Endogenous human milk peptide release is greater after preterm birth than term birth

Journal of Nutrition

Volumn 145, Issue 3, 2015, Pages 425-433

  Dallas, David C ^a   Smink, Christina J ^c   Robinson, Randall C ^a   Tian, Tian ^a   Guerrero, Andres ^a   Parker, Evan A ^a   Smilowitz, Jennifer T ^a   Hettinga, Kasper A ^c   Underwood, Mark A ^b   Lebrilla, Carlito B ^a   Bruce German, J ^a   Barile, Daniela ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Carboxypeptidase B2; Cytosol aminopeptidase; Functional peptide; Human milk; Mass spectrometry; Peptidomics; Plasmin; Premature; Term

Indexed keywords

ALPHA CASEIN; ALPHA LACTALBUMIN; BETA CASEIN; CATHEPSIN D; CYTOSOL AMINOPEPTIDASE; ELASTASE; IMMUNOGLOBULIN; LACTOFERRIN; MILK PROTEIN; OSTEOPONTIN; PLASMIN; PLASMINOGEN; SECRETORY COMPONENT; THROMBIN ACTIVATABLE FIBRINOLYSIS INHIBITOR; PEPTIDE;

ADULT; AMINO ACID SEQUENCE; ARTICLE; BREAST MILK; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME DEGRADATION; FEMALE; HUMAN; LIQUID CHROMATOGRAPHY; PEPTIDE LIBRARY; PREMATURE LABOR; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN SECRETION; TANDEM MASS SPECTROMETRY; TERM BIRTH; CHEMISTRY; COMPARATIVE STUDY; EVALUATION STUDY; LACTATION; METABOLISM; NEWBORN; NORMAL HUMAN; PREMATURITY; PROSPECTIVE STUDY;

CHROMATOGRAPHY, LIQUID; EVALUATION STUDIES AS TOPIC; FEMALE; HEALTHY VOLUNTEERS; HUMANS; INFANT, NEWBORN; INFANT, PREMATURE; LACTATION; MILK PROTEINS; MILK, HUMAN; PEPTIDES; PREMATURE BIRTH; PROSPECTIVE STUDIES; TANDEM MASS SPECTROMETRY; TERM BIRTH;

EID: 84928378606     PISSN: 00223166     EISSN: 15416100     Source Type: Journal    
DOI: 10.3945/jn.114.203646     Document Type: Article

References (53)

1. Dallas DC, Guerrero A, Khaldi N, Castillo PA, Martin WF, Smilowitz JT, Bevins CL, Barile D, German JB, Lebrilla CB. Extensive in vivo human milk peptidomics reveals specific proteolysis yielding protective antimicrobial peptides. J Proteome Res 2013;12:2295-304.
2. Ferranti P, Traisci MV, Picariello G, Nasi A, Boschi V, Siervo M, Falconi C, Chianese L, Addeo F. Casein proteolysis in human milk: tracing the pattern of casein breakdown and the formation of potential bioactive peptides. J Dairy Res 2004;71:74-87.
3. Guerrero A, Dallas DC, Contreras S, Chee S, Parker EA, Sun X, Dimapasoc LM, Barile D, German JB, Lebrilla CB. Mechanistic peptidomics: factors that dictate the specificity on the formation of endogenous peptides in human milk. Mol Cell Proteomics 2014;13: 3343-51.
4. Dallas DC, Guerrero A, Khaldi N, Borghese R, Bhandari A, Underwood MA, Lebrilla CB, German JB, Barile D. A peptidomic analysis of human milk digestion in the infant stomach reveals protein-specific degradation patterns. J Nutr 2014;144:815-20.
5. Heegaard CW, Larsen LB, Rasmussen LK, Højberg KE, Petersen TE, Andreasen PA. Plasminogen activation system in human milk. J Pediatr Gastroenterol Nutr 1997;25:159-66.
6. Větvicka V, Vagner J, Baudys M, Tang J, Foundling S, Fusek M. Human breast milk contains procathepsin D-detection by specific antibodies. Biochem Mol Biol Int 1993;30:921-8.
7. Borulf S, Lindberg T, Mansson M. Immunoreactive anionic trypsin and anionic elastase in human milk. Acta Paediatr Scand 1987;76:11-5.
8. Khaldi N, Vijayakumar V, Dallas DC, Guerrero A, Wickramasinghe S, Smilowitz JT, Medrano JF, Lebrilla CB, Shields DC, German JB. Predicting the important enzyme players in human breast milk digestion. J Agric Food Chem 2014;62:7225-32.
9. Zucht HD, Raida M, Adermann K, Mägert HJ, Forssmann WG. Casocidin-I: a casein-alpha(s2) derived peptide exhibits antibacterial activity. FEBS Lett 1995;372:185-8.
10. Anderson GH, Atkinson SA, Bryan MH. Energy and macronutrient content of human milk during early lactation from mothers giving birth prematurely and at term. Am J Clin Nutr 1981;34:258-65.
11. Bitman J, Wood L, Hamosh M, Hamosh P, Mehta NR. Comparison of the lipid composition of breast milk from mothers of term and preterm infants. Am J Clin Nutr 1983;38:300-12.
12. Lemons JA, Moye L, Hall D, Simmons M. Differences in the composition of preterm and term human milk during early lactation. Pediatr Res 1982;16:113-7.
13. Armaforte E, Curran E, Huppertz T, Ryan CA, Caboni MF, O'Connor PM, Ross RP, Hirtz C, Sommerer N, Chevalier F. Proteins and proteolysis in pre-term and term human milk and possible implications for infant formulae. Int Dairy J 2010;20:715-23.
14. Dallas DC, Guerrero A, Parker EA, Garay LA, Bhandari A, Lebrilla CB, Barile D, German JB. Peptidomic profile of milk of Holstein cows at peak lactation. J Agric Food Chem 2014;62:58-65.
15. Smith PK, Krohn RI, Hermanson G, Mallia A, Gartner F, Provenzano M, Fujimoto E, Goeke N, Olson B, Klenk D. Measurement of protein using bicinchoninic acid. Anal Biochem 1985;150:76-85.
16. Craig R, Beavis RC. TANDEM: matching proteins with tandem mass spectra. Bioinformatics 2004;20:1466-7.
17. Vizcaíno JA, Côté RG, Csordas A, Dianes JA, Fabregat A, Foster JM, Griss J, Alpi E, Birim M, Contell J. The Proteomics Identifications (PRIDE) database and associated tools: status in 2013. Nucleic Acids Res 2013;41:D1063-9.
18. Maruyama S, Nakagomi K, Tomizuka N, Suzuki H. Angiotensin I-converting enzyme inhibitor derived from an enzymatic hydrolysate of casein. II. Isolation and bradykinin-potentiating activity on the uterus and the ileum of rats. Agric Biol Chem 1985;49:1405-9.
19. Recio I, Visser S. Identification of two distinct antibacterial domains within the sequence of bovine a-s2-casein. Biochim Biophys Acta 1999;1428:314-26.
20. Minervini F, Algaron F, Rizzello C, Fox P, Monnet V, Gobbetti M. Angiotensin I-converting-enzyme-inhibitory and antibacterial peptides from Lactobacillus helveticus PR4 proteinase-hydrolyzed caseins of milk from six species. Appl Environ Microbiol 2003; 69:5297-305.
21. Hayes M, Stanton C, Fitzgerald GF, Ross RP. Putting microbes to work: dairy fermentation, cell factories and bioactive peptides. Part II: bioactive peptide functions. Biotechnol J 2007;2:435-49.
22. Parker EA. Peptidomics enzyme estimator. 2014 [cited 2014 Nov 1]. Available from: https://github.com/eparker05/Peptidomics-enzymeestimator.
23. Guerrero A, Dallas DC, Contreras S, Chee S, Parker EA, Sun X, Dimapasoc LM, Barile D, German JB, Lebrilla CB. Mechanistic peptidomics: factors that dictate specificity in the formation of endogenous peptides in human milk. Mol Cell Proteomics 2014;13:3343-51.
24. Eaton DL, Malloy B, Tsai SP, Henzel W, Drayna D. Isolation, molecular cloning, and partial characterization of a novel carboxypeptidase B from human plasma. J Biol Chem 1991;266:21833-8.
25. Hendriks D, Wang W, Scharpé S, Lommaert M-P, van Sande M. Purification and characterization of a new arginine carboxypeptidase in human serum. Biochim Biophys Acta 1990;1034:86-92.
26. P28838-Cytosol aminopeptidase. 2014 June 11 [cited 2014 Jul 8]. Available from: http://www.uniprot.org/uniprot/P28838.
27. Azuma N, Nagaune S, Ishino Y, Mori H, Kaminogawa S, Yamauchi K. DNA-synthesis stimulating peptides from human β-casein. Agric Biol Chem 1989;53:2631-4.
28. Politis I, Ng Kwai Hang K, Giroux R. Environmental factors affecting plasmin activity in milk. J Dairy Sci 1989;72:1713-8.
29. Ismail B, Nielsen S. Invited review: plasmin protease in milk: current knowledge and relevance to dairy industry. J Dairy Sci 2010;93:4999-5009.
30. Mansor R, Mullen W, Albalat A, Zerefos P, Mischak H, Barrett DC, Biggs A, Eckersall PD. A peptidomic approach to biomarker discovery for bovine mastitis. J Proteomics 2013;85:89-98.
31. Guerrero A, Dallas DC, Contreras S, Bhandari A, Cánovas A, Islas-Trejo A, Medrano JF, Parker EA, Wang M, Hettinga K, et al. Peptidomic analysis of healthy and subclinically mastitic bovine milk. Int Dairy J 2014 Oct 28 (Epub ahead of print; DOI: 10.1016/j.idairyj.2014.09.006).
32. Kaartinen L, Sandholm M. Regulation of plasmin activation in mastitic milk: correlation with inflammatory markers and growth of streptococcus agalactiae. Zentralbl Veterinarmed B 1987;34:42-50.
33. Bastian ED, Brown RJ. Plasmin in milk and dairy products: an update. Int Dairy J 1996;6:435-57.
34. Kelly A, O'Flaherty F, Fox P. Indigenous proteolytic enzymes in milk: a brief overview of the present state of knowledge. Int Dairy J 2006;16: 563-72.
35. Nguyen D-AD, Neville MC. Tight junction regulation in the mammary gland. J Mammary Gland Biol Neoplasia 1998;3:233-46.
36. Anderson G. The effect of prematurity on milk composition and its physiological basis. Fed Proc 1984;43:2438-42.
37. Lindberg T, Ohlsson K, Weström B. Protease inhibitors and their relation to protease activity in human-milk. Pediatr Res 1982;16:479-83.
38. Korycha-Dahl M, Dumas BR, Chene N, Martal J. Plasmin activity in milk. J Dairy Sci 1983;66:704-11.
39. Wickramasinghe S, Rincon G, Islas-Trejo A, Medrano JF. Transcriptional profiling of bovine milk using RNA sequencing. BMC Genomics 2012;13:45-58.
40. Molinari CE, Casadio YS, Hartmann BT, Livk A, Bringans S, Arthur PG, Hartmann PE. Proteome mapping of human skim milk proteins in term and preterm milk. J Proteome Res 2012;11:1696-714.
41. Christensen B, Schack L, Kläning E, Sørensen ES. Osteopontin is cleaved at multiple sites close to its integrin-binding motifs in milk and is a novel substrate for plasmin and cathepsin D. J Biol Chem 2010;285:7929-37.
42. Monti JC, Mermoud A-F, Jolles P. Trypsin in human milk. Experientia 1986;42:39-41.
43. Christensen U, Müllertz S. Mechanism of reaction of human plasmin with α-N-benzoyl-l-arginine-p-nitroanilide: titration of the enzyme. Biochim Biophys Acta 1974;334:187-98.
44. Palmer DJ, Kelly VC, Smit AM, Kuy S, Knight CG, Cooper GJ. Human colostrum: identification of minor proteins in the aqueous phase by proteomics. Proteomics 2006;6:2208-16.
45. Dallas DC, Underwood MA, Zivkovic AM, German JB. Digestion of protein in premature and term infants. J Nutr Disord Ther 2012;2:112.
46. Sato R, Noguchi T, Naito H. Casein phosphopeptide (CPP) enhances calcium absorption from the ligated segment of rat small intestine. J Nutr Sci Vitaminol (Tokyo) 1986;32:67-76.
47. Newburg DS, Walker WA. Protection of the neonate by the innate immune system of developing gut and of human milk. Pediatr Res 2007;61:2-8.
48. Lönnerdal B. Bioactive proteins in human milk: mechanisms of action. J Pediatr 2010;156:S26-30.
49. Borgström B, Lindquist B, Lundh G. Enzyme concentration and absorption of protein and glucose in duodenum of premature infants. AMA J Dis Child 1960;99:338-43.
50. Engberg S, Mansson M, Andersson Y, Jakobsson I, Lindberg T. Trypsin and elastase activity in duodenal juice from preterm infants before and after a meal of human milk. Prenat Neonatal Med 1999;4:466-71.
51. Arslanoglu S, Moro GE, Ziegler EE. Optimization of human milk fortification for preterm infants: new concepts and recommendations. J Perinat Med 2010;38:233-8.
52. Beck S, Wojdyla D, Say L, Betran AP, Merialdi M, Requejo JH, Rubens C, Menon R, Van Look PF. The worldwide incidence of preterm birth: a systematic review of maternal mortality and morbidity. Bull World Health Organ 2010;88:31-8.
53. Kwek JH, Iongh RD, Digby MR, Renfree MB, Nicholas KR, Familari M. Cross-fostering of the tammar wallaby Macropus eugenii pouch young accelerates fore-stomach maturation. Mech Dev 2009;126:449-63.