P38 MAPK signaling in postnatal tendon growth and remodeling

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Schwartz, Andrew J ^a   Sarver, Dylan C ^a   Sugg, Kristoffer B ^a   Dzierzawski, Justin T ^a   Gumucio, Jonathan P ^a   Mendias, Christopher L ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYALURONIC ACID; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE P38; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; IMIDAZOLE DERIVATIVE; PYRIDINE DERIVATIVE;

ACHILLES TENDON; ANIMAL TISSUE; ARTICLE; BIOCHEMICAL ANALYSIS; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; EXTRACELLULAR MATRIX; HISTOLOGY; IN VIVO STUDY; MALE; MUSCULOSKELETAL FUNCTION; NONHUMAN; PERICYTE; PLANTARIS MUSCLE; POSTNATAL GROWTH; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; TENDON GROWTH; TENDON REMODELING; TISSUE EXPANSION; ANIMAL; ANTAGONISTS AND INHIBITORS; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; MACROPHAGE; METABOLISM; NEUTROPHIL; PHYSIOLOGY; SPRAGUE DAWLEY RAT; TENDON;

ANIMALIA; RATTUS;

ANIMALS; CELL PROLIFERATION; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION, ENZYMOLOGIC; IMIDAZOLES; INTERLEUKIN-6; MACROPHAGES; MALE; MAP KINASE SIGNALING SYSTEM; NEUTROPHILS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PYRIDINES; RATS; RATS, SPRAGUE-DAWLEY; TENDONS;

EID: 84929493253     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0120044     Document Type: Article

References (56)

1. Davis ME, Gumucio JP, Sugg KB, Bedi A, Mendias CL. MMP inhibition as a potential method to augment the healing of skeletal muscle and tendon extracellular matrix. J Appl Physiol. 2013; 115: 884-891. doi: 10.1152/japplphysiol.00137.2013 PMID: 23640595
2. Kjaer M, Langberg H, Heinemeier K, Bayer ML, Hansen M, Holm S, et al. From mechanical loading to collagen synthesis, structural changes and function in human tendon. Scand J Med Sci Spor. 2009; 19: 500-510. doi: 10.1111/j.1600-0838.2009.00986.x PMID: 19706001
3. Pryce BA, Watson SS, Murchison ND, Staverosky JA, Dunker N, Schweitzer R. Recruitment and maintenance of tendon progenitors by TGFbeta signaling are essential for tendon formation. Development. 2009; 136: 1351-1361. doi: 10.1242/dev.027342 PMID: 19304887
4. Murchison ND, Price BA, Conner DA, Keene DR, Olson EN, Tabin CJ, et al. Regulation of tendon differentiation by scleraxis distinguishes force-transmitting tendons from muscle-anchoring tendons. Development. 2007; 134: 2697-2708. PMID: 17567668
5. Lorda-Diez CI, Montero JA, Martinez-Cue C, Garcia-Porrero JA, Hurle JM. Transforming growth factors beta coordinate cartilage and tendon differentiation in the developing limb mesenchyme. J Biol Chem. 2009; 284: 29988-29996. doi: 10.1074/jbc.M109.014811 PMID: 19717568
6. Maeda T, Sakabe T, Sunaga A, Sakai K, Rivera AL, Keene DR, et al. Conversion of mechanical force into TGF-beta-mediated biochemical signals. Curr Biol. 2009; 21: 933-941.
7. Mendias CL, Bakhurin KI, Faulkner JA. Tendons of myostatin-deficient mice are small, brittle, and hypocellular. P Natl Acad Sci USA. 2009; 105: 388-393.
8. Moustakas A, Heldin CH. The regulation of TGFbeta signal transduction. Development. 2009; 136: 3699-3714. doi: 10.1242/dev.030338 PMID: 19855013
9. Gumucio JP, Phan AC, Ruehlmann DG, Noah AC, Mendias CL. Synergist ablation induces rapid tendon growth through the synthesis of a neotendon matrix. J Appl Physiol. 2014; 117: 1287-1291. doi: 10.1152/japplphysiol.00720.2014 PMID: 25277742
10. Mendias CL, Gumucio JP, Bakhurin KI, Lynch EB, Brooks SV. Physiological loading of tendons induces scleraxis expression in epitenon fibroblasts. J Orthopaed Res. 2012; 30: 606-612.
11. Heinemeier K, Langberg H, Olesen JL, Kjaer M. Role of TGF-beta1 in relation to exercise-induced type I collagen synthesis in human tendinous tissue. J Appl Physiol. 2003; 95: 2390-2397. PMID: 12923117
12. Calve S, Isaac J, Gumucio JP, Mendias CL. Hyaluronic acid, HAS1, and HAS2 are significantly upregulated during muscle hypertrophy. Am J Physiol Cell Physiol. 2012; 303: 577-588.
13. McCarthy JJ, Mula J, Miyazaki M, Erfani R, Garrison K, Farooqui AB, et al. Effective fiber hypertrophy in satellite cell-depleted skeletal muscle. Development. 2011; 138: 3657-3666. doi: 10.1242/dev. 068858 PMID: 21828094
14. Hamilton DL, Philp A, MacKenzie MG, Patton A, Towler MC, Gallagher IJ, et al. Molecular brakes regulating mTORC1 activation in skeletal muscle following synergist ablation. Am J Physiol Endocrinol Metab. 2014; 307: 365-373.
15. Fry CS, Lee JD, Jackson JR, Kirby TJ, Stasko SA, Liu H, et al. Regulation of the muscle fiber microenvironment by activated satellite cells during hypertrophy. FASEB J. 2014; 28: 1654-1665. doi: 10.1096/fj. 13-239426 PMID: 24376025
16. Perez-Schindler J, Summermatter S, Santos G, Zorzato F, Handschin C. The transcriptional coactivator PGC-1alpha is dispensable for chronic overload-induced skeletal muscle hypertrophy and metabolic remodeling. P Natl Acad Sci USA. 2013; 110: 20314-20319. doi: 10.1073/pnas.1312039110 PMID: 24277823
17. Goodman CA, Mabrey DM, Frey JW, Miu MH, Schmidt EK, Pierre P, et al. Novel insights into the regulation of skeletal muscle protein synthesis as revealed by a new nonradioactive in vivo technique. FASEB J. 2011; 25: 1028-1039. doi: 10.1096/fj.10-168799 PMID: 21148113
18. Esser KA, White TP. Mechanical load affects growth and maturation of skeletal muscle grafts. J Appl Physiol. 1995; 78: 30-37. PMID: 7713828
19. Ettema GJ. Elastic and length-force characteristics of the gastrocnemius of the hopping mouse (Notomys alexis) and the rat (Rattus norvegicus). J Exp Biol. 1996; 199: 1277-1285. PMID: 8691113
20. Baud A, Hermsen R, Guryev V, Stridh P, Graham D, McBride MW, et al. Combined sequence-based and genetic mapping analysis of complex traits in outbred rats. Nat Genet. 2013; 45: 767-775. doi: 10. 1038/ng.2644 PMID: 23708188
21. Lee JC, Kassis S, Kumar S, Badger A, Adams JL. p38 mitogen-activated protein kinase inhibitors-mechanisms and therapeutic potentials. Pharmacol Therapeut. 1999; 82: 389-397.
22. Li J, Campanale NV, Liang RJ, Deane JA, Bertram JF, Ricardo SD. Inhibition of p38mitogen-activated protein kinase and transforming growth factor-beta1/Smad signaling pathways modulates the development of fibrosis in adriamycin-induced nephropathy. AmJ Pathol. 2006; 169: 1527-1540. PMID: 17071578
23. Mendias CL, Marcin JE, Calerdon DR, Faulkner JA. Contractile properties of EDL and soleus muscles of myostatin-deficient mice. J Appl Physiol. 2006; 101: 898-905. PMID: 16709649
24. Woessner JF. The determination of hydroxyproline in tissue and protein samples containing small proportions of this imino acid. Arch Biochem Biophys. 1961; 93: 440-447. PMID: 13786180
25. Mendias CL, Gumucio JP, Lynch EB. Mechanical loading and TGF-beta change the expression of multiple miRNAs in tendon fibroblasts. J Appl Physiol. 2012; 113: 56-62. doi: 10.1152/japplphysiol.00301. 2012 PMID: 22539168
26. Sugg KB, Lubardic J, Gumucio JP, Mendias CL. Changes in macrophage phenotype and induction of epithelial-to-mesenchymal transition genes following acute Achilles tenotomy and repair. J Orthopaed Res. 2014; 32: 944-951.
27. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc. 2008; 3: 1101-1108. PMID: 18546601
28. Millar NL, Reilly JH, Kerr SC, Campbell AL, Little KJ, LeachWJ, et al. Hypoxia: a critical regulator of early human tendinopathy. Ann Rheum Dis. 2012; 71: 302-310. doi: 10.1136/ard.2011.154229 PMID: 21972243
29. Itano N, Atsumi F, Sawai T, Yamada Y, Miyaishi O, Senga T, et al. Abnormal accumulation of hyaluronan matrix diminishes contact inhibition of cell growth and promotes cell migration. P Natl Acad Sci USA. 2002; 99: 3609-3614. PMID: 11891291
30. Meran S, Luo DD, Simpson R, Martin J, Wells A, Steadman R, et al. Hyaluronan facilitates transforming growth factor-beta1-dependent proliferation via CD44 and epidermal growth factor receptor interaction. J Biol Chem. 2011; 286: 17618-17630. doi: 10.1074/jbc.M111.226563 PMID: 21454519
31. Abate M, Schiavone C, Salini V. The use of hyaluronic acid after tendon surgery and in tendinopathies. Biomed Res Int. 2014; 783632: 1-6. doi: 10.1155/2014/783632 PMID: 24895610
32. Calve S, Odelberg SJ, Simon HG. A transitional extracellular matrix instructs cell behavior during muscle regeneration. Dev Biol. 2010; 344: 259-271. doi: 10.1016/j.ydbio.2010.05.007 PMID: 20478295
33. Girish KS, Kemparaju K. The magic glue hyaluronan and its eraser hyaluronidase: a biological overview. Life Sci. 2007; 80: 1921-1943. PMID: 17408700
34. Acharya A, Baek ST, Huang G, Eskiocak B, Goetsch S, Sung CY, et al. The bHLH transcription factor Tcf21 is required for lineage-specific EMT of cardiac fibroblast progenitors. Development. 2012; 139: 2139-2149. doi: 10.1242/dev.079970 PMID: 22573622
35. Tan Q, Lui PP, Lee YW. In vivo identity of tendon stem cells and the roles of stem cells in tendon healing. Stem Cells Dev. 2013; 22: 3128-3140. doi: 10.1089/scd.2013.0073 PMID: 23815595
36. Armulik A, Genove G, Betsholtz C. Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev Cell. 2011; 21: 193-215. doi: 10.1016/j.devcel.2011.07.001 PMID: 21839917
37. Birbrair A, Zhang T, Wang ZM, Messi ML, Mintz A, Delbono O. Type-1 pericytes participate in fibrous tissue deposition in aged skeletal muscle. Am J Physiol Cell Physiol. 2013; 305: 1098-1113.
38. Rowe RG, Keena D, Sabeh F, Willis AL, Weiss SJ. Pulmonary fibroblasts mobilize the membranetethered matrix metalloprotease, MT1-MMP, to destructively remodel and invade interstitial type I collagen barriers. Am J Physiol Lung Cell Mol Physiol. 2011; 301: 683-692. doi: 10.1152/ajplung.00187. 2011 PMID: 21840960
39. Eliasson P, Andersson T, Hammerman M, Aspenberg P. Primary gene response to mechanical loading in healing rat Achilles tendons. J Appl Physiol. 2013; 114: 1519-1526. doi: 10.1152/japplphysiol. 01500.2012 PMID: 23519232
40. Guerquin MJ, Charvet B, Nourissat G, Havis E, Ronsin O, Bonnin MA, et al. Transcription factor EGR1 directs tendon differentiation and promotes tendon repair. J Clin Invest. 2013; 123: 3564-3576. doi: 10. 1172/JCI67521 PMID: 23863709
41. Lejard V, Blais F, Guerquin MJ, Bonnet A, Bonnin MA, Havis E, et al. EGR1 and EGR2 involvement in vertebrate tendon differentiation. J Biol Chem. 2011; 286: 5855-5867. doi: 10.1074/jbc.M110.153106 PMID: 21173153
42. Havis E, Bonnin MA, Olivera-Martinez I, Nazaret N, Ruggiu M, Weibel J, et al. Transcriptomic analysis of mouse limb tendon cells during development. Development 2014; 141: 3683-3696. doi: 10.1242/dev.108654 PMID: 25249460
43. Kalluri R, Weinberg RA. The basics of epithelial-mesenchymal transition. J Clin Invest. 2009; 119: 1420-1428. doi: 10.1172/JCI39104 PMID: 19487818
44. Taylor SH, Al-Youha S, Van Agtmael T, Lu Y, Wong J, McGrouther DA, et al. Tendon is covered by a basement membrane epithelium that is required for cell retention and the prevention of adhesion formation. PloS One. 2011; 6: e16337. doi: 10.1371/journal.pone.0016337 PMID: 21298098
45. Ledford H. Cancer theory faces doubts. Nature. 2011; 472: 273. doi: 10.1038/472273a PMID: 21512545
46. Lin SL, Kisseleva T, Brenner DA, Duffield JS. Pericytes and perivascular fibroblasts are the primary source of collagen-producing cells in obstructive fibrosis of the kidney. Am J Pathol. 2008; 173: 1617-1627. doi: 10.2353/ajpath.2008.080433 PMID: 19008372
47. Chiquet M, Gelman L, Lutz R, Maier S. From mechanotransduction to extracellular matrix gene expression in fibroblasts. Biochimica et Biophysica Acta. 2009; 1793: 911-920. doi: 10.1016/j.bbamcr.2009. 01.012 PMID: 19339214
48. Bernet JD, Doles JD, Hall JK, Kelly Tanaka K, Carter TA, Olwin BB. p38 MAPK signaling underlies a cell-autonomous loss of stem cell self-renewal in skeletal muscle of aged mice. Nat Med. 2014; 20: 265-271. doi: 10.1038/nm.3465 PMID: 24531379
49. Perdiguero E, Sousa-Victor P, Ruiz-Bonilla V, Jardi M, Caelles C, Serrano AL, et al. p38/MKP-1-regulated AKT coordinates macrophage transitions and resolution of inflammation during tissue repair. J Cell Biol. 2011; 195: 307-322. doi: 10.1083/jcb.201104053 PMID: 21987635
50. Baeza-Raja B, Munoz-Canoves P. p38 MAPK-induced nuclear factor-kappaB activity is required for skeletal muscle differentiation: role of interleukin-6. Mol Biol Cell. 2004; 15: 2013-2026. PMID: 14767066
51. Langberg H, Olesen JL, Gemmer C, Kjaer M. Substantial elevation of interleukin-6 concentration in peritendinous tissue, in contrast to muscle, following prolonged exercise in humans. J Physiol. 2002; 542: 985-990. PMID: 12154195
52. Andersen MB, Pingel J, Kjaer M, Langberg H. Interleukin-6: a growth factor stimulating collagen synthesis in human tendon. J Appl Physiol. 2011; 110: 1549-1554. doi: 10.1152/japplphysiol.00037.2010 PMID: 21350025
53. Munoz-Canoves P, Scheele C, Pedersen BK, Serrano AL. Interleukin-6 myokine signaling in skeletal muscle: a double-edged sword? FASEB J. 2013; 280: 4131-4148. doi: 10.1111/febs.12338 PMID: 23663276
54. Davies SP, Reddy H, Caivano M, Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J. 2000; 351: 95-105. PMID: 10998351
55. Michna H, Hartmann G. Adaptation of tendon collagen to exercise. Int Orthopaed. 1989; 13: 161-165.
56. Heinemeier KM, Schjerling P, Heinemeier J, Magnusson SP, Kjaer M. Lack of tissue renewal in human adult Achilles tendon is revealed by nuclear bomb (14)C. FASEB J. 2013; 27: 2074-2079. doi: 10. 1096/fj.12-225599 PMID: 23401563