Sarcomere Formation Occurs by the Assembly of Multiple Latent Protein Complexes
The stereotyped striation of myofibrils is a conserved feature of muscle organization that is critical to its function. Although most components that constitute the basic myofibrils are well-characterized biochemically and are conserved across the animal kingdom, the mechanisms leading to the precise assembly of sarcomeres, the basic units of myofibrils, are poorly understood. To gain insights into this process, we investigated the functional relationships of sarcomeric protein complexes. Specifically, we systematically analyzed, using either RNAi in primary muscle cells or available genetic mutations, the organization of myofibrils in Drosophila muscles that lack one or more sarcomeric proteins. Our study reveals that the thin and thick filaments are mutually dependent on each other for striation. Further, the tension sensor complex comprised of zipper/Zasp/α-actinin is involved in stabilizing the sarcomere but not in its initial formation. Finally, integrins appear essential for the interdigitation of thin and thick filaments that occurs prior to striation. Thus, sarcomere formation occurs by the coordinated assembly of multiple latent protein complexes, as opposed to sequential assembly.
Vyšlo v časopise:
Sarcomere Formation Occurs by the Assembly of Multiple Latent Protein Complexes. PLoS Genet 6(11): e32767. doi:10.1371/journal.pgen.1001208
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1001208
Souhrn
The stereotyped striation of myofibrils is a conserved feature of muscle organization that is critical to its function. Although most components that constitute the basic myofibrils are well-characterized biochemically and are conserved across the animal kingdom, the mechanisms leading to the precise assembly of sarcomeres, the basic units of myofibrils, are poorly understood. To gain insights into this process, we investigated the functional relationships of sarcomeric protein complexes. Specifically, we systematically analyzed, using either RNAi in primary muscle cells or available genetic mutations, the organization of myofibrils in Drosophila muscles that lack one or more sarcomeric proteins. Our study reveals that the thin and thick filaments are mutually dependent on each other for striation. Further, the tension sensor complex comprised of zipper/Zasp/α-actinin is involved in stabilizing the sarcomere but not in its initial formation. Finally, integrins appear essential for the interdigitation of thin and thick filaments that occurs prior to striation. Thus, sarcomere formation occurs by the coordinated assembly of multiple latent protein complexes, as opposed to sequential assembly.
Zdroje
1. AhmadF
SeidmanJG
SeidmanCE
2005 The genetic basis for cardiac remodeling. Annu Rev Genomics Hum Genet 6 185 216
2. DalkilicI
KunkelLM
2003 Muscular dystrophies: genes to pathogenesis. Curr Opin Genet Dev 13 231 238
3. HoltzerH
HijikataT
LinZX
ZhangZQ
HoltzerS
1997 Independent assembly of 1.6 microns long bipolar MHC filaments and I-Z-I bodies. Cell Struct Funct 22 83 93
4. LinZ
LuMH
SchultheissT
ChoiJ
HoltzerS
1994 Sequential appearance of muscle-specific proteins in myoblasts as a function of time after cell division: evidence for a conserved myoblast differentiation program in skeletal muscle. Cell Motil Cytoskeleton 29 1 19
5. LuMH
DiLulloC
SchultheissT
HoltzerS
MurrayJM
1992 The vinculin/sarcomeric-alpha-actinin/alpha-actin nexus in cultured cardiac myocytes. J Cell Biol 117 1007 1022
6. RheeD
SangerJM
SangerJW
1994 The premyofibril: evidence for its role in myofibrillogenesis. Cell Motil Cytoskeleton 28 1 24
7. LoRussoSM
RheeD
SangerJM
SangerJW
1997 Premyofibrils in spreading adult cardiomyocytes in tissue culture: evidence for reexpression of the embryonic program for myofibrillogenesis in adult cells. Cell Motil Cytoskeleton 37 183 198
8. EhlerE
RothenBM
HammerleSP
KomiyamaM
PerriardJC
1999 Myofibrillogenesis in the developing chicken heart: assembly of Z-disk, M-line and the thick filaments. J Cell Sci 112 Pt 10 1529 1539
9. GregorioCC
GranzierH
SorimachiH
LabeitS
1999 Muscle assembly: a titanic achievement? Curr Opin Cell Biol 11 18 25
10. SparrowJC
SchockF
2009 The initial steps of myofibril assembly: integrins pave the way. Nat Rev Mol Cell Biol 10 293 298
11. BrownNH
1994 Null mutations in the alpha PS2 and beta PS integrin subunit genes have distinct phenotypes. Development 120 1221 1231
12. LeeM
CramEJ
ShenB
SchwarzbauerJE
2001 Roles for beta(pat-3) integrins in development and function of Caenorhabditis elegans muscles and gonads. J Biol Chem 276 36404 36410
13. SchwanderM
LeuM
StummM
DorchiesOM
RueggUT
2003 Beta1 integrins regulate myoblast fusion and sarcomere assembly. Dev Cell 4 673 685
14. VolkT
FesslerLI
FesslerJH
1990 A role for integrin in the formation of sarcomeric cytoarchitecture. Cell 63 525 536
15. BloorJW
BrownNH
1998 Genetic analysis of the Drosophila alphaPS2 integrin subunit reveals discrete adhesive, morphogenetic and sarcomeric functions. Genetics 148 1127 1142
16. BaiJ
BinariR
NiJQ
VijayakanthanM
LiHS
2008 RNA interference screening in Drosophila primary cells for genes involved in muscle assembly and maintenance. Development 135 1439 1449
17. BaiJ
SeppKJ
PerrimonN
2009 Culture of Drosophila primary cells dissociated from gastrula embryos and their use in RNAi screening. Nat Protoc 4 1502 1512
18. BaiJ
HartwigJH
PerrimonN
2007 SALS, a WH2-domain-containing protein, promotes sarcomeric actin filament elongation from pointed ends during Drosophila muscle growth. Dev Cell 13 828 842
19. SchultheissT
LinZX
LuMH
MurrayJ
FischmanDA
1990 Differential distribution of subsets of myofibrillar proteins in cardiac nonstriated and striated myofibrils. J Cell Biol 110 1159 1172
20. Van der VenPF
EhlerE
PerriardJC
FurstDO
1999 Thick filament assembly occurs after the formation of a cytoskeletal scaffold. J Muscle Res Cell Motil 20 569 579
21. SangerJW
KangS
SiebrandsCC
FreemanN
DuA
2005 How to build a myofibril. J Muscle Res Cell Motil 26 343 354
22. O'DonnellPT
BernsteinSI
1988 Molecular and ultrastructural defects in a Drosophila myosin heavy chain mutant: differential effects on muscle function produced by similar thick filament abnormalities. J Cell Biol 107 2601 2612
23. BernsteinSI
O'DonnellPT
CrippsRM
1993 Molecular genetic analysis of muscle development, structure, and function in Drosophila. Int Rev Cytol 143 63 152
24. NishiiK
MorimotoS
MinakamiR
MiyanoY
HashizumeK
2008 Targeted disruption of the cardiac troponin T gene causes sarcomere disassembly and defects in heartbeat within the early mouse embryo. Dev Biol 322 65 73
25. NongthombaU
ClarkS
CumminsM
AnsariM
StarkM
2004 Troponin I is required for myofibrillogenesis and sarcomere formation in Drosophila flight muscle. J Cell Sci 117 1795 1805
26. SehnertAJ
HuqA
WeinsteinBM
WalkerC
FishmanM
2002 Cardiac troponin T is essential in sarcomere assembly and cardiac contractility. Nat Genet 31 106 110
27. HitchcockSE
1975 Regulation of muscle contraction: bindings of troponin and its components to actin and tropomyosin. Eur J Biochem 52 255 263
28. PelletierL
O'TooleE
SchwagerA
HymanAA
Muller-ReichertT
2006 Centriole assembly in Caenorhabditis elegans. Nature 444 619 623
29. BloorJW
KiehartDP
2001 zipper Nonmuscle myosin-II functions downstream of PS2 integrin in Drosophila myogenesis and is necessary for myofibril formation. Dev Biol 239 215 228
30. JaniK
SchockF
2007 Zasp is required for the assembly of functional integrin adhesion sites. J Cell Biol 179 1583 1597
31. ClarkKA
BlandJM
BeckerleMC
2007 The Drosophila muscle LIM protein, Mlp84B, cooperates with D-titin to maintain muscle structural integrity. J Cell Sci 120 2066 2077
32. RoperK
MaoY
BrownNH
2005 Contribution of sequence variation in Drosophila actins to their incorporation into actin-based structures in vivo. J Cell Sci 118 3937 3948
33. LittlefieldR
FowlerVM
1998 Defining actin filament length in striated muscle: rulers and caps or dynamic stability? Annu Rev Cell Dev Biol 14 487 525
34. FyrbergC
KetchumA
BallE
FyrbergE
1998 Characterization of lethal Drosophila melanogaster alpha-actinin mutants. Biochem Genet 36 299 310
35. HakedaS
EndoS
SaigoK
2000 Requirements of Kettin, a giant muscle protein highly conserved in overall structure in evolution, for normal muscle function, viability, and flight activity of Drosophila. J Cell Biol 148 101 114
36. ZhangY
FeatherstoneD
DavisW
RushtonE
BroadieK
2000 Drosophila D-titin is required for myoblast fusion and skeletal muscle striation. J Cell Sci 113 Pt 17 3103 3115
37. Pack-ChungE
KurshanPT
DickmanDK
SchwarzTL
2007 A Drosophila kinesin required for synaptic bouton formation and synaptic vesicle transport. Nat Neurosci 10 980 989
38. NewmanSMJr
WrightTR
1981 A histological and ultrastructural analysis of developmental defects produced by the mutation, lethal(1)myospheroid, in Drosophila melanogaster. Dev Biol 86 393 402
39. PerkinsAD
EllisSJ
AsghariP
ShamsianA
MooreED
Integrin-mediated adhesion maintains sarcomeric integrity. Dev Biol 338 15 27
40. SchusterCM
DavisGW
FetterRD
GoodmanCS
1996 Genetic dissection of structural and functional components of synaptic plasticity. I. Fasciclin II controls synaptic stabilization and growth. Neuron 17 641 654
41. NiJQ
MarksteinM
BinariR
PfeifferB
LiuLP
2008 Vector and parameters for targeted transgenic RNA interference in Drosophila melanogaster. Nat Methods 5 49 51
42. BernsteinSI
FyrbergEA
DonadyJJ
1978 Isolation and partial characterization of Drosophila myoblasts from primary cultures of embryonic cells. J Cell Biol 78 856 865
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Genetika Reprodukčná medicínaČlánok vyšiel v časopise
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