Chronic high levels of the RCAN1-1 protein may promote neurodegeneration and Alzheimer disease

Free Radical Biology and Medicine

Volumn 62, Issue , 2013, Pages 47-51

  Ermak, Gennady ^a   Daviesn, Kelvin J A ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Alzheimer disease; Free radicals; Mitochondria; Neurodegeneration; Oxidative stress; RCAN1

Indexed keywords

CALCINEURIN; GLUCOCORTICOID; PHOSPHATASE; RCAN1 1 PROTEIN; RCAN1 1L PROTEIN; RCAN1 1S PROTEIN; RCAN1 4 PROTEIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; APOPTOSIS; BRAIN FUNCTION; CELL STRESS; CELLULAR STRESS RESPONSE; CHRONIC STRESS; CORTICOSTEROID BLOOD LEVEL; DENDRITIC SPINE; DENTATE GYRUS; DOWN SYNDROME; ENZYME INHIBITION; HIPPOCAMPUS; HUMAN; MENTAL STRESS; MITOCHONDRION; NERVE DEGENERATION; NERVE FIBER TRANSPORT; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW;

EID: 84884909788     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2013.01.016     Document Type: Review

References (52)

1. Davies, K. J.; Ermak, G.; Rothermel, B. A.; Pritchard, M.; Heitman, J.; Ahnn, J.; Henrique-Silva, F.; Crawford, D.; Canaider, S.; Strippoli, P.; Carinci, P.; Min, K. T.; Fox, D. S.; Cunningham, K. W.; Bassel-Duby, R.; Olson, E. N.; Zhang, Z.; Williams, R. S.; Gerber, H. P.; Perez-Riba, M.; Seo, H.; Cao, X.; Klee, C. B.; Redondo, J. M.; Maltais, L. J.; Bruford, E. A.; Povey, S.; Molkentin, J. D.; McKeon, F. D.; Duh, E. J.; Crabtree, G. R.; Cyert, M. S.; de la Luna, S.; Estivill, X. Renaming the DSCR1/Adapt78 gene family as RCAN: regulators of calci-neurin. FASEB J 21: 3023-3028; 2007. (Pubitemid 47565558)
2. Genesca, L.; Aubareda, A.; Fuentes, J. J.; Estivill, X.; De La Luna, S.; Perez-Riba, M. Phosphorylation of calcipressin 1 increases its ability to inhibit calcineurin and decreases calcipressin half-life. Biochem. J. 374: 567-575; 2003. (Pubitemid 37094118)
3. Ermak, G.; Harris, C. D.; Battocchio, D.; Davies, K. J. RCAN1 (DSCR1 or Adapt78) stimulates expression of GSK-3beta. FEBS J. 273: 2100-2109; 2006.
4. Crawford, D. R.; Leahy, K. P.; Abramova, N.; Lan, L.; Wang, Y.; Davies, K. J. Hamster adapt78 mRNA is a Down syndrome critical region homologue that is inducible by oxidative stress. Arch. Biochem. Biophys. 342: 6-12; 1997. (Pubitemid 27217096)
5. Wang, Y.; De Keulenaer, G. W.; Weinberg, E. O.; Muangman, S.; Gualberto, A.; Landschulz, K. T.; Turi, T. G.; Thompson, J. F.; Lee, R. T. Direct biomechanical induction of endogenous calcineurin inhibitor Down Syndrome Critical Region-1 in cardiac myocytes. Am. J. Physiol. Heart Circ. Physiol 283:H533-539; 2002. (Pubitemid 34790845)
6. Ermak, G.; Pritchard, M. A.; Dronjak, S.; Niu, B.; Davies, K. J. Do RCAN1 proteins link chronic stress with neurodegeneration? FASEB J 25: 3306-3311; 2011.
7. Leahy, K. P.; Crawford, D. R. adapt78 protects cells against stress damage and suppresses cell growth. Arch. Biochem. Biophys. 379: 221-228; 2000. (Pubitemid 30637457)
8. Ermak, G.; Harris, C. D.; Davies, K. J. The DSCR1 (Adapt78) isoform 1 protein calcipressin 1 inhibits calcineurin and protects against acute calcium-mediated stress damage, including transient oxidative stress. FASEB J 16: 814-824; 2002. (Pubitemid 34615130)
9. Ermak, G.; Morgan, T. E.; Davies, K. J. Chronic overexpression of the calcineurin inhibitory gene DSCR1 (Adapt78) is associated with Alzheimer's disease. J. Biol. Chem. 276: 38787-38794; 2001.
10. Cook, C. N.; Hejna, M. J.; Magnuson, D. J.; Lee, J. M. Expression of calcipres-sin1, an inhibitor of the phosphatase calcineurin, is altered with aging and Alzheimer's disease. J. Alzheimers Dis. 8: 63-73; 2005. (Pubitemid 41267325)
11. Harris, C. D.; Ermak, G.; Davies, K. J. Multiple roles of the DSCR1 (Adapt78 or RCAN1) gene and its protein product calcipressin 1 (or RCAN1) in disease. Cell Mol. Life Sci 62: 2477-2486; 2005. (Pubitemid 41801100)
12. Fuentes, J. J.; Genesca, L.; Kingsbury, T. J.; Cunningham, K. W.; Perez-Riba, M.; Estivill, X.; de la Luna, S. DSCR1, overexpressed in Down syndrome, is an inhibitor of calcineurin-mediated signaling pathways. Hum. Mol. Genet 9: 1681-1690; 2000. (Pubitemid 30427005)
13. Baek, K. H.; Zaslavsky, A.; Lynch, R. C.; Britt, C.; Okada, Y.; Siarey, R. J.; Lensch, M. W.; Park, I. H.; Yoon, S. S.; Minami, T.; Korenberg, J. R.; Folkman, J.; Daley, G. Q.; Aird, W. C.; Galdzicki, Z.; Ryeom, S. Down's syndrome suppression of tumour growth and the role of the calcineurin inhibitor DSCR1. Nature 459: 1126-1130; 2009.
14. Ermak, G.; Davies, K. J. DSCR1(Adapt78) - a Janus gene providing stress protection but causing Alzheimer's disease? IUBMB Life 55: 29-31; 2003. (Pubitemid 36427596)
15. Harris, C. D.; Ermak, G.; Davies, K. J. RCAN1-1L is overexpressed in neurons of Alzheimer's disease patients. FEBS J. 274: 1715-1724; 2007. (Pubitemid 46426906)
16. Lloret, A.; Badia, M. C.; Giraldo, E.; Ermak, G.; Alonso, M. D.; Pallardo, F. V.; Davies, K. J.; Vina, J. Amyloid-beta toxicity and tau hyperphosphorylation are linked via RCAN1 in Alzheimer's disease. J. Alzheimers Dis. 27: 701-709; 2011.
17. Porta, S.; Serra, S. A.; Huch, M.; Valverde, M. A.; Llorens, F.; Estivill, X.; Arbones, M. L.; Marti, E. RCAN1 (DSCR1) increases neuronal susceptibility to oxidative stress: a potential pathogenic process in neurodegeneration. Hum. Mol. Genet 16: 1039-1050; 2007. (Pubitemid 47062725)
18. Sun, X.; Wu, Y.; Chen, B.; Zhang, Z.; Zhou, W.; Tong, Y.; Yuan, J.; Xia, K.; Gronemeyer, H.; Flavell, R. A.; Song, W. Regulator of calcineurin 1 (RCAN1) facilitates neuronal apoptosis through caspase-3 activation. J. Biol. Chem. 286: 9049-9062; 2011.
19. Chang, K. T.; Shi, Y. J.; Min, K. T. The Drosophila homolog of Down's syndrome critical region 1 gene regulates learning: implications for mental retardation. Proc. Natl. Acad. Sci. USA 100: 15794-15799; 2003. (Pubitemid 38021069)
20. Chang, K. T.; Min, K. T. Upregulation of three Drosophila homologs of human chromosome 21 genes alters synaptic function: implications for Down syndrome. Proc. Natl. Acad. Sci. USA 106: 17117-17122; 2009.
21. Martin, K. R.; Corlett, A.; Dubach, D.; Mustafa, T.; Coleman, H. A.; Parkington, H. C.; Merson, T. D.; Bourne, J. A.; Porta, S.; Arbones, M. L.; Finkelstein, D. I.; Pritchard, M. A. Over-expression of RCAN1 causes Down syndrome-like hippocampal deficits that alter learning and memory. Hum. Mol. Genet 21: 3025-3041; 2012.
22. Ermak, G.; Sojitra, S.; Yin, F.; Cadenas, E.; Cuervo, A. M.; Davies, K. J. Chronic expression of RCAN1-1L protein induces mitochondrial autophagy and metabolic shift from oxidative phosphorylation to glycolysis in neuronal cells. J. Biol. Chem. 287: 14088-14098; 2012.
23. Michtalik, H. J.; Narayan, A. V.; Bhatt, N.; Lin, H. Y.; Mulligan, M. T.; Zhang, S. L.; Crawford, D. R. Multiple oxidative stress-response members of the Adapt78 family. Free Radic. Biol. Med. 37: 454-462; 2004. (Pubitemid 38901078)
24. Wilson, R. S.; Barnes, L. L.; Bennett, D. A.; Li, Y.; Bienias, J. L.; Mendes de Leon, C. F.; Evans, D. A. Proneness to psychological distress and risk of Alzheimer disease in a biracial community. Neurology 64: 380-382; 2005.
25. Magarinos, A. M.; McEwen, B. S. Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: comparison of stressors. Neuroscience 69: 83-88; 1995.
26. Pham, K.; Nacher, J.; Hof, P. R.; McEwen, B. S. Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in the adult rat dentate gyrus. Eur. J. Neurosci. 17: 879-886; 2003. (Pubitemid 36315258)
27. Liston, C.; Miller, M. M.; Goldwater, D. S.; Radley, J. J.; Rocher, A. B.; Hof, P. R.; Morrison, J. H.; McEwen, B. S. Stress-induced alterations in prefrontal cortical dendritic morphology predict selective impairments in perceptual atten-tional set-shifting. J. Neurosci. 26: 7870-7874; 2006. (Pubitemid 44315156)
28. Gould, E.; McEwen, B. S.; Tanapat, P.; Galea, L. A.; Fuchs, E. Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J. Neurosci. 17: 2492-2498; 1997. (Pubitemid 27137415)
29. Shen, M. U. L.; Oshida, T.; Miyauchi, J.; Yamada, M.; Miyashita, T. Identification of novel direct transcriptional targets of glucocorticoid receptor. Leukemia 18: 1850-1856; 2004. (Pubitemid 39534321)
30. Hirakawa, Y.; Nary, L. J.; Medh, R. D. Glucocorticoid evoked upregulation of RCAN1-1 in human leukemic CEM cells susceptible to apoptosis. J. Mol. Signaling 4: 6; 2009.
31. Cerqueira, J. J.; Catania, C.; Sotiropoulos, I.; Schubert, M.; Kalisch, R.; Almeida, O. F.; Auer, D. P.; Sousa, N. Corticosteroid status influences the volume of the rat cingulate cortex - a magnetic resonance imaging study. J. Psychiatr.. Res 39: 451-460; 2005. (Pubitemid 40909988)
32. Landfield, P. W.; Waymire, J. C.; Lynch, G. Hippocampal aging and adreno-corticoids: quantitative correlations. Science 202: 1098-1102; 1978.
33. Kulstad, J. J.; McMillan, P. J.; Leverenz, J. B.; Cook, D. G.; Green, P. S.; Peskind, E. R.; Wilkinson, C. W.; Farris, W.; Mehta, P. D.; Craft, S. Effects of chronic glucocorticoid administration on insulin-degrading enzyme and amyloid-beta peptide in the aged macaque. J. Neuropathol. Exp. Neurol. 64: 139-146; 2005. (Pubitemid 40349312)
34. Lupien, S. J.; de Leon, M.; de Santi, S.; Convit, A.; Tarshish, C.; Nair, N. P.; Thakur, M.; McEwen, B. S.; Hauger, R. L.; Meaney, M. J. Cortisol levels during human aging predict hippocampal atrophy and memory deficits. Nat. Neurosci. 1: 69-73; 1998. (Pubitemid 128652645)
35. Dai, J.; Buijs, R.; Swaab, D. Glucocorticoid hormone (cortisol) affects axonal transport in human cortex neurons but shows resistance in Alzheimer's disease. Br. J. Pharmacol 143: 606-610; 2004. (Pubitemid 39524278)
36. Giubilei, F.; Patacchioli, F. R.; Antonini, G.; Sepe Monti, M.; Tisei, P.; Bastianello, S.; Monnazzi, P.; Angelucci, L. Altered circadian cortisol secretion in Alzheimer's disease: clinical and neuroradiological aspects. J. Neurosci. Res. 66: 262-265; 2001. (Pubitemid 32912294)
37. Aisen, P. S.; Davis, K. L.; Berg, J. D.; Schafer, K.; Campbell, K.; Thomas, R. G.; Weiner, M. F.; Farlow, M. R.; Sano, M.; Grundman, M.; Thal, L. J. A randomized controlled trial of prednisone in Alzheimer's disease. Alzheimer's Disease Cooperative Study. Neurology 54: 588-593; 2000. (Pubitemid 30082922)
38. Green, K. N.; Billings, L. M.; Roozendaal, B.; McGaugh, J. L.; LaFerla, F. M. Glucocorticoids increase amyloid-beta and tau pathology in a mouse model of Alzheimer's disease. J. Neurosci. 26: 9047-9056; 2006. (Pubitemid 44319396)
39. Gorlach, J.; Fox, D. S.; Cutler, N. S.; Cox, G. M.; Perfect, J. R.; Heitman, J. Identification and characterization of a highly conserved calcineurin binding protein, CBP1/calcipressin, in Cryptococcus neoformans. EMBO J. 19: 3618-3629; 2000. (Pubitemid 30462120)
40. Kingsbury, T. J.; Cunningham, K. W. A conserved family of calcineurin regulators. Genes Dev. 14: 1595-1604; 2000. (Pubitemid 30460909)
41. Rothermel, B.; Vega, R. B.; Yang, J.; Wu, H.; Bassel-Duby, R.; Williams, R. S. A protein encoded within the Down syndrome critical region is enriched in striated muscles and inhibits calcineurin signaling. J. Biol. Chem. 275: 8719-8725; 2000. (Pubitemid 30180224)
42. Chang, K. T.; Min, K. T. Drosophila melanogaster homolog of Down syndrome critical region 1 is critical for mitochondrial function. Nat. Neurosci 8: 1577-1585; 2005. (Pubitemid 41573673)
43. Javadov, S.; Karmazyn, M. Mitochondrial permeability transition pore opening as an endpoint to initiate cell death and as a putative target for cardioprotection. Cell. Physiol. Biochem 20: 1-22; 2007. (Pubitemid 46956808)
44. Zorov, D. B.; Juhaszova, M.; Yaniv, Y.; Nuss, H. B.; Wang, S.; Sollott, S. J. Regulation and pharmacology of the mitochondrial permeability transition pore. Cardiovasc. Res. 83: 213-225; 2009.
45. Rodriguez-Enriquez, S.; He, L.; Lemasters, J. J. Role of mitochondrial permeability transition pores in mitochondrial autophagy. Int. J. Biochem. Cell Biol. 36: 2463-2472; 2004. (Pubitemid 39119759)
46. Rodriguez-Enriquez, S.; Kai, Y.; Maldonado, E.; Currin, R. T.; Lemasters, J. J. Roles of mitophagy and the mitochondrial permeability transition in remodeling of cultured rat hepatocytes. Autophagy 5: 1099-1106; 2009.
47. Balaban, R. S.; Nemoto, S.; Finkel, T. Mitochondria, oxidants, and aging. Cell 120: 483-495; 2005.
48. Broekemeier, K. M.; Pfeiffer, D. R. Inhibition of the mitochondrial permeability transition by cyclosporin A during long time frame experiments: relationship between pore opening and the activity of mitochondrial phos-pholipases. Biochemistry 34: 16440-16449; 1995. (Pubitemid 26006490)
49. Tatton, W. G.; Chalmers-Redman, R. M. Mitochondria in neurodegenerative apoptosis: an opportunity for therapy? Ann. Neurol. 44:S134-141; 1998. (Pubitemid 28423840)
50. Pritchard, M.; Reeves, R. H.; Dierssen, M.; Patterson, D.; Gardiner, K. J. Down syndrome and the genes of human chromosome 21: current knowledge and future potentials. Report on the Expert workshop on the biology of chromosome 21 genes: towards gene-phenotype correlations in Down syndrome. Washington D.C., September 28-October 1, 2007. Cytogenet. Genome Res 121: 67-77; 2008. (Pubitemid 351820633)
51. Dierssen, M.; Arque, G.; McDonald, J.; Andreu, N.; Martinez-Cue, C.; Florez, J.; Fillat, C. Behavioral characterization of a mouse model overexpressing DSCR1/RCAN1. PLoS One 6:e17010; 2011.
52. Keating, D. J.; Dubach, D.; Zanin, M. P.; Yu, Y.; Martin, K.; Zhao, Y. F.; Chen, C.; Porta, S.; Arbones, M. L.; Mittaz, L.; Pritchard, M. A. DSCR1/RCAN1 regulates vesicle exocytosis and fusion pore kinetics: implications for Down syndrome and Alzheimer's disease. Hum. Mol. Genet 17: 1020-1030; 2008.) (Pubitemid 351426036)