Anesthetics interfere with axon guidance in developing mouse neocortical neurons in vitro via a γ-aminobutyric acid type a receptor mechanism

Anesthesiology

Volumn 118, Issue 4, 2013, Pages 825-833

  Mintz, C David ^a   Barrett, Kendall M S ^a   Smith, Sarah C ^a   Benson, Deanna L ^b   Harrison, Neil L ^a  

^a P and S Building ^*  (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR GAMMA1; ANESTHETIC AGENT; ISOFLURANE; NETRIN 1; SEMAPHORIN 3A;

ALLOSTERISM; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN SLICE; CELL CULTURE; CELL GROWTH; CONTROLLED STUDY; FLUORESCENCE; FLUORESCENCE MICROSCOPY; IN VITRO STUDY; MOUSE; NERVE FIBER; NEUROTOXICITY; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; TISSUE SLICE;

ANALYSIS OF VARIANCE; ANESTHESIA, GENERAL; ANESTHETICS, INHALATION; ANIMALS; AXONS; BRAIN; CELLS, CULTURED; CHEMOTAXIS; GROWTH CONES; ISOFLURANE; MICE; MICE, INBRED C57BL; MICROSCOPY, FLUORESCENCE; NERVE GROWTH FACTORS; NEUROGENESIS; NEURONS; RECEPTORS, GABA; SIGNAL TRANSDUCTION;

EID: 84875905075     PISSN: 00033022     EISSN: 15281175     Source Type: Journal    
DOI: 10.1097/ALN.0b013e318287b850     Document Type: Article

References (52)

1. Block RI, Thomas JJ, Bayman EO, Choi JY, Kimble KK, Todd MM: Are anesthesia and surgery during infancy associated with altered academic performance during childhood? Anesthesiology 2012; 117:494-503
2. DiMaggio C, Sun LS , Li G: Early childhood exposure to anesthesia and risk of developmental and behavioral disorders in a sibling birth cohort. Anesth Analg 2011; 113:1143-51
3. DiMaggio C, Sun LS , Kakavouli A, Byrne MW, Li G: A retrospective cohort study of the association of anesthesia and hernia repair surgery with behavioral and developmental disorders in young children. J Neurosurg Anesthesiol 2009; 21:286-91
4. Ing C, DiMaggio C, Whitehouse A, Hegarty MK, Brady J, von Ungern-Sternberg BS, Davidson A, Wood AJ, Li G, Sun LS : Long-term differences in language and cognitive function after childhood exposure to anesthesia. Pediatrics 2012; 130:e476-85
5. Wilder RT, Flick RP, Sprung J, Katusic SK, Barbaresi WJ, Mickelson C, Gleich SJ, Schroeder DR, Weaver AL, Warner DO: Early exposure to anesthesia and learning disabilities in a population-based birth cohort. Anesthesiology 2009; 110:796-804
6. Davidson AJ: Anesthesia and neurotoxicity to the developing brain: The clinical relevance. Paediatr Anaesth 2011; 21:716-21
7. Istaphanous GK, Loepke AW: General anesthetics and the developing brain. Curr Opin Anaesthesiol 2009; 22:368-73
8. Kuehn BM: FDA considers data on potential risks of anesthesia use in infants, children. JAMA 2011; 305:1749-50, 53
9. Rappaport B, Mellon RD, Simone A, Woodcock J: Defining safe use of anesthesia in children. N Engl J Med 2011; 364:1387-90
10. Wilder RT: Is there any relationship between long-term behavior disturbance and early exposure to anesthesia? Curr Opin Anaesthesiol 2010; 23:332-6
11. Jevtovic-Todorovic V, Hartman RE, Izumi Y, Benshoff ND, Dikranian K, Zorumski CF, Olney JW, Wozniak DF: Early exposure to common anesthetic agents causes widespread neurodegeneration in the developing rat brain and persistent learning deficits. J Neurosci 2003; 23:876-82
12. Brambrink AM, Evers AS, Avidan MS, Farber NB, Smith DJ, Zhang X, Dissen GA, Creeley CE, Olney JW: Isofluraneinduced neuroapoptosis in the neonatal rhesus macaque brain. Anesthesiology 2010; 112:834-41
13. Lemkuil BP, Head BP, Pearn ML, Patel HH , Drummond JC, Patel PM: Isoflurane neurotoxicity is mediated by p75NTRRhoA activation and actin depolymerization. Anesthesiology 2011; 114:49-57
14. Wise-Faberowski L, Zhang H, Ing R, Pearlstein RD, Warner DS: Isoflurane-induced neuronal degeneration: An evaluation in organotypic hippocampal slice cultures. Anesth Analg 2005; 101:651-7
15. Cowan WM, Fawcett JW, O'Leary DD, Stanfield BB: Regressive events in neurogenesis. Science 1984; 225:1258-65
16. Oppenheim RW: Cell death during development of the nervous system. Annu Rev Neurosci 1991; 14:453-501
17. Engle EC: Human genetic disorders of axon guidance. Cold Spring Harb Perspect Biol 2010; 2:a001784
18. Kolodkin AL, Tessier-Lavigne M Mechanisms and molecules of neuronal wiring: A primer. Cold Spring Harb Perspect Biol 2011; 3
19. Kolodkin AL, Matthes DJ, Goodman CS: The semaphorin genes encode a family of transmembrane and secreted growth cone guidance molecules. Cell 1993; 75:1389-99
20. Luo Y, Raible D, Raper JA: Collapsin: A protein in brain that induces the collapse and paralysis of neuronal growth cones. Cell 1993; 75:217-27
21. Banker G, Goslin K: Culturing Nerve Cells, 2nd edition. Cambridge, MIT Press, 1998
22. Ma L, Song L, Radoi GE , Harrison NL: Transcriptional regulation of the mouse gene encoding the alpha-4 subunit of the GABAA receptor. J Biol Chem 2004; 279:40451-61
23. Frisa PS, Goodman MN, Smith GM, Silver J, Jacobberger JW: Immortalization of immature and mature mouse astrocytes with SV40 T antigen. J Neurosci Res 1994; 39:47-56
24. Mintz CD, Carcea I, McNickle DG, Dickson TC, Ge Y, Salton SR, Benson DL: ERM proteins regulate growth cone responses to Sema3A. J Comp Neurol 2008; 510:351-66
25. Polleux F, Giger RJ, Ginty DD, Kolodkin AL, Ghosh A: Patterning of cortical efferent projections by semaphorinneuropilin interactions. Science 1998; 282:1904-6
26. Lee HT , Kim M, Jan M, Emala CW: Anti-inflammatory and antinecrotic effects of the volatile anesthetic sevoflurane in kidney proximal tubule cells. Am J Physiol Renal Physiol 2006; 291:F67-78
27. Dotti CG, Sullivan CA, Banker GA: The establishment of polarity by hippocampal neurons in culture. J Neurosci 1988; 8:1454-68
28. Mintz CD, Smith SC, Barrett KM, Benson DL: Anesthetics interfere with the polarization of developing cortical neurons. J Neurosurg Anesthesiol 2012; 24:368-75
29. Kapfhammer JP, Xu H, Raper JA: The detection and quantification of growth cone collapsing activities. Nat Protoc 2007; 2:2005-11
30. Franks NP, Lieb WR: Molecular and cellular mechanisms of general anaesthesia. Nature 1994; 367:607-14
31. H ales TG , Lambert JJ: The actions of propofol on inhibitory amino acid receptors of bovine adrenomedullary chromaffin cells and rodent central neurones. Br J Pharmacol 1991; 104:619-28
32. Jones MV, Brooks PA, Harrison NL: Enhancement of gammaaminobutyric acid-activated Cl-currents in cultured rat hippocampal neurones by three volatile anaesthetics. J Physiol (Lond) 1992; 449:279-93
33. Nakahiro M, Yeh JZ, Brunner E, Narahashi T: General anesthetics modulate GABA receptor channel complex in rat dorsal root ganglion neurons. FASE B J 1989; 3:1850-4
34. Krasowski MD, Harrison NL: The actions of ether, alcohol and alkane general anaesthetics on GABAA and glycine receptors and the effects of TM2 and TM3 mutations. Br J Pharmacol 2000; 129:731-43
35. Dzoljic M, Van Duijn B: Nitrous oxide-induced enhancement of gamma-aminobutyric acidA-mediated chloride currents in acutely dissociated hippocampal neurons. Anesthesiology 1998; 88:473-80
36. Lin LH , Chen LL , Zirrolli JA, Harris RA: General anesthetics potentiate gamma-aminobutyric acid actions on gamma-aminobutyric acidA receptors expressed by Xenopus oocytes: Lack of involvement of intracellular calcium. J Pharmacol Exp Ther 1992; 263:569-78
37. Hopker VH, Shewan D, Tessier-Lavigne M, Poo M, Holt C: Growth-cone attraction to netrin-1 is converted to repulsion by laminin-1. Nature 1999; 401:69-73
38. Dent EW, Barnes AM, Tang F, Kalil K: Netrin-1 and semaphorin 3A promote or inhibit cortical axon branching, respectively, by reorganization of the cytoskeleton. J Neurosci 2004; 24:3002-12
39. Sepulveda B, Carcea I, Zhao B, Salton SR, Benson DL: L1 cell adhesion molecule promotes resistance to alcohol-induced silencing of growth cone responses to guidance cues. Neuroscience 2011; 180:30-40
40. S ernagor E, Chabrol F, Bony G, Cancedda L: GABAergic control of neurite outgrowth and remodeling during development and adult neurogenesis: General rules and differences in diverse systems. Front Cell Neurosci 2010; 4:11
41. Ge S, Goh EL , Sailor KA, Kitabatake Y, Ming GL , Song H: GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 2006; 439:589-93
42. H ubner CA, Lorke DE, Hermans-Borgmeyer I: Expression of the Na-K-2Cl-cotransporter NKCC1 during mouse development. Mech Dev 2001; 102:267-9
43. L oTurco JJ, Owens DF, Heath MJ, Davis MB, Kriegstein AR: GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 1995; 15:1287-98
44. Nishiyama M, von Schimmelmann MJ, Togashi K, Findley WM, Hong K: Membrane potential shifts caused by diffusible guidance signals direct growth-cone turning. Nat Neurosci 2008; 11:762-71
45. G omez TM, Robles E, Poo M, Spitzer NC: Filopodial calcium transients promote substrate-dependent growth cone turning. Science 2001; 291:1983-7
46. H ong K, Nishiyama M, Henley J, Tessier-Lavigne M, Poo M: Calcium signalling in the guidance of nerve growth by netrin-1. Nature 2000; 403:93-8
47. Zheng JQ, Felder M, Connor JA, Poo MM: Turning of nerve growth cones induced by neurotransmitters. Nature 1994; 368:140-4
48. T as PW, Gambaryan S, Roewer N: Volatile anesthetics affect the morphology of rat glioma C6 cells via RhoA, ERK, and Akt activation. J Cell Biochem 2007; 102:368-76
49. H u H, Marton TF, Goodman CS: Plexin B mediates axon guidance in Drosophila by simultaneously inhibiting active Rac and enhancing RhoA signaling. Neuron 2001; 32:39-51
50. O hnami S, Endo M, Hirai S, Uesaka N, Hatanaka Y, Yamashita T, Yamamoto N: Role of RhoA in activity-dependent cortical axon branching. J Neurosci 2008; 28:9117-21
51. Briner A, De Roo M, Dayer A, Muller D, Habre W, Vutskits L: Volatile anesthetics rapidly increase dendritic spine density in the rat medial prefrontal cortex during synaptogenesis. Anesthesiology 2010; 112:546-56
52. Briner A, Nikonenko I, De Roo M, Dayer A, Muller D, Vutskits L: Developmental stage-dependent persistent impact of propofol anesthesia on dendritic spines in the rat medial prefrontal cortex. Anesthesiology 2011; 115:282-93