The sarcomeric protein nebulin: Another multifunctio giant in charge of muscle strength optimization

Frontiers in Physiology

Volumn 3 FEB, Issue , 2012, Pages

  Ottenheijm, Coen A C ^a,b   Granzier, Henk ^b   Labeit, Siegfried ^c  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

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

^c UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Nebulin; Skeletal muscle; Thin filament

Indexed keywords

EID: 84866303478     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2012.00037     Document Type: Review

References (62)

1. Agrawal, P. B., Greenleaf, R. S., Tomczak, K. K., Lehtokari, V. L., Wallgren-Pettersson, C., Wallefeld, W., Laing, N. G., Darras, B. T., Maciver, S. K., Dormitzer, P. R., and Beggs, A. H. (2007). Nemaline myopathy with minicores caused by mutation of the CFL2 gene encoding the skeletal muscle actin-binding protein, cofilin-2. Am. J. Hum. Genet. 80, 162-167.
2. Anderson, S. L., Ekstein, J., Donnelly, M. C., Keefe, E. M., Toto, N. R., LeVoci, L. A., and Rubin, B. Y. (2004). Nemaline myopathy in the Ashke-nazi Jewish population is caused by a deletion in the nebulin gene. Hum. Genet. 115, 185-190.
3. Bang, M. L., Caremani, M., Brunello, E., Littlefield, R., Lieber, R. L., Chen, J., Lombardi, V., and Linari, M. (2009). Nebulin plays a direct role in promoting strong actin-myosin interactions. FASEB J. 23, 4117-4125.
4. Bang, M. L., Gregorio, C., and Labeit, S. (2002). Molecular dissection of the interaction of desmin with the C-terminal region of nebulin. J. Struct. Biol. 137, 119-127.
5. Bang, M. L., Li, X., Littlefield, R., Bremner, S., Thor, A., Knowlton, K. U., Lieber, R. L., and Chen, J. (2006). Nebulin-deficient mice exhibit shorter thin filament lengths and reduced contractile function in skeletal muscle. J. Cell Biol. 173, 905-916.
6. Brenner, B. (1988). Effect of Ca2+ on cross-bridge turnover kinetics in skinned single rabbit psoas fibers: implications for regulation of muscle contraction. Proc. Natl. Acad. Sci. U.S.A. 85, 3265-3269.
7. Buck, D., Hudson, B. D., Ottenheijm, C. A., Labeit, S., and Granzier, H. (2010). Differential splicing of the large sarcomeric protein nebulin during skeletal muscle development. J. Struct. Biol. 170, 325-333.
8. Burkholder, T. J., Fingado, B., Baron, S., and Lieber, R. L. (1994). Relationship between muscle fiber types and sizes and muscle architectural properties in the mouse hindlimb. J. Morphol. 221, 177-190.
9. Capetanaki, Y., Bloch, R. J., Koulou-menta, A., Mavroidis, M., and Psar-ras, S. (2007). Muscle intermediate filaments and their links to membranes and membranous organelles. Exp. Cell Res. 313, 2063-2076.
10. Castillo, A., Nowak, R., Littlefield, K. P., Fowler, V. M., and Littlefield, R. S. (2009). A nebulin ruler does not dictate thin filament lengths. Biophys. J. 96, 1856-1865.
11. Chandra, M., Mamidi, R., Ford, S., Hidalgo, C., Witt, C., Ottenheijm, C., Labeit, S., and Granzier, H. (2009). Nebulin alters cross-bridge cycling kinetics and increases thin filament activation: a novel mechanism for increasing tension and reducing tension cost. J. Biol. Chem. 284, 30889-30896.
12. Conover, G. M., and Gregorio, C. (2011). The desmin coil 1B mutation K190A impairs nebulin Z-disc assembly and destabilizes actin thin filaments. J. Cell. Sci. 124, 3463-3476.
13. Conover, G. M., Henderson, S. N., and Gregorio, C. C. (2009). A myopathy-linked desmin mutation perturbs striated muscle actin filament architecture. Mol. Biol. Cell 20, 834-845.
14. Costa, M. L., Escaleira, R., Cataldo, A., Oliveira, F., and Mermelstein, C. S. (2004). Desmin: molecular interactions and putative functions of the muscle intermediate filament protein. Braz. J. Med. Biol. Res. 37, 1819-1830.
15. dos Remedios, C. G., Chhabra, D., Kekic, M., Dedova, I. V., Tsubakihara, M., Berry, D. A., and Nosworthy, N. J. (2003). Actin binding proteins: regulation of cytoskeletal microfila-ments. Physiol. Rev. 83, 433-473.
16. Gautel, M., Goulding, D., Bullard, B., Weber, K., and Furst, D. O. (1996). The central Z-disk region of titin is assembled from a novel repeat in variable copy numbers. J. Cell. Sci. 109(Pt 11), 2747-2754.
17. Gokhin, D. S., Bang, M. L., Zhang, J., Chen, J., and Lieber, R. L. (2009). Reduced thin filament length in nebulin-knockout skeletal muscle alters isometric contractile properties. Am. J. Physiol. Cell Physiol. 296, C1123-C1132.
18. Gokhin, D. S., Kim, N. E., Lewis, S. A., Hoenecke, H. R., D'Lima, D. D., and Fowler, V. M. (2012). Thin filament length correlates with fiber type in human skeletal muscle. Am. J. Phys-iol. Cell Physiol. 302, C555-C565.
19. Gordon, A. M., Homsher, E., and Reg-nier, M. (2000). Regulation of contraction in striated muscle. Physiol. Rev. 80, 853-924.
20. Granzier, H. L., Akster, H. A., and Ter Keurs, H. E. (1991). Effect of thin filament length on the force-sarcomere length relation of skeletal muscle. Am. J. Physiol. 260, C1060-C1070.
21. Huxley, A. F., and Simmons, R. M. (1971). Proposed mechanism of force generation in striated muscle. Nature 233, 533-538.
22. Jin, J. P., and Wang, K. (1991). Cloning, expression, and protein interaction of human nebulin fragments composed of varying numbers of sequence modules. J. Biol. Chem. 266, 21215-21223.
23. Konhilas, J. P., Irving, T. C., and de Tombe, P. P. (2002). Length-dependent activation in three striated muscle types of the rat. J. Phys-iol. (Lond.) 544, 225-236.
24. Kruger, M., Wright, J., and Wang, K. (1991). 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.
25. Labeit, S., Gibson, T., Lakey, A., Leonard, K., Zeviani, M., Knight, P., Wardale, J., and Trinick, J. (1991). Evidence that nebulin is a protein-ruler in muscle thin filaments. FEBS Lett. 282, 313-316.
26. Labeit, S., and Kolmerer, B. (1995). The complete primary structure of human nebulin and its correlation to muscle structure. J. Mol. Biol. 248, 308-315.
27. Laing, N. G., Majda, B. T., Akkari, P. A., Layton, M. G., Mulley, J. C., Phillips, H., Haan, E. A., White, S. J., Beggs, A. H., and Kunkel, L. M. (1992). Assignment of a gene (NEMI) for auto-somal dominant nemaline myopa-thy to chromosome I. Am. J. Hum. Genet. 50, 576-583.
28. Laing, N. G., Wilton, S. D., Akkari, P. A., Dorosz, S., Boundy, K., Kneebone, C., Blumbergs, P., White, S., Watkins, H., and Love, D. R. (1995). A mutation in the alpha tropomyosin gene TPM3 associated with autoso-mal dominant nemaline myopathy NEM1. Nat. Genet. 10, 249.
29. Lehtokari, V. L., Greenleaf, R. S., Dech-ene, E. T., Kellinsalmi, M., Pelin, K., Laing, N. G., Beggs, A. H., and Wallgren-Pettersson, C. (2009). The exon 55 deletion in the neb-ulin gene - one single founder mutation with world-wide occurrence. Neuromuscul. Disord. 19, 179-181.
30. Lehtokari, V. L., Pelin, K., Sandbacka, M., Ranta, S., Donner, K., Muntoni, F., Sewry, C., Angelini, C., Bushby, K., Van den, B. P., Iannaccone, S., Laing, N. G., and Wallgren-Pettersson, C. (2006). Identification of 45 novel mutations in the nebu-lin gene associated with autosomal recessive nemaline myopathy. Hum. Mutat. 27, 946-956.
31. Littlefield, R. S., and Fowler, V. M. (2008). Thin filament length regulation in striated muscle sarcomeres: pointed-end dynamics go beyond a nebulin ruler. Semin. Cell Dev. Biol. 19, 511-519.
32. Lukoyanova, N., VanLoock, M. S., Orlova, A., Galkin, V. E., Wang, K., and Egelman, E. H. (2002). Each actin subunit has three neb-ulin binding sites: implications for steric blocking. Curr. Biol. 12, 383-388.
33. Lymn, R. W., and Taylor, E. W. (1971). Mechanism of adenosine triphosphate hydrolysis by actomyosin. Biochemistry 10, 4617-4624.
34. Malik, F. I., Hartman, J. J., Elias, K. A., Morgan, B., Rodriguez, H., Brejc, K., Anderson, R. L., Sueoka, S. H., Lee, K. H., Finer, J. T., Sakowicz, R., Baliga, R., Cox, D. R., Garard, M., Godinez, G., Kawas, R., Kray-nack, E., Lenzi, D., Lu, P. P., Muci, A., Niu, C., Qian, X., Pierce, D. W., Pokrovskii, M., Suehiro, I., Sylvester, R., Tochimoto, T., Valdez, C., Wang, W., Katori, T., Kass, D. A., Shen, Y. T., Vatner, S. F., and Morgans, D. J. (2011). Cardiac myosin activation: a potential therapeutic approach for systolic heart failure. Science 331, 1439-1443.
35. McElhinny, A. S., Kazmierski, S. T., Labeit, S., and Gregorio, C. C. (2003). Nebulin: the nebulous, multifunctional giant of striated muscle. Trends Cardiovasc. Med. 13, 195-201.
36. McElhinny, A. S., Kolmerer, B., Fowler, V. M., Labeit, S., and Gregorio, C. C. (2001). The N-terminal end of nebulin interacts with tropomod-ulin at the pointed ends of the thin filaments. J. Biol. Chem. 276, 583-592.
37. Millevoi, S., Trombitas, K., Kolmerer, B., Kostin, S., Schaper, J., Pelin, K., Granzier, H., and Labeit, S. (1998). Characterization of neb-ulette and nebulin and emerging concepts of their roles for vertebrate Z-discs. J. Mol. Biol. 282, 111-123.
38. Moncman, C. L., and Wang, K. (1995). Nebulette: a 107kD nebulin-like protein in cardiac muscle. Cell Motil. Cytoskeleton 32, 205-225.
39. Nowak, K. J., Wattanasirichaigoon, D., Goebel, H. H., Wilce, M., Pelin, K., Donner, K., Jacob, R. L., Hub-ner, C., Oexle, K., Anderson, J. R., Verity, C. M., North, K., Iannac-cone, S., Muller, C. R., Nurnberg, P., Muntoni, F., Sewry, C., Hughes, I., Sutphen, R., Lacson, A. G., Swo-boda, K. J., Vigneron, J., Wallgren-Pettersson, C., Beggs, A. H., and Laing, N. G. (1999). Mutations in the skeletal muscle alpha-actin gene in patients with actin myopathy and nemaline myopathy. Nat. Genet. 23, 208-212.
40. Ogut, O., Hossain, M. M., and Jin, J. P. (2003). Interactions between nebulin-like motifs and thin filament regulatory proteins. J. Biol. Chem. 278, 3089-3097.
41. Ottenheijm, C. A., Fong, C., Vangheluwe, P., Wuytack, F., Babu, G. J., Periasamy, M., Witt, C. C., Labeit, S., and Granzier, H. (2008). Sarcoplasmic reticulum calcium uptake and speed of relaxation are depressed in nebulin-free skeletal muscle. FASEB J. 22, 2912-2919.
42. Ottenheijm, C. A., and Granzier, H. (2010). Lifting the nebula: novel insights into skeletal muscle contractility. Physiology (Bethesda) 25, 304-310.
43. Ottenheijm, C. A., Hooijman, P., Dechene, E. T., Stienen, G. J., Beggs, A. H., and Granzier, H. (2010). Altered myofilament function depresses force generation in patients with nebulin-based nema-line myopathy (NEM2). J. Struct. Biol. 170, 334-343.
44. Ottenheijm, C. A., Lawlor, M. W., Stienen, G. J., Granzier, H., and Beggs, A. H. (2011). Changes in cross-bridge cycling underlie muscle weakness in patients with tropomyosin 3-based myopathy. Hum. Mol. Genet. 20, 2015-2025.
45. Ottenheijm, C. A., Witt, C. C., Stienen, G. J., Labeit, S., Beggs, A. H., and Granzier, H. (2009). Thin filament length dysregulation contributes to muscle weakness in nemaline myopathy patients with nebulin deficiency. Hum. Mol. Genet. 18, 2359-2369.
46. Pappas, C. T., Bhattacharya, N., Cooper, J. A., and Gregorio, C. C. (2008). Nebulin interacts with CapZ and regulates thin filament architecture within the Z-disc. Mol. Biol. Cell 19, 1837-1847.
47. Pappas, C. T., Krieg, P. A., and Grego-rio, C. C. (2010). Nebulin regulates actin filament lengths by a stabilization mechanism. J. Cell Biol. 189, 859-870.
48. Pelin, K., Hilpela, P., Donner, K., Sewry, C., Akkari, P. A., Wilton, S. D., Wat-tanasirichaigoon, D., Bang, M. L., Centner, T., Hanefeld, F., Odent, S., Fardeau, M., Urtizberea, J. A., Muntoni, F., Dubowitz, V., Beggs, A. H., Laing, N. G., Labeit, S., de la, Chapelle A., and Wallgren-Pettersson, C. (1999). Mutations in the neb-ulin gene associated with autoso-mal recessive nemaline myopathy. Proc. Natl. Acad. Sci. U.S.A. 96, 2305-2310.
49. Pollard, T. D., and Borisy, G. G. (2003). Cellular motility driven by assembly and disassembly of actin filaments. Cell 112, 453-465.
50. Root, D. D., and Wang, K. (1994). Calmodulin-sensitive interaction of human nebulin fragments with actin and myosin. Biochemistry 33, 12581-12591.
51. Ryan, M. M., Schnell, C., Strickland, C. D., Shield, L. K., Morgan, B., Iannaccone, S., Laing, N. G., Beggs, A. H., and North, K. (2001). Nema-line myopathy: a clinical study of 143 cases. Ann. Neurol. 50, 312-320.
52. Sambuughin, N., Yau, K. S., Olive, M., Duff, R. M., Bayarsaikhan, M., Lu, S., Gonzalez-Mera, L., Sivado-rai, P., Nowak, K. J., Ravenscroft, G., Mastaglia, F. L., North, K. N., Ilkovski, B., Kremer, H., Lammens, M., van Engelen, B. G., Fabian, V., Lamont, P., Davis, M. R., Laing, N. G., and Goldfarb, L. G. (2010). Dominant mutations in KBTBD13, a member of the BTB/Kelch family, cause nemaline myopathy with cores. Am. J. Hum. Genet. 87, 842-847.
53. Sanoudou, D., and Beggs, A. H. (2001). Clinical and genetic heterogeneity in nemaline myopathy - a disease of skeletal muscle thin filaments. Trends Mol. Med. 7, 362-368.
54. Shah, S. B., Su, F. C., Jordan, K., Mil-ner, D. J., Friden, J., Capetanaki, Y., and Lieber, R. L. (2002). Evidence for increased myofibrillar mobility in desmin-null mouse skeletal muscle. J. Exp. Biol. 205, 321-325.
55. Solaro, R. J., and de Tombe, P. P. (2008). Review focus series: sarcomeric proteins as key elements in integrated control of cardiac function. Cardio-vasc. Res. 77, 616-618.
56. Takano, K., Watanabe-Takano, H., Suetsugu, S., Kurita, S., Tsujita, K., Kimura, S., Karatsu, T., Takenawa, T., and Endo, T. (2010). Nebulin and N-WASP cooperate to cause IGF-1-induced sarcomeric actin filament formation. Science 330, 1536-1540.
57. Tonino, P., Pappas, C. T., Hudson, B. D., Labeit, S., Gregorio, C. C., and Granzier, H. (2010). Reduced myofibrillar connectivity and increased Z-disk width in nebulin-deficient skeletal muscle. J. Cell Sci. 123, 384-391.
58. Wallgren-Pettersson, C., Donner, K., Sewry, C., Bijlsma, E., Lammens, M., Bushby, K., Giovannucci Uzielli, M. L., Lapi, E., Odent, S., Akcoren, Z., Topaloglu, H., and Pelin, K. (2002). Mutations in the nebulin gene can cause severe congenital nemaline myopathy. Neuromuscul. Disord. 12, 674-679.
59. Wallgren-Pettersson, C., Pelin, K., Nowak, K. J., Muntoni, F., Romero, N. B., Goebel, H. H., North, K. N., Beggs, A. H., and Laing, N. G. (2004). Genotype-phenotype correlations in nemaline myopathy caused by mutations in the genes for nebulin and skeletal muscle alpha-actin. Neuromuscul. Disord. 14, 461-470.
60. Wang, K., and Ramirez-Mitchell, R. (1983). A network of transverse and longitudinal intermediate filaments is associated with sarcomeres of adult vertebrate skeletal muscle. J. Cell Biol. 96, 562-570.
61. Wang, K., and Wright, J. (1988). 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
62. Witt, C. C., Burkart, C., Labeit, D., McNabb, M., Wu, Y., Granzier, H., and Labeit, S. (2006). Nebulin regulates thin filament length, contractility, and Z-disk structure in vivo. EMBO J. 25, 3843-3855.