Soybean Ferritin Forms an Iron-Containing Oligomer in Tofu even after Heat Treatment

Journal of Agricultural and Food Chemistry

Volumn 63, Issue 40, 2015, Pages 8890-8895

  Masuda, Taro ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

ferritin; heat denaturation; iron; oligomer; secondary structure; soybean; subunit; tofu

Indexed keywords

BIOCHEMISTRY; DICHROISM; DIGITAL STORAGE; FOOD PROCESSING; HEAT TREATMENT; IRON; NUTRITION; OLIGOMERS; PROCESSED FOODS;

FERRITIN; HEAT DENATURATION; SECONDARY STRUCTURES; SOYBEAN; SUBUNIT; TOFU;

THERMAL PROCESSING (FOODS);

FERRITIN; IRON; VEGETABLE PROTEIN;

ANALYSIS; CHEMISTRY; COOKING; FOOD HANDLING; HEAT; SOY FOOD; SOYBEAN;

COOKING; FERRITINS; FOOD HANDLING; HOT TEMPERATURE; IRON; PLANT PROTEINS; SOY FOODS; SOYBEANS;

EID: 84944260315     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/acs.jafc.5b03080     Document Type: Article

References (46)

1. Zimmermann, M. B.; Hurrell, R. F. Nutritional iron deficiency Lancet 2007, 370, 511-20 10.1016/S0140-6736(07)61235-5
2. Gunshin, H.; Mackenzie, B.; Berger, U. V.; Gunshin, Y.; Romero, M. F.; Boron, W. F.; Nussberger, S.; Gollan, J. L.; Hediger, M. A. Cloning and characterization of a mammalian proton-coupled metal-ion transporter Nature 1997, 388, 482-8 10.1038/41343
3. McKie, A. T.; Barrow, D.; Latunde-Dada, G. O.; Rolfs, A.; Sager, G.; Mudaly, E.; Mudaly, M.; Richardson, C.; Barlow, D.; Bomford, A.; Peters, T. J.; Raja, K. B.; Shirali, S.; Hediger, M. A.; Farzaneh, F.; Simpson, R. J. An iron-regulated ferric reductase associated with the absorption of dietary iron Science 2001, 291, 1755-1759 10.1126/science.1057206
4. Harrison, P. M.; Arosio, P. Ferritins: Molecular properties, iron storage function and cellular regulation Biochim. Biophys. Acta, Bioenerg. 1996, 1275, 161-203 10.1016/0005-2728(96)00022-9
5. Briat, J. F.; Ravet, K.; Arnaud, N.; Duc, C.; Boucherez, J.; Touraine, B.; Cellier, F.; Gaymard, F. New insights into ferritin synthesis and function highlight a link between iron homeostasis and oxidative stress in plants Ann. Bot. 2010, 105, 811-22 10.1093/aob/mcp128
6. Ambe, S.; Ambe, F.; Nozaki, T. Mossbauer study of iron in soybean seeds J. Agric. Food Chem. 1987, 35, 292-296 10.1021/jf00075a002
7. Theil, E. C. Iron, ferritin, and nutrition Annu. Rev. Nutr. 2004, 24, 327-343 10.1146/annurev.nutr.24.012003.132212
8. Hoppler, M.; Zeder, C.; Walczyk, T. Quantification of ferritin-bound iron in plant samples by isotope tagging and species-specific isotope dilution mass spectrometry Anal. Chem. 2009, 81, 7368-7372 10.1021/ac900885j
9. Lukac, R. J.; Aluru, M. R.; Reddy, M. B. Quantification of ferritin from staple food crops J. Agric. Food Chem. 2009, 57, 2155-2161 10.1021/jf803381d
10. Zielinska-Dawidziak, M.; Hertig, I.; Piasecka-Kwiatkowska, D.; Staniek, H.; Nowak, K. W.; Twardowski, T. Study on iron availability from prepared soybean sprouts using an iron-deficient rat model Food Chem. 2012, 135, 2622-7 10.1016/j.foodchem.2012.06.113
11. Beard, J. L.; Burton, J. W.; Theil, E. C. Purified ferritin and soybean meal can be sources of iron for treating iron deficiency in rats J. Nutr. 1996, 126, 154-160
12. Davila-Hicks, P.; Theil, E. C.; Lonnerdal, B. Iron in ferritin or in salts (ferrous sulfate) is equally bioavailable in nonanemic women Am. J. Clin. Nutr. 2004, 80, 936-940
13. Lonnerdal, B. The importance and bioavailability of phytoferritin-bound iron in cereals and legume foods Int. J. Vitam. Nutr. Res. 2007, 77, 152-7 10.1024/0300-9831.77.3.152
14. Kalgaonkar, S.; Lönnerdal, B. Effects of dietary factors on iron uptake from ferritin by Caco-2 cells J. Nutr. Biochem. 2008, 19, 33-9 10.1016/j.jnutbio.2007.02.001
15. Theil, E. C.; Chen, H.; Miranda, C.; Janser, H.; Elsenhans, B.; Nunez, M. T.; Pizarro, F.; Schumann, K. Absorption of iron from ferritin is independent of heme iron and ferrous salts in women and rat intestinal segments J. Nutr. 2012, 142, 478-83 10.3945/jn.111.145854
16. San Martin, C. D.; Garri, C.; Pizarro, F.; Walter, T.; Theil, E. C.; Nunez, M. T. Caco-2 intestinal epithelial cells absorb soybean ferritin by mu2 (AP2)-dependent endocytosis J. Nutr. 2008, 138, 659-666
17. Kalgaonkar, S.; Lonnerdal, B. Receptor-mediated uptake of ferritin-bound iron by human intestinal Caco-2 cells J. Nutr. Biochem. 2009, 20, 304-11 10.1016/j.jnutbio.2008.04.003
18. Shayeghi, M.; Latunde-Dada, G. O.; Oakhill, J. S.; Laftah, A. H.; Takeuchi, K.; Halliday, N.; Khan, Y.; Warley, A.; McCann, F. E.; Hider, R. C.; Frazer, D. M.; Anderson, G. J.; Vulpe, C. D.; Simpson, R. J.; McKie, A. T. Identification of an intestinal heme transporter Cell 2005, 122, 789-801 10.1016/j.cell.2005.06.025
19. Theil, E. C. Iron homeostasis and nutritional iron deficiency J. Nutr. 2011, 141, 724S-728S 10.3945/jn.110.127639
20. Masuda, H.; Aung, M. S.; Nishizawa, N. K. Iron biofortification of rice using different transgenic approaches Rice (N Y) 2013, 6, 40 10.1186/1939-8433-6-40
21. Yoshihara, T.; Takaiwa, F.; Goto, F.; Shigemoto, N.; Toki, S. Iron fortification of rice seed by the soybean ferritin gene Nat. Biotechnol. 1999, 17, 282-286 10.1038/7029
22. Drakakaki, G.; Christou, P.; Stoger, E. Constitutive expression of soybean ferritin cDNA in transgenic wheat and rice results in increased iron levels in vegetative tissues but not in seeds Transgenic Res. 2000, 9, 445-452 10.1023/A:1026534009483
23. Drakakaki, G.; Marcel, S.; Glahn, R. P.; Lund, E. K.; Pariagh, S.; Fischer, R.; Christou, P.; Stoger, E. Endosperm-specific co-expression of recombinant soybean ferritin and Aspergillus phytase in maize results in significant increases in the levels of bioavailable iron Plant Mol. Biol. 2005, 59, 869-80 10.1007/s11103-005-1537-3
24. Wirth, J.; Poletti, S.; Aeschlimann, B.; Yakandawala, N.; Drosse, B.; Osorio, S.; Tohge, T.; Fernie, A. R.; Gunther, D.; Gruissem, W.; Sautter, C. Rice endosperm iron biofortification by targeted and synergistic action of nicotianamine synthase and ferritin Plant Biotechnol. J. 2009, 7, 631-44 10.1111/j.1467-7652.2009.00430.x
25. Kumar, G. B.; Srinivas, L.; Ganapathi, T. R. Iron fortification of banana by the expression of soybean ferritin Biol. Trace Elem. Res. 2011, 142, 232-41 10.1007/s12011-010-8754-6
26. Zielińska-Dawidziak, M. Plant Ferritin-A Source of iron to prevent its deficiency Nutrients 2015, 7, 1184-1201 10.3390/nu7021184
27. Renkema, J. M.; van Vliet, T. Heat-induced gel formation by soy proteins at neutral pH J. Agric. Food Chem. 2002, 50, 1569-73 10.1021/jf010763l
28. Riblett, A. L.; Herald, T. J.; Schmidt, K. A.; Tilley, K. A. Characterization of beta-conglycinin and glycinin soy protein fractions from four selected soybean genotypes J. Agric. Food Chem. 2001, 49, 4983-9 10.1021/jf0105081
29. Masuda, T.; Goto, F.; Yoshihara, T. A novel plant ferritin subunit from soybean that is related to a mechanism in iron release J. Biol. Chem. 2001, 276, 19575-19579 10.1074/jbc.M011399200
30. Masuda, T.; Goto, F.; Yoshihara, T.; Mikami, B. The universal mechanism for iron translocation to the ferroxidase site in ferritin, which is mediated by the well conserved transit site Biochem. Biophys. Res. Commun. 2010, 400, 94-99 10.1016/j.bbrc.2010.08.017
31. Masuda, T.; Morimoto, S.-I.; Mikami, B.; Toyohara, H. The extension peptide of plant ferritin from sea lettuce contributes to shell stability and surface hydrophobicity Protein Sci. 2012, 21, 786-796 10.1002/pro.2061
32. Masuda, T.; Goto, F.; Yoshihara, T.; Mikami, B. Crystal structure of plant ferritin reveals a novel metal binding site that functions as a transit site for metal transfer in ferritin J. Biol. Chem. 2010, 285, 4049-4059 10.1074/jbc.M109.059790
33. Theil, E. C.; Liu, X. S.; Tosha, T. Gated pores in the ferritin protein nanocage Inorg. Chim. Acta 2008, 361, 868-874 10.1016/j.ica.2007.08.025
34. Williams, S. M.; Chandran, A. V.; Vijayabaskar, M. S.; Roy, S.; Balaram, H.; Vishveshwara, S.; Vijayan, M.; Chatterji, D. A histidine aspartate ionic lock gates the iron passage in miniferritins from Mycobacterium smegmatis J. Biol. Chem. 2014, 289, 11042-58 10.1074/jbc.M113.524421
35. Hasan, M. R.; Tosha, T.; Theil, E. C. Ferritin contains less iron (59Fe) in cells when the protein pores are unfolded by mutation J. Biol. Chem. 2008, 283, 31394-400 10.1074/jbc.M806025200
36. Jin, W.; Takagi, H.; Pancorbo, B.; Theil, E. C. 'Opening' the ferritin pore for iron release by mutation of conserved amino acids at interhelix and loop sites Biochemistry 2001, 40, 7525-32 10.1021/bi002509c
37. Skikne, B.; Fonzo, D.; Lynch, S. R.; Cook, J. D. Bovine ferritin iron bioavailability in man Eur. J. Clin. Invest. 1997, 27, 228-33 10.1046/j.1365-2362.1997.970645.x
38. Bejjani, S.; Pullakhandam, R.; Punjal, R.; Nair, K. M. Gastric digestion of pea ferritin and modulation of its iron bioavailability by ascorbic and phytic acids in caco-2 cells World J. Gastroenterol. 2007, 13, 2083-2088
39. Lv, C.; Zhao, G.; Lönnerdal, B. Bioavailability of iron from plant and animal ferritins J. Nutr. Biochem. 2015, 26, 532-540 10.1016/j.jnutbio.2014.12.006
40. Murray-Kolb, L. E.; Welch, R.; Theil, E. C.; Beard, J. L. Women with low iron stores absorb iron from soybeans Am. J. Clin. Nutr. 2003, 77, 180-184
41. Lönnerdal, B. Soybean ferritin: implications for iron status of vegetarians Am. J. Clin. Nutr. 2009, 89, 1680S-1685S 10.3945/ajcn.2009.26736W
42. Wade, V. J.; Treffry, A.; Laulhere, J. P.; Bauminger, E. R.; Cleton, M. I.; Mann, S.; Briat, J. F.; Harrison, P. M. Structure and composition of ferritin cores from pea seed (Pisum sativum) Biochim. Biophys. Acta, Protein Struct. Mol. Enzymol. 1993, 1161, 91-96 10.1016/0167-4838(93)90201-2
43. Treffry, A.; Harrison, P. M.; Cleton, M. I.; de Bruijn, W. C.; Mann, S. A note on the composition and properties of ferritin iron cores J. Inorg. Biochem. 1987, 31, 1-6 10.1016/0162-0134(87)85001-8
44. Hoppler, M.; Schonbachler, A.; Meile, L.; Hurrell, R. F.; Walczyk, T. Ferritin-iron is released during boiling and in vitro gastric digestion J. Nutr. 2008, 138, 878-884
45. Morimoto, S.; Masuda, T.; Sugihara, I.; Toyohara, H. Identification and characterization of a ferritin gene and its product from the multicellular green alga Ulva pertusa Biosci., Biotechnol., Biochem. 2012, 76, 1913-9 10.1271/bbb.120400
46. Masuda, T.; Yamamoto, A.; Toyohara, H. The iron content and ferritin contribution in fresh, dried, and toasted nori Biosci., Biotechnol., Biochem. 2015, 79, 74-81 10.1080/09168451.2014.968087