IB4-saporin attenuates acute and eliminates chronic muscle pain in the rat

Experimental Neurology

Volumn 233, Issue 2, 2012, Pages 859-865

  Alvarez, Pedro ^a,b   Gear, Robert W ^a,b   Green, Paul G ^a,b   Levine, Jon D ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Chronic muscle pain; Isolectin b4; Myalgia; Nociceptor

Indexed keywords

ANALGESIC AGENT; ISOLECTIN B4 SAPORIN CONJUGATE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHRONIC PAIN; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; ERGONOMICS; GASTROCNEMIUS MUSCLE; HYPERALGESIA; MALE; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MYALGIA; NONHUMAN; PAIN ASSESSMENT; PAIN THRESHOLD; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT;

ACUTE PAIN; ANIMALS; CHRONIC PAIN; INJECTIONS, SPINAL; LECTINS; MALE; MUSCLE, SKELETAL; PAIN MEASUREMENT; PLANT LECTINS; RATS; RATS, SPRAGUE-DAWLEY; RIBOSOME INACTIVATING PROTEINS, TYPE 1;

EID: 84856515087     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2011.12.019     Document Type: Article

References (52)

1. Albers K.M., Woodbury C.J., Ritter A.M., Davis B.M., Koerber H.R. Glial cell-line-derived neurotrophic factor expression in skin alters the mechanical sensitivity of cutaneous nociceptors. J. Neurosci. 2006, 26:2981-2990.
2. Aley K.O., Messing R.O., Mochly-Rosen D., Levine J.D. Chronic hypersensitivity for inflammatory nociceptor sensitization mediated by the epsilon isozyme of protein kinase C. J. Neurosci. 2000, 20:4680-4685.
3. Alvarez P., Levine J.D., Green P.G. Eccentric exercise induces chronic alterations in musculoskeletal nociception in the rat. Eur. J. Neurosci. 2010, 32:819-825.
4. Ambalavanar R., Moritani M., Haines A., Hilton T., Dessem D. Chemical phenotypes of muscle and cutaneous afferent neurons in the rat trigeminal ganglion. J. Comp. Neurol. 2003, 460:167-179.
5. Armstrong R.B., Warren G.L., Warren J.A. Mechanisms of exercise-induced muscle fibre injury. Sports Med. 1991, 12:184-207.
6. Bogen O., Joseph E.K., Chen X., Levine J.D. GDNF hyperalgesia is mediated by PLCgamma, MAPK/ERK, PI3K, CDK5 and Src family kinase signaling and dependent on the IB4-binding protein versican. Eur. J. Neurosci. 2008, 28:12-19.
7. Bogen O., Dina O.A., Gear R.W., Levine J.D. Dependence of monocyte chemoattractant protein 1 induced hyperalgesia on the isolectin B4-binding protein versican. Neuroscience 2009, 159:780-786.
8. Bradbury E.J., Burnstock G., McMahon S.B. The expression of P2X3 purinoreceptors in sensory neurons: effects of axotomy and glial-derived neurotrophic factor. Mol. Cell. Neurosci. 1998, 12:256-268.
9. Braz J.M., Nassar M.A., Wood J.N., Basbaum A.I. Parallel "pain" pathways arise from subpopulations of primary afferent nociceptor. Neuron 2005, 47:787-793.
10. Breese N.M., George A.C., Pauers L.E., Stucky C.L. Peripheral inflammation selectively increases TRPV1 function in IB4-positive sensory neurons from adult mouse. Pain 2005, 115:37-49.
11. Della Torre G., Lucchi M.L., Brunetti O., Pettorossi V.E., Clavenzani P., Bortolami R. Central projections and entries of capsaicin-sensitive muscle afferents. Brain Res. 1996, 713:223-231.
12. Dina O.A., Levine J.D., Green P.G. Muscle inflammation induces a protein kinase C epsilon-dependent chronic-latent muscle pain. J. Pain 2008, 9:457-462.
13. Dina O.A., Joseph E.K., Levine J.D., Green P.G. Mechanisms mediating vibration-induced chronic musculoskeletal pain analyzed in the rat. J. Pain 2010, 11:369-377.
14. Ferrari L.F., Bogen O., Levine J.D. Nociceptor subpopulations involved in hyperalgesic priming. Neuroscience 2010, 165:896-901.
15. Hucho T.B., Dina O.A., Levine J.D. Epac mediates a cAMP-to-PKC signaling in inflammatory pain: an isolectin B4(+) neuron-specific mechanism. J. Neurosci. 2005, 25:6119-6126.
16. Jasmin L., Gogas K.R., Ahlgren S.C., Levine J.D., Basbaum A.I. Walking evokes a distinctive pattern of Fos-like immunoreactivity in the caudal brainstem and spinal cord of the rat. Neuroscience 1994, 58:275-286.
17. Joseph E.K., Levine J.D. Hyperalgesic priming is restricted to isolectin B4-positive nociceptors. Neuroscience 2010, 169:431-435.
18. Joseph E.K., Chen X., Bogen O., Levine J.D. Oxaliplatin acts on IB4-positive nociceptors to induce an oxidative stress-dependent acute painful peripheral neuropathy. J. Pain 2008, 9:463-472.
19. Kano Y., Sampei K., Matsudo H. Time course of capillary structure changes in rat skeletal muscle following strenuous eccentric exercise. Acta Physiol. Scand. 2004, 180:291-299.
20. Knyihár E., Csillik B. Effect of peripheral anatomy on the fine structure and histochemistry of the Rolando substance: degenerative atrophy of central processes of pseudounipolar cells. Exp. Brain Res. 1976, 26:73-87.
21. Kuhn J., Dina O.A., Goswami C., Suckow V., Levine J.D., Hucho T. GPR30 estrogen receptor agonists induce mechanical hyperalgesia in the rat. Eur. J. Neurosci. 2008, 27:1700-1709.
22. Ling L.J., Honda T., Shimada Y., Ozaki N., Shiraishi Y., Sugiura Y. Central projection of unmyelinated (C) primary afferent fibers from gastrocnemius muscle in the guinea pig. J. Comp. Neurol. 2003, 461:140-150.
23. McMahon S.B., Wall P.D. The distribution and central termination of single cutaneous and muscle unmyelinated fibres in rat spinal cord. Brain Res. 1985, 359:39-48.
24. Molander C., Ygge J., Dalsgaard C.J. Substance P-, somatostatin- and calcitonin gene-related peptide-like immunoreactivity and fluoride resistant acid phosphatase-activity in relation to retrogradely labeled cutaneous, muscular and visceral primary sensory neurons in the rat. Neurosci. Lett. 1987, 74:37-42.
25. Molliver D.C., Wright D.E., Leitner M.L., Parsadanian A.S., Doster K., Wen D., Yan Q., Snider W.D. IB4-binding DRG neurons switch from NGF to GDNF dependence in early postnatal life. Neuron 1997, 19:849-861.
26. Murase S., Terazawa E., Queme F., Ota H., Matsuda T., Hirate K., Kozaki Y., Katanosaka K., Taguchi T., Urai H., Mizumura K. Bradykinin and nerve growth factor play pivotal roles in muscular mechanical hyperalgesia after exercise (delayed-onset muscle soreness). J. Neurosci. 2010, 30:3752-3761.
27. Nasu T., Taguchi T., Mizumura K. Persistent deep mechanical hyperalgesia induced by repeated cold stress in rats. Eur. J. Pain 2010, 14:236-244.
28. Necking L.E., Lundborg G., Lundström R., Thornell L.E., Fridén J. Hand muscle pathology after long-term vibration exposure. J. Hand Surg. Br. 2004, 29:431-437.
29. Nishiguchi J., Sasaki K., Seki S., Chancellor M.B., Erickson K.A., de Groat W.C., Kumon H., Yoshimura N. Effects of isolectin B4-conjugated saporin, a targeting cytotoxin, on bladder overactivity induced by bladder irritation. Eur. J. Neurosci. 2004, 20:474-482.
30. O'Brien C., Woolf C.J., Fitzgerald M., Lindsay R.M., Molander C. Differences in the chemical expression of rat primary afferent neurons which innervate skin, muscle or joint. Neuroscience 1989, 32:493-502.
31. Panneton W.M., Gan Q., Juric R. The central termination of sensory fibers from nerves to the gastrocnemius muscle of the rat. Neuroscience 2005, 134:175-187.
32. Parada C.A., Yeh J.J., Reichling D.B., Levine J.D. Transient attenuation of protein kinase C epsilon can terminate a chronic hyperalgesic state in the rat. Neuroscience 2003, 120:219-226.
33. Pierce L.M., Rankin M.R., Foster R.T., Dolber P.C., Coates K.W., Kuehl T.J., Thor K.B. Distribution and immunohistochemical characterization of primary afferent neurons innervating the levator ani muscle of the female squirrel monkey. Am. J. Obstet. Gynecol. 2006, 195:987-996.
34. Plenderleith M.B., Snow P.J. The plant lectin Bandeiraea simplicifolia I-B4 identifies a subpopulation of small diameter primary sensory neurones which innervate the skin in the rat. Neurosci. Lett. 1993, 159:17-20.
35. Reichling D.B., Levine J.D. Critical role of nociceptor plasticity in chronic pain. Trends Neurosci. 2009, 32:611-618.
36. Reid A.J., Mantovani C., Shawcross S.G., Terenghi G., Wiberg M. Phenotype of distinct primary sensory afferent subpopulations and caspase-3 expression following axotomy. Histochem. Cell. Biol. 2011, 136:71-78.
37. Sant'Anna-da-Costa E., Carvalho S.L., Mendez-Otero R., Cavalcante L.A. Rapid loss of dorsal horn lectin binding after massive brachial plexus axotomy in young rats. Arch. Histol. Cytol. 1999, 62:249-252.
38. Shehab S.A., Spike R.C., Todd A.J. Do central terminals of intact myelinated primary afferents sprout into the superficial dorsal horn of rat spinal cord after injury to a neighboring peripheral nerve?. J. Comp. Neurol. 2004, 474:427-437.
39. Shin D.S., Kim E.H., Song K.Y., Hong H.J., Kong M.H., Hwang S.J. Neurochemical characterization of the TRPV1-positive nociceptive primary afferents innervating skeletal muscles in the rats. J. Korean Neurosurg. Soc. 2008, 43:97-104.
40. Snider W.D., McMahon S.B. Tackling pain at the source: new ideas about nociceptors. Neuron 1998, 20:629-632.
41. Suzuki H., Hase A., Kim B.Y., Miyata Y., Nonaka I., Arahata K., Akazawa C. Up-regulation of glial cell line-derived neurotrophic factor (GDNF) expression in regenerating muscle fibers in neuromuscular diseases. Neurosci. Lett. 1998, 257:165-167.
42. Suzuki H., Hase A., Miyata Y., Arahata K., Akazawa C. Prominent expression of glial cell line-derived neurotrophic factor in human skeletal muscle. J. Comp. Neurol. 1998, 402:303-312.
43. Taguchi T., Matsuda T., Tamura R., Sato J., Mizumura K. Muscular mechanical hyperalgesia revealed by behavioural pain test and c-Fos expression in the spinal dorsal horn after eccentric contraction in rats. J. Physiol. 2005, 564:259-268.
44. Takahashi K., Taguchi T., Itoh K., Okada K., Kawakita K., Mizumura K. Influence of surface anesthesia on the pressure pain threshold measured with different-sized probes. Somatosens. Mot. Res. 2005, 22:299-305.
45. Tarpley J.W., Kohler M.G., Martin W.J. The behavioral and neuroanatomical effects of IB4-saporin treatment in rat models of nociceptive and neuropathic pain. Brain Res. 2004, 1029:65-76.
46. Taylor-Blake B., Zylka M.J. Prostatic acid phosphatase is expressed in peptidergic and nonpeptidergic nociceptive neurons of mice and rats. PLoS One 2010, 5:e8674.
47. Vellani V., Zachrisson O., McNaughton P.A. Functional bradykinin B1 receptors are expressed in nociceptive neurones and are upregulated by the neurotrophin GDNF. J. Physiol. 2004, 560:391-401.
48. Vulchanova L., Olson T.H., Stone L.S., Riedl M.S., Elde R., Honda C.N. Cytotoxic targeting of isolectin IB4-binding sensory neurons. Neuroscience 2001, 108:143-155.
49. Wehrwein E.A., Roskelley E.M., Spitsbergen J.M. GDNF is regulated in an activity-dependent manner in rat skeletal muscle. Muscle Nerve 2002, 26:206-211.
50. Zebracki K., Drotar D. Pain and activity limitations in children with Duchenne or Becker muscular dystrophy. Dev. Med. Child. Neurol. 2008, 50:546-552.
51. Zimmerman M. Ethical guidelines for investigation of experimental pain in conscious animals. Pain 1983, 16:109.
52. Zylka M.J., Rice F.L., Anderson D.J. Topographically distinct epidermal nociceptive circuits revealed by axonal tracers targeted to Mrgprd. Neuron 2005, 45:17-25.