Amylase gene structures in primates: retroposon insertions and promoter evolution

Abstract

Amylase transcription in the human salivary gland results from the evolutionary juxtaposition of two inserted elements, a gamma-actin pseudogene and an endogenous retrovirus, to create an unusual salivary-specific promoter. We utilized these structures as molecular tags to characterize the amylase genes in extant primates by polymerase chain reaction amplification of promoter fragments from genomic DNA. Six distinct amylase promoter structures were identified, which allowed us to infer the structures of common ancestors and trace the evolution of the modern human amylase promoters. Our data show that integration of the pseudogene and retrovirus were evolutionarily recent events. The gamma-actin pseudogene integrated after the divergence of the New World monkeys from the primate ancestral tree, and the retrovirus integrated later, after the divergence of the Old World monkeys. The New World monkey amylase promoter represents the mammalian amylase precursor structure before integration of the two retroposons. Two distinct amylase genes were identified in the Old World monkeys, one with a complete gamma-actin pseudogene insert and another novel structure with a truncation of the gamma-actin sequences. We demonstrated abundant amylase expression in the saliva of an Old World monkey, indicating that the endogenous retrovirus is not required for amylase transcription in the primate salivary gland.

Genomewide screening for fusogenic human endogenous retrovirus envelopes identifies syncytin 2, a gene conserved on primate evolution

“…Conservation of the fusogenic function is a strong hint for a functional role of the gene in the physiology of the host and suggests a selective process by which the retroviral gene function has been diverted by the host to its own benefit. Similar diversions have already been described for ''parasitic'' genes, with examples of retroviral promoters that confer novel tissue specificities to nearby cellular genes (38)(39)(40), and examples of coding sequences of retroviral origin that, in the mouse, confer resistance to infections by exogenous retroviruses (reviewed in ref. 15).…”

KRAB zinc finger proteins

“…TEs endow the genomes of their host species with binding sites for transcription factors, which can then contribute to species-restricted phenotypes (reviewed by Thompson et al, 2016). For instance, mammals generally produce amylase in the pancreas, yet primates can release this enzyme in saliva too, owing to the insertion upstream of the amylase coding sequence of a HERV-E LTR driving expression in the salivary glands (Samuelson et al, 1996;Ting et al, 1992). Many other cases of LTR promoter exaptation have been documented, generally resulting in new or altered tissue-specific gene expression (Cohen et al, 2009;Stavenhagen and Robins, 1988;Rebollo et al, 2012a).…”

Mammalian Endogenous Retroviruses

“…A listing of such cases is available (164) and some examples are mentioned here. Among the first well-documented cases of ERVderived genic enhancers are the human amylase loci, where a HERV-E LTR acts as a parotid-specific enhancer (165), and the sex-limited protein (slp) gene in mouse, which is hormone responsive due to an upstream androgen-response element within an LTR (166,167). Another well-studied case occurs in the human betaglobin gene cluster.…”