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© 2008 American Society for Nutrition J. Nutr. 138:482-486, March 2008

Nutrient Physiology, Metabolism, and Nutrient-Nutrient Interactions

In Vitro Micellarization and Intestinal Cell Uptake of cis Isomers of Lycopene Exceed Those of All-trans Lycopene1,2

Mark L. Failla3,*, Chureeporn Chitchumroonchokchai3 and Betty K. Ishida4

3 Department of Human Nutrition, The Ohio State University, Columbus, OH 43210 and 4 USDA, Western Regional Research Center, Albany, CA 94710

* To whom correspondence should be addressed. E-mail: failla.3{at}osu.edu.


   ABSTRACT
TOP
 ABSTRACT
Introduction
 Materials and Methods
 Results
 Discussion
 LITERATURE CITED
 
The ratio of cis and all-trans lycopene (LYC) in human and animal tissues exceeds that in foods. The basis for this difference remains unknown, although differences in their stability, transport, and metabolism have been suggested. Here, we systematically compared the digestive stability, efficiency of micellarization, and uptake and intracellular stability of cis and all-trans isomers of LYC and carotenes using the coupled in vitro digestion and Caco-2 human intestinal cell model. Aril and oil from the carotenoid-rich gac fruit (Momordica cochinchinensis Spreng) were cooked with rice to provide a natural source of LYC and carotenes. The ratio of cis:trans isomers of LYC and β-carotene was similar before and after simulated gastric and small intestinal digestion with recovery of total carotenoids in the digesta exceeding 70%. Micellarization of cis isomers of LYC during digestion of meals with both gac aril and oil was significantly greater than that of the all-trans isomer but less than for the carotenes. Uptake of cis isomers of LYC by Caco-2 cells was similar to that of carotenes and significantly greater than all-trans LYC. Micellarized carotenoids were relatively stable in micelles incubated in the cell culture environment and after accumulation in Caco-2 cells. These data suggest that the greater bioaccessibility of cis compared with all-trans isomers of LYC contributes to the enrichment of the cis isomers in tissues and that gac fruit is an excellent source of bioaccessible LYC and provitamin A carotenoids.


   Introduction
TOP
 ABSTRACT
 Introduction
Materials and Methods
 Results
 Discussion
 LITERATURE CITED
 
Lycopene (LYC)5 is a noncyclic C40H56 carotenoid with greater potency for quenching singlet oxygen and scavenging oxygen radicals than {alpha}-tocopherol, β-carotene (βC), and other dietary carotenoids in model systems (1–3). The finding that regular ingestion of cooked tomato products was associated with decreased risk of prostate cancer (4) provided the impetus to investigate the content, isomeric profile, and biochemical activities of LYC in cells and tissues from animals and humans. One consistent and still unexplained observation is that concentrations of cis isomers of LYC are similar to or exceed that of all-trans LYC in animal and human tissues, although all-trans LYC is the predominant isomer in foods (5,6).

It is generally assumed that the different isomeric profile of LYC in foods and tissues results in part from postabsorptive isomerization or selective retention of the cis isomers (7). However, several investigators have suggested that isomerization of a portion of ingested all-trans LYC in the gastric lumen and the more efficient incorporation of cis isomers of LYC into mixed micelles also may contribute to the enrichment of the cis isomers in tissues (8–10). Other preabsorptive events that may contribute to the enrichment of cis isomers in tissues include the isomerization of all-trans to the cis configuration within mixed micelles or following incorporation into enterocytes, preferential uptake of cis LYC by enterocytes, and more efficient incorporation of cis LYC into chylomicrons for delivery to tissues. The investigation of such possibilities has been hampered in part by the low concentrations of cis LYC in most ingested foods and the relatively poor efficiency of micellarization and absorption of LYC (11–13).

We undertook this investigation to examine systematically the digestive stability, micellarization, intestinal cell uptake, and intracellular stability of all-trans and cis LYC. We selected ripened gac (Momordica cochinchinensis Spreng) fruit as the source of LYC, because the content of the carotenoid in this food markedly exceeds that in other natural sources (14,15). The fruit is indigenous to southern and southeast Asia and the seed pulp also contains relatively high levels of βC, {alpha}-tocopherol, and mono-unsaturated fatty acids, and PUFA. Gac is consumed during annual festivals when the red seed pulp of the fruit (aril) is used to color cooked rice, and its oil has been used as a provitamin A supplement (16). Moreover, plasma levels of retinol, {alpha}-carotene ({alpha}C), βC, and LYC significantly increased in preschool Vietnamese children fed 20 g gac fruit with rice for 30 d, suggesting that the provitamin A carotenoids in the fruit were bioavailable (14). We prepared rice meals with either gac aril or gac oil according to traditional styles. The foods were subjected to simulated gastric and small intestinal digestion (17). The efficiency of micellarization of carotenoids during simulated digestion has been recently shown to be highly correlated with in vivo micellarization and bioavailability of carotenoids in human studies (18). Mixed micelles formed during simulated digestion of rice with gac aril were incubated with differentiated cultures of Caco-2 human intestinal cells to determine uptake and intracellular stability of LYC and carotene isomers.


   Materials and Methods
TOP
 ABSTRACT
 Introduction
 Materials and Methods
Results
 Discussion
 LITERATURE CITED
 
    Chemicals and standards. Unless stated otherwise, all reagents and materials were purchased from Sigma Chemical, Fisher Scientific, and Gibco (Invitrogen). Sweet rice grain (California Cereal Product) was purchased at an Asian market in Columbus, OH.

    Preparation of test meals for in vitro digestion. Gac seed pulp (aril) was prepared from gac fruit and frozen at the USDA Western Regional Research Center in Albany, CA. Gac oil was a gift from Dr. Le Vuong that was prepared according to Vuong and King (16). Samples were forwarded to the Department of Human Nutrition at The Ohio State University where traditional rice meals were prepared. Frozen gac aril was ground in ice-cold mortar before adding 50 g to 220 g cooked rice and steaming for 20 min. Gac oil (4 g) was mixed with cooked rice (220 g) and steamed for 20 min. After steaming, meals with gac oil and aril were transferred to sealable plastic bags, cooled on ice, and mashed with a rolling pin to homogeneity. Aliquots were stored under a blanket of nitrogen in 50 mL polypropylene screw-cap tubes and stored at –80°C.

    In vitro digestion. Details for simulated gastric and small intestinal digestion have been previously described (17). Digestion tubes contained 871 mg and 837 mg rice meal with gac aril and gac oil, respectively. After completion of the small intestinal phase of simulated digestion, aliquots of chyme were centrifuged (167,000 x g; 35 min at 4°C) and the aqueous fraction was filtered (cellulose acetate, 0.22-µm pores) to prepare the micelle fraction. Aliquots of homogenized food, digesta, and micellar fraction were stored at –80°C under nitrogen and analyzed within 1 wk.

    Uptake of micellarized carotenoids by Caco-2 human intestinal cells. Stock cultures of Caco-2 cells (HTB-37, American Type Culture Collection) were maintained between passages 26 and 34 as previously described (17). To examine uptake of carotenoids from micelles generated during simulated small intestine digestion, Caco-2 cells were grown in T75 cm2 flasks to 11–14 d postconfluency. Spent medium was removed and monolayers were washed twice with basal DMEM at 37°C. Serum-free DMEM containing 250 mL/L of micellar fraction generated during simulated digestion of gac aril meal was added to washed monolayers (12.5 mL/flask). Medium was removed after 4 h and monolayers were washed twice with ice-cold PBS (pH 7.4) containing albumin (2 g/L) to remove residual carotenoids adhering to the cell surface (19) before 2 additional washes with ice-cold PBS. To assess the intracellular stability of carotenoids, cultures were incubated with medium containing micellar fraction for 4 h, washed once with PBS containing albumin at 37°C, and incubated with fresh DMEM without carotenoids for an additional 16 h. Monolayers were collected in 5 mL ice-cold PBS, centrifuged (400 x g; 5 min at 4°C) and cell pellets were stored at –80°C under nitrogen for a maximum of 1 wk. Integrity of monolayers of cultures exposed to medium containing micelle fraction generated during digestion of the rice meals with gac aril was similar to that of control cultures as assessed microscopically by mean number of "domes" per field (17).

    Extraction and analysis of carotenoids. Thawed samples (1–3 mL) of homogenized food, digesta, and micelle fraction were extracted by addition of 3 volumes of hexane:acetone (3:1) containing 4.5 mmol/L BHT, vortexed for 1 min, and centrifuged (2000 x g; 5 min) to separate phases. The extraction was repeated a total of 3 times and hexane fractions were combined and dried at room temperature under a stream of nitrogen. The film was resolubilized in methyl-tert-butyl-ether:methanol (MeOH) (1:1) and analyzed immediately. Cell pellets were thawed on ice before addition of 3.0 mL PBS and 1.5 mL of ethanol containing 34.6 mmol/L sodium dodecyl sulfate and 4.5 mmol/L BHT. The mixture was sonicated for 20 s on ice and carotenoids were extracted from the suspension as above.

Carotenoids were separated by HPLC using a YMC C30 analytical scale (4.5 x 250 mm) reverse phase column (Waters) with a C18 stationary-phase guard column. Separations were achieved using a gradient elution with a binary mobile phase of methanol:ammonium acetate (98:2) and MTBE (20). The concentration of carotenoids was calculated from comparison of the area under the curve with known concentrations of pure all-trans isomers of {alpha}C, βC, and LYC. The extinction coefficients (Formula) used were 2710 and 2592 for all-trans {alpha}C and all-trans βC in hexane at 450 nm, respectively, and 3450 for all-trans LYC in petroleum ether at 470 nm (21). All-trans carotenoids and their cis isomers were identified by UV-visible absorbance spectra recorded using a Waters 996 photodiode array detector (Waters) and comparison of retention times and absorbance spectra to previous separations with the C30 column (22). Although zeaxanthin and β-cryptoxanthin esters have been reported to account for as much as 18% total carotenoids in gac fruit (23), there was no attempt to quantify xanthophyll esters in the studies described below.

    Protein assays. Protein content of cell samples was determined by the bicinchoninic acid assay (Pierce) using bovine serum albumin as a standard.

    Statistical analysis of data. All data were analyzed using SPSS version 13. Descriptive statistics, including mean and SEM were calculated for the efficiency of micellarization of carotenoids from digested foods, the stability of micellarized carotenoids in cell culture medium, and the uptake of carotenoids by Caco-2 cells. Means were compared using 1-way ANOVA followed by Tukey's honestly significant difference post hoc test or paired t test. Differences were considered significant at P < 0.05. All tests were conducted in 3 independent replicates for each experiment and each experiment was repeated at least once to provide a minimum of 6 independent observations.


   Results
TOP
 ABSTRACT
 Introduction
 Materials and Methods
 Results
Discussion
 LITERATURE CITED
 
    Carotenoid composition of test meals. Rice meal with gac aril contained 839 nmol carotenes/g with all-trans LYC accounting for 59% of the total and all-trans βC accounting for 27% of the total (Table 1). Total carotene content of the rice meal with gac oil was approximately one-third that with aril. βC (66%) was the predominant carotenoid, because much of the LYC was lost during the drying and pressing of gac aril to prepare the oil. Another difference between the meals was the similar quantities of all-trans and cis isomers of LYC in the meal with gac oil, whereas the ratio of all-trans to cis LYC in the meal with gac aril was 8:1.


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  		TABLE 1 Concentrations of carotenoids in rice meals1

 
    Digestive stability and micellarization of carotenoids in test meals. Recovery of carotenoids after simulated gastric and small intestinal digestion of rice meal with gac aril was 73–83% and with gac oil was 65–83% (Table 2). The efficiency of micellarization of {alpha}C and βC (30–45%) during simulated digestion of the rice meals exceeded (P < 0.05) that of LYC (2–28%). Cis isomers of both βC and LYC partitioned into micelles more efficiently (P < 0.05) than the respective all-trans isomers during digestion. Also, micellarization of all-trans LYC during digestion of rice meal with gac oil was greater (P < 0.05) than that during digestion of the meal with gac aril. The micelle fraction generated during digestion of the meal with gac aril was used to investigate the uptake of carotenoids, because the concentration of carotenoids markedly exceeded that in the micellar fraction after digestion of the meal with gac oil (Table 2).


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  		TABLE 2 Digestive stability and the efficiency of micellarization of carotenoids in test meals1

 
    Uptake of micellarized carotenoids by Caco-2 cells. Filtered aqueous fraction from the digested rice meal with gac aril was diluted with basal DMEM and added to monolayers of differentiated Caco-2 cells. The quantities (picomoles) of micellarized {alpha}C, βC, and LYC in medium added to cultures of differentiated Caco-2 cells were 62 ± 0.2, 235 ± 1.1 (all-trans, 206; cis, 29), and 86 ± 1.0 (all-trans, 37; cis, 49), respectively. Apparent cellular accumulation of {alpha}C, cis βC, all-trans βC, and cis LYC from medium was 26–30% (Fig. 1). However, apparent uptake of all-trans LYC was lower (P < 0.001) than that of other carotenoids (Fig. 1).


Figure 1
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  		FIGURE 1  Apparent uptake of all-trans LYC by Caco-2 cells is less than that of other carotenoids. Data are means ± SEM, n = 6. Means without a common letter differ, P < 0.001.

 
    Stability of micellar and intracellular carotenoids. We examined the possibility that isomerization of carotenoids may occur following micellarization or after their uptake by the Caco-2 cells. The concentrations of {alpha}C, cis LYC, and all-trans LYC in medium containing micelles generated by digestion of rice meal with gac aril were not significantly changed during 4-h incubation in dishes without cells. All-trans and cis βC slightly but significantly (P < 0.05) decreased (9.1 ± 2.5%) and increased (7.0 ± 2.0%), respectively, during incubation (Fig. 2A). Caco-2 cells also were incubated in medium with micelles and one-half of the monolayers were collected after 4 h to quantify apparent uptake. Spent medium was removed from the other cultures and fresh medium without micelles was added. After incubation for an additional 16 h, cells contained 98–112% of the concentrations of all-trans βC, cis βC, and cis LYC at 4 h (Fig. 2B). Cellular content of {alpha}C and all-trans LYC decreased by 9 and 13%, respectively, during the overnight incubation (P < 0.05).


Figure 2
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  		FIGURE 2  Stability of LYC isomers and carotenes in micelles (A) generated during simulated digestion and after uptake by Caco-2 cells (B). Data are means ± SEM, n = 6. *The concentration of the indicated carotenoid changed during incubation, P < 0.05.

 

   Discussion
TOP
 ABSTRACT
 Introduction
 Materials and Methods
 Results
 Discussion
LITERATURE CITED
 
The absorption of carotenoids, like other highly lipophilic compounds in the diet, requires the partitioning of these compounds in bile salt micelles during small intestinal digestion, uptake across the brush border membrane of enterocytes, and incorporation into chylomicron particles for secretion into lymph. The transfer of carotenoids from the food matrix to micelles is referred to as bioaccessibility and represents the potential for their absorption or bioavailability. The primary finding of this study is that both the transfer of cis isomers of LYC to micelles during the digestion of rice meal with gac aril or oil and the subsequent uptake of cis LYC by Caco-2 intestinal epithelial cells were more efficient than that of all-trans LYC. These results suggest that such differences in the gastrointestinal processing of ingested cis and all-trans isomers of LYC contribute to the markedly increased ratio of cis:all-trans isomers in tissues compared with fresh and processed foods.

The ratio of cis:all-trans LYC remained relatively constant during simulated digestion of the test meal. Limited conversion of all-trans to cis isomers of LYC was reported when tomato paste was added to simulated and human gastric fluids (9) and within the stomach of ferret and human subjects (8,11). Boileau et al. (8) also observed more efficient incorporation of cis LYC into synthetic bile salt micelles, as well as greater enrichment of cis isomers compared with all-trans LYC in intestinal mucosa of ferrets. Our observation that the ratio of cis:all-trans LYC was stable within micelles generated during simulated digestion and following uptake by Caco-2 cells suggests that the observed enrichment of cis isomers is due to their more efficient uptake and not isomerization of all-trans:cis isomers in these compartments. It has been postulated the bends in the cis configurations decrease space occupied by the molecule in comparison to the linear all-trans structure. This likely prevents aggregation and crystal formation in lipid droplets, thereby facilitating incorporation into mixed micelles (24,25). It also is possible that the cis configuration of LYC may bind more favorably to membrane transporters responsible for the uptake of carotenoids across the brush border membrane of absorptive intestinal cells (26,27).

Increased bioaccessibility of cis LYC suggests greater bioavailability compared with all-trans LYC. Isomer-dependent differences in incorporation of LYC isomers in chylomicrons were not investigated in this study. However, Stahl and Sies (28) reported that cooking tomatoes increased the content of cis isomers of LYC and the absorption of LYC in human subjects. Recently, Unlu et al. (29) reported that fractional absorption of LYC from tangerine tomato sauce containing 97% tetra-cis and other cis isomers was 2.5 times greater than LYC from a high βC variety of tomato that contained all-trans LYC as the predominant isomer. The most abundant isomer of LYC in the triglyceride-rich fractions from the human subjects was the same as ingested, suggesting minimal isomerization during digestion and absorption. Burri et al. (30) also conducted a crossover human study feeding sauces made from tangerine or red tomatoes. They found that serum all-trans LYC concentrations increased more in the presence or after feeding the sauce containing tetra-cis and also containing all-trans LYC and other cis LYC isomers. Their data suggest that cis isomers of LYC might facilitate the absorption of all-trans LYC. Similar to the reported results with cis and all-trans isomers of LYC in the rice meals with gac, we also have observed that the incorporation of tetra-cis and other cis isomers of LYC into micelles during simulated digestion of fresh and cooked tangerine tomatoes significantly exceeds that of all-trans LYC in digested Roma tomatoes (M. Failla, M. Pusateri, C. Chitchumroonchokchai, and S. Schwartz, unpublished data).

The presence of high amounts of BC as well as LYC in gac facilitated direct comparison of bioaccessibility of isomers for the 2 carotenoids during digestion of the same food. The efficiency of micellarization of cis βC exceeded that of all-trans βC during digestion of the meals containing gac as reported previously for in vitro studies (31,32). However, all-trans βC is absorbed more efficiently than cis βC, suggesting decreased uptake of cis βC by absorptive epithelial cells, isomerization within the cell, or preferential incorporation of the all-trans isomer into chylomicrons (33). The bioaccessibility of cis and all-trans βC was greater than LYC for both digested meals. Others have noted that LYC is less accessible than carotenes and xanthophylls in vitro and in vivo (17,18,34). The extent of micellarization of both LYC and βC during simulated digestion of gac was considerably greater than reported for these carotenoids in other fruits and vegetables subjected to the same in vitro procedure (17,18). This difference may be due to the localization of the carotenoids in the lipid-rich matrix of gac aril that contains as much as 22% fatty acids by weight with palmitate, oleate, and linoleate, each comprising ~30% of total fatty acyl pool (14,15). It is likely that the carotenoids are soluble in this matrix, thereby facilitating their transfer to micelles during small intestinal digestion. The unsaturated fatty acyl groups also are expected to induce chylomicron formation and secretion for transfer of the carotenoids and their products to lymph (35), thereby contributing to the observed effectiveness of the gac supplement for improving vitamin A status of preschool Vietnamese children (13). Thus, gac fruit appears to represent an effective natural source of highly bioavailable LYC and βC.


   ACKNOWLEDGMENTS
 
The authors thank Le Vuong for helpful discussions about traditional styles of preparing meals containing gac and providing samples of gac oil and Mary Chapman for the preparation of gac seed aril.


   FOOTNOTES
 
1 Supported by the Initiative for Future Agriculture and Food Systems grant no. 2001-52102-11333 from the USDA Cooperative State Research, Education, and Extension Service and by the Ohio Agriculture Research and Development Center. Back

2 Author disclosures: M. L. Failla, C. Chitchumroonchokchai, and B. K. Ishida, no conflicts of interest. Back

5 Abbreviations used: {alpha}C, {alpha}-carotene; βC, β-carotene; LYC, lycopene. Back

Manuscript received 16 October 2007. Initial review completed 24 November 2007. Revision accepted 10 December 2007.


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 Materials and Methods
 Results
 Discussion
 LITERATURE CITED
 

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J. P. Mills, P. W. Simon, and S. A. Tanumihardjo
Biofortified Carrot Intake Enhances Liver Antioxidant Capacity and Vitamin A Status in Mongolian Gerbils
J. Nutr., September 1, 2008; 138(9): 1692 - 1698.
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