Laminin induced local axonal translation of β-actin mRNA is impaired in SMN-deficient motoneurons

Histochemistry and Cell Biology

Volumn 138, Issue 5, 2012, Pages 737-748

  Rathod, Reena ^a   Havlicek, Steven ^a   Frank, Nicolas ^a   Blum, Robert ^a   Sendtner, Michael ^a,b  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY HOSPITAL ERLANGEN   (Germany)

Author keywords

Actin; Laminin; Local translation; Motoneuron; MRNA transport; Spinal muscular atrophy

Indexed keywords

BETA ACTIN; LAMININ; MESSENGER RNA; SURVIVAL MOTOR NEURON PROTEIN; SURVIVAL MOTOR NEURON PROTEIN 2;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ANIMAL CELL; ARTICLE; CELL DENSITY; CELLULAR DISTRIBUTION; CEREBROSPINAL FLUID; EMBRYO; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GROWTH CONE; IN SITU HYBRIDIZATION; MOTOR NEURON DISEASE; MOUSE; MUSCLE ATROPHY; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RNA TRANSLATION; SIGNAL TRANSDUCTION; SPINAL CORD MOTONEURON; TIME LAPSE IMAGING; TRANSLATION REGULATION;

ACTINS; ANIMALS; AXONS; CELLS, CULTURED; DISEASE MODELS, ANIMAL; GROWTH CONES; HUMANS; LAMININ; MICE; MICE, TRANSGENIC; MOTOR NEURONS; PHOTOBLEACHING; PROTEIN BIOSYNTHESIS; RNA, MESSENGER; SIGNAL TRANSDUCTION; SPINAL MUSCULAR ATROPHIES OF CHILDHOOD; SURVIVAL OF MOTOR NEURON 1 PROTEIN; TIME-LAPSE IMAGING;

EID: 84868142568     PISSN: 09486143     EISSN: 1432119X     Source Type: Journal    
DOI: 10.1007/s00418-012-0989-1     Document Type: Article

References (43)

1. Aakalu G, Smith WB, Nguyen N, Jiang C, Schuman EM (2001) Dynamic visualization of local protein synthesis in hippocampal neurons. Neuron 30(2):489-502
2. Andreassi C, Riccio A (2009) To localize or not to localize: mRNA fate is in 30UTR ends. Trends Cell Biol 19(9):465-474. doi: 10.1016/j.tcb.2009.06.001
3. Bassell GJ, Warren ST (2008) Fragile X syndrome: loss of local mRNA regulation alters synaptic development and function. Neuron 60(2):201-214. doi:10.1016/j.neuron.2008.10.004
4. Bassell GJ, Zhang H, Byrd AL, Femino AM, Singer RH, Taneja KL, Lifshitz LM, Herman IM, Kosik KS (1998) Sorting of beta-actin mRNA and protein to neurites and growth cones in culture. J Neurosci 18(1):251-265
5. Bowerman M, Anderson CL, Beauvais A, Boyl PP, Witke W, Kothary R (2009) SMN, profilin IIa and plastin 3: a link between the deregulation of actin dynamics and SMA pathogenesis. Mol Cell Neurosci 42(1):66-74
6. Bowerman M, Shafey D, Kothary R (2007) Smn depletion alters profilin II expression and leads to upregulation of the RhoA/ROCK pathway and defects in neuronal integrity. J Mol Neurosci 32(2):120-131
7. Campbell DS, Holt CE (2001) Chemotropic responses of retinal growth cones mediated by rapid local protein synthesis and degradation. Neuron 32(6):1013-1026
8. Cheever TR, Li B, Ervasti JM (2012) Restricted morphological and behavioral abnormalities following ablation of beta-actin in the brain. PLoS One 7(3):e32970
9. Cheever TR, Olson EA, Ervasti JM (2011) Axonal regeneration and neuronal function are preserved in motor neurons lacking ss-actin in vivo. PLoS One 6(3):e17768
10. Condeelis J, Singer RH (2005) How and why does beta-actin mRNA target? Eur Cell Biol Org 97(1):97-110
11. Crawford TO, Pardo CA (1996) The neurobiology of childhood spinal muscular atrophy. Neurobiol Dis 3(2):97-110. doi:10.1006/nbdi.1996.0010
12. Garber KB, Visootsak J, Warren ST (2008) Fragile X syndrome. Eur J Hum Genet 16(6):666-672
13. Hengst U, Deglincerti A, Kim HJ, Jeon NL, Jaffrey SR (2009) Axonal elongation triggered by stimulus-induced local translation of a polarity complex protein. Nat Cell Biol 11(8):1024-1030
14. Holt CE, Bullock SL (2009) Subcellular mRNA localization in animal cells and why it matters. Science 326(5957):1212-1216. doi: 10.1126/science.1176488
15. Jablonka S, Beck M, Lechner BD, Mayer C, Sendtner M (2007) Defective Ca2? channel clustering in axon terminals disturbs excitability in motoneurons in spinal muscular atrophy. J Cell Biol 179(1):139-149. doi:10.1083/jcb.200703187
16. Jablonka S, Rossoll W, Schrank B, Sendtner M (2000) The role of SMN in spinal muscular atrophy. J Neurol 247(Suppl 1):I37-I42
17. Kabouridis PS, Magee AI, Ley SC (1997) S-acylation of LCK protein tyrosine kinase is essential for its signalling function in T lymphocytes. EMBO J 16(16):4983-4998. doi:10.1093/emboj/16.16.4983
18. Kiebler MA, Bassell GJ (2006) Neuronal RNA granules: movers and makers. Neuron 51(6):685-690
19. Kislauskis EH, Zhu X, Singer RH (1994) Sequences responsible for intracellular localization of beta-actin messenger RNA also affect cell phenotype. J Cell Biol 127(2):441-451
20. Leung KM, van Horck FP, Lin AC, Allison R, Standart N, Holt CE (2006) Asymmetrical beta-actin mRNA translation in growth cones mediates attractive turning to netrin-1. Nat Neurosci 9(10):1247-1256
21. Lin AC, Holt CE (2008) Function and regulation of local axonal translation. Curr Opin Neurobiol 18(1):60-68. doi:10.1016/j. conb.2008.05.004
22. Lois C, Hong EJ, Pease S, Brown EJ, Baltimore D (2002) Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science 295(5556):868-872. doi: 10.1126/science.1067081
23. McGovern VL, Gavrilina TO, Beattie CE, Burghes AH (2008) Embryonic motor axon development in the severe SMA mouse. Human Mol Genet 17(18):2900-2909
24. Monani UR, Sendtner M, Coovert DD, Parsons DW, Andreassi C, Le TT, Jablonka S, Schrank B, Rossoll W, Prior TW, Morris GE, Burghes AH (2000) The human centromeric survival motor neuron gene (SMN2) rescues embryonic lethality in Smn(-/-) mice and results in a mouse with spinal muscular atrophy. Human Mol Genet 9(3):333-339
25. Murray LM, Lee S, Baumer D, Parson SH, Talbot K, Gillingwater TH (2010) Pre-symptomatic development of lower motor neuron connectivity in a mouse model of severe spinal muscular atrophy. Human Mol Genet 19(3):420-433
26. Noakes PG, Gautam M, Mudd J, Sanes JR, Merlie JP (1995) Aberrant differentiation of neuromuscular junctions in mice lacking s-laminin/laminin beta 2. Nature 374(6519):258-262. doi:10.1038/374258a0
27. Oleynikov Y, Singer RH (2003) Real-time visualization of ZBP1 association with beta-actin mRNA during transcription and localization. Curr Biol 13(3):199-207
28. Patton BL, Miner JH, Chiu AY, Sanes JR (1997) Distribution and function of laminins in the neuromuscular system of developing, adult, and mutant mice. J Cell Biol 139(6):1507-1521
29. Piazzon N, Rage F, Schlotter F, Moine H, Branlant C, Massenet S (2008) In vitro and in cellulo evidences for association of the survival of motor neuron complex with the fragile X mental retardation protein. J Biol Chem 283(9):5598-5610. doi:10.1074/jbc.M707304200
30. Plantman S, Patarroyo M, Fried K, Domogatskaya A, Tryggvason K, Hammarberg H, Cullheim S (2008) Integrin-laminin interactions controlling neurite outgrowth from adult DRG neurons in vitro. Mol Cell Neurosci 39(1):50-62. doi:10.1016/j.mcn.2008.05.015
31. Porter BE, Sanes JR (1995) Gated migration: neurons migrate on but not onto substrates containing S-laminin. Developmental Biol 167(2):609-616. doi:10.1006/dbio.1995.1052
32. Rehberg M, Lepier A, Solchenberger B, Osten P, Blum R (2008) A new non-disruptive strategy to target calcium indicator dyes to the endoplasmic reticulum. Cell Calcium 44(4):386-399
33. Rodriguez AJ, Czaplinski K, Condeelis JS, Singer RH (2008) Mechanisms and cellular roles of local protein synthesis in mammalian cells. Curr Opin Cell Biol 20(2):144-149
34. Rossoll W, Jablonka S, Andreassi C, Kroning AK, Karle K, Monani UR, Sendtner M (2003) Smn, the spinal muscular atrophydetermining gene product, modulates axon growth and localization of beta-actin mRNA in growth cones of motoneurons. J Cell Biol 163(4):801-812. doi:10.1083/jcb.200304128
35. Sanes JR, Lichtman JW (2001) Induction, assembly, maturation and maintenance of a postsynaptic apparatus. Nat Rev Neurosci 2(11):791-805
36. Sasaki Y, Welshhans K, Wen Z, Yao J, Xu M, Goshima Y, Zheng JQ, Bassell GJ (2010) Phosphorylation of zipcode binding protein 1 is required for brain-derived neurotrophic factor signaling of local beta-actin synthesis and growth cone turning. J Neurosci 30(28):9349-9358. doi:10.1523/JNEUROSCI.0499-10. 2010
37. Smith WB, Aakalu G, Schuman EM (2001) Local protein synthesis in neurons. Curr Biol 11(22):R901-R903
38. Tiruchinapalli DM, Oleynikov Y, Kelic S, Shenoy SM, Hartley A, Stanton PK, Singer RH, Bassell GJ (2003) Activity-dependent trafficking and dynamic localization of zipcode binding protein 1 and beta-actin mRNA in dendrites and spines of hippocampal neurons. J Neurosci 23(8):3251-3261
39. Twiss JL, Fainzilber M (2009) Ribosomes in axons -scrounging from the neighbors? Trends Cell Biol 19(5):236-243. doi:10.1016/j.tcb.2009.02.007
40. Verkerk AJ, Pieretti M, Sutcliffe JS, Fu YH, Kuhl DP, Pizzuti A, Reiner O, Richards S, Victoria MF, Zhang FP et al (1991) Identification of a gene (FMR-1) containing a CGG repeat coincident with a breakpoint cluster region exhibiting length variation in fragile X syndrome. Cell 65(5):905-914
41. Wiese S, Herrmann T, Drepper C, Jablonka S, Funk N, Klausmeyer A, Rogers ML, Rush R, Sendtner M (2010) Isolation and enrichment of embryonic mouse motoneurons from the lumbar spinal cord of individual mouse embryos. Nat Protoc 5(1):31-38
42. Wu KY, Hengst U, Cox LJ, Macosko EZ, Jeromin A, Urquhart ER, Jaffrey SR (2005) Local translation of RhoA regulates growth cone collapse. Nature 436(7053):1020-1024
43. Yao J, Sasaki Y, Wen Z, Bassell GJ, Zheng JQ (2006) An essential role for beta-actin mRNA localization and translation in Ca2?-dependent growth cone guidance. Nat Neurosci 9(10):1265-1273. doi: 10.1038/nn1773