Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
RESEARCH ARTICLE

Identification of peptides in the terminal ileum of broiler chickens fed diets based on maize and soybean meal using proteomics

A. J. Cowieson A D , M. Klausen B , K. Pontoppidan B , M. Umar Faruk C , F. F. Roos A and A. M. B. Giessing B
+ Author Affiliations
- Author Affiliations

A DSM Nutritional Products, Wurmisweg 576, Kaiseraugst, Switzerland.

B Novozymes A/S, Krogshøjvej 36, 2880 Bagsværd, Denmark.

C DSM Nutritional Products, F-68128, Village-Neuf, France.

D Corresponding author. Email: aaron.cowieson@dsm.com

Animal Production Science 57(8) 1738-1750 https://doi.org/10.1071/AN16213
Submitted: 6 April 2016  Accepted: 28 April 2016   Published: 19 August 2016

Abstract

A total of 160 Ross PM3 birds were used in a two treatment feeding study in order to explore the usefulness of proteomics to identify the origin of peptides in ileal digesta. Two diets were fed, one conventional maize/soy-based diet acted as a reference whereas a second diet, formulated to be nutritionally equivalent to the reference diet in protein and energy provision, contained 20% raw soy meal in order to (putatively) elicit changes in intestinal protein flow. Each diet was fed to 10 replicate cages of eight birds per cage from Day 1 to 21. Feed and water were available ad libitum and an indigestible marker was included for assessment of ileal digestibility. Weight gain and feed intake were monitored and at the end of the trial period birds were killed, pancreatic mass was measured and the ileum was excised and the contents were collected, immediately frozen in liquid nitrogen and were subsequently lyophilised. Protein from the ileal digesta was extracted and exposed to proteomic analysis with peptide fragments identified and compared with an amalgamated database containing protein sequences from chicken, soy and maize. Addition of 20% raw soy meal to the maize/soy-based diet resulted in a reduction in weight gain, feed intake and an increase in feed conversion ratio (P < 0.001). Pancreatic mass was significantly increased and the apparent ileal digestibility of protein was significantly decreased by raw soy meal inclusion. Overall, a total of 248 proteins were identified from endogenous origin, 336 from soy and 411 from maize. However, the relative abundance of these proteins were ~20–30% for endogenous protein, 65–75% for soy protein and ~2–4% for maize protein. The addition of 20% raw soy meal resulted in an increase in the relative abundance of endogenous protein and a reduction in the relative abundance of protein from soy with no measurable effect on the presence of protein from maize. Specifically, in the endogenous protein fraction, there was a significant reduction in the relative abundance of metalloendopeptidase, aminopeptidase and alkaline phosphatase and a significant increase in the relative abundance of colipase and trypsin, in response to raw soy meal inclusion. For proteins originating from soybean, the addition of raw soy meal to the diet resulted in a significant increase in the relative abundance of protein from the 2S albumin fraction, Kunitz and Bowman–Birk trypsin inhibitors and soybean agglutinin whereas there was a reduction in the relative abundance of globulin and glycinin. Addition of raw soy meal to the diet also resulted in a significant increase in the presence of maize prolamin in the lumen and a significant decrease in the presence of globulin-2, β-1–3-glucanase and cystatin. These results demonstrate considerable potential of proteomics technology to identify changes in the digestion and secretion of protein in the intestine of chickens. Although these data are preliminary and based on an animal model that included diets that were formulated to have a chronic effect on intestinal physiology it is evident that changes in diet composition can have a profound effect on the origin of protein that leaves the ileum.

Additional keywords: digestion, maize grain, proteins, trypsin.


References

Angkanaporn K, Choct M, Bryden WL, Annison EF, Annison G (1994) Effects of wheat pentosans on endogenous amino acid losses in chickens. Journal of the Science of Food and Agriculture 66, 399–404.
Effects of wheat pentosans on endogenous amino acid losses in chickens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXit1yrsb8%3D&md5=704965d79f37b3af7903c24f2f4ca36fCAS |

Baker SF, Othman R, Wilton DC (1998) Tryptophan-containing mutant of human (Group IIa) secreted phospholipase A2 has a dramatically increased ability to hydrolyze phosphatidylcholine vesicles and cell membranes. Biochemistry 37, 13 203–13 211.
Tryptophan-containing mutant of human (Group IIa) secreted phospholipase A2 has a dramatically increased ability to hydrolyze phosphatidylcholine vesicles and cell membranes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXlsF2hsLk%3D&md5=399dd4c3f582f8bea4c5a687ffa363ecCAS |

Bass HW, Krawetz JE, O’Brian GR, Zinselmeier C, Habben JE, Boston RS (2004) Maize ribosomal-inactivating proteins (RIPs) with distinct expression patterns have similar requirements for proenzyme activation. The Journal of Experimental Biology 55, 2219–2233.

Behnke C, Yee VC, Le Trong I, Pedersen LC, Stenkamp RE, Kim S-S, Reeck GR, Teller DC (1998) Structural determinants of the bifunctional maize Hageman factor inhibitor: X-ray crystal structure at 1.95 Å resolution. Biochemistry 37, 15 277–15 288.
Structural determinants of the bifunctional maize Hageman factor inhibitor: X-ray crystal structure at 1.95 Å resolution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmsFyrur0%3D&md5=0348131626f40e4749a6b062f7b4d877CAS |

Bergström JH, Berg KA, Rodriguez-Pineiro AM, Stecher B, Johansson MEV, Hansson GC (2014) AGR2, an endoplasmic reticulum protein, is secreted into the gastrointestinal mucus. PLoS ONE 9, e104186
AGR2, an endoplasmic reticulum protein, is secreted into the gastrointestinal mucus.Crossref | GoogleScholarGoogle Scholar | 25111734PubMed |

Capriotti AL, Caruso G, Cavaliere C, Samperi R, Stampachiacchiere S, Chiozzi RZ, Lagana A (2014) Protein profile of mature soybean seeds and prepared soybean milk. Journal of Agricultural and Food Chemistry 62, 9893–9899.
Protein profile of mature soybean seeds and prepared soybean milk.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsFGhsLvJ&md5=0fc5b9e97b19a6b4a939d5d642820b3eCAS | 25229310PubMed |

Chui C-F, Falco SCA (1995) A new methionine-rich seed storage protein from maize. Plant Physiology 107, 291
A new methionine-rich seed storage protein from maize.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjtVOmtrY%3D&md5=f02113972f065fe91b9e0aaa46b562beCAS | 7870828PubMed |

Clarke E, Wiseman J (2005) Effects of variability in trypsin inhibitor content of soya bean meals on true and apparent ileal digestibility of amino acids and pancreas size in broiler chicks. Animal Feed Science and Technology 121, 125–138.
Effects of variability in trypsin inhibitor content of soya bean meals on true and apparent ileal digestibility of amino acids and pancreas size in broiler chicks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXks1Wnurw%3D&md5=92363939939862e9e3d5ae05d1f4a3d5CAS |

Cowieson AJ, Bedford MR (2009) The effect of phytase and carbohydrase on ileal amino acid digestibility in monogastric diets: complementary mode of action? World’s Poultry Science Journal 65, 609–624.
The effect of phytase and carbohydrase on ileal amino acid digestibility in monogastric diets: complementary mode of action?Crossref | GoogleScholarGoogle Scholar |

Cowieson AJ, Ravindran V (2007) Effect of phytic acid and microbial phytase on the flow and amino acid composition of endogenous protein at the terminal ileum of growing broiler chickens. British Journal of Nutrition 98, 745–752.
Effect of phytic acid and microbial phytase on the flow and amino acid composition of endogenous protein at the terminal ileum of growing broiler chickens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlWhsrjO&md5=81271d3e71ef244db26985f32f41f85bCAS | 17524177PubMed |

Cowieson AJ, Acamovic T, Bedford MR (2004) The effect of phytase and phytate on endogenous losses from broiler chickens. British Poultry Science 45, 101–108.
The effect of phytase and phytate on endogenous losses from broiler chickens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhs1Wgu7c%3D&md5=cd66944e7a7375e9d55f260b8773158dCAS | 15115207PubMed |

Cowieson AJ, Bedford MR, Selle PH, Ravindran V (2009) Phytate and microbial phytase: implications for endogenous nitrogen losses and nutrient availability. World’s Poultry Science Journal 65, 401–418.
Phytate and microbial phytase: implications for endogenous nitrogen losses and nutrient availability.Crossref | GoogleScholarGoogle Scholar |

Dia VP, Gomez T, Vernaza G, Berhow M, Chang YK, Gonzalez de Mejia E (2012) Bowman-Birk and Kunitz protease inhibitors among antinutrients and bioactives modified by germination and hydrolysis in Brazilian soybean cultivar BRS 133. Journal of Agricultural and Food Chemistry 60, 7886–7894.
Bowman-Birk and Kunitz protease inhibitors among antinutrients and bioactives modified by germination and hydrolysis in Brazilian soybean cultivar BRS 133.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVemtbnI&md5=3eb95236021b0ac779ac446f29de1764CAS | 22800092PubMed |

Dinkins RD, Reddy MSS, Meurer CA, Yan B, Trick H, Thibauld-Nissen F, Finer JJ, Parrott WA, Collins GB (2001) Increased sulfur amino acids in soybean plants overexpressing the maize 15 kDa zein protein. In Vitro Cellular & Developmental Biology. Plant 37, 742–747.
Increased sulfur amino acids in soybean plants overexpressing the maize 15 kDa zein protein.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XltlWhtQ%3D%3D&md5=7ef4a27e7e8368de7ee7cbcc8fcc6eeaCAS |

Fuller MF, Reeds PJ (1998) Nitrogen cycling in the gut. Annual Review of Nutrition 18, 385–411.
Nitrogen cycling in the gut.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXkvVWgt7c%3D&md5=f5ecbcb6cb48179da70197f6b5473ecbCAS | 9706230PubMed |

Gapusan RA, Yardley DG, Hughes BL (1990) The amylase gene-enzyme system of chickens. II. Biochemical characterization of allozymes. Biochemical Genetics 28, 553–560.
The amylase gene-enzyme system of chickens. II. Biochemical characterization of allozymes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXhvVSqu7o%3D&md5=e9c6740f6b0d77cd46c1eb9e9813af11CAS | 1707617PubMed |

Gholizadeh A (2012) Molecular analysis of maize cystatin expression as fusion product in Eschericia coli. Physiology and Molecular Biology of Plants 18, 237–244.
Molecular analysis of maize cystatin expression as fusion product in Eschericia coli.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XpvFCjtLw%3D&md5=2c9964a19583ad92745f02d6722405b1CAS | 23814438PubMed |

Green GM, Lyman RL (1972) Feedback regulation of pancreatic enzyme secretion as a mechanism for trypsin inhibitor-induced hypersecretion in rats. Experimental Biology and Medicine 140, 6–12.
Feedback regulation of pancreatic enzyme secretion as a mechanism for trypsin inhibitor-induced hypersecretion in rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE38Xkt12ktbw%3D&md5=9aa0de83e100a53ad863a4dc4812d856CAS |

He XM, Carter DC (1992) Atomic structure and chemistry of human serum albumin. Nature 358, 209–215.
Atomic structure and chemistry of human serum albumin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XlsVGmurg%3D&md5=13247a249ffeab17efc4ff6369a5fb5bCAS | 1630489PubMed |

Johansson MEV, Sjovall H, Hansson GC (2013) The gastrointestinal mucus system in health and disease. Nature Reviews. Gastroenterology & Hepatology 10, 352–361.
The gastrointestinal mucus system in health and disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXptVOlsrc%3D&md5=2b0acfddcf78e83c8b4a7f5ffd93aa58CAS |

Joudrier PE, Foard DE, Floener LA, Larkins BA (1987) Isolation and sequence of cDNA encoding the soybean protease inhibitors PI IV and C–II. Plant Molecular Biology 10, 35–42.
Isolation and sequence of cDNA encoding the soybean protease inhibitors PI IV and C–II.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXhvF2iurk%3D&md5=70996f8156ddfdfae41169b28997892cCAS | 24277461PubMed |

Kakade ML, Hoffa DE, Liener IE (1973) Contribution of trypsin inhibitors to the deleterious effects of unheated soybeans fed to rats. The Journal of Nutrition 103, 1772–1778.

Kant P, Lie W-Z, Pauls P (2009) PDC1, a maize defensin peptide expressed in Eschericia coli and Pichia pastoris inhibits growth of Fusarium graminearum. Peptides 30, 1593–1599.
PDC1, a maize defensin peptide expressed in Eschericia coli and Pichia pastoris inhibits growth of Fusarium graminearum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpt1Kiurg%3D&md5=4581c83433694a47e81b712ceba1f92dCAS | 19505517PubMed |

Kennedy AR (1998) Chemopreventative agents: protease inhibitors. Pharmacology & Therapeutics 78, 167–209.
Chemopreventative agents: protease inhibitors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjsVejurk%3D&md5=604ad2c91da33cebd4c469a916e12b96CAS |

Krogdahl A (1985) Digestion and absorption of lipids in poultry. The Journal of Nutrition 115, 675–685.

Lallès J-P (2014) Intestinal alkaline phosphatase: novel functions and protective effects. Nutrition Reviews 72, 82–94.
Intestinal alkaline phosphatase: novel functions and protective effects.Crossref | GoogleScholarGoogle Scholar | 24506153PubMed |

León I, Schwammle V, Jensen O, Sprenger R (2013) Quantitative assessment of in-solution digestion efficiency identifies optimal protocols for unbiased protein analysis. Molecular & Cellular Proteomics 12, 2992–3005.
Quantitative assessment of in-solution digestion efficiency identifies optimal protocols for unbiased protein analysis.Crossref | GoogleScholarGoogle Scholar |

Luo M, Hajjar KA (2013) Annexin A2 system in human biology: cell surface and beyond. Seminars in Thrombosis and Hemostasis 39, 338–346.
Annexin A2 system in human biology: cell surface and beyond.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXpvFeiu7s%3D&md5=41586c364701d902a3dfbe6c1718f2f5CAS | 23483454PubMed |

Meinke DW, Chen J, Beachy RN (1981) Expression of storage-protein genes during soybean seed development. Planta 153, 130–139.
Expression of storage-protein genes during soybean seed development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXmtVSks70%3D&md5=c7931d96962b8d0e0c0a7b081c2cd334CAS | 24276763PubMed |

Miner-Williams W, Moughan PJ, Fuller MF (2009) Endogenous components of digesta protein from the terminal ileum of pigs fed a casein-based diet. Journal of Agricultural and Food Chemistry 57, 2072–2078.
Endogenous components of digesta protein from the terminal ileum of pigs fed a casein-based diet.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1ajsr8%3D&md5=2330fc4b8fa86b803d3fde2ebfac9325CAS | 19203191PubMed |

Moreno FJ, Clemente A (2008) 2S albumin storage proteins: what makes them food allergens? The Open Biochemistry Journal 2, 16–28.
2S albumin storage proteins: what makes them food allergens?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlsleht78%3D&md5=5d1932fa5bbbf04063ea13cda42e64caCAS | 18949071PubMed |

Moughan PJ, Rutherfurd SM (2012) Gut luminal endogenous protein: implications for the determination of ileal amino acid digestibility in humans. British Journal of Nutrition 108, S258–S263.
Gut luminal endogenous protein: implications for the determination of ileal amino acid digestibility in humans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1arsbvL&md5=dd9e6ea8ffb8fafa3184a0083d1615d1CAS | 23107536PubMed |

Moughan PJ, Darragh AJ, Smith WC, Butts CA (1990) Perchloric and trichloroacetic acids as precipitants of protein in endogenous ileal digesta from the rat. Journal of the Science of Food and Agriculture 52, 13–21.
Perchloric and trichloroacetic acids as precipitants of protein in endogenous ileal digesta from the rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXkvFCht7s%3D&md5=37add0d01162ed9ada6f7e14c898cf4fCAS |

Nishida A, Lau CW, Mizoguchi A (2015) Examination of the role of galectins in intestinal inflammation. Galectins 1207, 231–248.

Park S-W, Zhen G, Verhaeghe C, Nakagami Y, Nguyenvu LT, Barczak AJ, Killeen N, Erle DJ (2009) The protein disulfide isomerase AGR2 is essential for production of intestinal mucus. Proceedings of the National Academy of Sciences of the United States of America 106, 6950–6955.
The protein disulfide isomerase AGR2 is essential for production of intestinal mucus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlvFSgsLc%3D&md5=7b6f9d5ecc9790b8bba3cc86b12a4837CAS | 19359471PubMed |

Porta H, Rocha-Sosa M (2002) Plant lipoxygenases. Physiological and molecular features. Plant Physiology 130, 15–21.
Plant lipoxygenases. Physiological and molecular features.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XntFOrsL0%3D&md5=89363c439f9c38454086b4a17df93488CAS | 12226483PubMed |

Ravindran V, Morel PCH, Rutherfurd SM, Thomas DV (2009) Endogenous flow of amino acids in the avian ileum as influenced by increasing dietary peptide concentrations. British Journal of Nutrition 101, 822–828.
Endogenous flow of amino acids in the avian ileum as influenced by increasing dietary peptide concentrations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXktleju7c%3D&md5=204249eb3d5d76359ac84168c834b859CAS | 18662428PubMed |

Rocha C, Durau JF, Barrilli LNE, Dahlke F, Maiorka P, Maiorka A (2014) The effect of raw and roasted soybeans on intestinal health, diet digestibility, and pancreas weight of broilers. Journal of Applied Poultry Research 23, 71–79.
The effect of raw and roasted soybeans on intestinal health, diet digestibility, and pancreas weight of broilers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjsFCks78%3D&md5=e4dfacebba91fe43b87290a5fce9724aCAS |

Shewry PR, Halford NG (2002) Cereal seed storage proteins: structures, properties and role in grain utilization. The Journal of Experimental Biology 53, 947–958.

Simon O, Zebrowska T, Bergner H, Munchmeyer R (1993) Investigations on the pancreatic and stomach secretion in pigs by means of continuous infusion of 14C-amino acids. Archives of Animal Nutrition 33, 9–12.

Sorgentini DA, Wagner JR, Anon MC (1995) Effects of thermal treatment of soy protein isolate on the characteristics and structure-function relationship of soluble and insoluble fractions. Journal of Agricultural and Food Chemistry 43, 2471–2479.
Effects of thermal treatment of soy protein isolate on the characteristics and structure-function relationship of soluble and insoluble fractions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXns1CjsLo%3D&md5=56ed834c2eb57aa9fcd83efcf7d7f6b5CAS |

Souffrant WB, Rerat A, Laplace JB, Darcy BV, Kohler R, Corring T, Gebhardt G (1993) Exogenous and endogenous contributions to nitrogen fluxes in the digestive tract of pigs fed a casein diet. III. Refluxing of endogenous nitrogen. Reproduction, Nutrition, Development 33, 373–382.
Exogenous and endogenous contributions to nitrogen fluxes in the digestive tract of pigs fed a casein diet. III. Refluxing of endogenous nitrogen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXivFOgs7Y%3D&md5=3d25f1e928af873fc4a8f8e08f4b52d2CAS | 8240681PubMed |

Westfall RJ, Hauge SM (1948) The nutritive quality and the trypsin inhibitor content of soybean flour heated at various temperatures. The Journal of Nutrition 36, 379–389.