Lifting the nebula: Novel insights into skeletal muscle contractility

Physiology

Volumn 25, Issue 5, 2010, Pages 304-310

  Ottenheijm, Coen A C ^a,b   Granzier, Henk ^a  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

MUSCLE PROTEIN; NEBULIN;

ANIMAL; CHEMISTRY; GENETICS; HUMAN; MOUSE; MUSCLE CONTRACTION; NEMALINE MYOPATHY; PATHOPHYSIOLOGY; PHYSIOLOGY; REVIEW; SARCOMERE; SKELETAL MUSCLE;

ANIMALS; HUMANS; MICE; MUSCLE CONTRACTION; MUSCLE PROTEINS; MUSCLE, SKELETAL; MYOPATHIES, NEMALINE; SARCOMERES;

EID: 77958057443     PISSN: 15489213     EISSN: 15489221     Source Type: Journal    
DOI: 10.1152/physiol.00016.2010     Document Type: Review

References (43)

1. Bang ML, Caremani M, Brunello E, Littlefield R, Lieber RL, Chen J, Lombardi V, Linari M. Nebulin plays a direct role in promoting strong actin-myosin interactions. FASEB J 23:4117-4125, 2009.
2. Bang ML, Gregorio C, Labeit S. Molecular dissection of the interaction of desmin with the C-terminal region of nebulin. J Struct Biol 137:119-127, 2002.
3. Bang ML, Li X, Littlefield R, Bremner S, Thor A, Knowlton KU, Lieber RL, Chen J. Nebulin-deficient mice exhibit shorter thin filament lengths and reduced contractile function in skeletal muscle. J Cell Biol 173:905-916, 2006.
4. 2+ on cross-bridge turnover kinetics in skinned single rabbit psoas fibers: implications for regulation of muscle contraction. Proc Natl Acad Sci USA 85:3265-3269, 1988.
5. Buck D, Hudson BD, Ottenheijm CA, Labeit S, Granzier H. Differential splicing of the large sarcomeric protein nebulin during skeletal muscle development. J Struct Biol 170:325-333, 2010.
6. Burkholder TJ, Fingado B, Baron S, Lieber RL. Relationship between muscle fiber types and sizes and muscle architectural properties in the mouse hindlimb. J Morphol 221:177-190, 1994.
7. Castillo A, Nowak R, Littlefield KP, Fowler VM, Littlefield RS. A nebulin ruler does not dictate thin filament lengths. Biophys J 96:1856-1865, 2009.
8. Chandra M, Mamidi R, Ford S, Hidalgo C, Witt C, Ottenheijm C, Labeit S, Granzier HL. Nebulin alters crossbridge cycling kinetics and increases thin filament activation: a novel mechanism for increasing tension and reducing tension cost. J Biol Chem 284:30889-30896, 2009.
9. Conover GM, Henderson SN, Gregorio CC. A myopathy-linked desmin mutation perturbs striated muscle actin filament architecture. Mol Biol Cell 20:834-845, 2009.
10. dos Remedios CG, Chhabra D, Kekic M, Dedova IV, Tsubakihara M, Berry DA, Nosworthy NJ. Actin binding proteins: regulation of cytoskeletal microfilaments. Physiol Rev 83:433-473, 2003.
11. Fischer RS, Fowler VM. Tropomodulins: life at the slow end. Trends Cell Biol 13:593-601, 2003.
12. Gokhin DS, Bang ML, Zhang J, Chen J, Lieber RL. Reduced thin filament length in nebulin-knockout skeletal muscle alters isometric contractile properties. Am J Physiol Cell Physiol 296:C1123-C1132, 2009.
13. Gordon AM, Homsher E, Regnier M. Regulation of contraction in striated muscle. Physiol Rev 80:853-924, 2000.
14. Granzier HL, Akster HA, Ter Keurs HE. Effect of thin filament length on the force-sarcomere length relation of skeletal muscle. Am J Physiol Cell Physiol 260:C1060-C1070, 1991.
15. Huxley AF, Simmons RM. Proposed mechanism of force generation in striated muscle. Nature 233:533-538, 1971.
16. Jin JP, Wang K. Cloning, expression, and protein interaction of human nebulin fragments composed of varying numbers of sequence modules. J Biol Chem 266:21215-21223, 1991.
17. Konhilas JP, Irving TC, de Tombe PP. Length-dependent activation in three striated muscle types of the rat. J Physiol 544:225-236, 2002.
18. Kruger M, Wright J, Wang K. Nebulin as a length regulator of thin filaments of vertebrate skeletal muscles: correlation of thin filament length, nebulin size, and epitope profile. J Cell Biol 115:97-107, 1991.
19. Labeit S, Gibson T, Lakey A, Leonard K, Zeviani M, Knight P, Wardale J, Trinick J. Evidence that nebulin is a protein-ruler in muscle thin filaments. FEBS Lett 282:313-316, 1991.
20. Labeit S, Kolmerer B. The complete primary structure of human nebulin and its correlation to muscle structure. J Mol Biol 248:308-315, 1995.
21. Littlefield R, Fowler VM. Defining actin filament length in striated muscle: rulers and caps or dynamic stability? Annu Rev Cell Dev Biol 14:487-525, 1998.
22. Littlefield RS, Fowler VM. Thin filament length regulation in striated muscle sarcomeres: Pointed-end dynamics go beyond a nebulin ruler. Semin Cell Dev Biol 19:511-519, 2008.
23. Lukoyanova N, Van Loock MS, Orlova A, Galkin VE, Wang K, Egelman EH. Each actin subunit has three nebulin binding sites: implications for steric blocking. Curr Biol 12:383-388, 2002.
24. Lymn RW, Taylor EW. Mechanism of adenosine triphosphate hydrolysis by actomyosin. Biochemistry 10:4617-4624, 1971.
25. Mainguy V, Maltais F, Saey D, Gagnon P, Martel S, Simon M, Provencher S. Peripheral muscle dysfunction in idiopathic pulmonary arterial hypertension. Thorax 65:113-117, 2009.
26. McElhinny AS, Kazmierski ST, Labeit S, Gregorio CC. Nebulin: the nebulous, multifunctional giant of striated muscle. Trends Cardiovasc Med 13:195-201, 2003.
27. McElhinny AS, Kolmerer B, Fowler VM, Labeit S, Gregorio CC. The N-terminal end of nebulin interacts with tropomodulin at the pointed ends of the thin filaments. J Biol Chem 276:583-592, 2001.
28. McElhinny AS, Schwach C, Valichnac M, Mount-Patrick S, Gregorio CC. Nebulin regulates the assembly and lengths of the thin filaments in striated muscle. J Cell Biol 170:947-957, 2005.
29. Millevoi S, Trombitas K, Kolmerer B, Kostin S, Schaper J, Pelin K, Granzier H, Labeit S. Characterization of nebulette and nebulin and emerging concepts of their roles for vertebrate Z-discs. J Mol Biol 282:111-123, 1998.
30. Moncman CL, Wang K. Nebulette: a 107 kD nebulin-like protein in cardiac muscle. Cell Motil Cytoskeleton 32:205-225, 1995.
31. Ogut O, Hossain MM, Jin JP. Interactions between nebulin-like motifs and thin filament regulatory proteins. J Biol Chem 278:3089-3097, 2003.
32. Ottenheijm CA, Fong C, Vangheluwe P, Wuytack F, Babu GJ, Periasamy M, Witt CC, Labeit S, Granzier H. Sarcoplasmic reticulum calcium up-take and speed of relaxation are depressed in nebulin-free skeletal muscle. FASEB J 22:2912-2919, 2008.
33. Ottenheijm CA, Hooijman P, Dechene ET, Stienen GJ, Beggs AH, Granzier H. Altered myofilament function depresses force generation in patients with nebulin-based nemaline myopathy (NEM2). J Struct Biol 170:334-343, 2010.
34. Ottenheijm CA, Witt CC, Stienen GJ, Labeit S, Beggs AH, Granzier H. Thin filament length dysregulation contributes to muscle weakness in nemaline myopathy patients with nebulin deficiency. Hum Mol Genet 18:2359-2369, 2009.
35. Pelin K, Donner K, Holmberg M, Jungbluth H, Muntoni F, Wallgren-Pettersson C. Nebulin mutations in autosomal recessive nemaline myopathy: an update. Neuromuscul Disord 12:680-686, 2002.
36. Pelin K, Hilpela P, Donner K, Sewry C, Akkari PA, Wilton SD, Wattanasirichaigoon D, Bang ML, Centner T, Hanefeld F, Odent S, Fardeau M, Urtizberea JA, Muntoni F, Dubowitz V, Beggs AH, Laing NG, Labeit S, de la CA, Wallgren-Pettersson C. Mutations in the nebulin gene associated with autosomal recessive nemaline myopathy. Proc Natl Acad Sci USA 96:2305-2310, 1999. (Pubitemid 29117910)
37. Pollard TD, Borisy GG. Cellular motility driven by assembly and disassembly of actin filaments. Cell 112:453-465, 2003.
38. Root DD, Wang K. Calmodulin-sensitive interaction of human nebulin fragments with actin and myosin. Biochemistry 33:12581-12591, 1994.
39. Shah SB, Su FC, Jordan K, Milner DJ, Friden J, Capetanaki Y, Lieber RL. Evidence for increased myofibrillar mobility in desmin-null mouse skeletal muscle. J Exp Biol 205:321-325, 2002.
40. Solaro RJ, de Tombe PP. Review focus series: sarcomeric proteins as key elements in integrated control of cardiac function. Cardiovasc Res 77:616-618, 2008.
41. Udaka J, Ohmori S, Terui T, Ohtsuki I, Ishiwata S, Kurihara S, Fukuda N. Disuse-induced preferential loss of the giant protein titin depresses muscle performance via abnormal sarcomeric organization. J Gen Physiol 131:33-41, 2008.
42. Wang K, Wright J. Architecture of the sarcomere matrix of skeletal muscle: immunoelectron microscopic evidence that suggests a set of parallel inextensible nebulin filaments anchored at the Z line. J Cell Biol 107:2199-2212, 1988.
43. Witt CC, Burkart C, Labeit D, McNabb M, Wu Y, Granzier H, Labeit S. Nebulin regulates thin filament length, contractility, and Z-disk structure in vivo. EMBO J 25:3843-3855, 2006.