Effect of burn injury on apoptosis and expression of apoptosis-related genes/proteins in skeletal muscles of rats

Springer Science and Business Media LLC - Tập 14 - Trang 52-65 - 2008
Hongjie Duan1, Jiake Chai1, Zhiyong Sheng1, Yongming Yao1, Huinan Yin1, Liming Liang1, Chuanan Shen1, Jing Lin1
1Department of Burns and Plastic Surgery, Burns Institute, First Hospital Affiliated to General Hospital of PLA (Formerly 304th Hospital of PLA), Beijing, China

Tóm tắt

The purpose of this study was to investigate the occurrence and possible mechanisms of apoptosis in skeletal muscles after burn injury. After a 40% body surface area burn to rats, TA muscles were examined for apoptosis at varying times by TEM, TUNEL and cell death ELISA assay. Thermal injury was found to induce apoptosis in skeletal muscle on the first day and maximal apoptosis appeared 4 days post-injury. Apoptotic ligands in serum assessed by ELISA revealed rapidly increase of TNF-α and subsequent increase of sFasL to sFas ratio after burn injury. It implied TNF-α induced apoptosis in early stage and FasL induced apoptosis in later stage after burn injury. Apoptosis-related genes/proteins in skeletal muscles examined by real-time PCR array and Western blotting showed pro-apoptotic genes/proteins, including Tnfrsf1a, Tnfrsf1b and Tnfsf6 in TNF ligand and receptor family, Bax and Bid in Bcl-2 family, caspase-3 and caspase-6 in caspase family, Dapk1, FADD and Cidea in death and CIDE domain family, Apaf-1 in CARD family, and Gadd45a were up-regulated, while anti-apoptotic gene Bnip1 was down-regulated compared with that of time-matched controls. In addition, increment of caspase-3, caspase-8 and caspase-9 activity provided further evidence for their role in apoptosis in skeletal muscle. Significant increase in expression in pro-apoptotic genes/proteins and activity of caspases suggested that death receptor-mediated signaling pathways and other apoptotic related pathways participated in apoptosis in skeletal muscle after burn injury. However, it was found that some anti-apoptotic genes such as Bcl2l1, Mcl-1, Nol-3, Il-10 and Prok2 were also up-regulated, which might imply the co-existence of protective response of the body after burns. In conclusion, the data suggest that apoptosis and pro-apoptotic signaling are enhanced in muscles of burned rats. To further elucidate the underlying apoptotic mechanisms mediating the atrophic response is important in establishing potential therapeutic interventions that could prevent and/or reduce skeletal muscle wasting and preserve its physiological function.

Tài liệu tham khảo

Nguyen TT, Gilpin DA, Meyer NA, Herndon DN (1996) Current treatment of severely burned patients. Ann Surg 223:14–25. doi:10.1097/00000658-199601000-00004 Faragher MW, Day BJ, Dennett X (1996) Critical care myopathy: an electrophysiological and histological study. Muscle Nerve 19:516–518. doi :10.1002/(SICI)1097-4598(199604)19:4<516::AID-MUS11>3.0.CO;2-N Cooney RN, Kimball SR, Vary TC (1997) Regulation of skeletal muscle protein turnover during sepsis: mechanisms and mediators. Shock 7:1–16. doi:10.1097/00024382-199701000-00001 Mitch WE, Goldberg AL (1996) Mechanisms of muscle wasting. The role of the ubiquitin-proteasome pathway. N Engl J Med 335:1897–1905. doi:10.1056/NEJM199612193352507 Fang CH, Tiao G, James H, Ogle C, Fischer JE, Hasselgren PO (1995) Burn injury stimulates multiple proteolytic pathways in skeletal muscle, including the ubiquitin-energy-dependent pathway. J Am Coll Surg 180:161–170 Chai JK, Wu YQ, Sheng ZY (2002) The relationship between skeletal muscle proteolysis and ubiquitin-proteasome proteolytic pathway in burned rats. Burns 28:527–533. doi:10.1016/S0305-4179(02)00049-9 Chai JK, Wu YQ, Sheng ZY (2003) Role of ubiquitin-proteasome pathway in skeletal muscle wasting in rats with endotoxemia. Crit Care Med 31:1802–1807. doi:10.1097/01.CCM.0000069728.49939.E4 Braga M, Sinha Hikim AP, Datta S, Ferrini MG, Brown D, Kovacheva EL et al (2008) Involvement of oxidative stress and caspase 2-mediated intrinsic pathway signaling in age-related increase in muscle cell apoptosis in mice. Apoptosis 13:822–832. doi:10.1007/s10495-008-0216-7 Agustí AG, Sauleda J, Miralles C, Gomez C et al (2002) Skeletal muscle apoptosis and weight loss in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 166:485–489. doi:10.1164/rccm.2108013 Adhihetty PJ, O’Leary MF, Chabi B, Wicks KL, Hood DA (2007) Effect of denervation on mitochondrially mediated apoptosis in skeletal muscle. J Appl Physiol 102:1143–1151. doi:10.1152/japplphysiol.00768.2006 Marzetti E, Lawler JM, Hiona A, Manini T, Seo AY, Leeuwenburgh C (2008) Modulation of age-induced apoptotic signaling and cellular remodeling by exercise and calorie restriction in skeletal muscle. Free Radic Biol Med 44:160–168. doi:10.1016/j.freeradbiomed.2007.05.028 Cheek DB (1985) The control of cell mass and replication. The DNA unit–a personal 20-year study. Early Hum Dev 12:211–239. doi:10.1016/0378-3782(85)90144-6 Fidzianska A, Kaminska A (1991) Apoptosis: a basic pathological reaction of injured neonatal muscle. Pediatr Pathol 11:421–429. doi:10.3109/15513819109064778 Dupont-Versteegden EE (2006) Apoptosis in skeletal muscle and its relevance to atrophy. World J Gastroenterol 12:7463–7466 Dupont-Versteegden EE (2005) Apoptosis in muscle atrophy: relevance to sarcopenia. Exp Gerontol 40:473–481. doi:10.1016/j.exger.2005.04.003 Primeau AJ, Adhihetty PJ, Hood DA (2002) Apoptosis in heart and skeletal muscle. Can J Appl Physiol 27:349–395 Krammer PH (2000) CD95’s deadly mission in the immune system. Nature 407:789–795. doi:10.1038/35037728 Yasuhara S, Perez ME, Kanakubo E, Yasuhara Y, Shin YS, Kaneki M et al (2000) Skeletal muscle apoptosis after burns is associated with activation of proapoptotic signals. Am J Physiol Endocrinol Metab 279:E1114–E1121 Ipaktchi K, Mattar A, Niederbichler AD, Hoesel LM, Vollmannshauser S, Hemmila MR et al (2006) Attenuating burn wound inflammatory signaling reduces systemic inflammation and acute lung injury. J Immunol 177(11):8065–8071 Bertin-Maghit M, Goudable J, Dalmas E, Steghens JP, Bouchard C, Gueugniaud PY et al (2000) Time course of oxidative stress after major burns. Intensive Care Med 26:800–803. doi:10.1007/s001340051250 Walker HL, Mason ADJ (1968) A standard animal burn. J Trauma 8:1049–1051. doi:10.1097/00005373-196811000-00006 Fang CH, Li BG, Wang JJ, Fischer JE, Hasselgren PO (1998) Treatment of burned rats with insulin-like growth factor I inhibits the catabolic response in skeletal muscle. Am J Physiol 275:R1091–R1098 Narula J, Haider N, Virmani R, Disalvo TG, Kolodgie FD, Hajjar RJ et al (1996) Apoptosis in myocytes in end-stage heart failure. N Engl J Med 335:1182–1189. doi:10.1056/NEJM199610173351603 Vescovo G, Volterrani M, Zennaro R, Sandri M, Ceconi C, Lorusso R et al (2000) Apoptosis in the skeletal muscle of patients with heart failure: investigation of clinical and biochemical changes. Heart 84:431–437. doi:10.1136/heart.84.4.431 Cain K, Inayat-Hussain SH, Kokileva L, Cohen GM (1994) DNA cleavage in rat liver nuclei activated by Mg2+ or Ca2+ +Mg2+ is inhibited by a variety of structurally unrelated inhibitors. Biochem Cell Biol 72:631–638 Clark AS, Kelly RA, Mitch WE (1984) Systemic response to thermal injury in rats. Accelerated protein degradation and altered glucose utilization in muscle. J Clin Invest 74:888–897. doi:10.1172/JCI111506 Hasselgren PO (1999) Pathways of muscle protein breakdown in injury and sepsis. Curr Opin Clin Nutr Metab Care 2:155–160. doi:10.1097/00075197-199903000-00011 Du J, Wang X, Miereles C, Bailey JL, Debigare R, Zheng B et al (2004) Activation of caspase-3 is an initial step triggering accelerated muscle proteolysis in catabolic conditions. J Clin Invest 113:115–123 Argilés JM, López-Soriano FJ, Busquets S (2008) Apoptosis signalling is essential and precedes protein degradation in wasting skeletal muscle during catabolic conditions. Int J Biochem Cell Biol 40:1674–1678. doi:10.1016/j.biocel.2008.02.001 Dupont-Versteegden EE, Murphy RJ, Houle JD, Gurley CM, Peterson CA (2000) Mechanisms leading to restoration of muscle size with exercise and transplantation after spinal cord injury. Am J Physiol Cell Physiol 279:C1677–C1684 Dupont-Versteegden EE, Murphy RJ, Houle JD, Gurley CM, Peterson CA (1999) Activated satellite cells fail to restore myonuclear number in spinal cord transected and exercised rats. Am J Physiol 277:C589–C597 Allen DL, Yasui W, Tanaka T, Ohira Y, Nagaoka S, Sekiguchi C, Hinds WE, Roy RR, Edgerton VR (1996) Myonuclear number and myosin heavy chain expression in rat soleus single muscle fibers after spacefl ight. J Appl Physiol 81:145–151 Allen DL, Linderman JK, Roy RR, Grindeland RE, Mukku V, Edgerton VR (1997) Growth hormone/IGF-I and/or resistive exercise maintains myonuclear number in hindlimb unweighted muscles. J Appl Physiol 83:1857–1861 Degens H (2007) Age-related skeletal muscle dysfunction: causes and mechanisms. J Musculoskelet Neuronal Interact 7:246–252 Phillips T, Leeuwenburgh C (2005) Muscle fiber specific apoptosis and TNF-alpha signaling in sarcopenia are attenuated by life-long calorie restriction. FASEB J 19:668–670 Li X, Yang Y, Ashwell JD (2002) TNF-RII and c-IAP1 mediate ubiquitination and degradation of TRAF2. Nature 416:345–347. doi:10.1038/416345a Nagata S (1997) Apoptosis by death factor. Cell 88:355–365. doi:10.1016/S0092-8674(00)81874-7 Garrido C, Galluzzi L, Brunet M, Puig PE, Didelot C, Kroemer G (2006) Mechanisms of cytochrome c release from mitochondria. Cell Death Differ 13:1423–1433. doi:10.1038/sj.cdd.4401950 Thornberry NA, Lazebnik Y (1998) Caspases: enemies within. Science 281:1312–1316. doi:10.1126/science.281.5381.1312 Cuconati A, White E (2002) Viral homologs of BCL-2: Role of apoptosis in the regulation of virus infection. Genes Dev 16:2465–2478. doi:10.1101/gad.1012702 Cory S, Adams JM (2002) The Bcl2 family: Regulators of the cellular life-or-death switch. Nat Rev Cancer 2:647–656. doi:10.1038/nrc883 Adams JM (2003) Ways of dying: multiple pathways to apoptosis. Genes Dev 17:2481–2495. doi:10.1101/gad.1126903 Hildesheim J, Bulavin DV, Anver MR, Alvord WG, Hollander MC, Vardanian L et al (2002) Gadd45a protects against UV irradiation-induced skin tumors, and promotes apoptosis and stress signaling via MAPK and p53. Cancer Res 62:7305–7315 Hildesheim J, Fornace AJ Jr (2002) Gadd45a: an elusive yet attractive candidate gene in pancreatic cancer. Clin Cancer Res 8:2475–2479 Zhang D, Song L, Li J, Wu K, Huang C (2006) Coordination of JNK1 and JNK2 is critical for GADD45alpha induction and its mediated cell apoptosis in arsenite responses. J Biol Chem 281:34113–34123. doi:10.1074/jbc.M602821200 Gupta M, Gupta SK, Hoffman B, Liebermann DA (2006) Gadd45a and Gadd45b Protect Hematopoietic Cells from UV-induced Apoptosis via Distinct Signaling Pathways, including p38 Activation and JNK Inhibition. J Biol Chem 281:17552–17558. doi:10.1074/jbc.M600950200 Mak SK, Kültz D (2004) Gadd45 proteins induce G2/M arrest and modulate apoptosis in kidney cells exposed to hyperosmotic stress. J Biol Chem 279:39075–39084. doi:10.1074/jbc.M406643200 Viswakarma N, Yu S, Naik S, Kashireddy P, Matsumoto K et al (2007) Transcriptional regulation of Cidea, mitochondrial cell death-inducing DNA fragmentation factor alpha-like effector A, in mouse liver by peroxisome proliferator-activated receptor alpha and gamma. J Biol Chem 282:18613–18624. doi:10.1074/jbc.M701983200 Gade P, Roy SK, Li H, Nallar SC, Kalvakolanu DV (2008) Critical role for transcription factor C/EBP-beta in regulating the expression of death-associated protein kinase 1. Mol Cell Biol 28:2528–2548. doi:10.1128/MCB.00784-07 Huang XL, Cui GH, Zhou KY (2008) Correlation of PI3K-Akt signal pathway to apoptosis of tumor cells. Ai Zheng 27:331–336 Sugita H, Kaneki M, Sugita M, Yasukawa T, Yasuhara S, Martyn JA (2005) Burn injury impairs insulin-stimulated Akt/PKB activation in skeletal muscle. Am J Physiol Endocrinol Metab 288:E585–E591. doi:10.1152/ajpendo.00321.2004 Koseki T, Inohara N, Chen S, Núñez G (1998) ARC, an inhibitor of apoptosis expressed in skeletal muscle and heart that interacts selectively with caspases. Proc Natl Acad Sci U S A 95:5156–5160. doi:10.1073/pnas.95.9.5156 Nam YJ, Mani K, Ashton AW, Peng CF, Krishnamurthy B, Hayakawa Y et al (2004) Inhibition of both the extrinsic and intrinsic death pathways through nonhomotypic death-fold interactions. Mol Cell 15:901–912. doi:10.1016/j.molcel.2004.08.020 Zhou QY (2006) The prokineticins: a novel pair of regulatory peptides. Mol Interv 6:330–338. doi:10.1124/mi.6.6.6 Bharhani MS, Borojevic R, Basak S, Ho E, Zhou P, Croitoru K (2006) IL-10 protects mouse intestinal epithelial cells from Fas-induced apoptosis via modulating Fas expression and altering caspase-8 and FLIP expression. Am J Physiol Gastrointest Liver Physiol 291:G820–G829. doi:10.1152/ajpgi.00438.2005 Alway SE, Siu PM (2008) Nuclear apoptosis contributes to sarcopenia. Exerc Sport Sci Rev 36:51–57