Antibiotics Increase Gut Metabolism and Antioxidant Proteins and Decrease Acute Phase Response and Necrotizing Enterocolitis in Preterm Neonates

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Jiang, Pingping ^a,b   Jensen, Michael Ladegaard ^b   Cilieborg, Malene Skovsted ^b   Thymann, Thomas ^b   Wan, Jennifer Man Fan ^a   Sit, Wai Hung ^a   Tipoe, George L ^a   Sangild, Per Torp ^b  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ALBUMIN; ALPHA GLUCOSIDASE; AMPICILLIN; ANTIBIOTIC AGENT; BIOLOGICAL MARKER; CATALASE; COMPLEMENT COMPONENT C3; DIPEPTIDYL PEPTIDASE IV; FIBRINOGEN; FICOLIN; GENTAMICIN; GLUTAMYL AMINOPEPTIDASE; HAPTOGLOBIN; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 27; INORGANIC PYROPHOSPHATASE; LACTASE; LAMININ RECEPTOR; METRONIDAZOLE; MICROSOMAL AMINOPEPTIDASE; PYROPHOSPHATASE 1; REGENERATING ISLET DERIVED PROTEIN 3GAMMA; TRANSFERRIN; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ACUTE PHASE RESPONSE; AMINO ACID METABOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; CARBOHYDRATE METABOLISM; COMPLEMENT SYSTEM; CONTROLLED STUDY; ENZYME ACTIVITY; FATTY ACID METABOLISM; FEMALE; GRAM POSITIVE BACTERIUM; INTESTINE VILLUS; IRON METABOLISM; MALE; NECROTIZING ENTEROCOLITIS; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PREMATURITY; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN SYNTHESIS; PROTEOMICS; SWINE; WESTERN BLOTTING;

BACTERIA (MICROORGANISMS); SUIDAE;

EID: 84866374358     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0044929     Document Type: Article

References (59)

1. Sangild PT, Siggers RH, Schmidt M, Elnif J, Bjornvad CR, et al. (2006) Diet- and colonization-dependent intestinal dysfunction predisposes to necrotizing enterocolitis in preterm pigs. Gastroenterology 130: 1776-1792.
2. Siggers RH, Siggers J, Thymann T, Boye M, Sangild PT, (2010) Nutritional modulation of the gut microbiota and immune system in preterm neonates susceptible to necrotizing enterocolitis. J Nutr Biochem 22: 511-521.
3. Sangild PT, (2006) Gut response to enteral nutrition in preterm infants and animals. Exp Biol Med 231: 1695-1711.
4. Wang Y, Hoenig JD, Malin KJ, Qamar S, Petrof EO, et al. (2009) 16S rRNA gene-based analysis of fecal microbiota from preterm infants with and without necrotizing enterocolitis. ISME J 3: 944-954.
5. Mai V, Young CM, Ukhanova M, Wang X, Sun Y, et al. (2011) Fecal microbiota in premature infants prior to necrotizing enterocolitis. PLoS ONE 6: e20647.
6. Preidis GA, Versalovic J, (2009) Targeting the human microbiome with antibiotics, probiotics, and prebiotics: gastroenterology enters the metagenomics era. Gastroenterology 136: 2015-2031.
7. Neu J, (2005) Neonatal necrotizing enterocolitis: An update. Acta Paediatrica 94: 100-105.
8. Fell JME, (2005) Neonatal inflammatory intestinal disease; necrotising enterocolitis and allergic colitis. Early Hum Dev 81: 117-122.
9. Thompson AM, Bizzarro MJ, (2008) Necrotizing enterocolitis in newborns: pathogenesis, prevention and management. Drugs 68: 1227-1238.
10. Siggers J, Sangild PT, Jensen TK, Siggers RH, Skovgaard K, et al. (2011) Transition from parenteral to enteral nutrition induces immediate diet-dependent gut histological and immunological responses in preterm neonates. Am J Physiol Gastrointest Liver Physiol 301: G435-G445.
11. Jiang P, Sangild PT, Sit W-H, Ngai HH-Y, Xu R, et al. (2009) Temporal proteomic analysis of intestine developing necrotizing enterocolitis following enteral formula feeding to preterm pigs. J Proteome Res 8: 72-81.
12. Jiang P, Sangild PT, Siggers RH, Sit W-H, Lee C-L, et al. (2010) Bacterial colonization affects the intestinal proteome of preterm pigs susceptible to necrotizing enterocolitis. Neonatology 99: 280-288.
13. Brook I, (2008) Microbiology and management of neonatal necrotizing enterocolitis. Am J Perinatol 25: 111-118.
14. Krediet TG, van Lelyveld N, Vijlbrief DC, Brouwers HAA, Kramer WLM, et al. (2003) Microbiological factors associated with neonatal necrotizing enterocolitis: protective effect of early antibiotic treatment. Acta Paediatr 92: 1180-1182.
15. Biçakçi Ü, Tander B, Aritürk E, Aydin B, Aydin O, et al. (2005) Effects of omeprazole and gentamicin on the biochemical and histopathological alterations of the hypoxia/ reoxygenation induced intestinal injury in newborn rats. Pediatr Surg Int 21: 800-805.
16. Bjornvad CR, Thymann T, Deutz NE, Burrin DG, Jensen SK, et al. (2008) Enteral feeding induces diet-dependent mucosal dysfunction, bacterial proliferation, and necrotizing enterocolitis in preterm pigs on parenteral nutrition. Am J Physiol Gastrointest Liver Physiol 295: G1092-G1103.
17. Schlapbach LJ, Mattmann M, Thiel S, Boillat C, Otth M, et al. (2010) Differential role of the lectin pathway of complement activation in susceptibility to neonatal sepsis. Clin Infect Dis 51: 153-162.
18. Pope MR, Hoffman SM, Tomlinson S, Fleming SD, (2010) Complement regulates TLR4-mediated inflammatory responses during intestinal ischemia reperfusion. Mol Immunol 48: 356-364.
19. Richardson WM, Sodhi CP, Russo A, Siggers RH, Afrazi A, et al. (2010) Nucleotide-binding oligomerization domain-2 inhibits toll-like receptor-4 signaling in the intestinal epithelium. Gastroenterology 139: 904-917.e906.
20. Soliman A, Michelsen KS, Karahashi H, Lu J, Meng FJ, et al. (2010) Platelet-activating factor induces TLR4 expression in intestinal epithelial cells: implication for the pathogenesis of necrotizing enterocolitis. PLoS ONE 5: e15044.
21. Jilling T, Simon D, Lu J, Meng FJ, Li D, et al. (2006) The roles of bacteria and TLR4 in rat and murine models of necrotizing enterocolitis. J Immunol 177: 3273-3282.
22. Schlapbach LJ, Aebi C, Fisch U, Ammann RA, Otth M, et al. (2008) Higher cord blood levels of mannose-binding lectin-associated serine protease-2 in infants with necrotising enterocolitis. Pediatr Res 64: 562-566.
23. Schlapbach LJ, Kessler U, Thiel S, Hansen AG, Nelle M, et al. (2009) M-ficolin in the neonatal period: Associations with need for mechanical ventilation and mortality in premature infants with necrotising enterocolitis. Mol Immunol 46: 2597-2603.
24. Endo Y, Matsushita M, Fujita T, (2011) The role of ficolins in the lectin pathway of innate immunity. Int J Biochem Cell Biol 43: 705-712.
25. Ito R, Shin-Ya M, Kishida T, Urano A, Takada R, et al. (2006) Interferon-gamma is causatively involved in experimental inflammatory bowel disease in mice. Clin Exp Immunol 146: 330-338.
26. Insenser M, Martinez-Garcia MA, Montes R, San-Millan JL, Escobar-Morreale HF (2010) Proteomic analysis of plasma in the polycystic ovary syndrome identifies novel markers involved in iron metabolism, acute-phase response, and inflammation. J Clin Endocrinol Metab: jc.2010-0220.
27. Tripathi A, Lammers KM, Goldblum S, Shea-Donohue T, Netzel-Arnett S, et al. (2009) Identification of human zonulin, a physiological modulator of tight junctions, as prehaptoglobin-2. Proc Natl Acad Sci USA 106: 16799-16804.
28. Cash HL, Whitham CV, Behrendt CL, Hooper LV, (2006) Symbiotic bacteria direct expression of an intestinal bactericidal lectin. Science 313: 1126-1130.
29. Brandl K, Plitas G, Mihu CN, Ubeda C, Jia T, et al. (2008) Vancomycin-resistant enterococci exploit antibiotic-induced innate immune deficits. Nature 455: 804-807.
30. Kinnebrew MA, Ubeda C, Zenewicz LA, Smith N, Flavell RA, et al. (2010) Bacterial flagellin stimulates toll like receptor 5 dependent defense against vancomycin resistant enterococcus infection. J Infect Dis 201: 534-543.
31. Petrof EO, Ciancio MJ, Chang EB, (2004) Role and regulation of intestinal epithelial heat shock proteins in health and disease. Chin J Dig Dis 5: 45-50.
32. Bhattacharyya S, Dudeja PK, Tobacman JK, (2009) ROS, Hsp27, and IKKβ mediate dextran sodium sulfate (DSS) activation of IκBa, NFκB, and IL-8. Inflamm Bowel Dis 15: 673-683.
33. Liu B, Yang Y, Qiu Z, Staron M, Hong F, et al. (2010) Folding of toll-like receptors by the HSP90 paralogue gp96 requires a substrate-specific cochaperone. Nat Commun 1: 79.
34. Liu B, Li Z, (2008) Endoplasmic reticulum HSP90b1 (gp96, grp94) optimizes B-cell function via chaperoning integrin and TLR but not immunoglobulin. Blood 112: 1223-1230.
35. Daugaard M, Jäättelä M, Rohde M, (2005) Hsp70-2 is required for tumor cell growth and survival. Cell Cycle 4: 877-880.
36. Vydra N, Winiarski B, Rak-Raszewska A, Piglowski W, Mazurek A, et al. (2009) The expression pattern of the 70-kDa heat shock protein Hspa2 in mouse tissues. Histochem Cell Biol 132: 319-330.
37. Eisenstein RS, (2000) Iron regulatory proteins and the molecular control of mammalian iron metabolism. Annu Rev Nutr 20: 627-662.
38. Zhang A-S, Enns CA, (2009) Molecular mechanisms of normal iron homeostasis. Hematology 2009: 207-214.
39. Sreedhar B, Nair KM, (2005) Modulation of aconitase, metallothionein, and oxidative stress in zinc-deficient rat intestine during zinc and iron repletion. Free Radic Biol Med 39: 999-1008.
40. Amano T, Fu L, Marshak A, Kwak O, Shi Y-B, (2005) Spatio-temporal regulation and cleavage by matrix metalloproteinase stromelysin-3 implicate a role for laminin receptor in intestinal remodeling during Xenopus laevis metamorphosis. Dev Dyn 234: 190-200.
41. Taylor CA, Sun Z, Cliche DO, Ming H, Eshaque B, et al. (2007) Eukaryotic translation initiation factor 5A induces apoptosis in colon cancer cells and associates with the nucleus in response to tumour necrosis factor [alpha] signalling. Exp Cell Res 313: 437-449.
42. Mathur S, Cleary KR, Inamdar N, Kim YH, Steck P, et al. (1998) Overexpression of elongation factor-1γ protein in colorectal carcinoma. Cancer 82: 816-821.
43. Hayano T, Kikuchi M, (1995) Cloning and sequencing of the cDNA encoding human P5. Gene 164: 377-378.
44. Pryer NK, Salama NR, Schekman R, Kaiser CA, (1993) Cytosolic Sec13p complex is required for vesicle formation from the endoplasmic reticulum in vitro. J Cell Biol 120: 865-875.
45. Wang C, Yoo Y, Fan H, Kim E, Guan K-L, et al. (2010) Regulation of integrin β1 recycling to lipid rafts by rab1a to promote cell migration. J Biol Chem 285: 29398-29405.
46. Chen CY, Balch WE, (2006) The Hsp90 chaperone complex regulates GDI-dependent Rab recycling. Mol Biol Cell 17: 3494-3507.
47. Edelmann MJ, Kessler BM, (2008) Ubiquitin and ubiquitin-like specific proteases targeted by infectious pathogens: Emerging patterns and molecular principles. Biochim Biophys Acta 1782: 809-816.
48. Haley B, Paunesku T, Protif{hook}á M, Woloschak GE, (2009) Response of heterogeneous ribonuclear proteins (hnRNP) to ionising radiation and their involvement in DNA damage repair. Int J Radiat Biol 85: 643-655.
49. Matsushima M, Takahashi T, Ichinose M, Miki K, Kurokawa K, et al. (1991) Structural and immunological evidence for the identity of prolyl aminopeptidase with leucyl aminopeptidase. Biochem Biophys Res Commun 178: 1459-1464.
50. Ko KM, Lee W, Yu J-R, Ahnn J, (2007) PYP-1, inorganic pyrophosphatase, is required for larval development and intestinal function in C. elegans. FEBS Letters 581: 5445-5453.
51. Chakravortty D, Nanda Kumar KS, (2000) Bacterial lipopolysaccharide induces cytoskeletal rearrangement in small intestinal lamina propria fibroblasts: actin assembly is essential for lipopolysaccharide signaling. Biochim Biophys Acta 1500: 125-136.
52. Habtezion A, Toivola DM, Asghar MN, Kronmal GS, Brooks JD, et al. (2011) Absence of keratin 8 confers a paradoxical microflora-dependent resistance to apoptosis in the colon. Proc Natl Acad Sci USA 108: 1445-1450.
53. Shi T, Moulton VR, Lapchak PH, Deng G-M, Dalle Lucca JJ, et al. (2009) Ischemia-mediated aggregation of the actin cytoskeleton is one of the major initial events resulting in ischemia-reperfusion injury. Am J Physiol Gastrointest Liver Physiol 296: G339-347.
54. Basavappa S, Vulapalli SR, Zhang H, Yule D, Coon S, et al. (2005) Chloride channels in the small intestinal cell line IEC-18. J Cell Physiol 202: 21-31.
55. Schultheiss G, Siefjediers A, Diener M, (2005) Muscarinic receptor etimulation activates a Ca2+ dependent Cl- conductance in rat distal colon. J Membr Biol 204: 117-127.
56. Loewen ME, Gabriel SE, Forsyth GW, (2002) The calcium-dependent chloride conductance mediator pCLCA1. Am J Physiol Cell Physiol 283: C412-C421.
57. Sangild PT, Sjostrom H, Noren O, Fowden AL, Silver M, (1995) The prenatal development and glucocorticoid control of brush-border hydrolases in the pig small intestine Pediatr Res. 37: 207-212.
58. Cilieborg MS, Boye M, Molbak L, Thymann T, Sangild PT, (2011) Preterm birth and necrotizing enterocolitis alter gut colonization in pigs. Pediatr Res 69: 10-16.
59. Jiang P, Wan JM-F, Sit W-H, Lee C-L, Schmidt M, et al. (2011) Enteral feeding in utero induces marked intestinal structural and functional proteome changes in pig fetuses. Pediatr Res 69.