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[Cancer Research 62, 4132-4141, July 15, 2002]
© 2002 American Association for Cancer Research

Tumor Biology

Herceptin-induced Inhibition of Phosphatidylinositol-3 Kinase and Akt Is Required for Antibody-mediated Effects on p27, Cyclin D1, and Antitumor Action1

F. Michael Yakes, Wichai Chinratanalab, Christoph A. Ritter, Walter King, Steven Seelig and Carlos L. Arteaga2

Departments of Medicine [F. M. Y., W. C., C. A. R., C. L. A.] and Cancer Biology [C. L. A.] and Vanderbilt-Ingram Cancer Center [C. L. A.], Vanderbilt University School of Medicine, Nashville, Tennessee 37232, and Vysis, Downers Grove, Illinois 60515 [W. K., S. S.]

We have examined whether inhibition of phosphatidylinositol-3 kinase (PI3K) and its target, the serine/threonine kinase Akt, play a role in the antitumor effect of the HER2 antibody Herceptin. Herceptin inhibited colony formation, down-regulated cyclin D1, and increased p27 protein levels in the HER2 gene-amplified BT-474 and SKBR-3 human breast cancer cells. These effects were temporally associated with the inhibition of PI3K activity in vitro as well as Akt function as measured by steady-state levels of phospho-Ser473 Akt and kinase activity against glycogen synthase kinase (GSK)-3ß. These responses were not observed in MDA-361 and MDA-453 cells, which do not exhibit HER2 gene amplification and are relatively resistant to Herceptin. Treatment of BT-474 cells with Herceptin inhibited the constitutive tyrosine phosphorylation of HER3 and disrupted the basal association of HER3 with HER2 and of HER3 with p85{alpha} potentially explaining the inhibition of PI3K. Treatment with either Herceptin or the PI3K inhibitor LY294002 increased the levels of p27 in the nucleus>cytosol, thus increasing the ratio of p27:Cdk2 in the nucleus and inhibiting Cdk2 activity and cell proliferation. Antisense p27 oligonucleotides abrogated the increase in p27 induced by Herceptin and prevented the antibody-mediated reduction in S phase. Transduction of BT-474 cells with an adenovirus-encoding active (myristoylated) Akt (Myr-Akt), but not with a ß-galactosidase control adenovirus, prevented the Herceptin- or LY294002-induced down-regulation of cyclin D1 and of phosphorylated GSK-3ß and prevented the accumulation of p27 in the nucleus and cytosol. In addition, Myr-Akt prevented Herceptin-induced inhibition of the cell proliferation of BT-474 cells and Herceptin-induced apoptosis of SKBR-3 cells. These data suggest that (a) changes in cell cycle- and apoptosis-regulatory molecules after HER2 blockade with Herceptin result, at least in part, from the inhibition of Akt; and (b) disabling PI3K and Akt is required for the antitumor effect of HER2 inhibitors.




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T. Holbro, R. R. Beerli, F. Maurer, M. Koziczak, C. F. Barbas III, and N. E. Hynes
The ErbB2/ErbB3 heterodimer functions as an oncogenic unit: ErbB2 requires ErbB3 to drive breast tumor cell proliferation
PNAS, July 22, 2003; 100(15): 8933 - 8938.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
T. Repka, E. G. Chiorean, J. Gay, K. E. Herwig, V. K. Kohl, D. Yee, and J. S. Miller
Trastuzumab and Interleukin-2 in HER2-positive Metastatic Breast Cancer: A Pilot Study
Clin. Cancer Res., July 1, 2003; 9(7): 2440 - 2446.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
X.-F. Le, F.-X. Claret, A. Lammayot, L. Tian, D. Deshpande, R. LaPushin, A. M. Tari, and R. C. Bast Jr.
The Role of Cyclin-dependent Kinase Inhibitor p27Kip1 in Anti-HER2 Antibody-induced G1 Cell Cycle Arrest and Tumor Growth Inhibition
J. Biol. Chem., June 20, 2003; 278(26): 23441 - 23450.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
M. L. Janmaat, F. A. E. Kruyt, J. A. Rodriguez, and G. Giaccone
Response to Epidermal Growth Factor Receptor Inhibitors in Non-Small Cell Lung Cancer Cells: Limited Antiproliferative Effects and Absence of Apoptosis Associated with Persistent Activity of Extracellular Signal-regulated Kinase or Akt Kinase Pathways
Clin. Cancer Res., June 1, 2003; 9(6): 2316 - 2326.
[Abstract] [Full Text] [PDF]


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