Loss of CB1 receptors leads to decreased cathepsin D levels and accelerated lipofuscin accumulation in the hippocampus

Mechanisms of Ageing and Development

Volumn 134, Issue 9, 2013, Pages 391-399

  Piyanova, Anastasia ^a,b   Albayram, Onder ^a   Rossi, Carlo Alberto ^b   Farwanah, Hany ^a   Michel, Kerstin ^a   Nicotera, Pierluigi ^b   Sandhoff, Konrad ^a   Bilkei Gorzo, Andras ^a  

^a UNIVERSITY OF BONN   (Germany)

^b GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

Author keywords

Autophagy; Endocannabinoid system; Hippocampus; LC3; Oxidative stress; P62

Indexed keywords

8 HYDROXYDEOXYGUANOSINE; CANNABINOID 1 RECEPTOR; CARBONYL DERIVATIVE; CATHEPSIN D; LC3 II PROTEIN; LIPOFUSCIN; MEMBRANE PROTEIN; PROTEIN P62; PROTEINASE; THIOBARBITURIC ACID REACTIVE SUBSTANCE; UNCLASSIFIED DRUG;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; BRAIN CORTEX; BRAIN HOMOGENATE; CONTROLLED STUDY; CORPUS STRIATUM; FEMALE; FLUORESCENCE ANALYSIS; GENOTYPE; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; KNOCKOUT MOUSE; LIPID PEROXIDATION; LYSOSOME; MACROMOLECULE; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CARBONYLATION; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; UPREGULATION;

AUTOPHAGY; ENDOCANNABINOID SYSTEM; HIPPOCAMPUS; LC3; OXIDATIVE STRESS; P62;

AGING; ANIMALS; AUTOPHAGY; BRAIN; CATHEPSIN D; ENDOCANNABINOIDS; FEMALE; HIPPOCAMPUS; INFLAMMATION; LIPID PEROXIDATION; LIPOFUSCIN; LYSOSOMES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; OXIDATIVE STRESS; OXYGEN; RECEPTOR, CANNABINOID, CB1; TISSUE DISTRIBUTION;

EID: 84885828571     PISSN: 00476374     EISSN: 18726216     Source Type: Journal    
DOI: 10.1016/j.mad.2013.08.001     Document Type: Article

References (58)

1. Albayram O., Alferink J., Pitsch J., Piyanova A., Neitzert K., Poppensieker K., Mauer D., Michel K., Legler A., Becker A., Monory K., Lutz B., Zimmer A., Bilkei-Gorzo A. Role of CB1 cannabinoid receptors on GABAergic neurons in brain aging. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:11256-11261.
2. Albayram O., Bilkei-Gorzo A., Zimmer A. Loss of CB1 receptors leads to differential age-related changes in reward-driven learning and memory. Front Aging Neurosci. 2012, 4:34.
3. Assuncao M., Santos-Marques M.J., Carvalho F., Lukoyanov N.V., Andrade J.P. Chronic green tea consumption prevents age-related changes in rat hippocampal formation. Neurobiol. Aging 2011, 32:707-717.
4. Bilkei-Gorzo A., Drews E., Albayram O., Piyanova A., Gaffal E., Tueting T., Michel K., Mauer D., Maier W., Zimmer A. Early onset of aging-like changes is restricted to cognitive abilities and skin structure in Cnr1(-/-) mice. Neurobiol. Aging 2012, 33. 200.e211-222.
5. Bilkei-Gorzo A., Racz I., Valverde O., Otto M., Michel K., Sastre M., Zimmer A. Early age-related cognitive impairment in mice lacking cannabinoid CB1 receptors. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:15670-15675.
6. Bishop N.A., Lu T., Yankner B.A. Neural mechanisms of ageing and cognitive decline. Nature 2010, 464:529-535.
7. Boland B., Kumar A., Lee S., Platt F.M., Wegiel J., Yu W.H., Nixon R.A. Autophagy induction and autophagosome clearance in neurons: relationship to autophagic pathology in Alzheimer's disease. J. Neurosci. 2008, 28:6926-6937.
8. Brailoiu G.C., Oprea T.I., Zhao P., Abood M.E., Brailoiu E. Intracellular cannabinoid type 1 (CB1) receptors are activated by anandamide. J. Biol. Chem. 2011, 286:29166-29174.
9. Bruce A.J., Baudry M. Oxygen free radicals in rat limbic structures after kainate-induced seizures. Free Radic. Biol. Med. 1995, 18:993-1002.
10. Brunk U.T., Terman A. The mitochondrial-lysosomal axis theory of aging: accumulation of damaged mitochondria as a result of imperfect autophagocytosis. Eur. J. Biochem. 2002, 269:1996-2002.
11. Cai J., Qi X., Kociok N., Skosyrski S., Emilio A., Ruan Q., Han S., Liu L., Chen Z., Bowes Rickman C., Golde T., Grant M.B., Saftig P., Serneels L., de Strooper B., Joussen A.M., Boulton M.E. beta-Secretase (BACE1) inhibition causes retinal pathology by vascular dysregulation and accumulation of age pigment. EMBO Mol. Med. 2012, 4:980-991.
12. Cao Y., Espinola J.A., Fossale E., Massey A.C., Cuervo A.M., MacDonald M.E., Cotman S.L. Autophagy is disrupted in a knock-in mouse model of juvenile neuronal ceroid lipofuscinosis. J. Biol. Chem. 2006, 281:20483-20493.
13. Di Marzo V., Bifulco M., De Petrocellis L. The endocannabinoid system and its therapeutic exploitation. Nat. Rev. Drug Discov. 2004, 3:771-784.
14. Donadelli M., Dando I., Zaniboni T., Costanzo C., Dalla Pozza E., Scupoli M.T., Scarpa A., Zappavigna S., Marra M., Abbruzzese A., Bifulco M., Caraglia M., Palmieri M. Gemcitabine/cannabinoid combination triggers autophagy in pancreatic cancer cells through a ROS-mediated mechanism. Cell Death Dis. 2011, 2:e152.
15. Dubey A., Forster M.J., Lal H., Sohal R.S. Effect of age and caloric intake on protein oxidation in different brain regions and on behavioral functions of the mouse. Arch. Biochem. Biophys. 1996, 333:189-197.
16. Dunlop R.A., Brunk U.T., Rodgers K.J. Oxidized proteins: mechanisms of removal and consequences of accumulation. IUBMB Life 2009, 61:522-527.
17. Ellert-Miklaszewska A., Ciechomska I., Kaminska B. Cannabinoid signaling in glioma cells. Adv. Exp. Med. Biol. 2013, 986:209-220.
18. Farwanah H., Kolter T., Sandhoff K. Mass spectrometric analysis of neutral sphingolipids: methods, applications, and limitations. Biochim. Biophys. Acta 2011.
19. Farwanah H., Wirtz J., Kolter T., Raith K., Neubert R.H., Sandhoff K. Normal phase liquid chromatography coupled to quadrupole time of flight atmospheric pressure chemical ionization mass spectrometry for separation, detection and mass spectrometric profiling of neutral sphingolipids and cholesterol. J. Chromatogr. B: Analyt. Technol. Biomed. Life Sci. 2009, 877:2976-2982.
20. Felbor U., Kessler B., Mothes W., Goebel H.H., Ploegh H.L., Bronson R.T., Olsen B.R. Neuronal loss and brain atrophy in mice lacking cathepsins B and L. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:7883-7888.
21. Fox J.H., Connor T., Chopra V., Dorsey K., Kama J.A., Bleckmann D., Betschart C., Hoyer D., Frentzel S., Difiglia M., Paganetti P., Hersch S.M. The mTOR kinase inhibitor Everolimus decreases S6 kinase phosphorylation but fails to reduce mutant huntingtin levels in brain and is not neuroprotective in the R6/2 mouse model of Huntington's disease. Mol. Neurodegen. 2010, 5:26.
22. Golden T.R., Hinerfeld D.A., Melov S. Oxidative stress and aging: beyond correlation. Aging Cell 2002, 1:117-123.
23. Gowran A., Campbell V.A. A role for p53 in the regulation of lysosomal permeability by delta 9-tetrahydrocannabinol in rat cortical neurones: implications for neurodegeneration. J. Neurochem. 2008, 105:1513-1524.
24. Harman D. Aging: a theory based on free radical and radiation chemistry. J. Gerontol. 1956, 11:298-300.
25. Heinrich M., Wickel M., Schneider-Brachert W., Sandberg C., Gahr J., Schwandner R., Weber T., Saftig P., Peters C., Brunner J., Kronke M., Schutze S. Cathepsin D targeted by acid sphingomyelinase-derived ceramide. EMBO J. 1999, 18:5252-5263.
26. Hekimi S., Guarente L. Genetics and the specificity of the aging process. Science 2003, 299:1351-1354.
27. Hohn A., Jung T., Grimm S., Grune T. Lipofuscin-bound iron is a major intracellular source of oxidants: role in senescent cells. Free Radic. Biol. Med. 2010, 48:1100-1108.
28. Hohn A., Sittig A., Jung T., Grimm S., Grune T. Lipofuscin is formed independently of macroautophagy and lysosomal activity in stress-induced prematurely senescent human fibroblasts. Free Radic. Biol. Med. 2012, 53:1760-1769.
29. Hutter E., Skovbro M., Lener B., Prats C., Rabol R., Dela F., Jansen-Durr P. Oxidative stress and mitochondrial impairment can be separated from lipofuscin accumulation in aged human skeletal muscle. Aging Cell 2007, 6:245-256.
30. Kadar T., Silbermann M., Brandeis R., Levy A. Age-related structural changes in the rat hippocampus: correlation with working memory deficiency. Brain Res. 1990, 512:113-120.
31. Kesner R.P. Behavioral functions of the CA3 subregion of the hippocampus. Learn. Mem. 2007, 14:771-781.
32. Kim S.H., Won S.J., Mao X.O., Jin K., Greenberg D.A. Involvement of protein kinase A in cannabinoid receptor-mediated protection from oxidative neuronal injury. J. Pharmacol. Exp. Ther. 2005, 313:88-94.
33. 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.
34. Kurz T. Can lipofuscin accumulation be prevented?. Rejuvenation Res. 2008, 11:441-443.
35. Levine R.L. Carbonyl modified proteins in cellular regulation, aging, and disease. Free Radic. Biol. Med. 2002, 32:790-796.
36. Levine R.L., Williams J.A., Stadtman E.R., Shacter E. Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol. 1994, 233:346-357.
37. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25:402-408.
38. Lutz B. Molecular biology of cannabinoid receptors. Prostaglandins Leukot. Essent. Fatty Acids 2002, 66:123-142.
39. Ma W., Coon S., Zhao L., Fariss R.N., Wong W.T. A2E accumulation influences retinal microglial activation and complement regulation. Neurobiol. Aging 2013, 34:943-960.
40. Masson O., Prebois C., Derocq D., Meulle A., Dray C., Daviaud D., Quilliot D., Valet P., Muller C., Liaudet-Coopman E. Cathepsin-D, a key protease in breast cancer, is up-regulated in obese mouse and human adipose tissue, and controls adipogenesis. PLoS ONE 2011, 6:e16452.
41. Mizushima N., Yoshimori T., Levine B. Methods in mammalian autophagy research. Cell 2010, 140:313-326.
42. Nakanishi H. Neuronal and microglial cathepsins in aging and age-related diseases. Ageing Res. Rev. 2003, 2:367-381.
43. Nakanishi H., Amano T., Sastradipura D.F., Yoshimine Y., Tsukuba T., Tanabe K., Hirotsu I., Ohono T., Yamamoto K. Increased expression of cathepsins E and D in neurons of the aged rat brain and their colocalization with lipofuscin and carboxy-terminal fragments of Alzheimer amyloid precursor protein. J. Neurochem. 1997, 68:739-749.
44. Nakanishi H., Zhang J., Koike M., Nishioku T., Okamoto Y., Kominami E., von Figura K., Peters C., Yamamoto K., Saftig P., Uchiyama Y. Involvement of nitric oxide released from microglia-macrophages in pathological changes of cathepsin D-deficient mice. J. Neurosci. 2001, 21:7526-7533.
45. Paxinos G., Franklin K. The Mouse Brain in Stereotaxic Coordinates 2001, Academic Press, London, UK.
46. Puighermanal E., Marsicano G., Busquets-Garcia A., Lutz B., Maldonado R., Ozaita A. Cannabinoid modulation of hippocampal long-term memory is mediated by mTOR signaling. Nat. Neurosci. 2009, 12:1152-1158.
47. Reznick A.Z., Packer L. Oxidative damage to proteins: spectrophotometric method for carbonyl assay. Methods Enzymol. 1994, 233:357-363.
48. Rozenfeld R., Devi L.A. Regulation of CB1 cannabinoid receptor trafficking by the adaptor protein AP-3. FASEB J. 2008, 22:2311-2322.
49. Salazar M., Carracedo A., Salanueva I.J., Hernandez-Tiedra S., Lorente M., Egia A., Vazquez P., Blazquez C., Torres S., Garcia S., Nowak J., Fimia G.M., Piacentini M., Cecconi F., Pandolfi P.P., Gonzalez-Feria L., Iovanna J.L., Guzman M., Boya P., Velasco G. Cannabinoid action induces autophagy-mediated cell death through stimulation of ER stress in human glioma cells. J. Clin. Invest. 2009, 119:1359-1372.
50. Sastre J., Pallardo F.V., Vina J. The role of mitochondrial oxidative stress in aging. Free Radic. Biol. Med. 2003, 35:1-8.
51. Shiozaki M., Yoshimura K., Shibata M., Koike M., Matsuura N., Uchiyama Y., Gotow T. Morphological and biochemical signs of age-related neurodegenerative changes in klotho mutant mice. Neuroscience 2008, 152:924-941.
52. Strazielle C., Jazi R., Verdier Y., Qian S., Lalonde R. Regional brain metabolism with cytochrome c oxidase histochemistry in a PS1/A246E mouse model of autosomal dominant Alzheimer's disease: correlations with behavior and oxidative stress. Neurochem. Int. 2009, 55:806-814.
53. Terman A., Brunk U.T. Lipofuscin. Int. J. Biochem. Cell Biol. 2004, 36:1400-1404.
54. Tsvetkov A.S., Miller J., Arrasate M., Wong J.S., Pleiss M.A., Finkbeiner S. A small-molecule scaffold induces autophagy in primary neurons and protects against toxicity in a Huntington disease model. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:16982-16987.
55. Vara D., Salazar M., Olea-Herrero N., Guzman M., Velasco G., Diaz-Laviada I. Anti-tumoral action of cannabinoids on hepatocellular carcinoma: role of AMPK-dependent activation of autophagy. Cell Death Differ. 2011, 18:1099-1111.
56. Velasco G., Galve-Roperh I., Sanchez C., Blazquez C., Haro A., Guzman M. Cannabinoids and ceramide: two lipids acting hand-by-hand. Life Sci. 2005, 77:1723-1731.
57. Walls K.C., Klocke B.J., Saftig P., Shibata M., Uchiyama Y., Roth K.A., Shacka J.J. Altered regulation of phosphatidylinositol 3-kinase signaling in cathepsin D-deficient brain. Autophagy 2007, 3:222-229.
58. Yamasaki R., Zhang J., Koshiishi I., Sastradipura Suniarti D.F., Wu Z., Peters C., Schwake M., Uchiyama Y., Kira J., Saftig P., Utsumi H., Nakanishi H. Involvement of lysosomal storage-induced p38 MAP kinase activation in the overproduction of nitric oxide by microglia in cathepsin D-deficient mice. Mol. Cell. Neurosci. 2007, 35:573-584.