Abstract
In an effort to clarify whether the lipid-lowering effect of hemoglobin is due to globin protein or heme, this study investigated the effects of dietary porcine hemoglobin (PH) and porcine globin (PG) on lipids contents of serum, liver, and feces in rats. Five-week-old male Wistar rats were divided into 3 dietary groups of 7 rats each, with one group receiving a control diet and the other groups receiving diets containing 1.25% (w/w) PH or 1.18% (w/w) PG for 4 weeks. The PH diet decreased triacylglycerol content in serum and cholesterol in serum and liver, whereas the PG diet reduced triacylglycerol content in serum and cholesterol in liver. Fecal lipid excretion in the PH group was significantly higher than in the PG group. Therefore, PH affected lipid excretion to feces due to globin protein as well as heme.
Keywords: porcine hemoglobin, globin, heme, lipid excretion, cholesterol
References
- 1.Nowak B, von Mueffling T. Porcine blood cell concentrates for food products: Hygiene, composition, and preservation. J. Food Protect. 2006;69:2183–2192. doi: 10.4315/0362-028x-69.9.2183. [DOI] [PubMed] [Google Scholar]
- 2.In MJ, Kim DC, Chae HJ, Oh NS. Effects of degree of hydrolysis and pH on the solubility of heme-iron enriched peptide in hemoglobin hydrolysate. Biosci. Biotech. Bioch. 2003;67:365–367. doi: 10.1271/bbb.67.365. [DOI] [PubMed] [Google Scholar]
- 3.Nyberg F, Sanderson K, Glamsta EL. The hemorphins: A new class of opioid peptides derived from the blood protein hemoglobin. Biopolymers. 1997;43:147–156. doi: 10.1002/(SICI)1097-0282(1997)43:2<147::AID-BIP8>3.0.CO;2-V. [DOI] [PubMed] [Google Scholar]
- 4.Kagawa K, Matsutaka H, Fukuhama C, Watanabe Y, Fujino H. Globin digest, acidic protease hydrolysate, inhibits dietary hypertriglyceridemia and Val-Val-Tyr-Pro, one of its constituents, possesses most superior effect. Life Sci. 1996;58:1745–1755. doi: 10.1016/0024-3205(96)00156-7. [DOI] [PubMed] [Google Scholar]
- 5.Zhao QY, Piot JM, Gautier V, Cottenceau G. Isolation and characterization of a bacterial growth-stimulating peptide from a peptic bovine hemoglobin hydrolysate. Appl. Microbiol. Biot. 1996;45:778–784. doi: 10.1007/s002530050762. [DOI] [PubMed] [Google Scholar]
- 6.Fukunaga K, Yukawa N, Hosomi R, Nishiyama T, Yoshida M. Dietary combination of fish oil and hemoglobin hydrolysates alters serum and liver lipid contents in rat. Food Nutr. Sci. 2013;4:86–93. doi: 10.4236/fns.2013.49A1014. [DOI] [Google Scholar]
- 7.Sun Q, Luo Y. Porcine hemoglobin hydrolysate prepared with pepsin: Antioxidant activities and their mechanisms. Int. J. Food Prop. 2011;14:840–853. doi: 10.1080/10942910903453405. [DOI] [Google Scholar]
- 8.Jayathilakan K, Sultana K, Radhakrishna K, Bawa AS. Utilization of byproducts and waste materials from meat, poultry and fish processing industries: A review. J. Food Sci. Technol. 2012;49:278–293. doi: 10.1007/s13197-011-0290-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Hosomi R, Fukunaga K, Nishiyama T, Yoshida M. Effects of porcine hemoglobin on serum lipid content and fecal lipid excretion in rats. J. Med. Food. 2014;17:302–309. doi: 10.1089/jmf.2013.2843. [DOI] [PubMed] [Google Scholar]
- 10.Yip YK, Waks M, Beychok S. Reconstitution of native human hemoglobin from separated globin chains and alloplex intermediates. P. Natl. Acad. Sci. USA. 1977;74:64–68. doi: 10.1073/pnas.74.1.64. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.White JA, Hart RJ, Fry JC. An evaluation of the Waters Pico-Tag system for the amino-acid analysis of food materials. J. Autom. Chem. 1986;8:170–177. doi: 10.1155/S1463924686000330. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227:680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
- 13.Reeves PG, Nielsen FH, Fahey G Jr. AIN-93 purified diets for laboratory rodents: Final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J. Nutr. 1993;123:1939–1951. doi: 10.1093/jn/123.11.1939. [DOI] [PubMed] [Google Scholar]
- 14.Horton JD, Bashmakov Y, Shimomura I, Shimano H. Regulation of sterol regulatory element binding proteins in livers of fasted and refed mice. P. Natl. Acad. Sci. USA. 1998;95:5987–5992. doi: 10.1073/pnas.95.11.5987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Rouser G, Fkeischer S, Yamamoto A. Two dimensional thin layer chromatographic separation of polar lipids and determination of phospholipids by phosphorus analysis of spots. Lipids. 1970;5:494–496. doi: 10.1007/BF02531316. [DOI] [PubMed] [Google Scholar]
- 16.Van De Kamer JH, Bokkel Huinink HT, Weyers HA. Rapid method for the determination of fat in feces. J. Biol. Chem. 1949;177:347–355. [PubMed] [Google Scholar]
- 17.Hosomi R, Fukunaga K, Arai H, Kanda S, Nishiyama T, Yoshida M. Effect of combination of dietary fish protein and fish oil on lipid metabolism in rats. J. Food Sci. Technol. 2013;50:266–274. doi: 10.1007/s13197-011-0343-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Ide T, Hong DD, Ranasinghe P, Takahashi Y, Kushiro M, Sugano M. Interaction of dietary fat types and sesamin on hepatic fatty acid oxidation in rats. Biochim. Biophys. Acta. 2004;1682:80–91. doi: 10.1016/j.bbalip.2004.02.001. [DOI] [PubMed] [Google Scholar]
- 19.Markwell MA, McGroarty EJ, Bieber LL, Tolbert NE. The subcellular distribution of carnitine acyltransferases in mammalian liver and kidney. A new peroxisomal enzyme. J. Biol. Chem. 1973;248:3426–3432. [PubMed] [Google Scholar]
- 20.Tanabe T, Nakanishi S, Hashimoto T, Ogiwara H, Nikawa JI, Numa S. [1] Acetyl-CoA carboxylase from rat liver: EC 6.4.1.2 Acetyl-CoA: Carbon-dioxide ligase (ADP-forming) Method Enzymol. 1981;71:5–16. doi: 10.1016/0076-6879(81)71003-6. [DOI] [PubMed] [Google Scholar]
- 21.Kelley DS, Nelson GJ, Hunt JE. Effect of prior nutritional status on the activity of lipogenic enzymes in primary monolayer cultures of rat hepatocytes. Biochem. J. 1986;235:87–90. doi: 10.1042/bj2350087. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Hsu RY, Lardy HA. Malic enzyme. In: Lowebsein LM, editor. Methods Enzymol. 1969. pp. 230–235. [Google Scholar]
- 23.Kelley DS, Kletzien RF. Ethanol modulation of the hormonal and nutritional regulation of glucose 6-phosphate dehydrogenase activity in primary cultures of rat hepatocytes. Biochem. J. 1984;217:543–549. doi: 10.1042/bj2170543. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 1951;193:265–275. [PubMed] [Google Scholar]
- 25.Hall WL, Millward DJ, Long SJ, Morgan LM. Casein and whey exert different effects on plasma amino acid profiles, gastrointestinal hormone secretion and appetite. Br. J. Nutr. 2003;89:239–248. doi: 10.1079/BJN2002760. [DOI] [PubMed] [Google Scholar]
- 26.Uzel C, Conrad ME. Absorption of heme iron. Semin. Hematol. 1998;35:27–34. [PubMed] [Google Scholar]
- 27.Matsumoto J, Mori N, Doi M, Kishida T, Ebihara K. Evaluation of iron bioavailability from bonito dark muscle using anemic rats. J. Agr. Food Chem. 2003;51:4478–4482. doi: 10.1021/jf021246l. [DOI] [PubMed] [Google Scholar]
- 28.Uemura K, Hosomi R, Fukunaga K, Nishiyama T, Yoshida M. Effect of difference in chemical species of dietary iron on iron status in rats. Trace Nutr. Res. 2010;27:13–16. [Google Scholar]
- 29.Moriyama T, Kishimoto K, Nagai K, Urade R, Ogawa T, Utsumi S, Maruyama N, Maebuchi M. Soybean beta-conglycinin diet suppresses serum triglyceride levels in normal and genetically obese mice by induction of beta-oxidation, downregulation of fatty acid synthase, and inhibition of triglyceride absorption. Biosci. Biotech. Bioch. 2004;68:352–359. doi: 10.1271/bbb.68.352. [DOI] [PubMed] [Google Scholar]
- 30.Hosomi R, Miyauchi K, Yamamoto D, Arai H, Nishiyama T, Yoshida M, Fukunaga K. Salmon protamine decreases serum and liver lipid contents by Inhibiting lipid absorption in an in vitro gastrointestinal digestion model and in rats. J. Food Sci. 2015;80:2346–2353. doi: 10.1111/1750-3841.13003. [DOI] [PubMed] [Google Scholar]
- 31.Okazaki Y, Tomotake H, Tsujimoto K, Sasaki M, Kato N. Consumption of a resistant protein, sericin, elevates fecal immunoglobulin A, mucins, and cecal organic acids in rats fed a high-fat diet. J. Nutr. 2011;141:1975–1981. doi: 10.3945/jn.111.144246. [DOI] [PubMed] [Google Scholar]
- 32.Morita T, Oh-hashi A, Takei K, Ikai M, Kasaoka S, Kiriyama S. Cholesterollowering effects of soybean, potato and rice proteins depend on their low methionine contents in rats fed a cholesterol-free purified diet. J. Nutr. 1997;127:470–477. doi: 10.1093/jn/127.3.470. [DOI] [PubMed] [Google Scholar]
- 33.Nagata Y, Ishiwaki N, Sugano M. Studies on the mechanism of antihypercholesterolemic action of soy protein and soy protein-type amino acid mixtures in relation to the casein counterparts in rats. J. Nutr. 1982;112:1614–1625. doi: 10.1093/jn/112.8.1614. [DOI] [PubMed] [Google Scholar]
- 34.Higaki N, Sato K, Suda H, Suzuka T, Komori T, Saeki T, Nakamura Y, Ohtsuki K, Iwami K, Kanamoto R. Evidence for the existence of a soybean resistant protein that captures bile acid and stimulates its fecal excretion. Biosci. Biotech. Bioch. 2006;70:2844–2852. doi: 10.1271/bbb.60237. [DOI] [PubMed] [Google Scholar]
- 35.Ma Y, Xiong YL. Antioxidant and bile acid binding activity of buckwheat protein in vitro digests. J. Agr. Food Chem. 2009;57:4372–4380. doi: 10.1021/jf803670u. [DOI] [PubMed] [Google Scholar]
- 36.Ijssennagger N, de Wit N, Muller M, van der Meer R. Dietary heme-mediated PPARalpha activation does not affect the heme-induced epithelial hyperproliferation and hyperplasia in mouse colon. PLoS ONE. 2012;7:e43260. doi: 10.1371/journal.pone.0043260. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37.Sesink AL, Termont DS, Kleibeuker JH, Van Der Meer R. Red meat and colon cancer: Dietary haem, but not fat, has cytotoxic and hyperproliferative effects on rat colonic epithelium. Carcinogenesis. 2000;21:1909–1915. doi: 10.1093/carcin/21.10.1909. [DOI] [PubMed] [Google Scholar]
