The initial analysis of a serine proteinase gene (AccSp10) from Apis cerana cerana: possible involvement in pupal development, innate immunity and abiotic stress responses

Cell Stress and Chaperones - Tập 22 - Trang 867-877 - 2017
Lijun Gao1,2, Hongfang Wang3, Zhenguo Liu3, Shuchang Liu1, Guangdong Zhao1, Baohua Xu3, Xingqi Guo1
1State Key Laboratory of Crop Biology College of Life Sciences, Shandong Agricultural University, Taian, People’s Republic of China
2College of Life Sciences, Taishan Medical University, Taian, People’s Republic of China
3College of Animal Science and Technology, Shandong Agricultural University, Taian, People’s Republic of China

Tóm tắt

Serine proteinases play important roles in innate immunity and insect development. We isolated a serine proteinase gene, designated AccSp10, from the Chinese honeybees (Apis cerana cerana). RT-qPCR and a Western blot analysis at different pupal development stages indicated that AccSp10 might be involved in melanin formation in pupae and promote pupal development. In adult workers, the expression of AccSp10 was upregulated by treatments mimicking harmful environments such as the presence of Bacillus bombysepticus, different temperatures (4, 24 and 42 °C), HgCl2, H2O2 and paraquat; the exception was treatment with VC (vitamin C), which did not upregulate AccSp10 expression. Western blot confirmed the results. A disc diffusion assay indicated that recombinant AccSp10 accelerated E. coli cell death during stimulation with harmful substances (HgCl2, paraquat and cumene hydroperoxide). These findings suggest that AccSp10 may be involved in the pupal development of Chinese honeybees and protection against microorganisms and abiotic harms.

Tài liệu tham khảo

Aggarwal K, Silverman N (2008) Positive and negative regulation of the Drosophila immune response. BMB Rep 41:267–277 Ahola V, Koskinen P, Wong SC, Kvist J, Paulin L, Auvinen P, Saastamoinen M, Frilander MJ, Lehtonen R, Hanski I (2015) Temperature- and sex-related effects of serine protease alleles on larval development in the Glanville fritillary butterfly. J Evol Biol 28(12):2224–2235 Alaux C, Ducloz F, Crauser D, Le Conte Y (2010) Diet effects on honeybees immunocompetence. Biol Lett 6:562–565 An MI, Choi CY (2010) Activity of antioxidant enzymes and physiological responses in ark shell, Scapharca broughtonii, exposed to thermal and osmotic stress: effects on hemolymph and biochemical parameters. Comparative Biochemistry & Physiology Part B Biochemistry & Molecular Biology 155:34–42 An C, Ishibashi J, Ragan EJ, Jiang H, Kanost MR (2009) Functions of Manduca sexta hemolymph proteinases HP6 and HP8 in two innate immune pathway. J Biol Chem 284:19716–19726 An C, Budd A, Kanost MR, Michel K (2011) Characterization of a regulatory unit that controls melanization and affects longevity of mosquitoes. Cellular & Molecular Life Sciences Cmls 68:1929–1939 Andersen SO (1985) 2—Sclerotization and tanning of the cuticle. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology biochemistry and pharmacology, vol 3. Pergamon Press, Oxford, pp 59–74 Anderson KV, Bokla L, Nüssleinvolhard C (1985a) Establishment of dorsal-ventral polarity in the Drosophila embryo: the induction of polarity by the Toll gene product. Cell 42:791–798 Anderson KV, Jürgens G, Nüsslein-Volhard C (1985b) Establishment of dorsal-ventral polarity in the Drosophila embryo: genetic studies on the role of the Toll gene product. Cell 42:779–789 Belvin MP, Anderson KV (1996) A conserved signalling pathway: the Drosophila toll-dorsal pathway. Annal Review of Cell and Developmental Biology 12:393–416 Bitondi MMG, Mora IM, Simões ZLP, Figueiredo VLC (1998) The Apis mellifera, pupal melanization program is affected by treatment with a juvenile hormone analogue. J Insect Physiol 44:499–507 Bulet P, Hetru C, Dimarcq JL, Hoffmann D (1999) Antimicrobial peptides in insects; structure and function. Developmental & Comparative Immunology 23:329–344 Burmeister C, Luërsen K, Heinick A, Hussein A, Domagalski M, Walter RD, Liebau E (2008) Oxidative stress in Caenorhabditis elegans: protective effects of the Omega class glutathione transferase (GSTO-1). Faseb Jounal 22:343–354 Carter P, Wells JA (1988) Dissecting the catalytic triad of a serine protease. Nature 332:564–568 Etlik O, Tomur A, Tuncer M, Ridvanağaoğlu AY, Andaç O (1997) Protective effect of antioxidant vitamins on red blood cell lipoperoxidation induced by SO2 inhalation. Journal of Basic & Clinical Physiology & Pharmacology 8:31–43 Gabriella F, Ioannis E, Ffrench-Constant RH, István V (2011) A serine proteinase homologue, SPH-3, plays a central role in insect immunity. J Immunol 186:4828–4834 Goldshmit Y, Erlich S, Pinkas-Kramarski R (2001) Neuregulin rescues PC12-ErbB4 cells from cell death induced by H2O2. Regulation of reactive oxygen species levels by phosphatidylinositol 3-kinase. J Biol Chem 276:46379–46385 Gorman MJ, Wang Y, Jiang H, Kanost MR (2007) Manduca sexta hemolymph proteinase 21 activates prophenoloxidase-activating proteinase 3 in an insect innate immune response proteinase cascade. J Biol Chem 282:11742–11749 Greenspan RJ, Finn JA, Hall JC (1980) Acetylcholinesterase mutants in drosophila and their effects on the structure and function of the cental nervous system. J Comp Neurol 189:741–774 Gupta S, Wang Y, Jiang H (2005) Manduca sexta prophenoloxidase serine proteinase homologs (SPHs) simultaneously. Insect Biochem Mol Biol 35:241–248 Halliwell B, Gutterridge JMC (1989) Production against radical damage: systems with problems, second edn. Free Radical Biology and Medicine Clarendon Press, Oxford Hallman GJ, Denlinger DL (1998) Temperature sensitivity in insects and application in integrated pest management. Westview Press, Oxford, p 29 Hashimoto C, Hudson KL, Anderson KV (1988) The Toll gene of Drosophila, required for dorsal-ventral embryonic polarity, appears to encode a transmembrane protein. Cell 52:269–279 Hiruma K, Riddiford LM (1988) Granular phenoloxidase involved in cuticular melanization in the tobacco hornworm: regulation of its synthesis in the epidermis by juvenile hormone. Dev Biol 130:87–97 Hodkova M, Hodek I (2004) Photoperiod, diapause and cold-hardiness. European Journal of Entomology 101:445–458 Hughes AL (2012) Evolution of the betaGRP/GNBP/beta-1,3-glucanase family of insects. Immunogenetics 64:549–558 Iwanaga S, Kawabata S, Muta T (1998) New types of clotting factors and defense molecules found in horseshoe crab hemolymph: their structures and functions. J Biol Chem 123:1–15 Jaenicke R (1991) Protein stability and molecular adaptation to extreme conditions. Eur J Biochem 202:715–728 James MN, Sielecki AR (1986) Molecular structure of an aspartic proteinase zymogen, porcine pepsinogen, at 1.8 A resolution. Nature 319:33–38 Jiang H, Kanost MR (2000) The clip-domain family of serine proteinases in arthropods. Insect Biochem Mol Biol 30:95–105 Jiang H, Vilcinskas A, Kanost MR (2010) Immunity in lepidopteran insects. Adv Exp Med Biol 34:89–100 Kambris Z, Brun S, Jang IH, Nam HJ, Romeo Y, Takahashi K, Lee WJ, Ueda R, Lemaitre B (2006) Drosophila, immunity: a large-scale in vivo RNAi screen identifies five serine proteases required for Toll activation. Curr Biol 16:808–813 Kanost MR, Jiang H, Yu XQ (2004) Innate immune responses of a lepidopteran insect, Manduca sexta. Immunol Rev 198:97–105 Kim CH, Kim SJ, Kan H, Kwon HM, Roh KB, Jiang R, Yang Y, Park JW, Lee HH, Ha NC, Kang HJ, Nonaka M, Söderhäll K, Lee BL (2008) A three-step proteolytic cascade mediates the activation of the peptidoglycan-induced toll pathway in an insect. J Biol Chem 283:1799–7607 Koštál V, Vambera J, Bastl J (2004) On the nature of pre-freeze mortality in insects: water balance, ion homeostasis and energy charge in the adults of Pyrrhocoris apterus. Jounal of experimental biology 207:1509–1521 Koštál V, Renault D, Mehrabianová A, Bastl J (2007) Insect cold tolerance and repair of chill-injury at fluctuating thermal regimes: role of ion homeostasis. Comparative Biochemistry & Physiology Part A Molecular & Integrative Physiology 147:231–238 Krem MM, Di Cera E (2002) Evolution of enzyme cascades from embryonic development to blood coagulation. Trends Biochem Sci 27:67–74 Lavine MD, Strand MR (2001) Surface characteristics of foreign targets that elicit an encapsulation response by the moth Pseudoplusia includens. J Insect Physiol 47:965–974 Lehrer RI, Ganz T (1999) Antimicrobial peptides in mammalian and insect host defence. Curr Opin Immunol 11:23–27 Lemaitre B, Nicolas E, Michaut L, Reichhart JM, Hoffmann JA (1996) The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86:973–983 Li L, Liu X, Guo Y, Ma E (2005) Activity of the enzymes of the antioxidative system in cadmium-treated Oxya chinensis, (Orthoptera Acridoidae). Environmental Toxicology & Pharmacology 20:412–416 Ligoxygakis P, Pelte N, Hoffmann JA, Reichhart JM (2002) Activation of Drosophila Toll during fungal infection by a blood serine protease. Science 297:114–116 Mavrouli MD, Tsakas S, Theodorou GL, Lampropoulou M, Marmaras VJ (2005) Map kinases mediate phagocytosis and melanization via prophenoloxidase activation in medfly hemocytes. Biochimica Et Biophysica Acta-biomembranes 1774:145–156 Michel T, Reichhart JM, Hoffmann JA, Royet J (2001) Drosophila Toll is activated by Gram-positive bacteria through a circulating peptidoglycan recognition protein. Nature 414:756–759 Michelette ERDF, Soares AEE (1993) Characterization of preimaginal developmental stages in Africanized honey bee workers (Apis mellifera L). Apidologie 24:431–440 Ming M, Obata F, Kuranaga E, Miura M (2014) Persephone/Spatzle pathogen sensors mediate the activation of Toll receptor signalling in response to endogenous danger signals in apoptosis-deficient Drosophila. J Biol Chem 289:7558–7568 Muta T, Iwanaga S (1996) The role of hemolymph coagulation in innate immunity. Curr Opin Immunol 8:41–47 Polgár L (2005) The catalytic triad of serine peptidases. Cellular & Molecular Life Sciences Cmls 62:2161–2172 Rawlings ND, Barrett AJ (1993) Evolutionary families of peptidases. J Cell Biochem 290:205–218 Rembold H (1987) Caste specific modulation of juvenile hormone titers in Apis mellifera. Insect Biochemistry 17:1003–1006 Roh KB, Kim CH, Lee H, Kwon HM, Park JW, Ryu JH, Kurokawa K, Ha NC, Lee WJ, Lemaitre B, Söderhäll K, Lee BL (2009) Proteolytic cascade for the activation of the insect toll pathway induced by the fungal cell wall component. J Biol Chem 284:19474–19481 Ross J, Jiang H, Kanost MR, Wang Y (2003) Serine proteases and their homologs in the Drosophila melanogaster genome: an initial analysis of sequence conservation and phylogenetic relationships. Gene 304:117–131 Scharlaken B, de Graaf DC, Goossens K, Brunain M, Peelman LJ, Jacobs FJ (2008) Reference gene selection for insect expression studies using quantitative real-time PCR: the honeybees, Apis mellifera, head after a bacterial challenge. J Insect Sci 8:1–10 Tang H, Kambris Z, Lemaitre B, Hashimoto C (2006) Two proteases defining a melanization cascade in the immune system of Drosophila. J Biol Chem 281:28097–28104 Trapasso LM, Simpson RM (1998) Positive and negative regulation of Easter, a member of the serine protease family hat controls dorsal-ventral patterning in the Drosophila embryo. Development 125:1261–1267 Veillard F, Troxler L, Reichhart JM (2015) Drosophila melanogaster clip-domain serine proteases: structure, function and regulation. Biochimie 122:255–269 Vu TK, Liu RW, Haaksma CJ, Tomasek JJ, Howard EW (1997) Identification and cloning of the membrane-associated serine protease, hepsin, from mouse preimplantation embryos. J Biol Chem 272:31315–31320 Walter MF, Biessmann H, Petersen NS (1990) Heat shock causes the collapse of the intermediate filament cytoskeleton in Drosophila, embryos. Dev Genet 11:270–279 Wang Y, Jiang H (2007) Reconstitution of a branch of the Manduca sexta prophenoloxidase activation cascade in vitro: snake-like hemolymph proteinase 21 (HP21) cleaved by HP14 activates prophenoloxidase-activating proteinase-2 precursor. Insect Biochem Mol Biol 37:1015–1025 Yang XQ, Zhang YL, Wang XQ, Dong H, Gao P, Jia LY (2016) Characterization of multiple heat-shock protein transcripts from Cydia pomonella: their response to extreme temperature and insecticide exposure. J Agric Food Chem 64:4288–4298 Yao P, Lu W, Meng F, Wang X, Xu B, Guo X (2013) Molecular cloning, expression and oxidative stress response of a mitochondrial thioredoxin peroxidase gene (Acctpx-3) from Apis cerana cerana. J Insect Physiol 59:273–282 Yoder JA, Denlinger DL (1991) Water balance in flesh fly pupae and water vapor absorption associated with diapause. J Exp Biol 157:273–286 Yoshida H, Ashida M (1986) Microbial activation of two serine enzymes and prophenoloxidase in the plasma fraction of hemolymph of the silkworm, Bombyx mori. Insect Biochemistry 16:539–545 Zhou Y, Wang F, Liu F, Wang C, Yan Y, Guo X, Xu B (2016) Cloning and molecular identification of triosephosphate isomerase gene from Apis cerana cerana and its role in response to various stresses. Apidologie 1:1–13 Zou Z, Lopez DL, Kanost MR, Evans JD, Jiang H (2006) Comparative analysis of serine protease-related genes in the honeybees genome: possible involvement in embryonic development and innate immunity. Insect Mol Biol 15:603–614