Ultrastructural study of the primary olfactory pathway in Macaca fascicularis

Journal of Comparative Neurology

Volumn 488, Issue 4, 2005, Pages 427-441

  Herrera, Loren P ^a   Casas, Carlos E ^a   Bates, Margaret L ^a   Guest, James D ^a,b  

^a UNIVERSITY OF MIAMI   (United States)

^b UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

Astrocytes; Fibroblasts; Fila olfactoria; Lamina propria; Non human primates; Olfactory bulb; Olfactory ensheathing cells; Perineurium; Schwann cells; Ultrastructure

Indexed keywords

ANIMAL CELL; ARTICLE; ASTROCYTE; BASAL CELL; CELL INTERACTION; CELL TRANSPLANTATION; FIBROBLAST; GLOMERULUS; LAMINA PROPRIA; MACACA; NERVE FIBER; NERVE FIBER GROWTH; NONHUMAN; OLFACTORY BULB; OLFACTORY ENSHEATHING CELL; OLFACTORY EPITHELIUM; OLFACTORY NERVOUS SYSTEM; PRIMATE; PRIORITY JOURNAL; TRANSMISSION ELECTRON MICROSCOPY;

ANIMALS; AXONS; INTERCELLULAR JUNCTIONS; MACACA FASCICULARIS; NEUROGLIA; OLFACTORY BULB; OLFACTORY MUCOSA; OLFACTORY PATHWAYS; OLFACTORY RECEPTOR NEURONS;

EID: 21644472682     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.20588     Document Type: Article

References (60)

1. Allison AC. 1953. The structure of the olfactory bulb and its relationship to the olfactory pathways in the rabbit and the rat. J Comp Neurol 98:309-353.
2. Au E, Roskams AJ. 2002. Culturing olfactory ensheathing glia from the mouse olfactory epithelium. Methods Mol Biol 198:49-54.
3. Au E, Roskams AJ. 2003. Olfactory ensheathing cells of the lamina propria in vivo and in vitro. Glia 41:224-236.
4. Au WW, Treloar HB, Greer CA. 2002. Sublaminar organization of the mouse olfactory bulb nerve layer. J Comp Neurol 446:68-80.
5. Bannister LH, Dodson HC. 1992. Endocytic pathways in the olfactory and vomeronasal epithelia of the mouse: ultrastructure and uptake of tracers. Microsc Res Tech 23:128-141.
6. Bartolomei JC, Greer CA. 2000. Olfactory ensheathing cells: bridging the gap in spinal cord injury. Neurosurgery 47:1057-1069.
7. Boyd JG, Lee J, Skihar V, Doucette R, Kawaja MD. 2004. LacZ-expressing olfactory ensheathing cells do not associate with myelinated axons after implantation into the compressed spinal cord. Proc Natl Acad Sci U S A 101:2162-2166.
8. Carlstedt T. 1977. Observations on the morphology at the transition between the peripheral and the central nervous system in the cat. IV. Unmyelinated fibres in S1 dorsal rootlets. Acta Physiol Scand Suppl 446:61-72.
9. Carlstedt T. 1985. Regenerating axons form nerve terminals at astrocytes. Brain Res 347:188-191.
10. Carlstedt T. 1997. Nerve fibre regeneration across the peripheral-central transitional zone. J Anat 190:51-56.
11. Chuah MI, Au C. 1991. Olfactory Schwann cells are derived from precursor cells in the olfactory epithelium. J Neurosci Res 29:172-180.
12. Doucette JR. 1986. Astrocytes in the olfactory bulb. In: Fedoroff S, Vernadakis A, editors. Astrocytes: development, morphology, and regional specialization, 1st ed. Orlando, FL: Academic Press, p 293-310.
13. Doucette R. 1991. PNS-CNS transitional zone of the first cranial nerve. J Comp Neurol 312:451-466.
14. Doucette R. 1993. Glial cells in the nerve fiber layer of the main olfactory bulb of embryonic and adult mammals. Microsc Res Tech 24:113-130.
15. Doucette R. 1995. Olfactory ensheathing cells: potential for glial cell transplantation into areas of CNS injury. Histol Histopathol 10:503-507.
16. Doucette R. 1996. Immunohistochemical localization of laminin, fibronectin and collagen type IV in the nerve fiber layer of the olfactory bulb. Int J Dev Neurosci 14:945-959.
17. Field P, Li Y, Raisman G. 2003. Ensheathment of the olfactory nerves in the adult rat. J Neurocytol 32:317-324.
18. Fraher JP. 1999. The transitional zone and CNS regeneration. J Anat 194:161-182.
19. Fraher JP. 2000. The transitional zone and CNS regeneration. J Anat 196:137-158.
20. Franklin RJ. 2002. Obtaining olfactory ensheathing cells from extracanial sources: a step closer to clinical transplant-mediated repair of the CNS? Brain 125:2-3.
21. Franklin RJ. 2003. Remyelination by transplanted olfactory ensheathing cells. Anat Rec 271B:71-76.
22. Gamble HJ, Eames RA. 1964. An electron microscope study of the connective tissues of human peripheral nerve. J Anat 98:655-663.
23. Gomez VM, Averill S, King V, Yang Q, Perez ED, Chacon SC, Ward R, Nieto-Sampedro M, Priestley J, Taylor J. 2003. Transplantation of olfactory ensheathing cells fails to promote significant axonal regeneration from dorsal roots into the rat cervical cord. J Neurocytol 32:53-70.
24. Graziadei PP, Karlan MS, Graziadei GA, Bernstein JJ. 1980. Neurogenesis of sensory neurons in the primate olfactory system after section of the fila olfactoria. Brain Res 186:289-300.
25. Gudino-Cabrera G, Pastor AM, de la Cruz RR, Delgado-Garcia JM, Nieto-Sampedro M. 2000. Limits to the capacity of transplants of olfactory glia to promote axonal regrowth in the CNS. Neuroreport 11:467-471.
26. Herrera L, Cases C, Bates M, Guest JD. 2004. Ultrastructural study of the olfactory pathway in Macaca fascicularis. Soc Neurosci Abstr.67.1.
27. Hirose T, Sano T, Hizawa K. 1986. Ultrastructural localization of S-100 protein in neurofibroma. Acta Neuropathol (Berl) 69:103-110.
28. Jafek BW. 1983. Ultrastructure of human nasal mucosa. Laryngoscope 93:1576-1599.
29. Jani HR, Raisman G. 2004. Ensheathing cell cultures from the olfactory bulb and mucosa. Glia 47:130-137.
30. Joseph NM, Mukouyama YS, Mosher JT, Jaegle M, Crone SA, Dormand EL, Lee KF, Meijer D, Anderson DJ, Morrison SJ. 2004. Neural crest stem cells undergo multilineage differentiation in developing peripheral nerves to generate endoneurial fibroblasts in addition to Schwann cells. Development 131:5599-5612.
31. Kafitz KW, Greer CA. 1998. Differential expression of extracellular matrix and cell adhesion molecules in the olfactory nerve and glomerular layers of adult rats. J Neurobiol 34:271-282.
32. Kasowski HJ, Kim H, Greer CA. 1999. Compartmental organization of the olfactory bulb glomerulus. J Comp Neurol 407:261-274.
33. Kato T, Honmou O, Uede T, Hashi K, Kocsis JD. 2000. Transplantation of human olfactory ensheathing cells elicits remyelination of demyelinated rat spinal cord. Glia 30:209-218.
34. Lakatos A, Barnett SC, Franklin RJ. 2003a. Olfactory ensheathing cells induce less host astrocyte response and chondroitin sulphate proteoglycan expression than Schwann cells following transplantation into adult CNS white matter. Exp Neurol 184:237-246.
35. Lakatos A, Smith PM, Barnett SC, Franklin RJ. 2003b. Meningeal cells enhance limited CNS remyelination by transplanted olfactory ensheathing cells. Brain 126:598-609.
36. Leopold DA, Hummel T, Schwob JE, Hong SC, Knecht M, Kobal G. 2000. Anterior distribution of human olfactory epithelium. Laryngoscope 110:417-421.
37. Li Y, Field PM, Raisman G. 1998. Regeneration of adult rat corticospinal axons induced by transplanted olfactory ensheathing cells. J Neurosci 18:10514-10524.
38. Li Y, Decherchi P, Raisman G. 2003a. Transplantation of olfactory ensheathing cells into spinal cord lesions restores breathing and climbing. J Neurosci 23:727-731.
39. Li Y, Sauve Y, Li D, Lund RD, Raisman G. 2003b. Transplanted olfactory ensheathing cells promote regeneration of cut adult rat optic nerve axons. J Neurosci 23:7783-7788.
40. Li Y, Carlstedt T, Berthold CH, Raisman G. 2004. Interaction of transplanted olfactory-ensheathing cells and host astrocytic processes provides a bridge for axons to regenerate across the dorsal root entry zone. Exp Neurol 188:300-308.
41. Liss L. 1956. The histology of the human olfactory bulb and the extracerebral part of the tract; a study with silver-carbonate. Ann Otol Rhinol Laryngol 65:680-691.
42. Lu J, Feron F, Mackay-Sim A, Waite PM. 2002. Olfactory ensheathing cells promote locomotor recovery after delayed transplantation into transected spinal cord. Brain 125:14-21.
43. Miller LA, Plopper CG, Hyde DM, Gerriets JE, Pieczarka EM, Tyler NK, Evans MJ, Gershwin LJ, Schelegle ES, Van Winkle LS. 2003. Immune and airway effects of house dust mite aeroallergen exposures during postnatal development of the infant rhesus monkey. Clin Exp Allergy 33:1686-1694.
44. Morrison EE, Costanzo RM. 1990. Morphology of the human olfactory epithelium. J Comp Neurol 297:1-13.
45. Ogasawara N. 1954. Histological study of olfactory bulb in man. Tohoku J Exp Med 59:357-369.
46. Peltonen J, Jaakkola S, Virtanen I, Pelliniemi L. 1987. Perineurial cells in culture. An immunocytochemical and electron microscopic study. Lab Invest 57:480-488.
47. Radtke C, Akiyama Y, Brokaw J, Lankford KL, Wewetzer K, Fodor WL, Kocsis JD. 2004. Remyelination of the nonhuman primate spinal cord by transplantation of H-transferase transgenic adult pig olfactory ensheathing cells. FASEB J 18:335-337.
48. Raisman G. 1985. Specialized neuroglial arrangement may explain the capacity of vomeronasal axons to reinnervate central neurons. Neuroscience 14:237-254.
49. Ramer LM, Richter MW, Roskams AJ, Tetzlaff W, Ramer MS. 2004. Peripherally-derived olfactory ensheathing cells do not promote primary afferent regeneration following dorsal root injury. Glia 47:189-206.
50. Ramon-Cueto A, Avila J. 1998. Olfactory ensheathing glia: properties and function. Brain Res Bull 46:175-187.
51. Ramon-Cueto A, Nieto-Sampedro M. 1992. Glial cells from adult rat olfactory bulb: immunocytochemical properties of pure cultures of ensheathing cells. Neuroscience 47:213-220.
52. Ramon-Cueto A, Nieto-Sampedro M. 1994. Regeneration into the spinal cord of transected dorsal root axons is promoted by ensheathing glia transplants. Exp Neurol 127:232-244.
53. Ramon-Cueto A, Perez J, Nieto-Sampedro M. 1993. In vitro enfolding of olfactory neurites by p75 NGF receptor positive ensheathing cells from adult rat olfactory bulb. Eur J Neurosci 5:1172-1180.
54. Ramon-Cueto A, Cordero MI, Santos-Benito FF, Avila J. 2000. Functional recovery of paraplegic rats and motor axon regeneration in their spinal cords by olfactory ensheathing glia. Neuron 25:425-435.
55. Schaefer ML, Bottger B, Silver WL, Finger TE. 2002. Trigeminal collaterals in the nasal epithelium and olfactory bulb: a potential route for direct modulation of olfactory information by trigeminal stimuli. J Comp Neurol 444:221-226.
56. Schwob JE. 2002. Neural regeneration and the peripheral olfactory system. Anat Rec 269:33-49.
57. Takami T, Oudega M, Bates ML, Wood PM, Kleitman N, Bunge MB. 2002. Schwann cell but not olfactory ensheathing glia transplants improve hindlimb locomotor performance in the moderately contused adult rat thoracic spinal cord. J Neurosci 22:6670-6681.
58. Thomas P, Olsson Y. 1984. Microscopic anatomy and function of the connective tissue components of peripheral nerve. In: Dyck P, Thomas P, Lambert E, Bunge RP, editors. Peripheral neuropathy. Philadelphia: WB Saunders. p 97-120.
59. Wang GY, Hirai K, Shimada H, Taji S, Zhong SZ. 1992. Behavior of axons, Schwann cells and perineurial cells in nerve regeneration within transplanted nerve grafts: effects of anti-laminin and anti-fibronectin antisera. Brain Res 583:216-226.
60. Williams SK, Franklin RJ, Barnett SC. 2004. Response of olfactory ensheathing cells to the degeneration and regeneration of the peripheral olfactory system and the involvement of the neuregulins. J Comp Neurol 470:50-62.