Fine-structural distribution of MMP-2 and MMP-9 activities in the rat skeletal muscle upon training: A study by high-resolution in situ zymography

Histochemistry and Cell Biology

Volumn 138, Issue 1, 2012, Pages 75-87

  Yeghiazaryan, Marine ^a   Żybura Broda, Katarzyna ^a   Cabaj, Anna ^a,b   Włodarczyk, Jakub ^a   Sławińska, Urszula ^a   Rylski, Marcin ^c   Wilczyński, Grzegorz M ^a  

^a NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

^b INSTITUTE OF BIOCYBERNETICS AND BIOMEDICAL ENGINEERING   (Poland)

^c MEDICAL CENTER FOR POSTGRADUATE EDUCATION   (Poland)

Author keywords

Cell nucleus; Exercise; Matrix metalloproteinase; Rat; Satellite cells; Skeletal muscle

Indexed keywords

GELATINASE; GELATINASE A; GELATINASE B; RNA POLYMERASE II;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL FRACTIONATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVITY; EXERCISE; EXTENSOR DIGITORUM LONGUS MUSCLE; HINDLIMB; IN SITU ZYMOGRAPHY; MALE; MONONUCLEAR CELL; MUSCLE FUNCTION; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SKELETAL MUSCLE; SKELETAL MUSCLE SATELLITE CELL; SOLEUS MUSCLE; UPREGULATION; ZYMOGRAPHY;

RATTUS;

EID: 84865123077     PISSN: 09486143     EISSN: 1432119X     Source Type: Journal    
DOI: 10.1007/s00418-012-0940-5     Document Type: Article

References (54)

1. Ahmad R, Rasheed Z, Ahsan H (2009) Biochemical and cellular toxicology of peroxynitrite: implications in cell death and autoimmune phenomenon. Immunopharmacol Immunotoxicol 31:388-396
2. Appell HJ, Forsberg S, Hollmann W (1988) Satellite cell activation in human skeletal muscle after training: evidence for muscle fiber neoformation. Int J Sports Med 9:297-299
3. Bassel-Duby R, Olson EN (2006) Signaling pathways in skeletal muscle remodeling. Annu Rev Biochem 75:19-37 (Pubitemid 44118024)
4. Baum O, Ganster M, Baumgartner I, Nieselt K, Djonov V (2007) Basement membrane remodeling in skeletal muscles of patients with limb ischemia involves regulation of matrix metalloproteinases and tissue inhibitor of matrix metalloproteinases. J Vasc Res 44:202-213 (Pubitemid 46597302)
5. Boldrin L, Muntoni F, Morgan JE (2010) Are human and mouse satellite cells really the same? J Histochem Cytochem 58:941-955
6. Buonanno A, Rosenthal N (1996) Molecular control of muscle diversity and plasticity. Dev Genet 19:95-107 (Pubitemid 26391248)
7. Carlson BM, Faulkner JA (1983) The regeneration of skeletal muscle fibers following injury: a review. Med Sci Sports Exerc 15: 187-198 (Pubitemid 13010547)
8. Carmeli E, Moas M, Reznick AZ, Coleman R (2004) Matrix metalloproteinases and skeletal muscle: a brief review. Muscle Nerve 29:191-197 (Pubitemid 38166839)
9. Carmeli E, Moas M, Lennon S, Powers SK (2005) High intensity exercise increases expression of matrix metalloproteinases in fast skeletal muscle fibres. Exp Physiol 90:613-619 (Pubitemid 40980162)
10. Cauwe B, Opdenakker G (2010) Intracellular substrate cleavage: a novel dimension in the biochemistry, biology and pathology of matrix metalloproteinases. Crit Rev Biochem Mol Biol 45: 351-423
11. Chakalova L, Fraser P (2010) Organization of transcription. Cold Spring Harb Perspect Biol 2:a000729
12. Chakraborti S, Mandal M, Das S, Mandal A, Chakraborti T (2003) Regulation of matrix metalloproteinases: an overview. Mol Cell Biochem 253:269-285
13. Chen X, Li Y (2009) Role of matrix metalloproteinases in skeletal muscle: migration, differentiation, regeneration and fibrosis. Cell Adh Migr 3:337-341
14. Cheng XC, Fang H, Xu WF (2008) Advances in assays of matrix metalloproteinases (MMPs) and their inhibitors. J Enzyme Inhib Med Chem 23:154-167 (Pubitemid 351404833)
15. Coker ML, Doscher MA, Thomas CV, Galis ZS, Spinale FG (1999) Matrix metalloproteinase synthesis and expression in isolated LV myocyte preparations. Am J Physiol 277:H777-H787 (Pubitemid 29415994)
16. Collier IE, Wilhelm SM, Eisen AZ, Marmer BL, Grant GA, Seltzer JL, Kronberger A, He CS, Bauer EA, Goldberg GI (1988) H-ras oncogene-transformed human bronchial epithelial cells (TBE-1) secrete a single metalloprotease capable of degrading basement membrane collagen. J Biol Chem 263:6579-6587
17. Dahiya S, Bhatnagar S, Hindi SM, Jiang C, Paul PK, Kuang S, KumarA (2011) Elevated levels of active matrix metalloproteinase-9 cause hypertrophy in skeletal muscle of normal and dystrophin-deficient mdx mice. Hum Mol Genet 20:4345-4359
18. Eguchi T, Kubota S, Kawata K, Mukudai Y, Uehara J, Ohgawara T, Ibaragi S, Sasaki A, Kuboki T, Takigawa M (2008) Novel transcription-factor-like function of human matrix metalloproteinase 3 regulating the CTGF/CCN2 gene. Mol Cell Biol 28: 2391-2413 (Pubitemid 351429984)
19. Fluck M (2006) Functional, structural and molecular plasticity of mammalian skeletal muscle in response to exercise stimuli. J Exp Biol 209:2239-2248 (Pubitemid 44065519)
20. Gawlak M, Gorkiewicz T, Gorlewicz A, Konopacki FA, Kaczmarek L, Wilczynski GM (2009) High resolution in situ zymography reveals matrix metalloproteinase activity at glutamatergic synapses. Neuroscience 158:167-176
21. Goldspink G (2003) Gene expression in muscle in response to exercise. J Muscle Res Cell Motil 24:121-126 (Pubitemid 37323615)
22. Howard E, Bullen E, Banda M (1991) Regulation of the autoactivation of human 72-kDa progelatinase by tissue inhibitor of metalloproteinases-2. J Biol Mis 266:13064-13069 (Pubitemid 21907308)
23. Irintchev A, Wernig A (1987) Muscle damage and repair in voluntarily running mice: strain and muscle differences. Cell Tissue Res 249:509-521
24. Kadi F, Thornell LE (1999) Training affects myosin heavy chain phenotype in the trapezius muscle of women. Histochem Cell Biol 112:73-78 (Pubitemid 29356306)
25. Kocturk S, Kayatekin BM, Resmi H, Acikgoz O, Kaynak C, Ozer E (2008) The apoptotic response to strenuous exercise of the gastrocnemius and solues muscle fibers in rats. Eur J Appl Physiol 102:515-524
26. Koskinen SO, Wang W, Ahtikoski AM, Kjaer M, Han XY, Komulainen J, Kovanen V, Takala TE (2001) Acute exercise induced changes in rat skeletal muscle mRNAs and proteins regulating type IV collagen content. Am J Physiol Regul Integr Comp Physiol 280:R1292-R1300
27. Koskinen SO, Heinemeier KM, Olesen JL, Langberg H, Kjaer M (2004) Physical exercise can influence local levels of matrix metalloproteinases and their inhibitors in tendon-related connective tissue. J Appl Physiol 96:861-864 (Pubitemid 38248655)
28. Kumar A, Bhatnagar S (2010) Matrix metalloproteinase inhibitor batimastat alleviates pathology and improves skeletal muscle function in dystrophin-deficient mdx mice. Am J Pathol 177: 248-260
29. Kwan JA, Schulze CJ, Wang W, Leon H, Sariahmetoglu M, Sung M, Sawicka J, Sims DE, Sawicki G, Schulz R (2004) Matrix metalloproteinase-2 (MMP-2) is present in the nucleus of cardiac myocytes and is capable of cleaving poly (ADP-ribose) polymerase (PARP) in vitro. FASEB J 18:690-692
30. Lee JS, Bruce CR, Spurrell BE, Hawley JA (2002) Effect of training on activation of extracellular signal-regulated kinase 1/2 and p38 mitogen-activated protein kinase pathways in rat soleus muscle. Clin Exp Pharmacol Physiol 29:655-660 (Pubitemid 34779614)
31. Mannello F, Medda V (2012) Nuclear localization of matrix metalloproteinases. Prog Histochem Cytochem 47:27-58
32. Markaki Y, Gunkel M, Schermelleh L, Beichmanis S, Neumann J, Heidemann M, Leonhardt H, Eick D, Cremer C, Cremer T (2010) Functional nuclear organization of transcription and DNA replication: a topographical marriage between chromatin domains and the interchromatin compartment. Cold Spring Harb Symp Quant Biol 75:475-492
33. Ohira Y (2000) Neuromuscular adaptation to microgravity environment. Jpn J Physiol 50:303-314
34. Pilegaard H, Ordway GA, Saltin B, Neufer PD (2000) Transcriptional regulation of gene expression in human skeletal muscle during recovery from exercise. Am J Physiol Endocrinol Metab 279: E806-E814
35. Renaud S, Leppert D (2007) Matrix metalloproteinases in neuromuscular disease. Muscle Nerve 36:1-13 (Pubitemid 47016155)
36. Rosenblatt JD, Yong D, Parry DJ (1994) Satellite cell activity is required for hypertrophy of overloaded adult rat muscle. Muscle Nerve 17:608-613 (Pubitemid 24157384)
37. Rullman E, Rundqvist H, Wagsater D, Fischer H, Eriksson P, Sundberg CJ, Jansson E, Gustafsson T (2007) A single bout of exercise activates matrix metalloproteinase in human skeletal muscle. J Appl Physiol 102:2346-2351 (Pubitemid 47080770)
38. Rullman E, Norrbom J, Stromberg A, Wagsater D, Rundqvist H, Haas T, Gustafsson T (2009) Endurance exercise activates matrix metalloproteinases in human skeletal muscle. J Appl Physiol 106:804-812
39. Sawicki G, Leon H, Sawicka J, Sariahmetoglu M, Schulze CJ, Scott PG, Szczesna-Cordary D, Schulz R (2005) Degradation of myosin light chain in isolated rat hearts subjected to ischemia-reperfusion injury: a new intracellular target for matrix metalloproteinase-2. Circulation 112:544-552 (Pubitemid 41060795)
40. Sbai O, Ould-Yahoui A, Ferhat L, Gueye Y, Bernard A, Charrat E, Mehanna A, Risso JJ, Chauvin JP, Fenouillet E, Rivera S, Khrestchatisky M (2010) Differential vesicular distribution and trafficking of MMP-2, MMP-9, and their inhibitors in astrocytes. Glia 58:344-366
41. Shefer G, Rauner G, Yablonka-Reuveni Z, Benayahu D (2010) Reduced satellite cell numbers and myogenic capacity in aging can be alleviated by endurance exercise. PLoS ONE 5:e13307
42. Simon DN, Wilson KL (2011) The nucleoskeleton as a genomeassociated dynamic "network of networks". Nat Rev Mol Cell Biol 12:695-708
43. Smith HK, Plyley MJ, Rodgers CD, McKee NH (1997) Skeletal muscle damage in the rat hindlimb following single or repeated daily bouts of downhill exercise. Int J Sports Med 18:94-100
44. Smith HK, Maxwell L, Rodgers CD, McKee NH, Plyley MJ (2001) Exercise-enhanced satellite cell proliferation and new myonuclear accretion in rat skeletal muscle. J Appl Physiol 90: 1407-1414 (Pubitemid 32220926)
45. Snoek-van Beurden PA, Von den Hoff JW (2005) Zymographic techniques for the analysis of matrix metalloproteinase and their inhibitors. Bio Techniques 38:73-83 (Pubitemid 40139420)
46. Sung MM, Schulz CG, Wang W, Sawicki G, Bautista-Lopez NL, Schulz R (2007) Matrix metalloproteinase-2 degrades the cytoskeletal protein alpha-actinin in peroxynitrite mediated myocardial injury. J Mol Cell Cardiol 43:429-436 (Pubitemid 47451426)
47. Szklarczyk A, Lapinska J, Rylski M, McKay RD, Kaczmarek L (2002) Matrix metalloproteinase-9 undergoes expression and activation during dendritic remodeling in adult hippocampus. J Neurosci 22:920-930 (Pubitemid 34141772)
48. Visse R, Nagase H (2003) Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ Res 92:827-839 (Pubitemid 36542523)
49. Wang W, Schulze CJ, Suarez-Pinzon WL, Dyck JR, Sawicki G, Schulz R (2002) Intracellular action of matrix metalloproteinase- 2 accounts for acute myocardial ischemia and reperfusion injury. Circulation 106:1543-1549
50. Wilhelm SM, Collier IE, Marmer BL, Eisen AZ, Grant GA, Goldberg GI (1989) SV40-transformed human lung fibroblasts secrete a 92-kDa type IV collagenase which is identical to that secreted by normal human macrophages. J Biol Chem 264:17213-17221 (Pubitemid 19255553)
51. Wretman C, Widegren U, Lionikas A, Westerblad H, Henriksson J (2000) Differential activation of mitogen-activated protein kinase signalling pathways by isometric contractions in isolated slowand fast-twitch rat skeletal muscle. Acta Physiol Scand 170:45-49
52. Yang Y, Candelario-Jalil E, Thompson JF, Cuadrado E, Estrada EY, Rosell A, Montaner J, Rosenberg GA (2010) Increased intranuclear matrix metalloproteinase activity in neurons interferes with oxidative DNA repair in focal cerebral ischemia. J Neurochem 112:134-149
53. Zanotti S, Saredi S, Ruggieri A, Fabbri M, Blasevich F, Romaggi S, Morandi L, MoraM(2007) Altered extracellular matrix transcript expression and protein modulation in primary Duchenne muscular dystrophy myotubes. Matrix Biol 26:615-624 (Pubitemid 350180391)
54. Zimowska M, Brzoska E, Swierczynska M, Streminska W, Moraczewski J (2008) Distinct patterns of MMP-9 and MMP-2 activity in slow and fast twitch skeletal muscle regeneration in vivo. Int J Dev Biol 52:307-314 (Pubitemid 351554718)