Denervation of skin in neuropathies: The sequence of axonal and Schwann cell changes in skin biopsies

Brain

Volumn 130, Issue 10, 2007, Pages 2703-2714

  Ebenezer, Gigi J ^a   McArthur, Justin C ^a   Thomas, Diane ^a   Murinson, Beth ^a   Hauer, Peter ^a   Polydefkis, Michael ^a   Griffin, John W ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Dermis; Epidermis; Schwann cell; Skin biopsy; Unmyelinated axon

Indexed keywords

PROTEIN P75; PROTEIN S 100;

ADULT; ARTICLE; CELL ORGANELLE; CLINICAL ARTICLE; CONTROLLED STUDY; DERMIS; ELECTRON MICROSCOPY; EPIDERMIS; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; MALE; MITOCHONDRION; MUSCLE DENERVATION; NERVE DEGENERATION; NERVE FIBER; NERVE FIBER TRANSECTION; NERVE FIBER TRANSPORT; NERVE TRANSECTION; NEUROFILAMENT; NEUROPATHY; PATHOLOGY; PRIORITY JOURNAL; SCHWANN CELL; SKIN BIOPSY; SWELLING;

ADULT; AXONS; BIOPSY; CHRONIC DISEASE; EPIDERMIS; FEMALE; HIV INFECTIONS; HUMANS; MALE; MICROSCOPY, ELECTRON; MIDDLE AGED; PERIPHERAL NERVOUS SYSTEM DISEASES; SCHWANN CELLS; SKIN; SURAL NERVE; WALLERIAN DEGENERATION;

EID: 34848915458     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awm199     Document Type: Article

References (57)

1. Ballin RH, Thomas PK. Changes at the nodes of ranvier during Wallerian degeneration: an electron microscope study. Acta Neuropathol (Berl) 1969; 14: 237-49.
2. Byers MR, Kvinnsland I, Bothwell M. Analysis of low affinity nerve growth factor receptor during pulpal healing and regeneration of myelinated and unmyelinated axons in replanted teeth. J Comp Neurol 1992; 326: 470-84.
3. Cauna N. The free penicillate nerve endings of the human hairy skin. J Anat 1973; 115: 277-88.
4. Cherry CL, Skolasky RL, Lal L, Creighton J, Hauer P, Raman SP, et al. Antiretroviral use and other risks for HIV-associated neuropathies in an international cohort. Neurology 2006; 66: 867-73.
5. Chiang MC, Lin YH, Pan CL, Tseng TJ, Lin WM, Hsieh ST. Cutaneous innervation in chronic inflammatory demyelinating polyneuropathy. Neurology 2002; 59: 1094-8.
6. Cornblath DR, McArthur JC. Predominantly sensory neuropathy in patients with AIDS and AIDS-related complex. Neurology 1988; 38: 794-96.
7. DCCT Research Group. The effect of intensive diabetes therapy on the development and progression of neuropathy. The Diabetes Control and Complications Trial Research Group. Ann Intern Med 1995; 122: 561-8.
8. Furey MJ, Midha R, Xu QG, Belkas J, Gordon T. Prolonged target deprivation reduces the capacity of injured motoneurons to regenerate. Neurosurgery 2007; 60: 723-32.
9. Giannini C, Dyck PJ. The fate of Schwann cell basement membranes in permanently transected nerves. J Neuropathol Exp Neurol 1990; 49: 550-63.
10. Gibbels E. Morphometry of unmyelinated nerve fibers. Clin Neuropathol 1989; 8: 179-87.
11. Gibbons CH, Griffin JW, Polydefkis M, Bonyhay I, Brown A, Hauer PE, et al. The utility of skin biopsy for prediction of progression in suspected small fiber neuropathy. Neurology 2006; 66: 256-8.
12. Griffin JW, George EB, Chaudhry V. Wallerian degeneration in peripheral nerve disease. Baillieres Clin Neurol 1996; 5: 65-75. Review.
13. Griffin JW, Hoke A, Nguyen TT. Textbook of neural repair and rehabilitation. In: Michael E. Selzer, Stephanie Clarke, Leonardo Cohen, Pamela Duncan, Fred Gage, editors. Neural repair and plasticity. Vol. 1. Cambridge: Cambridge University Press; 2006, Chapter 17. p. 293-303.
14. Griffin JW, Price DL. Schwann cell and glial responses in beta, beta'-iminodipropionitrile intoxication. I. Schwann cell and oligodendrocyte ingrowths. J Neurocytol 1981; 10: 995-1007.
15. Hart AM, Wilson AD, Montovani C, Smith C, Johnson M, Terenghi G, et al. Acetyl-l-carnitine: a pathogenesis based treatment for HIV-associated antiretroviral toxic neuropathy. AIDS 2004; 18: 1549-60.
16. Heine W, Conant K, Griffin JW, Hoke A. Transplanted neural stem cells promote axonal regeneration through chronically denervated peripheral nerves. Exp Neurol 2004; 189: 231-40.
17. Hoke A, Gordon T, Zochodne DW, Sulaiman OA. A decline in glial cellline-derived neurotrophic factor expression is associated with impaired regeneration after long-term Schwann cell denervation. Exp Neurol 2002; 173: 77-85.
18. Hoke A, Redett R, Hameed H, Jari R, Zhou C, Li ZB, et al. Schwann cells express motor and sensory phenotypes that regulate axon regeneration. J Neurosci 2006; 26: 9646-55.
19. Holland NR, Stocks A, Hauer P, Cornblath DR, Griffin JW, McArthur JC. Intraepidermal nerve fiber density in patients with painful sensory neuropathy. Neurology 1997; 48: 708-11.
20. Hsieh ST, Choi S, Lin WM, Chang YC, Mcarthur JC, Griffin JW. Epidermal denervation and its effects on keratinocytes and Langerhans cells. J Neurocytol 1996; 25: 513-24.
21. Kennedy WR, Wendelschafer-Crabb G. The innervation of human epidermis. J Neurol Sci 1993; 115: 184-90.
22. Kennedy WR, Wendelschafer-Crabb G, Johnson T. Quantitation of epidermal nerves in diabetic neuropathy. Neurology 1996; 47: 1042-48.
23. Kennedy WR, Wendelschafer-Crabb G, Polydefkis M, McArthur JC. Pathology and quantitation of cutaneous innervation. In: Dyck PJ, Thomas PK, editors. Peripheral Neuropathy. 4th edn. Philadelphia: Saunders; 2005. p. 869-96.
24. Ko MH, Chen WP, Hsieh ST. Neuropathology of skin denervation in acrylamide-induced neuropathy. Neurobiol Dis 2002; 11: 155-65.
25. Lauria G, Cornblath DR, Johansson O, McArthur JC, Mellgren SI, Nolano M, et al. European Federation of Neurological Societies. EFNS guidelines on the use of skin biopsy in the diagnosis of peripheral neuropathy. Eur J Neurol 2005; 12: 747-58.
26. Lauria G, Holland N, Hauer P, Cornblath DR, Griffin JW, McArthur JC. Epidermal innervation: changes with aging, topographic location, and in sensory neuropathy. J Neurol Sci 1999; 164: 172-8.
27. Lauria G, Morbin M, Lombardi R, Borgna M, Mazzoleni G, Sghirlanzoni A, et al. Axonal swellings predict the degeneration of epidermal nerve fibers in painful neuropathies. Neurology 2003; 61: 631-6.
28. Lauria G, Sghirlanzoni A, Lombardi R, Pareyson D. Epidermal nerve fiber density in sensory ganglionopathies: clinical and neurophysiologic correlations. Muscle Nerve 2001; 24: 1034-9.
29. Lee JE, Shun CT, Hsieh SC, Hsieh ST. Skin denervation in vasculitic neuropathy. Arch Neurol 2005; 62: 1570-3.
30. Lubinska L. Patterns of Wallerian degeneration of myelinated fibers in short and long peripheral stumps and in isolated segments of rat phrenic nerve. Interpretation of the role of axoplasmic flow of the trophic factor. Brain Res 1982; 233: 227-40.
31. Lunn ER, Perry VH, Brown MC, Rosen H, Gordon S. Absence of Wallerian degeneration does not hinder regeneration in peripheral nerve. Eur J Neurosci 1989; 1: 27-33.
32. McArthur JC, Griffin JW. Another tool for the neurologist's toolbox. Ann Neurol 2005; 57: 163-7.
33. McArthur JC, Stocks EA, Hauer P, Cornblath DR, Griffin JW. Epidermal nerve fiber density: normative reference range and diagnostic efficiency. Arch Neurol 1998; 55: 1513-20.
34. McCarthy BG, Hsieh ST, Stocks A, Hauer P, Macko C, Cornblath DR, et al. Cutaneous innervation in sensory neuropathies: evaluation by skin biopsy. Neurology 1995; 45: 1848-55.
35. Midha R, Munro CA, Chan S, Nitising A, Xu QG, Gordon T. Regeneration into protected and chronically denervated peripheral nerve stumps. Neurosurgery 2005; 57: 1289-99.
36. Miko TL, Le Maitre C, Kinfu Y. Damage and regeneration of peripheral nerves in advanced treated leprosy. Lancet 1993; 342: 521-5.
37. Murinson BB, Griffin JW. C-fiber structure varies with location in peripheral nerve. J Neuropathol Exp Neurol 2004; 63: 246-54.
38. Omdal R, Mellgren SI, Goransson L, Skjesol A, Lindal S, Koldingsnes W, et al. Small nerve fiber involvement in systemic lupus erythematosus: a controlled study. Arthritis Rheum 2002; 46: 1228-32.
39. Pan CL, Tseng TJ, Lin YH, Chiang MC, Lin WM, Hsieh ST. Cutaneous innervation in Guillain-Barré syndrome: pathology and clinical correlations. Brain 2003; 126: 386-97.
40. Periquet I, Novak V, Collins M, Nagaraja H, Erdem S, Nash S, et al. Painful sensory neuropathy; prospective evaluation using skin biopsy. Neurology 1999; 53: 1641-47.
41. Politis MJ, Pellegrino RG, Spencer PS. Ultrastructural studies of the dying-back process. V. Axonal neurofilaments accumulate at sites of 2,5-hexanedione application: evidence for nerve fibre dysfunction in experimental hexacarbon neuropathy. J Neurocytol 1980; 9: 505-16.
42. Polydefkis M, Yiannoutsos CT, Cohen BA, Hollander H, Schifitto G, Clifford DB, et al. Reduced intraepidermal nerve fiber density in HIV-associated sensory neuropathy. Neurology 2002; 58: 115-9.
43. Reilly MM, Staunton H. Peripheral nerve amyloidosis. Brain Pathol 1996; 6: 163-77.
44. Scott LJ, Griffin JW, Luciano C, Barton NW, Banerjee T, Crawford T, et al. Quantitative analysis of epidermal innervation in Fabry disease. Neurology 1999; 52: 1249-54.
45. Shetty VP, Antia NH, Jacobs JM. The pathology of early leprous neuropathy. J Neurol Sci 1988; 88: 115-31.
46. Singleton JR, Smith AG, Russell J, Feldman EL. Polyneuropathy with impaired glucose tolerance: implications for diagnosis and therapy. Curr Treat Options Neurol 2005; 7: 33-42.
47. Smith GA, Ramachandran P, Tripp S, Singleton RJ. Epidermal nerve innervation in impaired glucose tolerance and diabetes-associated neuropathy. Neurology 2001; 57: 1701-04.
48. Song XY, Zhou FH, Zhong JH, Wu LL, Zhou XF. Knockout of p75(NTR) impairs re-myelination of injured sciatic nerve in mice. J Neurochem 2006; 96: 833-42.
49. Spencer PS, Schaumburg HH. Ultrastructural studies of the dying-back process. III. The evolution of experimental peripheral giant axonal degeneration. J Neuropathol Exp Neurol 1977; 36: 276-99.
50. Spencer PS, Thomas PK. Ultrastructural studies of the dying-back process. II. The sequestration and removal by Schwann cells and oligodendrocytes of organelles from normal and diseases axons. J Neurocytol 1974; 3: 763-83.
51. Stocks EA, McArthur JC, Griffin JW, Mouton PR. An unbiased method for estimation of total epidermal nerve fiber length. J Neurocytol 1996; 25: 637-44.
52. Stoll G, Griffin JW, Li CY, Trapp BD. Wallerian degeneration in the peripheral nervous system: participation of both Schwann cells and macrophages in myelin degradation. J Neurocytol 1989; 18: 671-83.
53. Sulaiman OA, Gordon T. Effects of short- and long-term Schwann cell denervation on peripheral nerve regeneration, myelination, and size. Glia 2000; 32: 234-46.
54. Sulaiman OA, Midha R, Munro CA, Matsuyama T, Al-Majed A, Gordon T. Chronic Schwann cell denervation and the presence of a sensory nerve reduce motor axonal regeneration. Exp Neurol 2002; 176: 342-54.
55. Sumner CJ, Sheth S, Griffin JW, Cornblath DR, Polydefkis M. The spectrum of neuropathy in diabetes and impaired glucose tolerance. Neurology 2003; 60: 108-11.
56. Tsukita S, Ishikawa H. The movement of membranous organelles in axons. Electron microscopic identification of anterogradely and retrogradely transported organelles. J Cell Biol 1980; 84: 513-30.
57. Wendelschafer-Crabb G, Kennedy WR, Walk D. Morphological features of nerves in skin biopsies. J Neurol Sci 2006; 242: 15-21.