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European Journal of Trauma and Emergency Surgery

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01.12.2011 | Original Article

Effects on the ubiquitin proteasome system after closed soft-tissue trauma in rat skeletal muscle

verfasst von: N. Ponelies, D. Gosenca, N. Ising, M. Schoen, K. Ruppel, B. Vollmar, U. Obertacke

Erschienen in: European Journal of Trauma and Emergency Surgery | Ausgabe 6/2011

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Abstract

Previous studies have suggested that an increased catabolic stage of skeletal muscle in pathological situations is mainly a reflection of ubiquitin–proteasome system-controlled proteolysis. The proteolytic mechanisms that occur after local muscle trauma are poorly defined. We investigated the effects of closed soft-tissue trauma on ubiquitin–proteasome dependent protein breakdown in rats (n = 25). The enzymatic activities of the ubiquitination and proteasome reactions were both reduced (p < 0.05) immediately after contusion of the hind limb musculus extensor digitorum longus. The same effect was observed in extracts of lung tissue from the injured animals. Cellular levels of free and protein-conjugated ubiquitin were significantly elevated upon decreased proteolytic activity. Our data support an early-state anti-proteolytic role of the ubiquitin–proteasome pathway after local injury. This further implies that there is a yet-to-be elucidated complex regulatory mechanism of muscle regeneration that involves various proteolytic systems.

Medina R, Wing SS, Goldberg AL. Increase in levels of polyubiquitin and proteasome mRNA in skeletal muscle during starvation and denervation atrophy. Biochem J. 1995;307(Pt 3):631–7.PubMed

Song XM, Ryder JW, Kawano Y, Chibalin AV, Krook A, Zierath JR. Muscle fiber type specificity in insulin signal transduction. Am J Physiol. 1999;277:R1690–6.PubMed

Goldberg AL, Tischler M, DeMartino G, Griffin G. Hormonal regulation of protein degradation and synthesis in skeletal muscle. Fed Proc. 1980;39:31–6.PubMed

Li JB, Goldberg AL. Effects of food deprivation on protein synthesis and degradation in rat skeletal muscles. Am J Physiol. 1976;231:441–8.PubMed

Reid MB. Response of the ubiquitin–proteasome pathway to changes in muscle activity. Am J Physiol Regul Integr Comp Physiol. 2005;288:R1423–31.PubMedCrossRef

Sugden PH, Fuller SJ. Regulation of protein turnover in skeletal and cardiac muscle. Biochem J. 1991;273(Pt 1):21–37.PubMed

Lecker SH, Solomon V, Mitch WE, Goldberg AL. Muscle protein breakdown and the critical role of the ubiquitin–proteasome pathway in normal and disease states. J Nutr. 1999;129:227S–37S.PubMed

Mitch WE, Goldberg AL. Mechanisms of muscle wasting. The role of the ubiquitin–proteasome pathway. N Engl J Med. 1996;335:1897–905.PubMedCrossRef

Hasselgren PO, Menconi MJ, Fareed MU, Yang H, Wei W, Evenson A. Novel aspects on the regulation of muscle wasting in sepsis. Int J Biochem Cell Biol. 2005;37:2156–68.PubMedCrossRef

10.

Hasselgren PO, Wray C, Mammen J. Molecular regulation of muscle cachexia: it may be more than the proteasome. Biochem Biophys Res Commun. 2002;290:1–10.PubMedCrossRef

11.

Khal J, Wyke SM, Russell ST, Hine AV, Tisdale MJ. Expression of the ubiquitin–proteasome pathway and muscle loss in experimental cancer cachexia. Br J Cancer. 2005;93:774–80.PubMedCrossRef

12.

Lecker SH, Jagoe RT, Gilbert A, Gomes M, Baracos V, Bailey J, et al. Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J. 2004;18:39–51.PubMedCrossRef

13.

Voisin L, Breuille D, Combaret L, Pouyet C, Taillandier D, Aurousseau E, et al. Muscle wasting in a rat model of long-lasting sepsis results from the activation of lysosomal, Ca²⁺-activated, and ubiquitin–proteasome proteolytic pathways. J Clin Invest. 1996;97:1610–7.PubMedCrossRef

14.

Tisdale MJ. The ubiquitin–proteasome pathway as a therapeutic target for muscle wasting. J Support Oncol. 2005;3:209–17.PubMed

15.

Attaix D, Ventadour S, Codran A, Bechet D, Taillandier D, Combaret L. The ubiquitin–proteasome system and skeletal muscle wasting. Essays Biochem. 2005;41:173–86.PubMedCrossRef

16.

Lecker SH, Goldberg AL, Mitch WE. Protein degradation by the ubiquitin–proteasome pathway in normal and disease states. J Am Soc Nephrol. 2006;17:1807–19.PubMedCrossRef

17.

Larbaud D, Balage M, Taillandier D, Combaret L, Grizard J, Attaix D. Differential regulation of the lysosomal, Ca²⁺-dependent and ubiquitin/proteasome-dependent proteolytic pathways in fast-twitch and slow-twitch rat muscle following hyperinsulinaemia. Clin Sci (Lond). 2001;101:551–8.CrossRef

18.

Lee SW, Dai G, Hu Z, Wang X, Du J, Mitch WE. Regulation of muscle protein degradation: coordinated control of apoptotic and ubiquitin–proteasome systems by phosphatidylinositol 3 kinase. J Am Soc Nephrol. 2004;15:1537–45.PubMedCrossRef

19.

Dixon CE, Clifton GL, Lighthall JW, Yaghmai AA, Hayes RL. A controlled cortical impact model of traumatic brain injury in the rat. J Neurosci Methods. 1991;39:253–62.PubMedCrossRef

20.

Schaser KD, Vollmar B, Menger MD, Schewior L, Kroppenstedt SN, Raschke M, et al. In vivo analysis of microcirculation following closed soft-tissue injury. J Orthop Res. 1999;17:678–85.PubMedCrossRef

21.

Tscherne H, Oestern HJ. A new classification of soft-tissue damage in open and closed fractures (author’s transl). Unfallheilkunde. 1982;85:111–5.PubMed

22.

Ponelies N, Hirsch T, Krehmeier U, Denz C, Patel MB, Majetschak M. Cytosolic ubiquitin and ubiquitylation rates in human peripheral blood mononuclear cells during sepsis. Shock. 2005;24:20–5.PubMedCrossRef

23.

Majetschak M, Ponelies N, Hirsch T. Targeting the monocytic ubiquitin system with extracellular ubiquitin. Immunol Cell Biol. 2006;84:59–65.PubMedCrossRef

24.

Schaser KD, Bail HJ, Schewior L, Stover JF, Melcher I, Haas NP, Mittlmeier T. Acute effects of N-acetylcysteine on skeletal muscle microcirculation following closed soft tissue trauma in rats. J Orthop Res. 2005;23:231–41.PubMedCrossRef

25.

Kessler BM, Tortorella D, Altun M, Kisselev AF, Fiebiger E, Hekking BG, et al. Extended peptide-based inhibitors efficiently target the proteasome and reveal overlapping specificities of the catalytic beta-subunits. Chem Biol. 2001;8:913–29.PubMedCrossRef

26.

Meng L, Mohan R, Kwok BH, Elofsson M, Sin N, Crews CM. Epoxomicin, a potent and selective proteasome inhibitor, exhibits in vivo antiinflammatory activity. Proc Natl Acad Sci USA. 1999;96:10403–8.PubMedCrossRef

27.

Hobler SC, Williams A, Fischer D, Wang JJ, Sun X, Fischer JE, et al. Activity and expression of the 20S proteasome are increased in skeletal muscle during sepsis. Am J Physiol. 1999;277:R434–40.PubMed

28.

Mitch WE, Bailey JL, Wang X, Jurkovitz C, Newby D, Price SR. Evaluation of signals activating ubiquitin–proteasome proteolysis in a model of muscle wasting. Am J Physiol. 1999;276:C1132–8.PubMed

29.

Jagoe RT, Goldberg AL. What do we really know about the ubiquitin–proteasome pathway in muscle atrophy? Curr Opin Clin Nutr Metab Care. 2001;4:183–90.PubMedCrossRef

30.

Mansoor O, Beaufrere B, Boirie Y, Ralliere C, Taillandier D, Aurousseau E, et al. Increased mRNA levels for components of the lysosomal, Ca²⁺-activated, and ATP-ubiquitin-dependent proteolytic pathways in skeletal muscle from head trauma patients. Proc Natl Acad Sci USA. 1996;93:2714–8.PubMedCrossRef

31.

Fang CH, Li BG, James JH, King JK, Evenson AR, Warden GD, Hasselgren PO. Protein breakdown in muscle from burned rats is blocked by insulin-like growth factor i and glycogen synthase kinase-3β inhibitors. Endocrinology. 2005;146:3141–9.PubMedCrossRef

32.

Seiffert M, Gosenca D, Ponelies N, Ising N, Patel MB, Obertacke U, Majetschak M. Regulation of the ubiquitin proteasome system in mechanically injured human skeletal muscle. Physiol Res. 2007;56:227–33.PubMed

33.

Fisher BD, Baracos VE, Shnitka TK, Mendryk SW, Reid DC. Ultrastructural events following acute muscle trauma. Med Sci Sports Exerc. 1990;22:185–93.PubMed

34.

Fisher BD, Rathgaber M. An overview of muscle regeneration following acute injury. J Phys Ther Sci. 2006;18:57–66.CrossRef

35.

Gierer P, Vollmar B, Schaser KD, Andreas C, Gradl G, Mittlmeier T. Efficiency of small-volume resuscitation in restoration of disturbed skeletal muscle microcirculation after soft-tissue trauma and haemorrhagic shock. Langenbecks Arch Surg. 2004;389:40–5.PubMedCrossRef

36.

Tjader I, Essen P, Garlick PJ, McMnurlan MA, Rooyackers O, Wernerman J. Impact of surgical trauma on human skeletal muscle protein synthesis. Clin Sci (Lond). 2004;107:601–7.CrossRef

37.

Luo JL, Hammarqvist F, Andersson K, Wernerman J. Surgical trauma decreases glutathione synthetic capacity in human skeletal muscle tissue. Am J Physiol. 1998;275:E359–65.PubMed

38.

Farges MC, Balcerzak D, Fisher BD, Attaix D, Bechet D, Ferrara M, Baracos VE. Increased muscle proteolysis after local trauma mainly reflects macrophage-associated lysosomal proteolysis. Am J Physiol Endocrinol Metab. 2002;282:E326–35.PubMed

39.

Tawa NE Jr, Odessey R, Goldberg AL. Inhibitors of the proteasome reduce the accelerated proteolysis in atrophying rat skeletal muscles. J Clin Invest. 1997;100:197–203.PubMedCrossRef

40.

Zhu Q, Wani G, Wang QE, El-mahdy M, Snapka RM, Wani AA. Deubiquitination by proteasome is coordinated with substrate translocation for proteolysis in vivo. Exp Cell Res. 2005;307:436–51.PubMedCrossRef

41.

Kim JH, Park KC, Chung SS, Bang O, Chung CH. Deubiquitinating enzymes as cellular regulators. J Biochem (Tokyo). 2003;134:9–18.CrossRef

42.

Combaret L, Adegoke OA, Bedard N, Baracos V, Attaix D, Wing SS. USP19 is a ubiquitin-specific protease regulated in rat skeletal muscle during catabolic states. Am J Physiol Endocrinol Metab. 2005;288:E693–700.PubMedCrossRef

43.

Fuster G, Busquets S, Almendro V, Lopez-Soriano FJ, Argiles JM. Antiproteolytic effects of plasma from hibernating bears: a new approach for muscle wasting therapy? Clin Nutr. 2007;26:658–61.PubMedCrossRef

44.

Fielding RA, Manfredi TJ, Ding W, Fiatarone MA, Evans WJ, Cannon JG. Acute phase response in exercise. III. Neutrophil and IL-1 beta accumulation in skeletal muscle. Am J Physiol. 1993;265:R166–72.PubMed

45.

Tidball JG, Berchenko E, Frenette J. Macrophage invasion does not contribute to muscle membrane injury during inflammation. J Leukoc Biol. 1999;65:492–8.PubMed

46.

Gates C, Huard J. Management of skeletal muscle injuries in military personnel. Oper Tech Sports Med. 2005;13:247–56.CrossRef

47.

Charge SB, Rudnicki MA. Cellular and molecular regulation of muscle regeneration. Physiol Rev. 2004;84:209–38.PubMedCrossRef

Titel: Effects on the ubiquitin proteasome system after closed soft-tissue trauma in rat skeletal muscle
verfasst von: N. Ponelies
D. Gosenca
N. Ising
M. Schoen
K. Ruppel
B. Vollmar
U. Obertacke
Publikationsdatum: 01.12.2011
Verlag: Springer-Verlag
Erschienen in: European Journal of Trauma and Emergency Surgery / Ausgabe 6/2011
Print ISSN: 1863-9933
Elektronische ISSN: 1863-9941
DOI: https://doi.org/10.1007/s00068-011-0083-8

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