Molecular cloning and functional study of calreticulin from a lepidopteran pest, Pieris rapae

Developmental and Comparative Immunology

Volumn 38, Issue 1, 2012, Pages 55-65

  Wang, Lei ^a   Fang, Qi ^a   Zhu, Jiaying ^a,b   Wang, Fei ^a   Rean Akhtar, Zunnu ^a   Ye, Gongyin ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b SOUTHWEST FORESTRY UNIVERSITY   (China)

Author keywords

Calreticulin; Encapsulation; Innate immunity; Parasitization; Pieris rapae

Indexed keywords

CALRETICULIN; COMPLEMENTARY DNA; DOUBLE STRANDED RNA; MESSENGER RNA; RECOMBINANT CALRETICULIN; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIUM; BLOOD CELL; BUTTERFLY; CELL ENCAPSULATION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOPLASM; ENDOPLASMIC RETICULUM; EPIDERMIS; ESCHERICHIA COLI; FAT BODY; GENE EXPRESSION; MALPIGHIAN TUBULE; MICROCOCCUS LUTEUS; MIDGUT; MOLECULAR CLONING; NONHUMAN; PARASITOID; PIERIS RAPAE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PTEROMALUS PUPARUM; PUPA (LIFE CYCLE STAGE); RNA INTERFERENCE; WILD TYPE; YEAST;

ESCHERICHIA COLI; HEXAPODA; MICROCOCCUS LUTEUS; PIERIS RAPAE; PTEROMALUS PUPARUM;

EID: 84864332080     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2012.03.019     Document Type: Article

References (53)

1. Asgari S., Schmidt O. Is cell surface calreticulin involved in phagocytosis by insect hemocytes?. J. Insect Physiol. 2003, 49:545-550.
2. 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.
3. Cai J., Ye G.Y., Hu C. Parasitism of Pieris rapae (Lepidoptera : Pieridae) by a pupal endoparasitold, Pteromalus puparum (Hymenoptera : Pteromalidae): effects of parasitization and venom on host hemocytes. J. Insect Physiol. 2004, 50:315-322.
4. Choi J.Y., Whitten M.M., Cho M.Y., Lee K.Y., Kim M.S., Ratcliffe N.A., Lee B.L. Calreticulin enriched as an early-stage encapsulation protein in wax moth Galleria mellonella larvae. Dev. Comp. Immunol. 2002, 26:335-343.
5. Christensen A., Svensson K., Thelin L., Zhang W., Tintor N., Prins D., Funke N., Michalak M., Schulze-Lefert P., Saijo Y., Sommarin M., Widell S., Persson S. Higher plant calreticulins have acquired specialized functions in Arabidopsis. PLoS One 2010, 5:e11342.
6. Decca M.B., Carpio M.A., Bosc C., Galiano M.R., Job D., Andrieux A., Hallak M.E. Post-translational arginylation of calreticulin: a new isospecies of calreticulin component of stress granules. J. Biol. Chem. 2007, 282:8237-8245.
7. Fang Q., Wang L., Zhu J.Y., Li Y.M., Song Q.S., Stanley D.W., Akhtar Z.R., Ye G.Y. Expression of immune-response genes in lepidopteran host is suppressed by venom from an endoparasitoid, Pteromalus puparum. BMC Genomics 2010, 11:484.
8. Fang Q., Wang L., Zhu Y., Stanley D.W., Chen X., Hu C., Ye G. Pteromalus puparum venom impairs host cellular immune responses by decreasing expression of its scavenger receptor gene. Insect Biochem. Mol. Biol. 2011, 41:852-862.
9. Ferreira V., Molina M.C., Valck C., Rojas á., Aguilar L., Ramírez G., Schwaeble W., Ferreira A. Role of calreticulin from parasites in its interaction with vertebrate hosts. Mol. Immunol. 2004, 40:1279-1291.
10. Frasconi M., Chichiarelli S., Gaucci E., Mazzei F., Grillo C., Chinazzi A., Altieri F. Interaction of ERp57 with calreticulin: analysis of complex formation and effects of vancomycin. Biophys. Chem. 2012, 160:46-53.
11. Gamo S., Tomida J., Dodo K., Keyakidani D., Matakatsu H., Yamamoto D., Tanaka Y. Calreticulin mediates anesthetic sensitivity in Drosophila melanogaster. Anesthesiology 2003, 99:867-875.
12. Gardai S.J., McPhillips K.A., Frasch S.C., Janssen W.J., Starefeldt A., Murphy-Ullrich J.E., Bratton D.L., Oldenborg P.-A., Michalak M., Henson P.M. Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte. Cell 2005, 123:321-334.
13. 2+-binding chaperone of the endoplasmic reticulum. Int. J. Biochem. Cell Biol. 2005, 37:260-266.
14. Gold L.I., Eggleton P., Sweetwyne M.T., Van Duyn L.B., Greives M.R., Naylor S.M., Michalak M., Murphy-Ullrich J.E. Calreticulin: non-endoplasmic reticulum functions in physiology and disease. FASEB J. 2010, 24:665-683.
15. Goo T.W., Park S., Jin B.R., Yun E.Y., Kim I., Nho S.K., Kang S.W., Kwon O.Y. Endoplasmic reticulum stress response of Bombyx mori calreticulin. Mol. Biol. Rep. 2005, 32:133-139.
16. Hu C. Life-history and occurrence of Pteromalus-puparum L in Hangzhou. Acta Entomol. Sin. 1984, 27:302-307.
17. Hu J., Zhao H., Yu X., Liu J., Wang P., Chen J., Xu Q., Zhang W. Integrin β1 subunit from Ostrinia furnacalis hemocytes: molecular characterization, expression, and effects on the spreading of plasmatocytes. J. Insect Physiol. 2010, 56:1846-1856.
18. Jia X.-Y., He L.-H., Jing R.-L., Li R.-Z. Calreticulin: conserved protein and diverse functions in plants. Physiol. Plant. 2009, 136:127-138.
19. Johnson S., Michalak M., Opas M., Eggleton P. The ins and outs of calreticulin: from the ER lumen to the extracellular space. Trends Cell Biol. 2001, 11:122-129.
20. Kanost M. Serine proteinase inhibitors in arthropod immunity. Dev. Comp. Immunol. 1999, 23:291-301.
21. Kuraishi T., Manaka J., Kono M., Ishii H., Yamamoto N., Koizumi K., Shiratsuchi A., Lee B.L., Higashida H., Nakanishi Y. Identification of calreticulin as a marker for phagocytosis of apoptotic cells in Drosophila. Exp. Cell Res. 2007, 313:500-510.
22. Kwon M.S., Park C.S., Choi K.-R., Park C.-S., Ahnn J., Kim J.I., Eom S.H., Kaufman S.J., Song W.K. Calreticulin couples calcium release and calcium influx in integrin-mediated calcium signaling. Mol. Biol. Cell 2000, 11:1433-1443.
23. Lavine M.D., Strand M.R. Insect hemocytes and their role in immunity. Insect Biochem. Mol. Biol. 2002, 32:1295-1309.
24. Levin D.M., Breuer L.N., Zhuang S., Anderson S.A., Nardi J.B., Kanost M.R. A hemocyte-specific integrin required for hemocytic encapsulation in the tobacco hornworm Manduca sexta. Insect Biochem. Mol. Biol. 2005, 35:369-380.
25. Ling E.J., 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.
26. Liu H., Peatman E., Wang W., Abernathy J., Liu S., Kucuktas H., Lu J., Xu D.-H., Klesius P., Waldbieser G., Liu Z. Molecular responses of calreticulin genes to iron overload and bacterial challenge in channel catfish (Ictalurus punctatus). Dev. Comp. Immunol. 2011, 35:267-272.
27. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2-delta delta CT Method. Methods 2001, 25:402-408.
28. Lowenberger C. Innate immune response of Aedes aegypti. Insect Biochem. Mol. Biol. 2001, 31:219-229.
29. Luana W., Li F., Wang B., Zhang X., Liu Y., Xiang J. Molecular characteristics and expression analysis of calreticulin in Chinese shrimp Fenneropenaeus chinensis. Biochem. Physiol. B: Biochem. Mol. Biol. 2007, 147:482-491.
30. Michalak M., Corbett E.F., Mesaeli N., Nakamura K., Opas M. Calreticulin: one protein, one gene, many functions. Biochem. J. 1999, 344:281-292.
31. Michalak M., Groenendyk J., Szabo E., Gold L.I., Opas M. Calreticulin, a multi-process calcium-buffering chaperone of the endoplasmic reticulum. Biochem. J. 2009, 417:651-666.
32. Molinari M., Eriksson K.K., Calanca V., Galli C., Cresswell P., Michalak M., Helenius A. Contrasting functions of calreticulin and calnexin in glycoprotein folding and ER quality control. Mol. Cell 2004, 13:125-135.
33. Persson S., Rosenquist M., Sommarin M. Identification of a novel calreticulin isoform (Crt2) in human and mouse. Gene 2002, 297:151-158.
34. Pocanschi C.L., Kozlov G., Brockmeier U., Brockmeier A., Williams D.B., Gehring K. Structural and functional relationships between the lectin and arm domains of calreticulin. J. Biol. Chem. 2011, 286:27266-27277.
35. Qiu Y., Xi J., Du L., Roje S., Poovaiah B.W. A dual regulatory role of Arabidopsis calreticulin-2 in plant innate immunity. Plant J. 2012, 69:489-500.
36. Ramírez G., Valck C., Ferreira V.P., López N., Ferreira A. Extracellular Trypanosoma cruzi calreticulin in the host-parasite interplay. Trends Parasitol. 2011, 27:115-122.
37. Šilerová M., Kauschke E., Procházková P., Josková R., Tučková L., Bilej M. Characterization, molecular cloning and localization of calreticulin in Eisenia fetida earthworms. Gene 2007, 397:169-177.
38. Somogyi E., Petersson U., Hultenby K., Wendel M. Calreticulin-an endoplasmic reticulum protein with calcium-binding activity is also found in the extracellular matrix. Matrix Biol. 2003, 22:179-191.
39. Stanley D., Miller J., Tunaz H. Eicosanoid actions in insect immunity. J. Innate Immun. 2009, 1:282-290.
40. Stoltzfus J.R., Horton W.J., Grotewiel M.S. Odor-guided behavior in Drosophila requires calreticulin. J. Comp. Physiol. A 2003, 189:471-483.
41. Strand M.R. The insect cellular immune response. Insect Sci. 2008, 15:1-14.
42. Stroschein-Stevenson S.L., Foley E., O'Farrell P.H., Johnson A.D. Identification of Drosophila gene products required for phagocytosis of Candida albicans. PLoS Biol. 2006, 4:87-99.
43. Tang Q.Y., Feng M.G. DPS Data Processing System: Experimental Design, Statistical Analysis, and Data Mining 2007, Science Press, Beijing, China.
44. Thelin L., Mutwil M., Sommarin M., Persson S. Diverging functions among calreticulin isoforms in higher plants. Plant Signal. Behav. 2011, 6:905-910.
45. Vass E., Nappi A.J. Fruit fly immunity. Bioscience 2001, 51:529-535.
46. Visudtiphole V., Watthanasurorot A., Klinbunga S., Menasveta P., Kirtikara K. Molecular characterization of calreticulin: a biomarker for temperature stress responses of the giant tiger shrimp Penaeus monodon. Aquaculture 2010, 308:S100-S108.
47. Vitale A. Calreticulins are not all the same. Proc. Natl. Acad. Sci. USA 2009, 106:13151-13152.
48. Wang W.A., Groenendyk J., Michalak M. Calreticulin signaling in health and disease. Int. J. Biochem. Cell Biol. 2012, 10.1016/j.biocel.2012.02.009.
49. Wijeyesakere S.J., Gafni A.A., Raghavan M. Calreticulin is a thermostable protein with distinct structural responses to different divalent cation environments. J. Biol. Chem. 2011, 286:8771-8785.
50. Wu M.L., Ye G.Y., Zhu J.Y., Chen X.X., Hu C. Isolation and characterization of an immunosuppressive protein from venom of the pupa-specific endoparasitoid Pteromalus puparum. J. Invertebr. Pathol. 2008, 99:186-191.
51. Yan Q., Murphy-Ullrich J.E., Song Y. Molecular and structural insight into the role of key residues of thrombospondin-1 and calreticulin in thrombospondin-1-calreticulin binding. Biochemistry 2011, 50:566-573.
52. Zhang Z., Ye G.Y., Cai J., Hu C. Comparative venom toxicity between Pteromalus puparum and Nasonia vitripennis (Hymenoptera: Pteromalidae) toward the hemocytes of their natural hosts, non-target insects and cultured insect cells. Toxicon 2005, 46:337-349.
53. Zhang G.M., Schmidt O., Asgari S. A calreticulin-like protein from endoparasitoid venom fluid is involved in host hemocyte inactivation. Dev. Comp. Immunol. 2006, 30:756-764.