The atypical homeoprotein Pbx1a participates in the axonal pathfinding of mesencephalic dopaminergic neurons

Neural Development

Volumn 7, Issue 1, 2012, Pages

  Sgadò, Paola ^a,b   Ferretti, Elisabetta ^c   Grbec, Daniel ^b   Bozzi, Yuri ^a,d   Simon, Horst H ^b  

^a UNIVERSITY OF TRENTO   (Italy)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

^d CNR   (Italy)

Author keywords

Axonal outgrowth; Neurodegenerative disease; Prep1; Substantia nigra; Transcription factors; Ventral tegmentum

Indexed keywords

CELL SURFACE RECEPTOR; DCC PROTEIN, MOUSE; HOMEODOMAIN PROTEIN; NETRIN RECEPTORS; PBX1 PROTEIN, MOUSE; TRANSCRIPTION FACTOR; TUMOR SUPPRESSOR PROTEIN;

ANIMAL; ARTICLE; C57BL MOUSE; CYTOLOGY; DOPAMINERGIC NERVE CELL; GENE EXPRESSION REGULATION; GENETICS; MESENCEPHALON; METABOLISM; MOUSE; MOUSE MUTANT; NERVE FIBER; NEWBORN; PHYSIOLOGY;

ANIMALS; ANIMALS, NEWBORN; AXONS; DOPAMINERGIC NEURONS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; MESENCEPHALON; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, CELL SURFACE; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS;

EID: 84863106174     PISSN: None     EISSN: 17498104     Source Type: Journal    
DOI: 10.1186/1749-8104-7-24     Document Type: Article

References (56)

1. Burglin T. Analysis of TALE superclass homeobox genes (MEIS, PBC, KNOX, Iroquois, TGIF) reveals a novel domain conserved between plants and animals. Nucleic Acids Res 1997, 25:4173-4180. 10.1093/nar/25.21.4173, 147054, 9336443.
2. Laurent A, Bihan R, Omilli F, Deschamps S, Pellerin I. PBX proteins: much more than Hox cofactors. Int J Dev Biol 2008, 52:9-20. 10.1387/ijdb.072304al, 18033668.
3. Lufkin T. Transcriptional control of Hox genes in the vertebrate nervous system. Curr Opin Genet Dev 1996, 6:575-580. 10.1016/S0959-437X(96)80086-4, 8939732.
4. Gemel J, Jacobsen C, MacArthur CA. Fibroblast growth factor-8 expression is regulated by intronic engrailed and Pbx1-binding sites. J Biol Chem 1999, 274:6020-6026. 10.1074/jbc.274.9.6020, 10026229.
5. Peifer M, Wieschaus E. Mutations in the Drosophila gene extradenticle affect the way specific homeo domain proteins regulate segmental identity. Genes Dev 1990, 4:1209-1223. 10.1101/gad.4.7.1209, 1976570.
6. Moens CB, Selleri L. Hox cofactors in vertebrate development. Dev Biol 2006, 291:193-206. 10.1016/j.ydbio.2005.10.032, 16515781.
7. Selleri L, Depew MJ, Jacobs Y, Chanda SK, Tsang KY, Cheah KS, Rubenstein JL, O'Gorman S, Cleary ML. Requirement for Pbx1 in skeletal patterning and programming chondrocyte proliferation and differentiation. Development 2001, 128:3543-3557.
8. Kim SK, Selleri L, Lee JS, Zhang AY, Gu X, Jacobs Y, Cleary ML. Pbx1 inactivation disrupts pancreas development and in Ipf1-deficient mice promotes diabetes mellitus. Nat Genet 2002, 30:430-435. 10.1038/ng860, 11912494.
9. Schnabel C, Selleri L, Cleary M. Pbx1 is essential for adrenal development and urogenital differentiation. Genesis 2003, 37:123-130. 10.1002/gene.10235, 14595835.
10. Schnabel C, Godin R, Cleary M. Pbx1 regulates nephrogenesis and ureteric branching in the developing kidney. Dev Biol 2003, 254:262-276. 10.1016/S0012-1606(02)00038-6, 12591246.
11. Manley NR, Selleri L, Brendolan A, Gordon J, Cleary ML. Abnormalities of caudal pharyngeal pouch development in Pbx1 knockout mice mimic loss of Hox3 paralogs. Dev Biol 2004, 276:301-312. 10.1016/j.ydbio.2004.08.030, 15581866.
12. Brendolan A, Ferretti E, Salsi V, Moses K, Quaggin S, Blasi F, Cleary ML, Selleri L. A Pbx1-dependent genetic and transcriptional network regulates spleen ontogeny. Development 2005, 132:3113-3126. 10.1242/dev.01884, 15944191.
13. DiMartino J, Selleri L, Traver D, Firpo M, Rhee J, Warnke R, O'Gorman S, Weissman I, Cleary M. The Hox cofactor and proto-oncogene Pbx1 is required for maintenance of definitive hematopoiesis in the fetal liver. Blood 2001, 98:618-626. 10.1182/blood.V98.3.618, 11468159.
14. Sgadò P, Albéri L, Gherbassi D, Galasso SL, Ramakers GMJ, Alavian KN, Smidt MP, Dyck RH, Simon HH. Slow progressive degeneration of nigral dopaminergic neurons in postnatal Engrailed mutant mice. Proc Natl Acad Sci USA 2006, 103:15242-15247. 10.1073/pnas.0602116103, 1622807, 17015829.
15. Albéri L, Sgadò P, Simon HH. Engrailed genes are cell-autonomously required to prevent apoptosis in mesencephalic dopaminergic neurons. Development 2004, 131:3229-3236. 10.1242/dev.01128, 15175251.
16. Davis CA, Joyner AL. Expression patterns of the homeo box-containing genes En-1 and En-2 and the proto-oncogene int-1 diverge during mouse development. Genes Dev 1988, 2:1736-1744. 10.1101/gad.2.12b.1736, 2907320.
17. Joyner AL, Herrup K, Auerbach BA, Davis CA, Rossant J. Subtle cerebellar phenotype in mice homozygous for a targeted deletion of the En-2 homeobox. Science 1991, 251:1239-1243. 10.1126/science.1672471, 1672471.
18. Gosgnach S, Lanuza GM, Butt SJB, Saueressig H, Zhang Y, Velasquez T, Riethmacher D, Callaway EM, Kiehn O, Goulding M. V1 spinal neurons regulate the speed of vertebrate locomotor outputs. Nature 2006, 440:215-219. 10.1038/nature04545, 16525473.
19. Liu A, Joyner AL. EN and GBX2 play essential roles downstream of FGF8 in patterning the mouse mid/hindbrain region. Development 2001, 128:181-191.
20. Alavian KN, Scholz C, Simon HH. Transcriptional regulation of mesencephalic dopaminergic neurons: the full circle of life and death. Mov Disord 2008, 23:319-328. 10.1002/mds.21640, 18044702.
21. Erickson T, Scholpp S, Brand M, Moens CB, Waskiewicz AJ. Pbx proteins cooperate with Engrailed to pattern the midbrain-hindbrain and diencephalic-mesencephalic boundaries. Dev Biol 2007, 301:504-517. 10.1016/j.ydbio.2006.08.022, 1850147, 16959235.
22. Wagner K, Mincheva A, Korn B, Lichter P, Popperl H. Pbx4, a new Pbx family member on mouse chromosome 8, is expressed during spermatogenesis. Mech Dev 2001, 103:127-131. 10.1016/S0925-4773(01)00349-5, 11335119.
23. Saueressig H, Burrill J, Goulding M. Engrailed-1 and netrin-1 regulate axon pathfinding by association interneurons that project to motor neurons. Development 1999, 126:4201-4212.
24. Capdevila J, Tsukui T, Rodriquez Esteban C, Zappavigna V, Izpisua Belmonte JC. Control of vertebrate limb outgrowth by the proximal factor Meis2 and distal antagonism of BMPs by Gremlin. Mol Cell 1999, 4:839-849. 10.1016/S1097-2765(00)80393-7, 10619030.
25. Gonzalez-Crespo S, Morata G. Genetic evidence for the subdivision of the arthropod limb into coxopodite and telopodite. Development 1996, 122:3921-3928.
26. Morata G. How Drosophila appendages develop. Nat Rev Mol Cell Biol 2001, 2:89-97.
27. Ryoo HD, Marty T, Casares F, Affolter M, Mann RS. Regulation of Hox target genes by a DNA bound Homothorax/Hox/Extradenticle complex. Development 1999, 126:5137-5148.
28. Abu-Shaar M, Ryoo H, Mann R. Control of the nuclear localization of Extradenticle by competing nuclear import and export signals. Genes Dev 1999, 13:935-945. 10.1101/gad.13.8.935, 316638, 10215621.
29. Berthelsen J, Kilstrup-Nielsen C, Blasi F, Mavilio F, Zappavigna V. The subcellular localization of PBX1 and EXD proteins depends on nuclear import and export signals and is modulated by association with PREP1 and HTH. Genes Dev 1999, 13:946-953. 10.1101/gad.13.8.946, 316640, 10215622.
30. Mercader N, Leonardo E, Azpiazu N, Serrano A, Morata G, Martinez C, Torres M. Conserved regulation of proximodistal limb axis development by Meis1/Hth. Nature 1999, 402:425-429. 10.1038/46580, 10586884.
31. Jaw TJ, You LR, Knoepfler PS, Yao LC, Pai CY, Tang CY, Chang LP, Berthelsen J, Blasi F, Kamps MP, Sun YH. Direct interaction of two homeoproteins, homothorax and extradenticle, is essential for EXD nuclear localization and function. Mech Dev 2000, 91:279-291. 10.1016/S0925-4773(99)00316-0, 10704852.
32. Kilstrup-Nielsen C, Alessio M, Zappavigna V. PBX1 nuclear export is regulated independently of PBX-MEINOX interaction by PKA phosphorylation of the PBC-B domain. EMBO J 2003, 22:89-99. 10.1093/emboj/cdg010, 140055, 12505987.
33. Toresson H, Parmar M, Campbell K. Expression of Meis and Pbx genes and their protein products in the developing telencephalon: implications for regional differentiation. Mech Dev 2000, 94:183-187. 10.1016/S0925-4773(00)00324-5, 10842069.
34. Hu Z, Cooper M, Crockett D, Zhou R. Differentiation of the midbrain dopaminergic pathways during mouse development. J Comp Neurol 2004, 476:301-311. 10.1002/cne.20230, 15269972.
35. Lin L, Rao Y, Isacson O. Netrin-1 and slit-2 regulate and direct neurite growth of ventral midbrain dopaminergic neurons. Mol Cell Neurosci 2005, 28:547-555. 10.1016/j.mcn.2004.11.009, 15737744.
36. Xu B, Goldman JS, Rymar VV, Forget C, Lo PS, Bull SJ, Vereker E, Barker PA, Trudeau LE, Sadikot AF, Kennedy TE. Critical roles for the netrin receptor deleted in colorectal cancer in dopaminergic neuronal precursor migration, axon guidance, and axon arborization. Neuroscience 2010, 169:932-949. 10.1016/j.neuroscience.2010.05.025, 20493932.
37. Kennedy TE. Cellular mechanisms of netrin function: long-range and short-range actions. Biochem Cell Biol 2000, 78:569-575. 10.1139/o00-079, 11103947.
38. Livesey FJ, Hunt SP. Netrin and netrin receptor expression in the embryonic mammalian nervous system suggests roles in retinal, striatal, nigral, and cerebellar development. Mol Cell Neurosci 1997, 8:417-429. 10.1006/mcne.1997.0598, 9143559.
39. Zetterstrom RH, Williams R, Perlmann T, Olson L. Cellular expression of the immediate early transcription factors Nurr1 and NGFI-B suggests a gene regulatory role in several brain regions including the nigrostriatal dopamine system. Brain Res Mol Brain Res 1996, 41:111-120.
40. Simon HH, Saueressig H, Wurst W, Goulding MD, O'Leary DD. Fate of midbrain dopaminergic neurons controlled by the engrailed genes. J Neurosci 2001, 21:3126-3134.
41. Smidt M, Asbreuk C, Cox J, Chen H, Johnson R, Burbach J. A second independent pathway for development of mesencephalic dopaminergic neurons requires Lmx1b. Nat Neurosci 2000, 3:337-341. 10.1038/73902, 10725922.
42. Smidt M, Van Schaick H, Lanctot C, Tremblay J, Cox J, Van DKA, Wolterink G, Drouin J, Burbach J. A homeodomain gene Ptx3 has highly restricted brain expression in mesencephalic dopaminergic neurons. Proc Natl Acad Sci U S A 1997, 94:13305-13310. 10.1073/pnas.94.24.13305, 24304, 9371841.
43. Nosrat C, Tomac A, Hoffer B, Olson L. Cellular and developmental patterns of expression of Ret and glial cell line-derived neurotrophic factor receptor alpha mRNAs. Exp Brain Res 1997, 115:410-422. 10.1007/PL00005711, 9262196.
44. McCaffery P, Drager UC. High levels of a retinoic acid-generating dehydrogenase in the meso-telencephalic dopamine system. Proc Natl Acad Sci U S A 1994, 91:7772-7776. 10.1073/pnas.91.16.7772, 44484, 8052659.
45. Rhee JW, Arata A, Selleri L, Jacobs Y, Arata S, Onimaru H, Cleary ML. Pbx3 deficiency results in central hypoventilation. Am J Pathol 2004, 165:1343-1350. 10.1016/S0002-9440(10)63392-5, 1618620, 15466398.
46. Selleri L, DiMartino J, van Deursen J, Brendolan A, Sanyal M, Boon E, Capellini T, Smith KS, Rhee J, Pöpperl H, Grosveld G, Cleary ML. The TALE homeodomain protein Pbx2 is not essential for development and long-term survival. Mol Cell Biol 2004, 24:5324-5331. 10.1128/MCB.24.12.5324-5331.2004, 419882, 15169896.
47. Roberts V, van Dijk M, Murre C. Localization of Pbx1 transcripts in developing rat embryos. Mech Dev 1995, 51:193-198. 10.1016/0925-4773(95)00364-9, 7547467.
48. Bagri A, Marín O, Plump AS, Mak J, Pleasure SJ, Rubenstein JLR, Tessier-Lavigne M. Slit proteins prevent midline crossing and determine the dorsoventral position of major axonal pathways in the mammalian forebrain. Neuron 2002, 33:233-248. 10.1016/S0896-6273(02)00561-5, 11804571.
49. Dugan JP, Stratton A, Riley HP, Farmer WT, Mastick GS. Midbrain dopaminergic axons are guided longitudinally through the diencephalon by Slit/Robo signals. Mol Cell Neurosci 2011, 46:347-356. 10.1016/j.mcn.2010.11.003, 3021181, 21118670.
50. Comoletti D, De Jaco A, Jennings LL, Flynn RE, Gaietta G, Tsigelny I, Ellisman MH, Taylor P. The Arg451Cys-neuroligin-3 mutation associated with autism reveals a defect in protein processing. J Neurosci 2004, 24:4889-4893. 10.1523/JNEUROSCI.0468-04.2004, 15152050.
51. Hammond R, Blaess S, Abeliovich A. Sonic hedgehog is a chemoattractant for midbrain dopaminergic axons. PLoS One 2009, 4:e7007. 10.1371/journal.pone.0007007, 2742719, 19774071.
52. Kolk SM, Gunput R-AF, Tran TS, van den Heuvel DMA, Prasad AA, Hellemons AJCGM, Adolfs Y, Ginty DD, Kolodkin AL, Burbach JPH, Smidt MP, Pasterkamp RJ. Semaphorin 3 F is a bifunctional guidance cue for dopaminergic axons and controls their fasciculation, channeling, rostral growth, and intracortical targeting. J Neurosci 2009, 29:12542-12557. 10.1523/JNEUROSCI.2521-09.2009, 3097132, 19812329.
53. Vives J, Sasajala P, Chang KH, Zhao S, Li M. A mouse model for tracking nigrostriatal dopamine neuron axon growth. Genesis 2008, 46:125-131. 10.1002/dvg.20375, 18327786.
54. Stein E, Tessier-Lavigne M. Hierarchical organization of guidance receptors: silencing of netrin attraction by slit through a Robo/DCC receptor complex. Science 2001, 291:1928-1938. 10.1126/science.1058445, 11239147.
55. Lesnick TG, Papapetropoulos S, Mash DC, Ffrench-Mullen J, Shehadeh L, de Andrade M, Henley JR, Rocca WA, Ahlskog JE, Maraganore DM. A genomic pathway approach to a complex disease: axon guidance and Parkinson disease. PLoS Genet 2007, 3:e98. 10.1371/journal.pgen.0030098, 1904362, 17571925.
56. Lin L, Lesnick TG, Maraganore DM, Isacson O. Axon guidance and synaptic maintenance: preclinical markers for neurodegenerative disease and therapeutics. Trends Neurosci 2009, 32:142-149. 10.1016/j.tins.2008.11.006, 2954610, 19162339.