Differential temporal expression of milk miRNA during the lactation cycle of the marsupial tammar wallaby (Macropus eugenii)

Abstract

BackgroundLactation is a key aspect of mammalian evolution for adaptation of various reproductive strategies along different mammalian lineages. Marsupials, such as tammar wallaby, adopted a short gestation and a relatively long lactation cycle, the newborn is immature at birth and significant development occurs postnatally during lactation. Continuous changes of tammar milk composition may contribute to development and immune protection of pouch young. Here, in order to address the putative contribution of newly identified secretory milk miRNA in these processes, high throughput sequencing of miRNAs collected from tammar milk at different time points of lactation was conducted. A comparative analysis was performed to find distribution of miRNA in milk and blood serum of lactating wallaby.ResultsResults showed that high levels of miRNA secreted in milk and allowed the identification of differentially expressed milk miRNAs during the lactation cycle as putative markers of mammary gland activity and functional candidate signals to assist growth and timed development of the young. Comparative analysis of miRNA distribution in milk and blood serum suggests that milk miRNAs are primarily expressed from mammary gland rather than transferred from maternal circulating blood, likely through a new putative exosomal secretory pathway. In contrast, highly expressed milk miRNAs could be detected at significantly higher levels in neonate blood serum in comparison to adult blood, suggesting milk miRNAs may be absorbed through the gut of the young.ConclusionThe function of miRNA in mammary gland development and secretory activity has been proposed, but results from the current study also support a differential role of milk miRNA in regulation of development in the pouch young, revealing a new potential molecular communication between mother and young during mammalian lactation.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-1012) contains supplementary material, which is available to authorized users.

Milk MicroRNAs in Health and Disease

“…MicroRNAs have not only been found in human milk but also in milk from other mammals, including cows (Chen et al., ; Li, Liu, Jin, Lo, & Liu, ), pigs (Gu et al., ), mice (Title, Denzler, & Stoffel, ), rats (Izumi et al., ), goats (Hou et al., ), wallabies (Modepalli et al., ), dromedaries (Yassin, Abdel Hamid, Farid, Amer, & Warda, ), and pandas (Ma et al., ), in an ever‐increasing list of species.…”

“…Nevertheless, the conservation of the microRNAs between pups and mothers did not allow to discriminate between microRNAs transferred by the diet and those endogenously synthetized by the piglet in response to differential feeding (Gu et al., ). In wallaby, microRNAs usually associated with lactation were highly expressed in the newborns only fed with milk (Modepalli et al., ).…”

“…The majority of studies have only investigated this matter in silico using microRNA‐target identification tools and associated pathways/gene ontology analysis (Alsaweed et al., , ; Cai et al., , ; Carney et al., ; Chen et al., , , ; Chokeshaiusaha, Sananmuang, Puthier, & Nguyen, ; Do, Li, Dudemaine, & Ibeagha‐Awemu, ; Golan‐Gerstl, Elbaum Shiff, et al., ; Gu et al., , ; Hou et al., ; Kang et al., ; Li et al., , ; Liao et al., ; Liu et al., ; Lukasik & Zielenkiewicz, ; Modepalli et al., ; Munch et al., ; Shen et al., ; Simpson et al., ; Sun et al., ; Wang et al., ; Zhang et al., ; Zhou et al., ).…”

Changeover from signalling to energy-provisioning lipids during transition from colostrum to mature milk in the giant panda (Ailuropoda melanoleuca)

“…The term “external gestation” was originally applied to marsupials because they produce neonates of extraordinary altriciality following a very short gestation, and exhibit dramatic alterations in milk components with time575960 that may serve to provide nutrients required for early development that eutherians provide in utero .…”

Rapid changes in Atlantic grey seal milk from birth to desertion

“…This prolonged transition time may be associated with the altriciality of panda neonates, which is the most extreme known amongst eutherians, though not as pronounced as in marsupials [15,16].…”