Glucose sensing by carotid body glomus cells: Potential implications in disease

Frontiers in Physiology

Volumn 5, Issue OCT, 2014, Pages

  Gao, Lin ^a,b   Ortega Sáenz , Patricia ^a,b,c   García Fernández , María ^c   González Rodríguez , Patricia ^a,b   Caballero Eraso , Candela ^a   López Barneo , José ^a,b,c  

^a HOSPITAL UNIVERSITARIO VIRGEN DEL ROCÍO   (Spain)

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

^c UNIVERSITY OF SEVILLE   (Spain)

Author keywords

Carotid body; Chronic hypoxia; Diabetes; Glucose sensing; Hypoglycemia; Intermittent hypoxia; O2 sensing; Sleep apnea

Indexed keywords

GLUCOSE; INSULIN;

CARDIORESPIRATORY DISEASE; CAROTID BODY; CHEMORECEPTOR; DIABETES MELLITUS; DRUG TARGETING; GLUCOSE METABOLISM; GLUCOSE SENSING; GLUCOSE TRANSPORT; HEART DISEASE; HUMAN; HYPOXIA; METABOLIC DISORDER; NONHUMAN; OXYGEN SENSING; PATHOPHYSIOLOGY; RESPIRATORY TRACT DISEASE; REVIEW; SLEEP DISORDERED BREATHING;

EID: 84908361272     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2014.00398     Document Type: Review

References (61)

1. Abboud, F., and Kumar, R. (2014). Obstructive sleep apnea and insight into mechanisms of sympathetic overactivity. J. Clin. Invest. 124, 1454-1457. doi: 10.1172/JCI70420
2. Alvarez-Buylla, R., and De Alvarez-Buylla, E. R. (1988). Carotid sinus receptors participate in glucose homeostasis. Respir. Physiol. 72, 347-359. doi: 10.1016/0034-5687(88)90093-X
3. Alvarez-Buylla, R., and Roces de Alvarez-Buylla, E. (1994). Changes in blood glucose concentration in the carotid body-sinus modify brain glucose retention. Brain Res. 654, 167-170. doi: 10.1016/0006-8993(94)91585-7
4. Biggers, D. W., Myers, S. R., Neal, D., Stinson, R., Cooper, N. B., Jaspan, J. B., et al. (1989). Role of brain in counterregulation of insulin-induced hypoglycemia in dogs. Diabetes 38, 7-16. doi: 10.2337/diab.38.1.7
5. Bin-Jaliah, I., Maskell, P. D., and Kumar, P. (2004). Indirect sensing of insulin-induced hypoglycaemia by the carotid body in the rat. J. Physiol. 556, 255-266. doi: 10.1113/jphysiol.2003.058321
6. Buckler, K. J., and Turner, P. J. (2013). Oxygen sensitivity of mitochondrial function in rat arterial chemoreceptor cells. J. Physiol. 591, 3549-3563. doi: 10.1113/jphysiol.2013.257741
7. + channels mediate inhibition of orexin neurons by glucose. Neuron 50, 711-722. doi: 10.1016/j.neuron.2006.04.032
8. Calabresi, P., Ascone, C. M., Centonze, D., Pisani, A., Sancesario, G., D'Angelo, V., et al. (1997). Opposite membrane potential changes induced by glucose deprivation in striatal spiny neurons and in large aspiny interneurons. J. Neurosci. 17, 1940-1949.
9. Cane, P., Artal, R., and Bergman, R. N. (1986). Putative hypothalamic glucoreceptors play no essential role in the response to moderate hypoglycemia. Diabetes 35, 268-277. doi: 10.2337/diab.35.3.268
10. + conductance in rat carotid body type I cells. Neuroreport 12, 1421-1425. doi: 10.1097/00001756-200105250-00025
11. Clarke, J. A., Daly Mde, B., Ead, H. W., and Hennessy, E. M. (1999). The carotid body of the spontaneous insulin-dependent diabetic rat. Braz. J. Med. Biol. Res. 32, 85-91. doi: 10.1590/S0100-879X1999000100013
12. Cramer, J. A., Wiggins, R. H., Fudim, M., Engelman, Z. J., Sobotka, P. A., and Shah, L. M. (2014). Carotid body size on CTA: correlation with comorbidities. Clin. Radiol. 69, e33-e36. doi: 10.1016/j.crad.2013.08.016
13. Cutler, M. J., Swift, N. M., Keller, D. M., Wasmund, W. L., and Smith, M. L. (2004). Hypoxia-mediated prolonged elevation of sympathetic nerve activity after periods of intermittent hypoxic apnea. J. Appl. Physiol. (1985) 96, 754-761. doi: 10.1152/japplphysiol.00506.2003
14. Dahan, A., Nieuwenhuijs, D., and Teppema, L. (2007). Plasticity of central chemoreceptors: effect of bilateral carotid body resection on central CO2 sensitivity. PLoS Med. 4:e239. doi: 10.1371/journal.pmed.0040239
15. Dunn-Meynell, A. A., Routh, V. H., Kang, L., Gaspers, L., and Levin, B. E. (2002). Glucokinase is the likely mediator of glucosensing in both glucose-excited and glucose-inhibited central neurons. Diabetes 51, 2056-2065. doi: 10.2337/diabetes.51.7.2056
16. Fitzgerald, R. S., Shirahata, M., Chang, I., and Kostuk, E. (2009). The impact of hypoxia and low glucose on the release of acetylcholine and ATP from the incubated cat carotid body. Brain Res. 1270, 39-44. doi: 10.1016/j.brainres.2009.02.078
17. Gallego-Martin, T., Fernandez-Martinez, S., Rigual, R., Obeso, A., and Gonzalez, C. (2012). Effects of low glucose on carotid body chemoreceptor cell activity studied in cultures of intact organs and in dissociated cells. Am. J. Physiol. Cell Physiol. 302, C1128-C1140. doi: 10.1152/ajpcell.00196.2011
18. Garcia-Fernandez, M., Ortega-Saenz, P., Castellano, A., and Lopez-Barneo, J. (2007). Mechanisms of low-glucose sensitivity in carotid body glomus cells. Diabetes 56, 2893-2900. doi: 10.2337/db07-0122
19. Gonzalez-Martin, M. C., Vega-Agapito, M. V., Conde, S. V., Castaneda, J., Bustamante, R., Olea, E., et al. (2011). Carotid body function and ventilatory responses in intermittent hypoxia. Evidence for anomalous brainstem integration of arterial chemoreceptor input. J. Cell. Physiol. 226, 1961-1969. doi: 10.1002/jcp.22528
20. Hamilton-Wessler, M., Bergman, R. N., Halter, J. B., Watanabe, R. M., and Donovan, C. M. (1994). The role of liver glucosensors in the integrated sympathetic response induced by deep hypoglycemia in dogs. Diabetes 43, 1052-1060. doi: 10.2337/diab.43.8.1052
21. Hevener, A. L., Bergman, R. N., and Donovan, C. M. (1997). Novel glucosensor for hypoglycemic detection localized to the portal vein. Diabetes 46, 1521-1525. doi: 10.2337/diab.46.9.1521
22. Iiyori, N., Alonso, L. C., Li, J., Sanders, M. H., Garcia-Ocana, A., O'Doherty, R. M., et al. (2007). Intermittent hypoxia causes insulin resistance in lean mice independent of autonomic activity. Am. J. Respir. Crit. Care Med. 175, 851-857. doi: 10.1164/rccm.200610-1527OC
23. Koyama, Y., Coker, R. H., Denny, J. C., Lacy, D. B., Jabbour, K., Williams, P. E., et al. (2001). Role of carotid bodies in control of the neuroendocrine response to exercise. Am. J. Physiol. Endocrinol. Metab. 281, E742-E748.
24. Koyama, Y., Coker, R. H., Stone, E. E., Lacy, D. B., Jabbour, K., Williams, P. E., et al. (2000). Evidence that carotid bodies play an important role in glucoregulation in vivo. Diabetes 49, 1434-1442. doi: 10.2337/diabetes.49.9.1434
25. Kumar, P., and Prabhakar, N. R. (2012). Peripheral chemoreceptors: function and plasticity of the carotid body. Compr. Physiol. 2, 141-219. doi: 10.1002/cphy.c100069
26. Larsen, J. J., Hansen, J. M., Olsen, N. V., Galbo, H., and Dela, F. (1997). The effect of altitude hypoxia on glucose homeostasis in men. J. Physiol. 504(Pt 1), 241-249. doi: 10.1111/j.1469-7793.1997.241bf.x
27. Levin, B. E., Routh, V. H., Kang, L., Sanders, N. M., and Dunn-Meynell, A. A. (2004). Neuronal glucosensing: what do we know after 50 years? Diabetes 53, 2521-2528. doi: 10.2337/diabetes.53.10.2521
28. Limberg, J. K., Curry, T. B., Prabhakar, N. R., and Joyner, M. J. (2014). Is insulin the new intermittent hypoxia? Med. Hypotheses 82, 730-735. doi: 10.1016/j.mehy.2014.03.014
29. Livermore, S., Piskuric, N. A., Salman, S., and Nurse, C. A. (2012). Developmental regulation of glucosensing in rat adrenomedullary chromaffin cells: potential role of the K(ATP) channel. Adv. Exp. Med. Biol. 758, 191-198. doi: 10.1007/978-94-007-4584-1_27
30. Lopez-Barneo, J., Ortega-Saenz, P., Pardal, R., Pascual, A., and Piruat, J. I. (2008). Carotid body oxygen sensing. Eur. Respir. J. 32, 1386-1398. doi: 10.1183/09031936.00056408
31. 2+] in oxygen-sensing tissues. Respir. Physiol. 115, 215-227. doi: 10.1016/S0034-5687(99)00016-X
32. Lopez-Barneo, J., Pardal, R., and Ortega-Saenz, P. (2001). Cellular mechanism of oxygen sensing. Annu. Rev. Physiol. 63, 259-287. doi: 10.1146/annurev.physiol.63.1.259
33. McBryde, F. D., Abdala, A. P., Hendy, E. B., Pijacka, W., Marvar, P., Moraes, D. J., et al. (2013). The carotid body as a putative therapeutic target for the treatment of neurogenic hypertension. Nat. Commun. 4:2395. doi: 10.1038/ncomms3395
34. Minguez-Castellanos, A., Escamilla-Sevilla, F., Hotton, G. R., Toledo-Aral, J. J., Ortega-Moreno, A., Mendez-Ferrer, S., et al. (2007). Carotid body autotransplantation in Parkinson disease: a clinical and positron emission tomography study. J. Neurol. Neurosurg. Psychiatr. 78, 825-831. doi: 10.1136/jnnp.2006.106021
35. Nair, S., Gupta, A., Fudim, M., Robinson, C., Ravi, V., Hurtado-Rua, S., et al. (2013). CT angiography in the detection of carotid body enlargement in patients with hypertension and heart failure. Neuroradiology 55, 1319-1322. doi: 10.1007/s00234-013-1273-3
36. Nimbkar, N. V., and Lateef, F. (2005). Carotid body dysfunction: the possible etiology of non-insulin dependent diabetes mellitus and essential hypertension. Med. Hypotheses 65, 1067-1075. doi: 10.1016/j.mehy.2005.06.023
37. Ortega-Saenz, P., Pardal, R., Garcia-Fernandez, M., and Lopez-Barneo, J. (2003). Rotenone selectively occludes sensitivity to hypoxia in rat carotid body glomus cells. J. Physiol. 548, 789-800. doi: 10.1113/jphysiol.2003.039693
38. Ortega-Saenz, P., Pardal, R., Levitsky, K., Villadiego, J., Munoz-Manchado, A. B., Duran, R., et al. (2013). Cellular properties and chemosensory responses of the human carotid body. J. Physiol. 591, 6157-6173. doi: 10.1113/jphysiol.2013.263657
39. Ortiz, F. C., Del Rio, R., Ebensperger, G., Reyes, V. R., Alcayaga, J., Varas, R., et al. (2013). Inhibition of rat carotid body glomus cells TASK-like channels by acute hypoxia is enhanced by chronic intermittent hypoxia. Respir. Physiol. Neurobiol. 185, 600-607. doi: 10.1016/j.resp.2012.11.015
40. Pae, E. K., Ahuja, B., Kim, M., and Kim, G. (2013). Impaired glucose homeostasis after a transient intermittent hypoxic exposure in neonatal rats. Biochem. Biophys. Res. Commun. 441, 637-642. doi: 10.1016/j.bbrc.2013.10.102
41. Pardal, R., and Lopez-Barneo, J. (2002a). Carotid body thin slices: responses of glomus cells to hypoxia and K(+)-channel blockers. Respir. Physiol. Neurobiol. 132, 69-79. doi: 10.1016/S1569-9048(02)00050-2
42. Pardal, R., and Lopez-Barneo, J. (2002b). Low glucose-sensing cells in the carotid body. Nat. Neurosci. 5, 197-198. doi: 10.1038/nn812
43. Pardal, R., Ortega-Saenz, P., Duran, R., and Lopez-Barneo, J. (2007). Glia-like stem cells sustain physiologic neurogenesis in the adult mammalian carotid body. Cell 131, 364-377. doi: 10.1016/j.cell.2007.07.043
44. Paton, J. F., Sobotka, P. A., Fudim, M., Engelman, Z. J., Hart, E. C., McBryde, F. D., et al. (2013). The carotid body as a therapeutic target for the treatment of sympathetically mediated diseases. Hypertension 61, 5-13. doi: 10.1161/HYPERTENSIONAHA.111.00064
45. 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. U.S.A. 100, 10073-10078. doi: 10.1073/pnas.1734109100
46. Peng, Y. J., Rennison, J., and Prabhakar, N. R. (2004). Intermittent hypoxia augments carotid body and ventilatory response to hypoxia in neonatal rat pups. J. Appl. Physiol. (1985) 97, 2020-2025. doi: 10.1152/japplphysiol.00876.2003
47. Platero-Luengo, A., Gonzalez-Granero, S., Duran, R., Diaz-Castro, B., Piruat, J. I., Garcia-Verdugo, J. M., et al. (2014). An O2-sensitive glomus cell-stem cell synapse induces carotid body growth in chronic hypoxia. Cell 156, 291-303. doi: 10.1016/j.cell.2013.12.013
48. Polak, J., Shimoda, L. A., Drager, L. F., Undem, C., McHugh, H., Polotsky, V. Y., et al. (2013). Intermittent hypoxia impairs glucose homeostasis in C57BL6/J mice: partial improvement with cessation of the exposure. Sleep 36, 1483-1490; 1490A-1490B. doi: 10.5665/sleep.3040
49. Polotsky, V. Y., Li, J., Punjabi, N. M., Rubin, A. E., Smith, P. L., Schwartz, A. R., et al. (2003). Intermittent hypoxia increases insulin resistance in genetically obese mice. J. Physiol. 552, 253-264. doi: 10.1113/jphysiol.2003.048173
50. Ribeiro, M. J., Sacramento, J. F., Gonzalez, C., Guarino, M. P., Monteiro, E. C., and Conde, S. V. (2013). Carotid body denervation prevents the development of insulin resistance and hypertension induced by hypercaloric diets. Diabetes 62, 2905-2916. doi: 10.2337/db12-1463
51. Routh, V. H. (2002). Glucose-sensing neurons: are they physiologically relevant? Physiol. Behav. 76, 403-413. doi: 10.1016/S0031-9384(02)00761-8
52. Schuit, F. C., Huypens, P., Heimberg, H., and Pipeleers, D. G. (2001). Glucose sensing in pancreatic beta-cells: a model for the study of other glucose-regulated cells in gut, pancreas, and hypothalamus. Diabetes 50, 1-11. doi: 10.2337/diabetes.50.1.1
53. Schultz, H. D., Marcus, N. J., and Del Rio, R. (2013). Role of the carotid body in the pathophysiology of heart failure. Curr. Hypertens. Rep. 15, 356-362. doi: 10.1007/s11906-013-0368-x
54. Tasali, E., Mokhlesi, B., and Van Cauter, E. (2008). Obstructive sleep apnea and type 2 diabetes: interacting epidemics. Chest 133, 496-506. doi: 10.1378/chest.07-0828
55. Thorens, B. (2001). GLUT2 in pancreatic and extra-pancreatic gluco-detection (review). Mol. Membr. Biol. 18, 265-273. doi: 10.1080/09687680110100995
56. Timmers, H. J., Karemaker, J. M., Wieling, W., Marres, H. A., Folgering, H. T., and Lenders, J. W. (2003). Baroreflex and chemoreflex function after bilateral carotid body tumor resection. J. Hypertens. 21, 591-599. doi: 10.1097/00004872-200303000-00026
57. Ward, D. S., Voter, W. A., and Karan, S. (2007). The effects of hypo- and hyperglycaemia on the hypoxic ventilatory response in humans. J. Physiol. 582, 859-869. doi: 10.1113/jphysiol.2007.130112
58. Ward, D. S., Voter, W. A., and Karan, S. (2009). The role of the carotid bodies in the counter-regulatory response to hypoglycemia. Adv. Exp. Med. Biol. 648, 273-280. doi: 10.1007/978-90-481-2259-2_31
59. Wehrwein, E. A., Basu, R., Basu, A., Curry, T. B., Rizza, R. A., and Joyner, M. J. (2010). Hyperoxia blunts counterregulation during hypoglycaemia in humans: possible role for the carotid bodies? J. Physiol. 588, 4593-4601. doi: 10.1113/jphysiol.2010.197491
60. Weir, E. K., Lopez-Barneo, J., Buckler, K. J., and Archer, S. L. (2005). Acute oxygen-sensing mechanisms. N. Engl. J. Med. 353, 2042-2055. doi: 10.1056/NEJMra050002
61. Zhang, M., Buttigieg, J., and Nurse, C. A. (2007). Neurotransmitter mechanisms mediating low-glucose signalling in cocultures and fresh tissue slices of rat carotid body. J. Physiol. 578, 735-750. doi: 10.1113/jphysiol.2006.121871