Phylogenetic analysis of the vertebrate galectin family.

Galectins form a family of structurally related carbohydrate binding proteins (lectins) that have been identified in a large variety of metazoan phyla. They are involved in many biological processes such as morphogenesis, control of cell death, immunological response, and cancer. To elucidate the evolutionary history of galectins and galectin-like proteins in chordates, we have exploited three independent lines of evidence: (i) location of galectin encoding genes (LGALS) in the human genome; (ii) exon-intron organization of galectin encoding genes; and (iii) sequence comparison of carbohydrate recognition domains (CRDs) of chordate galectins. Our results suggest that a duplication of a mono-CRD galectin gene gave rise to an original bi-CRD galectin gene, before or early in chordate evolution. The N-terminal and C-terminal CRDs of this original galectin subsequently diverged into two different subtypes, defined by exon-intron structure (F4-CRD and F3-CRD). We show that all vertebrate mono-CRD galectins known to date belong to either the F3- or F4- subtype. A sequence of duplication and divergence events of the different galectins in chordates is proposed.

[1]  B. Honoré,et al.  Cloning, Expression, and Chromosome Mapping of Human Galectin-7 (*) , 1995, The Journal of Biological Chemistry.

[2]  K. Pienta,et al.  Galectin-3 induces endothelial cell morphogenesis and angiogenesis. , 2000, The American journal of pathology.

[3]  H. Inohara,et al.  Down-regulation of galectin-3 suppresses tumorigenicity of human breast carcinoma cells. , 2001, Clinical cancer research : an official journal of the American Association for Cancer Research.

[4]  J. Sacchettini,et al.  Multivalent protein-carbohydrate interactions. A new paradigm for supermolecular assembly and signal transduction. , 2001, Biochemistry.

[5]  A. Raz,et al.  Cell cycle arrest and inhibition of anoikis by galectin-3 in human breast epithelial cells. , 1999, Cancer research.

[6]  Remy Loris,et al.  Principles of structures of animal and plant lectins. , 2002, Biochimica et biophysica acta.

[7]  Martin Vingron,et al.  TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing , 2002, Bioinform..

[8]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[9]  G. Rabinovich,et al.  Role of galectins in inflammatory and immunomodulatory processes. , 2002, Biochimica et biophysica acta.

[10]  W. Makałowski Are we polyploids? A brief history of one hypothesis. , 2001, Genome research.

[11]  S. Barondes,et al.  Genomic sequence and organization of two members of a human lectin gene family. , 1991, Biochemistry.

[12]  A. Hughes Evolution of the Integrin α and β Protein Families , 2001, Journal of Molecular Evolution.

[13]  A. Sidow,et al.  Gene duplications and the origins of vertebrate development. , 1994, Development (Cambridge, England). Supplement.

[14]  A. Hughes Evolution of the integrin alpha and beta protein families. , 2001, Journal of molecular evolution.

[15]  M. P. Cummings PHYLIP (Phylogeny Inference Package) , 2004 .

[16]  S. Barondes,et al.  Sequence, Structure, and Chromosomal Mapping of the MouseLgals6 Gene, Encoding Galectin-6* , 1998, The Journal of Biological Chemistry.

[17]  J. Dunphy,et al.  Isolation and Characterization of a Novel Eosinophil-specific Galectin Released into the Lungs in Response to Allergen Challenge* , 2002, The Journal of Biological Chemistry.

[18]  Isabelle Camby,et al.  Galectins and cancer. , 2002, Biochimica et biophysica acta.

[19]  K. Acharya,et al.  Structural basis for the recognition of carbohydrates by human galectin-7. , 1998, Biochemistry.

[20]  André Gilles,et al.  Evidence of en bloc duplication in vertebrate genomes , 2002, Nature Genetics.

[21]  Richard D. Cummings,et al.  Galectins: A family of animal β-galactoside-binding lectins , 1994, Cell.

[22]  Manolo Gouy,et al.  SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny , 1996, Comput. Appl. Biosci..

[23]  J. Dunphy,et al.  Isolation and Characterization of a Novel Inducible Mammalian Galectin* , 2000, The Journal of Biological Chemistry.

[24]  R. Hegde,et al.  GRIFIN, a Novel Lens-specific Protein Related to the Galectin Family* , 1998, The Journal of Biological Chemistry.

[25]  T. Magnaldo,et al.  Galectin-7, a human 14-kDa S-lectin, specifically expressed in keratinocytes and sensitive to retinoic acid. , 1995, Developmental biology.

[26]  H. Leffler Galectins structure and function--a synopsis. , 2001, Results and problems in cell differentiation.

[27]  J. Spring,et al.  Genome duplication strikes back , 2002, Nature Genetics.

[28]  J Hirabayashi,et al.  The family of metazoan metal-independent beta-galactoside-binding lectins: structure, function and molecular evolution. , 1993, Glycobiology.

[29]  D. Kilpatrick Animal lectins: a historical introduction and overview. , 2002, Biochimica et biophysica acta.

[30]  J. Rini,et al.  New animal lectin structures. , 1999, Current opinion in structural biology.

[31]  S. Barondes,et al.  X-ray crystal structure of the human galectin-3 carbohydrate recognition domain at 2.1-A resolution. , 1998, The Journal of biological chemistry.

[32]  S. Barondes,et al.  X-ray crystal structure of the human dimeric S-Lac lectin, L-14-II, in complex with lactose at 2.9-A resolution. , 1994, The Journal of biological chemistry.

[33]  E. Robertson,et al.  Normal development of mice carrying a null mutation in the gene encoding the L14 S-type lectin. , 1993, Development.

[34]  C. Colnot,et al.  Expression of galectin-7 during epithelial development coincides with the onset of stratification. , 1999, The International journal of developmental biology.

[35]  C. Colnot,et al.  Embryonic implantation in galectin 1/galectin 3 double mutant mice , 1998, Developmental dynamics : an official publication of the American Association of Anatomists.

[36]  T. Hummel,et al.  Characterization of a novel Drosophila melanogaster galectin. Expression in developing immune, neural, and muscle tissues. , 2002, The Journal of biological chemistry.

[37]  John L. Wang,et al.  Intracellular functions of galectins. , 2002, Biochimica et biophysica acta.

[38]  D. Tenen,et al.  Molecular cloning and characterization of human eosinophil Charcot-Leyden crystal protein (lysophospholipase). Similarities to IgE binding proteins and the S-type animal lectin superfamily. , 1993, Journal of immunology.

[39]  Hans-Joachim Gabius,et al.  The sugar code: functional lectinomics. , 2002, Biochimica et biophysica acta.

[40]  H. Gabius,et al.  The 2.15 A crystal structure of CG-16, the developmentally regulated homodimeric chicken galectin. , 1999, Journal of molecular biology.

[41]  L. Yu,et al.  This information is current as Macrophages Chemoattractant for Monocytes and Human Galectin-3 Is a Novel , 2000 .

[42]  M. Hirashima,et al.  Characterization of the Xenopus Galectin Family , 2003, The Journal of Biological Chemistry.

[43]  K. Dyer,et al.  Eosinophil Charcot-Leyden crystal protein binds to beta-galactoside sugars. , 1996, Life sciences.

[44]  Victoria Prince,et al.  The Hox Paradox: More complex(es) than imagined. , 2002, Developmental biology.

[45]  A. Heck,et al.  Homodimeric galectin-7 (p53-induced gene 1) is a negative growth regulator for human neuroblastoma cells , 2003, Oncogene.

[46]  S. Barondes,et al.  X-ray Crystal Structure of the Human Galectin-3 Carbohydrate Recognition Domain at 2.1-Å Resolution* , 1998, The Journal of Biological Chemistry.

[47]  L. Amzel,et al.  Soluble β‐galactosyl‐binding lectin (galectin) from toad ovary: Crystallographic studies of two protein‐sugar complexes , 2000, Proteins.

[48]  S. Barondes,et al.  Galectins. Structure and function of a large family of animal lectins. , 1994, The Journal of biological chemistry.

[49]  S. Barondes,et al.  Galectins: a family of animal beta-galactoside-binding lectins. , 1994, Cell.

[50]  Martin Vingron,et al.  Modeling Amino Acid Replacement , 2000, J. Comput. Biol..

[51]  D. Larhammar,et al.  The human Hox-bearing chromosome regions did arise by block or chromosome (or even genome) duplications. , 2002, Genome research.

[52]  K. Kayser,et al.  Galectins-1 and -3 and their ligands in tumor biology , 1999, Journal of Cancer Research and Clinical Oncology.

[53]  B. Brenig,et al.  Construction of a 1.2-Mb BAC/PAC contig of the porcine gene RYR1 region on SSC 6q1.2 and comparative analysis with HSA 19q13.13. , 2002, Genomics.

[54]  G. Jarvis,et al.  Truncated galectin-3 inhibits tumor growth and metastasis in orthotopic nude mouse model of human breast cancer. , 2003, Clinical cancer research : an official journal of the American Association for Cancer Research.

[55]  S. Aparício,et al.  Vertebrate evolution: recent perspectives from fish. , 2000, Trends in genetics : TIG.

[56]  T. Magnaldo,et al.  Galectin-7, a marker of all types of stratified epithelia. , 1998, Differentiation; research in biological diversity.

[57]  H. Gabius Animal lectins and life: a guided tour into the realm of the sugar code , 2002 .

[58]  S. Barondes,et al.  Galectin-4 and Galectin-6 Are Two Closely Related Lectins Expressed in Mouse Gastrointestinal Tract* , 1998, The Journal of Biological Chemistry.

[59]  Douglas N W Cooper,et al.  Galectinomics: finding themes in complexity. , 2002, Biochimica et biophysica acta.

[60]  O Gascuel,et al.  BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data. , 1997, Molecular biology and evolution.

[61]  T. Yamane,et al.  Crystal structure of a conger eel galectin (congerin II) at 1.45A resolution: implication for the accelerated evolution of a new ligand-binding site following gene duplication. , 2002, Journal of molecular biology.