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BMC Physiology
Published in: BMC Physiology 1/2012

Open Access 01-12-2012 | Research article

VEGF induces sensory and motor peripheral plasticity, alters bladder function, and promotes visceral sensitivity

Authors: Anna P Malykhina, Qi Lei, Chris S Erickson, Miles L Epstein, Marcia R Saban, Carole A Davis, Ricardo Saban

Published in: BMC Physiology | Issue 1/2012

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Abstract

Background

This work tests the hypothesis that bladder instillation with vascular endothelial growth factor (VEGF) modulates sensory and motor nerve plasticity, and, consequently, bladder function and visceral sensitivity.
In addition to C57BL/6J, ChAT-cre mice were used for visualization of bladder cholinergic nerves. The direct effect of VEGF on the density of sensory nerves expressing the transient receptor potential vanilloid subfamily 1 (TRPV1) and cholinergic nerves (ChAT) was studied one week after one or two intravesical instillations of the growth factor.
To study the effects of VEGF on bladder function, mice were intravesically instilled with VEGF and urodynamic evaluation was assessed. VEGF-induced alteration in bladder dorsal root ganglion (DRG) neurons was performed on retrogradly labeled urinary bladder afferents by patch-clamp recording of voltage gated Na+ currents. Determination of VEGF-induced changes in sensitivity to abdominal mechanostimulation was performed by application of von Frey filaments.

Results

In addition to an overwhelming increase in TRPV1 immunoreactivity, VEGF instillation resulted in an increase in ChAT-directed expression of a fluorescent protein in several layers of the urinary bladder. Intravesical VEGF caused a profound change in the function of the urinary bladder: acute VEGF (1 week post VEGF treatment) reduced micturition pressure and longer treatment (2 weeks post-VEGF instillation) caused a substantial reduction in inter-micturition interval. In addition, intravesical VEGF resulted in an up-regulation of voltage gated Na+ channels (VGSC) in bladder DRG neurons and enhanced abdominal sensitivity to mechanical stimulation.

Conclusions

For the first time, evidence is presented indicating that VEGF instillation into the mouse bladder promotes a significant increase in peripheral nerve density together with alterations in bladder function and visceral sensitivity. The VEGF pathway is being proposed as a key modulator of neural plasticity in the pelvis and enhanced VEGF content may be associated with visceral hyperalgesia, abdominal discomfort, and/or pelvic pain.
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Literature
1.
Avelino A, Cruz F: TRPV1 (vanilloid receptor) in the urinary tract: expression, function and clinical applications. Naunyn Schmiedebergs Arch Pharmacol. 2006, 373 (4): 287-299. 10.1007/s00210-006-0073-2.CrossRefPubMed
2.
Andersson KE, Hedlund P: Pharmacologic perspective on the physiology of the lower urinary tract. Urology. 2002, 60 (5 Suppl 1): 13-20. discussion 20-11CrossRefPubMed
3.
Ford AP, Cockayne DA: ATP and P2X purinoceptors in urinary tract disorders. Handb Exp Pharmacol. 2011, 202: 485-526. 10.1007/978-3-642-16499-6_22.CrossRefPubMed
4.
Asfaw TS, Hypolite J, Northington GM, Arya LA, Wein AJ, Malykhina AP: Acute colonic inflammation triggers detrusor instability via activation of TRPV1 receptors in a rat model of pelvic organ cross-sensitization. Am J Physiol Regul Integr Comp Physiol. 2011, 300 (6): R1392-R1400. 10.1152/ajpregu.00804.2010.CrossRefPubMedPubMedCentral
5.
Saban R, Saban MR, Nguyen NB, Lu B, Gerard C, Gerard NP, Hammond TG: Neurokinin-1 (NK-1) receptor is required in antigen-induced cystitis. Am J Pathol. 2000, 156 (3): 775-780. 10.1016/S0002-9440(10)64944-9.CrossRefPubMedPubMedCentral
6.
Saban R, D'Andrea MR, Andrade-Gordon P, Derian CK, Dozmorov I, Ihnat MA, Hurst RE, Davis CA, Simpson C, Saban MR: Mandatory role of proteinase-activated receptor 1 in experimental bladder inflammation. BMC Physiol. 2007, 7: 4-10.1186/1472-6793-7-4.CrossRefPubMedPubMedCentral
7.
Schnegelsberg B, Sun TT, Cain G, Bhattacharya A, Nunn PA, Ford AP, Vizzard MA, Cockayne DA: Overexpression of NGF in mouse urothelium leads to neuronal hyperinnervation, pelvic sensitivity, and changes in urinary bladder function. Am J Physiol Regul Integr Comp Physiol. 2010, 298 (3): R534-R547. 10.1152/ajpregu.00367.2009.CrossRefPubMedPubMedCentral
8.
Alagiri M, Chottiner S, Ratner V, Slade D, Hanno PM: Interstitial cystitis: unexplained associations with other chronic disease and pain syndromes. Urology. 1997, 49 (5A Suppl): 52-57.CrossRefPubMed
9.
Lei Q, Malykhina AP: Colonic inflammation up-regulates voltage-gated sodium channels in bladder sensory neurons via activation of peripheral transient potential vanilloid 1 receptors. Neurogastroenterol Motil. 2012, 24 (6): 575-585. 10.1111/j.1365-2982.2012.01910.x. e257CrossRefPubMedPubMedCentral
10.
Martin P, Lewis J: Origins of the neurovascular bundle: interactions between developing nerves and blood vessels in embryonic chick skin. Int J Dev Biol. 1989, 33 (3): 379-387.PubMed
11.
Carmeliet P, Tessier-Lavigne M: Common mechanisms of nerve and blood vessel wiring. Nature. 2005, 436 (7048): 193-200. 10.1038/nature03875.CrossRefPubMed
12.
Mukouyama YS, Shin D, Britsch S, Taniguchi M, Anderson DJ: Sensory nerves determine the pattern of arterial differentiation and blood vessel branching in the skin. Cell. 2002, 109 (6): 693-705. 10.1016/S0092-8674(02)00757-2.CrossRefPubMed
13.
Yuan L, Moyon D, Pardanaud L, Breant C, Karkkainen MJ, Alitalo K, Eichmann A: Abnormal lymphatic vessel development in neuropilin 2 mutant mice. Development. 2002, 129 (20): 4797-4806.PubMed
14.
de Almodovar Ruiz C, Lambrechts D, Mazzone M, Carmeliet P: Role and therapeutic potential of VEGF in the nervous system. Physiol Rev. 2009, 89 (2): 607-648. 10.1152/physrev.00031.2008.CrossRef
15.
Charrua A, Reguenga C, Cordeiro JM, Correiade-Sa P, Paule C, Nagy I, Cruz F, Avelino A: Functional transient receptor potential vanilloid 1 is expressed in human urothelial cells. J Urol. 2009, 182 (6): 2944-2950. 10.1016/j.juro.2009.08.022.CrossRefPubMed
16.
Doran JF, Jackson P, Kynoch PA, Thompson RJ: Isolation of PGP 9.5, a new human neurone-specific protein detected by high-resolution two-dimensional electrophoresis. J Neurochem. 1983, 40 (6): 1542-1547. 10.1111/j.1471-4159.1983.tb08124.x.CrossRefPubMed
17.
Saban MR, Davis CA, Avelino A, Cruz F, Maier J, Bjorling DE, Sferra TJ, Hurst RE, Saban R: VEGF signaling mediates bladder neuroplasticity and inflammation in response to BCG. BMC Physiol. 2011, 11: 16-10.1186/1472-6793-11-16.CrossRefPubMedPubMedCentral
18.
Carmeliet P: Neuro-vascular link: from genetic insights to therapeutic perspectives. Bull Mem Acad R Med Belg. 2008, 163 (10-12): 445-451. discussion 451-442PubMed
19.
Avwenagha O, Campbell G, Bird MM: Distribution of GAP-43, beta-III tubulin and F-actin in developing and regenerating axons and their growth cones in vitro, following neurotrophin treatment. J Neurocytol. 2003, 32 (9): 1077-1089.CrossRefPubMed
20.
Birder LA, Wolf-Johnston AS, Sun Y, Chai TC: Alteration in TRPV1 and Muscarinic (M3) receptor expression and function in idiopathic overactive bladder urothelial cells. Acta Physiol (Oxf). 2013, 207 (1): 123-129. 10.1111/j.1748-1716.2012.02462.x.CrossRef
21.
Ritter AM, Martin WJ, Thorneloe KS: The voltage-gated sodium channel Nav1.9 is required for inflammation-based urinary bladder dysfunction. Neurosci Lett. 2009, 452 (1): 28-32. 10.1016/j.neulet.2008.12.051.CrossRefPubMed
22.
Carmeliet P: Blood vessels and nerves: common signals, pathways and diseases. Nat Rev Genet. 2003, 4 (9): 710-720. 10.1038/nrg1158.CrossRefPubMed
23.
Kuruvilla R, Zweifel LS, Glebova NO, Lonze BE, Valdez G, Ye H, Ginty DD: A neurotrophin signaling cascade coordinates sympathetic neuron development through differential control of TrkA trafficking and retrograde signaling. Cell. 2004, 118 (2): 243-255. 10.1016/j.cell.2004.06.021.CrossRefPubMed
24.
Tamaki M, Saito R, Ogawa O, Yoshimura N, Ueda T: Possible mechanisms inducing glomerulations in interstitial cystitis: relationship between endoscopic findings and expression of angiogenic growth factors. J Urol. 2004, 172 (3): 945-948. 10.1097/01.ju.0000135009.55905.cb.CrossRefPubMed
25.
Saban MR, Backer JM, Backer MV, Maier J, Fowler B, Davis CA, Simpson C, Wu X-R, Birder L, Freeman MR, Soker S, Saban R: VEGF receptors and neuropilins are expressed in the urothelial and neuronal cells in normal mouse urinary bladder and are up-regulated in inflammation. Am J Physiol Renal. 2008, 295: 10.1152/ajprenal.00618.02007.
26.
Saban R, Saban MR, Maier J, Fowler B, Tengowski M, Davis CA, Wu XR, Culkin DJ, Hauser P, Backer J, Hurst RE: Urothelial expression of neuropilins and VEGF receptors in control and interstitial cystitis patients. Am J Physiol Renal Physiol. 2008, 295 (6): F1613-F1623. 10.1152/ajprenal.90344.2008.CrossRefPubMedPubMedCentral
27.
Lee S, Chen TT, Barber CL, Jordan MC, Murdock J, Desai S, Ferrara N, Nagy A, Roos KP, Iruela-Arispe ML: Autocrine VEGF signaling is required for vascular homeostasis. Cell. 2007, 130 (4): 691-703. 10.1016/j.cell.2007.06.054.CrossRefPubMedPubMedCentral
28.
Sugimoto H, Hamano Y, Charytan D, Cosgrove D, Kieran M, Sudhakar A, Kalluri R: Neutralization of circulating vascular endothelial growth factor (VEGF) by anti-VEGF antibodies and soluble VEGF receptor 1 (sFlt-1) induces proteinuria. J Biol Chem. 2003, 278 (15): 12605-12608. 10.1074/jbc.C300012200.CrossRefPubMed
29.
Saban MR, Sferra TJ, Davis CA, Simpson C, Allen A, Maier J, Fowler B, Knowlton N, Birder L, Wu XR, Saban R: Neuropilin-VEGF signaling pathway acts as a key modulator of vascular, lymphatic, and inflammatory cell responses of the bladder to intravesical BCG treatment. Am J Physiol Renal Physiol. 2010, 299 (6): F1245-F1256. 10.1152/ajprenal.00352.2010.CrossRefPubMed
30.
Backer MV, Levashova Z, Patel V, Jehning BT, Claffey K, Blankenberg FG, Backer JM: Molecular imaging of VEGF receptors in angiogenic vasculature with single-chain VEGF based probes. Nat Med. 2007, 13 (4): 504-509. 10.1038/nm1522.CrossRefPubMed
31.
Saban R, Saban MR, Maier J, Fowler B, Tengowski M, Davis CA, Wu XR, Culkin DJ, Hauser P, Backer J, Hurst RE: Urothelial expression of neuropilins and VEGF receptors in control and interstitial cystitis patients. PMID: 18815217 American journal of physiology. Ren Physiol. 2008, 295 (6): F1613-F1623. 10.1152/ajprenal.90344.2008.CrossRef
32.
Saban MR, Backer JM, Backer MV, Maier J, Fowler B, Davis CA, Simpson C, Wu XR, Birder L, Freeman MR, Soker S, Hurst RE, Saban R: VEGF receptors and neuropilins are expressed in the urothelial and neuronal cells in normal mouse urinary bladder and are upregulated in inflammation. Am J Physiol Renal Physiol. 2008, 295 (1): F60-F72. 10.1152/ajprenal.00618.2007.CrossRefPubMedPubMedCentral
33.
Schmitt M, Horbach A, Kubitz R, Frilling A, Haussinger D: Disruption of hepatocellular tight junctions by vascular endothelial growth factor (VEGF): a novel mechanism for tumor invasion. J Hepatol. 2004, 41 (2): 274-283. 10.1016/j.jhep.2004.04.035.CrossRefPubMed
34.
Rodewald M, Herr D, Fraser HM, Hack G, Kreienberg R, Wulff C: Regulation of tight junction proteins occludin and claudin 5 in the primate ovary during the ovulatory cycle and after inhibition of vascular endothelial growth factor. Mol Hum Reprod. 2007, 13 (11): 781-789. 10.1093/molehr/gam066.CrossRefPubMed
35.
Nico B, Mangieri D, Crivellato E, Longo V, De Giorgis M, Capobianco C, Corsi P, Benagiano V, Roncali L, Ribatti D: HIF activation and VEGF overexpression are coupled with ZO-1 up-phosphorylation in the brain of dystrophic mdx mouse. Brain Pathol. 2007, 17 (4): 399-406. 10.1111/j.1750-3639.2007.00090.x.CrossRefPubMed
36.
Acharya P, Beckel J, Ruiz WG, Wang E, Rojas R, Birder L, Apodaca G: Distribution of the tight junction proteins ZO-1, occludin, and claudin-4, -8, and -12 in bladder epithelium. Am J Physiol Renal Physiol. 2004, 287 (2): F305-F318. 10.1152/ajprenal.00341.2003.CrossRefPubMed
37.
Saban MR, Sferra TJ, Davis CA, Simpson C, Allen A, Maier J, Fowler B, Knowlton N, Birder L, Wu XR, Saban R: Neuropilin-VEGF signaling pathway acts as a key modulator of vascular, lymphatic, and inflammatory cell responses of the bladder to intravesical BCG treatment. PMID: 20861073. Am J Physiol Renal Physiol. 2010, 299 (6): F1245-F1256. 10.1152/ajprenal.00352.2010.CrossRefPubMed
38.
Silva C, Avelino A, Souto-Moura C, Cruz F: A light- and electron-microscopic histopathological study of human bladder mucosa after intravesical resiniferatoxin application. BJU Int. 2001, 88 (4): 355-360. 10.1046/j.1464-410X.2001.02339.x.CrossRefPubMed
39.
Brockington A, Wharton SB, Fernando M, Gelsthorpe CH, Baxter L, Ince PG, Lewis CE, Shaw PJ: Expression of vascular endothelial growth factor and its receptors in the central nervous system in amyotrophic lateral sclerosis. J Neuropathol Exp Neurol. 2006, 65 (1): 26-36. 10.1097/01.jnen.0000196134.51217.74.CrossRefPubMed
40.
Ogunshola OO, Antic A, Donoghue MJ, Fan SY, Kim H, Stewart WB, Madri JA, Ment LR: Paracrine and autocrine functions of neuronal vascular endothelial growth factor (VEGF) in the central nervous system. J Biol Chem. 2002, 277 (13): 11410-11415. 10.1074/jbc.M111085200.CrossRefPubMed
41.
Damon DH: Vascular endothelial-derived semaphorin 3 inhibits sympathetic axon growth. Am J Physiol Heart Circ Physiol. 2006, 290 (3): H1220-H1225.CrossRefPubMed
42.
Marko SB, Damon DH: VEGF promotes vascular sympathetic innervation. Am J Physiol Heart Circ Physiol. 2008, 294 (6): H2646-H2652. 10.1152/ajpheart.00291.2008.CrossRefPubMed
43.
Freeman MR, Schneck FX, Gagnon ML, Corless C, Soker S, Niknejad K, Peoples GE, Klagsbrun M: Peripheral blood T lymphocytes and lymphocytes infiltrating human cancers express vascular endothelial growth factor: a potential role for T cells in angiogenesis. Cancer Res. 1995, 55 (18): 4140-4145.PubMed
44.
45.
46.
Burgu B, Medina Ortiz WE, Pitera JE, Woolf AS, Wilcox DT: Vascular endothelial growth factor mediates hypoxic stimulated embryonic bladder growth in organ culture. J Urol. 2007, 177 (4): 1552-1557. 10.1016/j.juro.2006.12.011.CrossRefPubMed
47.
Christmas TJ, Rode J, Chapple CR, Milroy EJ, Turner-Warwick RT: Nerve fibre proliferation in interstitial cystitis. Virchows Arch A Pathol Anat Histopathol. 1990, 416 (5): 447-451. 10.1007/BF01605152.CrossRefPubMed
48.
Lundeberg T, Liedberg H, Nordling L, Theodorsson E, Owzarski A, Ekman P: Interstitial cystitis: correlation with nerve fibres, mast cells and histamine. Br J Urol. 1993, 71 (4): 427-429. 10.1111/j.1464-410X.1993.tb15986.x.CrossRefPubMed
49.
Charrua A, Cruz CD, Cruz F, Avelino A: Transient receptor potential vanilloid subfamily 1 is essential for the generation of noxious bladder input and bladder overactivity in cystitis. J Urol. 2007, 177 (4): 1537-1541. 10.1016/j.juro.2006.11.046.CrossRefPubMed
50.
Dinis P, Charrua A, Avelino A, Yaqoob M, Bevan S, Nagy I, Cruz F: Anandamide-evoked activation of vanilloid receptor 1 contributes to the development of bladder hyperreflexia and nociceptive transmission to spinal dorsal horn neurons in cystitis. J Neurosci. 2004, 24 (50): 11253-11263. 10.1523/JNEUROSCI.2657-04.2004.CrossRefPubMed
51.
Wang ZY, Wang P, Merriam FV, Bjorling DE: Lack of TRPV1 inhibits cystitis-induced increased mechanical sensitivity in mice. Pain. 2008, 139 (1): 158-167. 10.1016/j.pain.2008.03.020.CrossRefPubMed
52.
Girard BM, Tompkins JD, Parsons RL, May V, Vizzard MA: Effects of CYP-induced cystitis on PACAP/VIP and receptor expression in micturition pathways and bladder function in mice with overexpression of NGF in urothelium. J Mol Neurosci. 2012, 48 (3): 730-743. 10.1007/s12031-012-9834-1.CrossRefPubMed
53.
Merrill L, Girard BM, May V, Vizzard MA: Transcriptional and translational plasticity in rodent urinary bladder TRP channels with urinary bladder inflammation, bladder dysfunction, or postnatal maturation. J Mol Neurosci. 2012, 48 (3): 744-756. 10.1007/s12031-012-9867-5.CrossRefPubMedPubMedCentral
54.
Lin G, Chen KC, Hsieh PS, Yeh CH, Lue TF, Lin CS: Neurotrophic effects of vascular endothelial growth factor and neurotrophins on cultured major pelvic ganglia. BJU Int. 2003, 92 (6): 631-635. 10.1046/j.1464-410X.2003.04439.x.CrossRefPubMed
55.
Lin G, Shindel AW, Fandel TM, Bella AJ, Lin CS, Lue TF: Neurotrophic effects of brain-derived neurotrophic factor and vascular endothelial growth factor in major pelvic ganglia of young and aged rats. BJU Int. 2010, 105 (1): 114-120. 10.1111/j.1464-410X.2009.08647.x.CrossRefPubMedPubMedCentral
56.
Stewart AL, Anderson RB, Kobayashi K, Young HM: Effects of NGF, NT-3 and GDNF family members on neurite outgrowth and migration from pelvic ganglia from embryonic and newborn mice. BMC Dev Biol. 2008, 8: 73-10.1186/1471-213X-8-73.CrossRefPubMedPubMedCentral
57.
Pereira Lopes FR, Lisboa BC, Frattini F, Almeida FM, Tomaz MA, Matsumoto PK, Langone F, Lora S, Melo PA, Borojevic R, Han SW, Martinez AM: Enhancement of sciatic nerve regeneration after vascular endothelial growth factor (VEGF) gene therapy. Neuropathol Appl Neurobiol. 2011, 37 (6): 600-612. 10.1111/j.1365-2990.2011.01159.x.CrossRefPubMed
58.
Nico B, Mangieri D, Benagiano V, Crivellato E, Ribatti D: Nerve growth factor as an angiogenic factor. Microvasc Res. 2008, 75 (2): 135-141. 10.1016/j.mvr.2007.07.004.CrossRefPubMed
59.
Fan BS, Lou JY: Enhancement of angiogenic effect of co-transfection human NGF and VEGF genes in rat bone marrow mesenchymal stem cells. Gene. 2011, 485 (2): 167-171. 10.1016/j.gene.2011.06.027.CrossRefPubMed
60.
Saygili E, Pekassa M, Saygili E, Rackauskas G, Hommes D, Noor-Ebad F, Gemein C, Zink MD, Schwinger RH, Weis J, Marx N, Schauerte P, Rana OR: Mechanical stretch of sympathetic neurons induces VEGF expression via a NGF and CNTF signaling pathway. Biochem Biophys Res Commun. 2011, 410 (1): 62-67. 10.1016/j.bbrc.2011.05.105.CrossRefPubMed
61.
Cesca F, Yabe A, Spencer-Dene B, Scholz-Starke J, Medrihan L, Maden CH, Gerhardt H, Orriss IR, Baldelli P, Al-Qatari M, Koltzenburg M, Adams RH, Benfenati F, Schiavo G: Kidins220/ARMS mediates the integration of the neurotrophin and VEGF pathways in the vascular and nervous systems. Cell Death Differ. 2012, 19 (2): 194-208. 10.1038/cdd.2011.141.CrossRefPubMedPubMedCentral
62.
Neubrand VE, Cesca F, Benfenati F, Schiavo G: Kidins220/ARMS as a functional mediator of multiple receptor signalling pathways. J Cell Sci. 2012, 125 (Pt 8): 1845-1854.CrossRefPubMed
63.
Sun B, Li Q, Dong L, Rong W: Ion channel and receptor mechanisms of bladder afferent nerve sensitivity. Auton Neurosci. 2010, 153 (1–2): 26-32.CrossRefPubMed
64.
Caterina MJ: Vanilloid receptors take a TRP beyond the sensory afferent. Pain. 2003, 105 (1–2): 5-9.CrossRefPubMed
65.
Dib-Hajj SD, Cummins TR, Black JA, Waxman SG: Sodium channels in normal and pathological pain. Annu Rev Neurosci. 2010, 33: 325-347. 10.1146/annurev-neuro-060909-153234.CrossRefPubMed
66.
Cheng Y, Keast JR: Effects of estrogens and bladder inflammation on mitogen-activated protein kinases in lumbosacral dorsal root ganglia from adult female rats. BMC Neurosci. 2009, 10: 156-10.1186/1471-2202-10-156.CrossRefPubMedPubMedCentral
67.
Yu SJ, Xia CM, Kay JC, Qiao LY: Activation of extracellular signal-regulated protein kinase 5 is essential for cystitis- and nerve growth factor-induced calcitonin gene-related peptide expression in sensory neurons. Mol Pain. 2012, 8 (1): 48-10.1186/1744-8069-8-48.CrossRefPubMedPubMedCentral
68.
Driscoll A, Teichman JM: How do patients with interstitial cystitis present?. J Urol. 2001, 166 (6): 2118-2120. 10.1016/S0022-5347(05)65517-6.CrossRefPubMed
69.
Yamaguchi O, Honda K, Nomiya M, Shishido K, Kakizaki H, Tanaka H, Yamanishi T, Homma Y, Takeda M, Araki I, Obara K, Nishizawa O, Igawa Y, Goto M, Yokoyama O, Seki N, Takei M, Yoshida M: Defining overactive bladder as hypersensitivity. Neurourol Urodyn. 2007, 26 (6 Suppl): 904-907.CrossRefPubMed
70.
Rush AM, Cummins TR, Waxman SG: Multiple sodium channels and their roles in electrogenesis within dorsal root ganglion neurons. J Physiol. 2007, 579 (Pt 1): 1-14.CrossRefPubMedPubMedCentral
71.
Waxman SG: Sodium channels, the electrogenisome and the electrogenistat: lessons and questions from the clinic. J Physiol. 2012, 590 (Pt 11): 2601-2612.CrossRefPubMedPubMedCentral
72.
Toledo-Aral JJ, Brehm P, Halegoua S, Mandel G: A single pulse of nerve growth factor triggers long-term neuronal excitability through sodium channel gene induction. Neuron. 1995, 14 (3): 607-611. 10.1016/0896-6273(95)90317-8.CrossRefPubMed
73.
Leffler A, Cummins TR, Dib-Hajj SD, Hormuzdiar WN, Black JA, Waxman SG: GDNF and NGF reverse changes in repriming of TTX-sensitive Na(+) currents following axotomy of dorsal root ganglion neurons. J Neurophysiol. 2002, 88 (2): 650-658.PubMed
74.
Dib-Hajj SD, Black JA, Cummins TR, Kenney AM, Kocsis JD, Waxman SG: Rescue of alpha-SNS sodium channel expression in small dorsal root ganglion neurons after axotomy by nerve growth factor in vivo. J Neurophysiol. 1998, 79 (5): 2668-2676.PubMed
75.
Liu CJ, Dib-Hajj SD, Black JA, Greenwood J, Lian Z, Waxman SG: Direct interaction with contactin targets voltage-gated sodium channel Na(v)1.9/NaN to the cell membrane. J Biol Chem. 2001, 276 (49): 46553-46561. 10.1074/jbc.M108699200.CrossRefPubMed
76.
Rush AM, Craner MJ, Kageyama T, Dib-Hajj SD, Waxman SG, Ranscht B: Contactin regulates the current density and axonal expression of tetrodotoxin-resistant but not tetrodotoxin-sensitive sodium channels in DRG neurons. Eur J Neurosci. 2005, 22 (1): 39-49. 10.1111/j.1460-9568.2005.04186.x.CrossRefPubMed
77.
Okuse K, Malik-Hall M, Baker MD, Poon WY, Kong H, Chao MV, Wood JN: Annexin II light chain regulates sensory neuron-specific sodium channel expression. Nature. 2002, 417 (6889): 653-656. 10.1038/nature00781.CrossRefPubMed
78.
Yang RH, Wang WT, Chen JY, Xie RG, Hu SJ: Gabapentin selectively reduces persistent sodium current in injured type-a dorsal root ganglion neurons. Pain. 2009, 143 (1–2): 48-55.CrossRefPubMed
79.
Wang W, Gu J, Li YQ, Tao YX: Are voltage-gated sodium channels on the dorsal root ganglion involved in the development of neuropathic pain?. Mol Pain. 2011, 7: 16-10.1186/1744-8069-7-16.CrossRefPubMedPubMedCentral
80.
Toth DM, Szoke E, Bolcskei K, Kvell K, Bender B, Bosze Z, Szolcsanyi J, Sandor Z: Nociception, neurogenic inflammation and thermoregulation in TRPV1 knockdown transgenic mice. Cell Mol Life Sci. 2011, 68 (15): 2589-2601. 10.1007/s00018-010-0569-2.CrossRefPubMed
81.
Dupont MC, Spitsbergen JM, Kim KB, Tuttle JB, Steers WD: Histological and neurotrophic changes triggered by varying models of bladder inflammation. J Urol. 2001, 166 (3): 1111-1118. 10.1016/S0022-5347(05)65931-9.CrossRefPubMed
82.
Bjorling DE, Wang ZY, Boldon K, Bushman W: Bacterial cystitis is accompanied by increased peripheral thermal sensitivity in mice. J Urol. 2008, 179 (2): 759-763. 10.1016/j.juro.2007.09.024.CrossRefPubMedPubMedCentral
83.
Guerios SD, Wang ZY, Boldon K, Bushman W, Bjorling DE: Blockade of NGF and trk receptors inhibits increased peripheral mechanical sensitivity accompanying cystitis in rats. Am J Physiol Regul Integr Comp Physiol. 2008, 295 (1): R111-R122. 10.1152/ajpregu.00728.2007.CrossRefPubMedPubMedCentral
84.
DeBerry J, Randich A, Shaffer AD, Robbins MT, Ness TJ: Neonatal bladder inflammation produces functional changes and alters neuropeptide content in bladders of adult female rats. J Pain. 2010, 11 (3): 247-255. 10.1016/j.jpain.2009.07.010.CrossRefPubMedPubMedCentral
85.
Randich A, Uzzell T, DeBerry JJ, Ness TJ: Neonatal urinary bladder inflammation produces adult bladder hypersensitivity. J Pain. 2006, 7 (7): 469-479. 10.1016/j.jpain.2006.01.450.CrossRefPubMed
86.
Robinson CJ, Stringer SE: The splice variants of vascular endothelial growth factor (VEGF) and their receptors. J Cell Sci. 2001, 114 (Pt 5): 853-865.PubMed
87.
Eichmann A, Makinen T, Alitalo K: Neural guidance molecules regulate vascular remodeling and vessel navigation. Genes Dev. 2005, 19 (9): 1013-1021. 10.1101/gad.1305405.CrossRefPubMed
88.
Tran J, Master Z, Yu JL, Rak J, Dumont DJ, Kerbel RS: A role for survivin in chemoresistance of endothelial cells mediated by VEGF. Proc Natl Acad Sci U S A. 2002, 99 (7): 4349-4354. 10.1073/pnas.072586399.CrossRefPubMedPubMedCentral
89.
Segarra M, Ohnuki H, Maric D, Salvucci O, Hou X, Kumar A, Li X, Tosato G: Semaphorin 6A regulates angiogenesis by modulating VEGF signaling. Blood. 2012, 120 (19): 4104-4115. 10.1182/blood-2012-02-410076.CrossRefPubMedPubMedCentral
90.
Yang S, Wu X, Luo C, Pan C, Pu J: Expression and clinical significance of hepaCAM and VEGF in urothelial carcinoma. World J Urol. 2010, 28 (4): 473-478. 10.1007/s00345-010-0573-z.CrossRefPubMed
91.
Saban MR, Nguyen NB, Hammond TG, Saban R: Gene expression profiling of mouse bladder inflammatory responses to LPS, substance P, and antigen-stimulation. Am J Pathol. 2002, 160 (6): 2095-2110. 10.1016/S0002-9440(10)61159-5.CrossRefPubMedPubMedCentral
92.
Yu W, Hill WG: Defining protein expression in the urothelium: a problem of more than transitional interest. Am J Physiol Renal Physiol. 2011, 301 (5): F932-942. 10.1152/ajprenal.00334.2011.CrossRefPubMedPubMedCentral
93.
Haarala M, Kiiholma P, Nurmi M, Uksila J, Alanen A: The role of Borrelia burgdorferi in interstitial cystitis. European urology. 2000, 37 (4): 395-399. 10.1159/000020184.CrossRefPubMed
94.
Charrua A, Cruz CD, Narayanan S, Gharat L, Gullapalli S, Cruz F, Avelino A: GRC-6211, a new oral specific TRPV1 antagonist, decreases bladder overactivity and noxious bladder input in cystitis animal models. J Urol. 2009, 181 (1): 379-386. 10.1016/j.juro.2008.08.121.CrossRefPubMed
95.
Finney-Hayward TK, Popa MO, Bahra P, Li S, Poll CT, Gosling M, Nicholson AG, Russell RE, Kon OM, Jarai G, Westwick J, Barnes PJ, Donnelly LE: Expression of transient receptor potential c6 channels in human lung macrophages. Am J Respir Cell Mol Biol. 2010, 43 (3): 296-304. 10.1165/rcmb.2008-0373OC.CrossRefPubMed
96.
Rudick CN, Chen MC, Mongiu AK, Klumpp DJ: Organ cross talk modulates pelvic pain. Am J Physiol Regul Integr Comp Physiol. 2007, 293 (3): R1191-1198. 10.1152/ajpregu.00411.2007.CrossRefPubMed
Metadata
Title
VEGF induces sensory and motor peripheral plasticity, alters bladder function, and promotes visceral sensitivity
Authors
Anna P Malykhina
Qi Lei
Chris S Erickson
Miles L Epstein
Marcia R Saban
Carole A Davis
Ricardo Saban
Publication date
01-12-2012
Publisher
BioMed Central
Published in
BMC Physiology / Issue 1/2012
Electronic ISSN: 1472-6793
DOI
https://doi.org/10.1186/1472-6793-12-15

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