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Chicken lens development: complete signature of expression of galectins during embryogenesis and evidence for their complex formation with α-, β-, δ-, and τ-crystallins, N-CAM, and N-cadherin obtained by affinity chromatography

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Abstract

The emerging multifunctionality of galectins by specific protein-glycan/protein interactions explains the interest to determine their expression during embryogenesis. Complete network analysis of all seven chicken galectins (CGs) is presented in the course of differentiation of eye lens that originates from a single type of progenitor cell. It answers the questions on levels of expression and individual patterns of distribution. A qualitative difference occurs in the CG-1A/B paralogue pair, underscoring conspicuous divergence. Considering different cell phenotypes, lens fiber and also epithelial cells can both express the same CG, with developmental upregulation for CG-3 and CG-8. Except for expression of the lens-specific CG (C-GRIFIN), no other CG appeared to be controlled by the transcription factors L-Maf and Pax6. Studying presence and nature of binding partners for CGs, we tested labeled galectins in histochemistry and in ligand blotting. Mass spectrometric (glyco)protein identification after affinity chromatography prominently yielded four types of crystallins, N-CAM, and, in the cases of CG-3 and CG-8, N-cadherin. Should such pairing be functional in situ, it may be involved in tightly packing intracellular lens proteins and forming membrane contact as well as in gaining plasticity and stability of adhesion processes. The expression of CGs throughout embryogenesis is postulated to give meaning to spatiotemporal alterations in the local glycome.

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References

  • Ahmad N, Gabius H-J, Kaltner H, André S, Kuwabara I, Liu F-T, Oscarson S, Norberg T, Brewer CF (2002) Thermodynamic binding studies of cell surface carbohydrate epitopes to galectins-1, -3 and -7. Evidence for differential binding specificities. Can J Chem 80:1096–1104

    CAS  Google Scholar 

  • Ahmad N, Gabius H-J, Sabesan S, Oscarson S, Brewer CF (2004) Thermodynamic binding studies of bivalent oligosaccharides to galectin-1, galectin-3 and the carbohydrate recognition domain of galectin-3. Glycobiology 14:817–825

    CAS  PubMed  Google Scholar 

  • Aich U, Beckley N, Shriver Z, Raman R, Viswanathan K, Hobbie S, Sasisekharan R (2011) Glycomics-based analysis of chicken red blood cells provides insight into the selectivity of the viral agglutination assay. FEBS J 278:1699–1712

    CAS  PubMed  PubMed Central  Google Scholar 

  • Amano M, Eriksson H, Manning JC, Detjen KM, André S, Nishimura S-I, Lehtiö J, Gabius H-J (2012) Tumour suppressor p16INK4a: anoikis-favouring decrease in N/O-glycan/cell surface sialylation by down-regulation of enzymes in sialic acid biosynthesis in tandem in a pancreatic carcinoma model. FEBS J 279:4062–4080

    CAS  PubMed  Google Scholar 

  • Andley UP, Malone JP, Townsend RR (2014) In vivo substrates of the lens molecular chaperones αA-crystallin and αB-crystallin. PLoS One 9:e95507

    PubMed  PubMed Central  Google Scholar 

  • André S, Sanchez-Ruderisch H, Nakagawa H, Buchholz M, Kopitz J, Forberich P, Kemmner W, Böck C, Deguchi K, Detjen KM, Wiedenmann B, von Knebel-Doeberitz M, Gress TM, Nishimura S-I, Rosewicz S, Gabius H-J (2007) Tumor suppressor p16INK4a: modulator of glycomic profile and galectin-1 expression to increase susceptibility to carbohydrate-dependent induction of anoikis in pancreatic carcinoma cells. FEBS J 274:3233–3256

    Google Scholar 

  • Arneson ML, Louis CF (1998) Structural arrangement of lens fiber cell plasma membrane protein MP20. Exp Eye Res 66:495–509

    CAS  PubMed  Google Scholar 

  • Atreya PL, Barnes J, Katar M, Alcala J, Maisel H (1989) N-Cadherin of the human lens. Curr Eye Res 8:947–956

  • Bagchi M, Katar M, Lewis J, Maisel H (2002) Associated proteins of lens adherens junction. J Cell Biochem 86:700–703

    CAS  PubMed  Google Scholar 

  • Bänfer S, Schneider D, Dewes J, Strauss MT, Freibert SA, Heimerl T, Maier UG, Elsässer HP, Jungmann R, Jacob R (2018) Molecular mechanism to recruit galectin-3 into multivesicular bodies for polarized exosomal secretion. Proc Natl Acad Sci USA 115:E4396–E4405

    PubMed  PubMed Central  Google Scholar 

  • Barondes SH (1997) Galectins: a personal overview. Trends Glycosci Glycotechnol 9:1–7

    CAS  Google Scholar 

  • Barondes SH, Haywood-Reid PL (1981) Externalization of an endogenous chicken muscle lectin with in vivo development. J Cell Biol 91:568–572

    CAS  PubMed  Google Scholar 

  • Barton KA, Hsu CD, Petrash JM (2009) Interactions between small heat shock protein α-crystallin and galectin-related interfiber protein (GRIFIN) in the ocular lens. Biochemistry 48:3956–3966

    CAS  PubMed  Google Scholar 

  • Bassnett S, Sikic H (2017) The lens growth process. Progr Retin Eye Res 60:181–200

    Google Scholar 

  • Bassnett S, Shi Y, Vrensen GF (2011) Biological glass: structural determinants of eye lens transparency. Phil Trans R Soc B 366:1250–1264

    PubMed  PubMed Central  Google Scholar 

  • Beebe DC, Vasiliev O, Guo J, Shui YB, Bassnett S (2001) Changes in adhesion complexes define stages in the differentiation of lens fiber cells. Invest Ophthalmol Vis Sci 42:727–734

    CAS  PubMed  Google Scholar 

  • Bhide GP, Colley KJ (2017) Sialylation of N-glycans: mechanism, cellular compartmentalization and function. Histochem Cell Biol 147:149–174

    CAS  PubMed  Google Scholar 

  • Boscher C, Zheng YZ, Lakshminarayan R, Johannes L, Dennis JW, Foster LJ, Nabi IR (2012) Galectin-3 protein regulates mobility of N-cadherin and GM1 ganglioside at cell-cell junctions of mammary carcinoma cells. J Biol Chem 287:32940–32952

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cao Z, Hao Z, Xin M, Yu L, Wang L, Zhang Y, Zhang X, Guo X (2018) Endogenous and exogenous galectin-3 promote the adhesion of tumor cells with low expression of MUC1 to HUVECs through upregulation of N-cadherin and CD44. Lab Invest 98:1642–1656

    CAS  PubMed  Google Scholar 

  • Chauhan S, Kumar S, Jain A, Ponpuak M, Mudd MH, Kimura T, Choi SW, Peters R, Mandell M, Bruun JA, Johansen T, Deretic V (2016) TRIMs and galectins globally cooperate and TRIM16 and galectin-3 co-direct autophagy in endomembrane damage homeostasis. Dev Cell 39:13–27

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chauss D, Basu S, Rajakaruna S, Ma Z, Gau V, Anastas S, Brennan LA, Hejtmancik JF, Menko AS, Kantorow M (2014) Differentiation state-specific mitochondrial dynamic regulatory networks are revealed by global transcriptional analysis of the developing chicken lens. G3 (Bethesda) 4:1515–1527

    CAS  Google Scholar 

  • Chaves JM, Gupta R, Srivastava K, Srivastava O (2017) Human αA-crystallin missing N-terminal domain poorly complexes with filensin and phakinin. Biochem Biophys Res Commun 494:402–408

    CAS  PubMed  Google Scholar 

  • Chen Y, Sagar V, Len HS, Peterson K, Fan J, Mishra S, McMurtry J, Wilmarth PA, David LL, Wistow G (2016) γ-Crystallins of the chicken lens: remnants of an ancient vertebrate gene family in birds. FEBS J 283:1516–1530

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chow RL, Lang RA (2001) Early eye development in vertebrates. Annu Rev Cell Dev Biol 17:255–296

    CAS  PubMed  Google Scholar 

  • Cooper DNW (2002) Galectinomics: finding themes in complexity. Biochim Biophys Acta 1572:209–231

    CAS  PubMed  Google Scholar 

  • Corfield AP (2015) Mucins: a biologically relevant glycan barrier in mucosal protection. Biochim Biophys Acta 1850:236–252

    CAS  PubMed  Google Scholar 

  • Corfield AP (2017) Eukaryotic protein glycosylation: a primer for histochemists and cell biologists. Histochem Cell Biol 147:119–147

    CAS  PubMed  Google Scholar 

  • Cvekl A, Zhang X (2017) Signaling and gene regulatory networks in mammalian lens development. Trends Genet 33:677–702

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dahm R, Branmke S, Dawczynski J, Nagaraj RH, Kasper M (2003) Developmental aspects of galectin expression in the lens. Histochem Cell Biol 119:219–226

    CAS  PubMed  Google Scholar 

  • Einhoff W, Fleischmann G, Freier T, Kummer H, Rüdiger H (1986) Interactions between lectins and other components of leguminous protein bodies. Biol Chem Hoppe-Seyler 367:15–25

    CAS  PubMed  Google Scholar 

  • Ferreira-Cornwell MC, Veneziale RW, Grunwald GB, Menko AS (2000) N-cCadherin function is required for differentiation-dependent cytoskeletal reorganization in lens cells in vitro. Exp Cell Res 256:237–247

    CAS  PubMed  Google Scholar 

  • Flores-Ibarra A, Vértesy S, Medrano FJ, Gabius H-J, Romero A (2018) Crystallization of a human galectin-3 variant with two ordered segments in the shortened N-terminal tail. Sci Rep 8:9835

    PubMed  PubMed Central  Google Scholar 

  • Franke WW, Rickelt S, Barth M, Pieperhoff S (2009) The junctions that don’t fit the scheme: special symmetrical cell-cell junctions of their own kind. Cell Tissue Res 338:1–17

    PubMed  PubMed Central  Google Scholar 

  • Freier T, Rüdiger H (1987) In vivo binding partners of the Lens culinaris lectin. Biol Chem Hoppe-Seyler 368:1215–1223

    CAS  PubMed  Google Scholar 

  • Gabius H-J (2017) How to crack the sugar code. Folia Biol (Praha) 63:121–131

    Google Scholar 

  • Gabius H-J, Roth J (2017) An introduction to the sugar code. Histochem Cell Biol 147:111–117

    CAS  PubMed  Google Scholar 

  • Gabius H-J, Wosgien B, Hendrys M, Bardosi A (1991) Lectin localization in human nerve by biochemically defined lectin-binding glycoproteins, neoglycoprotein and lectin-specific antibody. Histochemistry 95:269–277

    CAS  PubMed  Google Scholar 

  • Gabius H-J, Kaltner H, Kopitz J, André S (2015) The glycobiology of the CD system: a dictionary for translating marker designations into glycan/lectin structure and function. Trends Biochem Sci 40:360–376

    CAS  PubMed  Google Scholar 

  • Gansera R, Schurz H, Rüdiger H (1979) Lectin-associated proteins from the seeds of Leguminosae. Hoppe-Seyler’s Z Physiol Chem 360:1579–1585

    CAS  Google Scholar 

  • García Caballero G, Kaltner H, Michalak M, Shilova N, Yegres M, André S, Ludwig A-K, Manning JC, Schmidt S, Schnölzer M, Bovin NV, Reusch D, Kopitz J, Gabius H-J (2016a) Chicken GRIFIN: a homodimeric member of the galectin network with canonical properties and a unique expression profile. Biochimie 128-129:34–47

    PubMed  Google Scholar 

  • García Caballero G, Flores-Ibarra A, Michalak M, Khasbiullina N, Bovin NV, André S, Manning JC, Vértesy S, Ruiz FM, Kaltner H, Kopitz J, Romero A, Gabius H-J (2016b) Galectin-related protein: an integral member of the network of chicken galectins. 1. From strong sequence conservation of the gene confined to vertebrates to biochemical characteristics of the chicken protein and its crystal structure. Biochim Biophys Acta 1860:2285–2297

    PubMed  Google Scholar 

  • García Caballero G, Manning JC, Ludwig A-K, Ruiz FM, Romero A, Kaltner H, Gabius H-J (2018) Members of the galectin network with deviations from the canonical sequence signature. 1. Galectin-Related Inter-Fiber Protein (GRIFIN). Trends Glycosci Glycotechnol 30:SE1–SE9

    Google Scholar 

  • García Caballero G, Schmidt S, Schnölzer M, Schlötzer-Schrehardt U, Knospe C, Ludwig A-K, Manning JC, Muschler P, Kaltner H, Kopitz J, Gabius H-J (2019) Chicken GRIFIN: binding partners, developmental course of localization and activation of its lens-specific gene expression by L-Maf/Pax6. Cell Tissue Res 375:665–683

    PubMed  Google Scholar 

  • Geatrell JC, Gan PM, Mansergh FC, Kisiswa L, Jarrin M, Williams LA, Evans MJ, Boulton ME, Wride MA (2009) Apoptosis gene profiling reveals spatio-temporal regulated expression of the p53/Mdm2 pathway during lens development. Exp Eye Res 88:1137–1151

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ginsburg V, Neufeld EF (1969) Complex heterosaccharides of animals. Annu Rev Biochem 38:371–388

    CAS  PubMed  Google Scholar 

  • Gonen T, Donaldson P, Kistler J (2000) Galectin-3 is associated with the plasma membrane of lens fiber cells. Invest Ophthalmol Vis Sci 41:199–203

    CAS  PubMed  Google Scholar 

  • Gonen T, Grey AC, Jacobs MD, Donaldson PJ, Kistler J (2001) MP20, the second most abundant lens membrane protein and member of the tetraspanin superfamily, joins the list of ligands of galectin-3. BMC Cell Biol 2:17

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gorski JP, Liu F-T, Artigues A, Castagna LF, Osdoby P (2002) New alternatively spliced form of galectin-3, a member of the β-galactoside-binding animal lectin family, contains a predicted transmembrane-spanning domain and a leucine zipper motif. J Biol Chem 277:18840–18848

    CAS  Google Scholar 

  • Grainger RM (1992) Embryonic lens induction: shedding light on vertebrate tissue determination. Trends Genet 8:349–355

    CAS  PubMed  Google Scholar 

  • Griffith CM, Sanders EJ (1991) Changes in glycoconjugate expression during early chick embryo development: a lectin-binding study. Anat Rec 231:238–250

    CAS  PubMed  Google Scholar 

  • Halimi H, Rigato A, Byrne D, Ferracci G, Sebban-Kreuzer C, ElAntak L, Guerlesquin F (2014) Glycan dependence of Galectin-3 self-association properties. PLoS One 9:e111836

    PubMed  PubMed Central  Google Scholar 

  • Haltiwanger RS, Lowe JB (2004) Role of glycosylation in development. Annu Rev Biochem 73:491–537

    CAS  PubMed  Google Scholar 

  • Hamburger V, Hamilton HL (1951) A series of normal stages in the development of the chick embryo. J Morphol 88:49–92

    CAS  PubMed  Google Scholar 

  • Hamburger V, Hamilton HL (1992) A series of normal stages in the development of the chick embryo. Dev Dyn 195:231–272

    CAS  PubMed  Google Scholar 

  • Harrison FL, Chesterton CJ (1980) Factors mediating cell-cell recognition and adhesion. Galaptins, a recently discovered class of bridging molecules. FEBS Lett 122:157–165

    CAS  PubMed  Google Scholar 

  • Hatta K, Takeichi M (1986) Expression of N-cadherin adhesion molecules associated with early morphogenetic events in chick development. Nature 320:447–449

    CAS  PubMed  Google Scholar 

  • Higuero AM, Díez-Revuelta N, Abad-Rodríguez J (2017) The sugar code in neuronal physiology. Histochem Cell Biol 147:257–267

    CAS  PubMed  Google Scholar 

  • Hirabayashi J, Hashidate T, Arata Y, Nishi N, Nakamura T, Hirashima M, Urashima T, Oka T, Futai M, Müller WEG, Yagi F, Kasai K-i (2002) Oligosaccharide specificity of galectins: a search by frontal affinity chromatography. Biochim Biophys Acta 1572:232–254

    CAS  PubMed  Google Scholar 

  • Hong M-H, Weng I-C, Liu F-T (2018) Galectins as intracellular regulators of cellular responses through the detection of damaged endocytic vesicles. Trends Glycosci Glycotechnol 30:SE179–SE184

    Google Scholar 

  • Hrdlicková-Cela E, Plzák J, Smetana K Jr, Melkova Z, Kaltner H, Filipec M, Liu F-T, Gabius H-J (2001) Detection of galectin-3 in tear fluid at disease states and immunohistochemical and lectin histochemical analysis in human corneal and conjunctival epithelium. Br J Ophthalmol 85:1336–1340

    PubMed  PubMed Central  Google Scholar 

  • Ippel H, Miller MC, Vértesy S, Zheng Y, Canada FJ, Suylen D, Umemoto K, Romano C, Hackeng T, Tai G, Leffler H, Kopitz J, André S, Kübler D, Jiménez-Barbero J, Oscarson S, Gabius H-J, Mayo KH (2016) Intra- and intermolecular interactions of human galectin-3: assessment by full-assignment-based NMR. Glycobiology 26:888–903

    CAS  PubMed  PubMed Central  Google Scholar 

  • Iwaki J, Hirabayashi J (2018) Carbohydrate-binding specificity of human galectins: an overview by frontal affinity chromatography. Trends Glycosci Glycotechnol 30:SE137–SE153

    Google Scholar 

  • Jiang K, Rankin CR, Nava P, Sumagin R, Kamekura R, Stowell SR, Feng M, Parkos CA, Nusrat A (2014) Galectin-3 regulates desmoglein-2 and intestinal epithelial intercellular adhesion. J Biol Chem 289:10510–10517

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kaltner H, Seyrek K, Heck A, Sinowatz F, Gabius H-J (2002) Galectin-1 and galectin-3 in fetal development of bovine respiratory and digestive tracts. Comparison of cell type-specific expression profiles and subcellular localization. Cell Tissue Res 307:35–46

    CAS  PubMed  Google Scholar 

  • Kaltner H, Solís D, Kopitz J, Lensch M, Lohr M, Manning JC, Mürnseer M, Schnölzer M, André S, Sáiz JL, Gabius H-J (2008) Proto-type chicken galectins revisited: characterization of a third protein with distinctive hydrodynamic behaviour and expression pattern in organs of adult animals. Biochem J 409:591–599

    CAS  PubMed  Google Scholar 

  • Kaltner H, Kübler D, López-Merino L, Lohr M, Manning JC, Lensch M, Seidler J, Lehmann WD, André S, Solís D, Gabius H-J (2011) Toward comprehensive analysis of the galectin network in chicken: unique diversity of galectin-3 and comparison of its localization profile in organs of adult animals to the other four members of this lectin family. Anat Rec 294:427–444

    CAS  Google Scholar 

  • Kaltner H, García Caballero G, Sinowatz F, Schmidt S, Manning JC, André S, Gabius H-J (2016) Galectin-related protein: an integral member of the network of chicken galectins. 2. From expression profiling to its immunocyto- and histochemical localization and application as tool for ligand detection. Biochim Biophys Acta 1860:2298–2312

    CAS  PubMed  Google Scholar 

  • Kaltner H, Toegel S, García Caballero G, Manning JC, Ledeen RW, Gabius H-J (2017) Galectins: their network and roles in immunity/tumor growth control. Histochem Cell Biol 147:239–256

    CAS  PubMed  Google Scholar 

  • Kaltner H, García Caballero G, Ludwig A-K, Manning JC, Gabius H-J (2018) From glycophenotyping by (plant) lectin histochemistry to defining functionality of glycans by pairing with endogenous lectins. Histochem Cell Biol 149:547–568

    CAS  PubMed  Google Scholar 

  • Kaltner H, Abad-Rodrígez J, Corfield AP, Kopitz J, Gabius H-J (2019) The sugar code: letters and vocabulary, writers, editors and readers and biosignifacnce of functional glycan-lectin pairing. Biochem J 476:2623–2655

    CAS  PubMed  Google Scholar 

  • Kasai K-i (1997) Galectin: intelligent glue, non-bureaucratic bureaucrat or almighty supporting actor. Trends Glycosci Glycotechnol 9:167–170

    CAS  Google Scholar 

  • Kasai K-i (2018) Galectins: quadruple-faced proteins. Trends Glycosci Glycotechnol 30:SE221–SE223

    Google Scholar 

  • Katar M, Alcala J, Maisel H (1993) NCAM of the mammalian lens. Curr Eye Res 12:191–196

    CAS  PubMed  Google Scholar 

  • Knibbs RN, Agrwal N, Wang JL, Goldstein IJ (1993) Carbohydrate-binding protein 35. II. Analysis of the interaction of the recombinant polypeptide with saccharides. J Biol Chem 268:14940–14947

    CAS  PubMed  Google Scholar 

  • Kondoh H (1999) Transcription factors for lens development assessed in vivo. Curr Opin Genet Dev 9:301–308

    CAS  PubMed  Google Scholar 

  • Kopitz J (2017) Lipid glycosylation: a primer for histochemists and cell biologists. Histochem Cell Biol 147:175–198

    CAS  PubMed  Google Scholar 

  • Kopitz J, von Reitzenstein C, André S, Kaltner H, Uhl J, Ehemann V, Cantz M, Gabius H-J (2001) Negative regulation of neuroblastoma cell growth by carbohydrate-dependent surface binding of galectin-1 and functional divergence from galectin-3. J Biol Chem 276:35917–35923

    CAS  PubMed  Google Scholar 

  • Krzeminski M, Singh T, André S, Lensch M, Wu AM, Bonvin AMJJ, Gabius H-J (2011) Human galectin-3 (Mac-2 antigen): defining molecular switches of affinity to natural glycoproteins, structural and dynamic aspects of glycan binding by flexible ligand docking and putative regulatory sequences in the proximal promoter region. Biochim Biophys Acta 1810:150–161

    CAS  PubMed  Google Scholar 

  • Kummer H, Rüdiger H (1988) Characterization of a lectin-binding storage protein from pea (Pisum sativum). Biol Chem Hoppe-Seyler 369:639–646

    CAS  PubMed  Google Scholar 

  • Kuwabara T (1975) The maturation of the lens cell: a morphologic study. Exp Eye Res 20:427–443

    CAS  PubMed  Google Scholar 

  • Leffler H (2018) Galectin history, some stories, and some outstanding questions. Trends Glycosci Glycotechnol 30:SE129–SE135

    Google Scholar 

  • Lips KS, Kaltner H, Reuter G, Stierstorfer B, Sinowatz F, Gabius H-J (1999) Correspondence of gradual developmental increases of expression of galectin-reactive glycoconjugates with alterations of the total contents of the two differentially regulated galectins in chicken intestine and liver as indication for overlapping functions. Histol Histopathol 14:743–760

    CAS  PubMed  Google Scholar 

  • Louis CF, Hur KC, Galvan AC, TenBroek EM, Jarvis LJ, Eccleston ED, Howard JB (1989) Identification of an 18,000-dalton protein in mammalian lens fiber cell membranes. J Biol Chem 264:19967–19973

    CAS  PubMed  Google Scholar 

  • Ludwig A-K, Michalak M, Xiao Q, Gilles U, Medrano FJ, Ma H, FitzGerald FG, Hasley WD, Melendez-Davila A, Liu M, Rahimi K, Kostina NY, Rodriguez-Emmenegger C, Möller M, Lindner I, Kaltner H, Cudic M, Reusch D, Kopitz J, Romero A, Oscarson S, Klein ML, Gabius H-J, Percec V (2019) Design-functionality relationships for adhesion/growth-regulatory galectins. Proc Natl Acad Sci USA 116:2837–2842

    CAS  PubMed  PubMed Central  Google Scholar 

  • Maisel H, Hardling CV, Alcala JR, Kuszak JR, Bradley R (1981) The morphology of the lens. In: Bloemendal H (ed) Molecular and cellular biology of the eye lens. Wiley, New York, pp 49–84

    Google Scholar 

  • Manning JC, Romero A, Habermann FA, García Caballero G, Kaltner H, Gabius H-J (2017a) Lectins: a primer for histochemists and cell biologists. Histochem Cell Biol 147:199–222

    CAS  PubMed  Google Scholar 

  • Manning JC, García Caballero G, Knospe C, Kaltner H, Gabius H-J (2017b) Network analysis of adhesion/growth-regulatory galectins and their binding sites in adult chicken retina and choroid. J Anat 231:23–37

    CAS  PubMed  PubMed Central  Google Scholar 

  • Manning JC, García Caballero G, Ruiz FM, Romero A, Kaltner H, Gabius H-J (2018a) Members of the galectin network with deviations from the canonical sequence signature, 2. Galectin-Related Protein (GRP). Trends Glycosci Glycotechnol 30:SE11–SE20

  • Manning JC, García Caballero G, Knospe C, Kaltner H, Gabius H-J (2018b) Three-step monitoring of glycan and galectin profiles in the anterior segment of the adult chicken eye. Ann Anat 217:66–81

    PubMed  Google Scholar 

  • Michalak M, Warnken U, André S, Schnölzer M, Gabius H-J, Kopitz J (2017) Detection of proteome changes in human colon cancer induced by cell surface binding of growth-inhibitory galectin-4 using quantitative SILAC-based proteomics. J Proteome Res 15:4412–4422

    Google Scholar 

  • Miller MC, Ludwig A-K, Wichapong K, Kaltner H, Kopitz J, Gabius H-J, Mayo KH (2018) Adhesion/growth-regulatory galectins tested in combination: evidence for formation of hybrids as heterodimers. Biochem J 475:1003–1018

    CAS  PubMed  Google Scholar 

  • Muta M, Kamachi Y, Yoshimoto A, Higashi Y, Kondoh H (2002) Distinct roles of SOX2, Pax6 and Maf transcription factors in the regulation of lens-specific δ1-crystallin enhancer. Genes Cells 7:791–805

    CAS  PubMed  Google Scholar 

  • Ogden AT, Nunes I, Ko K, Wu S, Hines CS, Wang AF, Hegde RS, Lang RA (1998) GRIFIN, a novel lens-specific protein related to the galectin family. J Biol Chem 273:28889–28896

    CAS  PubMed  Google Scholar 

  • Philpott GW, Coulombre AJ (1965) Lens development. II. The differentiation of embryonic chick lens epithelial cells in vitro and in vivo. Exp Cell Res 38:635–644

    CAS  PubMed  Google Scholar 

  • Piatigorsky J (1981) Lens differentiation in vertebrates. A review of cellular and molecular features. Differentiation 19:134–153

    CAS  PubMed  Google Scholar 

  • Plzák J, Holíková Z, Smetana K Jr, Dvoránková B, Hercogová J, Kaltner H, Motlík J, Gabius H-J (2002) Differentiation-dependent glycosylation of cells in squamous cell epithelia detected by a mammalian lectin. Cells Tissues Organs 171:135–144

    PubMed  Google Scholar 

  • Rafferty MS (1985) Lens morphology. In: Maisel H (ed) The ocular lens: structure, function and pathology. Marcel Dekker, New York, pp 85–136

    Google Scholar 

  • Rapoport EM, Matveeva VK, Kaltner H, André S, Vokhmyanina OA, Pazynina GV, Severov VV, Ryzhov IM, Korchagina EY, Belyanchikov IM, Gabius H-J, Bovin NV (2015) Comparative lectinology: delineating glycan-specificity profiles of the chicken galectins using neoglycoconjugates in a cell assay. Glycobiology 25:726–734

    CAS  PubMed  Google Scholar 

  • Remington SG (1993) Chicken filensin: a lens fiber cell protein that exhibits sequence similarity to intermediate filament proteins. J Cell Sci 105:1057–1068

    CAS  PubMed  Google Scholar 

  • Reza HM, Yasuda K (2004) Roles of Maf family proteins in lens development. Dev Dyn 229:440–448

    CAS  PubMed  Google Scholar 

  • Ruiz FM, Gilles U, Ludwig A-K, Sehad C, Shiao TC, García Caballero G, Kaltner H, Lindner I, Roy R, Reusch D, Romero A, Gabius H-J (2018) Chicken GRIFIN: structural characterization in crystals and in solution. Biochimie 146:127–138

    CAS  PubMed  Google Scholar 

  • Sakakura Y, Hirabayashi J, Oda Y, Ohyama Y, Kasai K-i (1990) Structure of chicken 16-kDa β-galactoside-binding lectin. Complete amino acid sequence, cloning of cDNA and production of recombinant lectin. J Biol Chem 265:21573–21579

    CAS  PubMed  Google Scholar 

  • Sanchez-Ruderisch H, Fischer C, Detjen KM, Welzel M, Wimmel A, Manning JC, André S, Gabius H-J (2010) Tumor suppressor p16INK4a: downregulation of galectin-3, an endogenous competitor of the pro-anoikis effector galectin-1, in a pancreatic carcinoma model. FEBS J 277:3552–3563

    CAS  PubMed  Google Scholar 

  • Schecher G, Rüdiger H (1994) Interaction of the soybean (Glycine max) seed lectin with components of the soybean protein body membrane. Biol Chem Hoppe-Seyler 375:829–832

    CAS  PubMed  Google Scholar 

  • Slingsby C, Wistow GJ, Clark AR (2013) Evolution of crystallins for a role in the vertebrate eye lens. Protein Sci 22:367–380

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sparrow C, Leffler H, Barondes SH (1987) Multiple soluble β-galactoside-binding lectins from human lung. J Biol Chem 262:7383–7390

    CAS  PubMed  Google Scholar 

  • Straub BK, Boda J, Kuhn C, Schnoelzer M, Korf U, Kempf T, Spring H, Hatzfeld M, Franke WW (2003) A novel cell-cell junction system: the cortex adhaerens mosaic of lens fiber cells. J Cell Sci 116:4985–4995

    CAS  PubMed  Google Scholar 

  • Teichberg VI, Silman I, Beitsch DD, Resheff G (1975) A β-d-galactoside binding protein from electric organ tissue of Electrophorus electricus. Proc Natl Acad Sci USA 72:1383–1387

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thiery JP, Duband JL, Rutishauser U, Edelman GM (1982) Cell adhesion molecules in early chicken embryogenesis. Proc Natl Acad Sci USA 79:6737–6741

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ueda Y, Fukiage C, Shih M, Shearer TR, David LL (2002) Mass measurements of C-terminally truncated α-crystallins from two-dimensional gels identify Lp82 as a major endopeptidase in rat lens. Mol Cell Proteomics 1:357–365

    CAS  PubMed  Google Scholar 

  • Volk T, Geiger B (1986a) A-CAM: a 135-kD receptor of intercellular adherens junctions. I. Immunoelectron microscopic localization and biochemical studies. J Cell Biol 103:1441–1450

    CAS  PubMed  Google Scholar 

  • Volk T, Geiger B (1986b) A-CAM: a 135-kD receptor of intercellular adherens junctions. II. Antibody-mediated modulation of junction formation. J Cell Biol 103:1451–1464

    CAS  PubMed  Google Scholar 

  • Wang J, Lu ZH, Gabius H-J, Rohowsky-Kochan C, Ledeen RW, Wu G (2009) Cross-linking of GM1 ganglioside by galectin-1 mediates regulatory T cell activity involving TRPC5 channel activation: possible role in suppressing experimental autoimmune encephalomyelitis. J Immunol 182:4036–4045

    CAS  PubMed  Google Scholar 

  • Wang-Su S-T, McCormack AL, Yang S, Hosler MR, Mixon A, Riviere MA, Wilmarth PA, Andley UP, Garland D, Li H, David LL, Wagner BJ (2003) Proteome analysis of lens epithelia, fibers, and the HLE B-3 cell line. Invest Ophthalmol Vis Sci 44:4829–4836

    PubMed  Google Scholar 

  • Watanabe M, Kobayashi H, Yao R, Maisel H (1992) Adhesion and junction molecules in embryonic and adult lens cell differentiation. Acta Ophthalmol Suppl 205:46–52

    Google Scholar 

  • Watanabe M, Kobayashi H, Rutishauser U, Katar M, Alcala J, Maisel H (1989) NCAM in the differentiation of embryonic lens tissue. Dev Biol 135:414–423

    CAS  PubMed  Google Scholar 

  • Weinmann D, Kenn M, Schmidt S, Schmidt K, Walzer SM, Kubista B, Windhager R, Schreiner W, Toegel S, Gabius H-J (2018) Galectin-8 induces functional disease markers in human osteoarthritis and cooperates with galectins-1 and -3. Cell Mol Life Sci 75:4187–4205

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wistow G (1993) Lens crystallins: gene recruitment and evolutionary dynamism. Trends Biochem Sci 18:301–306

    CAS  PubMed  Google Scholar 

  • Wistow GJ, Piatigorsky J (1988) Lens crystallins: the evolution and expression of proteins for a highly specialized tissue. Annu Rev Biochem 57:479–504

    CAS  PubMed  Google Scholar 

  • Wu AM, Singh T, Liu J-H, Krzeminski M, Russwurm R, Siebert H-C, Bonvin AMJJ, André S, Gabius H-J (2007) Activity-structure correlations in divergent lectin evolution: fine specificity of chicken galectin CG-14 and computational analysis of flexible ligand docking for CG-14 and the closely related CG-16. Glycobiology 17:165–184

    CAS  PubMed  Google Scholar 

  • Xiao Q, Ludwig A-K, Romano C, Buzzacchera I, Sherman SE, Vetro M, Vértesy S, Kaltner H, Reed EH, Möller M, Wilson CJ, Hammer DA, Oscarson S, Klein ML, Gabius H-J, Percec V (2018) Exploring functional pairing between surface glycoconjugates and human galectins using programmable glycodendrimersomes. Proc Natl Acad Sci USA 115:E2509–E2518

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yao R, Alcala J, Maisel H (1996) Developmental changes in glycoconjugate composition during chick lens morphogenesis. Exp Eye Res 62:419–431

    CAS  PubMed  Google Scholar 

  • Yu LG, Andrews N, Zhao Q, McKean D, Williams JF, Connor LJ, Gerasimenko OV, Hilkens J, Hirabayashi J, Kasai K, Rhodes JM (2007) Galectin-3 interaction with Thomsen-Friedenreich disaccharide on cancer-associated MUC1 causes increased cancer cell endothelial adhesion. J Biol Chem 282:773–781

    CAS  PubMed  Google Scholar 

  • Zalik SE (1991) On the possible role of endogenous lectins in early animal development. Anat Embryol 183:521–536

    CAS  Google Scholar 

  • Zhao Y, Zheng D, Cvekl A (2018) A comprehensive spatial-temporal transcriptomic analysis of differentiating nascent mouse lens epithelial and fiber cells. Exp Eye Res 175:56–72

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zuber C, Roth J (2009) N-Glycosylation. In: Gabius H-J (ed) The Sugar Code. Fundamentals of glycosciences. Wiley-VCH, Weinheim, pp 87–110

    Google Scholar 

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Acknowledgments

We are grateful to Dr. P. Muschler for carefully examining reporter assay data and valuable advice and to Drs. B. Friday, A. Leddoz, and A. W. L. Nose for inspiring discussions and advice on language presentation as well as to the reviewers for their excellent recommendations and high-quality input.

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Authors and Affiliations

  1. Institute for Physiological Chemistry, Faculty of Veterinary Medicine, Ludwig-Maximilians-University Munich, Veterinärstr. 13, 80539, Munich, Germany

    Gabriel García Caballero, Sebastian Schmidt, Joachim C. Manning, Anna-Kristin Ludwig, Herbert Kaltner & Hans-Joachim Gabius

  2. Department of Applied Tumor Biology, Institute of Pathology, Medical School of the Ruprecht-Karls-University Heidelberg, Im Neuenheimer Feld 224, 69120, Heidelberg, Germany

    Malwina Michalak & Jürgen Kopitz

  3. Department of Ophthalmology, Friedrich-Alexander-University Erlangen-Nuremberg, Schwabachanlage 6, 91054, Erlangen, Germany

    Ursula Schlötzer-Schrehardt

  4. Institute of Anatomy, Histology and Embryology, Faculty of Veterinary Medicine, Ludwig-Maximilians-University Munich, Veterinärstr. 13, 80539, Munich, Germany

    Fred Sinowatz

  5. Functional Proteome Analysis, German Cancer Research Center (DKFZ), Im Neuenheimer Feld 581, 69120, Heidelberg, Germany

    Martina Schnölzer

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  1. Gabriel García Caballero
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García Caballero, G., Schmidt, S., Manning, J.C. et al. Chicken lens development: complete signature of expression of galectins during embryogenesis and evidence for their complex formation with α-, β-, δ-, and τ-crystallins, N-CAM, and N-cadherin obtained by affinity chromatography. Cell Tissue Res 379, 13–35 (2020). https://doi.org/10.1007/s00441-019-03129-0

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