Manipulating Galectin Expression in Zebrafish (Danio rerio).
Chiguang Feng, Mihai Nita-Lazar, Nuria González-Montalbán, Jingyu Wang, Justin Mancini, Sheng Wang, Chinnarajan Ravindran, Hafiz Ahmed, Gerardo R Vasta
Author Information
Chiguang Feng: Department of Microbiology and Immunology, Institute of Marine and Environmental Technology, University of Maryland Baltimore, Baltimore, MD, USA.
Mihai Nita-Lazar: Department of Microbiology and Immunology, Institute of Marine and Environmental Technology, University of Maryland Baltimore, Baltimore, MD, USA.
Nuria González-Montalbán: Department of Microbiology and Immunology, Institute of Marine and Environmental Technology, University of Maryland Baltimore, Baltimore, MD, USA.
Jingyu Wang: Department of Microbiology and Immunology, Institute of Marine and Environmental Technology, University of Maryland Baltimore, Baltimore, MD, USA.
Justin Mancini: Department of Microbiology and Immunology, Institute of Marine and Environmental Technology, University of Maryland Baltimore, Baltimore, MD, USA.
Sheng Wang: Department of Microbiology and Immunology, Institute of Marine and Environmental Technology, University of Maryland Baltimore, Baltimore, MD, USA.
Chinnarajan Ravindran: Department of Microbiology and Immunology, Institute of Marine and Environmental Technology, University of Maryland Baltimore, Baltimore, MD, USA.
Hafiz Ahmed: Department of Biochemistry, School of Medicine, Institute of Marine and Environmental Technology, University of Maryland Baltimore, Baltimore, MD, USA.
Gerardo R Vasta: Department of Microbiology and Immunology, Institute of Marine and Environmental Technology, University of Maryland Baltimore, Baltimore, MD, USA. gvasta@som.umaryland.edu.
Techniques for disrupting gene expression are invaluable tools for the analysis of the biological role of a gene product. Because of its genetic tractability and multiple advantages over conventional mammalian models, the zebrafish (Danio rerio) is recognized as a powerful system for gaining new insight into diverse aspects of human health and disease. Among the multiple mammalian gene families for which the zebrafish has shown promise as an invaluable model for functional studies, the galectins have attracted great interest due to their participation in early development, regulation of immune homeostasis, and recognition of microbial pathogens. Galectins are β-galactosyl-binding lectins with a characteristic sequence motif in their carbohydrate recognition domains (CRDs), that constitute an evolutionary conserved family ubiquitous in eukaryotic taxa. Galectins are emerging as key players in the modulation of many important pathological processes, which include acute and chronic inflammatory diseases, autoimmunity and cancer, thus making them potential molecular targets for innovative drug discovery. Here, we provide a review of the current methods available for the manipulation of gene expression in the zebrafish, with a focus on gene knockdown [morpholino (MO)-derived antisense oligonucleotides] and knockout (CRISPR-Cas) technologies.
Meeker ND, Trede NS (2008) Immunology and zebrafish: spawning new models of human disease. Dev Comp Immunol 32(7):745–757. https://doi.org/10.1016/j.dci.2007.11.011
[DOI: 10.1016/j.dci.2007.11.011]
Feitsma H, Cuppen E (2008) Zebrafish as a cancer model. Mol Cancer Res 6(5):685–694. https://doi.org/10.1158/1541-7786.MCR-07-2167
[DOI: 10.1158/1541-7786.MCR-07-2167]
Mahmood F, Mozere M, Zdebik AA, Stanescu HC, Tobin J, Beales PL, Kleta R, Bockenhauer D, Russell C (2013) Generation and validation of a zebrafish model of EAST (epilepsy, ataxia, sensorineural deafness and tubulopathy) syndrome. Dis Model Mech 6(3):652–660. https://doi.org/10.1242/dmm.009480
[DOI: 10.1242/dmm.009480]
Weyand AC, Shavit JA (2014) Zebrafish as a model system for the study of hemostasis and thrombosis. Curr Opin Hematol 21(5):418–422. https://doi.org/10.1097/MOH.0000000000000075
[DOI: 10.1097/MOH.0000000000000075]
Lohi O, Parikka M, Ramet M (2013) The zebrafish as a model for paediatric diseases. Acta Paediatr 102(2):104–110. https://doi.org/10.1111/j.1651-2227.2012.02835.x
[DOI: 10.1111/j.1651-2227.2012.02835.x]
Kanwal Z, Wiegertjes GF, Veneman WJ, Meijer AH, Spaink HP (2014) Comparative studies of toll-like receptor signalling using zebrafish. Dev Comp Immunol 46(1):35–52. https://doi.org/10.1016/j.dci.2014.02.003
[DOI: 10.1016/j.dci.2014.02.003]
Saralahti A, Ramet M (2015) Zebrafish and Streptococcal infections. Scand J Immunol 82(3):174–183. https://doi.org/10.1111/sji.12320
[DOI: 10.1111/sji.12320]
Streisinger G, Walker C, Dower N, Knauber D, Singer F (1981) Production of clones of homozygous diploid zebra fish (Brachydanio rerio). Nature 291(5813):293–296
[DOI: 10.1038/291293a0]
Driever W, Solnica-Krezel L, Schier AF, Neuhauss SC, Malicki J, Stemple DL, Stainier DY, Zwartkruis F, Abdelilah S, Rangini Z, Belak J, Boggs C (1996) A genetic screen for mutations affecting embryogenesis in zebrafish. Development 123:37–46
[DOI: 10.1242/dev.123.1.37]
Haffter P, Granato M, Brand M, Mullins MC, Hammerschmidt M, Kane DA, Odenthal J, van Eeden FJ, Jiang YJ, Heisenberg CP, Kelsh RN, Furutani-Seiki M, Vogelsang E, Beuchle D, Schach U, Fabian C, Nusslein-Volhard C (1996) The identification of genes with unique and essential functions in the development of the zebrafish, Danio rerio. Development 123:1–36
[DOI: 10.1242/dev.123.1.1]
Barbazuk WB, Korf I, Kadavi C, Heyen J, Tate S, Wun E, Bedell JA, McPherson JD, Johnson SL (2000) The syntenic relationship of the zebrafish and human genomes. Genome Res 10(9):1351–1358
[DOI: 10.1101/gr.144700]
Howe DG, Ramachandran S, Bradford YM, Fashena D, Toro S, Eagle A, Frazer K, Kalita P, Mani P, Martin R, Moxon ST, Paddock H, Pich C, Ruzicka L, Schaper K, Shao X, Singer A, Van Slyke CE, Westerfield M (2020) The Zebrafish information network: major gene page and home page updates. Nucleic Acids Res 49(D1):D1058–D1064. https://doi.org/10.1093/nar/gkaa1010
[DOI: 10.1093/nar/gkaa1010]
Vital C, Martins EP (2013) Socially-central zebrafish influence group behavior more than those on the social periphery. PLoS One 8(1):e55503. https://doi.org/10.1371/journal.pone.0055503
[DOI: 10.1371/journal.pone.0055503]
Manabe K, Dooling RJ, Takaku S (2013) Differential reinforcement of an approach response in zebrafish (Danio rerio). Behav Process 98:106–111. https://doi.org/10.1016/j.beproc.2013.05.013
[DOI: 10.1016/j.beproc.2013.05.013]
Fu CW, Horng JL, Tong SK, Cherng BW, Liao BK, Lin LY, Chou MY (2021) Exposure to silver impairs learning and social behaviors in adult zebrafish. J Hazard Mater 403:124031. https://doi.org/10.1016/j.jhazmat.2020.124031
[DOI: 10.1016/j.jhazmat.2020.124031]
Perathoner S, Cordero-Maldonado ML, Crawford AD (2016) Potential of zebrafish as a model for exploring the role of the amygdala in emotional memory and motivational behavior. J Neurosci Res 94(6):445–462. https://doi.org/10.1002/jnr.23712
[DOI: 10.1002/jnr.23712]
Gerlai R (2017) Zebrafish and relational memory: could a simple fish be useful for the analysis of biological mechanisms of complex vertebrate learning? Behav Process 141(Pt 2):242–250. https://doi.org/10.1016/j.beproc.2017.01.016
[DOI: 10.1016/j.beproc.2017.01.016]
Ahmed H, Du SJ, Vasta GR (2009) Knockdown of a galectin-1-like protein in zebrafish (Danio rerio) causes defects in skeletal muscle development. Glycoconj J 26(3):277–283. https://doi.org/10.1007/s10719-008-9178-9
[DOI: 10.1007/s10719-008-9178-9]
Ahmed H, Vasta GR (2008) Unlike mammalian GRIFIN, the zebrafish homologue (DrGRIFIN) represents a functional carbohydrate-binding galectin. Biochem Biophys Res Commun 371(3):350–355. https://doi.org/10.1016/j.bbrc.2008.04.078
[DOI: 10.1016/j.bbrc.2008.04.078]
Vasta GR, Ahmed H, Du S, Henrikson D (2004) Galectins in teleost fish: Zebrafish (Danio rerio) as a model species to address their biological roles in development and innate immunity. Glycoconj J 21(8–9):503–521. https://doi.org/10.1007/s10719-004-5541-7
[DOI: 10.1007/s10719-004-5541-7]
Ghosh A, Banerjee A, Amzel LM, Vasta GR, Bianchet MA (2019) Structure of the zebrafish galectin-1-L2 and model of its interaction with the infectious hematopoietic necrosis virus (IHNV) envelope glycoprotein. Glycobiology 29(5):419–430. https://doi.org/10.1093/glycob/cwz015
[DOI: 10.1093/glycob/cwz015]
Nita-Lazar M, Mancini J, Feng C, Gonzalez-Montalban N, Ravindran C, Jackson S, Heras-Sanchez Ade L, Giomarelli B, Ahmed H, Haslam SM, Wu G, Dell A, Ammayappan A, Vakharia VN, Vasta GR (2016) The zebrafish galectins Drgal1-L2 and Drgal3-L1 bind in vitro to the infectious hematopoietic necrosis virus (IHNV) glycoprotein and reduce viral adhesion to fish epithelial cells. Dev Comp Immunol 55:241–252. https://doi.org/10.1016/j.dci.2015.09.007
[DOI: 10.1016/j.dci.2015.09.007]
Taylor ME, Drickamer K (2003) Structure-function analysis of C-type animal lectins. Methods Enzymol 363:3–16. https://doi.org/10.1016/S0076-6879(03)01039-5
[DOI: 10.1016/S0076-6879(03)01039-5]
Vasta GR, Feng C, González-Montalbán N, Mancini J, Yang L, Abernathy K, Frost G, Palm C (2017) Functions of galectins as 'self/non-self'-recognition and effector factors. Pathog Dis 75(5):ftx046. https://doi.org/10.1093/femspd/ftx046
[DOI: 10.1093/femspd/ftx046]
Vasta GR (2020) Galectins in host-pathogen interactions: structural, functional and evolutionary aspects. Adv Exp Med Biol 1204:169–196. https://doi.org/10.1007/978-981-15-1580-4_7
[DOI: 10.1007/978-981-15-1580-4_7]
Vasta GR, Ahmed H, Tasumi S, Odom EW, Saito K (2007) Biological roles of lectins in innate immunity: molecular and structural basis for diversity in self/non-self recognition. Adv Exp Med Biol 598:389–406. https://doi.org/10.1007/978-0-387-71767-8_27
[DOI: 10.1007/978-0-387-71767-8_27]
Karlsson A, Christenson K, Matlak M, Bjorstad A, Brown KL, Telemo E, Salomonsson E, Leffler H, Bylund J (2009) Galectin-3 functions as an opsonin and enhances the macrophage clearance of apoptotic neutrophils. Glycobiology 19(1):16–20. https://doi.org/10.1093/glycob/cwn104
[DOI: 10.1093/glycob/cwn104]
Vasta GR (2009) Roles of galectins in infection. Nat Rev Microbiol 7(6):424–438. https://doi.org/10.1038/nrmicro2146
[DOI: 10.1038/nrmicro2146]
Davicino RC, Elicabe RJ, Di Genaro MS, Rabinovich GA (2011) Coupling pathogen recognition to innate immunity through glycan-dependent mechanisms. Int Immunopharmacol 11(10):1457–1463. https://doi.org/10.1016/j.intimp.2011.05.002 . S1567-5769(11)00213-X [pii]
[DOI: 10.1016/j.intimp.2011.05.002]
Rabinovich GA, Toscano MA, Jackson SS, Vasta GR (2007) Functions of cell surface galectin-glycoprotein lattices. Curr Opin Struct Biol 17(5):513–520. https://doi.org/10.1016/j.sbi.2007.09.002 . S0959-440X(07)00130-3 [pii]
[DOI: 10.1016/j.sbi.2007.09.002]
Guha P, Kaptan E, Bandyopadhyaya G, Kaczanowska S, Davila E, Thompson K, Martin SS, Kalvakolanu DV, Vasta GR, Ahmed H (2013) Cod glycopeptide with picomolar affinity to galectin-3 suppresses T-cell apoptosis and prostate cancer metastasis. Proc Natl Acad Sci U S A 110(13):5052–5057. https://doi.org/10.1073/pnas.1202653110
[DOI: 10.1073/pnas.1202653110]
Feng C, Ghosh A, Amin MN, Bachvaroff TR, Tasumi S, Pasek M, Banerjee A, Shridhar S, Wang LX, Bianchet MA, Vasta GR (2015) Galectin CvGal2 from the eastern oyster (Crassostrea virginica) displays unique specificity for ABH blood group oligosaccharides and differentially recognizes sympatric perkinsus species. Biochemistry 54(30):4711–4730. https://doi.org/10.1021/acs.biochem.5b00362
[DOI: 10.1021/acs.biochem.5b00362]
Shi X-Z, Wang L, Xu S, Zhang X-W, Zhao X-F, Vasta GR, Wang J-X (2014) A galectin from the kuruma shrimp (Marsupenaeus japonicus) functions as an opsonin and promotes bacterial clearance from hemolymph. PLoS One 9(3):e91794. https://doi.org/10.1371/journal.pone.0091794
[DOI: 10.1371/journal.pone.0091794]
Nita-Lazar M, Banerjee A, Feng C, Vasta GR (2015) Galectins regulate the inflammatory response in airway epithelial cells exposed to microbial neuraminidase by modulating the expression of SOCS1 and RIG1. Mol Immunol 68(2 Pt A):194–202. https://doi.org/10.1016/j.molimm.2015.08.005
[DOI: 10.1016/j.molimm.2015.08.005]
Nita-Lazar M, Banerjee A, Feng C, Amin MN, Frieman MB, Chen WH, Cross AS, Wang LX, Vasta GR (2015) Desialylation of airway epithelial cells during influenza virus infection enhances pneumococcal adhesion via galectin binding. Mol Immunol 65(1):1–16. https://doi.org/10.1016/j.molimm.2014.12.010
[DOI: 10.1016/j.molimm.2014.12.010]
Ahmed H, Fink NE, Vasta GR (1994) Elasmobranch and teleost fish contain thiol-dependent beta-galactoside-binding lectins that are cross-reactive with those identified and characterized in bovine spleen. Ann N Y Acad Sci 712:318–320
[DOI: 10.1111/j.1749-6632.1994.tb33582.x]
Muramoto K, Kagawa D, Sato T, Ogawa T, Nishida Y, Kamiya H (1999) Functional and structural characterization of multiple galectins from the skin mucus of conger eel, Conger myriaster. Comp Biochem Physiol B Biochem Mol Biol 123(1):33–45
[DOI: 10.1016/S0305-0491(99)00037-1]
Inagawa H, Kuroda A, Nishizawa T, Honda T, Ototake M, Yokomizo U, Nakanishi T, Soma G (2001) Cloning and characterisation of tandem-repeat type galectin in rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol 11(3):217–231
[DOI: 10.1006/fsim.2000.0307]
Ahmed H, Du SJ, O'Leary N, Vasta GR (2004) Biochemical and molecular characterization of galectins from zebrafish (Danio rerio): notochord-specific expression of a prototype galectin during early embryogenesis. Glycobiology 14(3):219–232. https://doi.org/10.1093/glycob/cwh032
[DOI: 10.1093/glycob/cwh032]
Summerton J (1999) Morpholino antisense oligomers: the case for an RNase H-independent structural type. Biochim Biophys Acta 1489(1):141–158
[DOI: 10.1016/S0167-4781(99)00150-5]
Nasevicius A, Ekker SC (2000) Effective targeted gene ‘knockdown’ in zebrafish. Nat Genet 26(2):216–220. https://doi.org/10.1038/79951
[DOI: 10.1038/79951]
Tallafuss A, Gibson D, Morcos P, Li Y, Seredick S, Eisen J, Washbourne P (2012) Turning gene function ON and OFF using sense and antisense photo-morpholinos in zebrafish. Development 139(9):1691–1699. https://doi.org/10.1242/dev.072702
[DOI: 10.1242/dev.072702]
McCallum CM, Comai L, Greene EA, Henikoff S (2000) Targeted screening for induced mutations. Nat Biotechnol 18(4):455–457. https://doi.org/10.1038/74542
[DOI: 10.1038/74542]
Wienholds E, van Eeden F, Kosters M, Mudde J, Plasterk RH, Cuppen E (2003) Efficient target-selected mutagenesis in zebrafish. Genome Res 13(12):2700–2707. https://doi.org/10.1101/gr.1725103
[DOI: 10.1101/gr.1725103]
Halloran MC, Sato-Maeda M, Warren JT, Su F, Lele Z, Krone PH, Kuwada JY, Shoji W (2000) Laser-induced gene expression in specific cells of transgenic zebrafish. Development 127(9):1953–1960
[DOI: 10.1242/dev.127.9.1953]
Hardy ME, Ross LV, Chien CB (2007) Focal gene misexpression in zebrafish embryos induced by local heat shock using a modified soldering iron. Dev Dyn 236(11):3071–3076. https://doi.org/10.1002/dvdy.21318
[DOI: 10.1002/dvdy.21318]
Curado S, Anderson RM, Jungblut B, Mumm J, Schroeter E, Stainier DY (2007) Conditional targeted cell ablation in zebrafish: a new tool for regeneration studies. Dev Dyn 236(4):1025–1035. https://doi.org/10.1002/dvdy.21100
[DOI: 10.1002/dvdy.21100]
Scheer N, Campos-Ortega JA (1999) Use of the Gal4-UAS technique for targeted gene expression in the zebrafish. Mech Dev 80(2):153–158
[DOI: 10.1016/S0925-4773(98)00209-3]
Scott EK (2009) The Gal4/UAS toolbox in zebrafish: new approaches for defining behavioral circuits. J Neurochem 110(2):441–456. https://doi.org/10.1111/j.1471-4159.2009.06161.x
[DOI: 10.1111/j.1471-4159.2009.06161.x]
Clark KJ, Voytas DF, Ekker SC (2011) A TALE of two nucleases: gene targeting for the masses? Zebrafish 8(3):147–149. https://doi.org/10.1089/zeb.2011.9993
[DOI: 10.1089/zeb.2011.9993]
Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337(6096):816–821. https://doi.org/10.1126/science.1225829
[DOI: 10.1126/science.1225829]
Hwang WY, Fu Y, Reyon D, Maeder ML, Tsai SQ, Sander JD, Peterson RT, Yeh JR, Joung JK (2013) Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat Biotechnol 31(3):227–229. https://doi.org/10.1038/nbt.2501
[DOI: 10.1038/nbt.2501]
Oliveira-de-Abreu E, Silva-Dos-Santos D, Lepletier A, Ramos TDP, Ferreira-Reis R, Vasconcelos-Fontes L, Ramos MT, Torres RC, Cotta-de-Almeida V, Carvalho VF, Villa-Verde DMS (2018) Lack of galectin-3 disrupts thymus homeostasis in association to increase of local and systemic glucocorticoid levels and steroidogenic machinery. Front Endocrinol 9:365. https://doi.org/10.3389/fendo.2018.00365
[DOI: 10.3389/fendo.2018.00365]
Ferragut F, Cagnoni AJ, Colombo LL, Sánchez Terrero C, Wolfenstein-Todel C, Troncoso MF, Vanzulli SI, Rabinovich GA, Mariño KV, Elola MT (2019) Dual knockdown of Galectin-8 and its glycosylated ligand, the activated leukocyte cell adhesion molecule (ALCAM/CD166), synergistically delays in vivo breast cancer growth. Biochim Biophys Acta, Mol Cell Res 1866(8):1338–1352. https://doi.org/10.1016/j.bbamcr.2019.03.010
[DOI: 10.1016/j.bbamcr.2019.03.010]
Yang N, Zhang W, He T, Xing Y (2017) Silencing of galectin-1 inhibits retinal neovascularization and ameliorates retinal hypoxia in a murine model of oxygen-induced ischemic retinopathy. Exp Eye Res 159:1–15. https://doi.org/10.1016/j.exer.2017.02.015
[DOI: 10.1016/j.exer.2017.02.015]
Morcos PA (2007) Achieving targeted and quantifiable alteration of mRNA splicing with Morpholino oligos. Biochem Biophys Res Commun 358(2):521–527. https://doi.org/10.1016/j.bbrc.2007.04.172
[DOI: 10.1016/j.bbrc.2007.04.172]
Benato F, Skobo T, Gioacchini G, Moro I, Ciccosanti F, Piacentini M, Fimia GM, Carnevali O, Dalla Valle L (2013) Ambra1 knockdown in zebrafish leads to incomplete development due to severe defects in organogenesis. Autophagy 9(4):476–495. https://doi.org/10.4161/auto.23278
[DOI: 10.4161/auto.23278]
Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, Zhang F (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339(6121):819–823. https://doi.org/10.1126/science.1231143
[DOI: 10.1126/science.1231143]
Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, Norville JE, Church GM (2013) RNA-guided human genome engineering via Cas9. Science 339(6121):823–826. https://doi.org/10.1126/science.1232033
[DOI: 10.1126/science.1232033]
Kang Y, Chu C, Wang F, Niu Y (2019) CRISPR/Cas9-mediated genome editing in nonhuman primates. Dis Model Mech 12(10). https://doi.org/10.1242/dmm.039982
Park JS, Lee KY, Han JY (2020) Precise genome editing in poultry and its application to industries. Genes 11(10):1182. https://doi.org/10.3390/genes11101182
[DOI: 10.3390/genes11101182]
Douris V, Denecke S, Van Leeuwen T, Bass C, Nauen R, Vontas J (2020) Using CRISPR/Cas9 genome modification to understand the genetic basis of insecticide resistance: Drosophila and beyond. Pestic Biochem Physiol 167:104595. https://doi.org/10.1016/j.pestbp.2020.104595
[DOI: 10.1016/j.pestbp.2020.104595]
Wada N, Ueta R, Osakabe Y, Osakabe K (2020) Precision genome editing in plants: state-of-the-art in CRISPR/Cas9-based genome engineering. BMC Plant Biol 20(1):234. https://doi.org/10.1186/s12870-020-02385-5
[DOI: 10.1186/s12870-020-02385-5]
Albadri S, De Santis F, Di Donato V, Del Bene F (2017) CRISPR/Cas9-mediated knockin and knockout in zebrafish. In: Jaenisch R, Zhang F, Gage F (eds) Genome editing in neurosciences. Springer, Cham, pp 41–49. https://doi.org/10.1007/978-3-319-60192-2_4
[DOI: 10.1007/978-3-319-60192-2_4]
Liu K, Petree C, Requena T, Varshney P, Varshney GK (2019) Expanding the CRISPR toolbox in Zebrafish for studying development and disease. Front Cell Dev Biol 7:13. https://doi.org/10.3389/fcell.2019.00013
[DOI: 10.3389/fcell.2019.00013]
Wu N, Liu B, Du H, Zhao S, Li Y, Cheng X, Wang S, Lin J, Zhou J, Deciphering Disorders Involving S, Study CO, Qiu G, Wu Z, Zhang J (2019) The progress of CRISPR/Cas9-mediated gene editing in generating mouse/zebrafish models of human skeletal diseases. Comput Struct Biotechnol J 17:954–962. https://doi.org/10.1016/j.csbj.2019.06.006
[DOI: 10.1016/j.csbj.2019.06.006]