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http://dx.doi.org/10.3347/kjp.2020.58.2.161

Changes in Protein Phosphorylation during Salivary Gland Degeneration in Haemaphysalis longicornis  

Xiao, Qi (Hebei Key Laboratory of Animal Physiology, Biochemistry and Molecular Biology, College of Life Sciences, Hebei Normal University)
Hu, Yuhong (Instrumental Analysis Center, Hebei Normal University)
Yang, Xiaohong (Department of Pathogenic Biology, College of Basic Medicine, Hebei Medical University)
Tang, Jianna (Hebei Key Laboratory of Animal Physiology, Biochemistry and Molecular Biology, College of Life Sciences, Hebei Normal University)
Wang, Xiaoshuang (Hebei Key Laboratory of Animal Physiology, Biochemistry and Molecular Biology, College of Life Sciences, Hebei Normal University)
Xue, Xiaomin (Hebei Key Laboratory of Animal Physiology, Biochemistry and Molecular Biology, College of Life Sciences, Hebei Normal University)
Li, Mengxue (Hebei Key Laboratory of Animal Physiology, Biochemistry and Molecular Biology, College of Life Sciences, Hebei Normal University)
Wang, Minjing (Hebei Key Laboratory of Animal Physiology, Biochemistry and Molecular Biology, College of Life Sciences, Hebei Normal University)
Zhao, Yinan (Hebei Key Laboratory of Animal Physiology, Biochemistry and Molecular Biology, College of Life Sciences, Hebei Normal University)
Liu, Jingze (Hebei Key Laboratory of Animal Physiology, Biochemistry and Molecular Biology, College of Life Sciences, Hebei Normal University)
Wang, Hui (Hebei Key Laboratory of Animal Physiology, Biochemistry and Molecular Biology, College of Life Sciences, Hebei Normal University)
Publication Information
Parasites, Hosts and Diseases / v.58, no.2, 2020 , pp. 161-171 More about this Journal
Abstract
The ticks feed large amount of blood from their hosts and transmit pathogens to the victims. The salivary gland plays an important role in the blood feeding. When the female ticks are near engorgement, the salivary gland gradually loses its functions and begins to rapidly degenerate. In this study, data-independent acquisition quantitative proteomics was used to study changes in the phosphorylation modification of proteins during salivary gland degeneration in Haemaphysalis longicornis. In this quantitative study, 400 phosphorylated proteins and 850 phosphorylation modification sites were identified. Trough RNA interference experiments, we found that among the proteins with changes in phosphorylation, apoptosis-promoting Hippo protein played a role in salivary gland degeneration.
Keywords
Tick; salivary gland; apoptosis; data-independent acquisition; RNA interference; Hippo;
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1 Yu X, Zhou Y, Cao J, Zhang H, Gong H, Zhou J. Caspase-1 participates in apoptosis of salivary glands in Rhipicephalus haemaphysaloides. Parasit Vectors 2017; 10: 225.   DOI
2 Wang H, Zhang X, Wang X, Zhang B, Wang M, Yang X, Han X, Wang R, Ren S, Hu Y, Liu J. Comprehensive analysis of the global protein changes that occur during salivary gland degeneration in female ixodid ticks Haemaphysalis longicornis. Front Physiol 2019; 9: 1943.   DOI
3 Hawkins LJ, Wang M, Zhang B, Xiao Q, Wang H, Storey KB. Glucose and urea metabolic enzymes are differentially phosphorylated during freezing, anoxia, and dehydration exposures in a freeze tolerant frog. Comp Biochem Physiol Part D Genomics Proteomics 2019; 30: 1-13.   DOI
4 Rigbolt KT, Vanselow JT, Blagoev B. GProX, a user-friendly platform for bioinformatics analysis and visualization of quantitative proteomics data. Mol Cell Proteomics 2011; 10: O110.007450.   DOI
5 Gong H, Umemiya R, Zhou J, Liao M, Zhang H, Jia H, Nishikawa Y, Xuan X, Fujisaki K. Blocking the secretion of saliva by silencing the HlYkt6, gene in the tick Haemaphysalis longicornis. Insect Biochem Mol Biol 2009; 39: 372-381.   DOI
6 Kocan KM, Zivkovic Z, Blouin EF, Naranjo V, Almazan C, Mitra R, de la Fuente J. Silencing of genes involved in Anaplasma marginale-tick interactions affects the pathogen developmental cycle in Dermacentor variabilis. BMC Dev Biol 2009; 9: 1-11.   DOI
7 Ren S, Zhang B, Xue X, Wang S, Zhao H, Zhang X, Wang M, Xiao Q, Wang H, Liu J. Salivary gland proteome analysis of developing adult female Haemaphysalis longicornis ticks: molecular motor and TCA cycle-related proteins play an important role throughout development. Parasit Vectors 2019; 12: 613.   DOI
8 Feng G, Zhu Z, Li WJ, Lin Q, Chai Y, Dong MQ, Ou G. Hippo kinases maintain polarity during directional cell migration in Caenorhabditis elegans. EMBO J 2017; 3: 334-345.
9 Dong Y, Du X, Ye J, Han M, Xu T, Zhuang Y, Tao W. A cell-intrinsic role for Mst1 in regulating thymocyte egress. J Immunol 2009; 183: 3865-3872.   DOI
10 Varelas X. The Hippo pathway effectors TAZ and YAP in development, homeostasis and disease. Development 2017; 141: 1614-1626.   DOI
11 Ura S, Masuyama N, Graves JD, Gotoh Y. MST1-JNK promotes apoptosis via caspase-dependent and independent pathways. Genes Cells 2001; 6: 519-530.   DOI
12 Niu YL, Li C, Zhang GY. Blocking Daxx trafficking attenuates neuronal cell death following ischemia/reperfusion in rat hippocampus CA1 region. Arch Biochem Biophys 2011; 515: 89-98.   DOI
13 Meng Z, Moroishi T, Guan KL. Mechanisms of Hippo pathway regulation. Gene Dev 2016; 30: 1-17.   DOI
14 Wu S, Huang J, Dong J, Pan D. Hippo encodes a Ste-20 family protein kinase that restricts cell proliferation and promotes apoptosis in conjunction with salvador and warts. Cell 2003; 114: 445-456.   DOI
15 Zheng Y, Wang W, Liu B, Deng H, Uster E, Pan D. Identification of Happyhour/MAP4K as alternative Hpo/Mst-like kinases in the Hippo kinase cascade. Dev Cell 2015; 34: 642-655.   DOI
16 Ecsedy JA, Michaelson JS, Leder P. Homeodomain-interacting protein kinase 1 modulates Daxx localization, phosphorylation, and transcriptional activity. Mol Cell Biol 2003; 23: 950-960.   DOI
17 Yang X, Khosravi-Far R, Chang HY, Baltimore D. Daxx, a novel Fas-binding protein that activates JNK and apoptosis. Cell 1997; 89: 1067-1076.   DOI
18 Fromental-Ramain C, Ramain P, Hamiche A. The Drosophila DAXX-like protein (DLP) cooperates with ASF1 for H3. 3 deposition and heterochromatin formation. Mol Cell Biol 2017; 37: e00597-16.
19 Miyata Y, Nishida E. CK2 controls multiple protein kinases by phosphorylating a kinase-targeting molecular chaperone, Cdc37. Mol Cell Biol 2004; 24: 4065-4074.   DOI
20 Lange BM, Rebollo E, Herold A, Gonzalez C. Cdc37 is essential for chromosome segregation and cytokinesis in higher eukaryotes. EMBO J 2002; 21; 5364-5374.   DOI
21 Fang X, Zhou J, Liu W, Duan X, Gala U, Sandoval H, Tong C. Dynamin regulates autophagy by modulating lysosomal function. J Genet Genomics 2016; 43: 77-86.   DOI
22 Hinshaw JE. Dynamin and its role in membrane fission. Annu Rev Cell Dev Bi 2000; 16: 483-519.   DOI
23 Eleniste PP, Huang S, Wayakanon K, Largura HW, Bruzzaniti A. Osteoblast differentiation and migration are regulated by dynamin GTPase activity. Int J Biochem Cell Biol 2014; 46: 9-18.   DOI
24 Praefcke GJ, McMahon HT. The dynamin superfamily: universal membrane tubulation and fission molecules? Nat Rev Mol Cell Biol 2004; 5: 133-147.   DOI
25 Yokoyama N, deBakker CD, Zappacosta F, Huddleston MJ, Annan RS, Ravichandran KS, Miller WT. Identification of tyrosine residues on ELMO1 that are phosphorylated by the Src-family kinase Hck. Biochemistry 2005; 44: 8841-8849.   DOI
26 Elliott MR, Zheng S, Park D, Woodson RI, Reardon MA, Juncadella IJ, Kinchen JM, Zhang J, Lysiak JJ, Ravichandran KS. Unexpected requirement for ELMO1 in clearance of apoptotic germ cells in vivo. Nature 2010; 467: 333-337.   DOI
27 Van Goethem E, Silva EA, Xiao H, Franc NC. The Drosophila TRPP cation channel, PKD2 and Dmel/Ced-12 act in genetically distinct pathways during apoptotic cell clearance. PLoS One 2012; 7: e31488.   DOI
28 Sun RX, Lai SJ, Yang Y, Li XL, Liu K, Yao HW, Zhou H, Li Y, Wang LP, Mu D, Yin WW, Fang LQ, Yu HJ, Cao WC. Mapping the distribution of tick-borne encephalitis in mainland China. Ticks Tick Borne Dis 2017; 8: 631-639.   DOI
29 Gondard M, Cabezas-Cruz A, Charles RA, Vayssier-Taussat M, Albina E, Moutailler S. Ticks and tick-borne pathogens of the caribbean: current understanding and future directions for more comprehensive surveillance. Front Cell Infect Microbiol 2017; 7: 490.   DOI
30 Narasimhan S, Schuijt TJ, Abraham NM, Rajeevan N, Coumou J, Graham M, Robson A, Wu MJ, Daffre S, Hovius JW, Fikrig E. Modulation of the tick gut milieu by a secreted tick protein favors Borrelia burgdorferi colonization. Nat Commun 2017; 8: 184.   DOI
31 Kaufman W. The influence of various factors on fluid secretion by in vitro salivary glands of ixodid ticks. J Exp Biol 1976; 64: 727-742.   DOI
32 Papa A, Tsergouli K, Tsioka K, Mirazimi A. Crimean-congo hemorrhagic fever: tick-host-virus interactions. Front Cell Infect Microbiol 2017; 7: 213.   DOI
33 Davies S, Abdullah S, Helps C, Tasker S, Newbury H, Wall R. Prevalence of ticks and tick-borne pathogens: Babesia and Borrelia species in ticks infesting cats of Great Britain. Vet Parasitol 2017; 244: 129-135.   DOI
34 Martins LA, Malossi CD, Galletti MFBM, Ribeiro JM, Fujita A, Esteves E, Costa FB, Labruna MB, Daffre S, Fogaca AC. The transcriptome of the salivary glands of Amblyomma aureolatum reveals the antimicrobial peptide microplusin as an important factor for the tick protection against Rickettsia rickettsii infection. Front Physiol 2019; 10: 529.
35 Hajdusek O, Sima R, Ayllon N, Jalovecka M, Perner J, de la Fuente J, Kopacek P. Interaction of the tick immune system with transmitted pathogens. Front Cell Infect Microbiol 2013: 3; 26.
36 Kotal J, Langhansova H, Lieskovska J, Andersen JF, Francischetti IM, Chavakis T, Kopecky J, Pedra JH, Kotsyfakis M, Chmelar J. Modulation of host immunity by tick saliva. J Proteomics 2015; 128: 58-68.   DOI
37 Ullah SA, Kaufman WR. Salivary gland degeneration and ovary development in the Rocky Mountain wood tick, Dermacentor andersoni Stiles (Acari: Ixodidae). II. Determination of the 'critical weight'. Ticks Tick-borne Dis 2014; 5: 516-522.   DOI
38 Harris RA, Kaufman WR. Hormonal control of salivary gland degeneration in the ixodid tick Amblyomma hebraeum. J Insect Physiol 1981; 27: 241-248.   DOI
39 Harris RA, Kaufman WR. Neural involvement in the control of salivary gland degeneration in the ixodid tick Amblyomma hebraeum. J Exp Biol 1984; 109: 281-290.   DOI
40 Tirloni L, Islam MS, Kim, TK, Diedrich JK, Yates JR 3rd, Pinto AF, Mulenga A, You MJ, Da Silva Vaz I Jr. Saliva from nymph and adult females of Haemaphysalis longicornis: a proteomic study. Parasites Vector 2015; 8: 338.   DOI
41 Harris RA, Kaufman WR. Ecdysteroids: possible candidates for the hormone which triggers salivary gland degeneration in the ixodid tick Amblyomma hebraeum. Experientia 1985; 41: 740-742.   DOI