Spice active ingredients affect the micellization, permeation and bioavailability of structurally different carotenoids in human intestinal epithelial Caco-2 cells.
Authors
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Department of Microbiology and Biotechnology, Jnana Bharathi Campus, Bangalore University, Bengaluru - 560 056 ,IN
Shivaprasad Shilpa -
Department of Microbiology and Biotechnology, Jnana Bharathi Campus, Bangalore University, Bengaluru - 560 056 ,INRudrappa Ambedkar
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Department of Microbiology and Biotechnology, Jnana Bharathi Campus, Bangalore University, Bengaluru - 560 056 ,INHulikere Jagdish Shwetha
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Department of Microbiology and Biotechnology, Jnana Bharathi Campus, Bangalore University, Bengaluru - 560 056 ,INRangaswamy Lakshminarayana
DOI:
https://doi.org/10.21048/IJND.2021.58.3.27336Keywords:
Carotenoids, Triglyceride-rich lipoproteins, Human intestinal epithelial cell line, Bioavailability, Brush-border membranesAbstract
Abstract
This study evaluated the influence of active spice ingredients on the bioaccessibility and bioavailability of different carotenoids at the enterocyte level. Briefly, carotenoids solubilized micellar fractions obtain by simulated digestion of spinach (β-carotene; BC and lutein; LUT) or brown seaweed (fucoxanthin; FUCO) or shrimp (astaxanthin; AST) either with or without curcumin/capsaicin/piperine. Further, physicochemical properties (particle size and viscosity) of micelles were analyzed and correlated bioaccessibility, permeability characteristics, and bioavailability of carotenoids in Caco-2 cells. The digestion of carotenoid's source with spice compound affected carotenoid solubilization/micellization, cumulative percent of particle size, and viscosity in the following order of spice compound treatments; curcumin > capsaicin > piperine > control. The carotenoids level in micelles higher in capsaicin and piperine than curcumin and control digested groups. The increased carotenoids bioaccessibility may be due to lesser hydrophobic interaction found in capsaicin and piperine than curcumin. Further, based on importance and distinct nature, BC and LUT were used bioavailability studies. The enhanced cellular uptake and secretion of carotenoids in triglycerides rich lipoproteins by capsaicin and piperine is due to changes in integrity, permeability, the fluidity of the epithelial barrier of absorption than curcumin and control groups. These findings opine the interaction of carotenoids with specific dietary component (spices) and their regulatory metabolism at the intestinal level is vital for the enteral nutrition of carotenoids.
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Accepted 2021-05-29
Published 2021-09-07
References
Riboli, E. and Norat, T. Epidemiologic evidence of the protective effect of fruit and vegetables on cancer risk. Am. J. Clin. Nutr., 2003, 78, 559S-569S. DOI: https://doi.org/10.1093/ajcn/78.3.559S
Arathi, B.P., Sowmya, P.R.R., Vijay, K., Baskaran, V. and Lakshminarayana, R. Metabolomics of carotenoids: The challenges and prospects- A review. Trds. Fd. Sci. Technol., 2015, 45, 105-117. DOI: https://doi.org/10.1016/j.tifs.2015.06.003
Bone, R.A., Landrum, J.T., Guerra, L.H. and Ruiz, C.A. LUT and zeaxanthin dietary supplements raise macular pigment density and serum concentrations of these carotenoids in humans. J. Nutr., 2003, 133, 992-998. DOI: https://doi.org/10.1093/jn/133.4.992
Chew, B.P., Brown, C.M., Park, J.S. and Mixter, P.F. Dietary LUT inhibits mouse mammary tumor growth by regulating angiogenesis and apoptosis. Anticancer Res., 2003, 23, 3333-3339.
Mares-Perlman, J. A., Millen, A. E., Ficek, T. L. and Hankinson, S. E. The body of evidence to support a protective role for Lutein and zeaxanthin in delaying chronic disease - Overview. J. Nutr., 2002, 132, 518S-524S. DOI: https://doi.org/10.1093/jn/132.3.518S
Shilpa, S., Shwetha, H. J., Raju, M. and Lakshminarayana, R. Factors affecting bioaccessibility and bio-efficacy of carotenoids. In carotenoids: Properties, processing and applications, Academic Press, 2020, 41-73. DOI: https://doi.org/10.1016/B978-0-12-817067-0.00002-6
Parker, R.S. Absorption, metabolism and transport of carotenoids. FASEB J., 1996, 10, 542551. DOI: https://doi.org/10.1096/fasebj.10.5.8621054
Faulks, R.M. and Southon, S. Challenges to understanding and measuring carotenoid bioavailability. Biochimi. Biophys. Acta., 2005, 1740, 95-100. DOI: https://doi.org/10.1016/j.bbadis.2004.11.012
Nagao, A., Maeda, M., Lim, B.P., Kobayashi, H. and Terao, J. Inhibition of BC-15, 15"²-dioxygenase activity by dietary flavonoids. J. Nutr. Biochem., 2000, 11, 348-355. DOI: https://doi.org/10.1016/S0955-2863(00)00090-5
Veda, S. and Srinivasan, K. Influence of dietary spices on the in vivo absorption of ingested BC in experimental rats. Br. J. Nutr., 2011, 105, 1429-1438. DOI: https://doi.org/10.1017/S0007114510005179
Tyssandier, V., Reboul, E., Dumas, J.F., Bouteloup-Demange, C., Armand, M., Marcand, J., Sallas, M. and Borel, P. Processing of vegetable-borne carotenoids in the human stomach and duodenum. Am. J. Physiol. Gastrointest. Liver Physiol., 2003, 284, G913-G923. DOI: https://doi.org/10.1152/ajpgi.00410.2002
Shoba, G., Joy, D., Joseph, T., Majeed, M., Rajendran, R. and Srinivas, P.S.S.R. Influence of piperine on the pharmacokinetics of curcumin in animals and human volunteers. Planta Med., 1998, 64, 353-356. DOI: https://doi.org/10.1055/s-2006-957450
Garrett, D.A., Failla, M.L. and Sarama, R.J. Development of an in vitro digestion method to assess carotenoid bioavailability from meals. J. Agri. Fd. Chem., 1999, 47, 4301-4309. DOI: https://doi.org/10.1021/jf9903298
Lakshminarayana, R., Raju, M., Krishnakantha, T.P. and Baskaran, V. Determination of major carotenoids in a few Indian leafy vegetables by high-performance liquid chromatography. J. Agri. Fd. Chem., 2005, 53, 2838-2842. DOI: https://doi.org/10.1021/jf0481711
Vijay, K., Sowmya, P.R.R., Arathi, B.P., Shilpa, S., Shwetha, H.J., Raju, M. and Lakshminarayana, R. Low-dose doxorubicin with carotenoids selectively alters redox status and upregulates oxidative stress-mediated apoptosis in breast cancer cells. Fd. Chem. Toxicol., 2018, 118, 675-690. DOI: https://doi.org/10.1016/j.fct.2018.06.027
Sowmya, P.R.R., Arathi, B.P., Vijay, K., Baskaran, V. and Lakshminarayana, R. AST from shrimp efficiently modulates oxidative stress and allied cell death progression in MCF-7 cells treated synergistically with BC and LUT from greens. Fd. Chem. Toxicol., 2017, 106, 58-69. DOI: https://doi.org/10.1016/j.fct.2017.05.024
During, A., Dawson, H.D. and Harrison, E.H. Carotenoid transport is decreased and expression of the lipid transporters SR-BI, NPC1L1 and ABCA1 is downregulated in Caco-2 cells treated with ezetimibe. The J. Nutr., 2005, 135, 2305-2312. DOI: https://doi.org/10.1093/jn/135.10.2305
Luchoomun, J. and Hussain, M.M. Assembly and secretion of chylomicrons by differentiated Caco-2 cells: Nascent triglycerides and preformed phospholipids are preferentially used for lipoprotein assembly. J. Biol. Chem., 1999, 274, 19565-19572. DOI: https://doi.org/10.1074/jbc.274.28.19565
Folch, J., Lees, M. and Stanley, G.S. A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem., 1957, 226, 497-509. DOI: https://doi.org/10.1016/S0021-9258(18)64849-5
Fletcher, M.J. A colorimetric method for estimating serum triglycerides. Clinica Chimica Acta., 1968, 22, 393-397. DOI: https://doi.org/10.1016/0009-8981(68)90041-7
Jensen-Jarolim, E., Gajdzik, L., Haberl, I., Kraft, D., Scheiner, O. and Graf, J. Hot spices influence permeability of human intestinal epithelial monolayers. J. Nutr., 1998, 128, 577-581. DOI: https://doi.org/10.1093/jn/128.3.577
Schmitz, J., Preiser, H., Maestracci, D., Ghosh, B.K., Cerda, J.J. and Crane, R.K. Purification of the human intestinal brush border membrane. Biochimi. Biophys. 1973, 323, 98-112. DOI: https://doi.org/10.1016/0005-2736(73)90434-3
Bernotti, S., Seidman, E., Sinnett, D., Brunet, S., Dionne, S., Delvin, E. and Levy, E. Inflammatory reaction without endogenous antioxidant response in Caco-2 cells exposed to iron/ascorbate-mediated lipid peroxidation. Am. J. Physiol. Gastrointest. Liver Physiol., 2003, 285, G898-G906. DOI: https://doi.org/10.1152/ajpgi.00042.2003
Castenmiller, J.J. and West, C.E. Bioavailability and bioconversion of carotenoids. Ann. Rev. Nutr., 1998, 18, 19-38. DOI: https://doi.org/10.1146/annurev.nutr.18.1.19
Lakshminarayana, R., Raju, M., Keshava Prakash, M.N. and Baskaran, V. Phospholipid, oleic acid micelles and dietary olive oil influence the LUT absorption and activity of antioxidant enzymes in rats. Lipids., 2009, 44, 799-806. DOI: https://doi.org/10.1007/s11745-009-3328-0
Mamatha, B.S. and Baskaran, V. Effect of micellar lipids, dietary fiber and BC on LUT bioavailability in aged rats with LUT deficiency. Nutr., 2011, 27, 960-966. DOI: https://doi.org/10.1016/j.nut.2010.10.011
Yonekura, L. and Nagao, A. Intestinal absorption of dietary carotenoids. Mol. Nutr. Fd. Res., 2007, 51, 107-115. DOI: https://doi.org/10.1002/mnfr.200600145
Borel, P. Factors affecting intestinal absorption of highly lipophilic food microconstituents (fat-soluble vitamins, carotenoids and phytosterols). Clin. Chem. Lab. Med., 2003, 41, 979-994. DOI: https://doi.org/10.1515/CCLM.2003.151
Reboul, E., Richelle, M., Perrot, E., Desmoulins-Malezet, C., Pirisi, V. and Borel, P. Bioaccessibility
of carotenoids and vitamin E from their main dietary sources. J. Agri. Fd. Chem., 2006, 54, 8749-8755. DOI: https://doi.org/10.1021/jf061818s
Sy, C., Gleize, B., Dangles, O., Landrier, J.F., Veyrat, C.C. and Borel, P. Effects of physicochemical
properties of carotenoids on their bioaccessibility, intestinal cell uptake and blood and tissue concentrations. Mol. Nutr. Fd. Res., 2012, 56, 1385-1397. DOI: https://doi.org/10.1002/mnfr.201200041
Erdman Jr, J.W., Bierer, T.L. and Gugger, E.T. Absorption and transport of carotenoids. Ann. New York Acad. Sci., 1993, 691, 76-85. DOI: https://doi.org/10.1111/j.1749-6632.1993.tb26159.x
Chen, B.H. and Han, L.H. Effects of different cooking methods on the yield of carotenoids in
water convolvulus (Ipomoea aquatica). J. Fd. Protect., 1990, 53), 1076-1078. DOI: https://doi.org/10.4315/0362-028X-53.12.1076
Iqbal, J. and Hussain, M. M. Intestinal lipid absorption.Am. J. Physiol. Endocrinol. Metabol., 2009, DOI: https://doi.org/10.1152/ajpendo.90899.2008
, E1183-E1194.
Khajuria, A., Thusu, N. and Zutshi, U. Piperine modulates permeability characteristics of intestine by inducing alterations in membrane dynamics: Influence on brush border membrane fluidity, ultrastructure and enzyme kinetics. Phytomed., 2002, 9, 224-231. DOI: https://doi.org/10.1078/0944-7113-00114
Prakash, U.N. and Srinivasan, K. Beneficial influence of dietary spices on the ultrastructure and
fluidity of the intestinal brush border in rats. Br. J. Nutr., 2010, 104, 31-39. DOI: https://doi.org/10.1017/S0007114510000334
