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Alexander Spirin (1931–2020): a Visionary Scientist, a Teacher, a Colleague, a Friend RETROSPECTIVE Valentina Evdokimovaa, Yuri Svitkinb, and Nahum Sonenbergb,1

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Alexander Spirin (1931–2020): a Visionary Scientist, a Teacher, a Colleague, a Friend RETROSPECTIVE Valentina Evdokimovaa, Yuri Svitkinb, and Nahum Sonenbergb,1 RETROSPECTIVE Alexander Spirin (1931–2020): A visionary scientist, a teacher, a colleague, a friend RETROSPECTIVE Valentina Evdokimovaa, Yuri Svitkinb, and Nahum Sonenbergb,1 There was a blizzard on the earth, In every corner, A candle was burning on the desk A candle burning Boris Pasternak, 1946 Alexander Sergeevich Spirin, an international member of the National Academy of Sciences, recited this poem by Boris Pasternak while lecturing to the bright minds nourished by him. Fatefully, he passed away on the snowy day of December 30, 2020, extinguishing one of the brightest candles, but leaving behind many others that he had set alight. Alex received his PhD degree from the A. N. Bach Institute of Biochemistry (Moscow) in 1957 under the mentorship of Andrey N. Belozersky, who in the 1930s discovered the universal occurrence of DNA in plants, previously assumed to exist only in animals. This was the time of the Khrushchev thaw and a period of intellectual exuberance in the Soviet Union and the world, with the discovery of the double helix by James Watson and Francis Crick. The first “student” whom Alex tutored in molecular biology was the President of the United Soviet Socialist Republic (USSR) Acad- emy of Sciences, Mstislav Keldysh, who was greatly Alexander Spirin in the classroom. Image credit: Institute enchanted by the new and enlightening science. of Protein Research. He granted Alex an opportunity to create a new Institute—the Institute of Protein Research—which was alive amid the blizzard of political and economic reali- cofounded by Alex and Oleg Ptitsyn in 1967. It is lo- cated just outside Moscow in the town of Pushchino, a ties of the country that, until 1991, was the USSR. Alex was a member of the Russian Academy of small academic center that had been especially built for biological research 10 years earlier. Alex’s philoso- Sciences, distinguished Professor and the head of phy was simple, but one often forsaken in modern sci- Department of Molecular Biology of Moscow State ence: Only scientific knowledge and the ability to University for almost half a century. His force of envision new directions in research are meritorious, personality, his dedicated teaching, monographs, — Ribosomes and the success of the individual depends on the team- and textbooks including the acclaimed work of many. At his institution, one of the best known (1)—shaped the directions of groundbreaking studies in the world dedicated to protein research, Alex cre- performed under his leadership or inspired by him. ated an intellectual hub, bringing together physicists, His lectures were renowned at the Faculty of Biology, structural biologists, and biochemists. It was his strong Moscow State University, with students and researchers belief that it is not past discovery, but the people and from around the city packing the auditorium to listen to scientific culture that propel new directions in science. Alex’s lectures on a myriad of topics, never repeating Alex and his team kept the fire of world-class science the same lecture twice. aDepartment of Computational Biology, Ontario Institute for Cancer Research, Toronto, ON M5G 0A3, Canada; and bDepartment of Biochemistry, Goodman Cancer Research Center, McGill University, Montreal, QC H3A 1A3, Canada Author contributions: V.E., Y.S., and N.S. wrote the paper. The authors declare no competing interest. Published under the PNAS license. 1To whom correspondence may be addressed. Email: [email protected]. Published April 2, 2021. PNAS 2021 Vol. 118 No. 14 e2103938118 https://doi.org/10.1073/pnas.2103938118 | 1of3 Downloaded by guest on October 4, 2021 While studying the correlation between RNA and Tom Steitz, and Venki Ramakrishnan. At the beginning DNA base compositions in different bacterial species, of the 1980s, Alex was directing several large groups Alex and Belozersky concluded that the large variabil- of scientists studying virtually every aspect of the ribo- ity in DNA base composition between species is some’s structure and function. The most notable were not reflected in the RNA. They postulated the exis- two groups, one led by Maria Garber with Sergei Tra- tence of a relatively minor fraction of species-specific khanov and Vladimir Shirokov, and the other led by (protein-coding) RNA hidden among a large mass of Alex with Marat Yusupov and Gulnara Yusupova. Six noncoding RNA, which was later recognized as evolu- years after the report of the first crystallization of ribo- tionarily conserved ribosomal RNA. The seminal work somal subunits by Yonath and Wittmann, the Garber– was published in Nature in 1958 (2), prompting re- Spirin team published the three-dimensional crystals searchers to reconsider the existing protein-coding of the 70S ribosomes and 30S subunit from Thermus models, proposed earlier by Crick and other promi- thermophilus (7). The 30S structure was subsequently nent leaders in the field. Subsequently, Jacob and solved by Ramakrishnan. Unfortunately, given limited Monod named this minor fraction of RNA “messenger resources in the Soviet Union, the momentum was RNA” (mRNA). lost, but Gulnara and Marat Yusupov continued to This paper set forth Alex’s life-long love affair with work on the ribosome crystallography project first in studying the structure and function of the ribosome. France, then in Harry Noller’s laboratory at the Univer- In the early 1960s, he proposed a model of the trans- sity of California, Santa Cruz, and solved the crystal lating ribosome, whereby the ribosome oscillates structure of the 70S ribosome–mRNA–tRNA complex between locked and unlocked states during the elon- (8), further fulfilling Alex’s dream. gation cycle of protein synthesis. He suggested that In hindsight, the road that leads to scientific dis- the principles of molecular Brownian ratchet machines coveries often seems straight and obvious. But when could explain the unidirectional translocation of standing at the head of the road, the ability to imagine mRNA and bound transfer RNA (tRNA) in the ribo- new paths, and to pursue a trail that may look “unlikely” some (3). Structural mobility of the ribosome during or “unfashionable” to others is a rare gift, a trademark translation was experimentally confirmed by Alex in of a truly exceptional visionary scientist. This requires collaboration with Lydia Gavrilova in 1976, by showing character and a good sense of direction, which cannot that thermal energy alone is sufficient to drive transla- be substituted by the most advanced technologies. tion under special conditions in the absence of elon- Alex had both of these qualities in abundance. gation factors and GTP (factor-free or “nonenzymatic” One of his visionary ideas, which is now coming translation) (4). In hindsight, this experiment had im- into full light, was articulated by Alex in FEBS Letters in portant evolutionary implications, as it was the first 1978 (9). Here, Alex discussed that in eukaryotes, spe- hint in support of the concept of an early RNA-based cific subsets of proteins are associated with mRNA at ribosome that did not need protein factors. different stages of its life, such as processing, nucleo- In the early 1980s, together with Nadezhda Belitsina cytoplasmic transport, functional activity, and decay. and Gulnara Yusupova (Tnalina), Alex demonstrated Concentration of these proteins near the sites of their the ribosomal template-free synthesis of polypeptides function, so-called compartmentalization, is of utmost from aminoacyl-tRNAs, driven by EF-Tu and EF-G importance in the eukaryotic cell, given its size, which elongation factors (5). In the same years, Alex formu- is about three orders-of-magnitude greater than that lated basic principles of the ribosome structure, such of prokaryotic cells. An important aspect of this hy- as the folding of ribosomal RNA and the assembly of pothesis is that mRNAs can be stored in a form of free, ribosomal proteins on the ribosomal RNA scaffold. nontranslated ribonucleoprotein particles, so-called This was later confirmed by X-ray and neutron scatter- RNPs or informosomes. In this form, mRNA is associ- ing, velocity sedimentation, and electron microscopy, ated with specific proteins capable of repressing and led by large groups of investigators, including Sultan “masking” mRNA from translation. One of these Agalarov, Igor Serdyuk, and Victor Vasiliev, and other proteins, p50 (YB-1/YBX1), was discovered by Lev groups outside of Russia. Ovchinnikov and colleagues. The existence of these The above basic biology achievements progressed types of proteins and the core principles of mRNA to the development of continuous cell-free translation packaging and translational regulation, envisioned systems capable of producing polypeptides in high by Alex and Ovchinnikov more than 40 years ago, laid yield, as reported in a Science paper (6), in coauthor- the foundation for many later studies, including stress ship with Vladimir Baranov and Yuri Alakhov. This also granules and P-bodies. resulted in advancing the Qβ-replicase–based method Alex was a maverick, as described by Venki of RNA amplification by Chetverin’s group to produce Ramakrishnan in his book Gene Machine, “a highly large amounts of mRNAs. imaginative scientist who would publish bold new Surely, Alex’s most thrilling and rewarding experi- ideas because he was unafraid to be wrong occasion- ence was the realization of his major dream: seeing the ally” (10). He did not bow to authority, scientific or ribosome at the atomic level. The race to crystallize otherwise. As a prominent member of the Soviet and solve the structure of the ribosome commenced Academy of Science, Alex did not sign a petition to in the 1980s led by the groups of Ada Yonath/Heintz- expel from the Academy Andrei Sakharov, a brilliant Gunther Wittmann and Alex, and was crowned in 2009 physicist, a dissident humanitarian, and Nobel Peace by a Nobel Prize in Chemistry awarded to Ada Yonath, Laureate. Astonishingly, Alex was one of very few 2of3 | PNAS Evdokimova et al.
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