Bovine lactoferrin regulates cell survival, apoptosis and inflammation in intestinal epithelial cells and preterm pig intestine

Journal of Proteomics

Volumn 139, Issue , 2016, Pages 95-102

  Nguyen, Duc Ninh ^a   Jiang, Pingping ^a   Stensballe, Allan ^b   Bendixen, Emøke ^c   Sangild, Per T ^a   Chatterton, Dereck E W ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b AALBORG UNIVERSITY   (Denmark)

^c AARHUS UNIVERSITY   (Denmark)

Author keywords

Apoptosis; Inflammation; Lactoferrin; Necrotizing enterocolitis

Indexed keywords

BOVINE LACTOFERRIN; HYPOXIA INDUCIBLE FACTOR 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; LACTOFERRIN; PROTEIN BAX; PROTEIN BCL 2; PROTEOME; UNCLASSIFIED DRUG; APOPTOSIS REGULATORY PROTEIN; CELL CYCLE PROTEIN;

AMINO ACID METABOLISM; ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BOVINE; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; ENERGY METABOLISM; GLYCOLYSIS; HEIGHT; INFLAMMATION; INTESTINE EPITHELIUM CELL; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NEWBORN; NONHUMAN; PIG; PREMATURITY; PRIORITY JOURNAL; PROTEIN SYNTHESIS; PROTEOMICS; SIGNAL TRANSDUCTION; STIMULATION; SUPPLEMENTATION; SURVIVAL; UPREGULATION; ANIMAL; DRUG EFFECTS; EPITHELIUM CELL; INTESTINE MUCOSA; METABOLISM; PATHOLOGY;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CATTLE; CELL CYCLE PROTEINS; CELL SURVIVAL; EPITHELIAL CELLS; INFLAMMATION; INTESTINAL MUCOSA; LACTOFERRIN; SWINE;

EID: 84961797227     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2016.03.020     Document Type: Article

References (50)

1. Marshall K. Therapeutic applications of whey protein. Altern. Med. Rev. 2004, 9:136-156.
2. Baker E.N., Baker H.M. A structural framework for understanding the multifunctional character of lactoferrin. Biochimie 2009, 91:3-10.
3. Adamkin D.H. Mother's milk, feeding strategies, and lactoferrin to prevent necrotizing enterocolitis. J. Parenter. Enter. Nutr. 2012, 36:25S-29S.
4. Jiang R., Lopez V., Kelleher S.L., Lönnerdal B. Apo- and holo-lactoferrin are both internalized by lactoferrin receptor via clathrin-mediated endocytosis but differentially affect ERK-signaling and cell proliferation in caco-2 cells. J. Cell. Physiol. 2011, 226:3022-3031.
5. Manzoni P., Decembrino L., Stolfi I., Pugni L., Rinaldi M., Cattani S., et al. Lactoferrin and prevention of late-onset sepsis in the pre-term neonates. Early Hum. Dev. 2010, 86:59-61.
6. Manzoni P., Rinaldi M., Cattani S., Pugni L., Romeo M.G., Messner H., et al. Bovine lactoferrin supplementation for prevention of late-onset sepsis in very low-birth-weight neonates: a randomized trial. J. Am. Med. Assoc. 2009, 302:1421-1428.
7. Togawa J.-I., Nagase H., Tanaka K., Inamori M., Nakajima A., Ueno N., et al. Oral administration of lactoferrin reduces colitis in rats via modulation of the immune system and correction of cytokine imbalance. J. Gastroenterol. Hepatol. 2002, 17:1291-1298.
8. Lee W.J., Farmer J.L., Hilty M., Kim Y.B. The protective effects of lactoferrin feeding against endotoxin lethal shock in germfree piglets. Infect. Immun. 1998, 66:1421-1426.
9. Orsi N. The antimicrobial activity of lactoferrin: current status and perspectives. Biometals 2004, 17:189-196.
10. Appelmelk B.J., An Y.Q., Geerts M., Thijs B.G., de Boer H.A., MacLaren D.M., et al. Lactoferrin is a lipid A-binding protein. Infect. Immun. 1994, 62:2628-2632.
11. Nguyen D.N., Li Y., Sangild P.T., Bering S.B., Chatterton D.E.W. Effects of bovine lactoferrin on the immature porcine intestine. Br. J. Nutr. 2014, 111:321-331.
12. Oh S.-M., Lee S.-H., Lee B.-J., Pyo C.-W., Yoo N.-K., Lee S.Y., et al. A distinct role of neutrophil lactoferrin in RelA/p65 phosphorylation on Ser536 by recruiting TNF receptor-associated factors to IkappaB kinase signaling complex. J. Immunol. 2007, 179:5686-5692.
13. Curran C.S., Demick K.P., Mansfield J.M. Lactoferrin activates macrophages via TLR4-dependent and -independent signaling pathways. Cell. Immunol. 2006, 242:23-30.
14. Lönnerdal B., Jiang R., Du X. Bovine lactoferrin can be taken up by the human intestinal lactoferrin receptor and exert bioactivities. J. Pediatr. Gastroenterol. Nutr. 2011.
15. Nguyen D.N., Jiang P., Jacobsen S., Sangild P.T., Bendixen E., Chatterton D.E.W. Protective effects of transforming growth factor β2 in intestinal epithelial cells by regulation of proteins associated with stress and endotoxin responses. PLoS ONE 2015, 10:e0117608.
16. Danielsen M., Hornshøj H., Siggers R.H., Jensen B.B., van Kessel A.G., Bendixen E. Effects of bacterial colonization on the porcine intestinal proteome. J. Proteome Res. 2007, 6:2596-2604.
17. Bennike T., Ayturk U., Haslauer C.M., Froehlich J.W., Proffen B.L., Barnaby O., et al. A normative study of the synovial fluid proteome from healthy porcine knee joints. J. Proteome Res. 2014.
18. Cox J., Hein M.Y., Luber C.A., Paron I., Nagaraj N., Mann M. MaxLFQ allows accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction. Mol. Cell. Proteomics 2014.
19. Chatterton D.E.W., Rasmussen J.T., Heegaard C.W., Sørensen E.S., Petersen T.E. In vitro digestion of novel milk protein ingredients for use in infant formulas: research on biological functions. Trends Food Sci. Technol. 2004, 15:373-383.
20. D. Bates, M. Mächler, B. Bolker, S. Walker, Fitting Linear Mixed-Effects Models using lme4, arXiv:1406.5823 [stat] (2014). (accessed September 1, 2014). http://arxiv.org/abs/1406.5823.
21. Hothorn T., Bretz F., Westfall P. Simultaneous inference in general parametric models. Biom. J. 2008, 50:346-363.
22. Sharma D., Shastri S. Lactoferrin and neonatology - role in neonatal sepsis and necrotizing enterocolitis: present, past and future. J. Matern. Fetal. Neonatal. Med. 2015, 1-8.
23. Ando K., Hasegawa K., Shindo K.-I., Furusawa T., Fujino T., Kikugawa K., et al. Human lactoferrin activates NF-kappaB through the Toll-like receptor 4 pathway while it interferes with the lipopolysaccharide-stimulated TLR4 signaling. FEBS J. 2010, 277:2051-2066.
24. Birgens H.S., Kristensen L.Ø., Borregaard N., Karle H., Hansen N.E. Lactoferrin-mediated transfer of iron to intracellular ferritin in human monocytes. Eur. J. Haematol. 1988, 41:52-57.
25. Shimmura S., Shimoyama M., Hojo M., Urayama K., Tsubota K. Reoxygenation injury in a cultured corneal epithelial cell line protected by the uptake of lactoferrin. Invest. Ophthalmol. Vis. Sci. 1998, 39:1346-1351.
26. Cozzi A., Levi S., Corsi B., Santambrogio P., Campanella A., Gerardi G., et al. Role of iron and ferritin in TNFα-induced apoptosis in HeLa cells. FEBS Lett. 2003, 537:187-192.
27. Lunt S.Y., Vander Heiden M.G. Aerobic glycolysis: meeting the metabolic requirements of cell proliferation. Annu. Rev. Cell Dev. Biol. 2011, 27:441-464.
28. Wakasugi K., Slike B.M., Hood J., Otani A., Ewalt K.L., Friedlander M., et al. A human aminoacyl-tRNA synthetase as a regulator of angiogenesis. PNAS 2002, 99:173-177.
29. Cun Y., Dai N., Li M., Xiong C., Zhang Q., Sui J., et al. APE1/Ref-1 enhances DNA binding activity of mutant p53 in a redox-dependent manner. Oncol. Rep. 2014, 31:901-909.
30. Park S.G., Schimmel P., Kim S. Aminoacyl tRNA synthetases and their connections to disease. PNAS 2008, 105:11043-11049.
31. Lim L.H.K., Pervaiz S. Annexin 1: the new face of an old molecule. FASEB J. 2007, 21:968-975.
32. Scannell M., Flanagan M.B., de Stefani A., Wynne K.J., Cagney G., Godson C., et al. Annexin-1 and peptide derivatives are released by apoptotic cells and stimulate phagocytosis of apoptotic neutrophils by macrophages. J. Immunol. 2007, 178:4595-4605.
33. Bidère N., Lorenzo H.K., Carmona S., Laforge M., Harper F., Dumont C., et al. Cathepsin D triggers Bax activation, resulting in selective apoptosis-inducing factor (AIF) relocation in T lymphocytes entering the early commitment phase to apoptosis. J. Biol. Chem. 2003, 278:31401-31411.
34. Baines C.P., Kaiser R.A., Purcell N.H., Blair N.S., Osinska H., Hambleton M.A., et al. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 2005, 434:658-662.
35. Li Y., Johnson N., Capano M., Edwards M., Crompton M. Cyclophilin-D promotes the mitochondrial permeability transition but has opposite effects on apoptosis and necrosis. Biochem. J. 2004, 383:101.
36. Hasegawa K., Wakino S., Yoshioka K., Tatematsu S., Hara Y., Minakuchi H., et al. Sirt1 protects against oxidative stress-induced renal tubular cell apoptosis by the bidirectional regulation of catalase expression. Biochem. Biophys. Res. Commun. 2008, 372:51-56.
37. Simon H.-U., Haj-Yehia A., Levi-Schaffer F. Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 2000, 5:415-418.
38. Rao D.S., Hyun T.S., Kumar P.D., Mizukami I.F., Rubin M.A., Lucas P.C., et al. Huntingtin-interacting protein 1 is overexpressed in prostate and colon cancer and is critical for cellular survival. J. Clin. Investig. 2002, 110:351-360. 10.1172/JCI15529.
39. Dragatsis I., Levine M.S., Zeitlin S. Inactivation of Hdh in the brain and testis results in progressive neurodegeneration and sterility in mice. Nat. Genet. 2000, 26:300-306.
40. Wu S., Luca F.D. Role of cholesterol in the regulation of growth plate chondrogenesis and longitudinal bone growth. J. Biol. Chem. 2004, 279:4642-4647.
41. Xia Y., Yeddula N., Leblanc M., Ke E., Zhang Y., Oldfield E., et al. Reduced cell proliferation by IKK2 depletion in a mouse lung-cancer model. Nat. Cell Biol. 2012, 14:257-265.
42. Hanington P.C., Barreda D.R., Belosevic M. A novel hematopoietic granulin induces proliferation of goldfish (Carassius auratus L.) macrophages. J. Biol. Chem. 2006, 281:9963-9970.
43. Feng J.Q., Guo F.-J., Jiang B.-C., Zhang Y., Frenkel S., Wang D.-W., et al. Granulin epithelin precursor: a bone morphogenic protein 2-inducible growth factor that activates Erk1/2 signaling and JunB transcription factor in chondrogenesis. FASEB J. 2010, 24:1879-1892.
44. Greijer A.E., van der Wall E. The role of hypoxia inducible factor 1 (HIF-1) in hypoxia induced apoptosis. J. Clin. Pathol. 2004, 57:1009-1014.
45. Hackam D.J., Afrazi A., Good M., Sodhi C.P. Innate immune signaling in the pathogenesis of necrotizing enterocolitis. Clin. Dev. Immunol. 2013, 2013:475415.
46. Zakharova E.T., Kostevich V.A., Sokolov A.V., Vasilyev V.B. Human apo-lactoferrin as a physiological mimetic of hypoxia stabilizes hypoxia-inducible factor-1 alpha. Biometals 2012, 25:1247-1259.
47. Semenza G.L. Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer 2003, 3:721-732.
48. Seliger B., Fedorushchenko A., Brenner W., Ackermann A., Atkins D., Hanash S., et al. Ubiquitin COOH-terminal hydrolase 1: a biomarker of renal cell carcinoma associated with enhanced tumor cell proliferation and migration. Clin. Cancer Res. 2007, 13:27-37.
49. Fähling M., Mrowka R., Steege A., Martinka P., Persson P.B., Thiele B.J. Heterogeneous nuclear ribonucleoprotein-A2/B1 modulate collagen prolyl 4-hydroxylase, α (I) mRNA stability. J. Biol. Chem. 2006, 281:9279-9286.
50. Tell G., Quadrifoglio F., Tiribelli C., Kelley M.R. The many functions of APE1/Ref-1: not only a DNA repair enzyme. Antioxid. Redox Signal. 2008, 11:601-619.