Trauma-hemorrhagic shock-induced pulmonary epithelial and endothelial cell injury utilizes different programmed cell death signaling pathways

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 296, Issue 3, 2009, Pages

  Barlos, Dimtrios ^a   Deitch, Edwin A ^a   Watkins, Anthony C ^a   Caputo, Frank J ^a   Lu, Qi ^a   Abungu, Billy ^a   Colorado, Iriana ^a   Xu, Da Zhong ^a   Feinman, Rena ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

Acute lung injury; Apoptosis inducing factor; Caspase 3

Indexed keywords

APOPTOSIS INDUCING FACTOR; BENZYLOXYCARBONYLVALYLALANYLASPARTYL FLUOROMETHYL KETONE; CASPASE 3; CELL PROTEIN; M30 PROTEIN; UNCLASSIFIED DRUG; AIFM1 PROTEIN, HUMAN; CASPASE; SMALL INTERFERING RNA;

ACUTE LUNG INJURY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DAMAGE; CELL PROTECTION; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; DNA FRAGMENTATION; ENDOTHELIUM CELL; ENZYME INHIBITION; EPITHELIUM CELL; FEMORAL VEIN; HEMORRHAGIC SHOCK; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; INFLAMMATION; LUNG ALVEOLUS CELL TYPE 2; LUNG ALVEOLUS EPITHELIUM; LUNG ENDOTHELIUM; LYMPH VESSEL; MALE; MESENTERY LYMPH NODE; MICROVASCULARIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; UMBILICAL VEIN; ANIMAL; CELL CULTURE; DRUG ANTAGONISM; GENETICS; LUNG; LYMPH; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; RNA INTERFERENCE; SPRAGUE DAWLEY RAT;

ACUTE LUNG INJURY; ANIMALS; APOPTOSIS; APOPTOSIS INDUCING FACTOR; CASPASES; CELLS, CULTURED; ENDOTHELIAL CELLS; EPITHELIAL CELLS; HUMANS; LUNG; LYMPH; MALE; RATS; RATS, SPRAGUE-DAWLEY; RNA INTERFERENCE; RNA, SMALL INTERFERING; SHOCK, HEMORRHAGIC; SIGNAL TRANSDUCTION;

EID: 64249118919     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00491.2007     Document Type: Article

References (55)

1. Adams CA Jr, Xu DZ, Lu Q, Deitch EA. Factors larger than 100 kd in post-hemorrhagic shock mesenteric lymph are toxic for endothelial cells. Surgery 129: 351-363, 2001. (Pubitemid 32200066)
2. Adams JM, Hauser CJ, Adams CA Jr, Xu DZ, Livingston DH, Deitch EA. Entry of gut lymph into the circulation primes rat neutrophil respiratory burst in hemorrhagic shock. Crit Care Med 29: 2194-2198, 2001.
3. Alam HB, Austin B, Koustova E, Rhee P. Resuscitation-induced pulmonary apoptosis and intracellular adhesion molecule-1 expression in rats are attenuated by the use of Ketone Ringer's solution. J Am Coll Surg 193: 255-263, 2001. (Pubitemid 32842444)
4. Ayuste EC, Chen H, Koustova E, Rhee P, Ahuja N, Chen Z, Valeri CR, Spaniolas K, Mehrani T, Alam HB. Hepatic and pulmonary apoptosis after hemorrhagic shock in swine can be reduced through modifications of conventional Ringer's solution. J Trauma 60: 52-63, 2006.
5. Bachofen M, Weibel ER. Structural alterations of lung parenchyma in the adult respiratory distress syndrome. Clin Chest Med 3: 35-56, 1982. (Pubitemid 12062058)
6. Bahi N, Zhang J, Llovera M, Ballester M, Comella JX, Sanchis D. Switch from caspase-dependent to caspase-independent death during heart development: essential role of endonuclease G in ischemia-induced DNA processing of differentiated cardiomyocytes. J Biol Chem 281: 22943-22952, 2006. (Pubitemid 44242324)
7. Bannerman DD, Eiting KT, Winn RK, Harlan JM. FLICE-like inhibitory protein (FLIP) protects against apoptosis and suppresses NF-kappaB activation induced by bacterial lipopolysaccharide. Am J Pathol 165: 1423-1431, 2004.
8. Belmokhtar CA, Hillion J, Ségal-Bendirdjian E. Staurosporine induces apoptosis through both caspase-dependent and caspase-independent mechanisms. Oncogene 20: 3354-3362, 2001. (Pubitemid 32588984)
9. Candé C, Vahsen N, Garrido C, Kroemer G. Apoptosis-inducing factor (AIF): caspase-independent after all. Cell Death Differ 11: 591-595, 2004. (Pubitemid 38786707)
10. Childs EW, Tharakan B, Hunter FA, Tinsley JH, Cao X. Apoptotic signaling induces hyperpermeability following hemorrhagic shock. Am J Physiol Heart Circ Physiol 292: H3179-H3189, 2007. (Pubitemid 47084574)
11. Cregan SP, Dawson VL, Slack RS. Role of AIF in caspase-dependent and caspase-independent cell death. Oncogene 23: 2785-2796, 2004.
12. Davidson MT, Deitch EA, Lu Q, Osband A, Feketeova E, Németh ZH, Haskó G, Xu DZ. A study of the biologic activity of trauma-hemorrhagic shock mesenteric lymph over time and the relative role of cytokines. Surgery 136: 32-41, 2004. (Pubitemid 38834217)
13. Dayal SD, Haskó G, Lu Q, Xu DZ, Caruso JM, Sambol JT, Deitch EA. Trauma/hemorrhagic shock mesenteric lymph upregulates adhesion molecule expression and IL-6 production in human umbilical vein endothelial cells. Shock 17: 491-495, 2002.
14. Deb S, Sun L, Martin B, Talens E, Burris D, Kaufmann C, Rich N, Rhee P. Lactated ringer's solution and hetastarch but not plasma resuscitation after rat hemorrhagic shock is associated with immediate lung apoptosis by the up-regulation of the Bax protein. J Trauma 49: 47-53, 2000.
15. Deitch EA. Animal models of sepsis and shock: a review and lessons learned. Shock 9: 1-11, 1998.
16. Deitch EA. Multiple organ failure. Pathophysiology and potential future therapy. Ann Surg 216: 117-134, 1992.
17. Deitch EA, Adams C, Lu Q, Xu DZ. A time course study of the protective effect of mesenteric lymph duct ligation on hemorrhagic shock-induced pulmonary injury and the toxic effects of lymph from shocked rats on endothelial cell monolayer permeability. Surgery 129: 39-47, 2001. (Pubitemid 32099255)
18. Deitch EA, Adams CA, Lu Q, Xu DZ. Mesenteric lymph from rats subjected to trauma-hemorrhagic shock are injurious to rat pulmonary microvascular endothelial cells as well as human umbilical vein endothelial cells. Shock 16: 290-293, 2001. (Pubitemid 33599117)
19. Deitch EA, Xu D, Kaiser VL. Role of the gut in the development of injury- and shock induced SIRS and MODS: the gut-lymph hypothesis, a review. Front Biosci 11: 520-528, 2006. (Pubitemid 43258161)
20. Denecker G, Vercammen D, Declercq W, Vandenabeele P. Apoptotic and necrotic cell death induced by death domain receptors. Cell Mol Life Sci 58: 356-370, 2001. (Pubitemid 32231972)
21. Geiser T, Atabai K, Jarreau PH, Ware LB, Pugin J, Matthay MA. Pulmonary edema fluid from patients with acute lung injury augments in vitro alveolar epithelial repair by an IL-1β-dependent mechanism. Am J Respir Crit Care Med 163: 1384-1388, 2001. (Pubitemid 32506603)
22. Hooper WC, Mensah GA, Haworth SG, Black SM, Garcia JG, Langleben D. Vascular endothelium summary statement V: pulmonary hypertension and acute lung injury: public health implications. Vascul Pharmacol 46: 327-329, 2007. (Pubitemid 46386496)
23. Jaeschke H, Fisher MA, Lawson JA, Simmons CA, Farhood A, Jones DA. Activation of caspase 3 (CPP32)-like proteases is essential for TNFα-induced hepatic parenchymal cell apoptosis and neutrophil-mediated necrosis in a murine endotoxin shock model. J Immunol 160: 3480-3486, 1998. (Pubitemid 28164742)
24. Jaskille A, Alam HB, Rhee P, Hanes W, Kirkpatrick JR, Koustova E. D-lactate increases pulmonary apoptosis by restricting phosphorylation of bad and eNOS in a rat model of hemorrhagic shock. J Trauma 57: 262-269, 2004. (Pubitemid 39166776)
25. Jernigan TW, Croce MA, Fabian TC. Apoptosis and necrosis in the development of acute lung injury after hemorrhagic shock. Am Surg 70: 1094-1098, 2004.
26. Jones EA, Shoskes DA. The effect of mycophenolate mofetil and polyphenolic bioflavonoids on renal ischemia reperfusion injury and repair. J Urol 163: 999-1004, 2000.
27. Joseph B, Marchetti P, Formstecher P, Kroemer G, Lewensohn R, Zhivotovsky B. Mitochondrial dysfunction is an essential step for killing of non-small cell lung carcinomas resistant to conventional treatment. Oncogene 21: 65-77, 2002. (Pubitemid 34076379)
28. Kaiser VL, Sifri ZC, Dikdan GS, Berezina T, Zaets S, Lu Q, Xu DZ, Deitch EA. Trauma-hemorrhagic shock mesenteric lymph from rat contains a modified form of albumin that is implicated in endothelial cell toxicity. Shock 23: 417-425, 2005. (Pubitemid 40571664)
29. Kiang JG, Lu X, Tabaku LS, Bentley TB, Atkins JL, Tsokos GC. Resuscitation with lactated Ringer solution limits the expression of molecular events associated with lung injury after hemorrhage. J Appl Physiol 98: 550-556, 2005. (Pubitemid 40129964)
30. Kim GT, Chun YS, Park JW, Kim MS. Role of apoptosis-inducing factor in myocardial cell death by ischemia-reperfusion. Biochem Biophys Res Commun 309: 619-1612, 2003.
31. Lee BI, Lee DJ, Cho KJ, Kim GW. Early nuclear translocation of endonuclease G and subsequent DNA fragmentation after transient focal cerebral ischemia in mice. Neurosci Lett 386: 23-27, 2005.
32. Leers MP, Kölgen W, Björklund V, Bergman T, Tribbick G, Persson B, Björklund P, Ramaekers FC, Björklund B, Nap M, Jörnvall H, Schutte B. Immunocytochemical detection and mapping of a cytokeratin 18 neo-epitope exposed during early apoptosis. J Pathol 187: 567-572, 1999.
33. Leist M, Jaattela M. Four deaths and a funeral: from caspases to alternative mechanisms. Nat Rev Mol Cell Biol 2: 589-598, 2001. (Pubitemid 33674010)
34. Li X, Nemoto M, Xu Z, Yu SW, Shimoji M, Andrabi SA, Haince JF, Poirier GG, Dawson TM, Dawson VL, Koehler RC. Influence of duration of focal cerebral ischemia and neuronal nitric oxide synthase on translocation of apoptosis-inducing factor to the nucleus. Neuroscience 144: 56-65, 2007.
35. Liu PL, Chen YL, Chen YH, Lin SJ, Kou YR. Wood smoke extract induces oxidative stress-mediated caspase-independent apoptosis in human lung endothelial cells: role of AIF and EndoG. Am J Physiol Lung Cell Mol Physiol 289: L739-L749, 2005.
36. Lu Q, Xu DZ, Davidson MT, Haskó G, Deitch EA. Hemorrhagic shock induces endothelial cell apoptosis, which is mediated by factors contained in mesenteric lymph. Crit Care Med 32: 2464-2470, 2004. (Pubitemid 39648229)
37. Martin TR, Hagimoto N, Nakamura M, Matute-Bello G. Apoptosis and epithelial injury in the lungs. Proc Am Thorac Soc 2: 214-220, 2005. (Pubitemid 41500848)
38. Mauriz JL, González P, Jorquera F, Olcoz JL, González- Gallego J. Caspase inhibition does not protect against liver damage in hemorrhagic shock. Shock 19: 33-37, 2003.
39. Mura M, Andrade CF, Han B, Seth R, Zhang Y, Bai XH, Waddell TK, Hwang D, Keshavjee S, Liu M. Intestinal ischemia-reperfusion-induced acute lung injury and oncotic cell death in multiple organs. Shock 28: 227-238, 2007. (Pubitemid 47220836)
40. Osband AJ, Deitch EA, Lu Q, Zaets S, Dayal S, Lukose B, Xu DZ. The role of oxidant-mediated pathways in the cytotoxicity of endothelial cells exposed to mesenteric lymph from rats subjected to trauma-hemorrhagic shock. Shock 20: 269-273, 2003.
41. Pelosi P, D'Onofrio D, Chiumello D, Paolo S, Chiara G, Capelozzi VL, Barbas CS, Chiaranda M, Gattinoni L. Pulmonary and extrapulmonary acute respiratory distress syndrome are different. Eur Respir J Suppl 42: 48s-56s, 2003. (Pubitemid 36975737)
42. Perl M, Chung CS, Lomas-Neira J, Rachel TM, Biffl WL, Cioffi WG, Ayala A. Silencing of Fas, but not caspase-8, in lung epithelial cells ameliorates pulmonary apoptosis, inflammation, and neutrophil influx after hemorrhagic shock and sepsis. Am J Pathol 167: 1545-1559, 2005. (Pubitemid 41713309)
43. Perl M, Chung CS, Perl U, Lomas-Neira J, de Paepe M, Cioffi WG, Ayala A. Fas-induced pulmonary apoptosis and inflammation during indirect acute lung injury. Am J Respir Crit Care Med 176: 591-601, 2007. (Pubitemid 47403277)
44. Perl M, Lomas-Neira J, Chung CS, Ayala A. Epithelial cell apoptosis and neutrophil recruitment in acute lung injury- a unifying hypothesis? What have we learned from small interfering RNAs. Mol Med 14: 465-475, 2008.
45. Rosenberg RD, Aird WC. Vascular-bed-specific hemostasis and hypercoagulable states. N Engl J Med 340: 1555-1564, 1999.
46. Sambol JT, Xu DZ, Adams CA, Magnotti LJ, Deitch EA. Mesenteric lymph duct ligation provides long term protection against hemorrhagic shock-induced lung injury. Shock 14: 416-420, 2000.
47. Sarin EL, Moore EE, Moore JB, Masuno T, Moore JL, Banerjee A, Silliman CC. Systemic neutrophil priming by lipid mediators in postshock mesenteric lymph exists across species. J Trauma 57: 950-954, 2004. (Pubitemid 39579277)
48. Senthil M, Watkins A, Barlos D, Xu DZ, Lu Q, Abungu B, Caputo F, Feinman R, Deitch EA. Intravenous injection of trauma-hemorrhagic shock mesenteric lymph causes lung injury that is dependent upon activation of the inducible nitric oxide synthase pathway. Ann Surg 246: 822-830, 2007. (Pubitemid 350035659)
49. Shires GT, Browder LK, Steljes TP, Williams SJ, Browder TD, Barber AE. The effect of shock resuscitation fluids on apoptosis. Am J Surg 189: 85-91, 2005.
50. Susin SA, Lorenzo HK, Zamzami N, Marzo I, Snow BE, Brothers GM, Mangion J, Jacotot E, Costantini P, Loeffler M, Larochette N, Goodlett DR, Aebersold R, Siderovski DP, Penninger JM, Kroemer G. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397: 441-446, 1999. (Pubitemid 29078912)
51. Tang PS, Mura M, Seth R, Liu M. Acute lung injury and cell death: how many ways can cells die? Am J Physiol Lung Cell Mol Physiol 294: L632-L641, 2008.
52. Tang PS, Tsang ME, Lodyga M, Bai XH, Miller A, Han B, Liu M. Lipopolysaccharide accelerates caspase-independent but cathepsin Bdependent death of human lung epithelial cells. J Cell Physiol 209: 457-467, 2006. (Pubitemid 44484637)
53. Upperman JS, Deitch EA, Guo W, Lu Q, Xu D. Post-hemorrhagic shock mesenteric lymph is cytotoxic to endothelial cells and activates neutrophils. Shock 10: 407-414, 1998. (Pubitemid 128463863)
54. Ware LB, Matthay MA. Alveolar fluid clearance is impaired in the majority of patients with acute lung injury and the acute respiratory distress sundrome. Am J Respir Crit Care Med 163: 1376-1383, 2001.
55. Yu SW, Wang H, Poitras MF, Coombs C, Bowers WJ, Federoff HJ, Poirier GG, Dawson TM, Dawson VL. Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science 297: 259-263, 2002. (Pubitemid 34761289)