Behavior of Pigment Cells Closely Correlates the Manner of Gastrulation in Sea Urchin Embryos

Takata, Hiromi; Kominami, Taro

doi:10.2108/zsj.21.1025

Cited by 21 publications

(29 citation statements)

References 40 publications

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“…In this process of extension, the wide, short gut rudiment is transformed into a long, thin tube. It has been proposed that contraction of the fi lopodia interconnecting the archenteron tip and the apical plate pulls the gut rudiment upward (Takata and Kominami 2004 ). At this point, the existence of tension in SMC fi lopodia is evident.…”

Section: Development Of Echinoidea (Sea Urchins)mentioning

confidence: 99%

Echinodermata

Arnone

Byrne

Martinez

2015

Evolutionary Developmental Biology of Invertebrates 6

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Section: Development Of Echinoidea (Sea Urchins)mentioning

confidence: 99%

Echinodermata

Arnone

Byrne

Martinez

2015

Evolutionary Developmental Biology of Invertebrates 6

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“…Given that a subset of veg1-derived cells form the S. purpuratus hindgut late in gastrulation, it is likely that C5a efflux activity in pigment cells is required for proper movement and orientation of veg1-derived hindgut cells. Interestingly, pigment cells have been reported to affect gastrulation in Echinometra mathaei (Takata and Kominami, 2004), a sea urchin closely related to S. purpuratus (Smith et al, 2006). However, in E. mathaei, pigment cells influence gastrulation movements during primary invagination.…”

Section: Contributions Of Veg-lineage Cells To the Gut And Timing Of mentioning

confidence: 99%

ABCC5 is required for cAMP-mediated hindgut invagination in sea urchin embryos

et al. 2015

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ATP-binding cassette (ABC) transporters are evolutionarily conserved proteins that pump diverse substrates across membranes. Many are known to efflux signaling molecules and are extensively expressed during development. However, the role of transporters in moving extracellular signals that regulate embryogenesis is largely unexplored. Here, we show that a mesodermal ABCC (MRP) transporter is necessary for endodermal gut morphogenesis in sea urchin embryos. This transporter, Sp-ABCC5a (C5a), is expressed in pigment cells and their precursors, which are a subset of the non-skeletogenic mesoderm (NSM) cells. C5a expression depends on Delta/Notch signaling from skeletogenic mesoderm and is downstream of Gcm in the aboral NSM gene regulatory network. Long-term imaging of development reveals that C5a knockdown embryos gastrulate, but ∼90% develop a prolapse of the hindgut by the late prism stage (∼8 h after C5a protein expression normally peaks). Since C5a orthologs efflux cyclic nucleotides, and cAMP-dependent protein kinase (Sp-CAPK/PKA) is expressed in pigment cells, we examined whether C5a could be involved in gastrulation through cAMP transport. Consistent with this hypothesis, membrane-permeable pCPT-cAMP rescues the prolapse phenotype in C5a knockdown embryos, and causes archenteron hyper-invagination in control embryos. In addition, the cAMP-producing enzyme soluble adenylyl cyclase (sAC) is expressed in pigment cells, and its inhibition impairs gastrulation. Together, our data support a model in which C5a transports sAC-derived cAMP from pigment cells to control late invagination of the hindgut. Little is known about the ancestral functions of ABCC5/MRP5 transporters, and this study reveals a novel role for these proteins in mesoderm-endoderm signaling during embryogenesis.

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“…The invagination is thought to occur autonomously and be caused by four factors; cell growth of the ectodermal layer to cause cell migration at the vegetal side into the blastocoel, growth of cells that compose the archenteron, elongation of the archenteron by rearrangement along the vegetal-animal axis, towing of the gut rudiment by SMCs forming filopodia (Takata and Kominami, 2001; Ettensohn, 1985; Hardin, 1988; Dan and Okazaki, 1956; Gustafson and Kinnander, 1956). However, secondary invagination is not caused by all four factors in all sea urchin species, resulting in species-specific variation, continuous invagination, and the cells around the blastopore invaginating continuously without lag phase between the first and second invagination (Ettensohn and Ingersoll, 1992; Kominami and Masui, 1996; Takata and Kominami, 2004). Therefore, sea urchin embryos exhibit species-specific morphologies at the blastula and gastrula stages.…”

Section: Introductionmentioning

confidence: 99%

“…We found that the indirect-developing temnopleurid Temnopleurus toreumaticus forms a wrinkled blastula with a thick blastular wall, whereas other indirect-developing species T. reevesii , T. hardwickii and Mespilia globulus form smoothed blastulae with a thin blastular wall (Kitazawa et al, 2009, 2010). Embryos of T. toreumaticus invaginate continuously to form an archenteron, whereas embryos of M. globulus have stepwise invagination such as that the archenteron elongates with two elongation steps and a lag phase between these steps (Takata and Kominami, 2004). However, gastrulation of T. reevesii and T. hardwickii is not fully understood, and in T. reevesii development until metamorphosis was described only recently (Kitazawa et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Morphological diversity of blastula formation and gastrulation in temnopleurid sea urchins

et al. 2016

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Embryos of temnopleurid sea urchins exhibit species-specific morphologies. While Temnopleurus toreumaticus has a wrinkled blastula and then invaginates continuously at gastrulation, others have a smooth blastula and their invagination is stepwise. We studied blastula and gastrula formation in four temnopleurids using light and scanning electron microscopy to clarify the mechanisms producing these differences. Unlike T. toreumaticus, blastomeres of mid-blastulae in T. reevesii, T. hardwickii and Mespilia globulus formed pseudopods. Before primary mesenchyme cells ingressed, embryos developed an area of orbicular cells in the vegetal plate. The cells surrounding the orbicular cells extended pseudopods toward the orbicular cell area in three Temnopleurus species. In T. toreumaticus, the extracellular matrix was well-developed and developed a hole-like structure that was not formed in others. Gastrulation of T. reevesii, T. hardwickii and M. globulus was stepwise, suggesting that differences of gastrulation are caused by all or some of the following factors: change of cell shape, rearrangement, pushing up and towing of cells. We conclude that (1) many aspects of early morphogenesis differ even among very closely related sea urchins with indirect development and (2) many of these differences may be caused by the cell shape and structure of blastomeres or by differences in extracellular matrix composition.

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Behavior of Pigment Cells Closely Correlates the Manner of Gastrulation in Sea Urchin Embryos

Cited by 21 publications

References 40 publications

Echinodermata

Echinodermata

ABCC5 is required for cAMP-mediated hindgut invagination in sea urchin embryos

Morphological diversity of blastula formation and gastrulation in temnopleurid sea urchins

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