Role of intestinal mucus and pancreatic proteases in the pathogenesis of trauma-hemorrhagic shock-induced gut barrier failure and multiple organ dysfunction syndrome

Journal of Organ Dysfunction

Volumn 4, Issue 3, 2008, Pages 168-176

  Sharpe, Susan M ^a   Doucet, Danielle R ^a   Qin, Xiaofa ^a   Deitch, Edwin A ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

Ischemia; Lymph; Mucus; Multiple organ failure; Peptide hydrolases; Reperfusion; Shock

Indexed keywords

PANCREAS ENZYME;

BACTERIUM; HEMORRHAGIC SHOCK; HUMAN; INJURY; INTESTINE FLORA; INTESTINE INJURY; INTESTINE ISCHEMIA; MUCUS; MULTIPLE ORGAN FAILURE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; REPERFUSION INJURY; REVIEW;

BACTERIA (MICROORGANISMS);

EID: 53949120704     PISSN: 17471060     EISSN: 17471079     Source Type: Journal    
DOI: 10.1080/17471060801931211     Document Type: Review

References (54)

1. Deitch EA. Multiple organ failure: pathophysiology and potential future therapy. Ann Surg 1992;216:117-34.
2. Moore FA, Sausaia A, Moore EE. Post injury multiple organ failure: a bimodal phenomenon. J Trauma 1996;40:501-12.
3. Deitch EA, Xu DZ, Lu Q. Gut lymph hypothesis of early shock and trauma-induced multiple organ dysfunction syndrome: a new look at gut origin sepsis. J Organ Dysfunct 2006;2:70-9.
4. Senthil M, Brown M, Xu DZ, Lu Q, Feketeova E, Deitch EA. Gut lymph hypothesis of systemic inflammatory response syndrome/multiple-organ dysfunction syndrome: validating studies in a porcine model. J Trauma 2006;60:958-65.
5. Deitch EA, Feketeova E, Adams JM, Forsythe RM, Xu DZ, Itagaki K, et al. Lymph from a primate baboon trauma-hemorrhagic shock model activates human neutrophils. Shock 2006;25:460-3.
6. Magnotti LS, Xu DZ, Lu Q, Deitch EA. Gut-derived mesenteric lymph: a link between burn and lung injury. Arch Surg 1999;134:1333-40.
7. Magnotti LJ, Deitch EA. Burns, bacterial translocation, gut barrier function, and failure. J Burn Care Rehabil 2005;26:383-91.
8. Clamp JR, Creeth JM. Some non-mucin components of mucus and their possible biological roles. Ciba Found Symp 1984;109:121-36.
9. Atuma C, Strugala V, Allen A, Holm L. The adherent gastrointestinal mucus gel layer: thickness and physical state in vivo. Am J Physiol Gastrointest Liver Physiol 2001;280:G922-9.
10. Lichtenberger LM. The hydrophobic barrier properties of gastrointestinal mucus. Annu Rev Physiol 1995;57:565-83.
11. Mack DR, Neumann AW, Policova A, Sherman PM. Surface hydrophobicity of the intestinal tract. Am J Physiol 1992;262:G171-7.
12. Hills BA, Butler BD, Lichtenberger LM. Gastric mucosal barrier: hydrophobic lining to the lumen of the stomach. Am J Physiol 1983;244:G561-8.
13. Lugea A, Salas A, Casalot J, Guarner F, Malagelada JR. Surface hydrophobicity of the rat colonic mucosa is a defensive barrier against macromolecules and toxins. Gut 2000;46:515-21.
14. Ethell MT, Hodgson DR, Hills BA. Evidence for surfactant contributing to the gastric mucosal barrier of the horse. Equine Vet J 2000;32:470-4.
15. Goggin PM, Northfield TC, Spychal RT. Factors affecting gastric mucosal hydrophobicity in man. Scand J Gastroenterol 1991;181:65-73.
16. Spychal RT, Goggin PM, Marrero JM, Saverymuttu SH, Yu CW, Corbishley CM, et al. Surface hydrophobicity of gastric mucosa in peptic ulcer disease: relationship to gastritis and Campylobacter pylori infection. Gastroenterology 1990;98:1250-4.
17. Bounous G, McArdle AH, Hodges DM, Hampson LG, Gurd FN. Biosynthesis of intestinal mucin in shock: relationship to tryptic hemorrhagic enteritis and permeability to curare. Ann Surg 1966;164:13-22.
18. Rupani B, Caputo FJ, Watkins AC, Vega D, Magnotti LJ, Deitch EA. Relationship between disruption of the unstirred mucus layer and intestinal restitution in loss of gut barrier function after trauma hemorrhagic shock. Surgery 2007;141:481-9.
19. Ikeda H, Yang CL, Tong J, Nishimaki H, Masuda K, Takeo T, et al. Rat small intestinal goblet cell kinetics in the process of restitution of surface epithelium subjected to ischemia-reperfusion injury. Dig Dis Sci 2002;47:590-601.
20. Albanese CT, Cardona M, Smith SD, Watkins S, Kurkchubasche AG, Ulman I, et al. Role of intestinal mucus in transepithelial passage of bacteria across the intact ileum in vitro. Surgery 1994;116:76-82.
21. Maxson RT, Dunlap JP, Tryka F, Jackson RJ, Smith SD. The role of mucus gel layer in intestinal bacterial translocation. J Surg Res 1994;57:682-6.
22. Wu L, Zaborina O, Zaborin A, Chang EB, Musch M, Holbrook C, et al. High-molecular weight polyethylene glycol prevents lethal sepsis due to intestinal Pseudomonas aeruginosa. Gastroenterology 2004;126:488-98.
23. Nimmerfall F, Rosenthaler J. Significance of the goblet-cell mucin layer, the outermost luminal barrier to passage through the gut wall. Biochem Biophys Res Commun 1980;94:960-6.
24. Qin X, Caputo FJ, Xu DZ, Deitch EA. Hydrophobicity of mucosal surface and its relationship to gut barrier function. Shock 2008;29:372-6.
25. Grisham MB, Von Ritter C, Smith BF, Lamont JT, Granger DN. Interaction between oxygen radicals and gastric mucin. Am J Physiol 1987;253:G93-6.
26. Forstner JF. Intestinal mucins in health and disease. Digestion 1978;17:234-63.
27. Kemper AC, Specian RD. Rat small intestine mucins: a quantitative analysis. Anat Rec 1991;229:219-26.
28. Lefer AM, Glenn TM. Role of the pancreas in the pathogenesis of circulatory shock. Adv Exp Med Biol 1971;23:311-35.
29. Glenn TM, Lefer AM. Significance of splanchnic proteases in the production of a toxic factor in hemorrhagic shock. Circ Res 1971;29:338-49.
30. Kistler EB, Hugli TE, Schmid-Schoenbein GW. The pancreas as a source of cardiovascular cell activating factors. Microcirculation 2000;7:183-92.
31. Mitsuoka H, Kistler EB, Schmid-Schoenbein GW. Generation of in vivo activating factors in the ischemic intestine by pancreatic enzymes. Proc Natl Acad Sci U S A 2000;97:1772-7.
32. Schmid-Schoenbein GW, Kistler EB, Hugli TE. Mechanisms for cell activation and its consequences for biorheology and microcirculation: multi-organ failure in shock. Biorheology 2000;38:185-201.
33. Mitsuoka H, Kistler EB, Schmid-Schoenbein GW. Protease inhibition in the intestinal lumen: attenuation of systemic inflammation and early indicators of multiple organ failure in shock. Shock 2002;17:205-9.
34. Kistler EB, Lefer AM, Hugli TE, Schmid-Schoenbein GW. Plasma activation during splanchnic arterial occlusion shock. Shock 2000;14:30-43.
35. Deitch EA, Shi HP, Lu Q, Feketeova E, Qu DZ. Serine proteases are involved in the pathogenesis of trauma-hemorrhagic shock-induced gut and lung injury. Shock 2003;19:452-6.
36. Cohen DB, Magnotti LJ, Lu Q, Xu DZ, Berezina TL, Zaets SB, et al. Pancreatic duct ligation reduces lung injury following trauma and hemorrhagic shock. Ann Surg 2004;240:885-91.
37. Caputo FJ, Rupani B, Watkins AC, Barlos D, Vega D, Senthil M, et al. Pancreatic duct ligation abrogates the trauma hemorrhage-induced gut barrier failure and the subsequent production of biologically active intestinal lymph. Shock 2007;28:441-6.
38. Kramp WJ, Waldo S, Schmid-Schoenbein GW, Hoyt D, Coimbra R, Hugli TE. Characterization of two classes of pancreatic shock factors: functional differences exhibited by hydrophilic and hydrophobic shock factors. Shock 2003;20:356-62.
39. Waldo SW, Rosario HS, Penn AH, Schmid-Schoenbein GW. Pancreatic digestive enzymes are potent generators of mediators for leukocyte activation and mortality. Shock 2003;20:138-43.
40. Bohm SK, Kong W, Bromme D, Smeekens SP, Anderson DC, Connolly A, et al. Molecular cloning, expression and potential functions of the human proteinase activated receptor-2. Biochem J 1996;314:1009-16.
41. Kong W, McConalogue K, Khitin LM, Hollenberg MD, Payan DG, Bohm SK, et al. Luminal trypsin may regulate enterocytes through proteinase-activated receptor 2. Proc Natl Acad Sci U S A 1997;94:8884-9.
42. Cenac N, Coelho AM, Nguyen C, Compton S, Andrade-Gordon P, MacNaughton WK, et al. Induction of intestinal inflammation in mouse by activation of proteinase-activated receptor-2. Am J Pathol 2002;161:1903-15.
43. Ferraro FJ, Rush BF Jr, Simonian GT, Bruce CJ, Murphy TF, Hsieh JT, et al. A comparison of survival at different degrees of hemorrhagic shock in germ-free and germ-bearing rats. Shock 1995;4:117-20.
44. Souza DG, Vieira AT, Soares AC, Pinho V, Nicoli JR, Vieira LQ, et al. The essential role of the intestinal microbiota in facilitating acute inflammatory responses. J Immunol 2004;173:4137-46.
45. Chang TW. Improvement of survival from hemorrhagic shock by enterectomy in rats: finding to implicate the role of the gut for irreversibility of hemorrhagic shock. J Trauma 1997;42:223-30.
46. Magnotti LJ, Xu DZ, Lu Q, Deitch EA. Gut-derived mesenteric lymph: a link between burn and lung injury. Arch Surg 1999;134:1333-41.
47. Deitch EA, Lu Q, Feketeova E, Hauser CJ, Xu DZ. Intestinal bacterial overgrowth induces the production of biologically active intestinal lymph. J Trauma 2004;56:105-10.
48. MacDonald TT, Monteleone G. Immunity, inflammation and allergy in the gut. Science 2005;307:1920-5.
49. Alverdy JC, Laughlin RS, Wu L. Influence of the critically ill state on host-pathogen interactions within the intestine: gut-derived sepsis redefined. Crit Care Med 2003;31:598-607.
50. Nazli A, Ping-Chang Y, Jury J, Howe K, Watson JL, Soederholm JD, et al. Epithelia under metabolic stress perceive commensal bacteria as a threat. Am J Pathol 2004;164:947-57.
51. Strober W, Fuss IJ, Blumberg RS. The immunology of mucosal models of inflammation. Annu Rev Immunol 2002;20:495-549.
52. Deitch EA, Morrison J, Berg R, Specian RD. Effect of hemorrhagic shock on bacterial translocation, intestinal morphology, and intestinal permeability in conventional and antibiotic-decontaminated rats. Crit Care Med 1990;18:529-36.
53. Lyte M. The role of microbial endocrinology in infectious disease. J Endocrinol 1993;137:343-5.
54. Miller MB, Bassler BL. Quorum sensing in bacteria. Annu Rev Microbiol 2001;55:165-99.