204
Xenopus
networks will create more opportunities for proteomic studies.
We can imagine that in the same way that RNA-sequencing
studies of phenotypes resulting from perturbations are now
commonplace (Kjolby et al., 2017), soon so will be multiplexed proteomics studies of control and perturbed embryos,
perhaps at multiple developmental stages. Not much has been
accomplished to date in the way of proteomic measurements
of the adult frogs, but embryological studies would greatly
beneft from the tissue protein expression atlas in Xenopus,
which is sure to both confrm widespread gene functional
homology but also bring surprises with regard to the tissue
expression differences across species. To date, Xenopus has
not been considered a model organism for aging research,
even though some research into reproductive system aging in
Xenopus has been done (Brocas et al., 1961; Kara, 1994). It is
not clear what the lifespan is or whether Xenopus undergoes
considerable senescence, and thus a proteomic study of aging
tissues presents an attractive direction.
The 2012 Nobel Prize in Physiology or Medicine was
awarded to Sir John Gurdon for his work on nuclear transfer and reprogramming in Xenopus, which he chose for the
ease of injection of somatic nuclei into oocytes. This wellestablished system presents another unfulf lled opportunity
for deep quantitative proteomic characterization.
ACKNOWLEDGMENTS
LP and EVI were supported by NIH grant R01-HD091846.
Illustrations © 2021 Natalya Zahn, CC BY-NC 4.0
REFERENCES
Briggs JA, Weinreb C, Wagner DE, Megason S, Peshkin L,
Kirschner MW, Klein AM. The dynamics of gene expression in vertebrate embryogenesis at single-cell resolution.
Science. 2018 Jun 1;360(6392):eaar5780. doi: 10.1126/
science.aar5780. PMID: 29700227; PMCID: PMC6038144.
Brocas J, Verzar F. The aging of Xenopus laevis, a South African frog.
Gerontologia. 1961;5:228–240. doi: 10.1159/000211062.
PMID: 13873222.
Chang C. Animal cap assay for TGF-β signaling. Methods Mol
Biol. 2016;1344:261–274. doi: 10.1007/978-1-4939-29665_16. PMID: 26520130.
Cheung TK, Lee CY, Bayer FP, McCoy A, Kuster B, Rose CM.
Defning the carrier proteome limit for single-cell proteomics. Nat Methods. 2020 Dec 7. doi: 10.1038/s41592020-01002-5. PMID: 33288958.
Cook ND. The case for reverse translation. J Theor Biol. 1977
Jan 7;64(1):113–135. doi: 10.1016/0022-5193(77)90116-3.
PMID: 319301.
Drew K, Lee C, Cox RM, Dang V, Devitt CC, McWhite CD,
Papoulas O, Huizar RL, Marcotte EM, Wallingford JB. A
systematic, label-free method for identifying RNA-associated
proteins in vivo provides insights into vertebrate ciliary beating machinery. Dev Biol. 2020 Nov 1;467(1–2):108–117. doi:
10.1016/j.ydbio.2020.08.008. PMID: 32898505; PMCID: PMC
7668317.
Gilchrist MJ, Veenstra GJC, Cho KWY. Transcriptomics and proteomics methods for Xenopus embryos and tissues. Cold Spring
Harb Protoc. 2020 Feb 3;2020(2):098350. doi: 10.1101/pdb.
top098350. PMID: 31772075; PMCID: PMC7362671.
Gupta M, Sonnett M, Ryazanova L, Presler M, Wühr M. Quantitative
proteomics of Xenopus embryos I, sample preparation.
Methods Mol Biol. 2018;1865:175–194. doi: 10.1007/978-14939-8784-9_13. PMID: 30151767; PMCID: PMC6564683.
Gurdon JB, Wakefeld L. Microinjection of amphibian oocytes
and eggs for the analysis of transcription. Microinjection
and Organelle Transplantation Techniques, eds Celis JE,
Graessmann A, Loyter A (Academic, London). 1986: 269–299.
Harland RM. A new view of embryo development and regeneration. Science. 2018 Jun 1;360(6392):967–968. doi: 10.1126/
science.aat8413. PMID: 29853675.
Hellsten U, Harland RM, Gilchrist MJ, Hendrix D, Jurka J,
Kapitonov V, Ovcharenko I, Putnam NH, Shu S, Taher L,
Blitz IL, Blumberg B, Dichmann DS, Dubchak I, Amaya
E, Detter JC, Fletcher R, Gerhard DS, Goodstein D, Graves
T, Grigoriev IV, Grimwood J, Kawashima T, Lindquist E,
Lucas SM, Mead PE, Mitros T, Ogino H, Ohta Y, Poliakov
AV, Pollet N, Robert J, Salamov A, Sater AK, Schmutz J,
Terry A, Vize PD, Warren WC, Wells D, Wills A, Wilson
RK, Zimmerman LB, Zorn AM, Grainger R, Grammer T,
Khokha MK, Richardson PM, Rokhsar DS. The genome of
the Western clawed frog Xenopus tropicalis. Science. 2010
Apr 30;328(5978):633–636. doi: 10.1126/science.1183670.
PMID: 20431018; PMCID: PMC2994648.
Horb M, Abu-Daya, A, Wlizla, M, Noble, A, Guille M. This Volume.
Chapter 14. Advances in Genome Editing Tools. 2021.
Kara TC. Ageing in amphibians. Gerontology. 1994;40(2–4):
161–173. doi: 10.1159/000213585. PMID: 7926854.
Karimi K, Fortriede JD, Lotay VS, Burns KA, Wang DZ, Fisher
ME, Pells TJ, James-Zorn C, Wang Y, Ponferrada VG, Chu S,
Chaturvedi P, Zorn AM, Vize PD. Xenbase: A genomic, epigenomic and transcriptomic model organism database. Nucleic
Acids Res. 2018 Jan 4;46(D1):D861–D868. doi: 10.1093/
nar/gkx936. PMID: 29059324; PMCID: PMC5753396.
Kjolby RAS, Harland RM. Genome-wide identif cation of Wnt/βcatenin transcriptional targets during Xenopus gastrulation.
Dev Biol. 2017 Jun 15;426(2):165–175. doi: 10.1016/j.ydbio.
2016.03.021. PMID: 27091726; PMCID: PMC6288011.
Klein AM, Mazutis L, Akartuna I, Tallapragada N, Veres A, Li
V, Peshkin L, Weitz DA, Kirschner MW. Droplet barcoding for single-cell transcriptomics applied to embryonic
stem cells. Cell. 2015 May 21;161(5):1187–1201. doi:
10.1016/j.cell.2015.04.044. PMID: 26000487; PMCID:
PMC4441768.
Lee C, Cox RM, Papoulas O, Horani A, Drew K, Devitt CC, Brody
SL, Marcotte EM, Wallingford JB. Functional partitioning of
a liquid-like organelle during assembly of axonemal dyneins.
Elife. 2020 Dec 2;9:e58662. doi: 10.7554/eLife.58662.
PMID: 33263282; PMCID: PMC7785291.
Leibovich A, Edri T, Klein SL, Moody SA, Fainsod A. Natural size
variation among embryos leads to the corresponding scaling in gene expression. Dev Biol. 2020 Jun 15;462(2):165–
179. doi: 10.1016/j.ydbio.2020.03.014. PMID: 32259520;
PMCID: PMC8073595.
Lim MY, O’Brien J, Paulo JA, Gygi SP. Improved method for
determining absolute phosphorylation stoichiometry using
Bayesian statistics and isobaric labeling. J Proteome Res.
2017 Nov 3;16(11):4217–4226. doi: 10.1021/acs.jproteome.
7b00571. PMID: 28985074; PMCID: PMC6301010.
Lindeboom RGH, Smits AH, Perino M, Veenstra GJC, Vermeulen
M. Mass spectrometry-based absolute quantifcation of single Xenopus embryo proteomes. Cold Spring Harb Protoc.
Xenopus
networks will create more opportunities for proteomic studies.
We can imagine that in the same way that RNA-sequencing
studies of phenotypes resulting from perturbations are now
commonplace (Kjolby et al., 2017), soon so will be multiplexed proteomics studies of control and perturbed embryos,
perhaps at multiple developmental stages. Not much has been
accomplished to date in the way of proteomic measurements
of the adult frogs, but embryological studies would greatly
beneft from the tissue protein expression atlas in Xenopus,
which is sure to both confrm widespread gene functional
homology but also bring surprises with regard to the tissue
expression differences across species. To date, Xenopus has
not been considered a model organism for aging research,
even though some research into reproductive system aging in
Xenopus has been done (Brocas et al., 1961; Kara, 1994). It is
not clear what the lifespan is or whether Xenopus undergoes
considerable senescence, and thus a proteomic study of aging
tissues presents an attractive direction.
The 2012 Nobel Prize in Physiology or Medicine was
awarded to Sir John Gurdon for his work on nuclear transfer and reprogramming in Xenopus, which he chose for the
ease of injection of somatic nuclei into oocytes. This wellestablished system presents another unfulf lled opportunity
for deep quantitative proteomic characterization.
ACKNOWLEDGMENTS
LP and EVI were supported by NIH grant R01-HD091846.
Illustrations © 2021 Natalya Zahn, CC BY-NC 4.0
REFERENCES
Briggs JA, Weinreb C, Wagner DE, Megason S, Peshkin L,
Kirschner MW, Klein AM. The dynamics of gene expression in vertebrate embryogenesis at single-cell resolution.
Science. 2018 Jun 1;360(6392):eaar5780. doi: 10.1126/
science.aar5780. PMID: 29700227; PMCID: PMC6038144.
Brocas J, Verzar F. The aging of Xenopus laevis, a South African frog.
Gerontologia. 1961;5:228–240. doi: 10.1159/000211062.
PMID: 13873222.
Chang C. Animal cap assay for TGF-β signaling. Methods Mol
Biol. 2016;1344:261–274. doi: 10.1007/978-1-4939-29665_16. PMID: 26520130.
Cheung TK, Lee CY, Bayer FP, McCoy A, Kuster B, Rose CM.
Defning the carrier proteome limit for single-cell proteomics. Nat Methods. 2020 Dec 7. doi: 10.1038/s41592020-01002-5. PMID: 33288958.
Cook ND. The case for reverse translation. J Theor Biol. 1977
Jan 7;64(1):113–135. doi: 10.1016/0022-5193(77)90116-3.
PMID: 319301.
Drew K, Lee C, Cox RM, Dang V, Devitt CC, McWhite CD,
Papoulas O, Huizar RL, Marcotte EM, Wallingford JB. A
systematic, label-free method for identifying RNA-associated
proteins in vivo provides insights into vertebrate ciliary beating machinery. Dev Biol. 2020 Nov 1;467(1–2):108–117. doi:
10.1016/j.ydbio.2020.08.008. PMID: 32898505; PMCID: PMC
7668317.
Gilchrist MJ, Veenstra GJC, Cho KWY. Transcriptomics and proteomics methods for Xenopus embryos and tissues. Cold Spring
Harb Protoc. 2020 Feb 3;2020(2):098350. doi: 10.1101/pdb.
top098350. PMID: 31772075; PMCID: PMC7362671.
Gupta M, Sonnett M, Ryazanova L, Presler M, Wühr M. Quantitative
proteomics of Xenopus embryos I, sample preparation.
Methods Mol Biol. 2018;1865:175–194. doi: 10.1007/978-14939-8784-9_13. PMID: 30151767; PMCID: PMC6564683.
Gurdon JB, Wakefeld L. Microinjection of amphibian oocytes
and eggs for the analysis of transcription. Microinjection
and Organelle Transplantation Techniques, eds Celis JE,
Graessmann A, Loyter A (Academic, London). 1986: 269–299.
Harland RM. A new view of embryo development and regeneration. Science. 2018 Jun 1;360(6392):967–968. doi: 10.1126/
science.aat8413. PMID: 29853675.
Hellsten U, Harland RM, Gilchrist MJ, Hendrix D, Jurka J,
Kapitonov V, Ovcharenko I, Putnam NH, Shu S, Taher L,
Blitz IL, Blumberg B, Dichmann DS, Dubchak I, Amaya
E, Detter JC, Fletcher R, Gerhard DS, Goodstein D, Graves
T, Grigoriev IV, Grimwood J, Kawashima T, Lindquist E,
Lucas SM, Mead PE, Mitros T, Ogino H, Ohta Y, Poliakov
AV, Pollet N, Robert J, Salamov A, Sater AK, Schmutz J,
Terry A, Vize PD, Warren WC, Wells D, Wills A, Wilson
RK, Zimmerman LB, Zorn AM, Grainger R, Grammer T,
Khokha MK, Richardson PM, Rokhsar DS. The genome of
the Western clawed frog Xenopus tropicalis. Science. 2010
Apr 30;328(5978):633–636. doi: 10.1126/science.1183670.
PMID: 20431018; PMCID: PMC2994648.
Horb M, Abu-Daya, A, Wlizla, M, Noble, A, Guille M. This Volume.
Chapter 14. Advances in Genome Editing Tools. 2021.
Kara TC. Ageing in amphibians. Gerontology. 1994;40(2–4):
161–173. doi: 10.1159/000213585. PMID: 7926854.
Karimi K, Fortriede JD, Lotay VS, Burns KA, Wang DZ, Fisher
ME, Pells TJ, James-Zorn C, Wang Y, Ponferrada VG, Chu S,
Chaturvedi P, Zorn AM, Vize PD. Xenbase: A genomic, epigenomic and transcriptomic model organism database. Nucleic
Acids Res. 2018 Jan 4;46(D1):D861–D868. doi: 10.1093/
nar/gkx936. PMID: 29059324; PMCID: PMC5753396.
Kjolby RAS, Harland RM. Genome-wide identif cation of Wnt/βcatenin transcriptional targets during Xenopus gastrulation.
Dev Biol. 2017 Jun 15;426(2):165–175. doi: 10.1016/j.ydbio.
2016.03.021. PMID: 27091726; PMCID: PMC6288011.
Klein AM, Mazutis L, Akartuna I, Tallapragada N, Veres A, Li
V, Peshkin L, Weitz DA, Kirschner MW. Droplet barcoding for single-cell transcriptomics applied to embryonic
stem cells. Cell. 2015 May 21;161(5):1187–1201. doi:
10.1016/j.cell.2015.04.044. PMID: 26000487; PMCID:
PMC4441768.
Lee C, Cox RM, Papoulas O, Horani A, Drew K, Devitt CC, Brody
SL, Marcotte EM, Wallingford JB. Functional partitioning of
a liquid-like organelle during assembly of axonemal dyneins.
Elife. 2020 Dec 2;9:e58662. doi: 10.7554/eLife.58662.
PMID: 33263282; PMCID: PMC7785291.
Leibovich A, Edri T, Klein SL, Moody SA, Fainsod A. Natural size
variation among embryos leads to the corresponding scaling in gene expression. Dev Biol. 2020 Jun 15;462(2):165–
179. doi: 10.1016/j.ydbio.2020.03.014. PMID: 32259520;
PMCID: PMC8073595.
Lim MY, O’Brien J, Paulo JA, Gygi SP. Improved method for
determining absolute phosphorylation stoichiometry using
Bayesian statistics and isobaric labeling. J Proteome Res.
2017 Nov 3;16(11):4217–4226. doi: 10.1021/acs.jproteome.
7b00571. PMID: 28985074; PMCID: PMC6301010.
Lindeboom RGH, Smits AH, Perino M, Veenstra GJC, Vermeulen
M. Mass spectrometry-based absolute quantifcation of single Xenopus embryo proteomes. Cold Spring Harb Protoc.