Biopsable neural tissues: Toward new biomarkers for Parkinson's disease?

Frontiers in Psychiatry

Volumn 1, Issue SEP, 2010, Pages

  Lebouvier, Thibaud ^a,b,c   Tasselli, Maddalena ^a   Paillusson, Sébastien ^a,b   Pouclet, Hélène ^a,c   Neunlist, Michel ^a,b   Derkinderen, Pascal ^a,b,c  

^a INSERM   (France)

^b UNIVERSITÉ DE NANTES   (France)

^c NANTES UNIVERSITY HOSPITAL   (France)

Author keywords

Alpha synuclein; Autonomic nervous system; Biomarker; Colonic biopsies; Enteric nervous system; Parkinson's disease; Salivary glands; Skin

Indexed keywords

EID: 81955161348     PISSN: None     EISSN: 16640640     Source Type: Journal    
DOI: 10.3389/fpsyt.2010.00128     Document Type: Review

References (55)

1. Abbott, R. D., Petrovitch, H., White, L. R., Masaki, K. H., Tanner, C. M., Curb, J. D., Grandinetti, A., Blanchette, P. L., Popper, J. S., and Ross, G. W. (2001). Frequency of bowel movements and the future risk of Parkinson's disease. Neurology 57, 456-462.
2. Ahlskog, J. E. (2007). Beating a dead horse: dopamine and Parkinson disease. Neurology 69, 1701-1711.
3. Anderson, J. P., Walker, D. E., Goldstein, J. M., de Laat, R., Banducci, K., Caccavello, R. J., Barbour, R., Huang, J., Kling, K., Lee, M., Diep, L., Keim, P. S., Shen, X., Chataway, T., Schlossmacher, M. G., Seubert, P., Schenk, D., Sinha, S., Gai, W. P., and Chilcote, T. J. (2006). Phosphorylation of Ser-129 is the dominant pathological modification of alpha-synuclein in familial and spo-radic Lewy body disease. J. Biol. Chem. 281, 29739-29752.
4. Beach, T. G., Adler, C. H., Sue, L. I., Vedders, L., Lue, L., White III, C. L., Akiyama, H., Caviness, J. N., Shill, H. A., Sabbagh, M. N., and Walker, D. G. (2010). Multi-organ distribution of phosphorylated alpha-synuclein his-topathology in subjects with Lewy body disorders. Acta Neuropathol. 119, 689-702.
5. Beach, T. G., White, C. L., III, Hladik, C. L., Sabbagh, M. N., Connor, D. J., Shill, H. A., Sue, L. I., Sasse, J., Bachalakuri, J., Henry-Watson, J., Akiyama, H., and Adler, C. H. (2009). Olfactory bulb alpha-synucleinopathy has high specificity and sensitivity for Lewy body disorders. Acta Neuropathol. 117, 169-174.
6. Benarroch, E. E. (2007). Enteric nervous system: functional organization and neurologic implications. Neurology 69, 1953-1957.
7. Berg, D., and Becker, G. (2002). Perspectives of B-mode transcranial ultrasound. Neuroimage 15, 463-473.
8. Bloch, A., Probst, A., Bissig, H., Adams, H., and Tolnay, M. (2006). Alpha-synuclein pathology of the spinal and peripheral autonomic nervous system in neurologically unimpaired elderly subjects. Neuropathol. Appl. Neurobiol. 32, 284-295.
9. Braak, H., and Del Tredici, K. (2008). Invited article: nervous system pathol-ogy in sporadic Parkinson disease. Neurology 70, 1916-1925.
10. Braak, H., Del Tredici, K., Bratzke, H., Hamm-Clement, J., Sandmann-Keil, D., and Rub, U. (2002). Staging of the intracerebral inclusion body pathology associated with idiopathic Parkinson's disease (preclinical and clinical stages). J. Neurol. 249(Suppl. 3), III/1-III/5.
11. Braak, H., Del Tredici, K., Rub, U., de Vos, R. A., Jansen Steur, E. N., and Braak, E. (2003). Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol. Aging 24, 197-211.
12. Braak, H., de Vos, R. A., Bohl, J., and Del Tredici, K. (2006). Gastric alpha-sy-nuclein immunoreactive inclusions in Meissner's and Auerbach's plexuses in cases staged for Parkinson's disease-related brain pathology. Neurosci. Lett. 396, 67-72.
13. Braak, H., Sastre, M., Bohl, J. R., de Vos, R. A., and Del Tredici, K. (2007). Parkinson's disease: lesions in dorsal horn layer I, involvement of para-sympathetic and sympathetic pre-and postganglionic neurons. Acta Neuropathol. 113, 421-429.
14. Caporali, R., Bonacci, E., Epis, O., Bobbio-Pallavicini, F., Morbini, P., and Montecucco, C. (2008). Safety and usefulness of minor salivary gland biopsy: retrospective analysis of 502 procedures performed at a single center. Arthritis Rheum. 59, 714-720.
15. Cersosimo, M. G., and Benarroch, E. E. (2008). Neural control of the gas-trointestinal tract: implications for Parkinson disease. Mov. Disord. 23, 1065-1075.
16. Cersosimo, M. G., Perandones, C., Micheli, F. E., Raina, G. B., Beron, A. M., Nasswetter, G. M. R., and Benarroch, E. E. (2010). "Alpha-synuclein immu-noreactivity in minor salivary glands: a potential pathological biomarker for Parkinson's disease?," in 14th International Congress on Parkinson's Disease and Movement Disorders, Buenos Aires, Argentina.
17. Chaudhuri, K. R., Healy, D. G., and Schapira, A. H. (2006). Non-motor symptoms of Parkinson's disease: diagnosis and management. Lancet Neurol. 5, 235-245.
18. DelleDonne, A., Klos, K. J., Fujishiro, H., Ahmed, Z., Parisi, J. E., Josephs, K. A., Frigerio, R., Burnett, M., Wszolek, Z. K., Uitti, R. J., Ahlskog, J. E., and Dickson, D. W. (2008). Incidental Lewy body disease and preclinical Parkinson disease. Arch. Neurol. 65, 1074-1080.
19. Del Tredici, K., Hawkes, C. H., Ghebremedhin, E., and Braak, H. (2010). Lewy pathology in the sub-mandibular gland of individuals with incidental Lewy body disease and sporadic Parkinson's disease. Acta Neuropathol. 119, 703-713.
20. Del Tredici, K., Rub, U., De Vos, R. A., Bohl, J. R., and Braak, H. (2002). Where does Parkinson disease pathology begin in the brain? J Neuropathol. Exp. Neurol. 61, 413-426.
21. Fujiwara, H., Hasegawa, M., Dohmae, N., Kawashima, A., Masliah, E., Goldberg, M. S., Shen, J., Takio, K., and Iwatsubo, T. (2002). alpha-Synuclein is phospho-rylated in synucleinopathy lesions. Nat. Cell Biol. 4, 160-164.
22. Hawkes, C. H., Del Tredici, K., and Braak, H. (2009). Parkinson's disease: the dual hit theory revisited. Ann. N. Y. Acad. Sci. 1170, 615-622.
23. Hong, Z., Shi, M., Chung, K. A., Quinn, J. F., Peskind, E. R., Galasko, D., Jankovic, J., Zabetian, C. P., Leverenz, J. B., Baird, G., Montine, T. J., Hancock, A. M., Hwang, H., Pan, C., Bradner, J., Kang, U. J., Jensen, P. H., and Zhang, J. (2010). DJ-1 and alpha-synuclein in human cerebrospinal fluid as biomar-kers of Parkinson's disease. Brain 133, 713-726.
24. Hughes, A. J., Daniel, S. E., Ben-Shlomo, Y., and Lees, A. J. (2002). The accu-racy of diagnosis of parkinsonian syndromes in a specialist movement disorder service. Brain 125, 861-870.
25. Ikemura, M., Saito, Y., Sengoku, R., Sakiyama, Y., Hatsuta, H., Kanemaru, K., Sawabe, M., Arai, T., Ito, G., Iwatsubo, T., Fukayama, M., and Murayama, S. (2008). Lewy body pathology involves cutaneous nerves. J. Neuropathol. Exp. Neurol. 67, 945-953.
26. Ironside, J. W., Hilton, D. A., Ghani, A., Johnston, N. J., Conyers, L., McCardle, L. M., and Best, D. (2000). Retrospective study of prion-protein accumulation in tonsil and appendix tissues. Lancet 355, 1693-1694.
27. Kikuchi, A., Takeda, A., Okamura, N., Tashiro, M., Hasegawa, T., Furumoto, S., Kobayashi, M., Sugeno, N., Baba, T., Miki, Y., Mori, F., Wakabayashi, K., Funaki, Y., Iwata, R., Takahashi, S., Fukuda, H., Arai, H., Kudo, Y., Yanai, K., and Itoyama, Y. (2010). In vivo visu-alization of alpha-synuclein deposition by carbon-11-labelled 2-[2-(2-dimeth-ylaminothiazol-5-yl)ethenyl]-6-[2-(fluoro)ethoxy]benzoxazole positron emission tomography in multiple sys-tem atrophy. Brain 133, 1772-1778.
28. Kovacs, T., Papp, M. I., Cairns, N. J., Khan, M. N., and Lantos, P. L. (2003). Olfactory bulb in multiple system atrophy. Mov. Disord. 18, 938-942.
29. Kupsky, W. J., Grimes, M. M., Sweeting, J., Bertsch, R., and Cote, L. J. (1987). Parkinson's disease and megacolon: concentric hyaline inclusions (Lewy bodies) in enteric ganglion cells. Neurology 37, 1253-1255.
30. Lebouvier, T., Chaumette, T., Damier, P., Coron, E., Touchefeu, Y., Vrignaud, S., Naveilhan, P., Galmiche, J. P., Bruley des Varannes, S., Derkinderen, P., and Neunlist, M. (2008). Pathological lesions in colonic biopsies dur-ing Parkinson's disease. Gut 57, 1741-1743.
31. Lebouvier, T., Chaumette, T., Paillusson, S., Duyckaerts, C., Bruley des Varannes, S., Neunlist, M., and Derkinderen, P. (2009a). The second brain and Parkinson's disease. Eur. J. Neurosci. 30, 735-741.
32. Lebouvier, T., Coron, E., Chaumette, T., Paillusson, S., Bruley des Varannes, S., Neunlist, M., and Derkinderen, P. (2009b). Routine colonic biopsies as a new tool to study the enteric nervous system in living patients. Neurogastroenterol Motil. 22, e11-e14.
33. Lebouvier, T., Neunlist, M., Bruley Des Varannes, S., Coron, E., Drouard, A., Nguyen, J. P., Chaumette, T., Tasselli, M., Paillusson, S., Flamand, M., Galmiche, J. P., Damier, P., and Derkinderen, P. (2010). Colonic biopsies to assess the neuropathology of Parkinson's disease and its rela-tionship with symptoms. PLoS ONE (in press).
34. Lees, A. J., Hardy, J., and Revesz, T. (2009). Parkinson's disease. Lancet 373, 2055-2066.
35. Marek, K., Jennings, D., Tamagnan, G., and Seibyl, J. (2008). Biomarkers for Parkinson's [corrected] disease: tools to assess Parkinson's disease onset and progression. Ann. Neurol. 64(Suppl. 2), S111-S121.
36. Martin, W. R., Wieler, M., and Gee, M. (2008). Midbrain iron content in early Parkinson disease: a potential biomarker of disease status. Neurology 70, 1411-1417.
37. Miki, Y., Tomiyama, M., Ueno, T., Haga, R., Nishijima, H., Suzuki, C., Mori, F., Kaimori, M., Baba, M., and Wakabayashi, K. (2010). Clinical avail-ability of skin biopsy in the diagnosis of Parkinson's disease. Neurosci. Lett. 469, 357-359.
38. Minguez-Castellanos, A., Chamorro, C. E., Escamilla-Sevilla, F., Ortega-Moreno, A., Rebollo, A. C., Gomez-Rio, M., Concha, A., and Munoz, D. G. (2007). Do alpha-synuclein aggre-gates in autonomic plexuses predate Lewy body disorders?: a cohort study. Neurology 68, 2012-2018.
39. Olanow, C. W., Rascol, O., Hauser, R., Feigin, P. D., Jankovic, J., Lang, A., Langston, W., Melamed, E., Poewe, W., Stocchi, F., and Tolosa, E. (2009). A double-blind, delayed-start trial of rasagiline in Parkinson's disease. N. Engl. J. Med. 361, 1268-1278.
40. Orimo, S., Uchihara, T., Nakamura, A., Mori, F., Kakita, A., Wakabayashi, K., and Takahashi, H. (2008). Axonal alpha-synuclein aggregates herald cen-tripetal degeneration of cardiac sym-pathetic nerve in Parkinson's disease. Brain 131, 642-650.
41. Parkkinen, L., Silveira-Moriyama, L., Holton, J. L., Lees, A. J., and Revesz, T. (2009). Can olfactory bulb biopsy be justified for the diagnosis of Parkinson's disease? Comments on "olfactory bulb alpha-synucleinopa-thy has high specificity and sensitiv-ity for Lewy body disorders". Acta Neuropathol. 117, 213-214; author reply 217-218.
42. Ponsen, M. M., Stoffers, D., Booij, J., van Eck-Smit, B. L., Wolters, E., and Berendse, H. W. (2004). Idiopathic hyposmia as a preclinical sign of Parkinson's disease. Ann. Neurol. 56, 173-181.
43. Postuma, R. B., Gagnon, J. F., Vendette, M., Fantini, M. L., Massicotte-Marquez, J., and Montplaisir, J. (2009). Quantifying the risk of neurodegenerative disease in idiopathic REM sleep behavior dis-order. Neurology 72, 1296-1300.
44. Qualman, S. J., Haupt, H. M., Yang, P., and Hamilton, S. R. (1984). Esophageal Lewy bodies associated with ganglion cell loss in achalasia. Similarity to Parkinson's disease. Gastroenterology 87, 848-856.
45. Rub, U., Del Tredici, K., Schultz, C., de Vos, R. A., Jansen Steur, E. N., Arai, K., and Braak, H. (2002). Progressive supranuclear palsy: neuronal and glial cytoskeletal pathology in the higher order processing autonomic nuclei of the lower brainstem. Neuropathol. Appl. Neurobiol. 28, 12-22.
46. Savica, R., Carlin, J. M., Grossardt, B. R., Bower, J. H., Ahlskog, J. E., Maraganore, D. M., Bharucha, A. E., and Rocca, W. A. (2009). Medical records documentation of constipa-tion preceding Parkinson disease: a case-control study. Neurology 73, 1752-1758.
47. Schapira, A. H., and Olanow, C. W. (2004). Neuroprotection in Parkinson disease: mysteries, myths, and misconceptions. JAMA 291, 358-364.
48. Schemann, M., and Neunlist, M. (2004). The human enteric nervous system. Neurogastroenterol. Motil. 16(Suppl. 1), 55-59.
49. Stern, M. B., and Siderowf, A. (2010). Parkinson's at risk syndrome: can Parkinson's disease be predicted? Mov. Disord. 25(Suppl. 1), S89-S93.
50. Thobois, S., Delamarre-Damier, F., and Derkinderen, P. (2005). Treatment of motor dysfunction in Parkinson's disease: an overview. Clin. Neurol. Neurosurg. 107, 269-281.
51. Wadsworth, J. D., Joiner, S., Hill, A. F., Campbell, T. A., Desbruslais, M., Luthert, P. J., and Collinge, J. (2001). Tissue distribution of protease resistant prion protein in variant Creutzfeldt-Jakob disease using a highly sensitive immunoblotting assay. Lancet 358, 171-180.
52. Wakabayashi, K., and Takahashi, H. (1997). Neuropathology of autonomic nervous system in Parkinson's disease. Eur. Neurol. 38(Suppl. 2), 2-7.
53. Wakabayashi, K., Takahashi, H., Ohama, E., Takeda, S., and Ikuta, F. (1993). Lewy bodies in the visceral autonomic nervous system in Parkinson's disease. Adv. Neurol. 60, 609-612.
54. Wakabayashi, K., Takahashi, H., Takeda, S., Ohama, E., and Ikuta, F. (1988). Parkinson's disease: the presence of Lewy bodies in Auerbach's and Meissner's plexuses. Acta Neuropathol. 76, 217-221.
55. Witt, M., Bormann, K., Gudziol, V., Pehlke, K., Barth, K., Minovi, A., Hahner, A., Reichmann, H., and Hummel, T. (2009). Biopsies of olfactory epithe-lium in patients with Parkinson's dis-ease. Mov. Disord. 24, 906-914.