Transforming growth factor beta induces sensory neuronal hyperexcitability, and contributes to pancreatic pain and hyperalgesia in rats with chronic pancreatitis

Molecular Pain

Volumn 8, Issue , 2012, Pages

  Zhu, Yaohui ^a   Colak, Tugba ^b   Shenoy, Mohan ^b   Liu, Liansheng ^a   Mehta, Kshama ^b   Pai, Reetesh ^d   Zou, Bende ^c   Xie, Xinmin S ^b,c   Pasricha, Pankaj J ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c AfaSci Inc   (United States)

^d UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Chronic pain; Chronic pancreatitis; Kv channels; Neuronal sensitization; Sensory neurons; Transforming growth factor beta

Indexed keywords

POTASSIUM CHANNEL KV1.4; TRANSFORMING GROWTH FACTOR BETA; VOLTAGE GATED POTASSIUM CHANNEL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHRONIC INFLAMMATION; CHRONIC PANCREATITIS; CONTROLLED STUDY; DOWN REGULATION; ELECTROSTIMULATION; HYPERALGESIA; IN VITRO STUDY; IN VIVO STUDY; KCNA4 GENE; NERVE EXCITABILITY; NEUROMODULATION; NOCICEPTION; NONHUMAN; PAIN RECEPTOR; POTASSIUM CURRENT; PRIORITY JOURNAL; RAT; SENSORY NERVE; SPINAL GANGLION;

ANIMALS; CELLS, CULTURED; ELECTROPHYSIOLOGY; GANGLIA, SPINAL; HYPERALGESIA; IMMUNOHISTOCHEMISTRY; KV1.4 POTASSIUM CHANNEL; MALE; PANCREATITIS, CHRONIC; RATS; RATS, SPRAGUE-DAWLEY; SENSORY RECEPTOR CELLS; TRANSFORMING GROWTH FACTOR BETA;

EID: 84865996297     PISSN: None     EISSN: 17448069     Source Type: Journal    
DOI: 10.1186/1744-8069-8-65     Document Type: Article

References (36)

1. Cheng JK, Ji RR. Intracellular signaling in primary sensory neurons and persistent pain. Neurochem Res 2008, 33:1970-1978. 10.1007/s11064-008-9711-z, 2570619, 18427980.
2. Bottner M, Krieglstein K, Unsicker K. The transforming growth factor-betas: structure, signaling, and roles in nervous system development and functions. J Neurochem 2000, 75:2227-2240.
3. Pohlers D, Brenmoehl J, Loffler I, et al. TGF-beta and fibrosis in different organs - molecular pathway imprints. Biochim Biophys Acta 2009, 1792:746-756. 10.1016/j.bbadis.2009.06.004, 19539753.
4. Delree P, Ribbens C, Martin D, et al. Plasticity of developing and adult dorsal root ganglion neurons as revealed in vitro. Brain Res Bull 1993, 30:231-237. 10.1016/0361-9230(93)90249-B, 8457871.
5. Stark B, Carlstedt T, Risling M. Distribution of TGF-beta, the TGF-beta type I receptor and the R-II receptor in peripheral nerves and mechanoreceptors; observations on changes after traumatic injury. Brain Res 2001, 913:47-56. 10.1016/S0006-8993(01)02757-3, 11532246.
6. Krieglstein K, Strelau J, Schober A, et al. TGF-beta and the regulation of neuron survival and death. J Physiol Paris 2002, 96:25-30. 10.1016/S0928-4257(01)00077-8, 11755780.
7. Krieglstein K, Unsicker K. Distinct modulatory actions of TGF-beta and LIF on neurotrophin-mediated survival of developing sensory neurons. Neurochem Res 1996, 21:843-850. 10.1007/BF02532308, 8873089.
8. Su SB, Motoo Y, Xie MJ, et al. Expression of transforming growth factor-beta in spontaneous chronic pancreatitis in the WBN/Kob rat. Dig Dis Sci 2000, 45:151-159. 10.1023/A:1005481931793, 10695628.
9. van Laethem JL, Deviere J, Resibois A, et al. Localization of transforming growth factor beta 1 and its latent binding protein in human chronic pancreatitis. Gastroenterology 1995, 108:1873-1881. 10.1016/0016-5085(95)90152-3, 7768393.
10. Xu GY, Winston JH, Shenoy M, et al. Enhanced excitability and suppression of A-type K + current of pancreas-specific afferent neurons in a rat model of chronic pancreatitis. Am J Physiol Gastrointest Liver Physiol 2006, 291:G424-G431. 10.1152/ajpgi.00560.2005, 16645160.
11. Rasband MN, Park EW, Vanderah TW, et al. Distinct potassium channels on pain-sensing neurons. Proc Natl Acad Sci U S A 2001, 98:13373-13378. 10.1073/pnas.231376298, 60878, 11698689.
12. Phuket TR, Covarrubias M. Kv4 Channels Underlie the Subthreshold-Operating A-type K-current in Nociceptive Dorsal Root Ganglion Neurons. Front Mol Neurosci 2009, 2:3. 2724030, 19668710.
13. Xu GY, Winston JH, Shenoy M, et al. Transient receptor potential vanilloid 1 mediates hyperalgesia and is up-regulated in rats with chronic pancreatitis. Gastroenterology 2007, 133:1282-1292. 10.1053/j.gastro.2007.06.015, 17698068.
14. Winston JH, He ZJ, Shenoy M, et al. Molecular and behavioral changes in nociception in a novel rat model of chronic pancreatitis for the study of pain. Pain 2005, 117:214-222. 10.1016/j.pain.2005.06.013, 16098667.
15. Anscher MS, Thrasher B, Zgonjanin L, et al. Small molecular inhibitor of transforming growth factor-beta protects against development of radiation-induced lung injury. Int J Radiat Oncol Biol Phys 2008, 71:829-837. 10.1016/j.ijrobp.2008.02.046, 18411002.
16. Echeverry S, Shi XQ, Haw A, et al. Transforming growth factor-beta1 impairs neuropathic pain through pleiotropic effects. Mol Pain 2009, 5:16. 10.1186/1744-8069-5-16, 2669449, 19327151.
17. Tramullas M, Lantero A, Diaz A, et al. BAMBI (bone morphogenetic protein and activin membrane-bound inhibitor) reveals the involvement of the transforming growth factor-beta family in pain modulation. J Neurosci 2010, 30:1502-1511. 10.1523/JNEUROSCI.2584-09.2010, 20107078.
18. O'Callaghan JP, Miller DB. Spinal glia and chronic pain. Metabolism 2010, 59(Suppl 1):S21-S26.
19. Farr M, Mathews J, Zhu DF, et al. Inflammation causes a long-term hyperexcitability in the nociceptive sensory neurons of Aplysia. Learn Mem 1999, 6:331-340. 311296, 10492014.
20. Zhang F, Endo S, Cleary LJ, et al. Role of transforming growth factor-beta in long-term synaptic facilitation in Aplysia. Science 1997, 275:1318-1320. 10.1126/science.275.5304.1318, 9036859.
21. Chin J, Angers A, Cleary LJ, et al. Transforming growth factor beta1 alters synapsin distribution and modulates synaptic depression in Aplysia. J Neurosci 2002, 22:RC220.
22. Chin J, Angers A, Cleary LJ, et al. TGF-beta1 in Aplysia: role in long-term changes in the excitability of sensory neurons and distribution of TbetaR-II-like immunoreactivity. Learn Mem 1999, 6:317-330. 311291, 10492013.
23. Zhu W, Xu P, Cuascut FX, et al. Activin acutely sensitizes dorsal root ganglion neurons and induces hyperalgesia via PKC-mediated potentiation of transient receptor potential vanilloid I. J Neurosci 2007, 27:13770-13780. 10.1523/JNEUROSCI.3822-07.2007, 18077689.
24. Xu P, Hall AK. Activin acts with nerve growth factor to regulate calcitonin gene-related peptide mRNA in sensory neurons. Neuroscience 2007, 150:665-674. 10.1016/j.neuroscience.2007.09.041, 2700348, 17964731.
25. Xu P, Van Slambrouck C, Berti-Mattera L, et al. Activin induces tactile allodynia and increases calcitonin gene-related peptide after peripheral inflammation. J Neurosci 2005, 25:9227-9235. 10.1523/JNEUROSCI.3051-05.2005, 16207882.
26. Dunlap K. Forskolin prolongs action potential duration and blocks potassium current in embryonic chick sensory neurons. Pflugers Arch 1985, 403:170-174. 10.1007/BF00584096, 2580271.
27. Takeda M, Tanimoto T, Nasu M, et al. Temporomandibular joint inflammation decreases the voltage-gated K + channel subtype 1.4-immunoreactivity of trigeminal ganglion neurons in rats. Eur J Pain 2008, 12:189-195. 10.1016/j.ejpain.2007.04.005, 17584507.
28. Wells JE, Rose ET, Rowland KC, et al. Kv1.4 subunit expression is decreased in neurons of painful human pulp. J Endod 2007, 33:827-829. 10.1016/j.joen.2007.03.013, 17804321.
29. Hayashi Y, Takimoto K, Chancellor MB, et al. Bladder hyperactivity and increased excitability of bladder afferent neurons associated with reduced expression of Kv1.4 alpha-subunit in rats with cystitis. Am J Physiol Regul Integr Comp Physiol 2009, 296:R1661-R1670. 10.1152/ajpregu.91054.2008, 2689836, 19279288.
30. Zhu Y, Mehta K, Li C, et al. Systemic administration of anti-NGF increases A-type potassium currents and decreases pancreatic nociceptor excitability in a rat model of chronic pancreatitis. Am J Physiol Gastrointest Liver Physiol 2011,
31. Zhu Y, Colak T, Shenoy M, et al. Nerve growth factor modulates TRPV1 expression and function and mediates pain in chronic pancreatitis. Gastroenterology 2011, 141:370-377. 10.1053/j.gastro.2011.03.046, 21473865.
32. Ma LJ, Jha S, Ling H, et al. Divergent effects of low versus high dose anti-TGF-beta antibody in puromycin aminonucleoside nephropathy in rats. Kidney Int 2004, 65:106-115. 10.1111/j.1523-1755.2004.00381.x, 14675041.
33. Inoue M, Shimohira I, Yoshida A, et al. Dose-related opposite modulation by nociceptin/orphanin FQ of substance P nociception in the nociceptors and spinal cord. J Pharmacol Exp Ther 1999, 291:308-313.
34. Souchelnytskyi S, Moustakas A, Heldin CH. TGF-beta signaling from a three-dimensional perspective: insight into selection of partners. Trends Cell Biol 2002, 12:304-307. 10.1016/S0962-8924(02)02300-0, 12185845.
35. Moustakas A, Heldin CH. Non-Smad TGF-beta signals. J Cell Sci 2005, 118:3573-3584. 10.1242/jcs.02554, 16105881.
36. Winston J, Toma H, Shenoy M, et al. Nerve growth factor regulates VR-1 mRNA levels in cultures of adult dorsal root ganglion neurons. Pain 2001, 89:181-186. 10.1016/S0304-3959(00)00370-5, 11166474.