Enhanced neurite outgrowth of human model (NT2) neurons by small-molecule inhibitors of Rho/ROCK signaling

PLoS ONE

Volumn 10, Issue 2, 2015, Pages

  Roloff, Frank ^a   Scheiblich, Hannah ^a   Dewitz, Carola ^a   Dempewolf, Silke ^a   Stern, Michael ^a   Bicker, Gerd ^a,b  

^a UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^b CENTER FOR SYSTEMS NEUROSCIENCE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; BETA TUBULIN; CYCLIC AMP; FASUDIL; IBUPROFEN; LYSOPHOSPHATIDIC ACID; PLACEBO; RETINOIC ACID; RHO GUANINE NUCLEOTIDE DISSOCIATION INHIBITOR; RHO KINASE; RHO KINASE INHIBITOR; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; PROTEIN KINASE INHIBITOR;

ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CULTURE MEDIUM; DRUG TARGETING; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME SPECIFICITY; HUMAN; HUMAN CELL; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NERVE REGENERATION; PHARMACOLOGICAL BLOCKING; SIGNAL TRANSDUCTION; CELL LINE; CELL SURVIVAL; DRUG EFFECTS; METABOLISM; NERVE CELL; NEURITE;

ANIMALIA;

CELL LINE; CELL SURVIVAL; ENZYME ACTIVATION; HUMANS; NEURITES; NEURONS; PROTEIN KINASE INHIBITORS; RHO-ASSOCIATED KINASES; SIGNAL TRANSDUCTION;

EID: 84923862294     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0118536     Document Type: Article

References (49)

1. Benowitz LI, Yin Y. Combinatorial treatments for promoting axon regeneration in the CNS: strategies for overcoming inhibitory signals and activating neurons' intrinsic growth state. Dev Neurobiol. 2007; 67:1148-1165. doi: 10.1002/dneu.20515 PMID: 17514713
2. Bradbury EJ, Moon LDF, Popat RJ, King VR, Bennett GS, Patel PN, et al. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature. 2002; 416:636-640. doi: 10.1038/416636a PMID: 11948352
3. Silver J, Miller JH. Regeneration beyond the glial scar. Nat Rev Neurosci. 2004; 5:146-156. doi: 10. 1038/nrn1326 PMID: 14735117
4. Schwab ME. Nogo and axon regeneration. Curr Opin Neurobiol. 2004; 14:118-124. doi: 10.1016/j. conb.2004.01.004 PMID: 15018947
5. Aguayo AJ, David S, Bray GM. Influences of the glial environment on the elongation of axons after injury: transplantation studies in adult rodents. J Exp Biol. 1981; 95:231-240. PMID: 7334319
6. Filbin MT. Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS. Nat Rev Neurosci. 2003; 4:703-713. doi: 10.1038/nrn1195 PMID: 12951563
7. McGee AW, Strittmatter SM. The Nogo-66 receptor: focusing myelin inhibition of axon regeneration. Trends Neurosci. 2003; 26:193-198. doi: 10.1016/S0166-2236(03)00062-6 PMID: 12689770
8. Tönges L, Koch J-C, Bähr M, Lingor P. ROCKing Regeneration: Rho Kinase Inhibition as Molecular Target for Neurorestoration. Front Mol Neurosci. 2011; 4:39. doi: 10.3389/fnmol.2011.00039 PMID: 22065949
9. Gallo G, Letourneau PC. Regulation of growth cone actin filaments by guidance cues. J Neurobiol. 2004; 58:92-102. doi: 10.1002/neu.10282 PMID: 14598373
10. Wu D, Yang P, Zhang X, Luo J, Haque ME, Yeh J, et al. Targeting a dominant negative rho kinase to neurons promotes axonal outgrowth and partial functional recovery after rat rubrospinal tract lesion. Mol Ther. 2009; 17:2020-2030. doi: 10.1038/mt.2009.168 PMID: 19623163
11. Boomkamp SD, Riehle MO, Wood J, Olson MF, Barnett SC. The development of a rat in vitro model of spinal cord injury demonstrating the additive effects of Rho and ROCK inhibitors on neurite outgrowth and myelination. Glia. 2012; 60:441-456. doi: 10.1002/glia.22278 PMID: 22139636
12. DeGeer J, Lamarche-Vane N. Rho GTPases in neurodegeneration diseases. Exp Cell Res. 2013; 319:2384-2394. doi: 10.1016/j.yexcr.2013.06.016 PMID: 23830879
13. Gu H, Yu SP, Gutekunst C-A, Gross RE, Wei L. Inhibition of the Rho signaling pathway improves neurite outgrowth and neuronal differentiation of mouse neural stem cells. Int J Physiol Pathophysiol Pharmacol. 2013; 5:11-20. PMID: 23525456
14. Dergham P, Ellezam B, Essagian C, Avedissian H, Lubell WD, McKerracher L. Rho signaling pathway targeted to promote spinal cord repair. J Neurosci. 2002; 22:6570-6577. doi: 20026637 PMID: 12151536
15. Lingor P, Teusch N, Schwarz K, Mueller R, Mack H, Bähr M, et al. Inhibition of Rho kinase (ROCK) increases neurite outgrowth on chondroitin sulphate proteoglycan in vitro and axonal regeneration in the adult optic nerve in vivo. J Neurochem. 2007; 103:181-189. doi: 10.1111/j.1471-4159.2007.04756.x PMID: 17608642
16. Wang X, Budel S, Baughman K, Gould G, Song K-H, Strittmatter SM. Ibuprofen enhances recovery from spinal cord injury by limiting tissue loss and stimulating axonal growth. J Neurotrauma. 2009; 26:81-95. doi: 10.1089/neu.2007.0464 PMID: 19125588
17. Fournier AE, Takizawa BT, Strittmatter SM. Rho kinase inhibition enhances axonal regeneration in the injured CNS. J Neurosci. 2003; 23:1416-1423. PMID: 12598630
18. Kopp MA, Liebscher T, Niedeggen A, Laufer S, Brommer B, Jungehulsing GJ, et al. Small-molecule-induced Rho-inhibition: NSAIDs after spinal cord injury. Cell Tissue Res. 2012; 349:119-132. doi: 10. 1007/s00441-012-1334-7 PMID: 22350947
19. Andrews PW, Damjanov I, Simon D, Banting GS, Carlin C, Dracopoli NC, et al. Pluripotent embryonal carcinoma clones derived from the human teratocarcinoma cell line Tera-2. Differentiation in vivo and in vitro. Lab Invest. 1984; 50:147-162. PMID: 6694356
20. Paquet-Durand F, Bicker G. Human model neurons in studies of brain cell damage and neural repair. Curr Mol Med. 2007; 7:541-554. PMID: 17896991
21. Tegenge MA, Roloff F, Bicker G. Rapid differentiation of human embryonal carcinoma stem cells (NT2) into neurons for neurite outgrowth analysis. Cell Mol Neurobiol. 2011; 31:635-643. doi: 10.1007/ s10571-011-9659-4 PMID: 21331625
22. Roloff F, Ziege S, BaumgärtnerW, Wewetzer K, Bicker G. Schwann cell-free adult canine olfactory ensheathing cell preparations from olfactory bulb and mucosa display differential migratory and neurite growth-promoting properties in vitro. BMC Neurosci. 2013; 14:141. doi: 10.1186/1471-2202-14-141 PMID: 24219805
23. Degasperi A, Birtwistle MR, Volinsky N, Rauch J, Kolch W, Kholodenko BN. Evaluating strategies to normalise biological replicates of Western blot data. PLoS ONE. 2014; 9:e87293. doi: 10.1371/journal. pone.0087293 PMID: 24475266
24. Hu R, Zhou J, Luo C, Lin J, Wang X, Li X, et al. Glial scar and neuroregeneration: histological, functional, and magnetic resonance imaging analysis in chronic spinal cord injury. J Neurosurg Spine. 2010; 13:169-180. doi: 10.3171/2010.3.SPINE09190 PMID: 20672952
25. Fu Q, Hue J, Li S. Nonsteroidal anti-inflammatory drugs promote axon regeneration via RhoA inhibition. J Neurosci. 2007; 27:4154-4164. doi: 10.1523/JNEUROSCI.4353-06.2007 PMID: 17428993
26. Watzlawick R, Sena ES, Dirnagl U, Brommer B, Kopp MA, Macleod MR, et al. Effect and reporting bias of RhoA/ROCK-blockade intervention on locomotor recovery after spinal cord injury: a systematic review and meta-analysis. JAMA Neurol. 2014; 71:91-99. doi: 10.1001/jamaneurol.2013.4684 PMID: 24297045
27. Ellezam B, Dubreuil C, Winton M, Loy L, Dergham P, Sellés-Navarro I, et al. Inactivation of intracellular Rho to stimulate axon growth and regeneration. Prog Brain Res. 2002; 137:371-380. PMID: 12440379
28. Kubo T, Hata K, Yamaguchi A, Yamashita T. Rho-ROCK inhibitors as emerging strategies to promote nerve regeneration. Curr Pharm Des. 2007; 13:2493-2499. PMID: 17692017
29. Lingor P, Tönges L, Pieper N, Bermel C, Barski E, Planchamp V, et al. ROCK inhibition and CNTF interact on intrinsic signalling pathways and differentially regulate survival and regeneration in retinal ganglion cells. Brain. 2008; 131:250-263. doi: 10.1093/brain/awm284 PMID: 18063589
30. Radtke C, Vogt PM. Peripheral nerve regeneration: a current perspective. Eplasty. 2009; 9:e47. PMID: 19907643
31. Gao X, Wang Y, Chen J, Peng J. The role of peripheral nerve ECM components in the tissue engineering nerve construction. Rev Neurosci. 2013; 24:443-453. doi: 10.1515/revneuro-2013-0022 PMID: 23907421
32. Archibald SJ, Shefner J, Krarup C, Madison RD. Monkey median nerve repaired by nerve graft or collagen nerve guide tube. J Neurosci. 1995; 15:4109-4123. PMID: 7751969
33. McDonald D, Cheng C, Chen Y, Zochodne D. Early events of peripheral nerve regeneration. Neuron Glia Biol. 2006; 2:139-147. doi: 10.1017/S1740925X05000347 PMID: 18634586
34. Cheng C, Webber CA, Wang J, Xu Y, Martinez JA, Liu WQ, et al. Activated RHOA and peripheral axon regeneration. Experimental Neurology. 2008; 212:358-369. doi: 10.1016/j.expneurol.2008.04.023 PMID: 18554585
35. Koliatsos VE, Price WL, Pardo CA, Price DL. Ventral root avulsion: an experimental model of death of adult motor neurons. J Comp Neurol. 1994; 342:35-44. doi: 10.1002/cne.903420105 PMID: 8207127
36. Martin LJ, Kaiser A, Price AC. Motor neuron degeneration after sciatic nerve avulsion in adult rat evolves with oxidative stress and is apoptosis. J Neurobiol. 1999; 40:185-201. PMID: 10413449
37. Natsume A, Mata M, Wolfe D, Oligino T, Goss J, Huang S, et al. Bcl-2 and GDNF delivered by HSV-mediated gene transfer after spinal root avulsion provide a synergistic effect. J Neurotrauma. 2002; 19:61-68. doi: 10.1089/089771502753460240 PMID: 11852979
38. Hoang TX, Nieto JH, Tillakaratne NJK, Havton LA. Autonomic and motor neuron death is progressive and parallel in a lumbosacral ventral root avulsion model of cauda equina injury. J Comp Neurol. 2003; 467:477-486. doi: 10.1002/cne.10928 PMID: 14624482
39. Reyes O, Sosa I, Kuffler DP. Promoting neurological recovery following a traumatic peripheral nerve injury. P R Health Sci J. 2005; 24:215-223. PMID: 16329686
40. Lang P, Gesbert F, Delespine-Carmagnat M, Stancou R, Pouchelet M, Bertoglio J. Protein kinase A phosphorylation of RhoA mediates the morphological and functional effects of cyclic AMP in cytotoxic lymphocytes. EMBO J. 1996; 15:510-519. PMID: 8599934
41. Dong JM, Leung T, Manser E, Lim L. cAMP-induced morphological changes are counteracted by the activated RhoA small GTPase and the Rho kinase ROKalpha. J Biol Chem. 1998; 273:22554-22562. PMID: 9712882
42. Sebök A, Nusser N, Debreceni B, Guo Z, Santos MF, Szeberenyi J, et al. Different roles for RhoA during neurite initiation, elongation, and regeneration in PC12 cells. J Neurochem. 1999; 73:949-960. PMID: 10461884
43. Flynn KC. The cytoskeleton and neurite initiation. Bioarchitecture. 2013;3.
44. Shiraishi M, Tanabe A, Saito N, Sasaki Y. Unphosphorylated MARCKS is involved in neurite initiation induced by insulin-like growth factor-I in SH-SY5Y cells. J Cell Physiol. 2006; 209:1029-1038. doi: 10. 1002/jcp.20814 PMID: 16941482
45. Hirose M, Ishizaki T, Watanabe N, Uehata M, Kranenburg O, Moolenaar WH, et al. Molecular dissection of the Rho-associated protein kinase (p160ROCK)-regulated neurite remodeling in neuroblastoma N1E-115 cells. J Cell Biol. 1998; 141:1625-1636. PMID: 9647654
46. Yamaguchi Y, Katoh H, Yasui H, Mori K, Negishi M. RhoA inhibits the nerve growth factor-induced Rac1 activation through Rho-associated kinase-dependent pathway. J Biol Chem. 2001; 276:18977-18983. doi: 10.1074/jbc.M100254200 PMID: 11279039
47. Bito H, Furuyashiki T, Ishihara H, Shibasaki Y, Ohashi K, Mizuno K, et al. A critical role for a Rho-associated kinase, p160ROCK, in determining axon outgrowth in mammalian CNS neurons. Neuron. 2000; 26:431-441. PMID: 10839361
48. Carafa M, Marianecci C, Di Marzio L, Rinaldi F, Meo C, Matricardi P, et al. A new vesicle-loaded hydrogel system suitable for topical applications: preparation and characterization. J Pharm Pharm Sci. 2011; 14:336-346. PMID: 21903019
49. Hu X, Wang N, Liu L, Liu W. Cyclodextrin-cross-linked diaminotriazine-based hydrogen bonding strengthened hydrogels for drug and reverse gene delivery. J Biomater Sci Polym Ed. 2013; 24:1869-1882. doi: 10.1080/09205063.2013.808150 PMID: 23862694