Hsp90 inhibition differentially destabilises MAP kinase and TGF-beta signalling components in cancer cells revealed by kinase-targeted chemoproteomics

BMC Cancer

Volumn 12, Issue , 2012, Pages

  Haupt, Armin ^a   Joberty, Gerard ^b   Bantscheff, Marcus ^b   Fröhlich, Holger ^b,c   Stehr, Henning ^a   Schweiger, Michal R ^a   Fischer, Axel ^a   Kerick, Martin ^a   Boerno, Stefan T ^a   Dahl, Andreas ^a   Lappe, Michael ^a   Lehrach, Hans ^a   Gonzalez, Cayetano ^d,e   Drewes, Gerard ^b   Lange, Bodo M H ^a  

^a MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^b GLAXOSMITHKLINE   (United Kingdom)

^c UNIVERSITY OF BONN   (Germany)

^d INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^e INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; BONE MORPHOGENETIC PROTEIN; GELDANAMYCIN; HEAT SHOCK PROTEIN 90; MITOGEN ACTIVATED PROTEIN KINASE; PROTEASOME; RECEPTOR INTERACTING PROTEIN SERINE THREONINE KINASE 2; TRANSFORMING GROWTH FACTOR BETA; BENZOQUINONE DERIVATIVE; ENZYME INHIBITOR; MACROCYCLIC LACTAM; RIPK2 PROTEIN, HUMAN;

ARTICLE; BINDING AFFINITY; BINDING SITE; CANCER CELL CULTURE; CANCER GROWTH; CANCER RESEARCH; CELL FUNCTION; CONTROLLED STUDY; ENZYME ANALYSIS; ENZYME INHIBITION; ENZYME STABILITY; MOLECULAR DYNAMICS; MOLECULAR RECOGNITION; MUTATION RATE; PRIMARY CELL CULTURE; PROTEIN STABILITY; PROTEIN TARGETING; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; STRUCTURAL PROTEOMICS; STRUCTURE ANALYSIS; CHEMISTRY; DRUG ANTAGONISM; DRUG EFFECT; GENETICS; HUMAN; METABOLISM; MUTATION; NEOPLASM; PROTEOMICS; TUMOR CELL LINE;

BENZOQUINONES; CELL LINE, TUMOR; ENZYME INHIBITORS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HSP90 HEAT-SHOCK PROTEINS; HUMANS; LACTAMS, MACROCYCLIC; MUTATION; NEOPLASMS; PROTEOMICS; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASE 2; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 84856078153     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-12-38     Document Type: Article

References (43)

1. Whitesell L, Lindquist SL. HSP90 and the chaperoning of cancer. Nat Rev Cancer 2005, 5:761-772. 10.1038/nrc1716, 16175177.
2. Richter K, Buchner J. Hsp90: chaperoning signal transduction. J Cell Physiol 2001, 188:281-290. 10.1002/jcp.1131, 11473354.
3. Pick E, Kluger Y, Giltnane JM, Moeder C, Camp RL, Rimm DL, Kluger HM. High HSP90 expression is associated with decreased survival in breast cancer. Cancer Res 2007, 67:2932-2937. 10.1158/0008-5472.CAN-06-4511, 17409397.
4. Yano M, Naito Z, Tanaka S, Asano G. Expression and roles of heat shock proteins in human breast cancer. Jpn J Cancer Res 1996, 87:908-915. 10.1111/j.1349-7006.1996.tb02119.x, 8878452.
5. Porter JR, Fritz CC, Depew KM. Discovery and development of Hsp90 inhibitors: a promising pathway for cancer therapy. Curr Opin Chem Biol 2010, 14:412-420. 10.1016/j.cbpa.2010.03.019, 20409745.
6. Trepel J, Mollapour M, Giaccone G, Neckers L. Targeting the dynamic HSP90 complex in cancer. Nat Rev Cancer 2010, 10:537-549. 10.1038/nrc2887, 20651736.
7. Kamal A, Thao L, Sensintaffar J, Zhang L, Boehm MF, Fritz LC, Burrows FJ. A high-affinity conformation of Hsp90 confers tumour selectivity on Hsp90 inhibitors. Nature 2003, 425:407-410. 10.1038/nature01913, 14508491.
8. Caldas-Lopes E, Cerchietti L, Ahn JH, Clement CC, Robles AI, Rodina A, Moulick K, Taldone T, Gozman A, Guo Y, et al. Hsp90 inhibitor PU-H71, a multimodal inhibitor of malignancy, induces complete responses in triple-negative breast cancer models. Proc Natl Acad Sci USA 2009, 106:8368-8373. 10.1073/pnas.0903392106, 2688867, 19416831.
9. Falsone SF, Gesslbauer B, Tirk F, Piccinini AM, Kungl AJ. A proteomic snapshot of the human heat shock protein 90 interactome. FEBS Lett 2005, 579:6350-6354. 10.1016/j.febslet.2005.10.020, 16263121.
10. Gano JJ, Simon JA. A proteomic investigation of ligand-dependent HSP90 complexes reveals CHORDC1 as a novel ADP-dependent HSP90-interacting protein. Mol Cell Proteomics 2009, 9:255-270. 2830838, 19875381.
11. Millson SH, Truman AW, King V, Prodromou C, Pearl LH, Piper PW. A two-hybrid screen of the yeast proteome for Hsp90 interactors uncovers a novel Hsp90 chaperone requirement in the activity of a stress-activated mitogen-activated protein kinase, Slt2p (Mpk1p). Eukaryot Cell 2005, 4:849-860. 10.1128/EC.4.5.849-860.2005, 1140089, 15879519.
12. Te J, Jia L, Rogers J, Miller A, Hartson SD. Novel subunits of the mammalian Hsp90 signal transduction chaperone. J Proteome Res 2007, 6:1963-1973. 10.1021/pr060595i, 17348703.
13. Tsaytler PA, Krijgsveld J, Goerdayal SS, Rudiger S, Egmond MR. Novel Hsp90 partners discovered using complementary proteomic approaches. Cell Stress Chaperones 2009, 14:629-638. 10.1007/s12192-009-0115-z, 2866955, 19396626.
14. Zhao R, Davey M, Hsu YC, Kaplanek P, Tong A, Parsons AB, Krogan N, Cagney G, Mai D, Greenblatt J, et al. Navigating the chaperone network: an integrative map of physical and genetic interactions mediated by the hsp90 chaperone. Cell 2005, 120:715-727. 10.1016/j.cell.2004.12.024, 15766533.
15. McClellan AJ, Xia Y, Deutschbauer AM, Davis RW, Gerstein M, Frydman J. Diverse cellular functions of the Hsp90 molecular chaperone uncovered using systems approaches. Cell 2007, 131:121-135. 10.1016/j.cell.2007.07.036, 17923092.
16. Bantscheff M, Eberhard D, Abraham Y, Bastuck S, Boesche M, Hobson S, Mathieson T, Perrin J, Raida M, Rau C, et al. Quantitative chemical proteomics reveals mechanisms of action of clinical ABL kinase inhibitors. Nat Biotechnol 2007, 25:1035-1044. 10.1038/nbt1328, 17721511.
17. Kiefer F, Arnold K, Kunzli M, Bordoli L, Schwede T. The SWISS-MODEL Repository and associated resources. Nucleic Acids Res 2009, 37:D387-392. 10.1093/nar/gkn750, 2686475, 18931379.
18. Kruse U, Pallasch CP, Bantscheff M, Eberhard D, Frenzel L, Ghidelli S, Maier SK, Werner T, Wendtner CM, Drewes G. Chemoproteomics-based kinome profiling and target deconvolution of clinical multi-kinase inhibitors in primary chronic lymphocytic leukemia cells. Leukemia 2010, 25:89-100.
19. Savitski MM, Fischer F, Mathieson T, Sweetman G, Lang M, Bantscheff M. Targeted data acquisition for improved reproducibility and robustness of proteomic mass spectrometry assays. J Am Soc Mass Spectrom 2010, 21:1668-1679. 10.1016/j.jasms.2010.01.012, 20171116.
20. Sharp S, Workman P. Inhibitors of the HSP90 molecular chaperone: current status. Adv Cancer Res 2006, 95:323-348.
21. Helms MW, Packeisen J, August C, Schittek B, Boecker W, Brandt BH, Buerger H. First evidence supporting a potential role for the BMP/SMAD pathway in the progression of oestrogen receptor-positive breast cancer. J Pathol 2005, 206:366-376. 10.1002/path.1785, 15892165.
22. Kodach LL, Bleuming SA, Musler AR, Peppelenbosch MP, Hommes DW, van den Brink GR, van Noesel CJ, Offerhaus GJ, Hardwick JC. The bone morphogenetic protein pathway is active in human colon adenomas and inactivated in colorectal cancer. Cancer 2008, 112:300-306. 10.1002/cncr.23160, 18008360.
23. Yano A, Tsutsumi S, Soga S, Lee MJ, Trepel J, Osada H, Neckers L. Inhibition of Hsp90 activates osteoclast c-Src signaling and promotes growth of prostate carcinoma cells in bone. Proc Natl Acad Sci USA 2008, 105:15541-15546. 10.1073/pnas.0805354105, 2563126, 18840695.
24. Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M. The KEGG resource for deciphering the genome. Nucleic Acids Res 2004, 32:D277-280. 10.1093/nar/gkh063, 308797, 14681412.
25. Schumacher JA, Crockett DK, Elenitoba-Johnson KS, Lim MS. Proteome-wide changes induced by the Hsp90 inhibitor, geldanamycin in anaplastic large cell lymphoma cells. Proteomics 2007, 7:2603-2616. 10.1002/pmic.200700108, 17610208.
26. Simizu S, Osada H. Mutations in the Plk gene lead to instability of Plk protein in human tumour cell lines. Nat Cell Biol 2000, 2:852-854. 10.1038/35041102, 11056542.
27. Citri A, Harari D, Shohat G, Ramakrishnan P, Gan J, Lavi S, Eisenstein M, Kimchi A, Wallach D, Pietrokovski S, Yarden Y. Hsp90 recognizes a common surface on client kinases. J Biol Chem 2006, 281:14361-14369. 10.1074/jbc.M512613200, 16551624.
28. Clarke PA, Hostein I, Banerji U, Stefano FD, Maloney A, Walton M, Judson I, Workman P. Gene expression profiling of human colon cancer cells following inhibition of signal transduction by 17-allylamino-17-demethoxygeldanamycin, an inhibitor of the hsp90 molecular chaperone. Oncogene 2000, 19:4125-4133. 10.1038/sj.onc.1203753, 10962573.
29. Maloney A, Clarke PA, Naaby-Hansen S, Stein R, Koopman JO, Akpan A, Yang A, Zvelebil M, Cramer R, Stimson L, et al. Gene and protein expression profiling of human ovarian cancer cells treated with the heat shock protein 90 inhibitor 17-allylamino-17-demethoxygeldanamycin. Cancer Res 2007, 67:3239-3253. 10.1158/0008-5472.CAN-06-2968, 17409432.
30. Kelland LR, Sharp SY, Rogers PM, Myers TG, Workman P. DT-Diaphorase expression and tumor cell sensitivity to 17-allylamino, 17-demethoxygeldanamycin, an inhibitor of heat shock protein 90. J Natl Cancer Inst 1999, 91:1940-1949. 10.1093/jnci/91.22.1940, 10564678.
31. Picard D. List of Hsp90 interactors. , http://www.picard.ch/downloads/Hsp90interactors.pdf
32. O'Reilly KE, Rojo F, She QB, Solit D, Mills GB, Smith D, Lane H, Hofmann F, Hicklin DJ, Ludwig DL, et al. mTOR inhibition induces upstream receptor tyrosine kinase signaling and activates Akt. Cancer Res 2006, 66:1500-1508. 10.1158/0008-5472.CAN-05-2925, 3193604, 16452206.
33. Carracedo A, Ma L, Teruya-Feldstein J, Rojo F, Salmena L, Alimonti A, Egia A, Sasaki AT, Thomas G, Kozma SC, et al. Inhibition of mTORC1 leads to MAPK pathway activation through a PI3K-dependent feedback loop in human cancer. J Clin Invest 2008, 118:3065-3074. 2518073, 18725988.
34. Blanco Calvo M, Bolos Fernandez V, Medina Villaamil V, Aparicio Gallego G, Diaz Prado S, Grande Pulido E. Biology of BMP signalling and cancer. Clin Transl Oncol 2009, 11:126-137. 10.1007/S12094-009-0328-8, 19293049.
35. Ye L, Mason MD, Jiang WG. Bone morphogenetic protein and bone metastasis, implication and therapeutic potential. Front Biosci 2011, 16:865-897. 10.2741/3725, 21196208.
36. Kim IY, Lee DH, Ahn HJ, Tokunaga H, Song W, Devereaux LM, Jin D, Sampath TK, Morton RA. Expression of bone morphogenetic protein receptors type-IA, -IB and -II correlates with tumor grade in human prostate cancer tissues. Cancer Res 2000, 60:2840-2844.
37. Kim IY, Lee DH, Lee DK, Ahn HJ, Kim MM, Kim SJ, Morton RA. Loss of expression of bone morphogenetic protein receptor type II in human prostate cancer cells. Oncogene 2004, 23:7651-7659. 10.1038/sj.onc.1207924, 15354178.
38. Heath EI, Hillman DW, Vaishampayan U, Sheng S, Sarkar F, Harper F, Gaskins M, Pitot HC, Tan W, Ivy SP, et al. A phase II trial of 17-allylamino-17-demethoxygeldanamycin in patients with hormone-refractory metastatic prostate cancer. Clin Cancer Res 2008, 14:7940-7946. 10.1158/1078-0432.CCR-08-0221, 3085545, 19047126.
39. Katsuno Y, Hanyu A, Kanda H, Ishikawa Y, Akiyama F, Iwase T, Ogata E, Ehata S, Miyazono K, Imamura T. Bone morphogenetic protein signaling enhances invasion and bone metastasis of breast cancer cells through Smad pathway. Oncogene 2008, 27:6322-6333. 10.1038/onc.2008.232, 18663362.
40. Owens P, Pickup MW, Novitskiy SV, Chytil A, Gorska AE, Aakre ME, West J, Moses HL. Breast Cancer Special Feature: Disruption of bone morphogenetic protein receptor 2 (BMPR2) in mammary tumors promotes metastases through cell autonomous and paracrine mediators. Proc Natl Acad Sci USA 2011,
41. Pouliot F, Blais A, Labrie C. Overexpression of a dominant negative type II bone morphogenetic protein receptor inhibits the growth of human breast cancer cells. Cancer Res 2003, 63:277-281.
42. Wagner EF, Nebreda AR. Signal integration by JNK and p38 MAPK pathways in cancer development. Nat Rev Cancer 2009, 9:537-549. 10.1038/nrc2694, 19629069.
43. Sos ML, Michel K, Zander T, Weiss J, Frommolt P, Peifer M, Li D, Ullrich R, Koker M, Fischer F, et al. Predicting drug susceptibility of non-small cell lung cancers based on genetic lesions. J Clin Invest 2009, 119:1727-1740. 10.1172/JCI37127, 2689116, 19451690.