Inter-cell type interactions that control JNK signaling in the Drosophila intestine

Peng Zhang (), Stephen M. Pronovost, Marco Marchetti, Chenge Zhang, Xiaoyu Kang, Tahmineh Kandelouei, Christopher Li and Bruce A. Edgar ()
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Peng Zhang: University of Utah
Stephen M. Pronovost: University of Utah
Marco Marchetti: University of Utah
Chenge Zhang: University of Utah
Xiaoyu Kang: University of Utah
Tahmineh Kandelouei: University of Utah
Christopher Li: University of Utah
Bruce A. Edgar: University of Utah

Nature Communications, 2024, vol. 15, issue 1, 1-14

Abstract: Abstract JNK signaling is a critical regulator of inflammation and regeneration, but how it is controlled in specific tissue contexts remains unclear. Here we show that, in the Drosophila intestine, the TNF-type ligand, Eiger (Egr), is expressed exclusively by intestinal stem cells (ISCs) and enteroblasts (EBs), where it is induced by stress and during aging. Egr preferentially activates JNK signaling in a paracrine fashion in differentiated enterocytes (ECs) via its receptor, Grindelwald (Grnd). N-glycosylation genes (Alg3, Alg9) restrain this activation, and stress-induced downregulation of Alg3 and Alg9 correlates with JNK activation, suggesting a regulatory switch. JNK activity in ECs induces expression of the intermembrane protease Rhomboid (Rho), driving secretion of EGFR ligands Keren (Krn) and Spitz (Spi), which in turn activate EGFR signaling in progenitor cells (ISCs and EBs) to stimulate their growth and division, as well as to produce more Egr. This study uncovers an N-glycosylation-controlled, paracrine JNK-EGFR-JNK feedforward loop that sustains ISC proliferation during stress-induced gut regeneration.

Date: 2024
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DOI: 10.1038/s41467-024-49786-w

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