Ambra1 knockdown in zebrafish leads to incomplete development due to severe defects in organogenesis

Autophagy

Volumn 9, Issue 4, 2013, Pages 476-495

  Benato, Francesca ^a   Skobo, Tatjana ^a   Gioacchini, Giorgia ^b   Moro, Isabella ^a   Ciccosanti, Fabiola ^c   Piacentini, Mauro ^c,d   Fimia, Gian Maria ^c   Carnevali, Oliana ^b   Valle, Luisa Dalla ^a  

^a UNIVERSITY OF PADOVA   (Italy)

^b UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^c NATIONAL INSTITUTE FOR INFECTIOUS DISEASES L SPALLANZANI   (Italy)

^d UNIVERSITY OF ROME TOR VERGATA   (Italy)

Author keywords

Ambra1; Autophagy; Development; Morpholino; Zebrafish

Indexed keywords

AMBRA 1A PROTEIN; AMBRA 1B PROTEIN; COMPLEMENTARY DNA; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; BRAIN DEVELOPMENT; CHROMOSOME 7; CONGENITAL MALFORMATION; CONTROLLED STUDY; CROSS HYBRIDIZATION; DEVELOPMENTAL STAGE; DNA SPLICING; EMBRYO; GENE SILENCING; GROWTH RETARDATION; IN SITU HYBRIDIZATION; LYSOSOME; MOLECULAR CLONING; NICK END LABELING; NONHUMAN; NUCLEOTIDE SEQUENCE; ORGANOGENESIS; PHENOTYPE; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA TRANSLATION; SEQUENCE ANALYSIS; STOP CODON; ZEBRA FISH;

EID: 84877341621     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.23278     Document Type: Article

References (41)

1. Ravikumar B, Futter M, Jahreiss L, Korolchuk VI, Lichtenberg M, Luo S, et al. Mammalian macroautophagy at a glance. J Cell Sci 2009; 122:1707-11; PMID:19461070; http://dx.doi.org/10.1242/jcs.031773
2. Sharp ZD. Aging and TOR: Interwoven in the fabric of life. Cell Mol Life Sci 2011; 68:587-97; PMID:20960025; http://dx.doi.org/10.1007/s00018-010-0542-0
3. García-Arencibia M, Hochfeld WE, Toh PP, Rubinsztein DC. Autophagy, a guardian against neurodegeneration. Semin Cell Dev Biol 2010; 21:691-8; PMID:20188203; http://dx.doi.org/10.1016/j.semcdb.2010.02.008
4. Cecconi F, Levine B. The role of autophagy in mammalian development: Cell makeover rather than cell death. Dev Cell 2008; 15:344-57; PMID:18804433; http://dx.doi.org/10.1016/j.devcel.2008.08.012
5. Rubinsztein DC, Gestwicki JE, Murphy LO, Klionsky DJ. Potential therapeutic applications of autophagy. Nat Rev Drug Discov 2007; 6:304-12; PMID:17396135; http://dx.doi.org/10.1038/nrd2272
6. Williams A, Jahreiss L, Sarkar S, Saiki S, Menzies FM, Ravikumar B, et al. Aggregate-prone proteins are cleared from the cytosol by autophagy: Therapeutic implications. Curr Top Dev Biol 2006; 76:89-101; PMID:17118264; http://dx.doi.org/10.1016/S0070-2153(06)76003-3
7. Levine B, Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008; 132:27-42; PMID:18191218; http://dx.doi.org/10.1016/j.cell.2007.12.018
8. Mizushima N, Levine B, Cuervo AM, Klionsky DJ. Autophagy fights disease through cellular self-digestion. Nature 2008; 451:1069-75; PMID:18305538; http://dx.doi.org/10.1038/nature06639
9. Grumati P, Coletto L, Sabatelli P, Cescon M, Angelin A, Bertaggia E, et al. Autophagy is defective in collagen VI muscular dystrophies, and its reactivation rescues myofiber degeneration. Nat Med 2010; 16:1313-20; PMID:21037586; http://dx.doi.org/10.1038/nm.2247
10. Di Bartolomeo S, Nazio F, Cecconi F. The role of autophagy during development in higher eukaryotes. Traffic 2010; 11:1280-9; PMID:20633243; http://dx.doi.org/10.1111/j.1600-0854.2010.01103.x
11. Huang WP, Klionsky DJ. Autophagy in yeast: A review of the molecular machinery. Cell Struct Funct 2002; 27:409-20; PMID:12576634; http://dx.doi.org/10.1247/csf.27.409
12. Matsunaga K, Saitoh T, Tabata K, Omori H, Satoh T, Kurotori N, et al. Two Beclin 1-binding proteins, Atg14L and Rubicon, reciprocally regulate autophagy at different stages. Nat Cell Biol 2009; 11:385-96; PMID:19270696; http://dx.doi.org/10.1038/ncb1846
13. Zhong Y, Wang QJ, Yue Z. Atg14L and Rubicon: Yin and yang of Beclin 1-mediated autophagy control. Autophagy 2009; 5:890-1; PMID:19556860
14. Fimia GM, Stoykova A, Romagnoli A, Giunta L, Di Bartolomeo S, Nardacci R, et al. Ambra1 regulates autophagy and development of the nervous system. Nature 2007; 447:1121-5; PMID:17589504
15. Di Bartolomeo S, Corazzari M, Nazio F, Oliverio S, Lisi G, Antonioli M, et al. The dynamic interaction of AMBRA1 with the dynein motor complex regulates mammalian autophagy. J Cell Biol 2010; 191:155-68; PMID:20921139; http://dx.doi.org/10.1083/jcb.201002100
16. Postlethwait J, Amores A, Cresko W, Singer A, Yan YL. Subfunction partitioning, the teleost radiation and the annotation of the human genome. Trends Genet 2004; 20:481-90; PMID:15363902; http://dx.doi.org/10.1016/j.tig. 2004.08.001
17. Jones DT, Taylor WR, Thornton JM. The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 1992; 8:275-82; PMID:1633570
18. Catchen JM, Conery JS, Postlethwait JH. Automated identification of conserved synteny after wholegenome duplication. Genome Res 2009; 19:1497-505; PMID:19465509; http://dx.doi.org/10.1101/gr.090480.108
19. Volff JN. Genome evolution and biodiversity in teleost fish. Heredity (Edinb) 2005; 94:280-94; PMID:15674378; http://dx.doi.org/10.1038/sj.hdy.6800635
20. Robu ME, Larson JD, Nasevicius A, Beiraghi S, Brenner C, Farber SA, et al. p53 activation by knockdown technologies. PLoS Genet 2007; 3:e78; PMID:17530925; http://dx.doi.org/10.1371/journal.pgen.0030078
21. Meyer A, Van de Peer Y. From 2R to 3R: Evidence for a fish-specific genome duplication (FSGD). Bioessays 2005; 27:937-45; PMID:16108068; http://dx.doi.org/10.1002/bies.20293
22. Behrends C, Sowa ME, Gygi SP, Harper JW. Network organization of the human autophagy system. Nature 2010; 466:68-76; PMID:20562859; http://dx.doi.org/10.1038/nature09204
23. Pagliarini V, Wirawan E, Romagnoli A, Ciccosanti F, Lisi G, Lippens S, et al. Proteolysis of Ambra1 during apoptosis has a role in the inhibition of the autophagic pro-survival response. Cell Death Differ 2012; 19:1495-504; PMID:22441670; http://dx.doi.org/10.1038/cdd.2012.27
24. Gioacchini G, Dalla Valle L, Benato F, Fimia GM, Nardacci R, Ciccosanti F, et al. Autophagy and apoptosis interplay in Danio rerio follicles development: Role of probiotic. Reprod Fertil Dev; In press
25. Kuma A, Hatano M, Matsui M, Yamamoto A, Nakaya H, Yoshimori T, et al. The role of autophagy during the early neonatal starvation period. Nature 2004; 432:1032-6; PMID:15525940; http://dx.doi.org/10.1038/nature03029
26. Komatsu M, Waguri S, Ueno T, Iwata J, Murata S, Tanida I, et al. Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J Cell Biol 2005; 169:425-34; PMID:15866887; http://dx.doi.org/10.1083/ jcb.200412022
27. Hu Z, Zhang J, Zhang Q. Expression pattern and functions of autophagy-related gene atg5 in zebrafish organogenesis. Autophagy 2011; 7:1514-27; PMID:22082871; http://dx.doi.org/10.4161/auto.7.12.18040
28. He C, Bartholomew CR, Zhou W, Klionsky DJ. Assaying autophagic activity in transgenic GFP-Lc3 and GFP-Gabarap zebrafish embryos. Autophagy 2009; 5:520-6; PMID:19221467; http://dx.doi.org/10.4161/auto.5.4.7768
29. Miller-Bertoglio VE, Fisher S, Sánchez A, Mullins MC, Halpern ME. Differential regulation of chordin expression domains in mutant zebrafish. Dev Biol 1997; 192:537-50; PMID:9441687; http://dx.doi.org/10.1006/dbio.1997.8788
30. Schulte-Merker S, Hammerschmidt M, Beuchle D, Cho KW, De Robertis EM, Nüsslein-Volhard C. Expression of zebrafish goosecoid and no tail gene products in wild-type and mutant no tail embryos. Development 1994; 120:843-52; PMID:7600961
31. Krauss S, Concordet JP, Ingham PW. A functionally conserved homolog of the Drosophila segment polarity gene hh is expressed in tissues with polarizing activity in zebrafish embryos. Cell 1993; 75:1431-44; PMID:8269519; http://dx.doi.org/10.1016/0092-8674(93)90628-4
32. Fimia GM, Piacentini M. Regulation of autophagy in mammals and its interplay with apoptosis. Cell Mol Life Sci 2010; 67:1581-8; PMID:20165902; http://dx.doi.org/10.1007/s00018-010-0284-z
33. Westerfield M. The Zebrafish Book. A Guide for the Laboratory Use of Zebrafish (Danio rerio), 3rd Edition. Eugene, OR, University of Oregon Press 1995
34. Lawrence C. The husbandry of zebrafish (Danio rerio): A review. Aquaculture 2007; 296:1-20; http://dx.doi.org/10.1016/j.aquaculture.2007.04.077
35. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF. Stages of embryonic development of the zebrafish. Dev Dyn 1995; 203:253-310; PMID:8589427; http://dx.doi.org/10.1002/aja.1002030302
36. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994; 22:4673-80; PMID:7984417; http://dx.doi.org/10.1093/nar/22.22.4673
37. Felsenstein J. Inferring phylogenies. Sunderland (MA): Sinauer Associates. 2004
38. Stamatakis A. RAxML-VI-HPC: Maximum likelihoodbased phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006; 22:2688-90; PMID:16928733; http://dx.doi.org/10.1093/bioinformatics/btl446
39. Felsenstein J. Confidence limits on phylogenies: An approach using bootstrap. Evolution 1985; 39:783-91; http://dx.doi.org/10.2307/2408678
40. Thisse C, Thisse B. High-resolution in situ hybridization to whole-mount zebrafish embryos. Nat Protoc 2008; 3:59-69; PMID:18193022; http://dx.doi.org/ 10.1038/nprot.2007.514
41. Serbedzija GN, Flynn E, Willett CE. Zebrafish angiogenesis: A new model for drug screening. Angiogenesis 1999; 3:353-9; PMID:14517415; http://dx.doi.org/10.1023/A:1026598300052