A peptide uncoupling CRMP-2 from the presynaptic Ca 2+ channel complex demonstrates efficacy in animal models of migraine and AIDS therapy-induced neuropathy

Translational Neuroscience

Volumn 3, Issue 1, 2012, Pages 1-8

  Ripsch, Matthew S ^a   Ballard, Carrie J ^a   Khanna, May ^a   Hurley, Joyce H ^a   White, Fletcher A ^a   Khanna, Rajesh ^a,b  

^a INDIANA UNIVERSITY   (United States)

^b Sophia Therapeutics LLC   (United States)

Author keywords

AIDS therapy induced neuropathic pain; Chronic pain; CRMP 2; d4T Zerit Stavudine; Meningeal blood flow; Migraine model; N type calcium channel; NTR; Uncoupling peptide

Indexed keywords

CALCIUM CHANNEL N TYPE; CALCIUM ION; CBD3 TAT FUSION PROTEIN; COLLAPSIN RESPONSE MEDIATOR PROTEIN 2; HYBRID PROTEIN; STAVUDINE; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL;

ADVERSE OUTCOME; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BINDING SITE; BIOAVAILABILITY; BLOOD FLOW; CONTROLLED STUDY; DISEASE ASSOCIATION; DOPPLER FLOWMETER; DRUG EFFECT; DRUG MECHANISM; FEMALE; FLOW RATE; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; INTERMETHOD COMPARISON; MALE; MIGRAINE; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NEUROPATHIC PAIN; NONHUMAN; OUTCOME ASSESSMENT; PAIN ASSESSMENT; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; RAT; TRIGEMINUS GANGLION;

EID: 84858405523     PISSN: 20813856     EISSN: 20816936     Source Type: Journal    
DOI: 10.2478/s13380-012-0002-4     Document Type: Article

References (45)

1. Institute of medicine report from the committee on advancing pain research care and education, Relieving pain in America: A blueprint for transforming prevention, care, education and research, The National Academies Press, 2011
2. T. P. Snutch 2005 Targeting chronic and neuropathic pain: the N-type calcium channel comes of age NeuroRx 2 662 670 16489373 10.1602/neurorx.2.4.662 (Pubitemid 41393273)
3. W. A. Catterall A. P. Few 2008 Calcium channel regulation and presynaptic plasticity Neuron 59 882 901 18817729 10.1016/j.neuron.2008.09.005 1:CAS:528:DC%2BD1cXht1amsbfI
4. H. Saegusa T. Kurihara S. Zong A. Kazuno Y. Matsuda T. Nonaka, et al. 2001 Suppression of inflammatory and neuropathic pain symptoms in mice lacking the N-type Ca2+ channel EMBO J. 20 2349 2356 11350923 10.1093/emboj/20.10.2349 1:CAS:528:DC%2BD3MXktFegur8%3D (Pubitemid 32452852)
5. D. Cizkova J. Marsala N. Lukacova M. Marsala S. Jergova J. Orendacova, et al. 2002 Localization of N-type Ca2+ channels in the rat spinal cord following chronic constrictive nerve injury Exp. Brain Res. 147 456 463 12444477 10.1007/s00221-002-1217-3 1:CAS:528:DC%2BD38XovVWht7k%3D (Pubitemid 35440498)
6. T. J. Bell C. Thaler A. J. Castiglioni T. D. Helton D. Lipscombe 2004 Cellspecific alternative splicing increases calcium channel current density in the pain pathway Neuron 41 127 138 14715140 10.1016/S0896-6273(03)00801-8 1:CAS:528:DC%2BD2cXnt12lsA%3D%3D (Pubitemid 38068440)
7. C. Altier C. S. Dale A. E. Kisilevsky K. Chapman A. J. Castiglioni E. A. Matthews, et al. 2007 Differential role of N-type calcium channel splice isoforms in pain J. Neurosci. 27 6363 6373 17567797 10.1523/JNEUROSCI.0307-07. 2007 1:CAS:528:DC%2BD2sXntVKrtLw%3D (Pubitemid 46920384)
8. G. W. Zamponi Z. P. Feng L. Zhang H. Pajouhesh Y. Ding F. Belardetti, et al. 2009 Scaffold-based design and synthesis of potent N-type calcium channel blockers Bioorg. Med. Chem. Lett. 19 6467 6472 19815411 10.1016/j.bmcl.2009.09. 008 1:CAS:528:DC%2BD1MXhtlWls7zP
9. G. W. Zamponi R. J. Lewis S. M. Todorovic S. P. Arneric T. P. Snutch 2009 Role of voltage-gated calcium channels in ascending pain pathways Brain Res. Rev. 60 84 89 19162069 10.1016/j.brainresrev.2008.12.021 1:CAS:528: DC%2BD1MXktV2nsbY%3D
10. Swensen A. M.; Herrington J.; Bugianesi R. M.; Dai G.; Haedo R. J.; Ratliff K. S. et al.; Characterization of the substituted N-triazole oxindole, TROX-1, a small molecule, state-dependent inhibitor of CaV2 calcium channels, Mol. Pharmacol.; 2011 epub ahead of print
11. C. Abbadie O. B. McManus S. Y. Sun R. M. Bugianesi G. Dai R. J. Haedo, et al. 2010 Analgesic effects of a substituted N-triazole oxindole (TROX-1), a state-dependent, voltage-gated calcium channel 2 blocker J. Pharmacol. Exp. Ther. 334 545 555 20439438 10.1124/jpet.110.166363 1:CAS:528:DC%2BC3cXht1Kisb7I
12. C. S. Bauer M. Nieto-Rostro W. Rahman A. Tran-Van-Minh L. Ferron L. Douglas, et al. 2009 The increased trafficking of the calcium channel subunit alpha2delta-1 to presynaptic terminals in neuropathic pain is inhibited by the alpha2delta ligand pregabalin J. Neurosci. 29 4076 4088 19339603 10.1523/JNEUROSCI.0356-09.2009 1:CAS:528:DC%2BD1MXktlaktL4%3D
13. J. M. Brittain A. D. Piekarz Y. Wang T. Kondo T. R. Cummins R. Khanna 2009 An atypical role for collapsin response mediator protein 2 (CRMP-2) in neurotransmitter release via interaction with presynaptic voltagegated Ca2+ channels J. Biol. Chem. 284 31375 31390 19755421 10.1074/jbc.M109.009951 1:CAS:528:DC%2BD1MXhtlCjsr%2FO
14. X. X. Chi B. S. Schmutzler J. M. Brittain C. M. Hingtgen G. D. Nicol R. Khanna 2009 Regulation of N-type voltage-gated calcium (CaV2.2) channels and transmitter release by collapsin response mediator protein-2 (CRMP-2) in sensory neurons J. Cell. Sci. 23 4351 4362 10.1242/jcs.053280
15. K. Hensley K. Venkova A. Christov W. Gunning J. Park 2011 Collapsin response mediator protein-2: an emerging pathologic feature and therapeutic target for neurodisease indications Mol. Neurobiol. 43 180 191 21271304 10.1007/s12035-011-8166-4 1:CAS:528:DC%2BC3MXlsFajurc%3D
16. N. Inagaki K. Chihara N. Arimura C. Ménager Y. Kawano N. Matsuo, et al. 2001 CRMP-2 induces axons in cultured hippocampal neurons Nat. Neurosci. 4 81 782 10.1038/90476 (Pubitemid 32702507)
17. N. Arimura A. Hattori T. Kimura S. Nakamuta Y. Funahashi S. Hirotsune, et al. 2009 CRMP-2 directly binds to cytoplasmic dynein and interferes with its activity J. Neurochem. 111 380 390 19659462 10.1111/j.1471-4159.2009.06317.x 1:CAS:528:DC%2BD1MXhtlSitrjE
18. T. Morita K. Sobue 2009 Specification of neuronal polarity regulated by local translation of CRMP2 and Tau via the mTOR-p70S6K pathway J. Biol. Chem. 284 27734 27745 19648118 10.1074/jbc.M109.008177 1:CAS:528:DC%2BD1MXhtFyjs73I
19. T. Yoshimura Y. Kawano N. Arimura S. Kawabata A. Kikuchi K. Kaibuchi 2005 GSK-3beta regulates phosphorylation of CRMP-2 and neuronal polarity Cell 120 137 149 15652488 10.1016/j.cell.2004.11.012 1:CAS:528:DC%2BD2MXot1CgsQ%3D%3D (Pubitemid 40094609)
20. Y. Wang J. M. Brittain S. M. Wilson R. Khanna 2010 Emerging roles of collapsin response mediator proteins (CRMPs) as regulators of voltage-gated calcium channels and synaptic transmission Commun. Integr. Biol. 3 1 4 10.4161/cib.3.1.9694
21. J. M. Brittain D. B. Duarte S. M. Wilson W. Zhu C. Ballard P. L. Johnson, et al. 2011 Suppression of inflammatory and neuropathic pain by uncoupling CRMP-2 from the presynaptic Ca(2+) channel complex Nat. Med. 17 822 829 21642979 10.1038/nm.2345 1:CAS:528:DC%2BC3MXntV2qu74%3D
22. S. M. Wilson J. M. Brittain A. D. Piekarz C. J. Ballard M. S. Ripsch T. R. Cummins, et al. 2011 Further insights into the antinociceptive potential of a peptide disrupting the N-type calcium channel-CRMP-2 signaling complex Channels (Austin) 5 449 456 10.4161/chan.5.5.17363 1:CAS:528:DC%2BC38Xit1Omsro%3D
23. M. Kurosawa K. Messlinger M. Pawlak R. F. Schmidt 1995 Increase of meningeal blood flow after electrical stimulation of rat dura mater encephali: mediation by calcitonin gene-related peptide Br. J. Pharmacol. 114 1397 1402 7606344 1:STN:280:DyaK2MzjtVWqsg%3D%3D
24. R. Gottselig K. Messlinger 2004 Noxious chemical stimulation of rat facial mucosa increases intracranial blood flow through a trigemino- parasympathetic reflex-an experimental model for vascular dysfunctions in cluster headache Cephalalgia 24 206 214 15009014 10.1111/j.1468-2982.2004.00649. x 1:STN:280:DC%2BD2c7hvV2lug%3D%3D (Pubitemid 38333780)
25. E. K. Joseph X. Chen S. G. Khasar J. D. Levine 2004 Novel mechanism of enhanced nociception in a model of AIDS therapy-induced painful peripheral neuropathy in the rat Pain 107 147 158 14715401 10.1016/j.pain.2003.10.010 (Pubitemid 38058710)
26. R. H. LaMotte R. M. Friedman C. Lu P. S. Khalsa M. A. Srinivasan 1998 Raised object on a planar surface stroked across the fingerpad: responses of cutaneous mechanoreceptors to shape and orientation J. Neurophysiol. 80 2446 2466 9819255 1:STN:280:DyaK1M%2Fjs1yruw%3D%3D (Pubitemid 28546177)
27. C. Ma Y. Shu Z. Zheng Y. Chen H. Yao K. W. Greenquist, et al. 2003 Similar electrophysiological changes in axotomized and neighboring intact dorsal root ganglion neurons J. Neurophysiol. 89 1588 1602 12612024 10.1152/jn.00855.2002 (Pubitemid 36324002)
28. P. J. Goadsby 2008 Calcitonin gene-related peptide (CGRP) antagonists and migraine: is this a new era? Neurology 70 1300 1301 18413584 10.1212/01.wnl.0000309214.25038.fd (Pubitemid 351550335)
29. J. Olesen H. C. Diener I. W. Husstedt P. J. Goadsby D. Hall U. Meier, et al. 2004 Calcitonin gene-related peptide receptor antagonist BIBN 4096 BS for the acute treatment of migraine N. Engl. J. Med. 350 1104 1110 15014183 10.1056/NEJMoa030505 1:CAS:528:DC%2BD2cXitV2qur0%3D (Pubitemid 38298990)
30. Y. Xiao J. A. Richter J. H. Hurley 2008 Release of glutamate and CGRP from trigeminal ganglion neurons: Role of calcium channels and 5-HT1 receptor signaling Mol. Pain 4 12 18416824 10.1186/1744-8069-4-12 (Pubitemid 351622384)
31. P. E. Kunkler C. J. Ballard G. S. Oxford J. H. Hurley 2011 TRPA1 receptors mediate environmental irritant-induced meningeal vasodilatation Pain 152 38 44 21075522 10.1016/j.pain.2010.08.021 1:CAS:528:DC%2BC3cXhsFyns7vN
32. S. K. Bhangoo M. S. Ripsch D. J. Buchanan R. J. Miller F. A. White 2009 Increased chemokine signaling in a model of HIV1-associated peripheral neuropathy Mol. Pain 5 48 19674450 10.1186/1744-8069-5-48
33. R. E. Westenbroek L. Hoskins W. A. Catterall 1998 Localization of Ca2+ channel subtypes on rat spinal motor neurons, interneurons, and nerve terminals J. Neurosci. 18 6319 6330 9698323 1:CAS:528:DyaK1cXlsVahtbY%3D (Pubitemid 28373237)
34. L. M. Kerr F. Filloux B. M. Olivera H. Jackson J. K. Wamsley 1988 Autoradiographic localization of calcium channels with [125I] omega-conotoxin in rat brain Eur. J. Pharmacol. 146 181 183 2450766 10.1016/0014-2999(88)90501-8 1:CAS:528:DyaL1cXhtV2is78%3D (Pubitemid 18030439)
35. B. Heinke E. Balzer J. Sandkuhler 2004 Pre- and postsynaptic contributions of voltage-dependent Ca2+ channels to nociceptive transmission in rat spinal lamina I neurons Eur. J. Neurosci. 19 103 111 14750968 10.1046/j.1460-9568.2003.03083.x 1:STN:280:DC%2BD2c%2FltVGqsw%3D%3D (Pubitemid 38122076)
36. S. Akerman D. J. Williamson P. J. Goadsby 2003 Voltage-dependent calcium channels are involved in neurogenic dural vasodilatation via a presynaptic transmitter release mechanism Br. J. Pharmacol. 140 558 566 12970082 10.1038/sj.bjp.0705456 1:CAS:528:DC%2BD3sXosFOgsLo%3D (Pubitemid 37330500)
37. M. Dux P. Santha G. Jancso 2003 Capsaicin-sensitive neurogenic sensory vasodilatation in the dura mater of the rat J. Physiol. 552 859 867 12949222 10.1113/jphysiol.2003.050633 1:CAS:528:DC%2BD2cXitlSnsA%3D%3D (Pubitemid 37428426)
38. K. Zimmermann P. W. Reeh B. Averbeck 2003 S+ -flurbiprofen but not 5-HT1 agonists suppress basal and stimulated CGRP and PGE2 release from isolated rat dura mater Pain 103 313 320 12791437 10.1016/S0304-3959(02)00459-1 1:CAS:528:DC%2BD3sXkt1entLw%3D (Pubitemid 36638819)
39. B. Peitl G. Petho R. Porszasz J. Nemeth J. Szolcsanyi 1999 Capsaicininsensitive sensory-efferent meningeal vasodilatation evoked by electrical stimulation of trigeminal nerve fibres in the rat Br. J. Pharmacol. 127 457 467 10385246 10.1038/sj.bjp.0702561 1:CAS:528:DyaK1MXjs1yqsb4%3D (Pubitemid 29245684)
40. K. Eikermann-Haerter M. A. Moskowitz 2008 Animal models of migraine headache and aura Curr. Opin. Neurol. 21 294 300 18451713 10.1097/WCO. 0b013e3282fc25de (Pubitemid 351653979)
41. U. Reuter R. M. del Sanchez M. A. Moskowitz 2000 Experimental models of migraine Funct. Neurol. 15 Suppl3 9 18 11200808 (Pubitemid 32051370)
42. A. Panconesi M. L. Bartolozzi L. Guidi 2009 Migraine pain: reflections against vasodilatation J. Headache Pain 10 317 325 19499287 10.1007/s10194-009- 0130-6
43. A. M. Strassman D. Levy 2006 Response properties of dural nociceptors in relation to headache J. Neurophysiol. 95 1298 1306 16492942 10.1152/jn.01293. 2005
44. G. J. Moyle M. Sadler 1998 Peripheral neuropathy with nucleoside antiretrovirals: risk factors, incidence and management Drug Saf. 19 481 494 9880091 10.2165/00002018-199819060-00005 1:CAS:528:DyaK1MXjvFOmtg%3D%3D (Pubitemid 29015407)
45. R. C. Deo E. F. Schmidt A. Elhabazi H. Togashi S. K. Burley S. M. Strittmatter 2004 Structural bases for CRMP function in plexin-dependent semaphorin3A signaling EMBO J. 23 9 22 14685275 10.1038/sj.emboj.7600021 1:CAS:528:DC%2BD2cXhtVeqtLk%3D (Pubitemid 38165743)