Stem cell heterogeneity drives the parasitic life cycle of Schistosoma mansoni

Wang, Bo; Lee, Jayhun; Li, Pengyang; Saberi, Amir; Yang, Haifeng; Liu, Chang; Zhao, Minglei; Newmark, Phillip A.

doi:10.7554/elife.35449

Cited by 76 publications

(223 citation statements)

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“…Recently, it was shown that schistosomula carry two types of stem cell populations: somatic stem cells and germinal cells 15 . The somatic stem cells are involved in somatic tissue differentiation and homeostasis during the parasite intra-mammalian development, whereas the germinal cells are presumed to give rise to germ cells (sperm and oocytes) in adult parasites 15 . Less than 24 hours after the cercaria enters the mammalian host to become schistosomulum, ~5 somatic stem cells at distinct locations begin to proliferate 15 (Figure 5B).…”

Section: Resultsmentioning

confidence: 99%

“…The somatic stem cells are involved in somatic tissue differentiation and homeostasis during the parasite intra-mammalian development, whereas the germinal cells are presumed to give rise to germ cells (sperm and oocytes) in adult parasites 15 . Less than 24 hours after the cercaria enters the mammalian host to become schistosomulum, ~5 somatic stem cells at distinct locations begin to proliferate 15 (Figure 5B). Germinal cells, on the other hand, are thought to be packaged in a distinct anatomical location called the germinal cell cluster, and only begin to proliferate ~ 1 week after penetrating the host 15 .…”

Section: Resultsmentioning

confidence: 99%

“…Less than 24 hours after the cercaria enters the mammalian host to become schistosomulum, ~5 somatic stem cells at distinct locations begin to proliferate 15 (Figure 5B). Germinal cells, on the other hand, are thought to be packaged in a distinct anatomical location called the germinal cell cluster, and only begin to proliferate ~ 1 week after penetrating the host 15 .…”

Section: Resultsmentioning

confidence: 99%

“…We identified a single stem/germinal cell cluster that expressed the canonical cell cycle markers histone h2a (Smp_086860) 15 and histone h2b (Smp_108390) 6 (Figure 5A). In addition, this cluster also had a significant enrichment of translational components (Supplementary Figure 1C).…”

Section: Resultsmentioning

confidence: 99%

“…Dramatic changes to the parasite are required that include posterior growth, remodelling of the musculature 9 and nervous system 10,11 as well as the development of the gonads 12 and gut 13 . This extensive tissue development starts in the schistosomula, with stem cells driving these transitions 6,14,15 . However, to decipher cellular and molecular mechanisms underlying schistosomula development, a detailed understanding of the spatial organisation and transcriptional programs of individual cells are needed.…”

Section: Introductionmentioning

confidence: 99%

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Single-cell atlas of the first intra-mammalian developmental stage of the human parasite Schistosoma mansoni

Soria

Lee

Chong

et al. 2019

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17Over 250 million people suffer from schistosomiasis, a tropical disease caused by parasitic 18 flatworms known as schistosomes. Humans become infected by free-swimming, water-borne 19 larvae, which penetrate the skin. The earliest intra-mammalian stage, called the 20 schistosomulum, undergoes a series of developmental transitions. These changes are critical 21 for the parasite to adapt to its new environment as it navigates through host tissues to reach its 22 niche, where it will grow to reproductive maturity. Unravelling the mechanisms that drive 23 intra-mammalian development requires knowledge of the spatial organisation and 24 transcriptional dynamics of different cell types that comprise the schistomulum body. To fill 25 these important knowledge gaps, we performed single-cell RNA sequencing on two-day old 26 schistosomula of Schistosoma mansoni. We identified likely gene expression profiles for 27 muscle, nervous system, tegument, parenchymal/primordial gut cells, and stem cells. In 28 addition, we validated cell markers for all these clusters by in situ hybridisation in 29 schistosomula and adult parasites. Taken together, this study provides a comprehensive cell-30 type atlas for the early intra-mammalian stage of this devastating metazoan parasite. 31 32 the parasite to survive for decades 5,6 . The schistosomula make their way into blood or 51 lymphatic vessels and, one week after infection, reach the lung capillaries 7 . The migration 52 through the lung requires coordinated neuromuscular activities, including cycles of muscle 53 elongation and contraction 8 , to squeeze through capillaries and reach the general circulation 7 . 54Over the following weeks, the parasites mature further into sexually reproducing adults. 55Dramatic changes to the parasite are required that include posterior growth, remodelling of the 56 musculature 9 and nervous system 10,11 as well as the development of the gonads 12 and gut 13 . 57This extensive tissue development starts in the schistosomula, with stem cells driving these 58 transitions 6,14,15 . However, to decipher cellular and molecular mechanisms underlying 59 schistosomula development, a detailed understanding of the spatial organisation and 60 transcriptional programs of individual cells are needed. 61 Important insights into major processes that underlie the transformations across the life cycle 62 have been gained from bulk transcriptomic studies 5,6,14-24 . However, these studies are not able 63 to quantify the relative abundance of different cell types from the absolute expression per cell, 64 and the signal from highly expressed genes in a minority of cells can often be masked by a 65 population averaging effect. Single-cell RNA sequencing has previously been used 66 successfully to characterise cell types [25][26][27][28][29][30][31][32] and understand how the cell expression profile 67 changes during differentiation 31-38 . Notable examples include recent studies in the free-living 68 planarian flatworm Schmidtea mediterranea 31,32,39 , a well-establishe...

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Section: Resultsmentioning

confidence: 99%