Dependence of monocyte chemoattractant protein 1 induced hyperalgesia on the isolectin B4-binding protein versican

Neuroscience

Volumn 159, Issue 2, 2009, Pages 780-786

  Bogen, O ^a   Dina, O A ^a   Gear, R W ^a   Levine, J D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

IB4; inflammation; MCP 1; pain; sensory neurons; versican

Indexed keywords

ADAMTS 4 PROTEIN; CHEMOKINE RECEPTOR CCR2; CHONDROITIN ABC LYASE; CHONDROITIN SULFATE; GLYCOSAMINOGLYCAN; ISOLECTIN B4; METALLOPROTEINASE; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN RET; SAPORIN; UNCLASSIFIED DRUG; VERSICAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; HYPERALGESIA; MALE; NOCICEPTIVE RECEPTOR; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN TARGETING; RAT;

ADAM PROTEINS; ANALYSIS OF VARIANCE; ANIMALS; CHEMOKINE CCL2; CHONDROITIN ABC LYASE; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG ADMINISTRATION ROUTES; HYPERALGESIA; LECTINS; MALE; NEUROTOXINS; OLIGORIBONUCLEOTIDES, ANTISENSE; PAIN MEASUREMENT; PAIN THRESHOLD; PROCOLLAGEN N-ENDOPEPTIDASE; RATS; RATS, SPRAGUE-DAWLEY; RIBOSOME INACTIVATING PROTEINS, TYPE 1; TIME FACTORS; VERSICANS;

EID: 60849135687     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2008.12.049     Document Type: Article

References (44)

1. Abbadie C., Lindia J.A., Cumiskey A.M., Peterson L.B., Mudgett J.S., Bayne E.K., DeMartino J.A., MacIntyre D.E., and Forrest M.J. Impaired neuropathic pain responses in mice lacking the chemokine receptor CCR2. Proc Natl Acad Sci U S A 100 (2003) 7947-7952
2. Alessandri-Haber N., Yeh J.J., Boyd A.E., Parada C.A., Chen X., Reichling D.B., and Levine J.D. Hypotonicity induces TRPV4-mediated nociception in rat. Neuron 39 (2003) 497-511
3. Aley K.O., Messing R.O., Mochly-Rosen D., and Levine J.D. Chronic hypersensitivity for inflammatory nociceptor sensitization mediated by the epsilon isozyme of protein kinase C. J Neurosci 20 (2000) 4680-4685
4. Bernfield M., Gotte M., Park P.W., Reizes O., Fitzgerald M.L., Lincecum J., and Zako M. Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem 68 (1999) 729-777
5. Bhangoo S., Ren D., Miller R.J., Henry K.J., Lineswala J., Hamdouchi C., Li B., Monahan P.E., Chan D.M., Ripsch M.S., and White F.A. Delayed functional expression of neuronal chemokine receptors following focal nerve demyelination in the rat: a mechanism for the development of chronic sensitization of peripheral nociceptors. Mol Pain 3 (2007) 38
6. Bogen O., Dreger M., Gillen C., Schroder W., and Hucho F. Identification of versican as an isolectin B4-binding glycoprotein from mammalian spinal cord tissue. FEBS J 272 (2005) 1090-1102
7. Bogen O., Joseph E.K., Chen X., and 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 28 (2008) 12-19
8. Bradbury E.J., Moon L.D., Popat R.J., King V.R., Bennett G.S., Patel P.N., Fawcett J.W., and McMahon S.B. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416 (2002) 636-640
9. Braunewell K.H., Martini R., LeBaron R., Kresse H., Faissner A., Schmitz B., and Schachner M. Upregulation of a chondroitin sulphate epitope during regeneration of mouse sciatic nerve: evidence that the immunoreactive molecules are related to the chondroitin sulphate proteoglycans decorin and versican. Eur J Neurosci 7 (1995) 792-804
10. Crown S.E., Yu Y., Sweeney M.D., Leary J.A., and Handel T.M. Heterodimerization of CCR2 chemokines and regulation by glycosaminoglycan binding. J Biol Chem 281 (2006) 25438-25446
11. Dina O.A., Hucho T., Yeh J., Malik-Hall M., Reichling D.B., and Levine J.D. Primary afferent second messenger cascades interact with specific integrin subunits in producing inflammatory hyperalgesia. Pain 115 (2005) 191-203
12. Dina O.A., Khasar S.G., Alessandri-Haber N., Green P.G., Messing R.O., and Levine J.D. Alcohol-induced stress in painful alcoholic neuropathy. Eur J Neurosci 27 (2008) 83-92
13. Dina O.A., Parada C.A., Yeh J., Chen X., McCarter G.C., and Levine J.D. Integrin signaling in inflammatory and neuropathic pain in the rat. Eur J Neurosci 19 (2004) 634-642
14. Gerke M.B., and Plenderleith M.B. Ultrastructural analysis of the central terminals of primary sensory neurones labelled by transganglionic transport of Bandeiraea simplicifolia I-isolectin B4. Neuroscience 127 (2004) 165-175
15. Hirose J., Kawashima H., Yoshie O., Tashiro K., and Miyasaka M. Versican interacts with chemokines and modulates cellular responses. J Biol Chem 276 (2001) 5228-5234
16. Hoogewerf A.J., Kuschert G.S., Proudfoot A.E., Borlat F., Clark-Lewis I., Power C.A., and Wells T.N. Glycosaminoglycans mediate cell surface oligomerization of chemokines. Biochemistry 36 (1997) 13570-13578
17. Jeon S.M., Lee K.M., Park E.S., Jeon Y.H., and Cho H.J. Monocyte chemoattractant protein-1 immunoreactivity in sensory ganglia and hindpaw after adjuvant injection. Neuroreport 19 (2008) 183-186
18. Joseph E.K., Bogen O., Alessandri-Haber N., and Levine J.D. PLC-beta 3 signals upstream of PKC epsilon in acute and chronic inflammatory hyperalgesia. Pain 132 (2007) 67-73
19. Joseph E.K., Chen X., Bogen O., and Levine J.D. Oxaliplatin acts on IB4-positive nociceptors to induce an oxidative stress-dependent acute painful peripheral neuropathy. J Pain 9 (2008) 463-472
20. Jung H., Toth P.T., White F.A., and Miller R.J. Monocyte chemoattractant protein-1 functions as a neuromodulator in dorsal root ganglia neurons. J Neurochem 104 (2008) 254-263
21. Kawashima H., Atarashi K., Hirose M., Hirose J., Yamada S., Sugahara K., and Miyasaka M. Oversulfated chondroitin/dermatan sulfates containing GlcAbeta1/IdoAalpha1-3GalNAc(4,6-O-disulfate) interact with L- and P-selectin and chemokines. J Biol Chem 277 (2002) 12921-12930
22. Kawashima H., Hirose M., Hirose J., Nagakubo D., Plaas A.H., and Miyasaka M. Binding of a large chondroitin sulfate/dermatan sulfate proteoglycan, versican, to L-selectin, P-selectin, and CD44. J Biol Chem 275 (2000) 35448-35456
23. Kuschert G.S., Coulin F., Power C.A., Proudfoot A.E., Hubbard R.E., Hoogewerf A.J., and Wells T.N. Glycosaminoglycans interact selectively with chemokines and modulate receptor binding and cellular responses. Biochemistry 38 (1999) 12959-12968
24. Malik-Hall M., Dina O.A., and Levine J.D. Primary afferent nociceptor mechanisms mediating NGF-induced mechanical hyperalgesia. Eur J Neurosci 21 (2005) 3387-3394
25. Menetski J., Mistry S., Lu M., Mudgett J.S., Ransohoff R.M., Demartino J.A., Macintyre D.E., and Abbadie C. Mice overexpressing chemokine ligand 2 (CCL2) in astrocytes display enhanced nociceptive responses. Neuroscience 149 (2007) 706-714
26. Nishiguchi J., Sasaki K., Seki S., Chancellor M.B., Erickson K.A., de Groat W.C., Kumon H., and Yoshimura N. Effects of isolectin B4-conjugated saporin, a targeting cytotoxin, on bladder overactivity induced by bladder irritation. Eur J Neurosci 20 (2004) 474-482
27. Proudfoot A.E., Handel T.M., Johnson Z., Lau E.K., Li Wang P., Clark-Lewis I., Borlat F., Wells T.N., and Kosco-Vilbois M.H. Glycosaminoglycan binding and oligomerization are essential for the in vivo activity of certain chemokines. Proc Natl Acad Sci U S A 100 (2003) 1885-1890
28. Qin X., Wan Y., and Wang X. CCL2 and CXCL1 trigger calcitonin gene-related peptide release by exciting primary nociceptive neurons. J Neurosci Res 82 (2005) 51-62
29. Randolph G.J., and Furie M.B. A soluble gradient of endogenous monocyte chemoattractant protein-1 promotes the transendothelial migration of monocytes in vitro. J Immunol 155 (1995) 3610-3618
30. Rollins B.J. Monocyte chemoattractant protein 1: a potential regulator of monocyte recruitment in inflammatory disease. Mol Med Today 2 (1996) 198-204
31. Sandy J.D., Westling J., Kenagy R.D., Iruela-Arispe M.L., Verscharen C., Rodriguez-Mazaneque J.C., Zimmermann D.R., Lemire J.M., Fischer J.W., Wight T.N., and Clowes A.W. Versican V1 proteolysis in human aorta in vivo occurs at the Glu441-Ala442 bond, a site that is cleaved by recombinant ADAMTS-1 and ADAMTS-4. J Biol Chem 276 (2001) 13372-13378
32. Snider W.D., and McMahon S.B. Tackling pain at the source: new ideas about nociceptors. Neuron 20 (1998) 629-632
33. Stucky C.L., and Lewin G.R. Isolectin B(4)-positive and -negative nociceptors are functionally distinct. J Neurosci 19 (1999) 6497-6505
34. Tanaka T., Minami M., Nakagawa T., and Satoh M. Enhanced production of monocyte chemoattractant protein-1 in the dorsal root ganglia in a rat model of neuropathic pain: possible involvement in the development of neuropathic pain. Neurosci Res 48 (2004) 463-469
35. Vulchanova L., Olson T.H., Stone L.S., Riedl M.S., Elde R., and Honda C.N. Cytotoxic targeting of isolectin IB4-binding sensory neurons. Neuroscience 108 (2001) 143-155
36. Westling J., Gottschall P.E., Thompson V.P., Cockburn A., Perides G., Zimmermann D.R., and Sandy J.D. ADAMTS4 (aggrecanase-1) cleaves human brain versican V2 at Glu405-Gln406 to generate glial hyaluronate binding protein. Biochem J 377 (2004) 787-795
37. White F.A., Bhangoo S.K., and Miller R.J. Chemokines: integrators of pain and inflammation. Nat Rev Drug Discov 4 (2005) 834-844
38. White F.A., Sun J., Waters S.M., Ma C., Ren D., Ripsch M., Steflik J., Cortright D.N., Lamotte R.H., and Miller R.J. Excitatory monocyte chemoattractant protein-1 signaling is upregulated in sensory neurons after chronic compression of the dorsal root ganglion. Proc Natl Acad Sci U S A 102 (2005) 14092-14097
39. Wight T.N. Versican: a versatile extracellular matrix proteoglycan in cell biology. Curr Opin Cell Biol 14 (2002) 617-623
40. Wu Y.J., La Pierre D.P., Wu J., Yee A.J., and Yang B.B. The interaction of versican with its binding partners. Cell Res 15 (2005) 483-494
41. Yamagata M., and Sanes J.R. Versican in the developing brain: lamina-specific expression in interneuronal subsets and role in presynaptic maturation. J Neurosci 25 (2005) 8457-8467
42. Zhang Y., and Rollins B.J. A dominant negative inhibitor indicates that monocyte chemoattractant protein 1 functions as a dimer. Mol Cell Biol 15 (1995) 4851-4855
43. Zheng P.S., Vais D., Lapierre D., Liang Y.Y., Lee V., Yang B.L., and Yang B.B. PG-M/versican binds to P-selectin glycoprotein ligand-1 and mediates leukocyte aggregation. J Cell Sci 117 (2004) 5887-5895
44. Zylka M.J., Rice F.L., and Anderson D.J. Topographically distinct epidermal nociceptive circuits revealed by axonal tracers targeted to Mrgprd. Neuron 45 (2005) 17-25