The ZZ domain of dystrophin in DMD: Making sense of missense mutations

Human Mutation

Volumn 35, Issue 2, 2014, Pages 257-264

  Vulin, Adeline ^a   Wein, Nicolas ^a   Strandjord, Dana M ^b   Johnson, Eric K ^a   Findlay, Andrew R ^a   Maiti, Baijayanta ^c   Howard, Michael T ^d   Kaminoh, Yuuki J ^a   Taylor, Laura E ^a   Simmons, Tabatha R ^a   Ray, Will C ^a   Montanaro, Federica ^a   Ervasti, Jim M ^b   Flanigan, Kevin M ^a,e  

^a THE RESEARCH INSTITUTE AT NATIONWIDE CHILDREN S HOSPITAL   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^e OHIO STATE UNIVERSITY   (United States)

Author keywords

Duchenne muscular dystrophy; Dystrophin; Missense mutation; ZZ domain

Indexed keywords

ALPHA SARCOGLYCAN; ASPARTIC ACID; BETA SARCOGLYCAN; CYSTEINE; DELTA SARCOGLYCAN; DNA BINDING PROTEIN; DYSTROBREVIN; DYSTROBREVIN ALPHA; DYSTROGLYCAN; DYSTROPHIN; DYSTROPHIN ASSOCIATED PROTEIN COMPLEX; GAMMA SARCOGLYCAN; MUTANT PROTEIN; RECOMBINANT PROTEIN; SYNTROPHIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CELL MEMBRANE; DENATURATION; DUCHENNE MUSCULAR DYSTROPHY; FLUOROMETRY; GENE CONSTRUCT; GENE MUTATION; GENETIC ENGINEERING; GENETIC TRANSFECTION; GENOMIC INSTABILITY; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; IMMUNOREACTIVITY; IN VITRO STUDY; IN VIVO STUDY; LIGHT SCATTERING; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MISSENSE MUTATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OUTCOME ASSESSMENT; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; SITE DIRECTED MUTAGENESIS; SYNTROPHIN ALPHA 1; TANDEM MASS SPECTROMETRY; THERMOSTABILITY; TRANSGENE; TRANSGENIC MOUSE; WESTERN BLOTTING; WILD TYPE; ZINC FINGER MOTIF; ZZ DOMAIN;

DUCHENNE MUSCULAR DYSTROPHY; DYSTROPHIN; MISSENSE MUTATION; ZZ DOMAIN;

ACTINS; ANIMALS; ASPARTIC ACID; CYSTEINE; DYSTROGLYCANS; DYSTROPHIN; GENETIC VARIATION; HUMANS; MICE; MICE, TRANSGENIC; MUSCULAR DYSTROPHY, DUCHENNE; MUTATION, MISSENSE; PROTEIN FOLDING; PROTEIN STABILITY; ZINC FINGERS;

EID: 84891912677     PISSN: 10597794     EISSN: 10981004     Source Type: Journal    
DOI: 10.1002/humu.22479     Document Type: Article

References (52)

1. Ahmed N, Nguyen TM, Morris GE. 1998. Flexible hinges in dystrophin. Biochem Soc Trans 26:S310.
2. Amann KJ, Renley BA, Ervasti JM. 1998. A cluster of basic repeats in the dystrophin rod domain binds F-actin through an electrostatic interaction. J Biol Chem 273:28419-28423.
3. Bies RD, Caskey CT, Fenwick R. 1992. An intact cysteine-rich domain is required for dystrophin function. J Clin Invest 90:666-672.
4. Braakman I, Bulleid NJ. 2011. Protein folding and modification in the mammalian endoplasmic reticulum. Annu Rev Biochem 80:71-99.
5. Brenman JE, Chao DS, Gee SH, McGee AW, Craven SE, Santillano DR, Wu Z, Huang F, Xia H, Peters MF, Froehner SC, Bredt DS. 1996. Interaction of nitric oxide synthase with the postsynaptic density protein PSD-95 and alpha1-syntrophin mediated by PDZ domains. Cell 84:757-767.
6. Castello A, Brocheriou V, Chafey P, Kahn A, Gilgenkrantz H. 1996. Characterization of the dystrophin-syntrophin interaction using the two-hybrid system in yeast. FEBS Lett 383:124-128.
7. Claessen JH, Kundrat L, Ploegh HL. 2012. Protein quality control in the ER: balancing the ubiquitin checkbook. Trends Cell Biol 22:22-32.
8. Cote PD, Moukhles H, Carbonetto S. 2002. Dystroglycan is not required for localization of dystrophin, syntrophin, and neuronal nitric-oxide synthase at the sarcolemma but regulates integrin alpha 7B expression and caveolin-3 distribution. J Biol Chem 277:4672-4679.
9. Cox GA, Sunada Y, Campbell KP, Chamberlain JS. 1994. Dp71 can restore the dystrophin-associated glycoprotein complex in muscle but fails to prevent dystrophy. Nat Genet 8:333-339.
10. Crosbie RH, Yamada H, Venzke DP, Lisanti MP, Campbell KP. 1998. Caveolin-3 is not an integral component of the dystrophin glycoprotein complex. FEBS Lett 427:279-282.
11. Deconinck N, Dan B. 2007. Pathophysiology of duchenne muscular dystrophy: current hypotheses. Pediatr Neurol 36:1-7.
12. Draviam RA, Wang B, Li J, Xiao X, Watkins SC. 2006. Mini-dystrophin efficiently incorporates into the dystrophin protein complex in living cells. J Muscle Res Cell Motil 27:53-67.
13. Flanigan KM, Dunn DM, von Niederhausern A, Soltanzadeh P, Gappmaier E, Howard MT, Sampson JB, Mendell JR, Wall C, King WM, Pestronk A, Florence JM, et al. 2009. Mutational spectrum of DMD mutations in dystrophinopathy patients: application of modern diagnostic techniques to a large cohort. Hum Mutat 30:1657-1666.
14. Flanigan KM, von Niederhausern A, Dunn DM, Alder J, Mendell JR, Weiss RB. 2003. Rapid direct sequence analysis of the dystrophin gene. Am J Hum Genet 72:931-939.
15. Garcia RA, Vasudevan K, Buonanno A. 2000. The neuregulin receptor ErbB-4 interacts with PDZ-containing proteins at neuronal synapses. Proc Natl Acad Sci USA 97:3596-3601.
16. Gee SH, Madhavan R, Levinson SR, Caldwell JH, Sealock R, Froehner SC. 1998. Interaction of muscle and brain sodium channels with multiple members of the syntrophin family of dystrophin-associated proteins. J Neurosci 18:128-137.
17. Goldberg LR, Hausmanowa-Petrusewicz I, Fidzianska A, Duggan DJ, Steinberg LS, Hoffman EP. 1998. A dystrophin missense mutation showing persistence of dystrophin and dystrophin-associated proteins yet a severe phenotype. Ann Neurol 44:971-976.
18. Greenberg DS, Sunada Y, Campbell KP, Yaffe D, Nudel U. 1994. Exogenous Dp71 restores the levels of dystrophin associated proteins but does not alleviate muscle damage in mdx mice. Nat Genet 8:340-344.
19. Hartley JL, Temple GF, Brasch MA. 2000. DNA cloning using in vitro site-specific recombination. Genome Res 10:1788-1795.
20. Helliwell TR, Ellis JM, Mountford RC, Appleton RE, Morris GE. 1992. A truncated dystrophin lacking the C-terminal domains is localized at the muscle membrane. Am J Hum Genet 50:508-514.
21. Henderson DM, Lee A, Ervasti JM. 2010. Disease-causing missense mutations in actin binding domain 1 of dystrophin induce thermodynamic instability and protein aggregation. Proc Natl Acad Sci USA 107:9632-9637.
22. Henderson DM, Lin AY, Thomas DD, Ervasti JM. 2012. The carboxy-terminal third of dystrophin enhances actin binding activity. J Mol Biol 416:414-424.
23. Hnia K, Zouiten D, Cantel S, Chazalette D, Hugon G, Fehrentz JA, Masmoudi A, Diment A, Bramham J, Mornet D, Winder SJ. 2007. ZZ domain of dystrophin and utrophin: topology and mapping of a beta-dystroglycan interaction site. Biochem J 401:667-677.
24. Hoffman EP, Garcia CA, Chamberlain JS, Angelini C, Lupski JR, Fenwick R. 1991. Is the carboxyl-terminus of dystrophin required for membrane association? A novel, severe case of Duchenne muscular dystrophy. Ann Neurol 30:605-610.
25. Huang X, Poy F, Zhang R, Joachimiak A, Sudol M, Eck MJ. 2000. Structure of a WW domain containing fragment of dystrophin in complex with beta-dystroglycan. Nat Struct Biol 7:634-638.
26. Ishikawa-Sakurai M, Yoshida M, Imamura M, Davies KE, Ozawa E. 2004. ZZ domain is essentially required for the physiological binding of dystrophin and utrophin to beta-dystroglycan. Hum Mol Genet 13:693-702.
27. James M, Nuttall A, Ilsley JL, Ottersbach K, Tinsley JM, Sudol M, Winder SJ. 2000. Adhesion-dependent tyrosine phosphorylation of (beta)-dystroglycan regulates its interaction with utrophin. J Cell Sci 113(Pt 10):1717-1726.
28. Johnson EK, Li B, Yoon JH, Flanigan KM, Martin PT, Ervasti J, Montanaro F. 2013. Identification of new dystroglycan complexes in skeletal muscle. PLoS One 8: e73224.
29. Johnson EK, Zhang L, Adams ME, Phillips A, Freitas MA, Froehner SC, Green-Church KB, Montanaro F. 2012. Proteomic analysis reveals new cardiac-specific dystrophin-associated proteins. PLoS One 7:e43515.
30. Jung D, Yang B, Meyer J, Chamberlain JS, Campbell KP. 1995. Identification and characterization of the dystrophin anchoring site on beta-dystroglycan. J Biol Chem 270:27305-27310.
31. Koenig M, Monaco AP, Kunkel LM. 1988. The complete sequence of dystrophin predicts a rod-shaped cytoskeletal protein. Cell 53:219-228.
32. Kramarcy NR, Vidal A, Froehner SC, Sealock R. 1994. Association of utrophin and multiple dystrophin short forms with the mammalian M(r) 58, 000 dystrophin-associated protein (syntrophin). J Biol Chem 269:2870-2876.
33. Lenk U, Oexle K, Voit T, Ancker U, Hellner KA, Speer A, Hubner C. 1996. A cysteine 3340 substitution in the dystroglycan-binding domain of dystrophin associated with Duchenne muscular dystrophy, mental retardation and absence of the ERG b-wave. Hum Mol Genet 5:973-975.
34. McNally EM, de Sa Moreira E, Duggan DJ, Bonnemann CG, Lisanti MP, Lidov HG, Vainzof M, Passos-Bueno MR, Hoffman EP, Zatz M, Kunkel LM. 1998. Caveolin-3 in muscular dystrophy. Hum Mol Genet 7:871-877.
35. Morris GE, Sedgwick SG, Ellis JM, Pereboev A, Chamberlain JS, Nguyen thi M. 1998. An epitope structure for the C-terminal domain of dystrophin and utrophin. Biochemistry 37:11117-11127.
36. Newey SE, Benson MA, Ponting CP, Davies KE, Blake DJ. 2000. Alternative splicing of dystrobrevin regulates the stoichiometry of syntrophin binding to the dystrophin protein complex. Curr Biol 10:1295-1298.
37. Nguyen TM, Ginjaar IB, van Ommen GJ, Morris GE. 1992. Monoclonal antibodies for dystrophin analysis. Epitope mapping and improved binding to SDS-treated muscle sections. Biochem J 288(Pt 2):663-668.
38. Niesen FH, Berglund H, Vedadi M. 2007. The use of differential scanning fluorimetry to detect ligand interactions that promote protein stability. Nat Protoc 2:2212-2221.
39. Ponting CP, Blake DJ, Davies KE, Kendrick-Jones J, Winder SJ. 1996. ZZ and TAZ: new putative zinc fingers in dystrophin and other proteins. Trends Biochem Sci 21:11-13.
40. Prior TW, Papp AC, Snyder PJ, Burghes AH, Bartolo C, Sedra MS, Western LM, Mendell JR. 1993. A missense mutation in the dystrophin gene in a Duchenne muscular dystrophy patient. Nat Genet 4:357-360.
41. Rafael JA, Cox GA, Corrado K, Jung D, Campbell KP, Chamberlain JS. 1996. Forced expression of dystrophin deletion constructs reveals structure-function correlations. J Cell Biol 134:93-102.
42. Recan D, Chafey P, Leturcq F, Hugnot JP, Vincent N, Tome F, Collin H, Simon D, Czernichow P, Nicholson LV, et al. 1992. Are cysteine-rich and COOH-terminal domains of dystrophin critical for sarcolemmal localization? J Clin Invest 89:712-716.
43. Rentschler S, Linn H, Deininger K, Bedford MT, Espanel X, Sudol M. 1999. The WW domain of dystrophin requires EF-hands region to interact with beta-dystroglycan. Biol Chem 380:431-442.
44. Ron D, Walter P. 2007. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8:519-529.
45. Rybakova IN, Humston JL, Sonnemann KJ, Ervasti JM. 2006. Dystrophin and utrophin bind actin through distinct modes of contact. J Biol Chem 281:9996-10001.
46. Sadoulet-Puccio HM, Rajala M, Kunkel LM. 1997. Dystrobrevin and dystrophin: an interaction through coiled-coil motifs. Proc Natl Acad Sci USA 94:12413-12418.
47. Scott JM, Li S, Harper SQ, Welikson R, Bourque D, DelloRusso C, Hauschka SD, Chamberlain JS. 2002. Viral vectors for gene transfer of micro-, mini-, or full-length dystrophin. Neuromuscul Disord 12(Suppl 1):S23-S29.
48. Singh SM, Kongari N, Cabello-Villegas J, Mallela KM. 2010. Missense mutations in dystrophin that trigger muscular dystrophy decrease protein stability and lead to cross-beta aggregates. Proc Natl Acad Sci USA 107:15069-15074.
49. Suzuki A, Yoshida M, Ozawa E. 1995. Mammalian alpha 1- and beta 1-syntrophin bind to the alternative splice-prone region of the dystrophin COOH terminus. J Cell Biol 128:373-381.
50. Venema VJ, Ju H, Zou R, Venema RC. 1997. Interaction of neuronal nitric-oxide synthase with caveolin-3 in skeletal muscle. Identification of a novel caveolin scaffolding/inhibitory domain. J Biol Chem 272:28187-28190.
51. Wang B, Li J, Xiao X. 2000. Adeno-associated virus vector carrying human minidystrophin genes effectively ameliorates muscular dystrophy in mdx mouse model. Proc Natl Acad Sci USA 97:13714-13719.
52. Yang B, Jung D, Rafael JA, Chamberlain JS, Campbell KP. 1995. Identification of alpha-syntrophin binding to syntrophin triplet, dystrophin, and utrophin. J Biol Chem 270:4975-4978.