Abstract
The olfactory ensheathing (glial) cells (OECs) have been identified to be useful candidate cells to support regeneration after being transplanted into injured fiber tracts of the central nervous system. We investigated by means of immunocytochemistry and freeze-fracturing the morphology and molecular composition of OEC tight junctions in the rat olfactory system. In addition, we tested the hypothesis whether tight junctions and orthogonal arrays of particles (OAPs) which contain the water channel protein aquaporin-4 (AQP4), are mutually exclusive as suggested in previous studies. In OECs, we found neither OAPs nor AQP4, but tight junctions immunoreactive for ZO-1, occludin, and claudin-5, but immunonegative for ZO-2 and claudin-3. To shed more light on the function of OEC tight junctions, we tested the permeability and tight junction composition of blood vessels and fila olfactoria. We found them both, permeable for infused lanthanum nitrate, and to be immunopositive for ZO-1 and claudin-5. The tight junctions of the OECs are discussed to be responsible for micro-compartmentalization within the olfactory fiber tract providing a benefit for axonal growth.
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Ablimit A, Matsuzaki T, Tajika Y, Aoki T, Hagiwara H, Takata K (2006) Immunolocalization of water channel aquaporins in the nasal olfactory mucosa. Arch Histol Cytol 69:1–12
Barnett SC, Chang L (2004) Olfactory ensheathing cells and CNS repair: going solo or in need of a friend? Trends Neurosci 27:54–60
Blinder KJ, Pumplin DW, Paul DL, Keller A (2003) Intercellular interactions in the mammalian olfactory nerve. J Comp Neurol 466:230–239
Bock P, Beineke A, Techangamsuwan S, Baumgärtner W, Wewetzer K (2007) Differential expression of HNK-1 and p75NTR in adult canine Schwann cells and olfactory ensheathing cells in situ but not in vitro. J Comp Neurol 505:572–585
Bokil H, Laaris N, Blinder K, Ennis M, Keller A (2001) Ephaptic interactions in the mammalian olfactory system. J Neurosci 21:173RC (1–5)
Dermietzel R (1973) Visualization by freeze-fracturing of regular structures in glial cell membranes. Naturwissenschaften 60:208
Endo M, Jain RK, Witwer B, Brown D (1999) Water channel (aquaporin-1) expression and distribution in mammary carcinomas and glioblastomas. Microvasc Res 58:89–98
Graziadei PP, Monti Graziadei GA (1985) Neurogenesis and plasticity of the olfactory sensory neurons. Ann NY Acad 457:127–142
Hussar P, Tserentsoodol N, Koyama H, Yokoo-Sugawara M, Matsuzaki T, Takami S, Takata K (2002) The glucose transporter GLUT1 and the tight junction protein occludin in nasal olfactory mucosa. Chem Senses 27:7–11
Iadecola C (2004) Neurovascular regulation in the normal brain and in Alzheimer’s disease. Nature Rev Neurosci 5:347–360
Imaizumi T, Lankford KL, Burton WV, Fodor WL, Kocsis JD (2000) Xenotransplantation of transgenic pig olfactory ensheathing cells promotes axonal regeneration in rat spinal cord. Nature Biotech 18:949–953
Jessen KR, Mirsky R (2005) The origin and development of glial cells in peripheral nerves. Nature Rev Neurosci 6:671–682
King LS, Kozono D, Agre P (2004) From structure to disease: the evolving tale of aquaporin biology. Nature Rev Mol Cell Biol 5:687–698
Li Y, Field PM, Raisman G (1997) Repair of adult rat corticospinal tract by transplants of olfactory ensheathing cells. Science 277:2000–2002
Li Y, Field PM, Raisman G (2005) Olfactory ensheathing cells and olfactory nerve fibroblasts maintain continuous open channels for regrowth of olfactory nerve fibres. Glia 52:245–251
Liebner S, Fischmann A, Rascher G, Duffner F, Grote E-H, Kalbacher H, Wolburg H (2000) Claudin-1 expression and tight junction morphology are altered in blood vessels of human glioblastoma multiforme. Acta Neuropathol 100:323–331
López-Vales R, Forés J , Navarro X, Verdú E (2007) Chronic transplantation of olfactory ensheathing cells promotes partial recovery after complete spinal cord transection in the rat. Glia 55:303–311
Lorenzo A (1992) Ultrastructural observations on blood vessels surrounding normal and regenerating spinal cord in newt. Ital J Anat Embryol 97:257–272
Mack A, Wolburg H (1986) Heterogeneity of glial membranes in the rat olfactory system as revealed by freeze-fracturing. Neurosci Lett 65:17–22
Mack A, Neuhaus J, Wolburg H (1987) Particular relationship between orthogonal arrays of particles and tight junctions as demonstrated in cells of the ventricular wall of the rat brain. Cell Tissue Res 248:619–625
Mack A F, Wolburg H (2006) Growing axons in fish optic nerve are accompanied by astrocytes interconnected by tight junctions. Brain Res 1103:25–31
Mackay-Sim A, Kittel P (1991) Cell dynamics in the adult mouse olfactory epithelium: a quantitative autoradiographic study. J Neurosci 11:979–984
Maunsbach AB, Marples D, Chin E, Ning G, Bondy C, Agre P, Nielsen S (1997) Aquaporin-1 water channel expression in human kidney. J Am Soc Nephrol 8:1–14
Menco BP (1988) Tight-junctional strands first appear in regions where three cells meet in differentiating olfactory epithelium: a freeze-fracture study. J Cell Sci 89:495–505
Miragall F (1983) Evidence for orthogonal arrays of particles in the plasma membranes of olfactory and vomeronasal sensory neurons of vertebrates. J Neurocytol 12:567–576
Miragall F, Krause D, De Vries U, Dermietzel R (1994) Expression of the tight junction protein ZO-1 in the olfactory system: presence of ZO-1 on olfactory sensory neurons and glial cells. J Comp Neurol 341:433–448
Miyamoto T, Morita K, Takemoto D, Takeuchi K, Kitano Y, Miyakawa T, Nakayama K, Okamura Y, Sasaki H, Miyachi Y, Furuse M, Tsukita S (2005) Tight junctions in Schwann cells of peripheral myelinated axons: a lesson from claudin-19-deficient mice. J Cell Biol 169:527–538
Morita K, Sasaki H, Furuse M, Tsukita S (1999) Endothelial claudin: claudin-5/TMVCF constitutes tight junction strands in endothelial cells. J Cell Biol 147:185–194
Nielsen S, Smith BL, Christensen EI, Agre P (1993) Distribution of the aquaporin CHIP in secretory and resorptive epithelial and capillary endothelia. Proc Natl Acad Sci USA 90:7275–7279
Pan W, Cain C, Yu Y, Kastin AJ (2006) Receptor-mediated transport of LIF across blood–spinal ciord barrier is upregulated after spinal cord injury. J Neuroimmunol 174:119–125
Piontek J, Winkler L, Wolburg H, Müller SL, Zuleger N, Piehl C, Wiesner B, Krause G, Blasig IE (2008) Formation of tight junction: determinants of homophilic interaction between classic claudins. FASEB J 22:146–158
Raisman G (2001) Olfactory ensheathing cells—another miracle cure for spinal cord injury? Nature Rev Neurosci 2:369–375
Rahner C, Mitic LL, Anderson JM (2001) Heterogeneity in expression and subcellular localization of claudins 2, 3, 4, and 5 in the rat liver, pancreas, and gut. Gastroeneterology 120:411–422
Ramón-Cueto A, Avila J (1998) Olfactory ensheathing glia: properties and function. Brain Res Bull 46:175–187
Rash JE, Davidson KGV, Yasumura T, Furman CS (2004) Freeze-fracture and immunogold analysis of aquaporin-4 (AQP4) square arrays, with models of AQP4 lattice assembly. Neuroscience 129:915–934
Rash JE, Davidson KGV, Kamasawa N, Yasumura T, Kawasama M, Zhang C, Michaels R, Restrepo D, Ottersen OP, Olson CO, Nagy JI (2005) Ultrastructural localization of connexins (Cx36, Cx43, Cx45), glutamate receptors and aquaporin-4 in rodent olfactory mucosa, olfactory nerve and olfactory bulb. J Neurocytol 34:307–341
Risling M, Lindao H, Cullheim S, Franson P (1989) A persistent defect in the blood–brain barrier after ventral funiculus lesion in adult cats: implications for CNS regeneration? Brain Res 494:13–21
Risling M, Fried K, Lindå H, Carlstedt T, Cullheim S (1993) Regrowth of motor axons following spinal cord lesions: distribution of laminin and collagen in the CNS scar tissue. Brain Res Bull 30:405–414
Simard M, Nedergaard M (2004) The neurobiology of glia in the context of water and water homeostasis. Neuroscience 129:877–896
Speake T, Freeman LJ, Brown PD (2003) Expression of aquaporin 1 and aquaporin 4 water channels in rat choroid plexus. Biochim Biophys Acta 1609:80–86
Verkman AS (2002) Aquaporin water channels and endothelial cell function. J Anat 200:617–627
Wewetzer K, Verdu E, Angelov DN, Navarro X (2002) Olfactory ensheathing glia and Schwann cells: two of a kind? Cell Tissue Res 309:337–45
Wolburg H (1995) Orthogonal arrays of intramembranous particles: a review with special reference to astrocytes. J Brain Res 36:239–258
Wolburg H (2006) The endothelial frontier. In: Dermietzel R, Spray DC, Nedergaard M (eds) Blood–brain barriers. From ontogeny to artificial interfaces. Wiley-VCH Weinheim pp 77–107
Wolburg H, Kästner R (1984) Astroglial–axonal interrelationship during regeneration of the optic nerve in goldfish. J Hirnforsch 25:493–504
Wolburg H, Kästner R, Kurz-Isler G (1983) Lack of orthogonal particle assemblies and presence of tight junctions in astrocytes of the goldfish (Carassius auratus). A freeze-fracture study. Cell Tissue Res 234:389–402
Wolburg H, Neuhaus J, Mack A (1986) The glio-axonal interaction and the problem of regeneration of axons in the central nervous system–concept and perspectives. Z Naturforsch 41c:1147–1155
Wolburg H, Wolburg-Buchholz K, Kraus J, Rascher-Eggstein G, Liebner S, Hamm S, Duffner F, Grote E-H, Risau W, Engelhardt B (2003) Localization of claudin-3 in tight junctions of the blood–brain barrier is selectively lost during experimental autoimmune encephalomyelitis and human glioblastoma multiforme. Acta Neuropathol 105:586–592
Xiang S, Pan W, Kastin AJ (2005) Strategies to create a regenerating environment for the injured spinal cord. Curr Pharm Des 11:1267–1277
Acknowledgments
This study was supported by a grant of the Hertie-foundation (grant number 1.01.1/07/003) to HW and KW-B. The skilful technical assistance of A. Adam (immunohistochemistry), E.-M. Knittel (freeze-fracturing), and G. Frommer-Kästle (ultrathin sections) is gratefully acknowledged.
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Wolburg, H., Wolburg-Buchholz, K., Sam, H. et al. Epithelial and endothelial barriers in the olfactory region of the nasal cavity of the rat. Histochem Cell Biol 130, 127–140 (2008). https://doi.org/10.1007/s00418-008-0410-2
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DOI: https://doi.org/10.1007/s00418-008-0410-2