Selective Decline of Synaptic Protein Levels in the Frontal Cortex of Female Mice Deficient in the Extracellular Metalloproteinase ADAMTS1

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Howell, Matthew D ^a   Torres Collado, Antoni X ^b   Iruela Arispe, M Luisa ^b   Gottschall, Paul E ^a  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAMTS1 PROTEIN; BREVICAN; MESSENGER RNA; NEUROCAN; VERSICAN;

ADAMTS1 GENE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN LEVEL; CONTROLLED STUDY; FEMALE; FRONTAL CORTEX; GENE; GENE EXPRESSION; MALE; MAZE TEST; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PROTEIN DEGRADATION; PROTEIN FUNCTION; SEX DIFFERENCE;

ADAM PROTEINS; ANIMALS; CEREBRAL CORTEX; EXTRACELLULAR MATRIX; FEMALE; LEARNING; MALE; MEMORY; MICE; NEURONAL PLASTICITY; RECEPTORS, AMPA; RNA, MESSENGER; SYNAPSES;

EID: 84867423386     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0047226     Document Type: Article

References (49)

1. Dityatev A, Schachner M, Sonderegger P, (2010) The dual role of the extracellular matrix in synaptic plasticity and homeostasis. Nat Rev Neurosci 11: 735-746.
2. Yamaguchi Y, (2000) Lecticans: organizers of the brain extracellular matrix. Cell Mol Life Sci 57: 276-289.
3. Bruckner G, Brauer K, Hartig W, Wolff JR, Rickmann MJ, et al. (1993) Perineuronal nets provide a polyanionic, glia-associated form of microenvironment around certain neurons in many parts of the rat brain. Glia 8: 183-200.
4. Pizzorusso T, Medini P, Berardi N, Chierzi S, Fawcett JW, et al. (2002) Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298: 1248-1251.
5. Gogolla N, Caroni P, Luthi A, Herry C, (2009) Perineuronal nets protect fear memories from erasure. Science 325: 1258-1261.
6. Fitch MT, Silver J, (2008) CNS injury, glial scars, and inflammation: Inhibitory extracellular matrices and regeneration failure. Exp Neurol 209: 294-301.
7. Bradbury EJ, Moon LD, Popat RJ, King VR, Bennett GS, et al. (2002) Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416: 636-640.
8. Huang WC, Kuo WC, Cherng JH, Hsu SH, Chen PR, et al. (2006) Chondroitinase ABC promotes axonal re-growth and behavior recovery in spinal cord injury. Biochem Biophys Res Commun 349: 963-968.
9. Schmalfeldt M, Bandtlow CE, Dours-Zimmermann MT, Winterhalter KH, Zimmermann DR, (2000) Brain derived versican V2 is a potent inhibitor of axonal growth. J Cell Sci 113 (Pt 5): 807-816.
10. Monnier PP, Sierra A, Schwab JM, Henke-Fahle S, Mueller BK, (2003) The Rho/ROCK pathway mediates neurite growth-inhibitory activity associated with the chondroitin sulfate proteoglycans of the CNS glial scar. Mol Cell Neurosci 22: 319-330.
11. Jones GC, Riley GP, (2005) ADAMTS proteinases: a multi-domain, multi-functional family with roles in extracellular matrix turnover and arthritis. Arthritis Res Ther 7: 160-169.
12. Porter S, Clark IM, Kevorkian L, Edwards DR, (2005) The ADAMTS metalloproteinases. Biochem J 386: 15-27.
13. Russell DL, Doyle KM, Ochsner SA, Sandy JD, Richards JS, (2003) Processing and localization of ADAMTS-1 and proteolytic cleavage of versican during cumulus matrix expansion and ovulation. J Biol Chem 278: 42330-42339.
14. Richards JS, Hernandez-Gonzalez I, Gonzalez-Robayna I, Teuling E, Lo Y, et al. (2005) Regulated expression of ADAMTS family members in follicles and cumulus oocyte complexes: evidence for specific and redundant patterns during ovulation. Biol Reprod 72: 1241-1255.
15. Mittaz L, Russell DL, Wilson T, Brasted M, Tkalcevic J, et al. (2004) Adamts-1 is essential for the development and function of the urogenital system. Biol Reprod 70: 1096-1105.
16. Shindo T, Kurihara H, Kuno K, Yokoyama H, Wada T, et al. (2000) ADAMTS-1: a metalloproteinase-disintegrin essential for normal growth, fertility, and organ morphology and function. J Clin Invest 105: 1345-1352.
17. Yokoyama H, Wada T, Kobayashi K, Kuno K, Kurihara H, et al. (2002) A disintegrin and metalloproteinase with thrombospondin motifs (ADAMTS)-1 null mutant mice develop renal lesions mimicking obstructive nephropathy. Nephrol Dial Transplant 17 (Suppl 9): 39-41.
18. Lee NV, Rodriguez-Manzaneque JC, Thai SN, Twal WO, Luque A, et al. (2005) Fibulin-1 acts as a cofactor for the matrix metalloprotease ADAMTS-1. J Biol Chem 280: 34796-34804.
19. Frischknecht R, Heine M, Perrais D, Seidenbecher CI, Choquet D, et al. (2009) Brain extracellular matrix affects AMPA receptor lateral mobility and short-term synaptic plasticity. Nat Neurosci 12: 897-904.
20. Hamel MG, Mayer J, Gottschall PE, (2005) Altered production and proteolytic processing of brevican by transforming growth factor beta in cultured astrocytes. J Neurochem 93: 1533-1541.
21. Hamel MG, Ajmo JM, Leonardo CC, Zuo F, Sandy JD, et al. (2008) Multimodal signaling by the ADAMTSs (a disintegrin and metalloproteinase with thrombospondin motifs) promotes neurite extension. Exp Neurol 210: 428-440.
22. Alamed J, Wilcock DM, Diamond DM, Gordon MN, Morgan D, (2006) Two-day radial-arm water maze learning and memory task; robust resolution of amyloid-related memory deficits in transgenic mice. Nat Protoc 1: 1671-1679.
23. Howell MD, Gottschall PE (2012) Altered synaptic marker abundance in the hippocampal stratum oriens of Ts65Dn mice is associated with exuberant expression of versican. ASN Neuro 4: art: e00073.doi:00010.01042/AN20110037.
24. Mayer J, Hamel MG, Gottschall PE, (2005) Evidence for proteolytic cleavage of brevican by the ADAMTSs in the dentate gyrus after excitotoxic lesion of the mouse entorhinal cortex. BMC Neurosci 6: 52.
25. Ajmo JM, Bailey LA, Howell MD, Cortez LK, Pennypacker KR, et al. (2010) Abnormal post-translational and extracellular processing of brevican in plaque-bearing mice over-expressing APPsw. J Neurochem 113: 784-795.
26. Gottschall PE, Ajmo JM, Eakin AK, Howell MD, Mehta H, et al. (2010) Panel of synaptic protein ELISAs for evaluating neurological phenotype. Exp Brain Res 201: 885-893.
27. Nairn AV, Kinoshita-Toyoda A, Toyoda H, Xie J, Harris K, et al. (2007) Glycomics of proteoglycan biosynthesis in murine embryonic stem cell differentiation. J Proteome Res 6: 4374-4387.
28. Milev P, Maurel P, Chiba A, Mevissen M, Popp S, et al. (1998) Differential regulation of expression of hyaluronan-binding proteoglycans in brain: aggreacan, versican neurocan and brevican. Biochem Biophys Res Comm 247: 207-2121.
29. Aya-ay J, Mayer J, Eakin AK, Muffly BG, Anello M, et al. (2005) The effect of hypoxic-ischemic brain injury in perinatal rats on the abundance and proteolysis of brevican and NG2. Exp Neurol 193: 149-162.
30. Wright JW, Brown TE, Harding JW, (2007) Inhibition of hippocampal matrix metalloproteinase-3 and-9 disrupts spatial memory. Neural Plast 2007: 73813.
31. Bozdagi O, Nagy V, Kwei KT, Huntley GW, (2007) In vivo roles for matrix metalloproteinase-9 in mature hippocampal synaptic physiology and plasticity. J Neurophysiol 98: 334-344.
32. Wang XB, Bozdagi O, Nikitczuk JS, Zhai ZW, Zhou Q, et al. (2008) Extracellular proteolysis by matrix metalloproteinase-9 drives dendritic spine enlargement and long-term potentiation coordinately. Proc Natl Acad Sci U S A 105: 19520-19525.
33. Yuan W, Matthews RT, Sandy JD, Gottschall PE, (2002) Association between protease-specific proteolytic cleavage of brevican and synaptic loss in the dentate gyrus of kainate-treated rats. Neuroscience 114: 1091-1101.
34. Prange CK, Pennacchio LA, Lieuallen K, Fan W, Lennon GG, (1998) Characterization of the human neurocan gene, CSPG3. Gene 221: 199-205.
35. Turk BE, Huang LL, Piro ET, Cantley LC, (2001) Determination of protease cleavage site motifs using mixture-based oriented peptide libraries. Nat Biotechnol 19: 661-667.
36. Tauchi R, Imagama S, Natori T, Ohgomori T, Muramoto A, et al. (2012) The endogenous proteoglycan-degrading enzyme ADAMTS-4 promotes functional recovery after spinal cord injury. J Neuroinflammation 9: 53.
37. Woolley CS, Gould E, Frankfurt M, McEwen BS, (1990) Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. J Neurosci 10: 4035-4039.
38. Gould E, Woolley CS, Frankfurt M, McEwen BS, (1990) Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J Neurosci 10: 1286-1291.
39. Woolley CS, McEwen BS, (1993) Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat. J Comp Neurol 336: 293-306.
40. Shozu M, Minami N, Yokoyama H, Inoue M, Kurihara H, et al. (2005) ADAMTS-1 is involved in normal follicular development, ovulatory process and organization of the medullary vascular network in the ovary. J Mol Endocrinol 35: 343-355.
41. Bosse R, Di Paolo T, (1995) Dopamine and GABAA receptor imbalance after ovariectomy in rats: model of menopause. J Psychiatry Neurosci 20: 364-371.
42. Cyr M, Bosse R, Di Paolo T, (1998) Gonadal hormones modulate 5-hydroxytryptamine2A receptors: emphasis on the rat frontal cortex. Neuroscience 83: 829-836.
43. O'Shea KS, Liu LH, Dixit VM, (1991) Thrombospondin and a 140 kd fragment promote adhesion and neurite outgrowth from embryonic central and peripheral neurons and from PC12 cells. Neuron 7: 231-237.
44. Christopherson KS, Ullian EM, Stokes CC, Mullowney CE, Hell JW, et al. (2005) Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell 120: 421-433.
45. Eroglu C, Allen NJ, Susman MW, O'Rourke NA, Park CY, et al. (2009) Gabapentin receptor alpha2delta-1 is a neuronal thrombospondin receptor responsible for excitatory CNS synaptogenesis. Cell 139: 380-392.
46. Raulo E, Tumova S, Pavlov I, Pekkanen M, Hienola A, et al. (2005) The two thrombospondin type I repeat domains of the heparin-binding growth-associated molecule bind to heparin/heparan sulfate and regulate neurite extension and plasticity in hippocampal neurons. J Biol Chem 280: 41576-41583.
47. Xu J, Xiao N, Xia J, (2010) Thrombospondin 1 accelerates synaptogenesis in hippocampal neurons through neuroligin 1. Nat Neurosci 13: 22-24.
48. Michaluk P, Mikasova L, Groc L, Frischknecht R, Choquet D, et al. (2009) Matrix metalloproteinase-9 controls NMDA receptor surface diffusion through integrin beta1 signaling. J Neurosci 29: 6007-6012.
49. Lee NV, Sato M, Annis DS, Loo JA, Wu L, et al. (2006) ADAMTS1 mediates the release of antiangiogenic polypeptides from TSP1 and 2. EMBO J 25: 5270-5283.