Increased uptake of [123I]meta-iodobenzylguanidine, [ 18F]fluorodopamine, and [3H]norepinephrine in mouse pheochromocytoma cells and tumors after treatment with the histone deacetylase inhibitors

Endocrine-Related Cancer

Volumn 18, Issue 1, 2011, Pages 143-157

  Martiniova, Lucia ^a,f   Perera, Shiromi M ^a   Brouwers, Frederieke M ^a   Alesci, Salvatore ^b   Abu Asab, Mones ^c   Marvelle, Amanda F ^a   Kiesewetter, Dale O ^d   Thomasson, David ^e   Morris, John C ^c   Kvetnansky, Richard ^f   Tischler, Arthur S ^g   Reynolds, James C ^h   Fojo, Antonio Tito ^c   Pacak, Karel ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d NATIONAL INSTITUTE OF BIOMEDICAL IMAGING AND BIOENGINEERING   (United States)

^e NATIONAL INSTITUTES OF HEALTH   (United States)

^f INSTITUTE OF EXPERIMENTAL ENDOCRINOLOGY   (Slovakia)

^g TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^h NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

(3 IODOBENZYL)GUANIDINE I 123; (3 IODOBENZYL)GUANIDINE I 131; 6 FLUORODOPAMINE F 18; DESIPRAMINE; NORADRENALIN; NORADRENALIN TRANSPORTER; RESERPINE; ROMIDEPSIN; TRICHOSTATIN A; (3 IODOBENZYL)GUANIDINE; 6 FLUORODOPAMINE; 6-FLUORODOPAMINE; ANTINEOPLASTIC AGENT; DIAGNOSTIC AGENT; DOPAMINE; DRUG DERIVATIVE; FLUORINE; HISTONE DEACETYLASE INHIBITOR; RADIOACTIVE IODINE; RADIOPHARMACEUTICAL AGENT;

ACETYLATION; ADVANCED CANCER; ANIMAL CELL; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER CELL; CANCER INHIBITION; CELL DIFFERENTIATION; CONTROLLED STUDY; FEMALE; IN VITRO STUDY; IN VIVO STUDY; LIVER METASTASIS; MOUSE; NONHUMAN; PARAGANGLIOMA; PHEOCHROMOCYTOMA; POSITRON EMISSION TOMOGRAPHY; ADJUVANT CHEMOTHERAPY; ADRENAL TUMOR; ANIMAL; CANCER TRANSPLANTATION; EVALUATION; LIVER TUMOR; METABOLISM; METASTASIS; MOUSE MUTANT; MULTIMODALITY CANCER THERAPY; NUDE MOUSE; PATHOLOGY; SCINTISCANNING; TUMOR CELL LINE; UPREGULATION;

3-IODOBENZYLGUANIDINE; ADRENAL GLAND NEOPLASMS; ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CELL LINE, TUMOR; CHEMOTHERAPY, ADJUVANT; COMBINED MODALITY THERAPY; DOPAMINE; FEMALE; FLUORINE RADIOISOTOPES; HISTONE DEACETYLASE INHIBITORS; IODINE RADIOISOTOPES; LIVER NEOPLASMS; MICE; MICE, KNOCKOUT; MICE, NUDE; NEOPLASM TRANSPLANTATION; NOREPINEPHRINE; PHEOCHROMOCYTOMA; RADIOPHARMACEUTICALS; UP-REGULATION;

EID: 79251514664     PISSN: 13510088     EISSN: 14796821     Source Type: Journal    
DOI: 10.1677/ERC-10-0090     Document Type: Article

References (70)

1. Adjalle R, Plouin PF, Pacak K & Lehnert H 2009 Treatment of malignant pheochromocytoma. Hormone and Metabolic Research 41 687-696. (doi:10.1055/s-0029-1231025)
2. Averbuch SD, Steakley CS, Young RC, Gelmann EP, Goldstein DS, Stull R & Keiser HR 1988 Malignant pheochromocytoma: effective treatment with a combination of cyclophosphamide, vincristine, and dacarbazine. Annals of Internal Medicine 109 267-273.
3. 123/131I-MIBG on efficacy, pharmacokinetics, and tissue distribution. Cancer Biotherapy & Radiopharmaceuticals 25 299-308. (doi:10.1089/cbr.2009.0695)
4. 131I-MIBG: dosimetric problems and perspectives. Medical and Pediatric Oncology 15 188-191. (doi:10.1002/mpo.2950150409)
5. Chen X, Gardner ER & Figg WD 2008 Determination of the cyclic depsipeptide FK228 in human and mouse plasma by liquid chromatography with mass-spectrometric detection. Journal of Chromatography. B. Analytical Technologies in the Biomedical and Life Sciences 865 153-158. (doi:10.1016/j.jchromb.2008.02.015)
6. Chen J, Zhang M, Ju W & Waldmann TA 2009 Effective treatment of a murine model of adult T-cell leukemia using depsipeptide and its combination with unmodified daclizumab directed toward CD25. Blood 113 1287-1293. (doi:10.1182/blood-2008-04-149658)
7. Cleary S & Phillips JK 2006 The norepinephrine transporter and pheochromocytoma. Annals of the New York Academy of Sciences 1073 263-269. (doi:10.1196/annals.1353.029)
8. Coleman RE, Stubbs JB, Barrett JA, de la Guardia M, Lafrance N & Babich JW 2009 Radiation dosimetry, pharmacokinetics, and safety of ultratrace Iobenguane I-131 in patients with malignant pheochromocytoma/ paraganglioma or metastatic carcinoid. Cancer Biotherapy & Radiopharmaceuticals 24 469-475. (doi:10.1089/cbr.2008.0584)
9. Cornelissen J, Tytgat GA, van den Brug M, van Kuilenburg AB, Voute PA & van Gennip AH 1997 Menadione inhibits MIBG uptake in two neuroendocrine cell lines. Journal of Neuro-Oncology 31 147-151. (doi:10.1023/A:1005718421774)
10. Eisenhofer G, Hovevey-Sion D, Kopin IJ, Miletich R, Kirk KL, Finn R & Goldstein DS 1989 Neuronal uptake and metabolism of 2- and 6-fluorodopamine: false neurotransmitters for positron emission tomographic imaging of sympathetically innervated tissues. Journal of Pharmacology and Experimental Therapeutics 248 419-427.
11. Eldadah BA, Pacak K, Eisenhofer G, Holmes C, Kopin IJ & Goldstein DS 2004 Cardiac uptake-1 inhibition by high circulating norepinephrine levels in patients with pheochromocytoma. Hypertension 43 1227-1232. (doi:10.1161/01.HYP. 0000127305.87552.d6)
12. 131I-MIBG). Annals of the New York Academy of Sciences 1073 465-490. (doi:10.1196/annals.1353.050)
13. Furuya F, Shimura H, Suzuki H, Taki K, Ohta K, Haraguchi K, Onaya T, Endo T & Kobayashi T 2004 Histone deacetylase inhibitors restore radioiodide uptake and retention in poorly differentiated and anaplastic thyroid cancer cells by expression of the sodium/iodide symporter thyroperoxidase and thyroglobulin. Endocrinology 145 2865-2875. (doi:10.1210/en.2003-1258)
14. Gaal J, Burnichon N, Korpershoek E, Roncelin I, Bertherat J, Plouin PF, de Krijger RR, Gimenez-Roqueplo AP & Dinjens WN 2010 Isocitrate dehydrogenase mutations are rare in pheochromocytomas and paragangliomas. Journal of Clinical Endocrinology and Metabolism 95 1274-1278. (doi:10.1210/jc.2009-2170)
15. Glowniak JV, Kilty JE, Amara SG, Hoffman BJ & Turner FE 1993 Evaluation of metaiodobenzylguanidine uptake by the norepinephrine, dopamine and serotonin transporters. Journal of Nuclear Medicine 34 1140-1146.
16. Goldsmith ME, Aguila A, Steadman K, Martinez A, Steinberg SM, Alley MC, Waud WR, Bates SE & Fojo T 2007 The histone deacetylase inhibitor FK228 given prior to adenovirus infection can boost infection in melanoma xenograft model systems. Molecular Cancer Therapeutics 6 496-505. (doi:10.1158/1535-7163. MCT-06-0431)
17. 131I]metaiodobenzylguanidine therapy for patients with metastatic pheochromocytoma and paraganglioma. Journal of Clinical Oncology 27 4162-4168. (doi:10.1200/JCO.2008.21.3496)
18. Green MV, Seidel J, Vaquero JJ, Jagoda E, Lee I & Eckelman WC 2001 High resolution PET, SPECT and projection imaging in small animals. Computerized Medical Imaging and Graphics 25 79-86. (doi:10.1016/S0895-6111(00)00057-4)
19. Gruning T, Tiepolt C, Zophel K, Bredow J, Kropp J & Franke WG 2003 Retinoic acid for redifferentiation of thyroid cancer - does it hold its promise? European Journal of Endocrinology 148 395-402. (doi:10.1530/eje.0. 1480395)
20. Hirokawa Y, Arnold M, Nakajima H, Zalcberg J & Maruta H 2005a Signal therapy of breast cancers by the HDAC inhibitor FK228 that blocks the activation of PAK1 and abrogates the tamoxifen-resistance. Cancer Biology & Therapy 4 956-960. (doi:10.4161/cbt.4.9.1911)
21. Hirokawa Y, Nakajima H, Hanemann CO, Kurtz A, Frahm S, Mautner V & Maruta H 2005b Signal therapy of NF1- deficient tumor xenograft in mice by the anti-PAK1 drug FK228. Cancer Biology & Therapy 4 379-381. (doi:10.4161/cbt.4.4.1649)
22. Huang H, Abraham J, Hung E, Averbuch S, Merino M, Steinberg SM, Pacak K & Fojo T 2008 Treatment of malignant pheochromocytoma/paraganglioma with cyclophosphamide, vincristine, and dacarbazine: recommendation from a 22-year follow-up of 18 patients. Cancer 113 2020-2028. (doi:10.1002/cncr.23812)
23. Hutchins GD, Miller MA, Soon VC & Receveur T 2008 Small animal PET imaging. Institute of Laboratory Animal Resources Journal 49 54-65.
24. Ichijo T, Voutetakis A, Cotrim AP, Bhattachryya N, Fujii M, Chrousos GP & Kino T 2005 The Smad6-histone deacetylase 3 complex silences the transcriptional activity of the glucocorticoid receptor: potential clinical implications. Journal of Biological Chemistry 280 42067-42077. (doi:10.1074/jbc.M509338200)
25. Jaques S Jr, Tobes MC, Sisson JC, Baker JA & Wieland DM 1984 Comparison of the sodium dependency of uptake of meta-lodobenzylguanidine and norepinephrine into cultured bovine adrenomedullary cells. Molecular Pharmacology 26 539-546.
26. John H, Ziegler WH, Hauri D & Jaeger P 1999 Pheochromocytomas: can malignant potential be predicted? Urology 53 679-683. (doi:10.1016/S0090- 4295(98)00612-8)
27. Keyes JW Jr 1995 SUV: standard uptake or silly useless value? Journal of Nuclear Medicine 36 1836-1839.
28. Kim MS, Blake M, Baek JH, Kohlhagen G, Pommier Y & Carrier F 2003 Inhibition of histone deacetylase increases cytotoxicity to anticancer drugs targeting DNA. Cancer Research 63 7291-7300.
29. Kitazono M, Robey R, Zhan Z, Sarlis NJ, Skarulis MC, Aikou T, Bates S & Fojo T 2001 Low concentrations of the histone deacetylase inhibitor, depsipeptide (FR901228), increase expression of the Na(+)/I(-) symporter and iodine accumulation in poorly differentiated thyroid carcinoma cells. Journal of Clinical Endocrinology and Metabolism 86 3430-3435. (doi:10.1210/jc.86.7.3430)
30. Kolby L, Bernhardt P, Levin-Jakobsen AM, Johanson V, Wangberg B, Ahlman H, Forssell-Aronsson E & Nilsson O 2003 Uptake of meta-iodobenzylguanidine in neuroendocrine tumours is mediated by vesicular monoamine transporters. British Journal of Cancer 89 1383-1388. (doi:10.1038/sj.bjc.6601276)
31. Kopf D, Bockisch A, Steinert H, Hahn K, Beyer J, Neumann HP, Hensen J & Lehnert H 1997 Octreotide scintigraphy and catecholamine response to an octreotide challenge in malignant phaeochromocytoma. Clinical Endocrinology 46 39-44. (doi:10.1046/j.1365-2265.1997.d01-1738.x)
32. Kumar A, Choi KH, Renthal W, Tsankova NM, Theobald DE, Truong HT, Russo SJ, Laplant Q, Sasaki TS, Whistler KN et al. 2005 Chromatin remodeling is a key mechanism underlying cocaine-induced plasticity in striatum. Neuron 48 303-314. (doi:10.1016/j.neuron.2005.09.023)
33. Lenders JW, Eisenhofer G, Mannelli M & Pacak K 2005 Phaeochromocytoma. Lancet 366 665-675. (doi:10.1016/S0140-6736(05)67139-5)
34. Li QY, Jones PL, Lafferty RP, Safer D & Levy RJ 2002 Thymosin beta4 regulation, expression and function in aortic valve interstitial cells. Journal of Heart Valve Disease 11 726-735.
35. Lingen B, Bruss M & Bonisch H 1994 Cloning and expression of the bovine sodium- and chloride-dependent noradrenaline transporter. FEBS Letters 342 235-238. (doi:10.1016/0014-5793(94)80508-3)
36. 131I-MIBG): a comprehensive review of 116 reported patients. Journal of Endocrinological Investigation 20 648-658.
37. Mann BS, Johnson JR, Cohen MH, Justice R & Pazdur R 2007 FDA approval summary: vorinostat for treatment of advanced primary cutaneous T-cell lymphoma. Oncologist 12 1247-1252. (doi:10.1634/theoncologist.12-10-1247)
38. Marks PA, Richon VM & Rifkind RA 2000 Histone deacetylase inhibitors: inducers of differentiation or apoptosis of transformed cells. Journal of the National Cancer Institute 92 1210-1216. (doi:10.1093/jnci/92.15.1210)
39. Marks P, Rifkind RA, Richon VM, Breslow R, Miller T & Kelly WK 2001 Histone deacetylases and cancer: causes and therapies. Nature Reviews. Cancer 1 194-202. (doi:10.1038/35106079)
40. Martiniova L, Kotys MS, Thomasson D, Schimel D, Lai EW, Bernardo M, Merino MJ, Powers JF, Ruzicka J, Kvetnansky R et al. 2009a Noninvasive monitoring of a murine model of metastatic pheochromocytoma: a comparison of contrast-enhanced microCT and non-enhanced MRI. Journal of Magnetic Resonance Imaging 29 685-691. (doi:10.1002/jmri.21654)
41. Martiniova L, Lai EW, Elkahloun AG, Abu-Asab M, Wickremasinghe A, Solis DC, Perera SM, Huynh TT, Lubensky IA, Tischler AS et al. 2009b Characterization of an animal model of aggressive metastatic pheochromocytoma linked to a specific gene signature. Clinical & Experimental Metastasis 26 239-250. (doi:10.1007/s10585-009-9236-0)
42. Molife R, Fong P, Scurr M, Judson I, Kaye S & de Bono J 2007 HDAC inhibitors and cardiac safety. Clinical Cancer Research 13 1068 (author reply 1068-1069). (doi:10.1158/1078-0432.CCR-06-1715)
43. Mundschenk J & Lehnert H 1998 Malignant pheochromocytoma. Experimental and Clinical Endocrinology & Diabetes 106 373-376. (doi:10.1055/s-0029-1212001)
44. Munver R, Del Pizzo JJ & Sosa RE 2003 Adrenal-preserving minimally invasive surgery: the role of laparoscopic partial adrenalectomy, cryosurgery, and radiofrequency ablation of the adrenal gland. Current Urology Reports 4 87-92. (doi:10.1007/s11934-003-0065-4)
45. Nomura K, Kimura H, Shimizu S, Kodama H, Okamoto T, Obara T & Takano K 2009 Survival of patients with metastatic malignant pheochromocytoma and efficacy of combined cyclophosphamide, vincristine, and dacarbazine chemotherapy. Journal of Clinical Endocrinology and Metabolism 94 2850-2856. (doi:10.1210/jc.2008-2697)
46. Ohta S, Lai EW, Morris JC, Pang AL, Watanabe M, Yazawa H, Zhang R, Green JE, Chan WY, Sirajuddin P et al. 2008 Metastasis-associated gene expression profile of liver and subcutaneous lesions derived from mouse pheochromocytoma cells. Molecular Carcinogenesis 47 245-251. (doi:10.1002/mc.20388)
47. O'Riordain DS, Young WF Jr, Grant CS, Carney JA & van Heerden JA 1996 Clinical spectrum and outcome of functional extraadrenal paraganglioma. World Journal of Surgery 20 916-921. (doi:10.1007/s002689900139)
48. Pacak K, Chrousos GP, Koch CA, Lenders JW & Eisenhofer G 2001a Pheochromocytoma: progress in diagnosis, therapy, and genetics. In Adrenal Disorders, 1st edn, pp 479-523. Eds A Margioris & GP Chrousos. Totowa: Humana Press.
49. Pacak K, Linehan WM, Eisenhofer G, Walther MM & Goldstein DS 2001b Recent advances in genetics, diagnosis, localization, and treatment of pheochromocytoma. Annals of Internal Medicine 134 315-329.
50. Piekarz RL, Frye AR, Wright JJ, Steinberg SM, Liewehr DJ, Rosing DR, Sachdev V, Fojo T & Bates SE 2006 Cardiac studies in patients treated with depsipeptide, FK228, in a phase II trial for T-cell lymphoma. Clinical Cancer Research 12 3762-3773. (doi:10.1158/1078-0432.CCR-05-2095)
51. Piekarz R, Luchenko V, Draper D, Wright J, Figg W, Fojo A & Bates S 2008 Phase I trial of romidepsin, a histone deacetylase inhibitor, given on days one, three and five in patients with thyroid and other advanced cancers. Journal of Clinical Oncology 26 abstr 3571.
52. Piekarz RL, Frye R, Turner M, Wright JJ, Allen SL, Kirschbaum MH, Zain J, Prince HM, Leonard JP, Geskin LJ et al. 2009 Phase II multi-institutional trial of the histone deacetylase inhibitor romidepsin as monotherapy for patients with cutaneous T-cell lymphoma. Journal of Clinical Oncology 27 5410-5417. (doi:10.1200/JCO.2008.21.6150)
53. Plouin PF, Gimenez-Roqueplo AP, La Batide Alanore A, Salenave S & Duclos JM 2000 Recent progress in the diagnosis, prognostic evaluation and treatment of pheochromocytomas. La Revue de Medecine Interne 21 1075-1085. (doi:10.1016/S0248-8663(00)00268-X)
54. Powers JF, Evinger MJ, Tsokas P, Bedri S, Alroy J, Shahsavari M & Tischler AS 2000 Pheochromocytoma cell lines from heterozygous neurofibromatosis knockout mice. Cell and Tissue Research 302 309-320. (doi:10.1007/ s004410000290)
55. 131I-metaiodobenzylguanidine therapy for 12 patients with malignant pheochromocytoma. Cancer 98 239-248. (doi:10.1002/cncr.11518)
56. Safford SD, Coleman RE, Gockerman JP, Moore J, Feldman JM, Leight GS Jr, Tyler DS & Olson JA Jr 2003 Iodine -131 metaiodobenzylguanidine is an effective treatment for malignant pheochromocytoma and paraganglioma. Surgery 134 956-962 (discussion 962-963). (doi:10.1016/S0039-6060(03)00426-4)
57. Sanderson L, Taylor GW, Aboagye EO, Alao JP, Latigo JR, Coombes RC & Vigushin DM 2004 Plasma pharmacokinetics and metabolism of the histone deacetylase inhibitor trichostatin a after intraperitoneal administration to mice. Drug Metabolism and Disposition 32 1132-1138. (doi:10.1124/dmd.104.000638)
58. Sandor V, Robbins AR, Robey R, Myers T, Sausville E, Bates SE & Sackett DL 2000a FR901228 causes mitotic arrest but does not alter microtubule polymerization. Anticancer Drugs 11 445-454. (doi:10.1097/00001813-200007000- 00005)
59. Sandor V, Senderowicz A, Mertins S, Sackett D, Sausville E, Blagosklonny MV & Bates SE 2000b P21-dependent g(1)arrest with downregulation of cyclin D1 and upregulation of cyclin E by the histone deacetylase inhibitor FR901228. British Journal of Cancer 83 817-825. (doi:10.1054/bjoc.2000.1327)
60. Seidel J 2003 Resolution uniformity and sensitivity of the NIH ATLAS small animal PET scanner: comparison to simulated LSO scanners without depth-of-interaction capability. IEEE Transactions on Nuclear Science 50 1347-1350. (doi:10.1109/TNS.2003.817282)
61. Shilkrut M, Bar-Deroma R, Bar-Sela G, Berniger A & Kuten A 2010 Low-dose iodine-131 metaiodobenzylguanidine therapy for patients with malignant pheochromocytoma and paraganglioma: single center experience. American Journal of Clinical Oncology 33 79-82. (doi:10.1097/COC.0b013e31819e2c28)
62. Simon D, Korber C, Krausch M, Segering J, Groth P, Gorges R, Grunwald F, Muller-Gartner HW, Schmutzler C, Kohrle J et al. 2002 Clinical impact of retinoids in redifferentiation therapy of advanced thyroid cancer: final results of a pilot study. European Journal of Nuclear Medicine and Molecular Imaging 29 775-782. (doi:10.1007/s00259-001-0737-6)
63. Sisson JC & Wieland DM 1986 Radiolabeled metaiodobenzylguanidine: pharmacology and clinical studies. American Journal of Physiologic Imaging 1 96-103.
64. Sisson JC, Shapiro B, Meyers L, Mallette S, Mangner TJ, Wieland DM, Glowniak JV, Sherman P & Beierwaltes WH 1987 Metaiodobenzylguanidine to map scintigraphically the adrenergic nervous system in man. Journal of Nuclear Medicine 28 1625-1636. (Pubitemid 17158139)
65. Sisson JC, Shapiro B, Shulkin BL, Urba S, Zempel S & Spaulding S 1999 Treatment of malignant pheochromocytomas with 131-I metaiodobenzylguanidine and chemotherapy. American Journal of Clinical Oncology 22 364-370. (doi:10.1097/00000421-199908000-00008)
66. Takahashi K, Ashizawa N, Minami T, Suzuki S, Sakamoto I, Hayashi K, Tomiyasu S, Sumikawa K, Kitamura K, Eto T et al. 1999 Malignant pheochromocytoma with multiple hepatic metastases treated by chemotherapy and transcatheter arterial embolization. Internal Medicine 38 349-354. (doi:10.2169/ internalmedicine.38.349)
67. 18F-FDG small animal PET scanning and 2-14C-DG autoradiography. Journal of Nuclear Medicine 45 1398-1405.
68. Ueda H, Manda T, Matsumoto S, Mukumoto S, Nishigaki F, Kawamura I & Shimomura K 1994a FR901228, a novel antitumor bicyclic depsipeptide produced by Chromobacterium violaceum No. 968. III. Antitumor activities on experimental tumors in mice. Journal of Antibiotics 47 315-323.
69. Ueda H, Nakajima H, Hori Y, Fujita T, Nishimura M, Goto T & Okuhara M 1994b FR901228, a novel antitumor bicyclic depsipeptide produced by Chromobacterium violaceum No. 968. I. Taxonomy, fermentation, isolation, physico-chemical and biological properties, and antitumor activity. Journal of Antibiotics 47 301-310.
70. Van Lint C, Emiliani S & Verdin E 1996 The expression of a small fraction of cellular genes is changed in response to histone hyperacetylation. Gene Expression 5 245-253.