Regulation of alternative VEGF-A mRNA splicing is a therapeutic target for analgesia

Abstract Vascular endothelial growth factor-A (VEGF-A) is best known as a key regulator of the formation of new blood vessels. Neutralization of VEGF-A with anti-VEGF therapy e.g. bevacizumab, can be painful, and this is hypothesized to result from a loss of VEGF-A-mediated neuroprotection. The mult...

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Published in	Neurobiology of disease Vol. 71; pp. 245 - 259
Main Authors	Hulse, R.P, Beazley-Long, N, Hua, J, Kennedy, H, Prager, J, Bevan, H, Qiu, Y, Fernandes, E.S, Gammons, M.V, Ballmer-Hofer, K, Gittenberger de Groot, A.C, Churchill, A.J, Harper, S.J, Brain, S.D, Bates, D.O, Donaldson, L.F
Format	Journal Article
Language	English
Published	United States Elsevier Inc 01.11.2014 Academic Press Elsevier
Subjects	Alternative mRNA splicing Animals Antibodies - pharmacology Antibodies - therapeutic use Benzofurans Disease Models, Animal DNA, Recombinant - genetics Enzyme Inhibitors - pharmacology Enzyme Inhibitors - therapeutic use Ganglia, Spinal - cytology Hyperalgesia - metabolism Male Mice Mice, Transgenic Neural Conduction - genetics Neuralgia - metabolism Neuralgia - therapy Neurology Neuropathy Nociceptors Pain Measurement Pain Threshold - physiology Quinolines Rats Rats, Wistar RNA, Messenger - genetics RNA, Messenger - metabolism Sensory Receptor Cells - drug effects Sensory Receptor Cells - metabolism TRPV Cation Channels - deficiency TRPV Cation Channels - genetics Vascular endothelial growth factor A Vascular Endothelial Growth Factor A - genetics Vascular Endothelial Growth Factor A - immunology Vascular Endothelial Growth Factor A - metabolism VEGFR2 vascular endothelial growth factor receptor 2 serine arginine protein kinase 1 isolectin B4 SRSF1 transient receptor potential vanilloid 1 dorsal root ganglia vascular endothelial growth factor-A serine arginine splice factor 1 TRPV1 Neuropathy VEGF-A partial saphenous nerve ligation injury Alternative mRNA splicing SRPK1 CV Vascular endothelial growth factor A conduction velocity DRG Nociceptors IB4 PSNI
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Abstract	Abstract Vascular endothelial growth factor-A (VEGF-A) is best known as a key regulator of the formation of new blood vessels. Neutralization of VEGF-A with anti-VEGF therapy e.g. bevacizumab, can be painful, and this is hypothesized to result from a loss of VEGF-A-mediated neuroprotection. The multiple vegf-a gene products consist of two alternatively spliced families, typified by VEGF-A165 a and VEGF-A165 b (both contain 165 amino acids), both of which are neuroprotective. Under pathological conditions, such as in inflammation and cancer, the pro-angiogenic VEGF-A165 a is upregulated and predominates over the VEGF-A165 b isoform. We show here that in rats and mice VEGF-A165 a and VEGF-A165 b have opposing effects on pain, and that blocking the proximal splicing event – leading to the preferential expression of VEGF-A165 b over VEGF165 a – prevents pain in vivo. VEGF-A165 a sensitizes peripheral nociceptive neurons through actions on VEGFR2 and a TRPV1-dependent mechanism, thus enhancing nociceptive signaling. VEGF-A165 b blocks the effect of VEGF-A165 a. After nerve injury, the endogenous balance of VEGF-A isoforms switches to greater expression of VEGF-Axxx a compared to VEGF-Axxx b, through an SRPK1-dependent pre-mRNA splicing mechanism. Pharmacological inhibition of SRPK1 after traumatic nerve injury selectively reduced VEGF-Axxx a expression and reversed associated neuropathic pain. Exogenous VEGF-A165 b also ameliorated neuropathic pain. We conclude that the relative levels of alternatively spliced VEGF-A isoforms are critical for pain modulation under both normal conditions and in sensory neuropathy. Altering VEGF-Axxx a/VEGF-Axxx b balance by targeting alternative RNA splicing may be a new analgesic strategy.
AbstractList	Abstract Vascular endothelial growth factor-A (VEGF-A) is best known as a key regulator of the formation of new blood vessels. Neutralization of VEGF-A with anti-VEGF therapy e.g. bevacizumab, can be painful, and this is hypothesized to result from a loss of VEGF-A-mediated neuroprotection. The multiple vegf-a gene products consist of two alternatively spliced families, typified by VEGF-A165 a and VEGF-A165 b (both contain 165 amino acids), both of which are neuroprotective. Under pathological conditions, such as in inflammation and cancer, the pro-angiogenic VEGF-A165 a is upregulated and predominates over the VEGF-A165 b isoform. We show here that in rats and mice VEGF-A165 a and VEGF-A165 b have opposing effects on pain, and that blocking the proximal splicing event – leading to the preferential expression of VEGF-A165 b over VEGF165 a – prevents pain in vivo. VEGF-A165 a sensitizes peripheral nociceptive neurons through actions on VEGFR2 and a TRPV1-dependent mechanism, thus enhancing nociceptive signaling. VEGF-A165 b blocks the effect of VEGF-A165 a. After nerve injury, the endogenous balance of VEGF-A isoforms switches to greater expression of VEGF-Axxx a compared to VEGF-Axxx b, through an SRPK1-dependent pre-mRNA splicing mechanism. Pharmacological inhibition of SRPK1 after traumatic nerve injury selectively reduced VEGF-Axxx a expression and reversed associated neuropathic pain. Exogenous VEGF-A165 b also ameliorated neuropathic pain. We conclude that the relative levels of alternatively spliced VEGF-A isoforms are critical for pain modulation under both normal conditions and in sensory neuropathy. Altering VEGF-Axxx a/VEGF-Axxx b balance by targeting alternative RNA splicing may be a new analgesic strategy. Vascular endothelial growth factor-A (VEGF-A) is best known as a key regulator of the formation of new blood vessels. Neutralization of VEGF-A with anti-VEGF therapy e.g. bevacizumab, can be painful, and this is hypothesized to result from a loss of VEGF-A-mediated neuroprotection. The multiple vegf-a gene products consist of two alternatively spliced families, typified by VEGF-A 165 a and VEGF-A 165 b (both contain 165 amino acids), both of which are neuroprotective. Under pathological conditions, such as in inflammation and cancer, the pro-angiogenic VEGF-A 165 a is upregulated and predominates over the VEGF-A 165 b isoform. We show here that in rats and mice VEGF-A 165 a and VEGF-A 165 b have opposing effects on pain, and that blocking the proximal splicing event – leading to the preferential expression of VEGF-A 165 b over VEGF 165 a – prevents pain in vivo. VEGF-A 165 a sensitizes peripheral nociceptive neurons through actions on VEGFR2 and a TRPV1-dependent mechanism, thus enhancing nociceptive signaling. VEGF-A 165 b blocks the effect of VEGF-A 165 a. After nerve injury, the endogenous balance of VEGF-A isoforms switches to greater expression of VEGF-A xxx a compared to VEGF-A xxx b, through an SRPK1-dependent pre-mRNA splicing mechanism. Pharmacological inhibition of SRPK1 after traumatic nerve injury selectively reduced VEGF-A xxx a expression and reversed associated neuropathic pain. Exogenous VEGF-A 165 b also ameliorated neuropathic pain. We conclude that the relative levels of alternatively spliced VEGF-A isoforms are critical for pain modulation under both normal conditions and in sensory neuropathy. Altering VEGF-A xxx a/VEGF-A xxx b balance by targeting alternative RNA splicing may be a new analgesic strategy. • The different vegf-a splice variants, VEGF-A 165 a and VEGF-A 165 b have pro- and anti-nociceptive actions respectively. • Pro-nociceptive actions of VEGF-A 165 a are dependent on TRPV1. • Alternative pre-mRNA splicing underpins peripheral sensitization by VEGF-A isoforms in normal and neuropathic animals. Vascular endothelial growth factor-A (VEGF-A) is best known as a key regulator of the formation of new blood vessels. Neutralization of VEGF-A with anti-VEGF therapy e.g. bevacizumab, can be painful, and this is hypothesized to result from a loss of VEGF-A-mediated neuroprotection. The multiple vegf-a gene products consist of two alternatively spliced families, typified by VEGF-A165a and VEGF-A165b (both contain 165 amino acids), both of which are neuroprotective. Under pathological conditions, such as in inflammation and cancer, the pro-angiogenic VEGF-A165a is upregulated and predominates over the VEGF-A165b isoform.We show here that in rats and mice VEGF-A165a and VEGF-A165b have opposing effects on pain, and that blocking the proximal splicing event – leading to the preferential expression of VEGF-A165b over VEGF165a – prevents pain in vivo. VEGF-A165a sensitizes peripheral nociceptive neurons through actions on VEGFR2 and a TRPV1-dependent mechanism, thus enhancing nociceptive signaling. VEGF-A165b blocks the effect of VEGF-A165a.After nerve injury, the endogenous balance of VEGF-A isoforms switches to greater expression of VEGF-Axxxa compared to VEGF-Axxxb, through an SRPK1-dependent pre-mRNA splicing mechanism. Pharmacological inhibition of SRPK1 after traumatic nerve injury selectively reduced VEGF-Axxxa expression and reversed associated neuropathic pain. Exogenous VEGF-A165b also ameliorated neuropathic pain.We conclude that the relative levels of alternatively spliced VEGF-A isoforms are critical for pain modulation under both normal conditions and in sensory neuropathy. Altering VEGF-Axxxa/VEGF-Axxxb balance by targeting alternative RNA splicing may be a new analgesic strategy. Vascular endothelial growth factor-A (VEGF-A) is best known as a key regulator of the formation of new blood vessels. Neutralization of VEGF-A with anti-VEGF therapy e.g. bevacizumab, can be painful, and this is hypothesized to result from a loss of VEGF-A-mediated neuroprotection. The multiple vegf-a gene products consist of two alternatively spliced families, typified by VEGF-A165a and VEGF-A165b (both contain 165 amino acids), both of which are neuroprotective. Under pathological conditions, such as in inflammation and cancer, the pro-angiogenic VEGF-A165a is upregulated and predominates over the VEGF-A165b isoform. We show here that in rats and mice VEGF-A165a and VEGF-A165b have opposing effects on pain, and that blocking the proximal splicing event – leading to the preferential expression of VEGF-A165b over VEGF165a – prevents pain in vivo. VEGF-A165a sensitizes peripheral nociceptive neurons through actions on VEGFR2 and a TRPV1-dependent mechanism, thus enhancing nociceptive signaling. VEGF-A165b blocks the effect of VEGF-A165a. After nerve injury, the endogenous balance of VEGF-A isoforms switches to greater expression of VEGF-Axxxa compared to VEGF-Axxxb, through an SRPK1-dependent pre-mRNA splicing mechanism. Pharmacological inhibition of SRPK1 after traumatic nerve injury selectively reduced VEGF-Axxxa expression and reversed associated neuropathic pain. Exogenous VEGF-A165b also ameliorated neuropathic pain. We conclude that the relative levels of alternatively spliced VEGF-A isoforms are critical for pain modulation under both normal conditions and in sensory neuropathy. Altering VEGF-Axxxa/VEGF-Axxxb balance by targeting alternative RNA splicing may be a new analgesic strategy. [Display omitted] •The different vegf-a splice variants, VEGF-A165a and VEGF-A165b have pro- and anti-nociceptive actions respectively.•Pro-nociceptive actions of VEGF-A165a are dependent on TRPV1.•Alternative pre-mRNA splicing underpins peripheral sensitization by VEGF-A isoforms in normal and neuropathic animals.
Author	Hulse, R.P Churchill, A.J Gittenberger de Groot, A.C Brain, S.D Harper, S.J Donaldson, L.F Prager, J Kennedy, H Beazley-Long, N Ballmer-Hofer, K Hua, J Fernandes, E.S Gammons, M.V Bevan, H Bates, D.O Qiu, Y
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BackLink	https://www.ncbi.nlm.nih.gov/pubmed/25151644$$D View this record in MEDLINE/PubMed
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Keywords	VEGFR2 vascular endothelial growth factor receptor 2 serine arginine protein kinase 1 isolectin B4 SRSF1 transient receptor potential vanilloid 1 dorsal root ganglia vascular endothelial growth factor-A serine arginine splice factor 1 TRPV1 Neuropathy VEGF-A partial saphenous nerve ligation injury Alternative mRNA splicing SRPK1 CV Vascular endothelial growth factor A conduction velocity DRG Nociceptors IB4 PSNI
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 These authors contributed equally to this work.
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Snippet	Abstract Vascular endothelial growth factor-A (VEGF-A) is best known as a key regulator of the formation of new blood vessels. Neutralization of VEGF-A with... Vascular endothelial growth factor-A (VEGF-A) is best known as a key regulator of the formation of new blood vessels. Neutralization of VEGF-A with anti-VEGF...
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SubjectTerms	Alternative mRNA splicing Animals Antibodies - pharmacology Antibodies - therapeutic use Benzofurans Disease Models, Animal DNA, Recombinant - genetics Enzyme Inhibitors - pharmacology Enzyme Inhibitors - therapeutic use Ganglia, Spinal - cytology Hyperalgesia - metabolism Male Mice Mice, Transgenic Neural Conduction - genetics Neuralgia - metabolism Neuralgia - therapy Neurology Neuropathy Nociceptors Pain Measurement Pain Threshold - physiology Quinolines Rats Rats, Wistar RNA, Messenger - genetics RNA, Messenger - metabolism Sensory Receptor Cells - drug effects Sensory Receptor Cells - metabolism TRPV Cation Channels - deficiency TRPV Cation Channels - genetics Vascular endothelial growth factor A Vascular Endothelial Growth Factor A - genetics Vascular Endothelial Growth Factor A - immunology Vascular Endothelial Growth Factor A - metabolism
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Title	Regulation of alternative VEGF-A mRNA splicing is a therapeutic target for analgesia
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