The zebrafish as a gerontology model in nervous system aging, disease, and repair

Ageing Research Reviews

Volumn 24, Issue , 2015, Pages 358-368

  Van houcke, Jessie ^a   De Groef, Lies ^a   Dekeyster, Eline ^a   Moons, Lieve ^a  

^a SKELETAL BIOLOGY AND ENGINEERING RESEARCH CENTER   (Belgium)

Author keywords

Aging; Cellular senescence; Nervous system; Zebrafish

Indexed keywords

AGING; CELL AGING; CELL COMMUNICATION; CELL DAMAGE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CENTRAL NERVOUS SYSTEM; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA FRAGMENTATION; EPIGENETICS; GENOMIC INSTABILITY; GERONTOLOGY; LIPID METABOLISM; NERVOUS SYSTEM DEVELOPMENT; NEUROLOGIC DISEASE; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PROTEIN HOMEOSTASIS; REVIEW; SENESCENCE; STEM CELL NICHE; TELOMERE; ZEBRA FISH; ANIMAL; DISEASE MODEL; HUMAN; METABOLISM; NERVOUS SYSTEM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

AGING; ANIMALS; DISEASE MODELS, ANIMAL; HUMANS; NERVOUS SYSTEM; NERVOUS SYSTEM DISEASES; ZEBRAFISH;

EID: 84957969416     PISSN: 15681637     EISSN: 18729649     Source Type: Journal    
DOI: 10.1016/j.arr.2015.10.004     Document Type: Review

References (143)

1. Adolf B., Chapouton P., Lam C.S., Topp S., Tannhauser B., Strahle U., Gotz M., Bally-Cuif L. Conserved and acquired features of adult neurogenesis in the zebrafish telencephalon. Dev. Biol. 2006, 295:278-293.
2. Alisch R.S., Barwick B.G., Chopra P., Myrick L.K., Satten G.A., Conneely K.N., Warren S.T. Age-associated DNA methylation in pediatric populations. Genome Res. 2012, 22:623-632.
3. Almaida-Pagan P.F., de Costa J., Mendiola P., Tocher D.R. Age-related changes in mitochondrial membrane composition of rainbow trout (Oncorhynchus mykiss) heart and brain. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2012, 163:129-137.
4. Almaida-Pagan P.F., de Costa J., Mendiola P., Tocher D.R. Changes in tissue and mitochondrial membrane composition during rapid growth, maturation and aging in rainbow trout, Oncorhynchus mykiss. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2012, 161:404-412.
5. Almaida-Pagan P.F., Lucas-Sanchez A., Tocher D.R. Changes in mitochondrial membrane composition and oxidative status during rapid growth, maturation and aging in zebrafish, Danio rerio. Biochim. Biophys. Acta 2014, 1841:1003-1011.
6. Anchelin M., Murcia L., Alcaraz-Perez F., Garcia-Navarro E.M., Cayuela M.L. Behaviour of telomere and telomerase during aging and regeneration in zebrafish. PloS One 2011, 6:e16955.
7. Anchelin M., Alcaraz-Perez F., Martinez C.M., Bernabe-Garcia M., Mulero V., Cayuela M.L. Premature aging in telomerase-deficient zebrafish. Dis. Model Mech. 2013, 6:1101-1112.
8. Arslan-Ergul A., Adams M.M. Gene expression changes in aging zebrafish (Danio rerio) brains are sexually dimorphic. BMC Neurosci. 2014, 15:29.
9. Barbazuk W.B., Korf I., Kadavi C., Heyen J., Tate S., Wun E., Bedell J.A., McPherson J.D., Johnson S.L. The syntenic relationship of the zebrafish and human genomes. Genome Res. 2000, 10:1351-1358.
10. Barzilai N., Huffman D.M., Muzumdar R.H., Bartke A. The critical role of metabolic pathways in aging. Diabetes 2012, 61:1315-1322.
11. Blackburn E.H., Greider C.W., Szostak J.W. Telomeres and telomerase: the path from maize, Tetrahymena and yeast to human cancer and aging. Nat. Med. 2006, 12:1133-1138.
12. Blasco M.A., Lee H.W., Hande M.P., Samper E., Lansdorp P.M., DePinho R.A., Greider C.W. Telomere shortening and tumor formation by mouse cells lacking telomerase RNA. Cell 1997, 91:25-34.
13. Brighina L., Prigione A., Begni B., Galbussera A., Andreoni S., Piolti R., Ferrarese C. Lymphomonocyte alpha-synuclein levels in aging and in Parkinson disease. Neurobiol. Aging 2010, 31:884-885.
14. Cailliet G.M., Andrews A.H., Burton E.J., Watters D.L., Kline D.E., Ferry-Graham L.A. Age determination and validation studies of marine fishes: do deep-dwellers live longer?. Exp. Gerontol. 2001, 36:739-764.
15. Cawthon R.M., Smith K.R., O'Brien E., Sivatchenko A., Kerber R.A. Association between telomere length in blood and mortality in people aged 60 years or older. Lancet 2003, 361:393-395.
16. Chan S.W., Blackburn E.H. New ways not to make ends meet: telomerase, DNA damage proteins and heterochromatin. Oncogene 2002, 21:553-563.
17. Chapouton P., Adolf B., Leucht C., Tannhauser B., Ryu S., Driever W., Bally-Cuif L. her5 expression reveals a pool of neural stem cells in the adult zebrafish midbrain. Development 2006, 133:4293-4303.
18. Chicco A.J., Sparagna G.C. Role of cardiolipin alterations in mitochondrial dysfunction and disease. Am. J. Physiol. Cell Physiol. 2007, 292:C33-C44.
19. Collado M., Blasco M.A., Serrano M. Cellular senescence in cancer and aging. Cell 2007, 130:223-233.
20. Collins K., Mitchell J.R. Telomerase in the human organism. Oncogene 2002, 21:564-579.
21. Conboy I.M., Rando T.A. Heterochronic parabiosis for the study of the effects of aging on stem cells and their niches. Cell Cycle 2012, 11:2260-2267.
22. Craig P.M., Moon T.W. Fasted zebrafish mimic genetic and physiological responses in mammals: a model for obesity and diabetes?. Zebrafish 2011, 8:109-117.
23. Deaton A.M., Bird A. CpG islands and the regulation of transcription. Genes Dev. 2011, 25:1010-1022.
24. Deeks S.G. HIV infection, inflammation, immunosenescence, and aging. Annu. Rev. Med. 2011, 62:141-155.
25. Ding L., Kuhne W.W., Hinton D.E., Song J., Dynan W.S. Quantifiable biomarkers of normal aging in the Japanese medaka fish (Oryzias latipes). PloS One 2010, 5:e13287.
26. Edelmann K., Glashauser L., Sprungala S., Hesl B., Fritschle M., Ninkovic J., Godinho L., Chapouton P. Increased radial glia quiescence, decreased reactivation upon injury and unaltered neuroblast behavior underlie decreased neurogenesis in the aging zebrafish telencephalon. J. Comp. Neurol. 2013, 521:3099-3115.
27. Fontana L., Partridge L., Longo V.D. Extending healthy life span-from yeast to humans. Science 2010, 328:321-326.
28. Garinis G.A., van der Horst G.T., Vijg J., Hoeijmakers J.H. DNA damage and ageing: new-age ideas for an age-old problem. Nat. Cell Biol. 2008, 10:1241-1247.
29. Gerhard G.S., Cheng K.C. A call to fins! Zebrafish as a gerontological model. Aging cell 2002, 1:104-111.
30. Gerhard G.S., Kauffman E.J., Wang X., Stewart R., Moore J.L., Kasales C.J., Demidenko E., Cheng K.C. Life spans and senescent phenotypes in two strains of zebrafish (Danio rerio). Exp. Gerontol. 2002, 37:1055-1068.
31. Gerhard G.S. Comparative aspects of zebrafish (Danio rerio) as a model for aging research. Exp. Gerontol. 2003, 38:1333-1341.
32. Gilbert M.J., Zerulla T.C., Tierney K.B. Zebrafish (Danio rerio) as a model for the study of aging and exercise: physical ability and trainability decrease with age. Exp. Gerontol. 2014, 50:106-113.
33. Gopalakrishnan S., Cheung N.K., Yip B.W., Au D.W. Medaka fish exhibits longevity gender gap, a natural drop in estrogen and telomere shortening during aging: a unique model for studying sex-dependent longevity. Front. Zool. 2013, 10:78.
34. Graciarena M., Dambly-Chaudiere C., Ghysen A. Dynamics of axonal regeneration in adult and aging zebrafish reveal the promoting effect of a first lesion. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:1610-1615.
35. Grandel H., Kaslin J., Ganz J., Wenzel I., Brand M. Neural stem cells and neurogenesis in the adult zebrafish brain: origin, proliferation dynamics, migration and cell fate. Dev. Biol. 2006, 295:263-277.
36. Green D.R., Galluzzi L., Kroemer G. Mitochondria and the autophagy-inflammation-cell death axis in organismal aging. Science 2011, 333:1109-1112.
37. Gruber R., Koch H., Doll B.A., Tegtmeier F., Einhorn T.A., Hollinger J.O. Fracture healing in the elderly patient. Exp. Gerontol. 2006, 41:1080-1093.
38. Haigis M.C., Yankner B.A. The aging stress response. Mol. Cell 2010, 40:333-344.
39. Harman D. The Free Radical Theory of Aging: effect of Age on Serum Copper Levels. J. Gerontol. 1965, 20:151-153.
40. Hartl F.U., Bracher A., Hayer-Hartl M. Molecular chaperones in protein folding and proteostasis. Nature 2011, 475:324-332.
41. Hatakeyama H., Nakamura K., Izumiyama-Shimomura N., Ishii A., Tsuchida S., Takubo K., Ishikawa N. The teleost Oryzias latipes shows telomere shortening with age despite considerable telomerase activity throughout life. Mech. Ageing Dev. 2008, 129:550-557.
42. Hayes A.J., Reynolds S., Nowell M.A., Meakin L.B., Habicher J., Ledin J., Bashford A., Caterson B., Hammond C.L. Spinal deformity in aged zebrafish is accompanied by degenerative changes to their vertebrae that resemble osteoarthritis. PloS One 2013, 8:e75787.
43. Hekimi S., Lapointe J., Wen Y. Taking a good look at free radicals in the aging process. Trends Cell Biol. 2011, 21:569-576.
44. Henriques C.M., Carneiro M.C., Tenente I.M., Jacinto A., Ferreira M.G. Telomerase is required for zebrafish lifespan. PLoS Genet. 2013, 9:e1003214.
45. Herbig U., Ferreira M., Condel L., Carey D., Sedivy J.M. Cellular senescence in aging primates. Science 2006, 311:1257.
46. Heyn H., Li N., Ferreira H.J., Moran S., Pisano D.G., Gomez A., Diez J., Sanchez-Mut J.V., Setien F., Carmona F.J., Puca A.A., Sayols S., Pujana M.A., Serra-Musach J., Iglesias-Platas I., Formiga F., Fernandez A.F., Fraga M.F., Heath S.C., Valencia A., Gut I.G., Wang J., Esteller M. Distinct DNA methylomes of newborns and centenarians. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:10522-10527.
47. Hiona A., Sanz A., Kujoth G.C., Pamplona R., Seo A.Y., Hofer T., Someya S., Miyakawa T., Nakayama C., Samhan-Arias A.K., Servais S., Barger J.L., Portero-Otin M., Tanokura M., Prolla T.A., Leeuwenburgh C. Mitochondrial DNA mutations induce mitochondrial dysfunction, apoptosis and sarcopenia in skeletal muscle of mitochondrial DNA mutator mice. PloS One 2010, 5:e11468.
48. Hoeijmakers J.H. DNA damage, aging, and cancer. N. Engl. J. Med. 2009, 361:1475-1485.
49. Holmes D.J., Fluckiger R., Austad S.N. Comparative biology of aging in birds: an update. Exp. Gerontol. 2001, 36:869-883.
50. Horvath S. DNA methylation age of human tissues and cell types. Genome Biol. 2013, 14:R115.
51. Howe K., Clark M.D., Torroja C.F., Torrance J., Berthelot C., Muffato M., Collins J.E., Humphray S., McLaren K., Matthews L., McLaren S., Sealy I., Caccamo M., Churcher C., Scott C., Barrett J.C., Koch R., Rauch G.J., White S., Chow W., Kilian B., Quintais L.T., Guerra-Assuncao J.A., Zhou Y., Gu Y., Yen J., Vogel J.H., Eyre T., Redmond S., Banerjee R., Chi J., Fu B., Langley E., Maguire S.F., Laird G.K., Lloyd D., Kenyon E., Donaldson S., Sehra H., Almeida-King J., Loveland J., Trevanion S., Jones M., Quail M., Willey D., Hunt A., Burton J., Sims S., McLay K., Plumb B., Davis J., Clee C., Oliver K., Clark R., Riddle C., Elliot D., Threadgold G., Harden G., Ware D., Begum S., Mortimore B., Kerry G., Heath P., Phillimore B., Tracey A., Corby N., Dunn M., Johnson C., Wood J., Clark S., Pelan S., Griffiths G., Smith M., Glithero R., Howden P., Barker N., Lloyd C., Stevens C., Harley J., Holt K., Panagiotidis G., Lovell J., Beasley H., Henderson C., Gordon D., Auger K., Wright D., Collins J., Raisen C., Dyer L., Leung K., Robertson L., Ambridge K., Leongamornlert D., McGuire S., Gilderthorp R., Griffiths C., Manthravadi D., Nichol S., Barker G., et al. The zebrafish reference genome sequence and its relationship to the human genome. Nature 2013, 496:498-503.
52. Irizarry R.A., Ladd-Acosta C., Wen B., Wu Z., Montano C., Onyango P., Cui H., Gabo K., Rongione M., Webster M., Ji H., Potash J.B., Sabunciyan S., Feinberg A.P. The human colon cancer methylome shows similar hypo- and hypermethylation at conserved tissue-specific CpG island shores. Nat. Genet. 2009, 41:178-186.
53. Ito Y., Tanaka H., Okamoto H., Ohshima T. Characterization of neural stem cells and their progeny in the adult zebrafish optic tectum. Dev. Biol. 2010, 342:26-38.
54. Itou J., Kawakami H., Burgoyne T., Kawakami Y. Life-long preservation of the regenerative capacity in the fin and heart in zebrafish. Biol. Open 2012, 1:739-746.
55. Jones P.A., Baylin S.B. The epigenomics of cancer. Cell 2007, 128:683-692.
56. Jung M., Pfeifer G.P. Aging and DNA methylation. BMC Biol. 2015, 13:7.
57. Jung T., Bader N., Grune T. Lipofuscin: formation, distribution, and metabolic consequences. Ann. N. Y. Acad. Sci. 2007, 1119:97-111.
58. Jury D.R., Kaveti S., Duan Z.H., Willard B., Kinter M., Londraville R. Effects of calorie restriction on the zebrafish liver proteome. Comp. Biochem. Physiol. D Genomics Proteom. 2008, 3:275-282.
59. Kao T.T., Chu C.Y., Lee G.H., Hsiao T.H., Cheng N.W., Chang N.S., Chen B.H., Fu T.F. Folate deficiency-induced oxidative stress contributes to neuropathy in young and aged zebrafish-implication in neural tube defects and Alzheimer's diseases. Neurobiol. Dis. 2014, 71:234-244.
60. Kaslin J., Ganz J., Geffarth M., Grandel H., Hans S., Brand M. Stem cells in the adult zebrafish cerebellum: initiation and maintenance of a novel stem cell niche. J. Neurosci. 2009, 29:6142-6153.
61. Kayo T., Allison D.B., Weindruch R., Prolla T.A. Influences of aging and caloric restriction on the transcriptional profile of skeletal muscle from rhesus monkeys. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:5093-5098.
62. Keller E.T., Murtha J.M. The use of mature zebrafish (Danio rerio) as a model for human aging and disease. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2004, 138:335-341.
63. Kelly K.A., Havrilla C.M., Brady T.C., Abramo K.H., Levin E.D. Oxidative stress in toxicology: established mammalian and emerging piscine model systems. Environ. Health Perspect. 1998, 106:375-384.
64. Key B., Devine C.A. Zebrafish as an experimental model: strategies for developmental and molecular neurobiology studies. Methods Cell Sci. 2003, 25:1-6.
65. Kimmel C.B., Ballard W.W., Kimmel S.R., Ullmann B., Schilling T.F. Stages of embryonic development of the zebrafish. Dev. Dyn. 1995, 203:253-310.
66. Kippin T.E., Martens D.J., van der Kooy D. p21 loss compromises the relative quiescence of forebrain stem cell proliferation leading to exhaustion of their proliferation capacity. Genes Dev. 2005, 19:756-767.
67. Kishi S., Lu K.P. A critical role for Pin2/TRF1 in ATM-dependent regulation. Inhibition of Pin2/TRF1 function complements telomere shortening, radiosensitivity, and the G(2)/M checkpoint defect of ataxia-telangiectasia cells. J. Biol. Chem. 2002, 277:7420-7429.
68. Kishi S., Uchiyama J., Baughman A.M., Goto T., Lin M.C., Tsai S.B. The zebrafish as a vertebrate model of functional aging and very gradual senescence. Exp. Gerontol. 2003, 38:777-786.
69. Kishi S., Bayliss P.E., Uchiyama J., Koshimizu E., Qi J., Nanjappa P., Imamura S., Islam A., Neuberg D., Amsterdam A., Roberts T.M. The identification of zebrafish mutants showing alterations in senescence-associated biomarkers. PLoS Genet. 2008, 4:e1000152.
70. Kishi S., Slack B.E., Uchiyama J., Zhdanova I.V. Zebrafish as a genetic model in biological and behavioral gerontology: where development meets aging in vertebrates-a mini-review. Gerontology 2009, 55:430-441.
71. Kishi S. Functional aging and gradual senescence in zebrafish. Ann. N.Y. Acad. Sci. 2004, 1019:521-526.
72. Kishi S. The search for evolutionary developmental origins of aging in zebrafish: a novel intersection of developmental and senescence biology in the zebrafish model system. Birth Defects Res. C Embryo Today 2011, 93:229-248.
73. Koga H., Kaushik S., Cuervo A.M. Protein homeostasis and aging: The importance of exquisite quality control. Ageing Res. Rev. 2011, 10:205-215.
74. Kovacs G.G., Adle-Biassette H., Milenkovic I., Cipriani S., van Scheppingen J., Aronica E. Linking pathways in the developing and aging brain with neurodegeneration. Neuroscience 2014, 269:152-172.
75. Kuilman T., Michaloglou C., Mooi W.J., Peeper D.S. The essence of senescence. Genes Dev. 2010, 24:2463-2479.
76. Kulis M., Queiros A.C., Beekman R., Martin-Subero J.I. Intragenic DNA methylation in transcriptional regulation, normal differentiation and cancer. Biochim. Biophys. Acta 2013, 1829:1161-1174.
77. Kurtz A., Oh S.J. Age related changes of the extracellular matrix and stem cell maintenance. Prev. Med. 2012, 54:S50-S56. Suppl.
78. López-Otín C., Blasco M.A., Partridge L., Serrano M., Kroemer G. The hallmarks of aging. Cell 2013, 153:1194-1217.
79. Lee B.Y., Han J.A., Im J.S., Morrone A., Johung K., Goodwin E.C., Kleijer W.J., DiMaio D., Hwang E.S. Senescence-associated beta-galactosidase is lysosomal beta-galactosidase. Aging cell 2006, 5:187-195.
80. Lightle S.A., Oakley J.I., Nikolova-Karakashian M.N. Activation of sphingolipid turnover and chronic generation of ceramide and sphingosine in liver during aging. Mech. Ageing Dev. 2000, 120:111-125.
81. Liu A.Y., Lee Y.K., Manalo D., Huang L.E. Attenuated heat shock transcriptional response in aging: molecular mechanism and implication in the biology of aging. EXS 1996, 77:393-408.
82. Liu Y., Snow B.E., Hande M.P., Baerlocher G., Kickhoefer V.A., Yeung D., Wakeham A., Itie A., Siderovski D.P., Lansdorp P.M., Robinson M.O., Harrington L. Telomerase-associated protein TEP1 is not essential for telomerase activity or telomere length maintenance in vivo. Mol. Cell. Biol. 2000, 20:8178-8184.
83. Lord C.J., Ashworth A. The DNA damage response and cancer therapy. Nature 2012, 481:287-294.
84. Lund T.C., Glass T.J., Tolar J., Blazar B.R. Expression of telomerase and telomere length are unaffected by either age or limb regeneration in Danio rerio. PloS One 2009, 4. 0007688.
85. Macleod D., Clark V.H., Bird A. Absence of genome-wide changes in DNA methylation during development of the zebrafish. Nat. Genet. 1999, 23:139-140.
86. Makhija D.T., Jagtap A.G. Studies on sensitivity of zebrafish as a model organism for Parkinson's disease: comparison with rat model. J. Pharmacol. Pharmacother. 2014, 5:39-46.
87. Manuel R., Gorissen M., Roca C.P., Zethof J., van de Vis H., Flik G., van den Bos R. Inhibitory avoidance learning in zebrafish (Danio rerio): effects of shock intensity and unraveling differences in task performance. Zebrafish 2014, 11:341-352.
88. Manuel R., Gorissen M., Stokkermans M., Zethof J., Ebbesson L.O., Vis H.V., Flik G., Bos R.V. The effects of environmental enrichment and age-related differences on inhibitory avoidance in zebrafish (Danio rerio Hamilton). Zebrafish 2015.
89. Mattison J.A., Roth G.S., Beasley T.M., Tilmont E.M., Handy A.M., Herbert R.L., Longo D.L., Allison D.B., Young J.E., Bryant M., Barnard D., Ward W.F., Qi W., Ingram D.K., de Cabo R. Impact of caloric restriction on health and survival in rhesus monkeys from the NIA study. Nature 2012, 489:318-321.
90. Mattson M.P., Magnus T. Ageing and neuronal vulnerability. Nat. Rev. Neurosci. 2006, 7:278-294.
91. Mizushima N., Levine B., Cuervo A.M., Klionsky D.J. Autophagy fights disease through cellular self-digestion. Nature 2008, 451:1069-1075.
92. Molofsky A.V., Slutsky S.G., Joseph N.M., He S., Pardal R., Krishnamurthy J., Sharpless N.E., Morrison S.J. Increasing p16INK4a expression decreases forebrain progenitors and neurogenesis during ageing. Nature 2006, 443:448-452.
93. Munzel E.J., Becker C.G., Becker T., Williams A. Zebrafish regenerate full thickness optic nerve myelin after demyelination, but this fails with increasing age. Acta Neuropathol. Commun. 2014, 2:77.
94. Murtha J.M., Keller E.T. Characterization of the heat shock response in mature zebrafish (Danio rerio). Exp. Gerontol. 2003, 38:683-691.
95. Novak C.M., Jiang X., Wang C., Teske J.A., Kotz C.M., Levine J.A. Caloric restriction and physical activity in zebrafish (Danio rerio). Neurosci. Lett. 2005, 383:99-104.
96. Oliveira R.F. Mind the fish: zebrafish as a model in cognitive social neuroscience. Front. Neural Circuits 2013, 7(131).
97. Patnaik B.K., Mahapatro N., Jena B.S. Ageing in fishes. Gerontology 1994, 40:113-132.
98. Philpott C., Donack C.J., Cousin M.A., Pierret C. Reducing the noise in behavioral assays: sex and age in adult zebrafish locomotion. Zebrafish 2012, 9:191-194.
99. Pospisilik J.A., Schramek D., Schnidar H., Cronin S.J., Nehme N.T., Zhang X., Knauf C., Cani P.D., Aumayr K., Todoric J., Bayer M., Haschemi A., Puviindran V., Tar K., Orthofer M., Neely G.G., Dietzl G., Manoukian A., Funovics M., Prager G., Wagner O., Ferrandon D., Aberger F., Hui C.C., Esterbauer H., Penninger J.M. Drosophila genome-wide obesity screen reveals hedgehog as a determinant of brown versus white adipose cell fate. Cell 2010, 140:148-160.
100. Powers E.T., Morimoto R.I., Dillin A., Kelly J.W., Balch W.E. Biological and chemical approaches to diseases of proteostasis deficiency. Ann. Rev. Biochem. 2009, 78:959-991.
101. Raffaello A., Rizzuto R. Mitochondrial longevity pathways. Biochim. Biophys. Acta 2011, 1813:260-268.
102. Rando T.A. Stem cells, ageing and the quest for immortality. Nature 2006, 441:1080-1086.
103. Reiter R.J., Tan D.X., Poeggeler B., Menendez-Pelaez A., Chen L.D., Saarela S. Melatonin as a free radical scavenger: implications for aging and age-related diseases. Ann. N. Y. Acad. Sci. 1994, 719:1-12.
104. Rera M., Bahadorani S., Cho J., Koehler C.L., Ulgherait M., Hur J.H., Ansari W.S., Lo T.J., Jones D.L., Walker D.W. Modulation of longevity and tissue homeostasis by the Drosophila PGC-1 homolog. Cell Metab. 2011, 14:623-634.
105. Rodier F., Campisi J. Four faces of cellular senescence. J. Cell Biol. 2011, 192:547-556.
106. Rosa C.E., Kuradomi R.Y., Almeida D.V., Lannes C.F., Figueiredo Mde A., Dytz A.G., Fonseca D.B., Marins L.F. GH overexpression modifies muscle expression of anti-oxidant enzymes and increases spinal curvature of old zebrafish. Exp. Gerontol. 2010, 45:449-456.
107. Ruckh J.M., Zhao J.W., Shadrach J.L., van Wijngaarden P., Rao T.N., Wagers A.J., Franklin R.J. Rejuvenation of regeneration in the aging central nervous system. Cell Stem Cell 2012, 10:96-103.
108. Ruhl T., Jonas A., Seidel N.I., Prinz N., Albayram O., Bilkei-Gorzo A., von der Emde G. Oxidation and cognitive impairment in the aging Zebrafish. Gerontology 2015, [ePub ahead of print].
109. Rupp B., Wullimann M.F., Reichert H. The zebrafish brain: a neuroanatomical comparison with the goldfish. Anat. Embryol. (Berl.) 1996, 194:187-203.
110. Salminen A., Ojala J., Kaarniranta K., Haapasalo A., Hiltunen M., Soininen H. Astrocytes in the aging brain express characteristics of senescence-associated secretory phenotype. Eur. J. Neurosci. 2011, 34:3-11.
111. Salminen A., Kaarniranta K., Kauppinen A. Inflammaging: disturbed interplay between autophagy and inflammasomes. Aging (Milano) 2012, 4:166-175.
112. Sanai N., Nguyen T., Ihrie R.A., Mirzadeh Z., Tsai H.H., Wong M., Gupta N., Berger M.S., Huang E., Garcia-Verdugo J.M., Rowitch D.H., Alvarez-Buylla A. Corridors of migrating neurons in the human brain and their decline during infancy. Nature 2011, 478:382-386.
113. Santana S., Rico E.P., Burgos J.S. Can zebrafish be used as animal model to study Alzheimer's disease?. Am. J. Neurodegener. Dis. 2012, 1:32-48.
114. Sasaki T., Kishi S. Molecular and chemical genetic approaches to developmental origins of aging and disease in zebrafish. Biochim. Biophys. Acta 2013, 1832:1362-1370.
115. Saverino C., Gerlai R. The social zebrafish: behavioral responses to conspecific, heterospecific, and computer animated fish. Behav. Brain Res. 2008, 191:77-87.
116. Schliebs R., Arendt T. The cholinergic system in aging and neuronal degeneration. Behav. Brain Res. 2011, 221:555-563.
117. Schmucker D.L. Age-related changes in liver structure and function: Implications for disease ?. Exp. Gerontol. 2005, 40:650-659.
118. Schumacher B., van der Pluijm I., Moorhouse M.J., Kosteas T., Robinson A.R., Suh Y., Breit T.M., van Steeg H., Niedernhofer L.J., van Ijcken W., Bartke A., Spindler S.R., Hoeijmakers J.H., van der Horst G.T., Garinis G.A. Delayed and accelerated aging share common longevity assurance mechanisms. PLoS Genet. 2008, 4:e1000161.
119. Sena L.A., Chandel N.S. Physiological roles of mitochondrial reactive oxygen species. Mol. cell 2012, 48:158-167.
120. Shah R.R., Nerurkar N.L., Wang C.C., Galloway J.L. Tensile properties of craniofacial tendons in the mature and aged zebrafish. J. Orthop. Res. 2015, 33:867-873.
121. Shimoda N., Izawa T., Yoshizawa A., Yokoi H., Kikuchi Y., Hashimoto N. Decrease in cytosine methylation at CpG island shores and increase in DNA fragmentation during zebrafish aging. Age (Dordr) 2014, 36:103-115.
122. Stenkamp D.L., Satterfield R., Muhunthan K., Sherpa T., Vihtelic T.S., Cameron D.A. Age-related cone abnormalities in zebrafish with genetic lesions in sonic hedgehog. Invest. Ophthalmol. Vis. Sci. 2008, 49:4631-4640.
123. Streit W.J., Xue Q.S. The brain's aging immune system. Aging Dis. 2010, 1:254-261.
124. Streit W.J., Sammons N.W., Kuhns A.J., Sparks D.L. Dystrophic microglia in the aging human brain. Glia 2004, 45:208-212.
125. Talens R.P., Christensen K., Putter H., Willemsen G., Christiansen L., Kremer D., Suchiman H.E., Slagboom P.E., Boomsma D.I., Heijmans B.T. Epigenetic variation during the adult lifespan: cross-sectional and longitudinal data on monozygotic twin pairs. Aging Cell 2012, 11:694-703.
126. Toussaint O., Medrano E.E., von Zglinicki T. Cellular and molecular mechanisms of stress-induced premature senescence (SIPS) of human diploid fibroblasts and melanocytes. Exp. Gerontol. 2000, 35:927-945.
127. Tsai S.B., Tucci V., Uchiyama J., Fabian N.J., Lin M.C., Bayliss P.E., Neuberg D.S., Zhdanova I.V., Kishi S. Differential effects of genotoxic stress on both concurrent body growth and gradual senescence in the adult zebrafish. Aging cell 2007, 6:209-224.
128. Vanhooren V., Libert C. The mouse as a model organism in aging research: usefulness, pitfalls and possibilities. Ageing Res. Rev. 2013, 12:8-21.
129. Vardy Y. The Alzheimer conundrum: entanglements of dementia and aging. Global Public Health 2015, 10:132-133.
130. Wang K., Klionsky D.J. Mitochondria removal by autophagy. Autophagy 2011, 7:297-300.
131. Wang C., Jurk D., Maddick M., Nelson G., Martin-Ruiz C., von Zglinicki T. DNA damage response and cellular senescence in tissues of aging mice. Aging cell 2009, 8:311-323.
132. Whitley D., Goldberg S.P., Jordan W.D. Heat shock proteins: a review of the molecular chaperones. J. Vasc. Surg. 1999, 29:748-751.
133. Winston G.W. Oxidants and antioxidants in aquatic animals. Comp. Biochem. Physiol. C Comp. Pharmacol. Toxicol. 1991, 100:173-176.
134. Woods I.G., Kelly P.D., Chu F., Ngo-Hazelett P., Yan Y.L., Huang H., Postlethwait J.H., Talbot W.S. A comparative map of the zebrafish genome. Genome Res. 2000, 10:1903-1914.
135. Worman H.J. Nuclear lamins and laminopathies. J. Pathol. 2012, 226:316-325.
136. Wullimann M.F., Mueller T. Teleostean and mammalian forebrains contrasted: evidence from genes to behavior. J. Comp. Neurol. 2004, 475:143-162.
137. Xi Y., Noble S., Ekker M. Modeling neurodegeneration in zebrafish. Curr. Neurol. Neurosci. Rep. 2011, 11:274-282.
138. Yarian C.S., Toroser D., Sohal R.S. Aconitase is the main functional target of aging in the citric acid cycle of kidney mitochondria from mice. Mech. Ageing Dev. 2006, 127:79-84.
139. Yeoman M., Scutt G., Faragher R. Insights into CNS ageing from animal models of senescence. Nat. Rev. Neurosci. 2012, 13:435-445.
140. Yoon J.C., Ng A., Kim B.H., Bianco A., Xavier R.J., Elledge S.J. Wnt signaling regulates mitochondrial physiology and insulin sensitivity. Genes Dev. 2010, 24:1507-1518.
141. Yu L., Tucci V., Kishi S., Zhdanova I.V. Cognitive aging in zebrafish. PloS One 2006, 1:e14.
142. Yuan X., Ishibashi S., Hatakeyama S., Saito M., Nakayama J., Nikaido R., Haruyama T., Watanabe Y., Iwata H., Iida M., Sugimura H., Yamada N., Ishikawa F. Presence of telomeric G-strand tails in the telomerase catalytic subunit TERT knockout mice. Genes Cells 1999, 4:563-572.
143. Zhdanova I.V., Yu L., Lopez-Patino M., Shang E., Kishi S., Guelin E. Aging of the circadian system in zebrafish and the effects of melatonin on sleep and cognitive performance. Brain Res. Bull. 2008, 75:433-441.