Terminal arbor degeneration - a novel lesion produced by the antineoplastic agent paclitaxel

European Journal of Neuroscience

Volumn 33, Issue 9, 2011, Pages 1667-1676

  Bennett, Gary J ^a,b   Liu, Guo K ^a   Xiao, Wen H ^a,b   Jin, Hai W ^a   Siau, Chiang ^a  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

Chemotherapy neuropathy; Intraepidermal nerve fiber; Neuropathic pain; Rat; Sensory neuropathy; Taxol

Indexed keywords

PACLITAXEL;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; CONCENTRATION RESPONSE; CONTROLLED STUDY; EPIDERMIS; INNERVATION; MALE; NERVE FIBER; NONHUMAN; PERIPHERAL NEUROPATHY; PRIORITY JOURNAL; RAT; SKIN NERVE; TERMINAL ARBOR DEGENERATION;

ANIMALS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; BEHAVIOR, ANIMAL; EPIDERMIS; MALE; NERVE DEGENERATION; NERVE FIBERS; NEURALGIA; PACLITAXEL; PAIN MEASUREMENT; PERIPHERAL NERVES; RATS; RATS, SPRAGUE-DAWLEY;

EID: 79955532091     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2011.07652.x     Document Type: Article

References (79)

1. Aley, K.O., Reichling, D.B. & Levine, J.D. (1996) Vincristine hyperalgesia in the rat: a model of painful vincristine neuropathy in humans. Neuroscience, 73, 259-265.
2. Authier, N., Gillet, J.P., Fialip, J., Eschalier, A. & Coudore, F. (2000) Description of a short-term Taxol-induced nociceptive neuropathy in rats. Brain Res., 887, 239-249.
3. Beiswenger, K.K., Calcutt, N.A. & Mizisin, A.P. (2008) Dissociation of thermal hypoalgesia and epidermal denervation in streptozotocin-diabetic mice. Neurosci. Lett., 442, 267-272.
4. Bergstresser, P.R. & Taylor, J.R. (1977) Epidermal 'turnover-time'- a new examination. Br. J. Dermatol., 96, 503-509.
5. Breathnach, A.S. (1977) Electron microscopy of cutaneous nerves and receptors. J. Invest. Dermatol., 69, 8-26.
6. Burkel, W.E. (1967) The histological fine structure of perineurium. Anat. Rec., 158, 177-190.
7. Calzada, B., Naves, F.J., Del Valle, M.E. & Vega, J.A. (1994) Distribution of protein gene product 9.5 (PGP 9.5) immunoreactivity in the dorsal root ganglia of adult rat. Ann. Anat., 176, 437-441.
8. Cata, J.P., Weng, H.R., Lee, B.N., Reubgen, J.M. & Dougherty, P.M. (2006) Clinical and experimental findings in humans and animals with chemotherapy-induced peripheral neuropathy. Minerva Anestesiol., 72, 151-169.
9. Cauna, N. (1968) Light and electron microscopical structure of sensory end-organs in human skin. In Kenshalo, D.R. (Ed.), The Skin Senses. CC Thomas, Springfield IL, pp. 15-37.
10. Cavaletti, G., Tredici, G., Braga, M. & Tazzari, S. (1995) Experimental peripheral neuropathy induced in adult rats by repeated intraperitoneal administration of taxol. Exp. Neurol., 133, 64-72.
11. Cavaletti, G., Cavalletti, E., Oggioni, N., Sottani, C., Minoia, C., D'Incalci, M., Zucchetti, M., Marmiroli, P. & Tredici, G. (2000) Distribution of paclitaxel within the nervous system of the rat after repeated intravenous administration. Neurotoxicology, 21, 389-393.
12. Chen, H. & Chan, D.C. (2006) Critical dependence of neurons on mitochondrial dynamics. Curr. Opin. Cell Biol., 18, 453-459.
13. Cliffer, K.D., Siuciak, J.A., Carson, S.R., Radley, H.E., Park, J.S., Lewis, D.R., Zlotchenko, E., Nguyen, T., Garcia, K., Tonra, J.R., Stambler, N., Cedarbaum, J.M., Bodine, S.C., Lindsay, R.M. & DiStefano, P.S. (1998) Physiological characterization of Taxol-induced large-fiber sensory neuropathy in the rat. Ann. Neurol., 43, 46-55.
14. Coërs, C. (1982) Motor and sensory endings in skeletal muscle - histology. In Haymaker, W. & Adams, R.D. (Eds), Histology and Histopathology of the Nervous System. CC Thomas, Springfield IL, pp. 1616-1622.
15. Devigili, G., Tugnoli, V., Penza, P., Camozzi, F., Lombardi, R., Melli, G., Broglio, L., Granieri, E. & Lauria, G. (2008) The diagnostic criteria for small fibre neuropathy - from symptoms to neuropathology. Brain, 131, 1912-1925.
16. Devor, M., Govrin-Lippmann, R., Frank, I. & Raber, P. (1985) Proliferation of primary sensory neurons in adult rat dorsal root ganglion and the kinetics of retrograde cell loss after sciatic nerve section. Somatosens Res, 3, 139-167.
17. Djouhri, L. & Lawson, S.N. (2004) A-beta-fiber nociceptive primary afferent neurons - a review of incidence and properties in relation to other afferent A-fiber neurons in mammals. Brain Res. Rev., 46, 131-145.
18. Dougherty, P.M., Cata, J.P., Cordella, J.V., Burton, A. & Weng, H.R. (2004) Taxol-induced sensory disturbance is characterized by preferential impairment of myelinated fiber function in cancer patients. Pain, 109, 132-142.
19. Ebenezer, G.J., McArthur, J.C., Thomas, D., Murinson, B., Hauer, P., Polydefkis, M. & Griffin, J.W. (2007) Denervation of skin in neuropathies - the sequence of axonal and Schwann cell changes in skin biopsies. Brain, 130, 2703-2714.
20. Flatters, S.J.L. & Bennett, G.J. (2004) Ethosuximide reverses paclitaxel- and vincristine-induced painful peripheral neuropathy. Pain, 109, 50-61.
21. Flatters, S.J.L. & Bennett, G.J. (2006) Studies of peripheral sensory nerves in paclitaxel-induced painful peripheral neuropathy - evidence for mitochondrial dysfunction. Pain, 122, 247-257.
22. Flatters, S.J.L., Xiao, W.H. & Bennett, G.J. (2006) Acetyl-L-carnitine prevents and reduces paclitaxel-induced painful neuropathy. Neurosci. Lett., 397, 219-223.
23. Forsyth, P.A., Balmaceda, C., Peterson, K., Seidman, A.D., Brasher, P. & DeAngelis, L.M. (1997) Prospective study of paclitaxel-induced peripheral neuropathy with quantitative sensory testing. J. Neurooncol., 35, 47-53.
24. S and other mutant mice. J. Neurocytol., 32, 863-881.
25. Hermann, N.R., McDerott, M.P., Henderson, D., Chen, L., Akowuah, K., Schifitto, G. & North East AIDS Dementia (NEAD) Consortium. (2004) Epidermal nerve fiber density, axonal swellings and QST as predictors of HIV distal sensory neuropathy. Muscle Nerve, 29, 420-427.
26. Herrmann, D.N., Griffin, J.W., Hauer, P., Cornblath, D.R. & McArthur, J.C. (1999) Epidermal nerve fiber density and sural nerve morphometry in peripheral neuropathies. Neurology, 53, 1634-1640.
27. Holland, N.R., Crawford, T.O., Hauer, P., Cornblath, D.R., Griffin, J.W. & McArthur, J.C. (1998) Small fiber sensory neuropathies - clinical course and neuropathology of idiopathic cases. Ann. Neurol., 44, 47-59.
28. Hsieh, S.T., Chiang, H.Y. & Lin, W.M. (2000) Pathology of nerve terminal degeneration in the skin. J. Neuropathol. Exp. Neurol., 59, 297-307.
29. Ikegami, K. & Koike, T. (2003) Non-apoptotic neurite degeneration in apoptotic neuronal death - pivotal role of mitochondrial function in neurites. Neuroscience, 122, 617-626.
30. Jamieson, S.M., Liu, J.J., Connor, B., Dragunow, M. & McKeage, M.J. (2007) Nucleolar enlargement, nuclear eccentricity and altered cell body immunostaining characteristics of large-sized sensory neurons following treatment of rats with paclitaxel. Neurotoxicology, 28, 1092-1098.
31. Jimenez-Andrade, J.M., Peters, C.M., Mejia, N.A., Ghilardi, J.R., Kuskowski, M.A. & Mantyh, P.W. (2006) Sensory neurons and their supporting cells located in the trigeminal, thoracic and lumbar ganglia differentially express markers of injury following intravenous administration of paclitaxel in the rat. Neurosci. Lett., 405, 62-67.
32. Jin, H.W., Flatters, S.J.L., Xiao, W.H., Mulhern, H.L. & Bennett, G.J. (2008) Prevention of paclitaxel-evoked painful peripheral neuropathy by acetyl-L-carnitine - effects on axonal mitochondria, sensory nerve fiber terminal arbors, and cutaneous Langerhans cells. Exptl. Neurol., 210, 229-237.
33. Kennedy, W.R. & Wendelschafer-Crabb, G. (1993) The innervation of human epidermis. J. Neurol. Sci., 115, 184-190.
34. Ko, M.H., Chen, W.P. & Hsieh, S.T. (2000) Cutaneous nerve degeneration induced by acrylamide in mice. Neurosci. Lett., 293, 195-198.
35. Kruger, L., Perl, E.R. & Sedivec, M.J. (1981) Fine structure of myelinated mechanical nociceptor endings in cat hairy skin. J. Comp. Neurol., 198, 137-154.
36. Lauria, G., Morbin, M., Lombardi, R., Borgna, M., Mazzoleni, G., Sghirlanzoni, A. & Pareyson, D. (2003) Axonal swellings predict the degeneration of epidermal nerve fibers in painful neuropathies. Neurology, 61, 631-636.
37. Lauria, G., Borgna, M., Morbin, M., Lombardi, R., Mazzoleni, G., Sghirlanzoni, A. & Pareyson, D. (2004) Tubule and neurofilament immunoreactivity in human hairy skin - markers for intraepidermal nerve fibers. Muscle Nerve, 30, 310-316.
38. Lauria, G., Cornblath, D.R., Johansson, O., McArthur, J.C., Mellgren, S.I., Nolano, M., Rosenberg, N., Sommer, C. & European Federation of Neurological Societies. (2005) EFNS guidelines on the use of skin biopsy in the diagnosis of peripheral neuropathy. Eur. J. Neurol., 12, 747-758.
39. Lipton, R.B., Apfel, S.C., Dutcher, J.P., Rosenberg, R., Kaplan, J., Berger, A., Einzig, A.I., Wiernik, P. & Schaumburg, H.H. (1989) Taxol produces a predominantly sensory neuropathy. Neurology, 39, 368-373.
40. LoPachin, R.M. (2005) Acrylamide neurotoxicity - neurological, morphological and molecular endpoints in animal models. Adv. Exp. Med. Biol., 561, 21-37.
41. Løseth, S., Stålberg, E., Jorde, R. & Mellgren, S.I. (2008) Early diabetic neuropathy - thermal thresholds and intraepidermal nerve fibre density in patients with normal nerve conduction studies. J. Neurol., 255, 1197-1202.
42. Melli, G., Keswani, S.C., Fischer, A., Chen, W. & Höke, A. (2006) Spatially distinct and functionally independent mechanisms of axonal degeneration in a model of HIV-associated sensory neuropathy. Brain, 129, 1330-1338.
43. Mironov, S.L. (2007) ADP regulates movements of mitochondria in neurons. Biophys. J., 92, 2944-2952.
44. Montagna, W. (1962) The Structure and Function of Skin. Academic Press, New York.
45. Navarro, N., Verdu, E., Wendelschafer-Crabb, G. & Kennedy, W.R. (1995) Innervation of the cutaneous structures in the mouse hind paw - a confocal microscopy immunohistochemical study. J. Neurosci. Res., 41, 111-120.
46. Neundörfer, B. & Thomas, P.K. (2003) Diabetic sensorimotor neuropathy - clinical features. In Gries, F.A., Cameron, N.E., Low, P.A. & Ziegler, D. (Eds), Textbook of Diabetic Neuropathy. Thieme, Stuttgart, pp. 199-204.
47. Orfanos, C.E. & Mahrle, G. (1973) Ultrastructure and cytochemistry of human cutaneous nerves. J. Invest. Dermatol., 61, 108-120.
48. Periquet, M.I., Novak, V., Collins, M.P., Nagaraja, H.N., Erdem, S., Nash, S.M., Freimer, M.L., Sahenk, Z., Kissel, J.T. & Mendell, J.R. (1999) Painful sensory neuropathy - prospective evaluation using skin biopsy. Neurology, 53, 1641-1647.
49. Persohn, E., Canta, A., Schoepfer, S., Traebert, M., Mueller, L., Gilardini, A., Galbiati, S., Nicolini, G., Scuteri, A., Lanzani, F., Giussani, G. & Cavaletti, G. (2005) Morphological and morphometric analysis of paclitaxel and docetaxel-induced peripheral neuropathy in rats. Eur. J. Cancer, 41, 1460-1466.
50. Peters, C.M., Jimenez-Andrade, J.M., Kuskowski, M.A., Ghilardi, J.R. & Mantyh, P.W. (2007a) An evolving cellular pathology occurs in dorsal root ganglia, peripheral nerve and spinal cord following intravenous administration of paclitaxel in the rat. Brain Res., 1168, 46-59.
51. Peters, C.M., Jimenez-Andrade, J.M., Jonas, B.M., Sevcik, M.A., Koewler, N.J., Ghilardi, J.R. & Mantyh, P.W. (2007b) Intravenous paclitaxel administration in the rat induces a peripheral sensory neuropathy characterized by macrophage infiltration and injury to sensory neurons and their supporting cells. Exp. Neurol., 203, 42-54.
52. Polomano, R.C., Mannes, A.J., Clark, U.S. & Bennett, G.J. (2001) A painful peripheral neuropathy in the rat produced by the chemotherapeutic drug, paclitaxel. Pain, 94, 293-304.
53. Quasthoff, S. & Hartung, H.P. (2002) Chemotherapy-induced peripheral neuropathy. J. Neurol., 249, 9-17.
54. Raff, M.C., Whitmore, A.V. & Finn, J.T. (2002) Axonal self-destruction and neurodegeneration. Science, 96, 868-871.
55. Ribeiro-da-Silva, A., Kenigsberg, R.L. & Cuello, A.C. (1991) Light and electron microscopic distribution of nerve growth factor receptor-like immunoreactivity in the skin of the rat lower lip. Neuroscience, 43, 631-646.
56. Sahenk, Z., Barohn, R., New, P. & Mendell, J.R. (1994) Taxol neuropathy. Electrodiagnostic and sural nerve biopsy findings. Arch. Neurol., 51, 726-729.
57. Siau, C. & Bennett, G.J. (2006) Dysregulation of neuronal calcium homeostasis in chemotherapy-evoked painful peripheral neuropathy. Anesth. Analg., 102, 1485-1490.
58. Siau, C., Xiao, W.H. & Bennett, G.J. (2006) Paclitaxel- and vincristine-evoked painful peripheral neuropathies - loss of epidermal innervation and activation of Langerhans cells. Exptl. Neurol., 201, 507-514.
59. Silva, A., Wang, Q., Wang, M., Ravula, S.K. & Glass, J.D. (2006) Evidence for direct axonal toxicity in vincristine neuropathy. J. Peripher. Nerv. Syst., 11, 211-216.
60. Sorrell, J.M. & Caplan, A.I. (2004) Fibroblast heterogeneity - more than skin deep. J. Cell Sci., 117, 667-675.
61. Starkey, M.L., Davies, M., Yip, P.K., Carter, L.M., Wong, D.J., McMahon, S.B. & Bradbury, E.J. (2009) Expression of the regeneration-associated protein SPRR1A in primary sensory neurons and spinal cord of the adult mouse following peripheral and central injury. J. Comp. Neurol., 513, 51-68.
62. Tanner, K.D., Levine, J.D. & Topp, K.S. (1998) Microtubule disorientation and axonal swelling in unmyelinated sensory axons during vincristine-induced painful neuropathy in rat. J. Comp. Neurol., 395, 481-492.
63. Topp, K.S., Tanner, K.D. & Levine, J.D. (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.
64. Tsujino, H., Kondo, E., Fukuoka, T., Dai, Y., Tokunaga, A., Miki, K., Yonenobu, K., Ochi, T. & Noguchi, K. (2000) Activating transcription factor 3 (ATF3) induction by axotomy in sensory and motoneurons - a novel neuronal marker of nerve injury. Mol. Cell. Neurosci., 15, 170-182.
65. Verstappen, C.C., Heimans, J.J., Hoekman, K. & Postma, T.J. (2003) Neurotoxic complications of chemotherapy in patients with cancer - clinical signs and optimal management. Drugs, 63, 1549-1563.
66. Verzé, L., Viglietti-Panzica, C., Maurizo, S., Sica, M. & Panzica, G. (2003a) Distribution of GAP-43 nerve fibers in the skin of the adult human hand. Anat. Rec. (A), 272, 467-473.
67. Verzé, L., Viglietti-Panzica, C., Panzica, G.C. & Ramieri, G. (2003b) Expression of neuropeptides and Growth-Associated Protein 43 (GAP-43) in cutaneous and mucosal nerve structures of the adult rat lower lip after mental nerve section. Ann. Anat., 185, 35-44.
68. Wallace, V.C., Blackbeard, J., Segerdahl, A.R., Hasnie, F., Pheby, T., McMahon, S.B. & Rice, A.S. (2007) Characterization of rodent models of HIV-gp120 and anti-retroviral-associated neuropathic pain. Brain, 130, 2688-2702.
69. Wang, L., Hilliges, M., Jernbert, T., Wieglb-Edstrom, D. & Johansson, O. (1990) Protein gene product 9.5-immunoreactive nerve fibres and cells in human skin. Cell Tiss. Res., 261, 25-33.
70. s mice are resistant to paclitaxel (Taxol) neuropathy. Ann. Neurol., 52, 442-447.
71. Wendelschafer-Crabb, G., Kennedy, W.R. & Walk, D. (2006) Morphological features of nerves in skin biopsies. J. Neurol. Sci., 242, 15-21.
72. Wiernik, P.H., Schwartz, E.L., Strauman, J.J., Dutcher, J.P., Lipton, R.B. & Paietta, E. (1987) Phase I clinical and pharmacokinetic study of taxol. Cancer Res., 47, 2486-2493.
73. Wilkinson, K.D., Lee, K.M., Deshpande, S., Duerksen-Hughes, P., Boss, J.M. & Pohl, J. (1989) The neuron-specific protein PGP 9.5 is a ubiquitin carboxyl-terminal hydrolase. Science, 246, 670-673.
74. Windebank, A.J. & Grisold, W. (2008) Chemotherapy-induced neuropathy. J. Peripher. Nerv. Syst., 13, 27-46.
75. Winklemann, R.K. (1967) Cutaneous nerves. In Zelickson, A.S. (Ed.), Ultrastructure of Normal and Abnormal Skin. Lea & Febiger, Philadelphia, pp. 202-227.
76. Xiao, W.H. & Bennett, G.J. (2008) Chemotherapy-evoked neuropathic pain - abnormal spontaneous discharge in A-fiber and C-fiber primary afferent neurons and its suppression by acetyl-L-carnitine. Pain, 144, 714-720.
77. Xiao, W.H., Bennett, G.J., Bordet, T. & Pruss, R.M. (2009) Olesoxime (cholest-4-en-3-one, oxime) - analgesic and neuroprotective effects in a rat model of painful peripheral neuropathy produced by the chemotherapeutic agent, paclitaxel. Pain, 147, 202-209.
78. th World Congress on Pain IASP, Montreal. Abstract # PW 097.
79. Zimmermann, M. (1983) Ethical guidelines for investigations of experimental pain in conscious animals. Pain, 16, 109-110.