Photobiomodulation Therapy Improves Acute Inflammatory Response in Mice: the Role of Cannabinoid Receptors/ATP-Sensitive K+ Channel/p38-MAPK Signalling Pathway
Although photobiomodulation therapy (PBM) has been applied clinically for the treatment of pain and inflammation, wound healing, sports and soft tissue injuries, as well as to repair injured spinal cords and peripheral nerves, it remains unclear which molecular substrates (receptor) are implicated i...
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| Veröffentlicht in: | Molecular neurobiology 2018-07, Vol.55 (7), p.5580-5593 |
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| creator | Neves, Laís M. S. Gonçalves, Elaine C. D. Cavalli, Juliana Vieira, Graziela Laurindo, Larissa R. Simões, Róli R. Coelho, Igor S. Santos, Adair R. S. Marcolino, Alexandre M. Cola, Maíra Dutra, Rafael C. |
| description | Although photobiomodulation therapy (PBM) has been applied clinically for the treatment of pain and inflammation, wound healing, sports and soft tissue injuries, as well as to repair injured spinal cords and peripheral nerves, it remains unclear which molecular substrates (receptor) are implicated in the cellular mechanisms of PBM. Here, we reported that PBM (660 nm, 30 mW, 0.06 cm
2
, 50 J/cm
2
, plantar irradiation) significantly inhibited carrageenan-induced paw oedema, but not noxious thermal response, through positive modulation to both CB1 and CB2 cannabinoid receptors. The use of CB1 antagonist AM281 or CB2 antagonist AM630 significantly reversed the anti-inflammatory effect of PBM. Analysis of signalling pathway downstream of cannabinoid receptors activation reveals that anti-inflammatory effects of PBM depend, in great extent, on its ability to activate ATP-dependent K
+
channels and p38 mitogen-activated protein kinase. Moreover, PBM therapy significantly reduced the levels of pro-inflammatory cytokine IL-6 in both paw and spinal cord, and restored the reduction of the level of anti-inflammatory cytokine IL-10 in spinal cord after carrageenan injection. Unlike the potent cannabinoid receptor agonist (WIN 55212-2), PBM did not exert any CNS-mediated effects in the tetrad assay. Finally, PBM does not reduce inflammation and noxious thermal response induced by LPS and zymosan, a TLR4 and TLR2/dectin-1 ligand, respectively. Thus, cannabinoid receptors and, possibly, the endocannabinoid system, represent an important site of action of PBM that opens the possibility of complementary and nonpsychotropic therapeutic interventions in clinical practice.
Graphical Abstract
ᅟ |
| doi_str_mv | 10.1007/s12035-017-0792-z |
| format | Article |
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2
, 50 J/cm
2
, plantar irradiation) significantly inhibited carrageenan-induced paw oedema, but not noxious thermal response, through positive modulation to both CB1 and CB2 cannabinoid receptors. The use of CB1 antagonist AM281 or CB2 antagonist AM630 significantly reversed the anti-inflammatory effect of PBM. Analysis of signalling pathway downstream of cannabinoid receptors activation reveals that anti-inflammatory effects of PBM depend, in great extent, on its ability to activate ATP-dependent K
+
channels and p38 mitogen-activated protein kinase. Moreover, PBM therapy significantly reduced the levels of pro-inflammatory cytokine IL-6 in both paw and spinal cord, and restored the reduction of the level of anti-inflammatory cytokine IL-10 in spinal cord after carrageenan injection. Unlike the potent cannabinoid receptor agonist (WIN 55212-2), PBM did not exert any CNS-mediated effects in the tetrad assay. Finally, PBM does not reduce inflammation and noxious thermal response induced by LPS and zymosan, a TLR4 and TLR2/dectin-1 ligand, respectively. Thus, cannabinoid receptors and, possibly, the endocannabinoid system, represent an important site of action of PBM that opens the possibility of complementary and nonpsychotropic therapeutic interventions in clinical practice.
Graphical Abstract
ᅟ</description><identifier>ISSN: 0893-7648</identifier><identifier>EISSN: 1559-1182</identifier><identifier>DOI: 10.1007/s12035-017-0792-z</identifier><identifier>PMID: 28980210</identifier><language>eng</language><publisher>New York: Springer US</publisher><subject>Animals ; Biomedical and Life Sciences ; Biomedicine ; Cannabinoid CB1 receptors ; Cannabinoid CB2 receptors ; Carrageenan ; Cell Biology ; Central nervous system ; Cytokines ; Cytokines - metabolism ; Edema ; Edema - complications ; Edema - pathology ; Edema - radiotherapy ; Endocannabinoid system ; Hyperalgesia - complications ; Hyperalgesia - pathology ; Immunomodulation ; Inflammation ; Inflammation - complications ; Inflammation - pathology ; Inflammation - radiotherapy ; Injuries ; Interleukin 10 ; Interleukin 6 ; Irradiation ; KATP Channels - metabolism ; Kinases ; Lectins, C-Type - metabolism ; Light therapy ; Lipopolysaccharides ; Low-Level Light Therapy ; Male ; MAP kinase ; MAP Kinase Signaling System ; Mice ; Models, Biological ; Neurobiology ; Neurology ; Neurosciences ; p38 Mitogen-Activated Protein Kinases - metabolism ; Pain ; Peripheral nerves ; Potassium channels ; Protein kinase ; Radiation ; Receptor, Cannabinoid, CB1 - metabolism ; Receptor, Cannabinoid, CB2 - metabolism ; Signal transduction ; Spinal cord ; Spinal Cord - pathology ; Therapeutic applications ; TLR2 protein ; TLR4 protein ; Toll-like receptors ; Toll-Like Receptors - metabolism ; Wound healing</subject><ispartof>Molecular neurobiology, 2018-07, Vol.55 (7), p.5580-5593</ispartof><rights>Springer Science+Business Media, LLC 2017</rights><rights>Molecular Neurobiology is a copyright of Springer, (2017). All Rights Reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c372t-e235a66a8fd60d0e287099d9d11c935525705b3e26ba78ab0139bb0e87dcb9763</citedby><cites>FETCH-LOGICAL-c372t-e235a66a8fd60d0e287099d9d11c935525705b3e26ba78ab0139bb0e87dcb9763</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s12035-017-0792-z$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s12035-017-0792-z$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>314,776,780,27901,27902,41464,42533,51294</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28980210$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Neves, Laís M. S.</creatorcontrib><creatorcontrib>Gonçalves, Elaine C. D.</creatorcontrib><creatorcontrib>Cavalli, Juliana</creatorcontrib><creatorcontrib>Vieira, Graziela</creatorcontrib><creatorcontrib>Laurindo, Larissa R.</creatorcontrib><creatorcontrib>Simões, Róli R.</creatorcontrib><creatorcontrib>Coelho, Igor S.</creatorcontrib><creatorcontrib>Santos, Adair R. S.</creatorcontrib><creatorcontrib>Marcolino, Alexandre M.</creatorcontrib><creatorcontrib>Cola, Maíra</creatorcontrib><creatorcontrib>Dutra, Rafael C.</creatorcontrib><title>Photobiomodulation Therapy Improves Acute Inflammatory Response in Mice: the Role of Cannabinoid Receptors/ATP-Sensitive K+ Channel/p38-MAPK Signalling Pathway</title><title>Molecular neurobiology</title><addtitle>Mol Neurobiol</addtitle><addtitle>Mol Neurobiol</addtitle><description>Although photobiomodulation therapy (PBM) has been applied clinically for the treatment of pain and inflammation, wound healing, sports and soft tissue injuries, as well as to repair injured spinal cords and peripheral nerves, it remains unclear which molecular substrates (receptor) are implicated in the cellular mechanisms of PBM. Here, we reported that PBM (660 nm, 30 mW, 0.06 cm
2
, 50 J/cm
2
, plantar irradiation) significantly inhibited carrageenan-induced paw oedema, but not noxious thermal response, through positive modulation to both CB1 and CB2 cannabinoid receptors. The use of CB1 antagonist AM281 or CB2 antagonist AM630 significantly reversed the anti-inflammatory effect of PBM. Analysis of signalling pathway downstream of cannabinoid receptors activation reveals that anti-inflammatory effects of PBM depend, in great extent, on its ability to activate ATP-dependent K
+
channels and p38 mitogen-activated protein kinase. Moreover, PBM therapy significantly reduced the levels of pro-inflammatory cytokine IL-6 in both paw and spinal cord, and restored the reduction of the level of anti-inflammatory cytokine IL-10 in spinal cord after carrageenan injection. Unlike the potent cannabinoid receptor agonist (WIN 55212-2), PBM did not exert any CNS-mediated effects in the tetrad assay. Finally, PBM does not reduce inflammation and noxious thermal response induced by LPS and zymosan, a TLR4 and TLR2/dectin-1 ligand, respectively. Thus, cannabinoid receptors and, possibly, the endocannabinoid system, represent an important site of action of PBM that opens the possibility of complementary and nonpsychotropic therapeutic interventions in clinical practice.
Graphical Abstract
ᅟ</description><subject>Animals</subject><subject>Biomedical and Life Sciences</subject><subject>Biomedicine</subject><subject>Cannabinoid CB1 receptors</subject><subject>Cannabinoid CB2 receptors</subject><subject>Carrageenan</subject><subject>Cell Biology</subject><subject>Central nervous system</subject><subject>Cytokines</subject><subject>Cytokines - metabolism</subject><subject>Edema</subject><subject>Edema - complications</subject><subject>Edema - pathology</subject><subject>Edema - radiotherapy</subject><subject>Endocannabinoid system</subject><subject>Hyperalgesia - complications</subject><subject>Hyperalgesia - pathology</subject><subject>Immunomodulation</subject><subject>Inflammation</subject><subject>Inflammation - complications</subject><subject>Inflammation - pathology</subject><subject>Inflammation - radiotherapy</subject><subject>Injuries</subject><subject>Interleukin 10</subject><subject>Interleukin 6</subject><subject>Irradiation</subject><subject>KATP Channels - metabolism</subject><subject>Kinases</subject><subject>Lectins, C-Type - metabolism</subject><subject>Light therapy</subject><subject>Lipopolysaccharides</subject><subject>Low-Level Light Therapy</subject><subject>Male</subject><subject>MAP kinase</subject><subject>MAP Kinase Signaling System</subject><subject>Mice</subject><subject>Models, Biological</subject><subject>Neurobiology</subject><subject>Neurology</subject><subject>Neurosciences</subject><subject>p38 Mitogen-Activated Protein Kinases - metabolism</subject><subject>Pain</subject><subject>Peripheral nerves</subject><subject>Potassium channels</subject><subject>Protein kinase</subject><subject>Radiation</subject><subject>Receptor, Cannabinoid, CB1 - metabolism</subject><subject>Receptor, Cannabinoid, CB2 - metabolism</subject><subject>Signal transduction</subject><subject>Spinal cord</subject><subject>Spinal Cord - pathology</subject><subject>Therapeutic applications</subject><subject>TLR2 protein</subject><subject>TLR4 protein</subject><subject>Toll-like receptors</subject><subject>Toll-Like Receptors - metabolism</subject><subject>Wound healing</subject><issn>0893-7648</issn><issn>1559-1182</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><recordid>eNp1kV1rFDEUhoModq3-AG8k4I0gcfPRTBLvlsWPpS0u7XodMjNndlJmkulkprL9M_5VU7YqCF7lQJ73PQkPQq8Z_cAoVcvEOBWSUKYIVYaT-ydowaQ0hDHNn6IF1UYQVZzpE_QipRtKOWdUPUcnXBtN87xAP7dtnGLpYx_ruXOTjwHvWhjdcMCbfhjjHSS8quYJ8CY0net7N8XxgK8gDTEkwD7gS1_BRzy1gK9iBzg2eO1CcKUP0deZrGDImbRc7bbkGkLyk78DfP4er9vMQbcchCaXq-05vvb74LrOhz3euqn94Q4v0bPGdQlePZ6n6PvnT7v1V3Lx7ctmvboglVB8IsCFdEXhdFMXtKbAtaLG1KZmrDJCSi4VlaUAXpROaVdSJkxZUtCqrkqjCnGK3h1785dvZ0iT7X2qoOtcgDgny8yZKpiRhcro23_QmziP-d3Jciq51lxpkSl2pKoxpjRCY4fR9248WEbtgz17tGezPftgz97nzJvH5rnsof6T-K0rA_wIpHwV9jD-Xf3_1l9RI6YA</recordid><startdate>20180701</startdate><enddate>20180701</enddate><creator>Neves, Laís M. 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S. ; Gonçalves, Elaine C. D. ; Cavalli, Juliana ; Vieira, Graziela ; Laurindo, Larissa R. ; Simões, Róli R. ; Coelho, Igor S. ; Santos, Adair R. S. ; Marcolino, Alexandre M. ; Cola, Maíra ; Dutra, Rafael C.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c372t-e235a66a8fd60d0e287099d9d11c935525705b3e26ba78ab0139bb0e87dcb9763</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Animals</topic><topic>Biomedical and Life Sciences</topic><topic>Biomedicine</topic><topic>Cannabinoid CB1 receptors</topic><topic>Cannabinoid CB2 receptors</topic><topic>Carrageenan</topic><topic>Cell Biology</topic><topic>Central nervous system</topic><topic>Cytokines</topic><topic>Cytokines - metabolism</topic><topic>Edema</topic><topic>Edema - complications</topic><topic>Edema - pathology</topic><topic>Edema - radiotherapy</topic><topic>Endocannabinoid system</topic><topic>Hyperalgesia - complications</topic><topic>Hyperalgesia - pathology</topic><topic>Immunomodulation</topic><topic>Inflammation</topic><topic>Inflammation - complications</topic><topic>Inflammation - pathology</topic><topic>Inflammation - radiotherapy</topic><topic>Injuries</topic><topic>Interleukin 10</topic><topic>Interleukin 6</topic><topic>Irradiation</topic><topic>KATP Channels - metabolism</topic><topic>Kinases</topic><topic>Lectins, C-Type - metabolism</topic><topic>Light therapy</topic><topic>Lipopolysaccharides</topic><topic>Low-Level Light Therapy</topic><topic>Male</topic><topic>MAP kinase</topic><topic>MAP Kinase Signaling System</topic><topic>Mice</topic><topic>Models, Biological</topic><topic>Neurobiology</topic><topic>Neurology</topic><topic>Neurosciences</topic><topic>p38 Mitogen-Activated Protein Kinases - metabolism</topic><topic>Pain</topic><topic>Peripheral nerves</topic><topic>Potassium channels</topic><topic>Protein kinase</topic><topic>Radiation</topic><topic>Receptor, Cannabinoid, CB1 - metabolism</topic><topic>Receptor, Cannabinoid, CB2 - metabolism</topic><topic>Signal transduction</topic><topic>Spinal cord</topic><topic>Spinal Cord - pathology</topic><topic>Therapeutic applications</topic><topic>TLR2 protein</topic><topic>TLR4 protein</topic><topic>Toll-like receptors</topic><topic>Toll-Like Receptors - metabolism</topic><topic>Wound healing</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Neves, Laís M. 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S.</creatorcontrib><creatorcontrib>Marcolino, Alexandre M.</creatorcontrib><creatorcontrib>Cola, Maíra</creatorcontrib><creatorcontrib>Dutra, Rafael C.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Health & Medical Complete (ProQuest)</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Psychology Database (Alumni)</collection><collection>Science Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>AUTh Library subscriptions: ProQuest Central</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biological Sciences</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>PML(ProQuest Medical Library)</collection><collection>ProQuest Psychology</collection><collection>ProQuest Science Journals</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>ProQuest One Psychology</collection><collection>ProQuest Central Basic</collection><collection>MEDLINE - Academic</collection><jtitle>Molecular neurobiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Neves, Laís M. S.</au><au>Gonçalves, Elaine C. D.</au><au>Cavalli, Juliana</au><au>Vieira, Graziela</au><au>Laurindo, Larissa R.</au><au>Simões, Róli R.</au><au>Coelho, Igor S.</au><au>Santos, Adair R. S.</au><au>Marcolino, Alexandre M.</au><au>Cola, Maíra</au><au>Dutra, Rafael C.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Photobiomodulation Therapy Improves Acute Inflammatory Response in Mice: the Role of Cannabinoid Receptors/ATP-Sensitive K+ Channel/p38-MAPK Signalling Pathway</atitle><jtitle>Molecular neurobiology</jtitle><stitle>Mol Neurobiol</stitle><addtitle>Mol Neurobiol</addtitle><date>2018-07-01</date><risdate>2018</risdate><volume>55</volume><issue>7</issue><spage>5580</spage><epage>5593</epage><pages>5580-5593</pages><issn>0893-7648</issn><eissn>1559-1182</eissn><abstract>Although photobiomodulation therapy (PBM) has been applied clinically for the treatment of pain and inflammation, wound healing, sports and soft tissue injuries, as well as to repair injured spinal cords and peripheral nerves, it remains unclear which molecular substrates (receptor) are implicated in the cellular mechanisms of PBM. Here, we reported that PBM (660 nm, 30 mW, 0.06 cm
2
, 50 J/cm
2
, plantar irradiation) significantly inhibited carrageenan-induced paw oedema, but not noxious thermal response, through positive modulation to both CB1 and CB2 cannabinoid receptors. The use of CB1 antagonist AM281 or CB2 antagonist AM630 significantly reversed the anti-inflammatory effect of PBM. Analysis of signalling pathway downstream of cannabinoid receptors activation reveals that anti-inflammatory effects of PBM depend, in great extent, on its ability to activate ATP-dependent K
+
channels and p38 mitogen-activated protein kinase. Moreover, PBM therapy significantly reduced the levels of pro-inflammatory cytokine IL-6 in both paw and spinal cord, and restored the reduction of the level of anti-inflammatory cytokine IL-10 in spinal cord after carrageenan injection. Unlike the potent cannabinoid receptor agonist (WIN 55212-2), PBM did not exert any CNS-mediated effects in the tetrad assay. Finally, PBM does not reduce inflammation and noxious thermal response induced by LPS and zymosan, a TLR4 and TLR2/dectin-1 ligand, respectively. Thus, cannabinoid receptors and, possibly, the endocannabinoid system, represent an important site of action of PBM that opens the possibility of complementary and nonpsychotropic therapeutic interventions in clinical practice.
Graphical Abstract
ᅟ</abstract><cop>New York</cop><pub>Springer US</pub><pmid>28980210</pmid><doi>10.1007/s12035-017-0792-z</doi><tpages>14</tpages></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 0893-7648 |
| ispartof | Molecular neurobiology, 2018-07, Vol.55 (7), p.5580-5593 |
| issn | 0893-7648 1559-1182 |
| language | eng |
| recordid | cdi_proquest_miscellaneous_1947619567 |
| source | MEDLINE; SpringerLink (Online service) |
| subjects | Animals Biomedical and Life Sciences Biomedicine Cannabinoid CB1 receptors Cannabinoid CB2 receptors Carrageenan Cell Biology Central nervous system Cytokines Cytokines - metabolism Edema Edema - complications Edema - pathology Edema - radiotherapy Endocannabinoid system Hyperalgesia - complications Hyperalgesia - pathology Immunomodulation Inflammation Inflammation - complications Inflammation - pathology Inflammation - radiotherapy Injuries Interleukin 10 Interleukin 6 Irradiation KATP Channels - metabolism Kinases Lectins, C-Type - metabolism Light therapy Lipopolysaccharides Low-Level Light Therapy Male MAP kinase MAP Kinase Signaling System Mice Models, Biological Neurobiology Neurology Neurosciences p38 Mitogen-Activated Protein Kinases - metabolism Pain Peripheral nerves Potassium channels Protein kinase Radiation Receptor, Cannabinoid, CB1 - metabolism Receptor, Cannabinoid, CB2 - metabolism Signal transduction Spinal cord Spinal Cord - pathology Therapeutic applications TLR2 protein TLR4 protein Toll-like receptors Toll-Like Receptors - metabolism Wound healing |
| title | Photobiomodulation Therapy Improves Acute Inflammatory Response in Mice: the Role of Cannabinoid Receptors/ATP-Sensitive K+ Channel/p38-MAPK Signalling Pathway |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-01T08%3A27%3A35IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_cross&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Photobiomodulation%20Therapy%20Improves%20Acute%20Inflammatory%20Response%20in%20Mice:%20the%20Role%20of%20Cannabinoid%20Receptors/ATP-Sensitive%20K+%20Channel/p38-MAPK%20Signalling%20Pathway&rft.jtitle=Molecular%20neurobiology&rft.au=Neves,%20La%C3%ADs%20M.%20S.&rft.date=2018-07-01&rft.volume=55&rft.issue=7&rft.spage=5580&rft.epage=5593&rft.pages=5580-5593&rft.issn=0893-7648&rft.eissn=1559-1182&rft_id=info:doi/10.1007/s12035-017-0792-z&rft_dat=%3Cproquest_cross%3E1947619567%3C/proquest_cross%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2052882783&rft_id=info:pmid/28980210&rfr_iscdi=true |