Journal: Proc Natl Acad Sci U S A / Year: 2019 Title: Three-dimensional structure of the basketweave Z-band in midshipman fish sonic muscle. Authors: Thomas Burgoyne / John M Heumann / Edward P Morris / Carlo Knupp / Jun Liu / Michael K Reedy / Kenneth A Taylor / Kuan Wang / Pradeep K Luther / Abstract: Striated muscle enables movement in all animals by the contraction of myriads of sarcomeres joined end to end by the Z-bands. The contraction is due to tension generated in each sarcomere between ...Striated muscle enables movement in all animals by the contraction of myriads of sarcomeres joined end to end by the Z-bands. The contraction is due to tension generated in each sarcomere between overlapping arrays of actin and myosin filaments. At the Z-band, actin filaments from adjoining sarcomeres overlap and are cross-linked in a regular pattern mainly by the protein α-actinin. The Z-band is dynamic, reflected by the 2 regular patterns seen in transverse section electron micrographs; the so-called small-square and basketweave forms. Although these forms are attributed, respectively, to relaxed and actively contracting muscles, the basketweave form occurs in certain relaxed muscles as in the muscle studied here. We used electron tomography and subtomogram averaging to derive the 3D structure of the Z-band in the swimbladder sonic muscle of type I male plainfin midshipman fish (, into which we docked the crystallographic structures of actin and α-actinin. The α-actinin links run diagonally between connected pairs of antiparallel actin filaments and are oriented at an angle of about 25° away from the actin filament axes. The slightly curved and flattened structure of the α-actinin rod has a distinct fit into the map. The Z-band model provides a detailed understanding of the role of α-actinin in transmitting tension between actin filaments in adjoining sarcomeres.
History
Deposition
Jul 6, 2019
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Header (metadata) release
Jul 31, 2019
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Map release
Jul 31, 2019
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Update
Aug 7, 2019
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Current status
Aug 7, 2019
Processing site: PDBe / Status: Released
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Structure visualization
Movie
Surface view with section colored by density value
Download / File: emd_10113.map.gz / Format: CCP4 / Size: 4.9 MB / Type: IMAGE STORED AS FLOATING POINT NUMBER (4 BYTES)
Annotation
Subtomogram average of a tomogram of basketweave Z-band found in sonic muscle in the swimbladder of male Type 1 midshipman fish.
Voxel size
X=Y=Z: 6.42 Å
Density
Contour Level
By AUTHOR: 165.0 / Movie #1: 165
Minimum - Maximum
125.395294000000007 - 176.195979999999992
Average (Standard dev.)
146.525599999999997 (±8.73213)
Symmetry
Space group: 1
Details
EMDB XML:
Map geometry
Axis order
X
Y
Z
Origin
0
0
0
Dimensions
80
80
200
Spacing
80
80
200
Cell
A: 513.6 Å / B: 513.6 Å / C: 1284.0 Å α=β=γ: 90.0 °
CCP4 map header:
mode
Image stored as Reals
Å/pix. X/Y/Z
6.42
6.42
6.42
M x/y/z
80
80
200
origin x/y/z
0.000
0.000
0.000
length x/y/z
513.600
513.600
1284.000
α/β/γ
90.000
90.000
90.000
start NX/NY/NZ
0
0
0
NX/NY/NZ
108
10
112
MAP C/R/S
1
2
3
start NC/NR/NS
0
0
0
NC/NR/NS
80
80
200
D min/max/mean
125.395
176.196
146.526
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Supplemental data
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Sample components
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Entire : Z-band of vertebrate striated muscle in basketweave form
Entire
Name: Z-band of vertebrate striated muscle in basketweave form
Components
Organelle or cellular component: Z-band of vertebrate striated muscle in basketweave form
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Supramolecule #1: Z-band of vertebrate striated muscle in basketweave form
Supramolecule
Name: Z-band of vertebrate striated muscle in basketweave form type: organelle_or_cellular_component / ID: 1 / Parent: 0 Details: Z-band studied in sonic muscle in the swimbladder of male Type 1 midshipman fish.
Type: POSITIVE / Material: Uranyl acetate and lead citrate Details: Conventionally stained with 2% uranyl acetate and Reynolds lead citrate
Sugar embedding
Material: Araldite Details: Sample was freeze-substituted in acetone and then embedded in araldiate
Grid
Material: COPPER / Mesh: 700
Vitrification
Cryogen name: ETHANE / Instrument: REICHERT-JUNG PLUNGER Details: Sample was cryo-protected with 30% sucrose (added to the relaxing solution).
Details
Fibers of swimbladder muscle (sonic muscle) of midshipman fish were rapidly frozen, freeze-substituted, embedded in resin, ~100 nm thin transverse sections cut, coated with 10 nm gold fiducials and stained with uranyl acetate and lead citrate.
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Electron microscopy
Microscope
FEI/PHILIPS CM200FEG
Image recording
Film or detector model: TVIPS TEMCAM-F415 (4k x 4k) / Digitization - Dimensions - Width: 4096 pixel / Digitization - Dimensions - Height: 4096 pixel / Number grids imaged: 1 / Average exposure time: 1.0 sec. / Average electron dose: 5.0 e/Å2
Electron beam
Acceleration voltage: 200 kV / Electron source: FIELD EMISSION GUN
Specimen holder model: OTHER / Cooling holder cryogen: NITROGEN
+
Image processing
Final reconstruction
Number classes used: 1 / Algorithm: BACK PROJECTION / Resolution.type: BY AUTHOR / Resolution: 39.0 Å / Resolution method: FSC 0.5 CUT-OFF / Software - Name: PEET (ver. 1.11.0 alpha) / Number subtomograms used: 5796
Extraction
Number tomograms: 1 / Number images used: 483 / Method: Semi-Automatic particle picking / Software - Name: PEET (ver. 1.11.0 alpha) Details: Automatic particle picking was performed by iterative refinement starting from a manually chosen initial reference and a uniform 2D grid of initial locations with spacing approximating that ...Details: Automatic particle picking was performed by iterative refinement starting from a manually chosen initial reference and a uniform 2D grid of initial locations with spacing approximating that of the unit cell. Selected points were windowed via cross-correlation thresholding and manual editing before further alignment and averaging.
Type: OTHER / Software - Name: PEET (ver. 1.11.0 alpha) Details: Normalised cross-correlation and weighted averaging in reciprocal space
Crystal parameters
Unit cell - A: 262 Å / Unit cell - B: 262 Å / Unit cell - C: 768 Å / Unit cell - γ: 90 ° / Unit cell - α: 90 ° / Unit cell - β: 90 ° / Space group: P43212
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