A comprehensive characterization of the caspase gene family in insects from the order Lepidoptera

BMC Genomics

Volumn 12, Issue , 2011, Pages

  Courtiade, Juliette ^a   Pauchet, Yannick ^a   Vogel, Heiko ^a   Heckel, David G ^a  

^a MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; CASPASE 2; CASPASE 3; CASPASE 4; CASPASE 5; CASPASE 6; INTERLEUKIN 1BETA CONVERTING ENZYME; PROTEIN P35;

ARTICLE; BIOINFORMATICS; CONTROLLED STUDY; DROSOPHILA; EXPRESSED SEQUENCE TAG; GENE ACTIVATION; GENE CLUSTER; GENE DUPLICATION; GENE FUNCTION; GENE IDENTIFICATION; GENE SEQUENCE; GENE STRUCTURE; GENETIC ANALYSIS; GENETIC CONSERVATION; GENETIC DATABASE; GENETIC VARIABILITY; INSECT GENOME; LEPIDOPTERA; MANDUCA SEXTA; NONHUMAN; PHYLOGENY; SEQUENCE HOMOLOGY; SILKWORM; SPECIES DIFFERENCE; AMINO ACID SEQUENCE; ANIMAL; CLASSIFICATION; ENZYMOLOGY; GENETICS; MOLECULAR GENETICS; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT;

BOMBYX MORI; DIPTERA; HEXAPODA; LEPIDOPTERA; MAMMALIA; MANDUCA SEXTA; NOCTUIDAE;

AMINO ACID SEQUENCE; ANIMALS; CASPASE 1; CASPASE 3; CASPASE 6; CASPASES; DROSOPHILA; EXPRESSED SEQUENCE TAGS; LEPIDOPTERA; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT;

EID: 79960025621     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-12-357     Document Type: Article

References (78)

1. Penaloza C, Orlanski S, Ye Y, Entezari-Zaher T, Javdan M, Zakeri Z. Cell death in mammalian development. Curr Pharm Des 2008, 14:184-196. 10.2174/138161208783378789, 18220829.
2. Amundson SA, Myers TG, Fornace AJ. Roles for p53 in growth arrest and apoptosis: putting on the brakes after genotoxic stress. Oncogene 1998, 17:3287-3299.
3. Creagh EM, Conroy H, Martin SJ. Caspase-activation pathways in apoptosis and immunity. Immunol Rev 2003, 193:10-21. 10.1034/j.1600-065X.2003.00048.x, 12752666.
4. Lockshin RA, Williams CM. Programmed cell death--II. Endocrine potentiation of the breakdown of the intersegmental muscles of silkmoths. Journal of Insect Physiology 1964, 10:643-649.
5. Weeks JC, Truman JW. Independent steroid control of the fates of motoneurons and their muscles during insect metamorphosis. J Neurosci 1985, 5:2290-2300.
6. Lockshin RA, Zakeri Z. Programmed cell death: early changes in metamorphosing cells. Biochem Cell Biol 1994, 72:589-596. 10.1139/o94-078, 7654332.
7. Truman JW. Cell death in invertebrate nervous systems. Annu Rev Neurosci 1984, 7:171-188. 10.1146/annurev.ne.07.030184.001131, 6324643.
8. Uwo MF, Ui-Tei K, Park P, Takeda M. Replacement of midgut epithelium in the greater wax moth, Galleria mellonela, during larval-pupal moult. Cell Tissue Res 2002, 308:319-331. 10.1007/s00441-002-0515-1, 12037588.
9. Parthasarathy R, Palli SR. Developmental and hormonal regulation of midgut remodeling in a lepidopteran insect, Heliothis virescens. Mechanisms of Development 2007, 124:23-34. 10.1016/j.mod.2006.09.002, 17107775.
10. Clem RJ. Baculoviruses and apoptosis: a diversity of genes and responses. Curr Drug Targets 2007, 8:1069-1074. 10.2174/138945007782151405, 17979666.
11. Koonin EV, Aravind L. Origin and evolution of eukaryotic apoptosis: the bacterial connection. Cell Death Differ 2002, 9:394-404. 10.1038/sj.cdd.4400991, 11965492.
12. Shaham S. Identification of Multiple Caenorhabditis elegans Caspases and Their Potential Roles in Proteolytic Cascades. Journal of Biological Chemistry 1998, 273:35109-35117. 10.1074/jbc.273.52.35109, 9857046.
13. Kumar S, Doumanis J. The fly caspases. Cell Death Differ 2000, 7:1039-1044. 10.1038/sj.cdd.4400756, 11139276.
14. Bryant B, Blair CD, Olson KE, Clem RJ. Annotation and expression profiling of apoptosis-related genes in the yellow fever mosquito, Aedes aegypti. Insect Biochem Mol Biol 2008, 38:331-345. 2258459, 18252247.
15. Chowdhury I, Tharakan B, Bhat GK. Caspases--An update. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 2008, 151:10-27.
16. Eckhart L, Ballaun C, Hermann M, VandeBerg JL, Sipos W, Uthman A, Fischer H, Tschachler E. Identification of Novel Mammalian Caspases Reveals an Important Role of Gene Loss in Shaping the Human Caspase Repertoire. Mol Biol Evol 2008, 25:831-841. 10.1093/molbev/msn012, 18281271.
17. Robertson AJ, Croce J, Carbonneau S, Voronina E, Miranda E, McClay DR, Coffman JA. The genomic underpinnings of apoptosis in Strongylocentrotus purpuratus. Developmental Biology 2006, 300:321-334. 10.1016/j.ydbio.2006.08.053, 17010332.
18. Ameisen JC. On the origin, evolution, and nature of programmed cell death: a timeline of four billion years. Cell Death Differ 2002, 9:367-393. 10.1038/sj.cdd.4400950, 11965491.
19. Talanian RV, Quinlan C, Trautz S, Hackett MC, Mankovich JA, Banach D, Ghayur T, Brady KD, Wong WW. Substrate specificities of caspase family proteases. J Biol Chem 1997, 272:9677-9682. 10.1074/jbc.272.15.9677, 9092497.
20. Garcia-Calvo M, Peterson EP, Rasper DM, Vaillancourt JP, Zamboni R, Nicholson DW, Thornberry NA. Purification and catalytic properties of human caspase family members. Cell Death Differ 1999, 6:362-369. 10.1038/sj.cdd.4400497, 10381624.
21. Nicholson DW. Caspase structure, proteolytic substrates, and function during apoptotic cell death. Cell Death Differ 1999, 6:1028-1042. 10.1038/sj.cdd.4400598, 10578171.
22. Dorstyn L, Colussi PA, Quinn LM, Richardson H, Kumar S. DRONC, an ecdysone-inducible Drosophila caspase. Proc Natl Acad Sci USA 1999, 96:4307-4312. 10.1073/pnas.96.8.4307, 16328, 10200258.
23. Fuentes-Prior P, Salvesen GS. The protein structures that shape caspase activity, specificity, activation and inhibition. Biochem J 2004, 384:201-232. 10.1042/BJ20041142, 1134104, 15450003.
24. Park HH, Lo YC, Lin SC, Wang L, Yang JK, Wu H. The death domain superfamily in intracellular signaling of apoptosis and inflammation. Annu Rev Immunol 2007, 25:561-586. 10.1146/annurev.immunol.25.022106.141656, 2904440, 17201679.
25. Chang HY, Yang X. Proteases for cell suicide: functions and regulation of caspases. Microbiol Mol Biol Rev 2000, 64:821-846. 10.1128/MMBR.64.4.821-846.2000, 99015, 11104820.
26. Fan TJ, Han LH, Cong RS, Liang J. Caspase family proteases and apoptosis. Acta Biochim Biophys Sin (Shanghai) 2005, 37:719-727.
27. Dorstyn L, Mills K, Lazebnik Y, Kumar S. The two cytochrome c species, DC3 and DC4, are not required for caspase activation and apoptosis in Drosophila cells. The Journal of Cell Biology 2004, 167:405-410. 10.1083/jcb.200408054, 2172470, 15533997.
28. Clem RJ, Fechhmeimer M, Miller LK. Prevention of apoptosis by a baculovirus gene during infection of insect cells. Science 1991, 254:1388-1390. 10.1126/science.1962198, 1962198.
29. Ahmad M, Srinivasula SM, Wang L, Litwack G, Fernandes-Alnemri T, Alnemri ES. Spodoptera frugiperda caspase-1, a novel insect death protease that cleaves the nuclear immunophilin FKBP46, is the target of the baculovirus antiapoptotic protein p35. J Biol Chem 1997, 272:1421-1424. 10.1074/jbc.272.3.1421, 8999805.
30. Liu Q, Qi Y, Chejanovsky N. Spodoptera littoralis caspase-1, a Lepidopteran effector caspase inducible by apoptotic signaling. Apoptosis 2005, 10:787-795. 10.1007/s10495-005-0365-x, 16133869.
31. Yang D, Chai L, Wang J, Zhao X. Molecular cloning and characterization of Hearm caspase-1 from Helicoverpa armigera. Mol Biol Rep 2007,
32. Hebert CG, Valdes JJ, Bentley WE. Investigating apoptosis: characterization and analysis of Trichoplusia ni-caspase-1 through overexpression and RNAi mediated silencing. Insect Biochem Mol Biol 2009, 39:113-124. 10.1016/j.ibmb.2008.10.009, 19027856.
33. Manji GA, Friesen PD. Apoptosis in motion. An apical, P35-insensitive caspase mediates programmed cell death in insect cells. J Biol Chem 2001, 276:16704-16710. 10.1074/jbc.M010179200, 11278634.
34. Zoog SJ, Schiller JJ, Wetter JA, Chejanovsky N, Friesen PD. Baculovirus apoptotic suppressor P49 is a substrate inhibitor of initiator caspases resistant to P35 in vivo. Embo J 2002, 21:5130-5140. 10.1038/sj.emboj.7594736, 129042, 12356729.
35. Seshagiri S, Miller LK. Baculovirus inhibitors of apoptosis (IAPs) block activation of Sf-caspase-1. Proc Natl Acad Sci USA 1997, 94:13606-13611. 10.1073/pnas.94.25.13606, 28353, 9391073.
36. Xia QY, Wang J, Zhou ZY, Li RQ, Fan W, Cheng DJ, Cheng TC, Qin JJ, Duan J, Xu HF, et al. The genome of a lepidopteran model insect, the silkworm Bombyx mori. Insect Biochemistry and Molecular Biology 2008, 38:1036-1045. 10.1016/j.ibmb.2008.11.004, 19121390.
37. Zhang JY, Pan MH, Sun ZY, Huang SJ, Yu ZS, Liu D, Zhao DH, Lu C. The genomic underpinnings of apoptosis in the silkworm, Bombyx mori. BMC Genomics 2010, 11:611. 10.1186/1471-2164-11-611, 3091752, 21040523.
38. Alnemri ES, Livingston DJ, Nicholson DW, Salvesen G, Thornberry NA, Wong WW, Yuan J. Human ICE/CED-3 Protease Nomenclature. Cell 1996, 87:171. 10.1016/S0092-8674(00)81334-3, 8861900.
39. Dorstyn L, Read SH, Quinn LM, Richardson H, Kumar S. DECAY, a Novel Drosophila Caspase Related to Mammalian Caspase-3 and Caspase-7. Journal of Biological Chemistry 1999, 274:30778-30783. 10.1074/jbc.274.43.30778, 10521468.
40. Fraser AG, Evan GI. Identification of a Drosophila melanogaster ICE/CED-3-related protease, drICE. Embo J 1997, 16:2805-2813. 10.1093/emboj/16.10.2805, 1169889, 9184225.
41. Fraser AG, McCarthy NJ, Evan GI. drICE is an essential caspase required for apoptotic activity in Drosophila cells. Embo J 1997, 16:6192-6199. 10.1093/emboj/16.20.6192, 1326303, 9321398.
42. Song Z, McCall K, Steller H. DCP-1, a Drosophila Cell Death Protease Essential for Development. Science 1997, 275:536-540. 10.1126/science.275.5299.536, 8999799.
43. Muro I, Berry DL, Huh JR, Chen CH, Huang H, Yoo SJ, Guo M, Baehrecke EH, Hay BA. The Drosophila caspase Ice is important for many apoptotic cell deaths and for spermatid individualization, a nonapoptotic process. Development 2006, 133:3305-3315. 10.1242/dev.02495, 16887831.
44. Xu D, Wang Y, Willecke R, Chen Z, Ding T, Bergmann A. The effector caspases drICE and dcp-1 have partially overlapping functions in the apoptotic pathway in Drosophila. Cell Death Differ 2006, 13:1697-1706. 10.1038/sj.cdd.4401920, 2519037, 16645642.
45. Bryant B, Ungerer MC, Liu Q, Waterhouse RM, Clem RJ. A caspase-like decoy molecule enhances the activity of a paralogous caspase in the yellow fever mosquito, Aedes aegypti. Insect Biochemistry and Molecular Biology 2010, 40:516-523. 10.1016/j.ibmb.2010.04.011, 2902568, 20417712.
46. Muro I, Monser K, Clem RJ. Mechanism of Dronc activation in Drosophila cells. J Cell Sci 2004, 117:5035-5041. 10.1242/jcs.01376, 15383617.
47. Snipas SJ, Drag M, Stennicke HR, Salvesen GS. Activation mechanism and substrate specificity of the Drosophila initiator caspase DRONC. Cell Death Differ 2008, 15:938-945. 10.1038/cdd.2008.23, 18309328.
48. Chen P, Rodriguez A, Erskine R, Thach T, Abrams JM. Dredd, a Novel Effector of the Apoptosis Activators Reaper, Grim, and Hid in Drosophila. Developmental Biology 1998, 201:202-216. 10.1006/dbio.1998.9000, 9740659.
49. Leulier F, Rodriguez A, Khush RS, Abrams JM, Lemaitre B. The Drosophila caspase Dredd is required to resist gram-negative bacterial infection. EMBO Rep 2000, 1:353-358. 10.1093/embo-reports/kvd073, 1083747, 11269502.
50. Doumanis J, Quinn L, Richardson H, Kumar S. STRICA, a novel Drosophila melanogaster caspase with an unusual serine/threonine-rich prodomain, interacts with DIAP1 and DIAP2. Cell Death Differ 2001, 8:387-394. 10.1038/sj.cdd.4400864, 11550090.
51. Harvey NL, Daish T, Mills K, Dorstyn L, Quinn LM, Read SH, Richardson H, Kumar S. Characterization of the Drosophila caspase, DAMM. J Biol Chem 2001, 276:25342-25350. 10.1074/jbc.M009444200, 11337486.
52. Baum JS, Arama E, Steller H, McCall K. The Drosophila caspases Strica and Dronc function redundantly in programmed cell death during oogenesis. Cell Death Differ 2007, 14:1508-1517. 10.1038/sj.cdd.4402155, 17464325.
53. Seol DW, Billiar TR. A Caspase-9 Variant Missing the Catalytic Site Is an Endogenous Inhibitor of Apoptosis. Journal of Biological Chemistry 1999, 274:2072-2076. 10.1074/jbc.274.4.2072, 9890966.
54. Ng PWP, Porter AG, Jänicke RU. Molecular Cloning and Characterization of Two Novel Pro-apoptotic Isoforms of Caspase-10. Journal of Biological Chemistry 1999, 274:10301-10308. 10.1074/jbc.274.15.10301, 10187817.
55. Pauchet Y, Freitak D, Heidel-Fischer HM, Heckel DG, Vogel H. Immunity or digestion: glucanase activity in a glucan-binding protein family from Lepidoptera. J Biol Chem 2009, 284:2214-2224.
56. d'Alencon E, Sezutsu H, Legeai F, Permal E, Bernard-Samain S, Gimenez S, Gagneur C, Cousserans F, Shimomura M, Brun-Barale A, et al. Extensive synteny conservation of holocentric chromosomes in Lepidoptera despite high rates of local genome rearrangements. Proc Natl Acad Sci USA 2010, 107:7680-7685. 10.1073/pnas.0910413107, 2867904, 20388903.
57. Nei M, Gojobori T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 1986, 3:418-426.
58. Nei M. Molecular evolution and phylogenetics. 2000, New York: Oxford Univ. Press.
59. Gu X. Statistical methods for testing functional divergence after gene duplication. Molecular Biology and Evolution 1999, 16:1664-1674.
60. Conant GC, Wagner A. Asymmetric Sequence Divergence of Duplicate Genes. Genome Research 2003, 13:2052-2058. 10.1101/gr.1252603, 403682, 12952876.
61. Panchin A, Gelfand M, Ramensky V, Artamonova I. Asymmetric and non-uniform evolution of recently duplicated human genes. Biology Direct 2010, 5:54. 10.1186/1745-6150-5-54, 2942815, 20825637.
62. Lynch M, Conery JS. The Evolutionary Fate and Consequences of Duplicate Genes. Science 2000, 290:1151-1155. 10.1126/science.290.5494.1151, 11073452.
63. Hughes AL. The Evolution of Functionally Novel Proteins after Gene Duplication. Proceedings of the Royal Society of London Series B: Biological Sciences 1994, 256:119-124. 10.1098/rspb.1994.0058, 8029240.
64. Pauchet Y, Wilkinson P, Vogel H, Nelson DR, Reynolds SE, Heckel DG, ffrench-Constant RH. Pyrosequencing the Manduca sexta larval midgut transcriptome: messages for digestion, detoxification and defence. Insect Mol Biol 2010, 19:61-75. 10.1111/j.1365-2583.2009.00936.x, 19909380.
65. Freitak D, Wheat CW, Heckel DG, Vogel H. Immune system responses and fitness costs associated with consumption of bacteria in larvae of Trichoplusia ni. BMC Biol 2007, 5:56. 10.1186/1741-7007-5-56, 2235825, 18154650.
66. Fischer HM, Wheat CW, Heckel DG, Vogel H. Evolutionary origins of a novel host plant detoxification gene in butterflies. Mol Biol Evol 2008, 25:809-820. 10.1093/molbev/msn014, 18296701.
67. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acids Res 1997, 25:4876-4882. 10.1093/nar/25.24.4876, 147148, 9396791.
68. Insecta Central. , http://insectacentral.org
69. Papanicolaou A, Stierli R, ffrench-Constant RH, Heckel DG. Next generation transcriptomes for next generation genomes using est2assembly. BMC Bioinformatics 2009, 10:447. 10.1186/1471-2105-10-447, 3087352, 20034392.
70. McIntosh AH, Ignoffo CM, Quhou C, Pappas M. Establishment of a cell ine from Heliothis armigera (Hbn.) (Lepidoptera: Noctuidae). In Vitro 1983, 19:589-590.
71. Katoh K, Toh H. Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 2008, 9:286-298. 10.1093/bib/bbn013, 18372315.
72. Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574. 10.1093/bioinformatics/btg180, 12912839.
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. 10.1093/molbev/msm092, 17488738.
74. LaCount DJ, Hanson SF, Schneider CL, Friesen PD. Caspase inhibitor P35 and inhibitor of apoptosis Op-IAP block in vivo proteolytic activation of an effector caspase at different steps. J Biol Chem 2000, 275:15657-15664. 10.1074/jbc.M000791200, 10747956.
75. Gu X, Vander Velden K. DIVERGE: phylogeny-based analysis for functional-structural divergence of a protein family. Bioinformatics 2002, 18:500-501. 10.1093/bioinformatics/18.3.500, 11934757.
76. ExPASy ScanProsite. , http://www.expasy.ch/tools/scanprosite
77. Kaikobase. , http://sgp.dna.affrc.go.jp/KAIKObase/
78. Shimomura M, Minami H, Suetsugu Y, Ohyanagi H, Satoh C, Antonio B, Nagamura Y, Kadono-Okuda K, Kajiwara H, Sezutsu H, et al. KAIKObase: an integrated silkworm genome database and data mining tool. BMC Genomics 2009, 10:486. 10.1186/1471-2164-10-486, 2770533, 19843344.