Expression of PTPRO in the interneurons of adult mouse olfactory bulb

Journal of Comparative Neurology

Volumn 518, Issue 2, 2010, Pages 119-136

  Kotani, Takenori ^a   Murata, Yoji ^a   Ohnishi, Hiroshi ^a   Mori, Munemasa ^a   Kusakari, Shinya ^a   Saito, Yasuyuki ^a   Okazawa, Hideki ^a   Bixby, John L ^b   Matozaki, Takashi ^a  

^a GUNMA UNIVERSITY   (Japan)

^b UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

CNS; Granule cells; Localization; Maturation; Periglomerular cells; Receptor type tyrosine phosphatase

Indexed keywords

4 AMINOBUTYRIC ACID; CALRETININ; NEUROCALCIN; PROTEIN PTPRO; RECEPTOR LIKE PROTEIN TYROSINE PHOSPHATASE; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; DIAGNOSTIC AGENT; DYES, REAGENTS, INDICATORS, MARKERS AND BUFFERS; EPHRIN RECEPTOR A4; MONOCLONAL ANTIBODY; PTPRO PROTEIN, MOUSE;

ANIMAL TISSUE; ARTICLE; BRAIN MATURATION; CONTROLLED STUDY; DENDRITE; FEMALE; GRANULE CELL; IMMUNOHISTOCHEMISTRY; INTERNEURON; MALE; MOUSE; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; CHEMISTRY; CYTOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; GENETIC TRANSFECTION; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; PLASMID; PREGNANCY;

ANIMALS; ANTIBODIES, MONOCLONAL; BIOLOGICAL MARKERS; CELLS, CULTURED; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GAMMA-AMINOBUTYRIC ACID; INDICATORS AND REAGENTS; INTERNEURONS; MALE; MICE; MICE, INBRED C57BL; OLFACTORY BULB; PLASMIDS; PREGNANCY; RECEPTOR, EPHA4; RECEPTOR-LIKE PROTEIN TYROSINE PHOSPHATASES, CLASS 3; TRANSFECTION;

EID: 77449089089     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22239     Document Type: Article

References (59)

1. Aguiar RC, Yakushijin Y, Kharbanda S, Tiwari S, Freeman GJ, Shipp MA. 1999. PTPROt: an alternatively spliced and developmentally regulated B-lymphoid phosphatase that promotes G0/G1 arrest. Blood 94:2403-2413.
2. Alonso A, Sasin J, Bottini N, Friedberg I, Friedberg I, Osterman A, Godzik A, Hunter T, Dixon J, Mustelin T. 2004. Protein tyrosine phosphatases in the human genome. Cell 117:699-711.
3. Andersen JN, Mortensen OH, Peters GH, Drake PG, Iversen LF, Olsen OH, Jansen PG, Andersen HS, Tonks NK, Møller NP. 2001. Structural and evolutionary relationships among protein tyrosine phosphatase domains. Mol Cell Biol 21:7117-7136.
4. Batista-Brito R, Close J, Machold R, Fishell G. 2008. The distinct temporal origins of olfactory bulb interneuron subtypes. J Neurosci 28:3966-3975.
5. Beltran PJ, Bixby JL, Masters BA. 2003. Expression of PTPRO during mouse development suggests involvement in axonogenesis and differentiation of NT-3- and NGF-dependent neurons. J Comp Neurol 456:384-395.
6. Benzing T. 2004. Signaling at the slit diaphragm. J Am Soc Nephrol 15:1382-1391.
7. Binns KL, Taylor PP, Sicheri F, Pawson T, Holland SJ. 2000. Phosphorylation of tyrosine residues in the kinase domain and juxtamembrane region regulates the biological and catalytic activities of Eph receptors. Mol Cell Biol 20:4791-4805.
8. Bodden K, Bixby JL. 1996. CRYP-2: a receptor-type tyrosine phosphatase selectively expressed by developing vertebrate neurons. J Neurobiol 31:309-324.
9. Bouvier D, Corera AT, Tremblay ME, Riad M, Chagnon M, Murai KK, Pasquale EB, Fon EA, Doucet G. 2008. Pre-synaptic and post-synaptic localization of EphA4 and EphB2 in adult mouse forebrain. J Neurochem 106:682-695.
10. Burette AC, Strehler EE, Weinberg RJ. 2009. "Fast" plasma membrane calcium pump PMCA2a concentrates in GABAergic terminals in the adult rat brain. J Comp Neurol 512:500-513.
11. De Marchis S, Bovetti S, Carletti B, Hsieh YC, Garzotto D, Peretto P, Fasolo A, Puche AC, Rossi F. 2007. Generation of distinct types of periglomerular olfactory bulb interneurons during development and in adult mice: implication for intrinsic properties of the subventricular zone progenitor population. J Neurosci 27:657-664.
12. Dehmelt L, Halpain S. 2004. Actin and microtubules in neurite initiation: are MAPs the missing link? J Neurobiol 58:18 -33.
13. Duan X, Kang E, Liu CY, Ming GL, Song H. 2008. Development of neural stem cell in the adult brain. Curr Opin Neurobiol 18:108-115.
14. Egger V, Urban NN. 2006. Dynamic connectivity in the mitral cell- granule cell microcircuit. Semin Cell Dev Biol 17:424-432.
15. Esclapez M, Tillakaratne NJ, Kaufman DL, Tobin AJ, Houser CR. 1994. Comparative localization of two forms of glutamic acid decarboxylase and their mRNAs in rat brain supports the concept of functional differences between the forms. J Neurosci 14:1834-1855.
16. Faul C, Asanuma K, Yanagida-Asanuma E, Kim K, Mundel P. 2007. Actin up: regulation of podocyte structure and function by components of the actin cytoskeleton. Trends Cell Biol 17:428-437.
17. Fong AY, Stornetta RL, Foley CM, Potts JT. 2005. Immunohistochemical localization of GAD67-expressing neurons and processes in the rat brainstem: subregional distribution in the nucleus tractus solitarius. J Comp Neurol 493:274-290.
18. Fuentes-Santamaria V, Alvarado JC, Taylor AR, Brunso-Bechtold JK, Henkel CK. 2005. Quantitative changes in calretinin immunostaining in the cochlear nuclei after unilateral cochlear removal in young ferrets. J Comp Neurol 483:458-475.
19. Goldshmit Y, McLenachan S, Turnley A. 2006. Roles of Eph receptors and ephrins in the normal and damaged adult CNS. Brain Res Rev 52:327-345.
20. Govek EE, Newey SE, Van Aelst L. 2005. The role of the Rho GTPases in neuronal development. Genes Dev 19:1- 49.
21. Hayashi A, Ohnishi H, Okazawa H, Nakazawa S, Ikeda H, Motegi S, Aoki N, Kimura S, Mikuni M, Matozaki T. 2004. Positive regulation of phagocytosis by SIRPβ and its signaling mechanism in macrophages. J Biol Chem 279:29450-29460.
22. Henkemeyer M, Itkis OS, Ngo M, Hickmott PW, Ethell IM. 2003. Multiple EphB receptor tyrosine kinases shape dendritic spines in the hippocampus. J Cell Biol 163:1313-1326.
23. Huot J. 2004. Ephrin signaling in axon guidance. Prog Neuropsychopharmacol Biol Psychiatry 28:813-818.
24. Huynh DP, Figueroa K, Hoang N, Pulst SM. 2000. Nuclear localization or inclusion body formation of ataxin-2 are not necessary for SCA2 pathogenesis in mouse or human. Nat Genet 26:44 -50.
25. Imamura F, Nagao H, Naritsuka H, Murata Y, Taniguchi H, Mori K. 2006. A leucine-rich repeat membrane protein, 5T4, is expressed by a subtype of granule cells with dendritic arbors in specific strata of the mouse olfactory bulb. J Comp Neurol 495:754-768.
26. Inoue E, Deguchi-Tawarada M, Togawa A, Matsui C, Arita K, Katahira-Tayama S, Sato T, Yamauchi E, Oda Y, Takai Y. 2009. Synaptic activity prompts γ-secretase-mediated cleavage of EphA4 and dendritic spine formation. J Cell Biol 185:551-564.
27. Kim JH, Lee JA, Song YM, Park CH, Hwang SJ, Kim YS, Kaang BK, Son H. 2006. Overexpression of calbindin-D28K in hippocampal progenitor cells increases neuronal differentiation and neurite outgrowth. FASEB J 20:109-111.
28. Kosaka K, Toida K, Aika Y, Kosaka T. 1998. How simple is the organization of the olfactory glomerulus? The heterogeneity of so-called periglomerular cells. Neurosci Res 30:101-110.
29. Lamprianou S, Harroch S. 2006. Receptor protein tyrosine phosphatase from stem cells to mature glial cells of the central nervous system. J Mol Neurosci 29:241-255.
30. Ledig MM, McKinnell IW, Mrsic-Flogel T, Wang J, Alvares C, Mason I, Bixby JL, Mueller BK, Stoker AW. 1999. Expression of receptor tyrosine phosphatases during development of the retinotectal projection of the chick. J Neurobiol 39:81-96.
31. Liebl DJ, Morris CJ, Henkemeyer M, Parada LF. 2003. mRNA expression of ephrins and Eph receptor tyrosine kinases in the neonatal and adult mouse central nervous system. J Neurosci Res 71:7-22.
32. Lledo PM, Saghatelyan A. 2005. Integrating new neurons into the adult olfactory bulb: joining the network, life-death decisions, and the effects of sensory experience. Trends Neurosci 28:248-254.
33. Mullen RJ, Buck CR, Smith AM. 1992. NeuN, a neuronal specific nuclear protein in vertebrates. Development 116:201-211.
34. Murata T, Ohnishi H, Okazawa H, Murata Y, Kusakari S, Hayashi Y, Miyashita M, Itoh H, Oldenborg PA, Furuya N, Matozaki T. 2006. CD47 promotes neuronal development through Srcand FRG/Vav2-mediated activation of Rac and Cdc42. J Neurosci 26:12397-12407.
35. Negishi M, Katoh H. 2002. Rho family GTPases as key regulators for neuronal network formation. J Biochem 132:157-166.
36. Parrish-Aungst S, Shipley MT, Erdelyi F, Szabo G, Puche AC. 2007. Quantitative analysis of neuronal diversity in the mouse olfactory bulb. J Comp Neurol 501:825-836.
37. Paul S, Lombroso PJ. 2003. Receptor and nonreceptor protein tyrosine phosphatases in the nervous system. Cell Mol Life Sci 60:2465-2482.
38. Penzes P, Cahill ME, Jones KA, Srivastava DP. 2008. Convergent CaMK and RacGEF signals control dendritic structure and function. Trends Cell Biol 18:405-413.
39. Pixley FJ, Lee PS, Dominguez MG, Einstein DB, Stanley ER. 1995. A heteromorphic protein-tyrosine phosphatase, PTPΦ, is regulated by CSF-1 in macrophages. J Biol Chem 270:27339-27347.
40. Sadakata H, Okazawa H, Sato T, Supriatna Y, Ohnishi H, Kusakari S, Murata Y, Ito T, Nishiyama U, Minegishi T, Harada A, Matozaki T. 2009. SAP-1 is a microvillus-specific protein tyrosine phosphatase that modulates intestinal tumorigenesis. Genes Cells 14:295-308.
41. Schaapveld RQ, Schepens JT, Bächner D, Attema J, Wieringa B, Jap PH, Hendriks WJ. 1998. Developmental expression of the cell adhesion molecule-like protein tyrosine phosphatases LAR, RPTPσ and RPTP in the mouse. Mech Dev 77:59-62.
42. Shamah SM, Lin MZ, Goldberg JL, Estrach S, Sahin M, Hu L, Bazalakova M, Neve RL, Corfas G, Debant A, Greenberg ME. 2001. EphA receptors regulate growth cone dynamics through the novel guanine nucleotide exchange factor ephexin. Cell 105:233-244.
43. Shintani T, Ihara M, Sakuta H, Takahashi H, Watakabe I, Noda M. 2006. Eph receptors are negatively controlled by protein tyrosine phosphatase receptor type O. Nat Neurosci 9:761-769.
44. Singec I, Knoth R, Ditter M, Hagemeyer CE, Rosenbrock H, Frotscher M, Volk B. 2002. Synaptic vesicle protein synaptoporin is differently expressed by subpopulations of mouse hippocampal neurons. J Comp Neurol 452:139-153.
45. St. John JA, Key B. 2001. EphB2 and two of its ligands have dynamic protein expression patterns in the developing olfactory system. Brain Res Dev Brain Res 126:43-56.
46. Stepanek L, Sun QL, Wang J, Wang C, Bixby JL. 2001. CRYP-2/ cPTPRO is a neurite inhibitory repulsive guidance cue for retinal neurons in vitro. J Cell Biol 154:867-878.
47. Stepanek L, Stoker AW, Stoeckli E, Bixby JL. 2005. Receptor tyrosine phosphatases guide vertebrate motor axons during development. J Neurosci 25:3813-3823.
48. Tagawa M, Shirasawa T, Yahagi Y, Tomoda T, Kuroyanagi H, Fujimura S, Sakiyama S, Maruyama N. 1997. Identification of a receptor-type protein tyrosine phosphatase expressed in postmitotic maturing neurons: its structure and expression in the central nervous system. Biochem J 321:865-871.
49. Teng J, Takei Y, Harada A, Nakata T, Chen J, Hirokawa N. 2001. Synergistic effects of MAP2 and MAP1B knockout in neuronal migration, dendritic outgrowth, and microtubule organization. J Cell Biol 155:65-76.
50. Thomas PE, Wharram BL, Goyal M, Wiggins JE, Holzman LB, Wiggins RC. 1994. GLEPP1, a renal glomerular epithelial cell (podocyte) membrane protein-tyrosine phosphatase. Identification, molecular cloning, and characterization in rabbit. J Biol Chem 269:19953-19962.
51. Tomemori T, Seki N, Suzuki Y, Shimizu T, Nagata H, Konno A, Shirasawa T. 2000. Isolation and characterization of murine orthologue of PTP-BK. Biochem Biophys Res Commun 276:974-981.
52. Trowern AR, Laight R, MacLean N, Mann DA. 1996. Detection of neuron-specific protein gene product (PGP) 9.5 in the rat and zebrafish using anti-human PGP9.5 antibodies. Neurosci Lett 210:21-24.
53. Wang R, St John PL, Wiggins RC, Abrahamson DR. 1999. 32 molecular cloning and expression of glomerular epithelial protein 1 (GLEPP1) in developing mouse kidney. J Histochem Cytochem 47:1650.
54. Weiler E, Benali A. 2005. Olfactory epithelia differentially express neuronal markers. J Neurocytol 34:217-240.
55. Wharram BL, Goyal M, Gillespie PJ, Wiggins JE, Kershaw DB, Holzman LB, Dysko RC, Saunders TL, Samuelson LC, Wiggins RC. 2000. Altered podocyte structure in GLEPP1 (Ptpro)-deficient mice associated with hypertension and low glomerular filtration rate. J Clin Invest 106:1281-1290.
56. Whitman MC, Greer CA. 2007a. Adult-generated neurons exhibit diverse developmental fates. Dev Neurobiol 67:1079-1093.
57. Whitman MC, Greer CA. 2007b. Synaptic integration of adult-generated olfactory bulb granule cells: basal axodendritic centrifugal input precedes apical dendrodendritic local circuits. J Neurosci 27:9951-9961.
58. Wu LW, Baylink DJ, Lau KH. 1996. Molecular cloning and expression of a unique rabbit osteoclastic phosphotyrosyl phosphatase. Biochem J 316:515-523.
59. Yang DH, Goyal M, Sharif K, Kershaw D, Thomas P, Dysko R, Wiggins R. 1996. Glomerular epithelial protein 1 and podocalyxin-like protein 1 in inflammatory glomerular disease (crescentic nephritis) in rabbit and man. Lab Invest 74:571-584.