Transport of Antihypertensive Peptide RVPSL, Ovotransferrin 328-332, in Human Intestinal Caco-2 Cell Monolayers

Journal of Agricultural and Food Chemistry

Volumn 63, Issue 37, 2015, Pages 8143-8150

  Ding, Long ^a   Wang, Liying ^a   Zhang, Yan ^a   Liu, Jingbo ^a  

^a JILIN UNIVERSITY   (China)

Author keywords

antihypertensive peptide; brush border membrane peptidase; Caco 2 cell monolayer; egg white; transport

Indexed keywords

CELL MEMBRANES; CYTOLOGY; MONOLAYERS; PEPTIDES; POSITIVE IONS; PROTEINS;

ANTIHYPERTENSIVE PEPTIDES; BRUSH BORDER MEMBRANES; CACO-2 CELLS; EGG WHITE; TRANSPORT;

CELLS;

ANTIHYPERTENSIVE AGENT; ARGINYL-VALYL-PROLYL-SERYL-LEUCINE; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; EGG PROTEIN; PEPTIDE FRAGMENT; PEPTIDE HYDROLASE;

CACO 2 CELL LINE; CHEMISTRY; ENZYMOLOGY; EPITHELIUM; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; INTESTINE; METABOLISM; MICROVILLUS; STRUCTURE ACTIVITY RELATION; TRANSPORT AT THE CELLULAR LEVEL;

ANGIOTENSIN-CONVERTING ENZYME INHIBITORS; ANTIHYPERTENSIVE AGENTS; BIOLOGICAL TRANSPORT; CACO-2 CELLS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; EGG PROTEINS; EPITHELIUM; HUMANS; INTESTINES; MICROVILLI; PEPTIDE FRAGMENTS; PEPTIDE HYDROLASES; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84942155041     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/acs.jafc.5b01824     Document Type: Article

References (51)

1. Iwaniak, A.; Minkiewicz, P.; Darewicz, M. Food-Originating ACE Inhibitors, Including Antihypertensive Peptides, as Preventive Food Components in Blood Pressure Reduction Compr. Rev. Food Sci. Food Saf. 2014, 13, 114-134 10.1111/1541-4337.12051
2. Erdmann, K.; Cheung, B. W. Y.; Schroeder, H. The possible roles of food-derived bioactive peptides in reducing the risk of cardiovascular disease J. Nutr. Biochem. 2008, 19, 643-654 10.1016/j.jnutbio.2007.11.010
3. Martinez-Maqueda, D.; Miralles, B.; Recio, I.; Hernandez-Ledesma, B. Antihypertensive peptides from food proteins: a review Food Funct. 2012, 3, 350-361 10.1039/c2fo10192k
4. Nakamura, Y.; Yamamoto, N.; Sakai, K.; Takano, T. Antihypertensive effect of sour milk and peptides isolated from it that are inhibitors to angiotensin I-converting enzyme J. Dairy Sci. 1995, 78, 1253-7 10.3168/jds.S0022-0302(95)76745-5
5. Miguel, M.; Gomez-Ruiz, J. A.; Recio, I.; Aleixandre, A. Changes in arterial blood pressure after single oral administration of milk-casein-derived peptides in spontaneously hypertensive rats Mol. Nutr. Food Res. 2010, 54, 1422-1427 10.1002/mnfr.200900448
6. Fujita, H.; Usui, H.; Kurahashi, K.; Yoshikawa, M. Isolation and characterization of ovokinin, a bradykinin B1 agonist peptide derived from ovalbumin Peptides 1995, 16, 785-90 10.1016/0196-9781(95)00054-N
7. Hidalgo, I. J.; Raub, T. J.; Borchardt, R. T. Characterization of the human colon carcinoma cell line (Caco-2) as a model system for intestinal epithelial permeability Gastroenterology 1989, 96, 736-749 10.1016/S0016-5085(89)80072-1
8. Artursson, P.; Karlsson, J. Correlation between oral drug absorption in humans and apparent drug permeability coefficients in human intestinal epithelial (Caco-2) cells Biochem. Biophys. Res. Commun. 1991, 175, 880-885 10.1016/0006-291X(91)91647-U
9. Shimizu, M.; Son, D. O. Food-derived peptides and intestinal functions Curr. Pharm. Des. 2007, 13, 885-895 10.2174/138161207780414287
10. Miguel, M.; Davalos, A.; Manso, M. A.; de la Pena, G.; Lasuncion, M. A.; Lopez-Fandino, R. Transepithelial transport across Caco-2 cell monolayers of antihypertensive egg-derived peptides. PepT1-mediated flux of Tyr-Pro-lle Mol. Nutr. Food Res. 2008, 52, 1507-1513 10.1002/mnfr.200700503
11. Artursson, P.; Palm, K.; Luthman, K. Caco-2 monolayers in experimental and theoretical predictions of drug transport Adv. Drug Delivery Rev. 2001, 46, 27-43 10.1016/S0169-409X(00)00128-9
12. Shimizu, K.; Sato, M.; Zhang, Y.; Kouguchi, T.; Takahata, Y.; Morimatsu, F.; Shimizu, M. Molecular Size of Collagen Peptide Reverses the Permeability of Caco-2 Cells Biosci., Biotechnol., Biochem. 2010, 74, 1123-1125 10.1271/bbb.100015
13. Vig, B. S.; Stouch, T. R.; Timoszyk, J. K.; Quan, Y.; Wall, D. A.; Smith, R. L.; Faria, T. N. Human PEPT1 pharmacophore distinguishes between dipeptide transport and binding J. Med. Chem. 2006, 49, 3636-3644 10.1021/jm0511029
14. Fei, Y. J.; Kanai, Y.; Nussberger, S.; Ganapathy, V.; Leibach, F. H.; Romero, M. F.; Singh, S. K.; Boron, W. F.; Hediger, M. A. Expression cloning of a mammalian proton-coupled oligopeptide transporter Nature 1994, 368, 563-566 10.1038/368563a0
15. Pauletti, G. M.; Okumu, F. W.; Borchardt, R. T. Effect of size and charge on the passive diffusion of peptides across Caco-2 cell monolayers via the paracellular pathway Pharm. Res. 1997, 14, 164-168 10.1023/A:1012040425146
16. Lei, L.; Sun, H.; Liu, D.; Liu, L.; Li, S. Transport of Val-Leu-Pro-Val-Pro in human intestinal epithelial (Caco-2) cell monolayers J. Agric. Food Chem. 2008, 56, 3582-3586 10.1021/jf703640p
17. Quiros, A.; Davalos, A.; Lasuncion, M. A.; Ramos, M.; Recio, I. Bioavailability of the antihypertensive peptide LHLPLP: Transepithelial flux of HLPLP Int. Dairy J. 2008, 18, 279-286 10.1016/j.idairyj.2007.09.006
18. Satake, M.; Enjoh, M.; Nakamura, Y.; Takano, T.; Kawamura, Y.; Arai, S.; Shimizu, M. Transepithelial transport of the bioactive tripeptide, Val-Pro-Pro, in human intestinal Caco-2 cell monolayers Biosci., Biotechnol., Biochem. 2002, 66, 378-384 10.1271/bbb.66.378
19. Kovacs-Nolan, J.; Phillips, M.; Mine, Y. Advances in the value of eggs and egg components for human health J. Agric. Food Chem. 2005, 53, 8421-8431 10.1021/jf050964f
20. Liu, J.; Yu, Z.; Zhao, W.; Lin, S.; Wang, E.; Zhang, Y.; Hao, H.; Wang, Z.; Chen, F. Isolation and identification of angiotensin-converting enzyme inhibitory peptides from egg white protein hydrolysates Food Chem. 2010, 122, 1159-1163 10.1016/j.foodchem.2010.03.108
21. Yu, Z.; Yin, Y.; Zhao, W.; Wang, F.; Yu, Y.; Liu, B.; Liu, J.; Chen, F. Characterization of ACE-Inhibitory Peptide Associated with Antioxidant and Anticoagulation Properties J. Food Sci. 2011, 76, C1149-C1155 10.1111/j.1750-3841.2011.02367.x
22. Yu, Z.; Yin, Y.; Zhao, W.; Chen, F.; Liu, J. Antihypertensive Effect of Angiotensin-Converting Enzyme Inhibitory Peptide RVPSL on Spontaneously Hypertensive Rats by Regulating Gene Expression of the Renin-Angiotensin System J. Agric. Food Chem. 2014, 62, 912-917 10.1021/jf405189y
23. Hubatsch, I.; Ragnarsson, E. G. E.; Artursson, P. Determination of drug permeability and prediction of drug absorption in Caco-2 monolayers Nat. Protoc. 2007, 2, 2111-2119 10.1038/nprot.2007.303
24. Shimizu, M.; Tsunogai, M.; Arai, S. Transepithelial transport of oligopeptides in the human intestinal cell, Caco-2 Peptides 1997, 18, 681-687 10.1016/S0196-9781(97)00002-8
25. Ding, L.; Zhang, Y.; Jiang, Y.; Wang, L.; Liu, B.; Liu, J. Transport of Egg White ACE-Inhibitory Peptide, Gln-Ile-Gly-Leu-Phe, in Human Intestinal Caco-2 Cell Monolayers with Cytoprotective Effect J. Agric. Food Chem. 2014, 62, 3177-3182 10.1021/jf405639w
26. Liu, J.; Yu, Z.; Zhao, W.; Lu, J.; Chen, F.; Lin, S. Liquid Chromatographic Assay of Peptides Activity with Inhibiting Angiotensin Converting Enzyme Chem. Res. Chin. Univ. 2010, 26, 712-716
27. Vermeirssen, V.; Van Camp, J.; Verstraete, W. Bioavailability of angiotensin I converting enzyme inhibitory peptides Br. J. Nutr. 2004, 92, 357-366 10.1079/BJN20041189
28. Howell, S.; Kenny, A. J.; Turner, A. J. A survey of membrane peptidases in two human colonic cell lines, Caco-2 and HT-29 Biochem. J. 1992, 284, 595-601 10.1042/bj2840595
29. Aertgeerts, K.; Ye, S.; Tennant, M. G.; Kraus, M. L.; Rogers, J.; Sang, B.-C.; Skene, R. J.; Webb, D. R.; Prasad, G. S. Crystal structure of human dipeptidyl peptidase IV in complex with a decapeptide reveals details on substrate specificity and tetrahedral intermediate formation Protein Sci. 2004, 13, 412-421 10.1110/ps.03460604
30. Wiedeman, P. E.; Trevillyan, J. M. Dipeptidyl peptidase IV inhibitors for the treatment of impaired glucose tolerance and type 2 diabetes Curr. Opin. Invest. Drugs 2003, 4, 412-420
31. Umezawa, H.; Aoyagi, T.; Ogawa, K.; Naganawa, H.; Hamada, M.; Takeuchi, T. Diprotins A and B, inhibitors of dipeptidyl aminopeptidase IV, produced by bacteria J. Antibiot. 1984, 37, 422-425 10.7164/antibiotics.37.422
32. Rahfeld, J.; Schierborn, M.; Hartrodt, B.; Neubert, K.; Heins, J. Are diprotin A (Ile-Pro-Ile) and diprotin B (Val-Pro-Leu) inhibitors or substrates of dipeptidyl peptidase IV? Biochim. Biophys. Acta, Protein Struct. Mol. Enzymol. 1991, 1076, 314-316 10.1016/0167-4838(91)90284-7
33. Fernandez-Musoles, R.; Salom, J. B.; Castello-Ruiz, M.; Contreras, M. d. M.; Recio, I.; Manzanares, P. Bioavailability of antihypertensive lactoferricin B-derived peptides: Transepithelial transport and resistance to intestinal and plasma peptidases Int. Dairy J. 2013, 32, 169-174 10.1016/j.idairyj.2013.05.009
34. Iwan, M.; Jarmolowska, B.; Bielikowicz, K.; Kostyra, E.; Kostyra, H.; Kaczmarski, M. Transport of mu-opioid receptor agonists and antagonist peptides across Caco-2 monolayer Peptides 2008, 29, 1042-1047 10.1016/j.peptides.2008.01.018
35. Sienkiewicz-Szlapka, E.; Jarmolowska, B.; Krawczuk, S.; Kostyra, E.; Kostyra, H.; Bielikowicz, K. Transport of bovine milk-derived opioid peptides across a Caco-2 monolayer Int. Dairy J. 2009, 19, 252-257 10.1016/j.idairyj.2008.10.007
36. Mentlein, R. Dipeptidyl-peptidase IV (CD26)-role in the inactivation of regulatory peptides Regul. Pept. 1999, 85, 9-24 10.1016/S0167-0115(99)00089-0
37. Hoffmann, T.; Reinhold, D.; Kahne, T.; Faust, J.; Neubert, K.; Frank, R.; Ansorge, S. Inhibition of dipeptidyl peptidase IV (DP IV) by anti-DP IV antibodies and non-substrate X-X-Pro- oligopeptides ascertained by capillary electrophoresis J. Chromatogr. A 1995, 716, 355-362 10.1016/0021-9673(95)00411-F
38. Sun, H.; Liu, D.; Li, S.; Qin, Z. Transepithelial Transport Characteristics of the Antihypertensive Peptide, Lys-Val-Leu-Pro-Val-Pro, in Human Intestinal Caco-2 Cell Monolayers Biosci., Biotechnol., Biochem. 2009, 73, 293-298 10.1271/bbb.80473
39. Shimizu, K.; Sato, M.; Zhang, Y.; Kouguchi, T.; Takahata, Y.; Morimatsu, F.; Shimizu, M. The Bioavailable Octapeptide Gly-Ala-Hyp-Gly-Leu-Hyp-Gly-Pro Stimulates Nitric Oxide Synthesis in Vascular Endothelial Cells J. Agric. Food Chem. 2010, 58, 6960-6965 10.1021/jf100388w
40. Chua, H. L.; Jois, S.; Sim, M. K.; Go, M. L. Transport of angiotensin peptides across the Caco-2 monolayer Peptides 2004, 25, 1327-1338 10.1016/j.peptides.2004.06.009
41. Cakir-Kiefer, C.; Miclo, L.; Balandras, F.; Dary, A.; Soligot, C.; Le Roux, Y. Transport Across Caco-2 Cell Monolayer and Sensitivity to Hydrolysis of Two Anxiolytic Peptides from alpha(s1)-Casein, alpha-Casozepine, and alpha(s1)-Casein-(f91-97): Effect of Bile Salts J. Agric. Food Chem. 2011, 59, 11956-11965 10.1021/jf202890e
42. Antunes, F.; Andrade, F.; Ferreira, D.; Nielsen, H. M.; Sarmento, B. Models to Predict Intestinal Absorption of Therapeutic Peptides and Proteins Curr. Drug Metab. 2013, 14, 4-20 10.2174/138920013804545160
43. Shimizu, M. Modulation of intestinal functions by food substances Nahrung 1999, 43, 154-158 10.1002/(SICI)1521-3803(19990601)43:3<154::AID-FOOD154>3.3.CO;2-1
44. Regazzo, D.; Molle, D.; Gabai, G.; Tome, D.; Dupont, D.; Leonil, J.; Boutrou, R. The (193-209) 17-residues peptide of bovine beta-casein is transported through Caco-2 monolayer Mol. Nutr. Food Res. 2010, 54, 1428-1435 10.1002/mnfr.200900443
45. Daniel, H. Molecular and integrative physiology of intestinal peptide transport Annu. Rev. Physiol. 2004, 66, 361-384 10.1146/annurev.physiol.66.032102.144149
46. Brandsch, M. Drug transport via the intestinal peptide transporter PepT1 Curr. Opin. Pharmacol. 2013, 13, 881-887 10.1016/j.coph.2013.08.004
47. Salamat-Miller, N.; Johnston, T. P. Current strategies used to enhance the paracellular transport of therapeutic polypeptides across the intestinal epithelium Int. J. Pharm. 2005, 294, 201-216 10.1016/j.ijpharm.2005.01.022
48. Marchiando, A. M.; Graham, W. V.; Turner, J. R. Epithelial Barriers in Homeostasis and Disease Annu. Rev. Pathol.: Mech. Dis. 2010, 5, 119-144 10.1146/annurev.pathol.4.110807.092135
49. Linnankoski, J.; Makela, J.; Palmgren, J.; Mauriala, T.; Vedin, C.; Ungell, A.-L.; Lazorova, L.; Artursson, P.; Urtti, A.; Yliperttula, M. Paracellular Porosity and Pore Size of the Human Intestinal Epithelium in Tissue and Cell Culture Models J. Pharm. Sci. 2010, 99, 2166-2175 10.1002/jps.21961
50. Brandsch, M.; Knutter, I.; Thunecke, F.; Hartrodt, B.; Born, I.; Borner, V.; Hirche, F.; Fischer, G.; Neubert, K. Decisive structural determinants for the interaction of proline derivatives with the intestinal H+/peptide symporter Eur. J. Biochem. 1999, 266, 502-508 10.1046/j.1432-1327.1999.00885.x
51. Brandsch, M.; Knuetter, I.; Bosse-Doenecke, E. Pharmaceutical and pharmacological importance of peptide transporters J. Pharm. Pharmacol. 2008, 60, 543-585 10.1211/jpp.60.5.0002