NELL2, a neuron-specific EGF-like protein, is selectively expressed in glutamatergic neurons and contributes to the glutamatergic control of GnRH neurons at puberty

Neuroendocrinology

Volumn 88, Issue 3, 2008, Pages 199-211

  Ha, Chang Man ^a   Choi, Jungil ^a   Choi, Eun Jung ^a   Costa, Maria E ^b   Lee, Byung Ju ^a   Ojeda, Sergio R ^b  

^a University of Ulsan   (South Korea)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Ca2+ binding protein; Epidermal growth factor like repeat domains; Female puberty; Glutamate release; Synaptophysin

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; ANTISENSE OLIGODEOXYNUCLEOTIDE; GONADORELIN; GROWTH FACTOR; MESSENGER RNA; PROTEIN NELL2; UNCLASSIFIED DRUG; VESICULAR GLUTAMATE TRANSPORTER 1; VESICULAR GLUTAMATE TRANSPORTER 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; BRAIN CORTEX; CONTROLLED STUDY; FEMALE; GABAERGIC SYSTEM; GONADORELIN RELEASE; HYPOTHALAMUS; IN VIVO STUDY; JUVENILE; NERVE CELL; NEUROENDOCRINE SYSTEM; NONHUMAN; NUCLEOTIDE SEQUENCE; PERINATAL PERIOD; PREOPTIC AREA; PREPUBERTY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; PUBERTY; RAT; SEXUAL DEVELOPMENT;

ANIMALS; FEMALE; GENE EXPRESSION; GLUTAMIC ACID; GONADOTROPIN-RELEASING HORMONE; HYPOTHALAMUS; NERVE TISSUE PROTEINS; NEURONS; NEUROSECRETORY SYSTEMS; ORGAN SPECIFICITY; RATS; RNA, MESSENGER; SEXUAL MATURATION;

EID: 48749118679     PISSN: 00283835     EISSN: None     Source Type: Journal    
DOI: 10.1159/000139579     Document Type: Article

References (45)

1. r 93 K protein with EGF-like repeats is strongly expressed in neural tissues of early stage chick embryos. Dev Dyn 1995;203:212-222.
2. Watanabe TK, Katagiri T, Suzuki M, Shimizu F, Fujiwara T, Kanemoto N, Nakamura Y, Hirai Y, Maekawa H, Takahashi E: Cloning and characterization of two novel human cDNAs (NELL1 and NELL2) encoding proteins with six EGF-like repeats. Genomics 1996;38:273-276.
3. Oyasu M, Kuroda S, Nakashita M, Fujimiya M, Kikkawa U, Saito N: Immunocytochemical localization of a neuron-specific thrombospondin-1-like protein, NELL2: light and electron microscopic studies in the rat brain. Mol Brain Res 2000;76:151-160.
4. Kuroda S, Oyasu M, Kawakami M, Kanayama N, Tanizawa K, Saito N, Abe T, Matsuhashi S, Ting K: Biochemical characterization and expression analysis of neural thrombospondin-1-like proteins NELL1 and NELL2. Biochem Biophys Res Commun 1999;265:79-86.
5. Nelson BR, Claes K, Todd V, Chaverra M, Lefcort F: NELL2 promotes motor and sensory neuron differentiation and stimulates mitogenesis in DRG in vivo. Dev Biol 2004;270:322-335.
6. Aihara K, Kuroda S, Kanayama N, Matsuyama S, Tanizawa K, Horie M: A neuron-specific family protein, NELL2, promotes survival of neurons through mitogen-activated protein kinases. Mol Brain Res 2003;116:86-93.
7. Davis CG: The many faces of epidermal growth factor repeats. New Biol 1990;2:410-419.
8. Handford PA, Mayhew M, Baron M, Winship PR, Campbell ID, Brownlee GG: Key residues involved in calcium-binding motifs in EGF-like domains. Nature 1991;351:164-167.
9. 2+-binding epidermal growth factor-like domain: its role in protein-protein interactions. Cell 1995;82:131-141.
10. Kuroda S, Tanizawa K: Involvement of epidermal growth factor-like domain of NELL proteins in the novel protein-protein interaction with protein kinase C. Biochem Biophys Res Commun 1999;265:752-757.
11. Kim H, Ha CM, Choi J, Choi EJ, Jeon J, Kim C, Park SK, Kang SS, Kim K, Lee BJ: Ontogeny and the possible function of a novel epidermal growth factor-like repeat domain-containing protein, NELL2, in the rat brain. J Neurochem 2002;83:1389-1400.
12. +-dependent inorganic phosphate cotransporter (DNPI) in the rat forebrain. Mol Brain Res 2000;83:34-43.
13. Takamori S, Rhee JS, Rosenmund C, John R: Identification of a vesicular glutamate transporter that defines a glutamatergic phenotype in neurons. Nature 2000;407:189-194.
14. Fremeau RT Jr, Troyer MD, Pahner I, Nygaard GO, Tran CH, Reimer RJ, Bellocchio EE, Fortin D, Storm-Mathisen J, Edwards RH: The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron 2001;31:247-260.
15. Ojeda SR, Terasawa E: Neuroendocrine regulation of puberty; in Pfaff D, Arnold A, Etgen A, Fahrbach S, Moss R, Rubin R (eds): Hormones, Brain and Behavior. New York, Elsevier, 2002, vol 4, pp 589-659.
16. Brann DW, Mahesh VB: Excitatory amino acids: evidence for a role in the control of reproduction and anterior pituitary hormone secretion. Endocrine Rev 1997;18:678-700.
17. Ojeda SR, Skinner MK: Puberty in the rat; in Neill JD (ed): The Physiology of Reproduction, ed 3. San Diego, Academic Press/Elsevier, 2006, pp 2061-2126.
18. Herbison AE: Physiology of the gonadotropin-releasing hormone neuronal network; in Neill JD (ed): Physiology of Reproduction, ed 3. San Diego, Academic Press/Elsevier, 2006, pp 1415-1482.
19. Renfranz PJ, Cunningham MG, McKay RDG: Region-specific differentiation of the hippocampal stem cell line HiB5 upon implantation into the developing mammalian brain. Cell 1991;66:713-729.
20. Martínez-Serrano A, Lundberg C, Horellou P, Fischer W, Bentiage C, Campbell K, McKay RDG, Mallet J, Björklund A: CNS-derived neural progenitor cells for gene transfer of nerve growth factor to the adult rat brain: Complete rescue of axotomized cholinergic neurons after transplantation into the septum. J Neurosci 1995;15:5668-5680.
21. Simmons DM, Arriza JL, Swanson LW: A complete protocol for in situ hybridization of messenger RNAs in brain and other tissues with radiolabeled single-stranded RNA probes. J Histotechnol 1989;12:169-181.
22. Berg-von der Emde K, Dees WL, Hiney JK, Hill DF, Dissen GA, Costa ME, Moholt-Siebert M, Ojeda SR: Neurotrophins and the neuroendocrine brain: different neurotrophins sustain anatomically and functionally segregated subsets of hypothalamic dopaminergic neurons. J Neurosci 1995;15:4223-4237.
23. Bilger M, Heger S, Brann DW, Paredes A, Ojeda SR: A conditional, tetracycline-regulated increase in gamma amino butyric acid production near LHRH nerve terminals disrupts estrous cyclicity in the rat. Endocrinology 2001;142:2102-2114.
24. Ma YJ, Hill DF, Creswick KE, Costa ME, Ojeda SR: Neuregulins signaling via a glial erbB2/erbB4 receptor complex contribute to the neuroendocrine control of mammalian sexual development. J Neurosci 1999;19:9913-9927.
25. A receptor subunits are expressed in LHRH neurons of juvenile female rats. Brain Res 1998;780:218-229.
26. Urbanski HF: Monoclonal antibodies to luteinizing hormone-releasing hormone: production, characterization, and immunocytochemical application. Biol Reprod 1991;44:681-686.
27. Bourguignon J-P, Franchimont P: Puberty-related increase in episodic LHRH release from rat hypothalamus in vitro. Endocrinology 1984;114:1941-1943.
28. Ojeda SR, Urbanski HF, Katz KH, Costa ME: Activation of estradiol positive feedback at puberty: estradiol sensitizes the LHRH releasing system at two different biochemical steps. Neuroendocrinology 1986;43:259-265.
29. Urbanski HF, Kim SO, Connolly ML: The influence of photoperiod and 6-methoxybenzoxazolinone on the reproductive axis of inbred LSH/Ss Lak male hamsters. J Reprod Fertil 1990;90:157-163.
30. Ojeda SR, Urbanski HF: Puberty in the rat; in Knobil E, Neill JD (eds): The Physiology of Reproduction, ed 2. New York, Raven Press, 1994, vol 2, pp 363-409.
31. Kaneko T, Fujiyama F: Complementary distribution of vesicular glutamate transporters in the central nervous system. Neurosci Res 2002;42:243-250.
32. van den Pol AN, Wuarin J-P, Dudek FE: Glutamate, the dominant excitatory transmitter in neuroendocrine regulation. Science 1990;250:1276-1278.
33. Urbanski HF, Ojeda SR: Activation of luteinizing hormone-releasing hormone release advances the onset of female puberty. Neuroendocrinology 1987;46:273-276.
34. Plant TM, Gay VL, Marshall GR, Arslan M: Puberty in monkeys is triggered by chemical stimulation of the hypothalamus. Proc Natl Acad Sci USA 1989;86:2506-2510.
35. Campbell RE, Han SK, Herbison AE: Biocytin filling of adult gonadotropin-releasing hormone neurons in situ reveals extensive, spiny, dendritic processes. Endocrinology 2005;146:1163-1169.
36. Campbell RE: Defining the gonadotrophin-releasing hormone neuronal network: transgenic approaches to understanding neurocircuitry. J Neuroendocrinol 2007;19:561-573.
37. Erecinska M, Silver IA: Metabolism and role of glutamate in mammalian brain. Prog Neurobiol 1990;35:245-296.
38. Montana V, Ni Y, Sunjara V, Hua X, Parpura V: Vesicular glutamate transporter-dependent glutamate release from astrocytes. J Neurosci 2004;24:2633-2642.
39. Nedergaard M, Ransom B, Goldman SA: New roles for astrocytes: Redefining the functional architecture of the brain. Trends Neurosci 2003;26:523-530.
40. Fellin T, Sul JY, D'Ascenzo M, Takano H, Pascual O, Haydon PG: Bidirectional astrocyte-neuron communication: the many roles of glutamate and ATP; in Purinergic Signalling in Neuron-Glia Interactions (Norvartis Foundation Symposium 276). Chichester, Wiley, 2006, pp 208-221.
41. Nelson BR, Matsuhashi S, Lefcort F: Restricted neural epidermal growth factor-like like 2 (NELL2) expression during muscle and neuronal differentiation. Mech Dev 2002;119(suppl 1):S11-S19.
42. Hwang EM, Kim DG, Lee BJ, Choi J, Kim E, Park N, Kang D, Han J, Choi WS, Hong SG, Park JY: Alternative splicing generates a novel non-secretable cytosolic isoform of NELL2. Biochem Biophys Res Commun 2007;353:805-811.
43. Mathews D, Andrews WW, Parker R Jr, Ojeda SR: A role for aromatizable androgens in female puberty. Biol Reprod 1987;36:836-843.
44. Choi EJ, Ha CM, Choi J, Kang SS, Choi WS, Park SK, Kim K, Lee BJ: Low-density cDNA array-coupled to PCR differential display identifies new estrogen-responsive genes during the postnatal differentiation of the rat hypothalamus. Mol Brain Res 2001;97:115-128.
45. Christopherson KS, Ullian EM, Stokes CC, Mullowney CE, Hell JW, Agah A, Lawler J, Mosher DF, Bornstein P, Barres BA: Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell 2005;120:421-433.