Deposition Form and Bioaccessibility of Keto-carotenoids from Mamey Sapote (Pouteria sapota), Red Bell Pepper (Capsicum annuum), and Sockeye Salmon (Oncorhynchus nerka) Filet

Journal of Agricultural and Food Chemistry

Volumn 64, Issue 9, 2016, Pages 1989-1998

  Chacón Ordóñez, Tania ^a,b   Esquivel, Patricia ^b   Jiménez, Víctor M ^a,b   Carle, Reinhold ^a,c   Schweiggert, Ralf M ^a  

^a UNIVERSITY OF HOHENHEIM   (Germany)

^b UNIVERSIDAD DE COSTA RICA   (Costa Rica)

^c KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

Author keywords

astaxanthin; capsanthin; chromoplast; cryptocapsin; globular; keto carotenoids; sapotexanthin; tubular; ultrastructure; carotene

Indexed keywords

BELLS; BIOCHEMISTRY; DEPOSITION; HIGH RESOLUTION TRANSMISSION ELECTRON MICROSCOPY; LIGHT TRANSMISSION; MICROSTRUCTURE; TRANSMISSION ELECTRON MICROSCOPY;

ASTAXANTHIN; CAPSANTHIN; CHROMOPLAST; CRYPTOCAPSIN; GLOBULAR; KETOCAROTENOIDS; SAPOTEXANTHIN; TUBULAR; ULTRASTRUCTURE;

PIGMENTS;

ANTIOXIDANT; ASTAXANTHIN; CAPSANTHIN; CAROTENOID; SAPOTEXANTHIN; XANTHOPHYLL;

ANIMAL; BIOAVAILABILITY; CHEMISTRY; COMPARATIVE STUDY; ELECTRON MICROSCOPY; FRUIT; PEPPER; PLASTID; POUTERIA; SALMONINE; ULTRASTRUCTURE;

ANIMALS; ANTIOXIDANTS; BIOLOGICAL AVAILABILITY; CAPSICUM; CAROTENOIDS; FRUIT; MICROSCOPY, ELECTRON; PLASTIDS; POUTERIA; SALMON; XANTHOPHYLLS;

EID: 84960357989     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/acs.jafc.5b06039     Document Type: Article

References (51)

1. Deming, D.; Boileau, T.; Heintz, K.; Atkinson, C.; Erdman, J. Carotenoids: Linking chemistry, absorption, and metabolism to potential roles in human health and disease. In Handbook of Antioxidants, 2 nd ed.; Cardenas, E., Packer, L., Eds.; Marcel Dekker Inc: New York, 2002; pp 189-221.
2. FAO/WH O. Vitamin A. FAO/WHO, Human vitamin and mineral requirements: Report of a joint FAO/WHO expert consultation; Bangkok, Thailand, 2002; pp 87-107.
3. Faulks, R. M.; Southon, S. Challenges to understanding and measuring carotenoid bioavailability Biochim. Biophys. Acta, Mol. Basis Dis. 2005, 1740, 95-100 10.1016/j.bbadis.2004.11.012
4. West, C. E.; Castenmiller, J. J. M. Quantification of the "SLAMENGHI" factors for carotenoid bioavailability and bioconversion Int. J. Vitam. Nutr. Res. 1998, 68, 371-377
5. Schweiggert, R. M.; Carle, R. Carotenoid deposition in plant and animal foods and its impact on bioavailability. Crit. Rev. Food Sci. Nutr. 2015, DOI: 10.1080/10408398.2015.1012756.
6. Fernández-García, E.; Carvajal-Lérida, I.; Jarén-Galán, M.; Garrido-Fernández, J.; Pérez-Gálvez, A.; Hornero-Méndez, D. Carotenoids bioavailability from foods: From plant pigments to efficient biological activities Food Res. Int. 2012, 46, 438-450 10.1016/j.foodres.2011.06.007
7. Aschoff, J. K.; Rolke, C. L.; Breusing, N.; Bosy-Westphal, A.; Högel, J.; Carle, R.; Schweiggert, R. M. Bioavailability of β-cryptoxanthin is greater from pasteurized orange juice than from fresh oranges-a randomized cross-over study Mol. Nutr. Food Res. 2015, 59, 1896-1904 10.1002/mnfr.201500327
8. Goñi, I.; Serrano, J.; Saura-Calixto, F. Bioaccessibility of β-carotene, lutein, and lycopene from fruits and vegetables J. Agric. Food Chem. 2006, 54, 5382-5387 10.1021/jf0609835
9. Schweiggert, R. M.; Mezger, D.; Schimpf, F.; Steingass, C. B.; Carle, R. Influence of chromoplast morphology on carotenoid bioaccessibility of carrot, mango, papaya, and tomato Food Chem. 2012, 135, 2736-2742 10.1016/j.foodchem.2012.07.035
10. Schweiggert, R. M.; Kopec, R. E.; Villalobos-Gutiérrez, M. G.; Högel, J.; Quesada, S.; Esquivel, P.; Schwartz, S. J.; Carle, R. Carotenoids are more bioavailable from papaya than from tomato and carrot in humans: a randomised cross-over study Br. J. Nutr. 2014, 111, 490-498 10.1017/S0007114513002596
11. Storebakken, T.; Foss, P.; Schiedt, K.; Austreng, E.; Liaaen-Jensen, S.; Manz, U. Carotenoids in diets for salmonids: IV. Pigmentation of Atlantic salmon with astaxanthin, astaxanthin dipalmitate and canthaxanthin Aquaculture 1987, 65, 279-292 10.1016/0044-8486(87)90241-9
12. Curl, A. L. Red pepper carotenoids: The carotenoids of red bell peppers J. Agric. Food Chem. 1962, 10, 504-509 10.1021/jf60124a020
13. Naguib, Y. M. A. Antioxidant activities of astaxanthin and related carotenoids J. Agric. Food Chem. 2000, 48, 1150-1154 10.1021/jf991106k
14. Matsufuji, H.; Nakamura, H.; Chino, M.; Takeda, M. Antioxidant activity of capsanthin and the fatty acid esters in paprika (Capsicum annuum) J. Agric. Food Chem. 1998, 46, 3468-3472 10.1021/jf980200i
15. Murillo, E.; McLean, R.; Britton, G.; Agocs, A.; Nagy, V.; Deli, J. Sapotexanthin, an A-provitamin carotenoid from red mamey (Pouteria sapota) J. Nat. Prod. 2011, 74, 283-285 10.1021/np1006982
16. Morera, J. A. El zapote; Centro Agronómico Tropical de Investigación y Enseñanza, CATIE: Turrialba, Costa Rica, 1992; pp 20.
17. Osterlie, M.; Bjerkeng, B.; Liaaen-Jensen, S. Plasma appearance and distribution of astaxanthin E/Z and R/S isomers in plasma lipoproteins of men after single dose administration of astaxanthin J. Nutr. Biochem. 2000, 11, 482-490 10.1016/S0955-2863(00)00104-2
18. Oshima, S.; Sakamoto, H.; Ishiguro, Y.; Terao, J. Accumulation and clearance of capsanthin in blood plasma after the ingestion of paprika juice in men J. Nutr. 1997, 127, 1475-1479
19. Deruère, J.; Römer, S.; d'Harlingue, A.; Backhaus, R. A.; Kuntz, M.; Camara, B. Fibril assembly and carotenoid overaccumulation in chromoplasts: A model for supramolecular lipoprotein structures Plant Cell 1994, 6, 119-133 10.2307/3869680
20. Matthews, S. J.; Ross, N. W.; Lall, S. P.; Gill, T. A. Astaxanthin binding protein in Atlantic salmon Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol. 2006, 144, 206-214 10.1016/j.cbpb.2006.02.007
21. Garrett, D. A.; Failla, M. L.; Sarama, R. J. Development of an in vitro digestion method to assess carotenoid bioavailability from meals J. Agric. Food Chem. 1999, 47, 4301-4309 10.1021/jf9903298
22. Bengtsson, A.; Larsson Alminger, M.; Svanberg, U. In vitro bioaccessibility of β-carotene from heat-processed orange-fleshed sweet potato J. Agric. Food Chem. 2009, 57, 9693-9698 10.1021/jf901692r
23. Schweiggert, U.; Kammerer, D. R.; Carle, R.; Schieber, A. Characterization of carotenoids and carotenoid esters in red pepper pods (Capsicum annuum L.) by high-performance liquid chromatography/atmospheric pressure chemical ionization mass spectrometry Rapid Commun. Mass Spectrom. 2005, 19, 2617-2628 10.1002/rcm.2104
24. Murillo, E.; Giuffrida, D.; Menchaca, D.; Dugo, P.; Torre, G.; Meléndez-Martinez, A. J.; Mondello, L. Native carotenoids composition of some tropical fruits Food Chem. 2013, 140, 825-836 10.1016/j.foodchem.2012.11.014
25. Turcsi, E.; Murillo, E.; Kurtán, T.; Szappanos, á.; Illyés, T.-Z.; Gulyás-Fekete, G.; Agócs, A.; Avar, P.; Deli, J. Isolation of β-cryptoxanthin-epoxides, precursors of cryptocapsin and 3′-deoxycapsanthin, from red mamey (Pouteria sapota) J. Agric. Food Chem. 2015, 63, 6059-6065 10.1021/acs.jafc.5b01936
26. Marín, A.; Ferreres, F.; Tomás-Barberán, F. A.; Gil, M. I. Characterization and quantitation of antioxidant constituents of sweet pepper (Capsicum annuum L.) J. Agric. Food Chem. 2004, 52, 3861-3869 10.1021/jf0497915
27. Yuan, J.-P.; Chen, F. Identification of astaxanthin isomers in Haematococcus lacustris by HPLC-photodiode array detection Biotechnol. Tech. 1997, 11, 455-459 10.1023/A:1018441411746
28. Vásquez-Caicedo, A. L.; Heller, A.; Neidhart, S.; Carle, R. Chromoplast morphology and β-carotene accumulation during postharvest ripening of mango cv. 'Tommy Atkins' J. Agric. Food Chem. 2006, 54, 5769-5776 10.1021/jf060747u
29. Schweiggert, R. M.; Steingass, C. B.; Heller, A.; Esquivel, P.; Carle, R. Characterization of chromoplasts and carotenoids of red- and yellow-fleshed papaya (Carica papaya L.) Planta 2011, 234, 1031-1044 10.1007/s00425-011-1457-1
30. Hempel, J.; Amrehn, E.; Quesada, S.; Esquivel, P.; Jiménez, V. M.; Heller, A.; Carle, R.; Schweiggert, R. M. Lipid-dissolved γ-carotene, β-carotene, and lycopene in globular chromoplasts of peach palm (Bactris gasipaes Kunth) fruits Planta 2014, 240, 1037-1050 10.1007/s00425-014-2121-3
31. Horner, H. T.; Healy, R. A.; Ren, G.; Fritz, D.; Klyne, A.; Seames, C.; Thornburg, R. W. Amyloplast to chromoplast conversion in developing ornamental tobacco floral nectaries provides sugar for nectar and antioxidants for protection Am. J. Bot. 2007, 94, 12-24 10.3732/ajb.94.1.12
32. Sitte, P. Role of lipid self-assembly in subcellular morphogenesis. In Cytomorphogenesis in Plants; Kiermayer, O., Ed; Springer: Wien, 1981; Vol. 8, pp 401-421.
33. Austin, J. R., II; Frost, E.; Vidi, P. A.; Kessler, F.; Staehelin, L. A. Plastoglobules are lipoprotein subcompartments of the chloroplast that are permanently coupled to thylakoid membranes and contain biosynthetic enzymes Plant Cell 2006, 18, 1693-1703 10.1105/tpc.105.039859
34. Sitte, P. Chromoplasts. In Pigments in Plants, Czygan, F. G. C., Ed.; G. Fischer VerI.: Stuttgart, 1980; pp 117-148.
35. Hempel, J.; Schädle, C. N.; Leptihn, S.; Carle, R.; Schweiggert, R. M. Structure related aggregation behavior of carotenoids and carotenoid esters J. Photochem. Photobiol., A 2016, 317, 161-174 10.1016/j.jphotochem.2015.10.024
36. Spano, F. C. Analysis of the UV/Vis and CD spectral line shapes of carotenoid assemblies: Spectral signatures of chiral H-aggregates J. Am. Chem. Soc. 2009, 131, 4267-4278 10.1021/ja806853v
37. Henmi, H.; Hata, M.; Hata, M. Studies on the carotenoids in the muscle of salmon-II. Astaxanthin and/or canthaxanthin-actomyosin complex in salmon muscle Nippon Suisan Gakkaishi 1989, 55, 1583-1589 10.2331/suisan.55.1583
38. Canene-Adams, K.; Erdman, J. W. Absorption, transport, distribution in tissues and bioavailability. In Carotenoids: Nutrition and Health, Britton, G.; Pfander, H.; Liaaen-Jensen, S., Eds.; Birkhäuser: Basel, Germany, 2009; Vol. 5, pp 115-148.
39. Breithaupt, D. E.; Weller, P.; Wolters, M.; Hahn, A. Plasma response to a single dose of dietary β-cryptoxanthin esters from papaya (Carica papaya L.) or non-esterified β-cryptoxanthin in adult human subjects: a comparative study Br. J. Nutr. 2003, 90, 795-801 10.1079/BJN2003962
40. Wingerath, T.; Stahl, W.; Sies, H. β-cryptoxanthin selectively increases in human chylomicrons upon ingestion of tangerine concentrate rich in β-cryptoxanthin esters Arch. Biochem. Biophys. 1995, 324, 385-390 10.1006/abbi.1995.0052
41. Breithaupt, D. E.; Bamedi, A.; Wirt, U. Carotenol fatty acid esters: easy substrates for digestive enzymes? Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol. 2002, 132, 721-728 10.1016/S1096-4959(02)00096-9
42. Tyssandier, V.; Lyan, B.; Borel, P. Main factors governing the transfer of carotenoids from emulsion lipid droplets to micelles Biochim. Biophys. Acta, Mol. Cell Biol. Lipids 2001, 1533, 285-292 10.1016/S1388-1981(01)00163-9
43. Breithaupt, D. E. Enzymatic hydrolysis of carotenoid fatty acid esters of red pepper (Capsicum annuum L.) by a lipase from Candida rugosa Z. Naturforsch., C: J. Biosci. 2000, 55, 971-975 10.1515/znc-2000-11-1220
44. O'Sullivan, L.; Jiwan, M. A.; Daly, T.; O'Brien, N. M.; Aherne, S. A. Bioaccessibility, uptake, and transport of carotenoids from peppers (Capsicum Spp.) using the coupled in vitro digestion and human intestinal Caco-2 cell model J. Agric. Food Chem. 2010, 58, 5374-5379 10.1021/jf100413m
45. Bell, J. W.; Farkas, B. E.; Hale, S. A.; Lanier, T. C. Effect of thermal treatment on moisture transport during steam cooking of skipjack tuna (Katsuwonas pelamis) J. Food Sci. 2001, 66, 307-313 10.1111/j.1365-2621.2001.tb11337.x
46. Sy, C.; Gleize, B.; Dangles, O.; Landrier, J.-F.; Veyrat, C. C.; Borel, P. Effects of physicochemical properties of carotenoids on their bioaccessibility, intestinal cell uptake, and blood and tissue concentrations Mol. Nutr. Food Res. 2012, 56, 1385-1397 10.1002/mnfr.201200041
47. Borel, P.; Grolier, P.; Armand, M.; Partier, A.; Lafont, H.; Lairon, D.; Azais-Braesco, V. Carotenoids in biological emulsions: solubility, surface-to-core distribution, and release from lipid droplets J. Lipid Res. 1996, 37, 250-261
48. Almela, L.; Fernández-López, J. A.; Candela, M. E.; Egea, C.; Alcázar, M. D. Changes in pigments, chlorophyllase activity, and chloroplast ultrastructure in ripening pepper for paprika J. Agric. Food Chem. 1996, 44, 1704-1711 10.1021/jf9504531
49. López-Hernández, J.; Oruña-Concha, M. J.; Simal-Lozano, J.; Vázquez-Blanco, M. E.; González-Castro, M. J. Chemical composition of padrón peppers (Capsicum annuum L.) grown in Galicia (N.W. Spain) Food Chem. 1996, 57, 557-559 10.1016/S0308-8146(96)00191-4
50. Riedl, J.; Linseisen, J.; Hoffmann, J.; Wolfram, G. Some dietary fibers reduce the absorption of carotenoids in women J. Nutr. 1999, 129, 2170-2176
51. Rock, C. L.; Swendseid, M. E. Plasma beta-carotene response in humans after meals supplemented with dietary pectin Am. J. Clin. Nutr. 1992, 55, 96-99