Differential expressions and roles of hypoxia-inducible factor-1α, -2α and -3α in the rat carotid body during chronic and intermittent hypoxia

Histology and Histopathology

Volumn 23, Issue 3, 2008, Pages 271-280

  Lam, Siu Yin ^a   Tipoe, George L ^a   Liong, Emily C ^a   Fung, Man Lung ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Carotid body; Hypoxia inducible factor; Intermittent hypoxia; Sleep apnea

Indexed keywords

RATTUS;

EID: 84863989372     PISSN: 02133911     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (47)

1. Chen J., He L., Dinger B., Stensaas L. and Fidone S. (2002). Role of endothelin and endothelin A-type receptor in adaptation of the carotid body to chronic hypoxia. Am. J. Physiol. Lung. Cell. Mol. Physiol. 282, L1314-L1323.
2. Chen Y., Tipoe G. L., Liong E., Leung S., Lam S.Y., Iwase R., Tjong Y.W. and Fung M.L. (2002). Chronic hypoxia enhances endothelin-1-induced intracellular calcium elevation in rat carotid body chemoreceptors and up-regulates ETA receptor expression. Pflugers. Arch. 443, 565-573.
3. Cockman M.E., Masson N., Mole D.R., Jaakkola P., Chang G.W., Clifford S.C., Maher E.R., Pugh C.W., Ratcliffe P.J. and Maxwell P.H. (2000). Hypoxia inducible factor-alpha binding and ubiquitylation by the von Hippel-Lindau tumor suppressor protein. J. Biol. Chem. 275, 25733-25741.
4. Czyzyk-Krzeska M.F., Bayliss D.A., Lawson E.E. and Millhorn D.E. (1992). Regulation of tyrosine hydroxylase gene expression in the rat carotid body by hypoxia. J. Neurochem. 58, 1538-1546.
5. Czyzyk-Krzeska M.F., Furnari B.A., Lawson E.E. and Millhorn D.E. (1994). Hypoxia increases rate of transcription and stability of tyrosine hydroxylase mRNA in pheochromocytoma (PC12) cells. J. Biol. Chem. 269, 760-764.
6. Dhillon D.P., Barer G.R. and Walsh M. (1984). The enlarged carotid body of the chronically hypoxic and chronically hypoxic and hypercapnic rat: a morphometric analysis. Q. J. Exp. Physiol. 69, 301-317.
7. Di Giulio C., Bianchi G., Cacchio M., Artese L., Rapino C., Macri M.A. and Di Ilio C. (2005). Oxygen and life span: chronic hypoxia as a model for studying HIF-1alpha, VEGF and NOS during aging. Respir. Physiol. Neurobiol. 147, 31-38.
8. Ema M., Taya S., Yokotani N., Sogawa K., Matsuda Y. and Fujii-Kuriyama Y. (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.
9. Ferrara N., Houck K., Jakeman L. and Leung D.W. (1992). Molecular and biological properties of the vascular endothelial growth factor family of proteins. Endocr. Rev. 13, 18-32.
10. Fletcher E.C. (2001). Invited review: Physiological consequences of intermittent hypoxia: systemic blood pressure. J. Appl. Physiol. 90, 1600-1605.
11. Fung M.L. (2003). Hypoxia-inducible factor-1: a molecular hint of physiological changes in the carotid body during long-term hypoxemia? Curr. Drug. Targets. Cardiovasc. Haematol. Disord. 3, 254-259.
12. Fung M.L. and Tipoe G.L. (2003). Role of HIF-1 in physiological adaptation of the carotid body during chronic hypoxia. Adv. Exp. Med. Biol. 536, 593-601.
13. Gonzalez C., Almaraz L., Obeso A. and Rigual R. (1994). Carotid body chemoreceptors: from natural stimuli to sensory discharges. Physiol. Rev. 74, 829-898.
14. Heidbreder M., Frohlich F., Johren O., Dendorfer A., Qadri F. and Dominiak P. (2003). Hypoxia rapidly activates HIF-3alpha mRNA expression. FASEB J. 17, 1541-1543.
15. Iturriaga R. and Alcayaga J. (2004). Neurotransmission in the carotid body: transmitters and modulators between glomus cells and petrosal ganglion nerve terminals. Brain Res. Brain Res. Rev. 47, 46-53.
16. Iyer N.V., Kotch L.E., Agani F., Leung S.W., Laughner E., Wenger R.H., Gassmann M., Gearhart J.D., Lawler A.M., Yu A.Y. and Semenza G.L. (1998). Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1 alpha. Genes. Dev. 12, 149-162.
17. Kline D.D., Peng Y.J., Manalo D.J., Semenza G.L. and Prabhakar N.R. (2002). Defective carotid body function and impaired ventilatory responses to chronic hypoxia in mice partially deficient for hypoxia-inducible factor 1 alpha. Proc. Natl. Acad. Sci. USA 99, 821-826.
18. Lahiri S., Rozanov C. and Cherniack N.S. (2000). Altered structure and function of the carotid body at high altitude and associated chemoreflexes. High. Alt. Med. Biol. 1, 63-74.
19. Lahiri S., Roy A., Baby S.M., Hoshi T., Semenza G.L. and Prabhakar N.R. (2006). Oxygen sensing in the body. Prog. Biophys. Mol. Biol. 91, 249-286.
20. Lam S.Y., Liong E.C., Tipoe G.L. and Fung M.L. (2006). Expression of HIF-2alpha and HIF-3alpha in the rat carotid body in chronic hypoxia. Adv. Exp. Med. Biol. 580, 29-36.
21. Lam S.Y., Tipoe G.L., Liong E.C. and Fung M.L. (2006). Hypoxia-inducible factor (HIF)-1alpha and endothelin-1 expression in the rat carotid body during intermittent hypoxia. Adv. Exp. Med. Biol. 580, 21-27.
22. Maxwell P.H., Wiesener M.S., Chang G.W., Clifford S.C., Vaux E.C., Cockman M.E., Wykoff C.C., Pugh C.W., Maher E.R. and Ratcliffe P.J. (1999). The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature. 399, 271-275.
23. Neufeld G., Cohen T., Gengrinovitch S. and Poltorak Z. (1999). Vascular endothelial growth factor (VEGF) and its receptors. FASEB J. 13, 9-22.
24. Nurse C.A. (2005). Neurotransmission and neuromodulation in the chemosensory carotid body. Auton. Neurosci. 120, 1-9.
25. Ohh M., Park C.W., Ivan M., Hoffman M.A., Kim T.Y., Huang L.E., Pavletich N., Chau V. and Kaelin W.G. (2000). Ubiquitination of hypoxia-inducible factor requires direct binding to the beta-domain of the von Hippel-Lindau protein. Nat. Cell. Biol. 2, 423-427.
26. Peng Y.J., Overholt J.L., Kline D., Kumar G.K. and Prabhakar N.R. (2003). Induction of sensory long-term facilitation in the carotid body by intermittent hypoxia: implications for recurrent apneas. Proc. Natl. Acad. Sci. USA 100, 10073-10078.
27. Peng Y.J., Yuan G., Ramakrishnan D., Sharma S.D., Bosch-Marce M., Kumar G.K., Semenza G.L. and Prabhakar N.R. (2006). Heterozygous HIF-1alpha deficiency impairs carotid body-mediated systemic responses and reactive oxygen species generation in mice exposed to intermittent hypoxia. J. Physiol. 577, 705-716.
28. Prabhakar N.R. (2000). Oxygen sensing by the carotid body chemoreceptors. J. Appl. Physiol. 88, 2287-2295.
29. Prabhakar N.R. (2001). Oxygen sensing during intermittent hypoxia: cellular and molecular mechanisms. J. Appl. Physiol. 90, 1986-1994.
30. Prabhakar N.R. and Jacono F.J. (2005) Cellular and molecular mechanisms associated with carotid body adaptations to chronic hypoxia. High. Alt. Med. Biol. 6, 112-120.
31. Prabhakar N.R., Fields R.D., Baker T. and Fletcher E.C. (2001). Intermittent hypoxia: cell to system. Am. J. Physiol. Lung. Cell. Mol. Physiol. 281, L524-L528.
32. Rey S., del Rio R., Alcayaga J. and Iturriaga R. (2004). Chronic intermittent hypoxia enhances cat chemosensory and ventilatory responses to hypoxia. J. Physiol. 560, 577-586.
33. Rey S., del Rio R. and Iturriaga R. (2006). Contribution of endothelin-1 to the enhanced carotid body chemosensory responses induced by chronic intermittent hypoxia. Brain. Res. 1086, 152-159.
34. Roy A., Volgin D.V., Baby S.M., Mokashi A., Kubin L. and Lahiri S (2004). Activation of HIF-1alpha mRNA by hypoxia and iron chelator in isolated rat carotid body. Neurosci. Lett. 363, 229-232.
35. Schnell P.O., Ignacak M.L., Bauer A.L., Striet J.B., Paulding W.R. and Czyzyk-Krzeska M.F. (2003). Regulation of tyrosine hydroxylase promoter activity by the von Hippel-Lindau tumor suppressor protein and hypoxia-inducible transcription factors. J. Neurochem. 85, 483-491.
36. Semenza G.L. (2000). HIF-1: mediator of physiological and pathophysiological responses to hypoxia. J. Appl. Physiol. 88, 1474-1480.
37. Semenza G.L. (2004). O2-regulated gene expression: transcriptional control of cardiorespiratory physiology by HIF-1. J. Appl. Physiol. 96, 1173-1177; discussion 1170-1172.
38. Semenza G.L. (2004). Hydroxylation of HIF-1: oxygen sensing at the molecular level. Physiology (Bethesda) 19, 176-182.
39. Tanimoto K., Makino Y., Pereira T. and Poellinger L. (2000). Mechanism of regulation of the hypoxia-inducible factor-1 alpha by the von Hippel-Lindau tumor suppressor protein. EMBO J. 19, 4298-4309.
40. Tian H., Hammer R.E., Matsumoto A.M., Russell D.W. and McKnight S.L. (1998). The hypoxia-responsive transcription factor EPAS1 is essential for catecholamine homeostasis and protection against heart failure during embryonic development. Genes. Dev. 12, 3320-3324.
41. Tipoe G.L. and Fung M.L. (2003). Expression of HIF-1alpha, VEGF and VEGF receptors in the carotid body of chronically hypoxic rat. Respir. Physiol. Neurobiol. 138, 143-154.
42. Tipoe G.L., White F.H. and Pritchett C.J. (1992). A morphometric study of histological variations during cellular differentiation of normal human colorectal epithelium. J. Anat. 181 (Pt 2), 189-197.
43. Tipoe G.L., Lau T.Y., Nanji A.A. and Fung M.L. (2006). Expression and functions of vasoactive substances regulated by hypoxia-inducible factor-1 in chronic hypoxemia. Cardiovasc. Hematol. Agents. Med. Chem. 4, 199-218.
44. Wang G.L., Jiang B.H., Rue E.A. and Semenza G.L. (1995). Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc. Natl. Acad. Sci. USA 92, 5510-5514.
45. Wang Z.Y. and Bisgard G.E. (2002). Chronic hypoxia-induced morphological and neurochemical changes in the carotid body. Microsc. Res. Tech. 59, 168-177.
46. Wiesener M.S., Turley H., Allen W.E., Willam C., Eckardt K.U., Talks K.L., Wood S.M., Gatter K.C., Harris A.L., Pugh C.W., Ratcliffe P.J. and Maxwell P.H. (1998). Induction of endothelial PAS domain protein-1 by hypoxia: characterization and comparison with hypoxia-inducible factor-1alpha. Blood 92, 2260-2268.
47. 2+/calmodulin kinase-dependent activation of hypoxia inducible factor 1 transcriptional activity in cells subjected to intermittent hypoxia. J. Biol. Chem. 280, 4321-4328.