Oral administration of a small molecule targeted to block proNGF binding to p75 promotes myelin sparing and functional recovery after spinal cord injury

Journal of Neuroscience

Volumn 33, Issue 2, 2013, Pages 397-410

  Tep, Chhavy ^a   Lim, Tae Hee ^a   Ko, Pyung On ^a   Getahun, Sami ^a   Ryu, Jae Cheon ^a   Goettl, Virginia M ^a   Massa, Stephen M ^b   Basso, Michele ^a   Longo, Frank M ^c   Yoon, Sung Ok ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C1; GLIAL FIBRILLARY ACIDIC PROTEIN; LM11A 31; MYELIN; NERVE GROWTH FACTOR; PROTEIN INHIBITOR; PROTEIN P75; PROTEOCHONDROITIN SULFATE; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD CEREBROSPINAL FLUID BARRIER; CONTROLLED STUDY; COORDINATION; DRUG DOSE COMPARISON; FEMALE; FORCED SWIMMING TEST; FRACTIONATION; HISTOLOGY; HYPERALGESIA; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; LAMINECTOMY; LOCOMOTION; MOTOR PERFORMANCE; MOUSE; MYELINATED NERVE; NEUROFILAMENT; NONHUMAN; OLIGODENDROGLIA; OPEN FIELD TEST; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SCHWANN CELL; SCORING SYSTEM; SPINAL CORD INJURY; WEIGHT REDUCTION; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; DNA; DOSE-RESPONSE RELATIONSHIP, DRUG; FORELIMB; HINDLIMB; HYPERALGESIA; IMMUNOHISTOCHEMISTRY; ISOLEUCINE; LOCOMOTION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA; MITOGEN-ACTIVATED PROTEIN KINASE 10; MORPHOLINES; MYELIN SHEATH; NERVE GROWTH FACTOR; POLYMERASE CHAIN REACTION; PROTEIN PRECURSORS; RECEPTOR, NERVE GROWTH FACTOR; SPINAL CORD INJURIES; SWIMMING;

EID: 84872055368     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0399-12.2013     Document Type: Article

References (52)

1. Abott NJ (2004) Prediction of blood-brain barrier permeation in drug discovery from in vivo, in vitro and in silico models. Drug Discov Today Technol 1:407-416. CrossRef
2. Basso DM, Fisher LC, Anderson AJ, Jakeman LB, McTigue DM, Popovich PG (2006) Basso mouse scale for locomotion detects differences in recovery after spinal cord injury in five common mouse strains. J Neurotrauma 23:635-659. CrossRef Medline
3. Beattie MS, Harrington AW, Lee R, Kim JY, Boyce SL, Longo FM, Bresnahan JC, Hempstead BL, Yoon SO (2002) ProNGF induces p75-mediated death of oligodendrocytes following spinal cord injury. Neuron 36:375-386. CrossRef Medline
4. Bennett GJ, Xie YK (1988) A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 33:87-107. CrossRef Medline
5. Bentley CA, Lee KF (2000) p75 is important for axon growth and schwann cell migration during development [In Process Citation]. J Neurosci 20: 7706-7715. Medline
6. Biernaskie J, Sparling JS, Liu J, Shannon CP, Plemel JR, Xie Y, Miller FD, Tetzlaff W (2007) Skin-derived precursors generate myelinating Schwann cells that promote remyelination and functional recovery after contusion spinal cord injury. J Neurosci 27:9545-9559. CrossRef Medline
7. Bradbury EJ, Moon LD, Popat RJ, King VR, Bennett GS, Patel PN, Fawcett JW, McMahon SB (2002) Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416:636-640. CrossRef Medline
8. Busch SA, Silver J (2007) The role of extracellular matrix in CNS regeneration. Curr Opin Neurobiol 17:120-127. CrossRef Medline
9. Cao Q, Xu XM, Devries WH, Enzmann GU, Ping P, Tsoulfas P, Wood PM, Bunge MB, Whittemore SR (2005) Functional recovery in traumatic spinal cord injury after transplantation of multineurotrophin-expressing glial-restricted precursor cells. J Neurosci 25:6947-6957. CrossRef Medline
10. Cao Q, He Q, Wang Y, Cheng X, Howard RM, Zhang Y, DeVries WH, Shields CB, Magnuson DS, Xu XM, Kim DH, Whittemore SR (2010) Transplantation of ciliary neurotrophic factor-expressing adult oligodendrocyte precursor cells promotes remyelination and functional recovery after spinal cord injury. J Neurosci 30:2989-3001. CrossRef Medline
11. Crowe MJ, Bresnahan JC, Shuman SL, Masters JN, Beattie MS (1997) Apoptosis and delayed degeneration after spinal cord injury in rats and monkeys [published erratum appears in Nat Med 1997 Feb;3:240]. Nat Med 3:73-76. CrossRef Medline
12. David S, Kroner A (2011) Repertoire of microglial and macrophage responses after spinal cord injury. Nat Rev Neurosci 12:388-399. CrossRef Medline
13. Demjen D, Klussmann S, Kleber S, Zuliani C, Stieltjes B, Metzger C, Hirt UA, Walczak H, Falk W, Essig M, Edler L, Krammer PH, Martin-Villalba A (2004) Neutralization of CD95 ligand promotes regeneration and functional recovery after spinal cord injury. Nat Med 10:389-395. CrossRef Medline
14. Gullo M, Hochreutener, E., Schnell, D., Scholl, J., Schwab, M.E., and Schnell, L. (2008) The Schnell Swim Test (SST) to measure motor function and recovery in spinal cord injured rats. Paper presented at the 6th International Conference on Methods and Techniques in Behavioral Research, Maastricht, The Netherlands, August. Proceedings of Measuring Behavior, p. 35-36.
15. Harrington AW, Leiner B, Blechschmitt C, Arevalo JC, Lee R, Mörl K, Meyer M, Hempstead BL, Yoon SO, Giehl KM (2004) Secreted proNGF is a pathophysiological death-inducing ligand after adult CNS injury. Proc Natl Acad Sci U S A 101:6226-6230. CrossRef Medline
16. Hofstetter CP, Holmström NA, Lilja JA, Schweinhardt P, Hao J, Spenger C, Wiesenfeld-Hallin Z, Kurpad SN, Frisén J, Olson L (2005) Allodynia limits the usefulness of intraspinal neural stem cell grafts; directed differentiation improves outcome. Nat Neurosci 8:346-353. CrossRef Medline
17. Hoschouer EL, Basso DM, Jakeman LB (2010) Aberrant sensory responses are dependent on lesion severity after spinal cord contusion injury in mice. Pain 148:328-342. CrossRef Medline
18. Karimi-Abdolrezaee S, Eftekharpour E, Wang J, Morshead CM, Fehlings MG (2006) Delayed transplantation of adult neural precursor cells promotes remyelination and functional neurological recovery after spinal cord injury. J Neurosci 26:3377-3389. CrossRef Medline
19. Karimi-Abdolrezaee S, Eftekharpour E, Wang J, Schut D, Fehlings MG (2010) Synergistic effects of transplanted adult neural stem/progenitor cells, chondroitinase, and growth factors promote functional repair and plasticity of the chronically injured spinal cord. J Neurosci 30:1657-1676. CrossRef Medline
20. Keirstead HS, Nistor G, Bernal G, Totoiu M, Cloutier F, Sharp K, Steward O (2005) Human embryonic stem cell-derived oligodendrocyte progenitor cell transplants remyelinate and restore locomotion after spinal cord injury. J Neurosci 25:4694-4705. CrossRef Medline
21. Kigerl KA, Lai W, Rivest S, Hart RP, Satoskar AR, Popovich PG (2007) Tolllike receptor (TLR)-2 and TLR-4 regulate inflammation, gliosis, and myelin sparing after spinal cord injury. J Neurochem 102:37-50. CrossRef Medline
22. Kim GM, Xu J, Song SK, Yan P, Ku G, Xu XM, Hsu CY (2001) Tumor necrosis factor receptor deletion reduces nuclear factor-kappaB activation, cellular inhibitor of apoptosis protein 2 expression, and functional recovery after traumatic spinal cord injury. J Neurosci 21:6617-6625. Medline
23. Kwon BK, Okon E, Hillyer J, Mann C, Baptiste D, Weaver LC, Fehlings MG, Tetzlaff W (2011) A systematic review of non-invasive pharmacologic neuroprotective treatments for acute spinal cord injury. J Neurotrauma 28:1545-1588. CrossRef Medline
24. Lee KF, Li E, Huber LJ, Landis SC, Sharpe AH, Chao MV, Jaenisch R (1992) Targeted mutation of the gene encoding the low affinity NGF receptor p75 leads to deficits in the peripheral sensory nervous system. Cell 69: 737-749. CrossRef Medline
25. Lewin GR, Ritter AM, Mendell LM (1993) Nerve growth factor-induced hyperalgesia in the neonatal and adult rat. J Neurosci 13:2136-2148. Medline
26. Li QM, Tep C, Yune TY, Zhou XZ, Uchida T, Lu KP, Yoon SO (2007) Opposite regulation of oligodendrocyte apoptosis by JNK3 and Pin1 after spinal cord injury. J Neurosci 27:8395-8404. CrossRef Medline
27. Liebscher T, Schnell L, Schnell D, Scholl J, Schneider R, Gullo M, Fouad K, Mir A, Rausch M, Kindler D, Hamers FP, Schwab ME (2005) Nogo-A antibody improves regeneration and locomotion of spinal cord-injured rats. Ann Neurol 58:706-719. CrossRef Medline
28. Lipinski CA, Lombardo F, Dominy BW, Feeney PJ (2001) Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv Drug Deliv Rev 46:3-26. CrossRef Medline
29. Liu J, Lillo C, Jonsson PA, Vande Velde CV, Ward CM, Miller TM, Subramaniam JR, Rothstein JD, Marklund S, Andersen PM, Brännström T, Gredal O, Wong PC, Williams DS, Cleveland DW (2004) Toxicity of familial ALS-linked SOD1 mutants from selective recruitment to spinal mitochondria. Neuron 43:5-17. CrossRef Medline
30. Liu K, Lu Y, Lee JK, Samara R, Willenberg R, Sears-Kraxberger I, Tedeschi A, Park KK, Jin D, Cai B, Xu B, Connolly L, Steward O, Zheng B, He Z (2010) PTEN deletion enhances the regenerative ability of adult corticospinal neurons. Nat Neurosci 13:1075-1081. CrossRef Medline
31. Liu X, Kim CN, Yang J, Jemmerson R, Wang X (1996) Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86:147-157. CrossRef Medline
32. Marchenko ND, Zaika A, Moll UM (2000) Death signal-induced localization of p53 protein to mitochondria. A potential role in apoptotic signaling. J Biol Chem 275:16202-16212. CrossRef Medline
33. Massa SM, Xie Y, Yang T, Harrington AW, Kim ML, Yoon SO, Kraemer R, Moore LA, Hempstead BL, Longo FM (2006) Small, nonpeptide p75NTR ligands induce survival signaling and inhibit proNGF-induced death. J Neurosci 26:5288-5300. CrossRef Medline
34. McDonald JW, Althomsons SP, Hyrc KL, Choi DW, Goldberg MP (1998) Oligodendrocytes from forebrain are highly vulnerable to AMPA/kainate receptor-mediated excitotoxicity. Nat Med 4:291-297. CrossRef Medline
35. Nykjaer A, Lee R, Teng KK, Jansen P, Madsen P, Nielsen MS, Jacobsen C, Kliemannel M, Schwarz E, Willnow TE, Hempstead BL, Petersen CM (2004) Sortilin is essential for proNGF-induced apoptosis. Nature 427: 843-848. CrossRef Medline
36. Ohori Y, Yamamoto S, Nagao M, Sugimori M, Yamamoto N, Nakamura K, Nakafuku M (2006) Growth factor treatment and genetic manipulation stimulate neurogenesis and oligodendrogenesis by endogenous neural progenitors in the injured adult spinal cord. J Neurosci 26:11948-11960. CrossRef Medline
37. Ohri SS, Maddie MA, Zhao Y, Qiu MS, Hetman M, Whittemore SR (2011) Attenuating the endoplasmic reticulum stress response improves functional recovery after spinal cord injury. Glia 59:1489-1502. CrossRef Medline
38. Park KK, Liu K, Hu Y, Smith PD, Wang C, Cai B, Xu B, Connolly L, Kramvis I, Sahin M, He Z (2008) Promoting axon regeneration in the adult CNS by modulation of the PTEN/mTOR pathway. Science 322:963-966. CrossRef Medline
39. Pearse DD, Pereira FC, Marcillo AE, Bates ML, Berrocal YA, Filbin MT, Bunge MB (2004) cAMP and Schwann cells promote axonal growth and functional recovery after spinal cord injury. Nat Med 10:610-616. CrossRef Medline
40. Pinzon A, Marcillo A, Quintana A, Stamler S, Bunge MB, Bramlett HM, Dietrich WD (2008) A re-assessment of minocycline as a neuroprotective agent in a rat spinal cord contusion model. Brain Res 1243:146-151. CrossRef Medline
41. Reagan-Shaw S, Nihal M, Ahmad N (2008) Dose translation from animal to human studies revisited. FASEB J 22:659-661. Medline
42. Ro LS, Chen ST, Tang LM, Jacobs JM (1999) Effect ofNGFand anti-NGF on neuropathic pain in rats following chronic constriction injury of the sciatic nerve. Pain 79:265-274. CrossRef Medline
43. Saganová K, Orendácová J, Cizková D, Vanický I (2008) Limited minocycline neuroprotection after balloon-compression spinal cord injury in the rat. Neurosci Lett 433:246-249. CrossRef Medline
44. Smith RR, Burke DA, Baldini AD, Shum-Siu A, Baltzley R, Bunger M, Magnuson DS (2006) The Louisville Swim Scale: a novel assessment of hindlimb function following spinal cord injury in adult rats. J Neurotrauma 23:1654-1670. CrossRef Medline
45. Song XY, Zhong JH, Wang X, Zhou XF (2004) Suppression of p75NTR does not promote regeneration of injured spinal cord in mice. J Neurosci 24: 542-546. CrossRef Medline
46. Sun F, He Z (2010) Neuronal intrinsic barriers for axon regeneration in the adult CNS. Curr Opin Neurobiol 20:510-518. CrossRef Medline
47. Totoiu MO, Keirstead HS (2005) Spinal cord injury is accompanied by chronic progressive demyelination. J Comp Neurol 486:373-383. CrossRef Medline
48. Wang KC, Kim JA, Sivasankaran R, Segal R, He Z (2002) P75 interacts with the Nogo receptor as a co-receptor for Nogo, MAG and OMgp. Nature 420:74-78. CrossRef Medline
49. Wong ST, Henley JR, Kanning KC, Huang KH, Bothwell M, Poo MM (2002) A p75(NTR) and Nogo receptor complex mediates repulsive signaling by myelin-associated glycoprotein. Nat Neurosci 5:1302-1308. CrossRef Medline
50. Yune TY, Lee JY, Jung GY, Kim SJ, Jiang MH, Kim YC, Oh YJ, Markelonis GJ, Oh TH (2007) Minocycline alleviates death of oligodendrocytes by inhibiting pro-nerve growth factor production in microglia after spinal cord injury. J Neurosci 27:7751-7761. CrossRef Medline
51. Zheng B, Atwal J, Ho C, Case L, He XL, Garcia KC, Steward O, Tessier-Lavigne M (2005) Genetic deletion of the Nogo receptor does not reduce neurite inhibition in vitro or promote corticospinal tract regeneration in vivo. Proc Natl Acad Sci U S A 102:1205-1210. CrossRef Medline
52. Zheng GZ, Bhatia P, Kolasa T, Patel M, El Kouhen OF, Chang R, Uchic ME, Miller L, Baker S, Lehto SG, Honore P, Wetter JM, Marsh KC, Moreland RB, Brioni JD, Stewart AO (2006) Correlation between brain/plasma ratios and efficacy in neuropathic pain models of selective metabotropic glutamate receptor 1 antagonists. Bioorg Med Chem Lett 16:4936-4940. CrossRef Medline