The distribution of E-cadherin expression in listeric rhombencephalitis of ruminants indicates its involvement in Listeria monocytogenes neuroinvasion

Neuropathology and Applied Neurobiology

Volumn 37, Issue 7, 2011, Pages 753-767

  Madarame, H ^a   Seuberlich, T ^b   Abril, C ^b   Zurbriggen, A ^b   Vandevelde, M ^b   Oevermann, A ^b  

^a AZABU UNIVERSITY   (Japan)

^b UNIVERSITY OF BERN   (Switzerland)

Author keywords

Brainstem encephalitis (rhombencephalitis); E cadherin expression; Listeria monocytogenes; Neuroinvasion; Oral mucosa; Schwann cells

Indexed keywords

GENE PRODUCT; INTERNALIN A; MYELIN ASSOCIATED GLYCOPROTEIN; PROTEIN GENE PRODUCT 9.5; UNCLASSIFIED DRUG; UVOMORULIN; VIRULENCE FACTOR;

ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL VIRULENCE; BOVIDS; CELL INVASION; CHOROID PLEXUS; CONTROLLED STUDY; ENCEPHALITIS; GANGLION; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; LISTERIA MONOCYTOGENES; LISTERIOSIS; MENINX; MYELINATED NERVE; NERVE FIBER; NEUROPATHOLOGY; NEUROPIL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RHOMBENCEPHALITIS; RHOMBENCEPHALON; SATELLITE CELL; SCHWANN CELL;

ANIMALS; BRAIN; BRAIN STEM; CADHERINS; CATTLE; CHOROID PLEXUS; ENCEPHALITIS; GOATS; LISTERIA MONOCYTOGENES; LISTERIOSIS; MOLECULAR SEQUENCE DATA; SHEEP;

EID: 80055071453     PISSN: 03051846     EISSN: 13652990     Source Type: Journal    
DOI: 10.1111/j.1365-2990.2011.01183.x     Document Type: Article

References (69)

1. Oevermann A, Zurbriggen A, Vandevelde M. Rhombencephalitis caused by Listeria monocytogenes in humans and ruminants: a Zoonosis on the rise? Interdiscip Perspect Infect Dis 2010; 2010: doi: 10.1155/2010/632513.
2. Siegman-Igra Y, Levin R, Weinberger M, Golan Y, Schwartz D, Samra Z, Konigsberger H, Yinnon A, Rahav G, Keller N, Bisharat N, Karpuch J, Finkelstein R, Alkan M, Landau Z, Novikov J, Hassin D, Rudnicki C, Kitzes R, Ovadia S, Shimoni Z, Lang R, Shohat T. Listeria monocytogenes infection in Israel and review of cases worldwide. Emerg Infect Dis 2002; 8: 305-10.
3. Bille J, Blanc DS, Schmid H, Boubaker K, Baumgartner A, Siegrist HH, Tritten ML, Lienhard R, Berner D, Anderau R, Treboux M, Ducommun JM, Malinverni R, Genne D, Erard PH, Waespi U. Outbreak of human listeriosis associated with tomme cheese in northwest Switzerland, 2005. Euro Surveill 2006; 11: 91-3.
4. Low JC, Donachie W. A review of Listeria monocytogenes and listeriosis. Vet J 1997; 153: 9-29.
5. Antal EA, Loberg EM, Dietrichs E, Maehlen J. Neuropathological findings in 9 cases of Listeria monocytogenes brain stem encephalitis. Brain Pathol 2005; 15: 187-91.
6. Oevermann A, Di PS, Doherr MG, Abril C, Zurbriggen A, Vandevelde M. Neuropathogenesis of naturally occurring encephalitis caused by Listeria monocytogenes in ruminants. Brain Pathol 2010; 20: 378-90.
7. Oevermann A, Botteron C, Seuberlich T, Nicolier A, Friess M, Doherr MG, Heim D, Hilbe M, Zimmer K, Zurbriggen A, Vandevelde M. Neuropathological survey of fallen stock: active surveillance reveals high prevalence of encephalitic listeriosis in small ruminants. Vet Microbiol 2008; 130: 320-9.
8. Charlton KM, Garcia MM. Spontaneous listeric encephalitis and neuritis in sheep. Light microscopic studies. Vet Pathol 1977; 14: 297-313.
9. Otter A, Blakemore WF. Observation on the presence of Listeria monocytogenes in axons. Acta Microbiol Hung 1989; 36: 125-31.
10. Urbaneck D. Zur Neuropathogenese der Listeriose. Histologische Untersuchungen am N. trigeminus bei spontan an zerebraler Form der Listeriose erkrankten Schafen. Arch Exp Veterinarmed 1962; 16: 61-80.
11. Blanot S, Joly MM, Vilde F, Jaubert F, Clement O, Frija G, Berche P. A gerbil model for rhombencephalitis due to Listeria monocytogenes. Microb Pathog 1997; 23: 39-48.
12. Erbar S, Diederich S, Maisner A. Selective receptor expression restricts Nipah virus infection of endothelial cells. Virol J 2008; 5: 142.
13. Arnberg N. Adenovirus receptors: implications for tropism, treatment and targeting. Rev Med Virol 2009; 19: 165-78.
14. Dodson KW, Pinkner JS, Rose T, Magnusson G, Hultgren SJ, Waksman G. Structural basis of the interaction of the pyelonephritic E. coli adhesin to its human kidney receptor. Cell 2001; 105: 733-43.
15. Klemm P, Schembri MA. Bacterial adhesins: function and structure. Int J Med Microbiol 2000; 290: 27-35.
16. Lecuit M. Understanding how Listeria monocytogenes targets and crosses host barriers. Clin Microbiol Infect 2005; 11: 430-6.
17. Mengaud J, Ohayon H, Gounon P, Mege R-M Cossart P. E-cadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial cells. Cell 1996; 84: 923-32.
18. Lecuit M, Nelson DM, Smith SD, Khun H, Huerre M, Vacher-Lavenu MC, Gordon JI, Cossart P. Targeting and crossing of the human maternofetal barrier by Listeria monocytogenes: role of internalin interaction with trophoblast E-cadherin. Proc Natl Acad Sci U S A 2004; 101: 6152-7.
19. Lecuit M, Vandormael-Pournin S, Lefort J, Huerre M, Gounon P, Dupuy C, Babinet C, Cossart P. A transgenic model for listeriosis: role of internalin in crossing the intestinal barrier. Science 2001; 292: 1722-5.
20. Disson O, Grayo S, Huillet E, Nikitas G, Langa-Vives F, Dussurget O, Ragon M, Le Monnier A, Babinet C, Cossart P, Lecuit M. Conjugated action of two species-specific invasion proteins for fetoplacental listeriosis. Nature 2008; 455: 1114-18.
21. Yagi T, Takeichi M. Cadherin superfamily genes: functions, genomic organization, and neurologic diversity. Genes Dev 2000; 14: 1169-80.
22. Taneyhill LA. To adhere or not to adhere: the role of Cadherins in neural crest development. Cell Adhes Migrat 2008; 2: 223-30.
23. Van Roy F, Berx G. The cell-cell adhesion molecule E-cadherin. Cell Mol Life Sci 2008; 65: 3756-88.
24. Willenegger S, Friess AE, Lang J, Stoffel MH. Immunohistochemical demonstration of lumbar intervertebral disc innervation in the dog. Anat Histol Embryol 2005; 34: 123-8.
25. Steck AJ, Murray N, Vandevelde M, Zurbriggen A. Human monoclonal antibodies to myelin-associated glycoprotein. Comparison of specificity and use for immunocytochemical localisation of the antigen. J Neuroimmunol 1983; 5: 145-56.
26. Jonquieres R, Bierne H, Mengaud J, Cossart P. The inlA gene of Listeria monocytogenes LO28 harbors a nonsense mutation resulting in release of internalin. Infect Immun 1998; 66: 3420-2.
27. Jacquet C, Doumith M, Gordon JI, Martin PM, Cossart P, Lecuit M. A molecular marker for evaluating the pathogenic potential of foodborne Listeria monocytogenes. J Infect Dis 2004; 189: 2094-100.
28. Damsky CH, Richa J, Solter D, Knudsen K, Buck CA. Identification and purification of a cell surface glycoprotein mediating intercellular adhesion in embryonic and adult tissue. Cell 1983; 34: 455-66.
29. Ito K, Okamoto I, Araki N, Kawano Y, Nakao M, Fujiyama S, Tomita K, Mimori T, Saya H. Calcium influx triggers the sequential proteolysis of extracellular and cytoplasmic domains of E-cadherin, leading to loss of beta-catenin from cell-cell contacts. Oncogene 1999; 18: 7080-90.
30. De Wever O, Derycke L, Hendrix A, De Meerleer G, Godeau F, Depypere H, Bracke M. Soluble cadherins as cancer biomarkers. Clin Exp Metastasis 2007; 24: 685-97.
31. Ferber EC, Kajita M, Wadlow A, Tobiansky L, Niessen C, Ariga H, Daniel J, Fujita Y. A role for the cleaved cytoplasmic domain of E-cadherin in the nucleus. J Biol Chem 2008; 283: 12691-700.
32. Marambaud P, Shioi J, Serban G, Georgakopoulos A, Sarner S, Nagy V, Baki L, Wen P, Efthimiopoulos S, Shao Z, Wisniewski T, Robakis NK. A presenilin-1/gamma-secretase cleavage releases the E-cadherin intracellular domain and regulates disassembly of adherens junctions. EMBO J 2002; 21: 1948-56.
33. Vallorosi CJ, Day KC, Zhao X, Rashid MG, Rubin MA, Johnson KR, Wheelock MJ, Day ML. Truncation of the beta-catenin binding domain of E-cadherin precedes epithelial apoptosis during prostate and mammary involution. J Biol Chem 2000; 275: 3328-34.
34. Rios-Doria J, Day KC, Kuefer R, Rashid MG, Chinnaiyan AM, Rubin MA, Day ML. The role of calpain in the proteolytic cleavage of E-cadherin in prostate and mammary epithelial cells. J Biol Chem 2003; 278: 1372-9.
35. Maretzky T, Reiss K, Ludwig A, Buchholz J, Scholz F, Proksch E, de Strooper B, Hartmann D, Saftig P. ADAM10 mediates E-cadherin shedding and regulates epithelial cell-cell adhesion, migration, and beta-catenin translocation. Proc Natl Acad Sci U S A 2005; 102: 9182-7.
36. Steinhusen U, Weiske J, Badock V, Tauber R, Bommert K, Huber O. Cleavage and shedding of E-cadherin after induction of apoptosis. J Biol Chem 2001; 276: 4972-80.
37. Fannon AM, Sherman DL, Ilyina-Gragerova G, Brophy PJ, Friedrich VL, Colman DR. Novel E-cadherin-mediated adhesion in peripheral nerve: Schwann cell architecture is stabilized by autotypic adherens junctions. J Cell Biol 1995; 129: 189-202.
38. Holman DW, Grzybowski DM, Mehta BC, Katz SE, Lubow M. Characterization of cytoskeletal and junctional proteins expressed by cells cultured from human arachnoid granulation tissue. Cerebrospinal Fluid Res 2005; 2: 9. doi: 10.1186/1743-8454-2-9.
39. Yamashima T. On Arachnoid villi and meningiomas: functional implication of ultrastructure, cell adhesion mechanisms, and extracellular matrix composition. Pathol Oncol Res 1996; 2: 144-9.
40. Tohma Y, Yamashima T, Yamashita J. Immunohistochemical localization of cell adhesion molecule epithelial cadherin in human arachnoid villi and meningiomas. Cancer Res 1992; 52: 1981-7.
41. Yamashima T, Tohma Y, Yamashita J. Expression of cell adhesion molecule E-cadherin in human arachnoid villi. J Neurosurg 1992; 77: 749-56.
42. Szmydynger-Chodobska J, Pascale CL, Pfeffer AN, Coulter C, Chodobski A. Expression of junctional proteins in choroid plexus epithelial cell lines: a comparative study. Cerebrospinal Fluid Res 2007; 4: 11. doi: 10.1186/1743-8454-4-11.
43. Figarella-Branger D, Lepidi H, Poncet C, Gambarelli D, Bianco N, Rougon G, Pellissier JF. Differential expression of cell adhesion molecules (CAM), neural CAM and epithelial cadherin in ependymomas and choroid plexus tumors. Acta Neuropathol 1995; 89: 248-57.
44. Pal D, Audus KL, Siahaan TJ. Modulation of cellular adhesion in bovine brain microvessel endothelial cells by a decapeptide. Brain Res 1997; 747: 103-13.
45. Abbruscato TJ, Davis TP. Protein expression of brain endothelial cell E-cadherin after hypoxia/aglycemia: influence of astrocyte contact. Brain Res 1999; 842: 277-86.
46. Rubin LL, Hall DE, Porter S, Barbu K, Cannon C, Horner HC, Janatpour M, Liaw CW, Manning K, Morales J. A cell culture model of the blood-brain barrier. J Cell Biol 1991; 115: 1725-35.
47. Fenyves AM, Behrens J, Spanel-Borowski K. Cultured microvascular endothelial cells (MVEC) differ in cytoskeleton, expression of cadherins and fibronectin matrix. A study under the influence of interferon-gamma. J Cell Sci 1993; 106: 879-90.
48. Calabria AR, Shusta EV. A genomic comparison of in vivo and in vitro brain microvascular endothelial cells. J Cereb Blood Flow Metab 2008; 28: 135-48.
49. Kiessling F, Kartenbeck J, Haller C. Cell-cell contacts in the human cell line ECV304 exhibit both endothelial and epithelial characteristics. Cell Tissue Res 1999; 297: 131-40.
50. Uchiyama N, Hasegawa M, Yamashima T, Yamashita J, Shimamura K, Takeichi M. Immunoelectron microscopic localization of E-cadherin in dorsal root ganglia, dorsal root and dorsal horn of postnatal mice. J Neurocytol 1994; 23: 460-8.
51. Shimamura K, Takahashi T, Takeichi M. E-cadherin expression in a particular subset of sensory neurons. Dev Biol 1992; 152: 242-54.
52. Takeichi M, Inuzuka H, Shimamura K, Matsunaga M, Nose A. Cadherin-mediated cell-cell adhesion and neurogenesis. Neurosci Res Suppl 1990; 13: S92-S96.
53. Shimamura K, Takeichi M. Local and transient expression of E-cadherin involved in mouse embryonic brain morphogenesis. Development 1992; 116: 1011-19.
54. Tricaud N, Perrin-Tricaud C, Bruses JL, Rutishauser U. Adherens junctions in myelinating Schwann cells stabilize Schmidt-Lanterman incisures via recruitment of p120 catenin to E-cadherin. J Neurosci 2005; 25: 3259-69.
55. Menichella DM, Arroyo EJ, Awatramani R, Xu T, Baron P, Vallat JM, Balsamo J, Lilien J, Scarlato G, Kamholz J, Scherer SS, Shy ME. Protein zero is necessary for E-cadherin-mediated adherens junction formation in Schwann cells. Mol Cell Neurosci 2001; 18: 606-18.
56. Barlow RM, McGorum B. Ovine listerial encephalitis: analysis, hypothesis and synthesis. Vet Rec 1985; 116: 233-6.
57. Akiyama Y, Asahi O, Hosoda T. Studies on the mechanism of infection of the brain with Listeria monocytogenes. Am J Vet Res 1957; 18: 147-57.
58. Jakob W. Further experimental studies on the pathogenesis of cerebral listeriosis in sheep. 3. The course of the experimental infection with L. monocytogenes in sheep with high protein and low protein nutrition. Arch Exp Veterinarmed 1967; 21: 1061-72.
59. Hasegawa M, Seto A, Uchiyama N, Kida S, Yamashima T, Yamashita J. Localization of E-cadherin in peripheral glia after nerve injury and repair. J Neuropathol Exp Neurol 1996; 55: 424-34.
60. Thomas PK. The connective tissue of peripheral nerve: an electron microscope study. J Anat 1963; 97: 35-44.
61. Corell M, Wicher G, Limbach C, Kilimann MW, Colman DR, Svenningsen AF. Spatiotemporal distribution and function of N-cadherin in postnatal Schwann cells: a matter of adhesion? J Neurosci Res 2010; 88: 2338-49.
62. Melendez-Vasquez CV, Rios JC, Zanazzi G, Lambert S, Bretscher A, Salzer JL. Nodes of Ranvier form in association with ezrin-radixin-moesin (ERM)-positive Schwann cell processes. Proc Natl Acad Sci U S A 2001; 98: 1235-40.
63. Antal EA, Loberg EM, Bracht P, Melby KK, Maehlen J. Evidence for intraaxonal spread of Listeria monocytogenes from the periphery to the central nervous system. Brain Pathol 2001; 11: 432-8.
64. Vazquez-Boland JA, Kuhn M, Berche P, Chakraborty T, Dominguez-Bernal G, Goebel W, Gonzalez-Zorn B, Wehland J, Kreft J. Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev 2001; 14: 584-640.
65. Alanne MH, Pummi K, Heape AM, Grenman R, Peltonen J, Peltonen S. Tight junction proteins in human Schwann cell autotypic junctions. J Histochem Cytochem 2009; 57: 523-9.
66. Spiegel I, Peles E. Cellular junctions of myelinated nerves. Mol Membr Biol 2002; 19: 95-101.
67. Johnson GC, Maddox CW, Fales WH, Wolff WA, Randle RF, Ramos JA, Schwartz H, Heise KM, Baetz AL, Wesley IV, Wagner DE. Epidemiologic evaluation of encephalitic listeriosis in goats. J Am Vet Med Assoc 1996; 208: 1695-9.
68. Jin Y, Dons L, Kristensson K, Rottenberg ME. Colony-stimulating factor 1-dependent cells protect against systemic infection with Listeria monocytogenes but facilitate neuroinvasion. Infect Immun 2002; 70: 4682-6.
69. Dramsi S, Levi S, Triller A, Cossart P. Entry of Listeria monocytogenes into neurons occurs by cell-to-cell spread: an in vitro study. Infect Immun 1998; 66: 4461-8.