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In memory of Syndey Brenner: his part of the discovery of messenger RNA

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All biology undergraduates learn the central dogma: DNA makes RNA and RNA makes protein. However, not long ago, this dogma was intensely debated because it was unclear if DNA or protein contained the genetic material of the cell. The famous double helix model opened the door to molecular biology in 1953. But it took an additional eight years to discover the messenger RNA. Sydney Brenner, who shared the 2002 Nobel Prize in Physiology or Medicine, was a key traveler in this long journey.  

Portrait photograph of Sydney Brenner, c. 1960s,  Copyright: MRC Laboratory of Molecular Biology

As described in his autobiography, My life in Science , Brenner thought about how genetic information guides protein synthesis even before he saw the double helix model in April 1953 at Cambridge. Inspired by the similar step size of nucleic acid (3.5 angstrom units) and amino acids (3.3 angstrom units) pointed out in William Astbury’s 1947 paper, Brenner developed his “pet theory” that amino acids join together at the same time nucleic acid strands are synthesized. At the time, people knew that DNA sequences defined proteins, but it was not clear whether there was an intermediate molecule between DNA and protein. With the discovery that protein synthesis occurs at ribosomes, it was largely assumed that the intermediate was the ribosomal RNA (rRNA). However, some people were skeptical about this. One reason for this skepticism was that in bacteria, the ratio of the amount of G+C to A+T in DNA varied a lot between bacteria species, while in rRNA the variation was trivial.

Another concern was what Brenner called the “paradox of the prodigious rate of protein synthesis.” While working with bacteriophages at Cambridge, Brenner and Francis Crick observed that after phage infection, 70% of protein made in the infected bacteria was the phage head protein instead of the bacteria protein. If rRNA is the intermediate for protein synthesis, a significant increase of new rRNA should be observed. However, there was no detectable rRNA synthesis. In 1956, Elliot Volkin and Lazarus Astrachan discovered that a small amount of short-lived RNA resembles the phage DNA in base composition rather than the bacterial DNA after phage infection, however, they were kind of focused on the idea that these new RNA could be the precursor of phage DNA. 

Four years later, the secret of the mysterious Volkin-Astrachan RNA was uncovered in Brenner’s living room. It was during an informal meeting of a small group of scientists, including Crick and François Jacob from Institut Pasteur in France. Jacob described the new findings from the famous Pa rdee, Ja cob and Mo nod (PaJaMo) mating experiment. Normally, bacteria synthesize galactosidase in a medium containing lactose. However, the lac- mutant cannot digest lactose until the gene that encodes the galactosidase is transferred into the cell. Galactosidase synthesis is extremely rapid, happening within minutes. Interestingly, when they let the bacteria produce galactosidase for some minutes and then destroyed the transferred DNA, galactosidase synthesis stopped immediately. These results ruled out the possibility of any stable intermediate like rRNA because if the intermediate were stable, galactosidase synthesis should have continued for a while after the gene was removed. Upon hearing Jacob’s description, suddenly, Brenner got excited and shouted to Crick, “Volkin-Astrachan; information intermediate; it’s short-lived; a short-lived intermediate! It must be! Look at the way it turns over in phage!”

The next step was to plan experiments testing whether the short-lived RNA was the intermediate messenger that guides protein synthesis. If Brenner’s hypothesis was correct, then the new RNA intermediate synthesized after phage infection should be associated with the old bacterial ribosomes.To do this, they needed a way to distinguish between the ‘new’ and ‘old’ ribosomes. Lucky for them, Matthew Meselson and Frank Stahl at California Institute of Technology (Caltech) developed the density gradient centrifugation experiment and successfully separated the isotope N 15 -labeled DNA from the N 14 DNA in a caesium chloride solution. The RNA intermediate experiment could use this approach to label bacterial ribosomes with isotopes before phage infection and resuspended in the medium without isotopes right after infection, which would make the old ribosomes heavier than the new ribosomes and therefore distinguishable by density gradient centrifugation. 

Jacob and Brenner went to Matt Meselson’s lab in California the following summer to test their new hypothesis. The experiment that followed was, as described by Brenner himself, a “hilarious story”. The experiment itself was complex, isotopes were expensive, samples needed to be spun in the centrifuges for nearly 20 hours or more, and the centrifuges were unreliable. And they only had three weeks! The first problem Jacob and Brenner encountered was that the ribosomes were not stable and dissociated during sedimentation in the centrifuge. They tried to troubleshoot, but to no avail. They even thought of purifying ribosomes from Dead Sea bacteria because they already live in a high salt environment and might be more tolerant of the high concentration of caesium chloride. Unfortunately, their phage couldn’t infect the Dead Sea bacteria. 

Frustrated and tired, they went to a nearby beach to, in Brenner’s own words, “rest their weary souls”. Jacob recalled this time in his autobiography: “There we were, collapsed on the sand, stranded in the sunlight like beached whales. My head felt empty. Growing, knitting his heavy eyebrows, with a nasty look, Sydney gazed at the horizon without saying a word.” Lying on the beach, it occurred to Brenner that magnesium stabilizes the ribosomes and the high caesium could displace the magnesium, making the ribosomes unstable! They ran back to the lab and set up their last-chance experiment of three samples with higher magnesium concentrations. During the chaos, Jacob dropped the radioactive phosphate in the water bath and the centrifuge broke down in the middle of the experiment! Luckily, they were able to borrow a centrifuge from a neighboring lab. Nervously, Brenner carried the rotor with the tubes to the cold room. He walked there because the elevator would shake the tubes, destroying the gradient he had worked so hard to create. In the end, they managed to finish the experiment and showed that the new radioactive RNA peaked at the same position with the old ribosomes! Later, these results were published in Nature in 1961, along with the discovery from James Watson’s lab that a fraction of rapidly labeled RNA of different sizes were associated with the ribosome active site (where protein synthesis happens). That same month, the term “messenger RNA” and it’s possible role in gene regulation was discussed in Jacob and Monod’s review article in Journal of Molecular Biology .

Even today, the exploration of messenger RNA never ends. I’m fascinated with how the friendship between scientists, critical thinking, effective communication, and collaboration all contributed to the discovery of messenger RNA. When we hear stories about scientific discoveries, it often sounds like a genius just appeared and came up with an idea that changed the world. But Sydney Brenner’s story shows that it’s not that simple. Scientists can make wrong hypotheses, create naive models and misinterpret results. Sometimes, experiments won’t work; sometimes people tell you not to try an experiment because it is unlikely to work; sometimes you get weird results; sometimes people question and laugh at your hypothesis. But sometimes you make fascinating discoveries. Sydney Brenner passed away in April 2019 at the age of 92. Brenner’s obsession with science, creative thinking, open mindedness, and persistent pursuit of answers will continue to inspire scientists like myself.

• Brenner, Sydney. My Life in Science . London, 2001.
• Hernandez, Victoria, “The Meselson-Stahl Experiment (1957–1958), by Matthew Meselson and Franklin Stahl”. Embryo Project Encyclopedia (2017-04-18). ISSN: 1940-5030 http://embryo.asu.edu/handle/10776/11481
• Meselson, Matthew, and Franklin W. Stahl. “The replication of DNA in Escherichia coli.” Proceedings of the national academy of sciences 44.7 (1958): 671-682.
• Brenner, Sydney, François Jacob, and Matthew Meselson. “An unstable intermediate carrying information from genes to ribosomes for protein synthesis.” Nature 190.4776 (1961): 576-581.
• Gros, François, et al. “Unstable ribonucleic acid revealed by pulse labelling of Escherichia coli.” Nature 190.4776 (1961): 581-585.
• Morange, Michel. “What history tells us XLV. The ‘instability’ of messenger RNA.” Journal of biosciences 43.2 (2018): 229-233.
• Cobb, Matthew. “Who discovered messenger RNA?.” Current Biology 25.13 (2015): R526-R532.

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Lazarus Astrachan, 78, Conducted RNA Studies

By Nicholas Wade

• Aug. 2, 2003

Dr. Lazarus Astrachan, a geneticist who conducted a famous experiment in the field of molecular biology, died on Sunday while visiting Israel. He was 78.

The cause was cancer, family members said.

Dr. Astrachan's experiment, performed with Dr. Elliot Volkin at the Oak Ridge National Laboratory in Tennessee, at first greatly puzzled biologists, but it eventually led to the discovery of messenger RNA, a pivotal actor in the operation of living cells.

At the time of his experiment, in 1957, the foremost problem in biology was to figure out how the hereditary information encoded in DNA was used by living cells to synthesize the proteins that are their working parts.

The structure of DNA, which resides in the nucleus of cells, had been discovered four years earlier by James Watson and Francis Crick. But proteins were known to be synthesized on miniature factories known as ribosomes, which are found outside the nucleus.

The belief at the time was that the ribosomes must be made in the nucleus, each imbued by the DNA with the information to make a certain kind of protein, and then exported to the cell's periphery. The chief ingredient of ribosomes is RNA, a close chemical cousin of DNA, which seemed capable in principle of carrying the same information.

The Volkin-Astrachan experiment showed that there were two kinds of RNA, a long-lived type found in the ribosomes and a transitory kind whose role was unclear. They also showed that the transitory kind was made when a virus invaded bacteria and that it resembled the virus's DNA, not the bacterium's.

Dr. Astrachan was then just 32, with a newly minted doctorate. His findings were not warmly embraced because they did not fit in with prevailing theory. But he and Dr. Volkin repeated their experiment several times, and the result seemed solid, even though anomalous.

At a meeting in Cambridge, England, in April 1960, Dr. Crick and his colleague Dr. Sydney Brenner were comparing notes on the protein synthesis problem with their French colleague François Monod.

During the conversation, Horace Freeland Judson wrote in his history of molecular biology, ''The Eighth Day of Creation,'' Dr. Brenner realized there must be a missing ingredient that carried information from the DNA in the cell's nucleus to the ribosomes in its periphery.

This ingredient, he conjectured, must be the same as the transitory form of RNA seen in the Volkin-Astrachan experiment.

Dr. Astrachan moved in 1961 to Case Western Reserve University, where he spent the rest of his career, retiring in 1990.

He was married for 50 years to Myrtle Bergman Astrachan, a psychologist. After her death he became friends with Dr. Nancy Caroline, a pioneer in the training of emergency medical technicians and the founder of the Hospice of the Upper Galilee in Israel. They were married in 2002, a few months before she died.

Dr. Astrachan is survived by his sons, Eric, of Wooster, Ohio, and Paul, of Austin, Tex.; a sister, Edith Schindler, of Palm Harbor, Fla.; and two grandchildren.

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• Correspondence
• Published: 29 November 2001

Messenger RNA: origins of a discovery

• Alvin M. Weinberg 1  

Nature volume  414 ,  page 485 ( 2001 ) Cite this article

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In his review of James Watson's Genes, Girls and Gamow (see Nature 413 , 775–776; 2001; clarification Nature 414 , 487; 2001), Horace Judson attributes the discovery of messenger RNA to François Jacob, Sydney Brenner and Matthew Meselson.

In fact, Jacob, Brenner and Francis Crick, at an informal meeting on Good Friday 1960, suddenly 'discovered' the unique RNA found first in 1956 by Elliot Volkin and Lazarus Astrachan. Good accounts of this event can be found in The Statue Within by Jacob and What Mad Pursuit by Crick.

In several publications in 1958, Volkin and Astrachan thoroughly described the unusual properties of this RNA, which they termed DNA-like RNA. These were precisely the properties that Jacob and Jacques Monod sought to assign to the unstable intermediate (which they called X), necessary for the synthesis of galactosidase.

Out of that Good Friday discussion on the lactose operon came the realization that Volkin and Astrachan's DNA-like RNA was indeed the genetic messenger, hence messenger RNA (mRNA).

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Weinberg, A. Messenger RNA: origins of a discovery. Nature 414 , 485 (2001). https://doi.org/10.1038/35107234

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Illuminating mRNA

In 1956, ORNL biologists Elliot "Ken" Volkin and Lazarus Astrachan observed the role that RNA plays when a virus infects a bacterium. Five years later, French scientists François Jacob and Jacques Monod further illuminated the function of mRNA, for which they received the 1965 Nobel Prize in Medicine and Physiology.

Insights into the role of RNA

Elliot Volkin

The COVID-19 pandemic has added a lot of new terms to daily conversation. Phrases like “mask mandate” and “social distancing” will probably fall into disuse when COVID-19 passes from the scene. However, “mRNA vaccine,” is likely to have more staying power.

mRNA is a specialized type of RNA — a molecule that’s similar to its cousin, DNA, the molecule that carries genetic information in all known forms of life.

Early studies

Studies on the structure of RNA were done at ORNL in the early 1950s by biologist, Elliot “Ken” Volkin and biochemist Waldo Cohn. They used radioisotope and chromatography techniques that were originally developed for plutonium production at the laboratory’s Graphite Reactor during World War II.

In 1956, further research by Volkin and ORNL biologist Lazarus Astrachan enabled them to observe the role that RNA plays when a virus infects a bacterium. This interaction proved to be critical to understanding the role that RNA plays in viral infections.

Paul Berg, winner of the 1980 Nobel Prize in chemistry, said Volkin and Astrachan discovered that when a bacteriophage virus infects a bacterium, “the virus ‘turns off’ the [bacterial] cell’s machinery for making its own proteins and ‘instructs’ the cell’s machinery to make proteins characteristic of the virus. That instruction entails making a new kind of RNA, a copy of the virus’s DNA. This discovery revealed a fundamental mechanism for gene action: the coding sequences of genes are copied into short-lived RNAs that are transported out of the nucleus into the cytoplasm, where they are translated into proteins.

“Because such RNAs transport information from genes in the nucleus to the cytoplasm they are designated as messenger RNAs.”

Former ORNL director, Alvin Weinberg said that Berg described these studies on messenger RNA (mRNA) as an “unsung but momentous discovery of a fundamental mechanism in genetic chemistry” and a “seminal discovery [that] has never received its proper due.”

DNA-like RNA

Volkin and Astrachan called this new kind of RNA “DNA-like RNA” and spent several years investigating its behavior. Their findings, published in 1956, received a less-than-enthusiastic reception in the biology community. Volkin reportedly thought that the findings weren’t widely accepted because they didn’t agree with theory at the time — even though he and Astrachan repeated the studies several times with the same results.

Five years later, French scientists François Jacob and Jacques Monod published a paper that further illuminated the function of mRNA, an accomplishment for which they received the 1965 Nobel Prize in Medicine and Physiology.

The success of mRNA vaccines in slowing the COVID-19 pandemic, makes it likely that we will soon see efforts to apply similar technology to the task of warding off a range of infectious diseases. It also illustrates the importance of basic scientific research — like Volkin and Astrachan’s findings — which, although they were dismissed at the time, ultimately helped to pave the way for a new class of pandemic-beating vaccines. —Jim Pearce

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A THEORY ON THE MECHANISM OF MESSENGER-RNA SYNTHESIS *

Geoffrey zubay.

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What history tells us XLV. The ‘instability’ of messenger RNA

• Published: 23 April 2018
• Volume 43 , pages 229–233, ( 2018 )

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I am indebted to David Marsh for his critical reading of the manuscript, and to the anonymous reviewer for her or his very helpful comments.

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Morange, M. What history tells us XLV. The ‘instability’ of messenger RNA. J Biosci 43 , 229–233 (2018). https://doi.org/10.1007/s12038-018-9760-7

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Issue Date : June 2018

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