Pheochromocytomas and paragangliomas: Assessment of malignant potential

Endocrine

Volumn 40, Issue 3, 2011, Pages 354-365

  Korevaar, Tim I M ^a   Grossman, Ashley B ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Clinical; Malignant; Molecular pathology; Paraganglioma; Pheochromocytoma

Indexed keywords

(3 IODOBENZYL)GUANIDINE I 123; (3 IODOBENZYL)GUANIDINE I 131; 3 O METHYLDOPAMINE; 6 FLUORODOPA F 18; ADRENALIN; AMINO ACID DECARBOXYLASE; CATECHOLAMINE; CHROMOGRANIN A; CYCLIN D1; CYCLOOXYGENASE 2; DOPAMINE; DOPAMINE BETA MONOOXYGENASE; FLUORODEOXYGLUCOSE F 18; HEAT SHOCK PROTEIN 90; HEPARANASE; KI 67 ANTIGEN; MICRORNA; NERVE CELL ADHESION MOLECULE; NORADRENALIN; NORMETADRENALIN; PHENYLETHANOLAMINE N METHYLTRANSFERASE; PROTEIN P27; PROTEIN P53; SUCCINATE DEHYDROGENASE; SUCCINATE DEHYDROGENASE B; TRANSCRIPTION FACTOR SNAIL; UNCLASSIFIED DRUG; VANILMANDELIC ACID; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2; TUMOR MARKER;

ADRENAL CANCER; ADRENAL DISEASE; ADRENAL SCINTISCANNING; BLOOD ANALYSIS; COMPUTER ASSISTED EMISSION TOMOGRAPHY; COMPUTER ASSISTED TOMOGRAPHY; DIFFUSION WEIGHTED IMAGING; DISEASE MARKER; GENE MUTATION; HISTOPATHOLOGY; HUMAN; HYPERTENSION; MALIGNANT TRANSFORMATION; MEDICAL ASSESSMENT; MICROARRAY ANALYSIS; NUCLEAR MAGNETIC RESONANCE IMAGING; PARAGANGLIOMA; PHEOCHROMOCYTOMA; POSITRON EMISSION TOMOGRAPHY; PREDICTION; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RELIABILITY; REVIEW; SDHB GENE; TUMOR VOLUME; URINALYSIS; ADRENAL TUMOR; AUTONOMIC NEUROPATHY; CELL TRANSFORMATION; CHEMODECTOMA; CLASSIFICATION; METABOLISM; MOLECULAR PATHOLOGY; PATHOLOGY; PRECANCER; PREDICTIVE VALUE;

ADRENAL GLAND NEOPLASMS; AUTONOMIC NERVOUS SYSTEM DISEASES; CELL TRANSFORMATION, NEOPLASTIC; HUMANS; PARAGANGLIOMA, EXTRA-ADRENAL; PATHOLOGY, MOLECULAR; PHEOCHROMOCYTOMA; PRECANCEROUS CONDITIONS; PREDICTIVE VALUE OF TESTS; TUMOR MARKERS, BIOLOGICAL;

EID: 84858784227     PISSN: 1355008X     EISSN: 15590100     Source Type: Journal    
DOI: 10.1007/s12020-011-9545-3     Document Type: Review

References (91)

1. G. Eisenhofer, S.R. Bornstein, F.M. Brouwers, N.K. Cheung, P.L. Dahia, R.R. de Krijger et al., Malignant pheochromocytoma: current status and initiatives for future progress. Endocr. Relat. Cancer 11(3), 423-436 (2004) (Pubitemid 39331275)
2. H. Lehnert, J. Mundschenk, K. Hahn, Malignant pheochromocytoma. Front. Horm. Res. 31, 155-162 (2004)
3. H.J. Timmers, F.M. Brouwers, A.R. Hermus, F.C. Sweep, A.A. Verhofstad, A.L. Verbeek et al., Metastases but not cardiovascular mortality reduces life expectancy following surgical resection of apparently benign pheochromocytoma. Endocr. Relat. Cancer 15(4), 1127-1133 (2008)
4. A. Chrisoulidou, G. Kaltsas, I. Ilias, A.B. Grossman, The diagnosis and management of malignant phaeochromocytoma and paraganglioma. Endocr. Relat. Cancer 14(3), 569-585 (2007) (Pubitemid 350074048)
5. K. Nomura, H. Kimura, S. Shimizu, H. Kodama, T. Okamoto, T. Obara et al., Survival of patients with metastatic malignant pheochromocytoma and efficacy of combined cyclophosphamide, vincristine, and dacarbazine chemotherapy. J. Clin. Endocrinol. Metab. 94(8), 2850-2856 (2009)
6. C. Jimenez, M. Ayala-Ramirez, L. Feng, M.M. Johnson, S. Ejaz, M.A. Habra 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. 96(3), 717-725 (2011)
7. N. Kimura, T. Watanabe, T. Noshiro, S. Shizawa, Y. Miura, Histological grading of adrenal and extra-adrenal pheochromocytomas and relationship to prognosis: a clinicopathological analysis of 116 adrenal pheochromocytomas and 30 extra-adrenal sympathetic paragangliomas including 38 malignant tumors. Endocr Pathol 16(1), 23-32 (2005) (Pubitemid 41278311)
8. V.E. Strong, T. Kennedy, H. Al-Ahmadie, L. Tang, J. Coleman, Y. Fong et al., Prognostic indicators of malignancy in adrenal pheochromocytomas: clinical, histopathologic, and cell cycle/ apoptosis gene expression analysis. Surgery 143(6), 759-768 (2008)
9. T. Zelinka, Z. Musil, J. Duskova, D. Burton, M.J. Merino, D. Milosevic, et al., Metastatic pheochromocytoma: Does the size and age matter? Eur. J. Clin. Invest. 41(10), 1121-1128 (2011)
10. P.F. Plouin, G. Chatellier, I. Fofol, P. Corvol, Tumor recurrence and hypertension persistence after successful pheochromocytoma operation. Hypertension 29(5), 1133-1139 (1997) (Pubitemid 27198222)
11. F. Feng, Y. Zhu, X. Wang, Y. Wu, W. Zhou, X. Jin et al., Predictive factors for malignant pheochromocytoma: analysis of 136 patients. J. Urol. 185(5), 1583-1590 (2011)
12. L.D. Thompson, Pheochromocytoma of the Adrenal gland Scaled Score (PASS) to separate benign from malignant neoplasms: a clinicopathologic and immunophenotypic study of 100 cases. Am. J. Surg. Pathol. 26(5), 551-566 (2002) (Pubitemid 34438716)
13. E. van der Harst, H.A. Bruining, H. Jaap Bonjer, F. van der Ham, W.N. Dinjens, S.W. Lamberts et al., Proliferative index in phaeochromocytomas: Does it predict the occurrence of metastases? J. Pathol. 191(2), 175-180 (2000) (Pubitemid 30394896)
14. Y. Zhu, H.C. He, F. Yuan, J. Zhang, W.B. Rui, J.P. Zhao et al., Heparanase-1 and cyclooxygenase-2: prognostic indicators of malignancy in pheochromocytomas. Endocrine 38(1), 93-99 (2010)
15. R.K. Whalen, A.F. Althausen, G.H. Daniels, Extra-adrenal pheochromocytoma. J. Urol. 147(1), 1-10 (1992)
16. R.I. Linnoila, H.R. Keiser, S.M. Steinberg, E.E. Lack, Histopathology of benign versus malignant sympathoadrenal paragangliomas: clinicopathologic study of 120 cases including unusual histologic features. Hum. Pathol. 21(11), 1168-1180 (1990) (Pubitemid 20382001)
17. A. Blank, A.M. Schmitt, E. Korpershoek, F. van Nederveen, T. Rudolph, N. Weber et al., SDHB loss predicts malignancy in pheochromocytomas/sympathetic paragangliomas, but not through hypoxia signalling. Endocr. Relat. Cancer 17(4), 919-928 (2010)
18. M. Maier-Woelfle, M. Brandle, P. Komminoth, P. Saremaslani, S. Schmid, T. Locher et al., A novel succinate dehydrogenase subunit B gene mutation, H132P, causes familial malignant sympathetic extra adrenal paragangliomas. J. Clin. Endocrinol. Metab. 89(1), 362-367 (2004) (Pubitemid 38183905)
19. H.P. Neumann, B. Bausch, S.R. McWhinney, B.U. Bender, O. Gimm, G. Franke et al., Germ-line mutations in nonsyndromic pheochromocytoma. N. Engl. J. Med. 346(19), 1459-1466 (2002) (Pubitemid 34755714)
20. S.M. Tavangar, A. Shojaee, H. Moradi Tabriz, V. Haghpanah, B. Larijani, R. Heshmat et al., Immunohistochemical expression of Ki67, c-erbB-2, and c-kit antigens in benign and malignant pheochromocytoma. Pathol. Res. Pract. 206(5), 305-309 (2010)
21. G. Chen, J. Yao, L. Mou, X. Fang, H. Huang, J. Liang et al., Clinical analysis of 249 cases of adrenal tumors in a Chinese hospital. Urol. Int. 85(3), 270-275 (2010)
22. J. Park, C. Song, M. Park, S. Yoo, S.J. Park, S. Hong et al., Predictive characteristics of malignant pheochromocytoma. Korean J. Urol. 52(4), 241-246 (2011)
23. H. John, W.H. Ziegler, D. Hauri, P. Jaeger, Pheochromocytomas: Can malignant potential be predicted? Urology 53(4), 679-683 (1999) (Pubitemid 29163029)
24. C. Boltze, J. Mundschenk, N. Unger, R. Schneider-Stock, B. Peters, C. Mawrin et al., Expression profile of the telomeric complex discriminates between benign and malignant pheochromocytoma. J. Clin. Endocrinol. Metab. 88(9), 4280-4286 (2003) (Pubitemid 37153732)
25. E.W. Lai, S.M. Perera, B. Havekes, H.J. Timmers, F.M. Brouwers, B. McElroy et al., Gender-related differences in the clinical presentation of malignant and benign pheochromocytoma. Endocrine 34(1-3), 96-100 (2008)
26. R.J. Hsiao, H.P. Neumann, R.J. Parmer, J.A. Barbosa, D.T. O'Connor, Chromogranin A in familial pheochromocytoma: diagnostic screening value, prediction of tumor mass, and postresection kinetics indicating two-compartment distribution. Am. J. Med. 88(6), 607-613 (1990) (Pubitemid 20192274)
27. R.J. Hsiao, R.J. Parmer, M.A. Takiyyuddin, D.T. O'Connor, Chromogranin A storage and secretion: sensitivity and specificity for the diagnosis of pheochromocytoma. Medicine (Baltim.) 70(1), 33-45 (1991)
28. F. Rao, H.R. Keiser, D.T. O'Connor, Malignant pheochromocytoma. Chromaffin granule transmitters and response to treatment. Hypertension 36(6), 1045-1052 (2000)
29. A. Szalat, M. Fraenkel, V. Doviner, A. Salmon, D.J. Gross, Malignant pheochromocytoma: predictive factors of malignancy and clinical course in 16 patients at a single tertiary medical center. Endocrine 39(2), 160-166 (2011)
30. E. van der Harst, W.W. de Herder, R.R. de Krijger, H.A. Bruining, H.J. Bonjer, S.W.J. Lamberts et al., The value of plasma markers for the clinical behaviour of phaeochromocytomas. Eur. J. Endocrinol. 147(1), 85-94 (2002) (Pubitemid 34814744)
31. C. Proye, P. Fossati, P. Fontaine, J. Lefebvre, M. Decoulx, J.L. Wemeau et al., Dopamine-secreting pheochromocytoma: An unrecognized entity? Classification of pheochromocytomas according to their type of secretion. Surgery 100(6), 1154-1162 (1986) (Pubitemid 17223236)
32. M. Schlumberger, C. Gicquel, J. Lumbroso, F. Tenenbaum, E. Comoy, J. Bosq et al., Malignant pheochromocytoma: clinical, biological, histologic and therapeutic data in a series of 20 patients with distant metastases. J. Endocrinol. Investig. 15(9), 631-642 (1992)
33. P.A. Tippett, A.J. McEwan, D.M. Ackery, A re-evaluation of dopamine excretion in phaeochromocytoma. Clin. Endocrinol. (Oxf.) 25(4), 401-410 (1986) (Pubitemid 16031777)
34. L. Amar, E. Baudin, N. Burnichon, S. Peyrard, S. Silvera, J. Bertherat et al., Succinate dehydrogenase B gene mutations predict survival in patients with malignant pheochromocytomas or paragangliomas. J. Clin. Endocrinol. Metab. 92(10), 3822-3828 (2007) (Pubitemid 47607629)
35. H. Chen, R.S. Sippel, M.S. O'Dorisio, A.I. Vinik, R.V. Lloyd, K. Pacak, The North American Neuroendocrine Tumor Society consensus guideline for the diagnosis and management of neuroendocrine tumors: pheochromocytoma, paraganglioma, and medullary thyroid cancer. Pancreas 39(6), 775-783 (2010)
36. H.J. Timmers, A. Kozupa, G. Eisenhofer, M. Raygada, K.T. Adams, D. Solis et al., Clinical presentations, biochemical phenotypes, and genotype-phenotype correlations in patients with succinate dehydrogenase subunit B-associated pheochromocytomas and paragangliomas. J. Clin. Endocrinol. Metab. 92(3), 779-786 (2007) (Pubitemid 46465640)
37. G. Eisenhofer, J.W. Lenders, H. Timmers, M. Mannelli, S.K. Grebe, L.C. Hofbauer et al., Measurements of plasma methoxytyramine, normetanephrine, and metanephrine as discriminators of different hereditary forms of pheochromocytoma. Clin. Chem. 57(3), 411-420 (2011)
38. G. Eisenhofer, H.J. Timmers, J.W. Lenders, S.R. Bornstein, O. Tiebel, M. Mannelli et al., Age at diagnosis of pheochromocytoma differs according to catecholamine phenotype and tumor location. J. Clin. Endocrinol. Metab. 96(2), 375-384 (2011)
39. E.A. Gerlo, C. Sevens, Urinary and plasma catecholamines and urinary catecholamine metabolites in pheochromocytoma: diagnostic value in 19 cases. Clin. Chem. 40(2), 250-256 (1994) (Pubitemid 24072583)
40. R. Mornex, C. Badet, L. Peyrin, Malignant pheochromocytoma: a series of 14 cases observed between 1966 and 1990. J. Endocrinol. Investig. 15(9), 643-649 (1992)
41. J. Axelrod, Methylation reactions in the formation and metabolism of catecholamines and other biogenic amines. Pharmacol. Rev. 18(1), 95-113 (1966)
42. A.E. Jacques, A. Sahdev, M. Sandrasagara, R. Goldstein, D. Berney, A.G. Rockall et al., Adrenal phaeochromocytoma: correlation of MRI appearances with histology and function. Eur. Radiol. 18(12), 2885-2892 (2008)
43. K. Brindle, New approaches for imaging tumour responses to treatment. Nat. Rev. Cancer 8(2), 94-107 (2008) (Pubitemid 351161320)
44. K.S. Bhatia, M.M. Ismail, A. Sahdev, A.G. Rockall, K. Hogarth, A. Canizales et al., 123I-Metaiodobenzylguanidine (MIBG) scintigraphy for the detection of adrenal and extra-adrenal phaeochromocytomas: CT and MRI correlation. Clin. Endocrinol. (Oxf.) 69(2), 181-188 (2008) (Pubitemid 352009037)
45. I. Ilias, C.C. Chen, J.A. Carrasquillo, M. Whatley, A. Ling, I. Lazurova et al., Comparison of 6-18F-fluorodopamine PET with 123I-metaiodobenzylguanidine and 111in-pentetreotide scintigraphy in localization of nonmetastatic and metastatic pheochromocytoma. J. Nucl. Med. 49(10), 1613-1619 (2008)
46. R. Mihai, F. Gleeson, D. Roskell, A. Parker, G. Sadler, Routine preoperative (123)I-MIBG scintigraphy for patients with phaeochromocytoma is not necessary. Langenbecks Arch. Surg. 393(5), 725-727 (2008)
47. U. Srirangalingam, B. Khoo, L. Walker, F. MacDonald, R.H. Skelly, E. George et al., Contrasting clinical manifestations of SDHB and VHL associated chromaffin tumours. Endocr. Relat. Cancer 16(2), 515-525 (2009)
48. H.J. Timmers, A. Kozupa, C.C. Chen, J.A. Carrasquillo, A. Ling, G. Eisenhofer et al., Superiority of fluorodeoxyglucose positron emission tomography to other functional imaging techniques in the evaluation of metastatic SDHB-associated pheochromocytoma and paraganglioma. J. Clin. Oncol. 25(16), 2262-2269 (2007) (Pubitemid 46954653)
49. E. van der Harst, W.W. de Herder, H.A. Bruining, H.J. Bonjer, R.R. de Krijger, S.W. Lamberts et al., [(123)I]Metaiodobenzylguanidine and [(111)In]octreotide uptake in benign and malignant pheochromocytomas. J. Clin. Endocrinol. Metab. 86(2), 685-693 (2001) (Pubitemid 32207482)
50. S. Hoegerle, E. Nitzsche, C. Altehoefer, N. Ghanem, T. Manz, I. Brink et al., Pheochromocytomas: detection with 18F DOPA whole body PET-initial results. Radiology 222(2), 507-512 (2002) (Pubitemid 34106126)
51. D. Taieb, L. Tessonnier, F. Sebag, P. Niccoli-Sire, I. Morange, C. Colavolpe et al., The role of 18F-FDOPA and 18F-FDG-PET in the management of malignant and multifocal phaeochromocytomas. Clin. Endocrinol. (Oxf.) 69(4), 580-586 (2008)
52. H.J. Timmers, M. Hadi, J.A. Carrasquillo, C.C. Chen, L. Martiniova, M. Whatley et al., The effects of carbidopa on uptake of 6-18F-Fluoro-L-DOPA in PET of pheochromocytoma and extra adrenal abdominal paraganglioma. J. Nucl. Med. 48(10), 1599-1606 (2007) (Pubitemid 47572706)
53. B. Havekes, K. King, E.W. Lai, J.A. Romijn, E.P. Corssmit, K. Pacak, New imaging approaches to phaeochromocytomas and paragangliomas. Clin. Endocrinol. (Oxf.) 72(2), 137-145 (2010)
54. H.J. Timmers, C.C. Chen, J.A. Carrasquillo, M. Whatley, A. Ling, B. Havekes et al., Comparison of 18F-fluoro-L-DOPA, 18F-fluoro-deoxyglucose, and 18F-fluorodopamine PET and 123I-MIBG scintigraphy in the localization of pheochromocytoma and paraganglioma. J. Clin. Endocrinol. Metab. 94(12), 4757-4767 (2009)
55. D.J. Kwekkeboom, H. Vanurk, B.K.H. Pauw, S.W.J. Lamberts, P.P.M. Kooij, R.P.L.M. Hoogma et al., Octreotide scintigraphy for the detection of paragangliomas. J. Nucl. Med. 34(6), 873-878 (1993) (Pubitemid 23174602)
56. T. van Gelder, G.T. Verhoeven, P. de Jong, H.Y. Oei, E.P. Krenning, V.D. Vuzevski et al., Dopamine-producing paraganglioma not visualized by iodine-123-MIBG scintigraphy. J. Nucl. Med. 36(4), 620-622 (1995)
57. G. Kaltsas, M. Korbonits, E. Heintz, J.J. Mukherjee, P.J. Jenkins, S.L. Chew et al., Comparison of somatostatin analog and metaiodobenzylguanidine radionuclides in the diagnosis and localization of advanced neuroendocrine tumors. J. Clin. Endocrinol. Metab. 86(2), 895-902 (2001) (Pubitemid 32207512)
58. A. Takano, N. Oriuchi, Y. Tsushima, A. Taketomi-Takahashi, T. Nakajima, Y. Arisaka et al., Detection of metastatic lesions from malignant pheochromocytoma and paraganglioma with diffusion-weighted magnetic resonance imaging: comparison with F-18-FDG positron emission tomography and I-123-MIBG scintigraphy. Ann. Nucl. Med. 22(5), 395-401 (2008) (Pubitemid 351938512)
59. D. Wu, A.S. Tischler, R.V. Lloyd, R.A. DeLellis, R. de Krijger, F. van Nederveen et al., Observer variation in the application of the Pheochromocytoma of the Adrenal Gland Scaled Score. Am. J. Surg. Pathol. 33(4), 599-608 (2009)
60. Y. Anouar, L. Yon, J. Guillemot, E. Thouennon, L. Barbier, A.P. Gimenez-Roqueplo et al., Development of novel tools for the diagnosis and prognosis of pheochromocytoma using peptide marker immunoassay and gene expression profiling approaches. Ann. N. Y. Acad. Sci. 1073, 533-540 (2006) (Pubitemid 44912048)
61. F.M. Brouwers, A.G. Elkahloun, P.J. Munson, G. Eisenhofer, J. Barb, W.M. Linehan et al., Gene expression profiling of benign and malignant pheochromocytoma. Ann. N. Y. Acad. Sci. 1073, 541-556 (2006) (Pubitemid 44912049)
62. E. Thouennon, A.G. Elkahloun, J. Guillemot, A.P. Gimenez- Roqueplo, J. Bertherat, A. Pierre et al., Identification of potential gene markers and insights into the pathophysiology of pheochromocytoma malignancy. J. Clin. Endocrinol. Metab. 92(12), 4865-4872 (2007) (Pubitemid 350223470)
63. J. Waldmann, V. Fendrich, J. Holler, M. Buchholz, E. Heinmoller, P. Langer et al., Microarray analysis reveals differential expression of benign and malignant pheochromocytoma. Endocr. Relat. Cancer 17(3), 743-756 (2010)
64. E. Nakamura, W.G. Kaelin Jr, Recent insights into the molecular pathogenesis of pheochromocytoma and paraganglioma. Endocr. Pathol. 17(2), 97-106 (2006) (Pubitemid 44965897)
65. J.F. Powers, M.J. Evinger, J. Zhi, K.L. Picard, A.S. Tischler, Pheochromocytomas in Nf1 knockout mice express a neural progenitor gene expression profile. Neuroscience 147(4), 928-937 (2007) (Pubitemid 47102544)
66. V. Hayry, K. Salmenkivi, J. Arola, P. Heikkila, C. Haglund, H. Sariola, High frequency of SNAIL-expressing cells confirms and predicts metastatic potential of phaeochromocytoma. Endocr. Relat. Cancer 16(4), 1211-1218 (2009)
67. J. Waldmann, E.P. Slater, P. Langer, M. Buchholz, A. Ramaswamy, M.K. Walz et al., Expression of the transcription factor snail and its target gene twist are associated with malignancy in pheochromocytomas. Ann. Surg. Oncol. 16(7), 1997-2005 (2009)
68. G. Moreno-Bueno, F. Portillo, A. Cano, Transcriptional regulation of cell polarity in EMT and cancer. Oncogene 27(55), 6958-6969 (2008)
69. V. Fendrich, J. Waldmann, F. Esni, A. Ramaswamy, M. Mullendore, M. Buchholz et al., Snail and Sonic Hedgehog activation in neuroendocrine tumors of the ileum. Endocr. Relat. Cancer 14(3), 865-874 (2007) (Pubitemid 350074074)
70. V. Fendrich, J. Waldmann, G. Feldmann, K. Schlosser, A. Konig, A. Ramaswamy et al., Unique expression pattern of the EMT markers Snail, Twist and E-cadherin in benign and malignant parathyroid neoplasia. Eur. J. Endocrinol. 160(4), 695-703 (2009)
71. J. Waldmann, G. Feldmann, E.P. Slater, P. Langer, M. Buchholz, A. Ramaswamy et al., Expression of the zinc-finger transcription factor Snail in adrenocortical carcinoma is associated with decreased survival. Br. J. Cancer 99(11), 1900-1907 (2008)
72. J. Yang, S.A. Mani, R.A. Weinberg, Exploring a new twist on tumor metastasis. Cancer Res. 66(9), 4549-4552 (2006)
73. P.L. Dahia, K.N. Ross, M.E. Wright, C.Y. Hayashida, S. Santagata, M. Barontini et al., A HIF1alpha regulatory loop links hypoxia and mitochondrial signals in pheochromocytomas. PLoS Genet. 1(1), 72-80 (2005)
74. A.P. Gimenez-Roqueplo, J. Favier, P. Rustin, J.J. Mourad, P.F. Plouin, P. Corvol et al., The R22X mutation of the SDHD gene in hereditary paraganglioma abolishes the enzymatic activity of complex II in the mitochondrial respiratory chain and activates the hypoxia pathway. Am. J. Hum. Genet. 69(6), 1186-1197 (2001) (Pubitemid 33124200)
75. W.G. Kaelin, Von Hippel-Lindau disease. Annu. Rev. Pathol. 2, 145-173 (2007)
76. T. Uchida, F. Rossignol, M.A. Matthay, R. Mounier, S. Couette, E. Clottes et al., Prolonged hypoxia differentially regulates hypoxia-inducible factor (HIF)-1alpha and HIF-2alpha expression in lung epithelial cells: implication of natural antisense HIF- 1alpha. J. Biol. Chem. 279(15), 14871-14878 (2004)
77. A. Cayre, F. Rossignol, E. Clottes, F. Penault-Llorca, aHIF but not HIF-1alpha transcript is a poor prognostic marker in human breast cancer. Breast Cancer Res. 5(6), R223-R230 (2003)
78. P.N. Span, J.U. Rao, S.B. Oude Ophuis, J.W. Lenders, F.C. Sweep, P. Wesseling et al., Overexpression of the natural antisense hypoxia-inducible factor-1alpha transcript is associated with malignant pheochromocytoma/ paraganglioma. Endocr. Relat. Cancer 18(3), 323-331 (2011)
79. T. Nishikimi, Adrenomedullin in the kidney-renal physiological and pathophysiological roles. Curr. Med. Chem. 14(15), 1689-1699 (2007) (Pubitemid 47010156)
80. T. Ishikawa, J. Chen, J. Wang, F. Okada, T. Sugiyama, T. Kobayashi et al., Adrenomedullin antagonist suppresses in vivo growth of human pancreatic cancer cells in SCID mice by suppressing angiogenesis. Oncogene 22(8), 1238-1242 (2003) (Pubitemid 36363387)
81. B. Uzan, A. Villemin, J.M. Garel, M. Cressent, Adrenomedullin is anti-apoptotic in osteoblasts through CGRP1 receptors and MEK-ERK pathway. J. Cell Physiol. 215(1), 122-128 (2008) (Pubitemid 351363197)
82. E. Thouennon, A. Pierre, Y. Tanguy, J. Guillemot, D.L. Manecka, M. Guerin et al., Expression of trophic amidated peptides and their receptors in benign and malignant pheochromocytomas: high expression of adrenomedullin RDC1 receptor and implication in tumoral cell survival. Endocr. Relat. Cancer 17(3), 637-651 (2010)
83. G.Y. Meyer-Rochow, N.E. Jackson, J.V. Conaglen, D.E. Whittle, M. Kunnimalaiyaan, H. Chen et al., MicroRNA profiling of benign and malignant pheochromocytomas identifies novel diagnostic and therapeutic targets. Endocr. Relat. Cancer 17(3), 835-846 (2010)
84. P.S. Soon, L.J. Tacon, A.J. Gill, C.P. Bambach, M.S. Sywak, P.R. Campbell et al., miR-195 and miR-483-5p Identified as predictors of poor prognosis in adrenocortical cancer. Clin. Cancer Res. 15(24), 7684-7692 (2009)
85. E.E. Elder, D. Xu, A. Hoog, U. Enberg, M. Hou, P. Pisa et al., KI-67 and hTERT Expression can aid in the distinction between malignant and benign pheochromocytoma and paraganglioma. Mod. Pathol. 16(3), 246-255 (2003) (Pubitemid 36337431)
86. J. Favier, P.F. Plouin, P. Corvol, J.M. Gasc, Angiogenesis and vascular architecture in pheochromocytomas: distinctive traits in malignant tumors. Am. J. Pathol. 161(4), 1235-1246 (2002)
87. R.M. Quiros, A.W. Kim, J. Maxhimer, P. Gattuso, X. Xu, R.A. Prinz, Differential heparanase-1 expression in malignant and benign pheochromocytomas. J. Surg. Res. 108(1), 44-50 (2002) (Pubitemid 35373814)
88. A. Khorram-Manesh, H. Ahlman, S. Jansson, O. Nilsson, N-Cadherin expression in adrenal tumors: upregulation in malignant pheochromocytoma and downregulation in adrenocortical carcinoma. Endocr. Pathol. 13(2), 99-110 (2002) (Pubitemid 34828130)
89. W. Yuan, W. Wang, B. Cui, T. Su, Y. Ge, L. Jiang et al., Overexpression of ERBB-2 was more frequently detected in malignant than benign pheochromocytomas by multiplex ligation-dependent probe amplification and immunohistochemistry. Endocr. Relat. Cancer 15(1), 343-350 (2008) (Pubitemid 351449752)
90. S. Ohta, E.W. Lai, A.L. Pang, F.M. Brouwers, W.Y. Chan, G. Eisenhofer et al., Downregulation of metastasis suppressor genes in malignant pheochromocytoma. Int. J. Cancer 114(1), 139-143 (2005) (Pubitemid 40194319)
91. P. Bjorklund, K. Cupisti, M. Fryknas, A. Isaksson, H.S. Willenberg, G. Akerstrom et al., Stathmin as a marker for malignancy in pheochromocytomas. Exp. Clin. Endocrinol. Diabetes 118(1), 27-30 (2010)