Vincristine and bortezomib cause axon outgrowth and behavioral defects in larval zebrafish

Journal of the Peripheral Nervous System

Volumn 17, Issue 1, 2012, Pages 76-89

  Khan, Tahsin M ^a   Benaich, Nathan ^a   Malone, Clare F ^a   Bernardos, Rebecca L ^b   Russell, Amy R ^a   Downes, Gerald B ^c   Barresi, Michael J ^b   Hutson, Lara D ^a  

^a WILLIAMS COLLEGE   (United States)

^b SMITH COLLEGE   (United States)

^c UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

Behavior; Chemotherapy; Development; Neuropathy; Proteasome inhibitor

Indexed keywords

BORTEZOMIB; VINCRISTINE;

ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR DISORDER; CELL CYCLE M PHASE; CELL CYCLE PROGRESSION; CONTROLLED STUDY; DRUG SCREENING; EMBRYO DEVELOPMENT; INNERVATION; LARVA; MOTOR NERVE; MUSCLE CONTRACTION; NERVE FIBER; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; SENSORIMOTOR FUNCTION; SENSORY NERVE; SWIMMING; ZEBRA FISH;

ANIMALS; ANTINEOPLASTIC AGENTS; AXONS; BEHAVIOR, ANIMAL; BORONIC ACIDS; IMMUNOHISTOCHEMISTRY; LARVA; PYRAZINES; VINCRISTINE; ZEBRAFISH;

EID: 84859395812     PISSN: 10859489     EISSN: 15298027     Source Type: Journal    
DOI: 10.1111/j.1529-8027.2012.00371.x     Document Type: Article

References (72)

1. Arastu-Kapur S, Anderl JL, Kraus M, Parlati F, Shenk KD, Lee SJ, Muchamuel T, Bennett MK, Driessen C, Ball AJ, Kirk CJ (2011). Nonproteasomal targets of the proteasome inhibitors bortezomib and carfilzomib: a link to clinical adverse events. Clin Cancer Res 17:2734-2743.
2. Argyriou AA, Iconomou G, Kalofonos HP (2008). Bortezomib-induced peripheral neuropathy in multiple myeloma: a comprehensive review of the literature. Blood 112:1593-1599.
3. Berger P, Young P, Suter U (2002). Molecular cell biology of Charcot-Marie-Tooth disease. Neurogenetics 4:1-15. (Pubitemid 36401753)
4. Berman J, Hsu K, Look AT (2003). Zebrafish as amodel organism for blood diseases. Br J Haematol 123:568-576. (Pubitemid 37468051)
5. Boon KL, Xiao S, McWhorter ML, Donn T, Wolf-Saxon E, Bohnsack MT, Moens CB, Beattie CE (2009). Zebrafish survival motor neuron mutants exhibit presynaptic neuromuscular junction defects. Hum Mol Genet 18:3615-3625.
6. Bradley WG, Lassman LP, Pearce GW, Walton JN (1970). The neuromyopathy of vincristine in man. Clinical, electrophysiological and pathological studies. J Neurol Sci 10:107-131.
7. Brustein E, Saint-Amant L, Buss RR, Chong M, McDearmid JR, Drapeau P (2003). Steps during the development of the zebrafish locomotor network. J Physiol Paris 97:77-86. (Pubitemid 38366299)
8. Burgess HA, Granato M (2007). Sensorimotor gating in larval zebrafish. J Neurosci 27:4984-4994. (Pubitemid 46699065)
9. Buss RR, Bourque CW, Drapeau P (2003). Membrane properties related to the firing behavior of zebrafish motoneurons. J Neurophysiol 89:657-664. (Pubitemid 36206114)
10. Cavaletti G, Nobile-Orazio E (2007). Bortezomib-induced peripheral neurotoxicity: still far from a painless gain. Haematologica 92:1308-1310. (Pubitemid 350144147)
11. Chaudhry V, Cornblath DR, Polydefkis M, Ferguson A, Borrello I (2008). Characteristics of bortezomib- and thalidomide-induced peripheral neuropathy. J Peripher Nerv Syst 13:275-282.
12. Chauhan D, Hideshima T, Anderson KC (2008). Targeting proteasomes as therapy in multiple myeloma. Adv Exp Med Biol 615:251-260.
13. Choi TY, Kim JH, Ko DH, Kim CH, Hwang JS, Ahn S, Kim SY, Kim CD, Lee JH, Yoon TJ (2007). Zebrafish as a new model for phenotype-based screening of melanogenic regulatory compounds. Pigment Cell Res 20:120-127. (Pubitemid 46439522)
14. Clarke JD, Hayes BP, Hunt SP, Roberts A (1984). Sensory physiology, anatomy and immunohistochemistry of Rohon-Beard neurones in embryos of Xenopus laevis. J Physiol 348:511-525. (Pubitemid 14061867)
15. Delforge M, Blade J, Dimopoulos MA, Facon T, Kropff M, Ludwig H, Palumbo A, Van Damme P, San-Miguel JF, Sonneveld P (2010). Treatment-related peripheral neuropathy in multiple myeloma: the challenge continues. Lancet Oncol 11:1086-1095.
16. Drapeau P, Saint-Amant L, Buss RR, Chong M, McDearmid JR, Brustein E (2002). Development of the locomotor network in zebrafish. Prog Neurobiol 68:85-111. (Pubitemid 35346806)
17. Dyck PJ, Thomas D (2005). Peripheral Neuropathy, 4th Edn. Saunders, Philadelphia.
18. Feitsma H, Cuppen E (2008). Zebrafish as a cancer model. Mol Cancer Res 6:685-694.
19. Flanagan-Steet H, Fox MA, Meyer D, Sanes JR (2005). Neuromuscular synapses can form in vivo by incorporation of initially aneural postsynaptic specializations. Development 132:4471-4481. (Pubitemid 41632226)
20. Frazer JK, Meeker ND, Rudner L, Bradley DF, Smith AC, Demarest B, Joshi D, Locke EE, Hutchinson SA, Tripp S, Perkins SL, Trede NS (2009). Heritable T-cell malignancy models established in a zebrafish phenotypic screen. Leukemia 23:1825-1835.
21. Gigant B, Wang C, Ravelli RB, Roussi F, Steinmetz MO, Curmi PA, Sobel A, Knossow M (2005). Structural basis for the regulation of tubulin by vinblastine. Nature 435:519-522. (Pubitemid 40734250)
22. Granato M, van Eeden FJ, Schach U, Trowe T, Brand M, Furutani-Seiki M, Haffter P, Hammerschmidt M, Heisenberg CP, Jiang YJ, Kane DA, Kelsh RN, Mullins MC, Odenthal J, Nusslein-Volhard C (1996). Genes controlling and mediating locomotion behavior of the zebrafish embryo and larva. Development 123:399-413. (Pubitemid 27056765)
23. Grider MH, Chen Q, Shine HD (2006). Semi-automated quantification of axonal densities in labeled CNS tissue. J Neurosci Methods 155:172-179. (Pubitemid 44233000)
24. Hallare A, Nagel K, Kohler HR, Triebskorn R (2006). Comparative embryotoxicity and proteotoxicity of three carrier solvents to zebrafish (Danio rerio) embryos. Ecotoxicol Environ Saf 63:378-388.
25. Haskins KM, Donoso JA, Himes RH (1981). Spirals and paracrystals induced by Vinca alkaloids: evidence that microtubule-associated proteins act as polycations. J Cell Sci 47:237-247. (Pubitemid 11134484)
26. Hideshima T, Chauhan D, Richardson P, Mitsiades C, Mitsiades N, Hayashi T, Munshi N, Dang L, Castro A, Palombella V, Adams J, Anderson KC (2002). NF-kappa B as a therapeutic target in multiple myeloma. J Biol Chem 277:16639-16647. (Pubitemid 34967682)
27. Hilkens PH, ven den Bent MJ (1997). Chemotherapy-induced peripheral neuropathy. J Peripher Nerv Syst 2:350-361.
28. Himes RH, Kersey RN, Heller-Bettinger I, Samson FE (1976). Action of the vinca alkaloids vincristine, vinblastine, and desacetyl vinblastine amide on microtubules in vitro. Cancer Res 36:3798-3802.
29. Hsu CH, Wen ZH, Lin CS, Chakraborty C (2007). The zebrafish model: use in studying cellular mechanisms for a spectrum of clinical disease entities. Curr Neurovasc Res 4:111-120. (Pubitemid 46708901)
30. Hutson LD, Chien CB (2002). Wiring the zebrafish: axon guidance and synaptogenesis. Curr Opin Neurobiol 12:87-92. (Pubitemid 34175279)
31. Kabashi E, Brustein E, Champagne N, Drapeau P (2011). Zebrafish models for the functional genomics of neurogenetic disorders. Biochim Biophys Acta 1812:335-345.
32. Kane RC, Dagher R, Farrell A, Ko CW, Sridhara R, Justice R, Pazdur R (2007). Bortezomib for the treatment of mantle cell lymphoma. Clin Cancer Res 13:5291-5294. (Pubitemid 47510352)
33. Kari G, Rodeck U, Dicker AP (2007). Zebrafish: an emerging model system for human disease and drug discovery. Clin Pharmacol Ther 82:70-80. (Pubitemid 46944200)
34. Kaufman CK, White RM, Zon L (2009). Chemical genetic screening in the zebrafish embryo. Nat Protoc 4:1422-1432.
35. Kempin S, Lee BJ III, Thaler HT, Koziner B, Hecht S, Gee T, Arlin Z, Little C, Straus D, Reich L, Phillips E, Al-Mondhiry H, Dowling M, Mayer K, Clarkson B (1982). Combination chemotherapy of advanced chronic lymphocytic leukemia: the M-2 protocol (vincristine, BCNU, cyclophosphamide, melphalan, and prednisone). Blood 60:1110-1121. (Pubitemid 13242292)
36. Khan ML, Stewart AK (2011). Carfilzomib: a novel second-generation proteasome inhibitor. Future Oncol 7:607-612.
37. Khersonsky SM, Jung DW, Kang TW, Walsh DP, Moon HS, Jo H, Jacobson EM, Shetty V, Neubert TA, Chang YT (2003). Facilitated forward chemical genetics using a tagged triazine library and zebrafish embryo screening. J Am Chem Soc 125:11804-11805. (Pubitemid 37175399)
38. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995). Stages of embryonic development of the zebrafish. Dev Dyn 203:253-310.
39. Langenau DM, Zon LI (2005). The zebrafish: a new model of T-cell and thymic development. Nat Rev Immunol 5:307-317. (Pubitemid 40516156)
40. Lefebvre JL, Ono F, Puglielli C, Seidner G, Franzini-Armstrong C, Brehm P, Granato M (2004). Increased neuromuscular activity causes axonal defects and muscular degeneration. Development 131:2605-2618. (Pubitemid 38877894)
41. Legha SS (1986). Vincristine neurotoxicity. Pathophysiology and management. Med Toxicol 1:421-427.
42. Leonard JP, Furman RR, Coleman M (2006). Proteasome inhibition with bortezomib: a new therapeutic strategy for non-Hodgkin's lymphoma. Int J Cancer 119:971-979. (Pubitemid 44121415)
43. Lightcap ES, McCormack TA, Pien CS, Chau V, Adams J, Elliott PJ (2000). Proteasome inhibition measurements: clinical application. Clin Chem 46:673-683. (Pubitemid 30318423)
44. Loeffler-Ragg J, Mueller D, Gamerith G, Auer T, Skvortsov S, Sarg B, Skvortsova I, Schmitz KJ, Martin HJ, Krugmann J, Alakus H, Maser E, Menzel J, Hilbe W, Lindner H, Schmid KW, Zwierzina H (2009). Proteomic identification of aldo-keto reductase AKR1B10 induction after treatment of colorectal cancer cells with the proteasome inhibitor bortezomib. Mol Cancer Ther 8:1995-2006.
45. MacDonald BK, Cockerell OC, Sander JW, Shorvon SD (2000). The incidence and lifetime prevalence of neurological disorders in a prospective community-based study in the UK. Brain 123:665-676. (Pubitemid 30162716)
46. Marques IJ, Weiss FU, Vlecken DH, Nitsche C, Bakkers J, Lagendijk AK, Partecke LI, Heidecke CD, Lerch MM, Bagowski CP (2009). Metastatic behaviour of primary human tumours in a zebrafish xenotransplantation model. BMC Cancer 9:128.
47. McKeown KA, Moreno R, Hall VL, Ribera AB, Downes GB (2012). Disruption of Eaat2b, a glutamate transporter, results in abnormal motor behaviors in developing zebrafish. Dev Biol 362:162-171.
48. McLeod JG, Penny R (1969). Vincristine neuropathy: an electrophysiological and histological study. J Neurol Neurosurg Psychiatry 32:297-304.
49. Mizgirev IV, Revskoy S (2010). A new zebrafish model for experimental leukemia therapy. Cancer Biol Ther 9:895-902.
50. Montagut C, Rovira A, Mellado B, Gascon P, Ross JS, Albanell J (2005). Preclinical and clinical development of the proteasome inhibitor bortezomib in cancer treatment. Drugs Today (Barc) 41:299-315. (Pubitemid 41058501)
51. Murphey RD, Stern HM, Straub CT, Zon LI (2006). A chemical genetic screen for cell cycle inhibitors in zebrafish embryos. Chem Biol Drug Des 68:213-219. (Pubitemid 44760246)
52. Myers PZ (1985). Spinal motoneurons of the larval zebrafish. J Comp Neurol 236:555-561.
53. Myers PZ, Eisen JS, Westerfield M (1986). Development and axonal outgrowth of identified motoneurons in the zebrafish. J Neurosci 6:2278-2289. (Pubitemid 16043672)
54. Oprea GE, Krober S, McWhorter ML, Rossoll W, Muller S, Krawczak M, Bassell GJ, Beattie CE, Wirth B (2008). Plastin 3 is a protective modifier of autosomal recessive spinal muscular atrophy. Science 320:524-527. (Pubitemid 351590664)
55. Paulus JD, Willer GB, Willer JR, Gregg RG, Halloran MC (2009). Muscle contractions guide rohon-beard peripheral sensory axons. J Neurosci 29:13190-13201.
56. Peterson RT, Shaw SY, Peterson TA, Milan DJ, Zhong TP, Schreiber SL, MacRae CA, Fishman MC (2004). Chemical suppression of a genetic mutation in a zebrafish model of aortic coarctation. Nat Biotechnol 22:595-599. (Pubitemid 38585912)
57. Ribera AB, Nusslein-Volhard C (1998). Zebrafish touch-insensitive mutants reveal an essential role for the developmental regulation of sodium current. J Neurosci 18:9181-9191. (Pubitemid 28512450)
58. Richardson PG, Barlogie B, Berenson J, Singhal S, Jagannath S, Irwin D, Rajkumar SV, Srkalovic G, Alsina M, Alexanian R, Siegel D, Orlowski RZ, Kuter D, Limentani SA, Lee S, Hideshima T, Esseltine DL, Kauffman M, Adams J, Schenkein DP, Anderson KC (2003). A phase 2 study of bortezomib in relapsed, refractory myeloma. N Engl J Med 348:2609-2617. (Pubitemid 36741588)
59. Rihel J, Prober DA, Arvanites A, Lam K, Zimmerman S, Jang S, Haggarty SJ, Kokel D, Rubin LL, Peterson RT, Schier AF (2010). Zebrafish behavioral profiling links drugs to biological targets and rest/wake regulation. Science 327:348-351.
60. Rosenthal S, Kaufman S (1974). Vincristine neurotoxicity. Ann Intern Med 80:733-737.
61. Sagasti A, Guido MR, Raible DW, Schier AF (2005). Repulsive interactions shape the morphologies and functional arrangement of zebrafish peripheral sensory arbors. Curr Biol 15:804-814. (Pubitemid 40689398)
62. Saint-Amant L, Drapeau P (1998). Time course of the development of motor behaviors in the zebrafish embryo. J Neurobiol 37:622-632. (Pubitemid 28549222)
63. San Miguel J, Blade J, Boccadoro M, Cavenagh J, Glasmacher A, Jagannath S, Lonial S, Orlowski RZ, Sonneveld P, Ludwig H (2006). A practical update on the use of bortezomib in the management of multiple myeloma. Oncologist 11:51-61. (Pubitemid 43152686)
64. Silva A, Wang Q, Wang M, Ravula SK, Glass JD (2006). Evidence for direct axonal toxicity in vincristine neuropathy. J Peripher Nerv Syst 11:211-216. (Pubitemid 44286071)
65. Smith AC, Raimondi AR, Salthouse CD, Ignatius MS, Blackburn JS, Mizgirev IV, Storer NY, de Jong JL, Chen AT, Zhou Y, Revskoy S, Zon LI, Langenau DM (2010). High-throughput cell transplantation establishes that tumor-initiating cells are abundant in zebrafish T-cell acute lymphoblastic leukemia. Blood 115:3296-3303.
66. Stoletov K, Klemke R (2008). Catch of the day: zebrafish as a human cancer model. Oncogene 27:4509-4520.
67. Taylor MR, Hurley JB, Van Epps HA, Brockerhoff SE (2004). A zebrafish model for pyruvate dehydrogenase deficiency: rescue of neurological dysfunction and embryonic lethality using a ketogenic diet. Proc Natl Acad Sci U S A 101:4584-4589. (Pubitemid 38437454)
68. Ton C, Parng C (2005). The use of zebrafish for assessing ototoxic and otoprotective agents. Hear Res 208:79-88. (Pubitemid 41427131)
69. Topp KS, Tanner KD, Levine JD (2000). Damage to the cytoskeleton of large diameter sensory neurons and myelinated axons in vincristine-induced painful peripheral neuropathy in the rat. J Comp Neurol 424:563-576. (Pubitemid 30643051)
70. Ubbels GA, Hara K, Koster CH, Kirschner MW (1983). Evidence for a functional role of the cytoskeleton in determination of the dorsoventral axis in Xenopus laeviseggs. J Embryol Exp Morphol 77:15-37. (Pubitemid 14128737)
71. Windebank AJ, Grisold W (2008). Chemotherapy-induced neuropathy. J Peripher Nerv Syst 13:27-46. (Pubitemid 351393018)
72. Yee NS, Pack M (2005). Zebrafish as a model for pancreatic cancer research. Methods Mol Med 103:273-298.