Deletion of the von Hippel-Lindau gene causes sympathoadrenal cell death and impairs chemoreceptor-mediated adaptation to hypoxia

EMBO Molecular Medicine

Volumn 6, Issue 12, 2014, Pages 1577-1592

  Macías, David ^a,b,c   Fernández Agüera, Mary Carmen ^a,b,c   Bonilla Henao, Victoria ^a,b,c   López Barneo, José ^a,b,c  

^a HOSPITAL UNIVERSITARIO VIRGEN DEL ROCÍO   (Spain)

^b UNIVERSITY OF SEVILLE   (Spain)

^c CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

Author keywords

Adult carotid body neurogenesis; Intolerance to hypoxia; Sympathoadrenal tumorigenesis; Vhl deficient mouse model; Von Hippel Lindau protein

Indexed keywords

HYPOXIA INDUCIBLE FACTOR; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; VON HIPPEL LINDAU PROTEIN; OXYGEN;

ACCLIMATIZATION; ADAPTATION; ADRENAL CORTEX ATROPHY; ADRENAL MEDULLA; ADRENERGIC SYSTEM; ADULT; ADULT STEM CELL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CAROTID BODY; CATECHOLAMINE NERVE CELL; CELL DEATH; CELL SURVIVAL; CHEMORECEPTOR; CONTROLLED STUDY; DOWN REGULATION; ENZYME INHIBITION; ERYTHROCYTOSIS; GENE DELETION; GENE OVEREXPRESSION; HEART VENTRICLE HYPERTROPHY; HYPOXIA; LUNG EDEMA; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PROTEIN DEFICIENCY; SYMPATHETIC GANGLION; ADRENAL TUMOR; ANIMAL; ANOXIA; APOPTOSIS; CHEMORECEPTOR CELL; CYTOLOGY; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; KNOCKOUT MOUSE; MALE; METABOLISM; PATHOPHYSIOLOGY; PHEOCHROMOCYTOMA;

ADRENAL GLAND NEOPLASMS; ADRENAL MEDULLA; ANIMALS; ANOXIA; APOPTOSIS; CELL DEATH; CHEMORECEPTOR CELLS; FEMALE; GENE DELETION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; MICE; MICE, KNOCKOUT; OXYGEN; PHEOCHROMOCYTOMA; VON HIPPEL-LINDAU TUMOR SUPPRESSOR PROTEIN;

EID: 84918566655     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.15252/emmm.201404153     Document Type: Article

References (50)

1. Ang SO, Chen H, Hirota K, Gordeuk VR, Jelinek J, Guan Y, Liu E, Sergueeva AI, Miasnikova GY, Mole D et al (2002) Disruption of oxygen homeostasis underlies congenital Chuvash polycythemia. Nat Genet 32: 614-621
2. -/- mice. Mol Cell Biol 28: 3386-3400
3. Boedeker CC, Erlic Z, Richard S, Kontny U, Gimenez-Roqueplo A-P, Cascon A, Robledo M, de Campos JM, van Nederveen FH, de Krijger RR et al (2009) Head and neck paragangliomas in von Hippel-Lindau disease and multiple endocrine neoplasia type 2. J Clin Endocrinol Metab 94: 1938-1944
4. Borden P, Houtz J, Leach SD, Kuruvilla R (2013) Sympathetic innervation during development is necessary for pancreatic islet architecture and functional maturation. Cell Rep 4: 287-301
5. Cantley J, Selman C, Shukla D, Abramov AY, Forstreuter F, Esteban MA, Claret M, Lingard SJ, Clements M, Harten SK et al (2009) Deletion of the von Hippel-Lindau gene in pancreatic beta cells impairs glucose homeostasis in mice. J Clin Invest 119: 125-135
6. Dauger S, Pattyn A, Lofaso F, Gaultier C, Goridis C, Gallego J, Brunet J-F (2003) Phox2b controls the development of peripheral chemoreceptors and afferent visceral pathways. Development 130: 6635-6642
7. Díaz-Castro B, Pintado CO, García-Flores P, López-Barneo J, Piruat JI (2012) Differential impairment of catecholaminergic cell maturation and survival by genetic mitochondrial complex II dysfunction. Mol Cell Biol 32: 3347-3357
8. Estus S, Zaks WJ, Freeman RS, Gruda M, Bravo R, Johnson EM (1994) Altered gene expression in neurons during programmed cell death: identification of c-jun as necessary for neuronal apoptosis. J Cell Biol 127: 1717-1727
9. Ghofrani HA, Reichenberger F, Kohstall MG, Mrosek EH, Seeger T, Olschewski H, Seeger W, Grimminger F (2004) Sildenafil increased exercise capacity during hypoxia at low altitudes and at Mount Everest base camp: a randomized, double-blind, placebo-controlled crossover trial. Ann Intern Med 141: 169-177
10. Gozal D, Hakim F, Kheirandish-Gozal L (2013) Chemoreceptors, baroreceptors, and autonomic deregulation in children with obstructive sleep apnea. Respir Physiol Neurobiol 185: 177-185
11. Haase VH (2005) The VHL tumor suppressor in development and disease: functional studies in mice by conditional gene targeting. Semin Cell Dev Biol 16: 564-574
12. Haase VH, Glickman JN, Socolovsky M, Jaenisch R (2001) Vascular tumors in livers with targeted inactivation of the von Hippel-Lindau tumor suppressor. Proc Natl Acad Sci USA 98: 1583-1588
13. Hempleman SC, Warburton SJ (2013) Comparative embryology of the carotid body. Respir Physiol Neurobiol 185: 3-8
14. Hickey MM, Lam JC, Bezman NA, Rathmell WK, Simon MC (2007) von Hippel-Lindau mutation in mice recapitulates Chuvash polycythemia via hypoxia-inducible factor-2alpha signaling and splenic erythropoiesis. J Clin Invest 117: 3879-3889
15. Joseph V, Pequignot J-M (2009) Breathing at high altitude. Cell Mol Life Sci 66: 3565-3573
16. Kaelin WG (2007) Von Hippel-Lindau disease. Annu Rev Pathol 2: 145-173
17. 2 sensing and cancer. Nat Rev Cancer 8: 865-873
18. Kameda Y, Ito M, Nishimaki T, Gotoh N (2008) FRS2 alpha 2F/2F mice lack carotid body and exhibit abnormalities of the superior cervical sympathetic ganglion and carotid sinus nerve. Dev Biol 314: 236-247
19. Kim WY, Safran M, Buckley MRM, Ebert BL, Glickman J, Bosenberg M, Regan M, Kaelin WG (2006) Failure to prolyl hydroxylate hypoxia-inducible factor alpha phenocopies VHL inactivation in vivo. EMBO J 25: 4650-4662
20. Koyama Y, Coker RH, Stone EE, Lacy DB, Jabbour K, Williams PE, Wasserman DH (2000) Evidence that carotid bodies play an important role in glucoregulation in vivo. Diabetes 49: 1434-1442
21. Lee S, Nakamura E, Yang H, Wei W, Linggi MS, Sajan MP, Farese RV, Freeman RS, Carter BD, Kaelin WG et al (2005) Neuronal apoptosis linked to EglN3 prolyl hydroxylase and familial pheochromocytoma genes: developmental culling and cancer. Cancer Cell 8: 155-167
22. Li M, Kim WY (2011) Two sides to every story: the HIF-dependent and HIF-independent functions of pVHL. J Cell Mol Med 15: 187-195
23. Lindeberg J, Usoskin D, Bengtsson H, Gustafsson A, Kylberg A, Söderström S, Ebendal T (2004) Transgenic expression of Cre recombinase from the tyrosine hydroxylase locus. Genesis 40: 67-73
24. López-Barneo J, Ortega-Sáenz P, Pardal R, Pascual A, Piruat JI (2008) Carotid body oxygen sensing. Eur Respir J 32: 1386-1398
25. Lopez-Barneo J, Pardal R, Ortega-Sáenz P (2001) Cellular mechanism of oxygen sensing. Annu Rev Physiol 63: 259-287
26. López-Jiménez E, Gómez-López G, Leandro-García LJ, Muñoz I, Schiavi F, Montero-Conde C, de Cubas AA, Ramires R, Landa I, Leskelä S et al (2010) Research resource: transcriptional profiling reveals different pseudohypoxic signatures in SDHB and VHL-related pheochromocytomas. Mol Endocrinol 24: 2382-2391
27. Macías D, Oya R, Saniger L, Martín F, Luque F (2009) A lentiviral vector that activates latent human immunodeficiency virus-1 proviruses by the overexpression of tat and that kills the infected cells. Hum Gene Ther 20: 1259-1268
28. Mack FA, Rathmell WK, Arsham AM, Gnarra J, Keith B, Simon MC (2003) Loss of pVHL is sufficient to cause HIF dysregulation in primary cells but does not promote tumor growth. Cancer Cell 3: 75-88
29. Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, Cockman ME, Wykoff CC, Pugh CW, Maher ER, Ratcliffe PJ (1999) The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399: 271-275
30. Mazure NM, Pouysségur J (2010) Hypoxia-induced autophagy: cell death or cell survival? Curr Opin Cell Biol 22: 177-180
31. McBryde FD, Abdala AP, Hendy EB, Pijacka W, Marvar P, Moraes DJA, Sobotka PA, Paton JFR (2013) The carotid body as a putative therapeutic target for the treatment of neurogenic hypertension. Nat Commun 4: 2395
32. Méndez-Ferrer S, Lucas D, Battista M, Frenette PS (2008) Haematopoietic stem cell release is regulated by circadian oscillations. Nature 452: 442-447
33. Muñoz-Bravo JL, Hidalgo-Figueroa M, Pascual A, López-Barneo J, Leal-Cerro A, Cano DA (2013) GDNF is required for neural colonization of the pancreas. Development 140: 3669-3679
34. Ortega-Sáenz P, Pardal R, Levitsky K, Villadiego J, Muñoz-Manchado AB, Durán R, Bonilla-Henao V, Arias-Mayenco I, Sobrino V, Ordóñez A et al (2013) Cellular properties and chemosensory responses of the human carotid body. J Physiol 591: 6157-6173
35. Pardal R, López-Barneo J (2002) Low glucose-sensing cells in the carotid body. Nat Neurosci 5: 197-198
36. Pardal R, Ortega-Sáenz P, Durán R, López-Barneo J (2007) Glia-like stem cells sustain physiologic neurogenesis in the adult mammalian carotid body. Cell 131: 364-377
37. Paton JFR, Ratcliffe L, Hering D, Wolf J, Sobotka PA, Narkiewicz K (2013) Revelations about carotid body function through its pathological role in resistant hypertension. Curr Hypertens Rep 15: 273-280
38. Perez IA, Keens TG (2013) Peripheral chemoreceptors in congenital central hypoventilation syndrome. Respir Physiol Neurobiol 185: 186-193
39. 2-sensitive glomus cell-stem cell synapse induces carotid body growth in chronic hypoxia. Cell 156: 291-303
40. Porzionato A, Macchi V, Stecco C, De Caro R (2013) The carotid body in Sudden Infant Death Syndrome. Respir Physiol Neurobiol 185: 194-201
41. Powell F, Milsom W, Mitchell G (1998) Time domains of the hypoxic ventilatory response. Respir Physiol 112: 123-134
42. Rotolo T, Smallwood PM, Williams J, Nathans J (2008) Genetically-directed, cell type-specific sparse labeling for the analysis of neuronal morphology. PLoS ONE 3: e4099
43. Schlisio S (2009) Neuronal apoptosis by prolyl hydroxylation: implication in nervous system tumours and the Warburg conundrum. J Cell Mol Med 13: 4104-4112
44. Schou L, Østergaard B, Rasmussen LS, Rydahl-Hansen S, Phanareth K (2012) Cognitive dysfunction in patients with chronic obstructive pulmonary disease-a systematic review. Respir Med 106: 1071-1081
45. Sutherland ER, Cherniack RM (2004) Management of chronic obstructive pulmonary disease. N Engl J Med 350: 2689-2697
46. Suzuki T, Kachi T (1995) Immunohistochemical studies on supporting cells in the adrenal medulla and pineal gland of adult rat, especially on S-100 protein, glial fibrillary acidic protein and vimentin. Kaibogaku Zasshi 70: 130-139
47. Timmers HJLM, Wieling W, Karemaker JM, Lenders JWM (2003) Denervation of carotid baro- and chemoreceptors in humans. J Physiol 553: 3-11
48. Wehrwein Ea, Basu R, Basu A, Curry TB, Rizza RA, Joyner MJ (2010) Hyperoxia blunts counterregulation during hypoglycaemia in humans: possible role for the carotid bodies? J Physiol 588: 4593-4601
49. Weir EK, López-Barneo J, Buckler KJ, Archer SL (2005) Acute oxygen-sensing mechanisms. N Engl J Med 353: 2042-2055
50. Young AP, Schlisio S, Minamishima YA, Zhang Q, Li L, Grisanzio C, Signoretti S, Kaelin WG (2008) VHL loss actuates a HIF-independent senescence programme mediated by Rb and p400. Nat Cell Biol 10: 361-369