- Email: [email protected]
The RNA world
Cell, Vol. 77. 901-803, June 17, 1994, Copyright 0 1994 by Cell Press
Book Review
The RNA World: A Snapshot in Time The RNA World Edited by Raymond F. Gesteland and John F. Atkins Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press (1993). 630 pp. $95.
These are happy times in the RNA world. Having recovered from the dizzying discovery of RNA as catalyst (Kruger et al., 1962; Gurrier-Takada et al., 1963) and caught a glimpse of the primordial past, we begin to gain insight into the structure and function of ribozymes, ribosomes, and spliceosomes. We ponder in amazement the practical fallout from these monumental discoveries. Who would have had the audacity 12 years ago to imagine RNA as a nucleic acid cleavage reagent, an affinity ligand, or a chemotherapeutic agent? The successes in fundamental and applied knowledge have gone beyond our wildest dreams. It must be clear that in such a rapidly moving field as RNA processing and evolution, a book on the topic can only provide a snapshot in time. Nevertheless, the snapshot presented in The RNA World captures provocative evolutionary thought, sound basic science, and a framework for future development of RNA as a reagent for the laboratory and the clinic. The book was named for the RNA world hypothesis, which posits that all modern life forms descended from a primordial self-replicating entity, reliant on RNA for both its genetic and enzymatic properties. While the discovery of ribozymes stood on its head one of the cornerstones of biochemistry-enzymes must be proteins-it immediately made the seductive idea of an RNA world more appealing. The chicken-or-the-egg DNA-or-protein paradox of the origin of life is thereby resolved, for both genetic information (the assumed role of DNA) and catalytic function (the assumed role of protein) could reside within the same molecule, RNA. The explicit statement of the RNA world hypothesis (Gilbert, 1966) was elicited by the demonstration of catalytic, template-dependent polymerization of oligoribonucleotides by the Tetrahymena intron ribozyme(Zaug and Cech, 1966). The idea was not entirely novel, however, with several important antecedents (reviewed in the chapter by S. Benner et al.) dating back to the preclassical era of molecular biology (Rich, 1962). Two chapters, one by S. Benner et al. and one by G. Joyce and L. Orgel, attempt to reconstruct the RNA world from a top-down and bottom-up perspective, respectively. While agreeing on the likelihood of an important role for RNA genomes and catalysts at some point in early evolution, these discussions bring home the difficulties and new paradoxes encountered in trying to specify what they were like or how they could have arisen. While the primordial RNA world may remain dimly perceived for the time being, its consequences for our present
and future provide plenty of meat for this volume. The book comprises a handsome compilation of articles on compelling topics. Following a foreword by F. Crick, a prologue by J. Watson, and the abovementioned chapters on the RNA world per se, there is consideration of the structure and evolution of the translation machinery, in the transition from an RNA to a DNA-protein world, with chapters by R. Weiss and J. Cherry, C. Woese and N. Pace, P. Moore, H. Noller, D. Still, J. Davies et al., M. Yarus, and T. Steitz. Treatments of RNA structure and catalysis were contributed by T. Cech, T. Pan et al., D. Turner and P. Bevilacqua, and J. Wyatt and I. Tinoco. These are interspersed with descriptions of the components, function, and evolution of the spliceosome by M. J. Moore et al. and by S. J. Baserga and J. A. Steitz. B. Bass has provided an overview, with evolutionary emphasis, on the remarkable process of RNA editing, whereas J. Tomizawa describes an example of the evolution of an RNA structure for regulatory rather than catalytic purpose. Some flashbacks are provided by consideration of RNA genomes by J. F. Atkins and by N. Maizels and A. M. Weiner, and a glimpse into the crystal ball is afforded by descriptions of in vitro evolution and selection strategies developed by L. Gold et al. and by J. Szostak and A. Ellington. The book ends with appendices on non-Watson-Crick base pair hydrogen-bonding schemes and on RNA pseudoknots by I. Tinoco and by W. Pleij, respectively. These last contributions will be especially appreciated by the structurally challenged molecular biologist. Inevitably, a book of this ilk cannot be all inclusive, and the editors are to be lauded for their selections. However, as E. Blackburn points out in the chapter on telomerase, ‘The view of evolution that asserts that the genetic material was first in the form of RNA raises the question of how the transition to DNA genomes occurred.” The lack of a more thorough treatment of reverse transcriptases than the necessarily brief overview given by N. Maizels and A. M. Weiner and by E. Blackburn herself is therefore unfortunate. The pivotal role of this enzyme in evolution and the link it provides between the RNA and DNA worlds are underscored by the landmark experiments of Wang and Lambowitz (1993), who demonstrated functional relationships between RNA-dependent RNA polymerases and reverse transcriptases. This recent discovery brings us to the continuing rapid progress in the field. In the short time since the book was released, we already know more about RNA structure and the architecture of the spliceosome (reviewed by Wise, 1993). We have a better understanding of the evolution of RNA editing than we did a few short months ago (Maslov et al., 1994). We have, since publication of the book, been stunned by the role of tRNA in transcription antitermination via a novel RNA-RNA interaction (Grundy and Henkin, 1993). Finally, we continue to be bombarded by the breathtaking potential of RNA as a high resolution molecular discriminator (Jenison et al., 1994) an antiviral agent, and anticarcinogen (see, for example, Barinaga, 1993). Does
Cell 802
this rapid progress beg a series of books entitled The RNA World? Must the snapshot give way to the video?
Conaway, R. C., and Conaway, J. W. (1994). Transcription: Mechanisms and Regulation. Raven Press, New York. 570 pp. $125.00. Cooper, N. G. (1994). The Human Genome Project: Deciphering the Blueprint of Heredity. University Science Books, Mill Valley, California. 360 pp. $38.00.
Marlene Belfort’ and David Shubt *Molecular Genetics Program Wadsworth Center New York State Department of Health Albany, New York 12201-0509 tDepartment of Biological Sciences Center for Molecular Genetics State University of New York at Albany Albany, New York 12222
Crabb. J. W. (1994). Techniques in Protein Chemistry V. Academic Press, San Diego, California. 569 pp. $55.00. Cragoe, E. J., Jr., Kleyman, T. R., and Slmchowltz, L. (1992). Amiloride and Its Analogs: Unique Cation Transport Inhibitors. VCH Publishers, New York. 368 pp. $115.00. Davis, L., Kuehl, M., and Battey, J. (1994). Basic Methods in Molecular Biology. Appleton & Lange, Norwalk, Connecticut. 777 pp. $49.95. Davison, A. J., and Elliott, R. M. (1993). Molecular Virology: A Practical Approach. Oxford University Press, New York. 315 pp. $42.00. Desjardlns, C., and Ewing, L. L. (1993). Cell and Molecular Biology of the Testis. Oxford University Press, New York. 497 pp. $125.00.
References
Dracopoli, N. S., Haines, J. L., Kort, B. R., Yoir, D. T., et al. (1994). Current Protocols in Human Genetics, Volume 1. Wiley-Liss, New York. $295.00.
Barinaga, M. (1993). Science 262, 1512-1514. Gilbert, W. (1988). Nature 319, 616. Grundy, F. J., and Henkin, T. M. (1993). Cell 74, 475-482. Gurrier-Takada, C. K., Gardiner, K., Marsh, T., Pace, N., and Altman, S. (1983). Cell 35, 849-857. Jenison, R. D., Gill, S. C., Pardi, A., and Polisky, B. (1994). Science 263, 1425-l 429. Kruger, K., Grabowski, P. J., Zaug, A. J., Sands, D. E., Gottschling, D. E., and Cech, T. R. (1982). Cell 31, 147-157. Maslov, D. A., Avila, H. A., Lake, J. A., and Simpson, L. (1994). Nature 368,345~346. Rich, A. (1962). In Horizons in Biochemistry, M. Kasha and B. Pullman, eds. (New York: Academic Press), pp. 103-126. Wang, H., and Lambowitz, A. M. (1993). Cell 75, 1071-1081.
Drenth, J. (1994). Principles of Protein X-Ray Crystallography. Springer-Verlag, New York. 305 pp. $49.50. Dyer, B. D., and Obar, R. A. (1994). Tracing the History of Eukaryotic Cells: The Enigmatic Smile. Columbia University Press, New York. 259 pp. $24.00. Eberwlne, J. H., Valentino, K. L., and Barchas, J. D. (1994). In Situ Hybridization in Neurobiology: Advances in Methodology. Oxford University Press, New York. 199 pp. $39.95. Erenpreiss, J. 0. (1993). Current Concepts of Malignant Growth, Part A: From a Normal Cell to Cancer. Zvaigzne Publishers, Riga, Latvia. 191 pp. $45.00. Everse, J., Vandegriff, K. D., and Winslow, R. M. (1994). Methods in Enzymology, Volume 231: Hemoglobins. Academic Press, San Diego, California. 743 pp. $105.00.
Wise, J. A. (1993). Science 262, 1976-1979. i’aug, A. J., and Cech, T. R. (1988). Science 231, 470-475.
Everse, J., Vandegriff, K. D., and Winslow, R. M. (1994). Methods in Enzymology, Volume 232: Hemoglobins, Part C: Biophysical Methods. Academic Press, San Diego, California. 725 pp. $99.00.
Books Received
Ewald, P. (1994). Evolutions of Infectious Disease. Oxford University Press, New York. 298 pp. $35.00. Adolph, K. W. (1994). Molecular Microbiology Techniques, Academic Press, San Diego, California. 398 pp. $65.00. Ashall, F. (1994). Remarkable Discoveries. Press, New York. 278 pp. $24.95.
Cambridge
Part A.
University
Bensasaon, R. V., Land, E. J., and Truscott, T. G. (1993). Excited States and Free Radicals in Biology and Medicine: Contributions from Flash Photolysis and Pulse Radiolysis. Oxford University Press, New York. 431 pp. $75.00. Boyd, C. A. R., and Noble, D. (1993). The Logic of Life: The Challenge of Integrative Physiology. Oxford University Press, New York. 226 pp. $14.95. Bridge, P. J. (1994). The Calculation of Genetic Risks: Worked Examples in DNA Diagnostics. Johns Hopkins University Press, Baltimore. 195 pp. $45.00. Campbell, A. K. (1994). Rubicon: The Fifth Dimension Duckworth, London. 304 pp. $39.50.
of Biology.
Cann, A. J. (1993). Principles of Molecular Virology. Academic Press, London. 234 pp. $18.50. Csrtwrlght, H. Y. (1994). Applications of Artificial Intelligence Chemistry. Oxford University Press, New York. 92 pp. $29.95.
in
Clerk, V. L., and Bavoll, P. M. (1994). Methods in Enzymology, Volume 235: Bacterial Pathogenesis, Part A: Identification and Regulation of Virulence Factors. Academic Press, Pasadena, California. 789 pp. $105.00.
Fentiman, I. S., and Taylor-Papadlmltrlou, J. (1993). Breast Cancer. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York. 239 pp. 569.00. Gezdar, A. F., and Carbone, D. P. (1994). The Biology and Molecular Geneticsof Lung Cancer. R. G. LandesCompany, Austin, Texas. 142 pp. $89.95. Gosden, J. R. (1994). Chromosome Analysis Protocols. The Humana Press, Totowa, New Jersey. 508 pp. $69.50. Granstein, R. D. (1994). Mechanisms of Immune Regulation. Basel. 336 pp. $229.00.
Karger,
Graves, D. J., Martin, B. L., and Wang, J. H. (1994). Co- and PostTranslational Modification of Proteins: Chemical Principles and Biological Effects. Oxford University Press, New York. 346 pp. $49.95. Griffin, A. M., and Griffin, H. 0. (1994). Computer Analysis of Sequence Data, Part I. The Humana Press, Totowa, New Jersey. 372 pp. $59.50. Griffin, A. M., and Grlffln, H. G. (1994). Computer Analysis of Sequence Data, Part II. The Humana Press, Totowa, New Jersey. 433 pp. $59.50. Gullo, V. P. (1994). The Discovery of Natural Products with Therapeutical Potential. Butterworth-Heinemann, Stoneham, Massachusetts, 461 pp. $115.00. Harwood, A. J. (1994). Protocols for Gene Analysis. The Humana Press, Totowa, New Jersey. 411 pp. $59.50.
Book Review
The RNA World: A Snapshot in Time The RNA World Edited by Raymond F. Gesteland and John F. Atkins Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press (1993). 630 pp. $95.
These are happy times in the RNA world. Having recovered from the dizzying discovery of RNA as catalyst (Kruger et al., 1962; Gurrier-Takada et al., 1963) and caught a glimpse of the primordial past, we begin to gain insight into the structure and function of ribozymes, ribosomes, and spliceosomes. We ponder in amazement the practical fallout from these monumental discoveries. Who would have had the audacity 12 years ago to imagine RNA as a nucleic acid cleavage reagent, an affinity ligand, or a chemotherapeutic agent? The successes in fundamental and applied knowledge have gone beyond our wildest dreams. It must be clear that in such a rapidly moving field as RNA processing and evolution, a book on the topic can only provide a snapshot in time. Nevertheless, the snapshot presented in The RNA World captures provocative evolutionary thought, sound basic science, and a framework for future development of RNA as a reagent for the laboratory and the clinic. The book was named for the RNA world hypothesis, which posits that all modern life forms descended from a primordial self-replicating entity, reliant on RNA for both its genetic and enzymatic properties. While the discovery of ribozymes stood on its head one of the cornerstones of biochemistry-enzymes must be proteins-it immediately made the seductive idea of an RNA world more appealing. The chicken-or-the-egg DNA-or-protein paradox of the origin of life is thereby resolved, for both genetic information (the assumed role of DNA) and catalytic function (the assumed role of protein) could reside within the same molecule, RNA. The explicit statement of the RNA world hypothesis (Gilbert, 1966) was elicited by the demonstration of catalytic, template-dependent polymerization of oligoribonucleotides by the Tetrahymena intron ribozyme(Zaug and Cech, 1966). The idea was not entirely novel, however, with several important antecedents (reviewed in the chapter by S. Benner et al.) dating back to the preclassical era of molecular biology (Rich, 1962). Two chapters, one by S. Benner et al. and one by G. Joyce and L. Orgel, attempt to reconstruct the RNA world from a top-down and bottom-up perspective, respectively. While agreeing on the likelihood of an important role for RNA genomes and catalysts at some point in early evolution, these discussions bring home the difficulties and new paradoxes encountered in trying to specify what they were like or how they could have arisen. While the primordial RNA world may remain dimly perceived for the time being, its consequences for our present
and future provide plenty of meat for this volume. The book comprises a handsome compilation of articles on compelling topics. Following a foreword by F. Crick, a prologue by J. Watson, and the abovementioned chapters on the RNA world per se, there is consideration of the structure and evolution of the translation machinery, in the transition from an RNA to a DNA-protein world, with chapters by R. Weiss and J. Cherry, C. Woese and N. Pace, P. Moore, H. Noller, D. Still, J. Davies et al., M. Yarus, and T. Steitz. Treatments of RNA structure and catalysis were contributed by T. Cech, T. Pan et al., D. Turner and P. Bevilacqua, and J. Wyatt and I. Tinoco. These are interspersed with descriptions of the components, function, and evolution of the spliceosome by M. J. Moore et al. and by S. J. Baserga and J. A. Steitz. B. Bass has provided an overview, with evolutionary emphasis, on the remarkable process of RNA editing, whereas J. Tomizawa describes an example of the evolution of an RNA structure for regulatory rather than catalytic purpose. Some flashbacks are provided by consideration of RNA genomes by J. F. Atkins and by N. Maizels and A. M. Weiner, and a glimpse into the crystal ball is afforded by descriptions of in vitro evolution and selection strategies developed by L. Gold et al. and by J. Szostak and A. Ellington. The book ends with appendices on non-Watson-Crick base pair hydrogen-bonding schemes and on RNA pseudoknots by I. Tinoco and by W. Pleij, respectively. These last contributions will be especially appreciated by the structurally challenged molecular biologist. Inevitably, a book of this ilk cannot be all inclusive, and the editors are to be lauded for their selections. However, as E. Blackburn points out in the chapter on telomerase, ‘The view of evolution that asserts that the genetic material was first in the form of RNA raises the question of how the transition to DNA genomes occurred.” The lack of a more thorough treatment of reverse transcriptases than the necessarily brief overview given by N. Maizels and A. M. Weiner and by E. Blackburn herself is therefore unfortunate. The pivotal role of this enzyme in evolution and the link it provides between the RNA and DNA worlds are underscored by the landmark experiments of Wang and Lambowitz (1993), who demonstrated functional relationships between RNA-dependent RNA polymerases and reverse transcriptases. This recent discovery brings us to the continuing rapid progress in the field. In the short time since the book was released, we already know more about RNA structure and the architecture of the spliceosome (reviewed by Wise, 1993). We have a better understanding of the evolution of RNA editing than we did a few short months ago (Maslov et al., 1994). We have, since publication of the book, been stunned by the role of tRNA in transcription antitermination via a novel RNA-RNA interaction (Grundy and Henkin, 1993). Finally, we continue to be bombarded by the breathtaking potential of RNA as a high resolution molecular discriminator (Jenison et al., 1994) an antiviral agent, and anticarcinogen (see, for example, Barinaga, 1993). Does
Cell 802
this rapid progress beg a series of books entitled The RNA World? Must the snapshot give way to the video?
Conaway, R. C., and Conaway, J. W. (1994). Transcription: Mechanisms and Regulation. Raven Press, New York. 570 pp. $125.00. Cooper, N. G. (1994). The Human Genome Project: Deciphering the Blueprint of Heredity. University Science Books, Mill Valley, California. 360 pp. $38.00.
Marlene Belfort’ and David Shubt *Molecular Genetics Program Wadsworth Center New York State Department of Health Albany, New York 12201-0509 tDepartment of Biological Sciences Center for Molecular Genetics State University of New York at Albany Albany, New York 12222
Crabb. J. W. (1994). Techniques in Protein Chemistry V. Academic Press, San Diego, California. 569 pp. $55.00. Cragoe, E. J., Jr., Kleyman, T. R., and Slmchowltz, L. (1992). Amiloride and Its Analogs: Unique Cation Transport Inhibitors. VCH Publishers, New York. 368 pp. $115.00. Davis, L., Kuehl, M., and Battey, J. (1994). Basic Methods in Molecular Biology. Appleton & Lange, Norwalk, Connecticut. 777 pp. $49.95. Davison, A. J., and Elliott, R. M. (1993). Molecular Virology: A Practical Approach. Oxford University Press, New York. 315 pp. $42.00. Desjardlns, C., and Ewing, L. L. (1993). Cell and Molecular Biology of the Testis. Oxford University Press, New York. 497 pp. $125.00.
References
Dracopoli, N. S., Haines, J. L., Kort, B. R., Yoir, D. T., et al. (1994). Current Protocols in Human Genetics, Volume 1. Wiley-Liss, New York. $295.00.
Barinaga, M. (1993). Science 262, 1512-1514. Gilbert, W. (1988). Nature 319, 616. Grundy, F. J., and Henkin, T. M. (1993). Cell 74, 475-482. Gurrier-Takada, C. K., Gardiner, K., Marsh, T., Pace, N., and Altman, S. (1983). Cell 35, 849-857. Jenison, R. D., Gill, S. C., Pardi, A., and Polisky, B. (1994). Science 263, 1425-l 429. Kruger, K., Grabowski, P. J., Zaug, A. J., Sands, D. E., Gottschling, D. E., and Cech, T. R. (1982). Cell 31, 147-157. Maslov, D. A., Avila, H. A., Lake, J. A., and Simpson, L. (1994). Nature 368,345~346. Rich, A. (1962). In Horizons in Biochemistry, M. Kasha and B. Pullman, eds. (New York: Academic Press), pp. 103-126. Wang, H., and Lambowitz, A. M. (1993). Cell 75, 1071-1081.
Drenth, J. (1994). Principles of Protein X-Ray Crystallography. Springer-Verlag, New York. 305 pp. $49.50. Dyer, B. D., and Obar, R. A. (1994). Tracing the History of Eukaryotic Cells: The Enigmatic Smile. Columbia University Press, New York. 259 pp. $24.00. Eberwlne, J. H., Valentino, K. L., and Barchas, J. D. (1994). In Situ Hybridization in Neurobiology: Advances in Methodology. Oxford University Press, New York. 199 pp. $39.95. Erenpreiss, J. 0. (1993). Current Concepts of Malignant Growth, Part A: From a Normal Cell to Cancer. Zvaigzne Publishers, Riga, Latvia. 191 pp. $45.00. Everse, J., Vandegriff, K. D., and Winslow, R. M. (1994). Methods in Enzymology, Volume 231: Hemoglobins. Academic Press, San Diego, California. 743 pp. $105.00.
Wise, J. A. (1993). Science 262, 1976-1979. i’aug, A. J., and Cech, T. R. (1988). Science 231, 470-475.
Everse, J., Vandegriff, K. D., and Winslow, R. M. (1994). Methods in Enzymology, Volume 232: Hemoglobins, Part C: Biophysical Methods. Academic Press, San Diego, California. 725 pp. $99.00.
Books Received
Ewald, P. (1994). Evolutions of Infectious Disease. Oxford University Press, New York. 298 pp. $35.00. Adolph, K. W. (1994). Molecular Microbiology Techniques, Academic Press, San Diego, California. 398 pp. $65.00. Ashall, F. (1994). Remarkable Discoveries. Press, New York. 278 pp. $24.95.
Cambridge
Part A.
University
Bensasaon, R. V., Land, E. J., and Truscott, T. G. (1993). Excited States and Free Radicals in Biology and Medicine: Contributions from Flash Photolysis and Pulse Radiolysis. Oxford University Press, New York. 431 pp. $75.00. Boyd, C. A. R., and Noble, D. (1993). The Logic of Life: The Challenge of Integrative Physiology. Oxford University Press, New York. 226 pp. $14.95. Bridge, P. J. (1994). The Calculation of Genetic Risks: Worked Examples in DNA Diagnostics. Johns Hopkins University Press, Baltimore. 195 pp. $45.00. Campbell, A. K. (1994). Rubicon: The Fifth Dimension Duckworth, London. 304 pp. $39.50.
of Biology.
Cann, A. J. (1993). Principles of Molecular Virology. Academic Press, London. 234 pp. $18.50. Csrtwrlght, H. Y. (1994). Applications of Artificial Intelligence Chemistry. Oxford University Press, New York. 92 pp. $29.95.
in
Clerk, V. L., and Bavoll, P. M. (1994). Methods in Enzymology, Volume 235: Bacterial Pathogenesis, Part A: Identification and Regulation of Virulence Factors. Academic Press, Pasadena, California. 789 pp. $105.00.
Fentiman, I. S., and Taylor-Papadlmltrlou, J. (1993). Breast Cancer. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York. 239 pp. 569.00. Gezdar, A. F., and Carbone, D. P. (1994). The Biology and Molecular Geneticsof Lung Cancer. R. G. LandesCompany, Austin, Texas. 142 pp. $89.95. Gosden, J. R. (1994). Chromosome Analysis Protocols. The Humana Press, Totowa, New Jersey. 508 pp. $69.50. Granstein, R. D. (1994). Mechanisms of Immune Regulation. Basel. 336 pp. $229.00.
Karger,
Graves, D. J., Martin, B. L., and Wang, J. H. (1994). Co- and PostTranslational Modification of Proteins: Chemical Principles and Biological Effects. Oxford University Press, New York. 346 pp. $49.95. Griffin, A. M., and Griffin, H. 0. (1994). Computer Analysis of Sequence Data, Part I. The Humana Press, Totowa, New Jersey. 372 pp. $59.50. Griffin, A. M., and Grlffln, H. G. (1994). Computer Analysis of Sequence Data, Part II. The Humana Press, Totowa, New Jersey. 433 pp. $59.50. Gullo, V. P. (1994). The Discovery of Natural Products with Therapeutical Potential. Butterworth-Heinemann, Stoneham, Massachusetts, 461 pp. $115.00. Harwood, A. J. (1994). Protocols for Gene Analysis. The Humana Press, Totowa, New Jersey. 411 pp. $59.50.