Lhx2-dependent specification of olfactory sensory neurons is required for successful integration of olfactory, vomeronasal, and GnRH neurons

FASEB Journal

Volumn 26, Issue 8, 2012, Pages 3464-3472

  Berghard, Anna ^a   Hägglund, Anna Carin ^b   Bohm, Staffan ^a   Carlsson, Leif ^b  

^a UMEÅ UNIVERSITY   (Sweden)

^b UMEÅ UNIVERSITY   (Sweden)

Author keywords

Gonadotropin releasing hormone neurons; Mouse embryo development; Puberty phenotype

Indexed keywords

GONADORELIN; HOMEODOMAIN PROTEIN; PROTEIN LHX2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL MIGRATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; FOREBRAIN; GENE; GENE EXPRESSION; HYPOPHYSIS CELL; HYPOPLASIA; HYPOTHALAMUS; IN SITU HYBRIDIZATION; INNERVATION; LHX2 GENE; MOUSE; MUTANT; NONHUMAN; OLFACTORY BULB; OLFACTORY NERVE; PHENOTYPE; POSTNATAL DEVELOPMENT; PRENATAL DEVELOPMENT; PRIORITY JOURNAL; PUBERTY; SENSORY NERVE CELL; TELENCEPHALON; VOMERONASAL ORGAN;

ANIMALS; CELL MOVEMENT; FEMALE; GONADOTROPIN-RELEASING HORMONE; LIM-HOMEODOMAIN PROTEINS; MALE; MICE; OLFACTORY BULB; OLFACTORY PATHWAYS; OLFACTORY RECEPTOR NEURONS; SENSORY RECEPTOR CELLS; TRANSCRIPTION FACTORS; VOMERONASAL ORGAN;

MUS;

EID: 84864758823     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-206193     Document Type: Article

References (36)

1. Cuschieri, A., and Bannister, L. H. (1975) The development of the olfactory mucosa in the mouse: light microscopy. J. Anat. 119, 277-286
2. Tucker, E. S., Lehtinen, M. K., Maynard, T., Zirlinger, M., Dulac, C., Rawson, N., Pevny, L., and Lamantia, A. S. (2010) Proliferative and transcriptional identity of distinct classes of neural precursors in the mammalian olfactory epithelium. Development 137, 2471-2481
3. Forni, P. E., Taylor-Burds, C., Melvin, V. S., Williams, T., and Wray, S. (2011) Neural crest and ectodermal cells intermix in the nasal placode to give rise to GnRH-1 neurons, sensory neurons, and olfactory ensheating cells. J. Neurosci. 31, 6915-6927
4. Buck, L., and Axel, R. (1991) A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65, 175-187
5. DeMaria, S., and Ngai, J. (2010) The cell biology of smell. J. Cell Biol. 191, 443-452
6. Tirindelli, R., Dibattista, M., Pifferi, S., and Menini, A. (2009) From pheromones to behavior. Physiol. Rev. 89, 921-956
7. Kolterud, A., Alenius, M., Carlsson, L., and Bohm, S. (2004) The Lim homeobox gene Lhx2 is required for olfactory sensory neuron identity. Development 131, 5319-5326 (Pubitemid 39562177)
8. Hirota, J., and Mombaerts, P. (2004) The LIM-homeodomain protein Lhx2 is required for complete development of mouse olfactory sensory neurons. Proc. Natl. Acad. Sci. U. S. A. 23, 8751-8755 (Pubitemid 38745843)
9. Hirota, J., Omura, M., and Mombaerts, P. (2007) Differential impact of Lhx2 deficiency on expression of class I and class II odorant receptor genes in mouse. Mol. Cell. Neurosci. 34, 679-688 (Pubitemid 46483086)
10. Allen Institute for Brain Science (2009) Developing Mouse Brain Atlas, Allen Institute for Brain Science, Seattle, WA, USA (Online). Available from: http://developingmouse.brain-map.org
11. Porter, F. D., Drago, J., Xu, Y., Cheema, S. S., Wassif, C., Huang, S. P., Lee, E., Grinberg, A., Massalas, J. S., Bodine, D., Alt, F., and Westphal, H. (1997) Lhx2, a LIM homeobox gene, is required for eye, forebrain, and definitive erythrocyte development. Development 124, 2935-2944 (Pubitemid 27370909)
12. Hägglund, A.-C., Dahl, L., and Carlsson, L. (2011) Lhx2 is required for patterning and expansion of a distinct progenitor cell population committed to eye development. PLoS One 6, e23387
13. Mangale, V. S., Hirokawa, K. E., Satyaki, P. R., Gokulchandran, N., Chikbire, S., Subramanian, L., Shetty, A. S., Martynoga, B., Paul, J., Mai, M. V., Li, Y., Flanagan, L. A., Tole, S., and Monuki, E. S. (2008) Lhx2 selector activity specifies cortical identity and suppresses hippocampal organizer fate. Science 319, 304-309
14. Chou, S.-J., Perez-Garcia, C. G., Kroll, T. T., and O'Leary, D. D. M. (2009) Lhx2 specifies regional fate in Emx1 lineage of telencephalic progenitors generating cerebral cortex. Nat. Neurosci. 12, 1377-1385
15. Törnvist, G., Sandberg, A., Hägglund, A.-C., and Carlsson, L. (2010) Cyclic expression of lhx2 regulates hair formation. PLoS Genet. 6, e1000904
16. Hinds, J. W., and Hinds, P. L. (1976) Synapse formation in the mouse olfactory bulb. I. Quantitative studies. J. Comp. Neurol. 169, 15-40
17. Soriano, P. (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21, 70-71
18. Norlin, E. M., Vedin, V., Bohm, S., and Berghard, A. (2005) Odorant-dependent, spatially restricted induction of c-fos in the olfactory epithelium of the mouse. J. Neurochem. 93, 1594-1602 (Pubitemid 40853283)
19. Ressler, K. J., Sullivan, S. L., and Buck, L. B. (1993) A zonal organization of odorant receptor gene expression in the olfactory epithelium. Cell 73, 597-609 (Pubitemid 23143357)
20. Berghard, A., and Buck, L. B. (1996) Sensory transduction in vomeronasal neurons: evidence for Gαo, Gαi2, and adenylyl cyclase II as major components of a pheromone signaling cascade. J. Neurosci. 16, 909-918 (Pubitemid 26140846)
21. Packard, A., Giel-Moloney, M., Leiter, A., and Schwob, J. E. (2011) Progenitor cell capacity of NeuroD1-expressing globose basal cells in the mouse olfactory epithelium. J. Comp. Neurol. 519, 3580-3596
22. Saha, B., Hari, P., Huilgol, D., and Tole, S. (2007) Dual role for LIM-homeodomain gene Lhx2 in the formation of the lateral olfactory tract. J. Neurosci. 27, 2290-2297 (Pubitemid 46340956)
23. Yoshida, K., Tobet, S. A., Crandall, J. E., Jimenez, T. P., and Schwarting, G. A. (1995) The migration of luteinizing hormone-releasing hormone neurons in the developing rat is associated with a transient, caudal projection of the vomeronasal nerve. J. Neurosci. 15, 7769-7777 (Pubitemid 26006888)
24. Schwarting, G. A., Raitcheva, D., Bless, E. P., Ackerman, S. L., and Tobet, S. (2004) G.A. Schwarting, D. Raitcheva, E.P. Bless, S.L. Ackerman, S. Tobet, Netrin 1-mediated chemoattraction regulates the migratory pathway of LHRH neurons. Eur. J. Neurosci. 19, 11-20 (Pubitemid 38122067)
25. Schwanzel-Fukuda, M., and Pfaff, D. W. (1989) Origin of luteinizing hormone-releasing hormone neurons. Nature 338, 161-164 (Pubitemid 19074106)
26. Wray, S., Grant, P., and Gainer, H. (1989) Evidence that cells expressing luteinizing hormone-releasing hormone mRNA in the mouse are derived from progenitor cells in the olfactory placode. Proc. Natl. Acad. Sci. U. S. A. 86, 8132-8136 (Pubitemid 19265333)
27. Gong, Q., and Shipley, M. T. (1995) Evidence that pioneer olfactory axons regulate telencephalon cell cycle kinetics to induce the formation of the olfactory bulb. Neuron 14, 91-101
28. Miller, A. M., Treloar, H. B., and Greer, C. A. (2010) Composition of the migratory mass during development of the olfactory nerve. J. Comp. Neurol. 518, 4825-4841
29. Hirata, T., Nakazawa, M., Yoshihara, S.-I., Miyachi, H., Kitamura, K., Yoshihara, Y., and Masahiko, H. (2006) Zinc-finger gene Fez in the olfactory sensory neurons regulates development of the olfactory bulb non-cell- autonomously. Development 133, 1433-1443 (Pubitemid 43732957)
30. Watanabe, Y., Inoue, K., Okuyama-Yamamoto, A., Nakai, N., Nakatani, J., Nibu, K., Sato, N., Iiboshi, Y., Yusa, K., Kondoh, G., Takeda, J., Terashima, T., and Takumi, T. (2009) Fezf1 is required for penetration of the basal lamina by olfactory axons to promote olfactory development. J. Comp. Neurol. 515, 565-584
31. Bentley, D., and Caudy, M. (1983) Pioneer axons lose directed growth after selective killing of guidepost cells. Nature 304, 62-65 (Pubitemid 13063105)
32. Takano-Maruyama, M., Chen, Y., and Gaufo, G. O. (2010) Placodal sensory ganglia coordinate the formation of the cranial visceral motor pathway. Dev. Dyn. 239, 1155-1161
33. Wierman, M. E., Kiseljak-Vassiliadesa, K., and Tobet, S. (2011) Gonadotropin-releasing hormone (GnRH) neuron migration: Initiation, maintenance and cessation as critical steps to ensure normal reproductive function. Front. Neuroendocrinol. 32, 43-52
34. Metz, H., and Wray, S. (2010) Use of mutant mouse lines to investigate origin of gonadotropin-releasing hormone-1 neurons: lineage independent of the adenohypophysis. Endocrinology 151, 766-773
35. Topaloglu, A. K., and Kotan, L. D. (2010) Molecular causes of hypogonadotropic hypogonadism. Curr. Opin. Obstet. Gynecol. 22, 264-270
36. Bianco, S. D. C., and Kaiser, U. B. (2009) The genetic and molecular basis of idiopathic hypogonadotropic hypogonadism. Nat. Rev. Endocrinol. 5, 569-576