Pro-inflammatory mediation of myoblast proliferation

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Otis, Jeffrey S ^d   Niccoli, Sarah ^a   Hawdon, Nicole ^a   Sarvas, Jessica L ^a,b   Frye, Melinda A ^c   Chicco, Adam J ^c   Lees, Simon J ^a,b,c  

^a NORTHERN ONTARIO SCHOOL OF MEDICINE   (Canada)

^b LAKEHEAD UNIVERSITY   (Canada)

^c Department of Ecosystem Science and Sustainability   (United States)

^d GEORGIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; MALE; MITOGENESIS; MOUSE; MUSCLE INJURY; MYOBLAST; MYOSITIS; NONHUMAN; PROTEIN EXPRESSION; RAT; SKELETAL MUSCLE; SKELETAL MUSCLE SATELLITE CELL;

ANIMALS; CELL LINE; CELL PROLIFERATION; CELLS, CULTURED; INTERLEUKIN-1BETA; INTERLEUKIN-6; MALE; MICE; MYOBLASTS; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84898623277     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0092363     Document Type: Article

References (100)

1. Mauro A (1961) Satellite cell of skeletal muscle fibers. JBiophysBiochemCytol 9: 493-495.
2. Hawke TJ, Garry DJ (2001) Myogenic satellite cells: physiology to molecular biology. J Appl Physiol 91: 534-551. (Pubitemid 32681081)
3. Tedesco FS, Dellavalle A, Diaz-Manera J, Messina G, Cossu G (2010) Repairing skeletal muscle: regenerative potential of skeletal muscle stem cells. J Clin Invest 120: 11-19.
4. Parise G, McKinnell IW, Rudnicki MA (2008) Muscle satellite cell and atypical myogenic progenitor response following exercise. Muscle Nerve 37: 611-619. (Pubitemid 351590552)
5. Sambasivan R, Yao R, Kissenpfennig A, Van Wittenberghe L, Paldi A, et al. (2011) Pax7-expressing satellite cells are indispensable for adult skeletal muscle regeneration. Development 138: 3647-3656.
6. Murphy MM, Lawson JA, Mathew SJ, Hutcheson DA, Kardon G (2011) Satellite cells, connective tissue fibroblasts and their interactions are crucial for muscle regeneration. Development 138: 3625-3637.
7. Lepper C, Partridge TA, Fan CM (2011) An absolute requirement for Pax7-positive satellite cells in acute injury-induced skeletal muscle regeneration. Development 138: 3639-3646.
8. Fielding RA, Manfredi TJ, Ding W, Fiatarone MA, Evans WJ, et al. (1993) Acute phase response in exercise. III. Neutrophil and IL-1 beta accumulation in skeletal muscle. Am J Physiol 265: R166-172. (Pubitemid 23224764)
9. Yin H, Price F, Rudnicki MA (2013) Satellite cells and the muscle stem cell niche. Physiol Rev 93: 23-67.
10. Lolmede K, Campana L, Vezzoli M, Bosurgi L, Tonlorenzi R, et al. (2009) Inflammatory and alternatively activated human macrophages attract vesselassociated stem cells, relying on separate HMGB1- and MMP-9-dependent pathways. J Leukoc Biol 85: 779-787.
11. Arnold L, Henry A, Poron F, Baba-Amer Y, van Rooijen N, et al. (2007) Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J Exp Med 204: 1057-1069. (Pubitemid 46798150)
12. Warren GL, Hulderman T, Jensen N, McKinstry M, Mishra M, et al. (2002) Physiological role of tumor necrosis factor alpha in traumatic muscle injury. FASEB J 16: 1630-1632.
13. Collins RA, Grounds MD (2001) The role of tumor necrosis factor-alpha (TNF-alpha) in skeletal muscle regeneration. Studies in TNF-alpha(-/-) and TNF-alpha(-/-)/LT-alpha(-/-) mice. J Histochem Cytochem 49: 989-1001. (Pubitemid 32675006)
14. Saclier M, Yacoub-Youssef H, Mackey AL, Arnold L, Ardjoune H, et al. (2013) Differentially activated macrophages orchestrate myogenic precursor cell fate during human skeletal muscle regeneration. Stem Cells 31: 384-396.
15. Almekinders LC, Gilbert JA (1986) Healing of experimental muscle strains and the effects of nonsteroidal antiinflammatory medication. Am J Sports Med 14: 303-308. (Pubitemid 16077336)
16. Mishra DK, Friden J, Schmitz MC, Lieber RL (1995) Anti-inflammatory medication after muscle injury. A treatment resulting in short-term improvement but subsequent loss of muscle function. J Bone Joint Surg Am 77: 1510-1519.
17. Barlow Y, Willoughby J (1992) Pathophysiology of soft tissue repair. Br Med Bull 48: 698-711.
18. Merrick MA (2002) Secondary injury after musculoskeletal trauma: a review and update. J Athl Train 37: 209-217. (Pubitemid 34693422)
19. Mikkelsen UR, Langberg H, Helmark IC, Skovgaard D, Andersen LL, et al. (2009) Local NSAID infusion inhibits satellite cell proliferation in human skeletal muscle after eccentric exercise. J Appl Physiol 107: 1600-1611.
20. Mendias CL, Tatsumi R, Allen RE (2004) Role of cyclooxygenase-1 and -2 in satellite cell proliferation, differentiation, and fusion. Muscle Nerve 30: 497-500. (Pubitemid 39288155)
21. Cornelison DD (2008) Context matters: in vivo and in vitro influences on muscle satellite cell activity. J Cell Biochem 105: 663-669.
22. Onozaki K (2013) [Interluekin-1: from regulation of cell proliferation to chronic inflammatory diseases]. Yakugaku Zasshi 133: 645-660.
23. Berger A (2000) Th1 and Th2 responses: what are they? BMJ 321: 424.
24. Allavena P, Sica A, Solinas G, Porta C, Mantovani A (2008) The inflammatory micro-environment in tumor progression: the role of tumor-associated macrophages. Crit Rev Oncol Hematol 66: 1-9. (Pubitemid 351324128)
25. Li W, Moylan JS, Chambers MA, Smith J, Reid MB (2009) Interleukin-1 stimulates catabolism in C2C12 myotubes. Am J Physiol Cell Physiol 297: C706-714.
26. Libby P, Warner SJ, Friedman GB (1988) Interleukin 1: a mitogen for human vascular smooth muscle cells that induces the release of growth-inhibitory prostanoids. J Clin Invest 81: 487-498. (Pubitemid 18075245)
27. Tidball JG (1995) Inflammatory cell response to acute muscle injury. Med Sci Sports Exerc 27: 1022-1032.
28. Spangelo BL, Farrimond DD, Pompilius M, Bowman KL (2000) Interleukin-1 beta and thymic peptide regulation of pituitary and glial cell cytokine expression and cellular proliferation. Ann N Y Acad Sci 917: 597-607.
29. Werner S, Smola H (2001) Paracrine regulation of keratinocyte proliferation and differentiation. Trends Cell Biol 11: 143-146. (Pubitemid 32295911)
30. Cantini M, Massimino ML, Rapizzi E, Rossini K, Catani C, et al. (1995) Human satellite cell proliferation in vitro is regulated by autocrine secretion of IL-6 stimulated by a soluble factor(s) released by activated monocytes. Biochem Biophys Res Commun 216: 49-53.
31. Wang X, Wu H, Zhang Z, Liu S, Yang J, et al. (2008) Effects of interleukin-6, leukemia inhibitory factor, and ciliary neurotrophic factor on the proliferation and differentiation of adult human myoblasts. Cell Mol Neurobiol 28: 113-124.
32. Serrano AL, Baeza-Raja B, Perdiguero E, Jardi M, Munoz-Canoves P (2008) Interleukin-6 is an essential regulator of satellite cell-mediated skeletal muscle hypertrophy. Cell Metab 7: 33-44.
33. Zhang C, Li Y, Wu Y, Wang L, Wang X, et al. (2013) Interleukin-6/signal transducer and activator of transcription 3 (STAT3) pathway is essential for macrophage infiltration and myoblast proliferation during muscle regeneration. J Biol Chem 288: 1489-1499.
34. Langen RC, Schols AM, Kelders MC, Wouters EF, Janssen-Heininger YM (2001) Inflammatory cytokines inhibit myogenic differentiation through activation of nuclear factor-kappaB. FASEB J 15: 1169-1180. (Pubitemid 32436302)
35. Luo G, Hershko DD, Robb BW, Wray CJ, Hasselgren PO (2003) IL-1beta stimulates IL-6 production in cultured skeletal muscle cells through activation of MAP kinase signaling pathway and NF-kappa B. Am J Physiol Regul Integr Comp Physiol 284: R1249-1254. (Pubitemid 36457567)
36. Prelovsek O, Mars T, Jevsek M, Podbregar M, Grubic Z (2006) High dexamethasone concentration prevents stimulatory effects of TNF-alpha and LPS on IL-6 secretion from the precursors of human muscle regeneration. Am J Physiol Regul Integr Comp Physiol 291: R1651-1656. (Pubitemid 44904131)
37. Dumke BR, Lees SJ (2011) Age-related impairment of T cell-induced skeletal muscle precursor cell function. American journal of physiology Cell physiology.
38. Rathbone CR, Booth FW, Lees SJ (2008) FoxO3a preferentially induces p27Kip1 expression while impairing muscle precursor cell-cycle progression. Muscle & nerve 37: 84-89.
39. Jump SS, Childs TE, Zwetsloot KA, Booth FW, Lees SJ (2009) Fibroblast growth factor 2-stimulated proliferation is lower in muscle precursor cells from old rats. Exp Physiol 94: 739-748.
40. Lees SJ, Rathbone CR, Booth FW (2006) Age-associated decrease in muscle precursor cell differentiation. Am J Physiol Cell Physiol 290: C609-C615.
41. Rathbone CR, Booth FW, Lees SJ (2009) Sirt1 increases skeletal muscle precursor cell proliferation. EurJCell Biol 88: 35-44.
42. Lees SJ, Childs TE, Booth FW (2008) p21(Cip1) expression is increased in ambient oxygen, compared to estimated physiological (5%) levels in rat muscle precursor cell culture. Cell Prolif 41: 193-207. (Pubitemid 351367489)
43. Lees SJ, Zwetsloot KA, Booth FW (2009) Muscle precursor cells isolated from aged rats exhibit an increased tumor necrosis factor- alpha response. Aging Cell 8: 26-35.
44. Lees SJ, Childs TE, Booth FW (2008) Age-Dependent FOXO Regulation Of p27Kip1 Expression Via A Conserved Binding Motif In Rat Muscle Precursor Cells. AmJPhysiol Cell Physiol.
45. O'Connor RS, Mills ST, Jones KA, Ho SN, Pavlath GK (2007) A combinatorial role for NFAT5 in both myoblast migration and differentiation during skeletal muscle myogenesis. J Cell Sci 120: 149-159. (Pubitemid 46206657)
46. Otis JS, Guidot DM (2009) Procysteine stimulates expression of key anabolic factors and reduces plantaris atrophy in alcohol-fed rats. Alcohol Clin Exp Res 33: 1450-1459.
47. Otis JS, Brown LA, Guidot DM (2007) Oxidant-induced atrogin-1 and transforming growth factor-beta1 precede alcohol-related myopathy in rats. Muscle Nerve 36: 842-848. (Pubitemid 350246933)
48. Otis JS, Guidot DM (2010) Procysteine increases alcohol-depleted glutathione stores in rat plantaris following a period of abstinence. Alcohol Alcohol 45: 495-500.
49. Otis JS, Ashikhmin YI, Brown LA, Guidot DM (2008) Effect of HIV-1-related protein expression on cardiac and skeletal muscles from transgenic rats. AIDS Res Ther 5: 8.
50. Clary CR, Guidot DM, Bratina MA, Otis JS (2011) Chronic alcohol ingestion exacerbates skeletal muscle myopathy in HIV-1 transgenic rats. AIDS Res Ther 8: 30.
51. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408. (Pubitemid 34164012)
52. Tidball JG, Villalta SA (2010) Regulatory interactions between muscle and the immune system during muscle regeneration. Am J Physiol Regul Integr Comp Physiol 298: R1173-1187.
53. Warren GL, Hulderman T, Mishra D, Gao X, Millecchia L, et al. (2005) Chemokine receptor CCR2 involvement in skeletal muscle regeneration. FASEB J 19: 413-415. (Pubitemid 40316534)
54. Schertzer JD, Lynch GS (2006) Comparative evaluation of IGF-I gene transfer and IGF-I protein administration for enhancing skeletal muscle regeneration after injury. Gene Ther 13: 1657-1664. (Pubitemid 44774210)
55. Nozaki M, Ota S, Terada S, Li Y, Uehara K, et al. (2012) Timing of the administration of suramin treatment after muscle injury. Muscle Nerve 46: 70-79.
56. Krause MP, Moradi J, Coleman SK, D'Souza DM, Liu C, et al. (2013) A novel GFP reporter mouse reveals Mustn1 expression in adult regenerating skeletal muscle, activated satellite cells and differentiating myoblasts. Acta Physiol (Oxf) 208: 180-190.
57. Griffin CA, Kafadar KA, Pavlath GK (2009) MOR23 promotes muscle regeneration and regulates cell adhesion and migration. Dev Cell 17: 649-661.
58. Dekeyser GJ, Clary CR, Otis JS (2013) Chronic alcohol ingestion delays skeletal muscle regeneration following injury. Regenerative Medicine Research 1: 1-12.
59. Jozsi AC, Dupont-Versteegden EE, Taylor-Jones JM, Evans WJ, Trappe TA, et al. (2000) Aged human muscle demonstrates an altered gene expression profile consistent with an impaired response to exercise. Mech Ageing Dev 120: 45-56.
60. Przybyla B, Gurley C, Harvey JF, Bearden E, Kortebein P, et al. (2006) Aging alters macrophage properties in human skeletal muscle both at rest and in response to acute resistance exercise. Exp Gerontol 41: 320-327.
61. Hamada K, Vannier E, Sacheck JM, Witsell AL, Roubenoff R (2005) Senescence of human skeletal muscle impairs the local inflammatory cytokine response to acute eccentric exercise. FASEB J 19: 264-266. (Pubitemid 40189276)
62. Trenerry MK, Carey KA, Ward AC, Farnfield MM, Cameron-Smith D (2008) Exercise-induced activation of STAT3 signaling is increased with age. Rejuvenation Res 11: 717-724.
63. Frost RA, Nystrom GJ, Lang CH (2003) Lipopolysaccharide and proinflammatory cytokines stimulate interleukin-6 expression in C2C12 myoblasts: role of the Jun NH2-terminal kinase. Am J Physiol Regul Integr Comp Physiol 285: R1153-1164. (Pubitemid 37296368)
64. Frost RA, Nystrom GJ, Lang CH (2002) Lipopolysaccharide regulates proinflammatory cytokine expression in mouse myoblasts and skeletal muscle. Am J Physiol Regul Integr Comp Physiol 283: R698-709. (Pubitemid 34951624)
65. Bethea JR, Gillespie GY, Benveniste EN (1992) Interleukin-1 beta induction of TNF-alpha gene expression: involvement of protein kinase C. J Cell Physiol 152: 264-273.
66. Collart MA, Baeuerle P, Vassalli P (1990) Regulation of tumor necrosis factor alpha transcription in macrophages: involvement of four kappa B-like motifs and of constitutive and inducible forms of NF-kappa B. Mol Cell Biol 10: 1498-1506.
67. Ozes ON, Mayo LD, Gustin JA, Pfeffer SR, Pfeffer LM, et al. (1999) NF-kappaB activation by tumour necrosis factor requires the Akt serine-threonine kinase. Nature 401: 82-85.
68. Jove M, Planavila A, Sanchez RM, Merlos M, Laguna JC, et al. (2006) Palmitate induces tumor necrosis factor-alpha expression in C2C12 skeletal muscle cells by a mechanism involving protein kinase C and nuclear factor-kappaB activation. Endocrinology 147: 552-561. (Pubitemid 43004310)
69. Jove M, Planavila A, Laguna JC, Vazquez-Carrera M (2005) Palmitate-induced interleukin 6 production is mediated by protein kinase C and nuclear-factor kappaB activation and leads to glucose transporter 4 down-regulation in skeletal muscle cells. Endocrinology 146: 3087-3095. (Pubitemid 41002818)
70. Boyd JH, Divangahi M, Yahiaoui L, Gvozdic D, Qureshi S, et al. (2006) Tolllike receptors differentially regulate CC and CXC chemokines in skeletal muscle via NF-kappaB and calcineurin. Infect Immun 74: 6829-6838. (Pubitemid 44913158)
71. Li YP, Lecker SH, Chen Y, Waddell ID, Goldberg AL, et al. (2003) TNF-alpha increases ubiquitin-conjugating activity in skeletal muscle by up-regulating UbcH2/E220k. FASEB J 17: 1048-1057. (Pubitemid 36676391)
72. Soltow QA, Lira VA, Betters JL, Long JH, Sellman JE, et al. (2010) Nitric oxide regulates stretch-induced proliferation in C2C12 myoblasts. J Muscle Res Cell Motil 31: 215-225.
73. Peake J, Della Gatta P, Cameron-Smith D (2010) Aging and its effects on inflammation in skeletal muscle at rest and following exercise-induced muscle injury. Am J Physiol Regul Integr Comp Physiol 298: R1485-1495.
74. Sung MS, Lee EG, Jeon HS, Chae HJ, Park SJ, et al. (2012) Quercetin inhibits IL-1beta-induced proliferation and production of MMPs, COX-2, and PGE2 by rheumatoid synovial fibroblast. Inflammation 35: 1585-1594.
75. Catanzaro R, Marotta F, Jain S, Rastmanesh R, Allegri F, et al. (2012) Beneficial effect of a sturgeon-based bioactive compound on gene expression of tumor necrosis factor-alpha, matrix metalloproteinases and type-10 collagen in human chondrocytes. J Biol Regul Homeost Agents 26: 337-345.
76. de Almeida P, Tomazoni SS, Frigo L, de Carvalho PD, Vanin AA, et al. (2013) What is the best treatment to decrease pro-inflammatory cytokine release in acute skeletal muscle injury induced by trauma in rats: low-level laser therapy, diclofenac, or cryotherapy? Lasers Med Sci.
77. Khan I, Blennerhassett MG, Kataeva GV, Collins SM (1995) Interleukin 1 beta induces the expression of interleukin 6 in rat intestinal smooth muscle cells. Gastroenterology 108: 1720-1728.
78. McGee DW, Beagley KW, Aicher WK, McGhee JR (1993) Transforming growth factor-beta and IL-1 beta act in synergy to enhance IL-6 secretion by the intestinal epithelial cell line, IEC-6. J Immunol 151: 970-978. (Pubitemid 23215763)
79. Parikh AA, Salzman AL, Fischer JE, Szabo C, Hasselgren PO (1997) Interleukin-1 beta and interferon-gamma regulate interleukin-6 production in cultured human intestinal epithelial cells. Shock 8: 249-255. (Pubitemid 127654334)
80. Sironi M, Breviario F, Proserpio P, Biondi A, Vecchi A, et al. (1989) IL-1 stimulates IL-6 production in endothelial cells. J Immunol 142: 549-553. (Pubitemid 19039975)
81. Chabaud M, Fossiez F, Taupin JL, Miossec P (1998) Enhancing effect of IL-17 on IL-1-induced IL-6 and leukemia inhibitory factor production by rheumatoid arthritis synoviocytes and its regulation by Th2 cytokines. J Immunol 161: 409-414. (Pubitemid 28285549)
82. Elias JA, Lentz V (1990) IL-1 and tumor necrosis factor synergistically stimulate fibroblast IL-6 production and stabilize IL-6 messenger RNA. J Immunol 145: 161-166. (Pubitemid 20217396)
83. McKay BR, De Lisio M, Johnston AP, O'Reilly CE, Phillips SM, et al. (2009) Association of interleukin-6 signalling with the muscle stem cell response following muscle-lengthening contractions in humans. PLoS One 4: e6027.
84. Toth KG, McKay BR, De Lisio M, Little JP, Tarnopolsky MA, et al. (2011) IL-6 induced STAT3 signalling is associated with the proliferation of human muscle satellite cells following acute muscle damage. PLoS One 6: e17392.
85. Knofler M, Kiss H, Mosl B, Egarter C, Husslein P (1997) Interleukin-1 stimulates tumor necrosis factor-alpha (TNF-alpha) release from cytotrophoblastic BeWo cells independently of induction of the TNF-alpha mRNA. FEBS Lett 405: 213-218. (Pubitemid 27136513)
86. Isumi Y, Kubo A, Katafuchi T, Kangawa K, Minamino N (1999) Adrenomedullin suppresses interleukin-1beta-induced tumor necrosis factoralpha production in Swiss 3T3 cells. FEBS Lett 463: 110-114. (Pubitemid 30001728)
87. Cumberbatch M, Singh M, Dearman RJ, Young HS, Kimber I, et al. (2006) Impaired Langerhans cell migration in psoriasis. J Exp Med 203: 953-960.
88. Kafoury RM, Madden MC (2005) Diesel exhaust particles induce the over expression of tumor necrosis factor-alpha (TNF-alpha) gene in alveolar macrophages and failed to induce apoptosis through activation of nuclear factor-kappaB (NF-kappaB). Int J Environ Res Public Health 2: 107-113. (Pubitemid 40965107)
89. Baeuerle PA (1998) Pro-inflammatory signaling: last pieces in the NF-kappaB puzzle? Curr Biol 8: R19-22.
90. Chevrel G, Granet C, Miossec P (2005) Contribution of tumour necrosis factor alpha and interleukin (IL) 1beta to IL6 production, NF-kappaB nuclear translocation, and class I MHC expression in muscle cells: in vitro regulation with specific cytokine inhibitors. Ann Rheum Dis 64: 1257-1262. (Pubitemid 41206239)
91. Turner NA, Das A, Warburton P, O'Regan DJ, Ball SG, et al. (2009) Interleukin-1alpha stimulates proinflammatory cytokine expression in human cardiac myofibroblasts. Am J Physiol Heart Circ Physiol 297: H1117-1127.
92. Trendelenburg AU, Meyer A, Jacobi C, Feige JN, Glass DJ (2012) TAK-1/p38/nNFkappaB signaling inhibits myoblast differentiation by increasing levels of Activin A. Skelet Muscle 2: 3.
93. Raingeaud J, Gupta S, Rogers JS, Dickens M, Han J, et al. (1995) Proinflammatory cytokines and environmental stress cause p38 mitogen-activated protein kinase activation by dual phosphorylation on tyrosine and threonine. J Biol Chem 270: 7420-7426.
94. Lee JG, Heur M (2013) Interleukin-1beta enhances cell migration through AP-1 and NF-kappaB pathway-dependent FGF2 expression in human corneal endothelial cells. Biol Cell 105: 175-189.
95. Lee TS, Song HJ, Jeong JH, Min YS, Shin CY, et al. (2006) IL-1beta activates p44/42 and p38 mitogen-activated protein kinases via different pathways in cat esophageal smooth muscle cells. World J Gastroenterol 12: 716-722. (Pubitemid 43380753)
96. Zhan M, Jin B, Chen SE, Reecy JM, Li YP (2007) TACE release of TNF-alpha mediates mechanotransduction-induced activation of p38 MAPK and myogenesis. J Cell Sci 120: 692-701. (Pubitemid 46437903)
97. Baeza-Raja B, Munoz-Canoves P (2004) p38 MAPK-induced nuclear factorkappaB activity is required for skeletal muscle differentiation: role of interleukin-6. Mol Biol Cell 15: 2013-2026. (Pubitemid 38401847)
98. Hayakawa M, Miyashita H, Sakamoto I, Kitagawa M, Tanaka H, et al. (2003) Evidence that reactive oxygen species do not mediate NF-kappaB activation. EMBO J 22: 3356-3366. (Pubitemid 36834865)
99. Schreck R, Meier B, Mannel DN, Droge W, Baeuerle PA (1992) Dithiocarbamates as potent inhibitors of nuclear factor kappa B activation in intact cells. J Exp Med 175: 1181-1194.
100. Frangogiannis NG (2008) The immune system and cardiac repair. Pharmacol Res 58: 88-111.