Sea lamprey
Sea lamprey research offers insight into vertebrate evolution, highlighting similarities in stem cell gene networks with jawed vertebrates and explaining differences in jaw formation. Credit: T. Lawrence, Great Lakes Fishery Commission
These invasive, blood-sucking fish “could hold the key to understanding where we come from.”
One of only two without a jaw vertebratesSea lampreys, which cause significant damage to Midwest fisheries, are also helping scientists understand the origins of two crucial stem cells that played key roles in vertebrate evolution.
Northwestern University Biologists have identified when the genetic network that regulates these stem cells may have evolved and have thus been able to better understand what could be responsible for the absence of mandibles in lampreys.
Both types of cells—pluripotent blastula cells (or embryonic stem cells) and neural crest cells—are both “pluripotent,” meaning they can become every other type of cell in the body.
In a new study, researchers compared genes from the lamprey to those from Xenopus, a jawed aquatic frog. Using comparative transcriptomics, the study revealed a surprisingly similar pluripotency gene network in jawless and jawed vertebrates, even down to the abundance of transcripts for key regulatory factors.
Differences in gene expression
But the researchers also discovered a key difference. While the two species“Blastula cells express the pou5 gene, a key regulator of stem cells, but this gene is not expressed in lamprey neural crest stem cells. Loss of this factor may have limited the ability of neural crest cells to form the cell types found in jawed vertebrates (animals with spines) that make up the skeleton of the head and jaw.
The study was recently published in the journal Nature Ecology & Evolution.
By comparing the biology of jawless and jawed vertebrates, researchers can better understand the evolutionary origins of the characteristics that define vertebrate animals, including humans, how differences in gene expression contribute to key differences in body plan, and what the common ancestor of all vertebrates looked like.
“Lampreys may be the key to understanding our origins,” said Carole LaBonne of Northwestern University, who led the study. “In evolutionary biology, if you want to understand the origins of a trait, you can’t look to more complex vertebrates that evolved independently for 500 million years. You have to go back to the most primitive version of the type of animal you’re studying, which brings us back to hagfish and lampreys, the last living examples of jawless vertebrates.”
An expert in developmental biology, LaBonne is a professor of molecular biosciences in the Weinberg College of Arts and Sciences. She holds the Erastus Otis Haven Chair and is part of the leadership of the National Science Foundation’s (NSF) new Simons National Institute for Theory and Mathematics in Biology.
LaBonne and his colleagues have previously shown that the developmental origin of neural crest cells is linked to the maintenance of the genetic regulatory network that controls pluripotency in blastula stem cells. In the new study, they explored the evolutionary origin of the links between these two stem cell populations.
Importance of neural crest cells
“Neural crest stem cells are like an evolutionary Lego set,” LaBonne said. “They become vastly different cell types, including neurons and muscles, and what all of these cell types have in common is a shared developmental origin within the neural crest.”
While embryonic stem cells at the blastula stage lose their pluripotency and become confined to distinct cell types relatively quickly as the embryo develops, neural crest cells retain the molecular toolkit that controls pluripotency later in development.
LaBonne’s team discovered a completely intact pluripotency network in lamprey blastula cells, stem cells whose role in jawless vertebrates had previously been an open question. This implies that blastula and neural crest stem cell populations from jawed and jawless vertebrates co-evolved at the base of vertebrates.
Joshua York, a postdoctoral researcher and first author at Northwestern University, observed “more similarities than differences” between the lamprey and the Xenopus.
“While most of the genes that control pluripotency are expressed in the lamprey neural crest, expression of one of these key genes – pou5 – was lost from these cells,” York said. “Surprisingly, even though pou5 is not expressed in the neural crest of a lamprey, it could promote neural crest formation when we expressed it in frogs, suggesting that this gene is part of an ancient pluripotency network that was present in our early vertebrate ancestors.”
The experiment also helped them hypothesize that the gene had been specifically lost in certain creatures, and not something that jawed vertebrates developed later.
“Another remarkable finding of the study is that even though these animals are separated by 500 million years of evolution, there are tight constraints on the levels of gene expression needed to promote pluripotency,” LaBonne said. “The big unanswered question is: Why?”
Reference: “Common Features of Blastula and Neural Crest Stem Cells Evolved in the Basis of Vertebrates” by Joshua R. York, Anjali Rao, Paul B. Huber, Elizabeth N. Schock, Andrew Montequin, Sara Rigney, and Carole LaBonne, July 26, 2024, Nature Ecology and Evolution.
DOI: 10.1038/s41559-024-02476-8
The document was funded by the National Institutes of Health (grants R01GM116538 and F32DE029113), the NSF (grant 1764421), the Simons Foundation (grant SFARI 597491-RWC), and the Walder Foundation through the Life Sciences Research Foundation. The study is dedicated to the memory of Dr. Joseph Walder.
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