Administration of a tropomyosin receptor kinase inhibitor attenuates sarcoma-induced nerve sprouting, neuroma formation and bone cancer pain

Molecular Pain

Volumn 6, Issue , 2010, Pages

  Ghilardi, Joseph R ^a   Freeman, Katie T ^a   Jimenez Andrade, Juan M ^b   Mantyh, William G ^b   Bloom, Aaron P ^b   Kuskowski, Michael A ^a   Mantyh, Patrick W ^a,b,c  

^a VA MEDICAL CENTER   (United States)

^b UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANALGESIC AGENT; ARRY 470; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; NEUROTROPHIN 3 RECEPTOR; PROTEIN TYROSINE KINASE A; RECEPTOR PROTEIN; UNCLASSIFIED DRUG; PROTEIN KINASE INHIBITOR;

ANALGESIC ACTIVITY; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE CANCER; BONE REMODELING; CANCER GROWTH; CANCER PAIN; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOSAGE SCHEDULE COMPARISON; DRUG EFFICACY; DRUG TARGETING; EARLY INTERVENTION; ENZYME INHIBITION; HUMAN; HUMAN CELL; MALE; MOUSE; NERVE SPROUTING; NEUROMA; NONHUMAN; PRIORITY JOURNAL; SARCOMA; SENSORY NERVE; STROMA CELL; ANIMAL; DISEASE MODEL; DRUG ANTAGONISM; DRUG EFFECT; PATHOLOGY; SENSORY RECEPTOR; TIME; TREATMENT OUTCOME; TUMOR VOLUME;

ANIMALS; BONE REMODELING; DISEASE MODELS, ANIMAL; MICE; NEUROMA; PROTEIN KINASE INHIBITORS; RECEPTOR, TRKA; SARCOMA; SENSORY RECEPTOR CELLS; TIME FACTORS; TREATMENT OUTCOME; TUMOR BURDEN;

EID: 78649756871     PISSN: None     EISSN: 17448069     Source Type: Journal    
DOI: 10.1186/1744-8069-6-87     Document Type: Article

References (49)

1. Mercadante S. Malignant bone pain: pathophysiology and treatment. Pain 1997, 69:1-18. 10.1016/S0304-3959(96)03267-8, 9060007.
2. Coleman RE. Skeletal complications of malignancy. Cancer 1997, 80:1588-94. 10.1002/(SICI)1097-0142(19971015)80:8+<1588::AID-CNCR9>3.0.CO;2-G, 9362426.
3. Xian CJ, Zhou XF. Treating skeletal pain: limitations of conventional anti-inflammatory drugs, and anti-neurotrophic factor as a possible alternative. Nat Clin Pract Rheumatol 2009, 5:92-8. 10.1038/ncprheum0982, 19182815.
4. Balano KB. Anti-inflammatory drugs and myorelaxants. Pharmacology and clinical use in musculoskeletal disease. Prim Care 1996, 23:329-34.
5. Feinberg SD. Prescribing analgesics. How to improve function and avoid toxicity when treating chronic pain. Geriatrics 2000, 55:44. 49-50, 53 passim.
6. Ivanhoe CB, Hartman ET. Clinical caveats on medical assessment and treatment of pain after TBI. J Head Trauma Rehabil 2004, 19:29-39. 10.1097/00001199-200401000-00004, 14732829.
7. Hansel TT, Kropshofer H, Singer T, Mitchell JA, George AJ. The safety and side effects of monoclonal antibodies. Nat Rev Drug Discov 2010, 9:325-38. 10.1038/nrd3003, 20305665.
8. Opar A. Kinase inhibitors attract attention as oral rheumatoid arthritis drugs. Nat Rev Drug Discov 2010, 9:257-8. 10.1038/nrd3155, 20357793.
9. Halvorson KG, Sevcik MA, Ghilardi JR, Sullivan LJ, Koewler NJ, Bauss F, Mantyh PW. Intravenous Ibandronate Rapidly Reduces Pain, Neurochemical Indices of Central Sensitization, Tumor Burden, and Skeletal Destruction in a Mouse Model of Bone Cancer. J Pain Symptom Manage 2008, 36(3):289-303. 10.1016/j.jpainsymman.2007.10.005, 2638081, 18411018.
10. Jimenez-Andrade JM, Mantyh WG, Bloom AP, Xu H, Ferng AS, Dussor G, Vanderah TW, Mantyh PW. A phenotypically restricted set of primary afferent nerve fibers innervate the bone versus skin: therapeutic opportunity for treating skeletal pain. Bone 2010, 46:306-13. 10.1016/j.bone.2009.09.013, 19766746.
11. Greenfield GQ, MV B, Cole BE. Orthopaedic Pain. Journal/Weiner's pain management: a practical guide for clinicians 2006, 465-76.
12. Small JR, Scadding JW, Landon DN. A fluorescence study of changes in noradrenergic sympathetic fibres in experimental peripheral nerve neuromas. J Neurol Sci 1990, 100:98-107. 10.1016/0022-510X(90)90019-J, 2089147.
13. Lindqvist A, Rivero-Melian C, Turan I, Fried K. Neuropeptide- and tyrosine hydroxylase-immunoreactive nerve fibers in painful Morton's neuromas. Muscle Nerve 2000, 23:1214-8. 10.1002/1097-4598(200008)23:8<1214::AID-MUS9>3.0.CO;2-A, 10918258.
14. Basbaum AI, Bautista DM, Scherrer G, Julius D. Cellular and molecular mechanisms of pain. Cell 2009, 139:267-84. 10.1016/j.cell.2009.09.028, 2852643, 19837031.
15. McMahon SB, Bennett DLH, Bevan S, McMahon SB, Koltzenburg M. Inflammatory mediators and modulators of pain. Journal/Wall and Melzack's textbook of pain 2006, xviii. 1239 p.
16. Paterson S, Schmelz M, McGlone F, Turner G, Rukwied R. Facilitated neurotrophin release in sensitized human skin. Eur J Pain 2009, 13:399-405. 10.1016/j.ejpain.2008.05.005, 18571954.
17. Pezet S, McMahon SB. Neurotrophins: mediators and modulators of pain. Annu Rev Neurosci 2006, 29:507-38. 10.1146/annurev.neuro.29.051605.112929, 16776595.
18. Averill S, McMahon SB, Clary DO, Reichardt LF, Priestley JV. Immunocytochemical localization of trkA receptors in chemically identified subgroups of adult rat sensory neurons. Eur J Neurosci 1995, 7:1484-1494. 10.1111/j.1460-9568.1995.tb01143.x, 2758238, 7551174.
19. Hefti FF, Rosenthal A, Walicke PA, Wyatt S, Vergara G, Shelton DL, Davies AM. Novel class of pain drugs based on antagonism of NGF. Trends Pharmacol Sci 2006, 27:85-91. 10.1016/j.tips.2005.12.001, 16376998.
20. Shu XQ, Mendell LM. Neurotrophins and hyperalgesia. Proc Natl Acad Sci USA 1999, 96:7693-6. 10.1073/pnas.96.14.7693, 33603, 10393882.
21. Malik-Hall M, Dina OA, Levine JD. Primary afferent nociceptor mechanisms mediating NGF-induced mechanical hyperalgesia. Eur J Neurosci 2005, 21:3387-94. 10.1111/j.1460-9568.2005.04173.x, 16026476.
22. Walsh GS, Krol KM, Kawaja MD. Absence of the p75 neurotrophin receptor alters the pattern of sympathosensory sprouting in the trigeminal ganglia of mice overexpressing nerve growth factor. J Neurosci 1999, 19:258-73.
23. Ghilardi JR, Freeman KT, Jimenez-Andrade JM, Mantyh WG, Bloom AP, Bouhana KS, Trollinger D, Winkler J, Lee P, Andrews SW, Kuskowski MA, Mantyh PW. Sustained blockade of neurotrophin receptors TrkA, TrkB and TrkC reduces non-malignant skeletal pain but not the maintenance of sensory and sympathetic nerve fibers. Bone 2010,
24. Chao MV. Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat Rev Neurosci 2003, 4:299-309. 10.1038/nrn1078, 12671646.
25. Behnia A, Zhang L, Charles M, Gold MS. Changes in TrkB-like immunoreactivity in rat trigeminal ganglion after tooth injury. J Endod 2003, 29:135-40. 10.1097/00004770-200302000-00012, 12597715.
26. Kashiba H, Uchida Y, Senba E. Distribution and colocalization of NGF and GDNF family ligand receptor mRNAs in dorsal root and nodose ganglion neurons of adult rats. Brain Res Mol Brain Res 2003, 110:52-62. 10.1016/S0169-328X(02)00584-3, 12573533.
27. Kobayashi K, Fukuoka T, Obata K, Yamanaka H, Dai Y, Tokunaga A, Noguchi K. Distinct expression of TRPM8, TRPA1, and TRPV1 mRNAs in rat primary afferent neurons with adelta/c-fibers and colocalization with trk receptors. J Comp Neurol 2005, 493:596-606. 10.1002/cne.20794, 16304633.
28. Zhu ZW, Friess H, Wang L, Bogardus T, Korc M, Kleeff J, Buchler MW. Nerve growth factor exerts differential effects on the growth of human pancreatic cancer cells. Clin Cancer Res 2001, 7:105-12.
29. Kerr BJ, Bradbury EJ, Bennett DL, Trivedi PM, Dassan P, French J, Shelton DB, McMahon SB, Thompson SW. Brain-derived neurotrophic factor modulates nociceptive sensory inputs and NMDA-evoked responses in the rat spinal cord. J Neurosci 1999, 19:5138-48.
30. Chaudhry V, Giuliani M, Petty BG, Lee D, Seyedsadr M, Hilt D, Cornblath DR. Tolerability of recombinant-methionyl human neurotrophin-3 (r-metHuNT3) in healthy subjects. Muscle Nerve 2000, 23:189-92. 10.1002/(SICI)1097-4598(200002)23:2<189::AID-MUS7>3.0.CO;2-8, 10639609.
31. Watanabe M, Endo Y, Kimoto K, Katoh-Semba R, Arakawa Y. Inhibition of adjuvant-induced inflammatory hyperalgesia in rats by local injection of neurotrophin-3. Neurosci Lett 2000, 282:61-4. 10.1016/S0304-3940(00)00842-9, 10713396.
32. Mantyh WG, Jimenez-Andrade JM, Stake JI, Bloom AP, Kaczmarska MJ, Taylor RN, Freeman KT, Ghilardi JR, Kuskowski MA, Mantyh PW. Blockade of nerve sprouting and neuroma formation markedly attenuates the development of late stage cancer pain. Neuroscience 2010, 1. 171(2):588-98.
33. Ozawa T, Ohtori S, Inoue G, Aoki Y, Moriya H, Takahashi K. The degenerated lumbar intervertebral disc is innervated primarily by peptide-containing sensory nerve fibers in humans. Spine 2006, 31:2418-22. 10.1097/01.brs.0000239159.74211.9c, 17023849.
34. Ozawa T, Aoki Y, Ohtori S, Takahashi K, Chiba T, Ino H, Moriya H. The dorsal portion of the lumbar intervertebral disc is innervated primarily by small peptide-containing dorsal root ganglion neurons in rats. Neurosci Lett 2003, 344:65-7. 10.1016/S0304-3940(03)00416-6, 12781923.
35. Mach DB, Rogers SD, Sabino MC, Luger NM, Schwei MJ, Pomonis JD, Keyser CP, Clohisy DR, Adams DJ, O'Leary P, Mantyh PW. Origins of skeletal pain: sensory and sympathetic innervation of the mouse femur. Neuroscience 2002, 113:155-66. 10.1016/S0306-4522(02)00165-3, 12123694.
36. Davies AM. Regulation of neuronal survival and death by extracellular signals during development. EMBO J 2003, 22:2537-45. 10.1093/emboj/cdg254, 156751, 12773370.
37. Ernsberger U. Role of neurotrophin signalling in the differentiation of neurons from dorsal root ganglia and sympathetic ganglia. Cell Tissue Res 2009, 336:349-84. 10.1007/s00441-009-0784-z, 19387688.
38. McMahon SB, Bennett DLH, Bevan S, Wall PD, McMahon SB, Koltzenburg M. Inflamatory mediators and modulators of pain. Journal/Wall and Melzack's Textbook of Pain 2006, 49-72.
39. Devor M, Wall PD. Type of sensory nerve fibre sprouting to form a neuroma. Nature 1976, 262:705-8. 10.1038/262705a0, 958442.
40. Sung JH, Mastri AR. Aberrant peripheral nerves and microneuromas in otherwise normal medullas. J Neuropathol Exp Neurol 1983, 42:522-8. 10.1097/00005072-198309000-00004, 6310057.
41. Madduri S, Papaloizos M, Gander B. Synergistic effect of GDNF and NGF on axonal branching and elongation in vitro. Neurosci Res 2009, 65:88-97. 10.1016/j.neures.2009.06.003, 19523996.
42. Kryger GS, Kryger Z, Zhang F, Shelton DL, Lineaweaver WC, Buncke HJ. Nerve growth factor inhibition prevents traumatic neuroma formation in the rat. J Hand Surg Am 2001, 26:635-44. 10.1053/jhsu.2001.26035, 11466637.
43. Black JA, Nikolajsen L, Kroner K, Jensen TS, Waxman SG. Multiple sodium channel isoforms and mitogen-activated protein kinases are present in painful human neuromas. Ann Neurol 2008, 64:644-53. 10.1002/ana.21527, 19107992.
44. Devor M, Keller CH, Ellisman MH. Spontaneous discharge of afferents in a neuroma reflects original receptor tuning. Brain Res 1990, 517:245-250. 10.1016/0006-8993(90)91033-D, 2375993.
45. Devor M, Govrin-Lippmann R. Axoplasmic transport block reduces ectopic impulse generation in injured peripheral nerves. Pain 1983, 16:73-85. 10.1016/0304-3959(83)90087-8, 6191267.
46. Devor M, Govrin-Lippmann R, Angelides K. Na+ channel immunolocalization in peripheral mammalian axons and changes following nerve injury and neuroma formation. J Neurosci 1993, 13:1976-92.
47. Ceyhan GO, Bergmann F, Kadihasanoglu M, Altintas B, Demir IE, Hinz U, Muller MW, Giese T, Buchler MW, Giese NA, Friess H. Pancreatic neuropathy and neuropathic pain-a comprehensive pathomorphological study of 546 cases. Gastroenterology 2009, 136:177-186 e1. 10.1053/j.gastro.2008.09.029, 18992743.
48. Winkler J. Analgesic effects of a potent and selective kinase inhibitor of neurotrophin receptors TrkA, TrkB, and TrkC. Journal/8th IASP Research Symposium 2009,
49. Bouhana KS, Impastato R, Jiang Y, Wallace RD, Hartley DP, Do MG, von Carlowitz I. Analgesic effects of a potent and selective kinase inhibitor of neurotrophin receptors TrkA, TrkB, and TrkC in a model of inflammatory pain. Journal/Keystone Symposium- Neurobiology of Pain 2008,