Nonyloxytryptamine mimics polysialic acid and modulates neuronal and glial functions in cell culture

Journal of Neurochemistry

Volumn 128, Issue 1, 2014, Pages 88-100

  Loers, Gabriele ^a   Saini, Vedangana ^b   Mishra, Bibhudatta ^a,g   Papastefanaki, Florentia ^c   Lutz, David ^a   Chaudhury, Sidhartha ^d   Ripoll, Daniel R ^d   Wallqvist, Anders ^d   Gul, Sheraz ^e   Schachner, Melitta ^a,f   Kaur, Gurcharan ^b  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b GURU NANAK DEV UNIVERSITY   (India)

^c HELLENIC PASTEUR INSTITUTE   (Greece)

^d U S ARMY MEDICAL RESEARCH AND MATERIEL COMMAND   (United States)

^e European Screeningport GmbH   (Germany)

^f RUTGERS UNIVERSITY   (United States)

^g UNIVERSITY OF MICHIGAN   (United States)

Author keywords

5 nonyloxytryptamine oxalate; migration; neural cell adhesion molecule; neurite outgrowth; polysialic acid; scratch injury

Indexed keywords

5 NONYLOXYTRYPTAMINE OXALATE; MICROTUBULE ASSOCIATED PROTEIN 2; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 735; NERVE CELL ADHESION MOLECULE; POLYSIALIC ACID; SEROTONIN AGONIST; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; ASTROCYTE; CELL FUNCTION; CELL MIGRATION; CONTROLLED STUDY; FEMALE; GLIA CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; MOUSE; MYELINATION; NERVE CELL; NERVE CELL CULTURE; NERVE FIBER GROWTH; NEUROMODULATION; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCHWANN CELL;

5-NONYLOXYTRYPTAMINE OXALATE; MIGRATION; NEURAL CELL ADHESION MOLECULE; NEURITE OUTGROWTH; POLYSIALIC ACID; SCRATCH INJURY;

ANIMALS; CELLS, CULTURED; FEMALE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUROGLIA; NEURONS; PROTEIN STRUCTURE, TERTIARY; SEROTONIN 5-HT1 RECEPTOR AGONISTS; SIALIC ACIDS; TRYPTAMINES;

MAMMALIA;

EID: 84890803714     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12408     Document Type: Article

References (61)

1. Assmann U., Szentivanyi A., Stark Y., Scheper T., Berski S., Dräger G., and, Schuster R. H., (2010) Fiber scaffolds of polysialic acid via electrospinning for peripheral nerve regeneration. J. Mater. Sci. Mater. Med. 21, 2115-2124.
2. Barreto G. E., Gonzalez J., Torres Y., and, Morales L., (2011) Astrocytic-neuronal crosstalk: implications for neuroprotection from brain injury. Neurosci. Res. 71, 107-113.
3. Berumen L. C., Rodríguez A., Miledi R., and, García-Alcocer G., (2012) Serotonin receptors in hippocampus. Sci. World J. 2012, 823493.
4. Bonfanti L., (2006) PSA-NCAM in mammalian structural plasticity and neurogenesis. Prog. Neurobiol. 80, 129-164. (Pubitemid 44739166)
5. Bonfanti L., and, Theodosis D. T., (2009) Polysialic acid and activity-dependent synapse remodeling. Cell Adh. Migr. 3, 43-50.
6. Brezun J. M., and, Daszuta A., (2000) Serotonergic reinnervation reverses lesion-induced decreases in PSA-NCAM labeling and proliferation of hippocampal cells in adult rats. Hippocampus 10, 37-46. (Pubitemid 30107588)
7. Charles P., Hernandez M. P., Stankoff B., Aigrot M. S., Colin C., Rougon G., Zalc B., and, Lubetzki C., (2000) Negative regulation of central nervous system myelination by polysialylated-neural cell adhesion molecule. Proc. Natl Acad. Sci. USA 97, 7585-7590. (Pubitemid 30431507)
8. Corfas G., Velardez M. O., Ko C. P., Ratner N., and, Peles E., (2004) Mechanisms and roles of axon-Schwann cell interactions. J. Neurosci. 24, 9250-9260. (Pubitemid 39426161)
9. Cremer H., Lange R., Christoph A., Plomann M., Vopper G., Roes J., Brown R., Baldwin S., Kraemer P., and, Scheff S., (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. (Pubitemid 24046046)
10. Decker L., Durbec P., Rougon G., and, Baron-Van Evercooren A., (2002) Loss of polysialic residues accelerates CNS neural precursor differentiation in pathological conditions. Mol. Cell. Neurosci. 19, 225-238. (Pubitemid 34211902)
11. Enriquez-Barreto L., Palazzetti C., Brennaman L. H., Maness P. F., and, Fairén A., (2012) Neural cell adhesion molecule, NCAM, regulates thalamocortical axonpathfinding and the organization of the cortical somatosensory representation in mouse. Front. Mol. Neurosci. 5, 76.
12. Etienne-Manneville S., (2006) In vitro assay of primary astrocyte migration as a tool to study Rho GTPase function in cell polarization. Methods Enzymol. 406, 565-578. (Pubitemid 43207469)
13. Evans S. V., Sigurskjold B. W., Jennings H. J., et al,. (1995) Evidence for the extended helical nature of polysaccharide epitopes. The 2.8 A resolution structure and thermodynamics of ligand binding of an antigen binding fragment specific for alpha-(2->8)-polysialic acid. Biochemistry 34, 6737-6744.
14. Falconer R. A., Errington R. J., Shnyder S. D., Smith P. J., and, Patterson L. H., (2012) Polysialyltransferase: a new target in metastatic cancer. Curr. Cancer Drug Targets 12, 925-939.
15. Franceschini I., Desroziers E., Caraty A., and, Duittoz A., (2010) The intimate relationship of gonadotropin-releasing hormone neurons with the polysialylated neural cell adhesion molecule revisited across development and adult plasticity. Eur. J. Neurosci. 32, 2031-2041.
16. Gaster L. M., Blaney F. E., Davies S., et al,. (1998) The selective 5-HT1B receptor inverse agonist 1'-methyl-5-[[2'-methyl-4'-(5-methyl-1,2, 4-oxadiazol-3-yl)biphenyl-4-yl]carbonyl]-2,3,6,7-tetrahydro- spiro[furo[2,3-f]indole-3,4'-piperidine] (SB-224289) potently blocks terminal 5-HT autoreceptor function both in vitro and in vivo. J. Med. Chem. 41, 1218-1235. (Pubitemid 28208177)
17. Ghosh M., Tuesta L. M., Puentes R., Patel S., Melendez K., El Maarouf A., Rutishauser U., and, Pearse D. D., (2012) Extensive cell migration, axon regeneration, and improved function with polysialic acid-modified Schwann cells after spinal cord injury. Glia 60, 979-992.
18. Glennon R. A., Hong S. S., Dukat M., Teitler M., and, Davis K., (1994) 5-(Nonyloxy)tryptamine: a novel high-affinity 5-HT1D beta serotonin receptor agonist. J. Med. Chem. 37, 2828-2830. (Pubitemid 24297797)
19. Gotti C., Sher E., Cabrini D., Bondiolotti G., Wanke E., Mancinelli E., and, Clementi F., (1987) Cholinergic receptors, ion channels, neurotransmitter synthesis, and neurite outgrowth are independently regulated during the in vitro differentiation of a human neuroblastoma cell line. Differentiation 24, 144-155.
20. Heckman C. J., Mottram C., Quinlan K., Theiss R., and, Schuster J., (2009) Motoneuron excitability: the importance of neuromodulatory inputs. Clin. Neurophysiol. 120, 2040-2054.
21. Hildebrandt H., Becker C., Glüer S., Rösner H., Gerardy-Schahn R., and, Rahmann H., (1998) Polysialic acid on the neural cell adhesion molecule correlates with expression of polysialyltransferases and promotes neuroblastoma cell growth. Cancer Res. 58, 779-784. (Pubitemid 28099491)
22. Irintchev A., Wu M. M., Lee H. J., Zhu H., Feng Y. P., Liu Y. S., Bernreuther C., Loers G., You S. W., and, Schachner M., (2011) Glycomimetic improves recovery after femoral injury in a non-human primate. J. Neurotrauma 28, 1295-1306.
23. Jungnickel J., Brämer C., Bronzlik P., Lipokatic-Takacs E., Weinhold B., Gerardy-Schahn R., and, Grothe C., (2009) Level and localization of polysialic acid is critical for early peripheral nerve regeneration. Mol. Cell. Neurosci. 40, 374-381.
24. Kleene R., Loers G., Langer J., Frobert Y., Buck F., and, Schachner M., (2007) Prion protein regulates glutamate-dependent lactate transport of astrocytes. J. Neurosci. 27, 12331-12340. (Pubitemid 350085463)
25. Kumar S., Parkash J., Kataria H., and, Kaur G., (2012) Enzymatic removal of polysialic acid from neural cell adhesion molecule interrupts gonadotropin releasing hormone (GnRH) neuron-glial remodeling. Mol. Cell. Endocrinol. 348, 95-103.
26. Lavdas A. A., Franceschini I., Dubois-Dalcq M., and, Matsas R., (2006) Schwann cells genetically engineered to express PSA show enhanced migratory potential without impairment of their myelinating ability in vitro. Glia 53, 868-878.
27. Loers G., Chen S., Grumet M., and, Schachner M., (2005) Signal transduction pathways implicated in neural recognition molecule L1 triggered neuroprotection and neuritogenesis. J. Neurochem. 92, 1463-1476. (Pubitemid 40389215)
28. Luo J., Bo X., Wu D., Yeh J., Richardson P., and, M, and, Zhang Y., (2011) Promoting survival, migration, and integration of transplanted Schwann cells by over-expressing polysialic acid. Glia 59, 424-434.
29. Magnani J. L., and, Ernst B., (2009) Glycomimetic drugs-a new source of therapeutic opportunities. Discov. Med. 8, 247-252.
30. Marino P., Norreel J. C., Schachner M., Rougon G., and, Amoureux M. C., (2009) A polysialic acid mimetic peptide promotes functional recovery in a mouse model of spinal cord injury. Exp. Neurol. 219, 163-174.
31. Masand S. N., Perron I. J., Schachner M., and, Shreiber D. I., (2012a) Neural cell type-specific responses to glycomimetic functionalized collagen. Biomaterials 33, 790-797.
32. Masand S. N., Chen J., Perron I. J., Hammerling B. C., Loers G., Schachner M., and, Shreiber D. I., (2012b) The effect of glycomimetic functionalized collagen on peripheral nerve repair. Biomaterials 33, 8353-8362.
33. Mehanna A., Mishra B., Kurschat N., Schulze C., Bian C., Loers G., Irintchev A., and, Schachner M., (2009) Polysialic acid glycomimetics promote myelination and functional recovery after peripheral nerve injury in mice. Brain 132, 1449-1462.
34. Mehanna A., Jakovcevski I., Acar A., Xiao M., Loers G., Rougon G., Irintchev A., and, Schachner M., (2010) Polysialic acid glycomimetic promotes functional recovery and plasticity after spinal cord injury in mice. Mol. Ther. 18, 34-43.
35. Mishra B., von der Ohe M., Schulze C., Bian S., Makhina T., Loers G., Kleene R., and, Schachner M., (2010) Functional role of the interaction between polysialic acid and extracellular histone H1. J. Neurosci. 30, 12400-12413.
36. Mollinedo F., and, Gajate C., (2003) Microtubules, microtubule interfering agents and apoptosis. Apoptosis 8, 413-450. (Pubitemid 37247987)
37. Nakata D., and, Troy F. A., (2005) Degree of polymerization (DP) of polysialic acid (polySia) on neural cell adhesion molecules (N-CAMs). J. Biol. Chem. 280, 38305-38316.
38. Neale R. F., Fallon S. L., Boyar W. C., Wasley J. W., Martin L. L., Stone G. A., Glaeser B. S., Sinton C. M., and, Williams M., (1987) Biochemical and pharmacological characterization of CGS 12066B, a selective serotonin-1B agonist. Eur. J. Pharmacol. 136, 1-9. (Pubitemid 17109585)
39. Nichols R. A., (2011) Serotonin, presynaptic 5-HTâ receptors and synaptic plasticity in the developing cerebellum. J. Physiol. 589, 5019-5020.
40. Oostland M., Sellmeijer J., and, van Hooft J. A., (2011) Transient expression of functional 5-HT3receptors by glutamatergic granule cells in the early postnatal mouse cerebellum. J. Physiol. 589, 4837-4846.
41. Papastefanaki F., Chen J., Lavdas A. A., Thomaidou D., Schachner M., and, Matsas R., (2007) Grafts of Schwann cells engineered to express PSA-NCAM promote functional recovery after spinal cord injury. Brain 130, 2159-2174. (Pubitemid 47236630)
42. Parkash J., and, Kaur G., (2005) Neuronal-glial plasticity in gonadotrophin releasing hormone release in adult female rats: role of the polysialylated form of neural cell adhesion molecule. J. Endocrinol. 186, 397-409. (Pubitemid 41167408)
43. Petridis A. K., El-Maarouf A., and, Rutishauser U., (2004) Polysialic acid regulates cell contact-dependent neuronal differentiation of progenitor cells from the subventricular zone. Dev. Dyn. 230, 675-684. (Pubitemid 38993867)
44. Poongodi G. L., Suresh N., Gopinath S. C., Chang T., Inoue S., and, Inoue Y., (2002) Dynamic change of neural cell adhesion molecule polysialylation on human neuroblastoma (IMR-32) and rat pheochromocytoma (PC-12) cells during growth and differentiation. J. Biol. Chem. 277, 28200-28211. (Pubitemid 34966774)
45. Prost L. R., Grim J. C., Tonelli M., and, Kiessling L. L., (2012) Noncarbohydrate glycomimetics and glycoprotein surrogates as DC-SIGN antagonists and agonists. ACS Chem. Biol. 7, 1603-1608.
46. Rameix-Welti M. A., Zarantonelli M. L., Giorgini D., Ruckly C., Marasescu M., van der Werf S., Alonso J. M., Naffakh N., and, Taha M. K., (2009) Influenza A virus neuraminidase enhances meningococcal adhesion to epithelial cells through interaction with sialic acid-containing meningococcal capsules. Infect. Immun. 77, 3588-3595.
47. Robert S. J., Zugaza J. L., Fischmeister R., Gardier A. M., and, Lezoualc'h F., (2001) The human serotonin 5-HT4 receptor regulates secretion of non-amyloidogenic precursor protein. J. Biol. Chem. 276, 44881-44888.
48. Rutishauser U., (2008) Polysialic acid in the plasticity of the developing and adult vertebrate nervous system. Nat. Rev. Neurosci. 9, 26-35. (Pubitemid 350295686)
49. Sánchez C., Díaz-Nido J., and, Avila J., (2000) Phosphorylation of microtubule-associated protein 2 (MAP2) and its relevance for the regulation of the neuronal cytoskeleton function. Prog. Neurobiol. 61, 133-168. (Pubitemid 30110476)
50. Sari Y., Miquel M. C., Brisorgueil M. J., Ruiz G., Doucet E., Hamon M., and, Vergé D., (1999) Cellular and subcellular localization of 5-hydroxytryptamine1B receptors in the rat central nervous system: immunocytochemical, autoradiographic and lesion studies. Neurosci. 88, 899-915. (Pubitemid 28518266)
51. Schlicker E., Werner U., Hamon M., Gozlan H., Nickel B., Szelenyi I., and, Göthert M., (1992) Anpirtoline, a novel, highly potent 5-HT1B receptor agonist with antinociceptive/antidepressant-like actions in rodents. Br. J. Pharmacol. 105, 732-738.
52. Schlosshauer B., Muller E., Schroder B., Planck H., and, Muller H. W., (2003) Rat Schwann cells in bioresorbable nerve guides to promote and accelerate axonal regeneration. Brain Res. 963, 321-326. (Pubitemid 36126314)
53. Senkov O., Tikhobrazova O., and, Dityatev A., (2012) PSA-NCAM: synaptic functions mediated by its interactions with proteoglycans and glutamate receptors. Int. J. Biochem. Cell Biol. 44, 591-595.
54. Simova O., Irintchev A., Mehanna A., Liu J., Dihné M., Bächle D., Sewald N., Loers G., and, Schachner M., (2006) Carbohydrate mimics promote functional recovery after peripheral nerve repair. Ann. Neurol. 6, 430-437. (Pubitemid 44684979)
55. Sofroniew M. V., and, Vinters H. V., (2010) Astrocytes: biology and pathology. Acta Neuropathol. 119, 7-35.
56. Theis T., Mishra B., von der Ohe M., Loers G., Prondzynski M., Pless O., Blackshear P. J., Schachner M., and, Kleene R., (2013) Functional role of the interaction between polysialic acid and myristoylated alanine-rich C kinase substrate at the plasma membrane. J. Biol. Chem. 288, 6726-6742.
57. Torregrossa P., Buhl L., Bancila M., Durbec P., Schafer C., Schachner M., and, Rougon G., (2004) Selection of poly-alpha 2,8-sialic acid mimotopes from a random phage peptide library and analysis of their bioactivity. J. Biol. Chem. 279, 30707-30714. (Pubitemid 38938003)
58. Venero C., Herrero A. I., Touyarot K., Cambon K., Lõpez- Fernández M. A., Berezin V., Bock E., and, Sandi C., (2006) Hippocampal up-regulation of NCAM expression and polysialylation plays a key role on spatial memory. Eur. J. Neurosci. 23, 1585-1595.
59. Wang S., Cesca F., Loers G., Schweizer M., Buck F., Benfenati F., Schachner M., and, Kleene R., (2011) Synapsin I is an oligomannose-carrying glycoprotein, acts as an oligomannose-binding lectin, and promotes neurite outgrowth and neuronal survival when released via glia-derived exosomes. J. Neurosci. 31, 7275-7290.
60. Yoder E. J., Tamir H., and, Ellisman M. H., (1997) Serotonin receptors expressed by myelinating Schwann cells in rat sciatic nerve. Brain Res. 753, 299-308. (Pubitemid 27151875)
61. Yoshida K., Rutishauser U., Crandall J. E., and, Schwarting G. A., (1999) Polysialic acid facilitates migration of luteinizing hormone-releasing hormone neurons on vomeronasal axons. J. Neurosci. 19, 794-801. (Pubitemid 29036030)