Transcriptomic, proteomic, and metabolomic landscape of positional memory in the caudal fin of zebrafish

Jeremy S. Rabinowitz, Aaron M. Robitaille, Yuliang Wang, Catherine A. Ray, Ryan Thummel, Haiwei Gu, Danijel Djukovic, Daniel Raftery, Jason D. Berndt, Randall T. Moon

Research output: Contribution to journalArticle

20 Citations (Scopus)

Abstract

Regeneration requires cells to regulate proliferation and patterning according to their spatial position. Positional memory is a property that enables regenerating cells to recall spatial information from the uninjured tissue. Positional memory is hypothesized to rely on gradients of molecules, few of which have been identified. Here, we quantified the global abundance of transcripts, proteins, and metabolites along the proximodistal axis of caudal fins of uninjured and regenerating adult zebrafish. Using this approach, we uncovered complex overlapping expression patterns for hundreds of molecules involved in diverse cellular functions, including development, bioelectric signaling, and amino acid and lipid metabolism. Moreover, 32 genes differentially expressed at the RNA level had concomitant differential expression of the encoded proteins. Thus, the identification of proximodistal differences in levels of RNAs, proteins, and metabolites will facilitate future functional studies of positional memory during appendage regeneration.

Original languageEnglish (US)
Pages (from-to)E717-E726
JournalProceedings of the National Academy of Sciences of the United States of America
Volume114
Issue number5
DOIs
StatePublished - Jan 31 2017
Externally publishedYes

Fingerprint

Metabolomics
Zebrafish
Proteomics
Regeneration
RNA
Proteins
Lipid Metabolism
Amino Acids
Genes

Keywords

  • Caudal fin
  • Growth control
  • Positional memory
  • Regeneration
  • Zebrafish

ASJC Scopus subject areas

  • General

Cite this

Transcriptomic, proteomic, and metabolomic landscape of positional memory in the caudal fin of zebrafish. / Rabinowitz, Jeremy S.; Robitaille, Aaron M.; Wang, Yuliang; Ray, Catherine A.; Thummel, Ryan; Gu, Haiwei; Djukovic, Danijel; Raftery, Daniel; Berndt, Jason D.; Moon, Randall T.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 114, No. 5, 31.01.2017, p. E717-E726.

Research output: Contribution to journalArticle

Rabinowitz, JS, Robitaille, AM, Wang, Y, Ray, CA, Thummel, R, Gu, H, Djukovic, D, Raftery, D, Berndt, JD & Moon, RT 2017, 'Transcriptomic, proteomic, and metabolomic landscape of positional memory in the caudal fin of zebrafish', Proceedings of the National Academy of Sciences of the United States of America, vol. 114, no. 5, pp. E717-E726. https://doi.org/10.1073/pnas.1620755114
Rabinowitz, Jeremy S. ; Robitaille, Aaron M. ; Wang, Yuliang ; Ray, Catherine A. ; Thummel, Ryan ; Gu, Haiwei ; Djukovic, Danijel ; Raftery, Daniel ; Berndt, Jason D. ; Moon, Randall T. / Transcriptomic, proteomic, and metabolomic landscape of positional memory in the caudal fin of zebrafish. In: Proceedings of the National Academy of Sciences of the United States of America. 2017 ; Vol. 114, No. 5. pp. E717-E726.
@article{3b58d8186168496daa362d6a5cec4ea7,
title = "Transcriptomic, proteomic, and metabolomic landscape of positional memory in the caudal fin of zebrafish",
abstract = "Regeneration requires cells to regulate proliferation and patterning according to their spatial position. Positional memory is a property that enables regenerating cells to recall spatial information from the uninjured tissue. Positional memory is hypothesized to rely on gradients of molecules, few of which have been identified. Here, we quantified the global abundance of transcripts, proteins, and metabolites along the proximodistal axis of caudal fins of uninjured and regenerating adult zebrafish. Using this approach, we uncovered complex overlapping expression patterns for hundreds of molecules involved in diverse cellular functions, including development, bioelectric signaling, and amino acid and lipid metabolism. Moreover, 32 genes differentially expressed at the RNA level had concomitant differential expression of the encoded proteins. Thus, the identification of proximodistal differences in levels of RNAs, proteins, and metabolites will facilitate future functional studies of positional memory during appendage regeneration.",
keywords = "Caudal fin, Growth control, Positional memory, Regeneration, Zebrafish",
author = "Rabinowitz, {Jeremy S.} and Robitaille, {Aaron M.} and Yuliang Wang and Ray, {Catherine A.} and Ryan Thummel and Haiwei Gu and Danijel Djukovic and Daniel Raftery and Berndt, {Jason D.} and Moon, {Randall T.}",
year = "2017",
month = "1",
day = "31",
doi = "10.1073/pnas.1620755114",
language = "English (US)",
volume = "114",
pages = "E717--E726",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
number = "5",

}

TY - JOUR

T1 - Transcriptomic, proteomic, and metabolomic landscape of positional memory in the caudal fin of zebrafish

AU - Rabinowitz, Jeremy S.

AU - Robitaille, Aaron M.

AU - Wang, Yuliang

AU - Ray, Catherine A.

AU - Thummel, Ryan

AU - Gu, Haiwei

AU - Djukovic, Danijel

AU - Raftery, Daniel

AU - Berndt, Jason D.

AU - Moon, Randall T.

PY - 2017/1/31

Y1 - 2017/1/31

N2 - Regeneration requires cells to regulate proliferation and patterning according to their spatial position. Positional memory is a property that enables regenerating cells to recall spatial information from the uninjured tissue. Positional memory is hypothesized to rely on gradients of molecules, few of which have been identified. Here, we quantified the global abundance of transcripts, proteins, and metabolites along the proximodistal axis of caudal fins of uninjured and regenerating adult zebrafish. Using this approach, we uncovered complex overlapping expression patterns for hundreds of molecules involved in diverse cellular functions, including development, bioelectric signaling, and amino acid and lipid metabolism. Moreover, 32 genes differentially expressed at the RNA level had concomitant differential expression of the encoded proteins. Thus, the identification of proximodistal differences in levels of RNAs, proteins, and metabolites will facilitate future functional studies of positional memory during appendage regeneration.

AB - Regeneration requires cells to regulate proliferation and patterning according to their spatial position. Positional memory is a property that enables regenerating cells to recall spatial information from the uninjured tissue. Positional memory is hypothesized to rely on gradients of molecules, few of which have been identified. Here, we quantified the global abundance of transcripts, proteins, and metabolites along the proximodistal axis of caudal fins of uninjured and regenerating adult zebrafish. Using this approach, we uncovered complex overlapping expression patterns for hundreds of molecules involved in diverse cellular functions, including development, bioelectric signaling, and amino acid and lipid metabolism. Moreover, 32 genes differentially expressed at the RNA level had concomitant differential expression of the encoded proteins. Thus, the identification of proximodistal differences in levels of RNAs, proteins, and metabolites will facilitate future functional studies of positional memory during appendage regeneration.

KW - Caudal fin

KW - Growth control

KW - Positional memory

KW - Regeneration

KW - Zebrafish

UR - http://www.scopus.com/inward/record.url?scp=85011317315&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85011317315&partnerID=8YFLogxK

U2 - 10.1073/pnas.1620755114

DO - 10.1073/pnas.1620755114

M3 - Article

C2 - 28096348

AN - SCOPUS:85011317315

VL - 114

SP - E717-E726

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 5

ER -