Calcium transport into the cells of the sea urchin larva in relation to spicule formation

Vidavsky, Netta; Addadi, Sefi; Schertel, Andreas; Ben-Ezra, David; Shpigel, Muki; Addadi, Lia; Weiner, Steve

doi:10.1073/pnas.1612017113

Title: Calcium transport into the cells of the sea urchin larva in relation to spicule formation

Abstract

Here, we investigated the manner in which the sea urchin larva takes up calcium from its body cavity into the primary mesenchymal cells (PMCs) that are responsible for spicule formation. We used the membrane-impermeable fluorescent dye calcein and alexa-dextran, with or without a calcium channel inhibitor, and imaged the larvae in vivo with selective-plane illumination microscopy. Both fluorescent molecules are taken up from the body cavity into the PMCs and ectoderm cells, where the two labels are predominantly colocalized in particles, whereas the calcium-binding calcein label is mainly excluded from the endoderm and is concentrated in the spicules. The presence of vesicles and vacuoles inside the PMCs that have openings through the plasma membrane directly to the body cavity was documented using high-resolution cryo-focused ion beam-SEM serial imaging. Some of the vesicles and vacuoles are interconnected to form large networks. We suggest that these vacuolar networks are involved in direct sea water uptake. We conclude that the calcium pathway from the body cavity into cells involves nonspecific endocytosis of sea water with its calcium.

Authors:: Vidavsky, Netta; Addadi, Sefi; Schertel, Andreas; Ben-Ezra, David; Shpigel, Muki; Addadi, Lia; Weiner, Steve

Publication Date:: Mon Oct 24 00:00:00 EDT 2016

Research Org.:: Univ. of Wisconsin, Madison, WI (United States)

Sponsoring Org.:: USDOE

OSTI Identifier:: 1329959

Alternate Identifier(s):: OSTI ID: 1464948

Grant/Contract Number:: FG02-07ER15899; AD 364 2-1

Resource Type:: Published Article

Journal Name:: Proceedings of the National Academy of Sciences of the United States of America

Additional Journal Information:: Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 113 Journal Issue: 45; Journal ID: ISSN 0027-8424

Publisher:: National Academy of Sciences, Washington, DC (United States)

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; SPIM imaging; endocytosis; in vivo imaging; biomineralization; cryo-FIB-SEM

Citation Formats


                    Vidavsky, Netta, Addadi, Sefi, Schertel, Andreas, Ben-Ezra, David, Shpigel, Muki, Addadi, Lia, and Weiner, Steve. Calcium transport into the cells of the sea urchin larva in relation to spicule formation.  United States: N. p., 2016. 
Web.  doi:10.1073/pnas.1612017113.

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                    Vidavsky, Netta, Addadi, Sefi, Schertel, Andreas, Ben-Ezra, David, Shpigel, Muki, Addadi, Lia, & Weiner, Steve. Calcium transport into the cells of the sea urchin larva in relation to spicule formation.  United States.  https://doi.org/10.1073/pnas.1612017113

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                    Vidavsky, Netta, Addadi, Sefi, Schertel, Andreas, Ben-Ezra, David, Shpigel, Muki, Addadi, Lia, and Weiner, Steve. Mon .  
"Calcium transport into the cells of the sea urchin larva in relation to spicule formation".  United States.  https://doi.org/10.1073/pnas.1612017113.

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@article{osti_1329959,

  title        = {Calcium transport into the cells of the sea urchin larva in relation to spicule formation},

  author       = {Vidavsky, Netta and Addadi, Sefi and Schertel, Andreas and Ben-Ezra, David and Shpigel, Muki and Addadi, Lia and Weiner, Steve},

  abstractNote = {Here, we investigated the manner in which the sea urchin larva takes up calcium from its body cavity into the primary mesenchymal cells (PMCs) that are responsible for spicule formation. We used the membrane-impermeable fluorescent dye calcein and alexa-dextran, with or without a calcium channel inhibitor, and imaged the larvae in vivo with selective-plane illumination microscopy. Both fluorescent molecules are taken up from the body cavity into the PMCs and ectoderm cells, where the two labels are predominantly colocalized in particles, whereas the calcium-binding calcein label is mainly excluded from the endoderm and is concentrated in the spicules. The presence of vesicles and vacuoles inside the PMCs that have openings through the plasma membrane directly to the body cavity was documented using high-resolution cryo-focused ion beam-SEM serial imaging. Some of the vesicles and vacuoles are interconnected to form large networks. We suggest that these vacuolar networks are involved in direct sea water uptake. We conclude that the calcium pathway from the body cavity into cells involves nonspecific endocytosis of sea water with its calcium.},

  doi          = {10.1073/pnas.1612017113},

  journal      = {Proceedings of the National Academy of Sciences of the United States of America},

  number       = 45,

  volume       = 113,

  place        = {United States},

  year         = {Mon Oct 24 00:00:00 EDT 2016},

  month        = {Mon Oct 24 00:00:00 EDT 2016}

}

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Similar Records

Title: Calcium transport into the cells of the sea urchin larva in relation to spicule formation

Abstract

Citation Formats

Transport of membrane-bound mineral particles in blood vessels during chicken embryonic bone development journal, February 2016

Accumulation of Eadioactive Calcium tn Larvae of the sea Urchin Pseudocentrotus Depressus journal, August 1963

The role of intracellular calcium phosphate in osteoblast-mediated bone apatite formation journal, August 2012

The role of seawater endocytosis in the biomineralization process in calcareous foraminifera journal, December 2009

An Early-Branching Microbialite Cyanobacterium Forms Intracellular Carbonates journal, April 2012

High calcium concentrations shift the mode of exocytosis to the kiss-and-run mechanism journal, May 1999

Turnover of Transmitter and Synaptic Vesicles at the frog Neuromuscular Junction journal, May 1973

Crystallization Pathways in Biomineralization journal, August 2011

Acidified seawater impacts sea urchin larvae pH regulatory systems relevant for calcification journal, October 2012

Studies on the Cellular Pathway Involved in Assembly of the Embryonic Sea Urchin Spicule journal, April 1993

Kiss-and-run and full-collapse fusion as modes of exo-endocytosis in neurosecretion journal, June 2006

Inhibition of45Ca2+ uptake in the eggs and embryos of the sea urchin,Anthocidaris crassispina, by several calcium antagonists, anion transport inhibitor, and chloride transport inhibitors journal, August 1985

Double Patch Clamp Reveals That Transient Fusion (Kiss-and-Run) Is a Major Mechanism of Secretion in Calf Adrenal Chromaffin Cells: High Calcium Shifts the Mechanism from Kiss-and-Run to Complete Fusion journal, March 2006

Mechanisms of Endocytosis journal, June 2009

Biomineralization of the Spicules of Sea Urchin Embryos journal, March 2002

Cryo FIB-SEM: Volume imaging of cellular ultrastructure in native frozen specimens journal, November 2013

A vacuole-like compartment concentrates a disordered calcium phase in a key coccolithophorid alga journal, April 2016

Differential effects of verapamil and flunarizine on cardiac L-type and T-type Ca channels journal, June 1988

Inositol Trisphosphate and Calcium Signaling journal, January 1988

Inhibitory effects of ethacrynic acid, furosemide, and nifedipine on the calcification of spicules in cultures of micromeres isolated from sea-urchin eggs journal, March 1986

Pathways of clathrin-independent endocytosis journal, August 2007

The form and Function of Metal-Containing ‘Granules’ in Invertebrate Tissues journal, November 1982

Calcein labelling and electrophysiology: insights on coral tissue permeability and calcification journal, May 2011

Mechanism for electrosilent Ca2+ transport to cause calcification of spicules in sea urchin embryos journal, July 1985

The dynamics of secretion during sea urchin embryonic skeleton formation journal, May 2008

Differentiation of the transmembrane Na and Ca channels in mammalian cardiac fibres by the use of specific inhibitors journal, January 1972

Energy Interconversion by the Ca2+-Dependent ATPase of the Sarcoplasmic Reticulum journal, June 1979

Bone mineralization pathways during the rapid growth of embryonic chicken long bones journal, July 2016

Biologically controlled synthesis and assembly of magnetite nanoparticles journal, January 2015

Biomineralization Within Vesicles: The Calcite of Coccoliths journal, January 2003

Biochemical Aspects of Active Transport journal, June 1967

The Bioavailability of Dietary Calcium journal, April 2000

Skeletal morphogenesis in the sea urchin embryo: regulation of primary mesenchyme gene expression and skeletal rod growth by ectoderm-derived cues journal, May 1997

Coral biomineralization: From the gene to the environment journal, November 2011

Quantal components of the end-plate potential journal, June 1954

Cellular Control Over Spicule Formation in Sea Urchin Embryos: A Structural Approach journal, March 1999

Mapping amorphous calcium phosphate transformation into crystalline mineral from the cell to the bone in zebrafish fin rays journal, March 2010

Mineral-bearing vesicle transport in sea urchin embryos journal, December 2015

Cryo-FIB-SEM serial milling and block face imaging: Large volume structural analysis of biological tissues preserved close to their native state journal, December 2016

STUDIES OF CALCIUM AND PHOSPHORUS METABOLISM: V. A STUDY OF THE BONE TRABECULAe AS A READILY AVAILABLE RESERVE SUPPLY OF CALCIUM. journal, January 1929

Macropinocytosis: an endocytic pathway for internalising large gulps journal, March 2011

Initial stages of calcium uptake and mineral deposition in sea urchin embryos journal, December 2013

Transport of membrane-bound mineral particles in blood vessels during chicken embryonic bone development
journal, February 2016

Accumulation of Eadioactive Calcium tn Larvae of the sea Urchin Pseudocentrotus Depressus
journal, August 1963

The role of intracellular calcium phosphate in osteoblast-mediated bone apatite formation
journal, August 2012

The role of seawater endocytosis in the biomineralization process in calcareous foraminifera
journal, December 2009

An Early-Branching Microbialite Cyanobacterium Forms Intracellular Carbonates
journal, April 2012

High calcium concentrations shift the mode of exocytosis to the kiss-and-run mechanism
journal, May 1999

Turnover of Transmitter and Synaptic Vesicles at the frog Neuromuscular Junction
journal, May 1973

Crystallization Pathways in Biomineralization
journal, August 2011

Acidified seawater impacts sea urchin larvae pH regulatory systems relevant for calcification
journal, October 2012

Studies on the Cellular Pathway Involved in Assembly of the Embryonic Sea Urchin Spicule
journal, April 1993

Kiss-and-run and full-collapse fusion as modes of exo-endocytosis in neurosecretion
journal, June 2006

Inhibition of45Ca2+ uptake in the eggs and embryos of the sea urchin,Anthocidaris crassispina, by several calcium antagonists, anion transport inhibitor, and chloride transport inhibitors
journal, August 1985

Double Patch Clamp Reveals That Transient Fusion (Kiss-and-Run) Is a Major Mechanism of Secretion in Calf Adrenal Chromaffin Cells: High Calcium Shifts the Mechanism from Kiss-and-Run to Complete Fusion
journal, March 2006

Mechanisms of Endocytosis
journal, June 2009

Biomineralization of the Spicules of Sea Urchin Embryos
journal, March 2002

Cryo FIB-SEM: Volume imaging of cellular ultrastructure in native frozen specimens
journal, November 2013

A vacuole-like compartment concentrates a disordered calcium phase in a key coccolithophorid alga
journal, April 2016

Differential effects of verapamil and flunarizine on cardiac L-type and T-type Ca channels
journal, June 1988

Inositol Trisphosphate and Calcium Signaling
journal, January 1988

Inhibitory effects of ethacrynic acid, furosemide, and nifedipine on the calcification of spicules in cultures of micromeres isolated from sea-urchin eggs
journal, March 1986

Pathways of clathrin-independent endocytosis
journal, August 2007

The form and Function of Metal-Containing ‘Granules’ in Invertebrate Tissues
journal, November 1982

Calcein labelling and electrophysiology: insights on coral tissue permeability and calcification
journal, May 2011

Mechanism for electrosilent Ca2+ transport to cause calcification of spicules in sea urchin embryos
journal, July 1985

The dynamics of secretion during sea urchin embryonic skeleton formation
journal, May 2008

Differentiation of the transmembrane Na and Ca channels in mammalian cardiac fibres by the use of specific inhibitors
journal, January 1972

Energy Interconversion by the Ca2+-Dependent ATPase of the Sarcoplasmic Reticulum
journal, June 1979

Bone mineralization pathways during the rapid growth of embryonic chicken long bones
journal, July 2016

Biologically controlled synthesis and assembly of magnetite nanoparticles
journal, January 2015

Biomineralization Within Vesicles: The Calcite of Coccoliths
journal, January 2003

Biochemical Aspects of Active Transport
journal, June 1967

The Bioavailability of Dietary Calcium
journal, April 2000

Skeletal morphogenesis in the sea urchin embryo: regulation of primary mesenchyme gene expression and skeletal rod growth by ectoderm-derived cues
journal, May 1997

Coral biomineralization: From the gene to the environment
journal, November 2011

Quantal components of the end-plate potential
journal, June 1954

Cellular Control Over Spicule Formation in Sea Urchin Embryos: A Structural Approach
journal, March 1999

Mapping amorphous calcium phosphate transformation into crystalline mineral from the cell to the bone in zebrafish fin rays
journal, March 2010

Mineral-bearing vesicle transport in sea urchin embryos
journal, December 2015

Cryo-FIB-SEM serial milling and block face imaging: Large volume structural analysis of biological tissues preserved close to their native state
journal, December 2016

STUDIES OF CALCIUM AND PHOSPHORUS METABOLISM: V. A STUDY OF THE BONE TRABECULAe AS A READILY AVAILABLE RESERVE SUPPLY OF CALCIUM.
journal, January 1929

Macropinocytosis: an endocytic pathway for internalising large gulps
journal, March 2011

Initial stages of calcium uptake and mineral deposition in sea urchin embryos
journal, December 2013