A human skeletal muscle interactome centered on proteins involved in muscular dystrophies: LGMD interactome
Tóm tắt
The complexity of the skeletal muscle and the identification of numerous human disease-causing mutations in its constitutive proteins make it an interesting tissue for proteomic studies aimed at understanding functional relationships of interacting proteins in both health and diseases. We undertook a large-scale study using two-hybrid screens and a human skeletal-muscle cDNA library to establish a proteome-scale map of protein-protein interactions centered on proteins involved in limb-girdle muscular dystrophies (LGMD). LGMD is a group of more than 20 different neuromuscular disorders that principally affect the proximal pelvic and shoulder girdle muscles. The interaction network we unraveled incorporates 1018 proteins connected by 1492 direct binary interactions and includes 1420 novel protein-protein interactions. Computational, experimental and literature-based analyses were performed to assess the overall quality of this network. Interestingly, LGMD proteins were shown to be highly interconnected, in particular indirectly through sarcomeric proteins. In-depth mining of the LGMD-centered interactome identified new candidate genes for orphan LGMDs and other neuromuscular disorders. The data also suggest the existence of functional links between LGMD2B/dysferlin and gene regulation, between LGMD2C/γ-sarcoglycan and energy control and between LGMD2G/telethonin and maintenance of genome integrity. This dataset represents a valuable resource for future functional investigations.
Tài liệu tham khảo
Stelzl U, Worm U, Lalowski M, Haenig C, Brembeck FH, Goehler H, Stroedicke M, Zenkner M, Schoenherr A, Koeppen S: A human protein-protein interaction network: a resource for annotating the proteome. Cell. 2005, 122: 957-968. 10.1016/j.cell.2005.08.029.
Rual JF, Venkatesan K, Hao T, Hirozane-Kishikawa T, Dricot A, Li N, Berriz GF, Gibbons FD, Dreze M, Ayivi-Guedehoussou N: Towards a proteome-scale map of the human protein-protein interaction network. Nature. 2005, 437: 1173-1178. 10.1038/nature04209.
Ewing RM, Chu P, Elisma F, Li H, Taylor P, Climie S, McBroom-Cerajewski L, Robinson MD, O'Connor L, Li M: Large-scale mapping of human protein-protein interactions by mass spectrometry. Mol Syst Biol. 2007, 3: 89-
Bouwmeester T, Bauch A, Ruffner H, Angrand PO, Bergamini G, Croughton K, Cruciat C, Eberhard D, Gagneur J, Ghidelli S: A physical and functional map of the human TNF-alpha/NF-kappa B signal transduction pathway. Nat Cell Biol. 2004, 6: 97-105. 10.1038/ncb1086.
Goehler H, Lalowski M, Stelzl U, Waelter S, Stroedicke M, Worm U, Droege A, Lindenberg KS, Knoblich M, Haenig C: A protein interaction network links GIT1, an enhancer of huntingtin aggregation, to Huntington's disease. Mol Cell. 2004, 15: 853-865. 10.1016/j.molcel.2004.09.016.
Lim J, Hao T, Shaw C, Patel AJ, Szabo G, Rual JF, Fisk CJ, Li N, Smolyar A, Hill DE: A protein-protein interaction network for human inherited ataxias and disorders of Purkinje cell degeneration. Cell. 2006, 125: 801-814. 10.1016/j.cell.2006.03.032.
Nigro V, Aurino S, Piluso G: Limb girdle muscular dystrophies: update on genetic diagnosis and therapeutic approaches. Curr Opin Neurol. 2011, 24: 429-436. 10.1097/WCO.0b013e32834aa38d.
Aurino S, Piluso G, Saccone V, Cacciottolo M, D'Amico F, Dionisi M, Totaro A, Belsito A, Di Vicino U, Nigro V: Candidate-gene testing for orphan limb-girdle muscular dystrophies. Acta Myol. 2008, 27: 90-97.
Guglieri M, Straub V, Bushby K, Lochmuller H: Limb-girdle muscular dystrophies. Curr Opin Neurol. 2008, 21: 576-584. 10.1097/WCO.0b013e32830efdc2.
Krogh A, Larsson B, von Heijne G, Sonnhammer EL: Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol. 2001, 305: 567-580. 10.1006/jmbi.2000.4315.
Nielsen H, Engelbrecht J, Brunak S, von Heijne G: A neural network method for identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Int J Neural Syst. 1997, 8: 581-599. 10.1142/S0129065797000537.
Finn RD, Tate J, Mistry J, Coggill PC, Sammut SJ, Hotz HR, Ceric G, Forslund K, Eddy SR, Sonnhammer EL, Bateman A: The Pfam protein families database. Nucleic Acids Res. 2008, 36: D281-D288. 10.1093/nar/gkn226.
Vojtek AB, Hollenberg SM: Ras-Raf interaction: two-hybrid analysis. Methods Enzymol. 1995, 255: 331-342.
Formstecher E, Aresta S, Collura V, Hamburger A, Meil A, Trehin A, Reverdy C, Betin V, Maire S, Brun C: Protein interaction mapping: a Drosophila case study. Genome Res. 2005, 15: 376-384. 10.1101/gr.2659105.
Fromont-Racine M, Rain JC, Legrain P: Toward a functional analysis of the yeast genome through exhaustive two-hybrid screens. Nat Genet. 1997, 16: 277-282. 10.1038/ng0797-277.
Maiweilidan Y, Klauza I, Kordeli E: Novel interactions of ankyrins-G at the costameres: the muscle-specific Obscurin/Titin-Binding-related Domain (OTBD) binds plectin and filamin C. Exp Cell Res. 2011, 317: 724-736. 10.1016/j.yexcr.2011.01.002.
Alhamidi M, Kjeldsen Buvang E, Fagerheim T, Brox V, Lindal S, Van Ghelue M, Nilssen O: Fukutin-related protein resides in the Golgi cisternae of skeletal muscle fibres and forms disulfide-linked homodimers via an N-terminal interaction. PLoS One. 2011, 6: e22968-10.1371/journal.pone.0022968.
Burgo A, Proux-Gillardeaux V, Sotirakis E, Bun P, Casano A, Verraes A, Liem RK, Formstecher E, Coppey-Moisan M, Galli T: A molecular network for the transport of the TI-VAMP/VAMP7 vesicles from cell center to periphery. Dev Cell. 2012, 23: 166-180. 10.1016/j.devcel.2012.04.019.
Bolte S, Cordelieres FP: A guided tour into subcellular colocalization analysis in light microscopy. J Microsc. 2006, 224: 213-232. 10.1111/j.1365-2818.2006.01706.x.
Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R, Lopez R: InterProScan: protein domains identifier. Nucleic Acids Res. 2005, 33: W116-W120. 10.1093/nar/gki442.
Mulder NJ, Apweiler R, Attwood TK, Bairoch A, Bateman A, Binns D, Bork P, Buillard V, Cerutti L, Copley R: New developments in the InterPro database. Nucleic Acids Res. 2007, 35: D224-D228. 10.1093/nar/gkl841.
Turner B, Razick S, Turinsky AL, Vlasblom J, Crowdy EK, Cho E, Morrison K, Donaldson IM, Wodak SJ: iRefWeb: interactive analysis of consolidated protein interaction data and their supporting evidence. Database (Oxford). 2010, 2010: baq023-10.1093/database/baq023.
Sherman BT, Huang da W, Tan Q, Guo Y, Bour S, Liu D, Stephens R, Baseler MW, Lane HC, Lempicki RA: DAVID Knowledgebase: a gene-centered database integrating heterogeneous gene annotation resources to facilitate high-throughput gene functional analysis. BMC Bioinformatics. 2007, 8: 426-10.1186/1471-2105-8-426.
da Huang W, Sherman BT, Lempicki RA: Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009, 4: 44-57.
Muller A, MacCallum RM, Sternberg MJ: Structural characterization of the human proteome. Genome Res. 2002, 12: 1625-1641. 10.1101/gr.221202.
Hilfiker S, Greengard P, Augustine GJ: Coupling calcium to SNARE-mediated synaptic vesicle fusion. Nat Neurosci. 1999, 2: 104-106. 10.1038/5659.
Bansal D, Miyake K, Vogel SS, Groh S, Chen CC, Williamson R, McNeil PL, Campbell KP: Defective membrane repair in dysferlin-deficient muscular dystrophy. Nature. 2003, 423: 168-172. 10.1038/nature01573.
Vignal E, Blangy A, Martin M, Gauthier-Rouviere C, Fort P: Kinectin is a key effector of RhoG microtubule-dependent cellular activity. Mol Cell Biol. 2001, 21: 8022-8034. 10.1128/MCB.21.23.8022-8034.2001.
Scita G, Nordstrom J, Carbone R, Tenca P, Giardina G, Gutkind S, Bjarnegard M, Betsholtz C, Di Fiore PP: EPS8 and E3B1 transduce signals from Ras to Rac. Nature. 1999, 401: 290-293. 10.1038/45822.
Sarparanta J, Jonson PH, Golzio C, Sandell S, Luque H, Screen M, McDonald K, Stajich JM, Mahjneh I, Vihola A: Mutations affecting the cytoplasmic functions of the co-chaperone DNAJB6 cause limb-girdle muscular dystrophy. Nat Genet. 2012, 44: 450–455-S451-452.
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T: Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003, 13: 2498-2504. 10.1101/gr.1239303.
Legrain P, Selig L: Genome-wide protein interaction maps using two-hybrid systems. FEBS Lett. 2000, 480: 32-36. 10.1016/S0014-5793(00)01774-9.
Kahle JJ, Gulbahce N, Shaw CA, Lim J, Hill DE, Barabasi AL, Zoghbi HY: Comparison of an expanded ataxia interactome with patient medical records reveals a relationship between macular degeneration and ataxia. Hum Mol Genet. 2011, 20: 510-527. 10.1093/hmg/ddq496.
Tee JM, Peppelenbosch MP: Anchoring skeletal muscle development and disease: the role of ankyrin repeat domain containing proteins in muscle physiology. Crit Rev Biochem Mol Biol. 2010, 45: 318-330. 10.3109/10409238.2010.488217.
Ogut O, Hossain MM, Jin JP: Interactions between nebulin-like motifs and thin filament regulatory proteins. J Biol Chem. 2003, 278: 3089-3097. 10.1074/jbc.M205853200.
Bader GD, Hogue CW: Analyzing yeast protein-protein interaction data obtained from different sources. Nat Biotechnol. 2002, 20: 991-997. 10.1038/nbt1002-991.
de Morree A, Hensbergen PJ, van Haagen HH, Dragan I, Deelder AM, Hoen PA t, Frants RR, van der Maarel SM: Proteomic analysis of the dysferlin protein complex unveils its importance for sarcolemmal maintenance and integrity. PLoS One. 2010, 5: e13854-10.1371/journal.pone.0013854.
van Haagen HH, Hoen PA t, de Morree A, van Roon-Mom WM, Peters DJ, Roos M, Mons B, van Ommen GJ, Schuemie MJ: In silico discovery and experimental validation of new protein-protein interactions. Proteomics. 2011, 11: 843-853. 10.1002/pmic.201000398.
Cacciottolo M, Belcastro V, Laval S, Bushby K, di Bernardo D, Nigro V: Reverse engineering gene network identifies new dysferlin-interacting proteins. J Biol Chem. 2011, 286: 5404-5413. 10.1074/jbc.M110.173559.
Comi GP, Fortunato F, Lucchiari S, Bordoni A, Prelle A, Jann S, Keller A, Ciscato P, Galbiati S, Chiveri L: Beta-enolase deficiency, a new metabolic myopathy of distal glycolysis. Ann Neurol. 2001, 50: 202-207. 10.1002/ana.1095.
Palenzuela L, Andreu AL, Gamez J, Vila MR, Kunimatsu T, Meseguer A, Cervera C, Fernandez Cadenas I, van der Ven PF, Nygaard TG: A novel autosomal dominant limb-girdle muscular dystrophy (LGMD 1F) maps to 7q32.1-32.2. Neurology. 2003, 61: 404-406. 10.1212/01.WNL.0000073984.46546.4F.
Tang BL, Zhang T, Low DY, Wong ET, Horstmann H, Hong W: Mammalian homologues of yeast sec31p. An ubiquitously expressed form is localized to endoplasmic reticulum (ER) exit sites and is essential for ER-Golgi transport. J Biol Chem. 2000, 275: 13597-13604. 10.1074/jbc.275.18.13597.
Starling A, Kok F, Passos-Bueno MR, Vainzof M, Zatz M: A new form of autosomal dominant limb-girdle muscular dystrophy (LGMD1G) with progressive fingers and toes flexion limitation maps to chromosome 4p21. Eur J Hum Genet. 2004, 12: 1033-1040. 10.1038/sj.ejhg.5201289.
Townley AK, Feng Y, Schmidt K, Carter DA, Porter R, Verkade P, Stephens DJ: Efficient coupling of Sec23-Sec24 to Sec13-Sec31 drives COPII-dependent collagen secretion and is essential for normal craniofacial development. J Cell Sci. 2008, 121: 3025-3034. 10.1242/jcs.031070.
Kramerova I, Kudryashova E, Venkatraman G, Spencer MJ: Calpain 3 participates in sarcomere remodeling by acting upstream of the ubiquitin-proteasome pathway. Hum Mol Genet. 2007, 16: 1006-10.1093/hmg/ddm044.
Hack AA, Cordier L, Shoturma DI, Lam MY, Sweeney HL, McNally EM: Muscle degeneration without mechanical injury in sarcoglycan deficiency. Proc Natl Acad Sci U S A. 1999, 96: 10723-10728. 10.1073/pnas.96.19.10723.
Barton ER: Restoration of gamma-sarcoglycan localization and mechanical signal transduction are independent in murine skeletal muscle. J Biol Chem. 2010, 285: 17263-17270. 10.1074/jbc.M109.063990.
Knoll R, Linke WA, Zou P, Miocic S, Kostin S, Buyandelger B, Ku CH, Neef S, Bug M, Schafer K: Telethonin deficiency is associated with maladaptation to biomechanical stress in the mammalian heart. Circ Res. 2011, 109: 758-769. 10.1161/CIRCRESAHA.111.245787.