Molecular status of pituitary carcinoma and atypical adenoma that contributes the effectiveness of temozolomide

Kaltsas GA, Grossman AB (1998) Malignant pituitary tumours. Pituitary 1:69–81 Ragel BT, Couldwell WT (2004) Pituitary carcinoma: a review of the literature. Neurosurg Focus 16:E7 Landman RE, Horwith M, Peterson RE, Khandji AG, Wardlaw SL (2002) Long-term survival with ACTH-secreting carcinoma of the pituitary: a case report and review of the literature. J Clin Endocrinol Metab 87:3084–3089 Lim S, Shahinian H, Maya MM, Yong W, Heaney AP (2006) Temozolomide: a novel treatment for pituitary carcinoma. Lancet Oncol 7:518–520 Syro LV, Uribe H, Penagos LC, Ortiz LD, Fadul CE, Horvath E, Kovacs K (2006) Antitumour effects of temozolomide in a man with a large, invasive prolactin-producing pituitary neoplasm. Clin Endocrinol (Oxf) 65:552–553 Kovacs K, Horvath E, Syro LV, Uribe H, Penagos LC, Ortiz LD, Fadul CE (2007) Temozolomide therapy in a man with an aggressive prolactin-secreting pituitary neoplasm: morphological findings. Hum Pathol 38:185–189 Fadul CE, Kominsky AL, Meyer LP, Kingman LS, Kinlaw WB, Rhodes CH, Eskey CJ, Simmons NE (2006) Long-term response of pituitary carcinoma to temozolomide Report of two cases. J Neurosurg 105:621–626 Neff LM, Weil M, Cole A, Hedges TR, Shucart W, Lawrence D, Zhu JJ, Tischler AS, Lechan RM (2007) Temozolomide in the treatment of an invasive prolactinoma resistant to dopamine agonists. Pituitary 10:81–86 Kovacs K, Scheithauer BW, Lombardero M, McLendon RE, Syro LV, Uribe H, Ortiz LD, Penagos LC (2008) MGMT immunoexpression predicts responsiveness of pituitary tumors to temozolomide therapy. Acta Neuropathol 115:261–262 Moskin O, Syro LV, Scheithauer BW, Ortiz LD, Fadul CE, Uribe H, Gonzalez R, Cusimano M, Horvath E, Rotondo F, Kovacs K (2011) Aggressive silent corticotroph adenoma progressing to pituitary carcinoma: the role of temozolomide therapy. Hormones (Athens) 10:162–167 Oritz LD, Syro LV, Scheithauer BW, Rotondo F, Uribe H, Fadul CE, Horvath E, Kovacs K (2012) Temozolomide in aggressive pituitary adenomas and carcinomas. Clinics (Sao Paulo) 67(Suppl 1):119–123 Guzel A, Tatli M, Senturk S, Guzel E, Cayli SR, Sav A (2008) Pituitary carcinoma presenting with multiple metastases: case report. J Child Neurol 23:1467–1471 McCormack AI, McDonald KL, Gill AJ, Clark SJ, Burt MG, Campbell KA, Braund WJ, Little NS, Cook RJ, Grossman AB, Robinson BG, Clifton-Bligh RJ (2009) Low O6-methylguanine-DNA methyltransferase (MGMT) expression and response to temozolomide in aggressive pituitary tumours. Clin Endocrinol (Oxf) 71:226–233 Mohammed S, Kovacs K, Mason W, Smyth H, Cusimano MD (2009) Use of temozolomide in aggressive pituitary tumors: case report. Neurosurgery 64:E773–E774 Byrne S, Karapetis C, Vrodos N (2009) A novel use of temozolomide in a patient with malignant prolactinoma. J Clin Neurosci 16:1694–1696 Hagen C, Schroeder HD, Hansen S, Hagen C, Andersen M (2009) Temozolomide treatment of a pituitary carcinoma and two pituitary macroadenomas resistant to conventional therapy. Eur J Endocrinol 161:631–637 Takeshita A, Inoshita N, Taguchi M, Okuda C, Fukuhara N, Oyama K, Ohashi K, Sano T, Takeuchi Y, Yamada S (2009) High incidence of low O(6)-methylguanine DNA methyltransferase expression in invasive macroadenomas of Cushing’s disease. Eur J Endocrinol 161:553–559 Moyes VJ, Alusi G, Sabin HI, Evanson J, Berney DM, Kovacs K, Monson JP, Plowman PN, Drake WM (2009) Treatment of Nelson’s syndrome with temozolomide. Eur J Endocrinol 160:115–119 Syro LV, Scheithauer BW, Ortiz LD, Fadul CE, Horvath E, Rotondo F, Kovacs K (2009) Effect of temozolomide in a patient with recurring oncocytic gonadotrophic pituitary adenoma. Hormones (Athens) 8:303–306 Thearle MS, Freda PU, Bruce JN, Isaacson SR, Lee Y, Fine RL (2009) Temozolomide (Temodar) and capecitabine (Xeloda) treatment of an aggressive corticotroph pituitary tumor. Pituitary. doi:10.1007/s11102-009-0211-1 Morin E, Berthelet F, Weisnagel J, Bidlingmaier M, Serri O (2012) Failure of temozolomide and conventional doses of pegvisomant to attain biochemical control in a severe case of acromegaly. Pituitary 15:97–100 Bode H, Seiz M, Lammert A, Brockmann MA, Back W, Hammes HP, Thomé C (2010) SOM230 (pasireotide) and temozolomide achieve sustained control of tumour progression and ACTH secretion in pituitary carcinoma with widespread metastases. Exp Clin Endocrinol Diabetes 118:760–763 Bush ZM, Longtine JA, Cunningham T, Schiff D, Jane JA Jr, Vance ML, Thorner MO, Laws ER Jr, Lopes MB (2010) Temozolomide treatment for aggressive pituitary tumors: correlation of clinical outcome with O(6)-methylguanine methyltransferase (MGMT) promoter methylation and expression. J Clin Endocrinol Metab 95:E280–E290 Curto L, Torre ML, Ferraù F, Pitini V, Altavilla G, Granata F, Longo M, Hofland LJ, Trimarchi F (2010) Cannavò S (2010) Temozolomide-induced shrinkage of a pituitary carcinoma causing Cushing’s disease–report of a case and literature review. Sci World J 10:2132–2138 Raverot G, Sturm N, de Fraipont F, Muller M, Salenave S, Caron P, Chabre O, Chanson P, Cortet-Rudelli C, Assaker R, Dufour H, Gaillard S, François P, Jouanneau E, Passagia JG, Bernier M, Cornélius A, Figarella-Branger D, Trouillas J, Borson-Chazot F, Brue T (2010) Temozolomide treatment in aggressive pituitary tumors and pituitary carcinomas: a French multicenter experience. J Clin Endocrinol Metab 95:4592–4599 Losa M, Mazza E, Terreni MR, McCormack A, Gill AJ, Motta M, Cangi MG, Talarico A, Mortini P, Reni M (2010) Salvage therapy with temozolomide in patients with aggressive or metastatic pituitary adenomas: experience in six cases. Eur J Endocrinol 163:843–851 Murakami M, Mizutani A, Asano S, Katakami H, Ozawa Y, Yamazaki K, Ishida Y, Takano K, Okinaga H, Matsuno A (2011) A mechanism of acquiring temozolomide resistance during transformation of atypical prolactinoma into prolactin-producing pituitary carcinoma: case report. Neurosurgery 68:E1761–E1767 Dillard TH, Gultekin SH, Delashaw JB Jr, Yedinak CG, Neuwelt EA, Fleseriu M (2011) Temozolomide for corticotroph pituitary adenomas refractory to standard therapy. Pituitary 14:80–91 Ersen A, Syro LV, Penagos L, Uribe H, Scheithauer BW, Ortiz LD, Rotondo F, Horvath E, Kovacs K (2012) Non-uniform response to temozolomide therapy in a pituitary gonadotroph adenoma. Can J Neurol Sci 39:683–685 Morokuma H, Ando T, Hayashida T, Horie I, Inoshita N, Murata F, Ueki I, Nakamura K, Imaizumi M, Usa T, Kawakami A (2012) A case of nonfunctioning pituitary carcinoma that responded to temozolomide treatment. Case Rep Endocrinol. doi:10.1155/2012/645914 (645914) Zemmoura I, Wierinckx A, Vasiljevic A, Jan M, Trouillas J, François P (2012) Aggressive and malignant prolactin pituitary tumors: pathological diagnosis and patient management. Pituitary. doi:10.1007/s11102-012-0448-y Philippon M, Morange I, Barrie M, Barlier A, Taieb D, Dufour H, Conte-Devolx B, Brue T, Castinetti F (2012) Long-term control of a MEN1 prolactin secreting pituitary carcinoma after temozolomide treatment. Ann Endocrinol (Paris) 73:225–229 Rotondo F, Cusimano M, Scheithauer BW, Coire C, Horvath E, Kovacs K (2012) Atypical, invasive, recurring Crooke cell adenoma of the pituitary. Hormone (Athens) 12:94–100 Whitelaw BC, Dworakowska D, Thomas NW, Barazi S, Riordan-Eva P, King AP, Hampton T, Landau DB, Lipscomb D, Buchanan CR, Gilbert JA, Aylwin SJ (2012) Temozolomide in the management of dopamine agonist-resistant prolactinomas. Clin Endocrinol (Oxf) 76:877–886 Arnold PM, Ratnasingam D, O’Neil MF, Johnson PL (2012) Pituitary carcinoma recurrent to the lumbar intradural extramedullary space: case report. J Spinal Cord Med 35:118–121 Annamalai AK, Dean AF, Kandasamy N, Kovacs K, Burton H, Halsall DJ, Shaw AS, Antoun NM, Cheow HK, Kirollos RW, Pickard JD, Simpson HL, Jefferies SJ, Burnet NG, Gurnell M (2012) Temozolomide responsiveness in aggressive corticotroph tumours: a case report and review of the literature. Pituitary 15:276–287 Batisse M, Raverot G, Maqdasy S, Durando X, Sturm N, Montoriol PF, Kemeny JL, Chazal J, Trouillas J, Tauveron I (2013) Aggressive silent GH pituitary tumor resistant to multiple treatments, including temozolomide. Cancer Invest 31:190–196 Bafaloukos D, Tsoutsos D, Kalofonos H, Chalkidou S, Panagiotou P, Linardou E, Briassoulis E, Efstathiou E, Polyzos A, Fountzilas G, Christodoulou C, Kouroussis C, Iconomou T, Gogas H (2005) Temozolomide and cisplatin versus temozolomide in patients with advanced melanoma: a randomized phase II study of the Hellenic Cooperative Oncology Group. Ann Oncol 16:950–957 Kulke M, Stuart K, Enzinger P, Ryan D, Clark J, Muzikansky A, Vincitore M, Michelini A, Fuchs C (2006) Phase II study of temozolomide and thalidomide in patients with metastatic neuroendocrine tumors. J Clin Oncol 24:401–406 Nagasubramanian R, Dolan M (2003) Temozolomide: realizing the promise and potential. Curr Opin Oncol 15:412–418 Liu L, Gerson SL (2006) Targeted modulation of MGMT: clinical implications. Clin Cancer Res 12:328–331 Gerson SL, Trey JE, Miller K, Berger NA (1986) Comparison of O6-alkylguanine-DNA alkyltransferase activity based on cellular DNA content in human, rat and mouse tissues. Carcinogenesis 7:745–749 Pegg AE (2000) Repair of O6-alkylguanine by alkyltransferases. Mutat Res 462:83–100 Gerson SL (2004) MGMT: its role in cancer aetiology and cancer therapeutics. Nat Rev Cancer 4:296–307 Schold S Jr, Brent TP, von Hofe E, Friedman HS, Mitra S, Bigner DD, Swenberg JA, Kleihues P (1989) O6-Alkylguanine-DNA alkyltransferase and sensitivity to procarbazine in human brain tumor xenografts. J Neurosurg 70:573–577 Yarosh DB (1985) The role of O6-methylguanine-DNA methyl-transferase in cell survival, mutagenesis, and carcinogenesis. Mutat Res 145:1–16 Mollemann M, Wolter M, Felsberg J, Collins VP, Reifenberger G (2005) Frequent promoter hypermethylation and low expression of the MGMT gene in oligodendroglial tumors. Int J Cancer 113:379–385 Levin N, Lavon I, Zelikovitsh B, Fuchs D, Bokstein F, Fellig Y, Siegal T (2006) Progressive low-grade oligodendrogliomas: response to temozolomide and correlation between genetic profile and O6-methylguanine DNA methyltransferase protein expression. Cancer 106:1759–1765 Chinot OL, Barrie M, Fuentes S, Eudes N, Lancelot S, Metellus P, Muracciole X, Braguer D, Ouafik L, Martin PM, Dufour H, Figarella-Branger D (2007) Correlation between O6-methylguanine-DNA methyltransferase and survival in inoperable newly diagnosed glioblastoma patients treated with neoadjuvant temozolomide. J Clin Oncol 25:1470–1475 Esteller M, Hamilton SR, Burger PC, Baylin SB, Herman JG (1999) Inactivation of the DNA repair gene O6-methylguanine-DNA methyltransferase by promoter hypermethylation is a common event in primary human neoplasia. Cancer Res 59:793–797 Hegi ME, Diserens AC, Godard S, Dietrich PY, Regli L, Ostermann S, Otten P, Van Melle G, de Tribolet N, Stupp R (2004) Clinical trial substantiates the predictive value of O-6-methylguanine-DNA methyltransferase promoter methylation in glioblastoma patients treated with temozolomide. Clin Cancer Res 10:1871–1874 Esteller M, Garcia-Foncillas J, Andion E, Goodman SN, Hidalgo OF, Vanaclocha V, Baylin SB, Herman JG (2000) Inactivation of the DNA-repair gene MGMT and the clinical response of gliomas to alkylating agents. N Engl J Med 343:1350–1354 Brent TP, Houghton PJ, Houghton JA (1985) O6-Alkylguanine-DNA alkyltransferase activity correlates with the therapeutic response of human rhabdomyosarcoma xenografts to 1-(2-chloroethyl)-3-(trans-4-methylcyclohexyl)-1-nitrosourea. Proc Natl Acad Sci USA 82:2985–2989 Gerson SL, Willson JK (1995) O6-Alkylguanine-DNA alkyltransferase. A target for the modulation of drug resistance. Hematol Oncol Clin North Am 9:431–450 Lindahl T, Sedgewick B, Sekiguchi M, Nakabeppu Y (1988) Regulation and expression of the adaptive response to alkylatingagents. Annu Rev Biochem 57:133–157 Erickson LC, Laurent G, Sharkey NA, Kohn KW (1980) DNA cross-linking and monoadduct repair in nitrosourea treated human tumor cells. Nature 288:727–729 Hickman MJ, Samson LD (2004) Apoptotic signaling in response to a single type of DNA lesion, O(6)- methylguanine. Mol Cell 14:105–116 Liu L, Markowitz S, Gerson SL (1996) Mismatch repair mutations override alkyltransferase in conferring resistance to temozolomide but not to 1,3-bis(2-chloroethyl)nitrosourea. Cancer Res 56:5375–5379 Pepponi R, Fuggetta MP, Marra G, Falcinelli S, Pagani E, Bonmassar E, Jiricny J, D’Atri S (2003) The effect of O6-alkylguanine-DNA alkyltransferase and mismatch repair activities on the sensitivity of human melanoma cells to temozolomide, 1,3-bis(2-chloroethyl)1-nitrosourea, and cisplatin. J Pharmacol ExpTher 304:661–668 Liu L, Schwartz S, Davis BM, Gerson SL (2002) Chemotherapy-induced O6-benzylguanine-resistant alkyltransferase mutations in mismatch repair-deficient colon cancer. Cancer Res 62:3070–3076 Bacolod MD, Johnson SP, Pegg AE, Dolan ME, Moschel RC, Bullock NS, Fang Q, Colvin OM, Modrich P, Bigner DD, Friedman HS (2004) Brain tumor cell lines resistant to O6-benzylguanine/1,3-bis(2-chloroethyl)-1-nitrosourea chemotherapy have O6-alkylguanine-DNA alkyltransferase mutations. Mol Cancer Ther 3:1127–1135 Bignami M, O’Driscoll M, Aquilina G, Karran P (2000) Unmasking a killer: DNA O6-methylguanine and the cytotoxicity of methylating agents. Mutat Res 462:71–82 Widhalm G, Wolfsberger S, Preusser M, Woehrer A, Kotter MR, Czech T, Marosi C, Knosp E (2009) O(6)-methylguanine DNA methyltransferase immunoexpression in nonfunctioning pituitary adenomas: are progressive tumors potential candidates for temozolomide treatment? Cancer 115:1070–1080 Hegi M, Diserens A, Gorlia T, Hamou M, de Tribolet N, Weller M, Kros J, Hainfellner J, Mason W, Mariani L, Bromberg J, Hau P, Mirimanoff R, Cairncross J, Janzer R, Stupp R (2005) MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 352:997–1003 Tanaka S, Kobayashi I, Utsuki S, Oka H, Yasui Y, Fujii K (2005) Down-regulation of O6-methylguanine-DNA methyltransferase gene expression in gliomas by platinum compounds. Oncol Rep 14:1275–1280 Fujimaki T, Ishii H, Matsuno A, Arai H, Nakagomi T (2007) Effectiveness of interferon-beta and temozolomide combination therapy against temozolomide-refractory recurrent anaplastic astrocytoma. World J Surg Oncol 5:89 Hirohata T, Asano K, Ogawa Y, Takano S, Amano K, Isozaki O, Iwai Y, Sakata K, Fukuhara N, Nishioka H, Yamada S, Fujio S, Arita K, Takano K, Tominaga A, Hizuka N, Ikeda H, Osamura RY, Tahara S, Ishii Y, Kawamata T, Shimatsu A, Teramoto A, Matsuno A (2013) DNA mismatch repair protein (MSH6) correlated with the responses of atypical pituitary adenomas and pituitary carcinomas to temozolomide: the national cooperative study by the Japan Society for Hypothalamic and Pituitary Tumors. J Clin Endocri Metab 98:1130–1136 Hunter C, Smith R, Cahill DP, Stephens P, Stevens C, Teague J, Greenman C, Edkins S, Bignell G, Davies H, O’Meara S, Parker A, Avis T, Barthorpe S, Brackenbury L, Buck G, Butler A, Clements J, Cole J, Dicks E, Forbes S, Gorton M, Gray K, Halliday K, Harrison R, Hills K, Hinton J, Jenkinson A, Jones D, Kosmidou V, Laman R, Lugg R, Menzies A, Perry J, Petty R, Raine K, Richardson D, Shepherd R, Small A, Solomon H, Tofts C, Varian J, West S, Widaa S, Yates A, Easton DF, Riggins G, Roy JE, Levine KK, Mueller W, Batchelor TT, Louis DN, Stratton MR, Futreal PA, Wooster R (2006) A hypermutation phenotype and somatic MSH6 mutations in recurrent human malignant gliomas after alkylator chemotherapy. Cancer Res 66:3987–3991 Cahill DP, Levine KK, Betensky RA, Codd PJ, Romany CA, Reavie LB, Batchelor TT, Futreal PA, Stratton MR, Curry WT, Iafrate AJ, Louis DN (2007) Loss of the mismatch repair protein MSH6 in human glioblastomas is associated with tumor progression during temozolomide treatment. Clin Cancer Res 13:2038–2045 Umar A, Koi M, Risinger JI, Glaab WE, Tindall KR, Kolodner RD, Boland CR, Barrett JC, Kunkel TA (1997) Correction of hypermutability, N-Methyl-N’-nitro-N-nitrosoguanidine resistance, and defective DNA mismatch repair by introducing chromosome 2 into human tumor cells with mutations in MSH2 and MSH6. Cancer Res 57:3949–3955 Hampel H, Frankel WL, Martin E, Arnold M, Khanduja K, Kuebler P, Nakagawa H, Sotamaa K, Prior TW, Westman J, Panescu J, Fix D, Lockman J, Comeras I, de la Chapelle A (2005) Screening for the Lynch syndrome (hereditary nonpolyposis colorectal cancer). N Engl J Med 352:1851–1860 Barnetson RA, Tenesa A, Farrington SM, Nicholl ID, Cetnarskyj R, Porteous ME, Campbell H, Dunlop MG (2006) Identification and survival of carriers of mutations in DNA mismatch-repair genes in colon cancer. N Engl J Med 354:2751–2763 Thapar K, Scheithauer BW, Kovacs K, Pernicone PJ, Laws ER Jr (1996) p53 expression in pituitary adenomas and carcinomas: correlation with invasiveness and tumor growth fractions. Neurosurgery 38:765–770 (discussion 770–771) Kaltsas GA, Nomikos P, Kontogeorgos G, Buchfelder M, Grossman AB (2005) Clinical review: diagnosis and management of pituitary carcinomas. J Clin Endocrinol Metab 90:3089–3099 Tanizaki Y, Jin L, Scheithauer BW, Kovacs K, Roncaroli F, Lloyd RV (2007) p53 Gene mutations in pituitary carcinomas. Endocr Pathol 18:217–222 Kawashima ST, Usui T, Sano T, Iogawa H, Hagiwara H, Tamanaha T, Tagami T, Naruse M, Hojo M, Takahashi JA, Shimatsu A (2009) p53 gene mutation in an atypical corticotroph adenoma with Cushing’s disease. Clin Endocrinol (Oxf) 70:656–657 Pinto EM, Siqueira SA, Cukier P, Fraqoso MC, Lin CJ, de Mendonca BB (2011) Possible role of a radiation-induced p53 mutation in a Nelson’s syndrome patient with a fatal outcome. Pituitary 14:400–404 Matsuno A, Mizutani A, Okinaga H, Takano K, Yamada S, Yamada SM, Nakaguchi H, Hoya K, Murakami M, Takeuchi M, Sugaya M, Itoh J, Takekoshi S, Osamura RY (2011) Functional molecular morphology of anterior pituitary cells, from hormone production to intracellular transport and secretion. Med Mol Morphol 44:63–70 Miyagami M, Katayama Y (2005) Angiogenesis of glioma: evaluation of ultrastructural characteristics of microvessels and tubular bodies (Weibel-Palade) in endothelial cells and immunohistochemical findings with VEGF and p53 protein. Med Mol Morphol 38:36–42 Rahmathulla G, Hovey EJ, Hashemi-Sadraei N, Ahluwalia MS (2013) Bevacizumab in high-grade gliomas: a review of its uses, toxicity assessment, and future treatment challenges. Onco Targets Ther 6:371–389 Ikeda H, Abe T, Watanabe K (2010) Usefulness of composite methionine positron emission tomography/3.0-tesla magnetic resonance imaging to detect the localization and extent of early-stage Cushing adenoma. J Neurosurg 112:750–755 Jouanneau E, Wierinckx A, Ducray F, Favrel V, Borson-Chazot F, Honnorat J, Trouillas J, Raverot G (2012) New targeted therapies in pituitary carcinoma resistant to temozolomide. Pituitary 15:37–43 Idbaih A, Omuro A, Ducray F, Hoang-Xuan K (2007) Molecular genetic markers as predictors of response to chemotherapy in gliomas. Curr Opin Oncol 19:606–611