Transfaunation and Repair of Damage in the Rat Tapeworm, Hymenolepis diminuta

Goodchild, Chauncey G.

doi:10.2307/3274314

Cited by 22 publications

(11 citation statements)

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“…We established H. diminuta in vitro culture conditions modified from Schiller's method (Schiller, 1965) and tested the regeneration competence of 1 cm amputated fragments (Figure 1b–c). The anterior-most fragments (head+neck+body) were competent to regenerate, confirming in vivo observations using amputation and transplantation (Read, 1967; Goodchild, 1958). Anterior fragments that were first decapitated (neck+body) were also competent to regenerate.…”

Section: Resultssupporting

confidence: 82%

“…Although it was known that anterior fragments containing the head, neck, and immature proglottids could regenerate into fully mature tapeworms once transplanted into a rat intestine (Read, 1967; Goodchild, 1958), fragments lacking heads could not be tested for regenerative ability using transplantation. Attempts were made to suture H. diminuta fragments with mutilated or removed heads into a rat intestine but these fragments were invariably flushed out (Goodchild, 1958). Here we employ a robust in vitro culture system that allowed us to test regeneration of any amputated H. diminuta fragment for the first time.…”

Section: Discussionmentioning

confidence: 99%

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Region-specific regulation of stem cell-driven regeneration in tapeworms

Rozario

Quinn

Wang

et al. 2019

eLife

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Tapeworms grow at rates rivaling the fastest-growing metazoan tissues. To propagate they shed large parts of their body; to replace these lost tissues they regenerate proglottids (segments) as part of normal homeostasis. Their remarkable growth and regeneration are fueled by adult somatic stem cells that have yet to be characterized molecularly. Using the rat intestinal tapeworm, Hymenolepis diminuta, we find that regenerative potential is regionally limited to the neck, where head-dependent extrinsic signals create a permissive microenvironment for stem cell-driven regeneration. Using transcriptomic analyses and RNA interference, we characterize and functionally validate regulators of tapeworm growth and regeneration. We find no evidence that stem cells are restricted to the regeneration-competent neck. Instead, lethally irradiated tapeworms can be rescued when cells from either regeneration-competent or regeneration-incompetent regions are transplanted into the neck. Together, the head and neck tissues provide extrinsic cues that regulate stem cells, enabling region-specific regeneration in this parasite.

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Section: Resultssupporting

confidence: 82%

Section: Discussionmentioning

confidence: 99%

Region-specific regulation of stem cell-driven regeneration in tapeworms

Rozario

Quinn

Wang

et al. 2019

eLife

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“…1b-c). The anterior-most fragments (head+neck+body) were competent to regenerate, confirming in vivo observations using amputation and transplantation 5,19 . Anterior fragments that were first decapitated (neck+body) were also competent to regenerate.…”

Section: Resultssupporting

confidence: 82%

“…Although it was known that anterior fragments containing the head, neck, and immature proglottids could regenerate into fully mature tapeworms once transplanted into a rat intestine 5,19 , fragments lacking heads could not be tested for regenerative ability using transplantation. Attempts were made to suture H. diminuta fragments with mutilated or removed heads into a rat intestine but these fragments were invariably flushed out 19 . Here we employ a robust in vitro culture system that allowed us to test regeneration of any amputated H. diminuta fragment for the first time.…”

Section: Discussionmentioning

confidence: 99%

Region-specific regulation of stem cell-driven regeneration in tapeworms

Rozario

Quinn

Wang³

et al. 2018

Preprint

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15Tapeworms grow at rates rivaling the fastest-growing metazoan tissues. To propagate 16 they shed large parts of their body; to replace these lost tissues they regenerate proglottids 17 (segments) as part of normal homeostasis. Their remarkable growth and regeneration are fueled 18 by adult somatic stem cells that have yet to be characterized molecularly. Using the rat intestinal 19 tapeworm, Hymenolepis diminuta, we find that regenerative potential is regionally limited to the 20 neck, where head-dependent extrinsic signals create a permissive microenvironment for stem 21 cell-driven regeneration. Using transcriptomic analyses and RNA interference, we characterize 22 and functionally validate regulators of tapeworm growth and regeneration. We find no evidence 23 that stem cells are restricted to the regeneration-competent neck. Instead, lethally irradiated 24 tapeworms can be rescued when cells from either regeneration-competent or regeneration-25 incompetent regions are transplanted into the neck. Together, the head and neck tissues provide 26 extrinsic cues that regulate stem cells, enabling region-specific regeneration in this parasite. 27 7 Previous in vivo studies have shown that H. diminuta can regenerate after serial rounds of 103 amputation and transplantation for over a decade 5 and perhaps indefinitely. Using in vitro culture, 104we confirmed that anterior fragments of H. diminuta can regenerate after at least four rounds of 105 serial amputation ( Fig. 1f-g). Decapitated (-head) fragments regenerated proglottids after the first 106 amputation; however, re-amputation abrogated regeneration (Fig. 1f-g). After decapitation, a 107 definitive neck could not be maintained and eventually, the whole tissue was comprised of 108 proglottids ( Fig. 1-figure supplement 2). Without the head, proglottid regeneration from the neck 109 is finite. Thus, while the neck is necessary and sufficient for proglottid regeneration, the head is 110 required to maintain an unsegmented neck and for persistent regeneration. 111If signals from the head regulate regeneration, is regenerative potential asymmetric across 112 the anterior-posterior (A-P) axis of the neck? We subdivided the neck into three 1 mm fragments 113 and found that the most-anterior neck fragments regenerated more proglottids than the middle or 114 posterior neck fragments ( Fig. 1h-i). Thus, regeneration potential is asymmetric across the neck 115

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“…Holmes did not find any Chandler (1939) reported that Hymenolqvis diminuta underwent an anterior migration in the rat intestine, between 7 and 10 days postinfection. Similarly Goodchild (1958) showed that transfaunated scoleces of H. diminuta migrated anteriorly when surgically implanted in the posterior region of the intestine. This anterior migration of transplants has recently been confirmed by Braten and Hopkins (1969).…”

Section: Introductionmentioning

confidence: 97%

Changes in the distribution of Hymenolepis diminuta (Cestoda: Cyclophyllidea) within the rat intestine during prepatent development

Cannon¹,

Mettrick²

1970

Can. J. Zool.

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METTRICK. 1970. Changes in the distribution of Hymenolepis diminuta (Cestoda: Cyclophyllidea) within the rat intestine during prepatent development. The changes in the distribution of Hymenolepis diminuta within the rat intestine have been followed over the period 3 to 16 days postinfection using rats, each infected with 10 cysticercoids of H. diminuta, fed ad libitum on Purina Rat Chow.The parameters investigated were distribution of scolex attachment sites in the intestine, and distribution of parasite biomass in the intestine based on strobila length, ex vivo weight distribution, and in vivo weight distribution. Both the scoleces and biomass of 3-and 5:day-old worms are concentrated m the second quarter of the intestine. The mean scolex attachment point for 5-day-old worms was 39% of the total intestinal length behind the pyloric sphincter. Between days 5 and 7 there was a marked anterior migration of the young worms, so that at 7 days the mean scolex attachment.site was 15y0 of the total intestinal length behind the stomach. Over the same period of time the mean in vivo weight distribution moved forward from a point 44% behind the pyloric sphincter to one only 23% along the intestine. After 7 days there was a gradual posteriad spreading of the scolex attachment sites and of the parasite biomass. Hymenolepis diminuta can attach itself anywhere in the anterior 75% of the intestine, including in front of the opening of the bile duct: no worms were found in the small intestine extending back into the caecum.The pattern of migration and the changes in worm distribution in the intestine suggest that H. diminuta selects an appropriate, but changing position, on one or more of the gradients that have been demonstrated or postulated along the length of the small intestine.It is also suggested that the long-term migration during prepatent development is interrelated, but distinct from the daily migrational movements that H. diminuta undergoes within the small intestine.

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Transfaunation and Repair of Damage in the Rat Tapeworm, Hymenolepis diminuta

Cited by 22 publications

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Region-specific regulation of stem cell-driven regeneration in tapeworms

Region-specific regulation of stem cell-driven regeneration in tapeworms

Region-specific regulation of stem cell-driven regeneration in tapeworms

Changes in the distribution of Hymenolepis diminuta (Cestoda: Cyclophyllidea) within the rat intestine during prepatent development

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