SDHB mutations are associated with response to temozolomide in patients with metastatic pheochromocytoma or paraganglioma

International Journal of Cancer

Volumn 135, Issue 11, 2014, Pages 2711-2720

  Hadoux, Julien ^a   Favier, Judith ^b,c   Scoazec, Jean Yves ^a   Leboulleux, Sophie ^a   Ghuzlan, Abir Al ^a   Caramella, Caroline ^a   Deandreis, Desiree ^a   Borget, Isabelle ^a   Loriot, Celine ^b,c   Chougnet, Cecile ^a   Letouze, Eric ^d   Young, Jacques ^e   Amar, Laurence ^f   Bertherat, Jerome ^g   Libe, Rosella ^h   Dumont, Frederic ^a   Deschamps, Frederic ^a   Schlumberger, Martin ^a   Gimenez Roqueplo, Anne Paule ^b,c,f   Baudin, Eric ^a  

^a INSTITUT GUSTAVE ROUSSY   (France)

^b PARIS CARDIOVASCULAR RESEARCH CENTER   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d Cartes d'Identité des Tumeurs Program   (France)

^e BICÊTRE HOSPITAL   (France)

^f HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

^g université Paris Cité   (France)

^h INSTITUT NATIONAL DU CANCER   (France)

Author keywords

Malignant pheochromocytoma; O(6) methylguanine DNA methyltransferase (MGMT); Paraganglioma; Succinate dehydrogenase B (SDHB); Temozolomide

Indexed keywords

CHROMOGRANIN A; METADRENALIN; METHYLATED DNA PROTEIN CYSTEINE METHYLTRANSFERASE; TEMOZOLOMIDE; ALKYLATING AGENT; DACARBAZINE; DNA METHYLTRANSFERASE; MGMT PROTEIN, HUMAN; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; SDHB PROTEIN, HUMAN; SUCCINATE DEHYDROGENASE; TUMOR MARKER; TUMOR SUPPRESSOR PROTEIN;

ADULT; AGED; ANEMIA; ARTICLE; ASTHENIA; COHORT ANALYSIS; CONSTIPATION; CORRELATION ANALYSIS; DNA METHYLATION; DRUG DOSE INCREASE; DRUG DOSE REDUCTION; DRUG EFFICACY; DRUG SAFETY; DRUG TOLERABILITY; FEMALE; FOLLOW UP; FRANCE; FRENCHMAN; GENE; GENE EXPRESSION; GERMLINE MUTATION; HUMAN; HYPERTENSION; IMMUNOHISTOCHEMISTRY; LEUKOPENIA; LYMPHOCYTOPENIA; MAJOR CLINICAL STUDY; MALE; MUCOSA INFLAMMATION; MULTIPLE CYCLE TREATMENT; NAUSEA AND VOMITING; PARAGANGLIOMA; PHEOCHROMOCYTOMA; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; PROMOTER REGION; RETROSPECTIVE STUDY; SDHB GENE; THROMBOCYTOPENIA; TREATMENT RESPONSE; ADRENAL GLAND NEOPLASMS; ANALOGS AND DERIVATIVES; BRAIN NEOPLASMS; CANCER STAGING; GENETICS; METASTASIS; MIDDLE AGED; MORTALITY; MUTATION; PATHOLOGY; POLYMERASE CHAIN REACTION; PROGNOSIS; SECONDARY; SURVIVAL RATE; VERY ELDERLY;

ADRENAL GLAND NEOPLASMS; ADULT; AGED; AGED, 80 AND OVER; ANTINEOPLASTIC AGENTS, ALKYLATING; BRAIN NEOPLASMS; DACARBAZINE; DNA METHYLATION; DNA MODIFICATION METHYLASES; DNA REPAIR ENZYMES; FEMALE; FOLLOW-UP STUDIES; HUMANS; MALE; MIDDLE AGED; MUTATION; NEOPLASM METASTASIS; NEOPLASM STAGING; PARAGANGLIOMA; PHEOCHROMOCYTOMA; POLYMERASE CHAIN REACTION; PROGNOSIS; PROMOTER REGIONS, GENETIC; RETROSPECTIVE STUDIES; SUCCINATE DEHYDROGENASE; SURVIVAL RATE; TUMOR MARKERS, BIOLOGICAL; TUMOR SUPPRESSOR PROTEINS;

EID: 84904256040     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.28913     Document Type: Article

References (39)

1. DeLellis RA, Lloyd RV, Heitz PU, et al. Pathology and genetics of tumours of endocrine organs. In: IARC WHO Classification of Tumours. France: IARC, 2004.
2. Gimenez-Roqueplo A-P, Dahia PL, Robledo M. An update on the genetics of paraganglioma, pheochromocytoma, and associated hereditary syndromes. Horm Metab Res 2012;44:328-33.
3. Hescot S, Leboulleux S, Amar L, et al. One-year progression-free survival of therapy-naive patients with malignant pheochromocytoma and paraganglioma. J Clin Endocrinol Metab 2013;98:4006-12.
4. Amar L, Baudin E, Burnichon N, et al. Succinate dehydrogenase B gene mutations predict survival in patients with malignant pheochromocytomas or paragangliomas. J Clin Endocrinol Metab 2007; 92:3822-8.
5. Ayala-Ramirez M, Feng L, Johnson MM, et al. Clinical risk factors for malignancy and overall survival in patients with pheochromocytomas and sympathetic paragangliomas: primary tumor size and primary tumor location as prognostic indicators. J Clin Endocrinol Metab 2011;96:717-25.
6. Feng F, Zhu Y, Wang X, et al. Predictive factors for malignant pheochromocytoma: analysis of 136 patients. J Urol 2011;185:1583-90.
7. Ayala-Ramirez M, Palmer JL, Hofmann M-C, et al. Bone metastases and skeletal-related events in patients with malignant pheochromocytoma and sympathetic paraganglioma. J Clin Endocrinol Metab 2013;98:1492-7.
8. Berruti A, Baudin E, Gelderblom H, et al., on behalf of the ESMO Guidelines Working Group. Adrenal cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 2012;23:vii131-vii138.
9. Averbuch SD, Steakley CS, Young RC, et al. Malignant pheochromocytoma: effective treatment with a combination of cyclophosphamide, vincristine, and dacarbazine. Ann Intern Med 1988;109:267-73.
10. Ayala-Ramirez M, Feng L, Habra MA, et al. Clinical benefits of systemic chemotherapy for patients with metastatic pheochromocytomas or sympathetic extra-adrenal paragangliomas: insights from the largest single-institutional experience. Cancer 2012;118:2804-12.
11. Huang H, Abraham J, Hung E, et al. Treatment of malignant pheochromocytoma/paraganglioma with cyclophosphamide, vincristine, and dacarbazine: recommendation from a 22-year follow-up of 18 patients. Cancer 2008;113:2020-8.
12. Patel SR, Winchester DJ, Benjamin RS. A 15-year experience with chemotherapy of patients with paraganglioma. Cancer 1995;76:1476-80.
13. Tanabe A, Naruse M, Nomura K, et al. Combination chemotherapy with cyclophosphamide, vincristine, and dacarbazine in patients with malignant pheochromocytoma and paraganglioma. Horm Cancer 2013;4:103-10.
14. He J, Makey D, Fojo T, et al. Successful chemotherapy of hepatic metastases in a case of succinate dehydrogenase subunit B-related paraganglioma. Endocrine 2009;36:189-93.
15. Jawed I, Amiri-Kordestani L, Velarde M, et al. High efficacy and continued tumor shrinkage with cyclophosphamide, vincristine, and dacarbazine (CVD) in patients (Pts) with malignant pheochromocytoma/paraganglioma harboring succinate dehydrogenase subunit B (SDHB) mutations. ASCO Meeting Abstracts 2011;29:2526.
16. Altimari AF, Badrinath K, Reisel HJ, et al. DTIC therapy in patients with malignant intraabdominal neuroendocrine tumors. Surgery 1987; 102:1009-17.
17. Bravo EL, Kalmadi SR, Gill I. Clinical utility of temozolomide in the treatment of malignant paraganglioma: a preliminary report. Horm Metab Res 2009;41:703-6.
18. Kulke MH, Stuart K, Enzinger PC, et al. Phase II study of temozolomide and thalidomide in patients with metastatic neuroendocrine tumors. J Clin Oncol 2006;24:401-6.
19. Dhodapkar M, Rubin J, Reid JM, et al. Phase I trial of temozolomide (NSC 362856) in patients with advanced cancer. Clin Cancer Res 1997;3: 1093-100.
20. Middleton MR, Grob JJ, Aaronson N, et al. Randomized phase III study of temozolomide versus dacarbazine in the treatment of patients with advanced metastatic malignant melanoma. J Clin Oncol 2000;18:158-66.
21. Hegi ME, Diserens A-C, Gorlia T, et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 2005;352:997-1003.
22. Kulke MH, Hornick JL, Frauenhoffer C, et al. O6-methylguanine DNA methyltransferase deficiency and response to temozolomide-based therapy in patients with neuroendocrine tumors. Clin Cancer Res 2009;15:338-45.
23. Eisenhauer EA, Therasse P, Bogaerts J, et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer 2009;45:228-47.
24. Wahl RL, Jacene H, Kasamon Y, et al. From RECIST to PERCIST: evolving Considerations for PET response criteria in solid tumors. J Nucl Med 2009;50 Suppl 1:122S-50S.
25. Buffet A, Venisse A, Nau V, et al. A decade (2001-2010) of genetic testing for pheochromocytoma and paraganglioma. Horm Metab Res 2012; 44:359-66.
26. Baudin E, Bidart JM, Bachelot A, et al. Impact of chromogranin A measurement in the work-up of neuroendocrine tumors. Ann Oncol 2001;12 Suppl 2:S79-82.
27. Baudin E, Gigliotti A, Ducreux M, et al. Neuronspecific enolase and chromogranin A as markers of neuroendocrine tumours. Br J Cancer 1998;78: 1102-7.
28. Amar L, Peyrard S, Rossignol P, Zinzindohoue F, et al. Changes in urinary total metanephrine excretion in recurrent and malignant pheochromocytomas and secreting paragangliomas. Ann N Y Acad Sci 2006;1073:383-91.
29. Abgral R, Leboulleux S, Déandreis D, et al. Performance of (18)fluorodeoxyglucose-positron emission tomography and somatostatin receptor scintigraphy for high Ki67 (-10%) welldifferentiated endocrine carcinoma staging. J Clin Endocrinol Metab 2011;96:665-71.
30. Dromain C, de Baere T, Lumbroso J, et al. Detection of liver metastases from endocrine tumors: a prospective comparison of somatostatin receptor scintigraphy, computed tomography, and magnetic resonance imaging. J Clin Oncol 2005;23: 70-8.
31. Leboulleux S, Dromain C, Vataire AL, et al. Prediction and diagnosis of bone metastases in welldifferentiated gastro-entero-pancreatic endocrine cancer: a prospective comparison of whole body magnetic resonance imaging and somatostatin receptor scintigraphy. J Clin Endocrinol Metab 2008;93:3021-8.
32. Ekeblad S, Sundin A, Janson ET, et al. Temozolomide as monotherapy is effective in treatment of advanced malignant neuroendocrine tumors. Clin Cancer Res 2007;13:2986-91.
33. Burnichon N, Vescovo L, Amar L, et al. Integrative genomic analysis reveals somatic mutations in pheochromocytoma and paraganglioma. Hum Mol Genet 2011;20:3974-85.
34. Bibikova M, Le J, Barnes B, et al. Genome-wide DNA methylation profiling using InfiniumVR assay. Epigenomics 2009;1:177-200.
35. Yao JC, Pavel M, Phan AT, et al. Chromogranin A and neuron-specific enolase as prognostic markers in patients with advanced pNET treated with everolimus. J Clin Endocrinol Metab 2011; 96:3741-9.
36. Letouze E, Martinelli C, Loriot C, et al. SDH mutations establish a hypermethylator phenotype in paraganglioma. Cancer Cell 2013;23: 739-52.
37. Nozieres C, Walter T, Joly M-O, et al. A SDHB malignant paraganglioma with dramatic response to temozolomide-capecitabine. Eur J Endocrinol 2012;166:1107-11.
38. Sharma S, Salehi F, Scheithauer BW, et al. Role of MGMT in tumor development, progression, diagnosis, treatment and prognosis. Anticancer Res 2009;29:3759-68.
39. Quillien V, Lavenu A, Karayan-Tapon L, et al. Comparative assessment of 5 methods (methylation-specific polymerase chain reaction, methylight, pyrosequencing, methylation-sensitive highresolution melting, and immunohistochemistry) to analyze O6-methylguanine-DNAmethyltranferase in a series of 100 glioblastoma patients. Cancer 2012;118:4201-11.