Intermittent hypoxia-mediated plasticity of acute O2 sensing requires altered red-ox regulation by HIF-1 and HIF-2

Annals of the New York Academy of Sciences

Volumn 1177, Issue , 2009, Pages 162-168

  Prabhakar, Nanduri R ^a   Kumar, Ganesh K ^a   Nanduri, Jayasri ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Adrenal chromaffin cells; Blood pressure; Breathing; Carotid body (CB); Catecholamines (CAs); HIFs; NADPH oxidase; O2 sensing; Reactive oxygen species (ROS); Superoxide dismutases

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1; REACTIVE OXYGEN METABOLITE;

ADRENAL FUNCTION; ADRENAL MEDULLA; CAROTID BODY; CHROMAFFIN CELL; CONFERENCE PAPER; NONHUMAN; OXIDATIVE STRESS; OXYGEN SENSING; PLASTICITY; TRANSCRIPTION REGULATION;

RATTUS;

EID: 70350379191     PISSN: 00778923     EISSN: 17496632     Source Type: Book Series    
DOI: 10.1111/j.1749-6632.2009.05034.x     Document Type: Conference Paper

References (37)

1. Prabhakar,N.R. 2006.O2 sensing at the mammalian CB: why multiple O2 sensors and multiple transmitters? Exp. Physiol. 91: 17-23.
2. Blanco, C.E., G.S. Dawes, M.A. Hanson &H.B.Mc- Cooke. 1984. The response to hypoxia of arterial chemoreceptors in fetal sheep and new-born lambs. J. Physiol. 351: 25-37.
3. Donnelly, D.F. 2000. Developmental aspects of oxygen sensing by the CB. J. Appl. Physiol. 88: 2296-2301.
4. Carroll, J.L. 2003. Developmental plasticity in respiratory control. J. Appl. Physiol. 94: 375-389.
5. Peng, Y.J., J. Rennison & N.R. Prabhakar. 2004. Intermittent hypoxia augments CB and ventilatory response to hypoxia in neonatal rat pups. J. Appl. Physiol. 97: 2020-2025.
6. Pawar, A., Y.J. Peng, F.J. Jacono & N.R. Prabhakar. 2008. Comparative analysis of neonatal and adult rat CB responses to chronic intermittent hypoxia. J. Appl. Physiol. 104: 1287-1294.
7. Nieto, F.J., T.B. Young, B.K. Lind, et al. 2000. Association of sleep-disordered breathing, sleep apnea, and hypertension in a large community-based study, Sleep Heart Health Study. JAMA 283: 1829-1836.
8. Poets, C.F.,M.P. Samuels & D.P. Southall. 1994. Epidemiology and pathophysiology of apnoea of prematurity. Biol. Neonate 65: 211-219.
9. Prabhakar, N.R., T.E. Dick, J. Nanduri & G.K. Kumar. 2007. Systemic, cellular and molecular analysis of chemoreflex-mediated sympathoexcitation by chronic intermittent hypoxia. Exp. Physiol. 92: 39-44.
10. Peng, Y.J. & N.R. Prabhakar. 2004. Effect of two paradigms of chronic intermittent hypoxia on CB sensory activity. J. Appl. Physiol. 96: 1236-1242.
11. Rey, S., R.D. Rio & R. Iturriaga. 2006. Contribution of endothelin-1 to the enhanced CB chemosensory responses induced by chronic intermittent hypoxia. Brain Res. 1086:: 152-159.
12. Peng, Y.J., G. Yuan, D. Ramakrishnan, et al. 2006. Heterozygous HIF-1alpha deficiency impairs CBmediated systemic responses and reactive oxygen species generation in mice exposed to intermittent hypoxia. J. Physiol. 577: 705-716.
13. Peng, Y.J., J.L. Overholt, D.D. Kline, et al. 2003. Induction of sensory long-term facilitation in the CB by intermittent hypoxia: implications for recurrent apneas. Proc. Natl. Acad. Sci. USA 100: 10073-10078.
14. Peng, Y.J. & N.R. Prabhakar. 2003. Reactive oxygen species in the plasticity of respiratory behavior elicited by chronic intermittent hypoxia. J. Appl. Physiol. 94: 2342-2349.
15. Al-Matary, A., I. Kutbi, M. Qurashi, et al. 2004. Increased peripheral chemoreceptor activity may be critical in destabilizing breathing in neonates. Semin. Perinatol. 28: 264-272.
16. Nock, M.L., J.M. Difiore, M.K. Arko & R.J. Martin. 2004. Relationship of the ventilatory response to hypoxia with neonatal apnea in preterm infants. J. Pediatr. 144: 291-295.
17. Julien, C., A. Bairam & V. Joseph. 2008. Chronic intermittent hypoxia reduces ventilatory long-term facilitation and enhances apnea frequency in newborn rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 294: R1356-R1366.
18. Kara, T., K. Narkiewicz & V.K. Somers. 2003. Chemoreflexes-physiology and clinical implications. Acta Physiol. Scand. 177: 377-384.
19. Prabhakar, N.R. 2001. Oxygen sensing during intermittent hypoxia: cellular and molecularmechanisms. J. Appl. Physiol. 90: 1986-1994.
20. Lesske, J., E.C. Fletcher, G. Bao & T. Unger. 1997. Hypertension caused by chronic intermittent hypoxia-influence of chemoreceptors and sympathetic nervous system. J. Hypertens. 12: 1593-1603.
21. Seidler, F.J. & T.A. Slotkin. 1986. Ontogeny of adrenomedullary responses to hypoxia and hypoglycemia: role of splanchnic innervation. Brain Res. Bull. 16: 11-14.
22. Kumar, G.K., V. Rai, S.D. Sharma, et al. 2006. Chronic intermittent hypoxia induces hypoxiaevoked catecholamine efflux in adult rat adrenal medulla via oxidative stress. J. Physiol. 575: 229-239.
23. Souvannakitti, D., G.K. Kumar, A. Fox & N.R. Prabhakar. 2009. Neonatal intermittent hypoxia leads to long-lasting facilitation of acute hypoxia-evoked catecholamine secretion from rat chromaffin cells. J. Neurophysiol. Apr 1. [Epub ahead of print.]
24. Bao, G., N. Metreveli, R. Li, et al. 1997. Blood pressure response to chronic episodic hypoxia: role of the sympathetic nervous system. J. Appl. Physiol. 83: 95-101.
25. Nanduri, J., G. Yuan, G.K. Kumar, et al. 2008. Transcriptional responses to intermittent hypoxia. Respir. Physiol. Neurobiol. 164: 277-281.
26. Semenza, G.L. 2000. HIF-1: mediator of physiological and pathophysiological responses to hypoxia. J. Appl. Physiol. 88: 1474-1480.
27. Tian, H., S.L. McKnight & D.W. Russell. 1997. Endothelial PAS domain protein 1 (EPAS1), a transcription factor selectively expressed in endothelial cells. Genes Dev. 11: 72-82.
28. Ema, M. et al. 1997. A novel bHLH-PAS factor with close sequence similarity to hypoxia-inducible factor 1alpha regulates the VEGF expression and is potentially involved in lung and vascular development. Proc. Natl. Acad. Sci. USA 94: 4273-4278.
29. Holmquist-Mengelbier, L. et al. 2006. Recruitment of HIF-1alpha and HIF-2alpha to common target genes is differentially regulated in neuroblastoma: HIF-2alpha promotes an aggressive phenotype. Cancer Cell 10: 413-423.
30. Nanduri, J., N. Wang, G. Yuan, et al. 2009. Intermittent hypoxia degrades HIF-2alpha via calpains resulting in oxidative stress: implications for recurrent apnea-induced morbidities. Proc. Natl. Acad. Sci. USA 106: 1199-1204.
31. Yuan, G., J. Nanduri, S. Khan, et al. 2008. Induction of HIF-1alpha expression by intermittent hypoxia: involvement of NADPH oxidase, Ca2 +signaling, prolyl hydroxylases, and mTOR. J. Cell Physiol. 217: 674-685.
32. Yuan, G., J. Nanduri, C.R. Bhasker, et al. 2005. Ca2+/calmodulin kinase-dependent activation of hypoxia inducible factor 1 transcriptional activity in cells subjected to intermittent hypoxia. J. Biol. Chem. 280: 4321-4328.
33. Zhan, G., F. Serrano, P. Fenik, et al. 2005. NADPH oxidase mediates hypersomnolence and brain oxidative injury in a murine model of sleep apnea. Am. J. Respir. Crit. Care Med. 172: 921-929.
34. Peng, Y.J., J. Nanduri, G. Yuan, et al. 2009. NADPH oxidase is required for the sensory plasticity of the CB by chronic intermittent hypoxia. J. Neurosci. 29: 4903-4910.
35. Scortegagna, M. et al. 2003. Multiple organ pathology, metabolic abnormalities and impaired homeostasis of reactive oxygen species in Epas1-/- mice. Nat. Genet. 35: 331-340.
36. Pawar, A., J. Nanduri, G. Yuan, et al. 2009. Reactive oxygen species-dependent endothelin signaling is required for augmented hypoxic sensory response of the neonatal CB by intermittent hypoxia. Am. J. Physiol. Regul. Integr. Comp. Physiol. 296: R735-R742.
37. Kuri, B.A., S.A. Khan, S.A. Chan, et al. 2007. Increased secretory capacity of mouse adrenal chromaffin cells by chronic intermittent hypoxia: involvement of protein kinase C. J. Physiol. 584: 313-319.