Geldanamycin inhibits migration of glioma cells in vitro: A potential role for hypoxia-inducible factor (HIF-1α) in glioma cell invasion

Journal of Cellular Physiology

Volumn 196, Issue 2, 2003, Pages 394-402

  Zagzag, David ^a,b,c   Nomura, Motohiro ^a   Friedlander, David R ^a   Blanco, C Y ^a   Gagner, Jean Pierre ^a   Nomura, Naoko ^a   Newcomb, Elizabeth W ^a,b  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NEW YORK UNIVERSITY   (United States)

^c NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANSAMYCIN DERIVATIVE; COBALT CHLORIDE; FOCAL ADHESION KINASE; GELDANAMYCIN; HEAT SHOCK PROTEIN 90; HYPOXIA INDUCIBLE FACTOR 1ALPHA; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN P53; VASCULOTROPIN;

ANGIOGENESIS; ANTINEOPLASTIC ACTIVITY; ARTICLE; BLOOD BRAIN BARRIER; CANCER CELL; CANCER INVASION; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFECT; ENDOTHELIUM CELL; ENZYME PHOSPHORYLATION; GLIOBLASTOMA; HUMAN; HUMAN CELL; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN FUNCTION; TRANSCRIPTION REGULATION; TREATMENT INDICATION; TREATMENT OUTCOME; TUMOR GROWTH; UPREGULATION;

ANTIBIOTICS, ANTINEOPLASTIC; BENZOQUINONES; CELL MOVEMENT; COBALT; EXTRACELLULAR MATRIX PROTEINS; FOCAL ADHESION KINASE 1; FOCAL ADHESION PROTEIN-TYROSINE KINASES; GLIOMA; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LACTAMS, MACROCYCLIC; NEOPLASM INVASIVENESS; OSMOLAR CONCENTRATION; PHOSPHORIC MONOESTER HYDROLASES; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; PTEN PHOSPHOHYDROLASE; QUINONES; TRANSCRIPTION FACTORS; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS;

EID: 0037784052     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.10306     Document Type: Article

References (55)

1. Abedi H, Zachary I. 1997. Vascular endothelial growth factor stimulates tyrosine phosphorylation and recruitment to new focal adhesions of focal adhesion kinase and paxillin in endothelial cells. J Biol Chem 272:15442-15451.
2. Arai Y, Kubota T, Nakagawa T, Kabuto M, Sato K, Kobayashi H. 1998. Production of urokinase-type plasminogen activator (u-PA) and plasminogen activator inhibitor-1 (PAI-1) in human brain tumors. Acta Neurochir (Wien) 140:377-386.
3. Bishop CD, Bates WR, Brandhorst BP. 2002. HSP90 function is required for morphogenesis in ascidian and echinoid embryos. Dev Genes Evol 212:70-80.
4. Blagosklonny MV, Toretsky J, Bohen S, Neckers L. 1996. Mutant conformation of p53 translated in vitro or in vivo requires functional HSP90. Proc Natl Acad Sci USA 93:8379-8383.
5. Brugge JS, Erikson E, Erikson RL. 1981. The specific interaction of the Rous sarcoma virus transforming protein, pp60src, with two cellular proteins. Cell 25:363-372.
6. Burridge K, Turner CE, Romer LH. 1992. Tyrosine phosphorylation of paxillin and 125FAK accompanies cell adhesion to extracellular matrix: A role in cytoskeletal assembly. J Cell Biol 119:893-903.
7. Byzova TV, Kim W, Midura RJ, Plow EF. 2000. Activation of integrin alpha(V)beta(3) regulates cell adhesion and migration to bone sialoprotein. Exp Cell Res 254:299-308.
8. Carmeliet P, Jain RK. 2000. Angiogenesis in cancer and other diseases. Nature 407:249-257.
9. Clark EA, Brugge JS. 1995. Integrins and signal transduction pathways: The road taken. Science 268:233-239.
10. Coumailleau P, Poellinger L, Gustafsson JA, Whitelaw ML. 1995. Definition of a minimal domain of the dioxin receptor that is associated with Hsp90 and maintains wild type ligand binding affinity and specificity. J Biol Chem 270:25291-25300.
11. Cuvier C, Jang A, Hill RP. 1997. Exposure to hypoxia, glucose starvation, and acidosis: Effect on invasive capacity of murine tumor cells and correlation with cathepsin (L+B) secretion. Clin Exp Metastasis 15:19-25.
12. Eberhard A, Kahlert S, Goede V, Hemmerlein B, Plate KH, Augustin HG. 2000. Heterogeneity of angiogenesis and blood vessel maturation in human tumors: Implications for antiangiogenic tumor therapies. Cancer Res 60:1388-1393.
13. Fitzpatrick TE, Graham CH. 1998. Stimulation of plasminogen activator inhibitor-1 expression in immortalized human trophoblast cells cultured under low levels of oxygen. Exp Cell Res 245:155-162.
14. Friedlander DR, Zagzag D, Schiff B, Cohen H, Allen JC, Kelly PJ, Grumet M. 1996. Migration of tumor cells on extracellular matrix proteins in vitro correlates with tumor type and grade, and involves αv and β1 integrins. Cancer Res 56:1939-1947.
15. Furuta Y, Ilic D, Kanazawa S, Takeda N, Yamamoto T, Aizawa S. 1995. Mesodermal defect in late phase of gastrulation by a targeted mutation of focal adhesion kinase, FAK. Oncogene 11:1989-1995.
16. Gradin K, McGuire J, Wenger RH, Kvietikova I, Whitelaw ML, Toftgard R, Tora L, Gassmann M, Poellinger L. 1996. Functional interference between hypoxia and dioxin signal transduction pathways: Competition for recruitment of the Arnt transcription factor. Mol Cell Biol 16:5221-5231.
17. Graeber TG, Osamanian C, Jacks T, Housman DE, Koch CJ, Lowe SW, Giaccia AJ. 1996. Hypoxia-mediated selection of cells with diminished apoptic potential in solid tumors. Nature 379:88-91.
18. Graham CH, Fitzpatrick TE, McCrae KR. 1998. Hypoxia stimulates urokinase receptor expression through a heme protein-dependent pathway. Blood 91:3300-3307.
19. Graham CH, Forsdike J, Fitzgerald CJ, Macdonald-Goodfellow S. 1999. Hypoxia-mediated stimulation of carcinoma cell invasiveness via upregulation of urokinase receptor expression. Int J Cancer 80:617-623.
20. Grenert JP, Sullivan WP, Fadden P, Haystead TA, Clark J, Mimnaugh E, Krutzsch H, Ochel HJ, Schulte TW, Sausville E, Neckers LM, Toft DO. 1997. The amino-terminal domain of heat shock protein 90 (hsp90) that binds geldanamycin is an ATP/ADP switch domain that regulates hsp90 conformation. J Biol Chem 272:23843-23850.
21. Haskell H, Natarajan M, Hecker T, Stewart J, Ding Q, Grammer JR, Gladson CL. 2002. Focal adhesion kinase (FAK) is expressed in the angiogenic blood vessels of malignant astrocytoma tumors in vivo and it is necessary for tube formation of brain capillary endothelial cells. J Neuropathol Exp Neurol 61:445.
22. Hecker TP, Grammer JR, Gillespie GY, Stewart J, Jr., Gladson CL. 2002. Focal adhesion kinase enhances signaling through the Shc/extracellular signal-regulated kinase pathway in anaplastic astrocytoma tumor biopsy samples. Cancer Res 62:2699-2707.
23. Ilic D, Furuta Y, Kanazawa S, Takeda N, Sobue K, Nakatsuji N, Nomura S, Fujimoto J, Okada M, Yamamoto T. 1995. Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 377:539-544.
24. Isaacs JS, Jung YJ, Mimnaugh EG, Martinez A, Cuttitta F, Neckers LM. 2002. Hsp90 regulates a von Hippel Lindau-independent hypoxia-inducible factor-1 alpha-degradative pathway. J Biol Chem 277:29936-29944.
25. Kalra VK, Shen Y, Sultana C, Rattan V. 1996. Hypoxia induces PECAM-1 phosphorylation and transendothelial migration of monocytes. Am J Physiol 271:2025-2034.
26. Kleihues P, Cavenee WK. 2000. World Health Organization Classification of Tumors: Pathology and genetics of tumors of the nervous system. Lyon: IARC Press.
27. Lehner CF, Kurer V, Eppenberger HM, Nigg EA. 1986. The nuclear lamin protein family in higher vertebrates. Identification of quantitatively minor lamin proteins by monoclonal antibodies. J Biol Chem 261:13293-13301.
28. Mabjeesh NJ, Posse DE, Willard MT, Kaur B, Van Meir EG, Simons JW, Zhong H. 2002. Geldanamycin induces degradation of hypoxia-inducible factor 1 alpha protein via the proteosome pathway in prostate cancer cells. Cancer Res 62:2478-2482.
29. Maher EA, Furnari FB, Bachoo RM, Rowitch DH, Louis DN, Cavenee WK, DePinho RA. 2001. Malignant glioma: Genetics and biology of a grave matter. Genes Dev 15:1311-1333.
30. Meininger CJ, Schelling ME, Granger HJ. 1988. Adenosine and hypoxia stimulate proliferation and migration of endothelial cells. Am J Physiol 255:554-562.
31. Mimnaugh EG, Chavany C, Neckers L. 1996. Polyubiquitination and proteasomal degradation of the p185c-erbB-2 receptor protein-tyrosine kinase induced by geldanamycin. J Biol Chem 271:22796-22801.
32. Minet E, Mottet D, Michel G, Roland I, Raes M, Remacle J, Michiels C. 1999. Hypoxia-induced activation of HIF-1: Role of HIF-1alpha-Hsp90 interaction. FEBS Lett 460:251-256.
33. Mohan PM, Chintala SK, Mohanam S, Gladson CL, Kim ES, Gokaslan ZL, Lakka SS, Roth JA, Fang B, Sawaya R, Kyritisis AP, Rao JS. 1999. Adenovirus-mediated delivery of antisense gene to urokinase-type plasminogen activator receptor suppresses glioma invasion and tumor growth. Cancer Res 59:3369-3373.
34. Plopper G, McNamee H, Dike LE, Bojanowski K, Ingber DE. 1995. Convergence of integrin and growth factor receptor signaling pathways within the focal adhesion complex. Mol Biol Cell 6:1349-1365.
35. Rapisarda A, Uranchimeg B, Scudiero DA, Selby M, Sausville EA, Shoemaker RH, Melillo G. 2002. Identification of small molecule inhibitors of hypoxia-inducible factor 1 transcriptional activation pathway. Cancer Res 62:4316-4324.
36. Ravi R, Mookerjee B, Bhujwalla ZM, Sutter CH, Artemov D, Zeng Q, Dillehay LE, Madan A, Semenza GL, Bedi A. 2000. Regulation of tumor angiogenesis by p53-induced degradation of hypoxia-inducible factor 1 alpha. Genes Dev 14:34-44.
37. Rousseau S, Houle F, Kotanides H, Witte L, Waltenberger J, Landry J, Huot J. 2000. Vascular endothelial growth factor (VEGF)-driven actin-based motility is mediated by VEGFR2 and requires concerted activation of stress-activated protein kinase 2 (SAPK2/p38) and geldanamycin-sensitive phosphorylation of focal adhesion kinase. J Biol Chem 275:10661-10672.
38. Sanchez ER, Toft DO, Schlesinger MJ, Pratt WB. 1985. Evidence that the 90-kDa phosphoprotein associated with the untransformed L-cell glucocorticoid receptor is a murine heat shock protein. J Biol Chem 260:12398-12401.
39. Sato S, Fujita N, Tsuruo T. 2000. Modulation of Akt kinase activity by binding to Hsp90. Proc Natl Acad Sci USA 97:10832-10837.
40. Schnur RC, Corman ML, Gallaschun RJ, Cooper BA, Dee MF, Doty JL, Muzzi ML, Moyer JD, DiOrio CI, Barbacci EG, et al. 1995. Inhibition of the oncogene product p185erbB-2 in vitro and in vivo by geldanamycin and dihydrogeldanamycin derivatives. J Med Chem 38:3806-3812.
41. Schulte TW, An WG, Neckers LM. 1997. Geldanamycin-induced destabilization of Raf-1 involves the proteasome. Biochem Biophys Res Commun 239:655-659.
42. Semenza GL. 2002. Involvement of hypoxia-inducible factor 1 in human cancer. Intern Med 41:79-83.
43. Shaknovich R, Shue G, Kohtz DS. 1992. Conformational activation of a basic helix-loop-helix protein (MyoD1) by the C-terminal region of murine HSP90 (HSP84). Mol Cell Biol 12:5059-5068.
44. Stancato LF, Chow YH, Hutchison KA, Perdew GH, Jove R, Pratt WB. 1993. Raf exists in a native heterocomplex with hsp90 and p50 that can be reconstituted in a cell-free system. J Biol Chem 268:21711-21716.
45. Stebbins CE, Russo AA, Schneider C, Rosen N, Hartl FU, Pavletich NP. 1997. Crystal structure of an Hsp90-geldanamycin complex: Targeting of a protein chaperone by an antitumor agent. Cell 89:239-250.
46. Stracke S, Ernst F, Jehle DR, Grunewald RW, Haller H, Keller F, Jehle PM. 1998. Differentiating and proliferative effects of HGF in renal proximal tubular cells are mediated via different signaling pathways. Nephrol Dial Transplant 13:1398-1405.
47. Tamura M, Gu J, Matsumoto K, Aota S, Parsons R, Yamada KM. 1998. Inhibition of cell migration, spreading, and focal adhesions by tumor suppressor PTEN. Science 280:1614-1617.
48. Whitesell L, Shifrin SD, Schwab G, Neckers LM. 1992. Benzoquinonoid ansamycins possess selective tumoricidal activity unrelated to src kinase inhibition. Cancer Res 52:1721-1728.
49. Whitesell L, Mimnaugh EG, De Costa B, Myers CE, Neckers LM. 1994. Inhibition of heat shock protein HSP90-pp60v-src heteroprotein complex formation by benzoquinone ansamycins: Essential role of stress proteins in oncogenic transformation. Proc Natl Acad Sci USA 91:8324-8328.
50. Whitesell L, Sutphin P, Ah WG, Schulte T, Blagosklonny MV, Neckers L. 1997. Geldanamycin-stimulated destabilization of mutated p53 is mediated by the proteasome in vivo. Oncogene 14:2809-2816.
51. Xu W, Mimnaugh E, Rosser MF, Nicchitta C, Marcu M, Yarden Y, Neckers L. 2001. Sensitivity of mature Erbb2 to geldanamycin is conferred by its kinase domain and is mediated by the chaperone protein Hsp90. J Biol Chem 276:3702-3708.
52. Zagzag D, Friedlander DR, Margolis B, Grumet M, Semenza GL, Zhong H, Simons JW, Holash J, Wiegand SJ, Yancopoulos GD. 2000a. Molecular events implicated in brain tumor angiogenesis and invasion. Pediatr Neurosurg 33:49-55.
53. Zagzag D, Zhong H, Scalzitti JM, Laughner E, Simons JW, Semenza GL. 2000b. Expression of hypoxia-inducible factor 1α in human brain tumors: Association with angiogenesis, invasion, and progression. Cancer 88:2606-2618.
54. Zagzag D, Shiff B, Jallo GI, Greco MA, Blanco C, Cohen H, Hukin J, Allen JC, Friedlander DR. 2002. Tenascin-C promotes microvascular cell migration and phosphorylation of focal adhesion kinase. Cancer Res 62:2660-2668.
55. Zundel W, Schindler S, Haas-Kogan D, Koong A, Kaper F, Chen E, Gottschalk AR, Ryan HE, Johnson RS, Jefferson AB, Stokoe D, Giacca AJ. 2000. Loss of PTEN facilitates HIF-1-mediated gene expression. Genes Dev 14:391-396.