The Nogo-C2/Nogo receptor complex regulates the morphogenesis of zebrafish lateral line primordium through modulating the expression of dkk1b, a Wnt signal inhibitor

Hao Wei Han, Chih Ming Chou, Cheng Ying Chu, Chia Hsiung Cheng, Chung Hsiang Yang, Chin Chun Hung, Pung Pung Hwang, Shyh Jye Lee, Yung Feng Liao, Chang Jen Huang

Research output: Contribution to journalArticle

6 Citations (Scopus)

Abstract

The fish lateral line (LL) is a mechanosensory system closely related to the hearing system of higher vertebrates, and it is composed of several neuromasts located on the surface of the fish. These neuromasts can detect changes in external water flow, to assist fish in maintaining a stationary position in a stream. In the present study, we identified a novel function of Nogo/Nogo receptor signaling in the formation of zebrafish neuromasts. Nogo signaling in zebrafish, like that in mammals, involves three ligands and four receptors, as well as three co-receptors (TROY, p75, and LINGO-1). We first demonstrated that Nogo-C2, NgRH1a, p75, and TROY are able to form a Nogo-C2 complex, and that disintegration of this complex causes defective neuromast formation in zebrafish. Time-lapse recording of the CldnB::lynEGFP transgenic line revealed that functional obstruction of the Nogo-C2 complex causes disordered morphogenesis, and reduces rosette formation in the posterior LL (PLL) primordium during migration. Consistent with these findings, hair-cell progenitors were lost from the PLL primordium in p75, TROY, and Nogo-C2/NgRH1a morphants. Notably, the expression levels of pea3, a downstream marker of Fgf signaling, and dkk1b, a Wnt signaling inhibitor, were both decreased in p75, TROY, and Nogo-C2/NgRH1a morphants; moreover, dkk1b mRNA injection could rescue the defects in neuromast formation resulting from knockdown of p75 or TROY. We thus suggest that a novel Nogo-C2 complex, consisting of Nogo-C2, NgRH1a, p75, and TROY, regulates Fgf signaling and dkk1b expression, thereby ensuring stable organization of the PLL primordium.

Original languageEnglish
Article numbere86345
JournalPLoS One
Volume9
Issue number1
DOIs
Publication statusPublished - Jan 21 2014

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Zebrafish
Danio rerio
Morphogenesis
morphogenesis
Fishes
receptors
Fish
Rosette Formation
Hearing
fish
Vertebrates
Mammals
Stem Cells
Disintegration
Ligands
Audition
hearing
Messenger RNA
Injections
Water

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Cite this

The Nogo-C2/Nogo receptor complex regulates the morphogenesis of zebrafish lateral line primordium through modulating the expression of dkk1b, a Wnt signal inhibitor. / Han, Hao Wei; Chou, Chih Ming; Chu, Cheng Ying; Cheng, Chia Hsiung; Yang, Chung Hsiang; Hung, Chin Chun; Hwang, Pung Pung; Lee, Shyh Jye; Liao, Yung Feng; Huang, Chang Jen.

In: PLoS One, Vol. 9, No. 1, e86345, 21.01.2014.

Research output: Contribution to journalArticle

Han, Hao Wei ; Chou, Chih Ming ; Chu, Cheng Ying ; Cheng, Chia Hsiung ; Yang, Chung Hsiang ; Hung, Chin Chun ; Hwang, Pung Pung ; Lee, Shyh Jye ; Liao, Yung Feng ; Huang, Chang Jen. / The Nogo-C2/Nogo receptor complex regulates the morphogenesis of zebrafish lateral line primordium through modulating the expression of dkk1b, a Wnt signal inhibitor. In: PLoS One. 2014 ; Vol. 9, No. 1.
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abstract = "The fish lateral line (LL) is a mechanosensory system closely related to the hearing system of higher vertebrates, and it is composed of several neuromasts located on the surface of the fish. These neuromasts can detect changes in external water flow, to assist fish in maintaining a stationary position in a stream. In the present study, we identified a novel function of Nogo/Nogo receptor signaling in the formation of zebrafish neuromasts. Nogo signaling in zebrafish, like that in mammals, involves three ligands and four receptors, as well as three co-receptors (TROY, p75, and LINGO-1). We first demonstrated that Nogo-C2, NgRH1a, p75, and TROY are able to form a Nogo-C2 complex, and that disintegration of this complex causes defective neuromast formation in zebrafish. Time-lapse recording of the CldnB::lynEGFP transgenic line revealed that functional obstruction of the Nogo-C2 complex causes disordered morphogenesis, and reduces rosette formation in the posterior LL (PLL) primordium during migration. Consistent with these findings, hair-cell progenitors were lost from the PLL primordium in p75, TROY, and Nogo-C2/NgRH1a morphants. Notably, the expression levels of pea3, a downstream marker of Fgf signaling, and dkk1b, a Wnt signaling inhibitor, were both decreased in p75, TROY, and Nogo-C2/NgRH1a morphants; moreover, dkk1b mRNA injection could rescue the defects in neuromast formation resulting from knockdown of p75 or TROY. We thus suggest that a novel Nogo-C2 complex, consisting of Nogo-C2, NgRH1a, p75, and TROY, regulates Fgf signaling and dkk1b expression, thereby ensuring stable organization of the PLL primordium.",
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AU - Chou, Chih Ming

AU - Chu, Cheng Ying

AU - Cheng, Chia Hsiung

AU - Yang, Chung Hsiang

AU - Hung, Chin Chun

AU - Hwang, Pung Pung

AU - Lee, Shyh Jye

AU - Liao, Yung Feng

AU - Huang, Chang Jen

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