Inherent variations in co-h2s-mediated carotid body O 2 sensing mediate hypertension and pulmonary edema

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 3, 2014, Pages 1174-1179

  Peng, Ying Jie ^a   Makarenko, Vladislav V ^a   Nanduri, Jayasri ^a   Vasavda, Chirag ^a,b   Raghuraman, Gayatri ^a   Yuan, Guoxiang ^a   Gadalla, Moataz M ^b   Kumar, Ganesh K ^a   Snyder, Solomon H ^b   Prabhakar, Nanduri R ^a  

^a University of Chicago   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cystathionine lyase; Gasotransmitters; High altitude hypoxia; Sympathetic tone

Indexed keywords

CARBON MONOXIDE; HEME OXYGENASE 2; HYDROGEN SULFIDE;

ADAPTATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CAROTID BODY; COMPARATIVE STUDY; CONTROLLED STUDY; HYPERSENSITIVITY; HYPERTENSION; HYPOBARISM; HYPOXIA; INFANT; LUNG EDEMA; MALE; NONHUMAN; OXYGEN SENSING; PRIORITY JOURNAL; RAT;

CYSTATHIONINE-Γ-LYASE; GASOTRANSMITTERS; HIGH-ALTITUDE HYPOXIA; SYMPATHETIC TONE;

ANIMALS; ANOXIA; BODY WEIGHT; CARBON MONOXIDE; CAROTID BODY; CATECHOLAMINES; CYSTATHIONINE GAMMA-LYASE; HEME OXYGENASE (DECYCLIZING); HYDROGEN SULFIDE; HYPERTENSION; IMMUNOHISTOCHEMISTRY; MALE; OXYGEN; OXYGEN CONSUMPTION; PULMONARY EDEMA; RATS; RATS, SPRAGUE-DAWLEY; REPRODUCIBILITY OF RESULTS; RESPIRATION; SIGNAL TRANSDUCTION; SPECIES SPECIFICITY; SPLANCHNIC NERVES;

EID: 84892937567     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1322172111     Document Type: Article

References (36)

1. Weil JV (2003) Variation in human ventilatory control-genetic influence on the hypoxic ventilatory response. Respir Physiol Neurobiol 135(2-3):239-246.
2. Dempsey JA, Forster HV (1982) Mediation of Ventilatory Adaptations. Physiol Rev 62(1):262-346.
3. Hackett PH, Roach RC, Schoene RB, Harrison GL, Mills WJ, Jr. (1988) Abnormal control of ventilation in high-altitude pulmonary edema. J Appl Physiol (1985) 64(3):1268-1272.
4. Matsuzawa Y, et al. (1989) Blunted hypoxic ventilatory drive in subjects susceptible to high-altitude pulmonary edema. J Appl Physiol (1985) 66(3):1152-1157.
5. Hohenhaus E, Paul A, McCullough RE, Kücherer H, Bärtsch P (1995) Ventilatory and pulmonary vascular response to hypoxia and susceptibility to high altitude pulmonary oedema. Eur Respir J 8(11):1825-1833.
6. Trzebski A (1992) Arterial chemoreceptor reflex and hypertension. Hypertension 19(6 Pt 1):562-566.
7. Tan ZY, et al. (2010) Chemoreceptor hypersensitivity, sympathetic excitation, and overexpression of ASIC and TASK channels before the onset of hypertension in SHR. Circ Res 106(3):536-545.
8. Hodges MR, Forster HV, Papanek PE, Dwinell MR, Hogan GE (2002) Ventilatory phenotypes among four strains of adult rats. J Appl Physiol (1985) 93(3):974-983.
9. Strohl KP, et al. (1997) Ventilation and metabolism among rat strains. J Appl Physiol (1985) 82(1):317-323.
10. Tankersley CG, Fitzgerald RS, Kleeberger SR (1994) Differential control of ventilation among inbred strains of mice. Am J Physiol 267(5 Pt 2):R1371-R1377.
11. Hayward LF, Castellanos M, Noah C (2012) Cardiorespiratory variability following repeat acute hypoxia in the conscious SHR versus two normotensive rat strains. Auton Neurosci 171(1-2):58-65.
12. Kumar P, Prabhakar NR (2012) Peripheral chemoreceptors: Function and plasticity of the carotid body. Compr Physiol 2(1):141-219.
13. Prabhakar NR (2013) Sensing hypoxia: Physiology, genetics and epigenetics. J Physiol 591(Pt 9):2245-2257.
14. Li Q, et al. (2010) A crucial role for hydrogen sulfide in oxygen sensing via modulating large conductance calcium-activated potassium channels. Antioxid Redox Signal 12(10):1179-1189.
15. Makarenko VV, et al. (2012) Endogenous H2S is required for hypoxic sensing by carotid body glomus cells. Am J Physiol Cell Physiol 303(9):C916-C923.
16. Peng YJ, et al. (2010) H2S mediates O2 sensing in the carotid body. Proc Natl Acad Sci USA 107(23):10719-10724.
17. Telezhkin V, et al. (2010) Mechanism of inhibition by hydrogen sulfide of native and recombinant BKCa channels. Respir Physiol Neurobiol 172(3):169-178.
18. Nurse CA, Fearon IM (2002) Carotid body chemoreceptors in dissociated cell culture. Microsc Res Tech 59(3):249-255.
19. Abeles RH, Walsh CT (1973) Acetylenic enzyme inactivators. Inactivation of gammacystathionase, in vitro and in vivo, by propargylglycine. J Am Chem Soc 95(18):6124-6125.
20. Asimakopoulou A, et al. (2013) Selectivity of commonly used pharmacological inhibitors for cystathionine β synthase (CBS) and cystathionine γ lyase (CSE). Br J Pharmacol 169(4):922-932.
21. Washtien W, Abeles RH (1977) Mechanism of inactivation of gamma-cystathionase by the acetylenic substrate analogue propargylglycine. Biochemistry 16(11):2485-2491.
22. Prabhakar NR, Dinerman JL, Agani FH, Snyder SH (1995) Carbon monoxide: A role in carotid body chemoreception. Proc Natl Acad Sci USA 92(6):1994-1997.
23. Maines MD, Trakshel GM, Kutty RK (1986) Characterization of two constitutive forms of rat liver microsomal heme oxygenase. Only one molecular species of the enzyme is inducible. J Biol Chem 261(1):411-419.
24. Snyder SH, Barañano DE (2001) Heme oxygenase: A font of multiple messengers. Neuropsychopharmacology 25(3):294-298.
25. Eadie GS (1942) The inhibition of cholinesterase by physostigmine and prostigmine. J Biol Chem 146:85-93.
26. Hofstee BH (1959) Non-inverted versus inverted plots in enzyme kinetics. Nature 184:1296-1298.
27. Roux JC, Brismar H, Aperia A, Lagercrantz H (2005) Developmental changes in HIF transcription factor in carotid body: Relevance for O2 sensing by chemoreceptors. Pediatr Res 58(1):53-57.
28. Yang G, et al. (2008) H2S as a physiologic vasorelaxant: Hypertension in mice with deletion of cystathionine gamma-lyase. Science 322(5901):587-590.
29. Mustafa AK, Gadalla MM, Snyder SH (2009) Signaling by gasotransmitters. Sci Signal 2(68):re2.
30. Scherrer U, et al. (1999) High-altitude pulmonary edema: From exaggerated pulmonary hypertension to a defect in transepithelial sodium transport. Adv Exp Med Biol 474:93-107.
31. Abdala AP, et al. (2012) Hypertension is critically dependent on the carotid body input in the spontaneously hypertensive rat. J Physiol 590(Pt 17):4269-4277.
32. Paton JF, et al. (2013) The carotid body as a therapeutic target for the treatment of sympathetically mediated diseases. Hypertension 61(1):5-13.
33. Peng YJ, et al. (2006) Heterozygous HIF-1alpha deficiency impairs carotid bodymediated systemic responses and reactive oxygen species generation in mice exposed to intermittent hypoxia. J Physiol 577(Pt 2):705-716.
34. Peng YJ, et al. (2012) Endothelin-1 mediates attenuated carotid baroreceptor activity by intermittent hypoxia. J Appl Physiol (1985) 112(1):187-196.
35. Lambert JL, Wiens RE (1974) Induced colorimetric method for carbon monoxide. Anal Chem 46(7):929-930.
36. Ryter S, Kvam E, Tyrrell RM (1999) Heme oxygenase activity determination by highperformance liquid chromatography. Methods Enzymol 300:322-336.