Transcriptomic response of Manduca sexta immune tissues to parasitization by the bracovirus associated wasp Cotesia congregata

Insect Biochemistry and Molecular Biology

Volumn 62, Issue , 2015, Pages 86-99

  Chevignon, Germain ^a   Cambier, Sébastien ^b   Da Silva, Corinne ^c   Poulain, Julie ^c   Drezen, Jean Michel ^a   Huguet, Elisabeth ^a   Moreau, Sébastien J M ^a  

^a UNIVERSITÉ DE TOURS   (France)

^b LUXEMBOURG INSTITUTE OF SCIENCE AND TECHNOLOGY   (Luxembourg)

^c CENTRE NATIONAL DE SÉQUENÇAGE   (France)

Author keywords

454 sequencing; Antimicrobial peptide; Innate immunity; Manduca sexta; Parasitoid; Polydnavirus; Transcriptome

Indexed keywords

BACTERIA (MICROORGANISMS); BRACOVIRUS; COTESIA CONGREGATA; COTESIA CONGREGATA BRACOVIRUS; MANDUCA SEXTA;

INSECT PROTEIN; TRANSCRIPTOME;

ANIMAL; BLOOD CELL; FAT BODY; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HOST PARASITE INTERACTION; IMMUNOLOGY; LARVA; MANDUCA; METABOLISM; PARASITOLOGY; PHYSIOLOGY; POLYDNAVIRIDAE; VIROLOGY; WASP;

ANIMALS; FAT BODY; FEMALE; GENE EXPRESSION REGULATION; HEMOCYTES; HOST-PARASITE INTERACTIONS; INSECT PROTEINS; LARVA; MANDUCA; POLYDNAVIRIDAE; TRANSCRIPTOME; WASPS;

EID: 84926376797     PISSN: 09651748     EISSN: 18790240     Source Type: Journal    
DOI: 10.1016/j.ibmb.2014.12.008     Document Type: Article

References (96)

1. Amaya K.E., Asgari S., Jung R., Hongskula M., Beckage N.E. Parasitization of Manduca sexta larvae by the parasitoid wasp Cotesia congregata induces an impaired host immune response. J.Insect. Physiol. 2005, 51:505-512.
2. Asgari S., Schmidt O., Theopold U. Apolydnavirus-encoded protein of an endoparasitoid wasp is an immune suppressor. J.Gen. Virol. 1997, 78:3061-3070.
3. Baeza Garcia A., Pierce R.J., Gourbal B., Werkmeister E., Colinet D., Reichhart J.-M., Dissous C., Coustau C. Involvement of the cytokine MIF in the snail host immune response to the parasite Schistosoma mansoni. PLoS Pathog. 2010, 6:e1001115.
4. Barat-Houari M., Hilliou F., Jousset F.-X., Sofer L., Deleury E., Rocher J., Ravallec M., Galibert L., Delobel P., Feyereisen R., Fournier P., Volkoff A.-N. Gene expression profiling of Spodoptera frugiperda hemocytes and fat body using cDNA microarray reveals polydnavirus-associated variations in lepidopteran host genes transcript levels. BMC Genomics 2006, 7:160.
5. Beck M., Strand M.R. RNA interference silences Microplitis demolitor bracovirus genes and implicates glc1.8 in disruption of adhesion in infected host cells. Virology 2003, 314:521-535.
6. Beck M.H., Strand M.R. Anovel polydnavirus protein inhibits the insect prophenoloxidase activation pathway. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:19267-19272.
7. Beckage N.E. Polydnaviruses as Endocrine Regulators. Parasitoid Viruses 2012, 163-168. Academic Press, San Diego. N.E. Beckage, J.-M. Drezen (Eds.).
8. Beckage N.E., Gelman D.B. Wasp parasitoid disruption of host development: implications for new biologically based strategies for insect control. Annu. Rev. Entomol. 2004, 49:299-330.
9. Beckage N.E., Kanost M.R. Effects of parasitism by the braconid wasp Cotesia congregata on host hemolymph proteins of the tobacco hornworm, Manduca sexta. Insect. Biochem.. Molec. Biol. 1993, 23:643-653.
10. Beckage N.E., Metclaf J.S., Nesbit D.J., Schleifer K.W., Zetlan S.R., de Buron I. Host hemolymph monophenoloxidase activity in parasitized Manduca sexta larvae and evidence for inhibition by wasp polydnavirus. Insect Biochem. 1990, 20:285-294.
11. Beckage N.E., Riddiford L.M. Effects of parasitism by Apanteles congregatus on the endocrine physiology of the tobacco hornworm Manduca sexta. Gen. Comp. Endocrinol. 1982, 47:308-322.
12. Benjamini Y., Hochberg Y. Controlling the False Discovery rate - a Practical and Powerful approach to multiple testing. J.Roy. Stat. Soc. B Met. 1995, 57:289-300.
13. Bézier A., Louis F., Jancek S., Periquet G., Thézé J., Gyapay G., Musset K., Lesobre J., Lenoble P., Dupuy C., Gundersen-Rindal D., Herniou E.A., Drezen J.-M. Functional endogenous viral elements in the genome of the parasitoid wasp Cotesia congregata: insights into the evolutionary dynamics of bracoviruses. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2013, 368:1626.
14. Bitra K., Suderman R.J., Strand M.R. Polydnavirus ank proteins bind NF-κB Homodimers and inhibit processing of Relish. PLoS Pathog. 2012, 8:e1002722.
15. Bortoluzzi S., d'Alessi F., Romualdi C., Danieli G.A. Differential expression of genes coding for ribosomal proteins in different human tissues. Bioinformatics 2001, 17:1152-1157.
16. Carver T., Harris S.R., Berriman M., Parkhill J., McQuillan J.A. Artemis: an integrated platform for visualization and analysis of high-throughput sequence-based experimental data. Bioinformatics 2012, 28:464-469.
17. Chevignon G., Thézé J., Cambier S., Poulain J., Da Silva C., Bézier A., Musset K., Moreau S.J.M., Drezen J.-M., Huguet E. Functional annotation of Cotesia congregata bracovirus: identification of the viral genes expressed in parasitized host immune tissues. J.Virol. 2014, 88:8795-8812.
18. David J.-P., Coissac E., Melodelima C., Poupardin R., Riaz M.A., Chandor-Proust A., Reynaud S. Transcriptome response to pollutants and insecticides in the dengue vector Aedes aegypti using next-generation sequencing technology. BMC Genomics 2010, 11:216.
19. Delaney J.R., Stöven S., Uvell H., Anderson K.V., Engström Y., Mlodzik M. Cooperative control of Drosophila immune responses by the JNK and NF-kappaB signaling pathways. EMBO J. 2006, 25:3068-3077.
20. Doucet D., Béliveau C., Dowling A., Simard J., Feng Q., Krell P.J., Cusson M. Prophenoloxidases 1 and 2 from the spruce budworm, Choristoneura fumiferana: molecular cloning and assessment of transcriptional regulation by a polydnavirus. Arch. Insect Biochem.. Physiol. 2008, 67:188-201.
21. Duchi S., Cavaliere V., Fagnocchi L., Grimaldi M.R., Falabella P., Graziani F., Gigliotti S., Pennacchio F., Gargiulo G. The impact on microtubule network of a bracovirus IκB-like protein. Cell. Mol. Life. Sci. 2010, 67:1699-1712.
22. Eleftherianos I., Xu M., Yadi H., Ffrench-Constant R.H., Reynolds S.E. Plasmatocyte-spreading peptide (PSP) plays a central role in insect cellular immune defenses against bacterial infection. J.Exp. Biol. 2009, 212:1840-1848.
23. Espagne E. Genome sequence of a Polydnavirus: insights into symbiotic virus evolution. Science 2004, 306:286-289.
24. Espagne E., Douris V., Lalmanach G., Provost B., Cattolico L., Lesobre J., Kurata S., Iatrou K., Drezen J.-M., Huguet E. Avirus essential for insect host-parasite interactions encodes cystatins. J.Virol. 2005, 79:9765-9776.
25. Etebari K., Asgari S. Conserved microRNA miR-8 blocks activation of the Toll pathway by upregulating Serpin 27 transcripts. RNA Biol. 2013, 10:1356-1364.
26. Etebari K., Palfreyman R.W., Schlipalius D., Nielsen L.K., Glatz R.V., Asgari S. Deep sequencing-based transcriptome analysis of Plutella xylostella larvae parasitized by Diadegma semiclausum. BMC Genomics 2011, 12:446.
27. Falabella P., Varricchio P., Provost B., Espagne E., Ferrarese R., Grimaldi A., de Eguileor M., Fimiani G., Ursini M.V., Malva C., Drezen J.-M., Pennacchio F. Characterization of the IkappaB-like gene family in polydnaviruses associated with wasps belonging to different Braconid subfamilies. J.Gen. Virol. 2007, 88:92-104.
28. Gueguen G., Kalamarz M.E., Ramroop J., Uribe J., Govind S. Polydnaviral ankyrin proteins aid parasitic wasp survival by coordinate and selective inhibition of hematopoietic and immune NF-kappa B signaling in insect hosts. PLoS Pathog. 2013, 9:e1003580.
29. Gunaratna R.T., Jiang H. Acomprehensive analysis of the Manduca sexta immunotranscriptome. Dev. Comp. Immunol. 2013, 39:388-398.
30. Gundersen-Rindal D., Dupuy C., Huguet E., Drezen J.-M. Parasitoid polydnaviruses: evolution, pathology and applications. Biocontrol Sci. Technol. 2013, 23:1-61.
31. Gupta V., Warner J.R. Ribosome-omics of the human ribosome. RNA 2014, 20:1004-1013.
32. Harwood S.H., McElfresh J.S., Nguyen A., Conlan C.A., Beckage N.E. Production of early expressed parasitism-specific proteins in alternate sphingid hosts of the braconid wasp Cotesia congregata. J.Invertebr. Pathol. 1998, 73:271-279.
33. Hepat R., Kim Y. Aviral factor, CpBV15α, interacts with a translation initiation factor, eIF2, to suppress host gene expression at a post-transcriptional level. J.Invertebr. Pathol. 2013, 114:34-41.
34. Herniou E.A., Huguet E., Theze J., Bézier A., Periquet G., Drezen J.-M. When parasitic wasps hijacked viruses: genomic and functional evolution of polydnaviruses. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2013, 368:20130051.
35. Hidayat P., Goodman W.G. Juvenile hormone and hemolymph juvenile hormone binding protein Titers and their interaction in the hemolymph of fourth Stadium Manduca sexta. Insect Biochem.. Molec. Biol. 1994, 24:709-715.
36. Jiang H. The biochemical basis of antimicrobial responses in Manduca sexta. Insect Sci. 2008, 15:53-66.
37. Jiang H., Ma C., Lu Z.-Q., Kanost M.R. Beta-1,3-glucan recognition protein-2 (betaGRP-2) from Manduca sexta; an acute-phase protein that binds beta-1,3-glucan and lipoteichoic acid to aggregate fungi and bacteria and stimulate prophenoloxidase activation. Insect. Biochem.. Molec. Biol. 2004, 34:89-100.
38. Jiang H., Vilcinskas A., Kanost M. Immunity in Lepidopteran insects. Advances in Experimental Medicine and Biology 2010, 181-204. K. Söderhäll (Ed.).
39. Kamimura M., Nakahara Y., Kanamori Y., Tsuzuki S., Hayakawa Y., Kiuchi M. Molecular cloning of silkworm paralytic peptide and its developmental regulation. Biochem.. Biophys. Res. Commun. 2001, 286:67-73.
40. Kamita S.G., Hammock B.D. Juvenile hormone esterase: biochemistry and structure. J.Pestic. Sci. 2010, 35:265-274.
41. Kanost M.R., Zepp M.K., Ladendorff N.E., Andersson L.A. Isolation and characterization of a hemocyte aggregation inhibitor from hemolymph of Manduca sexta larvae. Arch. Insect Biochem.. Physiol. 1994, 27:123-136.
42. Kim Y. Identification of host translation inhibitory factor of Campoletis sonorensis ichnovirus on the tobacco budworm, Heliothis virescens. Arch. Insect Biochem.. Physiol. 2005, 59:230-244.
43. Kondrashov N., Pusic A., Stumpf C.R., Shimizu K., Hsieh A.C., Xue S., Ishijima J., Shiroishi T., Barna M. Ribosome-mediated specificity in Hox mRNA translation and vertebrate tissue patterning. Cell 2011, 145:383-397.
44. Krisshnan N., Kodri D. Endocrine Control of Oxidative Stress in Insects 2012, 261-270. John Wiley & Sons, Inc. T. Farooqui, A.A. Farooqui (Eds.).
45. Lavine M., Beckage N.E. Temporal pattern of parasitism-induced immunosuppression in Manduca sexta larvae parasitized by Cotesia congregata. J.Insect. Physiol. 1996, 42:41-51.
46. Lavine M.D., Beckage N.E. Polydnaviruses: potent mediators of host insect immune dysfunction. Parasitol. Today (Regul. Ed.) 1995, 11:368-378.
47. Levin D.M., Breuer L.N., Zhuang S., Anderson S.A., Nardi J.B., Kanost M.R. Ahemocyte-specific integrin required for hemocytic encapsulation in the tobacco hornworm, Manduca sexta. Insect. Biochem.. Molec. Biol. 2005, 35:369-380.
48. Li W.-C., Riddiford L.M. The two duplicated insecticyanin genes, ins-a and ins-b are differentially expressed in the tobacco hornworm, Manduca sexta. Nucleic. Acids Res. 1994, 22:2945-2950.
49. Lillig C.H., Holmgren A. Thioredoxin and related molecules-from biology to health and disease. Antioxid. Redox Signal 2007, 9:25-47.
50. Ling E., Yu X.-Q. Hemocytes from the tobacco hornworm Manduca sexta have distinct functions in phagocytosis of foreign particles and self dead cells. Dev. Comp. Immunol. 2006, 30:301-309.
51. Ling E., Yu X.-Q. Cellular encapsulation and melanization are enhanced by immulectins, pattern recognition receptors from the tobacco hornworm Manduca sexta. Dev. Comp. Immunol. 2006, 30:289-299.
52. Lovallo N., Cox-Foster D.L. Alteration in FAD-glucose dehydrogenase activity and hemocyte behavior contribute to initial disruption of Manduca sexta immune response to Cotesia congregata parasitoids. J.Insect. Physiol. 1999, 45:1037-1048.
53. Lu Z., Beck M.H., Wang Y., Jiang H., Strand M.R. The viral protein Egf1.0 is a dual activity inhibitor of prophenoloxidase-activating proteinases 1 and 3 from Manduca sexta. J.Biol. Chem. 2008, 283:21325-21333.
54. Lu Z., Beck M.H., Strand M.R. Egf1.5 is a second phenoloxidase cascade inhibitor encoded by Microplitis demolitor bracovirus. Insect. Biochem.. Molec. Biol. 2010, 40:497-505.
55. Ma C., Kanost M.R. Abeta1,3-glucan recognition protein from an insect, Manduca sexta, agglutinates microorganisms and activates the phenoloxidase cascade. J.Biol. Chem. 2000, 275:7505-7514.
56. Magkrioti C., Iatrou K., Labropoulou V. Differential inhibition of BmRelish1-dependent transcription in lepidopteran cells by bracovirus ankyrin-repeat proteins. Insect. Biochem.. Molec. Biol. 2011, 41:993-1002.
57. Matsumoto Y., Oda Y., Uryu M., Hayakawa Y. Insect cytokine growth-blocking peptide triggers a termination system of cellular immunity by inducing its binding protein. J.Biol. Chem. 2003, 278:38579-38585.
58. Milne I., Stephen G., Bayer M., Cock P.J.A., Pritchard L., Cardle L., Shaw P.D., Marshall D. Using Tablet for visual exploration of second-generation sequencing data. Brief. Bioinforma. 2013, 14:193-202.
59. Moon A.E., Walker A.J., Goodbourn S. Regulation of transcription of the Aedes albopictus cecropin A1 gene: a role for p38 mitogen-activated protein kinase. Insect. Biochem.. Molec. Biol. 2011, 41:628-636.
60. Moreau S.J.M. "It stings a bit but it cleans well": Venoms of Hymenoptera and their antimicrobial potential. J.Insect. Physiol. 2013, 59:186-204.
61. Moreau S.J.M., Huguet E., Drezen J.-M. Polydnaviruses as tools to deliver waspvirulence factors to impair lepidopteran host immunity. Insect Infection and Immunity 2009, 137-158. Oxford Biology. J. Rolff, S.E. Reynolds (Eds.).
62. Mortazavi A., Williams B.A., Mccue K., Schaeffer L., Wold B. Mapping andquantifying mammalian transcriptomes by RNA-Seq. Nat. Meth. 2008, 5:621-628.
63. Nakahara Y., Kanamori Y., Kiuchi M., Kamimura M. Effects of silkworm paralytic peptide on invitro hematopoiesis and plasmatocyte spreading. Arch. Insect Biochem.. Physiol. 2003, 52:163-174.
64. Nardi J.B., Pilas B., Bee C.M., Zhuang S., Garsha K., Kanost M.R. Neuroglian-positive plasmatocytes of Manduca sexta and the initiation of hemocyte attachment to foreign surfaces. Dev. Comp. Immunol. 2006, 30:447-462.
65. Pennacchio F., Strand M.R. Evolution of developmental strategies in parasitic hymenoptera. Annu. Rev. Entomol. 2006, 51:233-258.
66. Provost B., Jouan V., Hilliou F., Delobel P., Bernardo P., Ravallec M., Cousserans F., Wajnberg E., Darboux I., Fournier P., Strand M.R., Volkoff A.-N. Lepidopteran transcriptome analysis following infection by phylogenetically unrelated polydnaviruses highlights differential and common responses. Insect. Biochem.. Molec. Biol. 2011, 41:582-591.
67. Provost B., Varricchio P., Arana E., Espagne E., Falabella P., Huguet E., La Scaleia R., Cattolico L., Poirié M., Malva C., Olszewski J.A., Pennacchio F., Drezen J.-M. Bracoviruses contain a large multigene family coding for protein tyrosine phosphatases. J.Virol. 2004, 78:13090-13103.
68. Ragan E.J., An C., Jiang H., Kanost M. Roles of haemolymph proteins in antimicrobial defences of Manduca sexta. Insect Infection and Immunity 2009, 34-48. Oxford Biology. J. Rolff, S.E. Reynolds (Eds.).
69. Riddiford L.M., Hice R.H. Developmental profiles of the mRNAs for Manduca arylphorin and two other storage proteins during the final larval instar of Manduca setxa. Insect Biochem. 1985, 15:489-502.
70. Ross D.R., Dunn P.E. Effect of parasitism by Cotesia congregata on the susceptibility of Manduca sexta larvae to bacterial infection. Dev. Comp. Immunol. 1989, 13:205-216.
71. Serbielle C., Moreau S., Veillard F., Voldoire E., Bézier A., Mannucci M.-A., Volkoff A.-N., Drezen J.-M., Lalmanach G., Huguet E. Identification of parasite-responsive cysteine proteases in Manduca sexta. Biol. Chem. 2009, 390:493-502.
72. Skinner W., Dennis P., Li J., MS R., Carney R. Isolation and identification of paralytic peptides from hemolymph of the lepidopteran insects Manduca sexta, Spodoptera exigua, and Heliothis virescens. J.Biol. Chem. 1991, 266:12873-12877.
73. Strand M.R., Clark K.D. Plasmatocyte spreading peptide induces spreading of plasmatocytes but represses spreading of granulocytes. Arch. Insect Biochem.. Physiol. 1999, 42:213-223.
74. Strand M.R., Hayakawa Y., Clark K. Plasmatocyte spreading peptide (PSP1) and growth blocking peptide (GBP) are multifunctional homologs. J.Insect. Physiol. 2000, 46:817-824.
75. Strand M.R. Polydnavirus gene expression profiling: what We know now. Parasitoid Viruses 2012, 139-147. Academic Press, San Diego. N.E. Beckage, J.-M. Drezen (Eds.).
76. Strand M.R. Polydnavirus gene products that interact with the host immune system. Parasitoid Viruses 2012, 149-161. Academic Press, San Diego. N.E. Beckage, J.-M. Drezen (Eds.).
77. Strand M.R., Noda T. Alteration in the haemocytes of Pseudoplusia includens after parasitism by Microplitis demolitor. J.Insect. Physiol. 1991, 37:839-850.
78. Suderman R.J., Pruijssers A.J., Strand M.R. Protein tyrosine phosphatase-H2 from a polydnavirus induces apoptosis of insect cells. J.Gen. Virol. 2008, 89:1411-1420.
79. Surakasi V.P., Nalini M., Kim Y. Host translational control of a polydnavirus, Cotesia plutellae bracovirus, by sequestering host eIF4A to prevent formation of a translation initiation complex. Insect. Mol. Biol. 2011, 20:609-618.
80. Suzuki R., Fujimoto Z., Shiotsuki T., Tsuchiya W., Momma M., Tase A., Miyazawa M., Yamazaki T. Structural mechanism of JH delivery in hemolymph by JHBP of silkworm, Bombyx mori. Sci. Rep. 2011, 1:133.
81. Tarazona S., García-Alcalde F., Dopazo J., Ferrer A., Conesa A. Differential expression in RNA-seq: a matter of depth. Genome Res. 2011, 21:2213-2223.
82. Thoetkiattikul H., Beck M., Strand M.R. Inhibitor kappa B-like proteins from a polydnavirus inhibit NF-kappa B activation and suppress the insect immune response. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:11426-11431.
83. Tian L., Guo E., Diao Y., Zhou S., Peng Q., Cao Y., Ling E., Li S. Genome-wide regulation of innate immunity by juvenile hormone and 20-hydroxyecdysone in the Bombyx fat body. BMC Genomics 2010, 11:549.
84. Wang Y., Jiang H., Kanost M. Biological activity of Manduca sexta paralytic and plasmatocyte spreading peptide and primary structure of its hemolymph precursor. Insect. Biochem.. Molec. Biol. 1999, 29:1075-1086.
85. Wu S.-F., Sun F.-D., Qi Y.-X., Yao Y., Fang Q., Huang J., Stanley D., Ye G.-Y. Parasitization by Cotesia chilonis influences gene expression in fatbody and hemocytes of Chilo suppressalis. PLoS One 2013, 8:e74309.
86. Xu X.-X., Zhong X., Yi H.-Y., Yu X.-Q. Manduca sexta gloverin binds microbial components and is active against bacteria and fungi. Dev. Comp. Immunol. 2012, 38:275-284.
87. Xue S., Barna M. Specialized ribosomes: a new frontier in gene regulation and organismal biology. Nat. Rev. Mol. Cell. Biol. 2012, 13:355-369.
88. Yang H.-J., Wang M.-X., Zhang P., Sabhat A., Malik F.A., Bhaskar R., Zhou F., Li X.-H., Hu J.-B., Sun C.-G., Niu Y.-S., Miao Y.-G. Cloning and characterization of the Bombyx mori ecdysone oxidase. Arch. Insect Biochem.. Physiol. 2011, 78:17-29.
89. Yu X.-Q., Kanost M.R. Binding of hemolin to bacterial lipopolysaccharide and lipoteichoic acid. Eur. J. Biochem. 2003, 269:1827-1834.
90. Yuan J.S., Reed A., Chen F., Stewart C.N. Statistical analysis of real-time PCR data. BMC Bioinforma. 2006, 7:85.
91. Zhong X., Xu X.-X., Yi H.-Y., Lin C., Yu X.-Q. AToll-Spatzle pathway in the tobacco hornworm, Manduca sexta. Insect. Biochem.. Molec. Biol. 2012, 42:514-524.
92. Zhu Y., Johnson T., Myers A., Kanost M. Identification by subtractive suppression hybridization of bacteria-induced genes expressed in Manduca sexta fat body. Insect. Biochem.. Molec. Biol. 2003, 33:541-559.
93. Zhang G., Lu Z.-Q., Jiang H., Asgari S. Negative regulation of prophenoloxidase (proPO) activation by a clip-domain serine proteinase homolog (SPH) from endoparasitoid venom. Insect. Biochem.. Molec. Biol. 2004, 34:477-483.
94. Zhuang S., Kelo L., Nardi J.B., Kanost M.R. Neuroglian on hemocyte surfaces is involved in homophilic and heterophilic interactions of the innate immune system of Manduca sexta. Dev. Comp. Immunol. 2007, 31:1159-1167.
95. Zhuang S., Kelo L., Nardi J.B., Kanost M.R. An integrin-tetraspanin interaction required for cellular innate immune responses of an insect, Manduca sexta. J.Biol. Chem. 2007, 282:22563-22572.
96. Zhang X., Zheng Y., Jagadeeswaran G., Ren R., Sunkar R., Jiang H. Identification and developmental profiling of conserved and novel microRNAs in Manduca sexta. Insect. Biochem.. Molec. Biol. 2012, 42:381-395.