Cadherins in maternal–foetal interactions: red queen with a green beard?

Cadherins are homophilic cell surface adhesion proteins, some of which mediate interactions between maternal and foetal tissues during mammalian pregnancy. David Haig suggested that these proteins may exhibit ‘green-beard gene’ effects, whereby the nature of binding between identical alleles in mother and foetus leads to differential levels of resource transfer. The selfish effects of such self-recognizing alleles should, however, be suppressed over evolutionary time by unlinked genes, which is expected to lead to antagonistic coevolution between placentally expressed cadherins and unlinked modifiers. Such molecular coevolution should leave a signature of positive selection, with high ratios of non-synonymous to synonymous amino acid substitution. We present evidence that three placentally expressed cadherin genes, E-cadherin, P-cadherin and VE-cadherin, have been subject to positive selection. By contrast, a ‘control’ cadherin that is not expressed in the placenta, H-cadherin, showed no evidence of selection. These results provide support for the hypothesis that the cadherin genes involved in maternal–foetal interactions have been subject to green-beard-effect mutations over the course of evolutionary history, leading to antagonistic coevolution with suppressing elements from the parliament of genes.

[1]  W. Hamilton.  The genetical evolution of social behaviour. I. , 1964, Journal of theoretical biology.

[2]  Wd Hamilton,et al.  The genetical theory of social behaviour. I, II , 1964 .

[3]  E. Leigh,et al.  Adaptation and diversity , 1971 .

[4]  R. Lewontin.  ‘The Selfish Gene’ , 1977, Nature.

[5]  G. Borgia,et al.  Group Selection, Altruism, and the Levels of Organization of Life , 1978 .

[6]  F. Jacob,et al.  A cell surface glycoprotein involved in the compaction of embryonal carcinoma cells and cleavage stage embryos , 1980, Cell.

[7]  Alan Grafen,et al.  Are green beard genes outlaws? , 1981, Animal Behaviour.

[8]  G. Edelman,et al.  Characterization of L-CAM, a major cell adhesion molecule from embryonic liver cells. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[9]  D. Queller,et al.  Kin selection and frequency dependence: a game theoretic approach , 1984 .

[10]  A. Nose,et al.  A novel cadherin cell adhesion molecule: its expression patterns associated with implantation and organogenesis of mouse embryos , 1986, The Journal of cell biology.

[11]  M. Ringwald,et al.  Molecular cloning of the mouse cell adhesion molecule uvomorulin: cDNA contains a B1-related sequence. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[12]  G. Edelman,et al.  Cellular expression of liver and neural cell adhesion molecules after transfection with their cDNAs results in specific cell-cell binding. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[13]  T. Guilford.  The Evolution of Conspicuous Coloration , 1988, American Naturalist.

[14]  G. Edelman,et al.  Cell sorting-out is modulated by both the specificity and amount of different cell adhesion molecules (CAMs) expressed on cell surfaces. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[15]  O. Blaschuk,et al.  Identification of a cadherin cell adhesion recognition sequence. , 1990, Developmental biology.

[16]  M. Takeichi,et al.  Cadherin cell adhesion receptors as a morphogenetic regulator. , 1991, Science.

[17]  Chris Graham,et al.  Genomic imprinting and the strange case of the insulin-like growth factor II receptor , 1991, Cell.

[18]  D. Haig,et al.  Genetic Conflicts in Human Pregnancy , 1993, The Quarterly Review of Biology.

[19]  B. Parr,et al.  The body language of cells: The intimate connection between cell adhesion and behavior , 1995, Cell.

[20]  Peter D. Kwong,et al.  Structural basis of cell-cell adhesion by cadherins , 1995, Nature.

[21]  M. Seif,et al.  Cell adhesion molecules on the oocyte and preimplantation human embryo. , 1995, Human reproduction.

[22]  W. Hendrickson,et al.  Considerations on the folding topology and evolutionary origin of cadherin domains. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[23]  M. Ikura,et al.  Solution structure of the epithelial cadherin domain responsible for selective cell adhesion , 1995, Science.

[24]  D. Haig,et al.  Gestational drive and the green-bearded placenta. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[25]  D. Haig,et al.  Altercation of Generations: Genetic Conflicts of Pregnancy , 1996, American journal of reproductive immunology.

[26]  Roderic D. M. Page,et al.  TreeView: an application to display phylogenetic trees on personal computers , 1996, Comput. Appl. Biosci..

[27]  M. Ikura,et al.  Structural basis of calcium-induced E-cadherin rigidification and dimerization , 1996, Nature.

[28]  E. Furth,et al.  Regulated expression of cadherin‐11 in human epithelial cells: A role for cadherin‐11 in trophoblast‐endometrium interactions? , 1996, Developmental dynamics : an official publication of the American Association of Anatomists.

[29]  Mitsuhiko Ikura,et al.  Structural basis of calcium-induced E-cadherin rigidification and dimerization , 1996 .

[30]  J. Engel,et al.  Homophilic adhesion of E‐cadherin occurs by a co‐operative two‐step interaction of N‐terminal domains. , 1996, The EMBO journal.

[31]  L. Hurst,et al.  Genetic Conflicts , 1996, The Quarterly Review of Biology.

[32]  Thomas L. Madden,et al.  Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. , 1997, Nucleic acids research.

[33]  Ziheng Yang,et al.  PAML: a program package for phylogenetic analysis by maximum likelihood , 1997, Comput. Appl. Biosci..

[34]  E. Dejana,et al.  Human cytotrophoblasts adopt a vascular phenotype as they differentiate. A strategy for successful endovascular invasion? , 1997, The Journal of clinical investigation.

[35]  D. Haig.  Parental antagonism, relatedness asymmetries, and genomic imprinting , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[36]  R. Nielsen,et al.  Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. , 1998, Genetics.

[37]  W. Gallin.  Evolution of the "classical" cadherin family of cell adhesion molecules in vertebrates. , 1998, Molecular biology and evolution.

[38]  L. Keller,et al.  Selfish genes: a green beard in the red fire ant , 1998, Nature.

[39]  O. Pertz,et al.  A new crystal structure, Ca2+ dependence and mutational analysis reveal molecular details of E‐cadherin homoassociation , 1999, The EMBO journal.

[40]  S K Das,et al.  Zonula occludens-1 and E-cadherin are coordinately expressed in the mouse uterus with the initiation of implantation and decidualization. , 1999, Developmental biology.

[41]  C. Maccalman,et al.  Regulation of beta-catenin mRNA and protein levels in human villous cytotrophoblasts undergoing aggregation and fusion in vitro: correlation with E-cadherin expression. , 2000, Journal of reproduction and fertility.

[42]  L. Sunde,et al.  Localization of E-cadherin in villous, extravillous and vascular trophoblasts during intrauterine, ectopic and molar pregnancy. , 2000, Molecular human reproduction.

[43]  Ziheng Yang,et al.  Statistical methods for detecting molecular adaptation , 2000, Trends in Ecology & Evolution.

[44]  D. Haig.  The Kinship Theory of Genomic Imprinting , 2000 .

[45]  M. Ilyas.  Adhesion molecule expression in breast cancer: the phoenix in tumour metastasis? , 2000, The Journal of pathology.

[46]  N. Goldman,et al.  Codon-substitution models for heterogeneous selection pressure at amino acid sites. , 2000, Genetics.

[47]  M. P. Cummings,et al.  PAUP* Phylogenetic analysis using parsimony (*and other methods) Version 4 , 2000 .

[48]  F. van Roy,et al.  Phylogenetic analysis of the cadherin superfamily allows identification of six major subfamilies besides several solitary members. , 2000, Journal of molecular biology.

[49]  Ziheng Yang,et al.  Adaptive Molecular Evolution , 2004, Handbook of Statistical Genomics.

[50]  Z. Yang,et al.  Accuracy and power of the likelihood ratio test in detecting adaptive molecular evolution. , 2001, Molecular biology and evolution.

[51]  D. Swofford.  PAUP*: Phylogenetic analysis using parsimony (*and other methods), Version 4.0b10 , 2002 .

[52]  Joseph P Bielawski,et al.  Accuracy and power of bayes prediction of amino acid sites under positive selection. , 2002, Molecular biology and evolution.

[53]  I. Shih,et al.  The Role of E-cadherin in the Motility and Invasion of Implantation Site Intermediate Trophoblast. , 2002, Placenta.

[54]  S. Carroll,et al.  Evolution of Key Cell Signaling and Adhesion Protein Families Predates Animal Origins , 2003, Science.

[55]  J. Strassmann,et al.  Single-Gene Greenbeard Effects in the Social Amoeba Dictyostelium discoideum , 2003, Science.

[56]  Pang Zj,et al.  Expression profile of trophoblast invasion-associated genes in the pre-eclamptic placenta. , 2003 .

[57]  F. Xing,et al.  Expression profile of trophoblast invasion-associated genes in the pre-eclamptic placenta , 2003, British journal of biomedical science.

[58]  M. Feldman,et al.  Extensive linkage disequilibrium, a common 16.7-kilobase deletion, and evidence of balancing selection in the human protocadherin alpha cluster. , 2003, American journal of human genetics.

[59]  S. Hirohashi,et al.  Cell adhesion system and human cancer morphogenesis , 2003, Cancer science.

[60]  B. Crespi,et al.  Social Slime Molds Meet Their Match , 2003, Science.

[61]  Anders Gorm Pedersen,et al.  RevTrans: multiple alignment of coding DNA from aligned amino acid sequences , 2003, Nucleic Acids Res..

[62]  Keith R. Johnson,et al.  Cadherins as modulators of cellular phenotype. , 2003, Annual review of cell and developmental biology.

[63]  Michael P. Cummings,et al.  PAUP* [Phylogenetic Analysis Using Parsimony (and Other Methods)] , 2004 .

[64]  B. Crespi,et al.  Parent‐Offspring Conflict in the Evolution of Vertebrate Reproductive Mode , 2004, The American Naturalist.

[65]  M. Stanhope,et al.  Molecules consolidate the placental mammal tree. , 2004, Trends in ecology & evolution.

[66]  D. Balding,et al.  Handbook of statistical genetics , 2004 .

[67]  J. Gordon,et al.  Targeting and crossing of the human maternofetal barrier by Listeria monocytogenes: role of internalin interaction with trophoblast E-cadherin. , 2004, Proceedings of the National Academy of Sciences of the United States of America.