RCAN1 regulates mitochondrial function and increases susceptibility to oxidative stress in mammalian cells

Oxidative Medicine and Cellular Longevity

Volumn 2014, Issue , 2014, Pages

  Peiris, Heshan ^a   Dubach, Daphne ^b   Jessup, Claire F ^a,c   Unterweger, Petra ^a   Raghupathi, Ravinarayan ^a   Muyderman, Hakan ^a   Zanin, Mark P ^a   Mackenzie, Kimberly ^a   Pritchard, Melanie A ^b   Keating, Damien J ^a  

^a FLINDERS UNIVERSITY   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; MAMMALS; NEURODEGENERATIVE DISEASES; NEURONS; OXIDATIVE STRESS;

ALZHEIMER'S DISEASE; CELLULAR ENERGY; DOWN'S SYNDROME; MITOCHONDRIAL DYSFUNCTION; MITOCHONDRIAL FUNCTION; MITOCHONDRIAL MEMBRANE POTENTIAL; NEURODEGENERATIVE DISORDERS; REACTIVE OXYGEN SPECIES;

MITOCHONDRIA;

CALCINEURIN; REACTIVE OXYGEN METABOLITE; REGULATOR OF CALCINEURIN 1; UNCLASSIFIED DRUG; HYDROGEN PEROXIDE; MUSCLE PROTEIN; RCAN1 PROTEIN, HUMAN; SIGNAL PEPTIDE;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN MITOCHONDRION; CELL FUNCTION; CELL VIABILITY; CHROMAFFIN CELL; CONTROLLED STUDY; DOWN SYNDROME; FEMALE; GENE OVEREXPRESSION; GENETIC SUSCEPTIBILITY; HUMAN; MAMMAL CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; MTT ASSAY; NERVE CELL CULTURE; NONHUMAN; OXIDATIVE STRESS; PC12 CELL LINE; PROTEIN EXPRESSION; ANIMAL; BIOLOGICAL MODEL; CELL SURVIVAL; DRUG EFFECTS; METABOLISM; MITOCHONDRION; NERVE CELL; RAT; TOXICITY; ULTRASTRUCTURE;

ANIMALS; CELL SURVIVAL; FEMALE; HYDROGEN PEROXIDE; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MITOCHONDRIA; MODELS, BIOLOGICAL; MUSCLE PROTEINS; NEURONS; OXIDATIVE STRESS; PC12 CELLS; RATS; REACTIVE OXYGEN SPECIES;

EID: 84903592181     PISSN: 19420900     EISSN: 19420994     Source Type: Journal    
DOI: 10.1155/2014/520316     Document Type: Article

References (51)

1. Fuentes J.-J., Pritchard M. A., Planas A. M., Bosch A., Ferrer I., Estivill X., A new human gene from the down syndrome critical region encodes a proline-rich protein highly expressed in fetal brain and heart. Human Molecular Genetics 1995 4 10 1935 1944 2-s2.0-0028856422
2. Ermak G., Morgan T. E., Davies K. J. A., Chronic overexpression of the calcineurin inhibitory gene DSCR1 (Adapt78) is associated with Alzheimer's disease. The Journal of Biological Chemistry 2001 276 42 38787 38794 2-s2.0-0037127258
3. Peiris H., Raghupathi R., Jessup C. F., Zanin M. P., Mohanasundaram D., Mackenzie K. D., Chataway T., Clarke J. N., Brealey J., Coates P. T., Pritchard M. A., Keating D. J., Increased expression of the glucose-responsive gene, RCAN1, causes hypoinsulinemia, β -cell dysfunction, and diabetes. Endocrinology 2012 153 11 5212 5221 2-s2.0-84867795201 10.1210/en.2011-2149
4. Fuentes J. J., Genescà L., Kingsbury T. J., Cunningham K. W., Pérez-Riba M., Estivill X., de La Luna S., DSCR1, overexpressed in Down syndrome, is an inhibitor of calcineurin-mediated signaling pathways. Human Molecular Genetics 2000 9 11 1681 1690 2-s2.0-0034234543 (Pubitemid 30427005)
5. Yang J., Rothermel B., Vega R. B., Frey N., McKinsey T. A., Olson E. N., Bassel-Duby R., Williams R. S., Independent signals control expression of the calcineurin inhibitory proteins MCIP1 and MCIP2 in striated muscles. Circulation Research 2000 87 12 E61 E68 2-s2.0-0034624137 10. 1161/?01.RES. 87. 12.e61
6. Keating D. J., Dubach D., Zanin M. P., Yu Y., Martin K., Zhao Y.-F., Chen C., Porta S., Arbonés M. L., Mittaz L., Pritchard M. A., DSCR1/RCAN1 regulates vesicle exocytosis and fusion pore kinetics: implications for down syndrome and Alzheimer's disease. Human Molecular Genetics 2008 17 7 1020 1030 2-s2.0-41149154002 10.1093/hmg/ddm374 (Pubitemid 351426036)
7. Zanin M. P., MacKenzie K. D., Peiris H., Pritchard M. A., Keating D. J., RCAN1 regulates vesicle recycling and quantal release kinetics via effects on calcineurin activity. Journal of Neurochemistry 2013 124 3 290 299 2-s2.0-84872093738 10.1111/jnc.12086
8. Martin K. R., Corlett A., Dubach D., Mustafa T., Coleman H. A., Parkington H. C., Merson T. D., Bourne J. A., Porta S., Arbonés M. L., Finkelstein D. I., Pritchard M. A., Over-expression of RCAN1 causes Down syndrome-like hippocampal deficits that alter learning and memory. Human Molecular Genetics 2012 21 13 3025 3041 2-s2.0-84863545043 10.1093/hmg/dds134
9. Martin K. R., Layton D., Seach N., Corlett A., Barallobre M. J., Arbonés M. L., Boyd R. L., Scott B., Pritchard M. A., Upregulation of RCAN1 causes down syndrome-like immune dysfunction. Journal of Medical Genetics 2013 50 7 444 454 2-s2.0-84883202984 10.1136/jmedgenet-2013-101522
10. Wu Y., Song W., Regulation of RCAN1 translation and its role in oxidative stress-induced apoptosis. FASEB Journal 2013 27 1 208 221 2-s2.0-84871901624 10.1096/fj.12-213124
11. Porta S., Serra S. A., Huch M., Valverde M. A., Llorens F., Estivill X., Arbonés M. L., Martí E., RCAN1 (DSCR1) increases neuronal susceptibility to oxidative stress: a potential pathogenic process in neurodegeneration. Human Molecular Genetics 2007 16 9 1039 1050 2-s2.0-34447306022 10.1093/hmg/ddm049 (Pubitemid 47062725)
12. Cho K. O., Kim Y. S., Cho Y. J., Kim S. Y., Upregulation of DSCR1 (RCAN1 or Adapt78) in the peri-infarct cortex after experimental stroke. Experimental Neurology 2008 212 1 85 92 2-s2.0-84860382474 10.1016/j.expneurol.2008.03.017
13. Sun X., Wu Y., Herculano B., Song W., RCAN1 overexpression exacerbates calcium overloading-induced neuronal apoptosis. PLoS ONE 2014 9 4 e95471 10.1371/journal.pone.0095471
14. Lee H. J., Kim Y. S., Sato Y., Cho Y.-J., RCAN1-4 knockdown attenuates cell growth through the inhibition of Ras signaling. FEBS Letters 2009 583 15 2557 2564 2-s2.0-67849101501 10.1016/j.febslet.2009.07.023
15. Kim Y. S., Lee H. J., Jang C., Kim H.-S., Cho Y.-J., Knockdown of RCAN1.4 increases susceptibility to FAS-mediated and DNA-damage-induced apoptosis by upregulation of p53 expression. Korean Journal of Physiology and Pharmacology 2009 13 6 483 489 2-s2.0-75749126534 10.4196/kjpp.2009.13.6.483
16. Harris C. D., Ermak G., Davies K. J. A., RCAN1-1L is overexpressed in neurons of Alzheimer's disease patients. FEBS Journal 2007 274 7 1715 1724 2-s2.0-33947193463 10.1111/j.1742-4658.2007.05717.x (Pubitemid 46426906)
17. Ermak G., Pritchard M. A., Dronjak S., Niu B., Davies K. J. A., Do RCAN1 proteins link chronic stress with neurodegeneration? FASEB Journal 2011 25 10 3306 3311 2-s2.0-80053928996 10.1096/fj.11-185728
18. Lloret A., Badia M.-C., Giraldo E., Ermak G., Alonso M.-D., Pallardó F. V., Davies K. J. A., Viña J., Amyloid- β toxicity and tau hyperphosphorylation are linked via RCAN1 in Alzheimer's disease. Journal of Alzheimer's Disease 2011 27 4 701 709 2-s2.0-84455173610 10.3233/JAD-2011-110890
19. Wischik C. M., Harrington C. R., Storey J. M., Tau-aggregation inhibitor therapy for Alzheimer's disease. Biochemical Pharmacology 2014 88 4 529 539 10.1016/j.bcp.2013.12.008
20. Holmes C., Boche D., Wilkinson D., Yadegarfar G., Hopkins V., Bayer A., Jones R. W., Bullock R., Love S., Neal J. W., Zotova E., Nicoll J. A., Long-term effects of A β 42 immunisation in Alzheimer's disease: follow-up of a randomised, placebo-controlled phase I trial. The Lancet 2008 372 9634 216 223 2-s2.0-47149112621 10.1016/S0140-6736(08)61075-2 (Pubitemid 351978111)
21. Ittner L. M., Ke Y. D., Delerue F., Bi M., Gladbach A., van Eersel J., Wölfing H., Chieng B. C., Christie M. J., Napier I. A., Eckert A., Staufenbiel M., Hardeman E., Götz J., Dendritic function of tau mediates amyloid- β toxicity in Alzheimer's disease mouse models. Cell 2010 142 3 387 397 2-s2.0-77955322042 10.1016/j.cell.2010.06.036
22. Ladner C. J., Czech J., Maurice J., Lorens S. A., Lee J. M., Reduction of calcineurin enzymatic activity in Alzheimer's disease: correlation with neuropathologic changes. Journal of Neuropathology and Experimental Neurology 1996 55 8 924 931 2-s2.0-0029798880 (Pubitemid 26287009)
23. Pierrot N., Santos S. F., Feyt C., Morel M., Brion J.-P., Octave J.-N., Calcium-mediated transient phosphorylation of tau and amyloid precursor protein followed by intraneuronal amyloid- β accumulation. The Journal of Biological Chemistry 2006 281 52 39907 39914 2-s2.0-33846031988 10.1074/jbc.M606015200 (Pubitemid 46041794)
24. Cook C. N., Hejna M. J., Magnuson D. J., Lee J. M., Expression of calcipressin1, an inhibitor of the phosphatase calcineurin, is altered with aging and Alzheimer's disease. Journal of Alzheimer's Disease 2005 8 1 63 73 2-s2.0-24644499539 (Pubitemid 41267325)
25. Lai F., Kammann E., Rebeck G. W., Anderson A., Chen Y., Nixon R. A., APOE genotype and gender effects on Alzheimer disease in 100 adults with down syndrome. Neurology 1999 53 2 331 336 2-s2.0-0033595202 (Pubitemid 29344355)
26. Helguera P., Seiglie J., Rodriguez J., Hanna M., Helguera G., Busciglio J., Adaptive downregulation of mitochondrial function in Down syndrome. Cell Metabolism 2013 17 1 132 140 2-s2.0-84872127080 10.1016/j.cmet.2012.12.005
27. Hirai K., Aliev G., Nunomura A., Fujioka H., Russell R. L., Atwood C. S., Johnson A. B., Kress Y., Vinters H. V., Tabaton M., Shimohama S., Cash A. D., Siedlak S. L., Harris P. L. R., Jones P. K., Petersen R. B., Perry G., Smith M. A., Mitochondrial abnormalities in Alzheimer's disease. Journal of Neuroscience 2001 21 9 3017 3023 2-s2.0-0035341254 (Pubitemid 32323483)
28. Busciglio J., Pelsman A., Wong C., Pigino G., Yuan M., Mori H., Yankner B. A., Altered metabolism of the amyloid β precursor protein is associated with mitochondrial dysfunction in Down's syndrome. Neuron 2002 33 5 677 688 2-s2.0-0037186074 10.1016/S0896-6273(02)00604-9 (Pubitemid 34219240)
29. Busciglio J., Yankner B. A., Apoptosis and increased generation of reactive oxygen species in Down's syndrome neurons in vitro. Nature 1995 378 6559 776 779 2-s2.0-0029417023 10.1038/378776a0
30. Capone G., Kim P., Jovanovich S., Payne L., Freund L., Welch K., Miller E., Trush M., Evidence for increased mitochondrial superoxide production in Down syndrome. Life Sciences 2002 70 24 2885 2895 2-s2.0-0037012806 10.1016/S0024-3205(02)01538-2 (Pubitemid 34442520)
31. Paz-Miguel J. E., Flores R., Sánchez-Velasco P., Ocejo-Vinyals G., Escribano de Diego J., López de Rego J., Leyva-Cobián F., Reactive oxygen intermediates during programmed cell death induced in the thymus of the Ts(1716)65Dn mouse, a murine model for human Down's syndrome. Journal of Immunology 1999 163 10 5399 5410 2-s2.0-0033571336
32. Smith M. A., Harris P. L. R., Sayre L. M., Perry G., Iron accumulation in Alzheimer disease is a source of redox-generated free radicals. Proceedings of the National Academy of Sciences of the United States of America 1997 94 18 9866 9868 2-s2.0-0030885482 10.1073/pnas.94.18.9866 (Pubitemid 27408156)
33. Smith M. A., Harris P. L. R., Sayre L. M., Beckman J. S., Perry G., Widespread peroxynitrite-mediated damage in Alzheimer's disease. Journal of Neuroscience 1997 17 8 2653 2657 2-s2.0-0346386580 (Pubitemid 27154998)
34. Rhein V., Song X., Wiesner A., Ittner L. M., Baysang G., Meier F., Ozmen L., Bluethmann H., Dröse S., Brandt U., Savaskan E., Czech C., Götz J., Eckert A., Amyloid- β and tau synergistically impair the oxidative phosphorylation system in triple transgenic Alzheimer's disease mice. Proceedings of the National Academy of Sciences of the United States of America 2009 106 47 20057 20062 2-s2.0-73949142307 10.1073/pnas.0905529106
35. Mutisya E. M., Bowling A. C., Beal M. F., Cortical cytochrome oxidase activity is reduced in Alzheimer's disease. Journal of Neurochemistry 1994 63 6 2179 2184 2-s2.0-0028110234 10.1046/j.1471-4159.1994.63062179.x (Pubitemid 24369993)
36. Lin H. Y., Michtalik H. J., Zhang S., Andersen T. T., van Riper D. A., Davies K. K. J. A., Ermak G., Petti L. M., Nachod S., Narayan A. V., Bhatt N., Crawford D. R., Oxidative and calcium stress regulate DSCR1 (Adapt78/MCIP1) protein. Free Radical Biology and Medicine 2003 35 5 528 539 2-s2.0-10744226066 10.1016/S0891-5849(03)00358-7 (Pubitemid 37289162)
37. Chang K. T., Min K.-T., Drosophila melanogaster homolog of Down syndrome critical region 1 is critical for mitochondrial function. Nature Neuroscience 2005 8 11 1577 1585 2-s2.0-27644557511 10.1038/nn1564 (Pubitemid 41573673)
38. Coupland R. E., Tomlinson A., The development and maturation of adrenal medullary chromaffin cells of the rat in vivo: a descriptive and quantitative study. International Journal of Developmental Neuroscience 1989 7 5 419 438 2-s2.0-0024441927 (Pubitemid 19257788)
39. Reers M., Smith T. W., Chen L. B., J-aggregate formation of a carbocyanine as a quantitative fluorescent indicator of membrane potential. Biochemistry 1991 30 18 4480 4486 2-s2.0-0025830873 10.1021/bi00232a015
40. Reers M., Smiley S. T., Mottola-Hartshorn C., Chen A., Lin M., Chen L. B., Mitochondrial membrane potential monitored by JC-1 dye. Methods in Enzymology 1995 260 406 417 2-s2.0-0028881848 10.1016/0076-6879(95)60154-6
41. Salvioli S., Ardizzoni A., Franceschi C., Cossarizza A., JC-1, but not DiOC6(3) or rhodamine 123, is a reliable fluorescent probe to assess ΔΨ changes in intact cells: implications for studies on mitochondrial functionality during apoptosis. FEBS Letters 1997 411 1 77 82 2-s2.0-0030612749 10.1016/S0014-5793(97)00669-8 (Pubitemid 27298375)
42. Zanin M. P., Phillips L., Mackenzie K. D., Keating D. J., Aging differentially affects multiple aspects of vesicle fusion kinetics. PLoS ONE 2011 6 11 2-s2.0-81355132241 10.1371/journal.pone.0027820 e27820
43. Balaban R. S., Nemoto S., Finkel T., Mitochondria, oxidants, and aging. Cell 2005 120 4 483 495 2-s2.0-13944278132 10.1016/j.cell.2005.02.001 (Pubitemid 40269763)
44. St-Pierre J., Buckingham J. A., Roebuck S. J., Brand M. D., Topology of superoxide production from different sites in the mitochondrial electron transport chain. The Journal of Biological Chemistry 2002 277 47 44784 44790 2-s2.0-0037160091 10.1074/jbc.M207217200 (Pubitemid 36159072)
45. Ermak G., Sojitra S., Yin F., Cadenas E., Cuervo A. M., Davies K. J. A., Chronic expression of RCAN1-1L protein induces mitochondrial autophagy and metabolic shift from oxidative phosphorylation to glycolysis in neuronal cells. The Journal of Biological Chemistry 2012 287 17 14088 14098 2-s2.0-84859949718 10.1074/jbc.M111.305342
46. Slupe A. M., Merrill R. A., Flippo K. H., Lobas M. A., Houtman J. C. D., Strack S., A calcineurin docking motif (LXVP) in dynamin-related protein 1 contributes to mitochondrial fragmentation and ischemic neuronal injury. The Journal of Biological Chemistry 2013 288 17 12353 12365 2-s2.0-84876942158 10.1074/jbc.M113.459677
47. Asai A., Qiu J.-H., Narita Y., Chi S., Saito N., Shinoura N., Hamada H., Kuchino Y., Kirino T., High level calcineurin activity predisposes neuronal cells to apoptosis. The Journal of Biological Chemistry 1999 274 48 34450 34458 2-s2.0-0033607543 10.1074/jbc.274.48.34450 (Pubitemid 129511792)
48. Springer J. E., Azbill R. D., Nottingham S. A., Kennedy S. E., Calcineurin-mediated BAD dephosphorylation activates the caspase-3 apoptotic cascade in traumatic spinal cord injury. Journal of Neuroscience 2000 20 19 7246 7251 2-s2.0-0034307421
49. Kakita T., Hasegawa K., Iwai-Kanai E., Adachi S., Morimoto T., Wada H., Kawamura T., Yanazume T., Sasayama S., Calcineurin pathway is required for endothelin-1-mediated protection against oxidant stress-induced apoptosis in cardiac myocytes. Circulation Research 2001 88 12 1239 1246 2-s2.0-0035933370 10.1161/hh1201.091794 (Pubitemid 32587839)
50. Reynolds G. P., Cutts A. J., Free radical damage in Down's syndrome brain. Biochemical Society Transactions 1993 21, article 221S 2-s2.0-0027256135 10.1042/bst021221s
51. Shi Q., Gibson G. E., Oxidative stress and transcriptional regulation in Alzheimer disease. Alzheimer Disease and Associated Disorders 2007 21 4 276 291 2-s2.0-37349049243 10.1097/WAD.0b013e31815721c3 (Pubitemid 350307432)