RNA-Seq identifies SPGs as a ventral skeletal patterning cue in sea urchins

Michael L. Piacentino; Daniel T. Zuch; Julie Fishman; Sviatlana Rose; Emily E. Speranza; Christy Li; Jia Yu; Oliver Chung; Janani Ramachandran; Patrick Ferrell; Vijeta Patel; Arlene Reyna; Hajerah Hameeduddin; James Chaves; Finnegan B. Hewitt; Evan Bardot; David Lee; Amanda B. Core; John D. Hogan; Jessica L. Keenan; Lingqi Luo; Jasmin Coulombe-Huntington; Todd A. Blute; Ekaterina Oleinik; Jonas Ibn-Salem; Albert J. Poustka; Cynthia A. Bradham

doi:10.1242/dev.129312

RNA-Seq identifies SPGs as a ventral skeletal patterning cue in sea urchins

Michael L. Piacentino, Daniel T. Zuch, Julie Fishman, Sviatlana Rose, Emily E. Speranza, Christy Li, Jia Yu, Oliver Chung, Janani Ramachandran, Patrick Ferrell, Vijeta Patel, Arlene Reyna, Hajerah Hameeduddin, James Chaves, Finnegan B. Hewitt, Evan Bardot, David Lee, Amanda B. Core, John D. Hogan, Jessica L. KeenanLingqi Luo, Jasmin Coulombe-Huntington, Todd A. Blute, Ekaterina Oleinik, Jonas Ibn-Salem, Albert J. Poustka, Cynthia A. Bradham

Research output: Contribution to journal › Article › peer-review

25 Scopus citations

Abstract

The sea urchin larval skeleton offers a simple model for formation of developmental patterns. The calcium carbonate skeleton is secreted by primary mesenchyme cells (PMCs) in response to largely unknown patterning cues expressed by the ectoderm. To discover novel ectodermal cues, we performed an unbiased RNA-Seq-based screen and functionally tested candidates; we thereby identified several novel skeletal patterning cues. Among these, we show that SLC26a2/7 is a ventrally expressed sulfate transporter that promotes a ventral accumulation of sulfated proteoglycans, which is required for ventral PMC positioning and skeletal patterning. We show that the effects of SLC perturbation are mimicked by manipulation of either external sulfate levels or proteoglycan sulfation. These results identify novel skeletal patterning genes and demonstrate that ventral proteoglycan sulfation serves as a positional cue for sea urchin skeletal patterning.

Original language	English
Pages (from-to)	703-714
Number of pages	12
Journal	Development (Cambridge)
Volume	143
Issue number	4
DOIs	https://doi.org/10.1242/dev.129312
State	Published - 15 Feb 2016
Externally published	Yes

Keywords

Patterning
RNA-Seq
Skeleton
Sulfated proteoglycan

Access to Document

10.1242/dev.129312

Cite this

Piacentino, M. L., Zuch, D. T., Fishman, J., Rose, S., Speranza, E. E., Li, C., Yu, J., Chung, O., Ramachandran, J., Ferrell, P., Patel, V., Reyna, A., Hameeduddin, H., Chaves, J., Hewitt, F. B., Bardot, E., Lee, D., Core, A. B., Hogan, J. D., ... Bradham, C. A. (2016). RNA-Seq identifies SPGs as a ventral skeletal patterning cue in sea urchins. Development (Cambridge), 143(4), 703-714. https://doi.org/10.1242/dev.129312

@article{a1500466840b4fe88913c34d4d95206a,

title = "RNA-Seq identifies SPGs as a ventral skeletal patterning cue in sea urchins",

abstract = "The sea urchin larval skeleton offers a simple model for formation of developmental patterns. The calcium carbonate skeleton is secreted by primary mesenchyme cells (PMCs) in response to largely unknown patterning cues expressed by the ectoderm. To discover novel ectodermal cues, we performed an unbiased RNA-Seq-based screen and functionally tested candidates; we thereby identified several novel skeletal patterning cues. Among these, we show that SLC26a2/7 is a ventrally expressed sulfate transporter that promotes a ventral accumulation of sulfated proteoglycans, which is required for ventral PMC positioning and skeletal patterning. We show that the effects of SLC perturbation are mimicked by manipulation of either external sulfate levels or proteoglycan sulfation. These results identify novel skeletal patterning genes and demonstrate that ventral proteoglycan sulfation serves as a positional cue for sea urchin skeletal patterning.",

keywords = "Patterning, RNA-Seq, Skeleton, Sulfated proteoglycan",

author = "Piacentino, {Michael L.} and Zuch, {Daniel T.} and Julie Fishman and Sviatlana Rose and Speranza, {Emily E.} and Christy Li and Jia Yu and Oliver Chung and Janani Ramachandran and Patrick Ferrell and Vijeta Patel and Arlene Reyna and Hajerah Hameeduddin and James Chaves and Hewitt, {Finnegan B.} and Evan Bardot and David Lee and Core, {Amanda B.} and Hogan, {John D.} and Keenan, {Jessica L.} and Lingqi Luo and Jasmin Coulombe-Huntington and Blute, {Todd A.} and Ekaterina Oleinik and Jonas Ibn-Salem and Poustka, {Albert J.} and Bradham, {Cynthia A.}",

note = "Publisher Copyright: {\textcopyright} 2016 Published by The Company of Biologists Ltd.",

year = "2016",

month = feb,

day = "15",

doi = "10.1242/dev.129312",

language = "English",

volume = "143",

pages = "703--714",

journal = "Development (Cambridge)",

issn = "0950-1991",

publisher = "Company of Biologists Ltd",

number = "4",

}

Piacentino, ML, Zuch, DT, Fishman, J, Rose, S, Speranza, EE, Li, C, Yu, J, Chung, O, Ramachandran, J, Ferrell, P, Patel, V, Reyna, A, Hameeduddin, H, Chaves, J, Hewitt, FB, Bardot, E, Lee, D, Core, AB, Hogan, JD, Keenan, JL, Luo, L, Coulombe-Huntington, J, Blute, TA, Oleinik, E, Ibn-Salem, J, Poustka, AJ & Bradham, CA 2016, 'RNA-Seq identifies SPGs as a ventral skeletal patterning cue in sea urchins', Development (Cambridge), vol. 143, no. 4, pp. 703-714. https://doi.org/10.1242/dev.129312

TY - JOUR

T1 - RNA-Seq identifies SPGs as a ventral skeletal patterning cue in sea urchins

AU - Piacentino, Michael L.

AU - Zuch, Daniel T.

AU - Fishman, Julie

AU - Rose, Sviatlana

AU - Speranza, Emily E.

AU - Li, Christy

AU - Yu, Jia

AU - Chung, Oliver

AU - Ramachandran, Janani

AU - Ferrell, Patrick

AU - Patel, Vijeta

AU - Reyna, Arlene

AU - Hameeduddin, Hajerah

AU - Chaves, James

AU - Hewitt, Finnegan B.

AU - Bardot, Evan

AU - Lee, David

AU - Core, Amanda B.

AU - Hogan, John D.

AU - Keenan, Jessica L.

AU - Luo, Lingqi

AU - Coulombe-Huntington, Jasmin

AU - Blute, Todd A.

AU - Oleinik, Ekaterina

AU - Ibn-Salem, Jonas

AU - Poustka, Albert J.

AU - Bradham, Cynthia A.

PY - 2016/2/15

Y1 - 2016/2/15

N2 - The sea urchin larval skeleton offers a simple model for formation of developmental patterns. The calcium carbonate skeleton is secreted by primary mesenchyme cells (PMCs) in response to largely unknown patterning cues expressed by the ectoderm. To discover novel ectodermal cues, we performed an unbiased RNA-Seq-based screen and functionally tested candidates; we thereby identified several novel skeletal patterning cues. Among these, we show that SLC26a2/7 is a ventrally expressed sulfate transporter that promotes a ventral accumulation of sulfated proteoglycans, which is required for ventral PMC positioning and skeletal patterning. We show that the effects of SLC perturbation are mimicked by manipulation of either external sulfate levels or proteoglycan sulfation. These results identify novel skeletal patterning genes and demonstrate that ventral proteoglycan sulfation serves as a positional cue for sea urchin skeletal patterning.

AB - The sea urchin larval skeleton offers a simple model for formation of developmental patterns. The calcium carbonate skeleton is secreted by primary mesenchyme cells (PMCs) in response to largely unknown patterning cues expressed by the ectoderm. To discover novel ectodermal cues, we performed an unbiased RNA-Seq-based screen and functionally tested candidates; we thereby identified several novel skeletal patterning cues. Among these, we show that SLC26a2/7 is a ventrally expressed sulfate transporter that promotes a ventral accumulation of sulfated proteoglycans, which is required for ventral PMC positioning and skeletal patterning. We show that the effects of SLC perturbation are mimicked by manipulation of either external sulfate levels or proteoglycan sulfation. These results identify novel skeletal patterning genes and demonstrate that ventral proteoglycan sulfation serves as a positional cue for sea urchin skeletal patterning.

KW - Patterning

KW - RNA-Seq

KW - Skeleton

KW - Sulfated proteoglycan

UR - http://www.scopus.com/inward/record.url?scp=84958259108&partnerID=8YFLogxK

U2 - 10.1242/dev.129312

DO - 10.1242/dev.129312

M3 - Article

C2 - 26755701

AN - SCOPUS:84958259108

SN - 0950-1991

VL - 143

SP - 703

EP - 714

JO - Development (Cambridge)

JF - Development (Cambridge)

IS - 4

ER -

RNA-Seq identifies SPGs as a ventral skeletal patterning cue in sea urchins

Abstract

Keywords

Access to Document

Fingerprint

Cite this