Emergence of hormonal and redox regulation of galectin-1 in placental mammals: Implication in maternal-fetal immune tolerance
Galectin-1 is an anti-inflammatory lectin with pleiotropic regulatory functions at the crossroads of innate and adaptive immunity. It is expressed in immune privileged sites and is implicated in establishing maternal-fetal immune tolerance, which is essential for successful pregnancy in eutherian ma...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2008-10, Vol.105 (41), p.15819-15824 |
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| creator | Than, Nandor Gabor Romero, Roberto Erez, Offer Weckle, Amy Tarca, Adi L Hotra, John Abbas, Asad Han, Yu Mi Kim, Sung-Su Kusanovic, Juan Pedro Gotsch, Francesca Hou, Zhuocheng Santolaya-Forgas, Joaquin Benirschke, Kurt Papp, Zoltan Grossman, Lawrence I Goodman, Morris Wildman, Derek E |
| description | Galectin-1 is an anti-inflammatory lectin with pleiotropic regulatory functions at the crossroads of innate and adaptive immunity. It is expressed in immune privileged sites and is implicated in establishing maternal-fetal immune tolerance, which is essential for successful pregnancy in eutherian mammals. Here, we show conserved placental localization of galectin-1 in primates and its predominant expression in maternal decidua. Phylogenetic footprinting and shadowing unveil conserved cis motifs, including an estrogen responsive element in the 5' promoter of LGALS1, that were gained during the emergence of placental mammals and could account for sex steroid regulation of LGALS1 expression, thus providing additional evidence for the role of galectin-1 in immune-endocrine cross-talk. Maximum parsimony and maximum likelihood analyses of 27 publicly available vertebrate and seven newly sequenced primate LGALS1 coding sequences reveal that intense purifying selection has been acting on residues in the carbohydrate recognition domain and dimerization interface that are involved in immune functions. Parsimony- and codon model-based phylogenetic analysis of coding sequences show that amino acid replacements occurred in early mammalian evolution on key residues, including gain of cysteines, which regulate immune functions by redox status-mediated conformational changes that disable sugar binding and dimerization, and that the acquired immunoregulatory functions of galectin-1 then became highly conserved in eutherian lineages, suggesting the emergence of hormonal and redox regulation of galectin-1 in placental mammals may be implicated in maternal-fetal immune tolerance. |
| doi_str_mv | 10.1073/pnas.0807606105 |
| format | Article |
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It is expressed in immune privileged sites and is implicated in establishing maternal-fetal immune tolerance, which is essential for successful pregnancy in eutherian mammals. Here, we show conserved placental localization of galectin-1 in primates and its predominant expression in maternal decidua. Phylogenetic footprinting and shadowing unveil conserved cis motifs, including an estrogen responsive element in the 5' promoter of LGALS1, that were gained during the emergence of placental mammals and could account for sex steroid regulation of LGALS1 expression, thus providing additional evidence for the role of galectin-1 in immune-endocrine cross-talk. Maximum parsimony and maximum likelihood analyses of 27 publicly available vertebrate and seven newly sequenced primate LGALS1 coding sequences reveal that intense purifying selection has been acting on residues in the carbohydrate recognition domain and dimerization interface that are involved in immune functions. Parsimony- and codon model-based phylogenetic analysis of coding sequences show that amino acid replacements occurred in early mammalian evolution on key residues, including gain of cysteines, which regulate immune functions by redox status-mediated conformational changes that disable sugar binding and dimerization, and that the acquired immunoregulatory functions of galectin-1 then became highly conserved in eutherian lineages, suggesting the emergence of hormonal and redox regulation of galectin-1 in placental mammals may be implicated in maternal-fetal immune tolerance.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.0807606105</identifier><identifier>PMID: 18824694</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Amino acids ; Animals ; Biological Evolution ; Biological Sciences ; Cells ; Computational Biology ; Databases, Nucleic Acid ; Dimerization ; Evolution ; Female ; Galectin 1 - genetics ; Galectin 1 - metabolism ; Gene expression ; Gene Expression Regulation - immunology ; Gene Expression Regulation - physiology ; Genetics ; Gonadal Steroid Hormones - physiology ; Hormones ; Humans ; Immune Tolerance ; Immunology ; Mammals ; Maternal-Fetal Exchange - immunology ; Molecular Sequence Data ; Oxidation-Reduction ; Phylogenetics ; Phylogeny ; Placenta ; Placenta - metabolism ; Pregnancy ; Primates ; T lymphocytes ; Vertebrates</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2008-10, Vol.105 (41), p.15819-15824</ispartof><rights>Copyright 2008 The National Academy of Sciences of the United States of America</rights><rights>Copyright National Academy of Sciences Oct 14, 2008</rights><rights>2008 by The National Academy of Sciences of the USA</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c620t-7797ab2a12957727583cde5255c5f4533279d32b278e543a8347f9ca8ed3eeb63</citedby><cites>FETCH-LOGICAL-c620t-7797ab2a12957727583cde5255c5f4533279d32b278e543a8347f9ca8ed3eeb63</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/105/41.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/25464499$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/25464499$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,727,780,784,803,885,27924,27925,53791,53793,58017,58250</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/18824694$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Than, Nandor Gabor</creatorcontrib><creatorcontrib>Romero, Roberto</creatorcontrib><creatorcontrib>Erez, Offer</creatorcontrib><creatorcontrib>Weckle, Amy</creatorcontrib><creatorcontrib>Tarca, Adi L</creatorcontrib><creatorcontrib>Hotra, John</creatorcontrib><creatorcontrib>Abbas, Asad</creatorcontrib><creatorcontrib>Han, Yu Mi</creatorcontrib><creatorcontrib>Kim, Sung-Su</creatorcontrib><creatorcontrib>Kusanovic, Juan Pedro</creatorcontrib><creatorcontrib>Gotsch, Francesca</creatorcontrib><creatorcontrib>Hou, Zhuocheng</creatorcontrib><creatorcontrib>Santolaya-Forgas, Joaquin</creatorcontrib><creatorcontrib>Benirschke, Kurt</creatorcontrib><creatorcontrib>Papp, Zoltan</creatorcontrib><creatorcontrib>Grossman, Lawrence I</creatorcontrib><creatorcontrib>Goodman, Morris</creatorcontrib><creatorcontrib>Wildman, Derek E</creatorcontrib><title>Emergence of hormonal and redox regulation of galectin-1 in placental mammals: Implication in maternal-fetal immune tolerance</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Galectin-1 is an anti-inflammatory lectin with pleiotropic regulatory functions at the crossroads of innate and adaptive immunity. It is expressed in immune privileged sites and is implicated in establishing maternal-fetal immune tolerance, which is essential for successful pregnancy in eutherian mammals. Here, we show conserved placental localization of galectin-1 in primates and its predominant expression in maternal decidua. Phylogenetic footprinting and shadowing unveil conserved cis motifs, including an estrogen responsive element in the 5' promoter of LGALS1, that were gained during the emergence of placental mammals and could account for sex steroid regulation of LGALS1 expression, thus providing additional evidence for the role of galectin-1 in immune-endocrine cross-talk. Maximum parsimony and maximum likelihood analyses of 27 publicly available vertebrate and seven newly sequenced primate LGALS1 coding sequences reveal that intense purifying selection has been acting on residues in the carbohydrate recognition domain and dimerization interface that are involved in immune functions. Parsimony- and codon model-based phylogenetic analysis of coding sequences show that amino acid replacements occurred in early mammalian evolution on key residues, including gain of cysteines, which regulate immune functions by redox status-mediated conformational changes that disable sugar binding and dimerization, and that the acquired immunoregulatory functions of galectin-1 then became highly conserved in eutherian lineages, suggesting the emergence of hormonal and redox regulation of galectin-1 in placental mammals may be implicated in maternal-fetal immune tolerance.</description><subject>Amino acids</subject><subject>Animals</subject><subject>Biological Evolution</subject><subject>Biological Sciences</subject><subject>Cells</subject><subject>Computational Biology</subject><subject>Databases, Nucleic Acid</subject><subject>Dimerization</subject><subject>Evolution</subject><subject>Female</subject><subject>Galectin 1 - genetics</subject><subject>Galectin 1 - metabolism</subject><subject>Gene expression</subject><subject>Gene Expression Regulation - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Than, Nandor Gabor</au><au>Romero, Roberto</au><au>Erez, Offer</au><au>Weckle, Amy</au><au>Tarca, Adi L</au><au>Hotra, John</au><au>Abbas, Asad</au><au>Han, Yu Mi</au><au>Kim, Sung-Su</au><au>Kusanovic, Juan Pedro</au><au>Gotsch, Francesca</au><au>Hou, Zhuocheng</au><au>Santolaya-Forgas, Joaquin</au><au>Benirschke, Kurt</au><au>Papp, Zoltan</au><au>Grossman, Lawrence I</au><au>Goodman, Morris</au><au>Wildman, Derek E</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Emergence of hormonal and redox regulation of galectin-1 in placental mammals: Implication in maternal-fetal immune tolerance</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2008-10-14</date><risdate>2008</risdate><volume>105</volume><issue>41</issue><spage>15819</spage><epage>15824</epage><pages>15819-15824</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><abstract>Galectin-1 is an anti-inflammatory lectin with pleiotropic regulatory functions at the crossroads of innate and adaptive immunity. 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Parsimony- and codon model-based phylogenetic analysis of coding sequences show that amino acid replacements occurred in early mammalian evolution on key residues, including gain of cysteines, which regulate immune functions by redox status-mediated conformational changes that disable sugar binding and dimerization, and that the acquired immunoregulatory functions of galectin-1 then became highly conserved in eutherian lineages, suggesting the emergence of hormonal and redox regulation of galectin-1 in placental mammals may be implicated in maternal-fetal immune tolerance.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>18824694</pmid><doi>10.1073/pnas.0807606105</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Amino acids Animals Biological Evolution Biological Sciences Cells Computational Biology Databases, Nucleic Acid Dimerization Evolution Female Galectin 1 - genetics Galectin 1 - metabolism Gene expression Gene Expression Regulation - immunology Gene Expression Regulation - physiology Genetics Gonadal Steroid Hormones - physiology Hormones Humans Immune Tolerance Immunology Mammals Maternal-Fetal Exchange - immunology Molecular Sequence Data Oxidation-Reduction Phylogenetics Phylogeny Placenta Placenta - metabolism Pregnancy Primates T lymphocytes Vertebrates |
| title | Emergence of hormonal and redox regulation of galectin-1 in placental mammals: Implication in maternal-fetal immune tolerance |
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