Folic acid modulates matrix metalloproteinase-2 expression, alleviates neuropathic pain, and improves functional recovery in spinal cord-injured rats

Annals of Neurosciences

Volumn 24, Issue 2, 2017, Pages 74-81

  Miranpuri, Gurwattan S ^a   Meethal, Sivan Vadakkadath ^a   Sampene, Emmanuel ^b   Chopra, Abhishek ^a   Buttar, Seah ^a   Nacht, Carrie ^a   Moreno, Neydis ^a   Patel, Kush ^a   Liu, Lisa ^a   Singh, Anupama ^a   Singh, Chandra K ^b   Hariharan, Nithya ^a   Iskandar, Bermans ^a   Resnick, Daniel K ^a  

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

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Contusion spinal cord injury; DNA methylation; Folic acid; Matrix metalloproteinase; Matrix metalloproteinase 2; Neuropathic pain; Thermal hyperalgesia

Indexed keywords

FOLIC ACID; GELATINASE A; MESSENGER RNA; NOTCH1 RECEPTOR; PLACEBO;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASSO BEATTIE AND BRESNAHAN SCORE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; CONVALESCENCE; DIET SUPPLEMENTATION; DNA METHYLATION; DRUG MECHANISM; FUNCTIONAL RECOVERY; GENE EXPRESSION REGULATION; HYPERALGESIA; MALE; MOLECULAR DYNAMICS; NERVE FIBER REGENERATION; NEUROPATHIC PAIN; NONHUMAN; OUTCOME ASSESSMENT; PROMOTER REGION; PROTEIN EXPRESSION; RAT; SCORING SYSTEM; SPINAL CORD INJURY; SPRAGUE DAWLEY RAT; THERMAL HYPERALGESIA; TRANSCRIPTION REGULATION; WESTERN BLOTTING;

EID: 85019179806     PISSN: 09727531     EISSN: 09763260     Source Type: Journal    
DOI: 10.1159/000475896     Document Type: Article

References (36)

1. 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.
2. Zhang H, Chang M, Hansen CN, Basso DM, Noble-Haeusslein LJ: Role of matrix metalloproteinases and therapeutic benefits of their inhibition in spinal cord injury. Neurotherapeutics 2011; 8: 206-220.
3. Pathak NN, Balaganur V, Lingaraju MC, More AS, Kant V, Kumar D, Kumar D, Tandan SK: Antihyperalgesic and anti-inflammatory effects of atorvastatin in chronic constriction injury-induced neuropathic pain in rats. Inflammation 2013; 36: 1468-1478.
4. Schomberg D, Miranpuri G, Duellman T, Crowell A, Vemuganti R, Resnick D: Spinal cord injury induced neuropathic pain: molecular targets and therapeutic approaches. Metab Brain Dis 2015; 30: 645-658.
5. Miranpuri GS, Schomberg DT, Alrfaei B, King KC, Rynearson B, Wesley VS, Khan N, Obiakor K, Wesley UV, Resnick DK: Role of matrix metalloproteinases 2 in spinal cord Injury- induced neuropathic pain. Ann Neurosci 2016; 23: 25-32.
6. Wang Y, Liu C, Guo QL, Yan JQ, Zhu XY, Huang CS, Zou WY: Intrathecal 5-azacytidine inhibits global DNA methylation and methyl- CpG-binding protein 2 expression and alleviates neuropathic pain in rats following chronic constriction injury. Brain Res 2011; 1418: 64-69.
7. Burzynski SR: Aging: gene silencing or gene activation? Med Hypotheses 2005; 64: 201-208.
8. Hackanson B, Robbel C, Wijermans P, Lübbert M: In vivo effects of decitabine in myelodysplasia and acute myeloid leukemia: review of cytogenetic and molecular studies. Ann Hematol 2005; 84(suppl 1):32-38.
9. Reichard JF, Puga A: Effects of arsenic exposure on DNA methylation and epigenetic gene regulation. Epigenomics 2010; 2: 87-104.
10. Chicoine E, Esteve PO, Robledo O, Van Themsche C, Potworowski EF, St-Pierre Y: Evidence for the role of promoter methylation in the regulation of MMP-9 gene expression. Biochem Biophys Res Commun 2002; 297: 765-772.
11. Iskandar BJ, Nelson A, Resnick D, et al: Folic acid supplementation enhances repair of the adult central nervous system. Ann Neurol 2004; 56: 221-227.
12. Iskandar BJ, Rizk E, Meier B, et al: Folate regulation of axonal regeneration in the rodent central nervous system through DNA methylation. J Clin Invest 2010; 120: 1603-1616.
13. 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.
14. 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 injur. Spine (Phila Pa 1976) 2006; 31: 2778-2782.
15. 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.
16. Park SW, Yi JH, Miranpuri G, Satriotomo I, Bowen K, Resnick DK, Vemuganti R: Thiazolidinedione class of peroxisome proliferator- activated 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.
17. 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; 17; 4: 36.
18. Ahmed MM, 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.
19. 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.
20. 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.
21. 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.
22. 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.
23. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ: Protein measurement with the Folin phenol reagent. J Biol Chem 1951; 193: 265-275.
24. de Castro RC Jr, Burns CL, McAdoo DJ, Romanic AM: Metalloproteinase increases in the injured rat spinal cord. Neuroreport 2000; 11:3551-3554.
25. Mott JD, Werb Z: Regulation of matrix biology by matrix metalloproteinases. Curr Opin Cell Biol 2004; 16: 558-564.
26. Esposito E, Genovese T, Caminiti R, Bramanti P, Meli R, Cuzzocrea S: Melatonin regulates matrix metalloproteinases after traumatic experimental spinal cord injury. J Pineal Res 2008; 45: 149-156.
27. Buss A, Pech K, Kakulas BA, Martin D, Schoenen J, Noth J, Brook GA: Matrix metalloproteinases and their inhibitors in human traumatic spinal cord injury. BMC Neurol 2007; 7:17.
28. 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.
29. Chernov AV, Strongin AY: Epigenetic regulation of matrix metalloproteinases and their collagen substrates in cancer. Biomol Concepts 2011; 2: 135-147.
30. Couillard J, Demers M, Lavoie G, St-Pierre Y: The role of DNA hypomethylation in the control of stromelysin gene expression. Biochem Biophy Res Comm 2006; 342: 1233-1239.
31. Filous AR, Miller JH, Coulson-Thomas YM, Horn KP, Alilain WJ, Silver J: Immature astrocytes promote CNS axonal regeneration when combined with chondroitinase ABC. Dev Neurobiol 2010; 70: 826-841.
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. Kobayashi K, Yamanaka H, Fukuoka T, Dai Y, Obata K, Noguchi K: P2Y 12 receptor upregulation in activated microglia is a gateway of p38 signaling and neuropathic pain. J Neurosci 2008; 28: 2892-2902.
34. Liu H, Huang GW, Zhang XM, Ren DL, X Wilson J: Folic acid supplementation stimulates notch signaling and cell proliferation in embryonic neural stem cells. J Clin Biochem Nutr 2010; 47: 174-180.
35. Zhang X, Liu H, Cong G, Tian Z, Ren D, Wilson JX, Huang G: Effects of folate on notch signaling and cell proliferation in neural stem cells of neonatal rats in vitro. J Nutr Sci Vitaminol (Tokyo) 2008; 54: 353-356.
36. Zhang C, Shen L: Folic acid in combination with adult neural stem cells for the treatment of spinal cord injury in rats. Int J Clin Exp Med 2015; 8: 10471-10480.