Graphene oxide nanosheets modulate spinal glutamatergic transmission and modify locomotor behaviour in an in vivo zebrafish model

Graphene oxide (GO), an oxidised form of graphene, is widely used for biomedical applications, due to its dispersibility in water and simple surface chemistry tunability. In particular, small (less than 500 nm in lateral dimension) and thin (1–3 carbon monolayers) graphene oxide nanosheets (s-GO) ha...

Full description

Saved in:
Bibliographic Details
Published inNanoscale horizons Vol. 5; no. 8; pp. 1250 - 1263
Main Authors Cellot, Giada, Vranic, Sandra, Shin, Yuyoung, Worsley, Robyn, Rodrigues, Artur Filipe, Bussy, Cyrill, Casiraghi, Cinzia, Kostarelos, Kostas, McDearmid, Jonathan Robert
Format Journal Article
LanguageEnglish
Published Cambridge Royal Society of Chemistry 01.08.2020
Subjects
Online AccessGet full text

Cover

Loading…
Abstract Graphene oxide (GO), an oxidised form of graphene, is widely used for biomedical applications, due to its dispersibility in water and simple surface chemistry tunability. In particular, small (less than 500 nm in lateral dimension) and thin (1–3 carbon monolayers) graphene oxide nanosheets (s-GO) have been shown to selectively inhibit glutamatergic transmission in neuronal cultures in vitro and in brain explants obtained from animals injected with the nanomaterial. This raises the exciting prospect that s-GO can be developed as a platform for novel nervous system therapeutics. It has not yet been investigated whether the interference of the nanomaterial with neurotransmission may have a downstream outcome in modulation of behaviour depending specifically on the activation of those synapses. To address this problem we use early stage zebrafish as an in vivo model to study the impact of s-GO on nervous system function. Microinjection of s-GO into the embryonic zebrafish spinal cord selectively reduces the excitatory synaptic transmission of the spinal network, monitored in vivo through patch clamp recordings, without affecting spinal cell survival. This effect is accompanied by a perturbation in the swimming activity of larvae, which is the locomotor behaviour generated by the neuronal network of the spinal cord. Such results indicate that the impact of s-GO on glutamate based neuronal transmission is preserved in vivo and can induce changes in animal behaviour. These findings pave the way for use of s-GO as a modulator of nervous system function.
AbstractList Graphene oxide (GO), an oxidised form of graphene, is widely used for biomedical applications, due to its dispersibility in water and simple surface chemistry tunability. In particular, small (less than 500 nm in lateral dimension) and thin (1–3 carbon monolayers) graphene oxide nanosheets (s-GO) have been shown to selectively inhibit glutamatergic transmission in neuronal cultures in vitro and in brain explants obtained from animals injected with the nanomaterial. This raises the exciting prospect that s-GO can be developed as a platform for novel nervous system therapeutics. It has not yet been investigated whether the interference of the nanomaterial with neurotransmission may have a downstream outcome in modulation of behaviour depending specifically on the activation of those synapses. To address this problem we use early stage zebrafish as an in vivo model to study the impact of s-GO on nervous system function. Microinjection of s-GO into the embryonic zebrafish spinal cord selectively reduces the excitatory synaptic transmission of the spinal network, monitored in vivo through patch clamp recordings, without affecting spinal cell survival. This effect is accompanied by a perturbation in the swimming activity of larvae, which is the locomotor behaviour generated by the neuronal network of the spinal cord. Such results indicate that the impact of s-GO on glutamate based neuronal transmission is preserved in vivo and can induce changes in animal behaviour. These findings pave the way for use of s-GO as a modulator of nervous system function.
Graphene oxide (GO), an oxidised form of graphene, is widely used for biomedical applications, due to its dispersibility in water and simple surface chemistry tunability. In particular, small (less than 500 nm in lateral dimension) and thin (1–3 carbon monolayers) graphene oxide nanosheets (s-GO) have been shown to selectively inhibit glutamatergic transmission in neuronal cultures in vitro and in brain explants obtained from animals injected with the nanomaterial. This raises the exciting prospect that s-GO can be developed as a platform for novel nervous system therapeutics. It has not yet been investigated whether the interference of the nanomaterial with neurotransmission may have a downstream outcome in modulation of behaviour depending specifically on the activation of those synapses. To address this problem we use early stage zebrafish as an in vivo model to study the impact of s-GO on nervous system function. Microinjection of s-GO into the embryonic zebrafish spinal cord selectively reduces the excitatory synaptic transmission of the spinal network, monitored in vivo through patch clamp recordings, without affecting spinal cell survival. This effect is accompanied by a perturbation in the swimming activity of larvae, which is the locomotor behaviour generated by the neuronal network of the spinal cord. Such results indicate that the impact of s-GO on glutamate based neuronal transmission is preserved in vivo and can induce changes in animal behaviour. These findings pave the way for use of s-GO as a modulator of nervous system function.
Author Cellot, Giada
Casiraghi, Cinzia
Kostarelos, Kostas
Vranic, Sandra
Shin, Yuyoung
McDearmid, Jonathan Robert
Worsley, Robyn
Rodrigues, Artur Filipe
Bussy, Cyrill
Author_xml – sequence: 1
  givenname: Giada
  orcidid: 0000-0001-9198-8402
  surname: Cellot
  fullname: Cellot, Giada
  organization: Department of Neuroscience, Psychology and Behaviour, College of Life Sciences, University of Leicester, Leicester, UK
– sequence: 2
  givenname: Sandra
  orcidid: 0000-0002-6653-7156
  surname: Vranic
  fullname: Vranic, Sandra
  organization: Nanomedicine Lab, Faculty of Biology, Medicine & Health and National Graphene Institute, University of Manchester, Manchester M13 9PT, UK
– sequence: 3
  givenname: Yuyoung
  orcidid: 0000-0003-4359-5406
  surname: Shin
  fullname: Shin, Yuyoung
  organization: Department of Chemistry, University of Manchester, Manchester M13 9PL, UK
– sequence: 4
  givenname: Robyn
  surname: Worsley
  fullname: Worsley, Robyn
  organization: Department of Chemistry, University of Manchester, Manchester M13 9PL, UK
– sequence: 5
  givenname: Artur Filipe
  orcidid: 0000-0002-4078-3455
  surname: Rodrigues
  fullname: Rodrigues, Artur Filipe
  organization: Nanomedicine Lab, Faculty of Biology, Medicine & Health and National Graphene Institute, University of Manchester, Manchester M13 9PT, UK
– sequence: 6
  givenname: Cyrill
  orcidid: 0000-0001-8870-443X
  surname: Bussy
  fullname: Bussy, Cyrill
  organization: Nanomedicine Lab, Faculty of Biology, Medicine & Health and National Graphene Institute, University of Manchester, Manchester M13 9PT, UK
– sequence: 7
  givenname: Cinzia
  orcidid: 0000-0001-7185-0377
  surname: Casiraghi
  fullname: Casiraghi, Cinzia
  organization: Department of Chemistry, University of Manchester, Manchester M13 9PL, UK
– sequence: 8
  givenname: Kostas
  orcidid: 0000-0002-2224-6672
  surname: Kostarelos
  fullname: Kostarelos, Kostas
  organization: Nanomedicine Lab, Faculty of Biology, Medicine & Health and National Graphene Institute, University of Manchester, Manchester M13 9PT, UK
– sequence: 9
  givenname: Jonathan Robert
  surname: McDearmid
  fullname: McDearmid, Jonathan Robert
  organization: Department of Neuroscience, Psychology and Behaviour, College of Life Sciences, University of Leicester, Leicester, UK
BookMark eNpdkU1LxDAQhoOs4Lp68RcEvIiwmjRN0xxl8QsWvei5TNOpzdIma9Iu6s1_bqviwcvMMDwzvPPOIZk575CQE84uOBP60mjXMKaUqvfIPGFSLjOVpbO_WmYH5DjGDWOM51zpXMzJ522AbYMOqX-zFVIHzscGsY-089XQQo80bq2Dlr60Qw_d2Agv1tA-gIudjdF6R8FVE27rd9p64zvf-0BLbGBn_RConYgp7uzO0w8sA9Q2NtMItkdkv4Y24vFvXpDnm-un1d1y_Xh7v7paL43gol6miUxQKJ3mOslL4NV4gKkEipQpyXPkkJQCdMmYLLXKMg7agCmrsjICmKjFgpz97N0G_zpg7ItRvcG2BYd-iEWScpnkko-2LMjpP3QznjF6MFGJGvVkfKLOfygTfIwB62IbbAfhveCsmB5SrPTD3fdDbsQXQo2Bqw
CitedBy_id crossref_primary_10_1021_acsnano_2c06609
crossref_primary_10_1039_D3NJ01004J
crossref_primary_10_3390_nano11092161
crossref_primary_10_1016_j_mattod_2021_08_013
crossref_primary_10_1007_s40097_021_00444_3
crossref_primary_10_1002_chem_202301762
crossref_primary_10_1039_D4NH00041B
crossref_primary_10_1038_s41390_021_01681_6
crossref_primary_10_1039_D3NR04490D
crossref_primary_10_1039_D3NH00428G
crossref_primary_10_1016_j_aquatox_2023_106550
crossref_primary_10_34133_bmef_0034
crossref_primary_10_1016_j_cis_2022_102824
crossref_primary_10_3389_fnins_2023_1162493
crossref_primary_10_1016_j_carbon_2024_119288
crossref_primary_10_1016_j_nantod_2023_102121
crossref_primary_10_1021_acsnano_2c04756
crossref_primary_10_1016_j_biomaterials_2021_120749
Cites_doi 10.1016/j.brainresrev.2007.06.018
10.1038/nnano.2014.224
10.1212/WNL.44.1.11
10.1016/j.neulet.2015.02.043
10.1038/aps.2009.24
10.1002/advs.201700595
10.1017/S1092852900010427
10.1155/2012/718203
10.1002/adma.201203700
10.1371/journal.pone.0166816
10.1016/j.nbd.2015.01.001
10.1038/nnano.2008.215
10.1126/science.1102896
10.1523/JNEUROSCI.06-08-02267.1986
10.1016/j.colsurfb.2017.05.078
10.1002/cne.20278
10.1021/acsnano.6b03438
10.1002/cne.902360411
10.1021/acs.nanolett.8b04903
10.1523/JNEUROSCI.3796-07.2008
10.1073/pnas.0703446104
10.1016/j.cub.2010.02.039
10.1088/2053-1583/aac05c
10.1073/pnas.0502848102
10.1002/cne.1266
10.1038/srep09562
10.1016/j.expneurol.2015.09.019
10.1152/ajpcell.2002.282.1.C1
10.1016/S0165-0270(99)00008-4
10.1021/acsnano.7b07734
10.1002/anie.201403335
10.1152/jn.00446.2009
10.1038/s41598-018-36663-y
10.1088/2053-1583/3/1/014006
10.1021/acsnano.6b00130
10.1007/s00702-014-1180-8
10.1016/j.cub.2012.10.025
10.1152/jn.2001.86.1.197
10.1038/ncomms6259
10.1002/dvdy.22113
10.1021/cr300335p
10.1016/j.ydbio.2005.04.017
10.1016/j.biomaterials.2014.03.087
10.1242/dev.099531
10.1007/s00702-013-1149-z
10.1126/science.1246736
10.1038/nature11458
10.1126/science.1158877
10.1002/jez.b.21127
10.1152/jn.1992.68.4.1121
10.1016/S0301-0082(03)00052-2
ContentType Journal Article
Copyright Copyright Royal Society of Chemistry 2020
Copyright_xml – notice: Copyright Royal Society of Chemistry 2020
DBID AAYXX
CITATION
7SR
7TB
7U5
8BQ
8FD
FR3
JG9
L7M
7X8
DOI 10.1039/c9nh00777f
DatabaseName CrossRef
Engineered Materials Abstracts
Mechanical & Transportation Engineering Abstracts
Solid State and Superconductivity Abstracts
METADEX
Technology Research Database
Engineering Research Database
Materials Research Database
Advanced Technologies Database with Aerospace
MEDLINE - Academic
DatabaseTitle CrossRef
Materials Research Database
Engineered Materials Abstracts
Technology Research Database
Mechanical & Transportation Engineering Abstracts
Solid State and Superconductivity Abstracts
Engineering Research Database
Advanced Technologies Database with Aerospace
METADEX
MEDLINE - Academic
DatabaseTitleList Materials Research Database
CrossRef
DeliveryMethod fulltext_linktorsrc
Discipline Engineering
EISSN 2055-6764
EndPage 1263
ExternalDocumentID 10_1039_C9NH00777F
GroupedDBID 0R~
AAEMU
AAIWI
AAJAE
AANOJ
AARTK
AAXHV
AAYXX
ABASK
ABDVN
ABJNI
ABPDG
ABRYZ
ACGFS
ACIWK
ADMRA
AEFDR
AENGV
AETIL
AFOGI
AGEGJ
AGRSR
AGSTE
AKBGW
ALMA_UNASSIGNED_HOLDINGS
ANUXI
APEMP
ASKNT
BLAPV
C6K
CITATION
EBS
ECGLT
GGIMP
H13
O9-
RAOCF
RCNCU
RPMJG
RRC
RSCEA
RVUXY
7SR
7TB
7U5
8BQ
8FD
FR3
JG9
L7M
7X8
ID FETCH-LOGICAL-c313f-4252e37948928ba1d179cd3e3407518e1a2b3a9b005b97661a9cacbdbdc3a03f3
ISSN 2055-6756
2055-6764
IngestDate Fri Aug 16 11:51:07 EDT 2024
Fri Sep 13 08:40:35 EDT 2024
Fri Aug 23 01:03:21 EDT 2024
IsDoiOpenAccess false
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 8
Language English
LinkModel OpenURL
MergedId FETCHMERGED-LOGICAL-c313f-4252e37948928ba1d179cd3e3407518e1a2b3a9b005b97661a9cacbdbdc3a03f3
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
ORCID 0000-0002-2224-6672
0000-0003-4359-5406
0000-0001-7185-0377
0000-0001-9198-8402
0000-0002-6653-7156
0000-0002-4078-3455
0000-0001-8870-443X
OpenAccessLink https://pubs.rsc.org/en/content/articlepdf/2020/nh/c9nh00777f
PQID 2427313618
PQPubID 2047513
PageCount 14
ParticipantIDs proquest_miscellaneous_2415285198
proquest_journals_2427313618
crossref_primary_10_1039_C9NH00777F
PublicationCentury 2000
PublicationDate 2020-08-01
PublicationDateYYYYMMDD 2020-08-01
PublicationDate_xml – month: 08
  year: 2020
  text: 2020-08-01
  day: 01
PublicationDecade 2020
PublicationPlace Cambridge
PublicationPlace_xml – name: Cambridge
PublicationTitle Nanoscale horizons
PublicationYear 2020
Publisher Royal Society of Chemistry
Publisher_xml – name: Royal Society of Chemistry
References Stoletov (C9NH00777F-(cit55)/*[position()=1]) 2007; 104
Myers (C9NH00777F-(cit23)/*[position()=1]) 1985; 236
Mao (C9NH00777F-(cit2)/*[position()=1]) 2013; 113
Hernandez (C9NH00777F-(cit31)/*[position()=1]) 2008; 3
Mukherjee (C9NH00777F-(cit30)/*[position()=1]) 2016; 11
Bitounis (C9NH00777F-(cit8)/*[position()=1]) 2013; 25
Kostarelos (C9NH00777F-(cit3)/*[position()=1]) 2014; 9
Hale (C9NH00777F-(cit24)/*[position()=1]) 2001; 437
Jasim (C9NH00777F-(cit29)/*[position()=1]) 2016; 3
Kostarelos (C9NH00777F-(cit7)/*[position()=1]) 2014; 344
Rauti (C9NH00777F-(cit10)/*[position()=1]) 2016; 10
Vranic (C9NH00777F-(cit45)/*[position()=1]) 2018; 12
Jana (C9NH00777F-(cit49)/*[position()=1]) 2017
Parichy (C9NH00777F-(cit34)/*[position()=1]) 2009; 238
Lewis (C9NH00777F-(cit22)/*[position()=1]) 2003; 69
Queenan (C9NH00777F-(cit46)/*[position()=1]) 2012; 2012
Tong (C9NH00777F-(cit44)/*[position()=1]) 2012; 22
Drapeau (C9NH00777F-(cit42)/*[position()=1]) 1999; 88
Nakano (C9NH00777F-(cit35)/*[position()=1]) 2005; 283
Geim (C9NH00777F-(cit6)/*[position()=1]) 2009; 324
Yang (C9NH00777F-(cit32)/*[position()=1]) 2013; 53
Fetcho (C9NH00777F-(cit26)/*[position()=1]) 2007; 308
Ren (C9NH00777F-(cit52)/*[position()=1]) 2018; 5
Mao (C9NH00777F-(cit48)/*[position()=1]) 2014; 35
Soares (C9NH00777F-(cit50)/*[position()=1]) 2017; 157
Novoselov (C9NH00777F-(cit1)/*[position()=1]) 2012; 490
Kuzum (C9NH00777F-(cit9)/*[position()=1]) 2014; 5
Fetcho (C9NH00777F-(cit27)/*[position()=1]) 2008; 57
Moreno (C9NH00777F-(cit38)/*[position()=1]) 2009; 102
Novoselov (C9NH00777F-(cit5)/*[position()=1]) 2005; 102
Gao (C9NH00777F-(cit40)/*[position()=1]) 2015; 591
Zhou (C9NH00777F-(cit13)/*[position()=1]) 2014; 121
Briggs (C9NH00777F-(cit20)/*[position()=1]) 2002; 282
Carp (C9NH00777F-(cit39)/*[position()=1]) 1992; 68
Yang (C9NH00777F-(cit51)/*[position()=1]) 2019; 34
Westerfield (C9NH00777F-(cit37)/*[position()=1]) 1986; 6
Rodrigues (C9NH00777F-(cit33)/*[position()=1]) 2018; 5
Buss (C9NH00777F-(cit43)/*[position()=1]) 2001; 86
Novoselov (C9NH00777F-(cit4)/*[position()=1]) 2004; 306
Lewerenz (C9NH00777F-(cit14)/*[position()=1]) 2015; 16
Friedrich (C9NH00777F-(cit21)/*[position()=1]) 2010; 20
Bramini (C9NH00777F-(cit11)/*[position()=1]) 2016; 10
Meldrum (C9NH00777F-(cit17)/*[position()=1]) 1994; 44
Dong (C9NH00777F-(cit15)/*[position()=1]) 2009; 30
Bosi (C9NH00777F-(cit54)/*[position()=1]) 2015; 5
Karthik (C9NH00777F-(cit56)/*[position()=1]) 2019; 9
Friedrich (C9NH00777F-(cit28)/*[position()=1]) 2010; 20
King (C9NH00777F-(cit19)/*[position()=1]) 2016; 275
Wick (C9NH00777F-(cit53)/*[position()=1]) 2014; 53
Higashijima (C9NH00777F-(cit25)/*[position()=1]) 2004; 480
Nelson (C9NH00777F-(cit47)/*[position()=1]) 2008; 28
Rauti (C9NH00777F-(cit12)/*[position()=1]) 2019; 19
Djuric (C9NH00777F-(cit41)/*[position()=1]) 2015; 76
Cortese (C9NH00777F-(cit16)/*[position()=1]) 2005; 10
Satou (C9NH00777F-(cit36)/*[position()=1]) 2013; 140
Ambrosi (C9NH00777F-(cit18)/*[position()=1]) 2014; 121
References_xml – volume: 57
  start-page: 1
  year: 2008
  ident: C9NH00777F-(cit27)/*[position()=1]
  publication-title: Brain Res. Rev.
  doi: 10.1016/j.brainresrev.2007.06.018
  contributor:
    fullname: Fetcho
– volume: 9
  start-page: 10
  year: 2014
  ident: C9NH00777F-(cit3)/*[position()=1]
  publication-title: Nat. Nanotechnol.
  doi: 10.1038/nnano.2014.224
  contributor:
    fullname: Kostarelos
– volume: 44
  start-page: 11
  year: 1994
  ident: C9NH00777F-(cit17)/*[position()=1]
  publication-title: Neurology
  doi: 10.1212/WNL.44.1.11
  contributor:
    fullname: Meldrum
– volume: 591
  start-page: 138
  year: 2015
  ident: C9NH00777F-(cit40)/*[position()=1]
  publication-title: Neurosci. Lett.
  doi: 10.1016/j.neulet.2015.02.043
  contributor:
    fullname: Gao
– volume-title: Carbon nanomaterials for biological and medical applications
  year: 2017
  ident: C9NH00777F-(cit49)/*[position()=1]
  contributor:
    fullname: Jana
– volume: 30
  start-page: 379
  year: 2009
  ident: C9NH00777F-(cit15)/*[position()=1]
  publication-title: Acta Pharmacol. Sin.
  doi: 10.1038/aps.2009.24
  contributor:
    fullname: Dong
– volume: 5
  start-page: 1700595
  year: 2018
  ident: C9NH00777F-(cit52)/*[position()=1]
  publication-title: Adv. Sci.
  doi: 10.1002/advs.201700595
  contributor:
    fullname: Ren
– volume: 10
  start-page: 10
  year: 2005
  ident: C9NH00777F-(cit16)/*[position()=1]
  publication-title: CNS Spectr.
  doi: 10.1017/S1092852900010427
  contributor:
    fullname: Cortese
– volume: 2012
  start-page: 718203
  year: 2012
  ident: C9NH00777F-(cit46)/*[position()=1]
  publication-title: Neural Plast.
  doi: 10.1155/2012/718203
  contributor:
    fullname: Queenan
– volume: 25
  start-page: 16
  year: 2013
  ident: C9NH00777F-(cit8)/*[position()=1]
  publication-title: Adv. Mater.
  doi: 10.1002/adma.201203700
  contributor:
    fullname: Bitounis
– volume: 11
  start-page: e0166816
  year: 2016
  ident: C9NH00777F-(cit30)/*[position()=1]
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0166816
  contributor:
    fullname: Mukherjee
– volume: 76
  start-page: 37
  year: 2015
  ident: C9NH00777F-(cit41)/*[position()=1]
  publication-title: Neurobiol. Dis.
  doi: 10.1016/j.nbd.2015.01.001
  contributor:
    fullname: Djuric
– volume: 3
  start-page: 9
  year: 2008
  ident: C9NH00777F-(cit31)/*[position()=1]
  publication-title: Nat. Nanotechnol.
  doi: 10.1038/nnano.2008.215
  contributor:
    fullname: Hernandez
– volume: 306
  start-page: 5696
  year: 2004
  ident: C9NH00777F-(cit4)/*[position()=1]
  publication-title: Science
  doi: 10.1126/science.1102896
  contributor:
    fullname: Novoselov
– volume: 6
  start-page: 8
  year: 1986
  ident: C9NH00777F-(cit37)/*[position()=1]
  publication-title: J. Neurosci.
  doi: 10.1523/JNEUROSCI.06-08-02267.1986
  contributor:
    fullname: Westerfield
– volume: 157
  start-page: 335
  year: 2017
  ident: C9NH00777F-(cit50)/*[position()=1]
  publication-title: Colloids Surf., B
  doi: 10.1016/j.colsurfb.2017.05.078
  contributor:
    fullname: Soares
– volume: 480
  start-page: 1
  year: 2004
  ident: C9NH00777F-(cit25)/*[position()=1]
  publication-title: J. Comp. Neurol.
  doi: 10.1002/cne.20278
  contributor:
    fullname: Higashijima
– volume: 10
  start-page: 7
  year: 2016
  ident: C9NH00777F-(cit11)/*[position()=1]
  publication-title: ACS Nano
  doi: 10.1021/acsnano.6b03438
  contributor:
    fullname: Bramini
– volume: 236
  start-page: 4
  year: 1985
  ident: C9NH00777F-(cit23)/*[position()=1]
  publication-title: J. Comp. Neurol.
  doi: 10.1002/cne.902360411
  contributor:
    fullname: Myers
– volume: 19
  start-page: 5
  year: 2019
  ident: C9NH00777F-(cit12)/*[position()=1]
  publication-title: Nano Lett.
  doi: 10.1021/acs.nanolett.8b04903
  contributor:
    fullname: Rauti
– volume: 28
  start-page: 2
  year: 2008
  ident: C9NH00777F-(cit47)/*[position()=1]
  publication-title: J. Neurosci.
  doi: 10.1523/JNEUROSCI.3796-07.2008
  contributor:
    fullname: Nelson
– volume: 104
  start-page: 17406
  year: 2007
  ident: C9NH00777F-(cit55)/*[position()=1]
  publication-title: Proc. Natl. Acad. Sci. U. S. A.
  doi: 10.1073/pnas.0703446104
  contributor:
    fullname: Stoletov
– volume: 20
  start-page: 8
  year: 2010
  ident: C9NH00777F-(cit28)/*[position()=1]
  publication-title: Curr. Biol.
  doi: 10.1016/j.cub.2010.02.039
  contributor:
    fullname: Friedrich
– volume: 5
  start-page: 035020
  year: 2018
  ident: C9NH00777F-(cit33)/*[position()=1]
  publication-title: 2D Mater.
  doi: 10.1088/2053-1583/aac05c
  contributor:
    fullname: Rodrigues
– volume: 102
  start-page: 30
  year: 2005
  ident: C9NH00777F-(cit5)/*[position()=1]
  publication-title: Proc. Natl. Acad. Sci. U. S. A.
  doi: 10.1073/pnas.0502848102
  contributor:
    fullname: Novoselov
– volume: 437
  start-page: 1
  year: 2001
  ident: C9NH00777F-(cit24)/*[position()=1]
  publication-title: J. Comp. Neurol.
  doi: 10.1002/cne.1266
  contributor:
    fullname: Hale
– volume: 5
  start-page: 9562
  year: 2015
  ident: C9NH00777F-(cit54)/*[position()=1]
  publication-title: Sci. Rep.
  doi: 10.1038/srep09562
  contributor:
    fullname: Bosi
– volume: 275
  start-page: 1
  year: 2016
  ident: C9NH00777F-(cit19)/*[position()=1]
  publication-title: Exp. Neurol.
  doi: 10.1016/j.expneurol.2015.09.019
  contributor:
    fullname: King
– volume: 282
  start-page: 1
  year: 2002
  ident: C9NH00777F-(cit20)/*[position()=1]
  publication-title: Am. J. Physiol.: Regul., Integr. Comp. Physiol.
  doi: 10.1152/ajpcell.2002.282.1.C1
  contributor:
    fullname: Briggs
– volume: 88
  start-page: 1
  year: 1999
  ident: C9NH00777F-(cit42)/*[position()=1]
  publication-title: J. Neurosci. Methods
  doi: 10.1016/S0165-0270(99)00008-4
  contributor:
    fullname: Drapeau
– volume: 12
  start-page: 2
  year: 2018
  ident: C9NH00777F-(cit45)/*[position()=1]
  publication-title: ACS Nano
  doi: 10.1021/acsnano.7b07734
  contributor:
    fullname: Vranic
– volume: 53
  start-page: 03
  year: 2013
  ident: C9NH00777F-(cit32)/*[position()=1]
  publication-title: Carbon
  contributor:
    fullname: Yang
– volume: 20
  start-page: 8
  year: 2010
  ident: C9NH00777F-(cit21)/*[position()=1]
  publication-title: Curr. Biol.
  doi: 10.1016/j.cub.2010.02.039
  contributor:
    fullname: Friedrich
– volume: 53
  start-page: 7714
  year: 2014
  ident: C9NH00777F-(cit53)/*[position()=1]
  publication-title: Angew. Chem., Int. Ed.
  doi: 10.1002/anie.201403335
  contributor:
    fullname: Wick
– volume: 102
  start-page: 2477
  issue: 4
  year: 2009
  ident: C9NH00777F-(cit38)/*[position()=1]
  publication-title: J. Neurophysiol.
  doi: 10.1152/jn.00446.2009
  contributor:
    fullname: Moreno
– volume: 9
  start-page: 4152
  year: 2019
  ident: C9NH00777F-(cit56)/*[position()=1]
  publication-title: Sci. Rep.
  doi: 10.1038/s41598-018-36663-y
  contributor:
    fullname: Karthik
– volume: 3
  start-page: 014006
  year: 2016
  ident: C9NH00777F-(cit29)/*[position()=1]
  publication-title: 2D Mater.
  doi: 10.1088/2053-1583/3/1/014006
  contributor:
    fullname: Jasim
– volume: 10
  start-page: 4
  year: 2016
  ident: C9NH00777F-(cit10)/*[position()=1]
  publication-title: ACS Nano
  doi: 10.1021/acsnano.6b00130
  contributor:
    fullname: Rauti
– volume: 121
  start-page: 8
  year: 2014
  ident: C9NH00777F-(cit13)/*[position()=1]
  publication-title: J. Neural Transm.
  doi: 10.1007/s00702-014-1180-8
  contributor:
    fullname: Zhou
– volume: 22
  start-page: 24
  year: 2012
  ident: C9NH00777F-(cit44)/*[position()=1]
  publication-title: Curr. Biol.
  doi: 10.1016/j.cub.2012.10.025
  contributor:
    fullname: Tong
– volume: 86
  start-page: 1
  year: 2001
  ident: C9NH00777F-(cit43)/*[position()=1]
  publication-title: J. Neurophysiol.
  doi: 10.1152/jn.2001.86.1.197
  contributor:
    fullname: Buss
– volume: 5
  start-page: 5259
  year: 2014
  ident: C9NH00777F-(cit9)/*[position()=1]
  publication-title: Nat. Commun.
  doi: 10.1038/ncomms6259
  contributor:
    fullname: Kuzum
– volume: 238
  start-page: 12
  year: 2009
  ident: C9NH00777F-(cit34)/*[position()=1]
  publication-title: Dev. Dyn.
  doi: 10.1002/dvdy.22113
  contributor:
    fullname: Parichy
– volume: 113
  start-page: 5
  year: 2013
  ident: C9NH00777F-(cit2)/*[position()=1]
  publication-title: Chem. Rev.
  doi: 10.1021/cr300335p
  contributor:
    fullname: Mao
– volume: 283
  start-page: 2
  year: 2005
  ident: C9NH00777F-(cit35)/*[position()=1]
  publication-title: Dev. Biol.
  doi: 10.1016/j.ydbio.2005.04.017
  contributor:
    fullname: Nakano
– volume: 35
  start-page: 23
  year: 2014
  ident: C9NH00777F-(cit48)/*[position()=1]
  publication-title: Biomaterials
  doi: 10.1016/j.biomaterials.2014.03.087
  contributor:
    fullname: Mao
– volume: 140
  start-page: 18
  year: 2013
  ident: C9NH00777F-(cit36)/*[position()=1]
  publication-title: Development
  doi: 10.1242/dev.099531
  contributor:
    fullname: Satou
– volume: 121
  start-page: 8
  year: 2014
  ident: C9NH00777F-(cit18)/*[position()=1]
  publication-title: J. Neural Transm.
  doi: 10.1007/s00702-013-1149-z
  contributor:
    fullname: Ambrosi
– volume: 344
  start-page: 6181
  year: 2014
  ident: C9NH00777F-(cit7)/*[position()=1]
  publication-title: Science
  doi: 10.1126/science.1246736
  contributor:
    fullname: Kostarelos
– volume: 16
  start-page: 9
  year: 2015
  ident: C9NH00777F-(cit14)/*[position()=1]
  publication-title: Front. Neurosci.
  contributor:
    fullname: Lewerenz
– volume: 490
  start-page: 192
  year: 2012
  ident: C9NH00777F-(cit1)/*[position()=1]
  publication-title: Nature
  doi: 10.1038/nature11458
  contributor:
    fullname: Novoselov
– volume: 324
  start-page: 5934
  year: 2009
  ident: C9NH00777F-(cit6)/*[position()=1]
  publication-title: Science
  doi: 10.1126/science.1158877
  contributor:
    fullname: Geim
– volume: 308
  start-page: 550
  year: 2007
  ident: C9NH00777F-(cit26)/*[position()=1]
  publication-title: J. Exp. Zool., Part B
  doi: 10.1002/jez.b.21127
  contributor:
    fullname: Fetcho
– volume: 68
  start-page: 1121
  year: 1992
  ident: C9NH00777F-(cit39)/*[position()=1]
  publication-title: J. Neurophysiol.
  doi: 10.1152/jn.1992.68.4.1121
  contributor:
    fullname: Carp
– volume: 69
  start-page: 6
  year: 2003
  ident: C9NH00777F-(cit22)/*[position()=1]
  publication-title: Prog. Neurobiol.
  doi: 10.1016/S0301-0082(03)00052-2
  contributor:
    fullname: Lewis
– volume: 34
  start-page: 4
  year: 2019
  ident: C9NH00777F-(cit51)/*[position()=1]
  publication-title: Environ. Toxicol.
  contributor:
    fullname: Yang
SSID ssj0001817983
Score 2.2742794
Snippet Graphene oxide (GO), an oxidised form of graphene, is widely used for biomedical applications, due to its dispersibility in water and simple surface chemistry...
SourceID proquest
crossref
SourceType Aggregation Database
StartPage 1250
SubjectTerms Biomedical materials
Graphene
In vivo methods and tests
Larvae
Nanomaterials
Nanosheets
Nervous system
Perturbation
Spinal cord
Swimming
Synapses
Zebrafish
Title Graphene oxide nanosheets modulate spinal glutamatergic transmission and modify locomotor behaviour in an in vivo zebrafish model
URI https://www.proquest.com/docview/2427313618/abstract/
https://search.proquest.com/docview/2415285198
Volume 5
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1Lj9MwELaW3QscEE9RWJAR3KIsSZyXj6tVuwWVIkGLyilybGebS7LqY0V747_wQ5lxnhUrBFysynUTy_N1Zjz-PEPIW8cFWcogtGUkfNsXfmDzOBS2lJHiwlNZaMoBfZyG47n_YREsjo5-9lhL2016Jve33iv5H6lCH8gVb8n-g2Tbh0IHfAb5QgsShvavZHyJ2aZBWVnl91xpqxBFuV5qvTEFbrAul7bW16bs1RVMQ4Bzqleg6bAuRLEGAa8bLjIMz7OdBYYNyXlI4Kxu72-RrA4jsL3Jb0prj-fMGWZBMiV0-q7tFN8OEtfWslzl-yYMiOcbeMBjlP1lLroIwFeYRS6rsHShVm3_l2WV1-DbdoeqqDUbZRtg_1ymu6Ifr_A6tlxDdMKoSENJNZSTurBdp_k8J8AbEVV68zN9S1-tuoMeQuOeGgavzemZdNerlOhv5sJhmG1V8gJrFUZR1hnFhggw_ZSM5pNJMhsuZnfIiRfxALb4J-fD2ftJF8uLMe0bkhnaWTaZcBl_1z3-0Pc5NP3Gn5k9IPfrjQg9r1D1kBzp4hG510tP-Zj8aPBFDb5ohy_a4ItW-KIH-KJ9fFGQLa3wRVt80RZfNMcR2CK-aIsvavD1hMxHw9nF2K5LdtiSuSyzwQJ4moGOj7kXp8JVsDBSMc18B8_3tCu8lAmThzMFRzh0BZdCpipVkgmHZewpOS7KQj8jNOXg2brw40ylPpMBD7RytYpV7Eo_S9MBedMsZnJdZWZJDKOC8eSCT8dmyUcDctqsc1L_c9cJuKURTDd04wF53X4Ny4KHZaLQ5RbHgGcL2xEeP__zI16Qux3MT8nxZrXVL8FR3aSvapz8Aqx4n7o
link.rule.ids 315,786,790,27957,27958
linkProvider Royal Society of Chemistry
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Graphene+oxide+nanosheets+modulate+spinal+glutamatergic+transmission+and+modify+locomotor+behaviour+in+an+in+vivo+zebrafish+model&rft.jtitle=Nanoscale+horizons&rft.au=Cellot%2C+Giada&rft.au=Vranic%2C+Sandra&rft.au=Shin%2C+Yuyoung&rft.au=Worsley%2C+Robyn&rft.date=2020-08-01&rft.pub=Royal+Society+of+Chemistry&rft.issn=2055-6764&rft.eissn=2055-6764&rft.volume=5&rft.issue=8&rft.spage=1250&rft.epage=1263&rft_id=info:doi/10.1039%2Fc9nh00777f&rft.externalDBID=NO_FULL_TEXT
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=2055-6756&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=2055-6756&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=2055-6756&client=summon