The chaperone co-inducer BGP-15 alleviates ventilation-induced diaphragm dysfunction

Science Translational Medicine

Volumn 8, Issue 350, 2016, Pages 350ra103-

  Salah, Heba ^a,b   Li, Meishan ^a   Cacciani, Nicola ^a   Gastaldello, Stefano ^a   Ogilvie, Hannah ^a   Akkad, Hazem ^a   Venkat Namuduri, Arvind ^a   Morbidoni, Valeria ^c   Artemenko, Konstantin A ^d   Balogh, Gabor ^e   Martinez Redondo, Vicente ^a   Jannig, Paulo ^a   Hedström, Yvette ^a   Dworkin, Barry ^a,f   Bergquist, Jonas ^d,g,h   Ruas, Jorge ^a   Vigh, Laszlo ^e   Salviati, Leonardo ^c   Larsson, Lars ^a,i  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

^c UNIVERSITY OF PADOVA   (Italy)

^d UPPSALA UNIVERSITY   (Sweden)

^e INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^f PENN STATE COLLEGE OF MEDICINE   (United States)

^g UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^h BINZHOU MEDICAL UNIVERSITY   (China)

ⁱ PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN 72; MYOSIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; O (2 HYDROXY 3 PIPERIDINOPROPYL)NICOTINIC AMIDOXIME; SOMATOMEDIN C RECEPTOR; SUMO 2 PROTEIN; SUMO 3 PROTEIN; OXIME; PIPERIDINE DERIVATIVE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ARTIFICIAL VENTILATION; ATROPHY; CONTROLLED STUDY; DIAPHRAGM ATROPHY; DIAPHRAGM DISEASE; DIAPHRAGM MUSCLE; DRUG EFFICACY; DRUG MECHANISM; ENZYME INHIBITION; FEMALE; INTENSIVE CARE UNIT; MITOCHONDRIAL RESPIRATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN INDUCTION; PROTEIN PROCESSING; RAT; RESPIRATORY CHAIN; SMOOTH MUSCLE CONTRACTION; SUMOYLATION; TREATMENT DURATION; VENTILATION INDUCED DIAPHRAGM DYSFUNCTION; ANIMAL; DIAPHRAGM; DRUG EFFECTS; MASS SPECTROMETRY; METABOLISM; PATHOLOGY; PROTEOMICS; SKELETAL MUSCLE CELL; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ANIMALS; DIAPHRAGM; FEMALE; INTENSIVE CARE UNITS; MASS SPECTROMETRY; MICROSCOPY, ELECTRON, TRANSMISSION; MUSCLE FIBERS, SKELETAL; OXIMES; PIPERIDINES; PROTEOMICS; RATS; RESPIRATION, ARTIFICIAL;

EID: 84982795909     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aaf7099     Document Type: Article

References (56)

1. G. S. Supinski, L. A. Callahan, Diaphragm weakness in mechanically ventilated critically ill patients. Crit. Care 17, R120 (2013).
2. B. J. Petrof, S. Jaber, S. Matecki, Ventilator-induced diaphragmatic dysfunction. Curr. Opin. Crit. Care 16, 19-25 (2010).
3. D. Testelmans, K. Maes, P. Wouters, N. Gosselin, K. Deruisseau, S. Powers, R. Sciot, M. Decramer, G. Gayan-Ramirez, Rocuronium exacerbates mechanical ventilation-induced diaphragm dysfunction in rats. Crit. Care Med. 34, 3018-3023 (2006).
4. A. Esteban, F. Frutos, M. J. Tobin, I. Alía, J. F. Solsona, V. Valverdu, R. Fernández, M. A. de la Cal, S. Benito, R. Tomás, D. Carriedo, S. Macías, J. Blanco; Spanish Lung Failure Collaborative Group, A comparison of four methods of weaning patients from mechanical ventilation. N. Engl. J. Med. 332, 345-350 (1995).
5. R. Corpeno, B. Dworkin, N. Cacciani, H. Salah, H.-M. Bergman, B. Ravara, M. Vitadello, L. Gorza, A.-M.Gustafson, Y.Hedström, J. Petersson, H.-Z. Feng, J.-P. Jin, H. Iwamoto, N. Yagi, K. Artemenko, J. Bergquist, L. Larsson, Time course analysis of mechanical ventilation-induced diaphragm contractile muscle dysfunction in the rat. J. Physiol. 592, 3859-3880 (2014).
6. L. Larsson, N. Cacciani, B. Dworkin, Reply from Lars Larsson, Nicola Cacciani and Barry Dworkin. J. Physiol. 593, 3391-3392 (2015).
7. H. Akkad, R. Corpeno, L. Larsson, Masseter muscle myofibrillar protein synthesis and degradation in an experimental critical illness myopathy model. PLOS One 9, e92622 (2014).
8. M. Llano-Diez, G. Renaud, M. Andersson, H. G. Marrero, N. Cacciani, H. Engquist, R. Corpeño, K. Artemenko, J. Bergquist, L. Larsson, Mechanisms underlying ICU muscle wasting and effects of passive mechanical loading. Crit. Care 16, R209 (2012).
9. G. Renaud, M. Llano-Diez, B. Ravara, L. Gorza, H.-Z. Feng, J.-P. Jin, N. Cacciani, A.-M. Gustafson, J. Ochala, R. Corpeno, M. Li, Y. Hedström, G. Charles Ford, K. S. Nair, L. Larsson, Sparing of muscle mass and function by passive loading in an experimental intensive care unit model. J. Physiol. 591, 1385-1402 (2013).
10. J. Ochala, K. Ahlbeck, P. J. Radell, L. I. Eriksson, L. Larsson, Factors underlying the early limb muscle weakness in acute quadriplegic myopathy using an experimental ICU porcine model. PLOS One 6, e20876 (2011).
11. H. Norman, J. Nordquist, P. Andersson, T. Ansved, X. Tang, B. Dworkin, L. Larsson, Impact of post-synaptic block of neuromuscular transmission, muscle unloading and mechanical ventilation on skeletal muscle protein and mRNA expression. Pflugers Arch. 453, 53-66 (2006).
12. J. Nordquist, A.-S. Höglund, H. Norman, X. Tang, B. Dworkin, L. Larsson, Transcription factors in muscle atrophy caused by blocked neuromuscular transmission and muscle unloading in rats. Mol. Med. 13, 461-470 (2007).
13. V. C. Banduseela, J. Ochala, Y.-W. Chen, H. Göransson, H. Norman, P. Radell, L. I. Eriksson, E. P. Hoffman, L. Larsson, Gene expression and muscle fiber function in a porcine ICU model. Physiol. Genomics 39, 141-159 (2009).
14. S. Aare, J. Ochala, H. S. Norman, P. Radell, L. I. Eriksson, H. Göransson, Y.-W. Chen, E. P. Hoffman, L. Larsson, Mechanisms underlying the sparing of masticatory versus limb muscle function in an experimental critical illness model. Physiol. Genomics 43, 1334-1350 (2011).
15. I. Gombos, T. Crul, S. Piotto, B. Güngör, Z. Török, G. Balogh, M. Péter, J. P. Slotte, F. Campana, A.-M. Pilbat, Á. Hunya, N. Tóth, Z. Literati-Nagy, L. Vígh Jr., A. Glatz, M. Brameshuber, G. J. Schütz, A. Hevener, M. A. Febbraio, I. Horváth, L. Vígh, Membrane-lipid therapy in operation: The HSP co-inducer BGP-15 activates stress signal transduction pathways by remodeling plasma membrane rafts. PLOS One 6, e28818 (2011).
16. B. Gungor, I. Gombos, T. Crul, F. Ayaydin, L. Szabó, Z. Török, L. Mátés, L. Vígh, I. Horváth, Rac1 participates in thermally induced alterations of the cytoskeleton, cell morphology and lipid rafts, and regulates the expression of heat shock proteins in B16F10 melanoma cells. PLOS One 9, e89136 (2014).
17. D. C. Henstridge, C. R. Bruce, B. G. Drew, K. Tory, A. Kolonics, E. Estevez, J. Chung, N. Watson, T. Gardner, R. S. Lee-Young, T. Connor, M. J. Watt, K. Carpenter, M. Hargreaves, S. L. McGee, A. L. Hevener, M. A. Febbraio, Activating HSP72 in rodent skeletal muscle increases mitochondrial number and oxidative capacity and decreases insulin resistance. Diabetes 63, 1881-1894 (2014).
18. J. Chung, A.-K. Nguyen, D. C. Henstridge, A. G. Holmes, M. H. S. Chan, J. L. Mesa, G. I. Lancaster, R. J. Southgate, C. R. Bruce, S. J. Duffy, I. Horvath, R. Mestril, M. J. Watt, P. L. Hooper, B. A. Kingwell, L. Vigh, A. Hevener, M. A. Febbraio, HSP72 protects against obesity-induced insulin resistance. Proc. Natl. Acad. Sci. U.S.A. 105, 1739-1744 (2008).
19. P. V. Escribá, X. Busquets, J.-i. Inokuchi, G. Balogh, Z. Török, I. Horváth, J. L. Harwood, L. Vígh, Membrane lipid therapy: Modulation of the cell membrane composition and structure as a molecular base for drug discovery and new disease treatment. Prog. Lipid Res. 59, 38-53 (2015).
20. R. L. Moss, Sarcomere length-tension relations of frog skinned muscle fibres during calcium activation at short lengths. J. Physiol. 292, 177-192 (1979).
21. P. Höök, X. Li, J. Sleep, S. Hughes, L. Larsson, In vitro motility speed of slow myosin extracted from single soleus fibres from young and old rats. J. Physiol. 520, 463-471 (1999).
22. M. Li, L. Larsson, Force-generating capacity of human myosin isoforms extracted from single muscle fibre segments. J. Physiol. 588, 5105-5114 (2010).
23. M. B. Reid, A. R. Judge, S. C. Bodine, Rebuttal from Michael B. Reid, Andrew R. Judge and Sue C. Bodine. J. Physiol. 592, 5351 (2014).
24. S. Larsen, J. Nielsen, C. N. Hansen, L. B. Nielsen, F.Wibrand, N. Stride, H. D. Schroder, R. Boushel, J. W. Helge, F. Dela, M. Hey-Mogensen, Biomarkers of mitochondrial content in skeletal muscle of healthy young human subjects. J. Physiol. 590, 3349-3360 (2012).
25. M. Spinazzi, A. Casarin, V. Pertegato, L. Salviati, C. Angelini, Assessment of mitochondrial respiratory chain enzymatic activities on tissues and cultured cells. Nat. Protoc. 7, 1235-1246 (2012).
26. G. Sapra, Y. K. Tham, N. Cemerlang, A. Matsumoto, H. Kiriazis, B. C. Bernardo, D. C. Henstridge, J. Y. Y.Ooi, L. Pretorius, E. J. H. Boey, L. Lim, J. Sadoshima, P. J. Meikle, N. A. Mellet, E. A. Woodcock, S. Marasco, T. Ueyama, X.-J. Du, M. A. Febbraio, J. R. McMullen, The small-molecule BGP-15 protects against heart failure and atrial fibrillation in mice. Nat. Commun. 5, 5705 (2014).
27. T. Crul, N. Toth, S. Piotto, P. Literati-Nagy, K. Tory, P. Haldimann, B. Kalmar, L. Greensmith, Z. Torok, G. Balogh, I. Gombos, F. Campana, S. Concilio, F. Gallyas, G. Nagy, Z. Berente, B. Gungor, M. Peter, A. Glatz, A. Hunya, Z. Literati-Nagy, L. Vigh, F. Hoogstra-Berends, A. Heeres, I. Kuipers, L. Loen, J.-P. Seerden, D. Zhang, R. A. M. Meijering, R. H. Henning, B. J. J. M. Brundel, H. H. Kampinga, L. Koranyi, Z. Szilvassy, J. Mandl, B. Sumegi, M. A. Febbraio, I. Horvath, P. L. Hooper, L. Vigh, Hydroximic acid derivatives: Pleiotropic hsp co-inducers restoring homeostasis and robustness. Curr. Pharm. Des. 19, 309-346 (2013).
28. M. D. Zilberberg, A. F. Shorr, Prolonged acute mechanical ventilation and hospital bed utilization in 2020 in the United States: Implications for budgets, plant and personnel planning. BMC Health Serv. Res. 8, 242 (2008).
29. S. Cogliati, C. Frezza, M. E. Soriano, T. Varanita, R. Quintana-Cabrera, M. Corrado, S. Cipolat, V. Costa, A. Casarin, L. C. Gomes, E. Perales-Clemente, L. Salviati, P. Fernandez-Silva, J. A. Enriquez, L. Scorrano, Mitochondrial cristae shape determines respiratory chain supercomplexes assembly and respiratory efficiency. Cell 155, 160-171 (2013).
30. D. C. Chan, Fusion and fission: Interlinked processes critical for mitochondrial health. Annu. Rev. Genet. 46, 265-287 (2012).
31. M. A. Zergeroglu, M. J. McKenzie, R. A. Shanely, D. VanGammeren, K. C. DeRuisseau, S. K. Powers, Mechanical ventilation-induced oxidative stress in the diaphragm. J. Appl. Physiol. 95, 1116-1124 (2003).
32. D. J. Falk, K. C. DeRuisseau, D. L. Van Gammeren, M. A. Deering, A. N. Kavazis, S. K. Powers, Mechanical ventilation promotes redox status alterations in the diaphragm. J. Appl. Physiol. 101, 1017-1024 (2006).
33. J. Ochala, L. Larsson, in Muscle: Fundamental Biology and Mechanisms and Disease, J. A. Hill, H. L. Sweeney, E. N. Olson, Eds. (Academic Press, London, 2012), pp. 1023-1030.
34. L. I. Larsson, Immunogold labelling of neuroendocrine peptides with special reference to antibody specificity and multiple staining techniques. Histochem. Cell Biol. 106, 93-103 (1996).
35. F. L. Sheeran, S. Pepe, Energy deficiency in the failing heart: Linking increased reactive oxygen species and disruption of oxidative phosphorylation rate. Biochim. Biophys. Acta 1757, 543-552 (2006).
36. S. M. Gehrig, C. van der Poel, T. A. Sayer, J. D. Schertzer, D. C. Henstridge, J. E. Church, S. Lamon, A. P. Russell, K. E. Davies, M. A. Febbraio, G. S. Lynch, Hsp72 preserves muscle function and slows progression of severe muscular dystrophy. Nature 484, 394-398 (2012).
37. M. K. Jacobson, E. L. Jacobson, Discovering new ADP-ribose polymer cycles: Protecting the genome and more. Trends Biochem. Sci. 24, 415-417 (1999).
38. R. Halmosi, Z. Berente, E. Osz, K. Toth, P. Literati-Nagy, B. Sumegi, Effect of poly(ADP-ribose) polymerase inhibitors on the ischemia-reperfusion-induced oxidative cell damage and mitochondrial metabolism in Langendorff heart perfusion system. Mol. Pharmacol. 59, 1497-1505 (2001).
39. K. Kovacs, A. Toth, P. Deres, T. Kalai, K. Hideg, B. Sumegi, Myocardial protection by selective poly(ADP-ribose) polymerase inhibitors. Exp. Clin. Cardiol. 9, 17-20 (2004).
40. J. Bowes, M. C. McDonald, J. Piper, C. Thiemermann, Inhibitors of poly (ADP-ribose) synthetase protect rat cardiomyocytes against oxidant stress. Cardiovasc. Res. 41, 126-134 (1999).
41. J. Ochala, A.-M. Gustafson, M. L. Diez, G. Renaud, M. Li, S. Aare, R. Qaisar, V. C. Banduseela, Y. Hedström, X. Tang, B. Dworkin, G. Charles Ford, K. S. Nair, S. Perera, M. Gautel, L. Larsson, Preferential skeletal muscle myosin loss in response to mechanical silencing in a novel rat intensive care unit model: Underlying mechanisms. J. Physiol. 589, 2007-2026 (2011).
42. L. Larsson, X. Li, L. Edström, L. I. Eriksson, H. Zackrisson, C. Argentini, S. Schiaffino, Acute quadriplegia and loss of muscle myosin in patients treated with nondepolarizing neuromuscular blocking agents and corticosteroids: Mechanisms at the cellular and molecular levels. Crit. Care Med. 28, 34-45 (2000).
43. B. R. Dworkin, S. Dworkin, Baroreflexes of the rat. III. Open-loop gain and electroencephalographic arousal. Am. J. Physiol. Regul. Integr. Comp. Physiol. 286, R597-R605 (2004).
44. B. R. Dworkin, S. Dworkin, Learning of physiological responses: I. Habituation, sensitization, and classical conditioning. Behav. Neurosci. 104, 298-319 (1990).
45. L. Larsson, R. L. Moss, Maximum velocity of shortening in relation to myosin isoform composition in single fibres from human skeletal muscles. J. Physiol. 472, 595-614 (1993).
46. P. Höök, L. Larsson, Actomyosin interactions in a novel single muscle fiber in vitro motility assay. J. Muscle Res. Cell Motil. 21, 357-365 (2000).
47. G. Balogh, M. Péter, G. Liebisch, I. Horváth, Z. Török, E. Nagy, A. Maslyanko, S. Benko″, G. Schmitz, J. L. Harwood, L. Vígh, Lipidomics reveals membrane lipid remodelling and release of potential lipid mediators during early stress responses in a murine melanoma cell line. Biochim. Biophys. Acta 1801, 1036-1047 (2010).
48. O. Antal, M. Péter, L. Hackler Jr., I. Mán, G. Szebeni, F. Ayaydin, K. Hideghéty, L. Vigh, K. Kitajka, G. Balogh, L. G. Puskás, Lipidomic analysis reveals a radiosensitizing role of gamma-linolenic acid in glioma cells. Biochim. Biophys. Acta 1851, 1271-1282 (2015).
49. R. Herzog, D. Schwudke, K. Schuhmann, J. L. Sampaio, S. R. Bornstein, M. Schroeder, A. Shevchenko, A novel informatics concept for high-throughput shotgun lipidomics based on the molecular fragmentation query language. Genome Biol. 12, R8 (2011).
50. A. Fabiato, Computer programs for calculating total from specified free or free from specified total ionic concentrations in aqueous solutions containing multiple metals and ligands. Methods Enzymol. 157, 378-417 (1988).
51. K. A. Edman, The velocity of unloaded shortening and its relation to sarcomere length and isometric force in vertebrate muscle fibres. J. Physiol. 291, 143-159 (1979).
52. J. D. Pardee, J. A. Spudich, Purification of muscle actin. Methods Enzymol. 85, 164-181 (1982).
53. M. Picard, K. White, D. M. Turnbull, Mitochondrial morphology, topology, and membrane interactions in skeletal muscle: A quantitative three-dimensional electron microscopy study. J. Appl. Physiol. 114, 161-171 (2013).
54. M. Spinazzi, A. Casarin, V. Pertegato, M. Ermani, L. Salviati, C. Angelini, Optimization of respiratory chain enzymatic assays in muscle for the diagnosis of mitochondrial disorders. Mitochondrion 11, 893-904 (2011).
55. J. Becker, S. V. Barysch, S. Karaca, C. Dittner, H.-H. Hsiao, M. B. Diaz, S. Herzig, H. Urlaub, F. Melchior, Detecting endogenous SUMO targets in mammalian cells and tissues. Nat. Struct. Mol. Biol. 20, 525-531 (2013).
56. A. R. Weber, D. Schuermann, P. Schär, Versatile recombinant SUMOylation system for the production of SUMO-modified protein. PLOS One 9, e102157 (2014).