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Molecular and Cellular Biology, January 2000, p. 672-683, Vol. 20, No. 2
0270-7306/0/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Cyclin D1 Is Required for Transformation by Activated Neu and Is Induced through an E2F-Dependent Signaling Pathway

Richard J. Lee,1 Chris Albanese,1 Maofu Fu,1 Mark D'Amico,1 Bing Lin,2 Genichi Watanabe,1 George K. Haines III,3 Peter M. Siegel,4 Mien-Chie Hung,5 Yosef Yarden,6 Jonathan M. Horowitz,2 William J. Muller,4 and Richard G. Pestell1,*

Department of Developmental and Molecular Biology and Department of Medicine, The Albert Einstein Cancer Center, Albert Einstein College of Medicine, Bronx, New York 104611; Department of Anatomy, Physiological Sciences, and Radiology, College of Veterinary Medicine, North Carolina State University, Raleigh, North Carolina 276062; Department of Pathology, Northwestern University Medical School, Chicago, Illinois 606113; Department of Pathology, McMaster University, West Hamilton, Ontario L8S 4K1, Canada4; Department of Tumor Biology, University of Texas M. D. Anderson Cancer Center, Houston, Texas 770305; and Department of Bioregulation, The Weizmann Institute of Science, Rehovot 76100, Israel6

Received 16 June 1999/Returned for modification 9 August 1999/Accepted 11 October 1999

The neu (c-erbB-2) proto-oncogene encodes a tyrosine kinase receptor that is overexpressed in 20 to 30% of human breast tumors. Herein, cyclin D1 protein levels were increased in mammary tumors induced by overexpression of wild-type Neu or activating mutants of Neu in transgenic mice and in MCF7 cells overexpressing transforming Neu. Analyses of 12 Neu mutants in MCF7 cells indicated important roles for specific C-terminal autophosphorylation sites and the extracellular domain in cyclin D1 promoter activation. Induction of cyclin D1 by NeuT involved Ras, Rac, Rho, extracellular signal-regulated kinase, c-Jun N-terminal kinase, and p38, but not phosphatidylinositol 3-kinase. NeuT induction of the cyclin D1 promoter required the E2F and Sp1 DNA binding sites and was inhibited by dominant negative E2F-1 or DP-1. Neu-induced transformation was inhibited by a cyclin D1 antisense or dominant negative E2F-1 construct in Rat-1 cells. Growth of NeuT-transformed mammary adenocarcinoma cells in nude mice was blocked by the cyclin D1 antisense construct. These results demonstrate that E2F-1 mediates a Neu-signaling cascade to cyclin D1 and identify cyclin D1 as a critical downstream target of neu-induced transformation.

* Corresponding author. Mailing address: The Albert Einstein Cancer Center, Departments of Medicine and Developmental and Molecular Biology, Albert Einstein College of Medicine, Chanin 302, 1300 Morris Park Ave., Bronx, NY 10461. Phone: (718) 430-8662. Fax: (718) 430-8674. E-mail: pestell{at}aecom.yu.edu.

Molecular and Cellular Biology, January 2000, p. 672-683, Vol. 20, No. 2
0270-7306/0/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.


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