Gastrointestinal and hepatic mechanisms limiting entry and dissemination of lipopolysaccharide into the systemic circulation

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 311, Issue 1, 2016, Pages G1-G15

  Guerville, Mathilde ^a   Boudry, Gaëlle ^a  

^a CEMAGREF   (France)

Author keywords

Antimicrobial peptides; Intestinal barrier function; Liver LPS detoxification; Metabolic endotoxemia; Sepsis

Indexed keywords

CARRIER PROTEIN; CLATHRIN; ENDOTOXIN; LIPOPOLYSACCHARIDE; LIPOPOLYSACCHARIDE BINDING PROTEIN; MUCIN; POLYPEPTIDE ANTIBIOTIC AGENT;

BACTERIAL COLONIZATION; BINDING AFFINITY; BIOSYNTHESIS; CARBOHYDRATE ANALYSIS; DEACETYLATION; DETOXIFICATION; ENDOCYTOSIS; ENDOTOXEMIA; GASTROINTESTINAL TRACT FUNCTION; GASTROINTESTINAL TRANSIT; GOBLET CELL; HOST RESISTANCE; HUMAN; IMMUNOCOMPETENT CELL; INTESTINE EPITHELIUM; INTESTINE FLORA; LAMINA PROPRIA; LIPID RAFT; LIVER FUNCTION; METABOLIC SYNDROME X; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; SEPSIS; SYSTEMIC CIRCULATION; TRANSCYTOSIS; ANIMAL; BACTERIAL TRANSLOCATION; BACTERIUM; BLOOD; CHEMISTRY; HOST PATHOGEN INTERACTION; IMMUNOLOGY; INTESTINE; LIVER; METABOLISM; MICROBIOLOGY; PERMEABILITY;

ANIMALS; BACTERIA; BACTERIAL TRANSLOCATION; GASTROINTESTINAL MICROBIOME; HOST-PATHOGEN INTERACTIONS; HUMANS; INTESTINES; LIPOPOLYSACCHARIDES; LIVER; PERMEABILITY; SEPSIS;

EID: 84984629889     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00098.2016     Document Type: Review

References (165)

1. Abreu MT. Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function. Nat Rev Immunol 10: 131–144, 2010.
2. Abreu MT, Fukata M, Arditi M. TLR signaling in the gut in health and disease. J Immunol 174: 4453–4460, 2005.
3. Akira S, Takeda K. Toll-like receptor signalling. Nat Rev Immunol 4: 499–511, 2004.
4. Albenberg L, Esipova TV, Judge CP, Bittinger K, Chen J, Laughlin A, Grunberg S, Baldassano RN, Lewis JD, Li H, Thom SR, Bushman FD, Vinogradov SA, Wu GD. Correlation between intraluminal oxygen gradient and radial partitioning of intestinal microbiota. Gastroenterology 147: 1055.e8–1063.e8, 2014.
5. Amar J, Burcelin R, Ruidavets JB, Cani PD, Fauvel J, Alessi MC, Chamontin B, Ferrieres J. Energy intake is associated with endotoxemia in apparently healthy men. Am J Clin Nutr 87: 1219–1223, 2008.
6. Angelakis E, Armougom F, Carriere F, Bachar D, Laugier R, Lagier JC, Robert C, Michelle C, Henrissat B, Raoult D. A metagenomic investigation of the duodenal microbiota reveals links with obesity. PloS One 10: e0137784, 2015.
7. Angus DC, van der Poll T. Severe sepsis and septic shock. N Engl J Med 369: 840–851, 2013.
8. Ayabe T, Satchell DP, Wilson CL, Parks WC, Selsted ME, Ouellette AJ. Secretion of microbicidal alpha-defensins by intestinal Paneth cells in response to bacteria. Nat Immunol 1: 113–118, 2000.
9. Bartholomew JW, Mittwer T. The Gram stain. Bacteriol Rev 16: 1–29, 1952.
10. Bates JM, Akerlund J, Mittge E, Guillemin K. Intestinal alkaline phosphatase detoxifies lipopolysaccharide and prevents inflammation in zebrafish in response to the gut microbiota. Cell Host Microbe 2: 371–382, 2007.
11. Beatty WL, Meresse S, Gounon P, Davoust J, Mounier J, Sansonetti PJ, Gorvel JP. Trafficking of Shigella lipopolysaccharide in polarized intestinal epithelial cells. J Cell Biol 145: 689–698, 1999.
12. Benoit B, Laugerette F, Plaisancie P, Geloen A, Bodennec J, Estienne M, Pineau G, Bernalier-Donadille A, Vidal H, Michalski MC. Increasing fat content from 20 to 45 wt% in a complex diet induces lower endotoxemia in parallel with an increased number of intestinal goblet cells in mice. Nutr Res 35: 346–356, 2015.
13. Bevins CL, Salzman NH. Paneth cells, antimicrobial peptides and maintenance of intestinal homeostasis. Nat Rev Microbiol 9: 356–368, 2011.
14. Bietrix F, Yan D, Nauze M, Rolland C, Bertrand-Michel J, Comera C, Schaak S, Barbaras R, Groen AK, Perret B, Terce F, Collet X. Accelerated lipid absorption in mice overexpressing intestinal SR-BI. J Biol Chem 281: 7214–7219, 2006.
15. Biswas SK, Lopez-Collazo E. Endotoxin tolerance: new mechanisms, molecules and clinical significance. Trends Immunol 30: 475–487, 2009.
16. Boudry G, Hamilton MK. Milk formula and intestinal barrier function. In: Handbook of Dietary and Nutritional Aspects of Bottle Feeding, edited by Preedy VR, Watson RR, Zibadi S. Wageningen, The Netherlands: Wageningen Academic, 2014, p. 571–586.
17. Boutagy NE, McMillan RP, Frisard MI, Hulver MW. Metabolic endotoxemia with obesity: is it real and is it relevant? Biochimie 124: 11–20, 2016.
18. Brown EM, Sadarangani M, Finlay BB. The role of the immune system in governing host-microbe interactions in the intestine. Nat Immunol 14: 660–667, 2013.
19. Cai L, Ji A, de Beer FC, Tannock LR, van der Westhuyzen DR. SR-BI protects against endotoxemia in mice through its roles in glucocorticoid production and hepatic clearance. J Clin Invest 118: 364–375, 2008.
20. Cai SF, Kirby RJ, Howles PN, Hui DY. Differentiation-dependent expression and localization of the class B type I scavenger receptor in intestine. J Lipid Res 42: 902–909, 2001.
21. Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D, Neyrinck AM, Fava F, Tuohy KM, Chabo C, Waget A, Delmee E, Cousin B, Sulpice T, Chamontin B, Ferrieres J, Tanti JF, Gibson GR, Casteilla L, Delzenne NM, Alessi MC, Burcelin R. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56: 1761–1772, 2007.
22. Cani PD, Bibiloni R, Knauf C, Waget A, Neyrinck AM, Delzenne NM, Burcelin R. Changes in gut microbiota control metabolic endotoxemia- induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 57: 1470–1481, 2008.
23. Canny G, Cario E, Lennartsson A, Gullberg U, Brennan C, Levy O, Colgan SP. Functional and biochemical characterization of epithelial bactericidal/permeability-increasing protein. Am J Physiol Gastrointest Liver Physiol 290: G557–G567, 2006.
24. Caradonna L, Amati L, Magrone T, Pellegrino NM, Jirillo E, Caccavo D. Enteric bacteria, lipopolysaccharides and related cytokines in inflammatory bowel disease: biological and clinical significance. J Endotoxin Res 6: 205–214, 2000.
25. Cario E, Brown D, McKee M, Lynch-Devaney K, Gerken G, Podolsky DK. Commensal-associated molecular patterns induce selective Toll-like receptor-trafficking from apical membrane to cytoplasmic compartments in polarized intestinal epithelium. Am J Pathol 160: 165–173, 2002.
26. Cario E, Podolsky DK. Differential alteration in intestinal epithelial cell expression of Toll-like receptor 3 (TLR3) and TLR4 in inflammatory bowel disease. Infect Immun 68: 7010–7017, 2000.
27. Caroff M, Karibian D. Structure of bacterial lipopolysaccharides. Carbohydr Res 338: 2431–2447, 2003.
28. Cash HL, Whitham CV, Behrendt CL, Hooper LV. Symbiotic bacteria direct expression of an intestinal bactericidal lectin. Science 313: 1126–1130, 2006.
29. Cerovic V, Jenkins CD, Barnes AG, Milling SW, MacPherson GG, Klavinskis LS. Hyporesponsiveness of intestinal dendritic cells to TLR stimulation is limited to TLR4. J Immunol 182: 2405–2415, 2009.
30. Chaby R. Des Endotoxines aux Lipopolysaccharides. Paris: Lavoisier, 2010.
31. Chaby R. Lipopolysaccharide-binding molecules: transporters, blockers and sensors. Cell Mol Life Sci 61: 1697–1713, 2004.
32. Chaby R, Pedron T, Girard R. Nontoxic forms of lipopolysaccharides, poorly cleared in vivo, are present in variable amounts in phenolextracted endotoxins. J Infect Dis 167: 131–140, 1993.
33. Chung CS, Chang PF, Liao CH, Lee TH, Chen Y, Lee YC, Wu MS, Wang HP, Ni YH. Differences of microbiota in small bowel and faeces between irritable bowel syndrome patients and healthy subjects. Scand J Gastroenterol 51: 410–419, 2016.
34. Creely SJ, McTernan PG, Kusminski CM, Fisher FM, Da Silva NF, Khanolkar M, Evans M, Harte AL, Kumar S. Lipopolysaccharide activates an innate immune system response in human adipose tissue in obesity and type 2 diabetes. Am J Physiol Endocrinol Metab 292: E740–E747, 2007.
35. Cullen TW, Schofield WB, Barry NA, Putnam EE, Rundell EA, Trent MS, Degnan PH, Booth CJ, Yu H, Goodman AL. Gut microbiota. Antimicrobial peptide resistance mediates resilience of prominent gut commensals during inflammation. Science 347: 170–175, 2015.
36. Davis JE, Gabler NK, Walker-Daniels J, Spurlock ME. Tlr-4 deficiency selectively protects against obesity induced by diets high in saturated fat. Obesity 16: 1248–1255, 2008.
37. de Haas CJ, Haas PJ, van Kessel KP, van Strijp JA. Affinities of different proteins and peptides for lipopolysaccharide as determined by biosensor technology. Biochem Biophys Res Commun 252: 492–496, 1998.
38. Dlugosz A, Winckler B, Lundin E, Zakikhany K, Sandstrom G, Ye W, Engstrand L, Lindberg G. No difference in small bowel microbiota between patients with irritable bowel syndrome and healthy controls. Sci Rep 5: 8508, 2015.
39. Doherty GJ, McMahon HT. Mechanisms of endocytosis. Annu Rev Biochem 78: 857–902, 2009.
40. Dowman JK, Tomlinson JW, Newsome PN. Pathogenesis of nonalcoholic fatty liver disease. QJM 103: 71–83, 2010.
41. Drago-Serrano ME, de la Garza-Amaya M, Luna JS, Campos- Rodriguez R. Lactoferrin-lipopolysaccharide (LPS) binding as key to antibacterial and antiendotoxic effects. Int Immunopharmacol 12: 1–9, 2012.
42. Dubin W, Martin TR, Swoveland P, Leturcq DJ, Moriarty AM, Tobias PS, Bleecker ER, Goldblum SE, Hasday JD. Asthma and endotoxin: lipopolysaccharide-binding protein and soluble CD14 in bronchoalveolar compartment. Am J Physiol Lung Cell Mol Physiol 270: L736–L744, 1996.
43. Dunzendorfer S, Lee HK, Soldau K, Tobias PS. TLR4 is the signaling but not the lipopolysaccharide uptake receptor. J Immunol 173: 1166–1170, 2004.
44. Dziarski R, Tapping RI, Tobias PS. Binding of bacterial peptidoglycan to CD14. J Biol Chem 273: 8680–8690, 1998.
45. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, Gill SR, Nelson KE, Relman DA. Diversity of the human intestinal microbial flora. Science 308: 1635–1638, 2005.
46. Elass-Rochard E, Roseanu A, Legrand D, Trif M, Salmon V, Motas C, Montreuil J, Spik G. Lactoferrin-lipopolysaccharide interaction: involvement of the 28–34 loop region of human lactoferrin in the high-affinity binding to Escherichia coli 055B5 lipopolysaccharide. Biochem J 312: 839–845, 1995.
47. Eliakim R, Mahmood A, Alpers DH. Rat intestinal alkaline phosphatase secretion into lumen and serum is coordinately regulated. Biochim Biophys Acta 1091: 1–8, 1991.
48. Emanuele E, Orsi P, Boso M, Broglia D, Brondino N, Barale F, di Nemi SU, Politi P. Low-grade endotoxemia in patients with severe autism. Neurosci Lett 471: 162–165, 2010.
49. Erridge C, Attina T, Spickett CM, Webb DJ. A high-fat meal induces low-grade endotoxemia: evidence of a novel mechanism of postprandial inflammation. Am J Clin Nutr 86: 1286–1292, 2007.
50. Erridge C, Bennett-Guerrero E, Poxton IR. Structure and function of lipopolysaccharides. Microbes Infect 4: 837–851, 2002.
51. Everard A, Geurts L, Caesar R, Van Hul M, Matamoros S, Duparc T, Denis RG, Cochez P, Pierard F, Castel J, Bindels LB, Plovier H, Robine S, Muccioli GG, Renauld JC, Dumoutier L, Delzenne NM, Luquet S, Backhed F, Cani PD. Intestinal epithelial MyD88 is a sensor switching host metabolism towards obesity according to nutritional status. Nat Commun 5: 5648, 2014.
52. Everard A, Lazarevic V, Derrien M, Girard M, Muccioli GG, Neyrinck AM, Possemiers S, Van Holle A, Francois P, de Vos WM, Delzenne NM, Schrenzel J, Cani PD. Responses of gut microbiota and glucose and lipid metabolism to prebiotics in genetic obese and dietinduced leptin-resistant mice. Diabetes 60: 2775–2786, 2011.
53. Everard A, Lazarevic V, Gaia N, Johansson M, Stahlman M, Backhed F, Delzenne NM, Schrenzel J, Francois P, Cani PD. Microbiome of prebiotic-treated mice reveals novel targets involved in host response during obesity. ISME J 8: 2116–2130, 2014.
54. Fernandez-Real JM, Perez del Pulgar S, Luche E, Moreno-Navarrete JM, Waget A, Serino M, Sorianello E, Sanchez-Pla A, Pontaque FC, Vendrell J, Chacon MR, Ricart W, Burcelin R, Zorzano A. CD14 modulates inflammation-driven insulin resistance. Diabetes 60: 2179–2186, 2011.
55. Forsythe RM, Xu DZ, Lu Q, Deitch EA. Lipopolysaccharide-induced enterocyte-derived nitric oxide induces intestinal monolayer permeability in an autocrine fashion. Shock 17: 180–184, 2002.
56. Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci USA 104: 13780–13785, 2007.
57. Fukuoka S, Richter W, Howe J, Andra J, Rossle M, Alexander C, Gutsmann T, Brandenburg K. Biophysical investigations into the interactions of endotoxins with bile acids. Innate immun 18: 307–317, 2012.
58. Fusunyan RD, Nanthakumar NN, Baldeon ME, Walker WA. Evidence for an innate immune response in the immature human intestine: Toll-like receptors on fetal enterocytes. Pediatr Res 49: 589–593, 2001.
59. Gazzano-Santoro H, Parent JB, Conlon PJ, Kasler HG, Tsai CM, Lill-Elghanian DA, Hollingsworth RI. Characterization of the structural elements in lipid A required for binding of a recombinant fragment of bactericidal/permeability-increasing protein rBPI23. Infect Immun 63: 2201–2205, 1995.
60. Ge Y, Ezzell RM, Warren HS. Localization of endotoxin in the rat intestinal epithelium. J Infect Dis 182: 873–881, 2000.
61. Ghoshal S, Witta J, Zhong J, de Villiers W, Eckhardt E. Chylomicrons promote intestinal absorption of lipopolysaccharides. J Lipid Res 50: 90–97, 2009.
62. Gioannini TL, Teghanemt A, Zhang D, Prohinar P, Levis EN, Munford RS, Weiss JP. Endotoxin-binding proteins modulate the susceptibility of bacterial endotoxin to deacylation by acyloxyacyl hydrolase. J Biol Chem 282: 7877–7884, 2007.
63. Goldberg RF, Austen WG Jr, Zhang X, Munene G, Mostafa G, Biswas S, McCormack M, Eberlin KR, Nguyen JT, Tatlidede HS, Warren HS, Narisawa S, Millan JL, and Hodin RA. Intestinal alkaline phosphatase is a gut mucosal defense factor maintained by enteral nutrition. Proc Natl Acad Sci USA 105: 3551–3556, 2008.
64. Grossman N, Leive L. Complement activation via the alternative pathway by purified Salmonella lipopolysaccharide is affected by its structure but not its O-antigen length. J Immunol 132: 376–385, 1984.
65. Gu S, Chen D, Zhang JN, Lv X, Wang K, Duan LP, Nie Y, Wu XL. Bacterial community mapping of the mouse gastrointestinal tract. PloS One 8: e74957, 2013.
66. Guo S, Al-Sadi R, Said HM, Ma TY. Lipopolysaccharide causes an increase in intestinal tight junction permeability in vitro and in vivo by inducing enterocyte membrane expression and localization of TLR-4 and CD14. Am J Pathol 182: 375–387, 2013.
67. Guo Y, Zhou G, He C, Yang W, He Z, Liu Z. Serum levels of lipopolysaccharide and 1,3-beta-D-glucan refer to the severity in patients with Crohn’s disease. Mediators Inflamm 2015: 843089, 2015.
68. Hampton RY, Golenbock DT, Penman M, Krieger M, Raetz CR. Recognition and plasma clearance of endotoxin by scavenger receptors. Nature 352: 342–344, 1991.
69. Harris HW, Grunfeld C, Feingold KR, Rapp JH. Human very low density lipoproteins and chylomicrons can protect against endotoxininduced death in mice. J Clin Invest 86: 696–702, 1990.
70. Haversen L, Ohlsson BG, Hahn-Zoric M, Hanson LA, Mattsby- Baltzer I. Lactoferrin down-regulates the LPS-induced cytokine production in monocytic cells via NF-kappaB. Cell Immunol 220: 83–95, 2002.
71. Hornef MW, Frisan T, Vandewalle A, Normark S, Richter-Dahlfors A. Toll-like receptor 4 resides in the Golgi apparatus and colocalizes with internalized lipopolysaccharide in intestinal epithelial cells. J Exp Med 195: 559–570, 2002.
72. Hornef MW, Normark BH, Vandewalle A, Normark S. Intracellular recognition of lipopolysaccharide by Toll-like receptor 4 in intestinal epithelial cells. J Exp Med 198: 1225–1235, 2003.
73. Hosoi T, Yokoyama S, Matsuo S, Akira S, Ozawa K. Myeloid differentiation factor 88 (MyD88)-deficiency increases risk of diabetes in mice. PloS One 5: e12537, 2010.
74. Hotamisligil GS. Inflammation and metabolic disorders. Nature 444: 860–867, 2006.
75. Howe SE, Lickteig DJ, Plunkett KN, Ryerse JS, Konjufca V. The uptake of soluble and particulate antigens by epithelial cells in the mouse small intestine. PloS One 9: e86656, 2014.
76. Hu Y, Peng J, Tai N, Hu C, Zhang X, Wong FS, Wen L. Maternal antibiotic treatment protects offspring from diabetes development in nonobese diabetic mice by generation of tolerogenic APCs. J Immunol 195: 4176–4184, 2015.
77. Jakaitis BM, Denning PW. Human breast milk and the gastrointestinal innate immune system. Clin Perinatol 41: 423–435, 2014.
78. Jakobsson HE, Abrahamsson TR, Jenmalm MC, Harris K, Quince C, Jernberg C, Bjorksten B, Engstrand L, Andersson AF. Decreased gut microbiota diversity, delayed Bacteroidetes colonisation and reduced Th1 responses in infants delivered by caesarean section. Gut 63: 559–566, 2014.
79. Johnson AR, Milner JJ, Makowski L. The inflammation highway: metabolism accelerates inflammatory traffic in obesity. Immunol Rev 249: 218–238, 2012.
80. Kaca W, Roth RI, Levin J. Hemoglobin, a newly recognized lipopolysaccharide (LPS)-binding protein that enhances LPS biological activity. J Biol Chem 269: 25078–25084, 1994.
81. Kallio KA, Hatonen KA, Lehto M, Salomaa V, Mannisto S, Pussinen PJ. Endotoxemia, nutrition, and cardiometabolic disorders. Acta Diabetol 52: 395–404, 2015.
82. Kirschning C, Unbehaun A, Lamping N, Pfeil D, Herrmann F, Schumann RR. Control of transcriptional activation of the lipopolysaccharide binding protein (LBP) gene by proinflammatory cytokines. Cytokines Cell Mol Ther 3: 59–62, 1997.
83. Kitchens RL, Thompson PA. Modulatory effects of sCD14 and LBP on LPS-host cell interactions. J Endotoxin Res 11: 225–229, 2005.
84. Kitchens RL, Wolfbauer G, Albers JJ, Munford RS. Plasma lipoproteins promote the release of bacterial lipopolysaccharide from the monocyte cell surface. J Biol Chem 274: 34116–34122, 1999.
85. Kleinridders A, Schenten D, Konner AC, Belgardt BF, Mauer J, Okamura T, Wunderlich FT, Medzhitov R, Bruning JC. MyD88 signaling in the CNS is required for development of fatty acid-induced leptin resistance and diet-induced obesity. Cell Metab 10: 249–259, 2009.
86. Kless C, Muller VM, Schuppel VL, Lichtenegger M, Rychlik M, Daniel H, Klingenspor M, Haller D. Diet-induced obesity causes metabolic impairment independent of alterations in gut barrier integrity. Mol Nutr Food Res 59: 968–978, 2015.
87. Knoop KA, McDonald KG, McCrate S, McDole JR, Newberry RD. Microbial sensing by goblet cells controls immune surveillance of luminal antigens in the colon. Mucosal Immunol 8: 198–210, 2015.
88. Koprivnjak T, Peschel A, Gelb MH, Liang NS, Weiss JP. Role of charge properties of bacterial envelope in bactericidal action of human group IIA phospholipase A2 against Staphylococcus aureus. J Biol Chem 277: 47636–47644, 2002.
89. Kritselis I, Tzanetakou V, Adamis G, Anthopoulos G, Antoniadou E, Bristianou M, Kotanidou A, Lignos M, Polyzos K, Retsas T, Sassopoulou P, Papaioannou AI, Sinapidis D, Sereti K, Vittoros V, Ghanas P, Gogos C, Giamarellos-Bourboulis EJ. The level of endotoxemia in sepsis varies in relation to the underlying infection: impact on final outcome. Immunol Lett 152: 167–172, 2013.
90. Labeta MO, Vidal K, Nores JE, Arias M, Vita N, Morgan BP, Guillemot JC, Loyaux D, Ferrara P, Schmid D, Affolter M, Borysiewicz LK, Donnet-Hughes A, Schiffrin EJ. Innate recognition of bacteria in human milk is mediated by a milk-derived highly expressed pattern recognition receptor, soluble CD14. J Exp Med 191: 1807–1812, 2000.
91. Lalles JP. Intestinal alkaline phosphatase: multiple biological roles in maintenance of intestinal homeostasis and modulation by diet. Nutr Rev 68: 323–332, 2010.
92. Lalles JP. Intestinal alkaline phosphatase: novel functions and protective effects. Nutr Rev 72: 82–94, 2014.
93. Laugerette F, Alligier M, Bastard JP, Drai J, Chanseaume E, Lambert- Porcheron S, Laville M, Morio B, Vidal H, Michalski MC. Overfeeding increases postprandial endotoxemia in men: inflammatory outcome may depend on LPS transporters LBP and sCD14. Mol Nutr Food Res 58: 1513–1518, 2014.
94. Laugerette F, Furet JP, Debard C, Daira P, Loizon E, Geloen A, Soulage CO, Simonet C, Lefils-Lacourtablaise J, Bernoud-Hubac N, Bodennec J, Peretti N, Vidal H, Michalski MC. Oil composition of high-fat diet affects metabolic inflammation differently in connection with endotoxin receptors in mice. Am J Physiol Endocrinol Metab 302: E374–E386, 2012.
95. Laugerette F, Vors C, Geloen A, Chauvin MA, Soulage C, Lambert- Porcheron S, Peretti N, Alligier M, Burcelin R, Laville M, Vidal H, Michalski MC. Emulsified lipids increase endotoxemia: possible role in early postprandial low-grade inflammation. J Nutr Biochem 22: 53–59, 2011.
96. Lee WJ, Farmer JL, Hilty M, Kim YB. The protective effects of lactoferrin feeding against endotoxin lethal shock in germfree piglets. Infect Immun 66: 1421–1426, 1998.
97. Levels JH, Abraham PR, van den Ende A, van Deventer SJ. Distribution and kinetics of lipoprotein-bound endotoxin. Infect Immun 69: 2821–2828, 2001.
98. Levy E, Menard D, Suc I, Delvin E, Marcil V, Brissette L, Thibault L, Bendayan M. Ontogeny, immunolocalisation, distribution and function of SR-BI in the human intestine. J Cell Sci 117: 327–337, 2004.
99. Li JD, Feng W, Gallup M, Kim JH, Gum J, Kim Y, Basbaum C. Activation of NF-kappaB via a Src-dependent Ras-MAPK-pp90rsk pathway is required for Pseudomonas aeruginosa-induced mucin overproduction in epithelial cells. Proc Natl Acad Sci USA 95: 5718–5723, 1998.
100. Lobo MV, Huerta L, Ruiz-Velasco N, Teixeiro E, de la Cueva P, Celdran A, Martin-Hidalgo A, Vega MA, Bragado R. Localization of the lipid receptors CD36 and CLA-1/SR-BI in the human gastrointestinal tract: towards the identification of receptors mediating the intestinal absorption of dietary lipids. J Histochem Cytochem 49: 1253–1260, 2001.
101. Loonen LM, Stolte EH, Jaklofsky MT, Meijerink M, Dekker J, van Baarlen P, Wells JM. REG3gamma-deficient mice have altered mucus distribution and increased mucosal inflammatory responses to the microbiota and enteric pathogens in the ileum. Mucosal Immunol 7: 939–947, 2014.
102. Lu M, Zhang M, Takashima A, Weiss J, Apicella MA, Li XH, Yuan D, Munford RS. Lipopolysaccharide deacylation by an endogenous lipase controls innate antibody responses to Gram-negative bacteria. Nat Immunol 6: 989–994, 2005.
103. Maitra SK, Rachmilewitz D, Eberle D, Kaplowitz N. The hepatocellular uptake and biliary excretion of endotoxin in the rat. Hepatology 1: 401–407, 1981.
104. Mani V, Hollis JH, Gabler NK. Dietary oil composition differentially modulates intestinal endotoxin transport and postprandial endotoxemia. Nutr Metab (Lond) 10: 6, 2013.
105. Mariat D, Firmesse O, Levenez F, Guimaraes V, Sokol H, Dore J, Corthier G, Furet JP. The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age. BMC Microbiol 9: 123, 2009.
106. Mimura Y, Sakisaka S, Harada M, Sata M, Tanikawa K. Role of hepatocytes in direct clearance of lipopolysaccharide in rats. Gastroenterology 109: 1969–1976, 1995.
107. Mollen KP, Gribar SC, Anand RJ, Kaczorowski DJ, Kohler JW, Branca MF, Dubowski TD, Sodhi CP, Hackam DJ. Increased expression and internalization of the endotoxin coreceptor CD14 in enterocytes occur as an early event in the development of experimental necrotizing enterocolitis. J Pediatr Surg 43: 1175–1181, 2008.
108. Monte SV, Caruana JA, Ghanim H, Sia CL, Korzeniewski K, Schentag JJ, Dandona P. Reduction in endotoxemia, oxidative and inflammatory stress, and insulin resistance after Roux-en-Y gastric bypass surgery in patients with morbid obesity and type 2 diabetes mellitus. Surgery 151: 587–593, 2012.
109. Mowat AM, Agace WW. Regional specialization within the intestinal immune system. Nat Rev Immunol 14: 667–685, 2014.
110. Muller CA, Autenrieth IB, Peschel A. Innate defenses of the intestinal epithelial barrier. Cell Mol Life Sci 62: 1297–1307, 2005.
111. Munford RS, Hall CL. Detoxification of bacterial lipopolysaccharides (endotoxins) by a human neutrophil enzyme. Science 234: 203–205, 1986.
112. Nikaido H. Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev 67: 593–656, 2003.
113. Nockher WA, Wigand R, Schoeppe W, Scherberich JE. Elevated levels of soluble CD14 in serum of patients with systemic lupus erythematosus. Clin Exp Immunol 96: 15–19, 1994.
114. Okuda S, Sherman DJ, Silhavy TJ, Ruiz N, Kahne D. Lipopolysaccharide transport and assembly at the outer membrane: the PEZ model. Nat Rev Microbiol 14: 337–345, 2016.
115. Opal SM. Endotoxins and other sepsis triggers. Contrib Nephrol 167: 14–24, 2010.
116. Otte JM, Cario E, Podolsky DK. Mechanisms of cross hyporesponsiveness to Toll-like receptor bacterial ligands in intestinal epithelial cells. Gastroenterology 126: 1054–1070, 2004.
117. Pasternak BA, D’Mello S, Jurickova II, Han X, Willson T, Flick L, Petiniot L, Uozumi N, Divanovic S, Traurnicht A, Bonkowski E, Kugathasan S, Karp CL, Denson LA. Lipopolysaccharide exposure is linked to activation of the acute phase response and growth failure in pediatric Crohn’s disease and murine colitis. Inflamm Bowel Dis 16: 856–869, 2010.
118. Pelaseyed T, Bergstrom JH, Gustafsson JK, Ermund A, Birchenough GM, Schutte A, van der Post S, Svensson F, Rodriguez- Pineiro AM, Nystrom EE, Wising C, Johansson ME, Hansson GC. The mucus and mucins of the goblet cells and enterocytes provide the first defense line of the gastrointestinal tract and interact with the immune system. Immunol Rev 260: 8–20, 2014.
119. Pendyala S, Walker JM, Holt PR. A high-fat diet is associated with endotoxemia that originates from the gut. Gastroenterology 142: 1100.e2–1101.e2, 2012.
120. Petsch D, Anspach FB. Endotoxin removal from protein solutions. J Biotechnol 76: 97–119, 2000.
121. Pierre N, Deldicque L, Barbe C, Naslain D, Cani PD, Francaux M. Toll-like receptor 4 knockout mice are protected against endoplasmic reticulum stress induced by a high-fat diet. PloS One 8: e65061, 2013.
122. Platt N, Gordon S. Is the class A macrophage scavenger receptor (SR-A) multifunctional?—the mouse’s tale. J Clin Invest 108: 649–654, 2001.
123. Plociennikowska A, Hromada-Judycka A, Borzecka K, Kwiatkowska K. Co-operation of TLR4 and raft proteins in LPS-induced pro-inflammatory signaling. Cell Mol Life Sci 72: 557–581, 2015.
124. Poltorak A, He X, Smirnova I, Liu MY, Van Huffel C, Du X, Birdwell D, Alejos E, Silva M, Galanos C, Freudenberg M, Ricciardi- Castagnoli P, Layton B, Beutler B. Defective LPS signaling in C3H/ HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282: 2085–2088, 1998.
125. Poupon R. Liver alkaline phosphatase: a missing link between choleresis and biliary inflammation. Hepatology 61: 2080–2090, 2015.
126. Pyo JS, Ko YS, Kang G, Kim DH, Kim WH, Lee BL, Sohn JH. Bile acid induces MUC2 expression and inhibits tumor invasion in gastric carcinomas. J Cancer Res Clin Oncol 141: 1181–1188, 2015.
127. Radin MS, Sinha S, Bhatt BA, Dedousis N, O’Doherty RM. Inhibition or deletion of the lipopolysaccharide receptor Toll-like receptor-4 confers partial protection against lipid-induced insulin resistance in rodent skeletal muscle. Diabetologia 51: 336–346, 2008.
128. Raetz CR, Reynolds CM, Trent MS, Bishop RE. Lipid A modification systems in gram-negative bacteria. Annu Rev Biochem 76: 295–329, 2007.
129. Raetz CR, Whitfield C. Lipopolysaccharide endotoxins. Annu Rev Biochem 71: 635–700, 2002.
130. Read TE, Harris HW, Grunfeld C, Feingold KR, Calhoun MC, Kane JP, Rapp JH. Chylomicrons enhance endotoxin excretion in bile. Infect Immun 61: 3496–3502, 1993.
131. Rensen PC, Oosten M, Bilt E, Eck M, Kuiper J, Berkel TJ. Human recombinant apolipoprotein E redirects lipopolysaccharide from Kupffer cells to liver parenchymal cells in rats in vivo. J Clin Invest 99: 2438–2445, 1997.
132. Rodriguez-Pineiro AM, Bergstrom JH, Ermund A, Gustafsson JK, Schutte A, Johansson ME, Hansson GC. Studies of mucus in mouse stomach, small intestine, and colon. II. Gastrointestinal mucus proteome reveals Muc2 and Muc5ac accompanied by a set of core proteins. Am J Physiol Gastrointest Liver Physiol 305: G348–G356, 2013.
133. Roncon-Albuquerque R Jr, Moreira-Rodrigues M, Faria B, Ferreira AP, Cerqueira C, Lourenco AP, Pestana M, von Hafe P, Leite- Moreira AF. Attenuation of the cardiovascular and metabolic complications of obesity in CD14 knockout mice. Life Sci 83: 502–510, 2008.
134. Rowlands BJ, Soong CV, Gardiner KR. The gastrointestinal tract as a barrier in sepsis. Br Med Bull 55: 196–211, 1999.
135. Sass V, Schneider T, Wilmes M, Korner C, Tossi A, Novikova N, Shamova O, Sahl HG. Human beta-defensin 3 inhibits cell wall biosynthesis in Staphylococci. Infect Immun 78: 2793–2800, 2010.
136. Schumann RR, Latz E. Lipopolysaccharide-binding protein. Chem Immunol 74: 42–60, 2000.
137. Selsted ME, Ouellette AJ. Mammalian defensins in the antimicrobial immune response. Nat Immunol 6: 551–557, 2005.
138. Shao B, Lu M, Katz SC, Varley AW, Hardwick J, Rogers TE, Ojogun N, Rockey DC, Dematteo RP, Munford RS. A host lipase detoxifies bacterial lipopolysaccharides in the liver and spleen. J Biol Chem 282: 13726–13735, 2007.
139. Simons K, Toomre D. Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 1: 31–39, 2000.
140. Siqueiros-Cendon T, Arevalo-Gallegos S, Iglesias-Figueroa BF, Garcia- Montoya IA, Salazar-Martinez J, Rascon-Cruz Q. Immunomodulatory effects of lactoferrin. Acta Pharmacol Sin 35: 557–566, 2014.
141. Smith PD, Smythies LE, Mosteller-Barnum M, Sibley DA, Russell MW, Merger M, Sellers MT, Orenstein JM, Shimada T, Graham MF, Kubagawa H. Intestinal macrophages lack CD14 and CD89 and consequently are down-regulated for LPS- and IgA-mediated activities. J Immunol 167: 2651–2656, 2001.
142. Suzuki M, Hisamatsu T, Podolsky DK. Gamma interferon augments the intracellular pathway for lipopolysaccharide (LPS) recognition in human intestinal epithelial cells through coordinated up-regulation of LPS uptake and expression of the intracellular Toll-like receptor 4-MD-2 complex. Infect Immun 71: 3503–3511, 2003.
143. Taveira da Silva AM, Kaulbach HC, Chuidian FS, Lambert DR, Suffredini AF, Danner RL. Brief report: shock and multiple-organ dysfunction after self-administration of Salmonella endotoxin. N Engl J Med 328: 1457–1460, 1993.
144. Tobias PS, Soldau K, Ulevitch RJ. Identification of a lipid A binding site in the acute phase reactant lipopolysaccharide binding protein. J Biol Chem 264: 10867–10871, 1989.
145. Tomita M, Ohkubo R, Hayashi M. Lipopolysaccharide transport system across colonic epithelial cells in normal and infective rat. Drug Metab Pharmacokinet 19: 33–40, 2004.
146. Tsukumo DM, Carvalho-Filho MA, Carvalheira JB, Prada PO, Hirabara SM, Schenka AA, Araujo EP, Vassallo J, Curi R, Velloso LA, Saad MJ. Loss-of-function mutation in Toll-like receptor 4 prevents diet-induced obesity and insulin resistance. Diabetes 56: 1986–1998, 2007.
147. Tuin A, Huizinga-Van der Vlag A, van Loenen-Weemaes AM, Meijer DK, Poelstra K. On the role and fate of LPS-dephosphorylating activity in the rat liver. Am J Physiol Gastrointest Liver Physiol 290: G377–G385, 2006.
148. Vaara M, Viljanen P. Binding of polymyxin B nonapeptide to gramnegative bacteria. Antimicrob Agents Chemother 27: 548–554, 1985.
149. Vaishnava S, Behrendt CL, Ismail AS, Eckmann L, Hooper LV. Paneth cells directly sense gut commensals and maintain homeostasis at the intestinal host-microbial interface. Proc Natl Acad Sci USA 105: 20858–20863, 2008.
150. van Ampting MT, Loonen LM, Schonewille AJ, Konings I, Vink C, Iovanna J, Chamaillard M, Dekker J, van der Meer R, Wells JM, Bovee-Oudenhoven IM. Intestinally secreted C-type lectin Reg3b attenuates salmonellosis but not listeriosis in mice. Infect Immun 80: 1115–1120, 2012.
151. Van Bossuyt H, De Zanger RB, Wisse E. Cellular and subcellular distribution of injected lipopolysaccharide in rat liver and its inactivation by bile salts. J Hepatol 7: 325–337, 1988.
152. van Deventer SJ, Buller HR, ten Cate JW, Aarden LA, Hack CE, Sturk A. Experimental endotoxemia in humans: analysis of cytokine release and coagulation, fibrinolytic, and complement pathways. Blood 76: 2520–2526, 1990.
153. van Langevelde P, Kwappenberg KM, Groeneveld PH, Mattie H, van Dissel JT. Antibiotic-induced lipopolysaccharide (LPS) release from Salmonella typhi: delay between killing by ceftazidime and imipenem and release of LPS. Antimicrob Agents Chemother 42: 739–743, 1998.
154. Vaure C, Liu Y. A comparative review of Toll-like receptor 4 expression and functionality in different animal species. Front Immunol 5: 316, 2014.
155. Viriyakosol S, Tobias PS, Kitchens RL, Kirkland TN. MD-2 binds to bacterial lipopolysaccharide. J Biol Chem 276: 38044–38051, 2001.
156. Vishnyakova TG, Bocharov AV, Baranova IN, Chen Z, Remaley AT, Csako G, Eggerman TL, Patterson AP. Binding and internalization of lipopolysaccharide by Cla-1, a human orthologue of rodent scavenger receptor B1. J Biol Chem 278: 22771–22780, 2003.
157. Vreugdenhil AC, Rousseau CH, Hartung T, Greve JW, van’t Veer C, Buurman WA. Lipopolysaccharide (LPS)-binding protein mediates LPS detoxification by chylomicrons. J Immunol 170: 1399–1405, 2003.
158. Vreugdenhil AC, Snoek AM, Greve JW, Buurman WA. Lipopolysaccharide- binding protein is vectorially secreted and transported by cultured intestinal epithelial cells and is present in the intestinal mucus of mice. J Immunol 165: 4561–4566, 2000.
159. Vreugdenhil AC, Snoek AM, van’t Veer C, Greve JW, Buurman WA. LPS-binding protein circulates in association with apoB-containing lipoproteins and enhances endotoxin-LDL/VLDL interaction. J Clin Invest 107: 225–234, 2001.
160. Wald D, Qin J, Zhao Z, Qian Y, Naramura M, Tian L, Towne J, Sims JE, Stark GR, Li X. SIGIRR, a negative regulator of Toll-like receptor-interleukin 1 receptor signaling. Nat Immunol 4: 920–927, 2003.
161. Wright SD, Ramos RA, Tobias PS, Ulevitch RJ, Mathison JC. CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein. Science 249: 1431–1433, 1990.
162. Zhang GH, Mann DM, Tsai CM. Neutralization of endotoxin in vitro and in vivo by a human lactoferrin-derived peptide. Infect Immun 67: 1353–1358, 1999.
163. Zhang R, Miller RG, Gascon R, Champion S, Katz J, Lancero M, Narvaez A, Honrada R, Ruvalcaba D, McGrath MS. Circulating endotoxin and systemic immune activation in sporadic amyotrophic lateral sclerosis (sALS). J Neuroimmunol 206: 121–124, 2009.
164. Zhao W, Wang Y, Liu S, Huang J, Zhai Z, He C, Ding J, Wang J, Wang H, Fan W, Zhao J, Meng H. The dynamic distribution of porcine microbiota across different ages and gastrointestinal tract segments. PloS One 10: e0117441, 2015.
165. Zweigner J, Gramm HJ, Singer OC, Wegscheider K, Schumann RR. High concentrations of lipopolysaccharide-binding protein in serum of patients with severe sepsis or septic shock inhibit the lipopolysaccharide response in human monocytes. Blood 98: 3800–3808, 2001.