Embryonic diapause highlighted by differential expression of mRNAs for ecdysteroidogenesis, transcription and lipid sparing in the cricket Allonemobius socius

Journal of Experimental Biology

Volumn 212, Issue 13, 2009, Pages 2075-2084

  Reynolds, Julie A ^a,b   Hand, Steven C ^a  

^a LOUISIANA STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Cell cycle; Diapause; Ecdysone; Lipid metabolism; Metabolic depression; qRT PCR

Indexed keywords

ECDYSTEROID; INSECT PROTEIN; MESSENGER RNA;

ANIMAL; ANIMAL EMBRYO; ARTICLE; BIOSYNTHESIS; CELL CYCLE; DNA REPLICATION; EMBRYO DEVELOPMENT; EXPRESSED SEQUENCE TAG; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GRYLLIDAE; LIPID METABOLISM; METABOLISM; PHYSIOLOGY; PRENATAL DEVELOPMENT; PROTEIN PROCESSING; SIGNAL TRANSDUCTION;

ANIMALS; CELL CYCLE; DNA REPLICATION; ECDYSTEROIDS; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; EXPRESSED SEQUENCE TAGS; GENE EXPRESSION REGULATION; GRYLLIDAE; INSECT PROTEINS; LIPID METABOLISM; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

ALLONEMOBIUS SOCIUS; NEMOBIINAE;

EID: 67649560598     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.027367     Document Type: Article

References (105)

1. Aggler, R. and Capaldi, R. A. (1990). Yeast cytochrome c oxidase subunit VII is essential for assembly of an active enzyme: cloning, sequencing, and characterization of the nuclear-encoded gene. J. Biol. Chem. 265, 16389-16393.
2. Anderson, K. V. and Lengyel, J. A. (1980). Changing rates of histone mRNA synthesis and turnover in Drosophila embryos. Cell 21, 717-727.
3. Benjamini, Y. and Hochberg, Y. (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Series B Stat. Methodol. 57, 289-300.
4. Blitvich, B. J., Rayms-Keller, A., Blair, C. D. and Beaty, B. J. (2001). Identification and sequence determination of mRNAs detected in dormant (diapausing) Aedes triseriatus mosquito embryos. DNA Seq. 12, 197-202.
5. Brock, T. J., Browse, J. and Watts, J. L. (2006). Genetic regulation of unsaturated fatty acid composition in C. elegans. PLoS Genet. 2, e108.
6. Chae, H. J., Ke, N., Kim, H. R., Chen, S., Godzik, A., Dickman, M. and Reed, J. C. (2003). Evolutionary conserved cyto protect i on provided by Bax lnhibitor-1 homologs from animals, plants, and yeast. Gene 323, 101-113.
7. Chavez, V. M., Marques, G., Delbrecque, J. P., Kobayashi, K., Hollingsworth, M., Burr, J., Natzle, J. E. and O'Connor, M. B. (2000). The Drosophila disembodied gene controls late embryonic morphogenesis and codes for a cytochrome p450 enzyme that regulates embryonic ecdysone levels. Development 127, 4114-4126.
8. Cho, W. L., Tsao, S. M., Hays, A. R., Walter, R., Chen, J. S., Snigirevskaya, E. S. and Raikhel, A. S. (1999). Mosquito cathpesin b-like protease involved in embryonic degradation of vitellin is produced as a latent extraovarian precursor. J. Biol. Chem. 274, 13311-13321.
9. Clegg, J. S. (2005). Desiccation tolerance in encysted embryos of the animal extremophile, Artemia. Integr. Comp. Biol. 45, 715-724.
10. Clegg, J. S., Drinkwater, L. E. and Sorgeloos, P. (1996). The metabolic status of diapause embryos of Artemia franciscana (SFB). Physiol. Zool. 69, 49-66.
11. Cossins, A., Fraser, J., Hughes, M. and Gracey, A. (2006). Post-genomic approaches to understanding the mechanisms of environmentally induced phenotypic plasticity. J. Exp. Biol. 209, 2328-2336.
12. Denlinger, D. L. (1986). Dormancy in tropical insects. Annu. Rev. Entomol. 31, 239-264.
13. Denlinger, D. L. (2002). Regulation of diapause. Annu. Rev. Entomol. 47, 93-122.
14. Dorel, C. and Coulon, M. (1988). Regulation of gene expression in pre-diapausing embryos of the silkworm, Bombyx mori: pattern of protein synthesis. Cell Differ. 23, 87-92.
15. 1-S transition. Mol. Ceil. Biol. 18, 141-151.
16. Etard, C., Gradl, D., Kunz, M., Eilers, M. and Wedlich, D. (2005). Pontin and Reptin regulate cell prolieration in early Xenopus embryos in collaboration with c-Myc and Miz-1. Mech. Dev. 122, 545-556.
17. Feyereisen, R. (2005). Insect cytochrome P450. In Comprehensive Molecular Insect Science, vol 4 (ed. L. I. Gilbert, K. Iatrou and S. S. Gill), pp. 1-77. Oxford: Elsevier.
18. Flannagan, R. D., Tammariello, S. P., Joplin, K. H., Cikra-Ireland, R. A., Yolcum, G. D. and Denlinger, D. L. (1998). Diapause-specific gene expression in pupae of the flesh fly Sarcophaga crassipalpis. Proc. Natl. Acad. Sci. USA 95, 5616-5620.
19. Fulton, B. B. (1931). A study of the genus Nemobius (Orthoptera: Gyllidae). Ann. Entomol. Soc. Am. 24, 205-237.
20. Gerenday, A. and Fallon, A. M. (2004). Ecdysone-induced accumulation of mosquito cells in the G1 phase of the cell cycle. J. Insect Physiol. 50, 831-838.
21. Gharib, B., Girardie, A. and Dereggi, M. (1981). Ecdysteroids and control of embryonic diapause: changes in ecdysteroid levels and exhogenous hormone effects in the eggs of Cochineal lepidosaphes. Experientia 37, 1107-1108.
22. Gilbert, L. I. (2004). Halloween genes encode P450 enzymes that mediate steroid hormone biosynthesis in Drosophila melanogaster. Mol. Cell. Endocrinol. 215, 1-10.
23. Gregg, P. C., Roberts, B. and Wentworth, S. L. (1987). Levels of ecdysteroids in diapause and nondiapause eggs of the Australian plague locust, Chortoicetes terminifera (Walker). J. Insect Physiol. 33, 237-242.
24. Guppy, M. and Withers, P. (1999). Metabolic depression in animals: physiological perspectives and biochemical generalizations. Biol. Rev. Camb. Philos. Soc. 74, 1-40.
25. Hahn, D. A. and Denlinger, D. L. (2007). Meeting the energetic demands of insect diapause: nutrient storage and utilization. J. Insect Physiol. 53, 760-773.
26. Hand, S. C. (1991). Metabolic dormancy in aquatic invertebrates. In Advances in Comparative and Environmental Physiology, vol. 8, pp. 1-50. New York: Springer-Verlag.
27. Hand, S. C. and Hardewig, I. (1996). Downregulation of cellular metabolism during environmental stress: mechanisms and implications. Annu. Rev. Physiol. 58, 539-563.
28. Hand, S. C., Podrabsky, J. E., Eads, B. D. and van Breukelen, F. (2001). Interrupted development in aquatic organisms: ecological context and physiological mechanisms. In Environment and Animal Development: Genes, Life Histories and Plasticity (ed. D. Atkinson and M. Thorndyke), pp. 219-234. Oxford: BIOS Scientific.
29. Hand, S. C., Jones, D., Menze, M. A. and Witt, T. L. (2007). Life without water: expression of plant LEA genes by an anhydrobiotic arthropod. J. Exp. Zool. 307A, 62-66.
30. Hazel, J. R. (1995). Thermal adaptation in biological membranes: is homeoviscous adaptation the explanation? Annu. Rev. Physiol. 57, 19-42.
31. Hochachka, P. W. and Guppy, M. (1987). Metabolic Arrest and the Control of Biological Time. Cambridge, MA: Harvard University Press.
32. Hochachka, P. W. and Somero, G. N. (2002). Biochemical Adaptation. New York: Oxford University Press.
33. Hogan, T. W. (1959). A rapid method for examining diapause embryos of Acheta commodus W. Nature 183, 269.
34. Hong, S. M., Nho, S. K., Kim, N. S., Lee, J. S. and Kang, S. W. (2006). Gene expression profiling in the silkworm, Bombyx mori, during early embryonic development. Zool. Sci. 23, 517-528.
35. Horike, N. and Sonobe, H. (1999). Ecdysone 20-monooxygenase in eggs of the silkworm, Bombyx mori: enzymatic properties and developmental changes. Arch. Insect Biochem. Physiol. 41, 9-17.
36. Horike, N., Takemori, H., Nonaka, Y., Sonobe, H. and Okamoto, M. (2000). Molecular cloning of NADPH-cytochrome P450 oxidoreductase from silkworm eggs: its involvement in 20-hydroxyecdysone biosynthesis during embryonic development. Eur. J Biochem. 267, 6914-6920.
37. Howard, D. J. and Furth, D. G. (1986). Review of the Allonemobius fasciatus (Orthoptera: Gryllidae) complex with the description of two new species separated by electrophoresis, songs and morphometries. Ann. Entomol. Soc. Am. 56, 472-481.
38. Huang, X., Warren, J. T. and Gilbert, L. I. (2008). New players in the regulation of ecdysone biosynthesis. J. Genet. Genomics 35, 1-10.
39. Huckelhoven, R. (2004). Bax lnhibitor-1, an ancient cell death suppressor in animals and plants with prokaryotic relatives. Apoptosis 9, 299-307.
40. Ioannou, Y. A. (2007). Neimann-Pick C proteins in sterol transport and absorption: flies in the ointment. Dev. Cell 12, 481-483.
41. Izumigama, S. and Suzuki, K. (1986). Nucleotide pools in the eggs of emma field cricket, Teleogryllus emma, and the two-spotted cricket, Gryllus bimaculatus (Orthoptera: Gryllidae). Appl. Entomol. Zool. 21, 405-410.
42. Jones, S. J. M., Riddle, D. L., Pouzyrev, A. T., Velculescu, V. E., Hillier, L., Eddy, S. R., Stricklin, S. L., Baillie, D. L., Waterson, R. and Marra, M. A. (2001). Changes in gene expression associted with developmental arrest and longevity in Caenorhabditis eiegans. Genome Res. 11, 1346-1352.
43. Joplin, K. H. and Denlinger, D. L. (1989). Cycles of protein synthesis during pupal diapause in the flesh fly, Sarcophaga crassipalpis. Arch. Insect Biochem. Physiol. 12, 111-122.
44. Kaocharern, P. (1958). Cytological Changes Associated With Diapause In Embryos Of The Grasshopper Melanoplus differentialis (Thomas). PhD Thesis, University of Wisconsin-Madison, Madison, WI, USA.
45. Kaygun, H. and Marzluff, W. F. (2005). Translation termination is involved in histone mRNA degradation when DNA replication is inhibited. Mol. Cell. Biol. 25, 6879-6888.
46. Kidokoro, K., Iwata, K. I., Fujiwara, Y. and Takeda, M. (2006). Effects of juvenile hormone analogs and 20-hydroxyecdysone on diapause temination in eggs of Locusta migratoria and Oxya yezoensis. J. Insect Physiol. 52, 473-479.
47. Kim, Y. J., Hwang Yoon, H. J., Lee, S. B., Ahn, M. I., Kim, N. S., Kim, I., Jeon, J. P. and Hwang, S. J. (2006). Expressed sequence tag analysis of the diapausing queen of the bumblee Bombus ignitus. Entomol. Res. 36, 191-195.
48. Koštál, V., Tollarová, M. and Doležel, D. (2008). Dynamism in physiology and gene transcription during reproductive diapause in a heteropteran bug, Pyrrhocoris apterus. J. Insect Physiol. 54, 77-88.
49. Lee, K. Y. and Denlinger, D. L. (1996). A role for ecdysteroids in the induction and maintennce of the pharate first instar diapause of the gyspy moth, Lymantria dispar. J. insect Physiol. 43, 289-296.
50. Lee, K. Y., Valaitis, A. P. and Denlinger, D. L. (1997). Further evidence that diapause in the gypsy moth, Lymantria dispar, is regulated by ecdysteroids: a comparison of diapause and nondiapause strains. J. Insect Physiol. 43, 897-903.
51. Lees, A. D. (1955). Physiology of Diapause in Arthropods. Cambridge: Cambridge University Press.
52. Li, Y., Park, J. S., Deng, J. H. and Bai, Y. (2006). Cytochrome c oxidase subunit IV is essential for assembly and respiratory function of the enzyme complex. J. Bioenerg. Biomembr. 38, 283-291.
53. Loomis, S. H., Hand, S. C. and Fell, P. E. (1996). Metabolism of gemmules from freshwater sponge, Eunapius fragilis, during diapause and post-diapause states. Biol. Bull. 191, 385-392.
54. Lopez, C. D., Martinovsky, G. and Naumovski, L. (2002). Inhibition of cell death by ribosomal protein L35a. Cancer Lett. 180, 195-202.
55. Luccio, E. D., Elling, R. A. and Wilson, D. K. (2006). Identification of a novel NADH-specific aldo-keto reductase using sequence and structural homologies. Biochem. J. 400, 105-114.
56. Maibeche-Coisne, M., Boscameric, M., Aragon, S., Lafont, R. and Dauphin-Villemant, C. (2001). Molecular cloning of a novel crustacean member of the aldoketoreductase superfamily, differentially expressed in the antennal glands. Biochem. Biophys. Res. Commun. 282, 314-320.
57. Medina, M., Leon, P. and Vallejo, C. G. (1988). Drosophila cathepsin B-like proteinase: a suggested role in yolk degradation. Arch. Biochem. Biophys. 263, 355-363.
58. Michaud, M. R. and Denlinger, D. L. (2006). Oleic acid is elevated in cell membranes during rapid cold-hardening and pupal diapause in the flesh fly, Sarcophaga crassipalpis. J. Insect Physiol., 52, 1073-1082.
59. Micheli, L., Leonardi, L., Conti, F., Buanne, P., Canu, N., Caruso, M. and Tirone, F. (2005). PC4 coactivates MyoD by relieving the histone deacetylase 4-mediated inhibition of myocyte enhancer factor 2C. Mol. Ceil. Biol. 25, 2242-2259.
60. Mimmack, M. L., Brooking, J. and Bahn, S. (2004). Quantitative polymerast chain reaction: validation of microarray results from postmortem brain studies. Biol. Psychiatry 55, 337-345.
61. Misener, S. R., Chen, C. P. and Walker, V. K. (2001). Cold tolerance and proline metabolic gene expression in Drosophila melanogaster. J. Insect Physiol. 47, 393-400.
62. Mousseau, T. A. and Roff, D. A. (1989). Adaptation to seasonality in a cricket: patterns of phenotypic and genotypic variation in body size and diapause expression along a dine in season length. Evolution 43, 1483-1496.
63. Mukhopadhyay, A., Hammen, P., Waltner-Law, M. and Weiner, H. (2002). Timing and structural consideration for the processing of mitochondrial matrix space proteins by the mitochondrial processing peptidase (MPP). Protein Sci. 11, 1026-1035.
64. Nakagaki, M., Takei, R., Nagashima, E. and Yaginuma, T. (1991). Cell cycles in embryos of the silkworm, Bombyx mori: G2-arrest at diapause stage. Roux's Arch. Dev. Biol. 200, 223-229.
65. Nicholls, D. G. and Ferguson, S. J. (2002). Bioenergetics 3. Amsterdam: Academic Press.
66. Nijhout, H. F. (1984). Insect Hormones. Princeton, NJ: Princeton University Press.
67. Noriega, F. G., Riveiro, J. M. C., Koener, J. F., Valenzuela, J. G., Hernandez-Martinez, S., Pham, V. M. and Feyereisen, R. (2006). Comparative genomics of insect juvenile hormone synthesis. Insect Biochem. Moi. Biol. 36, 366-374.
68. Ory, D. S. (2004). The Niemann-Pick disease genes regulators of cellular cholesterol homeostasis. Trends Cardiovasc. Med. 14, 66-72.
69. Podrabsky, J. E. and Hand, S. C. (1999). Bioenergetics of embryonic diapause in an annual killifish, Astrofundulis limnaeus. J. Exp. Biol. 202, 2567-2580.
70. Podrabsky, J. E. and Hand, S. C. (2000). Depression of protein synthesis during diapause in embryos of the annual killifish, Austrofundulus limnaeus. Physiol. Biochem. Zool. 73, 799-808.
71. Podrabsky, J. E., Carpenter, J. F. and Hand, S. C. (2001). Survival of water stress in annual fish embryos: dehydration avoidance and egg envelope amyloid fibers. Am. J. Physiol. 280, R123-R131.
72. Podrabsky, J. E., Lopez, J. P., Fan, T. W. M., Higashi, R. and Somero, G. N. (2007). Extreme anoxia tolerance in embryos of the annual killifish Austrofundulus limnaeus: insights from a metabolomics analysis. J. Exp. Biol. 210, 2253-2266.
73. Qi, D., Jin, H., Lilja, T. and Mannervik, M. (2006). Drosophila Reptin and other TIP60 complex components promote generation of silent chromatin. Genetics 174, 241-251.
74. Qiu, Z. and MacRae, T. H. (2007). Developmentally regulated synthesis of p8, a stress-associated transcription cofactor, in diapause-destined embryos of Artemia franciscana. Cell Stress Chaperones. 12, 255-264.
75. Qiu, Z., Tsoi, S. C. M. and MacRae, T. H. (2007). Gene expression in diapausedestined embryos of the crustacean. Mech. Dev. 124, 856-867.
76. Quan, G. X., Krell, P. J., Arif, B. M. and Feng, Q. (2006). Receptor of activated C kinase 1 (RACK1) is necessary for the 20-hydoxyecdysone-induced expression of the transcription factor CHR3 in the spruce budworm Choristoneura fumiferana. Insect Mol. Biol. 15, 79-87.
77. Rakshpal, R. (1962a). Respiratory metabolism during embryogenesis of Gryllus veletis (Alexander and Bigelow) (Orthoptera: Gryllidae). Physiol. Zool. 35, 47-51.
78. Rakshpal, R. (1962b). Respiratory metabolism during embryogenesis of a diapause species of field cricket, Gryllus pennsylvanicus Burmeister (Orthoptera, Gryllidae). J. Insect Physiol. 8, 217-221.
79. Ramlov, H. (1999). Microclimate and variations in haemolymph composition in the freezing-tolerant New Zealand alpine weta Hemideina maori Hutton (Orthoptera; Stenopelmatidae). J. Comp. Physiol. 6169, 224-235.
80. Reynolds, J. A. and Hand, S. C. (2004). Differences in isolated mitochondria are insufficient to account for respiratory depression during diapause in Artemia franciscana embryos. Physiol. Biochem. Zool. 77, 366-377.
81. Reynolds, J. A. and Hand, S. C. (2009). Decoupling development and energy flow during embryonic diapause in the cricket, Allonemobius socius. J. Exp. Biol. 212, 2065-2074.
82. Ribolla, P. E. and De Bianchi, A. G. (1995). Processing of procathepsin from Musca domestica eggs. Insect Biochem. Mol. Biol. 25, 1011-1017.
83. Rinehart, J. P., Robich, R. M. and Denlinger, D. L. (2006). Enhanced cold and dessication tolerance in diapausing adults of Culex pipiens, and a role for Hsp70 in response to cold shock but not as a component of the diapause program. J. Med. Entomol. A3, 713-722.
84. Robich, R. M., Rinehart, J. P., Kitchen, L. J. and Denlinger, D. L. (2007). Diapause-specific gene expression in the northern house mosquito, Culex pipiens L., identified by suppressive subtractive hybridization. J. Insect Physiol. 53, 235-245.
85. Shimada, K. and Riihima, A. (1990). Cold-induced freezing tolerance in diapausing and non-diapausing larvae of Chymomyza costa (Diptera: Drosophilidae) with accumulation of tehalose and proline. Cryo Letters 11, 243-250.
86. Sieglaff, D. H., Duncan, K. A., Brown, M. R. (2005). Expression of genes encoding proteins involved in ecdysteroidogenesis in the female mosquito, Aedes aegypti. Insect Biochem. Mol. Biol. 35, 471-490.
87. Sommer, A., Fischer, P., Krause, K., Boettcher, K., Brophys, P. M. and Walter, R. D. (2001). A stress-reponsive glyoxalase I from the parasitic nematode Onchocerca volvulus. Biochem. J. 353, 445-452.
88. Sonoda, S., Fukumoto, K., Izumi, Y., Yoshida, H. and Tsumuk, H. (2006). Cloning of heat shock protein genes (hsp90 and hsc70) and their expression during larval diapause and cold tolerance acquisition in the rice stem borer, Chilo suppressalis Walker. Arch. Insect Biochem. Physiol. 63,36-47.
89. Storey, J. D. and Tibshirani, R. (2003). Statistical significance for genomewide studies. Proc. Natl. Acad. Sci. USA 100, 9440-9445.
90. Storey, K. B. and Storey, J. M. (2007). Tribute to P. L. Lutz: putting life on 'pause' - molecular regulation of hypometabolism. J. Exp. Biol. 210, 1700-1714.
91. Suzuki, M. G., Terada, T., Kobayashi, M. and Shimada, T. (1999). Diapause-associated transcription of BmEts, a gene encoding an ETS transcription factor homolog in Bombyx mori. Insect Biochem. Mol. Biol. 29, 339-347.
92. Tachibana, S. I., Numata, H. and Goto, S. G. (2005). Gene expression of heat-shock proteins (Hsp23, Hsp70 and Hsp90) during and after larval diapause in the blow fly Lucilia sericata. J. Insect Physiol, 51, 641-647.
93. Tanaka, K., Ichinari, S., Iwanami, K., Yoshimatsu, S. and Suzuki, T. (2007). Arginine kinase from the beetle Cissites cephalotes (Olivier): molecular cloning, phylogenetic analysis and enzymatic properties. Insect Biochem. Moi. Biol. 37, 338-345.
94. Tauber, M. J. and Tauber, C. A. (1976). Insect seasonality: diapause maintenance, termination, and post-diapause development. Annu. Rev. Entomol. 21, 81-107.
95. Tawfik, A. I., Tanaka, Y. and Tanaka, S. (2002). Possible involvement of ecdysteroids in embryonic diapause of Locusta migratoria. J. Insect Physiol. 48, 743-749.
96. Tiku, P. E. , Gracey, A. Y., Macartney, A. I., Beynon, R. J. and Cossins, A. R. (1996). Cold-induced expression of delta 9-desaturase in carp by transcriptional and posttranslational mechanisms. Science 271, 815-818.
97. Visscher, S. N. (1976). The embryonic diapause of Aulocara elliotti (Orthoptera, Acrididiae). Cell. Tissue Res. 174, 433-452.
98. Wardhaugh, K. G. (2006). The effects of temperature and moisture on the inception of diapause in eggs of the Australian plague locust, Chortoicetes terminifera Walker (Orthoptera: Acrididae). Austral Ecol. 5, 187-191.
99. Wheatley, S., Kulkarni, S. and Karess, R. (1995). Drosophila nonmuscular myosin II is required for rapid cytoplasmic transport during oogenesis and for axial nuclear migration in early embryos. Development 121, 1937-1946.
100. Whiting, P. and Dinan, L. (1988). The occurrence of apolar ecdysteroid conjugates in newly-laid eggs of the house cricket, Acheta domesticus. J. Insect Physiol. 34, 625-631.
101. Xu, W. H., Sato, Y., Iked, A. M. and Yamashita, O. (1995). Molecular characterization of the gene encoding the precursor protein of diapause hormone and pheromone bioynthesis activating neuropeptide (DH-PBAN) of the silkworm, Bombyx mori, and its distribution in some insects. Biochim. Biophys. Acta 1261, 83-89.
102. Yamashita, O. and Hasegawa, K. (1985). Embryonic diapause. In Comprehensive Insect Physiology, Biochemistry and Pharmacology, vol 1. (ed. G. A. Kerkut and L. I. Gilbert), pp. 407-434. Oxford: Pergemon Press.
103. Young, P. E., Richman, A. M., Ketchum, A. S. and Kiehart, D. P. (1993). Morphogenesis in Drosophila requires non-muscle myosin heavy chain function. Genes Dev. 7, 29-41.
104. Zhao, X. F., An, X. M., Wang, J. X., Dong, D. J., Du, X. J., Sueda, S. and Kondo, H. (2005). Expression of the Helicoverpa cathepsin B-like proteinase during embryonic development. Arch. Insect Biochem. Physiol. 58, 39-46.
105. Zheng, N., Fraenkel, E., Pabo, C. O. and Pavletch, N. P. (1999). Structural basis of DNA recognition by the heterodimeric cell cycle transcription factor E2F-DP. Genes Dev. 13, 666-647.