorzin, L., Lapasin, R., & Cesàro, A. (2010). Food Chemistry, 122(2), 416–423.
Burgain, J., Gaiani, C., Linder, M., & Scher, J. (2011). Journal of Food Engineering, 104, 467–483.
Sohail, A., Turner, M. S., Coombes, A., Bostrom, T., & Bhandari, B. (2011). International Journal of Food Microbiology, 145(1), 162–168.
Kailasapathy, K. (2002). Current Issues in Intestinal Microbiology, 3(2), 39–48.
Betoret, E., Betoret, N., Arilla, A., Bennar, M., Barrera, C., Codoner, P., & Fito, P. (2011). Journal of Food Engineering. doi:10.1016/j.jfoodeng.2011.04.027.
Livney, Y. D. (2010). Current Opinion in Colloid and Interface Science, 15(1–2), 73–83.
Bhathena, J., Martoni, C., Kulamarva, A., Urbanska, A. M., Malhotra, M., & Prakash, S. (2009). Journal of Medicinal Food, 12(2), 310–319.
Sridevi, N., Vishwe, P., & Prabhune, A. (2009). Food Research International, 42(4), 516–520.
Kataria, J., Li, N., Wynn, J. L., & Neu, J. (2009). Nutrition Reviews, 67(9), 546–550.
Smaoui, S., Elleuch, L., Bejar, W., Karray-Rebai, I., Ayadi, I., Jaouadi, B., et al. (2010). Applied Biochemistry and Biotechnology, 162(4), 1132–1146.
Ostad, S. N., Salarian, A. A., Ghahramani, M. H., Fazeli, M. R., Samadi, N., & Jamalifar, H. (2009). Folia Microbiologica (Praha), 54(2), 157–160.
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This work is supported by the Ministry of Education and Science of Serbia, grant No. 41012.
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Pavlović, N., Stankov, K. & Mikov, M. Probiotics—Interactions with Bile Acids and Impact on Cholesterol Metabolism. Appl Biochem Biotechnol 168, 1880–1895 (2012). https://doi.org/10.1007/s12010-012-9904-4
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DOI: https://doi.org/10.1007/s12010-012-9904-4