Regulation of nicotinic acetylcholine receptor turnover by MuRF1 connects muscle activity to endo/lysosomal and atrophy pathways

Age

Volumn 35, Issue 5, 2013, Pages 1663-1674

  Rudolf, Rüdigger ^a,b   Bogomolovas, Julius ^c   Strack, Siegfried ^a   Choi, Kyeong Rok ^a   Khan, Muzamil Majid ^a   Wagner, Anika ^a   Brohm, Kathrin ^c   Hanashima, Akira ^c   Gasch, Alexander ^c   Labeit, Dittmar ^c   Labeit, Siegfried ^c  

^a KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^b MANNHEIM UNIVERSITY OF APPLIED SCIENCES   (Germany)

^c UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Acetylcholine receptor; Atrophy; Endocytosis; MuRF1; Neuromuscular junction

Indexed keywords

BAX INTERACTING FACTOR 1; ENDOPHILIN; MEMBRANE PROTEIN; MUSCLE RING FINGER 1 PROTEIN; NICOTINIC RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; ENZYME REGULATION; IMMUNOFLUORESCENCE; IMMUNOFLUORESCENCE TEST; IN VIVO STUDY; LYSOSOME; MOLECULAR IMAGING; MOUSE; MUSCLE ATROPHY; MUSCLE CONTRACTION; NEUROMUSCULAR SYNAPSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION;

ANIMALS; DISEASE MODELS, ANIMAL; ENDOCYTOSIS; LYSOSOMES; MICE; MICE, INBRED C57BL; MUSCLE PROTEINS; MUSCLE, SKELETAL; MUSCULAR ATROPHY; NEUROMUSCULAR JUNCTION; RECEPTORS, NICOTINIC; UBIQUITIN-PROTEIN LIGASES;

EID: 84888768664     PISSN: 01619152     EISSN: 15744647     Source Type: Journal    
DOI: 10.1007/s11357-012-9468-9     Document Type: Article

References (63)

1. Adams V, Mangner N, Gasch A, Krohne C, Gielen S, Hirner S, Thierse HJ, Witt CC, Linke A, Schuler G, Labeit S (2008) Induction of MuRF1 is essential for TNF-alpha-induced loss of muscle function in mice. J Mol Biol 384:48-59
2. Akaaboune M, Culican SM, Turney SG, Lichtman JW (1999) Rapid and reversible effects of activity on acetylcholine receptor density at the neuromuscular junction in vivo. Science 286:503-507
3. Andonian MH, Fahim MA (1987) Effects of endurance exercise on the morphology of mouse neuromuscular junctions during ageing. J Neurocytol 16:589-599
4. Andonian MH, Fahim MA (1988) Endurance exercise alters the morphology of fast- and slow-twitch rat neuromuscular junctions. Int J Sports Med 9:218-223
5. Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, Clarke BA, Poueymirou WT, Panaro FJ, Na E, Dharmarajan K, Pan ZQ, Valenzuela DM, DeChiara TM, Stitt TN, Yancopoulos GD, Glass DJ (2001) Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294:1704-1708
6. Bruneau E, Sutter D, Hume RI, Akaaboune M (2005) Identification of nicotinic acetylcholine receptor recycling and its role in maintaining receptor density at the neuromuscular junction in vivo. J Neurosci 25:9949-9959
7. Butikofer L, Zurlinden A, Bolliger MF, Kunz B, Sonderegger P (2011) Destabilization of the neuromuscular junction by proteolytic cleavage of agrin results in precocious sarcopenia. FASEB J 25:4378-4393
8. Centner T, Yano J, Kimura E, McElhinny AS, Pelin K, Witt CC, Bang ML, Trombitas K, Granzier H, Gregorio CC, Sorimachi H, Labeit S (2001) Identification ofmuscle specific ring finger proteins as potential regulators of the titin kinase domain. J Mol Biol 306:717-726
9. Chai RJ, Vukovic J, Dunlop S, Grounds MD, Shavlakadze T (2011) Striking denervation of neuromuscular junctions without lumbar motoneuron loss in geriatric mouse muscle. PLoS One 6:e28090
10. Changeux JP, Kasai M, Lee CY (1970) Use of a snake venom toxin to characterize the cholinergic receptor protein. Proc Natl Acad Sci U S A 67:1241-1247
11. Chen J, Mizushige T, Nishimune H (2012) Active zone density is conserved during synaptic growth but impaired in aged mice. J Comp Neurol 520:434-452
12. Cheung ZH, Ip NY (2009) Endophilin B1: guarding the gate to destruction. Commun Integr Biol 2:130-132
13. Choi KR, Berrera M, Reischl M, Strack S, Albrizio M, Röder IV, Wagner A, Petersen Y, Hafner M, Zaccolo M, Rudolf R (2012) Rapsyn mediates subsynaptic anchoring of PKA type I and stabilisation of acetylcholine receptor in vivo. J Cell Sci 125:714-723
14. Clementi F, Sher E, Erroi A (1983) Acetylcholine receptor degradation: study of mechanism of action of inhibitory drugs. Eur J Cell Biol 29:274-280
15. Cohen S, Brault JJ, Gygi SP, Glass DJ, Valenzuela DM, Gartner C, Latres E, Goldberg AL (2009) During muscle atrophy, thick, but not thin, filament components are degraded by MuRF1-dependent ubiquitylation. J Cell Biol 185:1083-1095
16. Courtney J, Steinbach JH (1981) Age changes in neuromuscular junction morphology and acetylcholine receptor distribution on rat skeletal muscle fibres. J Physiol 320:435-447
17. Dona M, Sandri M, Rossini K, Dell'Aica I, Podhorska-Okolow M, Carraro U (2003) Functional in vivo gene transfer into the myofibers of adult skeletal muscle. Biochem Biophys Res Commun 312:1132-1138
18. Engel AG, Lindstrom JM, Lambert EH, Lennon VA (1977) Ultrastructural localization of the acetylcholine receptor in myasthenia gravis and in its experimental autoimmune model. Neurology 27:307-315
19. Fambrough DM (1979) Control of acetylcholine receptors in skeletal muscle. Physiol Rev 59:165-227
20. Fumagalli G, Engel AG, Lindstrom J (1982) Ultrastructural aspects of acetylcholine receptor turnover at the normal end-plate and in autoimmune myasthenia gravis. J Neuropathol Exp Neurol 41:567-579
21. Glass DJ (2005) Skeletal muscle hypertrophy and atrophy signaling pathways. Int J Biochem Cell Biol 37:1974-1984
22. Glass DJ (2010) Signaling pathways perturbing muscle mass. Curr Opin Clin Nutr Metab Care 13:225-229
23. Gutmann E, Hanzlikova V (1976) Fast and slow motor units in ageing. Gerontology 22:280-300
24. Haglund K, Dikic I (2012) The role of ubiquitylation in receptor endocytosis and endosomal sorting. J Cell Sci 125:265-275
25. Hirner S, Krohne C, Schuster A, Hoffmann S, Witt S, Erber R, Sticht C, Gasch A, Labeit S, Labeit D (2008) MuRF1- dependent regulation of systemic carbohydrate metabolism as revealed from transgenic mouse studies. J Mol Biol 379:666-677
26. Huotari J, Helenius A (2011) Endosome maturation. EMBO J 30:3481-3500
27. Karlin A (2002) Emerging structure of the nicotinic acetylcholine receptors. Nat Rev Neurosci 3:102-114
28. Kumari S, Borroni V, Chaudhry A, Chanda B, Massol R, Mayor S, Barrantes FJ (2008) Nicotinic acetylcholine receptor is internalized via a Rac-dependent, dynamin-independent endocytic pathway. J Cell Biol 181:1179-1193
29. Latronico N, Peli E, Botteri M (2005a) Critical illness myopathy and neuropathy. Curr Opin Crit Care 11:126-132
30. Latronico N, Shehu I, Seghelini E (2005b) Neuromuscular sequelae of critical illness. Curr Opin Crit Care 11:381-390
31. Lecker SH, Jagoe RT, Gilbert A, Gomes M, Baracos V, Bailey J, Price SR, Mitch WE, Goldberg AL (2004) Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J 18:39-51
32. Levitt TA, Salpeter MM (1981) Denervated endplates have a dual population of junctional acetylcholine receptors. Nature 291:239-241
33. Levitt TA, Loring RH, Salpeter MM (1980) Neuronal control of acetylcholine receptor turnover rate at a vertebrate neuromuscular junction. Science 210:550-551
34. Loring RH, Salpeter MM (1980) Denervation increases turnover rate of junctional acetylcholine receptors. Proc Natl Acad Sci U S A 77:2293-2297
35. Lu Z, Je HS, Young P, Gross J, Lu B, Feng G (2007) Regulation of synaptic growth and maturation by a synapse-associated E3 ubiquitin ligase at the neuromuscular junction. J Cell Biol 177:1077-1089
36. Marchand S, Cartaud J (2002) Targeted trafficking of neurotransmitter receptors to synaptic sites. Mol Neurobiol 26:117-135
37. Marchand S, Bignami F, Stetzkowski-Marden F, Cartaud J (2000) The myristoylated protein rapsyn is cotargeted with the nicotinic acetylcholine receptor to the postsynaptic membrane via the exocytic pathway. J Neurosci 20:521-528
38. Marchand S, Devillers-Thiery A, Pons S, Changeux JP, Cartaud J (2002) Rapsyn escorts the nicotinic acetylcholine receptor along the exocytic pathway via association with lipid rafts. J Neurosci 22:8891-8901
39. Martyn JA, Fagerlund MJ, Eriksson LI (2009) Basic principles of neuromuscular transmission. Anaesthesia 64(Suppl 1):1-9
40. McElhinny AS, Kakinuma K, Sorimachi H, Labeit S, Gregorio CC (2002) Muscle-specific RING finger-1 interacts with titin to regulate sarcomeric M-line and thick filament structure and may have nuclear functions via its interaction with glucocorticoid modulatory element binding protein-1. J Cell Biol 157:125-136
41. Mrosek M, Labeit D, Witt S, Heerklotz H, von Castelmur E, Labeit S, Mayans O (2007) Molecular determinants for the recruitment of the ubiquitin-ligase MuRF-1 onto M-line titin. FASEB J 21:1383-1392
42. Müller JS, Mihaylova V, Abicht A, Lochmüller H (2007) Congenitalmyasthenic syndromes: spotlight on genetic defects of neuromuscular transmission. Expert Rev Mol Med 9:1-20
43. Ohno K, Engel AG (2002) Congenital myasthenic syndromes: genetic defects of the neuromuscular junction. Curr Neurol Neurosci Rep 2:78-88
44. Palace J, Beeson D (2008) The congenital myasthenic syndromes. J Neuroimmunol 201-202:2-5
45. Pestronk A, Drachman DB, Griffin JW (1980) Effects of aging on nerve sprouting and regeneration. Exp Neurol 70:65-82
46. Röder IV, Petersen Y, Choi KR, Witzemann V, Hammer JA 3rd, Rudolf R (2008) Role of Myosin va in the plasticity of the vertebrate neuromuscular junction in vivo. PLoS One 3: e3871
47. Röder IV, Choi KR, Reischl M, Petersen Y, Diefenbacher ME, Zaccolo M, Pozzan T, Rudolf R (2010) Myosin Va cooperates with PKA RIalpha to mediate maintenance of the endplate in vivo. Proc Natl Acad Sci U S A 107:2031-2036
48. Rowan SL, Rygiel K, Purves-Smith FM, Solbak NM, Turnbull DM, Hepple RT (2012) Denervation causes fiber atrophy and myosin heavy chain co-expression in senescent skeletal muscle. PLoS One 7:e29082
49. Rudolf R, Hafner M, Mongillo M (2012) Investigating second messenger signaling in vivo. Methods Enzymol 505:363-382
50. Sandri M, Sandri C, Gilbert A, Skurk C, Calabria E, Picard A, Walsh K, Schiaffino S, Lecker SH, Goldberg AL (2004) Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 117:399-412
51. Sanes JR, Lichtman JW (2001) Induction, assembly, maturation and maintenance of a postsynaptic apparatus. Nat Rev Neurosci 2:791-805
52. Shyng SL, Xu R, Salpeter MM (1991) Cyclic AMP stabilizes the degradation of original junctional acetylcholine receptors in denervated muscle. Neuron 6:469-475
53. Stanley EF, Drachman DB (1981) Denervation accelerates the degradation of junctional acetylcholine receptors. Exp Neurol 73:390-396
54. Stanley EF, Drachman DB (1983) Rapid degradation of "new" acetylcholine receptors at neuromuscular junctions. Science 222:67-69
55. Strack S, Petersen Y, Wagner A, Röder IV, Albrizio M, Reischl M, Wacker IU, Wilhelm C, Rudolf R (2011) A novel labeling approach identifies three stability levels of acetylcholine receptors in the mouse neuromuscular junction in vivo. PLoS One 6:e20524
56. Takahashi Y, Meyerkord CL, Wang HG (2009) Bif-1/endophilin B1: a candidate for crescent driving force in autophagy. Cell Death Differ 16:947-955
57. Tuffery AR (1971) Growth and degeneration of motor end-plates in normal cat hind limb muscles. J Anat 110:221-247
58. Valdez G, Tapia JC, Kang H, Clemenson GD Jr, Gage FH, Lichtman JW, Sanes JR (2010) Attenuation of age-related changes in mouse neuromuscular synapses by caloric restriction and exercise. Proc Natl Acad Sci U S A 107:14863-14868
59. Valkova C, Albrizio M, Röder IV, Schwake M, Betto R, Rudolf R, Kaether C (2011) Sorting receptor Rer1 controls surface expression of muscle acetylcholine receptors by ER retention of unassembled alpha-subunits. Proc Natl Acad Sci U S A 108:621-625
60. Wan J, Cheung AY, Fu WY, Wu C, Zhang M, Mobley WC, Cheung ZH, Ip NY (2008) Endophilin B1 as a novel regulator of nerve growth factor/TrkA trafficking and neurite outgrowth. J Neurosci 28:9002-9012
61. Witt CC, Witt SH, Lerche S, Labeit D, Back W, Labeit S (2008) Cooperative control of striated muscle mass and metabolism by MuRF1 and MuRF2. EMBO J 27:350-360
62. Yampolsky P, Pacifici PG, Lomb L, Giese G, Rudolf R, Röder IV, Witzemann V (2010a) Time lapse in vivo visualization of developmental stabilization of synaptic receptors at neuromuscular junctions. J Biol Chem 285:34589-34596
63. Yampolsky P, Pacifici PG, Witzemann V (2010b) Differential muscle-driven synaptic remodelin in the neuromuscular junction after denervation. Eur J Neurosci 31:646-658