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Cited by 60Muscle Physiology and DisordersHeat shock proteins researchMeat and Animal Product Quality

Modulation of Caspase Activity Regulates Skeletal Muscle Regeneration and Function in Response to Vasopressin and Tumor Necrosis Factor

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Moresi, Viviana, Garcia-Alvarez, Gisela, Pristerà, Alessandro, Rizzuto, Emanuele, Albertini, Maria C., Rocchi, Marco, Marazzi, Giovanna, Sassoon, David +2 more·2009·PLoS ONE
DOI 10.1371/journal.pone.0005570PMC PMC2680623
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Abstract

Muscle homeostasis involves de novo myogenesis, as observed in conditions of acute or chronic muscle damage. Tumor Necrosis Factor (TNF) triggers skeletal muscle wasting in several pathological conditions and inhibits muscle regeneration. We show that intramuscular treatment with the myogenic factor Arg(8)-vasopressin (AVP) enhanced skeletal muscle regeneration and rescued the inhibitory effects of TNF on muscle regeneration. The functional analysis of regenerating muscle performance following TNF or AVP treatments revealed that these factors exerted opposite effects on muscle function. Principal component analysis showed that TNF and AVP mainly affect muscle tetanic force and fatigue. Importantly, AVP counteracted the effects of TNF on muscle function when delivered in combination with the latter. Muscle regeneration is, at least in part, regulated by caspase activation, and AVP abrogated TNF-dependent caspase activation. The contrasting effects of AVP and TNF in vivo are recapitulated in myogenic cell cultures, which express both PW1, a caspase activator, and Hsp70, a caspase inhibitor. We identified PW1 as a potential Hsp70 partner by screening for proteins interacting with PW1. Hsp70 and PW1 co-immunoprecipitated and co-localized in muscle cells. In vivo Hsp70 protein level was upregulated by AVP, and Hsp70 overexpression counteracted the TNF block of muscle regeneration. Our results show that AVP counteracts the effects of TNF through cross-talk at the Hsp70 level. Therefore, muscle regeneration, both in the absence and in the presence of cytokines may be enhanced by increasing Hsp70 expression.

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  • Few data are available on caspase-induced apoptosis in COPD despite caspase-induced apoptosis being a known contributor of muscle wasting.

    “Surprisingly, few data are available to date in COPD despite the fact that caspase-induced apoptosis is a known contributor of muscle wasting [114].”

    From Main Pathogenic Mechanisms and Recent Advances in COPD Peripheral Skeletal Muscle Wasting (2023) · cites this paper as [114]

    The Introduction (page unavailable) links muscle wasting and impaired regeneration to TNF and caspase activity. But it describes the relevant caspase activation as non-apoptotic, so it does not establish the cited assertion that caspase-induced apoptosis contributes to muscle wasting. The paper also does not assess how much evidence is available in COPD. (LLM, conf=0.84)

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  1. [1]Mitchell PO Pavlath GK 2004 Skeletal muscle atrophy leads to loss and dysfunction of muscle precursor cells. Am J Physiol Cell Physiol 287 C1753 C1762 15329339
  2. [2]Mitchell PO Pavlath GK 2001 A muscle precursor cell-dependent pathway contributes to muscle growth after atrophy. Am J Physiol Cell Physiol 281 C1706 C1715 11600435
  3. [3]Graupe D Cerrel-Bazo H Kern H Carraro U 2008 Walking performance, medical outcomes and patient training in FES of innervated muscles for ambulation by thoracic-level complete paraplegics. Neurol Res 30 123 130 18397602
  4. [4]Coletti D Moresi V Adamo S Molinaro M Sassoon D 2005 Tumor necrosis factor-alpha gene transfer induces cachexia and inhibits muscle regeneration. Genesis 43 120 128 16158413
  5. [5]Guttridge DC Mayo MW Madrid LV Wang CY Baldwin AS Jr 2000 NF-kappaB-induced loss of MyoD messenger RNA: possible role in muscle decay and cachexia. Science 289 2363 2366 11009425
  6. [6]Moresi V Pristera A Scicchitano BM Molinaro M Teodori L 2008 Tumor necrosis factor-alpha inhibition of skeletal muscle regeneration is mediated by a caspase-dependent stem cell response. Stem Cells 26 997 1008 18258721
  7. [7]Clark IA 2007 How TNF was recognized as a key mechanism of disease. Cytokine Growth Factor Rev 18 335 343 17493863
  8. [8]Hodgetts S Radley H Davies M Grounds MD 2006 Reduced necrosis of dystrophic muscle by depletion of host neutrophils, or blocking TNFalpha function with Etanercept in mdx mice. Neuromuscul Disord 16 591 602 16935507
  9. [9]Coletti D Adamo S 2008 Highlights on Cachexia, from the 4th Cachexia Conference Tampa (FL), 6–9 Dec 2007. Basic Appl Myol 18 109 114
  10. [11]Coletti D Yang E Marazzi G Sassoon D 2002 TNFalpha inhibits skeletal myogenesis through a PW1-dependent pathway by recruitment of caspase pathways. EMBO J 21 631 642 11847111 PMC125350
  11. [12]Deng Y Wu X 2000 Peg3/Pw1 promotes p53-mediated apoptosis by inducing Bax translocation from cytosol to mitochondria. Proc Natl Acad Sci U S A 97 12050 12055 11050235 PMC17292
  12. [13]Schwarzkopf M Coletti D Sassoon D Marazzi G 2006 Muscle cachexia is regulated by a p53-PW1/Peg3-dependent pathway. Genes Dev 20 3440 3452 17182869 PMC1698450
  13. [14]Relaix F Weng X Marazzi G Yang E Copeland N 1996 Pw1, a novel zinc finger gene implicated in the myogenic and neuronal lineages. Dev Biol 177 383 396 8806818
  14. [15]Relaix F Wei X Li W Pan J Lin Y 2000 Pw1/Peg3 is a potential cell death mediator and cooperates with Siah1a in p53-mediated apoptosis. Proc Natl Acad Sci U S A 97 2105 2110 10681424 PMC15761
  15. [16]Li P Nijhawan D Budihardjo I Srinivasula SM Ahmad M 1997 Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91 479 489 9390557
  16. [17]Saleh A Srinivasula SM Balkir L Robbins PD Alnemri ES 2000 Negative regulation of the Apaf-1 apoptosome by Hsp70. Nat Cell Biol 2 476 483 10934467
  17. [19]Miyabara EH Martin JL Griffin TM Moriscot AS Mestril R 2006 Overexpression of inducible 70-kDa heat shock protein in mouse attenuates skeletal muscle damage induced by cryolesioning. Am J Physiol Cell Physiol 290 C1128 C1138 16291818
  18. [20]Senf SM Dodd SL McClung JM Judge AR 2008 Hsp70 overexpression inhibits NF-kappaB and Foxo3a transcriptional activities and prevents skeletal muscle atrophy. FASEB J 22 3836 3845 18644837 PMC6137947
  19. [23]Minotti S Scicchitano BM Nervi C Scarpa S Lucarelli M 1998 Vasopressin and insulin-like growth factors synergistically induce myogenesis in serum-free medium. Cell Growth Differ 9 155 163 9486852
  20. [24]Nervi C Benedetti L Minasi A Molinaro M Adamo S 1995 Arginine-vasopressin induces differentiation of skeletal myogenic cells and up-regulation of myogenin and Myf-5. Cell Growth Differ 6 81 89 7718487
  21. [25]Teti A Naro F Molinaro M Adamo S 1993 Transduction of arginine vasopressin signal in skeletal myogenic cells. Am J Physiol 265 C113 C121 8393277
  22. [26]Scicchitano BM Spath L Musaro A Molinaro M Adamo S 2002 AVP induces myogenesis through the transcriptional activation of the myocyte enhancer factor 2. Mol Endocrinol 16 1407 1416 12040025
  23. [27]Scicchitano BM Spath L Musaro A Molinaro M Rosenthal N 2005 Vasopressin-dependent myogenic cell differentiation is mediated by both Ca2+/calmodulin-dependent kinase and calcineurin pathways. Mol Biol Cell 16 3632 3641 15930130 PMC1182303
  24. [28]De Arcangelis V Coletti D Conti M Lagarde M Molinaro M 2003 IGF-I-induced differentiation of L6 myogenic cells requires the activity of cAMP-phosphodiesterase. Mol Biol Cell 14 1392 1404 12686596 PMC153109
  25. [29]Komati H Naro F Mebarek S De Arcangelis V Adamo S 2005 Phospholipase D is involved in myogenic differentiation through remodeling of actin cytoskeleton. Mol Biol Cell 16 1232 1244 15616193 PMC551488
  26. [30]Thibonnier M Graves MK Wagner MS Auzan C Clauser E 1996 Structure, sequence, expression, and chromosomal localization of the human V1a vasopressin receptor gene. Genomics 31 327 334 8838314
  27. [31]Alvisi M De Arcangelis V Ciccone L Palombi V Alessandrini M 2008 V1a vasopressin receptor expression is modulated during myogenic differentiation. Differentiation 76 371 380 18021262
  28. [32]Breton C Haenggeli C Barberis C Heitz F Bader CR 2002 Presence of functional oxytocin receptors in cultured human myoblasts. J Clin Endocrinol Metab 87 1415 1418 11889218
  29. [33]Melin B Eclache JP Geelen G Annat G Allevard AM 1980 Plasma AVP, neurophysin, renin activity, and aldosterone during submaximal exercise performed until exhaustion in trained and untrained men. Eur J Appl Physiol Occup Physiol 44 141 151 6997037
  30. [34]Alexander SL Irvine CH Ellis MJ Donald RA 1991 The effect of acute exercise on the secretion of corticotropin-releasing factor, arginine vasopressin, and adrenocorticotropin as measured in pituitary venous blood from the horse. Endocrinology 128 65 72 1846116
  31. [35]Convertino VA Keil LC Greenleaf JE 1983 Plasma volume, renin, and vasopressin responses to graded exercise after training. J Appl Physiol 54 508 514 6339451
  32. [36]Grounds MD Torrisi J 2004 Anti-TNFalpha (Remicade) therapy protects dystrophic skeletal muscle from necrosis. FASEB J 18 676 682 15054089
  33. [37]Coletti D Teodori L Albertini MC Rocchi M Pristera A 2007 Static magnetic fields enhance skeletal muscle differentiation in vitro by improving myoblast alignment. Cytometry A 71 846 856 17694560
  34. [38]Polekhina G House CM Traficante N Mackay JP Relaix F 2002 Siah ubiquitin ligase is structurally related to TRAF and modulates TNF-alpha signaling. Nat Struct Biol 9 68 75 11742346
  35. [39]Relaix F Wei XJ Wu X Sassoon DA 1998 Peg3/Pw1 is an imprinted gene involved in the TNF-NFkappaB signal transduction pathway. Nat Genet 18 287 291 9500555
  36. [40]Duguez S Bihan MC Gouttefangeas D Feasson L Freyssenet D 2003 Myogenic and nonmyogenic cells differentially express proteinases, Hsc/Hsp70, and BAG-1 during skeletal muscle regeneration. Am J Physiol Endocrinol Metab 285 E206 E215 12791605
  37. [42]Chen SE Jin B Li YP 2007 TNF-alpha regulates myogenesis and muscle regeneration by activating p38 MAPK. Am J Physiol Cell Physiol 292 C1660 C1671 17151142 PMC3099536
  38. [43]Nieto-Vazquez I Fernandez-Veledo S Kramer DK Vila-Bedmar R Garcia-Guerra L 2008 Insulin resistance associated to obesity: the link TNF-alpha. Arch Physiol Biochem 114 183 194 18629684
  39. [44]Dehoux M Gobier C Lause P Bertrand L Ketelslegers JM 2007 IGF-I does not prevent myotube atrophy caused by proinflammatory cytokines despite activation of Akt/Foxo and GSK-3beta pathways and inhibition of atrogin-1 mRNA. Am J Physiol Endocrinol Metab 292 E145 E150 16926385
  40. [45]Layne MD Farmer SR 1999 Tumor necrosis factor-alpha and basic fibroblast growth factor differentially inhibit the insulin-like growth factor-I induced expression of myogenin in C2C12 myoblasts. Exp Cell Res 249 177 187 10328964
  41. [46]Costelli P Muscaritoli M Bossola M Penna F Reffo P 2006 IGF-1 is downregulated in experimental cancer cachexia. Am J Physiol Regul Integr Comp Physiol 291 R674 R683 16614058
  42. [47]Frost RA Nystrom GJ Lang CH 2003 Tumor necrosis factor-alpha decreases insulin-like growth factor-I messenger ribonucleic acid expression in C2C12 myoblasts via a Jun N-terminal kinase pathway. Endocrinology 144 1770 1779 12697682
  43. [48]Naro F De Arcangelis V Sette C Ambrosio C Komati H 2003 A bimodal modulation of the cAMP pathway is involved in the control of myogenic differentiation in l6 cells. J Biol Chem 278 49308 49315 14506285
  44. [49]Olguin HC Yang Z Tapscott SJ Olwin BB 2007 Reciprocal inhibition between Pax7 and muscle regulatory factors modulates myogenic cell fate determination. J Cell Biol 177 769 779 17548510 PMC2064278
  45. [50]Oustanina S Hause G Braun T 2004 Pax7 directs postnatal renewal and propagation of myogenic satellite cells but not their specification. EMBO J 23 3430 3439 15282552 PMC514519
  46. [52]Pelosi L Giacinti C Nardis C Borsellino G Rizzuto E 2007 Local expression of IGF-1 accelerates muscle regeneration by rapidly modulating inflammatory cytokines and chemokines. FASEB J 21 1393 1402 17264161
  47. [53]Cohn RD Campbell KP 2000 Molecular basis of muscular dystrophies. Muscle Nerve 23 1456 1471 11003781
  48. [54]Setsuta K Seino Y Kitahara Y Arau M Ohbayashi T 2008 Elevated levels of both cardiomyocyte membrane and myofibril damage markers predict adverse outcomes in patients with chronic heart failure. Circ J 72 569 574 18362427
  49. [55]Decramer M 2001 Respiratory muscles in COPD: regulation of trophical status. Verh K Acad Geneeskd Belg 63 577 602 11813511
  50. [56]Reid MB Lannergren J Westerblad H 2002 Respiratory and limb muscle weakness induced by tumor necrosis factor-alpha: involvement of muscle myofilaments. Am J Respir Crit Care Med 166 479 484 12186824
  51. [57]Supinski GS Callahan LA 2006 Caspase activation contributes to endotoxin-induced diaphragm weakness. J Appl Physiol 100 1770 1777 16484358
  52. [58]Irintchev A Zweyer M Wernig A 1997 Impaired functional and structural recovery after muscle injury in dystrophic mdx mice. Neuromuscul Disord 7 117 125 9131653
  53. [59]Ishizaki Y Jacobson MD Raff MC 1998 A role for caspases in lens fiber differentiation. J Cell Biol 140 153 158 9425163 PMC2132591
  54. [60]Sordet O Rebe C Plenchette S Zermati Y Hermine O 2002 Specific involvement of caspases in the differentiation of monocytes into macrophages. Blood 100 4446 4453 12393560
  55. [61]Fujita J Crane AM Souza MK Dejosez M Kyba M 2008 Caspase activity mediates the differentiation of embryonic stem cells. Cell Stem Cell 2 595 601 18522852 PMC2494585
  56. [62]Mosser DD Caron AW Bourget L Meriin AB Sherman MY 2000 The chaperone function of hsp70 is required for protection against stress-induced apoptosis. Mol Cell Biol 20 7146 7159 10982831 PMC86268
  57. [63]Kojima A Goto K Morioka S Naito T Akema T 2007 Heat stress facilitates the regeneration of injured skeletal muscle in rats. J Orthop Sci 12 74 82 17260121
  58. [64]Kayani AC Close GL Broome CS Jackson MJ McArdle A 2008 Enhanced recovery from contraction-induced damage in skeletal muscles of old mice following treatment with the heat shock protein inducer 17-(allylamino)-17-demethoxygeldanamycin. Rejuvenation Res 11 1021 1030 19086912
  59. [65]Riederer I Negroni E Bigot A Bencze M Di SJ Aamiri A 2008 Heat shock treatment increases engraftment of transplanted human myoblasts into immunodeficient mice. Transplant Proc 40 624 630 18374147
  60. [66]Yaffe D 1968 Retention of differentiation potentialities during prolonged cultivation of myogenic cells. Proc Natl Acad Sci U S A 61 477 483 5245982 PMC225183
  61. [67]Jaattela M Wissing D Bauer PA Li GC 1992 Major heat shock protein hsp70 protects tumor cells from tumor necrosis factor cytotoxicity. EMBO J 11 3507 3512 1396553 PMC556808
  62. [68]Labarca C Paigen K 1980 A simple, rapid, and sensitive DNA assay procedure. Anal Biochem 102 344 352 6158890
  63. [69]Ostrovsky O Bengal E 2003 The mitogen-activated protein kinase cascade promotes myoblast cell survival by stabilizing the cyclin-dependent kinase inhibitor, p21WAF1 protein. J Biol Chem 278 21221 21231 12637563
  64. [70]Del PZ Musaro A Rizzuto E 2008 Measuring mechanical properties, including isotonic fatigue, of fast and slow MLC/mIgf-1 transgenic skeletal muscle. Ann Biomed Eng 36 1281 1290 18415017
  65. [71]Denti MA Incitti T Sthandier O Nicoletti C De Angelis FG 2008 Long-term benefit of adeno-associated virus/antisense-mediated exon skipping in dystrophic mice. Hum Gene Ther 19 601 608 18500943
  66. [72]Albertini MC Accorsi A Teodori L Pierfelici L Uguccioni F 2006 Use of multiparameter analysis for Vibrio alginolyticus viable but nonculturable state determination. Cytometry A 69 260 265 16528721
  67. [73]Albertini MC Teodori L Piatti E Piacentini MP Accorsi A 2003 Automated analysis of morphometric parameters for accurate definition of erythrocyte cell shape. Cytometry A 52 12 18 12596247
  68. [74]Anderson TW 1984 An Introduction to Multivariate Statistical Analysis New York Wiley

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Authors
Moresi, V., Garcia-Alvarez, G., Pristerà, A., Rizzuto, E., Albertini, M. C., Rocchi, M., Marazzi, G., Sassoon, D., Adamo, S., & Coletti, D.
Affiliations
  • Sapienza University of Rome (IT)
  • University of Urbino (IT)
  • Inserm (FR)
Corresponding author
Adamo, Sergio
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2009-05-18
Volume
4
Issue
5
Pages
e5570
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0005570
PMC
PMC2680623
OpenAlex
W2061779956
Cited by
60
References
5
Citations by year
2026: 1 · 2025: 1 · 2024: 1 · 2023: 4 · 2022: 1 · 2021: 2 · 2020: 3 · 2019: 6 · 2018: 8 · 2016: 5 · 2015: 2 · 2014: 6 · 2013: 4 · 2012: 2
FWCI
2.15
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • IRIS Research product catalog (Sapienza University of Rome) (submittedVersion, cc-by)
  • CINECA IRIS Institutional Research information system (University of Urbino) (submittedVersion)
Funders
  • Muscular Dystrophy Association
  • Kræftens Bekæmpelse
  • Università degli Studi di Padova
  • Agenzia Spaziale Italiana
  • National Institutes of Health (Hsp70, CA80058)
  • Directorate for Biological Sciences
  • National Cancer Institute (CA80058-06, CA 80058, P01CA080058)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Heat shock proteins research
  • Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Meat and Animal Product Quality
Keywords
skeletal muscle regeneration, caspase activation, TNF-α, HSP70, myogenesis, muscle atrophy, muscle fatigue, tetanic force, cytokine signaling, myogenic cells, protein-protein interaction
MeSH terms
Animals, Arginine Vasopressin, Cell Differentiation, Cell Line, Enzyme Activation, Female, Hemostatics, Immunohistochemistry, Tumor Necrosis Factor-alpha, Blotting, Western, Gene Expression, Electroporation, Muscle, Skeletal, HSP70 Heat-Shock Proteins, Reverse Transcriptase Polymerase Chain Reaction, Caspases, Immunoprecipitation, Mice, Rats, Kruppel-Like Transcription Factors

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