Prenatal development of NMDA receptor composition and function in trigeminal neurons

Archives of Histology and Cytology

Volumn 68, Issue 4, 2005, Pages 321-335

  Ishihama, Kohji ^a,b   Kogo, Mikihiko ^a   Wakisaka, Satoshi ^a   Turman Jr , Jack E ^b,c,d  

^a OSAKA UNIVERSITY   (Japan)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^d UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 3A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 3B; N METHYL DEXTRO ASPARTIC ACID RECEPTOR STIMULATING AGENT; RECEPTOR SUBUNIT; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN STEM; CONTROLLED STUDY; EMBRYO DEVELOPMENT; FETUS; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; IN VITRO STUDY; JAW MOVEMENT; MESENCEPHALON; MOTONEURON; NONHUMAN; PRENATAL DEVELOPMENT; PROTEIN ANALYSIS; PROTEIN FUNCTION; RAT; SUCKING; TRIGEMINAL NERVE;

ANIMALS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; MESENCEPHALON; N-METHYLASPARTATE; NEURONS; PROTEIN SUBUNITS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; TRIGEMINAL NERVE;

EID: 33244467213     PISSN: 09149465     EISSN: 13491717     Source Type: Journal    
DOI: 10.1679/aohc.68.321     Document Type: Article

References (89)

1. Abercrombie M: Estimation of nuclear population from microtome sections. Anat Rec 94: 239-247 (1946).
2. Bae YC, Park KP, Yoshida A, Nakagawa S, Kurata S, Chen K, Takemura M, Shigenaga Y: Identification of gamma-aminobutyric acid-immunoreactive axon endings associated with mesencephalic periodontal afferent terminals and morphometry of the two types of terminals in the cat supratrigeminal nucleus. J Comp Neurol 389: 127-138 (1997).
3. Barria A, Malinow R: Subunit-specific NMDA receptor trafficking to synapses. Neuron 35: 345-353 (2002).
4. Blahos J 2nd, Wenthold RJ: Relationship between N-methyl-D-aspartate receptor NR1 splice variants and NR2 subunits. J Biol Chem 271: 15669-15674 (1996).
5. Brose N, Gasic GP, Vetter DE, Sullivan JM, Heinemann SF: Protein chemical characterization and immunocytochemical localization of the NMDA receptor subunit NMDA R1. J Biol Chem 268: 22663-22671 (1993).
6. Carmignoto G, Vicini S: Activity-dependent decrease in NMDA receptor responses during development of the visual cortex. Science 258: 1007-1011 (1992).
7. Chatterton JE, Awobuluyi M, Premkumar LS, Takahashi H, Talantova M, Shin Y, Cui J, Tu S, Sevarino KA, Nakanishi N, Tong G, Lipton SA, Zhang D: Excitatory glycine receptors containing the NR3 family of NMDA receptor subunits. Nature 415: 793-798 (2002).
8. Chazot PL, Coleman SK, Cik M, Stephenson FA: Molecular characterization of N-methyl-D-aspartate receptors expressed in mammalian cells yields evidence for the coexistence of three subunit types within a discrete receptor molecule. J Biol Chem 269: 24403-24409 (1994).
9. Ciabarra AM, Sullivan JM, Gahn LG, Pecht G, Heinemann S, Sevarino KA: Cloning and characterization of chi-1: a developmentally regulated member of a novel class of ionotropic glutamate receptor family. J Neurosci 15: 6498-6508 (1995).
10. Clements JD, Westbrook GL: Activation kinetics reveal the number of glutamate and glycine binding sites on the N-methyl-D-aspartate receptor. Neuron 7: 605-613 (1991).
11. Copray JC, Liem RS, Ter Horst GJ, and Van Willigen JD: Dopaminergic afferents to the mesencephalic trigeminal nucleus of the rat: a light and electron microscope immunocytochemistry study. Brain Res 514: 343-348 (1990).
12. Cull-Candy S, Brickley S, Farrant M: NMDA receptor subunits: diversity, development and disease. Curr Opin Neurobiol 11: 327-335 (2001).
13. Das S, Sasaki YF, Rothe T, Premkumar LS, Takasu M, Crandall JE, Dikkes P, Conner DA, Rayudu PV, Cheung W, Chen HS, Lipton SA, Nakanishi N: Increased NMDA current and spine density in mice lacking the NMDA receptor subunit NR3A. Nature 393: 377-381 (1998).
14. Enomoto A, Kogo M, Koizumi H, Ishihama K, Yamanishi T: Localization of premotoneurons for an NMDA-induced repetitive rhythmical activity to TMNs. Neuroreport 13: 2303-2307 (2002).
15. Flatman JA, Schwindt PC, Crill WE, Stafstrom CE: Multiple actions of N-methyl-D-aspartate on cat neocortical neurons in vitro. Brain Res 266: 169-173 (1983).
16. Flint AC, Maisch US, Weishaupt JH, Kriegstein AR, Monyer H: NR2A subunit expression shortens NMDA receptor synaptic currents in developing neocortex. J Neurosci 17: 2469-2476 (1997).
17. Fukaya M, Hayashi Y, Watanabe M: NR2 to NR3B subunit switchover of NMDA receptors in early postnatal motoneurons. Eur J Neurosci 21: 1432-1436 (2005).
18. Gabbott PL, Somogyi J, Stewart MG, Hamori J: GABA-immunoreactive neurons in the rat cerebellum: a light and electron microscope study. J Comp Neurol 251: 474-490 (1986).
19. Greer JJ, Smith JC, Feldman JL: Role of excitatory amino acids in the generation and transmission of respiratory drive in neonatal rat. J Physiol 437: 727-749 (1991).
20. Greer JJ, Smith JC, Feldman JL: Respiratory and locomotor patterns generated in the fetal rat brain stem-spinal cord in vitro. J Neurophysiol 67: 996-999 (1992).
21. Guillery RW, Herrup K: Quantification without pontification: choosing a method for counting objects in sectioned tissues. J Comp Neurol 386: 2-7 (1997).
22. Hawkins LM, Chazot PL, Stephenson FA: Biochemical evidence for the co-association of three N-methyl-D-aspartate (NMDA) R2 subunits in recombinant NMDA receptors. J Biol Chem 274: 27211-27218 (1999).
23. Hirai H, Kirsch J, Laube B, Betz H, Kuhse J: The glycine binding site of the N-methyl-D-aspartate receptor subunit NR1: identification of novel determinants of co-agonist potentiation in the extracellular M3-M4 loop region. Proc Natl Acad Sci USA 93: 6031-6036 (1996).
24. Hsu SM, Raine L, Fanger H: The use of antiavidin antibody and avidin-biotin-peroxidase complex in immunoperoxidase technics. Am J Clin Pathol 75: 816-821 (1981).
25. Iinuma M, Yoshida S, Funakoshi M: A role of periodontal sensation in development of rhythmical chewing in dogs. Comp Biochem Physiol 107A (2): 389-395 (1994).
26. Ikeda K, Nagasawa M, Mori H, Araki K, Sakimura K, Watanabe M, Inoue Y, Mishina M: Cloning and expression of the epsilon 4 subunit of the NMDA receptor channel. FEBS Lett 313: 34-38 (1992).
27. Ishihama K, Kogo M, Koizumi H, Nomura K, Tanaka S, Yamanishi T, Enomoto A: Oral-motor patterns of rhythmic trigeminal activity generated in fetal rat brainstem in vitro. Dev Brain Res 145: 163-166 (2003).
28. Ishihama K, Turman JE Jr: Prenatal development of NMDA receptor subunits in rat trigeminal neurons. Soc Neurosci Abstr. (2004)
29. Ishii T, Moriyoshi K, Sugihara H, Sakurada K, Kadotani H, Yokoi M, Akazawa C, Shigemoto R, Mizuno N, Masu M: Molecular characterization of the family of the N-methyl-D-aspartate receptor subunits. J Biol Chem 268: 2836-2843 (1993).
30. Jacquin MF, Rhoades RW, Enfiejian HL, Egger MD: Organization and morphology of masticatory neurons in the rat: a retrograde HRP study. J Comp Neurol 218: 239-256 (1983).
31. Johnson JW, Ascher P: Glycine potentiates the NMDA response in cultured mouse brain neurons. Nature 325: 529-531 (1987).
32. Katakura N, Jia L, Nakamura Y: NMDA-induced rhythmical activity in XII nerve of isolated CNS from newborn rats. Neuroreport 6: 601-604 (1995).
33. Kim YI, Chandler SH: NMDA-induced burst discharge in guinea pig trigeminal motoneurons in vitro. J Neurophysiol 74: 334-346 (1995).
34. Kobayashi K, Lemke RP, Greer JJ: Ultrasound measurements of fetal breathing movements in the rat. J Appl Physiol 91: 316-320 (2001).
35. Kogo M, Funk GD, Chandler SH: Rhythmical oral-motor activity recorded in an in vitro brainstem preparation. Somatosens Mot Res 13: 39-48 (1996).
36. Kogo M, Tanaka S, Chandler SH, Matsuya T: Examination of the relationships between jaw opener and closer rhythmical muscle activity in an in vitro brainstem jaw-attached preparation. Somatosens Mot Res 15: 200-210 (1998).
37. Koizumi H, Ishihama K, Nomura K, Yamanishi T, Kogo M, Matsuya T: Differential discharge patterns of rhythmical activity in trigeminal motoneurons during fictive mastication and respiration in vitro. Brain Res Bull 58: 129-133 (2002).
38. Kuryatov A, Laube B, Betz H, Kuhse J: Mutational analysis of the glycine-binding site of the NMDA receptor: structural similarity with bacterial amino acid-binding proteins. Neuron 12: 1291-1300 (1994).
39. Kutsuwada T, Kashiwabuchi N, Mori H, Sakimura K, Kushiya E, Araki K, Meguro H, Masaki H, Kumanishi T, Arakawa M: Molecular diversity of the NMDA receptor channel. Nature 358: 36-41 (1992).
40. Kutsuwada T, Sakimura K, Manabe T, Takayama C, Katakura N, Kushiya E, Natsume R, Watanabe M, Inoue Y, Yagi T, Aizawa S, Arakawa M, Takahashi T, Nakamura Y, Mori H, Mishina M: Impairment of suckling response, trigeminal neuronal pattern formation, and hippocampal LTD in NMDA receptor epsilon 2 subunit mutant mice. Neuron 16: 333-344 (1996).
41. Laube B, Hirai H, Sturgess M, Betz H, Kuhse J: Molecular determinants of agonist discrimination by NMDA receptor subunits: analysis of the glutamate binding site on the NR2B subunit. Neuron 18: 493-503 (1997).
42. Laube B, Kuhse J, Betz H: Evidence for a tetrameric structure of recombinant NMDA receptors. J Neurosci 18: 2954-2961 (1998).
43. Lazarov NE: Comparative analysis of the chemical neuroanatomy of the mammalian trigeminal ganglion and mesencephalic trigeminal nucleus. Prog Neurobiol 66: 19-59 (2002).
44. Lester RA, Clements JD, Westbrook GL, Jahr CE: Channel kinetics determine the time course of NMDA receptor-mediated synaptic currents. Nature 346: 565-567 (1990).
45. Liu XB, Murray KD, Jones EG: Switching of NMDA receptor 2A and 2B subunits at thalamic and cortical synapses during early postnatal development. J Neurosci 24: 8885-8895 (2004).
46. Lopez de Armentia M, Sah P: Development and subunit composition of synaptic NMDA receptors in the amygdala: NR2B synapses in the adult central amygdala. J Neurosci 23: 6876-6883 (2003).
47. Lund JP, Kolta A, Westberg KG, Scott G: Brainstem mechanisms underlying feeding behaviors. Curr Opin Neurobiol 8: 718-724 (1998).
48. Lynch R: A qualitative investigation of the topographical representation of masticatory muscles within the motor trigeminal nucleus of the rat: a horseradish peroxidase study. Brain Res 327: 354-358 (1985).
49. MacDermott AB, Mayer ML, Westbrook GL, Smith SJ, Barker JL: NMDA-receptor activation increases cytoplasmic calcium concentration in cultured spinal cord neurones. Nature 321: 519-522 (1986).
50. Malenka RC, Kauer JA, Ferkel DJ, Mauk MD, Kelly PT, Nicoll RA, Waxham MN: An essential role for postsynaptic calmodulin and protein kinase activity in long-term potentiation. Nature 340: 554-557 (1989).
51. Matsuda K, Kamiya Y, Matsuda S, Yuzaki M: Cloning and characterization of a novel NMDA receptor subunit NR3B: a dominant subunit that reduces calcium permeability. Mol Brain Res 100: 43-52 (2002).
52. 2+ of NMDA responses in spinal cord neurones. Nature 309: 261-263 (1984).
53. Meguro H, Mori H, Araki K, Kushiya E, Kutsuwada T, Yamazaki M, Kumanishi T, Arakawa M, Sakimura K, Mishina: Functional characterization of a heteromeric NMDA receptor channel expressed from cloned cDNAs. Nature 357: 70-74 (1992).
54. Miller JL, Sonies BC, Macedonia C: Emergence of oropharyngeal, laryngeal and swallowing activity in the developing fetal upper aerodigestive tract: an ultrasound evaluation. Early Hum Dev 71: 61-87 (2003).
55. Monyer H, Sprengel R, Schoepfer R, Herb A, Higuchi M, Lomeli H, Burnashev N, Sakmann B, Seeburg PH: Heteromeric NMDA receptors: molecular and functional distinction of subtypes. Science 256: 1217-1221 (1992).
56. Monyer H, Burnashev N, Laurie DJ, Sakmann B, Seeburg PH: Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12: 529-540 (1994).
57. Mori H and Mishina M: Structure and function of the NMDA receptor channel. Neuropharmacology 34: 1219-1237 (1995).
58. Nakamura Y, Katakura N, Nakajima M: Generation of rhythmical ingestive activities of the trigeminal, facial, and hypoglossal motoneurons in in vitro CNS preparations isolated from rats and mice. J Med Dent Sci 46: 63-73 (1999).
59. Narayanan CH, Fox MW, Hamburger V: Prenatal development of spontaneous and evoked activity in the rat (Rattus norvegicus albinus). Behaviour 40: 100-134 (1971).
60. Nishi M, Hinds H, Lu HP, Kawata M, Hayashi Y: Motoneuron-specific expression of NR3B, a novel NMDA-type glutamate receptor subunit that works in a dominant-negative manner. J Neurosci 21: RC185 (1-6) (2001).
61. Nowak L, Bregestovski P, Ascher P, Herbet A, Prochiantz A: Magnesium gates glutamate-activated channels in mouse central neurones. Nature 307: 462-465 (1984).
62. Oshima S, Fukaya M, Masabumi N, Shirakawa T, Oguchi H, Watanabe M: Early onset of NMDA receptor GluR epsilon 1 (NR2A) expression and its abundant postsynaptic localization in developing motoneurons of the mouse hypoglossal nucleus. Neurosci Res 43: 239-250 (2002).
63. Patneau DK, Mayer ML: Structure-activity relationships for amino acid transmitter candidates acting at N-methyl-D-aspartate and quisqualate receptors. J Neurosci 10: 2385-2399 (1990).
64. rd ed. Academic Press. San Diego, 1997.
65. Pérez-Otaño I, Schulteis CT, Contractor A, Lipton SA, Trimmer JS, Sucher NJ, Heinemann SF: Assembly with the NR1 Subunit Is Required for Surface Expression of NR3A-Containing NMDA Receptors. J Neurosci 21: 1228-1237 (2991).
66. Priestley T, Laughton P, Myers J, Le Bourdelles B, Kerby J, Whiting PJ: Pharmacological properties of recombinant human N-methyl-D-aspartate receptors comprising NR1a/NR2A and NR1a/NR2B subunit assemblies expressed in permanently transfected mouse fibroblast cells. Mol Pharmacol 48: 841-848 (1995).
67. Quinlan EM, Olstein DH, Bear MF: Bidirectional, experience-dependent regulation of N-methyl-D-aspartate receptor subunit composition in the rat visual cortex during postnatal development. Proc Natl Acad Sci USA 96: 12876-12880 (1999).
68. Roche KW, Tingley WG, Huganir RL: Glutamate receptor phosphorylation and synaptic plasticity. Curr Opin Neurobiol 4: 383-388 (1994).
69. Sasaki YF, Rothe T, Premkumar LS, Das S, Cui J, Talantova MV, Wong HK, Gong X, Chan SF, Zhang D, Nakanishi N, Sucher NJ, Lipton SA: Characterization and comparison of the NR3A subunit of the NMDA receptor in recombinant systems and primary cortical neurons. J Neurophysiol 87: 2052-2063 (2002).
70. Schmidt BJ, Hochman S, MacLean JN: NMDA receptor-mediated oscillatory properties: potential role in rhythm generation in the mammalian spinal cord. Ann NY Acad Sci 860: 189-202 (1998).
71. Schwindt P, Crill W: Role of a persistent inward current in motoneuron bursting during spinal seizures. J Neurophysiol 43: 1296-1318 (1980).
72. Sheng M, Cummings J, Roldan LA, Jan YN, Jan LY: Changing subunit composition of heteromeric NMDA receptors during development of rat cortex. Nature 368: 144-147 (1994).
73. Smith TG Jr, Barker JL, Gainer H: Requirements for bursting pacemaker potential activity in molluscan neurones. Nature 253: 450-452 (1975).
74. Sucher NJ, Akbarian S, Chi CL, Leclerc CL, Awobuluyi M, Deitcher DL, Wu MK, Yuan JP, Jones EG, Lipton SA: Developmental and regional expression pattern of a novel NMDA receptor-like subunit (NMDAR-L) in the rodent brain. J Neurosci 15: 6509-6520 (1995).
75. Tanaka S, Kogo M, Chandler SH, Matsuya T: Localization of oral-motor rhythmogenic circuits in the isolated rat brainstem preparation. Brain Res 821: 190-199 (1999).
76. Tovar KR, Westbrook GL: The incorporation of NMDA receptors with a distinct subunit composition at nascent hippocampal synapses in vitro. J Neurosci 19: 4180-4188 (1999).
77. Tovar KR, Sprouffske K, Westbrook GL: Fast NMDA receptor-mediated synaptic currents in neurons from mice lacking the epsilon2 (NR2B) subunit. J Neurophysiol 83: 616-620 (2000).
78. Townsend M, Yoshii A, Mishina M, Constantine-Paton M: Developmental loss of miniature N-methyl-D-aspartate receptor currents in NR2A knockout mice. Proc Natl Acad Sci USA 100: 1340-1345 (2003).
79. Turman JE Jr, Ajdari J, Chandler SH: NMDA receptor NR1 and NR2A/B subunit expression in trigeminal neurons during early postnatal development. J Comp Neurol 409: 237-249 (1999).
80. Turman JE Jr, MacDonald AS, Pawl KE, Bringas P, Chandler SH: AMPA receptor subunit expression in trigeminal neurons during postnatal development. J Comp Neurol 427: 109-123 (2000).
81. Turman JE Jr, Hiyama L, Castillo M, Chandler SH: Expression of group I and II metabotropic glutamate receptors in trigeminal neurons during postnatal development. Dev Neurosci 23: 41-54 (2001).
82. Turman JE Jr, Lee OK, Chandler SH: Differential NR2A and NR2B expression between trigeminal neurons during early postnatal development. Synapse 44: 76-85 (2002).
83. Verdier D, Lund JP, Kolta A: Synaptic inputs to trigeminal primary afferent neurons cause firing and modulate intrinsic oscillatory activity. J Neurophysiol 92: 2444-2455 (2004).
84. Vicini S, Wang JF, Li JH, Zhu WJ, Wang YH, Luo JH, Wolfe BB, Grayson DR: Functional and pharmacological differences between recombinant N-methyl-D-aspartate receptors. J Neurophysiol 79: 555-566 (1998).
85. Watanabe M, Inoue Y, Sakimura K, Mishina M: Developmental changes in distribution of NMDA receptor channel subunit mRNAs. Neuroreport 3: 1138-1140 (1992).
86. Westneat MW, Hall WG: Ontogeny of feeding motor patterns in infant rats: an electromyographic analysis of suckling and chewing. Behav Neurosci 106: 539-554 (1992).
87. Wilson WA, Wachtel H: Negative resistance characteristic essential for the maintenance of slow oscillations in bursting neurons. Science 186: 932-934 (1974).
88. Zhang JD, Yoshida A, Shigenaga Y: Ultrastractural analysis of inputs around the soma of an intra-cellularly labeled masseter muscle spindle afferent in cat mesencephalic trigeminal nucleus. J Hirnforsch 38: 495-502 (1997).
89. Zucker RS: Calcium- and activity-dependent synaptic plasticity. Curr.Opin.Neurobiol 9: 305-313 (1999).