Skip to main content
Erschienen in: European Journal of Nutrition 8/2011

01.12.2011 | Original Contribution

Effect of dietary protein on heme iron uptake by Caco-2 cells

verfasst von: Pía Villarroel, Sebastián Flores, Fernando Pizarro, Daniel López de Romaña, Miguel Arredondo

Erschienen in: European Journal of Nutrition | Ausgabe 8/2011

Einloggen, um Zugang zu erhalten

Abstract

Objective

To study heme iron bioavailability and the role of dietary protein (animal and vegetable) on iron uptake using an in vitro model (Caco-2 cell line).

Methods

Caco-2 cells were seeded in bicameral chambers with different animal (beef, chicken or fish) or vegetable (peas, lentils, and soybeans) proteins or with pure animal (collagen and casein) or vegetable (gliadin, zein, and glutein) protein extracts. The effect of each protein over heme iron absorption was assessed.

Results

Intact heme uptake was higher than either heme plus albumin or digested heme plus albumin, but lower than digested heme. White meal exerted the highest inhibitory effect on hemin uptake. Heme iron uptake decreased in the presence of all legume extracts, but was not significantly different among them (one-way ANOVA, NS). Pure animal (collagen and casein) and vegetable (zein and glutelin) proteins increased heme iron uptake, except for gliadin.

Conclusion

Animal and vegetable protein in general decreased heme iron uptake. However, purified animal and vegetable protein induce an increase in heme iron uptake.
Literatur
1.
Zurück zum Zitat McCord JM (1998). Iron, free radicals, and oxidative injury. Semin Hematol 35: 5–12. Review McCord JM (1998). Iron, free radicals, and oxidative injury. Semin Hematol 35: 5–12. Review
2.
Zurück zum Zitat Turnbull A, Cleton F, Finch CA (1962) Iron absorption. IV. The absorption of hemoglobin iron. J Clin Invest 41:1897–1907CrossRef Turnbull A, Cleton F, Finch CA (1962) Iron absorption. IV. The absorption of hemoglobin iron. J Clin Invest 41:1897–1907CrossRef
3.
Zurück zum Zitat Hallberg L, Solvell L (1967) Absorption of hemoglobin iron in man. Acta Med Scand 181:335–354CrossRef Hallberg L, Solvell L (1967) Absorption of hemoglobin iron in man. Acta Med Scand 181:335–354CrossRef
4.
Zurück zum Zitat Callender ST, Mallett BJ, Smith MD (1957) Absorption of haemoglobin iron. Br J Haematol 3:186–192CrossRef Callender ST, Mallett BJ, Smith MD (1957) Absorption of haemoglobin iron. Br J Haematol 3:186–192CrossRef
5.
Zurück zum Zitat Conrad ME, Umbreit JN, Moore EG (1999) Iron absorption and transport. Am J Med Sci 318:213–229CrossRef Conrad ME, Umbreit JN, Moore EG (1999) Iron absorption and transport. Am J Med Sci 318:213–229CrossRef
6.
Zurück zum Zitat Conrad ME, Weintraub LR, Crosby WH (1964) The role of the intestine in iron kinetics. J Clin Invest 43:963–974CrossRef Conrad ME, Weintraub LR, Crosby WH (1964) The role of the intestine in iron kinetics. J Clin Invest 43:963–974CrossRef
7.
Zurück zum Zitat Crosby WH, Conrad ME Jr, Wheby MS (1963) The rate of iron accumulation in iron storage disease. Blood 22:429–440 Crosby WH, Conrad ME Jr, Wheby MS (1963) The rate of iron accumulation in iron storage disease. Blood 22:429–440
8.
Zurück zum Zitat Carpenter CE, Mahoney AW (1992) Contributions of heme and nonheme iron to human nutrition. Crit Rev Food Sci Nutr 31:333–367CrossRef Carpenter CE, Mahoney AW (1992) Contributions of heme and nonheme iron to human nutrition. Crit Rev Food Sci Nutr 31:333–367CrossRef
9.
Zurück zum Zitat Conrad ME, Benjamin BI, Williams HL, Foy AL (1967) Human absorption of hemoglobin-iron. Gastroenterology 53:5–10 Conrad ME, Benjamin BI, Williams HL, Foy AL (1967) Human absorption of hemoglobin-iron. Gastroenterology 53:5–10
10.
Zurück zum Zitat Monsen ER, Hallberg L, Layrisse M, Hegsted DM, Cook JD, Mertz W, Finch CA (1978) Estimation of available dietary iron. Am J Clin Nutr 31:134–141 Monsen ER, Hallberg L, Layrisse M, Hegsted DM, Cook JD, Mertz W, Finch CA (1978) Estimation of available dietary iron. Am J Clin Nutr 31:134–141
11.
Zurück zum Zitat Worthington MT, Cohn SM, Miller SK, Qi Luo RQ, Berg CL (2001) Characterization of a human plasma membrane heme transporter in intestinal and hepatocyte cell lines. Am J Physiol Gastrointest Liver Physiol 280:G1172–G1177 Worthington MT, Cohn SM, Miller SK, Qi Luo RQ, Berg CL (2001) Characterization of a human plasma membrane heme transporter in intestinal and hepatocyte cell lines. Am J Physiol Gastrointest Liver Physiol 280:G1172–G1177
12.
Zurück zum Zitat Shayeghi M, Latunde-Dada GO, Oakhill JS, Laftah AH, Takeuchi K, Halliday N, Khan Y, Warley A, McCann FE, Hider RC, Frazer DM, Anderson GJ, Vulpe CD, Simpson RJ, McKie AT (2005) Identification of an intestinal heme transporter. Cell 122:789–801CrossRef Shayeghi M, Latunde-Dada GO, Oakhill JS, Laftah AH, Takeuchi K, Halliday N, Khan Y, Warley A, McCann FE, Hider RC, Frazer DM, Anderson GJ, Vulpe CD, Simpson RJ, McKie AT (2005) Identification of an intestinal heme transporter. Cell 122:789–801CrossRef
13.
Zurück zum Zitat Bjorn-Rasmussen E, Hallberg L, Isaksson B, Arvidsson B (1974) Food iron absorption in man. Applications of the two-pool extrinsic tag method to measure heme and nonheme iron absorption from the whole diet. J Clin Invest 53:247–255CrossRef Bjorn-Rasmussen E, Hallberg L, Isaksson B, Arvidsson B (1974) Food iron absorption in man. Applications of the two-pool extrinsic tag method to measure heme and nonheme iron absorption from the whole diet. J Clin Invest 53:247–255CrossRef
14.
Zurück zum Zitat Uzel C, Conrad ME (1998) Absorption of heme iron. Semin Hematol 35:27–34 Uzel C, Conrad ME (1998) Absorption of heme iron. Semin Hematol 35:27–34
15.
Zurück zum Zitat Schricker BR, Miller DD (1983) Effects of cooking and chemical treatment on heme and non-heme iron in meat. J Food Sci 48:1340–1344CrossRef Schricker BR, Miller DD (1983) Effects of cooking and chemical treatment on heme and non-heme iron in meat. J Food Sci 48:1340–1344CrossRef
16.
Zurück zum Zitat Hallberg L, Rossander-Hulthen L, Brune M, Gleerup A (1993) Inhibition of haem-iron absorption in man by calcium. Br J Nutr 69:533–540CrossRef Hallberg L, Rossander-Hulthen L, Brune M, Gleerup A (1993) Inhibition of haem-iron absorption in man by calcium. Br J Nutr 69:533–540CrossRef
17.
Zurück zum Zitat Tenhunen R, Tokola O, Linden IB (1987) Haem arginate: a new stable haem compound. J Pharm Pharmacol 39:780–786CrossRef Tenhunen R, Tokola O, Linden IB (1987) Haem arginate: a new stable haem compound. J Pharm Pharmacol 39:780–786CrossRef
18.
Zurück zum Zitat Lee KS, Raymond LD, Schoen B, Raymond GJ, Kett L, Moore RA, Johnson LM, Taubner L, Speare JO, Onwubiko HA, Baron GS, Caughey WS, Caughey B (2007) Hemin interactions and alterations of the subcellular localization of prion protein. J Biol Chem 282:36525–36533CrossRef Lee KS, Raymond LD, Schoen B, Raymond GJ, Kett L, Moore RA, Johnson LM, Taubner L, Speare JO, Onwubiko HA, Baron GS, Caughey WS, Caughey B (2007) Hemin interactions and alterations of the subcellular localization of prion protein. J Biol Chem 282:36525–36533CrossRef
19.
Zurück zum Zitat Conrad ME, Umbreit JN (2000) Iron absorption and transport-an update. Am J Hematol 64:287–298CrossRef Conrad ME, Umbreit JN (2000) Iron absorption and transport-an update. Am J Hematol 64:287–298CrossRef
20.
Zurück zum Zitat Au AP, Reddy MB (2000) Caco-2 cells can be used to assess human iron bioavailability from a semipurified meal. J Nutr 130:1329–1334 Au AP, Reddy MB (2000) Caco-2 cells can be used to assess human iron bioavailability from a semipurified meal. J Nutr 130:1329–1334
21.
Zurück zum Zitat Fogh J, Wright WC, Loveless JD (1977) Absence of HeLa cell contamination in 169 cell lines derived from human tumors. J Natl Cancer Inst 58:209–214 Fogh J, Wright WC, Loveless JD (1977) Absence of HeLa cell contamination in 169 cell lines derived from human tumors. J Natl Cancer Inst 58:209–214
22.
Zurück zum Zitat Artursson P (1990) Epithelial transport of drugs in cell culture. I: a model for studying the passive diffusion of drugs over intestinal absorptive (Caco-2) cells. J Pharm Sci 79:476–482CrossRef Artursson P (1990) Epithelial transport of drugs in cell culture. I: a model for studying the passive diffusion of drugs over intestinal absorptive (Caco-2) cells. J Pharm Sci 79:476–482CrossRef
23.
Zurück zum Zitat Alvarez-Hernandez X, Nichols GM, Glass J (1991) Caco-2 cell line: a system for studying intestinal iron transport across epithelial cell monolayers. J Biochim Biophys Acta 1070:205–208CrossRef Alvarez-Hernandez X, Nichols GM, Glass J (1991) Caco-2 cell line: a system for studying intestinal iron transport across epithelial cell monolayers. J Biochim Biophys Acta 1070:205–208CrossRef
24.
Zurück zum Zitat Han O, Failla M, Hill A, Morris E, Smith J (1995) Reduction of Fe(III) is required for uptake of nonheme iron by Caco-2 cells. J Nutr 125:1291–1299 Han O, Failla M, Hill A, Morris E, Smith J (1995) Reduction of Fe(III) is required for uptake of nonheme iron by Caco-2 cells. J Nutr 125:1291–1299
25.
Zurück zum Zitat Nuñez MT, Alvarez X, Smith M, Tapia V, Glass J (1994) Role of redox systems on Fe3 + uptake by transformed human intestinal epithelial (Caco-2) cells. Am J Physiol 267:C1582–C1588 Nuñez MT, Alvarez X, Smith M, Tapia V, Glass J (1994) Role of redox systems on Fe3 + uptake by transformed human intestinal epithelial (Caco-2) cells. Am J Physiol 267:C1582–C1588
26.
Zurück zum Zitat Alvarez-Hernandez X, Smith M, Glass J (1994) Regulation of iron uptake and transport by transferrin in Caco-2 cells, an intestinal cell line. Biochim Biophys Acta 1192:215–222CrossRef Alvarez-Hernandez X, Smith M, Glass J (1994) Regulation of iron uptake and transport by transferrin in Caco-2 cells, an intestinal cell line. Biochim Biophys Acta 1192:215–222CrossRef
27.
Zurück zum Zitat Gangloff M, Lai C, Van Campen DR, Miller DD, Glahn RP (1996) Ferrous iron uptake but not transfer is down-regulated in Caco-2 cells grown in high iron serum-free medium. J Nutr 126:3118–3127 Gangloff M, Lai C, Van Campen DR, Miller DD, Glahn RP (1996) Ferrous iron uptake but not transfer is down-regulated in Caco-2 cells grown in high iron serum-free medium. J Nutr 126:3118–3127
28.
Zurück zum Zitat Nunez MT, Tapia V (1999) Transferrin stimulates iron absorption, exocytosis, and secretion in cultured intestinal cells. Am J Physiol 276:C1085–C1090 Nunez MT, Tapia V (1999) Transferrin stimulates iron absorption, exocytosis, and secretion in cultured intestinal cells. Am J Physiol 276:C1085–C1090
29.
Zurück zum Zitat Garcia MN, Flowers C, Cook JD (1996) The Caco-2 cell culture system can be used as a model to study food iron availability. J Nutr 126:251–258 Garcia MN, Flowers C, Cook JD (1996) The Caco-2 cell culture system can be used as a model to study food iron availability. J Nutr 126:251–258
30.
Zurück zum Zitat Glahn RP, Lai C, Hsu J, Thompson JF, Guo M, Van Campen DR (1998) Decreased citrate improves iron availability from infant formula: application of an in vitro digestion/Caco-2 cell culture model. J Nutr 128:257–264 Glahn RP, Lai C, Hsu J, Thompson JF, Guo M, Van Campen DR (1998) Decreased citrate improves iron availability from infant formula: application of an in vitro digestion/Caco-2 cell culture model. J Nutr 128:257–264
31.
Zurück zum Zitat Glahn RP, Lee OA, Yeung A, Goldman MI, Miller DD (1998) Caco-2 cell ferritin formation predicts nonradiolabeled food iron availability in an in vitro digestion/Caco-2 cell culture model. J Nutr 128:1555–1561 Glahn RP, Lee OA, Yeung A, Goldman MI, Miller DD (1998) Caco-2 cell ferritin formation predicts nonradiolabeled food iron availability in an in vitro digestion/Caco-2 cell culture model. J Nutr 128:1555–1561
32.
Zurück zum Zitat Arredondo M, Kloosterman J, Núñez S, Segovia F, Candia V, Flores S, Le Blanc S, Olivares M, Pizarro F (2008) Heme iron uptake by Caco-2 cells is a saturable, temperature sensitive and modulated by extracellular pH and potassium. Biol Trace Elem Res 125:109–119CrossRef Arredondo M, Kloosterman J, Núñez S, Segovia F, Candia V, Flores S, Le Blanc S, Olivares M, Pizarro F (2008) Heme iron uptake by Caco-2 cells is a saturable, temperature sensitive and modulated by extracellular pH and potassium. Biol Trace Elem Res 125:109–119CrossRef
33.
Zurück zum Zitat Chaney AL, Marbach EP (1962) Modified reagents for determination of urea and ammonia. Clin Chem 8:130–132 Chaney AL, Marbach EP (1962) Modified reagents for determination of urea and ammonia. Clin Chem 8:130–132
34.
Zurück zum Zitat Olivares M, Pizarro F, de Pablo S, Araya M, Uauy R (2004) Iron, zinc, and copper: contents in common Chilean foods and daily intakes in Santiago, Chile. Nutrition 20:205–212CrossRef Olivares M, Pizarro F, de Pablo S, Araya M, Uauy R (2004) Iron, zinc, and copper: contents in common Chilean foods and daily intakes in Santiago, Chile. Nutrition 20:205–212CrossRef
35.
Zurück zum Zitat Rebouche CJ, Wilcox CL, Widness JA (2004) Microanalysis of non-heme iron in animal tissues. J Biochem Biophys Methods 58:239–251CrossRef Rebouche CJ, Wilcox CL, Widness JA (2004) Microanalysis of non-heme iron in animal tissues. J Biochem Biophys Methods 58:239–251CrossRef
36.
Zurück zum Zitat Udaka J, Koga T, Tsuji H, Kimoto M, Takumi K (2000) Efficient extraction and some properties of storage proteins (prolamin and glutelin) in ancient rice cultivars. J Nutr Sci Vitaminol (Tokyo) 46:84–90CrossRef Udaka J, Koga T, Tsuji H, Kimoto M, Takumi K (2000) Efficient extraction and some properties of storage proteins (prolamin and glutelin) in ancient rice cultivars. J Nutr Sci Vitaminol (Tokyo) 46:84–90CrossRef
37.
Zurück zum Zitat Bamdad F, Hossein Goli A, Kadivar M (2006) Preparation and characterization of proteinous film from lentil (Lens culinaris): Edible film from lentil (Lens culinaris) Food. Res. Internat 39:106–111 Bamdad F, Hossein Goli A, Kadivar M (2006) Preparation and characterization of proteinous film from lentil (Lens culinaris): Edible film from lentil (Lens culinaris) Food. Res. Internat 39:106–111
38.
Zurück zum Zitat Tomoskozi S, Lasztity R, Haraszi R, Baticz O (2001) Isolation and study of the functional properties of pea proteins. Nahrung 45:399–401CrossRef Tomoskozi S, Lasztity R, Haraszi R, Baticz O (2001) Isolation and study of the functional properties of pea proteins. Nahrung 45:399–401CrossRef
39.
Zurück zum Zitat Lombardo ME, Lombardo ME, Araujo LS, Ciccarelli AB, Battle A (2005) A spectrophotometric method for estimating hemin in biological systems. Anal Biochem 341:199–203CrossRef Lombardo ME, Lombardo ME, Araujo LS, Ciccarelli AB, Battle A (2005) A spectrophotometric method for estimating hemin in biological systems. Anal Biochem 341:199–203CrossRef
40.
Zurück zum Zitat Lowry OH, Rosebrough N, Farr A, Randall R (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275 Lowry OH, Rosebrough N, Farr A, Randall R (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275
41.
Zurück zum Zitat Layrisse M, Martinez-Torres C, Roche M (1968) Effect of interaction of various foods on iron absorption. Am J Clin Nutr 21:1175–1183 Layrisse M, Martinez-Torres C, Roche M (1968) Effect of interaction of various foods on iron absorption. Am J Clin Nutr 21:1175–1183
42.
Zurück zum Zitat Layrisse M, Cook JD, Martinez-Torres C, Roche M, Kuhn IN, Finch CA (1969) Food iron absorption: a comparison of vegetable and animal foods. Blood 33:430–443 Layrisse M, Cook JD, Martinez-Torres C, Roche M, Kuhn IN, Finch CA (1969) Food iron absorption: a comparison of vegetable and animal foods. Blood 33:430–443
43.
Zurück zum Zitat Hallberg L, Bjom-Rasmussen E, Howard L, Rossander L (1979) Dietary heme iron absorption. A discussion of possible mechanisms for the absorption-promoting effect of meat and for the regulation of iron absorption. Scand J Gastroenterol 14:769–779CrossRef Hallberg L, Bjom-Rasmussen E, Howard L, Rossander L (1979) Dietary heme iron absorption. A discussion of possible mechanisms for the absorption-promoting effect of meat and for the regulation of iron absorption. Scand J Gastroenterol 14:769–779CrossRef
44.
Zurück zum Zitat Bjorn-Rasmussen E, Hallberg L (1979) Effect of animal proteins on the absorption of food iron in man. Nutr Metab 23:192–202CrossRef Bjorn-Rasmussen E, Hallberg L (1979) Effect of animal proteins on the absorption of food iron in man. Nutr Metab 23:192–202CrossRef
45.
Zurück zum Zitat Lynch SR, Dassenko SA, Morck TA, Beard JL, Cook JD (1985) Soy protein products and heme iron absorption in humans. Am J Clin Nutr 41:13–20 Lynch SR, Dassenko SA, Morck TA, Beard JL, Cook JD (1985) Soy protein products and heme iron absorption in humans. Am J Clin Nutr 41:13–20
46.
Zurück zum Zitat Vaghefi N, Nedjaoum F, Guillochon D, Bureau F, Arhan P, Bouglé D (2002) Influence of the extent of hemoglobin hydrolysis on the digestive absorption of heme iron. An in vitro study. J Agric Food Chem 50:4969–4973CrossRef Vaghefi N, Nedjaoum F, Guillochon D, Bureau F, Arhan P, Bouglé D (2002) Influence of the extent of hemoglobin hydrolysis on the digestive absorption of heme iron. An in vitro study. J Agric Food Chem 50:4969–4973CrossRef
47.
Zurück zum Zitat Dang TN, Bishop GM, Dringen R, Robinson SR (2010) The putative heme transporter HCP1 is expressed in cultured astrocytes and contributes to the uptake of hemin. Glia 58:55–65CrossRef Dang TN, Bishop GM, Dringen R, Robinson SR (2010) The putative heme transporter HCP1 is expressed in cultured astrocytes and contributes to the uptake of hemin. Glia 58:55–65CrossRef
48.
Zurück zum Zitat Layrisse M, Martinez-Torres C (1972) Model for measuring dietary absorption of heme iron: test with a complete meal. Am J Clin Nutr 25:401–411 Layrisse M, Martinez-Torres C (1972) Model for measuring dietary absorption of heme iron: test with a complete meal. Am J Clin Nutr 25:401–411
49.
Zurück zum Zitat Conrad ME, Weintraub LR, Sears DA, Crosby WH (1966) Absorption of hemoglobin iron. Am J Physiol 211:1123–1130 Conrad ME, Weintraub LR, Sears DA, Crosby WH (1966) Absorption of hemoglobin iron. Am J Physiol 211:1123–1130
50.
Zurück zum Zitat Hazell T, Ledward DA, Neale RJ (1978) Iron availability from meat. Br J Nutr 39:631–638CrossRef Hazell T, Ledward DA, Neale RJ (1978) Iron availability from meat. Br J Nutr 39:631–638CrossRef
51.
Zurück zum Zitat Hazell T, Ledward DA, Neale RJ (1982) Hemoglobin and meat iron absorption. Am J Clin Nutr 36:187–189 Hazell T, Ledward DA, Neale RJ (1982) Hemoglobin and meat iron absorption. Am J Clin Nutr 36:187–189
Metadaten
Titel
Effect of dietary protein on heme iron uptake by Caco-2 cells
verfasst von
Pía Villarroel
Sebastián Flores
Fernando Pizarro
Daniel López de Romaña
Miguel Arredondo
Publikationsdatum
01.12.2011
Verlag
Springer-Verlag
Erschienen in
European Journal of Nutrition / Ausgabe 8/2011
Print ISSN: 1436-6207
Elektronische ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-011-0173-8

Weitere Artikel der Ausgabe 8/2011

European Journal of Nutrition 8/2011 Zur Ausgabe

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

CAR-M-Zellen: Warten auf das große Fressen

22.05.2024 Onkologische Immuntherapie Nachrichten

Auch myeloide Immunzellen lassen sich mit chimären Antigenrezeptoren gegen Tumoren ausstatten. Solche CAR-Fresszell-Therapien werden jetzt für solide Tumoren entwickelt. Künftig soll dieser Prozess nicht mehr ex vivo, sondern per mRNA im Körper der Betroffenen erfolgen.

Chronische Verstopfung: „Versuchen Sie es mit grünen Kiwis!“

22.05.2024 Obstipation Nachrichten

Bei chronischer Verstopfung wirken Kiwis offenbar besser als Flohsamenschalen. Das zeigen die Daten aus einer randomisierten Studie, die der Gastroenterologe Oliver Pech beim Praxis-Update vorstellte.

So häufig greift rheumatoide Arthritis auf Organe über

21.05.2024 Rheumatoide Arthritis Nachrichten

Im Verlauf von rheumatoider Arthritis entwickeln viele Patienten extraartikuläre Manifestationen. Schwedische Forscher haben sich mit der Inzidenz und den Risikofaktoren befasst.

Blutdrucksenkung könnte Uterusmyome verhindern

Frauen mit unbehandelter oder neu auftretender Hypertonie haben ein deutlich erhöhtes Risiko für Uterusmyome. Eine Therapie mit Antihypertensiva geht hingegen mit einer verringerten Inzidenz der gutartigen Tumoren einher.

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.