β3GnT2 maintains adenylyl cyclase-3 signaling and axon guidance molecule expression in the olfactory epithelium

Journal of Neuroscience

Volumn 31, Issue 17, 2011, Pages 6576-6586

  Henion, Timothy R ^a   Faden, Ashley A ^a   Knott, Thomas K ^a   Schwarting, Gerald A ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; ADENYLATE CYCLASE 3; BETA3 GLYCOSYLTRANSFERASE 2; CYCLIC AMP; GLYCOSYLTRANSFERASE; NEUROPILIN 1; SEMAPHORIN 3A; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; ENZYME LOCALIZATION; MOUSE; NERVE FIBER; NERVE PROJECTION; NONHUMAN; OLFACTORY BULB; OLFACTORY EPITHELIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; UPREGULATION; WILD TYPE;

ADENYLATE CYCLASE; AGE FACTORS; AMINO SUGARS; ANIMALS; ANIMALS, NEWBORN; AXONS; CALCIUM-BINDING PROTEINS; CYCLIC AMP; GAP-43 PROTEIN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LECTINS; MICE; MICE, KNOCKOUT; N-ACETYLGLUCOSAMINYLTRANSFERASES; NEURAL CELL ADHESION MOLECULES; NEUROPILIN-1; OLFACTORY MUCOSA; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION;

EID: 79955758334     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0224-11.2011     Document Type: Article

References (45)

1. Bakalyar HA, Reed RR (1990) Identification ofaspecialized adenylyl cyclase that may mediate odorant detection. Science 250:1403-1406.
2. Bennett MK, Kulaga HM, Reed RR (2010) Odor-evoked gene regulation and visualization in olfactory receptor neurons. Mol Cell Neurosci 43:353-362.
3. Biellmann F, Henion TR, Bürki K, Hennet T (2008) Impaired sexual behavior in male mice deficient for the beta1-3 N-acetylglucosaminyltransferase-I gene. Mol Reprod Dev 75:699-706.
4. Carr VM, Farbman AI (1992) Ablation of the olfactory bulb up-regulates the rate of neurogenesis and induces precocious cell death in olfactory epithelium. Exp Neurol 115:55-59.
5. Chesler AT, Zou DJ, Le Pichon CE, Peterlin ZA, Matthews GA, Pei X, Miller MC, Firestein S (2007) A G protein/cAMP signal cascade is required for axonal convergence into olfactory glomeruli. Proc Natl Acad Sci USA 104:1039-1044.
6. Crandall JE, Dibble C, Butler D, Pays L, Ahmad N, Kostek C, Püschel AW, Schwarting GA (2000) Patterning of olfactory sensory connections is mediated by extracellular matrix proteins in the nerve layer of the olfactory bulb. J Neurobiol 45:195-206.
7. Cutforth T, Moring L, Mendelsohn M, Nemes A, Shah NM, Kim MM, Frisén J, Axel R (2003) Axonal ephrin-As and odorant receptors: coordinate determination of the olfactory sensory map. Cell 114:311-322.
8. Dal Col JA, Matsuo T, Storm DR, Rodriguez I (2007) Adenylyl cyclase-dependent axonal targeting in the olfactory system. Development 134:2481-2489.
9. 2+ channel Cav1.2. Science 293:98-101.
10. Feinstein P, Mombaerts P (2004) A contextual model for axonal sorting into glomeruli in the mouse olfactory system. Cell 117:817-831.
11. Helenius A, Aebi M (2001) Intracellular functions of N-linked glycans. Science 291:2364-2369.
12. Henion TR, Zhou D, Wolfer DP, Jungalwala FB, Hennet T (2001) Cloning of a mouse β1,3N-acetylglucosaminyltransferase GlcNAc(β1,3)Gal(beta 1,4)Glc-ceramide synthase gene encoding the key regulator of lacto-series glycolipid biosynthesis. J Biol Chem 276:30261-30269.
13. Henion TR, Raitcheva D, Grosholz R, Biellmann F, Skarnes WC, Hennet T, Schwarting GA (2005) β1,3-N-Acetylglucosaminytransferase 1 glycosyl-ation is required for axon pathfinding by olfactory sensory neurons. J Neurosci 25:1894-1903.
14. Imai T, Sakano H (2008) Odorant receptor-mediated signaling in the mouse. Curr Opin Neurobiol 18:251-260.
15. Imai T, Suzuki M, Sakano H (2006) Odorant receptor-derived cAMP signals direct axonal targeting. Science 314:657-661.
16. Imai T, Yamazaki T, Kobayakawa R, Kobayakawa K, Abe T, Suzuki M, Sakano H (2009) Pre-target axon sorting establishes the neural map topography. Science 325:585-590.
17. Jenkins PM, McEwen DP, Martens JR (2009) Olfactory cilia: linking sensory cilia function and human disease. Chem Senses 34:451-464.
18. Kaupp UB (2010) Olfactory signalling in vertebrates and insects: differences and commonalities. Nat Rev Neurosci 11:188-200.
19. Kleene SJ (2008) The electrochemical basis of odor transduction in vertebrate olfactory cilia. Chem Senses 33:839-859.
20. Leach BS, Collawn JF, Fish WW (1980) Behavior of glycopolypeptides with empirical molecular weight estimation methods. 1. In Sodium dode-cyl sulfate. Biochemistry 19:5734-5741.
21. Li W, Takahashi M, Shibukawa Y, Yokoe S, Gu J, Miyoshi E, Honke K, Ikeda Y, Taniguchi N (2007) Introduction of bisecting GlcNAc in N-glycans of adenylyl cyclase III enhances its activity. Glycobiology 17:655-662.
22. Mahanthappa NK, Cooper DN, Barondes SH, Schwarting GA (1994) Rat olfactory neurons can utilize the endogenous lectin, L-14, in a novel adhesion mechanism. Development 120:1373-1384.
23. 2+ increases. Proc Natl Acad Sci USA 106:3537-3542.
24. Merkle RK, Cummings RD (1987) Relationship of the terminal sequences to the length of poly-N-acetyllactosamine chains in asparagine-linked oligosaccharides from the mouse lymphoma cell line BW5147. Immobilized tomato lectin interacts with high affinity with glycopeptides containing long poly-N-acetyllactosamine chains. J Biol Chem 262:8179-8189.
25. Miller AM, Maurer LR, Zou DJ, Firestein S, Greer CA (2010) Axonfascicu-lation in the developing olfactory nerve. Neural Dev 5:20.
26. Mitchell KJ, Pinson KI, Kelly OG, Brennan J, Zupicich J, Scherz P, Leighton PA, Goodrich LV, Lu X, Avery BJ, Tate P, Dill K, Pangilinan E, Wakenight P, Tessier-Lavigne M, Skarnes WC (2001) Functional analysis of secreted and transmembrane proteins critical to mouse development. Nat Genet 28:241-249.
27. Mombaerts P, Wang F, Dulac C, Chao SK, Nemes A, Mendelsohn M, Ed-mondson J, Axel R (1996) Visualizing an olfactory sensory map. Cell 87:675-686.
28. Pasterkamp RJ, De Winter F, Holtmaat AJ, Verhaagen J (1998) Evidence for a role of the chemorepellent semaphorin III and its receptor neuropilin-1 in the regeneration of primary olfactory axons. J Neurosci 18:9962-9976.
29. Schwarting GA, Henion TR (2007) Lactosamine differentially affects olfactory sensory neuron projections to the olfactory bulb. Dev Neurobiol 67:1627-1640.
30. Schwarting GA, Henion TR (2008) Olfactory axon guidance: the modified rules. J Neurosci Res 86:11-17.
31. Schwarting GA, Kostek C, Ahmad N, Dibble C, Pays L, Püschel AW, (2000) Semaphorin 3A is required for normal guidance of olfactory axons in mice. J Neurosci 20:7691-7697.
32. Schwarting GA, Raitcheva D, Crandall JE, Burkhardt C, Püschel AW (2004) Semaphorin 3A mediated axon guidance regulates convergence and targeting of P2 odorant receptor axons. Eur J Neurosci 19:1800-1810.
33. Serizawa S, Miyamichi K, Takeuchi H, Yamagishi Y, Suzuki M, Sakano H (2006) A neuronal identity code for the odorant receptor-specific and activity-dependent axon sorting. Cell 127:1057-1069.
34. Shiraishi N, Natsume A, Togayachi A, Endo T, Akashima T, Yamada Y, Imai N, Nakagawa S, Koizumi S, Sekine S, Narimatsu H, Sasaki K (2001) Identification and characterization of three novel β1,3-N-acetylglucosaminyltransferases structurally related to the β1,3-galactosyltransferase family. J Biol Chem 276:3498-3507.
35. Storan MJ, Magnaldo T, Garagba MC, Zick Y, Key B (2004) Expression and putative role of lactoseries carbohydrates present on NCAM in the rat primary olfactory pathway. J Comp Neurol 475:289-302.
36. Suto F, Ito K, Uemura M, Shimizu M, Shinkawa Y, Sanbo M, Shinoda T, Tsuboi M, Takashima S, Yagi T, Fujisawa H (2005) Plexin-A4 mediates axon-repulsive activities of both secreted and transmembrane sema-phorins and plays roles in nerve fiber guidance. J Neurosci 25:3628-3637.
37. Taniguchi M, Nagao H, Takahashi YK, Yamaguchi M, Mitsui S, Yagi T, Mori K, Shimizu T (2003) Distorted odor maps in the olfactory bulb of semaphorin 3A-deficient mice. J Neurosci 23:1390-1397.
38. Togayachi A, Kozono Y, Ishida H, Abe S, Suzuki N, Tsunoda Y, Hagiwara K, Kuno A, Ohkura T, Sato N, Sato T, Hirabayashi J, Ikehara Y, Tachibana K, Narimatsu H (2007) Polylactosamine on glycoproteins influences basal levels of lymphocyte and macrophage activation. Proc Natl Acad Sci USA 104:15829-15834.
39. Trinh K, Storm DR (2003) Vomeronasal organ detects odorants in absence of signaling through main olfactory epithelium. Nat Neurosci 6:519-525.
40. Wang F, Nemes A, Mendelsohn M, Axel R (1998) ORs govern the formation of a precise topographic map. Cell 93:47-60.
41. Wei J, Zhao AZ, Chan GC, Baker LP, Impey S, Beavo JA, Storm DR (1998) Phosphorylation and inhibition of olfactory adenylyl cyclase by CaM kinase II in neurons: a mechanism for attenuation of olfactory signals. Neuron 21:495-504.
42. Wong ST, Trinh K, Hacker B, Chan GC, Lowe G, Gaggar A, Xia Z, Gold GH, Storm DR (2000) Disruption of the type III adenylyl cyclase gene leads to peripheral and behavioral anosmia in transgenic mice. Neuron 27:487-497.
43. Wu GC, Lai HL, Lin YW, Chu YT, Chern Y (2001) N-glycosylation and residues Asn805 and Asn890 are involved in the functional properties of type VI adenylyl cyclase. J Biol Chem 276:35450-35457.
44. Zhou D, Dinter A, Gallego G.R, Kamerling JP, Vliegenthart JF, Berger EG, Hennet T (1999) A β-1,3-N-acetylglucosaminyltransferase with poly-N-acetyllactosamine synthase activity is structurally related to β-1,3-galactosyltransferases. Proc Natl Acad Sci USA 96:406-411.
45. Zou DJ, Chesler AT, Le Pichon CE, Kuznetsov A, Pei X, Hwang EL, Firestein S (2007) Absence of adenylyl cyclase 3 perturbs peripheral olfactory projections in mice. J Neurosci 27:6675-6683.