The Hippo Pathway Controls a Switch between Retinal Progenitor Cell Proliferation and Photoreceptor Cell Differentiation in Zebrafish

被引:44
|
作者
Asaoka, Yoichi [1 ]
Hata, Shoji [1 ]
Namae, Misako [1 ]
Furutani-Seiki, Makoto [2 ]
Nishina, Hiroshi [1 ]
机构
[1] Tokyo Med & Dent Univ, Med Res Inst, Dept Dev & Regenerat Biol, Tokyo, Japan
[2] Univ Bath, Dept Biol & Biochem, Ctr Regenerat Med, Bath BA2 7AY, Avon, England
来源
PLOS ONE | 2014年 / 9卷 / 05期
基金
日本学术振兴会;
关键词
YES-ASSOCIATED PROTEIN; WW DOMAIN; SIGNALING PATHWAY; TRANSCRIPTIONAL ACTIVATOR; NEURONAL DIFFERENTIATION; EMBRYONIC-DEVELOPMENT; NEGATIVE REGULATION; FATE DETERMINATION; MAMMALIAN RETINA; SELF-RENEWAL;
D O I
10.1371/journal.pone.0097365
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
The precise regulation of numbers and types of neurons through control of cell cycle exit and terminal differentiation is an essential aspect of neurogenesis. The Hippo signaling pathway has recently been identified as playing a crucial role in promoting cell cycle exit and terminal differentiation in multiple types of stem cells, including in retinal progenitor cells. When Hippo signaling is activated, the core Mst1/2 kinases activate the Lats1/2 kinases, which in turn phosphorylate and inhibit the transcriptional cofactor Yap. During mouse retinogenesis, overexpression of Yap prolongs progenitor cell proliferation, whereas inhibition of Yap decreases this proliferation and promotes retinal cell differentiation. However, to date, it remains unknown how the Hippo pathway affects the differentiation of distinct neuronal cell types such as photoreceptor cells. In this study, we investigated whether Hippo signaling regulates retinogenesis during early zebrafish development. Knockdown of zebrafish mst2 induced early embryonic defects, including altered retinal pigmentation and morphogenesis. Similar abnormal retinal phenotypes were observed in zebrafish embryos injected with a constitutively active form of yap [(yap (5SA)]. Loss of Yap's TEAD-binding domain, two WW domains, or transcription activation domain attenuated the retinal abnormalities induced by yap (5SA), indicating that all of these domains contribute to normal retinal development. Remarkably, yap (5SA)-expressing zebrafish embryos displayed decreased expression of transcription factors such as otx5 and crx, which orchestrate photoreceptor cell differentiation by activating the expression of rhodopsin and other photoreceptor cell genes. Co-immunoprecipitation experiments revealed that Rx1 is a novel interacting partner of Yap that regulates photoreceptor cell differentiation. Our results suggest that Yap suppresses the differentiation of photoreceptor cells from retinal progenitor cells by repressing Rx1-mediated transactivation of photoreceptor cell genes during zebrafish retinogenesis.
引用
收藏
页数:13
相关论文
共 50 条
  • [21] Low-Level Gestational Lead Exposure Increases Retinal Progenitor Cell Proliferation and Rod Photoreceptor and Bipolar Cell Neurogenesis in Mice
    Giddabasappa, Anand
    Hamilton, W. Ryan
    Chaney, Shawntay
    Xiao, Weimin
    Johnson, Jerry E.
    Mukherjee, Shradha
    Fox, Donald A.
    ENVIRONMENTAL HEALTH PERSPECTIVES, 2011, 119 (01) : 71 - 77
  • [22] Characterisation of maturation of photoreceptor cell subtypes during zebrafish retinal development
    Crespo, Catia
    Knust, Elisabeth
    BIOLOGY OPEN, 2018, 7 (11):
  • [23] Hippo pathway regulates somatic development and cell proliferation of silkworm
    Li, Niannian
    Tong, Xiaoling
    Zeng, Jie
    Meng, Gang
    Sun, Fuze
    Hu, Hai
    Song, Jiangbo
    Lu, Cheng
    Dai, Fangyin
    GENOMICS, 2019, 111 (03) : 391 - 397
  • [24] The Hippo pathway effector Taz is required for cell morphogenesis and fertilization in zebrafish
    Dingare, Chaitanya
    Niedzwetzki, Alina
    Klemmt, Petra A.
    Godbersen, Svenja
    Fuentes, Ricardo
    Mullins, Mary C.
    Lecaudey, Virginie
    DEVELOPMENT, 2018, 145 (22):
  • [25] Electrospun SF/PLCL nanofibrous membrane: a potential scaffold for retinal progenitor cell proliferation and differentiation
    Zhang, Dandan
    Ni, Ni
    Chen, Junzhao
    Yao, Qinke
    Shen, Bingqiao
    Zhang, Yi
    Zhu, Mengyu
    Wang, Zi
    Ruan, Jing
    Wang, Jing
    Mo, Xiumei
    Shi, Wodong
    Ji, Jing
    Fan, Xianqun
    Gu, Ping
    SCIENTIFIC REPORTS, 2015, 5
  • [26] Electrospun SF/PLCL nanofibrous membrane: a potential scaffold for retinal progenitor cell proliferation and differentiation
    Dandan Zhang
    Ni Ni
    Junzhao Chen
    Qinke Yao
    Bingqiao Shen
    Yi Zhang
    Mengyu Zhu
    Zi Wang
    Jing Ruan
    Jing Wang
    Xiumei Mo
    Wodong Shi
    Jing Ji
    Xianqun Fan
    Ping Gu
    Scientific Reports, 5
  • [27] INVITRO ANALYSIS OF CELL-DIFFERENTIATION OF RETINAL PHOTORECEPTOR CELLS
    ARAKI, M
    DEVELOPMENT GROWTH & DIFFERENTIATION, 1988, 30 (04) : 421 - 421
  • [28] Differentiation of retinal progenitor cells into specific cell types
    Zahir, T
    Lavik, E
    Klassen, H
    Langer, R
    Young, MJ
    INVESTIGATIVE OPHTHALMOLOGY & VISUAL SCIENCE, 2003, 44 : U391 - U391
  • [29] Patterns of cell proliferation and rod photoreceptor differentiation in shark retinas
    Ferreiro-Galve, Susana
    Rodriguez-Moldes, Isabel
    Anadon, Ramon
    Candal, Eva
    JOURNAL OF CHEMICAL NEUROANATOMY, 2010, 39 (01) : 1 - 14
  • [30] DIFFERENTIATION OF A BIPOTENTIAL GLIAL PROGENITOR-CELL - WHAT CONTROLS THE TIMING AND THE CHOICE OF DEVELOPMENTAL PATHWAY
    RAFF, MC
    LILLIEN, LE
    JOURNAL OF CELL SCIENCE, 1988, : 77 - 83