Amelioration of cisplatin-induced experimental peripheral neuropathy by a small molecule targeting p75NTR

NeuroToxicology

Volumn 45, Issue , 2014, Pages 81-90

  Friesland, Amy ^a   Weng, Zhiying ^a,b   Duenas, Maria ^a   Massa, Stephen M ^c   Longo, Frank M ^d   Lu, Qun ^a  

^a EAST CAROLINA UNIVERSITY   (United States)

^b KUNMING MEDICAL UNIVERSITY   (China)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d STANFORD UNIVERSITY   (United States)

Author keywords

Chemotherapeutics; Kinases and phosphatases; P75NTR; Peripheral neuropathy; Rho GTPases

Indexed keywords

CALPEPTIN; CISPLATIN; LM 11A 31; NERVE GROWTH FACTOR RECEPTOR; NEUROPROTECTIVE AGENT; NEUROTROPHIN RECEPTOR P75; PROTEIN TYROSINE PHOSPHATASE SHP 2; RHO FACTOR; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; TYROSINE; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; ISOLEUCINE; LIGAND; LM11A-31; MORPHOLINE DERIVATIVE; TNFRSF16 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CHEMOTHERAPY; CONTROLLED STUDY; DRUG BIOAVAILABILITY; DRUG DOSE COMPARISON; DRUG MEGADOSE; DRUG TARGETING; ENZYME ACTIVATION; FEMALE; LOW DRUG DOSE; MALE; MORPHOMETRICS; MOUSE; MOUSE MODEL; NERVE CELL CULTURE; NERVE FUNCTION; NEUROPATHOLOGY; NEUROPROTECTION; NONHUMAN; PERIPHERAL NEUROPATHY; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SURAL NERVE; TREATMENT DURATION; VON FREY TEST; ANALOGS AND DERIVATIVES; ANIMAL; C57BL MOUSE; CELL CULTURE; CHEMICALLY INDUCED; DRUG EFFECTS; METABOLISM; NERVE CELL; PATHOLOGY; PHOSPHORYLATION; TOUCH;

ANIMALS; ANTINEOPLASTIC AGENTS; CELLS, CULTURED; CISPLATIN; FEMALE; ISOLEUCINE; LIGANDS; MALE; MICE; MICE, INBRED C57BL; MORPHOLINES; NEURONS; NEUROPROTECTIVE AGENTS; PERIPHERAL NERVOUS SYSTEM DISEASES; PHOSPHORYLATION; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 11; RECEPTORS, NERVE GROWTH FACTOR; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; SURAL NERVE; TOUCH PERCEPTION;

EID: 84908340185     PISSN: 0161813X     EISSN: 18729711     Source Type: Journal    
DOI: 10.1016/j.neuro.2014.09.005     Document Type: Article

References (50)

1. Ahnert-Hilger G., Höltje M., Grosse G., Pickert G., Mucke C., Nixdorf-Bergweiler B., et al. Differential effects of Rho GTPases on axonal and dendritic development in hippocampal neurones. J Neurochem 2004, 90:9-18.
2. 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.
3. Brabeck C., Beschorner R., Conrad S., Mittelbronn M., Bekure K., Meyermann R., et al. Lesional expression of RhoA and RhoB following traumatic brain injury in humans. J Neurotrauma 2004, 21:697-706.
4. Cascinu S., Cordella L., Del Ferro E., Fronzoni M., Catalano G. Neuroprotective effect of reduced glutathione on cisplatin-based chemotherapy in advanced gastric cancer: a randomized double-blind placebo-controlled trial. J Clin Oncol 1995, 13:26-32.
5. Cheng C., Webber C.A., Wang J., Xu Y., Martinez J.A., Liu W.Q., et al. Activated RHOA and peripheral axon regeneration. Exp Nephrol 2008, 212:358-369.
6. Chomiak T., Hu B. What is the optimal value of the g-ratio for myelinated fibers in the rat CNS? A theoretical approach. PLoS ONE 2009, 4:e7754.
7. Cosgaya J.M., Chan J.R., Shooter E.M. The neurotrophin receptor p75NTR as a positive modulator of myelination. Science 2002, 298:1245-1248.
8. Dergham P., Ellezam B., Essagian C., Avedissian H., Lubell W.D., McKerracher L. Rho signaling pathway targeted to promote spinal cord repair. J Neurosci 2002, 22:6570-6577.
9. Dong J.M., 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.
10. Dotti C.G., Sullivan C.A., Banker G.A. The establishment of polarity by hippocampal neurons in culture. J Neurosci 1988, 8:1454-1468.
11. Dubreuil C.I., Marklund N., Deschamps K., McIntosh T.K., McKerracher L. Activation of Rho after traumatic brain injury and seizure in rats. Exp Nephrol 2006, 198:361-369.
12. Dubreuil C.I., Winton M.J., McKerracher L. Rho activation patterns after spinal cord injury and the role of activated Rho in apoptosis in the central nervous system. J Cell Biol 2003, 162:233-243.
13. Ellerbroek S.M., Wennerberg K., Burridge K. Serine phosphorylation negatively regulates RhoA in vivo. J Biol Chem 2003, 278:19023-19031.
14. Feng Y., Schlösser F.J., Sumpio B.E. The Semmes Weinstein monofilament examination as a screening tool for diabetic peripheral neuropathy. J Vasc Surg 2009, 50:675-682.
15. Gregg R.W., Molepo J.M., Monpetit V.J., Mikael N.Z., Redmond D., Gadia M., et al. Cisplatin neurotoxicity: the relationship between dosage, time, and platinum concentration in neurologic tissues, and morphologic evidence of toxicity. J Clin Oncol 1992, 10:795-803.
16. Grisold W., Cavaletti G., Windebank A.J. Peripheral neuropathies from chemotherapeutics and targeted agents: diagnosis, treatment, and prevention. Neuro Oncol 2012, 14(Suppl. 4):iv45-iv54.
17. Gutiérrez-Gutiérrez G., Sereno M., Miralles A., Casado-Sáenz E., Gutiérrez-Rivas E. Chemotherapy-induced peripheral neuropathy: clinical features, diagnosis, prevention and treatment strategies. Clin Transl Oncol 2010, 12:81-91.
18. Huang H., Zhu L., Reid B.R., Drobny G.P., Hopkins P.B. Solution structure of a cisplatin-induced DNA interstrand cross-link. Science 1995, 270:1842-1845.
19. Jaggi A.S., Singh N. Mechanisms in cancer-chemotherapeutic drugs-induced peripheral neuropathy. Toxicology 2012, 291:1-9.
20. James S.E., Burden H., Burgess R., Xie Y., Yang T., Massa S.M., et al. Anti-cancer drug induced neurotoxicity and identification of Rho pathway signaling modulators as potential neuroprotectants. Neurotoxicology 2008, 29:605-612.
21. James S.E., Dunham M., Carrion-Jones M., Murashov A., Lu Q. Rho kinase inhibitor Y-27632 facilitates recovery from experimental peripheral neuropathy induced by anti-cancer drug cisplatin. Neurotoxicology 2010, 31:188-194.
22. Jones S.B., Lu H.Y., Lu Q. Abl tyrosine kinase promotes dendrogenesis by inducing actin cytoskeletal rearrangements in cooperation with Rho family small GTPases in hippocampal neurons. J Neurosci 2004, 24:8510-8521.
23. Kaley T.J., Deangelis L.M. Therapy of chemotherapy-induced peripheral neuropathy. Br J Haematol 2009, 145:3-14.
24. Koeppen S., Verstappen C.C.P., Körte R. Lack of neuroprotection by an ACTH (4-9) analogue. A randomized trial in patients treated with vincristine for Hodgkin's or non-Hodgkin's lymphoma. J Cancer Res Clin Oncol 2004, 130:153-160.
25. Kontaridis M.I., Eminaga S., Fornaro M., Zito C.I., Sordella R., Settleman J., et al. SHP-2 positively regulates myogenesis by coupling to the Rho GTPase signaling pathway. Mol Cell Biol 2004, 24:5340-5352.
26. Kranenburg O., Poland M., Gebbink M., Oomen L., Moolenaar W.H. Dissociation of LPA-induced cytoskeletal contraction from stress fiber formation by differential localization of RhoA. J Cell Sci 1997, 110(Pt. 19):2417-2427.
27. Longo F.M., Massa S.M. Small molecule modulation of p75 neurotrophin receptor functions. CNS Neurol Disord Drug Targets 2008, 7:63-70.
28. Massa S.M., Xie Y., Yang T., Harrington A.W., Kim M.L., Yoon S.O., et al. Small, nonpeptide p75NTR ligands induce survival signaling and inhibit proNGF-induced death. J Neurosci 2006, 26:5288-5300.
29. McDonald E.S., Randon K.R., Knight A., Windebank A.J. Cisplatin preferentially binds to DNA in dorsal root ganglion neurons in vitro and in vivo: a potential mechanism for neurotoxicity. Neurobiol Dis 2005, 18:305-313.
30. Nakayama A.Y., Harms M.B., Luo L. Small GTPases Rac and Rho in the maintenance of dendritic spines and branches in hippocampal pyramidal neurons. J Neurosci 2000, 20:5329-5338.
31. Pace A., Carpano S., Galie E. Vitamin E in the neuroprotection of cisplatin induced peripheral neurotoxicity and ototoxicity. J Clin Oncol 2007, 25:18. (meeting abstracts).
32. Pace A., Giannarelli D., Galiè E., Savarese A., Carpano S., Della Giulia M., et al. Vitamin E neuroprotection for cisplatin neuropathy: a randomized, placebo-controlled trial. Neurology 2010, 74:762-766.
33. Pace A., Savarese A., Picardo M., Maresca V., Pacetti U., Del Monte G., et al. Neuroprotective effect of vitamin E supplementation in patients treated with cisplatin chemotherapy. J Clin Oncol 2003, 21:927-931.
34. Park S.B., Krishnan A.V., Lin C.S., Goldstein D., Friedlander M., Kiernan M.C. Mechanisms underlying chemotherapy-induced neurotoxicity and the potential for neuroprotective strategies. Curr Med Chem 2008, 15:3081-3094.
35. Rushton W.A. A theory of the effects of fibre size in medullated nerve. J Physiol (Lond) 1951, 115:101-122.
36. Routhier A., Astuccio M., Lahey D., Monfredo N., Johnson A., Callahan W., et al. Pharmacological inhibition of Rho-kinase signaling with Y-27632 blocks melanoma tumor growth. Oncol Rep 2010, 23:861-867.
37. Sawada N., Itoh H., Yamashita J., Doi K., Inoue M., Masatsugu K., et al. cGMP-dependent protein kinase phosphorylates and inactivates RhoA. Biochem Biophys Res Commun 2001, 280:798-805.
38. Smyth J.F., Bowman A., Perren T. Glutathione reduces the toxicity and improves quality of life of women diagnosed with ovarian cancer treated with cisplatin: results of a double-blind, randomised trial. Ann Oncol 1997, 8:569-573.
39. Song X.Y., Zhou F.H., Zhong J.H., Wu L.L., Zhou X.F. Knockout of p75(NTR) impairs re-myelination of injured sciatic nerve in mice. J Neurochem 2006, 96:833-842.
40. Sordella R., Jiang W., Chen G.C., Curto M., Settleman J. Modulation of Rho GTPase signaling regulates a switch between adipogenesis and myogenesis. Cell 2003, 113:147-158.
41. Strumberg D., Brügge S., Korn M.W., Koeppen S., Ranft J., Scheiber G., et al. Evaluation of long-term toxicity in patients after cisplatin-based chemotherapy for non-seminomatous testicular cancer. Ann Oncol 2002, 13:229-236.
42. Ta L.E., Low P.A., Windebank A.J. Mice with cisplatin and oxaliplatin-induced painful neuropathy develop distinct early responses to thermal stimuli. Mol Pain 2009, 5:5-9.
43. Tatsumi S., Mabuchi T., Katano T., Matsumura S., Abe T., Hidaka H., et al. Involvement of Rho-kinase in inflammatory and neuropathic pain through phosphorylation of myristoylated alanine-rich C-kinase substrate (MARCKS). Neuroscience 2005, 131:491-498.
44. Threadgill R., Bobb K., Ghosh A. Regulation of dendritic growth and remodeling by Rho, Rac, and Cdc42. Neuron 1997, 19:625-634.
45. Verdú E., Vilches J.J., Rodríguez F.J., Ceballos D., Valero A., Navarro X. Physiological and immunohistochemical characterization of cisplatin-induced neuropathy in mice. Muscle Nerve 1999, 22:329-340.
46. Walters C.E., Pryce G., Hankey D.J., Sebti S.M., Hamilton A.D., Baker D., et al. Inhibition of Rho GTPases with protein prenyltransferase inhibitors prevents leukocyte recruitment to the central nervous system and attenuates clinical signs of disease in an animal model of multiple sclerosis. J Immunol 2002, 168:4087-4094.
47. Yamashita T., Tohyama M. The p75 receptor acts as a displacement factor that releases Rho from Rho-GDI. Nat Neurosci 2003, 6:461-467.
48. Zhou Y., Su Y., Li B., Liu F., Ryder J.W., Wu X., et al. Nonsteroidal anti-inflammatory drugs can lower amyloidogenic Abeta42 by inhibiting Rho. Science 2003, 302:1215-1217.
49. van der Hoop R.G., Vecht C.J., van der Burg M.E., Elderson A., Boogerd W., Heimans J.J., et al. Prevention of cisplatin neurotoxicity with an ACTH(4-9) analogue in patients with ovarian cancer. N Engl J Med 1990, 322:89-94.
50. van der Hoop R.G., van der Burg M.E., ten Bokkel Huinink W.W., van Houwelingen C., Neijt J.P. Incidence of neuropathy in 395 patients with ovarian cancer treated with or without cisplatin. Cancer 1990, 66:1697-1702.