Podocalyxin is a novel polysialylated neural adhesion protein with multiple roles in neural development and synapse formation

PLoS ONE

Volumn 5, Issue 8, 2010, Pages

  Vitureira, Nathalia ^a,b,c   Andrés, Rosa ^a,b,c   Pérez Martínez, Esther ^a,b,c   Martínez, Albert ^a,b,c   Bribián, Ana ^a,b,c,d   Blasi, Juan ^c   Chelliah, Shierley ^e   López Doménech, Guillermo ^a,b,c   de Castro, Fernando ^d   Burgaya, Ferran ^a,b,c   McNagny, Kelly ^e   Soriano, Eduardo ^a,b,c  

^a INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^b CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

^c UNIVERSITY OF BARCELONA   (Spain)

^d HOSPITAL NACIONAL DE PARAPLÉJICOS   (Spain)

^e UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

EZRIN; PODOCALYXIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SODIUM PROTON EXCHANGE PROTEIN; SODIUM PROTON EXCHANGER REGULATORY FACTOR 1; SODIUM PROTON EXCHANGER REGULATORY FACTOR 2; UNCLASSIFIED DRUG; CYTOSKELETON PROTEIN; GUANOSINE TRIPHOSPHATASE; NERVE CELL ADHESION MOLECULE; PHOSPHOPROTEIN; RHOG PROTEIN, MOUSE; SIALIC ACID DERIVATIVE; SIALOGLYCOPROTEIN; SODIUM HYDROGEN EXCHANGER REGULATORY FACTOR; SODIUM-HYDROGEN EXCHANGER REGULATORY FACTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BRAIN NERVE CELL; CONTROLLED STUDY; EMBRYO; IN VITRO STUDY; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN INTERACTION; SYNAPSE; SYNAPTOGENESIS; ANIMAL; BRAIN; CYTOLOGY; FEMALE; GENE EXPRESSION REGULATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NEURITE; PHYSIOLOGY; PREGNANCY;

MUS;

ANIMALS; BRAIN; CYTOSKELETAL PROTEINS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GTP PHOSPHOHYDROLASES; MICE; NEURAL CELL ADHESION MOLECULES; NEURITES; PHOSPHOPROTEINS; PREGNANCY; RHOA GTP-BINDING PROTEIN; SIALIC ACIDS; SIALOGLYCOPROTEINS; SODIUM-HYDROGEN ANTIPORTER; SYNAPSES;

EID: 77957786825     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0012003     Document Type: Article

References (65)

1. Mann F, Chauvet S, Rougon G (2007) Semaphorins in development and adult brain: Implication for neurological diseases. Prog Neurobiol 82: 57-79.
2. Round J, Stein E (2007) Netrin signaling leading to directed growth cone steering. Curr Opin Neurobiol 17: 15-21.
3. Tessier-Lavigne M, Goodman CS (1996) The molecular biology of axon guidance. Science 274: 1123-1133.
4. Holmberg J, Clarke DL, Frisen J (2000) Regulation of repulsion versus adhesion by different splice forms of an Eph receptor. Nature 408: 203-206.
5. Wilkinson DG (2001) Multiple roles of EPH receptors and ephrins in neural development. Nat Rev Neurosci 2: 155-164.
6. Castellani V, Chedotal A, Schachner M, Faivre-Sarrailh C, Rougon G (2000) Analysis of the L1-deficient mouse phenotype reveals cross-talk between Sema3A and L1 signaling pathways in axonal guidance. Neuron 27: 237-249.
7. Maness PF, Schachner M (2007) Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration. Nat Neurosci 10: 19-26.
8. Seki T, Rutishauser U (1998) Removal of polysialic acid-neural cell adhesion molecule induces aberrant mossy fiber innervation and ectopic synaptogenesis in the hippocampus. J Neurosci 18: 3757-3766.
9. Stoeckli ET, Landmesser LT (1995) Axonin-1, Nr-CAM, and Ng-CAM play different roles in the in vivo guidance of chick commissural neurons. Neuron 14: 1165-1179.
10. Tomasiewicz H, Ono K, Yee D, Thompson C, Goridis C, et al. (1993) Genetic deletion of a neural cell adhesion molecule variant (N-CAM-180) produces distinct defects in the central nervous system. Neuron 11: 1163-1174.
11. Castellani V, De Angelis E, Kenwrick S, Rougon G (2002) Cis and trans interactions of L1 with neuropilin-1 control axonal responses to semaphorin 3A. Embo J 21: 6348-6357.
12. Paratcha G, Ledda F, Ibañez CF (2003) The neural cell adhesion NCAM is an alternative signalling receptor for GDNF family ligands. Cell 113: 867-879.
13. Garcia-Frigola C, Burgaya F, Calbet M, Lopez-Domenech G, de Lecea L, et al. (2004) A collection of cDNAs enriched in upper cortical layers of the embryonic mouse brain. Brain Res Mol Brain Res 122: 133-150.
14. Vitureira N, McNagny K, Soriano E, Burgaya F (2005) Pattern of expression of the podocalyxin gene in the mouse brain during development. Gene Expr Patterns 5: 349-354.
15. Kershaw D, Beck SG, Wharram BL, Wiggins JE, Goyal M, et al. (1997) Molecular cloning and characterization of human podocalyxin - like protein: orthologous relationship to rabbit PCLP1 and rat podocalyxin. J Biol Chem 272: 15708-15714.
16. Kershaw D, Thomas P, Wharram M, Goyal J, Wiggins C, et al. (1995) Molecular cloning, expression and characterization of podocalyxin-like protein 1 from rabbit as a transmembrane protein of glomerular podocytes and vascular endothelium. J Biol Chem 270: 29439-29446.
17. Takeda T, Go WT, Orlando RA, Farquhar MG (2000) Expression of Podocalyxin inhibits cell-cell adhesion and modifies junctional properties in Madin-darby Canine Kidney Cells. Molecular Biology of the Cell 11: 3291-3232.
18. Takeda T, McQuistan T, Orlando RA, Farquhar MG (2001) Loss of glomerular foot process is associated with uncoupling of podocalyxin from the actin cytoskeleton. J Clin Invest 108: 289-301.
19. Doyonnas R, Kershaw DB, Duhme C, Merkens H, Chelliah S, et al. (2001) Anuria, omphalocele, and perinatal lethality in mice lacking the CD34-related protein podocalyxin. J Exp Med 194: 13-27.
20. Kershaw D, Thomas P, Wharram M, Goyal J, Wiggins C, et al. (1995) Molecular cloning, expression and characterization of podocalyxin-like protein 1 from rabbit as a transmembrane preotein of glomerular podocytes and vascular endothelium. J Biol Chem 270: 29439-29446.
21. McNagny KI, Pettersson F, Rossi I, Flamme A, Shevchenko A, et al. (1997) Thrombomucin, a novel cell surface protein that defines thrombocytes and multipotent hematopoietic preogenitors. J Cell Biol 138: 1395-1407.
22. Miettinen A, Solin ML, Reivinen J, Juvonen E, Vaisanen R (1999) Podocalyxin in rat platelets and megakaryocytes. Am J Pathol 154: 813-822.
23. Sassetti C, Tangemann K, Singer MS, Kershaw DB, Rosen SD (1998) Identification of podocalyxin-like protein as a high endothelial venule ligand for L-selectin: parallels to CD34. J Exp Med 187: 1965-1975.
24. Somasiri A, Nielsen JS, Makretsov N, McCoy ML, Prentice L, et al. (2004) Overexpression of the anti-adhesin podocalyxin is an independent predictor of breast cancer progression. Cancer Res 64: 5068-5073.
25. Takeda T (2003) Podocyte cytoskeleton is connected to the integral membrane protein podocalyxin through Na+/H+-exchanger regulatory factor 2 and ezrin. Clin Exp Nephrol 7: 260-269.
26. Angata K, Huckaby V, Ranscht B, Terskikh A, Marth JD, et al. (2007) Polysialic acid-directed migration and differentiation of neural precursors are essential for mouse brain development. Mol Cell Biol 27: 6659-6668.
27. Eckardt M, Bukalo O, Chazal G, Wang L, Goridis C, et al. (2000) Mice deficient in the polysialyltransferase ST8SialIV/PST-1 allow discrimination of the roles of the neural cell adhesion molecule protein and polysialic in neural development and plasticity. The Journal of Neuroscience 20: 5234-5244.
28. Kiss JZ, Rougon G (1997) Cell biology of polysialic acid. Curr Opin Neurobiol 7: 640-646.
29. Rodriguez RB, Butta N, Larrucea S, Alonso S, Parrilla R (2006) Production and characterization of murine monoclonal antibodies against human podocalyxin. Tissue Antigens 68: 407-417.
30. Hara T, Nakano Y, Tanaka M, Tamura K, Sekiguchi T, et al. (1999) Identification of podocalyxin-like protein 1 as a novel cell surface marker of hemangioblasts in the murine aorta-gonad-mesonephros region. Immunity 11: 567-578.
31. Dekan G, Gabel C, Farquhar MG (1991) Sulfate contributes to the negative charge of podocalyxin, the major sialoglycoprotein of the glomerular filtration slit. Proc Natl Acad Sci USA 88: 5398-5402.
32. Kleene R, Schachner M (2004) Glycans and neural cell interactions. Nat Rev Neurosci 5: 195-208.
33. Orlando RA, Takeda T, Zak B, Schmieder S, Benoit VM, et al. (2001) The glomerular epithelial cell anti.adhesin podocalyxin associates with the actin cytoskeleton through interactions with ezrin. J Am Soc Nephrol 12: 1589-1598.
34. Schmieder S, Nagai M, Orlando RA, Takeda T, Farquhar MG (2004) Podocalyxin activates RhoA and induces actin reorganization through NHERF1 and Ezrin in MDCK cells. J Am Soc Nephrol 15: 2289-2298.
35. Hevner RF, Shi L, Justice N, Hsueh Y, Sheng M, et al. (2001) Tbr1 regulates differentiation of the preplate and layer 6. Neuron 29: 353-366.
36. Alcantara S, Ruiz M, De Castro F, Soriano E, Sotelo C (2000) Netrin 1 acts as an attractive or as a repulsive cue for distinct migrating neurons during the development of the cerebellar system. Development 127: 1359-1372.
37. Sotelo C, Chedotal A (2005) Development of the olivocerebellar system: migration and formation of cerebellar maps. Prog Brain Res 148: 1-20.
38. Yee KT, Simon HH, Tessier-Lavigne M, O'Leary DM (1999) Extension of long leading processes and neuronal migration in the mammalian brain directed by the chemoattractant netrin-1. Neuron 24: 607-622.
39. Dalva MB, McClelland AC, Kayser MS (2007) Cell adhesion molecules: signalling functions at the synapse. Nat Rev Neurosci 8: 206-220.
40. Dityatev A, Dityateva G, Sytnyk V, Delling M, Toni N, et al. (2004) Polysialylated neural cell adhesion molecule promotes remodeling and formation of hippocampal synapses. J Neurosci 24: 9372-9382.
41. Nielsen JS, McNagny KM (2008) Novel functions of the CD34 family. J Cell Sci 121: 3683-3692.
42. Cremer H, Lange R, Christoph A, Plomann M, Vopper G, et al. (1994) Inactivation of the N-CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning. Nature 367: 455-459.
43. Ono K, Tomasiewicz H, Magnuson T, Rutishauser U (1994) N-CAM mutation inhibits tangential neuronal migration and is phenocopied by enzymatic removal of polysialic acid. Neuron 13: 595-609.
44. Cohen-Cory S, Fraser SE (1995) Effects of brain-derived neurotrophic factor on optic axon branching and remodelling in vivo. Nature 378: 192-196.
45. Dent EW, Barnes AM, Tang F, Kalil K (2004) Netrin-1 and semaphorin 3A promote or inhibit cortical axon branching, respectively, by reorganization of the cytoskeleton. J Neurosci 24: 3002-3012.
46. Tang F, Kalil K (2005) Netrin-1 induces axon branching in developing cortical neurons by frequency-dependent calcium signaling pathways. J Neurosci 25: 6702-6715.
47. Lee T, Winter C, Marticke SS, Lee A, Luo L (2000) Essential roles of Drosophila RhoA in the regulation of neuroblast proliferation and dendritic but not axonal morphogenesis. Neuron 25: 307-316.
48. Li Z, Van Aelst L, Cline HT (2000) Rho GTPases regulate distinct aspects of dendritic arbor growth in Xenopus central neurons in vivo. Nat Neurosci 3: 217-225.
49. Tan P, Hughes M, Bains J, Wong J, Nielsen J, et al. (2010) Podocalyxin Associates with CXCR4 and Modulates Hematopoietic Cell Migration.
50. Cremer H, Chazal G, Goridis C, Represa A (1997) NCAM is essential for axonal growth ans fasciculation in the hippocampus. Molecular and Cellular Neuroscience 8: 232.
51. Wiencken-Barger AE, Mavity-Hudson J, Bartsch U, Schachner M, Casagrande VA (2004) The role of L1 in axon pathfinding and fasciculation. Cereb Cortex 14: 121-131.
52. Rolf B, Bastmeyer M, Schanchner M, Bartsch U (2002) Pathfinding errors of corticospinal axons in neural cell adhesion molecule-deficient mice. The Journal of Neuroscience 22: 8357-8362.
53. Weinhold B, Seidenfaden R, Rockle I, Muhlenhoff M, Schertzinger F, et al. (2005) Genetic ablation of polysialic acid causes severe neurodevelopmental defects rescued by deletion of the neural cell adhesion molecule. J Biol Chem 280: 42971-42977.
54. Bukalo O, Fentrop N, Lee AY, Salmen B, Law JW, et al. (2004) Conditional ablation of the neural cell adhesion molecule reduces precision of spatial learning, long-term potentiation, and depression in the CA1 subfield of mouse hippocampus. J Neurosci 24: 1565-1577.
55. Muller D, Wang C, Skibo G, Toni N, Cremer H, et al. (1996) PSA-NCAM is required for activity-induced synaptic plasticity. Neuron 17: 413-422.
56. Senkov O, Sun M, Weinhold B, Gerardy-Schahn R, Schachner M, et al. (2006) Polysialylated neural cell adhesion molecule is involved in induction of long-term potentiation and memory acquisition and consolidation in a fear-conditioning paradigm. J Neurosci 26: 10888-109898.
57. Dityatev A, Dityateva G, Schachner M (2000) Synaptic strength as a function of post-versus presynaptic expression of the neural cell adhesion molecule NCAM. Neuron 26: 207-217.
58. Moscoso LM, Cremer H, Sanes JR (1998) Organization and reorganization of neuromuscular junctions in mice lacking neural cell adhesion molecule, tenascin-C, or fibroblast growth factor-5. J Neurosci 18: 1465-1477.
59. Packard M, Mathew D, Budnik V (2003) FASt remodeling of synapses in Drosophila. Curr Opin Neurobiol 13: 527-534.
60. Mayford M, Barzilai A, Keller F, Schacher S, Kandel ER (1992) Modulation of an NCAM-related adhesion molecule with long-term synaptic plasticity in Aplysia. Science 256: 638-644.
61. Di Cristo G, Chattopadhyaya B, Kuhlman SJ, Fu Y, Belanger MC, et al. (2007) Activity-dependent PSA expression regulates inhibitory maturation and onset of critical period plasticity. Nat Neurosci 10: 1569-1577.
62. Vicario-Abejon C, Owens D, McKay R, Segal M (2002) Role of neurotrophins in central synapse formation and stabilization. Nat Rev Neurosci 3: 965-974.
63. Del Rio JA, Heimrich B, Borrell V, Forster E, Drakew A, et al. (1997) A role for Cajal-Retzius cells and reelin in the development of hippocampal connections. Nature 385: 70-74.
64. Stoppini L, Buchs PA, Muller D (1991) A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 37: 173-182.
65. Soriano E, Del Rio JA, Martinez-Guijarro FJ, Ferrer I, Lopez C (1991) Immunocytochemical detection of 59-bromodeoxyuridine in fluoro-gold-labeled neurons: a simple technique to combine retrograde axonal tracing and neurogenetic characterization of neurons. J Histochem Cytochem 39: 1565-1570.