TY - JOUR
T1 - Toll signalling promotes blastema cell proliferation during cricket leg regeneration via insect macrophages
AU - Bando, Tetsuya
AU - Okumura, Misa
AU - Bando, Yuki
AU - Hagiwara, Marou
AU - Hamada, Yoshimasa
AU - Ishimaru, Yoshiyasu
AU - Mito, Taro
AU - Kawaguchi, Eri
AU - Inoue, Takeshi
AU - Agata, Kiyokazu
AU - Noji, Sumihare
AU - Ohuchi, Hideyo
N1 - Funding Information:
This work was supported by a Grant-in-Aid for Scientific Research on Innovative Areas (22124003 to S.N.) and a Grant-in-Aid for Creative Scientific Research (15K06897, 18K06184 to T.B.) from the Ministry of Education, Culture, Sports, Science, and Technology of Japan.
Publisher Copyright:
© 2020 Company of Biologists Ltd. All rights reserved.
PY - 2020
Y1 - 2020
N2 - Hemimetabolous insects, such as the two-spotted cricket Gryllus bimaculatus, can recover lost tissues, in contrast to the limited regenerative abilities of human tissues. Following cricket leg amputation, the wound surface is covered by the wound epidermis, and plasmatocytes, which are insect macrophages, accumulate in the wound region. Here, we studied the function of Toll-related molecules identified by comparative RNA sequencing during leg regeneration. Of the 11 Toll genes in the Gryllus genome, expression of Toll2-1, Toll2-2 and Toll2-5 was upregulated during regeneration. RNA interference (RNAi) of Toll, Toll2-1, Toll2-2, Toll2-3 or Toll2-4 produced regeneration defects in more than 50% of crickets. RNAi of Toll2-2 led to a decrease in the ratio of S- and M-phase cells, reduced expression of JAK/STAT signalling genes, and reduced accumulation of plasmatocytes in the blastema. Depletion of plasmatocytes in crickets using clodronate also produced regeneration defects, as well as fewer proliferating cells in the regenerating legs. Plasmatocyte depletion also downregulated the expression of Toll and JAK/STAT signalling genes in the regenerating legs. These results suggest that Spz-Toll-related signalling in plasmatocytes promotes leg regeneration through blastema cell proliferation by regulating the Upd-JAK/STAT signalling pathway.
AB - Hemimetabolous insects, such as the two-spotted cricket Gryllus bimaculatus, can recover lost tissues, in contrast to the limited regenerative abilities of human tissues. Following cricket leg amputation, the wound surface is covered by the wound epidermis, and plasmatocytes, which are insect macrophages, accumulate in the wound region. Here, we studied the function of Toll-related molecules identified by comparative RNA sequencing during leg regeneration. Of the 11 Toll genes in the Gryllus genome, expression of Toll2-1, Toll2-2 and Toll2-5 was upregulated during regeneration. RNA interference (RNAi) of Toll, Toll2-1, Toll2-2, Toll2-3 or Toll2-4 produced regeneration defects in more than 50% of crickets. RNAi of Toll2-2 led to a decrease in the ratio of S- and M-phase cells, reduced expression of JAK/STAT signalling genes, and reduced accumulation of plasmatocytes in the blastema. Depletion of plasmatocytes in crickets using clodronate also produced regeneration defects, as well as fewer proliferating cells in the regenerating legs. Plasmatocyte depletion also downregulated the expression of Toll and JAK/STAT signalling genes in the regenerating legs. These results suggest that Spz-Toll-related signalling in plasmatocytes promotes leg regeneration through blastema cell proliferation by regulating the Upd-JAK/STAT signalling pathway.
KW - Blastema
KW - Gryllus bimaculatus
KW - JAK/STAT signalling
KW - Macrophages
KW - Regeneration
KW - Toll-related signalling
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U2 - 10.1242/dev.199916
DO - 10.1242/dev.199916
M3 - Article
C2 - 34622924
AN - SCOPUS:85119965226
SN - 0950-1991
VL - 149
JO - Development (Cambridge)
JF - Development (Cambridge)
IS - 8
M1 - dev199916
ER -