Molecular imaging of the efficacy of heat shock protein 90 inhibitors in living subjects.

Heat shock protein 90 alpha (Hsp90 alpha)/p23 and Hsp90 beta/p23 interactions are crucial for proper folding of proteins involved in cancer and neurodegenerative diseases. Small molecule Hsp90 inhibitors block Hsp90 alpha/p23 and Hsp90 beta/p23 interactions in part by preventing ATP binding to Hsp90. The importance of isoform-selective Hsp90 alpha/p23 and Hsp90 beta/p23 interactions in determining the sensitivity to Hsp90 was examined using 293T human kidney cancer cells stably expressing split Renilla luciferase (RL) reporters. Interactions between Hsp90 alpha/p23 and Hsp90 beta/p23 in the split RL reporters led to complementation of RL activity, which was determined by bioluminescence imaging of intact cells in cell culture and living mice using a cooled charge-coupled device camera. The three geldanamycin-based and seven purine-scaffold Hsp90 inhibitors led to different levels of inhibition of complemented RL activities (10-70%). However, there was no isoform selectivity to both classes of Hsp90 inhibitors in cell culture conditions. The most potent Hsp90 inhibitor, PU-H71, however, led to a 60% and 30% decrease in RL activity (14 hr) in 293T xenografts expressing Hsp90 alpha/p23 and Hsp90 beta/p23 split reporters respectively, relative to carrier control-treated mice. Molecular imaging of isoform-specific Hsp90 alpha/p23 and Hsp90 beta/p23 interactions and efficacy of different classes of Hsp90 inhibitors in living subjects have been achieved with a novel genetically encoded reporter gene strategy that should help in accelerating development of potent and isoform-selective Hsp90 inhibitors.

[1]  J. Myung,et al.  Expressional patterns of chaperones in ten human tumor cell lines , 2004, Proteome Science.

[2]  Sanjiv S Gambhir,et al.  Molecular imaging of homodimeric protein–protein interactions in living subjects , 2004, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[3]  A. Kamal,et al.  Synthesis and biological evaluation of a new class of geldanamycin derivatives as potent inhibitors of Hsp90. , 2004, Journal of medicinal chemistry.

[4]  P. Csermely,et al.  Comparative analysis of the ATP-binding sites of Hsp90 by nucleotide affinity cleavage: a distinct nucleotide specificity of the C-terminal ATP-binding site. , 2003, European journal of biochemistry.

[5]  H. Lehrach,et al.  A Human Protein-Protein Interaction Network: A Resource for Annotating the Proteome , 2005, Cell.

[6]  Sanjiv S. Gambhir,et al.  Molecular Imaging of Drug-Modulated Protein-Protein Interactions in Living Subjects , 2004, Cancer Research.

[7]  G. Chiosis,et al.  Synthesis of a red-shifted fluorescence polarization probe for Hsp90. , 2006, Bioorganic & medicinal chemistry letters.

[8]  Kathryn E Luker,et al.  Optimizing luciferase protein fragment complementation for bioluminescent imaging of protein-protein interactions in live cells and animals. , 2004, Methods in enzymology.

[9]  Sreenath V. Sharma,et al.  Development of radicicol analogues. , 2003, Current cancer drug targets.

[10]  N. Rosen,et al.  Targeting wide-range oncogenic transformation via PU24FCl, a specific inhibitor of tumor Hsp90. , 2004, Chemistry & biology.

[11]  G. Chiosis Discovery and development of purine-scaffold Hsp90 inhibitors. , 2006, Current topics in medicinal chemistry.

[12]  Julie L Prior,et al.  Imaging reversal of multidrug resistance in living mice with bioluminescence: MDR1 P-glycoprotein transports coelenterazine. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[13]  N. Rosen,et al.  A small molecule designed to bind to the adenine nucleotide pocket of Hsp90 causes Her2 degradation and the growth arrest and differentiation of breast cancer cells. , 2001, Chemistry & biology.

[14]  S S Gambhir,et al.  Noninvasive imaging of protein–protein interactions in living subjects by using reporter protein complementation and reconstitution strategies , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[15]  P. Csermely,et al.  Hsp90 isoforms: functions, expression and clinical importance , 2004, FEBS letters.

[16]  S. Gambhir,et al.  Optical imaging of Renilla luciferase reporter gene expression in living mice , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[17]  Z. Naito,et al.  Expression of hsp90 and cyclin D1 in human breast cancer. , 1999, Cancer letters.

[18]  Gabriela Chiosis,et al.  Evaluation of 8-arylsulfanyl, 8-arylsulfoxyl, and 8-arylsulfonyl adenine derivatives as inhibitors of the heat shock protein 90. , 2005, Journal of medicinal chemistry.

[19]  J. Caldwell,et al.  A time-resolved fluorescence resonance energy transfer-based HTS assay and a surface plasmon resonance-based binding assay for heat shock protein 90 inhibitors. , 2004, Analytical biochemistry.

[20]  J. Novotný,et al.  Firefly Luciferase Produces Hydrogen Peroxide as a Coproduct in Dehydroluciferyl Adenylate Formation , 2006, Chembiochem : a European journal of chemical biology.

[21]  Neal Rosen,et al.  Imaging the pharmacodynamics of HER2 degradation in response to Hsp90 inhibitors , 2004, Nature Biotechnology.

[22]  Gabriela Chiosis,et al.  Identification of potent water soluble purine-scaffold inhibitors of the heat shock protein 90. , 2006, Journal of medicinal chemistry.

[23]  L. Neckers,et al.  Heat shock protein 90 , 2003, Current opinion in oncology.

[24]  Jason C. Young,et al.  Inhibition of GR‐mediated transcription by p23 requires interaction with Hsp90 , 2004, FEBS letters.

[25]  Gary D Luker,et al.  Visualizing protein-protein interactions in living animals. , 2003, Methods.

[26]  N. Rosen,et al.  Inhibition of heat shock protein 90 function by ansamycins causes the morphological and functional differentiation of breast cancer cells. , 2001, Cancer research.

[27]  H. Müller-Hermelink,et al.  STAT3 and MAPK signaling maintain overexpression of heat shock proteins 90α and β in multiple myeloma cells, which critically contribute to tumor-cell survival , 2007 .

[28]  S S Gambhir,et al.  Monitoring protein-protein interactions using split synthetic renilla luciferase protein-fragment-assisted complementation. , 2003, Analytical chemistry.

[29]  T. Takagi,et al.  Mechanism of dimer formation of the 90-kDa heat-shock protein. , 1995, European journal of biochemistry.

[30]  J. Sloan,et al.  Phase I trial of 17-allylamino-17-demethoxygeldanamycin in patients with advanced cancer. , 2005, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[31]  Sanjiv Sam Gambhir,et al.  Consensus guided mutagenesis of Renilla luciferase yields enhanced stability and light output. , 2006, Protein engineering, design & selection : PEDS.

[32]  D. Solit,et al.  Heat shock protein-90 inhibitors: a chronicle from geldanamycin to today's agents. , 2006, Current opinion in investigational drugs.

[33]  L. Fritz,et al.  A high-affinity conformation of Hsp90 confers tumour selectivity on Hsp90 inhibitors , 2003, Nature.

[34]  Neal Rosen,et al.  Hsp90: a novel target for cancer therapy. , 2006, Current topics in medicinal chemistry.

[35]  D. Scudiero,et al.  New colorimetric cytotoxicity assay for anticancer-drug screening. , 1990, Journal of the National Cancer Institute.

[36]  L. Pearl,et al.  High-throughput screening assay for inhibitors of heat-shock protein 90 ATPase activity. , 2004, Analytical biochemistry.

[37]  N. Rosen,et al.  Development of purine-scaffold small molecule inhibitors of Hsp90. , 2003, Current cancer drug targets.

[38]  N. Rosen,et al.  Development of a purine-scaffold novel class of Hsp90 binders that inhibit the proliferation of cancer cells and induce the degradation of Her2 tyrosine kinase. , 2002, Bioorganic & medicinal chemistry.

[39]  C. Nicchitta,et al.  Synthesis of Hsp90 dimerization modulators. , 2006, Bioorganic & medicinal chemistry letters.

[40]  D. Toft,et al.  Dimerization and N-terminal domain proximity underlie the function of the molecular chaperone heat shock protein 90. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[41]  P. Workman,et al.  Chaperoning cell death: a critical dual role for Hsp90 in small-cell lung cancer. , 2007, Nature chemical biology.

[42]  Igor Stagljar,et al.  Application of the split-ubiquitin membrane yeast two-hybrid system to investigate membrane protein interactions. , 2004, Methods.

[43]  Hong Zhang,et al.  Targeting multiple signal transduction pathways through inhibition of Hsp90 , 2004, Journal of Molecular Medicine.

[44]  S. Lakhani,et al.  Phase I pharmacokinetic and pharmacodynamic study of 17-allylamino, 17-demethoxygeldanamycin in patients with advanced malignancies. , 2005, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[45]  Wei Li,et al.  Noninvasive imaging of protein–protein interactions in living animals , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[46]  Bin Chen,et al.  The HSP90 family of genes in the human genome: insights into their divergence and evolution. , 2005, Genomics.

[47]  A. Kamal,et al.  Therapeutic and diagnostic implications of Hsp90 activation , 2004, Trends in Molecular Medicine.