Loss of ALS-associated TDP-43 in zebrafish causes muscle degeneration, vascular dysfunction, and reduced motor neuron axon outgrowth

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 13, 2013, Pages 4986-4991

  Schmid, Bettina ^a,b,c   Hruscha, Alexander ^a   Hogl, Sebastian ^a,d   Banzhaf Strathmann, Julia ^a   Strecker, Katrin ^b   Van Der Zee, Julie ^e,f   Teucke, Mathias ^b   Eimer, Stefan ^g   Hegermann, Jan ^g   Kittelmann, Maike ^g   Kremmer, Elisabeth ^h   Cruts, Marc ^e,f   Solchenberger, Barbara ^b   Hasenkamp, Laura ^b   Van Bebber, Frauke ^a   Van Broeckhoven, Christine ^e,f   Edbauer, Dieter ^a,c   Lichtenthaler, Stefan F ^a,c,d   Haass, Christian ^a,b,c  

^a GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c Munich Cluster for Systems Neurology ^*  (Germany)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^e DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^f UNIVERSITY OF ANTWERP   (Belgium)

^g EUROPEAN NEUROSCIENCE INSTITUTE   (Germany)

^h INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

Neurodegeneration; Proteomics; Zinc finger nuclease

Indexed keywords

ALPHA ACTININ; FILAMIN; MYOSIN HEAVY CHAIN; TAR DNA BINDING PROTEIN; VINCULIN; ZINC FINGER NUCLEASE;

ALLELE; AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; CAUSE OF DEATH; CIRCULATION; CONTROLLED STUDY; FRONTAL CORTEX; GENOME; HEART MUSCLE CELL; IMMUNOBLOTTING; IN SITU HYBRIDIZATION; LOSS OF FUNCTION MUTATION; MOTONEURON; MUSCLE ATROPHY; MUTANT; NERVE FIBER GROWTH; NONHUMAN; ORTHOLOGY; PHENOTYPE; PRIORITY JOURNAL; SMOOTH MUSCLE FIBER; SPINAL CORD NERVE CELL; STOP CODON; TACTILE STIMULATION; UPREGULATION; VASCULAR DISEASE; WESTERN BLOTTING; ZEBRA FISH;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; AXONS; CONTRACTILE PROTEINS; DNA-BINDING PROTEINS; HUMANS; MICROFILAMENT PROTEINS; MOTOR NEURONS; MUSCULAR ATROPHY; MUTATION; PROTEIN STRUCTURE, TERTIARY; VASCULAR DISEASES; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO;

EID: 84875508368     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1218311110     Document Type: Article

References (51)

1. Neumann M, et al. (2006) Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 314(5796):130-133.
2. Van Langenhove T, van der Zee J, Van Broeckhoven C (2012) The molecular basis of the frontotemporal lobar degeneration-amyotrophic lateral sclerosis spectrum. Ann Med 44(8):817-828.
3. Polymenidou M, et al. (2011) Long pre-mRNA depletion and RNA missplicing contribute to neuronal vulnerability from loss of TDP-43. Nat Neurosci 14(4):459-468.
4. Tollervey JR, et al. (2011) Characterizing the RNA targets and position-dependent splicing regulation by TDP-43. Nat Neurosci 14(4):452-458.
5. Xiao S, et al. (2011) RNA targets of TDP-43 identified by UV-CLIP are deregulated in ALS. Mol Cell Neurosci 47(3):167-180.
6. Arai T, et al. (2006) TDP-43 is a component of ubiquitin-positive tau-negative inclusions in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Biochem Biophys Res Commun 351(3):602-611.
7. Kiernan MC, et al. (2011) Amyotrophic lateral sclerosis. Lancet 377(9769):942-955.
8. Sieben A, et al. (2012) The genetics and neuropathology of frontotemporal lobar degeneration. Acta Neuropathol 124(3):353-372.
9. Cruts M, Theuns J, Van Broeckhoven C (2012) Locus-specific mutation databases for neurodegenerative brain diseases. Hum Mutat 33(9):1340-1344.
10. Buratti E, et al. (2005) TDP-43 binds heterogeneous nuclear ribonucleoprotein A/B through its C-terminal tail: An important region for the inhibition of cystic fibrosis transmembrane conductance regulator exon 9 splicing. J Biol Chem 280(45): 37572-37584.
11. 2 in vivo. Nucleic Acids Res 37(12):4116-4126.
12. Ayala YM, et al. (2011) TDP-43 regulates its mRNA levels through a negative feedback loop. EMBO J 30(2):277-288.
13. Avendaño-Vázquez SE, et al. (2012) Autoregulation of TDP-43 mRNA levels involves interplay between transcription, splicing, and alternative polyA site selection. Genes Dev 26(15):1679-1684.
14. Buratti E, Baralle FE (2011) TDP-43: New aspects of autoregulation mechanisms in RNA binding proteins and their connection with human disease. FEBS J 278(19): 3530-3538.
15. Mackenzie IR, Rademakers R, Neumann M (2010) TDP-43 and FUS in amyotrophic lateral sclerosis and frontotemporal dementia. Lancet Neurol 9(10):995-1007.
16. Shankaran SS, et al. (2008) Missense mutations in the progranulin gene linked to frontotemporal lobar degeneration with ubiquitin-immunoreactive inclusions reduce progranulin production and secretion. J Biol Chem 283(3):1744-1753.
17. Urnov FD, Rebar EJ, Holmes MC, Zhang HS, Gregory PD (2010) Genome editing with engineered zinc finger nucleases. Nat Rev Genet 11(9):636-646.
18. Kraemer BC, et al. (2010) Loss of murine TDP-43 disrupts motor function and plays an essential role in embryogenesis. Acta Neuropathol 119(4):409-419.
19. Wu LS, et al. (2010) TDP-43, a neuro-pathosignature factor, is essential for early mouse embryogenesis. Genesis 48(1):56-62.
20. Sephton CF, et al. (2010) TDP-43 is a developmentally regulated protein essential for early embryonic development. J Biol Chem 285(9):6826-6834.
21. Kabashi E, et al. (2008) TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis. Nat Genet 40(5):572-574.
22. Rutherford NJ, et al. (2008) Novel mutations in TARDBP (TDP-43) in patients with familial amyotrophic lateral sclerosis. PLoS Genet 4(9):e1000193.
23. Vance C, et al. (2009) Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6. Science 323(5918):1208-1211.
24. Kwiatkowski TJ, Jr., et al. (2009) Mutations in the FUS/TLS gene on chromosome 16 cause familial amyotrophic lateral sclerosis. Science 323(5918):1205-1208.
25. Chi NC, et al. (2008) Foxn4 directly regulates tbx2b expression and atrioventricular canal formation. Genes Dev 22(6):734-739.
26. Carmeliet P, Tessier-Lavigne M (2005) Common mechanisms of nerve and blood vessel wiring. Nature 436(7048):193-200.
27. Chiang W, Greaser ML, Lyons GE (2000) Filamin isogene expression during mouse myogenesis. Dev Dyn 217(1):99-108.
28. van der Ven PF, et al. (2000) Characterization of muscle filamin isoforms suggests a possible role of gamma-filamin/ABP-L in sarcomeric Z-disc formation. Cell Motil Cytoskeleton 45(2):149-162.
29. Thompson TG, et al. (2000) Filamin 2 (FLN2): A muscle-specific sarcoglycan interacting protein. J Cell Biol 148(1):115-126.
30. Kabashi E, et al. (2010) Gain and loss of function of ALS-related mutations of TARDBP (TDP-43) cause motor deficits in vivo. Hum Mol Genet 19(4):671-683.
31. Fiesel FC, Schurr C, Weber SS, Kahle PJ (2011) TDP-43 knockdown impairs neurite outgrowth dependent on its target histone deacetylase 6. Mol Neurodegener 6:64.
32. Iguchi Y, et al. (2009) TDP-43 depletion induces neuronal cell damage through dysregulation of Rho family GTPases. J Biol Chem 284(33):22059-22066.
33. Kawahara Y, Mieda-Sato A (2012) TDP-43 promotes microRNA biogenesis as a component of the Drosha and Dicer complexes. Proc Natl Acad Sci USA 109(9):3347-3352.
34. Isogai S, Lawson ND, Torrealday S, Horiguchi M, Weinstein BM (2003) Angiogenic network formation in the developing vertebrate trunk. Development 130(21): 5281-5290.
35. Santoro MM, Pesce G, Stainier DY (2009) Characterization of vascular mural cells during zebrafish development. Mech Dev 126(8-9):638-649.
36. Sehnert AJ, Stainier DY (2002) A window to the heart: Can zebrafish mutants help us understand heart disease in humans? Trends Genet 18(10):491-494.
37. Wegorzewska I, Baloh RH (2011) TDP-43-based animal models of neurodegeneration: New insights into ALS pathology and pathophysiology. Neurodegener Dis 8(4): 262-274.
38. Vorgerd M, et al. (2005) A mutation in the dimerization domain of filamin c causes a novel type of autosomal dominant myofibrillar myopathy. Am J Hum Genet 77(2): 297-304.
39. Duff RM, et al. (2011) Mutations in the N-terminal actin-binding domain of filamin C cause a distal myopathy. Am J Hum Genet 88(6):729-740.
40. Fujita M, et al. (2012) Filamin C plays an essential role in the maintenance of the structural integrity of cardiac and skeletal muscles, revealed by the medaka mutant zacro. Dev Biol 361(1):79-89.
41. Ruparelia AA, Zhao M, Currie PD, Bryson-Richardson RJ (2012) Characterization and investigation of zebrafish models of filamin-related myofibrillar myopathy. Hum Mol Genet 21(18):4073-4083.
42. Feng Y, Walsh CA (2004) The many faces of filamin: A versatile molecular scaffold for cell motility and signalling. Nat Cell Biol 6(11):1034-1038.
43. Chiang PM, et al. (2010) Deletion of TDP-43 down-regulates Tbc1d1, a gene linked to obesity, and alters body fat metabolism. Proc Natl Acad Sci USA 107(37):16320-16324.
44. Wu LS, Cheng WC, Shen CK (2012) Targeted depletion of TDP-43 expression in the spinal cord motor neurons leads to the development of amyotrophic lateral sclerosislike phenotypes in mice. J Biol Chem 287(33):27335-27344.
45. Zhong Z, et al. (2008) ALS-causing SOD1 mutants generate vascular changes prior to motor neuron degeneration. Nat Neurosci 11(4):420-422.
46. Lambrechts D, Carmeliet P (2006) VEGF at the neurovascular interface: Therapeutic implications for motor neuron disease. Biochim Biophys Acta 1762(11-12):1109-1121.
47. Bell RD, et al. (2010) Pericytes control key neurovascular functions and neuronal phenotype in the adult brain and during brain aging. Neuron 68(3):409-427.
48. Ishikawa T, Morita M, Nakano I (2007) Constant blood flow reduction in premotor frontal lobe regions in ALS with dementia A SPECT study with 3D-SSP. Acta Neurol Scand 116(5):340-344.
49. Tanaka M, et al. (1993) Cerebral blood flow and oxygen metabolism in progressive dementia associated with amyotrophic lateral sclerosis. J Neurol Sci 120(1):22-28.
50. Rule RR, Schuff N, Miller RG, WeinerMW(2010) Gray matter perfusion correlates with disease severity in ALS. Neurology 74(10):821-827.
51. Winkler EA, et al. (2013) Blood-spinal cord barrier breakdown and pericyte reductions in amyotrophic lateral sclerosis. Acta Neuropathol 125(1):111-120.