Conjugation with alginate oligosaccharide via the controlled Maillard reaction in a dry state is an effective method for the preparation of salmon myofibrillar protein with excellent anti-inflammatory activity

Abstract

The efficacy of the controlled Maillard reaction with alginate oligosaccharide (AO) in a dry state was examined for development of an anti-inflammatory compound from fish myofibrillar protein (Mf). Lyophilized Mf from spawned-out chum salmon was mixed with AO (half of the total protein weight) and incubated at 60 °C and 35 % relative humidity for 0–6 h, followed by digestion with pepsin and trypsin. The anti-inflammatory activity of the digested peptide was improved with the progress of the AO conjugation, and dMSA4 (prepared from Mf–AO conjugate by reaction for 4 h, with 49.6 μg/mg protein of AO attached) was most effective in inhibiting secretions of inflammation-related compounds in lipopolysaccharide (LPS)-stimulated RAW264.7 macrophages. Likewise, dMSA4 suppressed the LPS-induced gene and protein expression of inducible nitric oxide synthase, tumor necrosis factor-α, interleukin-6, and cyclooxygenase (COX)-2, while COX-1 expression was unaffected. Furthermore, oral administration of dMSA4 and the Mf–AO conjugate prior to proteolysis inhibited carrageenan-induced paw volume expansion in mice. These results indicate that AO conjugation using the controlled Maillard reaction in a dry state is a useful approach for enhancing the anti-inflammatory activity of salmon Mf as a nutraceutical food material.

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References

  1. 1.

    Chen GY, Nuñez G (2010) Sterile inflammation: sensing and reacting to damage. Nat Rev Immunol 10:826–837

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  2. 2.

    Daniel K, Podlsky MD (2002) Inflammatory bowel disease. N Engl J Med 347:417–429

    Article  Google Scholar 

  3. 3.

    Pearson TA, Mensah GA, Alexander RW, Anderson JL, Cannon RO, Criqui M, Fadl YY, Fortmann SP, Hong Y, Myers GL, Rifai N, Smith SC, Taubert K, Tracy RP, Vinicor F (2003) Markers of inflammation and cardiovascular disease: application to clinical and public health practice: a statement for healthcare professionals from the centers for disease control and prevention and the American Heart Association. Circulation 107:499–511

    Article  PubMed  Google Scholar 

  4. 4.

    Glass CK, Saijo K, Winner B, Marchetto MC, Gage FH (2010) Mechanisms underlying inflammation in neurodegeneration. Cell 140:918–934

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  5. 5.

    Wellen KE, Hotamisligil GS (2005) Inflammation, stress, and diabetes. J Clin Invest 115:1111–1119

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  6. 6.

    Wu X, Schauss AG (2012) Mitigation of inflammation with foods. J Agric Food Chem 60:6703–6717

    CAS  Article  PubMed  Google Scholar 

  7. 7.

    Chan MM, Fong D, Ho CT, Huang HI (1997) Inhibition of inducible nitric oxide synthase gene expression and enzyme activity by epigallocatechin gallate, a natural product from green tea. Biochem Pharmacol 54:1281–1286

    CAS  Article  PubMed  Google Scholar 

  8. 8.

    Lin YL, Tsai SH, Lin-Shiau SY, Ho CT, Linet JK (1999) Theaflavin-3,3′-digallate from black tea blocks the nitric oxide synthase by down-regulating the activation of NF-kappaB in macrophages. Eur J Pharmacol 367:379–388

    CAS  Article  PubMed  Google Scholar 

  9. 9.

    Ren J, Chung SH (2007) Anti-inflammatory effect of alpha-linolenic acid and its mode of action through the inhibition of nitric oxide production and inducible nitric oxide synthase gene expression via NF-kappaB and mitogen-activated protein kinase pathways. J Agric Food Chem 55:5073–5080

    CAS  Article  PubMed  Google Scholar 

  10. 10.

    Kim JA, Kong CS, Pyun SY, Kim SK (2010) Phosphorylated glucosamine inhibits the inflammatory response in LPS-stimulated PMA-differentiated THP-1 cells. Carbohydr Res 345:1851–1855

    CAS  Article  PubMed  Google Scholar 

  11. 11.

    Wang J, Mazza G (2002) Inhibitory effects of anthocyanins and other phenolic compounds on nitric oxide production in LPS/IFN-γ-activated. J Agric Food Chem 50:850–857

    CAS  Article  PubMed  Google Scholar 

  12. 12.

    Yamaguchi M, Yoshida K, Uchida M (2009) Novel functions of bovine milk-derived alpha-lactalbumin: anti-nociceptive and anti-inflammatory activity caused by inhibiting cyclooxygenase-2 and phospholipase A2. Biol Pharm Bull 32:366–371

    CAS  Article  PubMed  Google Scholar 

  13. 13.

    Hartog A, Leenders I, van der Kraan PM, Garssen J (2007) Anti-inflammatory effects of orally ingested lactoferrin and glycine in different zymosan-induced inflammation models: evidence for synergistic activity. Int Immunopharmacol 7:1784–1792

    CAS  Article  PubMed  Google Scholar 

  14. 14.

    FAO Fisheries and Aquaculture Department (2012) The state of world fisheries and aquaculture 2012. Food and Agriculture Organization of the United Nations, Rome, pp 3–5

    Google Scholar 

  15. 15.

    Je JY, Park PJ, Kwon JY, Kim SK (2004) A novel angiotensin I converting enzyme inhibitory peptide from Alaska pollack (Theragra chalcogramma) frame protein hydrolysate. J Agric Food Chem 52:7842–7845

    CAS  Article  PubMed  Google Scholar 

  16. 16.

    Ren J, Wang H, Zhao M, Cui C, Hu X (2010) Enzymatic hydrolysis of grass carp myofibrillar protein and antioxidant properties of hydrolysates. Czech J Food Sci 28:475–484

    CAS  Google Scholar 

  17. 17.

    Lavigne C, Tremblay F, Asselin G, Jacques H, Marette A (2001) Prevention of skeletal muscle insulin resistance by dietary cod protein in high fat-fed rats. Am J Physiol Endocrinol Metab 281:E62–E71

    CAS  PubMed  Google Scholar 

  18. 18.

    Ryan JT, Ross RP, Bolton D, Fitzgerald GF, Stanton C (2012) Bioactive peptides from muscle sources: meat and fish. Nutrients 3:765–791

    Article  Google Scholar 

  19. 19.

    Saeki H (2012) Protein–saccharide interaction. In: Hettiarachchy NS et al (eds) Food proteins and peptide, chemistry, functionality, interactions and commercialization. CRC Press, New York, pp 230–261

    Google Scholar 

  20. 20.

    Nakamura S, Ogawa M, Nakai S, Kato A, Kitts DD (1998) Antioxidant activity of a maillard-type phosvitin-galactomannan conjugate with emulsifying properties and heat stability. J Agric Food Chem 46:3958–3963

    CAS  Article  Google Scholar 

  21. 21.

    Junfeng F, Yanyan Z, Szesze T, Fengjuan L, Manyu Z, Saito M, Eizo Tatsumi E, Lite L (2006) Improving functional properties of soy protein hydrolysate by conjugation with curdlan. J Food Sci 71:C285–C291

    Article  Google Scholar 

  22. 22.

    Nakamura S, Kato A (2000) Multi-functional biopolymer prepared by covalent attachment of galactomannan to egg-white proteins through naturally occurring Maillard reaction. Nahrung 44:201–206

    CAS  Article  PubMed  Google Scholar 

  23. 23.

    Iwan M, Vissers YM, Fiedorowicz E, Kostyra H, Kostyra E, Savelkoul HF, Wichers HJ (2011) Impact of Maillard reaction on immunoreactivity and allergenicity of the hazelnut allergen Cor a 11. J Agric Food Chem 59:7163–7171

    CAS  Article  PubMed  Google Scholar 

  24. 24.

    Isono M, Saeki H, Nishimura K (2012) Properties of glycated chicken myofibrillar proteins with enhanced antioxidant abilities. J Home Econ Jpn 63:461–468

    CAS  Google Scholar 

  25. 25.

    Saigusa M, Nishizawa M, Shimizu Y, Saeki H (2015) In vitro and in vivo anti-inflammatory activity of digested peptides derived from salmon myofibrillar protein conjugated with a small quantity of alginate oligosaccharide. Biosci Biotechnol Biochem 79:1518–1527

    CAS  Article  PubMed  Google Scholar 

  26. 26.

    Sato R, Katayama S, Sawabe T, Saeki H (2003) Stability and emulsion-forming ability of water-soluble fish myofibrillar protein prepared by conjugation with alginate oligosaccharide. J Agric Food Chem 51:4376–4381

    CAS  Article  PubMed  Google Scholar 

  27. 27.

    Takeda H, Iida T, Okada A, Ootsuka H, Ohshita T, Masutani E, Katayama S, Saeki H (2007) Feasibility study on water solubilization of spawned out salmon meat by conjugation with alginate oligosaccharide. Fish Sci 73:924–930

    CAS  Article  Google Scholar 

  28. 28.

    Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    CAS  Article  PubMed  Google Scholar 

  29. 29.

    Zacharius RM, Zell TE, Morrison JH, Woodlock JJ (1969) Glycoprotein staining following electrophoresis on acrylamide gels. Anal Biochem 30:148–152

    CAS  Article  PubMed  Google Scholar 

  30. 30.

    Gornall AG, Bardawill CJ, David MM (1949) Determination of serum proteins by means of the biuret reaction. J Biol Chem 177:751–766

    CAS  PubMed  Google Scholar 

  31. 31.

    Dubois M, Gilles AK, Hamilton KJ, Rebers AP, Smith F (1956) Colorimetric method for determination of sugers and related substances. Anal Chem 28:350–356

    CAS  Article  Google Scholar 

  32. 32.

    Hernandez MJM, Alvarez-coque MCG (1992) Availble lysine in protein assay using o-phthalaldehyde/N-acetyl l-cysteine spectrophotometric method. J Food Sci 57:503–505

    Article  Google Scholar 

  33. 33.

    Baer HP, Schmidt K, Mayer B, Kukovetz WR (1995) Pentamidine does not interfere with nitrite formation in activated RAW 264.7 macrophages but inhibits constitutive brain nitric oxide synthase. Life Sci 57:1973–1980

    CAS  Article  PubMed  Google Scholar 

  34. 34.

    Suzuki K, Koh YH, Mizuno H, Hamaoka R, Taniguchi N (1998) Overexpression of aldehyde reductase protects PC12 cells from the cytotoxicity of methylglyoxal or 3-deoxyglucosone. J Biochem 123:353–357

    CAS  Article  PubMed  Google Scholar 

  35. 35.

    Kitts DD, Xiu-Min C, Hao J (2012) Demonstration of antioxidant and anti-inflammatory bioactivities from sugar-amino acid Maillard reaction products. J Agric Food Chem 60:6718–6727

    CAS  Article  PubMed  Google Scholar 

  36. 36.

    Okada N, Hirata A, Murakami Y, Shoji M, Sakagami H, Fujisawa S (2005) Induction of cytotoxicity and apoptosis and inhibition of cyclooxygenase-2 gene expression by eugenol-related compounds. Anticancer Res 25:3263–3269

    CAS  PubMed  Google Scholar 

  37. 37.

    Dubois RN, Abramson SB, Crofford L, Gupta RA, Simon LS, Van De Putte LB, Lipsky PE (1998) Cyclooxygenase in biology and disease. FASEB J 12:1063–1073

    CAS  PubMed  Google Scholar 

  38. 38.

    Jones MK, Wang H, Peskar BM, Levin E, Itani RM, Sarfeh IJ, Tarnawski AS (1999) Inhibition of angiogenesis by nonsteroidal anti-inflammatory drugs: insight into mechanisms and implications for cancer growth and ulcer healing. Nat Med 5:1418–1423

    CAS  Article  PubMed  Google Scholar 

  39. 39.

    Egan LJ, Toruner M (2006) NF-kappaB signaling: pros and cons of altering NF-kappaB as a therapeutic approach. Ann N Y Acad Sci 1072:114–122

    CAS  Article  PubMed  Google Scholar 

  40. 40.

    Håversen L, Ohlsson BG, Hahn-Zoric M, Hanson LA, Mattsby-Baltzer I (2002) Lactoferrin down-regulates the LPS-induced cytokine production in monocytic cells via NF-kappa B. Cell Immunol 220:83–95

    Article  PubMed  Google Scholar 

  41. 41.

    De Mejia EG, Dia VP (2009) Lunasin and lunasin-like peptides inhibit inflammation through suppression of NF-kappaB pathway in the macrophage. Peptides 30:2388–2398

    Article  PubMed  Google Scholar 

  42. 42.

    Singh S, Aggarwal BB (1995) Activation of transcription factor NF-kappaB is suppressed by curcumin (diferuloylmethane). J Biol Chem 270:24995–25000

    CAS  Article  PubMed  Google Scholar 

  43. 43.

    Cuzzocrea S, Sautebin L, De Sarro G, Costantino G, Rombolà L, Mazzon E, Ialenti A, De Sarro A, Ciliberto G, Di Rosa M, Caputi AP, Thiemermann C (1999) Role of IL-6 in the pleurisy and lung injury caused by carrageenan. J Immunol 163:5094–5104

    CAS  PubMed  Google Scholar 

  44. 44.

    Tan-No K, Nakajima T, Shoji T, Nakagawasai O, Niijima F, Ishikawa M, Endo Y, Sato T, Satoh S, Tadano T (2006) Anti-inflammatory effect of propolis through inhibition of nitric oxide production on carrageenin-induced mouse paw edema. Biol Pharm Bull 29:96–99

    CAS  Article  PubMed  Google Scholar 

  45. 45.

    Omote K, Hazama K, Kawamata T, Kawamata M, Nakayaka Y, Toriyabe M, Namiki A (2001) Peripheral nitric oxide in carrageenan-incuced inflammation. Brain Res 912:171–175

    CAS  Article  PubMed  Google Scholar 

  46. 46.

    Sato R, Sawabe T, Saeki H (2005) Characterization of fish myofibrillar protein by conjugation with alginate oligosaccharide prepared using genetic recombinant alginate lyase. J Food Sci 70:58–62

    Article  Google Scholar 

  47. 47.

    Sato R, Sawabe T, Kishimura H, Hayashi K, Saeki H (2000) Preparation of neoglycoprotein from carp myofibrillar protein and alginate oligosaccharide: improved solubility in low ionic strength medium. J Agric Food Chem 48:17–21

    CAS  Article  PubMed  Google Scholar 

  48. 48.

    Maitena U, Katayama S, Sato R, Saeki H (2004) Improved solubility and stability of carp myosin by conjugation with alginate oligosaccharide. Fish Sci 70:896–902

    CAS  Article  Google Scholar 

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Acknowledgments

We deeply appreciate the technical assistance of Mr. Yutaka Shimizu, Ph.D., Hokkaido University, for instruction on immunoblotting strategy. We deeply appreciate Hideki Kishimura, Associate Professor, Hokkaido University, for instruction on PCR strategy. We thank Hokkaido Mitsui Chemical Industry Co., Ltd., for supplying alginate oligosaccharide. Part of this work was supported by the Japan Science and Technology Agency, A-STEP Program (FS stage), 2010.

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Correspondence to Hiroki Saeki.

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Nishizawa, M., Saigusa, M. & Saeki, H. Conjugation with alginate oligosaccharide via the controlled Maillard reaction in a dry state is an effective method for the preparation of salmon myofibrillar protein with excellent anti-inflammatory activity. Fish Sci 82, 357–367 (2016). https://doi.org/10.1007/s12562-015-0959-3

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Keywords

  • Alginate oligosaccharide
  • Anti-inflammation
  • Maillard reaction
  • Muscle protein
  • Salmon