Molecular cloning, characterization and expression analysis of ATG1 in the silkworm, Bombyx mori

Gene

Volumn 511, Issue 2, 2012, Pages 326-337

  Casati, Barbara ^a   Terova, Genciana ^a   Cattaneo, Anna Giulia ^a   Rimoldi, Simona ^a   Franzetti, Eleonora ^a   de Eguileor, Magda ^a   Tettamanti, Gianluca ^a  

^a UNIVERSITY OF INSUBRIA   (Italy)

Author keywords

Autophagy; Fat body; Lepidoptera; Midgut; Starvation

Indexed keywords

ADENOSINE TRIPHOSPHATE; AUTOPHAGY 1 PROTEIN; COMPLEMENTARY DNA; MAGNESIUM; MEMBRANE PROTEIN; MESSENGER RNA; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BINDING SITE; BOMBYX MORI; CATALYSIS; CONTROLLED STUDY; COPY NUMBER VARIATION; FAT BODY; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; HUMAN; LARVA; MALPIGHIAN TUBULE; MIDGUT; MOLECULAR CLONING; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STRUCTURE; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY; UPREGULATION; YEAST;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BOMBYX; CELL LINE; CLONING, MOLECULAR; DNA PRIMERS; DNA, COMPLEMENTARY; GENE EXPRESSION REGULATION; HUMANS; IMMUNOHISTOCHEMISTRY; INSECT PROTEINS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN PROCESSING, POST-TRANSLATIONAL; REAL-TIME POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY, AMINO ACID;

ANIMALIA; BOMBYX MORI; HEXAPODA; LEPIDOPTERA; MAMMALIA;

EID: 84868214237     PISSN: 03781119     EISSN: 18790038     Source Type: Journal    
DOI: 10.1016/j.gene.2012.09.086     Document Type: Article

References (86)

1. Aguinaldo A.M., et al. Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 1997, 387:489-493.
2. Akai H. The structure and ultrastructure of the silk gland. Experientia 1983, 39:443-449.
3. Arrese E.L., Soulages J.L. Insect fat body: energy, metabolism, and regulation. Annu. Rev. Entomol. 2010, 55:207-225.
4. Barth J.M., Szabad J., Hafen E., Köhler K. Autophagy in Drosophila ovaries is induced by starvation and is required for oogenesis. Cell Death Differ. 2011, 18:915-924.
5. Bass B.P., et al. Cell-autonomous requirement for DNaseII in nonapoptotic cell death. Cell Death Differ. 2009, 16:1362-1371.
6. Blom N., Gammeltoft S., Brunak S. Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J. Mol. Biol. 1999, 294:1351-1362.
7. Blom N., Sicheritz-Pontén T., Gupta R., Gammeltoft S., Brunak S. Prediction of post-translational glycosylation and phosphorylation of proteins from the amino acid sequence. Proteomics 2004, 4:1633-1649.
8. Cappellozza L., Cappellozza S., Saviane A., Sbrenna G. Artificial diet rearing system for the silkworm Bombyx mori (Lepidoptera: Bombycidae): effect of vitamin C deprivation on larval growth and cocoon production. Appl. Entomol. Zool. 2005, 40:405-412.
9. Chan E.Y., Tooze S.A. Evolution of Atg1 function and regulation. Autophagy 2009, 5:758-765.
10. Chan E.Y., Longatti A., McKnight N.C., Tooze S.A. Kinase-inactivated ULK proteins inhibit autophagy via their conserved C-terminal domains using an Atg13-independent mechanism. Mol. Cell. Biol. 2009, 29:157-171.
11. Chang Y.Y., Neufeld T.P. An Atg1/Atg13 complex with multiple roles in TOR-mediated autophagy regulation. Mol. Biol. Cell 2009, 20:2004-2014.
12. Chang Y.Y., Neufeld T.P. Autophagy takes flight in Drosophila. FEBS Lett. 2010, 584:1342-1349.
13. Colombani J., Raisin S., Pantalacci S., Radimerski T., Montagne J., Léopold P. A nutrient sensor mechanism controls Drosophila growth. Cell 2003, 114:739-749.
14. Egan D., Kim J., Shaw R.J., Guan K.L. The autophagy initiating kinase ULK1 is regulated via opposing phosphorylation by AMPK and mTOR. Autophagy 2011, 7:643-644.
15. Franzetti E., et al. Autophagy precedes apoptosis during the remodeling of silkworm larval midgut. Apoptosis 2012, 17:305-324.
16. Goncu E., Parlak O. Some autophagic and apoptotic features of programmed cell death in the anterior silk glands of the silkworm, Bombyx mori. Autophagy 2008, 4:1069-1072.
17. Gutternigg M., et al. Biosynthesis of truncated N-linked oligosaccharides results from non-orthologous hexosaminidase-mediated mechanisms in nematodes, plants and insects. J. Biol. Chem. 2007, 282:27825-27840.
18. Hakim R.S., Baldwin K., Smagghe G. Regulation of midgut growth, development, and metamorphosis. Annu. Rev. Entomol. 2010, 55:593-608.
19. Hanks S.K., Hunter T. Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J. 1995, 9:576-596.
20. Horton P., et al. WoLF PSORT: protein localization predictor. Nucleic Acids Res. 2007, 35:W585-W587.
21. Hosokawa N., et al. Nutrient-dependent mTORC1 association with the ULK1-Atg13-FIP200 complex required for autophagy. Mol. Biol. Cell 2009, 20:1981-1991.
22. Hou Y.C., Chittaranjan S., Barbosa S.G., McCall K., Gorski S.M. Effector caspase Dcp-1 and IAP protein Bruce regulate starvation-induced autophagy during Drosophila melanogaster oogenesis. J. Cell Biol. 2008, 182:1127-1139.
23. Hunter S., et al. InterPro: the integrative protein signature database. Nucleic Acids Res. 2009, 37:D211-D215. (Database issue).
24. Itakura E., Mizushima N. Characterization of autophagosome formation site by a hierarchical analysis of mammalian Atg proteins. Autophagy 2010, 6:764-776.
25. Johansen M.B., Kiemer L., Brunak S. Analysis and prediction of mammalian protein glycation. Glycobiology 2006, 16:844-853.
26. Jones D.T. Improving the accuracy of transmembrane protein topology prediction using evolutionary information. Bioinformatics 2007, 23:538-544.
27. Jones D.T., Taylor W.R., Thornton J.M. A model recognition approach to the prediction of all-helical membrane protein structure and topology. Biochemistry 1994, 33:3038-3049.
28. Julenius K. NetCGlyc 1.0: prediction of mammalian C-mannosylation sites. Glycobiology 2007, 17:868-876.
29. Julenius K., Mølgaard A., Gupta R., Brunak S. Prediction, conservation analysis and structural characterization of mammalian mucin-type O-glycosylation sites. Glycobiology 2005, 15:153-164.
30. Kamada Y., Funakoshi T., Shintani T., Nagano K., Ohsumi M., Ohsumi Y. Tor-mediated induction of autophagy via an Apg1 protein kinase complex. J. Cell Biol. 2000, 150:1507-1513.
31. Kamada Y., et al. Tor directly controls the Atg1 kinase complex to regulate autophagy. Mol. Cell. Biol. 2010, 30:1049-1058.
32. Kiguchi K., Agui N. Ecdysteroid levels and developmental events during larval moulting in the silkworm, Bombyx mori. J. Insect Physiol. 1981, 27:805-812.
33. Kijanska M., et al. Activation of Atg1 kinase in autophagy by regulated phosphorylation. Autophagy 2010, 6:1168-1178.
34. Klionsky D.J. Autophagy: from phenomenology to molecular understanding in less than a decade. Nat. Rev. Mol. Cell Biol. 2007, 8:931-937.
35. Klionsky D.J., et al. A unified nomenclature for yeast autophagy-related genes. Dev. Cell 2003, 5:539-545.
36. Klionsky D.J., et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012, 8:445-544.
37. Krogh A., Larsson B., von Heijne G., Sonnhammer E.L. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 2001, 305:567-580.
38. Kundu M. ULK1, mammalian target of rapamycin, and mitochondria: linking nutrient availability and autophagy. Antioxid. Redox. Signal. 2011, 14:1953-1958.
39. Kuroyanagi H., et al. Human ULK1, a novel serine/threonine kinase related to UNC-51 kinase of Caenorhabditis elegans: cDNA cloning, expression, and chromosomal assignment. Genomics 1998, 51:76-85.
40. Lee S.B., et al. ATG1, an autophagy regulator, inhibits cell growth by negatively regulating S6 kinase. EMBO Rep. 2007, 8:360-365.
41. Levine B., Klionsky D.J. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev. Cell 2004, 6:463-477.
42. Li Q., et al. Autophagy, apoptosis and ecdysis-related gene expression in the silk gland of the silkworm (Bombyx mori) during metamorphosis. Can. J. Zool. 2010, 88:1169-1178.
43. Li Q., Zheng S., Liu L., Tettamanti G., Cao Y., Feng Q. Expression of autophagy-related genes in the anterior silk gland of Bombyx mori during metamorphosis. Can. J. Zool. 2011, 89:1019-1026.
44. Loewith R., et al. Two TOR complexes, only one of which is rapamycin sensitive, have distinct roles in cell growth control. Mol. Cell 2002, 10:457-468.
45. Lomelí H., Vázquez M. Emerging roles of the SUMO pathway in development. Cell Mol. Life Sci. 2011, 68:4045-4064.
46. Lommel M., Strahl S. Protein O-mannosylation: conserved from bacteria to humans. Glycobiology 2009, 19:816-828.
47. Malagoli D., et al. Autophagy and its physiological relevance in arthropods: current knowledge and perspectives. Autophagy 2010, 6:575-588.
48. Matsuura A., Tsukada M., Wada Y., Ohsumi Y. Apg1p, a novel protein kinase required for the autophagic process in Saccharomyces cerevisiae. Gene 1997, 192:245-250.
49. Mizushima N. The role of the Atg1/ULK1 complex in autophagy regulation. Curr. Opin. Cell Biol. 2010, 22:132-139.
50. Mizushima N., Ohsumi Y., Yoshimori T. Autophagosome formation in mammalian cells. Cell Struct. Funct. 2002, 27:421-429.
51. Mizushima N., Levine B., Cuervo A.M., Klionsky D.J. Autophagy fights disease through cellular self-digestion. Nature 2008, 451:1069-1075.
52. Mpakou V.E., Nezis I.P., Stravopodis D.J., Margaritis L.H., Papassideri I.S. Different modes of programmed cell death during oogenesis of the silkmoth Bombyx mori. Autophagy 2008, 4:97-100.
53. Nezis I.P., et al. Cell death during Drosophila melanogaster early oogenesis is mediated through autophagy. Autophagy 2009, 5:298-302.
54. Nezis I.P., et al. Autophagic degradation of dBruce controls DNA fragmentation in nurse cells during late Drosophila melanogaster oogenesis. J. Cell Biol. 2010, 190:523-531.
55. Noda T., Ohsumi Y. Tor, a phosphatidylinositol kinase homologue, controls autophagy in yeast. J. Biol. Chem. 1998, 273:3963-3966.
56. Nordahl Petersen T., Brunak S., von Heijne G., Nielsen H. SignalP 4.0 - discriminating signal peptides from transmembrane regions. Nat. Methods 2011, 8:785-786.
57. Ogura K., et al. Caenorhabditis elegans unc-51 gene required for axonal elongation encodes a novel serine/threonine kinase. Genes Dev. 1994, 8:2389-2400.
58. Owa C., Aoki F., Nagata M. Gene expression and lysosomal content of silkworm peritracheal athrocytes. J. Insect Physiol. 2008, 54:1286-1292.
59. Pettersen E.F., et al. UCSF Chimera - a visualization system for exploratory research and analysis. J. Comput. Chem. 2004, 25:1605-1612.
60. Pierleoni A., Indio V., Savojardo C., Fariselli P., Martelli P.L., Casadio R. MemPype: a pipeline for the annotation of eukaryotic membrane proteins. Nucleic Acids Res. 2011, 39:W375-W380. (Web Server issue).
61. Ren J., et al. Systematic study of protein sumoylation: development of a site-specific predictor of SUMOsp 2.0. Proteomics 2009, 9:3409-3412.
62. Roy A., Kucukural A., Zhang Y. I-TASSER: a unified platform for automated protein structure and function prediction. Nat. Protoc. 2010, 5:725-738.
63. Ryerse J.S. Developmental changes in Malpighian tubule cell structure. Tissue Cell 1979, 11:533-551.
64. Saitou N., Nei M. The neighbor-joining method - a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 1987, 4:406-425.
65. Sakaguchi B. Gametogenesis, fertilization and embryogenesis of the silkworm. The Silkworm: An Important Laboratory Tool 1978, 5-10. Kodansha, Tokyo. Y. Tazima (Ed.).
66. Scott R.C., Schuldiner O., Neufeld T.P. Role and regulation of starvation-induced autophagy in the Drosophila fat body. Dev. Cell 2004, 7:167-178.
67. Scott R.C., Juhász G., Neufeld T.P. Direct induction of autophagy by Atg1 inhibits cell growth and induces apoptotic cell death. Curr. Biol. 2007, 17:1-11.
68. Shang L., Wang X. AMPK and mTOR coordinate the regulation of Ulk1 and mammalian autophagy initiation. Autophagy 2011, 7:924-926.
69. Sigrist C.J., et al. PROSITE: a documented database using patterns and profiles as motif descriptors. Brief. Bioinform. 2002, 3:265-274.
70. Sigrist C.J., et al. PROSITE, a protein domain database for functional characterization and annotation. Nucleic Acids Res. 2010, 38:D161-D166. (Database issue).
71. Sumithra P., Britto C.P., Krishnan M. Modes of cell death in the pupal perivisceral fat body tissue of the silkworm Bombyx mori L. Cell Tissue Res. 2010, 339:349-358.
72. Suzuki K., Kirisako T., Kamada Y., Mizushima N., Noda T., Ohsumi Y. The pre-autophagosomal structure organized by concerted functions of APG genes is essential for autophagosome formation. EMBO J. 2001, 20:5971-5981.
73. Tamura K., Dudley J., Nei M., Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007, 24:1596-1599.
74. Terashima J., Yasuhara N., Iwami M., Sakurai S., Sakurai S. Programmed cell death triggered by insect steroid hormone, 20-hydroxyecdysone, in the anterior silk gland of the silkworm, Bombyx mori. Dev. Genes Evol. 2000, 210:545-558.
75. Tettamanti G., et al. Programmed cell death and stem cell differentiation are responsible for midgut replacement in Heliothis virescens during prepupal instar. Cell Tissue Res. 2007, 330:345-359.
76. Tettamanti G., Grimaldi A., Pennacchio F., de Eguileor M. Lepidopteran larval midgut during prepupal instar: digestion or self-digestion?. Autophagy 2007, 3:630-631.
77. Vandenborre G., et al. Diversity in protein glycosylation among insect species. PLoS One 2011, 6:e16682.
78. Wang C.W., Klionsky D.J. The molecular mechanism of autophagy. Mol. Med. 2003, 9:65-76.
79. Xie Z., Klionsky D. Autophagosome formation: core machinery and adaptations. Nat. Cell Biol. 2007, 9:1102-1109.
80. Yan J., et al. Identification of mouse ULK1, a novel protein kinase structurally related to C. elegans UNC-51. Biochem. Biophys. Res. Commun. 1998, 246:222-227.
81. Yeh Y.Y., Wrasman K., Herman P.K. Autophosphorylation within the Atg1 activation loop is required for both kinase activity and the induction of autophagy in Saccharomyces cerevisiae. Genetics 2010, 185:871-882.
82. Yeh Y.Y., et al. The identification and analysis of phosphorylation sites on the Atg1 protein kinase. Autophagy 2011, 7:716-726.
83. Zhang Y. Template-based modeling and free modeling by I-TASSER in CASP7. Proteins 2007, 69:108-117.
84. Zhang Y. I-TASSER server for protein 3D structure prediction. BMC Bioinforma. 2008, 9:40.
85. Zhang X., et al. Systematic cloning and analysis of autophagy-related genes from the silkworm Bombyx mori. BMC Mol. Biol. 2009, 10:50.
86. Zhou S., et al. Two Tor genes in the silkworm Bombyx mori. Insect Mol. Biol. 2010, 19:727-735.