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Review
. 2013 Mar 8;288(10):6904-11.
doi: 10.1074/jbc.R112.424523. Epub 2013 Jan 17.

Glycan evolution in response to collaboration, conflict, and constraint

Stevan A Springer  1 , Pascal Gagneux
Affiliations
Review

Glycan evolution in response to collaboration, conflict, and constraint

Stevan A Springer et al. J Biol Chem. .

Abstract

Glycans, oligo- and polysaccharides secreted or attached to proteins and lipids, cover the surfaces of all cells and have a regulatory capacity and structural diversity beyond any other class of biological molecule. Glycans may have evolved these properties because they mediate cellular interactions and often face pressure to evolve new functions rapidly. We approach this idea two ways. First, we discuss evolutionary innovation. Glycan synthesis, regulation, and mode of chemical interaction influence the spectrum of new forms presented to evolution. Second, we describe the evolutionary conflicts that arise when alleles and individuals interact. Glycan regulation and diversity are integral to these biological negotiations. Glycans are tasked with such an amazing diversity of functions that no study of cellular interaction can begin without considering them. We propose that glycans predominate the cell surface because their physical and chemical properties allow the rapid innovation required of molecules on the frontlines of evolutionary conflict.

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Figures

FIGURE 1.
FIGURE 1.
Evolutionary conflicts between alleles and individuals. For single allele-single individual, single alleles conflict with themselves when their positive effects in one context cause negative effects in another. Selectins on epithelial cells bind glycans on leukocytes and guide them to sites of inflammation; this can also be exploited by cancer cells (72). Regulatory or functional changes that separate conflicting tasks are expected to evolve in response. For single allele-multiple individuals, conflicts can extend across individuals that share an allele. Females that lack Neu5Gc raise antibodies against it. Males that lack Neu5Gc have higher rates of fertilization, and females have lower rates (14). Individual-specific regulation could resolve these conflicts. For multiple genes-single individual, selfish alleles can bias reproduction in their favor at the cost of individual reproduction, causing conflict with other genes in the genome. Mutant PMM2 alleles are passed to children more often than expected but increase the risk of congenital disorders of glycosylation (79). Other genes are selected to suppress the selfish allele, often by modification of chromosomal recombination and linkage. For multiple genes-multiple individuals, molecular markers of self cause cells to direct benefits toward identical genetic relatives, but they can be exploited by pathogen mimics. Co-evolution is a common outcome, as hosts develop more reliable markers of self, and pathogens develop more effective molecular mimics (8, 86).
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