Cathepsin K deficiency in mice induces structural and metabolic changes in the central nervous system that are associated with learning and memory deficits

BMC Neuroscience

Volumn 12, Issue , 2011, Pages

  Dauth, Stephanie ^a   Sîrbulescu, Ruxandra F ^a,c   Jordans, Silvia ^a,d   Rehders, Maren ^a   Avena, Linda ^a   Oswald, Julia ^a   Lerchl, Alexander ^a   Saftig, Paul ^b   Brix, Klaudia ^a  

^a JACOBS UNIVERSITY BREMEN   (Germany)

^b UNIVERSITY OF KIEL   (Germany)

^c NORTHEASTERN UNIVERSITY   (United States)

^d UNIVERSITY OF BONN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CATHEPSIN B; CATHEPSIN D; CATHEPSIN K; CATHEPSIN L; CYCLIC NUCLEOTIDE PHOSPHODIESTERASE; CYSTATIN C; GLIAL FIBRILLARY ACIDIC PROTEIN; MESSENGER RNA; CTSK PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY LABELING; ANXIETY; ARTICLE; ASTROCYTE; BRAIN CORTEX; BRAIN REGION; CELL COUNT; CENTRAL NERVOUS SYSTEM; CEREBELLUM; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC SYSTEM; ENZYME ACTIVITY; ENZYME HISTOCHEMISTRY; GENE DELETION; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; IMMUNOFLUORESCENCE MICROSCOPY; LEARNING DISORDER; MEMORY DISORDER; MESENCEPHALON; MOUSE; NONHUMAN; OLIGODENDROGLIA; PROTEIN DEGRADATION; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SYNAPSE VESICLE; WILD TYPE; ANIMAL; BRAIN; C57BL MOUSE; ENZYME ACTIVATION; MALE; METABOLISM; MOUSE MUTANT; PATHOLOGY; TISSUE DISTRIBUTION;

ANIMALS; BRAIN; CATHEPSIN K; ENZYME ACTIVATION; LEARNING DISORDERS; MALE; MEMORY DISORDERS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; TISSUE DISTRIBUTION;

EID: 79960666941     PISSN: None     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/1471-2202-12-74     Document Type: Article

References (73)

1. Brix K, Dunkhorst A, Mayer K, Jordans S. Cysteine cathepsins: cellular roadmap to different functions. Biochimie 2008, 90:194-207. 10.1016/j.biochi.2007.07.024, 17825974.
2. Bromme D, Okamoto K. Human cathepsin O2, a novel cysteine protease highly expressed in osteoclastomas and ovary molecular cloning, sequencing and tissue distribution. Biol Chem Hoppe Seyler 1995, 376:379-384. 10.1515/bchm3.1995.376.6.379, 7576232.
3. Gelb BD, Shi GP, Chapman HA, Desnick RJ. Pycnodysostosis, a lysosomal disease caused by cathepsin K deficiency. Science 1996, 273:1236-1238. 10.1126/science.273.5279.1236, 8703060.
4. Saftig P, Hunziker E, Wehmeyer O, Jones S, Boyde A, Rommerskirch W, Moritz JD, Schu P, von Figura K. Impaired osteoclastic bone resorption leads to osteopetrosis in cathepsin-K-deficient mice. Proc Natl Acad Sci USA 1998, 95:13453-13458. 10.1073/pnas.95.23.13453, 24840, 9811821.
5. Kiviranta R, Morko J, Uusitalo H, Aro HT, Vuorio E, Rantakokko J. Accelerated turnover of metaphyseal trabecular bone in mice overexpressing cathepsin K. J Bone Miner Res 2001, 16:1444-1452. 10.1359/jbmr.2001.16.8.1444, 11499867.
6. Desmarais S, Masse F, Percival MD. Pharmacological inhibitors to identify roles of cathepsin K in cell-based studies: a comparison of available tools. Biol Chem 2009, 390:941-948. 10.1515/BC.2009.092, 19453281.
7. Podgorski I. Future of anticathepsin K drugs: dual therapy for skeletal disease and atherosclerosis?. Future Med Chem 2009, 1:21-34. 10.4155/fmc.09.4, 2780340, 20126511.
8. Dauth S, Arampatzidou M, Rehders M, Yu DMT, Führer D, Brix K. Thyroid cathepsin K - roles in physiology and thyroid disease. Clin Rev Bone and Miner Metab 2011, 9:94-106.
9. Punturieri A, Filippov S, Allen E, Caras I, Murray R, Reddy V, Weiss SJ. Regulation of elastinolytic cysteine proteinase activity in normal and cathepsin K-deficient human macrophages. J Exp Med 2000, 192:789-799. 10.1084/jem.192.6.789, 2193285, 10993910.
10. Buhling F, Gerber A, Hackel C, Kruger S, Kohnlein T, Bromme D, Reinhold D, Ansorge S, Welte T. Expression of cathepsin K in lung epithelial cells. Am J Respir Cell Mol Biol 1999, 20:612-619.
11. Haeckel C, Krueger S, Buehling F, Broemme D, Franke K, Schuetze A, Roese I, Roessner A. Expression of cathepsin K in the human embryo and fetus. Dev Dyn 1999, 216:89-95. 10.1002/(SICI)1097-0177(199910)216:2<89::AID-DVDY1>3.0.CO;2-9, 10536050.
12. Tepel C, Bromme D, Herzog V, Brix K. Cathepsin K in thyroid epithelial cells: sequence, localization and possible function in extracellular proteolysis of thyroglobulin. J Cell Sci 2000, 113:4487-4498.
13. Jordans S, Jenko-Kokalj S, Kuhl NM, Tedelind S, Sendt W, Bromme D, Turk D, Brix K. Monitoring compartment-specific substrate cleavage by cathepsins B, K, L, and S at physiological pH and redox conditions. BMC Biochem 2009, 10:23. 10.1186/1471-2091-10-23, 2759951, 19772638.
14. Bernstein HG, Bukowska A, Dobrowolny H, Bogerts B, Lendeckel U. Cathepsin K and schizophrenia. Synapse 2007, 61:252-253. 10.1002/syn.20358, 17230547.
15. Sîrbulescu R, Jordans S, Lerchl A, Saftig P, Kühl NM, Brix K. Trafficking of cysteine cathepsin to the extracellular thyroid follicle lumen helps mice to improve their memory and learning skills. In Book of abstracts/Xth International Symposium on Proteinase Inhibitors and Biological Control, Portoroz, Slovenia, June 23-27, 2007 2007, 53. Jožef Stefan Institute, Ljubljana, Slovenia, Dolinar M, Stoka V, Turk B and Turk V.
16. Friedrichs B, Tepel C, Reinheckel T, Deussing J, von Figura K, Herzog V, Peters C, Saftig P, Brix K. Thyroid functions of mouse cathepsins B, K, and L. J Clin Invest 2003, 111:1733-1745. 156100, 12782676.
17. Koike M, Nakanishi H, Saftig P, Ezaki J, Isahara K, Ohsawa Y, Schulz-Schaeffer W, Watanabe T, Waguri S, Kametaka S, Shibata M, Yamamoto K, Kominami E, Peters C, von Figura K, Uchiyama Y. Cathepsin D deficiency induces lysosomal storage with ceroid lipofuscin in mouse CNS neurons. J Neurosci 2000, 20:6898-6906.
18. Felbor U, Kessler B, Mothes W, Goebel HH, Ploegh HL, Bronson RT, Olsen BR. Neuronal loss and brain atrophy in mice lacking cathepsins B and L. Proc Natl Acad Sci USA 2002, 99:7883-7888. 10.1073/pnas.112632299, 122989, 12048238.
19. Houseweart MK, Pennacchio LA, Vilaythong A, Peters C, Noebels JL, Myers RM. Cathepsin B but not cathepsins L or S contributes to the pathogenesis of Unverricht-Lundborg progressive myoclonus epilepsy (EPM1). J Neurobiol 2003, 56:315-327. 10.1002/neu.10253, 12918016.
20. Desmarais S, Black WC, Oballa R, Lamontagne S, Riendeau D, Tawa P, Duong le T, Pickarski M, Percival MD. Effect of cathepsin K inhibitor basicity on in vivo off-target activities. Mol Pharmacol 2008, 73:147-156.
21. Feher LZ, Kalman J, Puskas LG, Gyulveszi G, Kitajka K, Penke B, Palotas M, Samarova EI, Molnar J, Zvara A, Matin K, Bodi N, Hugyecz M, Pakaski M, Bjelik A, Juhasz A, Bogats G, Janka Z, Palotas A. Impact of haloperidol and risperidone on gene expression profile in the rat cortex. Neurochem Int 2005, 47:271-280. 10.1016/j.neuint.2005.04.020, 15941608.
22. Ko F, Tallerico T, Seeman P. Antipsychotic pathway genes with expression altered in opposite direction by antipsychotics and amphetamine. Synapse 2006, 60:141-151. 10.1002/syn.20287, 16715494.
23. Lendeckel U, Kahne T, Ten Have S, Bukowska A, Wolke C, Bogerts B, Keilhoff G, Bernstein HG. Cathepsin K generates enkephalin from beta-endorphin: a new mechanism with possible relevance for schizophrenia. Neurochem Int 2009, 54:410-417. 10.1016/j.neuint.2009.01.011, 19428782.
24. Lecaille F, Weidauer E, Juliano MA, Bromme D, Lalmanach G. Probing cathepsin K activity with a selective substrate spanning its active site. Biochem J 2003, 375:307-312. 10.1042/BJ20030468, 1223680, 12837132.
25. Kingham PJ, Pocock JM. Microglial secreted cathepsin B induces neuronal apoptosis. J Neurochem 2001, 76:1475-1484. 10.1046/j.1471-4159.2001.00146.x, 11238732.
26. Holscher C. Time, space and hippocampal functions. Rev Neurosci 2003, 14:253-284. 10.1515/REVNEURO.2003.14.3.253, 14513868.
27. Asagiri M, Hirai T, Kunigami T, Kamano S, Gober HJ, Okamoto K, Nishikawa K, Latz E, Golenbock DT, Aoki K, Ohya K, Imai Y, Morishita Y, Miyazono K, Kato S, Saftig P, Takayanagi H. Cathepsin K-dependent toll-like receptor 9 signaling revealed in experimental arthritis. Science 2008, 319:624-627. 10.1126/science.1150110, 18239127.
28. Streit WJ, Xue QS. Life and death of microglia. J Neuroimmune Pharmacol 2009, 4:371-379. 10.1007/s11481-009-9163-5, 19680817.
29. Vaccari A, Rossetti ZL, de Montis G, Stefanini E, Martino E, Gessa GL. Neonatal hypothyroidism induces striatal dopaminergic dysfunction. Neuroscience 1990, 35:699-706. 10.1016/0306-4522(90)90340-A, 2199846.
30. Kandel ER. The biology of memory: a forty-year perspective. J Neurosci 2009, 29:12748-12756. 10.1523/JNEUROSCI.3958-09.2009, 19828785.
31. Bjorklund A, Dunnett SB. Dopamine neuron systems in the brain: an update. Trends Neurosci 2007, 30:194-202. 10.1016/j.tins.2007.03.006, 17408759.
32. Rose AA, Siegel PM. Emerging therapeutic targets in breast cancer bone metastasis. Future Oncol 2010, 6:55-74. 10.2217/fon.09.138, 20021209.
33. Yang M, Sun J, Zhang T, Liu J, Zhang J, Shi MA, Darakhshan F, Guerre-Millo M, Clement K, Gelb BD, Dolgnov G, Shi GP. Deficiency and inhibition of cathepsin K reduce body weight gain and increase glucose metabolism in mice. Arterioscler Thromb Vasc Biol 2008, 28:2202-2208. 10.1161/ATVBAHA.108.172320, 2736686, 18818416.
34. Rachner TD, Khosla S, Hofbauer LC. Osteoporosis: now and the future. Lancet 2011, 377:1276-1287. 10.1016/S0140-6736(10)62349-5, 21450337.
35. Horn S, Heuer H. Thyroid hormone action during brain development: more questions than answers. Mol Cell Endocrinol 2010, 315:19-26. 10.1016/j.mce.2009.09.008, 19765631.
36. Portella AC, Carvalho F, Faustino L, Wondisford FE, Ortiga-Carvalho TM, Gomes FC. Thyroid hormone receptor beta mutation causes severe impairment of cerebellar development. Mol Cell Neurosci 2010, 44:68-77. 10.1016/j.mcn.2010.02.004, 20193766.
37. Gan L, Ye S, Chu A, Anton K, Yi S, Vincent VA, von Schack D, Chin D, Murray J, Lohr S, Patthy L, Gonzalez-Zulueta M, Nikolich K, Urfer R. Identification of cathepsin B as a mediator of neuronal death induced by Abeta-activated microglial cells using a functional genomics approach. J Biol Chem 2004, 279:5565-5572.
38. Kikuchi H, Yamada T, Furuya H, Doh-ura K, Ohyagi Y, Iwaki T, Kira J. Involvement of cathepsin B in the motor neuron degeneration of amyotrophic lateral sclerosis. Acta Neuropathol 2003, 105:462-468.
39. Graber S, Maiti S, Halpain S. Cathepsin B-like proteolysis and MARCKS degradation in sub-lethal NMDA-induced collapse of dendritic spines. Neuropharmacology 2004, 47:706-713. 10.1016/j.neuropharm.2004.08.004, 15458842.
40. Hook V, Yasothornsrikul S, Greenbaum D, Medzihradszky KF, Troutner K, Toneff T, Bundey R, Logrinova A, Reinheckel T, Peters C, Bogyo M. Cathepsin L and Arg/Lys aminopeptidase: a distinct prohormone processing pathway for the biosynthesis of peptide neurotransmitters and hormones. Biol Chem 2004, 385:473-480. 10.1515/BC.2004.055, 15255178.
41. Hayward MD, Low MJ. Naloxone's suppression of spontaneous and food-conditioned locomotor activity is diminished in mice lacking either the dopamine D(2) receptor or enkephalin. Brain Res Mol Brain Res 2005, 140:91-98.
42. Abrahamson M, Alvarez-Fernandez M, Nathanson CM. Cystatins. Biochem Soc Symp 2003, 179-199.
43. Salvesen G, Nagase H. Inhibition of proteolytic enzymes. In Proteolytic Enzymes: a Practical Approach 1989, 1983-1104. IRL Press at Oxford University, Beyon RJ and Bond JS.
44. Tizon B, Sahoo S, Yu H, Gauthier S, Kumar AR, Mohan P, Figliola M, Pawlik M, Grubb A, Uchiyama Y, Bandyopadhyay U, Cuervo AM, Nixon RA, Levy E. Induction of autophagy by cystatin C: a mechanism that protects murine primary cortical neurons and neuronal cell lines. PLoS One 2010, 5:e9819. 10.1371/journal.pone.0009819, 2843718, 20352108.
45. Nakabayashi H, Hara M, Shimuzu K. Clinicopathologic significance of cystatin C expression in gliomas. Hum Pathol 2005, 36:1008-1015. 10.1016/j.humpath.2005.06.021, 16153465.
46. Pennacchio LA, Bouley DM, Higgins KM, Scott MP, Noebels JL, Myers RM. Progressive ataxia, myoclonic epilepsy and cerebellar apoptosis in cystatin B-deficient mice. Nat Genet 1998, 20:251-258. 10.1038/3059, 9806543.
47. Barres BA. The mystery and magic of glia: a perspective on their roles in health and disease. Neuron 2008, 60:430-440. 10.1016/j.neuron.2008.10.013, 18995817.
48. Fellin T. Communication between neurons and astrocytes: relevance to the modulation of synaptic and network activity. J Neurochem 2009, 108:533-544. 10.1111/j.1471-4159.2008.05830.x, 19187090.
49. Rossi D, Volterra A. Astrocytic dysfunction: insights on the role in neurodegeneration. Brain Res Bull 2009, 80:224-232. 10.1016/j.brainresbull.2009.07.012, 19631259.
50. Streit WJ. Microglia as neuroprotective, immunocompetent cells of the CNS. Glia 2002, 40:133-139. 10.1002/glia.10154, 12379901.
51. Voon V, Fernagut PO, Wickens J, Baunez C, Rodriguez M, Pavon N, Juncos JL, Obeso JA, Bezard E. Chronic dopaminergic stimulation in Parkinson's disease: from dyskinesias to impulse control disorders. Lancet Neurol 2009, 8:1140-1149. 10.1016/S1474-4422(09)70287-X, 19909912.
52. Pezze MA, Feldon J. Mesolimbic dopaminergic pathways in fear conditioning. Prog Neurobiol 2004, 74:301-320. 10.1016/j.pneurobio.2004.09.004, 15582224.
53. Adriani W, Sargolini F, Coccurello R, Oliverio A, Mele A. Role of dopaminergic system in reactivity to spatial and non-spatial changes in mice. Psychopharmacology (Berl) 2000, 150:67-76.
54. Nagatsu T, Levitt M, Udenfriend S. Tyrosine Hydroxylase. the Initial Step in Norepinephrine Biosynthesis. J Biol Chem 1964, 239:2910-2917.
55. Ichihara K, Nabeshima T, Kameyama T. Effects of dopamine receptor agonists on passive avoidance learning in mice: interaction of dopamine D1 and D2 receptors. Eur J Pharmacol 1992, 213:243-249. 10.1016/0014-2999(92)90688-Z, 1355736.
56. de Oliveira AR, Reimer AE, Brandao ML. Dopamine D2 receptor mechanisms in the expression of conditioned fear. Pharmacol Biochem Behav 2006, 84:102-111. 10.1016/j.pbb.2006.04.012, 16780936.
57. Margolis EB, Lock H, Chefer VI, Shippenberg TS, Hjelmstad GO, Fields HL. Kappa opioids selectively control dopaminergic neurons projecting to the prefrontal cortex. Proc Natl Acad Sci USA 2006, 103:2938-2942. 10.1073/pnas.0511159103, 1413839, 16477003.
58. Canalis E. New Treatment Modalities in Osteoporosis. Endocr Pract 2010, 16:855-863. 10.4158/EP10048.RA, 20350910.
59. Karl T, Pabst R, von Horsten S. Behavioral phenotyping of mice in pharmacological and toxicological research. Exp Toxicol Pathol 2003, 55:69-83. 10.1078/0940-2993-00301, 12940631.
60. Rodriguiz RM, Wetsel WC. Assessments of Cognitive Deficits in Mutant Mice. Animal Models of Cognitive Impairment 2006, Boca Raton (FL): CRC Press, Levin ED and Buccafusco JJ, Chapter 12.
61. Pellow S, Chopin P, File SE, Briley M. Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods 1985, 14:149-167. 10.1016/0165-0270(85)90031-7, 2864480.
62. Karasawa J, Hashimoto K, Chaki S. D-Serine and a glycine transporter inhibitor improve MK-801-induced cognitive deficits in a novel object recognition test in rats. Behav Brain Res 2008, 186:78-83. 10.1016/j.bbr.2007.07.033, 17854919.
63. Zhuang X, Oosting RS, Jones SR, Gainetdinov RR, Miller GW, Caron MG, Hen R. Hyperactivity and impaired response habituation in hyperdopaminergic mice. Proc Natl Acad Sci USA 2001, 98:1982-1987. 10.1073/pnas.98.4.1982, 29368, 11172062.
64. Barkus C, McHugh SB, Sprengel R, Seeburg PH, Rawlins JN, Bannerman DM. Hippocampal NMDA receptors and anxiety: at the interface between cognition and emotion. Eur J Pharmacol 2010, 626:49-56. 10.1016/j.ejphar.2009.10.014, 2824088, 19836379.
65. Bannerman DM, Rawlins JN, McHugh SB, Deacon RM, Yee BK, Bast T, Zhang WN, Pothuizen HH, Feldon J. Regional dissociations within the hippocampus--memory and anxiety. Neurosci Biobehav Rev 2004, 28:273-283. 10.1016/j.neubiorev.2004.03.004, 15225971.
66. Figueiredo J, Reis A, Vaz R, Leao M, Cruz C. Porencephalic cyst in pycnodysostosis. J Med Genet 1989, 26:782-784. 10.1136/jmg.26.12.782, 1015763, 2614800.
67. Klose M, Grote K, Lerchl A. Temporal control of spermatogenesis is independent of the central circadian pacemaker in Djungarian hamsters (Phodopus sungorus). Biol Reprod 2011, 84:124-129. 10.1095/biolreprod.110.085126, 20826727.
68. Neuhoff V, Philipp K, Zimmer HG, Mesecke S. A simple, versatile, sensitive and volume-independent method for quantitative protein determination which is independent of other external influences. Hoppe Seylers Z Physiol Chem 1979, 360:1657-1670. 10.1515/bchm2.1979.360.2.1657, 92445.
69. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 1987, 162:156-159.
70. Barrett AJ. Fluorimetric assays for cathepsin B and cathepsin H with methylcoumarylamide substrates. Biochem J 1980, 187:909-912. 1162479, 6897924.
71. Mayer K, Vreemann A, Qu H, Brix K. Release of endo-lysosomal cathepsins B, D, and L from IEC6 cells in a cell culture model mimicking intestinal manipulation. Biol Chem 2009, 390:471-480. 10.1515/BC.2009.047, 19284293.
72. Yasuda Y, Kageyama T, Akamine A, Shibata M, Kominami E, Uchiyama Y, Yamamoto K. Characterization of new fluorogenic substrates for the rapid and sensitive assay of cathepsin E and cathepsin D. J Biochem 1999, 125:1137-1143.
73. Carpenter AE, Jones TR, Lamprecht MR, Clarke C, Kang IH, Friman O, Guertin DA, Chang JH, Lindquist RA, Moffat J, Golland P, Sabatini DM. CellProfiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol 2006, 7:R100. 10.1186/gb-2006-7-10-r100, 1794559, 17076895.