Colloidal aspects of protein digestion

Current Opinion in Colloid and Interface Science

Volumn 15, Issue 1-2, 2010, Pages 102-108

  Mackie, Alan ^a   Macierzanka, Adam ^a  

^a NORWICH RESEARCH PARK   (United Kingdom)

Author keywords

Biosurfactant; Digestion; Emulsion; Enzyme; Interface; Protein

Indexed keywords

ALLERGENIC PROTEIN; ANIMAL EXPERIMENTS; BILE ACID; BIOSURFACTANT; CLEAVAGE SITES; COLLOIDAL ASPECT; COLLOIDAL INTERACTION; DIGESTION; DIGESTION PROCESS; GASTROINTESTINAL TRACT; HEALTH ISSUES; IN-VITRO; LOCAL FLEXIBILITY; MILK PROTEIN; PROTECTIVE EFFECTS; PROTEIN DIGESTION; SMALL INTESTINE;

ADSORPTION; BIOMOLECULES; EMULSIFICATION; ENZYMES; PHOSPHOLIPIDS; RESEARCH;

SURFACE ACTIVE AGENTS;

BILE ACID; ENZYME; LIPID; MILK PROTEIN; PHOSPHOLIPID; PROTEIN; SURFACTANT;

ADSORPTION; COLLOID; DIGESTION; EMULSION; FOOD; GASTROINTESTINAL TRACT; HEALTH; HUMAN; IN VITRO STUDY; MEDICAL RESEARCH; NONHUMAN; NUTRITION; PHYSIOLOGY; PROTEIN DEGRADATION; PROTEIN PROCESSING; PROTEIN PURIFICATION; REVIEW; SMALL INTESTINE; STOMACH;

EID: 75849141780     PISSN: 13590294     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cocis.2009.11.005     Document Type: Review

References (54)

1. Mun S., Decker E.A., and McClements D.J. Influence of emulsifier type on in vitro digestibility of lipid droplets by pancreatic lipase. Food Res Int 40 (2007) 770-781. This article was one of the first published looking at the possibility of using the interfacial layer of an emulsion to control rates of lipolysis and subsequently satiety through the "ileal brake", which requires the presence of lipid in the ileum.
2. Foltz M., Ansems P., Schwarz J., Tasker M.C., Lourbakos A., and Gerhardt C.C. Protein hydrolysates induce CCK release from enteroendocrine cells and act as partial agonists of the CCK1 receptor. J Agric Food Chem 56 (2008) 837-843
3. Moreno F.J. Gastrointestinal digestion of food allergens: effect on their allergenicity. Biomed Pharmacother 61 (2007) 50-60. Moreno looks at the development of more physiologically relevant in vitro digestion models as a tool for assessing allergenic potential in food protein.
4. Kneepkens C.M., and Meijer Y. Clinical practice. Diagnosis and treatment of cow's milk allergy. Eur J Pediatr 168 (2009) 891-896
5. Sinn J., and Osborn D.A. Formulas containing hydrolysed protein for prevention of allergy and food intolerance in infants. Cochrane Database Syst Rev (2006) CD003664
6. Untersmayr E., and Jensen-Jarolim E. Mechanisms of type I food allergy. Pharmacol Ther 112 (2006) 787-798
7. Jenkins J.A., Breiteneder H., and Mills E.N. Evolutionary distance from human homologs reflects allergenicity of animal food proteins. J Allergy Clin Immunol 120 (2007) 1399-1405. This paper is the first to address the philo-genetic importance of small differences in protein structure with regard to their allergenic potential. The paper compares animal protein structures with the structures of the same proteins found in humans.
8. Jenkins J.A., Griffiths-Jones S., Shewry P.R., Breiteneder H., and Mills E.N. Structural relatedness of plant food allergens with specific reference to cross-reactive allergens: an in silico analysis. J Allergy Clin Immunol 115 (2005) 163-170. This was the first paper to analyse the protein folds of an extensive list of allergenic proteins and showed that 67% of plant food allergens belong to just 4 fold families.
9. Bublin M., Radauer C., Knulst A., Wagner S., Scheiner O., Mackie A.R., et al. Effects of gastrointestinal digestion and heating on the allergenicity of the kiwi allergens Act d 1, actinidin, and Act d 2, a thaumatin-like protein. Mol Nutr Food Res 52 (2008) 1130-1139
10. Lucas J.S., Cochrane S.A., Warner J.O., and Hourihane J.O. The effect of digestion and pH on the allergenicity of kiwifruit proteins. Pediatr Allergy Immunol 19 (2008) 392-398
11. Eiwegger T., Rigby N., Mondoulet L., Bernard H., Krauth M.T., Boehm A., et al. Gastro-duodenal digestion products of the major peanut allergen Ara h 1 retain an allergenic potential. Clin Exp Allergy 36 (2006) 1281-1288. This article highlights the complexity of both immune disease and the digestive process in a very clear way, showing that proteins can still be allergenic even after extensive digestion.
12. Adel-Patient K., Bernard H., and Wal J.M. Fate of food allergens in the digestive tract. Revue Francaise d'Allergie et d'Immunologie Clinique 48 (2008) 335-343
13. Stanciuc N., van der Plancken I., Rotaru G., and Hendrickx M. Denaturation impact in susceptibility of beta-lactoglobulin to enzymatic hydrolysis: a kinetic study. Review Roumaine de Chemie 53 (2008) 921-929
14. Peyron S., Mouecoucou J., Fremont S., Sanchez C., and Gontard N. Effects of heat treatment and pectin addition on beta-lactoglobulin allergenicity. J Agric Food Chem 54 (2006) 5643-5650
15. Chicon R., Belloque J., Alonso E., and Lopez-Fandino R. Immuno reactivity and digestibility of high-pressure-treated whey proteins. Int Dairy J 18 (2008) 367-376
16. Chicon R., Lopez-Fandino R., Alonso E., and Belloque J. Proteolytic pattern, antigenicity, and serum immunoglobulin E binding of beta-lactoglobulin hydrolysates obtained by pepsin and high-pressure treatments. J Dairy Sci 91 (2008) 928-938. The article highlights the use of novel processing (high pressure) and more importantly the adiabatic heating it induces to denature proteins and thus make them more susceptible to proteolysis. Again the results showed that digestion does not readily remove the immunogenic capacity of the protein.
17. Zeece M., Huppertz T., and Kelly A. Effect of high-pressure treatment on in-vitro digestibility of beta-lactoglobulin. Innovative Food Science & Emerging Technologies 9 (2008) 62-69
18. Mariniello L., Giosafatto C.V., Di P.P., Sorrentino A., and Porta R. Synthesis and resistance to in vitro proteolysis of transglutaminase cross-linked phaseolin, the major storage protein from Phaseolus vulgaris. J Agric Food Chem 55 (2007) 4717-4721
19. Tsoukala A., Papalamprou E., Makri E., Doxastakis G., and Braudo E.E. Adsorption at the air-water interface and emulsification properties of grain legume protein derivatives from pea and broad bean. Colloids Surf, B Biointerfaces 53 (2006) 203-208
20. Hur S.J., Decker E.A., and McClements D.J. Influence of initial emulsifier type on microstructural changes occurring in emulsified lipids during in vitro digestion. Food Chem 114 (2009) 253-262. This paper builds on previous work by the group and introduces for the first time an in vitro model that includes oral, gastric and duodenal processing. Several individual, contrasting food emulsifiers were used to produce emulsions for digestion. The type of emulsifier had only a limited effect on the microstructural changes of the emulsions being digested. However, the authors pointed out that this was in contrast to in vivo studies performed by others, and emphasised the need for more realistic in vitro models of digestion.
21. Reis P.M., Raab T.W., Chuat J.Y., Leser M.E., Miller R., Watzke H.J., et al. Influence of surfactants on lipase fat digestion in a model gastro-intestinal system. Food Biophysics 3 (2008) 370-381. In vitro gastric lipolysis of emulsified triglycerides was shown to decrease in the presence of different food-grade surfactants: Sn-2 monopalmitin, β-lactoglobulin or lysophosphatodylcholine. However, only the monopalmitin caused a systematic decrease in the hydrolysis throughout the entire simulated gastro-intestinal tract. The authors used the TIM model of digestion in combination with interfacial measurements and mathematical modelling of interfacial composition to provide a better understanding of the importance of colloidal interfaces and transport processes in digestion.
22. Sandra S., Decker E.A., and McClements D.J. Effect of interfacial protein cross-linking on the in vitro digestibility of emulsified corn oil by pancreatic lipase. J Agric Food Chem 56 (2008) 7488-7494. This represents an attempt to change rates of lipolysis by modifying interfacial composition of lecithin or β-lactoglobulin stabilised emulsions. The similarity in results between the different samples highlights the complexity of achieving this goal.
23. Restani P., Ballabio C., Di Lorenzo C., Tripodi S., and Fiocchi A. Molecular aspects of milk allergens and their role in clinical events. Anal Bioanal Chem 395 (2009) 47-56
24. Monaci L., Tregoat V., van Hengel A.J., and Anklam E. Milk allergens, their characteristics and their detection in food: a review. Eur Food Res Technol 223 (2006) 149-179
25. Macierzanka A., Sancho A.I., Mills E., Rigby N.M., and Mackie A.R. Emulsification alters simulated gastrointestinal proteolysis of b-casein and b-lactoglobulin. Soft Matter 5 (2009) 538-550. The article reports on two important colloidal aspects of protein digestion, adsorption to the oil-water interface in emulsion and interaction with physiological gastro-intestinal surfactants. For two contrasting milk proteins studied, β-casein and β-lactoglobulin, it was shown in vitro that emulsification can markedly enhance their simulated gastro-intestinal proteolysis. This highlights the importance of food matrix structure in the digestion of protein in the gastro-intestinal environment. Digestibility of proteins and/or stability of emulsions have been found to be significantly affected by gastric phosphatidylcholine and duodenal bile acids. The extensive experimental work presented in the report comprises both physico-chemical and biochemical characterisations of the studied systems in simulated gastric and duodenal digestion.
26. Sarkar A., Goh K.K.T., Singh R.P., and Singh H. Behaviour of an oil-in-water emulsion stabilized by beta-lactoglobulin in an in vitro gastric model. Food Hydrocoll 23 (2009) 1563-1569. In vitro model of digestion was used to look at the gastric breakdown of β-lactoglobulin in emulsion. Adsorption to the oil-water interface made the protein susceptible to pepsin, which is in agreement with the previous study on the proteolysis in emulsion (Ref. 25).
27. Tunçtürk Y., and Zorba O. The effects of enzymatic hydrolysis of casein on apparent yield stress and some emulsion properties. Food Hydrocoll 20 (2006) 475-482
28. Armand M., Pasquier B., Borel P., Andre M., Senft M., Peyrot J., et al. Emulsion and absorption of lipids: the importance of physicochemical properties. Ocl-Oleagineux Corps Gras Lipides 4 (1997) 178-185
29. Marciani L., Wickham M., Singh G., Bush D., Pick B., Cox E., et al. Enhancement of intragastric acid stability of a fat emulsion meal delays gastric emptying and increases cholecystokinin release and gallbladder contraction. Am J Physiol: Gastrointest Liver Physiol 292 (2007) G1607-G1613
30. Marciani L., Faulks R., Wickham MS B.D., Pick B., Wright J., Cox E.F., Fillery-Travis A., et al. Effect of intragastric acid stability of fat emulsions on gastric emptying, plasma lipid profile and postprandial satiety. Br J Nutr 101 (2009) 919-928. Whilst this excellent paper does not address protein digestion it does show very clearly the importance of colloidal behaviour and emulsion stability in the GI tract in vivo in humans. The results link lipid phase separation to gastric emptying and appetite and blood plasma lipids.
31. Sletten G.B.G., Holden L., Egaas E., and Faeste C.K. Differential influence of the degree of processing on immunogenicity following proteolysis of casein and beta-lactoglobulin. Food and Agric Immunol 19 (2008) 213-228. The impact of food processing on proteolytic digestion and immunoreactivity was shown. Differences in fat content had no apparent effect.
32. Adachi A., Horikawa T., Shimizu H., Sarayama Y., Ogawa T., Sjolander S., et al. Soybean beta-conglycinin as the main allergen in a patient with food-dependent exercise-induced anaphylaxis by tofu: food processing alters pepsin resistance. Clin Exp Allergy 39 (2009) 167-173
33. Lundin L., Golding M., and Wooster T.J. Understanding food structure and function in developing food for appetite control. Nutr Diet 65 (2008) S79-S85. The review focused on the role of the structure of individual macronutrients on the digestion of foods and the appetite control.
34. Norton I., Moore S., and Fryer P. Understanding food structuring and breakdown: engineering approaches to obesity. Obes Rev 8 (2007) 83-88
35. Mandalari G., Mackie A.M., Rigby N.M., Wickham M.S., and Mills E.N. Physiological phosphatidylcholine protects bovine beta-lactoglobulin from simulated gastrointestinal proteolysis. Mol Nutr Food Res 53 1 (2009) S131-S139. Physiological phosphatidylcholine was found to enhance the resistance of bovine milk allergen β-lactoglobulin to in vitro gastro-intestinal proteolysis. The significant protective effect observed under the simulated duodenal conditions was dependent on the native folded structure of the protein and was shown for lipid present in the form of both vesicular dispersion and mixed micelles with bile acids. This report draws attention to interactions between protein allergens and lipids in the gut, which were suggested to have potential effect on the allergenicity of protein.
36. Moreno F.J., Mackie A.R., and Mills E. Phospholipid interactions protect the milk allergen alpha-lactalbumin from proteolysis during in vitro digestion. J Agric Food Chem 53 (2005) 9810-9816. The in vitro pepsinolysis of the bovine milk allergen α-lactalbumin was slowed by interactions with vesicular phosphatidylcholine present at physiologically relevant levels. The protein was found to unfold at gastric, acid pH and able to penetrate into the phosphatidylcholine vesicles. These findings indicate that the interactions of proteins with other food components and/or physiological surfactants may be important in effecting the breakdown of proteins in the gastro-intestinal tract in vivo.
37. Keiderling T.A., and Zhang X.Q. Lipid-induced conformational transitions of beta-lactoglobulin. Biochemistry 45 (2006) 8444-8452
38. Zhang XQ G.N., and Keiderling T.A. Electrostatic and hydrophobic interactions governing the interaction and binding of beta-lactoglobulin to membranes. Biochemistry 46 (2007) 5252-5260
39. Burke JE D.E. Phospholipase A(2) biochemistry. Cardiovasc Drugs Ther 23 (2009) 49-59
40. Dupont D, Mandalari G, Molle D, Jardin J, Leonil J, Faulks R, Wickham MS, Mills ENC, Mackie AR: Comparative resistance of food proteins to adult and infant in vitro digestion models. Molecular Nutrition & Food Research in press, doi:10.1002/mnfr.200900142. The article shows a comparison between an adult and an infant in vitro model of human proteolysis. The models differed mainly in the levels of proteases, phosphatidylcholine and bile salts. Ovalbumin and β-casein were digested more slowly in the infant model compared to the adult one. However, the opposite effect was observed for β-lactoglobulin and was suggested to be due to lower concentration of phosphatidylcholine protecting the protein in the infant model. The work gives valuable insights on the possible fate of dietary/allergenic proteins in "immature" infant gastro-intestinal tract.
41. Gass J., Vora H., Hofmann A.F., Gray G.M., and Khosla C. Enhancement of dietary protein digestion by conjugated bile acids. Gastroenterology 133 (2007) 16-23. Digestion of several dietary proteins by trypsin and chymotrypsin was shown to be markedly increased in presence of conjugated bile acids under simulated intestinal conditions. This was suggested to be attributed to the destabilisation of the tertiary structures of the proteins by the bile acids. The findings could be of great importance for the in vitro simulations of the digestion process since bile acids were previously thought to be mainly important for lipid digestion.
42. Walstra P., Waninge R.P., Bastiaans J., Niewenhuijse H., Nylander T., Paulsson M., et al. Competitive adsorption between β-casein or β-lactoglobulin and model milk membrane lipids at oil-water interfaces. J Agric Food Chem 53 (2005) 716-724
43. Maldonado-Valderrama J, Gunning AP, Ridout MJ, Wilde PJ, Morris VJ: The effect of physiological conditions on the surface structure of proteins: Setting the scene for human digestion of emulsions. Eur. Phys. J. E 2009;30:165-174. Simulated gastric conditions (i.e. pH 2.5, 37 °C) were shown to display a synergistic effect on the weakening of the interfacial β-lactoglobulin layers. The resulting rearrangements of the adsorbed protein made it more susceptible to displacement by a model surfactant (Tween 20).
44. Dickinson E. Structure formation in casein-based gels, foams, and emulsions. Colloids Surf, A Physicochem Eng Asp 288 (2006) 3-11
45. Hofmann A.F., and LR H. Bile acids: chemistry, pathochemistry, biology, pathobiology, and therapeutics. Cell Mol Life Sci 65 (2008) 2461-2483
46. Armand M. Lipases and lipolysis in the human digestive tract: where do we stand?. Curr Opin Clin Nutr Metab Care 10 (2007) 156-164. In this review paper, different lipases from the human digestive tract were compared in terms of their mode of action.
47. Maldonado-Valderrama J., Woodward N.C., Gunning A.P., Ridout M.J., Husband F.A., Mackie A.R., et al. Interfacial characterization of beta-lactoglobulin networks: displacement by bile salts. Langmuir 24 (2008) 6759-6767. Atomic force microscopy and interfacial physico-chemical analytical methods were used to characterise the mechanism of displacement of adsorbed β-lactoglobulin layers by bile acids at neutral pH. The authors highlighted the importance of the molecular structure of these surfactants on their efficiency in the displacement process.
48. Gunning A.P., Mackie A.R., Gunning P.A., Woodward N., Wilde P.J., and Morris V.J. The effect of surfactant type on surfactant-protein interactions at the air-water interface. Biomacromolecules 5 (2004) 984-991
49. Sarkar A., Horne D., and Singh H. Interactions of milk protein stabilized oil-in-water emulsions with bile salts in a simulated upper intestinal model. Food Hydrocolloids 24 2-3 (2010) 142-151
50. Ten Have G., Engelen M.R.K.J., Lulking Y.C., and Deutz N. Absorption kinetics of amino acids, peptides, and intact proteins. International Journal of Sport Nutrition and Exercise Metabolism 17 (2007) S23-S36
51. West C.M., Kopper R.A., and Helm R.M. Comparison of physiological and in vitro porcine gastric fluid digestion. Int Arch Allergy Immunol 141 (2006) 217-222. This article compares an in vitro model of digestion with in vivo data from piglets. The results highlight the importance of the food matrix and showed that allergens allergenic protein can be continuously released as the food matrix is gradually digested as it travels down the GI tract.
52. Goetze O., Steingoetter A., Menne D., van der Voort I.R., Kwiatek M.A., Boesiger P., et al. The effect of macronutrients on gastric volume responses and gastric emptying in humans: a magnetic resonance imaging study. Am J Physiol: Gastrointest Liver Physiol 292 (2007) G11-G17. The authors show non-invasively for the first time the link between three different meal types and rates of gastric emptying. Results showed that a "fat" meal was emptied much faster than a "protein" meal.
53. Mortensen L.S., Hartvigsen M.L., Brader L.J., Astrup A., Schrezenmeir J., Holst J.J., et al. Differential effects of protein quality on postprandial lipemia in response to a fat-rich meal in type 2 diabetes: comparison of whey, casein, gluten, and cod protein. American Journal of Clinical Nutrition 90 (2009) 41-48. In this paper the authors show that fat digestion was significantly affected by the type of protein that was consumed with it. Whey protein had the most suppressing effect of the four protein types used.
54. Veldhorst M.A.B., Nieuwenhuizen A.G., Hochstenbach-Waelen A., van Vught A.J.A.H., Westerterp K.R., Engelen M.P.K.J., et al. Dose-dependent satiating effect of whey relative to casein or soy. Physiol Behav 96 (2009) 675-682