Abstract
The systemic pathophysiologic changes following thermal injuries affect multiple organs and body systems leading to clinical manifestations including shock, intestinal alterations, respiratory and renal failure, immunosuppression and others. Recent advances in the comprehension of mechanisms underlying systemic complications of thermal injuries have contributed to uncover part of the cellular and molecular basis that underlie such changes. Recently, programmed cell death (apoptosis) has been considered playing an important role in the development of such pathological events. Therefore, investigators utilizing animal models and clinical studies involving human primates have produced a large body of information suggesting that apoptosis is associated with most of the tissue damages triggered by severe thermal injuries. In order to draw the attention on the important role of apoptosis on systemic complications of thermal injuries, in this review we describe most of these studies, discuss possible cellular and molecular mechanisms and indicate ways to utilize them for the development of therapeutic strategies by which apoptosis may be prevented or counteracted.
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Al-Ghoul WM, Khan M, Fazal N et al (2004) Mechanisms of postburn intestinal barrier dysfunction in the rat: roles of epithelial cell renewal, E-cadherin, and neutrophil extravasation. Crit Care Med 32(8):1730–1739
Magnotti LJ, Deitch EA (2005) Burns, bacterial translocation, gut barrier function, and failure. J Burn Care Rehabil 26(5):383–391
Wolf SE, Ikeda H, Matin S et al (1999) Cutaneous burn increases apoptosis in the gut epithelium of mice. J Am Coll Surg 188(1):10–16
Lightfoot E Jr, Horton JW, Maass DL et al (1999) Major burn trauma in rats promotes cardiac and gastrointestinal apoptosis. Shock 11(1):29–34
Varedi M, Chinery R, Greeley GH Jr et al (2001) Thermal injury effects on intestinal crypt cell proliferation and death are cell position dependent. Am J Physiol Gastrointest Liver Physiol 280(1):G157–G163
Noda T, Iwakiri R, Fujimoto K et al (1998) Programmed cell death induced by ischemia-reperfusion in rat intestinal mucosa. Am J Physiol 274(2 Pt 1):G270–G276
Jones WG 2nd, Minei JP, Barber AE et al (1990) Bacterial translocation and intestinal atrophy after thermal injury and burn wound sepsis. Ann Surg 211(4):399–405
Ezzell RM, Carter EA, Yarmush ML et al (1993) Thermal injury-induced changes in the rat intestine brush border cytoskeleton. Surgery 114(3):591–597
Ramzy PI, Wolf SE, Irtun O et al (2000) Gut epithelial apoptosis after severe burn: effects of gut hypoperfusion. J Am Coll Surg 190(3):281–287
Zhang C, Sheng ZY, Hu S et al (2002) The influence of apoptosis of mucosal epithelial cells on intestinal barrier integrity after scald in rats. Burns 28(8):731–737
Zhang C, Sheng ZY, Hu S et al (2004) The role of oxygen-free radical in the apoptosis of enterocytes in scalded rats after delayed resuscitation. J Trauma 56(3):611–617
Chen LW, Hsu CM, Wang JS et al (1998) Specific inhibition of iNOS decreases the intestinal mucosal peroxynitrite level and improves the barrier function after thermal injury. Burns 24(8):699–705
Ocal K, Avlan D, Cinel I et al (2004) The role of poly(ADP-ribose) synthetase inhibition on the intestinal mucosal barrier after thermal injury. Burns 30(8):785–792
Zhou Y, Wang Q, Evers BM et al (2005) Signal transduction pathways involved in oxidative stress-induced intestinal epithelial cell apoptosis. Pediatr Res 58(6):1192–1197
Kojima M, Iwakiri R, Wu B et al (2003) Effects of antioxidative agents on apoptosis induced by ischaemia-reperfusion in rat intestinal mucosa. Aliment Pharmacol Ther 18(Suppl 1):139–145
Spies M, Chappell VL, Dasu MR et al (2002) Role of TNF-alpha in gut mucosal changes after severe burn. Am J Physiol Gastrointest Liver Physiol 283(3):G703–G708
Wu X, Woodside KJ, Song J et al (2004) Burn-induced gut mucosal homeostasis in TCR delta receptor-deficient mice. Shock 21(1):52–57
Ocal K, Avlan D, Cinel I et al (2004) The effect of N-acetylcysteine on oxidative stress in intestine and bacterial translocation after thermal injury. Burns 30(8):778–784
Chen LW, Hwang B, Wang JS et al (2004) Hypertonic saline-enhanced postburn gut barrier failure is reversed by inducible nitric oxide synthase inhibition. Crit Care Med 32(12):2476–2484
Chen LW, Hsu CM, Cha MC et al (1999) Changes in gut mucosal nitric oxide synthase (NOS) activity after thermal injury and its relation with barrier failure. Shock 11(2):104–110
Huang KF, Chung DH, Herndon DN (1993) Insulinlike growth factor 1 (IGF-1) reduces gut atrophy and bacterial translocation after severe burn injury. Arch Surg 128(1):47–53
Jeschke MG, Debroy MA, Wolf SE et al (2000) Burn and starvation increase programmed cell death in small bowel epithelial cells. Dig Dis Sci 45(2):415–420
Peng YZ, Yuan ZQ, Xiao GX (2001) Effects of early enteral feeding on the prevention of enterogenic infection in severely burned patients. Burns 27(2):145–149
Sheng CY, Gao WY, Guo ZR et al (1997) Anisodamine restores bowel circulation in burn shock. Burns 23(2):142–146
Hu S, Sheng ZY (2002) The effects of anisodamine and dobutamine on gut mucosal blood flow during gut ischemia/reperfusion. World J Gastroenterol 8(3):555–557
Tadros T, Traber DL, Heggers JP et al (2003) Effects of interleukin-1alpha administration on intestinal ischemia and reperfusion injury, mucosal permeability, and bacterial translocation in burn and sepsis. Ann Surg 237(1):101–109
Wu XW, Spies M, Chappell VL et al (2002) Effect of bombesin on gut mucosal impairment after severe burn. Shock 18(6):518–522
Yagmurdur MC, Turk E, Moray G et al (2005) Effects of heparin on bacterial translocation and gut epithelial apoptosis after burn injury in the rat: dose-dependent inhibition of the complement cascade. Burns 31(5):603–609
Jeschke MG, Herndon DN, Finnerty CC et al (2005) The effect of growth hormone on gut mucosal homeostasis and cellular mediators after severe trauma. J Surg Res 127(2):183–189
Jeschke MG, Bolder U, Finnerty CC et al (2005) The effect of hepatocyte growth factor on gut mucosal apoptosis and proliferation, and cellular mediators after severe trauma. Surgery 138(3):482–489
Teodorczyk-Injeyan JA, Cembrzynska-Nowak M, Lalani S et al (1995) Immune deficiency following thermal trauma is associated with apoptotic cell death. J Clin Immunol 15(6):318–328
Pellegrini JD, De AK, Kodys K et al (2000) Relationships between T lymphocyte apoptosis and anergy following trauma. J Surg Res 88(2):200–206
Cakir B, Cevik H, Contuk G et al (2005) Leptin ameliorates burn-induced multiple organ damage and modulates postburn immune response in rats. Regul Pept 125(1–3):135–144
Masson I, Mathieu J, Nolland XB et al (1998) Role of nitric oxide in depressed lymphoproliferative responses and altered cytokine production following thermal injury in rats. Cell Immunol 186(2):121–132
Masson I, Mathieu J, Nolland XB et al (1998) Role of nitric oxide in depressed lymphoproliferative responses and altered cytokine production following thermal injury in rats. Cell Immunol 186(2):121–132
Valenti LM, Mathieu J, Chancerelle Y et al (2005) High levels of endogenous nitric oxide produced after burn injury in rats arrest activated T lymphocytes in the first G1 phase of the cell cycle and then induce their apoptosis. Exp Cell Res 306(1):150–167
Daniel T, Alexander M, Hubbard WJ et al (2006) Nitric oxide contributes to the development of a post-injury Th2 T-cell phenotype and immune dysfunction. J Cell Physiol 208(2):418–427
Maile R, Barnes CM, Nielsen AI et al (2006) Lymphopenia-induced homeostatic proliferation of CD8 +T cells is a mechanism for effective allogeneic skin graft rejection following Burn Injury. J Immunol 176(11):6717–6726
Chitnis D, Dickerson C, Munster AM et al (1996) Inhibition of apoptosis in polymorphonuclear neutrophils from burn patients. J Leukoc Biol 59(6):835–839
Ogura H, Hashiguchi N, Tanaka H et al (2002) Long-term enhanced expression of heat shock proteins and decelerated apoptosis in polymorphonuclear leukocytes from major burn patients. J Burn Care Rehabil 23(2):103–109
Hu Z, Sayeed MM (2004) Suppression of mitochondria-dependent neutrophil apoptosis with thermal injury. Am J Physiol Cell Physiol 286(1):C170–C178
Hu Z, Sayeed MM (2005) Activation of PI3-kinase/PKB contributes to delay in neutrophil apoptosis after thermal injury. Am J Physiol Cell Physiol 288(5):C1171–C1178
Fukuzuka K, Rosenberg JJ, Gaines GC et al (1999) Caspase-3-dependent organ apoptosis early after burn injury. Ann Surg 229(6):851–858
Fukuzuka K, Edwards CK 3rd, Clare-Salzler M et al (2000) Glucocorticoid-induced, caspase-dependent organ apoptosis early after burn injury. Am J Physiol Regul Integr Comp Physiol 278(4):R1005–R1018
Nakanishi T, Nishi Y, Sato EF et al (1998) Thermal injury induces thymocyte apoptosis in the rat. J Trauma 44(1):143–148
Fukuzuka K, Edwards CK 3rd, Clare-Salzer M et al (2000) Glucocorticoid and Fas ligand induced mucosal lymphocyte apoptosis after burn injury. J Trauma 49(4):710–716
Cho K, Adamson LK, Greenhalgh DG (2001) Parallel self-induction of TNF-alpha and apoptosis in the thymus of mice after burn injury. J Surg Res 98(1):9–15
Hobson KG, Cho K, Adamson LK et al (2002) Burn-induced thymic apoptosis corresponds with altered TGF-beta(1) and Smad 2/3. J Surg Res 105(1):4–9
Nishimura T, Nishiura T, deSerres S et al (2000) Transforming growth factor-beta1 and splenocyte apoptotic cell death after burn injuries. J Burn Care Rehabil 21(2):128–134
Maekawa T, Kajihara H, Okabayashi K et al (2002) Impairment of splenic B and T lymphocytes in the early period after severe thermal injury: immunohistochemical and electron microscopic analysis. Burns 28(4):329–339
Patenaude J, D’Elia M, Hamelin C et al (2005) Burn injury induces a change in T cell homeostasis affecting preferentially CD4+ T cells. J Leukoc Biol 77(2):141–150
Woodside KJ, Spies M, Wu XW et al (2003) Decreased lymphocyte apoptosis by anti-tumor necrosis factor antibody in Peyer’s patches after severe burn. Shock 20(1):70–73
Xia PY, Zheng J, Zhou H et al (2002) Relationship between lymphocyte apoptosis and endotoxin translocation after thermal injury in rats. World J Gastroenterol 8(3):546–550
St-Pierre DM, Choiniere M, Forget R et al (1998) Muscle strength in individuals with healed burns. Arch Phys Med Rehabil 79(2):155–161
Padfield KE, Astrakas LG, Zhang Q et al (2005) Burn injury causes mitochondrial dysfunction in skeletal muscle. Proc Natl Acad Sci USA 102(15):5368–5373
Astrakas LG, Goljer I, Yasuhara S et al (2005) Proton NMR spectroscopy shows lipids accumulate in skeletal muscle in response to burn trauma-induced apoptosis. FASEB J 19(11):1431–1440
Mitch WE, Goldberg AL (1996) Mechanisms of muscle wasting. The role of the ubiquitin-proteasome pathway. N Engl J Med 335:1897–1905
Pereira C, Murphy K, Jeschke M et al (2005) Post burn muscle wasting and the effects of treatments. Int J Biochem Cell Biol 37(10):1948–1961
Jagoe RT, Goldberg AL (2001) What do we really know about the ubiquitin-proteasome pathway in muscle atrophy? Curr Opin Clin Nutr Metab Care 4(3):183–190
Chai J, Wu Y, Sheng Z (2002) The relationship between skeletal muscle proteolysis and ubiquitin-proteasome proteolytic pathway in burned rats. Burns 28(6):527–533
Fagan JM, Ganguly M, Stockman H et al (1999) Posttranslational modifications of cardiac and skeletal muscle proteins by reactive oxygen species after burn injury in the rat. Ann Surg 229(1):106–114
Orzechowski A, Jank M, Gajkowska B et al (2003) Delineation of signalling pathway leading to antioxidant-dependent inhibition of dexamethasone-mediated muscle cell death. J Muscle Res Cell Motil 24(1):33–53
Ruff RL, Secrist D (1984) Inhibitors of prostaglandin synthesis or cathepsin B prevent muscle wasting due to sepsis in the rat. J Clin Invest 73:1483–1486
Williams A, Wang JJ, Wang L et al (1998) Sepsis in mice stimulates muscle proteolysis in the absence of IL-6. Am J Physiol 275:R1983–R1991
Tsujinaka T, Fujita J, Ebisui C et al (1996) Interleukin 6 receptor antibody inhibits muscle atrophy and modulates proteolytic systems in interleukin 6 transgenic mice. J Clin Invest 97:244–249
Garcia-Martinez C, Agell N, Llovera M et al (1993) Tumour necrosis factor-alpha increases the ubiquitinization of rat skeletal muscle proteins. FEBS Lett 323:211–214
Goodman MN (1991) Tumor necrosis factor induces skeletal muscle protein breakdown in rats. Am J Physiol 260:E727–E730
Billiau A (1996) Interferon-gamma: biology and role in pathogenesis. Adv Immunol 62:61–130
Madihally SV, Toner M, Yarmush ML et al (2002) Interferon gamma modulates trauma-induced muscle wasting and immune dysfunction. Ann Surg 236(5):649–657
Lee MC, Wee GR, Kim JH (2005) Apoptosis of skeletal muscle on steroid-induced myopathy in rats. J Nutr 135(7):1806S–1808S
Orzechowski A, Jank M, Gajkowska B, Sadkowski T, Godlewskia MM (2003) A novel antioxidant-inhibited dexamethasone-mediated and caspase-3-independent muscle cell death. Ann N Y Acad Sci 1010:205–208
Yasuhara S, Kanakubo E, Perez ME et al (1999) The 1999 Moyer award. Burn injury induces skeletal muscle apoptosis and the activation of caspase pathways in rats. J Burn Care Rehabil 20(6):462–470
Yasuhara S, Perez ME, Kanakubo E et al (2000) Skeletal muscle apoptosis after burns is associated with activation of proapoptotic signals. Am J Physiol Endocrinol Metab 279(5):E1114–E1121
Westermann S, Vollmar B, Thorlacius H et al (1999) Surface cooling inhibits tumor necrosis factor-alpha-induced microvascular perfusion failure, leukocyte adhesion, and apoptosis in the striated muscle. Surgery 126(5):881–889
Tredget EE, Yu YM (1992) The metabolic effects of thermal injury. World J Surg 16(1):68–79
Vemula M, Berthiaume F, Jayaraman A et al (2004) Expression profiling analysis of the metabolic and inflammatory changes following burn injury in rats. Physiol Genomics 18(1): 87–98
Barrow RE, Mlcak R, Barrow LN et al (2004) Increased liver weights in severely burned children: comparison of ultrasound and autopsy measurements. Burns 30(6):565–568
Barrow RE, Hawkins HK, Aarsland A et al (2005) Identification of factors contributing to hepatomegaly in severely burned children. Shock 24(6):523–528
Patel T, Roberts LR, Jones BA et al (1998) Dysregulation of apoptosis as a mechanism of liver disease: an overview. Semin Liver Dis 18:105–114
Rodrigues CMP, Fan G, Ma X et al (1998) A novel role for ursodeoxycholic acid in inhibiting apoptosis by modulating mitochondrial membrane perturbation. J Clin Invest 101: 2790–2799
Faubion WA, Gores GJ (1999) Death receptors in liver biology and pathobiology. Hepatology 29:1–4
Sodeman T, Bronk SF, Roberts PJ et al (2000) Bile salts mediate hepatocyte apoptosis by increasing cell surface trafficking of Fas. Am J Physiol Gastrointest Liver Physiol 278:G992–G999
Faubion W A, Guicciardi ME, Miyoshi H et al (1999) Toxic bile salts induce rodent hepatocyte apoptosis via direct activation of Fas. J Clin Invest 103:137–145
Jeschke MG, Low JF, Spies M et al (2001) Cell proliferation, apoptosis, NF-kappaB expression, enzyme, protein, and weight changes in livers of burned rats. Am J Physiol Gastrointest Liver Physiol 280(6):G1314–G1320
Nishimura T, Nishiura T, deSerres S et al (2000) Impact of burn injury on hepatic TGF-beta1 expression and plasma TGF-beta1 levels. J Trauma 48(1):39–44
Li ZQ, Zhou YP (2002) Apoptosis and necrosis of hepatocytes induced in vitro by subeschar tissue fluid from guinea pigs with burn injury. Di Yi Jun Yi Da Xue Xue Bao 22(5):430–431
Jeschke MG, Herndon DN, Barrow RE (2000) Insulin-like growth factor I in combination with insulin-like growth factor binding protein 3 affects the hepatic acute phase response and hepatic morphology in thermally injured rats. Ann Surg 231(3):408–416
Jeschke MG, Herndon DN, Vita R et al (2001) IGF-I/BP-3 administration preserves hepatic homeostasis after thermal injury which is associated with increases in no and hepatic NF-kappa B. Shock 16(5):373–379
Horton JW, Maass DL, White DJ, Sanders B, Murphy J (2004) Effects of burn serum on myocardial inflammation and function. Shock 22(5):438–445
White DJ, Maass DL, Sanders B et al (2002) Cardiomyocyte intracellular calcium and cardiac dysfunction after burn trauma. Crit Care Med 30(1):14–22
Maass DL, Hybki DP, White J et al (2002) The time course of cardiac NF-kappaB activation and TNF-alpha secretion by cardiac myocytes after burn injury: contribution to burn-related cardiac contractile dysfunction. Shock 17(4):293–299
Maass DL, White J, Horton JW (2002) IL-1beta and IL-6 act synergistically with TNF-alpha to alter cardiac contractile function after burn trauma. Shock 18(4):360–366
Maass DL, White J, Sanders B et al (2005) Role of cytosolic vs. mitochondrial Ca2+ accumulation in burn injury-related myocardial inflammation and function. Am J Physiol Heart Circ Physiol 288(2):H744–H751
Murphy JT, Giroir B, Horton JW (1999) Thermal injury alters myocardial sarcoplasmic reticulum calcium channel function. J Surg Res 82(2):244–252
Ballard-Croft C, Carlson D, Maass DL, Horton JW (2004) Burn trauma alters calcium transporter protein expression in the heart. J Appl Physiol 97(4):1470–1476
Maass DL, White DJ, Sanders B et al (2005) Cardiac myocyte accumulation of calcium in burn injury: cause or effect of myocardial contractile dysfunction. J Burn Care Rehabil 26(3):252–259
Sikes PJ, Zhao P, Maass DL et al (2001) Time course of myocardial sodium accumulation after burn trauma: a (31)P- and (23)Na-NMR study. J Appl Physiol 91(6):2695–2702
McDonald TE, Grinman MN, Carthy CM et al (2000) Endotoxin infusion in rats induces apoptotic and survival pathways in hearts. Am J Physiol Heart Circ Physiol 279(5):H2053–H2061
Lancel S, Petillot P, Favory R et al (2005) Expression of apoptosis regulatory factors during myocardial dysfunction in endotoxemic rats. Crit Care Med 33(3):492–496
Carlson DL, Willis MS, White DJ et al (2005) Tumor necrosis factor-alpha-induced caspase activation mediates endotoxin-related cardiac dysfunction. Crit Care Med 33(5):1021–1028
Iwai-Kanai E, Hasegawa K, Fujita M et al (2002) Basic fibroblast growth factor protects cardiac myocytes from iNOS-mediated apoptosis. J Cell Physiol 190(1):54–62
Lightfoot E Jr, Horton JW, Maass DL et al (1999) Major burn trauma in rats promotes cardiac and gastrointestinal apoptosis. Shock 11(1):29–34
Wang GQ, Xia ZF, Yu BJ et al (2001) Cardiac apoptosis in burned rats with delayed fluid resuscitation. Burns 27(3):250–253
Carlson DL, Lightfoot E Jr, Bryant DD et al (2002) Burn plasma mediates cardiac myocyte apoptosis via endotoxin. Am J Physiol Heart Circ Physiol 282(5):H1907–H1914
Horton JW, White DJ, Maass D et al (1999) Calcium antagonists improve cardiac mechanical performance after thermal trauma. J Surg Res 87(1):39–50
Suzuki J, Bayna E, Dalle Molle E et al (2003) Nicotine inhibits cardiac apoptosis induced by lipopolysaccharide in rats. J Am Coll Cardiol 41(3):482–488
Huang Y, Hu A (2004) Molecular mechanism of c-jun antisense gene transfection in alleviating injury of cardiomyocytes treated with burn serum and hypoxia. World J Surg 28(10):951–957
Lund T, Onarheim H, Reed RK (1992) Pathogenesis of edema formation in burn injuries. World J. Surg 16:2–9
Nishimura N, Hiranuma N (1982) Respiratory changes after major burn injury. Crit Care Med 102:25–28
Aikawa N, Shinozawa Y, Ishibiki K et al (1983) Clinical analysis of multiple organ failure in burned patients. Burns 13:103–109
Nash G, Foley FD, Langlinais P (1974) Pulmonary interstitial edema and hyaline membranes in adult burn patients. Electron microscopic observations. Hum Pathol 5(2):149–160
Demling RH, Kramer G, Harms B (1984) Role of thermal injury-induced hypoproteinemia on fluid flux and protein permeability in burned and unburned tissue. Surgery 95:136–144
Kramer GC, Harms B, Demling RH et al (1982) Mechanisms of redistribution of plasma protein following acute protein depletion. Am J Physiol 243:803–809
Kramer G, Harms B, Gunther R et al (1981) The effects of hypoproteinemia on blood to lymph fluid transport in sheep lung. Circ Res 47:1173–1180
Roselli RJ (1981) Influence of plasma protein concentration on lung lymph flow and L/P ratio. Physiologist 24:16–24
Darling GE, Keresteci MA, Ibanez D et al (1996) Pulmonary complications in inhalation injuries with associated cutaneous burn. J Trauma 40:83–89
Herndon DN, Barrow RE, Linares HA et al (1988) Inhalation injury in burned patients: effects and treatment. Burns Incl Therm Inj 14:349–356
Thompson PB, Herndon DN, Traber DL et al (1986) Effect on mortality of inhalation injury. J Trauma 26:163–165
Hales CA, Elsasser TH, Ocampo P et al (1997) TNF-a in smoke inhalation lung injury. J Appl Physiol 82:1433–1437
Bidani A, Wang CZ, Heming TA (1998) Cotton smoke inhalation primes alveolar macrophages for tumor necrosis factor-α production and suppresses macrophage antimicrobial activities. Lung 176:325–336
Turnage RH, Nwariaku F, Murphy J et al (2002) Mechanisms of pulmonary microvascular dysfunction during severe burn injury. World J Surg 26(7):848–853
Ward PA, Till GO (1990) Pathophysiologic events related to thermal injury of skin. J Trauma 30:S75–S79
Till GO, Hatherill JR, Tourtellotte WW et al (1985) Lipid peroxidation and acute lung injury after thermal trauma to skin: evidence of a role for hydroxyl radical. Am J Pathol 119:376–384
Till GO, Beauchamp C, Menapace D et al (1983) Oxygen radical dependent lung damage following thermal injury of rat skin. J. Trauma 23:269–277
Rodriguez JL, Miller CG, Garner WL et al (1993) Correlation of the local and systemic cytokine response with clinical outcome following thermal injury. J Trauma 34:684–694
Fang WH, Yao YM, Shi ZG, Yu Y, Wu Y, Lu LR, Sheng ZY (2003) The mRNA expression patterns of tumor necrosis factor-alpha and TNFR-I in some vital organs after thermal injury. World J Gastroenterol 9(5):1038–1044
Herlihy JP, Vermeulen MW, Joseph PM et al (1995) Impaired alveolar macrophage function in smoke inhalation injury. J Cell Physiol 163(1):1–8
Vertrees RA, Nason R, Hold MD et al (2004) Smoke/burn injury-induced respiratory failure elicits apoptosis in ovine lungs and cultured lung cells, ameliorated with arteriovenous CO2 removal. Chest 125(4):1472–1482
Yamada Y, Endo S, Nakae H et al (2003) Examination of soluble Fas (sFas) and soluble Fas ligand (sFasL) in patients with burns. Burns 29(8):799–802
Yasuhara S, Kaneki M, Sugita H et al (2006) Adipocyte apoptosis after burn injury is associated with altered fat metabolism. J Burn Care Res 27(3):367–376
Zhu CH, Ying DJ, Mi JH et al (2004) The zinc finger protein A20 protects endothelial cells from burns serum injury. Burns 30(2):127–133
Harada T, Izaki S, Tsutsumi H et al (1998) Apoptosis of hair follicle cells in the second-degree burn wound under hypernatremic conditions. Burns 24(5):464–469
French LE, Tschopp J (2003) Protein-based therapeutic approaches targeting death receptors. Cell Death Differ 10(1):117–123
Fischer U, Schulze-Osthoff K (2005) New approaches and therapeutics targeting apoptosis in disease. Pharmacol Rev 57(2):187–215
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Gravante, G., Delogu, D. & Sconocchia, G. “Systemic apoptotic response” after thermal burns. Apoptosis 12, 259–270 (2007). https://doi.org/10.1007/s10495-006-0621-8
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DOI: https://doi.org/10.1007/s10495-006-0621-8