Proteoglycan abnormalities in olfactory epithelium tissue from subjects diagnosed with schizophrenia

Schizophrenia Research

Volumn 150, Issue 2-3, 2013, Pages 366-372

  Pantazopoulos, Harry ^a,b   Boyer Boiteau, Anne ^b   Holbrook, Eric H ^c,d   Jang, Woochan ^d   Hahn, Chang Gyu ^e   Arnold, Steven E ^e   Berretta, Sabina ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MCLEAN HOSPITAL   (United States)

^c MASSACHUSETTS EYE AND EAR INFIRMARY   (United States)

^d TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Chondroitin sulfate proteoglycans; Extracellular matrix; Olfactory epithelium; Postmortem; Schizophrenia

Indexed keywords

PROTEOCHONDROITIN SULFATE;

ADULT; AGED; ARTICLE; AUTOPSY; BASAL CELL; CELL DENSITY; CELL MATURATION; CELLULAR DISTRIBUTION; CLINICAL ARTICLE; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; NERVE CELL DIFFERENTIATION; NERVE FIBER; OLFACTORY EPITHELIUM; OLFACTORY RECEPTOR; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEFECT; PROTEIN EXPRESSION;

BOVINE ALBUMIN SERUM; BSA; C-CSPG; CHLORPROMAZINE-EQUIVALENT; CHONDROITIN SULFATE PROTEOGLYCAN; CHONDROITIN SULFATE PROTEOGLYCANS; CPZ; CSPG; CYTOPLASMIC CHONDROITIN SULFATE PROTEOGLYCAN; EXTRACELLULAR MATRIX; GAG; GAP43; GLYCOSAMINOGLYCAN; GROWTH ASSOCIATE PROTEIN 43; NEURAL STEM/CELL PROGENITOR; NSCP; OE; OLFACTORY EPITHELIUM; OLFACTORY MARKER PROTEIN; OLFACTORY RECEPTOR NEURON; OMP; ORN; P-CSPG; PBS-TX; PERICELLULAR CHONDROITIN SULFATE PROTEOGLYCAN; PHOSPHATE BUFFER-TRITON X; PMI; POSTMORTEM; POSTMORTEM TIME INTERVAL; RE; RECEPTOR TYROSINE PHOSPHATASE ZETA; RESPIRATORY EPITHELIUM; RPTPZ; SCHIZOPHRENIA; SCID; STRUCTURED CLINICAL INTERVIEW FOR DSM DISORDERS; SZ; WFA; WISTERIA FLORIBUNDA AGGLUTININ;

ADULT; AGED; AGED, 80 AND OVER; BIOPSY; CASE-CONTROL STUDIES; FEMALE; GAP-43 PROTEIN; HUMANS; MALE; MIDDLE AGED; OLFACTORY MARKER PROTEIN; OLFACTORY MUCOSA; PLANT LECTINS; PROTEOGLYCANS; RECEPTOR-LIKE PROTEIN TYROSINE PHOSPHATASES, CLASS 5; RECEPTORS, CELL SURFACE; RECEPTORS, N-ACETYLGLUCOSAMINE; SCHIZOPHRENIA; VERSICANS;

EID: 84886278980     PISSN: 09209964     EISSN: 15732509     Source Type: Journal    
DOI: 10.1016/j.schres.2013.08.013     Document Type: Article

References (50)

1. Arnold S.E., Rioux L. Challenges, status, and opportunities for studying developmental neuropathology in adult schizophrenia. Schizophr. Bull. 2001, 27(3):395-416.
2. Arnold S.E., Han L.Y., Moberg P.J., Turetsky B.I., Gur R.E., Trojanowski J.Q., Hahn C.G. Dysregulation of olfactory receptor neuron lineage in schizophrenia. Arch. Gen. Psychiatry 2001, 58(9):829-835.
3. Atanasova B., Graux J., El Hage W., Hommet C., Camus V., Belzung C. Olfaction: a potential cognitive marker of psychiatric disorders. Neurosci. Biobehav. Rev. 2008, 32(7):1315-1325.
4. Beites C.L., Kawauchi S., Crocker C.E., Calof A.L. Identification and molecular regulation of neural stem cells in the olfactory epithelium. Exp. Cell Res. 2005, 306(2):309-316.
5. Belluscio L., Katz L.C. Symmetry, stereotypy, and topography of odorant representations in mouse olfactory bulbs. J. Neurosci. 2001, 21(6):2113-2122.
6. Berretta S. Extracellular matrix abnormalities in schizophrenia. Neuropharmacology 2012, 62(3):1584-1597.
7. Brewer W.J., Pantelis C., Anderson V., Velakoulis D., Singh B., Copolov D.L., McGorry P.D. Stability of olfactory identification deficits in neuroleptic-naive patients with first-episode psychosis. Am. J. Psychiatry 2001, 158(1):107-115.
8. Buxbaum J.D., Georgieva L., Young J.J., Plescia C., Kajiwara Y., Jiang Y., Moskvina V., Norton N., Peirce T., Williams H., Craddock N.J., Carroll L., Corfas G., Davis K.L., Owen M.J., Harroch S., Sakurai T., O'Donovan M.C. Molecular dissection of NRG1-ERBB4 signaling implicates PTPRZ1 as a potential schizophrenia susceptibility gene. Mol. Psychiatry 2008, 13(2):162-172.
9. Carulli D., Laabs T., Geller H.M., Fawcett J.W. Chondroitin sulfate proteoglycans in neural development and regeneration. Curr. Opin. Neurobiol. 2005, 15(1):116-120.
10. Clarris H.J., Rauch U., Key B. Dynamic spatiotemporal expression patterns of neurocan and phosphacan indicate diverse roles in the developing and adult mouse olfactory system. J. Comp. Neurol. 2000, 423(1):99-111.
11. Dityatev A., Seidenbecher C.I., Schachner M. Compartmentalization from the outside: the extracellular matrix and functional microdomains in the brain. Trends Neurosci. 2010, 33(11):503-512.
12. Dours-Zimmermann M.T., Zimmermann D.R. A novel glycosaminoglycan attachment domain identified in two alternative splice variants of human versican. J. Biol. Chem. 1994, 269(52):32992-32998.
13. Enwright J.F.I., Arion D., Fish K., Lewis D. Decreased perineuronal net labeling and altered parvalbumin immunoreactivity in the dorsal lateral prefrontal cortex of subjects with schizophrenia 2012, Society for Neuroscience.
14. Fan Y., Abrahamsen G., McGrath J.J., Mackay-Sim A. Altered cell cycle dynamics in schizophrenia. Biol. Psychiatry 2012, 71(2):129-135.
15. Farbman A.I., Margolis F.L. Olfactory marker protein during ontogeny: immunohistochemical localization. Dev. Biol. 1980, 74(1):205-215.
16. Feron F., Perry C., Hirning M.H., McGrath J., Mackay-Sim A. Altered adhesion, proliferation and death in neural cultures from adults with schizophrenia. Schizophr. Res. 1999, 40(3):211-218.
17. Frischknecht R., Heine M., Perrais D., Seidenbecher C.I., Choquet D., Gundelfinger E.D. Brain extracellular matrix affects AMPA receptor lateral mobility and short-term synaptic plasticity. Nat. Neurosci. 2009, 12(7):897-904.
18. Gonzalez M.L., Silver J. Axon-glia interactions regulate ECM patterning in the postnatal rat olfactory bulb. J. Neurosci. 1994, 14(10):6121-6131.
19. Graziadei P.P. Cell dynamics in the olfactory mucosa. Tissue Cell 1973, 5(1):113-131.
20. Hahn C.G., Han L.Y., Rawson N.E., Mirza N., Borgmann-Winter K., Lenox R.H., Arnold S.E. In vivo and in vitro neurogenesis in human olfactory epithelium. J. Comp. Neurol. 2005, 483(2):154-163.
21. Harrison P.J. Schizophrenia susceptibility genes and their neurodevelopmental implications: focus on neuregulin 1. Novartis Found. Symp. 2007, 288:246-255. (discussion 255-249, 276-281).
22. Hayar A., Karnup S., Shipley M.T., Ennis M. Olfactory bulb glomeruli: external tufted cells intrinsically burst at theta frequency and are entrained by patterned olfactory input. J. Neurosci. 2004, 24(5):1190-1199.
23. Holbrook E.H., Wu E., Curry W.T., Lin D.T., Schwob J.E. Immunohistochemical characterization of human olfactory tissue. Laryngoscope 2011, 121(8):1687-1701.
24. Ito Y., Hikino M., Yajima Y., Mikami T., Sirko S., von Holst A., Faissner A., Fukui S., Sugahara K. Structural characterization of the epitopes of the monoclonal antibodies 473HD, CS-56, and MO-225 specific for chondroitin sulfate D-type using the oligosaccharide library. Glycobiology 2005, 15(6):593-603.
25. Klausmeyer A., Conrad R., Faissner A., Wiese S. Influence of glial-derived matrix molecules, especially chondroitin sulfates, on neurite growth and survival of cultured mouse embryonic motoneurons. J. Neurosci. Res. 2011, 89(2):127-141.
26. Kopala L.C., Clark C., Hurwitz T. Olfactory deficits in neuroleptic naive patients with schizophrenia. Schizophr. Res. 1993, 8(3):245-250.
27. Maeda N. Structural variation of chondroitin sulfate and its roles in the central nervous system. Cent. Nerv. Syst. Agents Med. Chem. 2010, 10(1):22-31.
28. Maeda N., Fukazawa N., Ishii M. Chondroitin sulfate proteoglycans in neural development and plasticity. Front. Biosci. 2010, 15:626-644.
29. Mauney S.A., Athanas K.M., Pantazopoulos H., Shaskan N., Passeri E., Berretta S., Woo T.U. Developmental pattern of perineuronal nets in the human prefrontal cortex and their deficit in schizophrenia. Biol. Psychiatry 2013, 74(6):427-435.
30. McCurdy R.D., Feron F., Perry C., Chant D.C., McLean D., Matigian N., Hayward N.K., McGrath J.J., Mackay-Sim A. Cell cycle alterations in biopsied olfactory neuroepithelium in schizophrenia and bipolar I disorder using cell culture and gene expression analyses. Schizophr. Res. 2006, 82(2-3):163-173.
31. Meyer-Puttlitz B., Junker E., Margolis R.U., Margolis R.K. Chondroitin sulfate proteoglycans in the developing central nervous system. II. Immunocytochemical localization of neurocan and phosphacan. J. Comp. Neurol. 1996, 366(1):44-54.
32. Moberg P.J., Agrin R., Gur R.E., Gur R.C., Turetsky B.I., Doty R.L. Olfactory dysfunction in schizophrenia: a qualitative and quantitative review. Neuropsychopharmacology 1999, 21(3):325-340.
33. Moran A., Avendano C., Reinoso-Suarez F. Thalamic afferents to the motor cortex in the cat. A horseradish peroxidase study. Neurosci. Lett. 1982, 33:229-233.
34. Morrison E.E., Costanzo R.M. Morphology of the human olfactory epithelium. J. Comp. Neurol. 1990, 297(1):1-13.
35. Pantazopoulos H., Woo T.-U.W., Lim M.P., Lange N., Berretta S. Extracellular matrix-glial abnormalities in the amygdala and entorhinal cortex of subjects diagnosed with schizophrenia. Arch. Gen. Psychiatry 2010, 67(2):155-166.
36. Perry C., Mackay-Sim A., Feron F., McGrath J. Olfactory neural cells: an untapped diagnostic and therapeutic resource. The 2000 Ogura Lecture. Laryngoscope 2002, 112(4):603-607.
37. Popp S., Andersen J.S., Maurel P., Margolis R.U. Localization of aggrecan and versican in the developing rat central nervous system. Dev. Dyn. 2003, 227(1):143-149.
38. Purushothaman A., Sugahara K., Faissner A. Chondroitin sulfate "wobble motifs" modulate maintenance and differentiation of neural stem cells and their progeny. J. Biol. Chem. 2012, 287(5):2935-2942.
39. Rhodes K.E., Fawcett J.W. Chondroitin sulphate proteoglycans: preventing plasticity or protecting the CNS?. J. Anat. 2004, 204(1):33-48.
40. Schwob J.E. Neural regeneration and the peripheral olfactory system. Anat. Rec. 2002, 269(1):33-49.
41. Sirko S., von Holst A., Weber A., Wizenmann A., Theocharidis U., Gotz M., Faissner A. Chondroitin sulfates are required for fibroblast growth factor-2-dependent proliferation and maintenance in neural stem cells and for epidermal growth factor-dependent migration of their progeny. Stem Cells 2010, 28(4):775-787.
42. Takahashi N., Sakurai T., Bozdagi-Gunal O., Dorr N.P., Moy J., Krug L., Gama-Sosa M., Elder G.A., Koch R.J., Walker R.H., Hof P.R., Davis K.L., Buxbaum J.D. Increased expression of receptor phosphotyrosine phosphatase-[beta]/[zeta] is associated with molecular, cellular, behavioral and cognitive schizophrenia phenotypes. Transl. Psychiatry 2011, 1:e8.
43. Tisay K.T., Key B. The extracellular matrix modulates olfactory neurite outgrowth on ensheathing cells. J. Neurosci. 1999, 19(22):9890-9899.
44. Turetsky B.I., Kohler C.G., Gur R.E., Moberg P.J. Olfactory physiological impairment in first-degree relatives of schizophrenia patients. Schizophr. Res. 2008, 102(1-3):220-229.
45. Turetsky B.I., Hahn C.G., Arnold S.E., Moberg P.J. Olfactory receptor neuron dysfunction in schizophrenia. Neuropsychopharmacology 2009, 34(3):767-774.
46. Verhaagen J., Oestreicher A.B., Gispen W.H., Margolis F.L. The expression of the growth associated protein B50/GAP43 in the olfactory system of neonatal and adult rats. J. Neurosci. 1989, 9(2):683-691.
47. von Holst A., Sirko S., Faissner A. The unique 473HD-Chondroitinsulfate epitope is expressed by radial glia and involved in neural precursor cell proliferation. J. Neurosci. 2006, 26(15):4082-4094.
48. Wu Y., Sheng W., Chen L., Dong H., Lee V., Lu F., Wong C.S., Lu W.Y., Yang B.B. Versican V1 isoform induces neuronal differentiation and promotes neurite outgrowth. Mol. Biol. Cell 2004, 15(5):2093-2104.
49. Yanagisawa M., Yu R.K. The expression and functions of glycoconjugates in neural stem cells. Glycobiology 2007, 17(7):57R-74R.
50. Yoshihara Y., Mori K. Basic principles and molecular mechanisms of olfactory axon pathfinding. Cell Tissue Res. 1997, 290(2):457-463.