Role of hypoxia and hif2α in development of the sympathoadrenal cell lineage and chromaffin cell tumors with distinct catecholamine phenotypic features

Advances in Pharmacology

Volumn 68, Issue , 2013, Pages 285-317

  Richter, Susan ^a   Qin, Nan ^a   Pacak, Karel ^b   Eisenhofer, Graeme ^a  

^a UNIVERSITY HOSPITAL CARL GUSTAV CARUS   (Germany)

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

Author keywords

Catecholamines; Chromaffin cell; Hypoxia; Hypoxia inducible factor 2; Paraganglioma; Pheochromocytoma; Sympathoadrenal development

Indexed keywords

BIOLOGICAL MARKER; CATECHOLAMINE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; VON HIPPEL LINDAU PROTEIN;

ADRENERGIC SYSTEM; ANGIOGENESIS; ARTICLE; ASTROCYTOMA; BRAIN CELL; CARCINOGENESIS; CATECHOLAMINE RELEASE; CATECHOLAMINE SYNTHESIS; CELL DIFFERENTIATION; CELL LINEAGE; CELL MATURATION; CHROMAFFIN CELL; EMBRYO DEVELOPMENT; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION PROFILING; GENE MUTATION; GENOTYPE PHENOTYPE CORRELATION; GLIOMA; HEAD AND NECK CANCER; HYPOXIA; KIDNEY CARCINOMA; MELANOMA; NEUROBLASTOMA; NONHUMAN; PARAGANGLIOMA; PHENOTYPIC VARIATION; PHEOCHROMOCYTOMA; PRIORITY JOURNAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TUMOR CELL;

CATECHOLAMINES; CHROMAFFIN CELL; HYPOXIA; HYPOXIA-INDUCIBLE FACTOR 2; PARAGANGLIOMA; PHEOCHROMOCYTOMA; SYMPATHOADRENAL DEVELOPMENT;

ADRENAL GLAND NEOPLASMS; ANIMALS; ANOXIA; CATECHOLAMINES; CHROMAFFIN CELLS; GENOTYPE; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; PARAGANGLIOMA; PHENOTYPE; PHEOCHROMOCYTOMA;

EID: 84884309204     PISSN: 10543589     EISSN: 15578925     Source Type: Book Series    
DOI: 10.1016/B978-0-12-411512-5.00014-2     Document Type: Chapter

References (165)

1. Acker T., Diez-Juan A., Aragones J., Tjwa M., Brusselmans K., Moons L., et al. Genetic evidence for a tumor suppressor role of HIF-2alpha. Cancer Cell 2005, 8(2):131-141.
2. Adams M.B., McMillen I.C. Actions of hypoxia on catecholamine synthetic enzyme mRNA expression before and after development of adrenal innervation in the sheep fetus. The Journal of Physiology 2000, 529(Pt 3):519-531.
3. Ahmad A., Ahmad S., Glover L., Miller S.M., Shannon J.M., Guo X., et al. Adenosine A2A receptor is a unique angiogenic target of HIF-2alpha in pulmonary endothelial cells. Proceedings of the National Academy of Sciences of the United States of America 2009, 106(26):10684-10689.
4. Amar L., Baudin E., Burnichon N., Peyrard S., Silvera S., Bertherat J., et al. Succinate dehydrogenase B gene mutations predict survival in patients with malignant pheochromocytomas or paragangliomas. Journal of Clinical Endocrinology and Metabolism 2007, 92(10):3822-3828.
5. Amar L., Bertherat J., Baudin E., Ajzenberg C., Bressac-de Paillerets B., Chabre O., et al. Genetic testing in pheochromocytoma or functional paraganglioma. Journal of Clinical Oncology 2005, 23(34):8812-8818.
6. Appelhoff R.J., Tian Y.M., Raval R.R., Turley H., Harris A.L., Pugh C.W., et al. Differential function of the prolyl hydroxylases PHD1, PHD2, and PHD3 in the regulation of hypoxia-inducible factor. Journal of Biological Chemistry 2004, 279(37):38458-38465.
7. Astuti D., Hart-Holden N., Latif F., Lalloo F., Black G.C., Lim C., et al. Genetic analysis of mitochondrial complex II subunits SDHD, SDHB and SDHC in paraganglioma and phaeochromocytoma susceptibility. Clinical Endocrinology 2003, 59(6):728-733.
8. Bajou K., Noel A., Gerard R.D., Masson V., Brunner N., Holst-Hansen C., et al. Absence of host plasminogen activator inhibitor 1 prevents cancer invasion and vascularization. Nature Medicine 1998, 4(8):923-928.
9. Bayley J.P., van Minderhout I., Hogendoorn P.C., Cornelisse C.J., van der Wal A., Prins F.A., et al. Sdhd and SDHD/H19 knockout mice do not develop paraganglioma or pheochromocytoma. PLoS One 2009, 4(11):e7987.
10. Baysal B.E., Ferrell R.E., Willett-Brozick J.E., Lawrence E.C., Myssiorek D., Bosch A., et al. Mutations in SDHD, a mitochondrial complex II gene, in hereditary paraganglioma. Science 2000, 287(5454):848-851.
11. Bertout J.A., Majmundar A.J., Gordan J.D., Lam J.C., Ditsworth D., Keith B., et al. HIF2alpha inhibition promotes p53 pathway activity, tumor cell death, and radiation responses. Proceedings of the National Academy of Sciences of the United States of America 2009, 106(34):14391-14396.
12. Bishop T., Gallagher D., Pascual A., Lygate C.A., de Bono J.P., Nicholls L.G., et al. Abnormal sympathoadrenal development and systemic hypotension in PHD3-/- mice. Molecular and Cellular Biology 2008, 28(10):3386-3400.
13. Biswas S., Troy H., Leek R., Chung Y.L., Li J.L., Raval R.R., et al. Effects of HIF-1alpha and HIF2alpha on growth and metabolism of clear-cell renal cell carcinoma 786-0 xenografts. Journal of Oncology 2010, 2010:757908.
14. Blank A., Schmitt A.M., Korpershoek E., van Nederveen F., Rudolph T., Weber N., et al. SDHB loss predicts malignancy in pheochromocytomas/sympathethic paragangliomas, but not through hypoxia signalling. Endocrine-Related Cancer 2010, 17(4):919-928.
15. Bournaud R., Hidalgo J., Yu H., Girard E., Shimahara T. Catecholamine secretion from rat foetal adrenal chromaffin cells and hypoxia sensitivity. Pflügers Archiv 2007, 454(1):83-92.
16. Branco-Price C., Zhang N., Schnelle M., Evans C., Katschinski D.M., Liao D., et al. Endothelial cell HIF-1alpha and HIF-2alpha differentially regulate metastatic success. Cancer Cell 2012, 21(1):52-65.
17. Brouwers F.M., Eisenhofer G., Tao J.J., Kant J.A., Adams K.T., Linehan W.M., et al. High frequency of SDHB germline mutations in patients with malignant catecholamine-producing paragangliomas: Implications for genetic testing. Journal of Clinical Endocrinology and Metabolism 2006, 91(11):4505-4509.
18. Brouwers F.M., Elkahloun A.G., Munson P.J., Eisenhofer G., Barb J., Linehan W.M., et al. Gene expression profiling of benign and malignant pheochromocytoma. Annals of the New York Academy of Sciences 2006, 1073:541-556.
19. Brown S.T., Kelly K.F., Daniel J.M., Nurse C.A. Hypoxia inducible factor (HIF)-2 alpha is required for the development of the catecholaminergic phenotype of sympathoadrenal cells. Journal of Neurochemistry 2009, 110(2):622-630.
20. Brown S.T., Reyes E.P., Nurse C.A. Chronic hypoxia upregulates adenosine 2a receptor expression in chromaffin cells via hypoxia inducible factor-2alpha: Role in modulating secretion. Biochemical and Biophysical Research Communications 2011, 412(3):466-472.
21. Burnichon N., Briere J.J., Libe R., Vescovo L., Riviere J., Tissier F., et al. SDHA is a tumor suppressor gene causing paraganglioma. Human Molecular Genetics 2010, 19(15):3011-3020.
22. Burnichon N., Vescovo L., Amar L., Libe R., de Reynies A., Venisse A., et al. Integrative genomic analysis reveals somatic mutations in pheochromocytoma and paraganglioma. Human Molecular Genetics 2011, 20(20):3974-3985.
23. Carpenter E., Hatton C.J., Peers C. Effects of hypoxia and dithionite on catecholamine release from isolated type I cells of the rat carotid body. The Journal of Physiology 2000, 523(Pt 3):719-729.
24. Carroll V.A., Ashcroft M. Role of hypoxia-inducible factor (HIF)-1alpha versus HIF-2alpha in the regulation of HIF target genes in response to hypoxia, insulin-like growth factor-I, or loss of von Hippel-Lindau function: Implications for targeting the HIF pathway. Cancer Research 2006, 66(12):6264-6270.
25. Casanova S., Rosenberg-Bourgin M., Farkas D., Calmettes C., Feingold N., Heshmati H.M., et al. Phaeochromocytoma in multiple endocrine neoplasia type 2 A: Survey of 100 cases. Clinical Endocrinology 1993, 38(5):531-537.
26. Cascon A., Pita G., Burnichon N., Landa I., Lopez-Jimenez E., Montero-Conde C., et al. Genetics of pheochromocytoma and paraganglioma in Spanish patients. Journal of Clinical Endocrinology and Metabolism 2009, 94(5):1701-1705.
27. Cervera A.M., Bayley J.P., Devilee P., McCreath K.J. Inhibition of succinate dehydrogenase dysregulates histone modification in mammalian cells. Molecular Cancer 2009, 8:89.
28. Chazaud B., Ricoux R., Christov C., Plonquet A., Gherardi R.K., Barlovatz-Meimon G. Promigratory effect of plasminogen activator inhibitor-1 on invasive breast cancer cell populations. American Journal of Pathology 2002, 160(1):237-246.
29. Chen H., Houshmand G., Mishra S., Fong G.H., Gittes G.K., Esni F. Impaired pancreatic development in Hif2-alpha deficient mice. Biochemical and Biophysical Research Communications 2010, 399(3):440-445.
30. Cheung C.Y. Direct adrenal medullary catecholamine response to hypoxia in fetal sheep. Journal of Neurochemistry 1989, 52(1):148-153.
31. Comino-Mendez I., de Cubas A.A., Bernal C., Alvarez-Escola C., Sanchez-Malo C., Ramirez-Tortosa C.L., et al. Tumoral EPAS1 (HIF2A) mutations explain sporadic pheochromocytoma and paraganglioma in the absence of erythrocytosis. Human Molecular Genetics 2013, 22(11):2169-2176.
32. Comino-Mendez I., Gracia-Aznarez F.J., Schiavi F., Landa I., Leandro-Garcia L.J., Leton R., et al. Exome sequencing identifies MAX mutations as a cause of hereditary pheochromocytoma. Nature Genetics 2011, 43(7):663-667.
33. Covello K.L., Kehler J., Yu H., Gordan J.D., Arsham A.M., Hu C.J., et al. HIF-2alpha regulates Oct-4: Effects of hypoxia on stem cell function, embryonic development, and tumor growth. Genes & Development 2006, 20(5):557-570.
34. Czyzyk-Krzeska M.F., Bayliss D.A., Lawson E.E., Millhorn D.E. Regulation of tyrosine hydroxylase gene expression in the rat carotid body by hypoxia. Journal of Neurochemistry 1992, 58(4):1538-1546.
35. Czyzyk-Krzeska M.F., Furnari B.A., Lawson E.E., Millhorn D.E. Hypoxia increases rate of transcription and stability of tyrosine hydroxylase mRNA in pheochromocytoma (PC12) cells. Journal of Biological Chemistry 1994, 269(1):760-764.
36. Dahia P.L., Ross K.N., Wright M.E., Hayashida C.Y., Santagata S., Barontini M., et al. A HIF1alpha regulatory loop links hypoxia and mitochondrial signals in pheochromocytomas. PLoS Genetics 2005, 1(1):72-80.
37. Dang C.V., Kim J.W., Gao P., Yustein J. The interplay between MYC and HIF in cancer. Nature Reviews. Cancer 2008, 8(1):51-56.
38. Dasgupta B., Yi Y., Chen D.Y., Weber J.D., Gutmann D.H. Proteomic analysis reveals hyperactivation of the mammalian target of rapamycin pathway in neurofibromatosis 1-associated human and mouse brain tumors. Cancer Research 2005, 65(7):2755-2760.
39. Dechant G. Chat in the trophic web: NGF activates Ret by inter-RTK signaling. Neuron 2002, 33(2):156-158.
40. Dimsdale J.E., Coy T., Ziegler M.G., Ancoli-Israel S., Clausen J. The effect of sleep apnea on plasma and urinary catecholamines. Sleep 1995, 18(5):377-381.
41. Donnelly D.F. Development of carotid body/petrosal ganglion response to hypoxia. Respiratory Physiology & Neurobiology 2005, 149(1-3):191-199.
42. Donnelly D.F., Doyle T.P. Developmental changes in hypoxia-induced catecholamine release from rat carotid body, in vitro. The Journal of Physiology 1994, 475(2):267-275.
43. Ducsay C.A., Hyatt K., Mlynarczyk M., Root B.K., Kaushal K.M., Myers D.A. Long-term hypoxia modulates expression of key genes regulating adrenomedullary function in the late gestation ovine fetus. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 2007, 293(5):R1997-R2005.
44. Eisenhofer G., Huynh T.T., Elkahloun A., Morris J.C., Bratslavsky G., Linehan W.M., et al. Differential expression of the regulated catecholamine secretory pathway in different hereditary forms of pheochromocytoma. American Journal of Physiology, Endocrinology and Metabolism 2008, 295(5):E1223-E1233.
45. Eisenhofer G., Huynh T.T., Pacak K., Brouwers F.M., Walther M.M., Linehan W.M., et al. Distinct gene expression profiles in norepinephrine- and epinephrine-producing hereditary and sporadic pheochromocytomas: Activation of hypoxia-driven angiogenic pathways in von Hippel-Lindau syndrome. Endocrine-Related Cancer 2004, 11(4):897-911.
46. Eisenhofer G., Lenders J.W., Siegert G., Bornstein S.R., Friberg P., Milosevic D., et al. Plasma methoxytyramine: A novel biomarker of metastatic pheochromocytoma and paraganglioma in relation to established risk factors of tumour size, location and SDHB mutation status. European Journal of Cancer 2012, 48(11):1739-1749.
47. Eisenhofer G., Pacak K., Huynh T.T., Qin N., Bratslavsky G., Linehan W.M., et al. Catecholamine metabolomic and secretory phenotypes in phaeochromocytoma. Endocrine-Related Cancer 2011, 18(1):97-111.
48. Eisenhofer G., Timmers H.J., Lenders J.W., Bornstein S.R., Tiebel O., Mannelli M., et al. Age at diagnosis of pheochromocytoma differs according to catecholamine phenotype and tumor location. Journal of Clinical Endocrinology and Metabolism 2011, 96(2):375-384.
49. Eisenhofer G., Walther M.M., Huynh T.T., Li S.T., Bornstein S.R., Vortmeyer A., et al. Pheochromocytomas in von Hippel-Lindau syndrome and multiple endocrine neoplasia type 2 display distinct biochemical and clinical phenotypes. Journal of Clinical Endocrinology and Metabolism 2001, 86(5):1999-2008.
50. Estus S., Zaks W.J., Freeman R.S., Gruda M., Bravo R., Johnson E.M. Altered gene expression in neurons during programmed cell death: Identification of c-jun as necessary for neuronal apoptosis. The Journal of Cell Biology 1994, 127(6 Pt 1):1717-1727.
51. Evinger M.J., Cikos S., Nwafor-Anene V., Powers J.F., Tischler A.S. Hypoxia activates multiple transcriptional pathways in mouse pheochromocytoma cells. Annals of the New York Academy of Sciences 2002, 971:61-65.
52. Favier J., Briere J.J., Burnichon N., Riviere J., Vescovo L., Benit P., et al. The Warburg effect is genetically determined in inherited pheochromocytomas. PLoS One 2009, 4(9):e7094.
53. Favier J., Buffet A., Gimenez-Roqueplo A.P. HIF2A mutations in paraganglioma with polycythemia. The New England Journal of Medicine 2012, 367(22):2161. author reply 2161-2162.
54. Favier J., Igaz P., Burnichon N., Amar L., Libe R., Badoual C., et al. Rationale for anti-angiogenic therapy in pheochromocytoma and paraganglioma. Endocrine Pathology 2012, 23(1):34-42.
55. Favier J., Kempf H., Corvol P., Gasc J.M. Cloning and expression pattern of EPAS1 in the chicken embryo. Colocalization with tyrosine hydroxylase. FEBS Letters 1999, 462(1-2):19-24.
56. Fukuda T., Ishii K., Nanmoku T., Isobe K., Kawakami Y., Takekoshi K. 5-Aminoimidazole-4-carboxamide-1-beta-4-ribofuranoside stimulates tyrosine hydroxylase activity and catecholamine secretion by activation of AMP-activated protein kinase in PC12 cells. Journal of Neuroendocrinology 2007, 19(8):621-631.
57. Gamboa A., Gamboa J.L., Holmes C., Sharabi Y., Leon-Velarde F., Fischman G.J., et al. Plasma catecholamines and blood volume in native Andeans during hypoxia and normoxia. Clinical Autonomic Research 2006, 16(1):40-45.
58. Giatromanolaki A., Sivridis E., Fiska A., Koukourakis M.I. Hypoxia-inducible factor-2 alpha (HIF-2 alpha) induces angiogenesis in breast carcinomas. Applied Immunohistochemistry & Molecular Morphology 2006, 14(1):78-82.
59. Gimenez-Roqueplo A.P., Favier J., Rustin P., Rieubland C., Crespin M., Nau V., et al. Mutations in the SDHB gene are associated with extra-adrenal and/or malignant phaeochromocytomas. Cancer Research 2003, 63(17):5615-5621.
60. Gordan J.D., Bertout J.A., Hu C.J., Diehl J.A., Simon M.C. HIF-2alpha promotes hypoxic cell proliferation by enhancing c-myc transcriptional activity. Cancer Cell 2007, 11(4):335-347.
61. Gozal E., Shah Z.A., Pequignot J.M., Pequignot J., Sachleben L.R., Czyzyk-Krzeska M.F., et al. Tyrosine hydroxylase expression and activity in the rat brain: Differential regulation after long-term intermittent or sustained hypoxia. Journal of Applied Physiology 2005, 99(2):642-649.
62. Gustafsson M.V., Zheng X., Pereira T., Gradin K., Jin S., Lundkvist J., et al. Hypoxia requires notch signaling to maintain the undifferentiated cell state. Developmental Cell 2005, 9(5):617-628.
63. Guzy R.D., Sharma B., Bell E., Chandel N.S., Schumacker P.T. Loss of the SdhB, but Not the SdhA, subunit of complex II triggers reactive oxygen species-dependent hypoxia-inducible factor activation and tumorigenesis. Molecular and Cellular Biology 2008, 28(2):718-731.
64. Ham J., Babij C., Whitfield J., Pfarr C.M., Lallemand D., Yaniv M., et al. A c-Jun dominant negative mutant protects sympathetic neurons against programmed cell death. Neuron 1995, 14(5):927-939.
65. Hao H.X., Khalimonchuk O., Schraders M., Dephoure N., Bayley J.P., Kunst H., et al. SDH5, a gene required for flavination of succinate dehydrogenase, is mutated in paraganglioma. Science 2009, 325(5944):1139-1142.
66. Holmquist-Mengelbier L., Fredlund E., Lofstedt T., Noguera R., Navarro S., Nilsson H., et al. Recruitment of HIF-1alpha and HIF-2alpha to common target genes is differentially regulated in neuroblastoma: HIF-2alpha promotes an aggressive phenotype. Cancer Cell 2006, 10(5):413-423.
67. Hu C.J., Iyer S., Sataur A., Covello K.L., Chodosh L.A., Simon M.C. Differential regulation of the transcriptional activities of hypoxia-inducible factor 1 alpha (HIF-1alpha) and HIF-2alpha in stem cells. Molecular and Cellular Biology 2006, 26(9):3514-3526.
68. Hu C.J., Wang L.Y., Chodosh L.A., Keith B., Simon M.C. Differential roles of hypoxia-inducible factor 1alpha (HIF-1alpha) and HIF-2alpha in hypoxic gene regulation. Molecular and Cellular Biology 2003, 23(24):9361-9374.
69. Hui A.S., Striet J.B., Gudelsky G., Soukhova G.K., Gozal E., Beitner-Johnson D., et al. Regulation of catecholamines by sustained and intermittent hypoxia in neuroendocrine cells and sympathetic neurons. Hypertension 2003, 42(6):1130-1136.
70. Imtiyaz H.Z., Williams E.P., Hickey M.M., Patel S.A., Durham A.C., Yuan L.J., et al. Hypoxia-inducible factor 2alpha regulates macrophage function in mouse models of acute and tumor inflammation. Journal of Clinical Investigation 2010, 120(8):2699-2714.
71. Jogi A., Ora I., Nilsson H., Lindeheim A., Makino Y., Poellinger L., et al. Hypoxia alters gene expression in human neuroblastoma cells toward an immature and neural crest-like phenotype. Proceedings of the National Academy of Sciences of the United States of America 2002, 99(10):7021-7026.
72. Johansen J.L., Sager T.N., Lotharius J., Witten L., Mork A., Egebjerg J., et al. HIF prolyl hydroxylase inhibition increases cell viability and potentiates dopamine release in dopaminergic cells. Journal of Neurochemistry 2010, 115(1):209-219.
73. Kaelin W.G., Ratcliffe P.J. Oxygen sensing by metazoans: The central role of the HIF hydroxylase pathway. Molecular Cell 2008, 30(4):393-402.
74. Kanstrup I.L., Poulsen T.D., Hansen J.M., Andersen L.J., Bestle M.H., Christensen N.J., et al. Blood pressure and plasma catecholamines in acute and prolonged hypoxia: Effects of local hypothermia. Journal of Applied Physiology 1999, 87(6):2053-2058.
75. Keith B., Johnson R.S., Simon M.C. HIF1alpha and HIF2alpha: Sibling rivalry in hypoxic tumour growth and progression. Nature Reviews. Cancer 2012, 12(1):9-22.
76. Kim W.Y., Perera S., Zhou B., Carretero J., Yeh J.J., Heathcote S.A., et al. HIF2alpha cooperates with RAS to promote lung tumorigenesis in mice. Journal of Clinical Investigation 2009, 119(8):2160-2170.
77. King K.S., Prodanov T., Kantorovich V., Fojo T., Hewitt J.K., Zacharin M., et al. Metastatic pheochromocytoma/paraganglioma related to primary tumor development in childhood or adolescence: Significant link to SDHB mutations. Journal of Clinical Oncology 2011, 29(31):4137-4142.
78. Kobayashi K., Morita S., Sawada H., Mizuguchi T., Yamada K., Nagatsu I., et al. Targeted disruption of the tyrosine hydroxylase locus results in severe catecholamine depletion and perinatal lethality in mice. Journal of Biological Chemistry 1995, 270(45):27235-27243.
79. Koh M.Y., Darnay B.G., Powis G. Hypoxia-associated factor, a novel E3-ubiquitin ligase, binds and ubiquitinates hypoxia-inducible factor 1alpha, leading to its oxygen-independent degradation. Molecular and Cellular Biology 2008, 28(23):7081-7095.
80. Koh M.Y., Lemos R., Liu X., Powis G. The hypoxia-associated factor switches cells from HIF-1alpha- to HIF-2alpha-dependent signaling promoting stem cell characteristics, aggressive tumor growth and invasion. Cancer Research 2011, 71(11):4015-4027.
81. Koh M.Y., Powis G. Passing the baton: The HIF switch. Trends in Biochemical Sciences 2012, 37(9):364-372.
82. Kondo K., Kim W.Y., Lechpammer M., Kaelin W.G. Inhibition of HIF2alpha is sufficient to suppress pVHL-defective tumor growth. PLoS Biology 2003, 1(3):E83.
83. Kumar G.K., Overholt J.L., Bright G.R., Hui K.Y., Lu H., Gratzl M., et al. Release of dopamine and norepinephrine by hypoxia from PC-12 cells. American Journal of Physiology 1998, 274(6 Pt 1):C1592-C1600.
84. Kumar G.K., Rai V., Sharma S.D., Ramakrishnan D.P., Peng Y.J., Souvannakitti D., et al. Chronic intermittent hypoxia induces hypoxia-evoked catecholamine efflux in adult rat adrenal medulla via oxidative stress. The Journal of Physiology 2006, 575(Pt 1):229-239.
85. Lam S.Y., Tipoe G.L., Liong E.C., Fung M.L. Differential expressions and roles of hypoxia-inducible factor-1alpha, -2alpha and -3alpha in the rat carotid body during chronic and intermittent hypoxia. Histology and Histopathology 2008, 23(3):271-280.
86. Latif F., Tory K., Gnarra J., Yao M., Duh F.M., Orcutt M.L., et al. Identification of the von Hippel-Lindau disease tumor suppressor gene. Science 1993, 260(5112):1317-1320.
87. Lee S., Nakamura E., Yang H., Wei W., Linggi M.S., Sajan M.P., et al. Neuronal apoptosis linked to EglN3 prolyl hydroxylase and familial pheochromocytoma genes: Developmental culling and cancer. Cancer Cell 2005, 8(2):155-167.
88. Letouzé E., Martinelli C., Loriot C., Burnichon N., Abermil N., Ottolenghi C., et al. SDH mutations establish a hypermethylator phenotype in paraganglioma. Cancer Cell 2013, 23(6):739-752.
89. Li Z., Bao S., Wu Q., Wang H., Eyler C., Sathornsumetee S., et al. Hypoxia-inducible factors regulate tumorigenic capacity of glioma stem cells. Cancer Cell 2009, 15(6):501-513.
90. Lipscomb E.A., Sarmiere P.D., Crowder R.J., Freeman R.S. Expression of the SM-20 gene promotes death in nerve growth factor-dependent sympathetic neurons. Journal of Neurochemistry 1999, 73(1):429-432.
91. Lipscomb E.A., Sarmiere P.D., Freeman R.S. SM-20 is a novel mitochondrial protein that causes caspase-dependent cell death in nerve growth factor-dependent neurons. Journal of Biological Chemistry 2001, 276(7):5085-5092.
92. Lomb D.J., Desouza L.A., Franklin J.L., Freeman R.S. Prolyl hydroxylase inhibitors depend on extracellular glucose and hypoxia-inducible factor (HIF)-2alpha to inhibit cell death caused by nerve growth factor (NGF) deprivation: Evidence that HIF-2alpha has a role in NGF-promoted survival of sympathetic neurons. Molecular Pharmacology 2009, 75(5):1198-1209.
93. Lopez-Jimenez E., Gomez-Lopez G., Leandro-Garcia L.J., Munoz I., Schiavi F., Montero-Conde C., et al. Research resource: Transcriptional profiling reveals different pseudohypoxic signatures in SDHB and VHL-related pheochromocytomas. Molecular Endocrinology 2010, 24(12):2382-2391.
94. Lorenzo F.R., Yang C., Ng Tang Fui M., Vankayalapati H., Zhuang Z., Huynh T., et al. A novel EPAS1/HIF2A germline mutation in a congenital polycythemia with paraganglioma. J Mol Med (Berl) 2012, 91(4):507-512.
95. Mamet J., Peyronnet J., Roux J.C., Perrin D., Cottet-Emard J.M., Pequignot J.M., et al. Long-term prenatal hypoxia alters maturation of adrenal medulla in rat. Pediatric Research 2002, 51(2):207-214.
96. Mannelli M., Castellano M., Schiavi F., Filetti S., Giacche M., Mori L., et al. Clinically guided genetic screening in a large cohort of italian patients with pheochromocytomas and/or functional or nonfunctional paragangliomas. Journal of Clinical Endocrinology and Metabolism 2009, 94(5):1541-1547.
97. Maranchie J.K., Vasselli J.R., Riss J., Bonifacino J.S., Linehan W.M., Klausner R.D. The contribution of VHL substrate binding and HIF1-alpha to the phenotype of VHL loss in renal cell carcinoma. Cancer Cell 2002, 1(3):247-255.
98. Mastrogiannaki M., Matak P., Keith B., Simon M.C., Vaulont S., Peyssonnaux C. HIF-2alpha, but not HIF-1alpha, promotes iron absorption in mice. Journal of Clinical Investigation 2009, 119(5):1159-1166.
99. Mazumdar J., Hickey M.M., Pant D.K., Durham A.C., Sweet-Cordero A., Vachani A., et al. HIF-2alpha deletion promotes Kras-driven lung tumor development. Proceedings of the National Academy of Sciences of the United States of America 2010, 107(32):14182-14187.
100. Mazumdar J., O'Brien W.T., Johnson R.S., LaManna J.C., Chavez J.C., Klein P.S., et al. O2 regulates stem cells through Wnt/beta-catenin signalling. Nature Cell Biology 2010, 12(10):1007-1013.
101. Mojet M.H., Mills E., Duchen M.R. Hypoxia-induced catecholamine secretion in isolated newborn rat adrenal chromaffin cells is mimicked by inhibition of mitochondrial respiration. The Journal of Physiology 1997, 504(Pt 1):175-189.
102. Morrison S.J., Csete M., Groves A.K., Melega W., Wold B., Anderson D.J. Culture in reduced levels of oxygen promotes clonogenic sympathoadrenal differentiation by isolated neural crest stem cells. Journal of Neuroscience 2000, 20(19):7370-7376.
103. Mulligan L.M., Kwok J.B., Healey C.S., Elsdon M.J., Eng C., Gardner E., et al. Germ-line mutations of the RET proto-oncogene in multiple endocrine neoplasia type 2A. Nature 1993, 363(6428):458-460.
104. Naranjo-Suarez S., Castellanos M.C., Alvarez-Tejado M., Vara A., Landazuri M.O., del Peso L. Down-regulation of hypoxia-inducible factor-2 in PC12 cells by nerve growth factor stimulation. Journal of Biological Chemistry 2003, 278(34):31895-31901.
105. Neumann H.P., Bausch B., McWhinney S.R., Bender B.U., Gimm O., Franke G., et al. Germ-line mutations in nonsyndromic pheochromocytoma. The New England Journal of Medicine 2002, 346(19):1459-1466.
106. Niemann S., Muller U. Mutations in SDHC cause autosomal dominant paraganglioma, type 3. Nature Genetics 2000, 26(3):268-270.
107. Nilsson H., Jogi A., Beckman S., Harris A.L., Poellinger L., Pahlman S. HIF-2alpha expression in human fetal paraganglia and neuroblastoma: Relation to sympathetic differentiation, glucose deficiency, and hypoxia. Experimental Cell Research 2005, 303(2):447-456.
108. Noguera R., Fredlund E., Piqueras M., Pietras A., Beckman S., Navarro S., et al. HIF-1alpha and HIF-2alpha are differentially regulated in vivo in neuroblastoma: High HIF-1alpha correlates negatively to advanced clinical stage and tumor vascularization. Clinical Cancer Research 2009, 15(23):7130-7136.
109. Nolting S., Grossman A.B. Signaling pathways in pheochromocytomas and paragangliomas: Prospects for future therapies. Endocrine Pathology 2012, 23(1):21-33.
110. Pacak K., Jochmanova I., Prodanov T., Yang C., Merino M., Fojo T., et al. A new syndrome of paraganglioma and somatostatinoma associated with polycythemia. Journal of Clinical Oncology 2013, 31(13):1690-1698.
111. Padbury J.F. Functional maturation of the adrenal medulla and peripheral sympathetic nervous system. Baillière's Clinical Endocrinology and Metabolism 1989, 3(3):689-705.
112. Paulick R., Kastendieck E., Wernze H. Catecholamines in arterial and venous umbilical blood: Placental extraction, correlation with fetal hypoxia, and transcutaneous partial oxygen tension. Journal of Perinatal Medicine 1985, 13(1):31-42.
113. Peng J., Zhang L., Drysdale L., Fong G.H. The transcription factor EPAS-1/hypoxia-inducible factor 2alpha plays an important role in vascular remodeling. Proceedings of the National Academy of Sciences of the United States of America 2000, 97(15):8386-8391.
114. Peterson S., Bogenmann E. The RET and TRKA pathways collaborate to regulate neuroblastoma differentiation. Oncogene 2004, 23(1):213-225.
115. Petrella B.L., Lohi J., Brinckerhoff C.E. Identification of membrane type-1 matrix metalloproteinase as a target of hypoxia-inducible factor-2 alpha in von Hippel-Lindau renal cell carcinoma. Oncogene 2005, 24(6):1043-1052.
116. Phillippe M. Fetal catecholamines. American Journal of Obstetrics and Gynecology 1983, 146(7):840-855.
117. Pietras A., Gisselsson D., Ora I., Noguera R., Beckman S., Navarro S., et al. High levels of HIF-2alpha highlight an immature neural crest-like neuroblastoma cell cohort located in a perivascular niche. The Journal of Pathology 2008, 214(4):482-488.
118. Pietras A., Hansford L.M., Johnsson A.S., Bridges E., Sjolund J., Gisselsson D., et al. HIF-2alpha maintains an undifferentiated state in neural crest-like human neuroblastoma tumor-initiating cells. Proceedings of the National Academy of Sciences of the United States of America 2009, 106(39):16805-16810.
119. Pietras A., von Stedingk K., Lindgren D., Pahlman S., Axelson H. JAG2 induction in hypoxic tumor cells alters Notch signaling and enhances endothelial cell tube formation. Molecular Cancer Research 2011, 9(5):626-636.
120. Pollard P.J., El-Bahrawy M., Poulsom R., Elia G., Killick P., Kelly G., et al. Expression of HIF-1alpha, HIF-2alpha (EPAS1), and their target genes in paraganglioma and pheochromocytoma with VHL and SDH mutations. Journal of Clinical Endocrinology and Metabolism 2006, 91(11):4593-4598.
121. Pomares F.J., Canas R., Rodriguez J.M., Hernandez A.M., Parrilla P., Tebar F.J. Differences between sporadic and multiple endocrine neoplasia type 2A phaeochromocytoma. Clinical Endocrinology 1998, 48(2):195-200.
122. Prabhakar N.R., Kumar G.K. Mechanisms of sympathetic activation and blood pressure elevation by intermittent hypoxia. Respiratory Physiology & Neurobiology 2010, 174(1-2):156-161.
123. Qin Y., Yao L., King E.E., Buddavarapu K., Lenci R.E., Chocron E.S., et al. Germline mutations in TMEM127 confer susceptibility to pheochromocytoma. Nature Genetics 2010, 42(3):229-233.
124. Raghuraman G., Prabhakar N.R., Kumar G.K. Differential regulation of tyrosine hydroxylase by continuous and intermittent hypoxia. Advances in Experimental Medicine and Biology 2012, 758:381-385.
125. Rankin E.B., Biju M.P., Liu Q., Unger T.L., Rha J., Johnson R.S., et al. Hypoxia-inducible factor-2 (HIF-2) regulates hepatic erythropoietin in vivo. Journal of Clinical Investigation 2007, 117(4):1068-1077.
126. Rankin E.B., Rha J., Unger T.L., Wu C.H., Shutt H.P., Johnson R.S., et al. Hypoxia-inducible factor-2 regulates vascular tumorigenesis in mice. Oncogene 2008, 27(40):5354-5358.
127. Raval R.R., Lau K.W., Tran M.G., Sowter H.M., Mandriota S.J., Li J.L., et al. Contrasting properties of hypoxia-inducible factor 1 (HIF-1) and HIF-2 in von Hippel-Lindau-associated renal cell carcinoma. Molecular and Cellular Biology 2005, 25(13):5675-5686.
128. Ream M.A., Chandra R., Peavey M., Ray A.M., Roffler-Tarlov S., Kim H.G., et al. High oxygen prevents fetal lethality due to lack of catecholamines. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 2008, 295(3):R942-R953.
129. Ricketts C.J., Forman J.R., Rattenberry E., Bradshaw N., Lalloo F., Izatt L., et al. Tumor risks and genotype-phenotype-proteotype analysis in 358 patients with germline mutations in SDHB and SDHD. Human Mutation 2010, 31(1):41-51.
130. Roda J.M., Wang Y., Sumner L.A., Phillips G.S., Marsh C.B., Eubank T.D. Stabilization of HIF-2alpha induces sVEGFR-1 production from tumor-associated macrophages and decreases tumor growth in a murine melanoma model. Journal of Immunology 2012, 189(6):3168-3177.
131. Sato M., Tanaka T., Maemura K., Uchiyama T., Sato H., Maeno T., et al. The PAI-1 gene as a direct target of endothelial PAS domain protein-1 in adenocarcinoma A549 cells. American Journal of Respiratory Cell and Molecular Biology 2004, 31(2):209-215.
132. Schlingensiepen K.H., Wollnik F., Kunst M., Schlingensiepen R., Herdegen T., Brysch W. The role of Jun transcription factor expression and phosphorylation in neuronal differentiation, neuronal cell death, and plastic adaptations in vivo. Cellular and Molecular Neurobiology 1994, 14(5):487-505.
133. Schlisio S., Kenchappa R.S., Vredeveld L.C., George R.E., Stewart R., Greulich H., et al. The kinesin KIF1Bbeta acts downstream from EglN3 to induce apoptosis and is a potential 1p36 tumor suppressor. Genes & Development 2008, 22(7):884-893.
134. Schmitt P., Garcia C., Soulier V., Pujol J.F., Pequignot J.M. Influence of long-term hypoxia on tyrosine hydroxylase in the rat carotid body and adrenal gland. Journal of the Autonomic Nervous System 1992, 40(1):13-19.
135. Schmitt P., Pequignot J., Hanchin F., Pujol J.F., Pequignot J.M. Regional specificity of long-term regulation of tyrosine hydroxylase in some catecholaminergic rat brainstem areas. II. Effect of a chronic dihydralazine treatment. Brain Research 1993, 611(1):61-66.
136. Schnell P.O., Ignacak M.L., Bauer A.L., Striet J.B., Paulding W.R., Czyzyk-Krzeska M.F. Regulation of tyrosine hydroxylase promoter activity by the von Hippel-Lindau tumor suppressor protein and hypoxia-inducible transcription factors. Journal of Neurochemistry 2003, 85(2):483-491.
137. Scortegagna M., Ding K., Zhang Q., Oktay Y., Bennett M.J., Bennett M., et al. HIF-2alpha regulates murine hematopoietic development in an erythropoietin-dependent manner. Blood 2005, 105(8):3133-3140.
138. Scortegagna M., Morris M.A., Oktay Y., Bennett M., Garcia J.A. The HIF family member EPAS1/HIF-2alpha is required for normal hematopoiesis in mice. Blood 2003, 102(5):1634-1640.
139. Selak M.A., Armour S.M., MacKenzie E.D., Boulahbel H., Watson D.G., Mansfield K.D., et al. Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-alpha prolyl hydroxylase. Cancer Cell 2005, 7(1):77-85.
140. Skuli N., Majmundar A.J., Krock B.L., Mesquita R.C., Mathew L.K., Quinn Z.L., et al. Endothelial HIF-2alpha regulates murine pathological angiogenesis and revascularization processes. Journal of Clinical Investigation 2012, 122(4):1427-1443.
141. Smith E.H., Janknecht R., Maher L.J. Succinate inhibition of alpha-ketoglutarate-dependent enzymes in a yeast model of paraganglioma. Human Molecular Genetics 2007, 16(24):3136-3148.
142. Souvannakitti D., Nanduri J., Yuan G., Kumar G.K., Fox A.P., Prabhakar N.R. NADPH oxidase-dependent regulation of T-type Ca2+ channels and ryanodine receptors mediate the augmented exocytosis of catecholamines from intermittent hypoxia-treated neonatal rat chromaffin cells. Journal of Neuroscience 2010, 30(32):10763-10772.
143. Straub J.A., Lipscomb E.A., Yoshida E.S., Freeman R.S. Induction of SM-20 in PC12 cells leads to increased cytochrome c levels, accumulation of cytochrome c in the cytosol, and caspase-dependent cell death. Journal of Neurochemistry 2003, 85(2):318-328.
144. Takeda N., O'Dea E.L., Doedens A., Kim J.W., Weidemann A., Stockmann C., et al. Differential activation and antagonistic function of HIF-{alpha} isoforms in macrophages are essential for NO homeostasis. Genes & Development 2010, 24(5):491-501.
145. Talks K.L., Turley H., Gatter K.C., Maxwell P.H., Pugh C.W., Ratcliffe P.J., et al. The expression and distribution of the hypoxia-inducible factors HIF-1alpha and HIF-2alpha in normal human tissues, cancers, and tumor-associated macrophages. American Journal of Pathology 2000, 157(2):411-421.
146. Tang X., Mo C., Wang Y., Wei D., Xiao H. Anti-tumour strategies aiming to target tumour-associated macrophages. Immunology 2013, 138(2):93-104.
147. Taylor S.C., Batten T.F., Peers C. Hypoxic enhancement of quantal catecholamine secretion. Evidence for the involvement of amyloid beta-peptides. Journal of Biological Chemistry 1999, 274(44):31217-31222.
148. Thomas S.A., Matsumoto A.M., Palmiter R.D. Noradrenaline is essential for mouse fetal development. Nature 1995, 374(6523):643-646.
149. Tian H., Hammer R.E., Matsumoto A.M., Russell D.W., McKnight S.L. The hypoxia-responsive transcription factor EPAS1 is essential for catecholamine homeostasis and protection against heart failure during embryonic development. Genes & Development 1998, 12(21):3320-3324.
150. Tsui-Pierchala B.A., Milbrandt J., Johnson E.M. NGF utilizes c-Ret via a novel GFL-independent, inter-RTK signaling mechanism to maintain the trophic status of mature sympathetic neurons. Neuron 2002, 33(2):261-273.
151. Vanharanta S., Shu W., Brenet F., Hakimi A.A., Heguy A., Viale A., et al. Epigenetic expansion of VHL-HIF signal output drives multiorgan metastasis in renal cancer. Nature Medicine 2013, 19(1):50-56.
152. Viskochil D., Buchberg A.M., Xu G., Cawthon R.M., Stevens J., Wolff R.K., et al. Deletions and a translocation interrupt a cloned gene at the neurofibromatosis type 1 locus. Cell 1990, 62(1):187-192.
153. Waldmann J., Fendrich V., Holler J., Buchholz M., Heinmoller E., Langer P., et al. Microarray analysis reveals differential expression of benign and malignant pheochromocytoma. Endocrine-Related Cancer 2010, 17(3):743-756.
154. Walther M.M., Herring J., Enquist E., Keiser H.R., Linehan W.M. von Recklinghausen's disease and pheochromocytomas. Journal of Urology 1999, 162(5):1582-1586.
155. Wang X., Schneider A. HIF-2alpha-mediated activation of the epidermal growth factor receptor potentiates head and neck cancer cell migration in response to hypoxia. Carcinogenesis 2010, 31(7):1202-1210.
156. Warnecke C., Zaborowska Z., Kurreck J., Erdmann V.A., Frei U., Wiesener M., et al. Differentiating the functional role of hypoxia-inducible factor (HIF)-1alpha and HIF-2alpha (EPAS-1) by the use of RNA interference: Erythropoietin is a HIF-2alpha target gene in Hep3B and Kelly cells. The FASEB Journal 2004, 18(12):1462-1464.
157. Wong D.L., Tai T.C., Wong-Faull D.C., Claycomb R., Siddall B.J., Bell R.A., et al. Stress and adrenergic function: HIF1alpha, a potential regulatory switch. Cellular and Molecular Neurobiology 2010, 30(8):1451-1457.
158. Xia Z., Dickens M., Raingeaud J., Davis R.J., Greenberg M.E. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 1995, 270(5240):1326-1331.
159. Xiao M., Yang H., Xu W., Ma S., Lin H., Zhu H., et al. Inhibition of alpha-KG-dependent histone and DNA demethylases by fumarate and succinate that are accumulated in mutations of FH and SDH tumor suppressors. Genes & Development 2012, 26(12):1326-1338.
160. Yamashita T., Ohneda K., Nagano M., Miyoshi C., Kaneko N., Miwa Y., et al. Hypoxia-inducible transcription factor-2alpha in endothelial cells regulates tumor neovascularization through activation of ephrin A1. Journal of Biological Chemistry 2008, 283(27):18926-18936.
161. Yang S., Kim J., Ryu J.H., Oh H., Chun C.H., Kim B.J., et al. Hypoxia-inducible factor-2alpha is a catabolic regulator of osteoarthritic cartilage destruction. Nature Medicine 2010, 16(6):687-693.
162. Yang C., Sun M.G., Matro J., Huynh T.T., Rahimpour S., Prchal J.T., et al. Novel HIF2A mutations disrupt oxygen sensing leading to polycythemia, paragangliomas and somatostatinomas. Blood 2013, 121(13):2563-2566.
163. Yuan H.T., Khankin E.V., Karumanchi S.A., Parikh S.M. Angiopoietin 2 is a partial agonist/antagonist of Tie2 signaling in the endothelium. Molecular and Cellular Biology 2009, 29(8):2011-2022.
164. Zhou Q.Y., Quaife C.J., Palmiter R.D. Targeted disruption of the tyrosine hydroxylase gene reveals that catecholamines are required for mouse fetal development. Nature 1995, 374(6523):640-643.
165. Zhuang Z., Yang C., Lorenzo F., Merino M., Fojo T., Kebebew E., et al. Somatic HIF2A gain-of-function mutations in paraganglioma with polycythemia. The New England Journal of Medicine 2012, 367(10):922-930.