Transcriptomic analysis supports similar functional roles for the two thymuses of the tammar wallaby

Abstract

BackgroundThe thymus plays a critical role in the development and maturation of T-cells. Humans have a single thoracic thymus and presence of a second thymus is considered an anomaly. However, many vertebrates have multiple thymuses. The tammar wallaby has two thymuses: a thoracic thymus (typically found in all mammals) and a dominant cervical thymus. Researchers have known about the presence of the two wallaby thymuses since the 1800s, but no genome-wide research has been carried out into possible functional differences between the two thymic tissues. Here, we used pyrosequencing to compare the transcriptomes of a cervical and thoracic thymus from a single 178 day old tammar wallaby.ResultsWe show that both the tammar thoracic and the cervical thymuses displayed gene expression profiles consistent with roles in T-cell development. Both thymuses expressed genes that mediate distinct phases of T-cells differentiation, including the initial commitment of blood stem cells to the T-lineage, the generation of T-cell receptor diversity and development of thymic epithelial cells. Crucial immune genes, such as chemokines were also present. Comparable patterns of expression of non-coding RNAs were seen. 67 genes differentially expressed between the two thymuses were detected, and the possible significance of these results are discussed.ConclusionThis is the first study comparing the transcriptomes of two thymuses from a single individual. Our finding supports that both thymuses are functionally equivalent and drive T-cell development. These results are an important first step in the understanding of the genetic processes that govern marsupial immunity, and also allow us to begin to trace the evolution of the mammalian immune system.

The development of the immune tissues in marsupial pouch young

“…In marsupials with both types of thymus, the tissues appear to be histologically identical and to have the same function, but the cervical thymus is larger, and development of the thoracic thymus lags behind that of the cervical thymus (Stanley et al, ). Consistent with previous reports that in those animals that possess both cervical and thoracic thymi these tissues have identical histology and function, Wong et al () reported that the transcriptome of the cervical and thoracic thymus of the tammar wallaby both display gene expression profiles that are consistent with their roles in T‐cell development and provides further evidence that the two thymi are functionally equivalent and both drive T‐cell development. Further, all major TCR classes were expressed in both thymi, as well as RAG‐1 and RAG‐2 transcripts (Wong et al, ), genes that are involved in the rearrangement and recombination of T‐cell receptors and immunoglobulin molecules.…”

On the prenatal initiation of T cell development in the opossum Monodelphis domestica

“…In these species the cervical thymus matures earlier in postnatal development than the thoracic thymus, and the two thymuses appear to be functionally redundant (Stanley et al 1972; Ashman et al 1977; Basden et al 1996; Wong et al 2011; Duncan et al 2012). Previous attempts to detect the initiation of T cell development in perinatal Australasian marsupials have not been fruitful.…”

Marsupials and monotremes possess a novel family of MHC class I genes that is lost from the eutherian lineage

“…To find support for the expression of UTs in several marsupials, sequencing data from the following immune tissue cDNA or Expressed Sequence Tag (EST) libraries were searched: Roche 454 sequencing data from tammar wallaby, Macropus eugenii , thoracic and cervical thymus cDNA libraries [GenBank:SRX019250,SRX019249] [ 41 ]; Roche 454 sequencing data from Tasmanian devil, Sarcophilus harisii , spleen and lymph node cDNA libraries [EMBL:PRJEB7940]; Roche 454 sequencing data from the opossum, Monodelphis domestica , thymus cDNA libraries (Katina Krasnec and Robert Miller, unpublished data); 17,818 ESTs from brushtail possum, Trichosurus vulpecula, spleen, lymph node and stimulated splenocytes [GenBank:LIBEST_019237]; and a small set of 1319 ESTs from a northern brown bandicoot, Isoodon macrourus, thymus ESTs [GenBank:EE743888-EE745206] [ 42 ].…”