D-serine released by astrocytes in brainstem regulates breathing response to CO2 levels

Nature Communications

Volumn 8, Issue 1, 2017, Pages

  Beltran Castillo S ^a   Olivares, M J ^a   Contreras, R A ^a   Zuniga G ^a   Llona, I ^a   Von Bernhardi, R ^a,b   Eugenin J L ^a  

^a UNIVERSIDAD DE SANTIAGO DE CHILE   (Chile)

^b PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

BAFILOMYCIN A1; BREFELDIN A; CALCIUM; CARBENOXOLONE; CARBON DIOXIDE; DEXTRO AMINO ACID OXIDASE; DEXTRO SERINE; DIZOCILPINE; FLUOROACETATE SODIUM; GAP JUNCTION PROTEIN; GLUTAMIC ACID; ISOMERASE INHIBITOR; MEMBRANE PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PANNEXIN 1; PHENAZINE DERIVATIVE; PHENAZINE ETHOSULFATE; PHENAZINE METHOSULFATE; PROBENECID; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; RACEMASE; SERINE; SERINE RACEMASE; SODIUM CHLORIDE; UNCLASSIFIED DRUG; FLUOROACETIC ACID;

ANTAGONISM; BRAIN; CARBON DIOXIDE; CHEMICAL BINDING; CHEMORECEPTION; ENZYME; ENZYME ACTIVITY; HOMEOSTASIS; INDUCED RESPONSE; PHYSIOLOGICAL RESPONSE;

ADULT; AMINO ACID SYNTHESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN SLICE; BRAIN STEM; BREATHING; BREATHING MECHANICS; BREATHING RATE; CHEMORECEPTOR; CONTROLLED STUDY; ENZYMATIC DEGRADATION; EXTRACELLULAR CALCIUM; FEMALE; HYPERCAPNIA; IN VITRO STUDY; IN VIVO STUDY; LIQUID CHROMATOGRAPHY-MASS SPECTROMETRY; MALE; MEDULLA OBLONGATA; METABOLIC INHIBITION; MOUSE; NEOCORTEX; NEWBORN; NONHUMAN; RAPHE NUCLEUS; RESPIRATION DEPRESSION; RESPIRATORY ACIDOSIS; SINGLE DRUG DOSE; WAKEFULNESS; ANIMAL; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; INBRED MOUSE STRAIN; METABOLISM; PATHOPHYSIOLOGY;

MUS;

ANIMALS; ASTROCYTES; BRAIN STEM; CARBON DIOXIDE; CELLS, CULTURED; FEMALE; FLUOROACETATES; HYPERCAPNIA; MALE; MICE, INBRED STRAINS; RECEPTORS, N-METHYL-D-ASPARTATE; RESPIRATION; SERINE;

EID: 85030991558     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/s41467-017-00960-3     Document Type: Article

References (70)

1. Feldman, J. L., Del Negro, C. A. & Gray, P. A. Understanding the rhythm of breathing: so near, yet so far. Annu. Rev. Physiol. 75, 423-452 (2013).
2. Nattie, E. & Li, A. Central chemoreceptors: locations and functions. Compr. Physiol. 2, 221-254 (2012).
3. Gourine, A. V., Llaudet, E., Dale, N. & Spyer, K. M. ATP is a mediator of chemosensory transduction in the central nervous system. Nature 436, 108-111 (2005).
4. Gourine, A. V. et al. Astrocytes control breathing through pH-dependent release of ATP. Science 329, 571-575 (2010).
5. Howarth, C. et al. A critical role for astrocytes in hypercapnic vasodilation in brain. J. Neurosci. 37, 2403-2414 (2017).
6. Eugenin, J. et al. Expression pattern of scavenger receptors and amyloid-beta phagocytosis of astrocytes and microglia in culture are modified by acidosis: implications for Alzheimer'sdisease. J. Alzheimers Dis. 53, 857-873 (2016).
7. Wenker, I. C., Kreneisz, O., Nishiyama, A. & Mulkey, D. K. Astrocytes in the retrotrapezoid nucleus sense H+ by inhibition of a Kir4.1-Kir5.1-like current and may contribute to chemoreception by a purinergic mechanism. J. Neurophysiol. 104, 3042-3052 (2010).
8. 2 and O2 sensitivity. Proc. Natl Acad. Sci. USA 107, 2325-2330 (2010).
9. Wang, S. et al. TASK-2 channels contribute to pH sensitivity of retrotrapezoid nucleus chemoreceptor neurons. J. Neurosci. 33, 16033-16044 (2013).
10. Kumar, N. N. et al. Regulation of breathing by CO(2) requires the proton-activated receptor GPR4 in retrotrapezoid nucleus neurons. Science 348, 1255-1260 (2015).
11. Sobrinho, C. R. et al. Purinergic signalling contributes to chemoreception in the retrotrapezoid nucleus but not the nucleus of the solitary tract or medullary raphe. J. Physiol. 592, 1309-1323 (2014).
12. Kasymov, V. et al. Differential sensitivity of brainstem versus cortical astrocytes to changes in pH reveals functional regional specialization of astroglia. J. Neurosci. 33, 435-441 (2013).
13. Ding, X., Ma, N., Nagahama, M., Yamada, K. & Semba, R. Localization of D-serine and serine racemase in neurons and neuroglias in mouse brain. Neurol. Sci. 32, 263-267 (2011).
14. Wolosker, H., Blackshaw, S. & Snyder, S. H. Serine racemase: a glial enzyme synthesizing D-serine to regulate glutamate-N-methyl-D-aspartate neurotransmission. Proc. Natl Acad. Sci. USA 96, 13409-13414 (1999).
15. Kartvelishvily, E., Shleper, M., Balan, L., Dumin, E. & Wolosker, H. Neuron-derived D-serine release provides a novel means to activate N-methyl-D- aspartate receptors. J. Biol. Chem. 281, 14151-14162 (2006).
16. Hashimoto, A. et al. The presence of free D-serine in rat brain. FEBS Lett. 296, 33-36 (1992).
17. Williams, S. M., Diaz, C. M., Macnab, L. T., Sullivan, R. K. & Pow, D. V. Immunocytochemical analysis of D-serine distribution in the mammalian brain reveals novel anatomical compartmentalizations in glia and neurons. Glia 53, 401-411 (2006).
18. Mothet, J. P. et al. D-serine is an endogenous ligand for the glycine site of the N-methyl-D-aspartate receptor. Proc. Natl Acad. Sci. USA 97, 4926-4931 (2000).
19. Furukawa, H. & Gouaux, E. Mechanisms of activation, inhibition and specificity: crystal structures of the NMDA receptor NR1 ligand-binding core. EMBO J. 22, 2873-2885 (2003).
20. Matsui, T. et al. Functional comparison of D-serine and glycine in rodents: the effect on cloned NMDA receptors and the extracellular concentration. J. Neurochem. 65, 454-458 (1995).
21. Schell, M. J., Brady, R. O. Jr., Molliver, M. E. & Snyder, S. H. D-serine as a neuromodulator: regional and developmental localizations in rat brain glia resemble NMDA receptors. J. Neurosci. 17, 1604-1615 (1997).
22. Papouin, T. et al. Synaptic and extrasynaptic NMDA receptors are gated by different endogenous coagonists. Cell 150, 633-646 (2012).
23. Greer, J. J., Smith, J. C. & Feldman, J. L. Role of excitatory amino acids in the generation and transmission of respiratory drive in neonatal rat. J. Physiol. 437, 727-749 (1991).
24. Funk, G. D. et al. Functional respiratory rhythm generating networks in neonatal mice lacking NMDAR1 gene. J. Neurophysiol. 78, 1414-1420 (1997).
25. Morgado-Valle, C. & Feldman, J. L. NMDA receptors in preBotzinger complex neurons can drive respiratory rhythm independent of AMPA receptors. J. Physiol. 582, 359-368 (2007).
26. Nattie, E. in pH and Brain Function (eds K. Kaila & B. R. Ransom) 535-560 (Wiley-Liss Inc., 1998).
27. Muller, D. J., Hand, G. M., Engel, A. & Sosinsky, G. E. Conformational changes in surface structures of isolated connexin 26 gap junctions. EMBO J. 21 , 3598-3607 (2002).
28. Poornima, V. et al. P2X7 receptor-pannexin 1 hemichannel association: effect of extracellular calcium on membrane permeabilization. J. Mol. Neurosci. 46, 585-594 (2012).
29. Hashimoto, A., Oka, T. & Nishikawa, T. Extracellular concentration of endogenous free D-serine in the rat brain as revealed by in vivo microdialysis. Neuroscience 66, 635-643 (1995).
30. Fukushima, T., Kawai, J., Imai, K. & Toyo'oka, T. Simultaneous determination of D- and L-serine in rat brain microdialysis sample using a column-switching HPLC with fluorimetric detection. Biomed. Chromatogr. 18, 813-819 (2004).
31. Liu, Y. et al. Exposure to cyclic intermittent hypoxia increases expression of functional NMDA receptors in the rat carotid body. J. Appl. Physiol. 106, 259-267 (2009).
32. Hulsmann, S., Oku, Y., Zhang, W. & Richter, D. W. Metabolic coupling between glia and neurons is necessary for maintaining respiratory activity in transverse medullary slices of neonatal mouse. Eur. J. Neurosci. 12, 856-862 (2000).
33. Van Horn, M. R., Sild, M. & Ruthazer, E. S. D-serine as a gliotransmitter and its roles in brain development and disease. Front. Cell. Neurosci. 7, 39 (2013).
34. 2/H+ sensitivity of astrocytes. J. Neurosci. 36, 10750-10758 (2016).
35. 2-dependent release of ATP in the medulla oblongata contributes to central respiratory chemosensitivity. J. Physiol. 588, 3901-3920 (2010).
36. Silverman, W., Locovei, S. & Dahl, G. Probenecid, a gout remedy, inhibits pannexin 1 channels. Am. J. Physiol. Cell Physiol. 295, C761 -767 (2008).
37. Chiu, Y. H., Ravichandran, K. S. & Bayliss, D. A. Intrinsic properties and regulation of pannexin 1 channel. Channels 8, 103-109 (2014).
38. Sandilos, J. K. & Bayliss, D. A. Physiological mechanisms for the modulation of pannexin 1 channel activity. J. Physiol. 590, 6257-6266 (2012).
39. Scemes, E. & Spray, D. C. Extracellular K(+) and astrocyte signaling via connexin and pannexin channels. Neurochem. Res. 37, 2310-2316 (2012).
40. Silverman, W. R. et al. The pannexin 1 channel activates the inflammasome in neurons and astrocytes. J. Biol. Chem. 284, 18143-18151 (2009).
41. Kim, J. E. & Kang, T. C. The P2X7 receptor-pannexin-1 complex decreases muscarinic acetylcholine receptor-mediated seizure susceptibility in mice. J. Clin. Invest. 121, 2037-2047 (2011).
42. Iglesias, R., Dahl, G., Qiu, F., Spray, D. C. & Scemes, E. Pannexin 1: the molecular substrate of astrocyte "hemichannels". J. Neurosci. 29, 7092-7097 (2009).
43. Pan, H. C., Chou, Y. C. & Sun, S. H. P2X7 R-mediated Ca(2+)-independent d- serine release via pannexin-1 of the P2X7 R-pannexin-1 complex in astrocytes. Glia 63, 877-893 (2015).
44. Mothet, J. P. et al. Glutamate receptor activation triggers a calcium-dependent and SNARE protein-dependent release of the gliotransmitter D-serine. Proc. Natl Acad. Sci. USA 102, 5606-5611 (2005).
45. Papouin, T. & Oliet, S. H. Organization, control and function of extrasynaptic NMDA receptors. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 369, 20130601 (2014).
46. Benneyworth, M. A., Li, Y., Basu, A. C., Bolshakov, V. Y. & Coyle, J. T. Cell selective conditional null mutations of serine racemase demonstrate a predominate localization in cortical glutamatergic neurons. Cell Mol. Neurobiol. 32, 613-624 (2012).
47. Rosenberg, D. et al. Neuronal release of D-serine: a physiological pathway controlling extracellular D-serine concentration. FASEB J. 24, 2951-2961 (2010).
48. Miya, K. et al. Serine racemase is predominantly localized in neurons in mouse brain. J. Comp. Neurol. 510, 641-654 (2008).
49. Wolosker, H. Serine racemase and the serine shuttle between neurons and astrocytes. Biochim. Biophys. Acta 1814, 1558-1566 (2011).
50. Horiike, K., Tojo, H., Arai, R., Nozaki, M. & Maeda, T. D-amino-acid oxidase is confined to the lower brain stem and cerebellum in rat brain: regional differentiation of astrocytes. Brain. Res. 652, 297-303 (1994).
51. Ray, R. S. et al. Impaired respiratory and body temperature control upon acute serotonergic neuron inhibition. Science 333, 637-642 (2011).
52. Cerpa, V. J. et al. Medullary 5-HT neurons: switch from tonic respiratory drive to chemoreception during postnatal development. Neuroscience 344,1-14 (2017).
53. Wang, W. & Richerson, G. B. Development of chemosensitivity of rat medullary raphe neurons. Neuroscience 90, 1001-1011 (1999).
54. Panatier, A. et al. Glia-derived D-serine controls NMDA receptor activity and synaptic memory. Cell 125, 775-784 (2006).
55. Fossat, P. et al. Glial D-serine gates NMDA receptors at excitatory synapses in prefrontal cortex. Cereb. Cortex 22, 595-606 (2012).
56. Hagiwara, H., Iyo, M. & Hashimoto, K. Neonatal disruption ofserine racemase causes schizophrenia-like behavioral abnormalities in adulthood: clinical rescue by d-serine. PLoS ONE 8, e62438 (2013).
57. Stevens, E. R., Gustafson, E. C., Sullivan, S. J., Esguerra, M. & Miller, R. F. Light- evoked NMDA receptor-mediated currents are reduced by blocking D-serine synthesis in the salamander retina. Neuroreport 21 , 239-244 (2010).
58. Sasabe, J. et al. D-serine is a key determinant of glutamate toxicity in amyotrophic lateral sclerosis. EMBO J. 26, 4149-4159 (2007).
59. Strisovsky, K., Jiraskova, J., Mikulova, A., Rulisek, L. & Konvalinka, J. Dual substrate and reaction specificity in mouse serine racemase: identification of high-affinity dicarboxylate substrate and inhibitors and analysis of the beta-eliminase activity. Biochemistry 44, 13091-13100 (2005).
60. Kim, P. M. et al. Serine racemase: activation by glutamate neurotransmission via glutamate receptor interacting protein and mediation of neuronal migration. Proc. Natl Acad. Sci. USA 102, 2105-2110 (2005).
61. Eugenin, J. et al. Prenatal to early postnatal nicotine exposure impairs central chemoreception and modifies breathing pattern in mouse neonates: a probable link to sudden infant death syndrome. J. Neurosci. 28, 13907-13917 (2008).
62. Pena, F., Parkis, M. A., Tryba, A. K. & Ramirez, J. M. Differential contribution of pacemaker properties to the generation of respiratory rhythms during normoxia and hypoxia. Neuron 43, 105-117 (2004).
63. Dememes, D., Mothet, J. P. & Nicolas, M. T. Cellular distribution of D-serine, serine racemase and D-amino acid oxidase in the rat vestibular sensory epithelia. Neuroscience 137, 991-997 (2006).
64. Puyal, J., Martineau, M., Mothet, J. P., Nicolas, M. T. & Raymond, J. Changes in D-serine levels and localization during postnatal development of the rat vestibular nuclei. J. Comp. Neurol. 497, 610-621 (2006).
65. Martineau, M. et al. Storage and uptake of D-serine into astrocytic synaptic-like vesicles specify gliotransmission. J. Neurosci. 33, 3413-3423 (2013).
66. Balu, D. T., Takagi, S., Puhl, M. D., Benneyworth, M. A. & Coyle, J. T. D-serine and serine racemase are localized to neurons in the adult mouse and human forebrain. Cell Mol. Neurobiol. 34, 419-435 (2014).
67. Esposito, S. et al. Contribution of serine racemase/d-serine pathway to neuronal apoptosis. Aging Cell 11, 588-598 (2012).
68. Waniewski, R. A. & Martin, D. L. Preferential utilization ofacetate byastrocytes is attributable to transport. J. Neurosci. 18, 5225-5233 (1998).
69. Swanson, R. A. & Graham, S. H. Fluorocitrate and fluoroacetate effects on astrocyte metabolism in vitro. Brain Res. 664,94-100 (1994).
70. Proudfoot, A. T., Bradberry, S. M. & Vale, J. A. Sodium fluoroacetate poisoning. Toxicol. Rev. 25, 213-219 (2006).