Cite this paper:
LIU Jun, XU Fei, JI Peng, LI Li, ZHANG Guofan. Involvement of clustered oyster Wnt genes in gut formation[J]. Journal of Oceanology and Limnology, 2018, 36(5): 1746-1752

Involvement of clustered oyster Wnt genes in gut formation

LIU Jun1,2,4, XU Fei1,3,4, JI Peng1,2,4, LI Li1,4,5, ZHANG Guofan1,3,4
1 Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China;
2 University of Chinese Academy of Sciences, Beijing 100049, China;
3 Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266000, China;
4 National & Local Joint Engineering Laboratory of Ecological Mariculture, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China;
5 Laboratory for Marine Fisheries and Aquaculture, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266000, China
Abstract:
Genes encoding Wnt ligands play important roles in organ development. The Wnt10-Wnt6-Wnt1-Wnt9 cluster widely presents in many metazoan genomes, indicating the importance of gene arrangement. Hypothesis has been proposed that they may be coordinately regulated. However, few expression correlations were identified in model animals. We analyzed the tissue expression pattern of clustered oyster Wnt10, Wnt6, Wnt1, and Wnt9a genes in this study. The results indicated the highest expression level in adult gut system of these clustered Wnt genes, except for Wnt6, which had highest expression in mantle. Further whole-mount immunofluorescence assay indicated that Wnt6 protein was restricted to gut region in oyster larvae. These results suggest the possible important role of the Wnt10-Wnt6-Wnt1-Wnt9 cluster in oyster gut formation.
Key words:    gene cluster|tissue distribution|digestive gland|immunofluorescence|Crassostrea gigas   
Received: 2017-04-28   Revised:
Tools
PDF (629 KB) Free
Print this page
Add to favorites
Email this article to others
Authors
Articles by LIU Jun
Articles by XU Fei
Articles by JI Peng
Articles by LI Li
Articles by ZHANG Guofan
References:
Adamska M, Degnan S M, Green K M, Adamski M, Craigie A, Larroux C, Degnan B M, Fraser J. 2007. Wnt and TGF-β expression in the sponge Amphimedon queenslandica and the origin of metazoan embryonic patterning. PLoS One, 2(10):e1031, https://doi.org/10.1371/journal.pone.0001031.
Adamska M, Larroux C, Adamski M, Green K, Lovas E, Koop D, Richards G S, Zwafink C, Degnan B M. 2010. Structure and expression of conserved Wnt pathway components in the demosponge Amphimedon queenslandica. Evolution & Development, 12(5):494-518, https://doi.org/10.1111/j.1525-142X.2010.00435.x.
Bao Y B, Xu F, Shimeld S M. 2017. Phylogenetics of lophotrochozoan bHLH genes and the evolution of lineage-specific gene duplicates. Genome Biology and Evolution, 9(4):869-886, https://doi.org/10.1093/gbe/evx047.
Bodine P V N. 2008. Wnt signaling control of bone cell apoptosis. Cell Research, 18(2):248-253, https://doi.org/10.1038/cr.2008.13.
Bolognesi R, Beermann A, Farzana L, Wittkopp N, Lutz R, Balavoine G, Brown S J, Schröder R. 2008. Tribolium Wnts:evidence for a larger repertoire in insects with overlapping expression patterns that suggest multiple redundant functions in embryogenesis. Development Genes and Evolution, 218(3-4):193-202, https://doi.org/10.1007/s00427-007-0170-3.
Brooke N M, Garcia-Fernàndez J, Holland P W H. 1998. The ParaHox gene cluster is an evolutionary sister of the Hox gene cluster. Nature, 392(6679):920-922, https://doi.org/10.1038/31933.
Cho S J, Vallès Y, Giani V C, Seaver E C, Weisblat D A. 2010. Evolutionary dynamics of the wnt gene family:a lophotrochozoan perspective. Molecular Biology and Evolution, 27(7):1 645-1 658, https://doi.org/10.1093/molbev/msq052.
Cohen E D, Mariol M C, Wallace R M H, Weyers J, Kamberov Y G, Pradel J, Wilder E L. 2002. DWnt4 regulates cell movement and focal adhesion kinase during Drosophila ovarian morphogenesis. Developmental Cell, 2(4):437-448, https://doi.org/10.1016/S1534-5807(02)00142-9.
Cordero J B, Ridgway R A, Valeri N, Nixon C, Frame M C, Muller W J, Vidal M, Sansom O J. 2014. c-Src drives intestinal regeneration and transformation. EMBO Journal, 33(13):1 474-1 491, https://doi.org/10.1002/embj.201387454.
Croce J, Range R, Wu S Y, Miranda E, Lhomond G, Peng J C F, Lepage T, McClay D R. 2011. Wnt6 activates endoderm in the sea urchin gene regulatory network. Development, 138(15):3 297-3 306, https://doi.org/10.1242/dev.058792.
Doumpas N, Jékely G, Teleman A A. 2013. Wnt6 is required for maxillary palp formation in Drosophila. BMC Biology, 11:104, https://doi.org/10.1186/1741-7007-11-104.
Du Y S, Zhang L L, Xu F, Huang B Y, Zhang G F, Li L. 2013. Validation of housekeeping genes as internal controls for studying gene expression during Pacific oyster(Crassostrea gigas) development by quantitative realtime PCR. Fish & Shellfish Immunology, 34(3):939-945, https://doi.org/10.1016/j.fsi.2012.12.007.
Dyachuk V, Odintsova N. 2009. Development of the larval muscle system in the mussel Mytilus trossulus (Mollusca, Bivalvia). Development, Growth & Differentiation, 51(2):69-79, https://doi.org/10.1111/j.1440-169X.2008.01081.x.
Eisenmann D M. 2005. Wnt signaling (June 25, 2005), WormBook, ed. The C. elegans Research Community, WormBook. http://www.wormbook.org.
Gessert S, Kuhl M. 2010. The multiple phases and faces of wnt signaling during cardiac differentiation and development. Circulation Research, 107(2):186-199, https://doi.org/10.1161/CIRCRESAHA.110.221531.
Graba Y, Gieseler K, Aragnol D, Laurenti P, Mariol M C, Berenger H, Sagnier T, Pradel J. 1995. DWnt-4, a novel Drosophila Wnt gene acts downstream of homeotic complex genes in the visceral mesoderm. Development, 121(1):209-218.
Gregorieff A, Pinto D, Begthel H, Destree O, Kielman M, Clevers H. 2005. Expression pattern of Wnt signaling components in the adult intestine. Gastroenterology, 129(2):626-638, https://doi.org/10.1016/j.gastro.2005.06.007.
Hartin S N, Hudson M L, Yingling C, Ackley B D. 2015. A synthetic lethal screen identifies a role for Lin-44/Wnt in C. elegans embryogenesis. PLoS One, 10(5):e0121397, https://doi.org/10.1371/journal.pone.0121397.
Hayden L, Schlosser G, Arthur W. 2015. Functional analysis of centipede development supports roles for Wnt genes in posterior development and segment generation. Evolution & Development, 17(1):49-62, https://doi.org/10.1111/ede.12112.
Heller R S, Dichmann D S, Jensen J, Miller C, Wong G, Madsen O D, Serup P. 2002. Expression patterns of Wnts, Frizzleds, sFRPs, and misexpression in transgenic mice suggesting a role for Wnts in pancreas and foregut pattern formation. Developmental Dynamics, 225(3):260-270, https://doi.org/10.1002/dvdy.10157.
Hobmayer B, Rentzsch F, Kuhn K, Happel C M, von Laue C C, Snyder P, Rothbächer U, Holstein T W. 2000. WNT signalling molecules act in axis formation in the diploblastic metazoan Hydra. Nature, 407(6801):186-189, https://doi.org/10.1038/35025063.
Holstein T W. 2012. The evolution of the Wnt pathway. Cold Spring Harbor Perspectives in Biology, 4(7):a007922, https://doi.org/10.1101/cshperspect.a007922.
Huang W, Xu F, Qu T, Zhang R, Li L, Que H, Zhang G F. 2015. Identification of thyroid hormones and functional characterization of thyroid hormone receptor in the pacific oyster Crassostrea gigas provide insight into evolution of the thyroid hormone system. PLoS One, 10(12):e0144991, https://doi.org/10.1371/journal.pone.0144991.
Inaki M, Yoshikawa S, Thomas J B, Aburatani H, Nose A. 2007. Wnt4 is a local repulsive cue that determines synaptic target specificity. Current Biology, 17(18):1 574-1 579, https://doi.org/10.1016/j.cub.2007.08.013.
Janson K, Cohen E D, Wilder E L. 2001. Expression of DWnt6, DWnt10, and DFz4 during Drosophila development.Mechanisms of Development, 103(1-2):117-120, https://doi.org/10.1016/S0925-4773(01)00323-9.
Janssen R, Le Gouar M, Pechmann M, Poulin F, Bolognesi R, Schwager E E, Hopfen C, Colbourne J K, Budd G E, Brown S J, Prpic N M, Kosiol C, Vervoort M, Damen W G M, Balavoine G, McGregor A P. 2010. Conservation, loss, and redeployment of Wnt ligands in protostomes:implications for understanding the evolution of segment formation. BMC Evolutionary Biology, 10:374, https://doi.org/10.1186/1471-2148-10-374.
Kusserow A, Pang K, Sturm C, Hrouda M, Lentfer J, Schmidt H A, Technau U, von Haeseler A, Hobmayer B, Martindale M Q, Holstein T W. 2005. Unexpected complexity of the Wnt gene family in a sea anemone. Nature, 433(7022):156-160, https://doi.org/10.1038/nature03158.
Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-△△CT method. Methods, 25(4):402-408, https://doi.org/10.1006/meth.2001.1262.
Logan C Y, Nusse R. 2004. The Wnt signaling pathway in development and disease. Annual Review of Cell and Developmental Biology, 20:781-810, https://doi.org/10.1146/annurev.cellbio.20.010403.113126.
Miller J R. 2002. The Wnts. Genome Biol., 3(1):reviews3001.
Murat S, Hopfen C, McGregor A P. 2010. The function and evolution of Wnt genes in arthropods. Arthropod Structure & Development, 39(6):446-452, https://doi.org/10.1016/j.asd.2010.05.007.
Nelson W J, Nusse R. 2004. Convergence of Wnt, β-catenin, and cadherin pathways. Science, 303(5663):1 483-1 487, https://doi.org/10.1126/science.1094291.
Nusse R, Varmus H E. 1992. Wnt genes. Cell, 69(7):1 073-1 087, https://doi.org/10.1016/0092-8674(92)90630-U.
Nusse R. 2001. An ancient cluster of Wnt paralogues. Trends in Genetics, 17(8):443.
Nusse R. 2008. Wnt signaling and stem cell control. Cell Research, 18(5):523-527, https://doi.org/10.1038/cr.2008.47.
Qu T, Huang B Y, Zhang L L, Li L, Xu F, Huang W, Li C Y, Du Y S, Zhang G F, LeBlanc A C. 2014. Identification and functional characterization of two executioner caspases in Crassostrea gigas. PLoS One, 9(2):e89040, https://doi.org/10.1371/journal.pone.0089040.
Ryan J F, Baxevanis A D. 2007. Hox, Wnt, and the evolution of the primary body axis:insights from the early-divergent phyla. Biology Direct, 2:37, https://doi.org/10.1186/1745-6150-2-37.
Saito-Diaz K, Chen T W, Wang X X, Thorne C A, Wallace H A, Page-McCaw A, Lee E. 2013. The way Wnt works:components and mechanism. Growth Factors, 31(1):1-31, https://doi.org/10.3109/08977194.2012.752737.
Shimizu T, Bae Y K, Muraoka O, Hibi M. 2005. Interaction of Wnt and caudal-related genes in zebrafish posterior body formation. Developmental Biology, 279(1):125-141, https://doi.org/10.1016/j.ydbio.2004.12.007.
Sun L N, Yang H S, Chen M Y, Xu D X. 2013. Cloning and expression analysis of Wnt6 and Hox6 during intestinal regeneration in the sea cucumber Apostichopus japonicus. Genetics and Molecular Research, 12(4):5 321-5 334, https://doi.org/10.4238/2013.November.7.7.
Takeuchi T, Koyanagi R, Gyoja F, Kanda M, Hisata K, Fujie M, Goto H, Yamasaki S, Nagai K, Morino Y, Miyamoto H, Endo K, Endo H, Nagasawa H, Kinoshita S, Asakawa S, Watabe S, Satoh N, Kawashima T. 2016. Bivalvespecific gene expansion in the pearl oyster genome:implications of adaptation to a sessile lifestyle. Zoological Letters, 2:3, https://doi.org/10.1186/s40851-016-0039-2.
Thorpe C J, Schlesinger A, Carter J C, Bowerman B. 1997. Wnt signaling polarizes an early C. elegans blastomere to distinguish endoderm from mesoderm. Cell, 90(4):695-705, https://doi.org/10.1016/S0092-8674(00)80530-9.
Ulrich F, Concha M L, Heid P J, Voss E, Witzel S, Roehl H, Tada M, Wilson S W, Adams R J, Soll D R, Heisenberg C P. 2003. Slb/Wnt11 controls hypoblast cell migration and morphogenesis at the onset of zebrafish gastrulation. Development, 130(22):5 375-5 384, https://doi.org/10.1242/dev.00758.
Voronezhskaya E E, Nezlin L P, Odintsova N A, Plummer J T, Croll R P. 2008. Neuronal development in larval mussel Mytilus trossulus (Mollusca:Bivalvia). Zoomorphology, 127(2):97-110, https://doi.org/10.1007/s00435-007-0055-z.
Wodarz A, Nusse R. 1998. Mechanisms of Wnt signaling in development. Annual Review of Cell and Developmental Biology, 14:59-88, https://doi.org/10.1146/annurev.cellbio.14.1.59.
Yue F, Shi X W, Zhou Z, Wang L L, Wang M Q, Yang J L, Qiu L M, Song L S. 2013. The expression of immune-related genes during the ontogenesis of scallop Chlamys farreri and their response to bacterial challenge. Fish & Shellfish Immunology, 34(3):855-864, https://doi.org/10.1016/j.fsi.2012.12.023.
Zhai Z Z, Kondo S, Ha N, Boquete J P, Brunner M, Ueda R, Lemaitre B. 2015. Accumulation of differentiating intestinal stem cell progenies drives tumorigenesis.Nature Communications, 6:10 219, https://doi.org/10.1038/ncomms10219.
Zhang G F, Fang X D, Guo X M, Li L, Luo R B, Xu F, Yang P C, Zhang L L, Wang X T, Qi H G, Xiong Z Q, Que H Y, Xie Y L, Holland P W H, Paps J, Zhu Y B, Wu F C, Chen Y X, Wang J F, Peng C F, Meng J, Yang L, Liu J, Wen B, Zhang N, Huang Z Y, Zhu Q H, Feng Y, Mount A, Hedgecock D, Xu Z, Liu Y J, Domazet-Lošo T, Du Y S, Sun X Q, Zhang S D, Liu B H, Cheng P Z, Jiang X T, Li J, Fan D D, Wang W, Fu W J, Wang T, Wang B, Zhang J B, Peng Z Y, Li Y X, Li N, Wang J P, Chen M S, He Y, Tan F J, Song X R, Zheng Q M, Huang R L, Yang H L, Du X D, Chen L, Yang M, Gaffney P M, Wang S, Luo L H, She Z C, Ming Y, Huang W, Zhang S, Huang B Y, Zhang Y, Qu T, Ni P X, Miao G Y, Wang J J, Wang Q, Steinberg C E W, Wang H Y, Li N, Qian L M, Zhang G J, Li Y R, Yang H M, Liu X, Wang J, Yin Y, Wang J. 2012. The oyster genome reveals stress adaptation and complexity of shell formation. Nature, 490(7418):49-54, https://doi.org/10.1038/nature11413.
Copyright © Haiyang Xuebao