Joel L. Sussman is Professor Emeritus of Structural Biology at the Weizmann Institute of Science in Rehovot and is Co-Director of the Israel Structural Proteomics Center. In 1994–99, he was also the director of the Protein Data Bank (PDB).
He sent the following comment:
Please see attached a few changes and additions I've made to "From PDB to AlphaFold". [these are listed below]
1) The few points I've added in the early days of molecular graphics are essential as they were crucial for the PDB and AlphaFold. This is especially true for the first 3D PDB Browser.
2) AutoDep revolutionized the deposition and validation process at the PDB, and it opened up a close collaboration with the PDBe at the EBI. It streamed the deposition process and significantly improved the quality of the entries in the PDB.
3) The 25th Anniversary of the PDB and the 10th Anniversary of Swiss-Prot was held in Jerusalem. It was a real turning point in the field, as it was one of the first (if not THE first) meetings that brought together the sequence and 3D structure field. It is unlikely that you can include all the photos I've sent (which are only a few from the conference), but you can maybe include thumbnail-size images of them, which would expand if clicked on. Many scientists would be happy to see some of these early photos of the scientists who became real stars in the field. I'd hate losing them if something happened to my faculty website.
4) I had an incredible meeting with Nature's Editor-in-Chief, Philip Cambell. When I visited his office in London early in 1998, there was no chance that he would consider reversing Nature's long-standing policy regarding NOT requiring deposition and release of the 3D structure of biomacromolecules as a requirement for publication in Nature. To my absolute shock, he agreed virtually immediately. With me in his office, he phoned the Editor-in-Chief of Science, Floyd Bloom. They decided to publish similar editorials stating that this policy change was unequivocal. The shift in policy by Nature and Science made all the difference in the world for requiring the release of structural data, and almost all other journals quickly followed suit.
[Suggested changes and additions to "From PDB to AlphaFold". Several have been already added to the timeline, and for others further historical research is ongoing, to help present their context.]
1965 At MIT’s Project Mac, Cyrus Levinthal and Bob Langridge used computer graphics for the first time to display a protein structure, i.e., myoglobin. 3D visualization was achieved simply by rotating the structure on the screen. (Levinthal 1966).
1969 Cyrus Levinthal described the paradox of protein folding: the folding process must be guided by specific interactions and not by a random search through all possible conformations, which would take an immensely long time (Levinthal, 1969).
1971 August. At the ACA Conference in Ames, Iowa, the first 3D molecular graphics film was shown in a lecture by Joel L. Sussman on very small RNA structure, UpA [https://www.youtube.com/watch?v=PraieqBi048] (Seeman et al, 1971).
1995 The first 3DB Browser was released by the PDB-BNL. It dramatically enhanced the PDB's printed index listings and various ad hoc search protocols that had been developed to find PDB entries. Selected proteins in the PDB could be easily downloaded, and their molecular structures visualized on lab computers (Stampf et al, 1995 & Sussman et al, 2001) via RasM (Sayle, 1995) and other 3D visualization tools.
Figure 2: 3DB Browser as a tool to visualize recently published structures. (1) Search for author: Hendrickson; text query: HIV. (2) Six hits obtained, PDB ID Code 1GC1 highlighted. (3) 3DB Browser Atlas page. Ovals highlight the expression systems used for the different components in the multicomponent system. (4) Structure as visualized with MDL's Chemscape Chime plug-in.
1996: The PDB release of AutoDep, the first web-based tool for macromolecular structure deposition and validation. It was developed at the PDB-BNL, but was also given to the PDBe, who used it as the first remote site for deposition in the PDB. Within 3 months of its release, over 50% of all new submissions were deposited via AutoDep. n.b. This was when the WWW was very young, and people weren't as familiar with it as they are today. In fact, AutoDep predated any web submission of papers to journals (Lin, 2000).
1996 November. A conference celebrating the 25th Anniversary of the PDB and the 10th Anniversary of Swiss-Prot was held in Jerusalem. [http://www.weizmann.ac.il/csb/faculty_pages/Sussman/pdb25sp10]. This was one of the first meetings at which 3D structural data and sequence information were analyzed synergistically. It is remarkable how many scientists attended this meeting in 1996 and continued to be active in the field for many years following: Enrique Abola, Lia Addadi, Amos Bairoch, Nir Ben-Tal, Frances C. Bernstein, Herbert J. Bernstein, Helen Berman, Tom Blundel, Steven E. Brenner, Stephen H. Bryant, Cyrus Chothia, Miroslaw Cygler, Meir Edelman, David Eisenberg, Ken Fasman, Alan Fersht, Gary Gilliland, Adrian Goldman, Arthur Grollman, Mitchell Guss, Michal Harel, Osnat Herzberg, Barry Honig, Leroy Hood, Amnon Horovitz, Joel Janin, Chen Keasar, Ephraim Katzir, John Kendrew, Olga Kennard, Michael Levitt, Laua Lai, Doron Lancet, Olivier Lichtarge, Dawie Lin, N.O.Manning, Edgar Meyer. Leonid Mirny, John Moult, John Norvell, Ruth Nussinov, Wilma Olsen, Manuel C. Peitch, Shmuel Pietrokovski, Jaime Prilusky, Otto Ritter, John Rosenberg, Mark Safro, Chris Sander, Gideon Schreiber, Boaz Shaanan, Manfred Sipp, Jeffrey Skolnck, Bill Studier, Joel L. Sussman, Muttaiya Sundaralingam. Janet Thornton, Ed Trifonov, Tomitake Tsukihara, Ron, Unger, Keith D. Watenpaugh, Shoshan Wodak, and Ada Yonath.
Photographs of some of these young scientists can be seen at: https://www.weizmann.ac.il/csb/faculty_pages/Sussman/pdb25sp10/Picture-index.html and a few are shown below
Figure 3. Cover of abstract book of the conference celebrating the 25th Anniversary of the PDB and the 10th Anniversary of Swiss-Prot that was held in Jerusalem in Nov 1996.
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Figure 4. Photographs from the 25th Anniversary of the PDB and the 10th Anniversary of Swiss-Prot, which was held in Jerusalem, November 1996. (a) Left to right, Edgar Meyer, unknown, Enrique Abola, Nancy Manning & the 7th President of Israel, Ezer Weizman; (b) Keith Watenpaugh & Eli Admon; (c) Amos Bairoch; (d) Olga Kennard; (e) Janet Thornton; (f) Left to right, 4th President of Israel, Ephraim Katzir, Chris Sander, Janet Thornton, Olga Kennard, Barry Honig & Schneior Lifson (g) Left to right, Helen M. Berman, Janet Thornton, Shoshana Wodak & Olga Kennard; (h) Chris Sander; (i) Shoshana Wodak & Michel Levitt; (j) Joel L. Sussman & the 4th President of Israel, Ephraim Katzir; (k) center Edgar Meyer; (l) Wilman Olson & Muttaiya Sundaralingam; (m) Gideon Schreiber & Cyrus Chothia; (n) Bill Studier; (o) Leroy Hood; (p) Cyrus Chothia, JanethThronton Joel Janin, unkown, Shoshana Wodak, Joel L. Sussman & Helen M. Berman, (q) Peer Bork; (r) Joel L. Sussman, John Kendrew & the 4th President of Israel, Ephraim Katzir; (s) Tom Blundell; (t) John Moult, Stephen Bryant & Osnat Hertzberg; (u) Janet Thornton & Stephen Bryant; (v) Jaime Prilusky; (w) Frances Bernstein
1998 Nature, Science and PNAS reversed their long-standing policy of not requiring the immediate release of high-resolution structural coordinate data upon publication. This occurred in the Spring of 1998, following a visit by Joel L. Sussman, Head of the PDB, to Philip Cambell, the Editor-in-Chief of Nature, in London, to discuss the possibility of changing Nature’s policy of not requiring deposition of 3D macromolecular structures in the PDB. Cambell was very open to the idea and immediately phoned Floyd Bloom, the Editor-in-Chief of Science. They discussed that matter and immediately agreed to issue a joint statement with their new policy of requiring the deposition of the structures to the PDB and its release at the time of publication. Joel was amazed that Nature was speaking with Science(!).
Nature stated in their 9-Jul-1998 issue that "It is clear that there is a significant majority opinion in the community against permitting a one-year hold. Accordingly, Nature, simultaneously with Science, is changing its policy. Any paper containing new structural data received on or after 1 October 1998 will not be accepted without an accession number from the Brookhaven Protein Data Bank (PDB) accompanied by an assurance that unrestricted (“layer-1”) release will occur at or before the time of publication." Floyd Bloom, of Science, published in their 10-Jul-1998 issue a very similar editorial: https://www.science.org/doi/full/10.1126/science.281.5374.175c. The Editor-in-Chief of PNAS published a similar editorial in the 28-April01998 issue.
Figure 5. Editorial by Nick Cozzarelli in PNAS detailing the new policy requiring deposition of structures in the PDB-BNL.
REFERENCES
(see also links within the text)
Levinthal, C. 1966. Molecular model-building by computer, Scientific American, 214(6). pp. 42-52.
Levinthal, C. (1969) How to fold graciously, in: J.T.P. DeBrunner, E. Munck (Eds.) Mossbauer Spectroscopy in Biological Systems Proceedings, Univ of Illinois Press, Illinois, 67(41), pp. 22-24.
Lin, D., Manning, N.O., Jiang, J., Abola, E.E., Stampf, D., Prilusky, J., and Sussman, J.L. 2000. AutoDep©: A web based system for deposition and validation of macromolecular structural information, Acta Crystallographica D Biological Crystallograrphy, 56(7) pp. 828-841.
Sayle R.A. and Milner-White, E.J. (1995). RASMOL: biomolecular graphics for all. TIBS, 20(9) pp. 374-376
Seeman, N.C., Sussman, J.L., Berman, H.M., & Kim, S.-H. (1971). Nucleic acid conformation: crystal structure of a naturally occurring dinucleoside phosphate (UpA). Nature New Biology, 233(37). pp. 90-92.
Stampf, D.R., Felder, C.E., & Sussman, J..L. (1995). PDBbrowse--a graphics interface to the Brookhaven Protein Data Bank, Nature, 374(6522) pp. 572-574.
Sussman, J.L, Lin, D., Jiang, J., Manning, N.O., Prilusky, J. & Abola, E.E. 2001. The protein data bank at Brookhaven, in: M.G. Rossmann, E. Arnold (Eds.) International Tables for Crystallography, Volume F. Crystallography of Biological Macromolecules, Kluwer Academic Publishers, Dordrecht, pp. 649-656.
The following additional comment was received from Joel, with information about the extensive efforts in 1996 to promote deposition of structural data at the time of publication (with delayed release still allowed upon request) and the subsequent changes in the rate of submissions. It also contains more details about the 3DB browser and about its importance.
1) 1996 At an ‘International Seminar-Cum-School on Macromolecular Crystallographic Data’ at Calcutta, India, in November 1995, a formal discussion of the archival journal requirements for data deposition was held. This resulted in a letter to the editor of Nature (as well as seven other journals) that contained, in part, the following:
“… We recommend, therefore, that publication of macromolecular crystal structures should be accompanied by deposition of atomic parameters and also structure amplitudes …”
The 8 letters are:
· Baker, E. N. , Blundell, T. L., Vijayan, M., Dodson, E., Dodson, G., Gilliland, G. I. and Sussman, J.L. 1996. Crystallographic data deposition Nature 379(6562) pp. 202.
· Baker, E. N. , Blundell, T. L., Vijayan, M., Dodson, E., Gilliland, G. I. and Sussman, J.L. 1996. Deposition of macromolecular data. Acta Crystallographica D Biological Crystallography 52(3), pp. 609.
· Baker, E. N. , Blundell, T. L., Vijayan, M., Dodson, E., Dodson, G., Gilliland, G. I. and Sussman, J.L. 1996. Archival journal requirements for data deposition. Biophysical Journal 70(6) pp. 2994.
· Baker, E. N. , Blundell, T. L., Vijayan, M., Dodson, E., Dodson, G., Gilliland, G. I. and Sussman, J.L. 1996. International Seminar-cum-School on Macromolecular Crystallographic Data at Calcutta, India. Anticancer Drug Design 11(2) pp. 173-174.
· Baker, E. N. , Blundell, T. L., Vijayan, M., Dodson, E., Dodson, G., Gilliland, G. I. and Sussman, J.L. 1996. A formal discussion of the archival journal requirements for data deposition. Biochem Biophys Res Commun 219(3) pp. 976-977.
· Baker, E. N. , Blundell, T. L., Vijayan, M., Dodson, E., Dodson, G., Gilliland, G. I. and Sussman, J.L. 1996. Publication of macromolecular crystal structures. FEBS Lett 380(3) pp.301
· Baker, E. N. , Blundell, T. L., Vijayan, M., Dodson, E., Dodson, G., Gilliland, G. I. and Sussman, J.L. 1996. Diffraction data deposition. Structure 4(2) pp. 217.
· Baker, E. N. , Blundell, T. L., Vijayan, M., Dodson, E., Dodson, G., Gilliland, G. I. and Sussman, J.L. 1996. Archival journal requirements of macromolecular crystallographic data. Journal of Biomololecular and Structural Dynamics 13(4) pp. 583.
These letters, together with a change in the scientific community in favor of depositing experimental data with the 3D coordinates to the PDB, can be seen in the letter to the editor (Jiang et al., 1996). It contains a table showing a significant increase in the percent of X-ray structures deposited to the PDB, which included structure factors, from 25% in 1994 to 63% in 1997.
It stresses the importance of a standard format for experimental data: “. . .In order to facilitate the use of deposited structure factors, we at the PDB, together with a number of macromolecular crystallographers and the IUCr Working Group on Macromolecular CIF, developed a standard interchange format for structure factors [PDBStructure Factor mmCIF at Protein Data Bank Quart. Newslett. No. 74, p. 1 (1995) [https://files.wwpdb.org/pub/pdb/doc/newsletters/bnl/news74_oct95/newslttr.txt]. Finally, it concludes with:
“ …The ready availability of structure-factor files in a standard format has made it possible for any scientist to validate a structure in the PDB versus its experimentally observed data. … The PDB has also observed that one of the most popular uses for these stored structure factors is for the crystallographer who did the experiment to be able to retrieve his/her own data which have been misplaced in their laboratory.”
Jiang, J., Abola, E. and Sussman, J.L. (1998). Deposition of structure factors at the protein data bank. Acta Crystallographica D Biological Crystallography 55(1) pp. 4.
2) 1995 The first PDB Browser was released by the PDB-BNL. It dramatically enhanced the PDB's printed index listings and various ad hoc search protocols developed to find PDB entries. Selected proteins in the PDB could be easily downloaded, and their molecular structures visualized on lab computers (Stampf et al, 1995 & Sussman et al., 2001) via RasMol (Sayle, 1995) and other 3D visualization tools. The following year, the browser was significantly improved, becoming the “3DB Browser” (Prilusky et al, 1996, Sussman et al, 1998)
[See Figure 2 above for image of 3DB Browser]
Figure 2: 3DB Browser (Prilusky et al., 1996, Sussman et al., 1998) as a tool to search and visualize 3D biomacromolecular structures. (1) Search for author: Hendrickson; text query: HIV. (2) Six hits were obtained, with PDB ID Code 1GC1 highlighted. (3) 3DB Browser Atlas page. Ovals highlight the expression systems used for the different components in the multicomponent system. (4) Structure as visualized with MDL's Chemscape Chime plug-in or alternatively via RasMol (Sayle, 1995)
Prilusky, J., Sussman, J.L. and Abola, E.E. (1996) Three dimensional database of biomacromolecules structure (3DB): a 'multi-tool' based browser as a solution for complex data and complex queries. in Abstract of 10 Anniversay of the Swiss-Prot Database and the 25th anniversary of the Protein Data Bank [https://www.weizmann.ac.il/csb/faculty_pages/Sussman/pdb25sp10/abstracts/Abola.html]
Sussman, J.L, Lin, D., Jiang, J., Manning, N.O., Prilusky, J., Ritter, O. and Abola, E.E. (1998). Protein Data Bank (PDB): a database of 3D structural information of biological macromolecules. Acta Crystallographica D Biological Crystallography 54(6) pp. 1078-1084