Intestinal cytoskeleton degradation precedes tight junction loss following hemorrhagic shock

Shock

Volumn 31, Issue 2, 2009, Pages 164-169

  Thuijls, Geertje ^a   De Haan, Jacco Juri ^a   Derikx, Joep P M ^a   Daissormont, Isabelle ^a   Hadfoune, M'Hamed ^a   Heineman, Erik ^a   Buurman, Wim A ^a,b  

^a MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^b MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Actin cytoskeleton severing; Actin depolymerizing factor cofilin; Gut barrier; Kidney barrier; Liver barrier; Systemic inflammation

Indexed keywords

ACTIN; CLAUDIN 3; F ACTIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL TRANSLOCATION; CONTROLLED STUDY; CYTOSKELETON; HEMORRHAGIC SHOCK; INTESTINE; KIDNEY FAILURE; LIVER; LIVER FAILURE; MALE; MESENTERY LYMPH NODE; MULTIPLE ORGAN FAILURE; NONHUMAN; PROTEIN DEGRADATION; RAT; SPLEEN; TIGHT JUNCTION;

ACTINS; ANIMALS; BIOLOGICAL TRANSPORT; CYTOSKELETON; INFLAMMATION; INTESTINES; KIDNEY; LIVER; MALE; MODELS, BIOLOGICAL; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; SHOCK, HEMORRHAGIC; TIGHT JUNCTIONS;

EID: 59649121303     PISSN: 10732322     EISSN: None     Source Type: Journal    
DOI: 10.1097/SHK.0b013e31817fc310     Document Type: Article

References (37)

1. Moore FA, Sauaia A, Moore EE, Haenel JB, Burch JM, Lezotte DC: Postinjury multiple organ failure: a bimodal phenomenon. J Trauma 40:501-512, 1996.
2. Peitzman AB, Billiar TR, Harbrecht BG, Kelly E, Udekwu AO, Simmons RL: Hemorrhagic shock. Curr Probl Surg 32:925-1002, 1995.
3. Hassoun HT, Kone BC, Mercer DW, Moody FG, Weisbrodt NW, Moore FA: Post-injury multiple organ failure: the role of the gut. Shock 15:1-10, 2001.
4. Stevenson BR: Understanding tight junction clinical physiology at the molecular level. J Clin Invest 104:3-4, 1999.
5. Baker JW, Deitch EA, Li M, Berg RD, Specian RD: Hemorrhagic shock induces bacterial translocation from the gut. J Trauma 28:896-906, 1988.
6. Fink MP, Delude RL: Epithelial barrier dysfunction: a unifying theme to explain the pathogenesis of multiple organ dysfunction at the cellular level. Crit Care Clin 21:177-196, 2005.
7. Han X, Fink MP, Yang R, Delude RL: Increased iNOS activity is essential for intestinal epithelial tight junction dysfunction in endotoxemic mice. Shock 21:261-270, 2004.
8. Xu DZ, Lu Q, Deitch EA: Nitric oxide directly impairs intestinal barrier function. Shock 17:139-145, 2002.
9. Anderson JM: Leaky junctions and cholestasis: a tight correlation. Gastroenterology 110:1662-1665, 1996.
10. Kwon O, Nelson WJ, Sibley R, Huie P, Scandling JD, Dafoe D, Alfrey E, Myers BD: Backleak, tight junctions, and cell- cell adhesion in postischemic injury to the renal allograft. J Clin Invest 101:2054-2064, 1998.
11. Fink MP: Intestinal epithelial hyperpermeability: update on the pathogenesis of gut mucosal barrier dysfunction in critical illness. Curr Opin Crit Care 9:143-151, 2003.
12. Deitch EA, Forsythe R, Anjaria D, Livingston DH, Lu Q, Xu DZ, Redl H: The role of lymph factors in lung injury, bone marrow suppression, and endothelial cell dysfunction in a primate model of trauma-hemorrhagic shock. Shock 22:221-228, 2004.
13. Lappalainen P, Drubin DG: Cofilin promotes rapid actin filament turnover in vivo. Nature 388:78-82, 1997.
14. Rosenblatt J, Agnew BJ, Abe H, Bamburg JR, Mitchison TJ: Xenopus actin depolymerizing factor/cofilin (XAC) is responsible for the turnover of actin filaments in Listeria monocytogenes tails. J Cell Biol 136:1323-1332, 1997.
15. Schwartz N, Hosford M, Sandoval RM, Wagner MC, Atkinson SJ, Bamburg J, Molitoris BA: Ischemia activates actin depolymerizing factor: role in proximal tubule microvillar actin alterations. Am J Physiol 276:F544-F551, 1999.
16. Theriot JA: Accelerating on a treadmill: ADF/cofilin promotes rapid actin filament turnover in the dynamic cytoskeleton. J Cell Biol 136:1165-1168, 1997.
17. Carothers AM, Javid SH, Moran AE, Hunt DH, Redston M, Bertagnolli MM: Deficient E-cadherin adhesion in C57BL/6J-Min/ + mice is associated with increased tyrosine kinase activity and RhoA-dependent actomyosin contractility. Exp Cell Res 312:387-400, 2006.
18. Andrianantoandro E, Pollard TD: Mechanism of actin filament turnover by severing and nucleation at different concentrations of ADF/cofilin. Mol Cell 24:13-23, 2006.
19. Minamide LS, Striegl AM, Boyle JA, Meberg PJ, Bamburg JR: Neurodegenerative stimuli induce persistent ADF/cofilin-actin rods that disrupt distal neurite function. Nat Cell Biol 2:628-636, 2000.
20. Ivanov AI, McCall IC, Parkos CA, Nusrat A: Role for actin filament turnover and a myosin II motor in cytoskeleton-driven disassembly of the epithelial apical junctional complex. Mol Biol Cell 15:2639-2651, 2004.
21. AshworthSL, Sandoval RM, Hosford M, Bamburg JR, Molitoris BA: Ischemic injury induces ADF relocalization to the apical domain of rat proximal tubule cells. Am J Physiol Renal Physiol 280:F886-F894, 2001.
22. Shaw AE, Minamide LS, Bill CL, Funk JD, Maiti S, Bamburg JR: Cross-reactivity of antibodies to actin-depolymerizing factor/cofilin family proteins and identification of the major epitope recognized by a mammalian actin-depolymerizing factor/cofilin antibody. Electrophoresis 25:2611-2620, 2004.
23. Meberg PJ, Ono S, Minamide LS, Takahashi M, Bamburg JR: Actin depolymerizing factor and cofilin phosphorylation dynamics: response to signals that regulate neurite extension. Cell Motil Cytoskeleton 39:172-190, 1998.
24. Luyer MD, Buurman WA, Hadfoune M, Jacobs JA, Konstantinov SR, Dejong CH, Greve JW: Pretreatment with high-fat enteral nutrition reduces endotoxin and tumor necrosis factor-alpha and preserves gut barrier function early after hemorrhagic shock. Shock 21:65-71, 2004.
25. BarkT, Katouli M, Ljungqvist O, Mollby R, Svenberg T: Bacterial translocation after non-lethal hemorrhage in the rat. Circ Shock 41:60-65, 1993.
26. Luyer MD, Jacobs JA, Vreugdenhil AC, Hadfoune M, Dejong CH, Buurman WA, Greve JW: Enteral administration of high-fat nutrition before and directly after hemorrhagic shock reduces endotoxemia and bacterial translocation. Ann Surg 239:257-264, 2004.
27. Clayburgh DR, Barrett TA, Tang Y, Meddings JB, Van Eldik LJ, Watterson DM, Clarke LL, Mrsny RJ, Turner JR: Epithelial myosin light chain kinase-dependent barrier dysfunction mediates T cell activation-induced diarrhea in vivo. J Clin Invest 115:2702-2715, 2005.
28. Grossmann J, Maxson JM, Whitacre CM, Orosz DE, Berger NA, Fiocchi C, Levine AD: New isolation technique to study apoptosis in human intestinal epithelial cells. Am J Pathol 153:53-62, 1998.
29. McGough A, Pope B, Chiu W, Weeds A: Cofilin changes the twist of F-actin: implications for actin filament dynamics and cellular function. J Cell Biol 138:771-781, 1997.
30. Matsuda M, Kubo A, Furuse M, Tsukita S: A peculiar internalization of claudins, tight junction-specific adhesion molecules, during the intercellular movement of epithelial cells. J Cell Sci 117:1247-1257, 2004.
31. Ivanov AI, Nusrat A, Parkos CA: Endocytosis of the apical junctional complex: mechanisms and possible roles in regulation of epithelial barriers. Bioessays 27:356-365, 2005.
32. Clayburgh DR, Rosen S, Witkowski ED, Wang F, Blair S, Dudek S, Garcia JG, Alverdy JC, Turner JR: A differentiation-dependent splice variant of myosin light chain kinase, MLCK1, regulates epithelial tight junction permeability. J Biol Chem 279:55506-55513, 2004.
33. Turner JR, Rill BK, Carlson SL, Carnes D, Kerner R, Mrsny RJ, Madara JL: Physiological regulation of epithelial tight junctions is associated with myosin light-chain phosphorylation. Am J Physiol 273:C1378-C1385, 1997.
34. Shen L, Black ED, Witkowski ED, Lencer WI, Guerriero V, Schneeberger EE, Turner JR: Myosin light chain phosphorylation regulates barrier function by remodeling tight junction structure. J Cell Sci 119:2095-2106, 2006.
35. Hartel FV, Rodewald CW, Aslam M, Gunduz D, Hafer L, Neumann J, Piper HM, Noll T: Extracellular ATP induces assembly and activation of the myosin light chain phosphatase complex in endothelial cells. Cardiovasc Res 74: 487-496, 2007.
36. Kushida M, Takeuchi T, Fujita A, Hata F: Dependence of Ca2+-induced contraction on ATP in alpha-toxin-permeabilized preparations of rat femoral artery. J Pharmacol Sci 93:171-179, 2003.
37. Blair SA, Kane SV, Clayburgh DR, Turner JR: Epithelial myosin light chain kinase expression and activity are upregulated in inflammatory bowel disease. Lab Invest 86:191-201, 2006.