Protein Phosphatase 1 β Paralogs Encode the Zebrafish Myosin Phosphatase Catalytic Subunit

Jayashankar, Vaishali; Nguyen, Michael J; Carr, Brandon W.; Zheng, Dale C.; Rosales, Joseph B.; Rosales, Joshua B.; Weiser, Douglas C.

doi:10.1371/journal.pone.0075766

Cited by 16 publications

(32 citation statements)

References 89 publications

(138 reference statements)

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“…However, this delamination typically occurred after the effect on doming movements became visible in the transplanted embryos (not shown), arguing against this function of RhoA being responsible for the observed doming defect. Conversely, we also performed transplantation of either a large patch of pky donor surface cells (∼100 cells) replacing a smaller patch of surface cells (∼60 cells) in pky host embryos or, alternatively, of a patch of pky donor surface cells overexpressing myosin phosphatase 1 ( mypt1 ) (Jayashankar et al., 2013), which reduces actomyosin contraction in those cells, replacing a similar-sized patch of surface cells in pky hosts (Figures 7C and 7E). We reasoned that in both of these transplantations, we locally normalize expansion of pky surface cells without changing their genotype (Figure S6I), allowing us to specifically analyze the effect of modulating surface cell expansion on doming in pky mutants.…”

Section: Resultsmentioning

confidence: 99%

“…The following expression constructs were used: membrane-GFP (mem-GFP) (Kimmel and Meyer, 2010), membrane-RFP (mem-RFP) (Iioka et al., 2004), H2B-EGFP (Keller et al., 2008), H2A-mCherry (Arboleda-Estudillo et al., 2010), RhoA (Takesono et al., 2012), and N-terminal fragment of Mypt1 (Jayashankar et al., 2013). mRNA was synthesized using mMESSAGE mMACHINE SP6 kit (Ambion).…”

Section: Methodsmentioning

confidence: 99%

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The Physical Basis of Coordinated Tissue Spreading in Zebrafish Gastrulation

et al. 2017

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SummaryEmbryo morphogenesis relies on highly coordinated movements of different tissues. However, remarkably little is known about how tissues coordinate their movements to shape the embryo. In zebrafish embryogenesis, coordinated tissue movements first become apparent during “doming,” when the blastoderm begins to spread over the yolk sac, a process involving coordinated epithelial surface cell layer expansion and mesenchymal deep cell intercalations. Here, we find that active surface cell expansion represents the key process coordinating tissue movements during doming. By using a combination of theory and experiments, we show that epithelial surface cells not only trigger blastoderm expansion by reducing tissue surface tension, but also drive blastoderm thinning by inducing tissue contraction through radial deep cell intercalations. Thus, coordinated tissue expansion and thinning during doming relies on surface cells simultaneously controlling tissue surface tension and radial tissue contraction.

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Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

The Physical Basis of Coordinated Tissue Spreading in Zebrafish Gastrulation

et al. 2017

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“…Considering the important role of PP1b in maintaining muscle attachments and cell adhesion in nonmuscle tissues in Drosophila (68), as well as in morphogenesis of zebrafish (13), nutrient absorption (which depends on the tegument of S. japonicum) could have been suppressed by knocking down Sj-pp1cs. This assumption is supported by the observed down-regulation of tegument-associated genes (69,70), such as the components of basement membrane including type I, IV collagens (Sjp_0034120, Sjp_0099760) and a basement membrane-specific heparin sulfate proteoglycan core protein (Sjp_0073100), the cytoskeleton and motor proteins, including keratin 9 (Sjp_ 0075140), dynein light chain 2 (Sjp_0008620) and paramyosin (Sjp_0027340), and tegument surface protein dysferlin (Sjp_0078120) and myoferlin (Sjp_0090660) of males, as well as the cell adhesion protein C-type lectin (Sjp_0033720) of females.…”

Section: Discussionmentioning

confidence: 99%

Serine/threonine protein phosphatase 1 (PP1) controls growth and reproduction in Schistosoma japonicum

Zhao

et al. 2018

The FASEB Journal

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Schistosomiasis is a human parasitic disease caused by flatworms of the genus Schistosoma. Adult female schistosomes produce numerous eggs that are responsible for the pathogenesis and transmission of the disease, and the maturation of female gonads depends on the permanent pairing of females and males. Signaling protein kinases have been proven to control female gonad differentiation after pairing; however, little is known about the roles of protein phosphatases in the developmental and reproductive biology of schistosomes. Here we explored 3 genes encoding catalytic subunits of serine/threonine protein phosphatase 1 (PP1c) that were structurally and evolutionarily conserved in Schistosoma japonicum. In situ hybridization showed transcripts of 3 Sj-pp1c genes mainly localized in the reproductive organs and tissues. Triple knockdown of Sj-pp1c genes by RNA interference caused stunted growth and decreased pairing stability of worm pairs, as well as a remarkable reduction in cell proliferation activity and defects in reproductive maturation and fecundity. Transcriptomic analysis post-RNA interference suggested that Sj-pp1c genes are involved in controlling worm development and maturation mainly by regulating cell proliferation, eggshell synthesis, nutritional metabolism, cytoskeleton organization, and neural process. Our study provides the first insight into the fundamental contribution of Sj-PP1c to molecular mechanisms underlying the reproductive biology of schistosomes.-Zhao, L., Lu, Z., He, X., Mughal, M. N., Fang, R., Zhou, Y., Zhao, J., Gasser, R. B., Grevelding, C. G., Ye, Q., Hu, M. Serine/threonine protein phosphatase 1 (PP1) controls growth and reproduction in Schistosoma japonicum.

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“…Inhibition of PP1 results in severe defects in morphogenetic cell movements and patterning. Mis-regulation of PP1 results in severe gastrulation defects inducing characteristic phenotypes, including a shortened and broadened body axis, reduced axial migration of the prechordal plate, disruption of cell polarity and changes in cellular protrusive activity [58,59]. We anticipated that the overexpression of active phosphatase inhibitors, such as Cpi-17 or Phi-1, would disrupt early development.…”

Section: Expression Of Cpi-17 Paralogs But Not Phi-1 Paralogs Rescumentioning

confidence: 99%

The Evolution of Duplicated Genes of the Cpi-17/Phi-1 (ppp1r14) Family of Protein Phosphatase 1 Inhibitors in Teleosts

Lang

Virk

Zheng

et al. 2020

IJMS

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The Cpi-17 (ppp1r14) gene family is an evolutionarily conserved, vertebrate specific group of protein phosphatase 1 (PP1) inhibitors. When phosphorylated, Cpi-17 is a potent inhibitor of myosin phosphatase (MP), a holoenzyme complex of the regulatory subunit Mypt1 and the catalytic subunit PP1. Myosin phosphatase dephosphorylates the regulatory myosin light chain (Mlc2) and promotes actomyosin relaxation, which in turn, regulates numerous cellular processes including smooth muscle contraction, cytokinesis, cell motility, and tumor cell invasion. We analyzed zebrafish homologs of the Cpi-17 family, to better understand the mechanisms of myosin phosphatase regulation. We found single homologs of both Kepi (ppp1r14c) and Gbpi (ppp1r14d) in silico, but we detected no expression of these genes during early embryonic development. Cpi-17 (ppp1r14a) and Phi-1 (ppp1r14b) each had two duplicate paralogs, (ppp1r14aa and ppp1r14ab) and (ppp1r14ba and ppp1r14bb), which were each expressed during early development. The spatial expression pattern of these genes has diverged, with ppp1r14aa and ppp1r14bb expressed primarily in smooth muscle and skeletal muscle, respectively, while ppp1r14ab and ppp1r14ba are primarily expressed in neural tissue. We observed that, in in vitro and heterologous cellular systems, the Cpi-17 paralogs both acted as potent myosin phosphatase inhibitors, and were indistinguishable from one another. In contrast, the two Phi-1 paralogs displayed weak myosin phosphatase inhibitory activity in vitro, and did not alter myosin phosphorylation in cells. Through deletion and chimeric analysis, we identified that the difference in specificity for myosin phosphatase between Cpi-17 and Phi-1 was encoded by the highly conserved PHIN (phosphatase holoenzyme inhibitory) domain, and not the more divergent N- and C- termini. We also showed that either Cpi-17 paralog can rescue the knockdown phenotype, but neither Phi-1 paralog could do so. Thus, we provide new evidence about the biochemical and developmental distinctions of the zebrafish Cpi-17 protein family.

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Protein Phosphatase 1 β Paralogs Encode the Zebrafish Myosin Phosphatase Catalytic Subunit

Cited by 16 publications

References 89 publications

The Physical Basis of Coordinated Tissue Spreading in Zebrafish Gastrulation

The Physical Basis of Coordinated Tissue Spreading in Zebrafish Gastrulation

Serine/threonine protein phosphatase 1 (PP1) controls growth and reproduction in Schistosoma japonicum

The Evolution of Duplicated Genes of the Cpi-17/Phi-1 (ppp1r14) Family of Protein Phosphatase 1 Inhibitors in Teleosts

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