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Title: Triggering typical nemaline myopathy with compound heterozygous nebulin mutations reveals myofilament structural changes as pathomechanism

Abstract

Nebulin is a giant protein that winds around the actin filaments in the skeletal muscle sarcomere. Compound-heterozygous mutations in the nebulin gene (NEB) cause typical nemaline myopathy (NM), a muscle disorder characterized by muscle weakness with limited treatment options. We created a mouse model with a missense mutation p.Ser6366Ile and a deletion of NEB exon 55, the Compound-Het model that resembles typical NM. We show that Compound-Het mice are growth-retarded and have muscle weakness. Muscles have a reduced myofibrillar fractional-area and sarcomeres are disorganized, contain rod bodies, and have longer thin filaments. In contrast to nebulin-based severe NM where haplo-insufficiency is the disease driver, Compound-Het mice express normal amounts of nebulin. X-ray diffraction revealed that the actin filament is twisted with a larger radius, that tropomyosin and troponin behavior is altered, and that the myofilament spacing is increased. The unique disease mechanism of nebulin-based typical NM reveals novel therapeutic targets.

Authors:
 [1]; ORCiD logo [2];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [2];  [1];  [1]; ORCiD logo [1];  [1];  [2]; ORCiD logo [1]
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  1. Univ. of Arizona, Tucson, AZ (United States)
  2. Illinois Inst. of Technology, Chicago, IL (United States)
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
Sponsoring Org.:
A Foundation Building Strength; National Institute of Arthritis and Musculoskeletal and Skin Diseases (NIAMS); USDOE Office of Science (SC); National Institute of General Medical Sciences (NIGMS); National Institutes of Health (NIH)
OSTI Identifier:
1631850
Grant/Contract Number:  
R01AR053897; AC02-06CH11357; 9 P41 GM103622; 1S10OD018090-01
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 11; Journal Issue: 1; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
ENGLISH
Subject:
59 BASIC BIOLOGICAL SCIENCES; Cytoskeleton; Muscle; Neuromuscular disease

Citation Formats

Lindqvist, Johan, Ma, Weikang, Li, Frank, Hernandez, Yaeren, Kolb, Justin, Kiss, Balazs, Tonino, Paola, van der Pijl, Robbert, Karimi, Esmat, Gong, Henry, Strom, Josh, Hourani, Zaynab, Smith III, John E., Ottenheijm, Coen, Irving, Thomas, and Granzier, Henk. Triggering typical nemaline myopathy with compound heterozygous nebulin mutations reveals myofilament structural changes as pathomechanism. United States: N. p., 2020. Web. doi:10.1038/s41467-020-16526-9.
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Lindqvist, Johan, Ma, Weikang, Li, Frank, Hernandez, Yaeren, Kolb, Justin, Kiss, Balazs, Tonino, Paola, van der Pijl, Robbert, Karimi, Esmat, Gong, Henry, Strom, Josh, Hourani, Zaynab, Smith III, John E., Ottenheijm, Coen, Irving, Thomas, & Granzier, Henk. Triggering typical nemaline myopathy with compound heterozygous nebulin mutations reveals myofilament structural changes as pathomechanism. United States. https://doi.org/10.1038/s41467-020-16526-9
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Lindqvist, Johan, Ma, Weikang, Li, Frank, Hernandez, Yaeren, Kolb, Justin, Kiss, Balazs, Tonino, Paola, van der Pijl, Robbert, Karimi, Esmat, Gong, Henry, Strom, Josh, Hourani, Zaynab, Smith III, John E., Ottenheijm, Coen, Irving, Thomas, and Granzier, Henk. Mon . "Triggering typical nemaline myopathy with compound heterozygous nebulin mutations reveals myofilament structural changes as pathomechanism". United States. https://doi.org/10.1038/s41467-020-16526-9. https://www.osti.gov/servlets/purl/1631850.
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@article{osti_1631850,
title = {Triggering typical nemaline myopathy with compound heterozygous nebulin mutations reveals myofilament structural changes as pathomechanism},
author = {Lindqvist, Johan and Ma, Weikang and Li, Frank and Hernandez, Yaeren and Kolb, Justin and Kiss, Balazs and Tonino, Paola and van der Pijl, Robbert and Karimi, Esmat and Gong, Henry and Strom, Josh and Hourani, Zaynab and Smith III, John E. and Ottenheijm, Coen and Irving, Thomas and Granzier, Henk},
abstractNote = {Nebulin is a giant protein that winds around the actin filaments in the skeletal muscle sarcomere. Compound-heterozygous mutations in the nebulin gene (NEB) cause typical nemaline myopathy (NM), a muscle disorder characterized by muscle weakness with limited treatment options. We created a mouse model with a missense mutation p.Ser6366Ile and a deletion of NEB exon 55, the Compound-Het model that resembles typical NM. We show that Compound-Het mice are growth-retarded and have muscle weakness. Muscles have a reduced myofibrillar fractional-area and sarcomeres are disorganized, contain rod bodies, and have longer thin filaments. In contrast to nebulin-based severe NM where haplo-insufficiency is the disease driver, Compound-Het mice express normal amounts of nebulin. X-ray diffraction revealed that the actin filament is twisted with a larger radius, that tropomyosin and troponin behavior is altered, and that the myofilament spacing is increased. The unique disease mechanism of nebulin-based typical NM reveals novel therapeutic targets.},
doi = {10.1038/s41467-020-16526-9},
journal = {Nature Communications},
number = 1,
volume = 11,
place = {United States},
year = {Mon Jun 01 00:00:00 EDT 2020},
month = {Mon Jun 01 00:00:00 EDT 2020}
}
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https://doi.org/10.1038/s41467-020-16526-9
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Figures / Tables:

Fig. 1 Fig. 1: Basic characterization of the mouse strains. a Top: Nebulin localizes to the thin filament of the skeletal muscle sarcomere. Bottom: The structure of mouse nebulin with the S6366I site indicated (in super-repeat 22, orange) and the ΔExon55 site (in super-repeat 9, pink). A mouse was created with compoundmore » heterozygous Neb mutations: one missense mutation in exon 106 (NebS6366I) and one in-frame deletion of exon 55 (NebΔexon55), the Neb S6366I/Δexon55, or Compound-Het for short. b When breeding Het NebS6366I parents, genotypes of offspring follow Mendelian genetic ratios (top) and when breeding Het NebS6366I with Het NebΔexon55 parents (bottom), offspring also closely follows Mendelian genetics. c Body weight vs. days-of-life. Gompers non-linear least squares fit with as null hypothesis that one curve fits all data sets. Test (Sum-of-squares F-test) reveals that the null hypothesis is rejected (p≤ 0.0001; F (DFn, DFd): 63 (3,341)). (Results of male mice are shown with similar results found for female mice (not shown).) d Tibia length is reduced in Compound-Het and NebS6366I homozygous 4 months old male mice. An ordinary one-way ANOVA without matching or paring was performed with a posthoc multiple testing comparison with multiple testing correction (Sidak). *p= 0.02; **p= 0.008. e Grip strength in Compound-Het and NebS6366I mice, 1, 4 and 10 mo of age. A two-way ANOVA (no matching) reveals a significant effect of age and genotype on grip strength but without interaction. A posthoc multiple testing comparison with multiple testing correction (Dunnett) reveals a significant grip strength reduction at all 3 ages in Compound-Het mice and a significant reduction in 10 mo old NebS6366I mice. **p < 0.01; ****p < 0.0001. f In 3 mo old male mice (left) Compound-Het mice have a 35% decreased maximal lower limb force and NebS6366I Hom have a 7% reduction. In 10 mo old male mice (middle) the reduction is 37% and 18% and in 10 mo old female mice (right) the reduction is 37% and 18%. Non-linear least squares fit to Hill curve with as null hypothesis that one curve fits all data sets. Test (Sum-of-squares F-test) reveals that the null hypothesis is rejected in each panel (****p≤ 0.0001; F (DFn, DFd): 104.2 (8,208)). g Relative force-frequency relation (same data as in f, left) shows a left shift for both the Compound-Het and NebS6366I Hom mice with increased relative force at the shown frequencies of 40 and 60 Hz (One-way ANOVA without matching or paring performed with a posthoc multiple testing comparison with multiple testing correction (Sidak). ****p < 0.0001. Inset: decreased frequency for ½ maximal force in Compound-Het mice. Ordinary one-way ANOVA without matching or paring. A posthoc multiple testing comparison with multiple testing correction (Sidak). *p= 0.02. Number of mice in b 291 (top) and 668 (bottom); c, d: WT: 21, Compound-Het: 18, and NebS6366I Hom: 16; e 1 mo 19, 14, 12; 4 mo: 22, 18, 12; 10 mo 14, 6, 10. f left and g: WT: 9, Compound-Het: 7, and NebS6366I Hom: 6; f middle: WT: 6, Compound-Het: 2, and NebS6366I Hom: 6; f right WT: 6, Compound-Het: 4, and NebS6366I Hom: 3. g Inset 9 WT mice, 6 Compound-Het mice and 7 NebS6366I Hom mice. Bar values are mean ± SEM. Source data are provided as a Source Data file.« less
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Works referenced in this record:

Interactions between Nebulin-like Motifs and Thin Filament Regulatory Proteins
journal, November 2002

  • Ogut, Ozgur; Hossain, M. Moazzem; Jin, Jian-Ping
  • Journal of Biological Chemistry, Vol. 278, Issue 5
  • DOI: 10.1074/jbc.M205853200

Expression of Distinct Classes of Titin Isoforms in Striated and Smooth Muscles by Alternative Splicing, and Their Conserved Interaction with Filamins
journal, September 2006

  • Labeit, Siegfried; Lahmers, Sunshine; Burkart, Christoph
  • Journal of Molecular Biology, Vol. 362, Issue 4
  • DOI: 10.1016/j.jmb.2006.07.077

Tropomodulins and Leiomodins: Actin Pointed End Caps and Nucleators in Muscles
journal, May 2017

Titin/connectin-based modulation of the Frank-Starling mechanism of the heart
journal, February 2006

  • Fukuda, Norio; Granzier, Henk L.
  • Journal of Muscle Research and Cell Motility, Vol. 26, Issue 6-8
  • DOI: 10.1007/s10974-005-9038-1

Extensibility and Symmetry of Actin Filaments in Contracting Muscles
journal, December 1999

The Filament Lattice of Striated Muscle
journal, April 1998

Deleting nebulin's C-terminus reveals its importance to sarcomeric structure and function and is sufficient to invoke nemaline myopathy
journal, January 2019

  • Li, Frank; Barton, Elisabeth R.; Granzier, Henk
  • Human Molecular Genetics, Vol. 28, Issue 10
  • DOI: 10.1093/hmg/ddz016

Altered Contractility of Skeletal Muscle in Mice Deficient in Titin’s M-Band Region
journal, October 2009

  • Ottenheijm, Coen A. C.; Hidalgo, Carlos; Rost, Katharina
  • Journal of Molecular Biology, Vol. 393, Issue 1
  • DOI: 10.1016/j.jmb.2009.08.009

Nebulin-deficient mice exhibit shorter thin filament lengths and reduced contractile function in skeletal muscle
journal, June 2006

  • Bang, Marie-Louise; Li, Xiaodong; Littlefield, Ryan
  • Journal of Cell Biology, Vol. 173, Issue 6
  • DOI: 10.1083/jcb.200603119

Dominantly inherited distal nemaline/cap myopathy caused by a large deletion in the nebulin gene
journal, February 2019

  • Kiiski, Kirsi J.; Lehtokari, Vilma-Lotta; Vihola, Anna K.
  • Neuromuscular Disorders, Vol. 29, Issue 2
  • DOI: 10.1016/j.nmd.2018.12.007

Altered myofilament function depresses force generation in patients with nebulin-based nemaline myopathy (NEM2)
journal, May 2010

  • Ottenheijm, Coen A. C.; Hooijman, Pleuni; DeChene, Elizabeth T.
  • Journal of Structural Biology, Vol. 170, Issue 2
  • DOI: 10.1016/j.jsb.2009.11.013

SMASH – semi-automatic muscle analysis using segmentation of histology: a MATLAB application
journal, January 2014

Tissue Triage and Freezing for Models of Skeletal Muscle Disease
journal, January 2014

  • Meng, Hui; Janssen, Paul M. L.; Grange, Robert W.
  • Journal of Visualized Experiments, Issue 89
  • DOI: 10.3791/51586

Nemaline Myopathy: a new Congenital Myopathy
journal, January 1963

Nemaline myopathy in the Ashkenazi Jewish population is caused by a deletion in the nebulin gene
journal, June 2004

Myosin Head Configurations in Resting and Contracting Murine Skeletal Muscle
journal, September 2018

  • Ma, Weikang; Gong, Henry; Irving, Thomas
  • International Journal of Molecular Sciences, Vol. 19, Issue 9
  • DOI: 10.3390/ijms19092643

The nebulin SH3 domain is dispensable for normal skeletal muscle structure but is required for effective active load bearing in mouse
journal, September 2013

  • Yamamoto, D. L.; Vitiello, C.; Zhang, J.
  • Journal of Cell Science, Vol. 126, Issue 23
  • DOI: 10.1242/jcs.137026

Nebulin, a helical actin binding protein.
journal, April 1994

Complete genomic structure of the human nebulin gene and identification of alternatively spliced transcripts
journal, July 2004

  • Donner, Kati; Sandbacka, Maria; Lehtokari, Vilma-Lotta
  • European Journal of Human Genetics, Vol. 12, Issue 9
  • DOI: 10.1038/sj.ejhg.5201242

Nebulin Alters Cross-bridge Cycling Kinetics and Increases Thin Filament Activation: A NOVEL MECHANISM FOR INCREASING TENSION AND REDUCING TENSION COST
journal, September 2009

  • Chandra, Murali; Mamidi, Ranganath; Ford, Steven
  • Journal of Biological Chemistry, Vol. 284, Issue 45
  • DOI: 10.1074/jbc.M109.049718

Deleting exon 55 from the nebulin gene induces severe muscle weakness in a mouse model for nemaline myopathy
journal, May 2013

  • Ottenheijm, Coen A. C.; Buck, Danielle; de Winter, Josine M.
  • Brain, Vol. 136, Issue 6
  • DOI: 10.1093/brain/awt113

Nebulin deficiency in adult muscle causes sarcomere defects and muscle-type-dependent changes in trophicity: novel insights in nemaline myopathy
journal, June 2015

  • Li, Frank; Buck, Danielle; De Winter, Josine
  • Human Molecular Genetics, Vol. 24, Issue 18
  • DOI: 10.1093/hmg/ddv243

The giant protein titin regulates the length of the striated muscle thick filament
journal, October 2017

Rate of force generation in muscle: correlation with actomyosin ATPase activity in solution.
journal, May 1986

  • Brenner, B.; Eisenberg, E.
  • Proceedings of the National Academy of Sciences, Vol. 83, Issue 10
  • DOI: 10.1073/pnas.83.10.3542

Evidence that nebulin is a protein-ruler in muscle thin filaments
journal, May 1991

Ultrastructure of skeletal muscle fibers studied by a plunge quick freezing method: myofilament lengths
journal, July 1994

An Atomic Model of Actin Filaments Cross-Linked by Fimbrin and Its Implications for Bundle Assembly and Function
journal, May 2001

  • Volkmann, Niels; DeRosier, David; Matsudaira, Paul
  • The Journal of Cell Biology, Vol. 153, Issue 5
  • DOI: 10.1083/jcb.153.5.947

Nebulin interactions with actin and tropomyosin are altered by disease-causing mutations
journal, January 2014

  • Marttila, Minttu; Hanif, Mubashir; Lemola, Elina
  • Skeletal Muscle, Vol. 4, Issue 1
  • DOI: 10.1186/2044-5040-4-15

Nebulin and titin modulate cross-bridge cycling and length-dependent calcium sensitivity
journal, April 2019

  • Mijailovich, Srboljub M.; Stojanovic, Boban; Nedic, Djordje
  • The Journal of General Physiology, Vol. 151, Issue 5
  • DOI: 10.1085/jgp.201812165

Novel mutations in NEB cause abnormal nebulin expression and markedly impaired muscle force generation in severe nemaline myopathy
journal, January 2011

  • Lawlor, Michael W.; Ottenheijm, Coen A.; Lehtokari, Vilma-Lotta
  • Skeletal Muscle, Vol. 1, Issue 1
  • DOI: 10.1186/2044-5040-1-23

Myopathology in congenital myopathies
journal, February 2017

  • Sewry, C. A.; Wallgren-Pettersson, C.
  • Neuropathology and Applied Neurobiology, Vol. 43, Issue 1
  • DOI: 10.1111/nan.12369

Distal myopathy caused by homozygous missense mutations in the nebulin gene
journal, April 2007

  • Wallgren-Pettersson, C.; Lehtokari, V. -L.; Kalimo, H.
  • Brain, Vol. 130, Issue 6
  • DOI: 10.1093/brain/awm094

Nemaline myopathy: A clinical study of 143 cases
journal, January 2001

  • Ryan, Monique M.; Schnell, Christina; Strickland, Corinne D.
  • Annals of Neurology, Vol. 50, Issue 3
  • DOI: 10.1002/ana.1080

Identification of 45 novel mutations in the nebulin gene associated with autosomal recessive nemaline myopathy
journal, January 2006

  • Lehtokari, Vilma-Lotta; Pelin, Katarina; Sandbacka, Maria
  • Human Mutation, Vol. 27, Issue 9
  • DOI: 10.1002/humu.20370

Thick-Filament Extensibility in Intact Skeletal Muscle
journal, October 2018

The Complete Mouse Nebulin Gene Sequence and the Identification of Cardiac Nebulin
journal, May 2003

Muscle histopathology in nebulin-related nemaline myopathy: ultrastrastructural findings correlated to disease severity and genotype
journal, April 2014

  • Malfatti, Edoardo; Lehtokari, Vilma-Lotta; Böhm, Johann
  • Acta Neuropathologica Communications, Vol. 2, Issue 1
  • DOI: 10.1186/2051-5960-2-44

Genetics of the nemaline myopathies and the myotubular myopathies
journal, August 1998

Nebulin stiffens the thin filament and augments cross-bridge interaction in skeletal muscle
journal, September 2018

  • Kiss, Balázs; Lee, Eun-Jeong; Ma, Weikang
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 41
  • DOI: 10.1073/pnas.1804726115

Nebulin increases thin filament stiffness and force per cross-bridge in slow-twitch soleus muscle fibers
journal, October 2018

  • Kawai, Masataka; Karam, Tarek S.; Kolb, Justin
  • The Journal of General Physiology, Vol. 150, Issue 11
  • DOI: 10.1085/jgp.201812104

Sarcomere Dysfunction in Nemaline Myopathy
journal, May 2017

  • de Winter, Josine M.; Ottenheijm, Coen A. C.
  • Journal of Neuromuscular Diseases, Vol. 4, Issue 2
  • DOI: 10.3233/JND-160200

Nebulin regulates thin filament length, contractility, and Z-disk structure in vivo
journal, August 2006

  • Witt, Christian C.; Burkart, Christoph; Labeit, Dietmar
  • The EMBO Journal, Vol. 25, Issue 16
  • DOI: 10.1038/sj.emboj.7601242

Sarcoplasmic reticulum calcium uptake and speed of relaxation are depressed in nebulin-free skeletal muscle
journal, August 2008

  • Ottenheijm, Coen A. C.; Fong, Chi; Vangheluwe, Peter
  • The FASEB Journal, Vol. 22, Issue 8
  • DOI: 10.1096/fj.07-104372

A nebulin super-repeat panel reveals stronger actin binding toward the ends of the super-repeat region: Nebulin Binding of Actin
journal, November 2018

  • Laitila, Jenni; Lehtonen, Johanna; Lehtokari, Vilma-Lotta
  • Muscle & Nerve, Vol. 59, Issue 1
  • DOI: 10.1002/mus.26350

Reduced myofibrillar connectivity and increased Z-disk width in nebulin-deficient skeletal muscle
journal, January 2010

  • Tonino, P.; Pappas, C. T.; Hudson, B. D.
  • Journal of Cell Science, Vol. 123, Issue 3
  • DOI: 10.1242/jcs.042234

Nebulin mutations in autosomal recessive nemaline myopathy: an update
journal, October 2002

The exon 55 deletion in the nebulin gene – One single founder mutation with world-wide occurrence
journal, March 2009

  • Lehtokari, Vilma-Lotta; Greenleaf, Rebecca S.; DeChene, Elizabeth T.
  • Neuromuscular Disorders, Vol. 19, Issue 3
  • DOI: 10.1016/j.nmd.2008.12.001

Modulation of Muscle Atrophy, Fatigue and MLC Phosphorylation by MuRF1 as Indicated by Hindlimb Suspension Studies on MuRF1-KO Mice
journal, January 2010

  • Labeit, Siegfried; Kohl, Christine H.; Witt, Christian C.
  • Journal of Biomedicine and Biotechnology, Vol. 2010
  • DOI: 10.1155/2010/693741

Each Actin Subunit Has Three Nebulin Binding Sites
journal, March 2002

Congenital myopathies: disorders of excitation–contraction coupling and muscle contraction
journal, February 2018

  • Jungbluth, Heinz; Treves, Susan; Zorzato, Francesco
  • Nature Reviews Neurology, Vol. 14, Issue 3
  • DOI: 10.1038/nrneurol.2017.191

Nemaline myopathies: a current view
journal, June 2019

  • Sewry, Caroline A.; Laitila, Jenni M.; Wallgren-Pettersson, Carina
  • Journal of Muscle Research and Cell Motility, Vol. 40, Issue 2
  • DOI: 10.1007/s10974-019-09519-9

Thin filament length dysregulation contributes to muscle weakness in nemaline myopathy patients with nebulin deficiency
journal, April 2009

  • Ottenheijm, C. A. C.; Witt, C. C.; Stienen, G. J.
  • Human Molecular Genetics, Vol. 18, Issue 13
  • DOI: 10.1093/hmg/ddp168

Relationship between muscle fiber types and sizes and muscle architectural properties in the mouse hindlimb
journal, August 1994

  • Burkholder, Thomas J.; Fingado, Brian; Baron, Stephanie
  • Journal of Morphology, Vol. 221, Issue 2
  • DOI: 10.1002/jmor.1052210207

Nebulin plays a direct role in promoting strong actin-myosin interactions
journal, December 2009

  • Bang, Marie-Louise; Caremani, Marco; Brunello, Elisabetta
  • The FASEB Journal, Vol. 23, Issue 12
  • DOI: 10.1096/fj.09-137729

Mutation-specific effects on thin filament length in thin filament myopathy: Thin Filament Myopathy
journal, April 2016

  • Winter, Josine M. de; Joureau, Barbara; Lee, Eun-Jeong
  • Annals of Neurology, Vol. 79, Issue 6
  • DOI: 10.1002/ana.24654

New Insights into the Structural Roles of Nebulin in Skeletal Muscle
journal, January 2010

  • Ottenheijm, Coen A. C.; Granzier, Henk
  • Journal of Biomedicine and Biotechnology, Vol. 2010
  • DOI: 10.1155/2010/968139

Nemaline myopathy: current concepts. The ENMC International Consortium and Nemaline Myopathy.
journal, September 1997

  • North, K. N.; Laing, N. G.; Wallgren-Pettersson, C.
  • Journal of Medical Genetics, Vol. 34, Issue 9
  • DOI: 10.1136/jmg.34.9.705

Mutations in the nebulin gene associated with autosomal recessive nemaline myopathy
journal, March 1999

  • Pelin, K.; Hilpela, P.; Donner, K.
  • Proceedings of the National Academy of Sciences, Vol. 96, Issue 5
  • DOI: 10.1073/pnas.96.5.2305

The BioCAT undulator beamline 18ID: a facility for biological non-crystalline diffraction and X-ray absorption spectroscopy at the Advanced Photon Source
journal, August 2004

  • Fischetti, R.; Stepanov, S.; Rosenbaum, G.
  • Journal of Synchrotron Radiation, Vol. 11, Issue 5
  • DOI: 10.1107/S0909049504016760

X-ray diffraction evidence for the extensibility of actin and myosin filaments during muscle contraction
journal, December 1994

Mutation Update: The Spectra of Nebulin Variants and Associated Myopathies
journal, November 2014

  • Lehtokari, Vilma-Lotta; Kiiski, Kirsi; Sandaradura, Sarah A.
  • Human Mutation, Vol. 35, Issue 12
  • DOI: 10.1002/humu.22693

Vertical agarose gel electrophoresis and electroblotting of high-molecular-weight proteins
journal, June 2003

  • Warren, Chad M.; Krzesinski, Paul R.; Greaser, Marion L.
  • ELECTROPHORESIS, Vol. 24, Issue 11
  • DOI: 10.1002/elps.200305392

Developmental Control of Titin Isoform Expression and Passive Stiffness in Fetal and Neonatal Myocardium
journal, March 2004

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