Lineage-based primary muscle fiber type diversification independent of MEF2 and NFAT in chick embryos

Journal of Muscle Research and Cell Motility

Volumn 31, Issue 5-6, 2011, Pages 369-381

  Theobald, Jillian ^a   Dimario, Joseph X ^a  

^a ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

Author keywords

Avian; Embryonic; Fiber type; Lineage; Myoblast; Myogenesis; Promoter

Indexed keywords

MYOCYTE SPECIFIC ENHANCER BINDING FACTOR 2; MYOCYTE-SPECIFIC ENHANCER-BINDING FACTOR 2; MYOGENIC FACTOR; TRANSCRIPTION FACTOR NFAT;

ANIMAL; ARTICLE; CELL LINEAGE; CHICK EMBRYO; CYTOLOGY; GENETICS; METABOLISM; MYOBLAST; SKELETAL MUSCLE;

ANIMALS; CELL LINEAGE; CHICK EMBRYO; MUSCLE FIBERS, SKELETAL; MYOBLASTS; MYOGENIC REGULATORY FACTORS; NFATC TRANSCRIPTION FACTORS;

AVES;

EID: 79952315640     PISSN: 01424319     EISSN: 15732657     Source Type: Journal    
DOI: 10.1007/s10974-011-9242-0     Document Type: Article

References (55)

1. DL Allen LA Leinwand 2002 Intracellular calcium and myosin isoform transitions. Calcineurin and calcium-calmodulin kinase pathways regulate preferential activation of the IIa myosin heavy chain promoter J Biol Chem 277 45323 45330 1:CAS:528:DC%2BD38Xosl2ltL4%3D 10.1074/jbc.M208302200 12235157 (Pubitemid 36159139)
2. DL Allen CA Sartorius LK Sycuro LA Leinwand 2001 Different pathways regulate expression of the skeletal myosin heavy chain genes J Biol Chem 276 43524 43533 1:CAS:528:DC%2BD3MXos12nsbw%3D 10.1074/jbc.M108017200 11551968
3. DL Allen JN Weber LK Sycuro LA Leinwand 2005 Myocyte enhancer factor-2 and serum response factor binding elements regulate fast Myosin heavy chain transcription in vivo J Biol Chem 280 17126 17134 1:CAS:528:DC%2BD2MXjsFOgtL0%3D 10.1074/jbc.M501207200 15728583 (Pubitemid 41389177)
4. V Andrés M Cervera V Mahdavi 1995 Determination of the consensus binding site for MEF2 expressed in muscle and brain reveals tissue-specific sequence constraints J Biol Chem 270 23246 23249 10.1074/jbc.270.40.23246 7559475
5. E Bandman R Matsuda RC Strohman 1982 Developmental appearance of myosin heavy and light chain isoforms in vivo and in vitro in chicken skeletal muscle Dev Biol 93 508 518 1:CAS:528:DyaL38XlvFKgsro%3D 10.1016/0012-1606(82)90138-5 7141112 (Pubitemid 13197409)
6. CR Beals NA Clipstone SN Ho GR Crabtree 1997 Nuclear localization of NF-ATc by a calcineurin-dependent, cyclosporin-sensitive intramolecular interaction Genes & Dev 11 824 834 1:CAS:528:DyaK2sXisl2qtbo%3D 10.1101/gad.11.7.824 (Pubitemid 27175290)
7. PH Bonner SD Hauschka 1974 Clonal analysis of vertebrate myogenesis. I. Early developmental events in the chick limb Dev Biol 37 317 328 1:STN:280:DyaE2c7ls1GrsQ%3D%3D 10.1016/0012-1606(74)90152-3 4826279
8. J Butler E Cosmos J Brierley 1982 Differentiation of muscle fiber types in aneurogenic brachial muscles of the chick embryo J Exp Zool 224 65 80 1:CAS:528:DyaL3sXhsVyjsw%3D%3D 10.1002/jez.1402240108 6217281
9. E Calabria S Ciciliot I Moretti M Garcia A Picard KA Dyar G Pallafacchina J Tothova S Schiaffino M Murgia 2009 NFAT isoforms control activity-dependent muscle fiber type specification Proc Natl Acad Sci 106 13335 13340 1:CAS:528:DC%2BD1MXhtVOitrzP 10.1073/pnas.0812911106 19633193
10. S Calvo P Venepally J Cheng A Buonanno 1999 Fiber-type-specific transcription of the troponin I slow gene is regulated by multiple elements Mol Cell Biol 19 515 525 1:CAS:528:DyaK1MXhvFOrsg%3D%3D 9858575 (Pubitemid 29018453)
11. S Calvo D Vullhorst P Venepally J Cheng I Karavanova A Buonanno 2001 Molecular dissection of DNA sequences and factors involved in slow muscle-specific transcription Mol Cell Biol 21 8490 8503 1:CAS:528: DC%2BD3MXovVegsbg%3D 10.1128/MCB.21.24.8490-8503.2001 11713284 (Pubitemid 33108608)
12. LD Carvalho LK Teixeira N Carrossini AT Caldeira KM Ansel A Rao JP Viola 2007 The NFAT1 transcription factor is a repressor of cyclin A2 gene expression Cell Cycle 6 1789 1795 1:CAS:528:DC%2BD2sXhtFWlsr%2FE 10.4161/cc.6.14.4473 17637565 (Pubitemid 47327933)
13. ER Chin EN Olson JA Richardson Q Yang C Humphries JM Shelton H Wu W Zhu R Bassel-Duby RS Williams 1998 A calcineurin-dependent transcriptional pathway controls skeletal muscle fiber type Genes Dev 12 2499 2509 1:CAS:528: DyaK1cXlslOitLs%3D 10.1101/gad.12.16.2499 9716403 (Pubitemid 28406953)
14. MK Choo H Yeo M Zayzafoon 2009 NFATc1 mediates HDAC-dependent transcriptional repression of osteocalcin expression during osteoblast differentiation Bone 45 579 589 1:CAS:528:DC%2BD1MXpsF2jsL0%3D 10.1016/j.bone.2009.05.009 19463978
15. JR Crew K Falzari JX DiMario 2010 Muscle fiber type specific induction of slow myosin heavy chain 2 gene expression by electrical stimulation Exp Cell Res 316 1039 1049 1:CAS:528:DC%2BC3cXivFKgtb0%3D 10.1016/j.yexcr.2010.01.008 20070941
16. MT Crow FE Stockdale 1986 Myosin expression and specialization among the earliest muscle fibers of the developing avian limb Dev Biol 113 238 254 1:CAS:528:DyaL28XosFOjtA%3D%3D 10.1016/0012-1606(86)90126-0 3943663 (Pubitemid 16047334)
17. MT Crow FE Stockdale 1986 The developmental program of fast myosin heavy chain expression in avian skeletal muscles Dev Biol 118 333 342 1:CAS:528:DyaL2sXkslCitQ%3D%3D 10.1016/0012-1606(86)90002-3 3539659 (Pubitemid 17212387)
18. JX DiMario PE Funk 1999 Protein kinase C activity regulates slow myosin heavy chain 2 gene expression in slow lineage skeletal muscle fibers Dev Dyn 216 177 189 1:CAS:528:DyaK1MXmvVymu7Y%3D 10.1002/(SICI)1097-0177(199910)216: 2<177::AID-DVDY8>3.0.CO;2-M 10536057 (Pubitemid 29471180)
19. JX DiMario FE Stockdale 1997 Both myoblast lineage and innervation determine fiber type and are required for expression of the slow myosin heavy chain 2 gene Dev Biol 188 167 180 1:CAS:528:DyaK2sXltlKgs78%3D 10.1006/dbio.1997.8619 9245520 (Pubitemid 27360095)
20. JX DiMario SE Fernyak FE Stockdale 1993 Myoblasts transferred to the limbs of embryos are committed to specific fibre fates Nature 362 165 167 1:STN:280:DyaK3s7ps1Ojsw%3D%3D 10.1038/362165a0 8383807 (Pubitemid 23085257)
21. SE Dunn AR Simard R Bassel-Duby RS Williams RN Michel 2001 Nerve activity-dependent modulation of calcineurin signaling in adult fast and slow skeletal muscle fibers J Biol Chem 276 45243 45254 1:CAS:528: DC%2BD3MXovFensbw%3D 10.1074/jbc.M105445200 11555650
22. DG Edmondson T-C Cheng P Cserjesi T Chakraborty EN Olson 1992 Analysis of the myogenin promoter reveals an indirect pathway for positive autoregulation mediated by the muscle-specific enhancer factor MEF-2 Mol Cell Biol 12 3665 3677 1:CAS:528:DyaK3sXkt1ajtbc%3D 1324403
23. DG Edmondson GE Lyons JF Martin EN Olson 1994 Mef2 gene expression marks the cardiac and skeletal muscle lineages during mouse embryogenesis Development 120 1251 1263 1:CAS:528:DyaK2cXltlSktLo%3D 8026334 (Pubitemid 24150050)
24. K Esser T Nelson V Lupa-Kimball E Blough 1999 The CACC box and myocyte enhancer factor-2 sites within the myosin light chain 2 slow promoter cooperate in regulating nerve-specific transcription in skeletal muscle J Biol Chem 274 12095 12102 1:CAS:528:DyaK1MXislGlt7s%3D 10.1074/jbc.274.17.12095 10207035 (Pubitemid 29197883)
25. JW Fickett 1996 Quantitative discrimination of MEF2 sites Mol Cell Biol 16 437 441 1:CAS:528:DyaK28XhtVKhtA%3D%3D 8524326 (Pubitemid 126506992)
26. WD Funk WE Wright 1992 Cyclic amplification and selection of targets for multicomponent complexes: myogenin interacts with factors recognizing binding sites for basic helix-loop-helix, nuclear factor 1, myocyte-specific enhancer-binding factor 2, and COMP1 factor Proc Natl Acad Sci 89 9484 9488 1:CAS:528:DyaK3sXhvFag 10.1073/pnas.89.20.9484 1329097
27. LA Gossett DJ Kelvin EA Sternberg EN Olson 1989 A new myocyte-specific enhancer-binding factor that recognizes a conserved element associated with multiple muscle-specific genes Mol Cell Biol 9 5022 5033 1:CAS:528:DyaK3cXhvVam 2601707 (Pubitemid 19275973)
28. H Jiang T Jordan J Li H Li JX DiMario 2004 Innervation-dependent regulation of the slow myosin heavy chain 2 promoter in avian skeletal muscle fiber types Dev Dyn 231 292 302 1:CAS:528:DC%2BD2cXosFOqsbg%3D 10.1002/dvdy.20137 15366006 (Pubitemid 39238055)
29. HB Kim M Kong TM Kim YH Suh WH Kim JH Lim JH Song MH Jung 2006 NFATc4 and ATF3 negatively regulate adiponectin gene expression in 3T3-L1 adipocytes Diabetes 55 1342 1352 1:CAS:528:DC%2BD28XksFahtL0%3D 10.2337/db05-1507 16644691 (Pubitemid 44195373)
30. H-P Kubis RJ Scheibe JD Meibner G Nornung G Gros 2002 Fast-to-slow transformation and nuclear import/export kinetics of the transcription factor NFATc1 during electrostimulation of rabbit muscle cells in culture J Physiol 541 835 847 1:CAS:528:DC%2BD38XlsVWns74%3D 10.1113/jphysiol.2002.017574 12068044 (Pubitemid 35190244)
31. Y Liu WR Randall MF Schneider 2005 Activity-dependent and -independent nuclear fluxes of HDAC4 mediated by different kinases in adult skeletal muscle J Cell Biol 168 887 897 1:CAS:528:DC%2BD2MXisFSgtLc%3D 10.1083/jcb.200408128 15767461 (Pubitemid 40397003)
32. KJA McCullagh E Calabria G Pallafacchina S Ciciliot AL Serrano C Argentini JM Kalhovde T Lømo S Schiaffino 2004 NFAT is a nerve activity sensor in skeletal muscle and controls activity-dependent myosin switching Proc Natl Acad Sci 101 10590 10595 1:CAS:528:DC%2BD2cXmtFWmsLk%3D 10.1073/pnas.0308035101 15247427 (Pubitemid 38955786)
33. IS McLennan 1983 Neural dependence and independence of myotube production in chicken hindlimb muscles Dev Biol 98 287 294 1:STN:280:DyaL3s3mt1Ohuw%3D%3D 10.1016/0012-1606(83)90359-7 6873458 (Pubitemid 13078026)
34. JB Miller FE Stockdale 1986 Developmental origins of skeletal muscle fibers: clonal analysis of myogenic cell lineages based on expression of fast and slow myosin heavy chains Proc Natl Acad Sci 83 3860 3864 1:CAS:528:DyaL28Xkt1ahsLw%3D 10.1073/pnas.83.11.3860 3520558 (Pubitemid 16062383)
35. JB Miller FE Stockdale 1986 Developmental regulation of the multiple myogenic cell lineages of the avian embryo J Cell Biol 103 2197 2208 1:CAS:528:DyaL2sXhtFKrs74%3D 10.1083/jcb.103.6.2197 3782296 (Pubitemid 17216647)
36. EA Miska C Karlsson E Langley SJ Nielsen J Pines T Kouzarides 1999 HDAC4 deacetylase associates with and represses the MEF2 transcription factor EMBO J 18 5099 5107 1:CAS:528:DyaK1MXms1ajtrw%3D 10.1093/emboj/18.18.5099 10487761 (Pubitemid 29443811)
37. DL Mitchell JX DiMario 2010 AP-2α suppresses skeletal myoblast proliferation and represses fibroblast growth factor receptor 1 promoter activity Exp Cell Res 316 194 202 1:CAS:528:DC%2BD1MXhsFShu7jK 10.1016/j.yexcr.2009.08.008 19699737
38. JD Molkentin BL Black JF Martin EN Olson 1995 Cooperative interaction of muscle gene expression by MEF2 and myogenic bHLH proteins Cell 83 1125 1136 1:CAS:528:DyaK28XhsVOnsA%3D%3D 10.1016/0092-8674(95)90139-6 8548800 (Pubitemid 26007804)
39. PS Naidu DC Ludolph RQ To TJ Hinterberger SF Konieczny 1995 Myogenin and MEF2 function synergistically to activate the MRF4 promoter during myogenesis Mol Cell Biol 15 2707 2715 1:STN:280:DyaK2M3lsl2msA%3D%3D 7739551
40. T Nguyen R Lindner A Tedeschi K Forsberg A Green A Wuttke P Gaub S Di Giovanni 2009 NFAT-3 is a transcriptional repressor of the growth-associated protein 43 during neuronal maturation J Biol Chem 284 18816 18823 1:CAS:528:DC%2BD1MXotVKnsb8%3D 10.1074/jbc.M109.015719 19443652
41. MC O'Neill FE Stockdale 1972 A kinetic analysis of myogenesis in vitro J Cell Biol 52 52 65 10.1083/jcb.52.1.52 5006948
42. M Oh I Rybkin V Copeland MP Czubryt JM Shelton E van Rooij JA Richardson LJ DeWindt R Bassel-Duby EN Olsen BA Rothermel 2005 Calcineurin is necessary for the maintenance but not embryonic development of slow muscle fibers Mol Cell Biol 25 6629 6638 1:CAS:528:DC%2BD2MXntVShu7Y%3D 10.1128/MCB.25.15.6629-6638. 2005 16024798 (Pubitemid 41023236)
43. S Page JB Miller JX DiMario EJ Hager A Moser FE Stockdale 1992 Developmentally regulated expression of three slow isoforms of myosin heavy chain: diversity among the first fibers to form in avian muscle Dev Biol 154 118 128 1:CAS:528:DyaK3sXhvFGrsQ%3D%3D 10.1016/0012-1606(92)90053-J 1426621
44. MJ Potthoff EN Olson 2007 MEF2: a central regulator of diverse developmental programs Development 134 4131 4140 1:CAS:528: DC%2BD1cXmtFehtA%3D%3D 10.1242/dev.008367 17959722
45. ZA Rana K Gundersen A Buonanno 2008 Activity-dependent repression of muscle genes by NFAT Proc Natl Acad Sci 105 5921 5926 1:CAS:528: DC%2BD1cXltVymsLY%3D 10.1073/pnas.0801330105 18408153 (Pubitemid 351758474)
46. PJ Reiser RL Moss GG Giulian ML Greaser 1985 Shortening velocity in single fibers from adult rabbit soleus muscles is correlated with myosin heavy chain composition J Biol Chem 260 9077 9080 1:CAS:528:DyaL2MXltVaks7c%3D 4019463 (Pubitemid 15249878)
47. PJ Reiser ML Greaser RL Moss 1988 Myosin heavy chain composition of single cells from avian slow skeletal muscle is strongly correlated with velocity of shortening during development Dev Biol 129 400 407 1:CAS:528:DyaL1cXls1Ols7Y%3D 10.1016/0012-1606(88)90387-9 3417046
48. P Shore AD Sharrocks 1995 The MADS-box family of transcription factors Eur J Biochem 229 1 13 1:CAS:528:DyaK2MXltFSgtbo%3D 10.1111/j.1432-1033.1995. tb20430.x 7744019
49. FE Stockdale 1992 Myogenic cell lineages Dev Biol 154 284 298 1:STN:280:DyaK3s%2FltVOqsQ%3D%3D 10.1016/0012-1606(92)90068-R 1426639
50. SJ Swoap RB Hunter EJ Stevenson HM Felton NV Kansagra JM Lang KA Esser SC Kandarian 2000 The calcineurin-NFAT pathway and muscle fiber-type gene expression Am J Physiol Cell Physiol 279 C915 C924 1:CAS:528: DC%2BD3cXnsFOrs7Y%3D 11003571
51. SJ Tapscott 2005 The circuitry of a master switch: Myod and the regulation of skeletal muscle gene transcription Development 132 2685 2695 1:CAS:528:DC%2BD2MXmtF2ls7g%3D 10.1242/dev.01874 15930108 (Pubitemid 40932860)
52. J Tothova B Blaauw G Pallafacchina R Rudolf C Argentini C Reggiani S Schiaffino 2006 NFATc1 nucleocytoplasmic shuttling is controlled by nerve activity in skeletal muscle J Cell Sci 119 1604 1611 1:CAS:528: DC%2BD28XlsFekurk%3D 10.1242/jcs.02875 16569660 (Pubitemid 43732986)
53. PM Wigmore DJ Evans 2002 Molecular and cellular mechanisms involved in the generation of fiber diversity during myogenesis Int Rev Cytol 216 175 232 1:CAS:528:DC%2BD38XlsVartLw%3D 10.1016/S0074-7696(02)16006-2 12049208 (Pubitemid 34552689)
54. H Wu FJ Naya TA McKinsey B Mercer JM Shelton ER Chin AR Simard RN Michel R Bassel-Duby EN Olson RS Williams 2000 MEF2 responds to multiple calcium-regulated signals in the control of skeletal muscle fiber type EMBO J 19 1963 1973 1:CAS:528:DC%2BD3cXktFWiuro%3D 10.1093/emboj/19.9.1963 10790363 (Pubitemid 30237572)
55. H Wu B Rothermel S Kanatous P Rosenberg FJ Naya JM Shelton KA Hutcheson JM DiMaio EN Olson R Bassel-Duby RS Williams 2001 Activation of MEF2 by muscle activity is mediated through a calcineurin-dependent pathway EMBO J 20 6414 6423 1:CAS:528:DC%2BD3MXovFOntLc%3D 10.1093/emboj/20.22.6414 11707412 (Pubitemid 33078714)