Effect of dietary cellulose supplementation on gut barrier function and apoptosis in a murine model of endotoxemia

English version

Autoři: Valentina Di Caro ^aff001; Alicia M. Alcamo ^aff001; Jessica L. Cummings ^aff001; Robert S. B. Clark ^aff001; Elizabeth A. Novak ^aff004; Kevin P. Mollen ^aff004; Michael J. Morowitz ^aff004; Rajesh K. Aneja ^aff001
Působiště autorů: Department of Critical Care Medicine, University of Pittsburgh School of Medicine, Pittsburgh, PA, United States of America ^aff001; Department of Pediatrics, University of Pittsburgh School of Medicine, Pittsburgh, PA, United States of America ^aff002; Division of Pediatric Critical Care Medicine, UPMC Children’s Hospital of Pittsburgh, Pittsburgh, PA, United States of America ^aff003; Department of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, PA, United States of America ^aff004; Division of Pediatric General and Thoracic Surgery, UPMC Children’s Hospital of Pittsburgh, Pittsburgh, PA, United States of America ^aff005
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0224838

Souhrn

The gut plays a vital role in critical illness, and alterations in the gut structure and function have been reported in endotoxemia and sepsis models. Previously, we have demonstrated a novel link between the diet-induced alteration of the gut microbiome with cellulose and improved outcomes in sepsis. As compared to mice receiving basal fiber (BF) diet, mice that were fed a non-fermentable high fiber (HF) diet demonstrated significant improvement in survival and decreased organ injury in both cecal-ligation and puncture (CLP) and endotoxin sepsis models. To understand if the benefit conferred by HF diet extends to the gut structure and function, we hypothesized that HF diet would be associated with a reduction in sepsis-induced gut epithelial loss and permeability in mice. We demonstrate that the use of dietary cellulose decreased LPS-mediated intestinal hyperpermeability and protected the gut from apoptosis. Furthermore, we noted a significant increase in epithelial cell proliferation, as evidenced by an increase in the percentage of bromodeoxyuridine-positive cells in HF fed mice as compared to BF fed mice. Thus, the use of HF diet is a simple and effective tool that confers benefit in a murine model of sepsis, and understanding the intricate relationship between the epithelial barrier, gut microbiota, and diet will open-up additional therapeutic avenues for the treatment of gut dysfunction in critical illness.

Klíčová slova:

Diet – Gastrointestinal tract – Mouse models – Apoptosis – Microbiome – Sepsis – Cellulose – Permeability

Zdroje

1. Kalhs P, Brugger S, Schwarzinger I, Greinix HT, Keil F, Kyrle PA, et al. Microangiopathy following allogeneic marrow transplantation. Association with cyclosporine and methylprednisolone for graft-versus-host disease prophylaxis. Transplantation. 1995;60(9):949–57. 7491699.

2. Mittal R, Coopersmith CM. Redefining the gut as the motor of critical illness. Trends Mol Med. 2014;20(4):214–23. doi: 10.1016/j.molmed.2013.08.004 24055446.

3. Dickson RP. The microbiome and critical illness. Lancet Respir Med. 2016;4(1):59–72. doi: 10.1016/S2213-2600(15)00427-0 26700442.

4. Singer M, Deutschman CS, Seymour CW, Shankar-Hari M, Annane D, Bauer M, et al. The Third International Consensus Definitions for Sepsis and Septic Shock (Sepsis-3). Jama. 2016;315(8):801–10. doi: 10.1001/jama.2016.0287 26903338.

5. Ubeda C, Taur Y, Jenq RR, Equinda MJ, Son T, Samstein M, et al. Vancomycin-resistant Enterococcus domination of intestinal microbiota is enabled by antibiotic treatment in mice and precedes bloodstream invasion in humans. J Clin Invest. 2010;120(12):4332–41. doi: 10.1172/JCI43918 21099116.

6. Taur Y, Xavier JB, Lipuma L, Ubeda C, Goldberg J, Gobourne A, et al. Intestinal domination and the risk of bacteremia in patients undergoing allogeneic hematopoietic stem cell transplantation. Clin Infect Dis. 2012;55(7):905–14. doi: 10.1093/cid/cis580 22718773.

7. Kitsios GD, Morowitz MJ, Dickson RP, Huffnagle GB, McVerry BJ, Morris A. Dysbiosis in the intensive care unit: Microbiome science coming to the bedside. Journal of critical care. 2017;38:84–91. doi: 10.1016/j.jcrc.2016.09.029 27866110.

8. Hill DA, Hoffmann C, Abt MC, Du Y, Kobuley D, Kirn TJ, et al. Metagenomic analyses reveal antibiotic-induced temporal and spatial changes in intestinal microbiota with associated alterations in immune cell homeostasis. Mucosal Immunol. 2010;3(2):148–58. Epub 2009/11/27. doi: 10.1038/mi.2009.132 19940845; PubMed Central PMCID: PMC2824244.

9. Morowitz MJ, Di Caro V, Pang D, Cummings J, Firek B, Rogers MB, et al. Dietary Supplementation With Nonfermentable Fiber Alters the Gut Microbiota and Confers Protection in Murine Models of Sepsis. Crit Care Med. 2017;45(5):e516–e23. doi: 10.1097/CCM.0000000000002291 28252538.

10. Kuo SM. The interplay between fiber and the intestinal microbiome in the inflammatory response. Adv Nutr. 2013;4(1):16–28. doi: 10.3945/an.112.003046 23319119.

11. Vernazza CL, Gibson GR, Rastall RA. Carbohydrate preference, acid tolerance and bile tolerance in five strains of Bifidobacterium. J Appl Microbiol. 2006;100(4):846–53. doi: 10.1111/j.1365-2672.2006.02832.x 16553741.

12. Desai MS, Seekatz AM, Koropatkin NM, Kamada N, Hickey CA, Wolter M, et al. A Dietary Fiber-Deprived Gut Microbiota Degrades the Colonic Mucus Barrier and Enhances Pathogen Susceptibility. Cell. 2016;167(5):1339–53 e21. doi: 10.1016/j.cell.2016.10.043 27863247.

13. Carrico CJ, Meakins JL, Marshall JC, Fry D, Maier RV. Multiple-organ-failure syndrome. Arch Surg. 1986;121(2):196–208. doi: 10.1001/archsurg.1986.01400020082010 3484944.

14. Clark JA, Coopersmith CM. Intestinal crosstalk: a new paradigm for understanding the gut as the "motor" of critical illness. Shock (Augusta, Ga. 2007;28(4):384–93. doi: 10.1097/shk.0b013e31805569df 17577136.

15. Yoseph BP, Klingensmith NJ, Liang Z, Breed ER, Burd EM, Mittal R, et al. Mechanisms of Intestinal Barrier Dysfunction in Sepsis. Shock. 2016;46(1):52–9. doi: 10.1097/SHK.0000000000000565 27299587.

16. Coopersmith CM, Stromberg PE, Davis CG, Dunne WM, Amiot DM 2nd, Karl IE, et al. Sepsis from Pseudomonas aeruginosa pneumonia decreases intestinal proliferation and induces gut epithelial cell cycle arrest. Crit Care Med. 2003;31(6):1630–7. doi: 10.1097/01.CCM.0000055385.29232.11 12794397.

17. Coopersmith CM, Stromberg PE, Dunne WM, Davis CG, Amiot DM 2nd, Buchman TG, et al. Inhibition of intestinal epithelial apoptosis and survival in a murine model of pneumonia-induced sepsis. Jama. 2002;287(13):1716–21. doi: 10.1001/jama.287.13.1716 11926897.

18. Di Caro V, Cummings JL, Alcamo AM, Piganelli JD, Clark RSB, Morowitz MJ, et al. Dietary Cellulose Supplementation Modulates the Immune Response in a Murine Endotoxemia Model. Shock. 2018. doi: 10.1097/SHK.0000000000001180 30080745.

19. Turner JR. Intestinal mucosal barrier function in health and disease. Nature reviews Immunology. 2009;9(11):799–809. doi: 10.1038/nri2653 19855405.

20. Odenwald MA, Turner JR. Intestinal permeability defects: is it time to treat? Clinical gastroenterology and hepatology: the official clinical practice journal of the American Gastroenterological Association. 2013;11(9):1075–83. doi: 10.1016/j.cgh.2013.07.001 23851019; PubMed Central PMCID: PMC3758766.

21. Rupani B, Caputo FJ, Watkins AC, Vega D, Magnotti LJ, Lu Q, et al. Relationship between disruption of the unstirred mucus layer and intestinal restitution in loss of gut barrier function after trauma hemorrhagic shock. Surgery. 2007;141(4):481–9. doi: 10.1016/j.surg.2006.10.008 17383525.

22. Bischoff SC, Barbara G, Buurman W, Ockhuizen T, Schulzke JD, Serino M, et al. Intestinal permeability—a new target for disease prevention and therapy. BMC Gastroenterol. 2014;14:189. doi: 10.1186/s12876-014-0189-7 25407511.

23. Khounlotham M, Kim W, Peatman E, Nava P, Medina-Contreras O, Addis C, et al. Compromised intestinal epithelial barrier induces adaptive immune compensation that protects from colitis. Immunity. 2012;37(3):563–73. doi: 10.1016/j.immuni.2012.06.017 22981539.

24. Laukoetter MG, Nava P, Lee WY, Severson EA, Capaldo CT, Babbin BA, et al. JAM-A regulates permeability and inflammation in the intestine in vivo. J Exp Med. 2007;204(13):3067–76. doi: 10.1084/jem.20071416 18039951.

25. Li Q, Zhang Q, Wang C, Liu X, Li N, Li J. Disruption of tight junctions during polymicrobial sepsis in vivo. J Pathol. 2009;218(2):210–21. doi: 10.1002/path.2525 19235836.

26. Lyons JD, Coopersmith CM. Pathophysiology of the Gut and the Microbiome in the Host Response. Pediatric critical care medicine: a journal of the Society of Critical Care Medicine and the World Federation of Pediatric Intensive and Critical Care Societies. 2017;18(3_suppl Suppl 1):S46–S9. doi: 10.1097/PCC.0000000000001046 28248833; PubMed Central PMCID: PMC5333129.

27. Podolsky DK. Regulation of intestinal epithelial proliferation: a few answers, many questions. Am J Physiol. 1993;264(2 Pt 1):G179–86. doi: 10.1152/ajpgi.1993.264.2.G179 8447399.

28. Potoka DA, Upperman JS, Zhang XR, Kaplan JR, Corey SJ, Grishin A, et al. Peroxynitrite inhibits enterocyte proliferation and modulates Src kinase activity in vitro. Am J Physiol Gastrointest Liver Physiol. 2003;285(5):G861–9. doi: 10.1152/ajpgi.00412.2002 12842830.

29. Hsiao EY, McBride SW, Hsien S, Sharon G, Hyde ER, McCue T, et al. Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell. 2013;155(7):1451–63. Epub 2013/12/10. doi: 10.1016/j.cell.2013.11.024 24315484; PubMed Central PMCID: PMC3897394.

30. Khosravi A, Mazmanian SK. Disruption of the gut microbiome as a risk factor for microbial infections. Curr Opin Microbiol. 2013;16(2):221–7. Epub 2013/04/20. doi: 10.1016/j.mib.2013.03.009 23597788.

31. Khosravi A, Yanez A, Price JG, Chow A, Merad M, Goodridge HS, et al. Gut microbiota promote hematopoiesis to control bacterial infection. Cell Host Microbe. 2014;15(3):374–81. Epub 2014/03/19. doi: 10.1016/j.chom.2014.02.006 24629343; PubMed Central PMCID: PMC4144825.

32. Cabrera-Perez J, Badovinac VP, Griffith TS. Enteric immunity, the gut microbiome, and sepsis: Rethinking the germ theory of disease. Exp Biol Med (Maywood). 2017;242(2):127–39. Epub 2016/09/17. doi: 10.1177/1535370216669610 27633573; PubMed Central PMCID: PMC5167116.

33. Stoutenbeek CP, Van Saene HK, Miranda DR, Zandstra DF. A new technique of infection prevention in the intensive care unit by selective decontamination of the digestive tract. Acta Anaesthesiol Belg. 1983;34(3):209–21. 6316704.

34. Silvestri L, van Saene HK. Selective decontamination of the digestive tract: an update of the evidence. HSR Proc Intensive Care Cardiovasc Anesth. 2012;4(1):21–9. 23440328.

35. Saidel-Odes L, Polachek H, Peled N, Riesenberg K, Schlaeffer F, Trabelsi Y, et al. A randomized, double-blind, placebo-controlled trial of selective digestive decontamination using oral gentamicin and oral polymyxin E for eradication of carbapenem-resistant Klebsiella pneumoniae carriage. Infect Control Hosp Epidemiol. 2012;33(1):14–9. doi: 10.1086/663206 22173517.

36. Oostdijk EAN, Kesecioglu J, Schultz MJ, Visser CE, de Jonge E, van Essen EHR, et al. Effects of decontamination of the oropharynx and intestinal tract on antibiotic resistance in ICUs: a randomized clinical trial. Jama. 2014;312(14):1429–37. doi: 10.1001/jama.2014.7247 25271544.

Effect of dietary cellulose supplementation on gut barrier function and apoptosis in a murine model of endotoxemia

Souhrn

Klíčová slova:

Zdroje

PLOS One

Aktuální možnosti diagnostiky a léčby litiáz