Role of matrix metalloproteinases 2 in spinal cord injury-induced neuropathic pain

Annals of Neurosciences

Volumn 23, Issue 1, 2016, Pages 25-32

  Miranpuri, Gurwattan S ^a   Schomberg, Dominic T ^a   Alrfaei, Bahauddeen ^a   King, Kevin C ^a   Rynearson, Bryan ^a   Wesley, Vishwas S ^a   Khan, Nayab ^a   Obiakor, Kristen ^a   Wesley, Umadevi V ^a   Resnick, Daniel K ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

Contusion spinal cord injury; ERK MAPK; Matrix metalloproteinases; Neuropathic pain; Thermal hyperalgesia; catenin

Indexed keywords

BETA CATENIN; GELATINASE A; MITOGEN ACTIVATED PROTEIN KINASE; WNT PROTEIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHRONIC PAIN; CONTROLLED STUDY; DISEASE ACTIVITY; DISEASE ASSOCIATION; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME PHOSPHORYLATION; FUNCTIONAL ASSESSMENT; LOCOMOTION; MALE; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; NEUROPATHIC PAIN; NONHUMAN; PAIN ASSESSMENT; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RAT; SCORING SYSTEM; SIGNAL TRANSDUCTION; SPINAL CORD INJURY; UPREGULATION;

EID: 84961230907     PISSN: 09727531     EISSN: 09763260     Source Type: Journal    
DOI: 10.1159/000443553     Document Type: Article

References (43)

1. National Spinal Cord Injury Statistical Center: The 2010 Annual Report for the Spinal Cord Injury Model Systems, National Spinal Cord Injury Statistical Center, Birmingham, Alabama, which is funded by grant number H133A060039 from the National Institute on Disability and Rehabilitation Research, Office of Special Education and Rehabilitative Services, U. S. Department of Education.
2. Finnerup NB, Sindrup SH, Jensen TS: Chronic neuropathic pain: mechanisms, drug targets and measurement. Fundam Clin Pharmacol 2007; 21: 129-136.
3. Yezierski RP: Spinal cord injury: a model of central neuropathic pain. Neurosignals 2005; 14: 182-193.
4. Barrett H, McClelland JM, Rutkowski SB, Siddall PJ: Pain characteristics in patients admitted to hospital with complications after spinal cord injury. Arch Phys Med Rehabil 2003; 84: 789-795.
5. Siddall PJ, McClelland JM, Rutkowski SB, Cousins MJ: A longitudinal study of the prevalence and characteristics of pain in the first 5 years following spinal cord injury. Pain 2003; 103: 249-257.
6. Noble LJ, Donovan F, Igarashi T, Goussev S, Werb Z: Matrix metalloproteinases limit functional recovery after spinal cord injury by modulation of early vascular events. J Neurosci 2002; 22: 7526-7535.
7. Kawasaki Y, Xu ZZ, Wang X, Park JY, Zhuang ZY, Tan PH, Gao YJ, Roy K, Corfas G, Lo EH, Ji RR: Distinct roles of matrix metalloproteases in the early-and late-phase development of neuropathic pain. Nat Med 2008; 14: 331-336.
8. Detloff MR, Fisher LC, McGaughy V, Longbrake EE, Popovich PG, Basso DM: Remote activation of microglia and pro-inflammatory cytokines predict the onset and severity of below-level neuropathic pain after spinal cord injury in rats. Exp Neurol 2008; 212: 337-347.
9. de Castro RC Jr, Burns CL, McAdoo DJ, Romanic AM: Metalloproteinase increases in the injured rat spinal cord. Neuroreport 2000; 11: 3551-3554.
10. Ji H, Wang J, Nika H, Hawke D, Keezer S, Ge Q, Fang B, Fang X, Fang D, Litchfield DW, Aldape K, Lu Z: EGF-induced ERK activation promotes CK2-mediated disassociation of alpha-catenin from beta-catenin and transactivation of beta-catenin. Mol Cell 2009; 36: 547-559.
11. Pang XY, Liu T, Jiang F, Ji YH: Activation of spinal ERK signaling pathway contributes to pain-related responses induced by scorpion Buthus martensi Karch venom. Toxicon 2008; 51: 994-1007.
12. Zhang X, Chen G, Xue Q, Yu B: Early changes of beta-catenins and menins in spinal cord dorsal horn after peripheral nerve injury. Cell Mol Neurobiol 2010; 30: 885-890.
13. Wu B, Crampton SP, Hughes CC: Wnt signaling induces matrix metalloproteinase expression and regulates T cell transmigration. Immunity 2007; 26: 227-239.
14. Bikkavilli RK, Malbon CC: Mitogen-activated protein kinases and Wnt/beta-catenin signaling: molecular conversations among signaling pathways. Commun Integr Biol 2009; 2: 46-49.
15. Resnick DK, Cechvala CF, Yan Y, Witwer BP, Sun D, Zhang S: Adult olfactory ensheathing cell transplantation for acute spinal cord injury. J Neurotrauma 2003; 20: 279-285.
16. Resnick DK, Schmitt C, Miranpuri GS, Dhodda VK, Isaacson J, Vemuganti R: Molecular evidence of repair and plasticity following spinal cord injury. Neuroreport 2004; 15: 837-839.
17. Schmitt C, Miranpuri GS, Dhodda VK, Isaacson J, Vemuganti R, Resnick DK: Changes in spinal cord injury-induced gene expression in rat are strain-dependent. Spine J 2006; 6: 113-119.
18. DomBourian MG, Turner NA, Gerovac TA, Vemuganti R, Miranpuri GS, Türeyen K, Satriotomo I, Miletic V, Resnick DK: B1 and TRPV-1 receptor genes and their relationship to hyperalgesia following spinal cord injury. Spine (Phila Pa 1976) 2006; 31: 2778-2782.
19. Rajpal S, Gerovac TA, Turner NA, Tilghman JI, Allcock BK, McChesney SL, Miranpuri GS, Park SW, Resnick DK: Antihyperalgesic effects of vanilloid-1 and bradykinin-1 receptor antagonists following spinal cord injury in rats. J Neurosurg Spine 2007; 6: 420-424.
20. Park SW, Yi JH, Miranpuri G, et al: Thiazolidinedione class of peroxisome proliferatoractivated receptor gamma agonists prevents neuronal damage, motor dysfunction, myelin loss, neuropathic pain, and inflammation after spinal cord injury in adult rats. J Pharmacol Exp Ther 2007; 320: 1002-1012.
21. Cramer SW, Baggott C, Cain J, Tilghman J, Allcock B, Miranpuri G, Rajpal S, Sun D, Resnick D: The role of cation-dependent chloride transporters in neuropathic pain following spinal cord injury. Mol Pain 2008; 4: 36.
22. Ahmed M, Rajpal S, Sweeney C, Gerovac TA, Allcock B, McChesney S, Patel AU, Tilghman JI, Miranpuri GS, Resnick DK: Cannabinoid subtype-2 receptors modulate the antihyperalgesic effect of WIN 55, 212-2 in rats with neuropathic spinal cord injury pain. Spine J 2010; 10: 1049-1054.
23. Kim HT, Kim T, Novotny B, Khan N, Aksamit J, Siegel S, Miranpuri GS, Resnick DK: Thermal hyperalgesia assessment for rats after spinal cord injury: developing a valid and useful pain index. Spine J 2014; 14: 984-989.
24. Ahmed MM, Lee H, Clark Z, Miranpuri GS, Nacht C, Patel K, Liu L, Joslin J, Kintner D, Resnick DK: Pathogenesis of spinal cord injury induced edema and neuropathic pain: expression of multiple isoforms of WNK1. Ann Neurosci 2014; 21: 97-103.
25. Basso DM, Beattie MS, Bresnahan JC: A sensitive and reliable locomotor rating scale for open field testing in rats. J Neurotrauma 1995; 12: 1-21.
26. Hargreaves K, Dubner R, Brown F, Flores C, Joris J: A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 1988; 32: 77-88.
27. Wang X, Jung J, Asahi M, Chwang W, Russo L, Moskowitz MA, Dixon CE, Fini ME, Lo EH: Effects of matrix metalloproteinase-9 gene knock-out on morphological and motor outcomes after traumatic brain injury. J Neurosci 2000; 20: 7037-7042.
28. Rice AS, Farquhar-Smith WP, Nagy I: Endocannabinoids and pain: spinal and peripheral analgesia in inflammation and neuropathy. Prostaglandins Leukot Essent Fatty Acids 2002; 66: 243-256.
29. Ramer R, Hinz B: Cyclooxygenase-2 and tissue inhibitor of matrix metalloproteinases-1 confer the antimigratory effect of cannabinoids on human trabecular meshwork cells. Biochem Pharmacol 2010; 80: 846-857.
30. Li WH, Lee YM, Kim JY, Kang S, Kim S, Kim KH, Park CH, Chung JH: Transient receptor potential vanilloid-1 mediates heat-shock-induced matrix metalloproteinase-1 expression in human epidermal keratinocytes. J Invest Dermatol 2007; 127: 2328-2335.
31. Parks WC, Wilson CL, López-Boado YS: Matrix metalloproteinases as modulators of inflammation and innate immunity. Nat Rev Immunol 2004; 4: 617-629.
32. Chattopadhyay S, Myers RR, Janes J, Shubayev V: Cytokine regulation of MMP-9 in peripheral glia: implications for pathological processes and pain in injured nerve. Brain Behav Immun 2007; 21: 561-568.
33. Rosenberg GA, Cunningham LA, Wallace J, Alexander S, Estrada EY, Grossetete M, Razhagi A, Miller K, Gearing A: Immunohistochemistry of matrix metalloproteinases in reperfusion injury to rat brain: activation of MMP-9 linked to stromelysin-1 and microglia in cell cultures. Brain Res 2001; 893: 104-112.
34. Rosenberg GA: Matrix metalloproteinases in neuroinflammation. Glia 2002; 39: 279-291.
35. Yong VW: Metalloproteinases: mediators of pathology and regeneration in the CNS. Nat Rev Neurosci 2005; 6: 931-944.
36. Zhao BQ, Wang S, Kim HY, Storrie H, Rosen BR, Mooney DJ, Wang X, Lo EH: Role of matrix metalloproteinases in delayed cortical responses after stroke. Nat Med 2006; 12: 441-445.
37. Ahmed MM, King KC, Pearce SM, Ramsey MA, Miranpuri GS, Resnick DK: Novel targets for spinal cord injury related neuropathic pain. Ann Neurosci 2011; 18: 162-167.
38. Lakhan SE, Avramut M: Matrix metalloproteinases in neuropathic pain and migraine: friends, enemies, and therapeutic targets. Pain Res Treat 2012; 2012: 952906.
39. Kobayashi K, Yamanaka H, Fukuoka T, Dai Y, Obata K, Noguchi K: P2Y12 receptor upregulation in activated microglia is a gateway of p38 signaling and neuropathic pain. J Neurosci 2008; 28: 2892-2902.
40. Liu S, Liu YP, Huang ZJ, Zhang YK, Song AA, Ma PC, Song XJ: Wnt/Ryk signaling contributes to neuropathic pain by regulating sensory neuron excitability and spinal synaptic plasticity in rats. Pain 2015; 156: 2572-2584.
41. Yang C, Iyer RR, Yu AC, Yong RL, Park DM, Weil RJ, Ikejiri B, Brady RO, Lonser RR, Zhuang Z: β-Catenin signaling initiates the activation of astrocytes and its dysregulation contributes to the pathogenesis of astrocytomas. Proc Natl Acad Sci U S A 2012; 109: 6963-6968.
42. Takahashi-Yanaga F, Sasaguri T: The Wnt/ beta-catenin signaling pathway as a target in drug discovery. J Pharmacol Sci 2007; 104: 293-302.
43. Maiese K, Li F, Chong ZZ, Shang YC: The Wnt signaling pathway: aging gracefully as a protectionist? Pharmacol Ther 2008; 118: 58-81.