Astrocytes release prostaglandin E2 to modify respiratory network activity

eLife

Volumn 6, Issue , 2017, Pages

  Forsberg, David ^a   Ringstedt, Thomas ^a   Herlenius, Eric ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; MAS RELATED G PROTEIN COUPLED RECEPTOR MEMBER A1; PEPTIDES AND PROTEINS; PROSTAGLANDIN E2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN STEM; CALCIUM SIGNALING; DATA ANALYSIS; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; ORGAN CULTURE; RESPIRATORY NERVE CELL; TIME LAPSE IMAGING; TRANSGENIC MOUSE; ANIMAL; DRUG EFFECT; FLUORESCENCE IMAGING; METABOLISM; PHYSIOLOGY; RESPIRATION CENTER;

ANIMALS; ASTROCYTES; CALCIUM SIGNALING; DINOPROSTONE; MICE, TRANSGENIC; OPTICAL IMAGING; RESPIRATORY CENTER;

EID: 85032899906     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.29566     Document Type: Article

References (45)

1. Angelova PR, Kasymov V, Christie I, Sheikhbahaei S, Turovsky E, Marina N, Korsak A, Zwicker J, Teschemacher AG, Ackland GL, Funk GD, Kasparov S, Abramov AY, Gourine AV. 2015. Functional oxygen sensitivity of astrocytes. Journal of Neuroscience 35:10460-10473. DOI: https://doi.org/10.1523/JNEUROSCI.0045-15.2015, PMID: 26203141
2. Ben Haim L, Rowitch DH. 2017. Functional diversity of astrocytes in neural circuit regulation. Nature Reviews Neuroscience 18:31-41. DOI: https://doi.org/10.1038/nrn.2016.159, PMID: 27904142
3. Brenner M, Kisseberth WC, Su Y, Besnard F, Messing A. 1994. GFAP promoter directs astrocyte-specific expression in transgenic mice. Journal of Neuroscience 14:1030-1037. PMID: 8120611
4. Cao X, Li LP, Wang Q, Wu Q, Hu HH, Zhang M, Fang YY, Zhang J, Li SJ, Xiong WC, Yan HC, Gao YB, Liu JH, Li XW, Sun LR, Zeng YN, Zhu XH, Gao TM. 2013. Astrocyte-derived ATP modulates depressive-like behaviors. Nature Medicine 19:773-777. DOI: https://doi.org/10.1038/nm.3162, PMID: 23644515
5. Dong X, Han S, Zylka MJ, Simon MI, Anderson DJ. 2001. A diverse family of GPCRs expressed in specific subsets of nociceptive sensory neurons. Cell 106:619-632. DOI: https://doi.org/10.1016/S0092-8674(01)00483-4, PMID: 11551509
6. Erlichman JS, Li A, Nattie EE. 1998. Ventilatory effects of glial dysfunction in a rat brain stem chemoreceptor region. Journal of Applied Physiology 85:1599-1604. PMID: 9804558
7. Erlichman JS, Leiter JC, Gourine AV. 2010. ATP, glia and central respiratory control. Respiratory Physiology & Neurobiology 173:305-311. DOI: https://doi.org/10.1016/j.resp.2010.06.009, PMID: 20601205
8. Fiacco TA, Agulhon C, Taves SR, Petravicz J, Casper KB, Dong X, Chen J, McCarthy KD. 2007. Selective stimulation of astrocyte calcium in situ does not affect neuronal excitatory synaptic activity. Neuron 54:611-626. DOI: https://doi.org/10.1016/j.neuron.2007.04.032, PMID: 17521573
9. Forsberg D, Horn Z, Tserga E, Smedler E, Silberberg G, Shvarev Y, Kaila K, Uhlén P, Herlenius E. 2016. CO2-evoked release of PGE2 modulates sighs and inspiration as demonstrated in brainstem organotypic culture. eLife 5:e14170. DOI: https://doi.org/10.7554/eLife.14170, PMID: 27377173
10. Forsberg D, Thonabulsombat C, Jäderstad J, Jäderstad LM, Olivius P, Herlenius E. 2017. functional stem cell integration into neural networks assessed by organotypic slice cultures. Current protocols in stem cell biology 42:2D 13 11-21312. DOI: https://doi.org/10.1002/cpsc.34, PMID: 28806855
11. Fukuda Y, Honda Y, Schläfke ME, Loeschcke HH. 1978. Effect of H+ on the membrane potential of silent cells in the ventral and dorsal surface layers of the rat medulla in vitro. Pflugers Archiv European Journal of Physiology 376:229-235. DOI: https://doi.org/10.1007/BF00584955, PMID: 30068
12. Fukushi I, Takeda K, Yokota S, Hasebe Y, Sato Y, Pokorski M, Horiuchi J, Okada Y. 2016. Effects of arundic acid, an astrocytic modulator, on the cerebral and respiratory functions in severe hypoxia. Respiratory Physiology & Neurobiology 226:24-29. DOI: https://doi.org/10.1016/j.resp.2015.11.011, PMID: 26592145
13. Gourine AV, Llaudet E, Dale N, Spyer KM. 2005. Release of ATP in the ventral medulla during hypoxia in rats: role in hypoxic ventilatory response. Journal of Neuroscience 25:1211-1218. DOI: https://doi.org/10.1523/JNEUROSCI.3763-04.2005, PMID: 15689558
14. Gourine AV, Kasymov V, Marina N, Tang F, Figueiredo MF, Lane S, Teschemacher AG, Spyer KM, Deisseroth K, Kasparov S. 2010. Astrocytes control breathing through pH-dependent release of ATP. Science 329:571-575. DOI: https://doi.org/10.1126/science.1190721, PMID: 20647426
15. Gourine AV, Kasparov S. 2011. Astrocytes as brain interoceptors. Experimental Physiology 96:411-416. DOI: https://doi.org/10.1113/expphysiol.2010.053165, PMID: 21257664
16. Gourine AV, Funk GD. 2017. On the existence of a central respiratory oxygen sensor. Journal of Applied Physiology:jap.00194.2017. DOI: https://doi.org/10.1152/japplphysiol.00194.2017
17. Grass D, Pawlowski PG, Hirrlinger J, Papadopoulos N, Richter DW, KirchhoffF, Hülsmann S. 2004. Diversity of functional astroglial properties in the respiratory network. Journal of Neuroscience 24:1358-1365. DOI: https://doi.org/10.1523/JNEUROSCI.4022-03.2004, PMID: 14960607
18. Hartelt N, Skorova E, Manzke T, Suhr M, Mironova L, Kügler S, Mironov SL. 2008. Imaging of respiratory network topology in living brainstem slices. Molecular and Cellular Neuroscience 37:425-431. DOI: https://doi.org/10. 1016/j.mcn.2007.10.011, PMID: 18203620
19. Hawkins VE, Takakura AC, Trinh A, Malheiros-Lima MR, Cleary CM, Wenker IC, Dubreuil T, Rodriguez EM, Nelson MT, Moreira TS, Mulkey DK. 2017. Purinergic regulation of vascular tone in the retrotrapezoid nucleus is specialized to support the drive to breathe. eLife 6:e25232. DOI: https://doi.org/10.7554/eLife.25232, PMID: 2 8387198
20. Herlenius E, Thonabulsombat C, Forsberg D, Jäderstad J, Jäderstad LM, Björk L, Olivius P. 2012. Functional stem cell integration assessed by organotypic slice cultures. Current Protocols in Stem Cell Biology Chapter 2: 13. DOI: https://doi.org/10.1002/9780470151808.sc02d13s23, PMID: 23154935
21. Hofstetter AO, Saha S, Siljehav V, Jakobsson PJ, Herlenius E. 2007. The induced prostaglandin E2 pathway is a key regulator of the respiratory response to infection and hypoxia in neonates. PNAS 104:9894-9899. DOI: https://doi.org/10.1073/pnas.0611468104, PMID: 17535900
22. Huckstepp RT, id Bihi R, Eason R, Spyer KM, Dicke N, Willecke K, Marina N, Gourine AV, Dale N. 2010. Connexin hemichannel-mediated CO2-dependent release of ATP in the medulla oblongata contributes to central respiratory chemosensitivity. The Journal of Physiology 588:3901-3920. DOI: https://doi.org/10.1113/jphysiol.2010.192088, PMID: 20736421
23. Huxtable AG, Zwicker JD, Alvares TS, Ruangkittisakul A, Fang X, Hahn LB, Posse de Chaves E, Baker GB, Ballanyi K, Funk GD. 2010. Glia contribute to the purinergic modulation of inspiratory rhythm-generating networks. Journal of Neuroscience 30:3947-3958. DOI: https://doi.org/10.1523/JNEUROSCI.6027-09.2010, PMID: 20237265
24. Lin W, Kemper A, McCarthy KD, Pytel P, Wang JP, Campbell IL, Utset MF, Popko B. 2004. Interferon-gamma induced medulloblastoma in the developing cerebellum. Journal of Neuroscience 24:10074-10083. DOI: https://doi.org/10.1523/JNEUROSCI.2604-04.2004, PMID: 15537876
25. Lorier AR, Huxtable AG, Robinson DM, Lipski J, Housley GD, Funk GD. 2007. P2Y1 receptor modulation of the pre-Bötzinger complex inspiratory rhythm generating network in vitro. Journal of Neuroscience 27:993-1005. DOI: https://doi.org/10.1523/JNEUROSCI.3948-06.2007, PMID: 17267553
26. Meigh L, Greenhalgh SA, Rodgers TL, Cann MJ, Roper DI, Dale N. 2013. CO2directly modulates connexin 26 by formation of carbamate bridges between subunits. eLife 2:e01213. DOI: https://doi.org/10.7554/eLife.01213, PMID: 24220509
27. Okada Y, Sasaki T, Oku Y, Takahashi N, Seki M, Ujita S, Tanaka KF, Matsuki N, Ikegaya Y. 2012. Preinspiratory calcium rise in putative pre-Botzinger complex astrocytes. The Journal of Physiology 590:4933-4944. DOI: https://doi.org/10.1113/jphysiol.2012.231464, PMID: 22777672
28. Oku Y, Fresemann J, Miwakeichi F, Hülsmann S. 2016. Respiratory calcium fluctuations in low-frequency oscillating astrocytes in the pre-Bötzinger complex. Respiratory Physiology & Neurobiology 226:11-17. DOI: https://doi.org/10.1016/j.resp.2015.02.002, PMID: 25747384
29. Parpura V, Heneka MT, Montana V, Oliet SH, Schousboe A, Haydon PG, Stout RF, Spray DC, Reichenbach A, Pannicke T, Pekny M, Pekna M, Zorec R, Verkhratsky A. 2012. Glial cells in (patho)physiology. Journal of Neurochemistry 121:4-27. DOI: https://doi.org/10.1111/j.1471-4159.2012.07664.x, PMID: 22251135
30. Pascual O, Casper KB, Kubera C, Zhang J, Revilla-Sanchez R, Sul JY, Takano H, Moss SJ, McCarthy K, Haydon PG. 2005. Astrocytic purinergic signaling coordinates synaptic networks. Science 310:113-116. DOI: https://doi.org/10.1126/science.1116916, PMID: 16210541
31. Phillips WS, Herly M, Del Negro CA, Rekling JC. 2016. Organotypic slice cultures containing the preBötzinger complex generate respiratory-like rhythms. Journal of Neurophysiology 115:1063-1070. DOI: https://doi.org/10.1152/jn.00904.2015, PMID: 26655824
32. Rajani V, Zhang Y, Jalubula V, Rancic V, SheikhBahaei S, Zwicker JD, Pagliardini S, Dickson CT, Ballanyi K, Kasparov S, Gourine AV, Funk GD. 2017. Release of ATP by pre-Bötzinger complex astrocytes contributes to the hypoxic ventilatory response via a Ca(2+)-dependent P2Y1 receptor mechanism. The Journal of Physiology. DOI: https://doi.org/10.1113/JP274727, PMID: 28678385
33. Ruangkittisakul A, Schwarzacher SW, Secchia L, Poon BY, Ma Y, Funk GD, Ballanyi K. 2006. High sensitivity to neuromodulator-activated signaling pathways at physiological [K+] of confocally imaged respiratory center neurons in on-line-calibrated newborn rat brainstem slices. Journal of Neuroscience 26:11870-11880. DOI: https://doi.org/10.1523/JNEUROSCI.3357-06.2006, PMID: 17108160
34. Ruangkittisakul A, Panaitescu B, Ballanyi K. 2011. K(+) and Ca2(+) dependence of inspiratory-related rhythm in novel “calibrated” mouse brainstem slices. Respiratory Physiology & Neurobiology 175:37-48. DOI: https://doi.org/10.1016/j.resp.2010.09.004, PMID: 20833274
35. Ruangkittisakul A, Kottick A, Picardo MC, Ballanyi K, Del Negro CA. 2014. Identification of the pre-Bötzinger complex inspiratory center in calibrated “sandwich” slices from newborn mice with fluorescent Dbx1 interneurons. Physiological Reports 2:e12111. DOI: https://doi.org/10.14814/phy2.12111, PMID: 25138790
36. Schnell C, Fresemann J, Hülsmann S. 2011. Determinants of functional coupling between astrocytes and respiratory neurons in the pre-Bötzinger complex. PLoS One 6:e26309. DOI: https://doi.org/10.1371/journal. pone.0026309, PMID: 22039458
37. Siljehav V, Olsson Hofstetter A, Jakobsson PJ, Herlenius E. 2012. mPGES-1 and prostaglandin E2: vital role in inflammation, hypoxic response, and survival. Pediatric Research 72:460-467. DOI: https://doi.org/10.1038/pr. 2012.119, PMID: 22926547
38. Siljehav V, Shvarev Y, Herlenius E. 2014 1985. Il-1b and prostaglandin E2 attenuate the hypercapnic as well as the hypoxic respiratory response via prostaglandin E receptor type 3 in neonatal mice. Journal of Applied Physiology 117:1027-1036. DOI: https://doi.org/10.1152/japplphysiol.00542.2014, PMID: 25213632
39. Siljehav V, Hofstetter AM, Leifsdottir K, Herlenius E. 2015. Prostaglandin E2 mediates cardiorespiratory disturbances during infection in neonates. The Journal of Pediatrics 167:1207-1213. DOI: https://doi.org/10. 1016/j.jpeds.2015.08.053, PMID: 26434370
40. Smedler E, Malmersjö S, Uhlén P. 2014. Network analysis of time-lapse microscopy recordings. Frontiers in Neural Circuits 8:111. DOI: https://doi.org/10.3389/fncir.2014.00111, PMID: 25278844
41. Stoppini L, Buchs PA, Muller D. 1991. A simple method for organotypic cultures of nervous tissue. Journal of Neuroscience Methods 37:173-182. DOI: https://doi.org/10.1016/0165-0270(91)90128-M, PMID: 1715499
42. Turovsky E, Karagiannis A, Abdala AP, Gourine AV. 2015. Impaired CO2 sensitivity of astrocytes in a mouse model of Rett syndrome. The Journal of Physiology 593:3159-3168. DOI: https://doi.org/10.1113/JP270369, PMID: 25981852
43. Turovsky E, Theparambil SM, Kasymov V, Deitmer JW, Del Arroyo AG, Ackland GL, Corneveaux JJ, Allen AN, Huentelman MJ, Kasparov S, Marina N, Gourine AV. 2016. Mechanisms of CO2/H+ sensitivity of astrocytes. Journal of Neuroscience 36:10750-10758. DOI: https://doi.org/10.1523/JNEUROSCI.1281-16.2016, PMID: 277 98130
44. Young JK, Dreshaj IA, Wilson CG, Martin RJ, Zaidi SI, Haxhiu MA. 2005. An astrocyte toxin influences the pattern of breathing and the ventilatory response to hypercapnia in neonatal rats. Respiratory Physiology & Neurobiology 147:19-30. DOI: https://doi.org/10.1016/j.resp.2005.01.009, PMID: 15848120
45. Young SZ, Platel JC, Nielsen JV, Jensen NA, Bordey A. 2010. GABA(A) increases calcium in subventricular zone astrocyte-like cells through l-and t-type voltage-gated calcium channels. Frontiers in cellular neuroscience 4:8. DOI: https://doi.org/10.3389/fncel.2010.00008, PMID: 20422045