Blockade of P2 nucleotide receptors after spinal cord injury reduced the gliotic response and spared tissue

Journal of Molecular Neuroscience

Volumn 46, Issue 1, 2012, Pages 167-176

  Rodríguez Zayas, Ana E ^a   Torrado, Aranza I ^a   Rosas, Odrick R ^a   Santiago, José M ^a   Figueroa, Johnny D ^b   Miranda, Jorge D ^a  

^a UNIVERSITY OF PUERTO RICO SCHOOL OF MEDICINE   (Puerto Rico)

^b LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Glial scar; PPADS; Purinergic; Spare tissue; Suramin; Trauma

Indexed keywords

BUPRENORPHINE; CEFAZOLIN; PURINERGIC P2X2 RECEPTOR; PURINERGIC P2Y1 RECEPTOR; PURINERGIC P2Y12 RECEPTOR; PURINERGIC P2Y2 RECEPTOR; PURINERGIC P2Y4 RECEPTOR; PYRIDOXAL PHOSPHATE 6 AZOPHENYL 2',4' DISULFONIC ACID; SURAMIN; PURINERGIC P2 RECEPTOR; PURINERGIC P2 RECEPTOR ANTAGONIST; PURINERGIC P2Y6 RECEPTOR;

ANIMAL TISSUE; ARTICLE; ASTROCYTOSIS; CONTROLLED STUDY; DRUG EFFECT; FEMALE; GLIOSIS; IMMUNOHISTOCHEMISTRY; MOLECULAR BIOLOGY; NONHUMAN; OPEN FIELD TEST; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCAR FORMATION; SPINAL CORD INJURY; ANIMAL EXPERIMENT; ANIMAL MODEL; LOCOMOTION; NERVE FIBER REGENERATION; QUANTITATIVE ANALYSIS;

ANIMALIA; RATTUS;

ANIMALS; ANTINEOPLASTIC AGENTS; ASTROCYTES; BEHAVIOR, ANIMAL; FEMALE; GLIAL FIBRILLARY ACIDIC PROTEIN; GLIOSIS; MOTOR ACTIVITY; PLATELET AGGREGATION INHIBITORS; PURINERGIC P2 RECEPTOR ANTAGONISTS; PYRIDOXAL PHOSPHATE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, PURINERGIC P2; RECOVERY OF FUNCTION; RNA, MESSENGER; SPINAL CORD; SPINAL CORD INJURIES; SURAMIN;

EID: 84858864306     PISSN: 08958696     EISSN: 15591166     Source Type: Journal    
DOI: 10.1007/s12031-011-9567-6     Document Type: Article

References (77)

1. Abbracchio MP, Saffrey MJ, Hopker V, Burnstock G (1994) Modulation of astroglial cell proliferation by analogues of adenosine and ATP in primary cultures of rat striatum. Neuroscience 59:67-76 (Pubitemid 24125033)
2. Abbracchio MP, Burnstock G, Boeynaems JM et al (2006) International Union of Pharmacology LVIII: update on the P2Y G protein-coupled nucleotide receptors: from molecular mechanisms and pathophysiology to therapy. Pharmacol Rev 58:281-341 (Pubitemid 44394905)
3. Basso DM, Beattie MS, Bresnahan JC (1995) A sensitive and reliable locomotor rating scale for open field testing in rats. J Neurotrauma 12:1-21
4. Becker T, Anliker B, Becker CG et al (2000) Tenascin-R inhibits regrowth of optic fibers in vitro and persists in the optic nerve of mice after injury. Glia 29:330-346 (Pubitemid 30121423)
5. Burnstock G (1997) The past, present and future of purine nucleotides as signalling molecules. Neuropharmacology 36:1127-1139
6. Burnstock G (2000) P2X receptors in sensory neurones. Br J Anaesth 84:476-488
7. Bush TG, Puvanachandra N, Horner CH et al (1999) Leukocyte infiltration, neuronal degeneration, and neurite outgrowth after ablation of scar-forming, reactive astrocytes in adult transgenic mice. Neuron 23:297-308 (Pubitemid 29315725)
8. Cafferty WB, Yang SH, Duffy PJ, Li S, Strittmatter SM (2007) Functional axonal regeneration through astrocytic scar genetically modified to digest chondroitin sulfate proteoglycans. J Neurosci 27:2176-2185 (Pubitemid 46340954)
9. Cavaliere F, Florenzano F, Amadio S et al (2003) Up-regulation of P2X2, P2X4 receptor and ischemic cell death: prevention by P2 antagonists. Neuroscience 120:85-98 (Pubitemid 36782634)
10. Charlton SJ, Brown CA, Weisman GA, Turner JT, Erb L, Boarder MR (1996) PPADS and suramin as antagonists at cloned P2Y- and P2U-purinoceptors. Br J Pharmacol 118:704-710
11. Chiu FC, Goldman JE (1985) Regulation of glial fibrillary acidic protein (GFAP) expression in CNS development and in pathological states. J Neuroimmunol 8:283-292 (Pubitemid 15025256)
12. Collo G, North RA, Kawashima E et al (1996) Cloning OF P2X5 and P2X6 receptors and the distribution and properties of an extended family of ATP-gated ion channels. J Neurosci 16:2495-2507 (Pubitemid 26124346)
13. Cruz-Orengo L, Figueroa JD, Velazquez I et al (2006) Blocking EphA4 upregulation after spinal cord injury results in enhanced chronic pain. Exp Neurol 202:421-433 (Pubitemid 44692684)
14. Di Prospero NA, Zhou XR, Meiners S, McAuliffe WG, Ho SY, Geller HM (1998) Suramin disrupts the gliotic response following a stab wound injury to the adult rat brain. J Neurocytol 27:491-506 (Pubitemid 29204653)
15. Dijkstra S, Geisert EE Jr, Dijkstra CD, Bar PR, Joosten EA (2001) CD81 and microglial activation in vitro: proliferation, phagocytosis and nitric oxide production. J Neuroimmunol 114:151-159 (Pubitemid 32184736)
16. Ducker TB, Kindt GW, Kempf LG (1971) Pathological findings in acute experimental spinal cord trauma. J Neurosurg 35:700-708
17. Erb L, Liao Z, Seye CI, Weisman GA (2006) P2 receptors: intracellular signaling. Pflugers Arch 452:552-562 (Pubitemid 44015090)
18. Fam SR, Gallagher CJ, Salter MW (2000) P2Y(1) purinoceptor-mediated Ca(2+) signaling and Ca(2+) wave propagation in dorsal spinal cord astrocytes. J Neurosci 20:2800-2808 (Pubitemid 30220304)
19. Faulkner JR, Herrmann JE,Woo MJ, Tansey KE, Doan NB, Sofroniew MV (2004) Reactive astrocytes protect tissue and preserve function after spinal cord injury. J Neurosci 24:2143-2155 (Pubitemid 38314546)
20. Ferrari D, Chiozzi P, Falzoni S et al (1997) ATP-mediated cytotoxicity in microglial cells. Neuropharmacology 36:1295-1301 (Pubitemid 27465617)
21. Fields RD, Burnstock G (2006) Purinergic signalling in neuron-glia interactions. Nat Rev Neurosci 7:423-436 (Pubitemid 44012283)
22. Fields RD, Stevens-Graham B (2002) New insights into neuron-glia communication. Science 298:556-562
23. Figueroa JD, Benton RL, Velazquez I et al (2006) Inhibition of EphA7 up-regulation after spinal cord injury reduces apoptosis and promotes locomotor recovery. J Neurosci Res 84:1438-1451 (Pubitemid 44683138)
24. Fitch MT, Silver J (1997) Glial cell extracellular matrix: boundaries for axon growth in development and regeneration. Cell Tissue Res 290:379-384 (Pubitemid 27470072)
25. Fitch MT, Doller C, Combs CK, Landreth GE, Silver J (1999) Cellular and molecular mechanisms of glial scarring and progressive cavitation: in vivo and in vitro analysis of inflammation-induced secondary injury after CNS trauma. J Neurosci 19:8182-8198 (Pubitemid 30226738)
26. Fournier AE, Strittmatter SM (2001) Repulsive factors and axon regeneration in the CNS. Curr Opin Neurobiol 11:89-94 (Pubitemid 32155954)
27. Franke H, Illes P (2006) Involvement of P2 receptors in the growth and survival of neurons in the CNS. Pharmacol Ther 109:297-324 (Pubitemid 43132815)
28. Franke H, Krugel U, Schmidt R, Grosche J, Reichenbach A, Illes P (2001) P2 receptor-types involved in astrogliosis in vivo. Br J Pharmacol 134:1180-1189 (Pubitemid 33097247)
29. Franke H, Krugel U, Illes P (2006) P2 receptors and neuronal injury. Pflugers Arch 452:622-644 (Pubitemid 44015097)
30. Franke H, Sauer C, Rudolph C, Krügel U, Hengstler JG, Illes P (2009) P2 receptor-mediated stimulation of the PI3-K/Akt-pathway in vivo. Glia 57:1031-1045
31. Gordon JL (1986) Extracellular ATP: effects, sources and fate. Biochem J 233:309-319
32. Hansson E, Ronnback L (2003) Glial neuronal signaling in the centralnervous system. FASEB J 17:341-348 (Pubitemid 36292950)
33. Haydon PG (2001) GLIA: listening and talking to the synapse. Nat Rev Neurosci 2:185-193
34. Hulsebosch CE (2002) Recent advances in pathophysiology and treatment of spinal cord injury. Adv Physiol Educ 26:238-255
35. Iannotti C, Zhang YP, Shields LB et al (2006) Dural repair reduces connective tissue scar invasion and cystic cavity formation after acute spinal cord laceration injury in adult rats. J Neurotrauma 23:853-865 (Pubitemid 43962846)
36. Irizarry-Ramirez M, Willson CA, Cruz-Orengo L et al (2005) Upregulation of EphA3 receptor after spinal cord injury. J Neurotrauma 22:929-935 (Pubitemid 41153877)
37. Jacobson KA, Ivanov AA, de Castro S, Harden TK, Ko H (2009) Development of selective agonists and antagonists of P2Y receptors. Purinergic Signal 5:75-89
38. Kato S, Gondo T, Hoshii Y, Takahashi M, Yamada M, Ishihara T (1998) Confocal observation of senile plaques in Alzheimer's disease: senile plaque morphology and relationship between senile plaques and astrocytes. Pathol Int 48:332-340 (Pubitemid 28355156)
39. Kharlamov A, Jones SC, Kim DK (2002) Suramin reduces infarct volume in a model of focal brain ischemia in rats. Exp Brain Res 147:353-359 (Pubitemid 35341009)
40. Kobayashi K, Fukuoka T, Yamanaka H et al (2006) Neurons and glial cells differentially express P2Y receptor mRNAs in the rat dorsal root ganglion and spinal cord. J Comp Neurol 498:443-454 (Pubitemid 44232686)
41. Laird MD, Vender JR, Dhandapani KM (2008) Opposing roles for reactive astrocytes following traumatic brain injury. Neurosignals 16:154-164 (Pubitemid 351263222)
42. Lambrecht G, Braun K, Damer M et al (2002) Structure-activity relationships of suramin and pyridoxal-5′-phosphate derivatives as P2 receptor antagonists. Curr Pharm Des 8:2371-2399 (Pubitemid 35339325)
43. Laping NJ, Teter B, Nichols NR, Rozovsky I, Finch CE (1994) Glial fibrillary acidic protein: regulation by hormones, cytokines, and growth factors. Brain Pathol 4:259-275 (Pubitemid 24261932)
44. Lazarowski ER, Homolya L, Boucher RC, Harden TK (1997) Direct demonstration of mechanically induced release of cellular UTP and its implication for uridine nucleotide receptor activation. J Biol Chem 272:24348-24354 (Pubitemid 27418640)
45. McGraw J, Hiebert GW, Steeves JD (2001) Modulating astrogliosis after neurotrauma. J Neurosci Res 63:109-115 (Pubitemid 32041861)
46. McKerracher L, David S, Jackson DL, Kottis V, Dunn RJ, Braun PE (1994) Identification of myelin-associated glycoprotein as a major myelin-derived inhibitor of neurite growth. Neuron 13:805-811
47. Merkler D, Metz GA, Raineteau O, Dietz V, Schwab ME, Fouad K (2001) Locomotor recovery in spinal cord-injured rats treated with an antibody neutralizing the myelin-associated neurite growth inhibitor Nogo-A. J Neurosci 21:3665-3673 (Pubitemid 32422831)
48. Miranda JD, White LA, Marcillo AE, Willson CA, Jagid J, Whittemore SR (1999) Induction of Eph B3 after spinal cord injury. Exp Neurol 156:218-222 (Pubitemid 29153000)
49. Myer DJ, Gurkoff GG, Lee SM, Hovda DA, Sofroniew MV (2006) Essential protective roles of reactive astrocytes in traumatic brain injury. Brain 129:2761-2772 (Pubitemid 44523749)
50. Nakamura M, Bregman BS (2001) Differences in neurotrophic factor gene expression profiles between neonate and adult rat spinal cord after injury. Exp Neurol 169:407-415 (Pubitemid 32524435)
51. Neary JT, Baker L, Jorgensen SL, Norenberg MD (1994) Extracellular ATP induces stellation and increases glial fibrillary acidic protein content and DNA synthesis in primary astrocyte cultures. Acta Neuropathol 87:8-13 (Pubitemid 24011543)
52. Neary JT, Rathbone MP, Cattabeni F, Abbracchio MP, Burnstock G (1996) Trophic actions of extracellular nucleotides and nucleosides on glial and neuronal cells. Trends Neurosci 19:13-18 (Pubitemid 26011579)
53. Okada S, Nakamura M, Mikami Y et al (2004) Blockade of interleukin-6 receptor suppresses reactive astrogliosis and ameliorates functional recovery in experimental spinal cord injury. J Neurosci Res 76:265-276 (Pubitemid 38451214)
54. Park E, Velumian AA, Fehlings MG (2004) The role of excitotoxicity in secondary mechanisms of spinal cord injury: a review with an emphasis on the implications for white matter degeneration. J Neurotrauma 21:754-774 (Pubitemid 38880247)
55. Pasterkamp RJ, Anderson PN, Verhaagen J (2001) Peripheral nerve injury fails to induce growth of lesioned ascending dorsal column axons into spinal cord scar tissue expressing the axon repellent Semaphorin3A. Eur J Neurosci 13:457-471 (Pubitemid 32158777)
56. Peng W, Cotrina ML, Han X et al (2009) Systemic administration of an antagonist of the ATP-sensitive receptor P2X7 improves recovery after spinal cord injury. Proc Natl Acad Sci USA 106:12489-12493
57. Popovich PG, Guan Z, Wei P, Huitinga I, van Rooijen N, Stokes BT (1999) Depletion of hematogenous macrophages promotes partial hindlimb recovery and neuroanatomical repair after experimental spinal cord injury. Exp Neurol 158:351-365 (Pubitemid 29382826)
58. Popovich PG, van Rooijen N, Hickey WF, Preidis G, McGaughy V (2003) Hematogenous macrophages express CD8 and distribute to regions of lesion cavitation after spinal cord injury. Exp Neurol 182:275-287 (Pubitemid 36937081)
59. Rathbone MP, Middlemiss PJ, Gysbers JW et al (1999) Trophic effects of purines in neurons and glial cells. Prog Neurobiol 59:663-690 (Pubitemid 29457587)
60. Rodriguez-Zayas AE, Torrado AI, Miranda JD (2010) P2Y2 receptor expression is altered in rats after spinal cord injury. Int J Dev Neurosci 28:413-421
61. Santiago JM, Rosas O, Torrado AI, Gonzalez MM, Kalyan-Masih PO, Miranda JD (2009) Molecular, anatomical, physiological, and behavioral studies of rats treated with buprenorphine after spinal cord injury. J Neurotrauma 26:1783-1793
62. Scemes E, Suadicani SO, Spray DC (2000) Intercellular communication in spinal cord astrocytes: fine tuning between gap junctions and P2 nucleotide receptors in calcium wave propagation. J Neurosci 20:1435-1445 (Pubitemid 30220423)
63. Schnell L, Schwab ME (1990) Axonal regeneration in the rat spinal cord produced by an antibody against myelin-associated neurite growth inhibitors. Nature 343:269-272 (Pubitemid 20030644)
64. Sidoryk-Wegrzynowicz M, Wegrzynowicz M, Lee E, Bowman A, Aschner M (2010) Role of astrocytes in brain function and disease. Toxicol Pathol 39(1):115-123
65. Sinescu C, Popa F, Grigorean VTet al (2010)Molecular basis of vascular events following spinal cord injury. J Med Life 3:254-261
66. Skaper SD, Facci L, Culbert AA et al (2006) P2X(7) receptors on microglial cells mediate injury to cortical neurons in vitro. Glia 54:234-242 (Pubitemid 44230860)
67. Sofroniew MV, Vinters HV (2010) Astrocytes: biology and pathology. Acta Neuropathol 119:7-35
68. Tanhoffer RA, Yamazaki RK, Nunes EA et al (2007) Glutamine concentration and immune response of spinal cord-injured rats. J Spinal Cord Med 30:140-146 (Pubitemid 46942229)
69. Tompkins JD, Parsons RL (2006) Exocytotic release of ATP and activation of P2X receptors in dissociated guinea pig stellate neurons. Am J Physiol Cell Physiol 291:C1062-C1071 (Pubitemid 44771825)
70. Wang X, Arcuino G, Takano T et al (2004) P2X7 receptor inhibition improves recovery after spinal cord injury. Nat Med 10:821-827 (Pubitemid 39070855)
71. Washburn KB, Neary JT (2006) P2 purinergic receptors signal to STAT3 in astrocytes: difference in STAT3 responses to P2Y and P2X receptor activation. Neuroscience 142:411-423 (Pubitemid 44415340)
72. Weisman GA, Wang M, Kong Q et al (2005) Molecular determinants of P2Y2 nucleotide receptor function: implications for proliferative and inflammatory pathways in astrocytes. Mol Neurobiol 31:169-183 (Pubitemid 41271201)
73. Widenfalk J, Lundstromer K, Jubran M, Brene S, Olson L (2001) Neurotrophic factors and receptors in the immature and adult spinal cord after mechanical injury or kainic acid. J Neurosci 21:3457-3475 (Pubitemid 32422810)
74. Williams A, Piaton G, Lubetzki C (2007) Astrocytes-friends or foes in multiple sclerosis? Glia 55:1300-1312
75. Willson CA, Irizarry-Ramirez M, Gaskins HE et al (2002) Upregulation of EphA receptor expression in the injured adult rat spinal cord. Cell Transplant 11:229-239 (Pubitemid 34665823)
76. Zhang D, Hu X, Qian L, O'Callaghan JP, Hong JS (2010) Astrogliosis in CNS pathologies: is there a role for microglia? Mol Neurobiol 41:232-241
77. Zimmermann H (2006) Nucleotide signaling in nervous system development. Pflugers Arch 452:573-588