Rax regulates hypothalamic tanycyte differentiation and barrier function in mice

Journal of Comparative Neurology

Volumn 522, Issue 4, 2014, Pages 876-899

  Miranda Angulo, Ana L ^a,b   Byerly, Mardi S ^a   Mesa, Janny ^a   Wang, Hong ^a   Blackshaw, Seth ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSIDAD DE ANTIOQUIA   (Colombia)

Author keywords

CSF Brain barrier; Ectopic ependymal cells; Rarres2 expression; Rax haploinsufficiency; Thinning of the third ventricular wall

Indexed keywords

EVANS BLUE; PROTEIN RAX; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN THIRD VENTRICLE; CELL WALL; DIFFUSION; EPENDYMA CELL; FEMALE; HAPLOINSUFFICIENCY; HYPOTHALAMUS NUCLEUS; MALE; MOLECULAR BIOLOGY; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; TANYCYTE;

CSF-BRAIN BARRIER; ECTOPIC EPENDYMAL CELLS; RARRES2 EXPRESSION; RAX HAPLOINSUFFICIENCY; THINNING OF THE THIRD VENTRICULAR WALL;

ANIMALS; CELL DIFFERENTIATION; CHEMOTACTIC FACTORS; EPENDYMOGLIAL CELLS; EVANS BLUE; EYE PROTEINS; FEMALE; GENE EXPRESSION REGULATION; GENOTYPE; HOMEODOMAIN PROTEINS; HYPOTHALAMUS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NEUROGLIA; RECEPTORS, G-PROTEIN-COUPLED; RNA, MESSENGER; THIRD VENTRICLE; TRANSCRIPTION FACTORS;

EID: 84892451039     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23451     Document Type: Article

References (65)

1. Agnati LF, Zoli M, Stromberg I, Fuxe K. 1995. Intercellular communication in the brain: wiring versus volume transmission. Neuroscience 69:711-726.
2. Altman J, Bayer SA. 1978. Development of the diencephalon in the rat. III. Ontogeny of the specialized ventricular linings of the hypothalamic third ventricle. J Comp Neurol 182:995-1015.
3. Alvarez-Bolado G, Paul FA, Blaess S. 2012. Sonic hedgehog lineage in the mouse hypothalamus: from progenitor domains to hypothalamic regions. Neural Dev 7:4-7.
4. Andreazzoli M, Gestri G, Cremisi F, Casarosa S, Dawid IB, Barsacchi G. 2003. Xrx1 controls proliferation and neurogenesis in Xenopus anterior neural plate. Development 130:5143-5154.
5. Batailler M, Mullier A, Sidibe A, Delagrange P, Prevot V, Jockers R, Migaud M. 2012. Neuroanatomical distribution of the orphan GPR50 receptor in adult sheep and rodent brains. J Neuroendocrinol 24:798-808.
6. Bleier R. 1971. The relations of ependyma to neurons and capillaries in the hypothalamus: a Golgi-Cox study. J Comp Neurol 142:439-463.
7. Bolborea M, Dale N. 2013. Hypothalamic tanycytes: potential roles in the control of feeding and energy balance. Trends Neurosci 36:91-100.
8. Casarosa S, Amato MA, Andreazzoli M, Gestri G, Barsacchi G, Cremisi F. 2003. Xrx1 controls proliferation and multipotency of retinal progenitors. Mol Cell Neurosci 22:25-36.
9. Coppola A, Liu ZW, Andrews ZB, Paradis E, Roy MC, Friedman JM, Ricquier D, Richard D, Horvath TL, Gao XB, Diano S. 2007. A central thermogenic-like mechanism in feeding regulation: an interplay between arcuate nucleus T3 and UCP2. Cell Metab 5:21-33.
10. Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A. 1997. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci 17:5046-5061.
11. Duenas M, Luquin S, Chowen JA, Torres-Aleman I, Naftolin F, Garcia-Segura LM. 1994. Gonadal hormone regulation of insulin-like growth factor-I-like immunoreactivity in hypothalamic astroglia of developing and adult rats. Neuroendocrinology 59:528-538.
12. Dziegielewska KM, Knott GW, Saunders NR. 2000. The nature and composition of the internal environment of the developing brain. Cell Mol Neurobiol 20:41-56.
13. Ernst MC, Sinal CJ. 2010. Chemerin: at the crossroads of inflammation and obesity. Trends Endocrinol Metab 21:660-667.
14. Fernandez-Galaz MC, Torres-Aleman I, Garcia-Segura LM. 1996. Endocrine-dependent accumulation of IGF-I by hypothalamic glia. Neuroreport 8:373-377.
15. Frayling C, Britton R, Dale N. 2011. ATP-mediated glucosensing by hypothalamic tanycytes. J Physiol 589:2275-2286.
16. Fry DL, Mahley RW, Weisgraber KH, Oh SY. 1977. Simultaneous accumulation of Evans blue dye and albumin in the canine aortic wall. Am J Physiol 233:H66-H79.
17. Furukawa T, Mukherjee S, Bao ZZ, Morrow EM, Cepko CL. 2000. Rax, Hes1, and notch1 promote the formation of Muller glia by postnatal retinal progenitor cells. Neuron 26:383-394.
18. Gundersen GG, Bulinski JC. 1986. Distribution of tyrosinated and nontyrosinated alpha-tubulin during mitosis. J Cell Biol 102:1118-1126.
19. Gundersen GG, Kalnoski MH, Bulinski JC. 1984. Distinct populations of microtubules: tyrosinated and nontyrosinated alpha tubulin are distributed differently in vivo. Cell 38:779-789.
20. Haan N, Goodman T, Najdi-Samiei A, Stratford CM, Rice R, El AE, Bellusci S, Hajihosseini MK. 2013. Fgf10-expressing tanycytes add new neurons to the appetite/energy-balance regulating centers of the postnatal and adult hypothalamus. J Neurosci 33:6170-6180.
21. Hajos F, Basco E. 1984. The surface-contact glia. Adv Anat Embryol Cell Biol 84:1-79.
22. Jain R, Pan J, Driscoll J.A., Wisner JW, Huang T, Gunsten SP, You Y, Brody SL. 2010. Temporal relationship between primary and motile ciliogenesis in airway epithelial cells. Am J Respir Cell Mol Biol 43:731-739.
23. Langlet F, Levin BE, Luquet S, Mazzone M, Messina A, Dunn-Meynell AA, Balland E, Lacombe A, Mazur D, Carmeliet P, Bouret SG, Prevot V, Dehouck B. (2013a) Tanycytic VEGF-A Boosts Blood-Hypothalamus Barrier Plasticity and Access of Metabolic Signals to the Arcuate Nucleus in Response to Fasting. Cell Metab 17:607-61.
24. Langlet F, Mullier A, Bouret SG, Prevot V, Dehouck B. (2013b) Tanycyte-like cells form a blood-cerebrospinal fluid barrier in the circumventricular organs of the mouse brain. J Comp Neurol 2013, Doi: 10.1002/cne.23355.
25. Lavado A, Oliver G. 2011. Six3 is required for ependymal cell maturation. Development 138:5291-5300.
26. Lee DA, Blackshaw S. 2012. Functional implications of hypothalamic neurogenesis in the adult mammalian brain. Int J Dev Neurosci 30:615-621.
27. Lee DA, Bedont JL, Pak T, Wang H, Song J, Miranda-Angulo A, Takiar V, Charubhumi V, Balordi F, Takebayashi H, Aja S, Ford E, Fishell G, Blackshaw S. 2012. Tanycytes of the hypothalamic median eminence form a diet-responsive neurogenic niche. Nat Neurosci 15:700-702.
28. Li J, Tang Y, Cai D. 2012. IKKbeta/NF-kappaB disrupts adult hypothalamic neural stem cells to mediate a neurodegenerative mechanism of dietary obesity and pre-diabetes. Nat Cell Biol 14:999-1012.
29. Lu F, Kar D, Gruenig N, Zhang ZW, Cousins N, Rodgers HM, Swindell EC, Jamrich M, Schuurmans C, Mathers PH, Kurrasch DM. 2013. Rax is a selector gene for mediobasal hypothalamic cell types. J Neurosci 33:259-272.
30. Marcet B, Chevalier B, Luxardi G, Coraux C, Zaragosi LE, Cibois M, Robbe-Sermesant K, Jolly T, Cardinaud B, Moreilhon C, Giovannini-Chami L, Nawrocki-Raby B, Birembaut P, Waldmann R, Kodjabachian L, Barbry P. 2011. Control of vertebrate multiciliogenesis by miR-449 through direct repression of the Delta/Notch pathway. Nat Cell Biol 13:693-699.
31. Marsili A, Sanchez E, Singru P, Harney JW, Zavacki AM, Lechan RM, Larsen PR. 2011. Thyroxine-induced expression of pyroglutamyl peptidase II and inhibition of TSH release precedes suppression of TRH mRNA and requires type 2 deiodinase. J Endocrinol 211:73-78.
32. Mathers PH, Grinberg A, Mahon KA, Jamrich M. 1997. The Rx homeobox gene is essential for vertebrate eye development. Nature 387:603-607.
33. Mathew TC. 2008. Regional analysis of the ependyma of the third ventricle of rat by light and electron microscopy. Anat Histol Embryol 37:9-18.
34. Millhouse OE. 1971. A Golgi study of third ventricle tanycytes in the adult rodent brain. Z Zellforsch Mikrosk Anat 121:1-13.
35. Monroe BG, Paull WK. 1974. Ultrastructural changes in the hypothalamus during development and hypothalamic activity: the median eminence. Prog Brain Res 41:185-208.
36. Mullier A, Bouret SG, Prevot V, Dehouck B. 2010. Differential distribution of tight junction proteins suggests a role for tanycytes in blood-hypothalamus barrier regulation in the adult mouse brain. J Comp Neurol 518:943-962.
37. Nakao N, Ono H, Yamamura T, Anraka T, Takagi T, Higashi K, Yasuo S, Katou Y, Kageyama S, Uno Y, Kasukawa T, Iigo M, Sharp PJ, Iwasawa A, Suzuki Y, Sugano S, Nimi T, Mizutani M, Namikawa T, Ebihara S, Veda HR, Yoshimura T. 2008. Thyrotrophin in the pars tuberalis triggers photoperiodic response. Nature 452:317-322.
38. O'Callaghan C, Sikand K, Rutman A. 1999. Respiratory and brain ependymal ciliary function. Pediatr Res 46:704-707.
39. Orellana JA, Saez PJ, Cortes-Campos C, Elizondo RJ, Shoji KF, Contreras-Duarte S, Figueroa V, Velarde V, Jiang JX, Nualart F, Saez JC, Garcia MA. 2012. Glucose increases intracellular free Ca(2+) in tanycytes via ATP released through connexin 43 hemichannels. Glia 60:53-68.
40. Paturle-Lafanechere L, Manier M, Trigault N, Pirollet F, Mazarguil H, Job D. 1994. Accumulation of delta 2-tubulin, a major tubulin variant that cannot be tyrosinated, in neuronal tissues and in stable microtubule assemblies. J Cell Sci 107:1529-1543.
41. Peruzzo B, Pastor FE, Blazquez JL, Schobitz K, Pelaez B, Amat P, Rodriguez EM. 2000. A second look at the barriers of the medial basal hypothalamus. Exp Brain Res 132:10-26.
42. Prevot V, Croix D, Bouret S, Dutoit S, Tramu G, Stefano GB, Beauvillain JC. 1999. Definitive evidence for the existence of morphological plasticity in the external zone of the median eminence during the rat estrous cycle: implication of neuro-glio-endothelial interactions in gonadotropin-releasing hormone release. Neuroscience 94:809-819.
43. Robins SC, Stewart I, McNay DE, Taylor V, Giachino C, Goetz M, Ninkovic J, Briancon N, Maratos-Flier E, Flier JS, Kokoeva MV, Placzek M. α-Tanycytes of the adult hypothalamic third ventricle include distinct populations of FGF-responsive neural progenitors. Nat Commun. 2013;4:2049.
44. Rodriguez EM, Gonzalez CB, Delannoy L. 1979. Cellular organization of the lateral and postinfundibular regions of the median eminence in the rat. Cell Tissue Res 201:377-408.
45. Rodriguez EM, Blazquez JL, Pastor FE, Pelaez B, Pena P, Peruzzo B, Amat P. 2005. Hypothalamic tanycytes: a key component of brain-endocrine interaction. Int Rev Cytol 247:89-164.
46. Rodriguez EM, Blazquez JL, Guerra M. 2010. The design of barriers in the hypothalamus allows the median eminence and the arcuate nucleus to enjoy private milieus: the former opens to the portal blood and the latter to the cerebrospinal fluid. Peptides 31:757-776.
47. Rutzel H, Schiebler TH. 1980. Prenatal and early postnatal development of the glial cells in the median eminence of the rat. Cell Tissue Res 211:117-137.
48. Sanchez E, Vargas MA, Singru PS, Pascual I, Romero F, Fekete C, Charli JL, Lechan RM. 2009. Tanycyte pyroglutamyl peptidase II contributes to regulation of the hypothalamic-pituitary-thyroid axis through glial-axonal associations in the median eminence. Endocrinology 150:2283-2291.
49. Satir P, Christensen ST. 2007. Overview of structure and function of mammalian cilia. Annu Rev Physiol 69:377-400.
50. Sawamoto K, Wichterle H, Gonzalez-Perez O, Cholfin JA, Yamada M, Spassky N, Murcia NS, Garcia-Verdugo JM, Marin O, Rubenstein JL, Tessier-Lavigne M, Okano H, Alvarez-Buylla A. 2006. New neurons follow the flow of cerebrospinal fluid in the adult brain. Science 311:629-632.
51. Seress L. 1980. Development and structure of the radial glia in the postnatal rat brain. Anat Embryol (Berl) 160:213-226.
52. Sharma HS, Johanson CE. 2007. Blood-cerebrospinal fluid barrier in hyperthermia. Prog Brain Res 162:459-478.
53. Shimogori T, Lee DA, Miranda-Angulo A, Yang Y, Wang H, Jiang L, Yoshida AC, Kataoka A, Mashiko H, Avetisyan M, Qi L, Qian J, Blackshaw S. 2010. A genomic atlas of mouse hypothalamic development. Nat Neurosci 13:767-775.
54. Simerly R. 1994. The rat nervous system. San Diego: Academic Press.
55. Spandidos A, Wang X, Wang H, Dragnev S, Thurber T, Seed B. 2008. A comprehensive collection of experimentally validated primers for polymerase chain reaction quantitation of murine transcript abundance. BMC Genomics 9:633.
56. Spandidos A, Wang X, Wang H, Seed B. 2010. PrimerBank: a resource of human and mouse PCR primer pairs for gene expression detection and quantification. Nucleic Acids Res 38:D792-D799.
57. Sternson SM. 2013. Hypothalamic survival circuits: blueprints for purposive behaviors. Neuron 77:810-824.
58. Stubbs JL, Vladar EK, Axelrod JD, Kintner C. 2012. Multicilin promotes centriole assembly and ciliogenesis during multiciliate cell differentiation. Nat Cell Biol 14:140-147.
59. Sunkin SM, Ng L, Lau C, Dolbeare T, Gilbert TL, Thompson CL, Hawrylycz M, Dang C. 2013. Allen Brain Atlas: an integrated spatio-temporal portal for exploring the central nervous system. Nucleic Acids Res 41:D996-D1008.
60. Terada K, Furukawa T. 2010. Sumoylation controls retinal progenitor proliferation by repressing cell cycle exit in Xenopus laevis. Dev Biol 347:180-194.
61. Tucker P, Laemle L, Munson A, Kanekar S, Oliver ER, Brown N, Schlecht H, Vetter M, Glaser T. 2001. The eyeless mouse mutation (ey1) removes an alternative start codon from the Rx/Rax homeobox gene. Genesis 31:43-53.
62. Voronina VA, Kozlov S, Mathers PH, Lewandoski M. 2005. Conditional alleles for activation and inactivation of the mouse Rx homeobox gene. Genesis 41:160-164.
63. Walsh RJ, Brawer JR, Lin PL. 1978. Early postnatal development of ependyma in the third ventricle of male and female rats. Am J Anat 151:377-407.
64. Xu Y, Tamamaki N, Noda T, Kimura K, Itokazu Y, Matsumoto N, Dezawa M, Ide C. 2005. Neurogenesis in the ependymal layer of the adult rat 3rd ventricle. Exp Neurol 192:251-264.
65. Yu X, Ng CP, Habacher H, Roy S. 2008. Foxj1 transcription factors are master regulators of the motile ciliogenic program. Nat Genet 40:1445-1453.