Calpains Mediate Integrin Attachment Complex Maintenance of Adult Muscle in
Two components of integrin containing attachment complexes, UNC-97/PINCH and UNC-112/MIG-2/Kindlin-2, were recently identified as negative regulators of muscle protein degradation and as having decreased mRNA levels in response to spaceflight. Integrin complexes transmit force between the inside and outside of muscle cells and signal changes in muscle size in response to force and, perhaps, disuse. We therefore investigated the effects of acute decreases in expression of the genes encoding these multi-protein complexes. We find that in fully developed adult Caenorhabditis elegans muscle, RNAi against genes encoding core, and peripheral, members of these complexes induces protein degradation, myofibrillar and mitochondrial dystrophies, and a movement defect. Genetic disruption of Z-line– or M-line–specific complex members is sufficient to induce these defects. We confirmed that defects occur in temperature-sensitive mutants for two of the genes: unc-52, which encodes the extra-cellular ligand Perlecan, and unc-112, which encodes the intracellular component Kindlin-2. These results demonstrate that integrin containing attachment complexes, as a whole, are required for proper maintenance of adult muscle. These defects, and collapse of arrayed attachment complexes into ball like structures, are blocked when DIM-1 levels are reduced. Degradation is also blocked by RNAi or drugs targeting calpains, implying that disruption of integrin containing complexes results in calpain activation. In wild-type animals, either during development or in adults, RNAi against calpain genes results in integrin muscle attachment disruptions and consequent sub-cellular defects. These results demonstrate that calpains are required for proper assembly and maintenance of integrin attachment complexes. Taken together our data provide in vivo evidence that a calpain-based molecular repair mechanism exists for dealing with attachment complex disruption in adult muscle. Since C. elegans lacks satellite cells, this mechanism is intrinsic to the muscles and raises the question if such a mechanism also exists in higher metazoans.
Vyšlo v časopise:
Calpains Mediate Integrin Attachment Complex Maintenance of Adult Muscle in. PLoS Genet 8(1): e32767. doi:10.1371/journal.pgen.1002471
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002471
Souhrn
Two components of integrin containing attachment complexes, UNC-97/PINCH and UNC-112/MIG-2/Kindlin-2, were recently identified as negative regulators of muscle protein degradation and as having decreased mRNA levels in response to spaceflight. Integrin complexes transmit force between the inside and outside of muscle cells and signal changes in muscle size in response to force and, perhaps, disuse. We therefore investigated the effects of acute decreases in expression of the genes encoding these multi-protein complexes. We find that in fully developed adult Caenorhabditis elegans muscle, RNAi against genes encoding core, and peripheral, members of these complexes induces protein degradation, myofibrillar and mitochondrial dystrophies, and a movement defect. Genetic disruption of Z-line– or M-line–specific complex members is sufficient to induce these defects. We confirmed that defects occur in temperature-sensitive mutants for two of the genes: unc-52, which encodes the extra-cellular ligand Perlecan, and unc-112, which encodes the intracellular component Kindlin-2. These results demonstrate that integrin containing attachment complexes, as a whole, are required for proper maintenance of adult muscle. These defects, and collapse of arrayed attachment complexes into ball like structures, are blocked when DIM-1 levels are reduced. Degradation is also blocked by RNAi or drugs targeting calpains, implying that disruption of integrin containing complexes results in calpain activation. In wild-type animals, either during development or in adults, RNAi against calpain genes results in integrin muscle attachment disruptions and consequent sub-cellular defects. These results demonstrate that calpains are required for proper assembly and maintenance of integrin attachment complexes. Taken together our data provide in vivo evidence that a calpain-based molecular repair mechanism exists for dealing with attachment complex disruption in adult muscle. Since C. elegans lacks satellite cells, this mechanism is intrinsic to the muscles and raises the question if such a mechanism also exists in higher metazoans.
Zdroje
1. FebbraioMAPedersenBK 2005 Contraction-induced myokine production and release: is skeletal muscle an endocrine organ? Exerc Sport Sci Rev 33 114 119
2. HillAVHartreeW 1920 The four phases of heat-production of muscle. J Physiol 54 84 128
3. HuxleyAFNiedergerkeR 1954 Structural changes in muscle during contraction; interference microscopy of living muscle fibres. Nature 173 971 973
4. SpargoEPrattOEDanielPM 1979 Metabolic functions of skeletal muscles of man, mammals, birds and fishes: a review. J R Soc Med 72 921 925
5. ClarkKAMcElhinnyASBeckerleMCGregorioCC 2002 Striated muscle cytoarchitecture: an intricate web of form and function. Annu Rev Cell Dev Biol 18 637 706
6. ChanceBLeighJSJrClarkBJMarisJKentJ 1985 Control of oxidative metabolism and oxygen delivery in human skeletal muscle: a steady-state analysis of the work/energy cost transfer function. Proc Natl Acad Sci U S A 82 8384 8388
7. TisdaleMJ 2000 Protein Loss in Cancer Cachexia. Science 289 2293 2294
8. LandiFRussoALiperotiRPahorMTosatoM 2010 Midarm muscle circumference, physical performance and mortality: Results from the aging and longevity study in the Sirente geographic area (ilSIRENTE study). Clinical Nutrition 29 441 447
9. JanssenIShepardDSKatzmarzykPTRoubenoffR 2004 The Healthcare Costs of Sarcopenia in the United States. Journal of the American Geriatrics Society 52 80 85
10. YelinE 2003 Cost of musculoskeletal diseases: impact of work disability and functional decline. The Journal of Rheumatology 68 8 11
11. ArrigoA-PTanakaKGoldbergALWelchWJ 1988 Identity of the 19S ‘prosome’ particle with the large multifunctional protease complex of mammalian cells (the proteasome). Nature 331 192 194
12. HershkoACiechanoverARoseIA 1979 Resolution of the ATP-dependent proteolytic system from reticulocytes: a component that interacts with ATP. Proc Natl Acad Sci U S A 76 3107 3110
13. NovikoffABBeaufayHde DuveC 1956 ELECTRON MICROSCOPY OF LYSOSOME-RICH FRACTIONS FROM RAT LIVER. The Journal of Biophysical and Biochemical Cytology 2 179 184
14. Murachi TTKHatanakaMMurakamiT 1980 Intracellular Ca2+-dependent protease (calpain) and its high-molecular-weight endogenous inhibitor (calpastatin). Advances in Enzyme Regulation 19 18
15. YuanJShahamSLedouxSEllisHMHorvitzHR 1993 The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1[beta]-converting enzyme. Cell 75 641 652
16. SandriM 2008 Signaling in Muscle Atrophy and Hypertrophy. Physiology 23 160 170
17. ZdinakLAGreenbergIBSzewczykNJBarmadaSJCardamone-RaynerM 1997 Transgene-coded chimeric proteins as reporters of intracellular proteolysis: Starvation-induced catabolism of a lacZ fusion protein in muscle cells of Caenorhabditis elegans. Journal of Cellular Biochemistry 67 143 153
18. SzewczykNHartmanJBarmadaSJacobsonL 2000 Genetic defects in acetylcholine signalling promote protein degradation in muscle cells of Caenorhabditis elegans. J Cell Sci 113 2003 2010
19. SzewczykNJJacobsonLA 2003 Activated EGL-15 FGF receptor promotes protein degradation in muscles of Caenorhabditis elegans. EMBO J 22 5058 5067
20. SzewczykNJPetersonBKBarmadaSJParkinsonLPJacobsonLA 2007 Opposed growth factor signals control protein degradation in muscles of Caenorhabditis elegans. EMBO J 26 935 943
21. BulowHEBoulinTHobertO 2004 Differential functions of the C. elegans FGF receptor in axon outgrowth and maintenance of axon position. Neuron 42 367 374
22. HigashibataASzewczykNJConleyCAImamizo-SatoMHigashitaniA 2006 Decreased expression of myogenic transcription factors and myosin heavy chains in Caenorhabditis elegans muscles developed during spaceflight. J Exp Biol 209 3209 3218
23. HobertOMoermanDGClarkKABeckerleMCRuvkunG 1999 A Conserved LIM Protein That Affects Muscular Adherens Junction Integrity and Mechanosensory Function in Caenorhabditis elegans. The Journal of Cell Biology 144 45 57
24. RogalskiTMMullenGPGilbertMMWilliamsBDMoermanDG 2000 The UNC-112 Gene in Caenorhabditis elegansEncodes a Novel Component of Cell–Matrix Adhesion Structures Required for Integrin Localization in the Muscle Cell Membrane. The Journal of Cell Biology 150 253 264
25. LeeMCramEJShenBSchwarzbauerJE 2001 Roles for β(pat-3) Integrins in Development and Function ofCaenorhabditis elegans Muscles and Gonads. Journal of Biological Chemistry 276 36404 36410
26. GordonSEFlückMBoothFW 2001 Selected Contribution: Skeletal muscle focal adhesion kinase, paxillin, and serum response factor are loading dependent. Journal of Applied Physiology 90 1174 1183
27. KlossnerSDurieuxA-CFreyssenetDFlueckM 2009 Mechano-transduction to muscle protein synthesis is modulated by FAK. European Journal of Applied Physiology 106 389 398
28. LecroiseyCSégalatLGieselerK 2007 The C. elegans; dense body: anchoring and signaling structure of the muscle. Journal of Muscle Research and Cell Motility 28 79 87
29. ShephardFAdenleAAJacobsonLASzewczykNJ 2011 Identification and Functional Clustering of Genes Regulating Muscle Protein Degradation from amongst the Known C. elegans Muscle Mutants. PLoS ONE 6 e24686 doi:10.1371/journal.pone.0024686
30. MoermanDGWilliamsBD 2006 Sarcomere assembly in C. elegans muscle. WormBook 1 16
31. QadotaHBenianGM 2010 Molecular structure of sarcomere-to-membrane attachment at M-Lines in C. elegans muscle. J Biomed Biotechnol 2010 864749
32. WarnerAQadotaHBenianGMVoglAWMoermanDG 2011 The Caenorhabditis elegans paxillin orthologue, PXL-1, is required for pharyngeal muscle contraction and for viability. Mol Biol Cell 22 2551 2563
33. LecroiseyCMartinEMariolMCGrangerLSchwabY 2008 DYC-1, a protein functionally linked to dystrophin in Caenorhabditis elegans is associated with the dense body, where it interacts with the muscle LIM domain protein ZYX-1. Mol Biol Cell 19 785 796
34. HoppePEChauJFlanaganKAReedyARSchrieferLA 2010 Caenorhabditis elegans unc-82 encodes a serine/threonine kinase important for myosin filament organization in muscle during growth. Genetics 184 79 90
35. BenianGMTinleyTLTangXBorodovskyM 1996 The Caenorhabditis elegans gene unc-89, required fpr muscle M-line assembly, encodes a giant modular protein composed of Ig and signal transduction domains. J Cell Biol 132 835 848
36. HikitaTQadotaHTsuboiDTayaSMoermanDG 2005 Identification of a novel Cdc42 GEF that is localized to the PAT-3-mediated adhesive structure. Biochemical and Biophysical Research Communications 335 139 145
37. SzewczykNJPetersonBKJacobsonLA 2002 Activation of Ras and the Mitogen-Activated Protein Kinase Pathway Promotes Protein Degradation in Muscle Cells of Caenorhabditis elegans. Mol Cell Biol 22 4181 4188
38. FostelJLBenner CosteLJacobsonLA 2003 Degradation of transgene-coded and endogenous proteins in the muscles of Caenorhabditis elegans. Biochemical and Biophysical Research Communications 312 173 177
39. BenianGMTinleyTLTangXBorodovskyM 1996 The Caenorhabditis elegans gene unc-89, required fpr muscle M-line assembly, encodes a giant modular protein composed of Ig and signal transduction domains. The Journal of Cell Biology 132 835 848
40. RogalskiTMWilliamsBDMullenGPMoermanDG 1993 Products of the unc-52 gene in Caenorhabditis elegans are homologous to the core protein of the mammalian basement membrane heparan sulfate proteoglycan. Genes Dev 7 1471 1484
41. RogalskiTMGilbertMMDevenportDNormanKRMoermanDG 2003 DIM-1, a Novel Immunoglobulin Superfamily Protein in Caenorhabditis elegans, Is Necessary for Maintaining Bodywall Muscle Integrity. Genetics 163 905 915
42. OteyCARachlinAMozaMArnemanDCarpenO 2005 The palladin/myotilin/myopalladin family of actin-associated scaffolds. Int Rev Cytol 246 31 58
43. PlenefischJDZhuXHedgecockEM 2000 Fragile skeletal muscle attachments in dystrophic mutants of Caenorhabditis elegans: isolation and characterization of the mua genes. Development 127 1197 1207
44. MariolMCMartinEChambonnierLSegalatL 2007 Dystrophin-dependent muscle degeneration requires a fully functional contractile machinery to occur in C. elegans. Neuromuscul Disord 17 56 60
45. WilliamsBDWaterstonRH 1994 Genes critical for muscle development and function in Caenorhabditis elegans identified through lethal mutations. J Cell Biol 124 475 490
46. MeissnerBWarnerAWongKDubeNLorchA 2009 An Integrated Strategy to Study Muscle Development and Myofilament Structure in Caenorhabditis elegans. PLoS Genet 5 e1000537 doi:10.1371/journal.pgen.1000537
47. NormanKRCordesSQadotaHRahmaniPMoermanDG 2007 UNC-97/PINCH is involved in the assembly of integrin cell adhesion complexes in Caenorhabditis elegans body wall muscle. Developmental Biology 309 45 55
48. PerkinsADEllisSJAsghariPShamsianAMooreEDW 2010 Integrin-mediated adhesion maintains sarcomeric integrity. Developmental Biology 338 15 27
49. KohTJEscobedoJ 2004 Cytoskeletal disruption and small heat shock protein translocation immediately after lengthening contractions. Am J Physiol Cell Physiol 286 C713 722
50. LangeSXiangFYakovenkoAViholaAHackmanP 2005 The kinase domain of titin controls muscle gene expression and protein turnover. Science 308 1599 1603
51. IchishitaRTanakaKSugiuraYSayanoTMiharaK 2008 An RNAi Screen for Mitochondrial Proteins Required to Maintain the Morphology of the Organelle in Caenorhabditis elegans. Journal of Biochemistry 143 449 454
52. StarrDAHanM 2002 Role of ANC-1 in Tethering Nuclei to the Actin Cytoskeleton. Science 298 406 409
53. IwaiTTanonakaKInoueRKasaharaSMotegiK 2002 Sodium accumulation during ischemia induces mitochondrial damage in perfused rat hearts. Cardiovasc Res 55 141 149
54. JospinMMariolMCSegalatLAllardB 2004 Patch clamp study of the UNC-105 degenerin and its interaction with the LET-2 collagen in Caenorhabditis elegans muscle. J Physiol 557 379 388
55. BrodayLKolotuevIDidierCBhoumikAPodbilewiczB 2004 The LIM domain protein UNC-95 is required for the assembly of muscle attachment structures and is regulated by the RING finger protein RNF-5 in C. elegans. The Journal of Cell Biology 165 857 867
56. KovacsALGordonPBGrotterodEMSeglenPO 1998 Inhibition of hepatocytic autophagy by adenosine, adenosine analogs and AMP. Biol Chem 379 1341 1347
57. SyntichakiPXuKDriscollMTavernarakisN 2002 Specific aspartyl and calpain proteases are required for neurodegeneration in C. elegans. Nature 419 939 944
58. FoxRMWatsonJDVon StetinaSEMcDermottJBrodiganTM 2007 The embryonic muscle transcriptome of Caenorhabditis elegans. Genome Biol 8 R188
59. EtheridgeTNemotoKHashizumeTMoriCSugimotoT 2011 The Effectiveness of RNAi in Caenorhabditis elegans Is Maintained during Spaceflight. PLoS ONE 6 e20459 doi:10.1371/journal.pone.0020459
60. LebartMCBenyaminY 2006 Calpain involvement in the remodeling of cytoskeletal anchorage complexes. FEBS J 273 3415 3426
61. BeckmannJSSpencerM 2008 Calpain 3, the “gatekeeper” of proper sarcomere assembly, turnover and maintenance. Neuromuscul Disord 18 913 921
62. OjimaKKawabataYNakaoHNakaoKDoiN 2010 Dynamic distribution of muscle-specific calpain in mice has a key role in physical-stress adaptation and is impaired in muscular dystrophy. The Journal of Clinical Investigation 120 2672 2683
63. RichardIBrouxOAllamandVFougerousseFChiannilkulchaiN 1995 Mutations in the proteolytic enzyme calpain 3 cause limb-girdle muscular dystrophy type 2A. Cell 81 27 40
64. ChartonKDanièleNViholaARoudautCGicquelE 2010 Removal of the calpain 3 protease reverses the myopathology in a mouse model for titinopathies. Human Molecular Genetics 19 4608 4624
65. FrancisRWaterstonRH 1991 Muscle cell attachment in Caenorhabditis elegans. J Cell Biol 114 465 479
66. HreskoMCSchrieferLAShrimankarPWaterstonRH 1999 Myotactin, a novel hypodermal protein involved in muscle-cell adhesion in Caenorhabditis elegans. J Cell Biol 146 659 672
67. HallDHAltunZF 2008 C. elegans Atlas: Cold Spring Harbor Laboratory press
68. BelkinAMRettaSFPletjushkinaOYBalzacFSilengoL 1997 Muscle beta1D integrin reinforces the cytoskeleton-matrix link: modulation of integrin adhesive function by alternative splicing. J Cell Biol 139 1583 1595
69. GiannoneGSheetzMP 2006 Substrate rigidity and force define form through tyrosine phosphatase and kinase pathways. Trends Cell Biol 16 213 223
70. ByerlyLCassadaRCRussellRL 1976 The life cycle of the nematode Caenorhabditis elegans. I. Wild-type growth and reproduction. Dev Biol 51 23 33
71. KrauseM 1995 MyoD and myogenesis in C. elegans. Bioessays 17 219 228
72. HarfeBDBrandaCSKrauseMSternMJFireA 1998 MyoD and the specification of muscle and non-muscle fates during postembryonic development of the C. elegans mesoderm. Development 125 2479 2488
73. GhoshSRHopeIA 2010 Determination of the mobility of novel and established Caenorhabditis elegans sarcomeric proteins in vivo. Eur J Cell Biol 89 437 448
74. RogalskiTMGilchristEJMullenGPMoermanDG 1995 Mutations in the unc-52 gene responsible for body wall muscle defects in adult Caenorhabditis elegans are located in alternatively spliced exons. Genetics 139 159 169
75. SpartzAKHermanRKShawJE 2004 SMU-2 and SMU-1, Caenorhabditis elegans homologs of mammalian spliceosome-associated proteins RED and fSAP57, work together to affect splice site choice. Mol Cell Biol 24 6811 6823
76. SorimachiHHataSOnoY 2010 Expanding members and roles of the calpain superfamily and their genetically modified animals. Exp Anim 59 549 566
77. KammengaJEDoroszukARiksenJAHazendonkESpiridonL 2007 A Caenorhabditis elegans wild type defies the temperature-size rule owing to a single nucleotide polymorphism in tra-3. PLoS Genet 3 e34 doi:10.1371/journal.pgen.0030034
78. MackenzieJMJrGarceaRLZengelJMEpsteinHF 1978 Muscle development in Caenorhabditis elegans: Mutants exhibiting retarded sarcomere construction. Cell 15 751 762
79. KimuraKTanakaNNakamuraNTakanoSOhkumaS 2007 Knockdown of Mitochondrial Heat Shock Protein 70 Promotes Progeria-like Phenotypes in Caenorhabditis elegans. Journal of Biological Chemistry 282 5910 5918
80. MargalitANeufeldEFeinsteinNWilsonKLPodbilewiczB 2007 Barrier to autointegration factor blocks premature cell fusion and maintains adult muscle integrity in C. elegans. The Journal of Cell Biology 178 661 673
81. CrameriRMAagaardPQvortrupKLangbergHOlesenJ 2007 Myofibre damage in human skeletal muscle: effects of electrical stimulation versus voluntary contraction. The Journal of Physiology 583 365 380
82. MayerUSaherGFasslerRBornemannAEchtermeyerF 1997 Absence of integrin [alpha]7 causes a novel form of muscular dystrophy. Nat Genet 17 318 323
83. ShayeDDGreenwaldI 2011 OrthoList: A Compendium of C. elegans Genes with Human Orthologs. PLoS ONE 6 e20085 doi:10.1371/journal.pone.0020085
84. BrennerS 1974 The genetics of Caenorhabditis elegans. Genetics 77 71 94
85. FireAXuSMontgomeryMKKostasSADriverSE 1998 Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391 806 811
86. BenedettiCHaynesCMYangYHardingHPRonD 2006 Ubiquitin-like protein 5 positively regulates chaperone gene expression in the mitochondrial unfolded protein response. Genetics 174 229 239
87. FraserAGKamathRSZipperlenPMartinez-CamposMSohrmannM 2000 Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature 408 325 330
88. ChenNHarrisTWAntoshechkinIBastianiCBieriT 2005 WormBase: a comprehensive data resource for Caenorhabditis biology and genomics. Nucleic Acids Res 33 D383 389
89. RualJFCeronJKorethJHaoTNicotAS 2004 Toward improving Caenorhabditis elegans phenome mapping with an ORFeome-based RNAi library. Genome Res 14 2162 2168
90. LinJJ 1981 Monoclonal antibodies against myofibrillar components of rat skeletal muscle decorate the intermediate filaments of cultured cells. Proc Natl Acad Sci U S A 78 2335 2339
91. FrancisGRWaterstonRH 1985 Muscle organization in Caenorhabditis elegans: localization of proteins implicated in thin filament attachment and I-band organization. J Cell Biol 101 1532 1549
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2012 Číslo 1
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Microenvironmental Regulation by Fibrillin-1
- Poly(ADP-Ribose) Polymerase 1 (PARP-1) Regulates Ribosomal Biogenesis in Nucleoli
- Parallel Mapping and Simultaneous Sequencing Reveals Deletions in and Associated with Discrete Inherited Disorders in a Domestic Dog Breed
- Two-Component Elements Mediate Interactions between Cytokinin and Salicylic Acid in Plant Immunity