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The role of translation in neoplastic transformation from a pathologist's point of view

Oncogene volume 23, pages 3230–3247 (2004)Cite this article

Abstract

Increased cell proliferation, which is a hallmark of aggressive malignant neoplasms, requires a general increase in protein synthesis and a specific increase in the synthesis of replication-promoting proteins. Transient increase in the general protein synthesis rate, as well as preferential translation of specific mRNAs coding for growth promoting proteins (e.g. cyclin D1), takes place during normal mitogenic response. A number of extensively studied growth signal transduction pathways (Ras, PI3K, MAPK, mTOR-dependent pathways) activate the function and expression of various components of the translational machinery. In abnormal situations, constitutive activation of signal transduction pathways (e.g. oncogenic activation of Ras or Myc) leads to continuous upregulation of key elements of translational machinery. On the other hand, tumor suppressor genes (p53, pRb) downregulate ribosomal and tRNA synthesis, and their inactivation results in uncontrolled production of these translational components. During recent years, a significant effort has been dedicated to determining whether expression of translation factors is increased in human tumors using clinical biopsy specimens. The results of these studies indicate that expression of particular translation initiation factors is not always increased in human neoplasms. The pattern of expression is characteristic for a particular tumor type. For example, eIF-4E is usually increased in bronchioloalveolar carcinomas but not in squamous cell carcinomas of the lung. Interestingly, in certain highly proliferative and aggressive neoplasms (e.g. squamous cell carcinoma of the lung, melanoma), the expression of eIF-4E is barely detectable. These findings suggest that mechanisms for increasing general protein synthesis in various neoplasms differ significantly. Finally, the possibility of qualitative alterations in the translational machinery, rather than a simple increase in the activity of its components, is discussed along with the possibility of targeting those qualitative differences for tumor therapy.

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Acknowledgements

I acknowledge the help and collaboration of my colleagues during early years of research on cell cycle: Eugene A Kuznetsov (Semashko Moscow Medical Institute), Olga I Epifanova, Boris V Loginov and Galina F Makarova (Institute of Molecular Biology, Russian Academy of Sciences, Moscow). I acknowledge invaluable contribution and support from my colleagues and collaborators: Emmett V Schmidt and James Michaelson (Massachusetts General Hospital), Jane-Jane Chen, Philippe LeBoulch, Lee Gehrke and Irving M London (Harvard-MIT Division of Health Sciences and Technology), Roger Kaspar (SomaGenics Inc., Santa Cruz, CA, USA), Nahum Sonenberg (McGill University, Montreal), Vitaly Polunovsky (University of Minnesota, Minneapolis), Bruce Woda, Lou Savas, Irma Szymanski, Armando E. Fraire, Liberto Pechet, Ashraf Khan (University of Massachusetts Medical Center, Worcester), Marshall E Kadin and German Pihan (Beth-Israel Deaconess Medical Center, Boston), Songtao Wang (St Clare Hospital, Pittsburgh, PA), James Pullman and Michael J Hutzler (Albert Einstein College of Medicine, New York), and Ilya N Trakht (Columbia University, New York). Assistance of Charles Key (Pathology Department, University of New Mexico, Albuquerque) with information on cancer statistics is appreciated. I appreciate helpful information on cytomorphology of the nucleus and nucleoli in neoplastic cells provided by Leopold G Koss (Albert Einstein College of Medicine, New York). I extend special thanks to Roger Kaspar (SomaGenics Inc., Santa Cruz, CA) and Jane-Jane Chen (Harvard-MIT Division of Health Sciences and Technology) for invaluable comments on this article during preparation for publication.

The excellent secretarial assistance of Bernadine Romero (Department of Pathology, University of New Mexico, Albuquerque) and assistance of Hunter Gough and Matthew Petitt (Department of Pathology, University of New Mexico, Albuquerque) in preparation of the figures is greatly appreciated. The author was supported in part by the American Brain Tumor Association and a Research Fellowship Award from Johnson and Johnson during his work at Massachusetts General Hospital and Massachusetts Institute of Technology, respectively. The author's studies on human neoplasms were supported by a Teaching Fund from the Department of Pathology, University of Massachusetts Medical Center. Present support is provided by research funds from the Pathology Department, University of New Mexico. I dedicate this article to my parents, Boris and Maya Rozenvald, in appreciation of their support and encouragement.

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  1. Department of Pathology, Division of Hematopathology, University of New Mexico, BRF Building, Room 323 B, MSC08 4640, 1 University of New Mexico, Albuquerque, 87131, NM, USA

    Igor B Rosenwald

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Rosenwald, I. The role of translation in neoplastic transformation from a pathologist's point of view. Oncogene 23, 3230–3247 (2004). https://doi.org/10.1038/sj.onc.1207552

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