Axon responses of embryonic stem cell-derived dopaminergic neurons to semaphorins 3A and 3C

Journal of Neuroscience Research

Volumn 88, Issue 5, 2010, Pages 971-980

  Tamariz, Elisa ^a   Díaz Martínez, N Emmanuel ^b   Díaz, Néstor F ^b   García Peña, Claudia M ^a   Velasco, Iván ^b   Varela Echavarría, Alfredo ^a  

^a INSTITUTO DE NEUROBIOLOGÍA   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Collagen gels; Dopamine neurons; Embryonic stem cells; Neuropilin; Semaphorins

Indexed keywords

BLOCKING ANTIBODY; NEUROPILIN 1; NEUROPILIN 2; PROTEIN ANTIBODY; SEMAPHORIN; SEMAPHORIN 3A; SEMAPHORIN 3C; SEMAPHORIN 3F; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG;

ARTICLE; CELL TRANSPLANTATION; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DRUG EXPOSURE; EMBRYO; EMBRYONIC STEM CELL; HUMAN; HUMAN CELL; MESENCEPHALON; NERVE FIBER; NERVE FIBER GROWTH; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ANIMALS; ANTIBODIES, NEUTRALIZING; CELL DIFFERENTIATION; CELL LINE; CELLS, CULTURED; DOPAMINE; EMBRYONIC STEM CELLS; GRAFT SURVIVAL; GROWTH CONES; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; NERVE TISSUE PROTEINS; NEUROGENESIS; NEUROPILINS; PARKINSON DISEASE; PHENOTYPE; RATS; RATS, WISTAR; SEMAPHORIN-3A; SEMAPHORINS; STEM CELL TRANSPLANTATION; SUBSTANTIA NIGRA;

EID: 77950144041     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22268     Document Type: Article

References (40)

1. Bagri A, Marin O, Plump AS, Mak J, Pleasure SJ, Rubenstein JL, Tessier-Lavigne M. 2002. Slit proteins prevent midline crossing and determine the dorsoventral position of major axonal pathways in the mammalian forebrain. Neuron 33:233-248.
2. Barberi T, Klivenyi P, Calingasan NY, Lee H, Kawamata H, Loonam K, Perrier AL, Bruses J, Rubio ME, Topf N, Tabar V, Harrison NL, Beal MF, Moore MA, Studer L. 2003. Neural subtype specification of fertilization and nuclear transfer embryonic stem cells and application in parkinsonian mice. Nat Biotechnol 21:1200-1207.
3. Bartlett LE, Mendez I. 2005. Dopaminergic reinnervation of the globus pallidus by fetal nigral grafts in the rodent model of Parkinson's disease. Cell Transplant 14:119-127.
4. Chauvet S, Cohen S, Yoshida Y, Fekrane L, Livet J, Gayet O, Segu L, Buhot MC, Jessell TM, Henderson CE, Mann F. 2007. Gating of Sema3E/plexinD1 signaling by neuropilin-1 switches axonal repulsion to attraction during brain development. Neuron 56:807-822.
5. Chen H, Chedotal A, He Z, Goodman CS, Tessier-Lavigne M. 1997. Neuropilin-2, a novel member of the neuropilin family, is a high affinity receptor for the semaphorins Sema E and Sema IV but not Sema III. Neuron 19:547-559.
6. Diaz NF, Guerra-Arraiza C, Diaz-Martinez NE, Salazar P, Molina-Hernandez A, Camacho-Arroyo I, Velasco I. 2007. Changes in the content of estrogen alpha and progesterone receptors during differentiation of mouse embryonic stem cells to dopamine neurons. Brain Res Bull 73:75-80.
7. Diaz NF, Diaz-Martinez NE, Camacho-Arroyo I, Velasco I. 2009. Estradiol promotes proliferation of dopaminergic precursors resulting in a higher proportion of dopamine neurons derived from mouse embryonic stem cells. Int J Dev Neurosci 27:493-500.
8. Dunnett SB, Rogers DC, Richards SJ. 1989. Nigrostriatal reconstruction after 6-OHDA lesions in rats: combination of dopamine-rich nigral grafts and nigrostriatal "bridge" grafts. Exp Brain Res 75:523-535.
9. He Z, Tessier-Lavigne M. 1997. Neuropilin is a receptor for the axonal chemorepellent semaphorin III. Cell 90:739-751.
10. Hernandez-Montiel HL, Tamariz E, Sandoval-Minero MT, Varela-Echavarria A. 2008. Semaphorins 3A, 3C, and 3F in mesencephalic dopaminergic axon pathfinding. J Comp Neurol 506:387-397.
11. Isacson O, Bjorklund LM, Schumacher JM. 2003. Toward full restoration of synaptic and terminal function of the dopaminergic system in Parkinson's disease by stem cells. Ann Neurol 53(Suppl 3):S135-S146; discussion S146-S148.
12. Kawasaki H, Mizuseki K, Nishikawa S, Kaneko S, Kuwana Y, Nakanishi S, Nishikawa SI, Sasai Y. 2000. Induction of midbrain dopaminergic neurons from ES cells by stromal cell-derived inducing activity. Neuron 28:31-40.
13. Kim JH, Auerbach JM, Rodriguez-Gomez JA, Velasco I, Gavin D, Lumelsky N, Lee SH, Nguyen J, Sanchez-Pernaute R, Bankiewicz K, McKay R. 2002. Dopamine neurons derived from embryonic stem cells function in an animal model of Parkinson's disease. Nature 418:50-56.
14. Kitsukawa T, Shimizu M, Sanbo M, Hirata T, Taniguchi M, Bekku Y, Yagi T, Fujisawa H. 1997. Neuropilin-semaphorin III/D-mediated chemorepulsive signals play a crucial role in peripheral nerve projection in mice. Neuron 19:995-1005.
15. Kolodkin AL, Levengood DV, Rowe EG, Tai YT, Giger RJ, Ginty DD. 1997. Neuropilin is a semaphorin III receptor. Cell 90:753-762.
16. Koncina E, Roth L, Gonthier B, Bagnard D. 2007. Role of semaphorins during axon growth and guidance. Adv Exp Med Biol 621:50-64.
17. Lee SH, Lumelsky N, Studer L, Auerbach JM, McKay RD. 2000. Efficient generation of midbrain and hindbrain neurons from mouse embryonic stem cells. Nat Biotechnol 18:675-679.
18. Lin L, Isacson O. 2006. Axonal growth regulation of fetal and embryonic stem cell-derived dopaminergic neurons by netrin-1 and slits. Stem Cells 24:2504-2513.
19. Lin L, Rao Y, Isacson O. 2005. Netrin-1 and slit-2 regulate and direct neurite growth of ventral midbrain dopaminergic neurons. Mol Cell Neurosci 28:547-555.
20. Lindvall O, Kokaia Z. 2006. Stem cells for the treatment of neurological disorders. Nature 441:1094-1096.
21. Livesey FJ, Hunt SP. 1997. Netrin and netrin receptor expression in the embryonic mammalian nervous system suggests roles in retinal, striatal, nigral, and cerebellar development. Mol Cell Neurosci 8:417-429.
22. Marillat V, Cases O, Nguyen-Ba-Charvet KT, Tessier-Lavigne M, Sotelo C, Chedotal A. 2002. Spatiotemporal expression patterns of slit and robo genes in the rat brain. J Comp Neurol 442:130-155.
23. Mendez I, Sadi D, Hong M. 1996. Reconstruction of the nigrostriatal pathway by simultaneous intrastriatal and intranigral dopaminergic transplants. J Neurosci 16:7216-7227.
24. Neufeld G, Lange T, Varshavsky A, Kessler O. 2007. Semaphorin signaling in vascular and tumor biology. Adv Exp Med Biol 600:118-131.
25. Parmar M, Li M. 2007. Early specification of dopaminergic phenotype during ES cell differentiation. BMC Dev Biol 7:86.
26. Pasterkamp RJ, Kolodkin AL. 2003. Semaphorin junction: making tracks toward neural connectivity. Curr Opin Neurobiol 13:79-89.
27. Rodriguez-Gomez JA, Lu JQ, Velasco I, Rivera S, Zoghbi SS, Liow JS, Musachio JL, Chin FT, Toyama H, Seidel J, Green MV, Thanos PK, Ichise M, Pike VW, Innis RB, McKay RD. 2007. Persistent dopamine functions of neurons derived from embryonic stem cells in a rodent model of Parkinson disease. Stem Cells 25:918-928.
28. Roy NS, Cleren C, Singh SK, Yang L, Beal MF, Goldman SA. 2006. Functional engraftment of human ES cell-derived dopaminergic neurons enriched by coculture with telomerase-immortalized midbrain astrocytes. Nat Med 12:1259-1268.
29. Shintani A, Nakao N, Kakishita K, Itakura T. 2008. Generation of dopamine neurons from embryonic stem cells in the presence of the neuralizing activity of bone marrow stromal cells derived from adult mice. J Neurosci Res 86:2829-2838.
30. Sieber BA, Kuzmin A, Canals JM, Danielsson A, Paratcha G, Arenas E, Alberch J, Ogren SO, Ibanez CF. 2004. Disruption of EphA/ephrin-a signaling in the nigrostriatal system reduces dopaminergic innervation and dissociates behavioral responses to amphetamine and cocaine. Mol Cell Neurosci 26:418-428.
31. Smidt MP, Burbach JP. 2007. How to make a mesodiencephalic dopaminergic neuron. Nat Rev Neurosci 8:21-32.
32. Soldner F, Hockemeyer D, Beard C, Gao Q, Bell GW, Cook EG, Hargus G, Blak A, Cooper O, Mitalipova M, Isacson O, Jaenisch R. 2009. Parkinson's disease patient-derived induced pluripotent stem cells free of viral reprogramming factors. Cell 136:964-977.
33. Suzuki K, Kumanogoh A, Kikutani H. 2008. Semaphorins and their receptors in immune cell interactions. Nat Immunol 9:17-23.
34. Takahashi T, Nakamura F, Jin Z, Kalb RG, Strittmatter SM. 1998. Semaphorins A and E act as antagonists of neuropilin-1 and agonists of neuropilin-2 receptors. Nat Neurosci 1:487-493.
35. Tropepe V, Hitoshi S, Sirard C, Mak TW, Rossant J, van der Kooy D. 2001. Direct neural fate specification from embryonic stem cells: a primitive mammalian neural stem cell stage acquired through a default mechanism. Neuron 30:65-78.
36. Wernig M, Zhao JP, Pruszak J, Hedlund E, Fu D, Soldner F, Broccoli V, Constantine-Paton M, Isacson O, Jaenisch R. 2008. Neurons derived from reprogrammed fibroblasts functionally integrate into the fetal brain and improve symptoms of rats with Parkinson's disease. Proc Natl Acad Sci U S A 105:5856-5861.
37. Yamamoto N, Tamada A, Murakami F. 2002. Wiring of the brain by a range of guidance cues. Prog Neurobiol 68:393-407.
38. Yue Y, Widmer DA, Halladay AK, Cerretti DP, Wagner GC, Dreyer JL, Zhou R. 1999. Specification of distinct dopaminergic neural pathways: roles of the Eph family receptor EphB1 and ligand ephrin-B2. J Neurosci 19:2090-2101.
39. Yurek DM, Fletcher-Turner A. 2004. Comparison of embryonic stem cell-derived dopamine neuron grafts and fetal ventral mesencephalic tissue grafts: morphology and function. Cell Transplant 13:295-306.
40. Zhao S, Maxwell S, Jimenez-Beristain A, Vives J, Kuehner E, Zhao J, O'Brien C, de Felipe C, Semina E, Li M. 2004. Generation of embryonic stem cells and transgenic mice expressing green fluorescence protein in midbrain dopaminergic neurons. Eur J Neurosci 19:1133-1140.