Secretagogin is a Ca2+-binding protein identifying prospective extended amygdala neurons in the developing mammalian telencephalon

European Journal of Neuroscience

Volumn 31, Issue 12, 2010, Pages 2166-2177

  Mulder, Jan ^a   Spence, Lauren ^a   Tortoriello, Giuseppe ^a   Dinieri, Jennifer A ^b   Uhlén, Mathias ^c   Shui, Bo ^d   Kotlikoff, Michael I ^d   Yanagawa, Yuchio ^e,f   Aujard, Fabienne ^g   Hökfelt, Tomas ^h   Hurd, Yasmin L ^b   Harkany, Tibor ^a,h  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c ALBANOVA UNIVERSITY CENTER   (Sweden)

^d Cornell University ^*  (United States)

^e GUNMA UNIVERSITY   (Japan)

^f JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^g MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^h KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Ca2+ binding protein; Extended amygdala; Forebrain; Mouse; Primate

Indexed keywords

4 AMINOBUTYRIC ACID; CALCIUM BINDING PROTEIN; SECRETAGOGIN; UNCLASSIFIED DRUG; SCGN PROTEIN, HUMAN; SECRETAGOGIN PROTEIN, MOUSE;

AMYGDALOID NUCLEUS; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BRAIN NERVE CELL; CORPUS STRIATUM; EMBRYO; HUMAN; HUMAN TISSUE; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; SUBSTANTIA INNOMINATA; TELENCEPHALON; ANIMAL; ANIMAL EMBRYO; CHEIROGALEIDAE; CYTOLOGY; FEMALE; GENE EXPRESSION PROFILING; GENETICS; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; MAMMAL; METABOLISM; NERVE CELL; ORGANOGENESIS; PHYSIOLOGY; PRENATAL DEVELOPMENT;

AMYGDALA; ANIMALS; CALCIUM-BINDING PROTEINS; CHEIROGALEIDAE; EMBRYO, MAMMALIAN; FEMALE; GENE EXPRESSION PROFILING; HUMANS; MAMMALS; MICE; NEURONS; ORGANOGENESIS; TELENCEPHALON;

EID: 77953790537     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2010.07275.x     Document Type: Article

References (60)

1. Aguado, T., Palazuelos, J., Monory, K., Stella, N., Cravatt, B., Lutz, B., Marsicano, G., Kokaia, Z., Guzman, M. Galve-Roperh, I. (2006) The endocannabinoid system promotes astroglial differentiation by acting on neural progenitor cells. J. Neurosci., 26, 1551 1561.
2. Andressen, C., Blumcke, I. Celio, M.R. (1993) Calcium-binding proteins: selective markers of nerve cells. Cell Tissue Res., 271, 181 208.
3. Arita, D.Y., Di Marco, G.S., Schor, N. Casarini, D.E. (2002) Purification and characterization of the active form of tyrosine hydroxylase from mesangial cells in culture. J. Cell. Biochem., 87, 58 64.
4. Attems, J., Quass, M., Gartner, W., Nabokikh, A., Wagner, L., Steurer, S., Arbes, S., Lintner, F. Jellinger, K. (2007) Immunoreactivity of calcium binding protein secretagogin in the human hippocampus is restricted to pyramidal neurons. Exp. Gerontol., 42, 215 222.
5. Attems, J., Preusser, M., Grosinger-Quass, M., Wagner, L., Lintner, F. Jellinger, K. (2008) Calcium-binding protein secretagogin-expressing neurones in the human hippocampus are largely resistant to neurodegeneration in Alzheimer's disease. Neuropathol. Appl. Neurobiol., 34, 23 32.
6. Berghuis, P., Rajnicek, A.M., Morozov, Y.M., Ross, R.A., Mulder, J., Urban, G.M., Monory, K., Marsicano, G., Matteoli, M., Canty, A., Irving, A.J., Katona, I., Yanagawa, Y., Rakic, P., Lutz, B., Mackie, K. Harkany, T. (2007) Hardwiring the brain: endocannabinoids shape neuronal connectivity. Science, 316, 1212 1216.
7. Bernier, P.J., Bedard, A., Vinet, J., Levesque, M. Parent, A. (2002) Newly generated neurons in the amygdala and adjoining cortex of adult primates. Proc. Natl. Acad. Sci. USA, 99, 11464 11469.
8. Bons, N., Silhol, S., Barbie, V., Mestre-Frances, N. Albe-Fessard, D. (1998) A stereotaxic atlas of the grey lesser mouse lemur brain (Microcebus murinus). Brain Res. Bull., 46, 1 173.
9. Bossolasco, P., Cova, L., Calzarossa, C., Rimoldi, S.G., Borsotti, C., Deliliers, G.L., Silani, V., Soligo, D. Polli, E. (2005) Neuro-glial differentiation of human bone marrow stem cells in vitro. Exp. Neurol., 193, 312 325.
10. Brun, P., Dupret, J.M., Perret, C., Thomasset, M. Mathieu, H. (1987) Vitamin D-dependent calcium-binding proteins (CaBPs) in human fetuses: comparative distribution of 9K CaBP mRNA and 28K CaBP during development. Pediatr. Res., 21, 362 367.
11. 2+ buffers and synaptic efficacy. Cell Calcium, 37, 489 495.
12. Carleton, A., Petreanu, L.T., Lansford, R., Alvarez-Buylla, A. Lledo, P.M. (2003) Becoming a new neuron in the adult olfactory bulb. Nat. Neurosci., 6, 507 518.
13. Celio, M.R. (1990) Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience, 35, 375 475.
14. Cohen, S. Greenberg, M.E. (2008) Communication between the synapse and the nucleus in neuronal development, plasticity, and disease. Annu. Rev. Cell Dev. Biol., 24, 183 209.
15. Fishell, G. Kriegstein, A.R. (2003) Neurons from radial glia: the consequences of asymmetric inheritance. Curr. Opin. Neurobiol., 13, 34 41.
16. Flames, N. Marin, O. (2005) Developmental mechanisms underlying the generation of cortical interneuron diversity. Neuron, 46, 377 381.
17. Freund, T.F. Buzsaki, G. (1996) Interneurons of the hippocampus. Hippocampus, 6, 347 470.
18. Fritschy, J.M. (2008) Is my antibody-staining specific? How to deal with pitfalls of immunohistochemistry Eur. J. Neurosci., 28, 2365 2370.
19. Gartner, W., Vila, G., Daneva, T., Nabokikh, A., Koc-Saral, F., Ilhan, A., Majdic, O., Luger, A. Wagner, L. (2007) New functional aspects of the neuroendocrine marker secretagogin based on the characterization of its rat homolog. Am. J. Physiol Endocrinol. Metab, 293, E347 E354.
20. Geula, C., Schatz, C.R. Mesulam, M.M. (1993) Differential localization of NADPH-diaphorase and calbindin-D28k within the cholinergic neurons of the basal forebrain, striatum and brainstem in the rat, monkey, baboon and human. Neuroscience, 54, 461 476.
21. Gleeson, J.G., Lin, P.T., Flanagan, L.A. Walsh, C.A. (1999) Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron, 23, 257 271.
22. Hartig, W., Seeger, J., Naumann, T., Brauer, K. Bruckner, G. (1998) Selective in vivo fluorescence labelling of cholinergic neurons containing p75(NTR) in the rat basal forebrain. Brain Res., 808, 155 165.
23. Heizmann, C.W. (1986) Intracellular calcium-binding proteins: structure and possible functions. J. Cardiovasc. Pharmacol., 8 (Suppl 8 S7 S12.
24. Hurd, Y.L. (2003) In situ hybridization with isotopic riboprobes for detection of striatal neuropeptide mRNA expression after dopamine stimulant administration. Methods Mol. Med., 79, 119 135.
25. Hurd, Y.L., Wang, X., Anderson, V., Beck, O., Minkoff, H. Dow-Edwards, D. (2005) Marijuana impairs growth in mid-gestation fetuses. Neurotoxicol. Teratol., 27, 221 229.
26. Karlsen, A.E., Hagopian, W.A., Grubin, C.E., Dube, S., Disteche, C.M., Adler, D.A., Barmeier, H., Mathewes, S., Grant, F.J. Foster, D. (1991) Cloning and primary structure of a human islet isoform of glutamic acid decarboxylase from chromosome 10. Proc. Natl. Acad. Sci. U S A, 88, 8337 8341.
27. Keays, D.A., Tian, G., Poirier, K., Huang, G.J., Siebold, C., Cleak, J., Oliver, P.L., Fray, M., Harvey, R.J., Molnar, Z., Pinon, M.C., Dear, N., Valdar, W., Brown, S.D., Davies, K.E., Rawlins, J.N., Cowan, N.J., Nolan, P., Chelly, J. Flint, J. (2007) Mutations in alpha-tubulin cause abnormal neuronal migration in mice and lissencephaly in humans. Cell, 128, 45 57.
28. Kitanaka, J., Takemura, M., Matsumoto, K., Mori, T. Wanaka, A. (1998) Structure and chromosomal localization of a murine LIM/homeobox gene, Lhx8. Genomics, 49, 307 309.
29. Klausberger, T. Somogyi, P. (2008) Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science, 321, 53 57.
30. Lai, M., Lu, B., Xing, X., Xu, E., Ren, G. Huang, Q. (2006) Secretagogin, a novel neuroendocrine marker, has a distinct expression pattern from chromogranin A. Virchows Arch., 449, 402 409.
31. McDonald, A.J. Pearson, J.C. (1989) Coexistence of GABA and peptide immunoreactivity in non-pyramidal neurons of the basolateral amygdala. Neurosci. Lett., 100, 53 58.
32. Mesulam, M.M., Mufson, E.J., Wainer, B.H. Levey, A.I. (1983) Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience, 10, 1185 1201.
33. Meyer, G., Soria, J.M., Martinez-Galan, J.R., Martin-Clemente, B. Fairen, A. (1998) Different origins and developmental histories of transient neurons in the marginal zone of the fetal and neonatal rat cortex. J. Comp. Neurol., 397, 493 518.
34. Mulder, J., Bjorling, E., Jonasson, K., Wernerus, H., Hober, S., Hokfelt, T. Uhlen, M. (2009a) Tissue profiling of the mammalian central nervous system using human antibody-based proteomics. Mol. Cell Proteomics, 8, 1612 1622.
35. 2+-binding protein specifying subpopulations of telencephalic neurons. Proc. Natl. Acad. Sci. USA, 106, 22492 22497.
36. Nagatsuka, Y., Hara-Yokoyama, M., Kasama, T., Takekoshi, M., Maeda, F., Ihara, S., Fujiwara, S., Ohshima, E., Ishii, K., Kobayashi, T., Shimizu, K. Hirabayashi, Y. (2003) Carbohydrate-dependent signaling from the phosphatidylglucoside-based microdomain induces granulocytic differentiation of HL60 cells. Proc. Natl. Acad. Sci. USA, 100, 7454 7459.
37. Nicholls, D.G. (2009) Mitochondrial calcium function and dysfunction in the central nervous system. Biochim. Biophys. Acta, 1787, 1416 1424.
38. Paxinos, G. Franklin, K.B.J. 2001. The mouse brain in stereotaxic coordinates. Academic Press
39. Pencea, V. Luskin, M.B. (2003) Prenatal development of the rodent rostral migratory stream. J. Comp. Neurol., 463, 402 418.
40. Perret, M. (1990) Influence of social-factors on sex-ratio at birth, maternal investment and young survival in a prosimian primate. Behav. Ecol. Sociobiol., 27, 447 454.
41. Perret, M. (1992) Environmental and social determinants of sexual function in the male lesser mouse lemur (Microcebus murinus). Folia Primatol. (Basel), 59, 1 25.
42. Perret, M. Aujard, F. (2001) Regulation by photoperiod of seasonal changes in body weight and reproductive function in the lesser mouse lemur (Microcebus murinus): differential responses by sex. Int. J. Primatol., 22, 5 24.
43. Riedel, A., Hartig, W., Seeger, G., Gartner, U., Brauer, K. Arendt, T. (2002) Principles of rat subcortical forebrain organization: a study using histological techniques and multiple fluorescence labeling. J. Chem. Neuroanat., 23, 75 104.
44. Rogstam, A., Linse, S., Lindqvist, A., James, P., Wagner, L. Berggard, T. (2007) Binding of calcium ions and SNAP-25 to the hexa EF-hand protein secretagogin. Biochem. J., 401, 353 363.
45. Sanchez, M.P., Frassoni, C., varez-Bolado, G., Spreafico, R. Fairen, A. (1992) Distribution of calbindin and parvalbumin in the developing somatosensory cortex and its primordium in the rat: an immunocytochemical study. J. Neurocytol., 21, 717 736.
46. Schnell, S.A., Staines, W.A. Wessendorf, M.W. (1999) Reduction of lipofuscin-like autofluorescence in fluorescently labeled tissue. J. Histochem. Cytochem., 47, 719 730.
47. Schwaller, B., Buchwald, P., Blumcke, I., Celio, M.R. Hunziker, W. (1993) Characterization of a polyclonal antiserum against the purified human recombinant calcium binding protein calretinin. Cell Calcium, 14, 639 648.
48. Solbach, S. Celio, M.R. (1991) Ontogeny of the calcium binding protein parvalbumin in the rat nervous system. Anat. Embryol. (Berl), 184, 103 124.
49. Strehler, E.E., Filoteo, A.G., Penniston, J.T. Caride, A.J. (2007) Plasma-membrane Ca(2+) pumps: structural diversity as the basis for functional versatility. Biochem. Soc. Trans., 35, 919 922.
50. Sugitani, Y., Nakai, S., Minowa, O., Nishi, M., Jishage, K., Kawano, H., Mori, K., Ogawa, M. Noda, T. (2002) Brn-1 and Brn-2 share crucial roles in the production and positioning of mouse neocortical neurons. Genes Dev., 16, 1760 1765.
51. Swanson, L.W. Petrovich, G.D. (1998) What is the amygdala? Trends Neurosci., 21, 323 331.
52. Tallini, Y.N., Shui, B., Greene, K.S., Deng, K.Y., Doran, R., Fisher, P.J., Zipfel, W. Kotlikoff, M.I. (2006) BAC transgenic mice express enhanced green fluorescent protein in central and peripheral cholinergic neurons. Physiol. Genomics, 27, 391 397.
53. Tamamaki, N., Yanagawa, Y., Tomioka, R., Miyazaki, J., Obata, K. Kaneko, T. (2003) Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J. Comp. Neurol., 467, 60 79.
54. Uhlen, M., Bjorling, E., Agaton, C., Szigyarto, C.A., Amini, B., Andersen, E., Andersson, A.C., Angelidou, P., Asplund, A., Asplund, C., Berglund, L., Bergstrom, K., Brumer, H., Cerjan, D., Ekstrom, M., Elobeid, A., Eriksson, C., Fagerberg, L., Falk, R., Fall, J., Forsberg, M., Bjorklund, M.G., Gumbel, K., Halimi, A., Hallin, I., Hamsten, C., Hansson, M., Hedhammar, M., Hercules, G., Kampf, C., Larsson, K., Lindskog, M., Lodewyckx, W., Lund, J., Lundeberg, J., Magnusson, K., Malm, E., Nilsson, P., Odling, J., Oksvold, P., Olsson, I., Oster, E., Ottosson, J., Paavilainen, L., Persson, A., Rimini, R., Rockberg, J., Runeson, M., Sivertsson, A., Skollermo, A., Steen, J., Stenvall, M., Sterky, F., Stromberg, S., Sundberg, M., Tegel, H., Tourle, S., Wahlund, E., Walden, A., Wan, J., Wernerus, H., Westberg, J., Wester, K., Wrethagen, U., Xu, L.L., Hober, S. Ponten, F. (2005) A human protein atlas for normal and cancer tissues based on antibody proteomics. Mol. Cell Proteomics, 4, 1920 1932.
55. Verney, C. Derer, P. (1995) Cajal-Retzius neurons in human cerebral cortex at midgestation show immunoreactivity for neurofilament and calcium-binding proteins. J. Comp. Neurol., 359, 144 153.
56. 2+-binding protein. J. Biol. Chem., 275, 24740 24751.
57. Wang, X., Dow-Edwards, D., Anderson, V., Minkoff, H. Hurd, Y.L. (2004) In utero marijuana exposure associated with abnormal amygdala dopamine D2 gene expression in the human fetus. Biol. Psychiatry, 56, 909 915.
58. Wonders, C.P. Anderson, S.A. (2006) The origin and specification of cortical interneurons. Nat. Rev. Neurosci., 7, 687 696.
59. Woodruff, A.R. Sah, P. (2007a) Inhibition and synchronization of basal amygdala principal neuron spiking by parvalbumin-positive interneurons. J. Neurophysiol., 98, 2956 2961.
60. Woodruff, A.R. Sah, P. (2007b) Networks of parvalbumin-positive interneurons in the basolateral amygdala. J. Neurosci., 27, 553 563.